Diseases and Pathogens of Eucalypts

D i s e a s e s a n d Pa t h o g e n s o f

EUCALYPTS

Dedication This book is dedicated to the memory of Dr Geoffrey Charles Marks (1932–90) who, after 27 years of experience as a Forest Pathologist with the Victorian Government and as a teacher of Forest Pathology at the University of Melbourne, saw the need for such a book. He initiated its writing and undertook the initial planning of its structure and authorship. Geoff was born in Sri Lanka (formerly Ceylon) and was an outstanding athlete and scholar, representing his country as a swimmer at the Helsinki Olympics and completing an honours degree in science at the University of Ceylon, followed by an MSc (1961) and PhD (1963) while on a Rockefeller Foundation Scholarship at the University of Wisconsin. He took up his appointment with the then Forests Commission of Victoria in Melbourne in 1963 and thereafter was involved in the study of eucalypt diseases, being a central participant in the initial studies of dieback caused by Phytophthora cinnamomi in Victorian eucalypt forests. He also initiated early studies on the eucalypt leaf pathogen, Mycosphaerella, in southern Australia. His keen intellect, enlightened attitudes, great enthusiasm and curiosity, waspish good humour and propensity to provoke critical discussion inspired colleagues and led to fruitful collaborations with many people. He developed a deep appreciation of the eucalypt forests of his adopted country, and from this grew his keen understanding of their ecology and pathology. He conducted wide ranging field studies on many aspects of forest pathology and greatly enjoyed field trips to investigate disease problems in the diverse forests of Victoria, tirelessly speculating about the complex causes of the diseases and planning experimental studies with whomever was fortunate enough to accompany him. While returning home from one of these long trips to the forests of eastern Victoria he was seriously injured in a car accident. He showed great courage in recovery, and never lost his enthusiasm, expressed at the time by his delight in initiating and planning this book. He was not destined to see this work to fruition as he died suddenly in August 1990. Vale, Geoff. We hope this book has not fallen too far short of your vision.

Title

D i s e a s e s a n d Pa t h o g e n s o f

EUCALYPTS

P. J. Keane, G. A. Kile, F. D. Podger and B. N. Brown (Editors)

© CSIRO 2000 All rights reserved. Except under the conditions described in the Australian Copyright Act 1968 and subsequent amendments, no part of this publication may be reproduced, stored in a retrieval system or transmitted in any form or by any means, electronic, mechanical, photocopying, recording, duplicating or otherwise, without the prior permission of the copyright owner. Contact CSIRO PUBLISHING for all permission requests. National Library of Australia Cataloguing-in-Publication entry Diseases and pathogens of eucalypts. Bibliography. Includes index. ISBN 0 643 06523 7 (paperback). ISBN 0 643 09012 6 (eBook). 1. Eucalyptus – Diseases and pests – Australia. I. Keane, Philip J. 634.9737660994 This book is available from: CSIRO PUBLISHING

PO Box 1139 (150 Oxford Street) Collingwood VIC 3066 Australia Tel: (03) 9662 7666 Int: +(613) 9662 7666 Fax: (03) 9662 7555 Int: +(613) 9662 7555 Email: [email protected] http://www.publish.csiro.au Typeset by Desktop Concepts P/L, Melbourne Printed in Australia by Brown Prior Anderson Cover photographs Upper: Crown decline typical of that observed in trees of Eucalyptus obliqua and E. regnans affected by regrowth dieback and Armillaria. Lower: Crinkle leaf caused by Mycosphaerella cryptica on tip leaves of a seedling of Eucalyptus obliqua. Publication of this book was supported by a grant from the Standing Committee on Forestry of the Australian Ministerial Council on Forestry, Fisheries and Aquaculture.

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Preface Contributors

xiii xvi

Section I: The Eucalypts—Their Importance, Diversity and Biology 1

Economic and Social Importance of Eucalypts

1

J.W. Turnbull

2

Summary

1

1.1

Introduction

2

1.2

Eucalypts in native forests

2

1.3

Eucalypts as exotics

3

1.4

Industrial eucalypt plantations

4

1.5

Eucalypts in the rural landscape

5

1.6

Conclusion

7

1.7

References

7

Morphology, Phylogeny, Origin, Distribution and Genetic Diversity of the Eucalypts

11

B.M. Potts and L.A. Pederick Summary

11

2.1

Introduction

12

2.2

Morphology

12

2.3

Phylogeny

14

2.4

Origins

16

2.5

Distribution

18

2.6

Hybridisation

21

2.7

Genetic variation

23

2.8

Genetic variation in susceptibility to disease

24

2.9

Factors affecting disease risk in plantations

26

2.10

Acknowledgments

27

2.11

References

27

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3

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Growth Habits and Silviculture of Eucalypts

35

R.G. Florence

4

Summary

35

3.1

Introduction

36

3.2

Growth habits of the eucalypts

36

3.3

Sivicultural practice in natural forests

38

3.4

Ecologically sustainable silviculture

40

3.5

New directions in silviculture

42

3.6

Eucalypt plantations

43

3.7

Conclusion

44

3.8

References

44

Ecology of Eucalypt Regeneration

47

D.H. Ashton

5

Summary

47

4.1

Introduction

48

4.2

Characteristics of eucalypts in relation to their regeneration

50

4.3

Conditions required for regeneration

51

4.4

Major modes of regeneration

51

4.5

In synthesis—the strategies of survival

58

4.6

References

59

Physiology of Eucalypts in Relation to Disease

61

C.L. Beadle

6

Summary

61

5.1

Introduction

62

5.2

Productivity and light interception

62

5.3

Biomass production, partitioning of dry mass and foliage

63

5.4

Gas exchange and stomatal conductance

64

5.5

Water relations

66

5.6

Conclusion

68

5.7

References

68

Mycorrhizas of Eucalypts

71

G.A. Chilvers

vi

Summary

71

6.1

Introduction

72

6.2

Structure of eucalypt mycorrhizas

73

6.3

Functioning of mycorrhizas

74

6.4

The fungal partners of eucalypts

83

6.5

Mycorrhizal infection cycles

86

6.6

Ecology of mycorrhizas

87

6.7

Manipulating eucalypt mycorrhizas

90

6.8

References

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Section II: The Diseases of Eucalypts—Their Causes and Biology 7

Diseases and Fungi of the Reproductive Structures of Eucalypts

103

B.N. Brown

8

Summary 7.1 Introduction 7.2 Fungi of flowers and capsules and their pathogenicity 7.3 Seed fungi of eucalypts 7.4 Control of seed fungi 7.5 Conclusion 7.6 References

103 104 104 106 114 115 115

Disease during Propagation of Eucalypts

119

B.N. Brown and F.A. Ferreira

9

Summary 8.1 Introduction 8.2 Diseases with abiotic causes 8.3 Fungal diseases 8.4 Principal diseases of eucalypt cuttings 8.5 Conclusion 8.6 References

119 120 120 121 143 143 143

Fungal Diseases of Eucalypt Foliage

153

R.F. Park, P.J. Keane, M.J. Wingfield and P.W. Crous

10

Summary 9.1 Introduction 9.2 Target spot (Aulographina eucalypti) 9.3 Leaf spot, leaf blotch and crinkle leaf blight (Mycosphaerella species) 9.4 Biotrophic infections 9.5 Powdery mildews (Oidium species) 9.6 Eucalypt rust (Puccinia psidii) 9.7 Angular, vein-limited leaf spots 9.8 White leaf and shoot blight (Sporothrix pitereka ) 9.9 Winter leaf spot (Piggotia substellata and Ceuthospora innumera) 9.10 Leaf spots and speckles of minor importance 9.11 Leaf spots and blights of stressed plants 9.12 Conclusion 9.13 Acknowledgments 9.14 References

153 154 155 163 175 191 191 193 206 206 210 218 227 230 230

Canker Diseases of Eucalypts

241

K.M. Old and E.M. Davison Summary 10.1 Introduction 10.2 Fungal invasion and host responses 10.3 Effect of plant stress on the development of cankers 10.4 Major canker diseases of eucalypts

241 242 242 244 245

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10.5 10.6 10.7 10.8

11

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Opportunistic pathogens associated with cankers in eucalypts Conclusion Acknowledgments References

Diseases of Eucalypts Caused by Soilborne Species of Phytophthora and Pythium

248 252 252 253

259

B.L. Shearer and I.W. Smith

12

Summary 11.1 Introduction 11.2 Origin of the pathogens 11.3 Host range 11.4 Distribution patterns and effect of disease 11.5 Host–pathogen interactions 11.6 Pathogenicity of Pythiaceae on eucalypts 11.7 Effects of disease on wood production and conservation values 11.8 Pathogen dynamics 11.9 Resistance mechanisms 11.10 Effects of environment on disease development in established infections 11.11 Conclusion 11.12 Acknowledgment 11.13 References

259 260 261 261 262 264 267 269 272 280 282 284 284 284

Woody Root Rots of Eucalypts

293

G.A. Kile

13

Summary 12.1 Introduction 12.2 Armillaria root disease 12.3 Pseudophaeolus root disease 12.4 Ganoderma root rot 12.5 Other woody root diseases 12.6 Conclusion 12.7 References

293 294 294 300 301 301 302 303

Stem and Butt Rot of Eucalypts

307

G.A. Kile and G.C. Johnson Summary 13.1 Introduction 13.2 Causal organisms and hosts 13.3 The decay process 13.4 Factors affecting decay development 13.5 Particular heart rots and stem conditions 13.6 Conclusion 13.7 Acknowledgments 13.8 References

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307 308 308 323 327 331 332 333 333

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14

Diseases of Eucalypts Associated with Viruses, Phytoplasmas, Bacteria and Nematodes

339

T.J. Wardlaw, G.A. Kile and J.C. Dianese Summary 14.1 Introduction 14.2 Virus-like diseases 14.3 Diseases associated with phytoplasmas 14.4 Diseases caused by bacteria 14.5 Diseases associated with nematodes 14.6 Conclusion 14.7 References

15

Mistletoes and other Phanerogams Parasitic on Eucalypts

339 340 340 341 343 346 348 349

353

N. Reid and Z. Yan Summary 15.1 Introduction 15.2 Mistletoes parasitic on eucalypts 15.3 Native cherries parasitic on eucalypts 15.4 Dodder-laurels parasitic on eucalypts 15.5 Acknowledgments 15.6 References

16

Nutritional Disorders and other Abiotic Stresses of Eucalypts

353 354 354 375 377 378 378

385

P. Snowdon

17

Summary 16.1 Introduction 16.2 Diagnosis 16.3 Nutrient deficiencies 16.4 Toxicities 16.5 Water as an abiotic factor 16.6 Frost 16.7 Artificial environments 16.8 Miscellaneous abnormalities 16.9 Conclusion 16.10 References

385 386 386 386 395 398 400 401 402 402 403

Eucalypt Diseases of Complex Etiology

411

K.M. Old Summary 17.1 Introduction 17.2 Etiology of diebacks and declines 17.3 Diebacks of native forests and woodlands 17.4 Forest diebacks associated with drought 17.5 Forest diebacks associated with successional changes 17.6 Forest and woodland diebacks associated with chronic insect herbivory 17.7 Plantation diseases of complex etiology

411 412 412 414 414 416 416 421

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17.8 17.9

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Conclusion References

422 423

Colour Plates Section III: Management of Eucalypt Diseases 18

Management of Eucalypt Diseases—Options and Constraints

427

J.A. Simpson and F.D. Podger Summary 18.1 Introduction 18.2 Environmental concerns 18.3 Quarantine and eradication 18.4 Forest health surveillance 18.5 Approaches to disease management 18.6 Political and legislative considerations 18.7 Conclusion 18.8 Acknowledgments 18.9 References

19

Management of Disease in Native Eucalypt Forests and Woodlands

427 428 430 431 432 433 438 439 440 440

445

F.D. Podger and P.J. Keane

20

Summary 19.1 Introduction 19.2 Management of dieback caused by Phytophthora cinnamomi 19.3 Management of dieback diseases of complex etiology 19.4 Management of root rot caused by Armillaria luteobubalina 19.5 Management of foliar and canker diseases 19.6 Management of stem and butt rots 19.7 Conclusion 19.8 Acknowledgments 19.8 References

445 446 449 460 464 466 467 469 470 470

Management of Phytophthora cinnamomi during Bauxite Mining in Eucalyptus marginata Forest—A Special Case

477

I.J. Colquhoun and P.E. Elliott Summary 20.1 Introduction 20.2 The mining operation 20.3 Objectives of rehabilitation and the dieback management program 20.4 The management strategy 20.5 Procedures for disease control 20.6 Success in management of disease 20.7 Conclusion 20.8 References

x

477 478 478 479 479 481 483 485 485

C O N T E N T S

21

Management of Disease during Eucalypt Propagation

487

B.N. Brown Summary 21.1 Management of nursery diseases—general principles 21.2 Two minimal-disease nursery systems 21.3 Control of particular nursery diseases 21.4 Control of principal diseases of eucalypt cutting programs 21.5 Conclusion 21.6 Acknowledgments 21.7 References

22

Management of Disease in Eucalypt Plantations

487 488 491 493 510 510 511 511

519

P.D. Gadgil, T.J. Wardlaw, F.A. Ferreira, J.K. Sharma, M.A. Dick, M.J. Wingfield and P.W. Crous Summary 22.1 Introduction 22.2 Disease and the selection of species 22.3 Disease management strategies 22.4 Conclusion 22.5 Acknowledgments 22.6 References

Animal Index Birds and Mammals Scientific Names Birds and Mammals Common Names Insects Nematodes

519 520 520 523 527 527 527

531 531 531 531 531

Fungi and other Microorganisms (Actinomycetes, Bacteria, Oomycota, Phytoplasmas) Index

532

Plant Index

548

Eucalypt (Angophora, Corymbia, Eucalyptus) Scientific Names Eucalypt (Angophora, Corymbia, Eucalyptus) Common Names Other Plants

Subject Index

548 552 556

558

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P R E F A C E

The eucalypts (genera Eucalyptus, Corymbia and Angophora) are a unique group of mainly tree species. Despite more than two centuries of scientific study, their taxonomic circumscription is still incomplete. As recently as July 2000, 11 new and disparate species were described from tropical and subtropical Australia (Hill, K.D. and Johnson, L.A.S., 2000, Telopea 8, 503–539). From early European perceptions of them as strange, tough, unwanted trees that dominated the harsh landscape and frustrated the early agricultural development of the isolated continent of Australia, they have become taxa of worldwide importance for large-scale and small-scale planting (see Chapter 1). They now include the most widely planted hardwoods in diverse climates around the world, including the semiarid regions of North Africa, Central Asia and the Middle East, the Mediterranean regions of North Africa, southern Europe, the Middle East and California, the cool mountain regions of South America and Africa, and the tropics and subtropics of Central and South America, Africa and Asia. Eucalypts have become an integral part of the South American landscape, to the extent that they are a pervading presence in the literature of the region. In India, China and Vietnam they have become so well established that people refer to local landraces of particular species or hybrids. In the warmer climatic regions, they are important ecologically, socially and industrially. As well as helping to meet the growing world demand for cellulose fibre, timber and fuelwood, they are being used to renew the seriously depleted timber and firewood resources associated with poverty in many countries, for soil stabilisation in degraded environments and as an addition to the garden resources of subsistence farmers (see Chapter 1). This book is concerned with disease in trees

growing in a wide range of situations, from native plant communities being managed for conservation purposes or mainly for timber and fibre production to intensively managed plantations. Many species of eucalypts are in the process of domestication. Increasingly, even in Australia, the trend is towards the planting of eucalypts and their manipulation by selection, breeding, clonal propagation and intensive silviculture. Seed of a great diversity of provenances collected from the wild in Australia, Papua New Guinea and Indonesia is being used in selection and breeding programs in many countries. In Australia, there has been increasing awareness of the importance of the eucalypts in their natural environment, particularly for land conservation and protection, for conservation of native flora and fauna, and for the conservation of the ultimate repository of the vast genetic resource of eucalypt species, provenances and families adapted to a diverse range of environments. This has led to the development of forest and land management practices concerned with their protection and preservation, and the restoration of degraded eucalypt-dominated communities. The more than 700 species of eucalypts range from those adapted to the semiarid environments that dominate much of the Australian continent, to those, including some of the world's tallest and most majestic trees, adapted to the cooler, wetter environments in the south-east and south-west of the country, to those adapted to the warm, wet environments in the northern subtropical and tropical regions (see Chapter 4). Ring counts on free-standing, single-stemmed trees in the tall forests have provided evidence of their great longevity (up to 450 years) (Hickey, J.E., Su, W., Rowe, P., Brown, M.J. and Edwards, L., 1999,

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Australian Forestry 62, 66–71). Although the eucalypts still dominate the Australian landscape, since European settlement there have been massive changes in the scale and condition of eucalypt forests and woodlands resulting from large-scale clearing for agriculture and urban development, introduction of exotic plants and animals, alteration to fire regimes, harvesting, and changes in hydrological balance and salinity across the landscape. Further changes to the situation of eucalypts in Australia have accompanied the planting of eucalypts in altered rural and urban environments, as individual trees, shelter belts, amenity plantings or in large plantations. These changes, relatively sudden in evolutionary terms, have led to an increased awareness of the physiological and nutritional requirements of the eucalypts (see Chapters 5 and 16), of the importance of eucalypt mycorrhizas (see Chapter 6), and of the potential destructiveness of pests and diseases. Since the 1950s, it has become increasingly apparent that many remnant native forests and woodlands are suffering ill health, with symptoms generally referred to as ‘dieback’, associated with environmental stresses and increased pest and disease pressure. Remnant trees in agricultural and grazing lands have suffered increasingly from ‘rural dieback’, a syndrome associated with increased insect attack (see Chapter 17). Large areas of forest in south-east and south-west Australia have suffered decline and, in certain forests, mass deaths caused by Phytophthora cinnamomi (see Chapter 11). Patches of forest in south-east Australia were killed by the native agaric, Armillaria luteobubalina (see Chapter 12). The early attempts at cultivation of eucalypts in plantations in Australia revealed the potential destructiveness of several highly adapted leaf pathogens (see Chapter 9). These diseases alerted the community to the dangers of increased occurrence and intensity of disease epidemics associated with the great changes wrought by European settlers on native eucalypt vegetation. When eucalypts were first grown outside Australia in the absence of their coevolved parasites, they often appeared healthier and more vigorous than in their native lands. Later, as the plantings became more extensive, the trees began to suffer attack by nonspecialist pathogens, especially in the humid subtropics and tropics. In New Zealand, they were badly damaged by leaf pathogens introduced from Australia, while in South Africa they were attacked

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by some pathogens which appear to have spread from local plants onto the introduced eucalypts. In South America, a destructive rust pathogen and a canker pathogen have transferred to eucalypts from local myrtaceous hosts. There are serious concerns that if these ‘new-encounter’ pathogens are introduced to Australia they could cause great damage in eucalypt-dominated vegetation. Certainly the widespread planting, often in intensive culture, of eucalypts around the world has created new opportunities for the adaptation and spread of pathogens and pests. As a result of the occurrence of disease problems in both native eucalypt communities and plantations outside Australia, there has been an upsurge in interest in the pathology of eucalypts over the last 40 years, as reflected in the burgeoning literature on the subject. It is an opportune time to review knowledge of the biotic and abiotic factors affecting the health of eucalypts, and to bring together the disparate literature on the subject as a basis for further research. With this in mind, Geoff Marks initiated the writing of this book. His death in 1990 prevented his participation beyond the planning stage, but the eventual production of the book is a tribute to his enthusiasm for the field of eucalypt health, his 27 years of research on diseases of eucalypts, particularly dieback associated with Phytophthora cinnamomi, and the encouragement he gave to others. This book is intended not only as a catalogue of current knowledge about the diseases of eucalypts but also as a handbook to facilitate further research into their biology and management. The book is concerned with the health of eucalypt-dominated plant communities in Australia, and of small social plantings and large industrial plantations around the world, not just with a narrow account of diseases of the trees. The rapid expansion of eucalypt planting, first outside and lately within Australia, and the more intensive management of native forests have resulted in a growing interest in the physiology, nutrition, adaptation, genetics, ecology, silviculture and management of the eucalypts. While the book has a strong emphasis on disease in production forests, it also addresses disease in native eucalyptdominated forests and woodlands and in remnant or isolated, planted eucalypts.

P R E F A C E

The book concerns a complex and wide ranging field. Accordingly, it includes a substantial introduction to the biology, ecology and physiology of the eucalypts (Section I) as a basis for further discussion of particular diseases (Section II) and the management options for these diseases in natural, semi-natural and planted communities (Section III). In particular, the genetic diversity of the eucalypts and their adaptation to a wide climatic and edaphic range in Australia and nearby countries is discussed in some detail in Chapter 2 and Chapter 4 as a basis for development of disease management through matching of genotypes to sites and selection of disease resistant planting stock. This book should serve as a timely reminder that the eucalyptdominated communities across Australia and in nearby countries are an invaluable repository of the diverse genetic resource of the eucalypts. In Chapter 3, the growth habits and silviculture of eucalypts is discussed in relation to development of management strategies for maintaining forest health. The ecology of eucalypt regeneration in native communities is introduced in Chapter 4 as a basis for developing knowledge and management expertise in control of diseases in the most disease-prone phases of forest management, namely regeneration in native forests, and production of planting stock and early establishment in plantations. Harvesting and regeneration activities in native forests often result in dense seedling regeneration which may suffer severe epidemics of foliar disease not unlike those expected in crowded plantations. The physiology of eucalypts in relation to their response to stresses including pathogens is introduced in Chapter 5 in anticipation of future research on the physiological effect of diseases of eucalypts and how this might be ameliorated. Chapter 6 reviews knowledge of the mycorrhizas of eucalypts, a subject of great importance to the nutrition and health of the trees. Mycorrhizas are of concern to all involved in management of eucalypt forests and are of particular interest to anyone with a mycological interest in the forests, particularly plant pathologists who are often involved in research into mycorrhizas as well as diseases. This chapter provides a basis for further research on manipulation of mycorrhizas for adaptation of eucalypts to new sites and for combating soilborne diseases. Knowledge of the biology of eucalypts is crucial for developing disease management practices, especially for diseases of native forests and woodlands, which often have

complex etiology and can be ameliorated only by modification of normal silvicultural practices. The chapters in Section II include much background biology of the diseases and their causal organisms, along with discussion of the pathology and management of the diseases. This allows the chapters to stand alone as an introduction to the diseases. In Chapter 9, on foliar diseases, it was necessary to include much taxonomic detail of the causal organisms, reflecting the early stage of development of research into these diseases. Throughout the book, the presentation of Latin binomials of fungal species and their authorities follows Authors of Fungal Names by P.M. Kirk and A.E. Ansell, published by the International Mycological Institute, Kew, in 1992. However, the style of R.K. Brummitt and C.E. Powell (1992, Authors of Plant Names, Royal Botanic Gardens, Kew) has been followed in omitting gaps between initials and surnames. The inclusion of taxonomic details of the fungi referred to in the literature has helped to highlight and clarify discrepancies in the naming of fungi. Much synonymy exists and the organism index, researched and compiled by B.N. Brown, serves as an invaluable guide to the current state of nomenclature. Authorities and Australian common names for eucalypt species are listed in the Index. In Chapter 15, on phanerogamic parasites, much underlying ecology of the parasites is presented as a basis for their management in remnant eucalypt vegetation and on forest verges in Australia. Management of nutritional disorders requires knowledge of the physiological role and interactions of various nutrients (see Chapter 16). In Section III, the options and constraints for management of disease in both native forests and plantations are discussed (see Chapter 18). In Chapter 19, detailed approaches to management of disease in native forests are discussed, with particular emphasis on management of dieback caused by Phytophthora cinnamomi, which has been central to forest pathology in Australia for four decades. A particular instance of intensive management of eucalypt dieback in association with bauxite mining in the Eucalyptus marginata forests of southwest Australia is reviewed in Chapter 20. Finally, the more intensive disease management practices in eucalypt nurseries (see Chapter 21) and plantations (see Chapter 22) are reviewed from an international perspective.

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Although the book provides a comprehensive review of the state of knowledge of eucalypt diseases, it also shows that our knowledge of most diseases is preliminary—there is much to be learnt. We hope that this book will provide a basis for more intensive

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studies of the nutrition, adaptation and diseases of the eucalypts, leading to improved health, productivity and sustainability of these species in native eucalypt communities, and in both large plantations and smaller plantings around the world.

C O N T R I B U T O R S

D.H. Ashton Department of Botany, La Trobe University, Bundoora, Vic. 3083, Australia Email: [email protected]

David Ashton completed his PhD in 1956 at the University of Melbourne on the ecology of Eucalyptus regnans and then undertook further studies at Cambridge University, in Germany and in the USA. In 1960, he took up a lectureship in ecology in the School of Botany at the University of Melbourne, where he continued research on the ecology of E. regnans and diversified into studies of a wide range of ecosystems from coastal heath to alpine-antarctic. From 1975 to 1986 he collaborated on ecological studies of the forests of Chile and Argentina. He is an Associate of the School of Botany and also a Research Fellow in the Department of Botany, La Trobe University. C.L. Beadle Cooperative Research Centre for Sustainable Production Forestry and CSIRO Forestry and Forest Products, GPO Box 252-12, Hobart, Tas. 7001, Australia Email: [email protected]

Chris Beadle obtained his PhD in Botany from the University of Aberdeen in 1977. Since 1983 he has worked for CSIRO Forestry and Forest Products in Hobart, where he is now a Principal Research Scientist and Program Manager of the Sustainable Management Program in the Cooperative Research Centre for Sustainable Production Forestry. B.N. Brown 15 Harefield Street, Indooroopilly, Qld 4068, Australia Email: [email protected]

Bruce Brown obtained his BAgSc (Hons) from the University of Queensland in 1963 and his PhD from the University of Auckland in 1978. He was a Forest Pathologist with the Queensland Department of Forestry (subsequently the Forest Service of the

Queensland Department of Primary Industries) from 1963 until 1991. He studied a wide range of forest diseases in nurseries, plantations and natural forests. He was heavily involved in the control of nursery diseases, and investigated Phytophthora cinnamomi in forest nurseries, Pinus and Eucalyptus plantings and natural vegetation (including tropical rainforests) of Queensland. Recently he has worked as consultant on several projects. G.A. Chilvers 23 Keats Street, Byron Bay, NSW 2481, Australia Email: [email protected]

Graham Chilvers obtained his BScAgr from the University of Sydney, majoring in Plant Pathology under Professor N.H. White, and his PhD at the Australian National University, working on mycorrhizas of eucalypts under Professor L.D. Pryor. He spent two periods of sabbatical leave at the University of Oxford working on mycorrhizas with Professor J.L. Harley. For most of his career he was a Senior Lecturer in the Botany Department, Australian National University. His major research interest was in eucalypt mycorrhizas, but he also studied and lectured in diverse areas of plant-microbe relationships and microbial ecology. I.J. Colquhoun Alcoa of Australia, Booragoon, WA 6154, Australia Email: [email protected]

Ian Colquhoun is a Senior Research Scientist with the Environmental Department of Alcoa World Alumina Australia. He received his BSc in Botany from the University of Glasgow in 1976, and his PhD from the University of Western Australia in 1986 for a dissertation on the physiology of Australian native plants. In 1980, he joined Alcoa to supervise a project on the hydrological balance of revegetated minepits. In 1989, his responsibilities extended to the interaction between the hydrology of rehabilitated minepits, tree xvii

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physiology and Phytophthora root rot. His present responsibilities include the development of disease control measures for mining, coordinating plant pathology research projects and supervising plant physiology projects based in the jarrah forest and rehabilitated minepits.

Davis. Since 1971 he has lectured at the University of Brasilia where he is currently Professor and Chairman of the Department of Plant Pathology. He has conducted research on a wide range of diseases of agricultural and forest species, with an emphasis on diseases of eucalypts, especially guava rust and bacterial wilt.

P.W. Crous Department of Plant Pathology, University of Stellenbosch, Private Bag XI, Matieland 7602, South Africa Email: [email protected]

Pedro Crous did his MSc(Agric) on leaf diseases of Eucalyptus, which set the stage for much of his future research. He obtained his PhD(Agric) in 1992, dealing with Cylindrocladium and related fungi, with specific reference to woody hosts. He has since continued studies on this group, but also initiated projects on Mycosphaerella, Botryosphaeria and their anamorphs. His main interests are anamorph/ teleomorph connections, and the integration of DNA and morphological data in the phylogeny of fungi. He is Professor of Mycology and Chair of the Department of Plant Pathology at the University of Stellenbosch. He is also the President of the Southern African Society for Plant Pathology.

M.A. Dick New Zealand Forest Research Institute, Private Bag 3020, Rotorua, New Zealand Email: [email protected]

Margaret Dick obtained a BSc in Botany and has worked since 1972 as a forest pathologist with the New Zealand Forest Research Institute, concentrating on fungal diseases. She has studied foliage diseases of eucalypts in plantations, root diseases of pine, and more recently Cyclaneusma needle cast of Pinus radiata. She has also been involved in pest risk analysis, particularly of the threat posed by pine pitch canker to plantation forests in New Zealand. For over 20 years she has supervised the forest disease diagnostic service. This has included identification and monitoring of foliage diseases on eucalypt species during their testing for adaptation to local conditions. P.E. Elliott

E.M. Davison School of Environmental Biology, Curtin University, GPO Box U 1987, Perth, WA 6001, Australia Email: [email protected]

Elaine Davison received her BSc Honours from the University of Bristol in 1963 and her PhD from the same university in 1967. From 1968 to 1972 she worked as a Plant Pathologist at the Botanic Garden and at the Waite Agricultural Research Institute in Adelaide. In 1979, she was a post-doctoral research fellow at the University of Oxford. From 1979 to 1986 she worked as a Mycologist/Plant Pathologist with the Department of Conservation and Environment, and from 1986 to 1995 she was a Principal Research Scientist at the Department of Conservation and Land Management in Western Australia, concerned with diseases of eucalypts. She is now a Senior Research Associate and works as a consultant based at Curtin University of Technology.

WMC Resources Ltd, QV1 Building, 250 St George’s Terrace, Perth, WA 6000, Australia Email: [email protected]

Peter Elliott obtained his MSc in Natural Resource Management from the University of Western Australia. In 1990 he was the senior environmental scientist with Alcoa and coordinated the development of the intensive dieback management program. This involved him in developing strategies, policies and procedures for management of operations in jarrah forests, in consultation with a wide range of Alcoa employees and government agencies. As Corporate Manager—Environmental Systems, he was later responsible for the development of Environmental Management Systems for WMC Resources Ltd. He has recently been appointed Manager—Planning and System Services in the Corporate Human Resources and Development Group of the company. F.A. Ferreira

J.C. Dianese Departmento de Fitopatologia, Universidade de Brasilia, 70919 Brasilia, DF, Brazil Email: [email protected]

Jose Dianese obtained his BS in agronomy from the Universidade Federal de Viçosa and his MS and PhD in plant pathology from the University of California, xviii

Departmento de Fitopatologia, Universidade Federal de Viçosa, 36571.000 Viçosa, Minas Gerais, Brazil Email: [email protected]

Francisco Ferreira is a forest pathologist with over 25 years of experience in teaching, research and extension on the etiology and management of forest diseases in Brazil, including diseases on eucalypts, pines and

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rubber. He has been concerned with nursery diseases, rust diseases and defence mechanisms in the bark and xylem as they relate to the diagnosis and control of biotic and abiotic trunk diseases. He has undertaken extension activities related to the diagnosis and management of diseases of eucalypts for both private companies and public institutions in Brazil and other countries in South America and Europe. He is currently Professor of Forest Pathology at the Federal University of Viçosa. R.G. Florence Department of Forestry, Australian National University, GPO Box 4, Canberra, ACT 2601, Australia Email: [email protected]

Ross Florence graduated from the Australian Forestry School and the University of Queensland in 1953 and worked on silviculture of native forests with the Queensland Forest Service. He obtained his PhD from the University of Sydney in 1961 for studies on the ecology of native forests. He joined the Department of Forestry of the Australian National University in 1965 where he lectured in silviculture, forest ecology, and planning and policy. He wrote Ecology and Silviculture of Eucalypt Forests, published by CSIRO Publishing in 1996. P.D. Gadgil New Zealand Forest Research Institute, Private Bag 3020, Rotorua, New Zealand Email: [email protected]

Peter Gadgil obtained his PhD in the area of microbial ecology from the University of Cambridge in 1962 and has been a forest pathologist with the New Zealand Forest Research Institute since 1965. His main areas of work have been needle diseases of Pinus radiata (Dothistroma needle blight, Cyclaneusma needle cast), stem decay in Eucalyptus spp. and, with Ruth Gadgil, the influence of mycorrhizal fungi on litter decomposition in coniferous forests. More recently, he has concentrated on the eradication of Dutch elm disease from New Zealand, methods of forest health surveillance and the investigation of pathways by which forest pests and pathogens can reach New Zealand.

a research scientists with CSIRO Forestry and Forest Products in Clayton, Vic., where he worked for 21 years until 2000, specialising in decay of wood and natural durability of timber. P.J. Keane Department of Botany, La Trobe University, Bundoora, Vic. 3083, Australia Email: [email protected]

Philip Keane obtained a BAgSc(Hons), specialising in plant pathology, from the University of Adelaide, and a PhD from the University of Papua New Guinea for studies on the cause and control of a dieback disease of cocoa. Since 1975 he has lectured in botany, environmental biology, mycology and plant pathology at La Trobe University where he is now an Associate Professor. His research interests include foliar diseases of eucalypts and diseases of a wide range of agricultural crops, with a special interest in resistance to disease, biological control and plant diseases in the tropics. G.A. Kile CSIRO Forestry and Forest Products, PO Box E4008, Kingston, Canberra, ACT 2604, Australia Email: [email protected]

After completing his BAgrSc(Hons) and PhD at the University of Tasmania, Glen Kile undertook research on diseases in native forests in Australia, particularly Armillaria and stem rot fungi in eucalypts, Chalara australis in Nothofagus forests, and some dieback diseases of complex etiology. He identified Armillaria luteobubalina as a major pathogen in eucalypt forests, amenity plantings and horticulture in Australia and conducted taxonomic and population studies of Armillaria. He was appointed Director of the Cooperative Research Centre for Temperate Hardwood Forestry in 1991, Chief of CSIRO Division of Forestry in 1992 and Chief of CSIRO Forestry and Forest Products in 1996. He is a member of the Standing Committee on Forestry of the Australian Ministerial Council on Forestry, Fisheries and Aquaculture, and Chairman of its Committee on Forest Health. He is a member of the editorial boards of Australasian Plant Pathology and the European Journal of Forest Pathology.

G.C. Johnson 10 Glendowan Road, Mt Waverley, Vic. 3149, Australia

Gary Johnston completed his BScFor(Hons) and MSc(Forestry) at the University of British Colombia and obtained his PhD from the Australian National University where he studied under Professor D.M. Griffin and Dr W.A. Heather. He taught forestry at the University of Melbourne before taking up a position as

K.M. Old CSIRO Forestry and Forest Products, PO Box E4008, Kingston, Canberra, ACT 2604, Australia Email: [email protected]

Ken Old obtained his BSc(Hons) in agricultural botany from the University of Nottingham in 1961 and his PhD from the University of Minnesota in 1964. He lectured xix

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in plant pathology, mycology and soil microbiology at Dundee University from 1964 to 1978. He joined CSIRO Forestry and Forest Products in 1978 and was Assistant Chief from 1992 to 1999. He is currently a Chief Reseach Scientist. His main research interests have included genetic variation in Phytophthora cinnamomi, canker diseases of eucalypts, foliar pathogens of eucalypts and acacias in plantations in tropical Australia and south-east Asia, and stem defect in regrowth eucalypt forests in south-east Australia. R.F. Park University of Sydney, Plant Breeding Institute Cobbitty, PMB 11, Camden, NSW 2570, Australia Email: [email protected]

Robert Park obtained his BSc(Hons) and PhD from La Trobe University where he studied the pathology of Mycosphaerella species infecting eucalypts in southeast Australia. He is currently a Senior Research Fellow at the University of Sydney, Plant Breeding Institute, Cobbitty, where he works as a plant pathologist concerned mainly with ecological aspects of cereal rusts and breeding of cereals for resistance to rusts. He was awarded an Alexander von Humbolt Fellowship in 1995 and spent one year at the Technical University of Munich studying European populations of wheat leaf rust. Since his student days he has maintained an interest in the diversity of the foliar pathogens of eucalypts. L.A. Pederick 17 Yanigin Drive, Glen Waverley, Vic. 3150, Australia

Leon Pederick obtained his BScFor and PhD from the University of Melbourne and worked as a research scientist for the forest service of the Victorian Government from 1958 to 1993. He specialised in genetics of forest trees and for over 30 years led a breeding program for Pinus radiata. He also undertook extensive provenance and progeny trials with several eucalypt species, especially Eucalyptus nitens. He is a Fellow of the Institute of Foresters of Australia, and was awarded the Institute's N.W. Jolly Medal for 1991. F.D. Podger 19 Stanstead Crescent, Marangaroo, WA 6064, Australia

Frank Podger obtained a BSc(For) from the University of Western Australia, a DipFor from the Australian Forestry School, Canberra, an MScFor from the University of Melbourne, and a PhD from the University of Auckland. His early career with the WA Forests Department involved field training in forest management in eucalypt forests. In 1959, under federal employ he researched the cause of a destructive xx

epidemic of dieback in the jarrah forests, first reporting in 1964 its association with the exotic pathogen Phytophthora cinnamomi and publishing proof of its cause in 1972. For this he received an inaugural Scientific Achievement Award from IUFRO. He has since studied diseases of native vegetation in all States of Australia and has also had an interest in fire effects ecology and its interactions with Ph. cinnamomi. In the last decade he has consulted to governments in Tasmania and Western Australia on management for amelioration of disease in native forests and its sociopolitical implications. From 1993 to 1996 he chaired a review of management of Phytophthora root rot in Western Australia. In 1999, he produced a source document on which was based a National Threat Abatement Plan for amelioration of the threat posed to conservation values by the epidemic of Phytophthora root rot. B.M. Potts Cooperative Research Centre for Sustainable Production Forestry, School of Plant Science, University of Tasmania, GPO Box 252-55, Hobart, Tas. 7001, Australia Email: [email protected]

Brad Potts completed his PhD at the University of Tasmania in 1983 where he is currently a Senior Lecturer in the School of Plant Science and Manager of the Genetic Improvement Program of the Collaborative Research Centre for Sustainable Production Forestry. Within this program he is leader of the research project on the reproductive biology and genetics of eucalypts and works closely with quantitative and molecular geneticists at the University of Tasmania on the natural history and breeding of eucalypts. He has worked in and maintains active research collaboration with scientists in France, Chile and the USA and has specialised in studies of hybridisation, genetics and evolution of the eucalypts. N. Reid Ecosystem Management, University of New England, Armidale, NSW 2351, Australia Email: [email protected]

Nick Reid completed a BSc(Hons) and PhD in Botany at the University of Adelaide. His early research career spanned ornithology, rangeland ecology and the reproductive and population biology of arid zone mistletoes. An academic posting in Mexico led to ecological research on the vegetation dynamics, phenology and ethnobotany of subtropical thornscrub. He is currently Associate Professor and Convenor of Ecosystem Management in the School of Rural Sciences and Natural Resources at the University of New

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England, where he teaches agroforestry, park and wildland management, and sustainable land management. His current research includes the role of trees in farm ecosystems, native vegetation management in rural and wildland environments, revegetation technologies and mistletoe management. J.K. Sharma Kerala Forest Research Institute, Peechi Trichur 680 653, Kerala, India Email: [email protected]

Jyoti Sharma obtained his PhD in Botany (Plant Pathology) from Agra University and was a lecturer at Agra College for eight years. Later, he spent five years at the Australian National University, Canberra, doing post-doctoral research in forest pathology. He joined the KFRI in 1978 as the Scientist-in-Charge, Plant Pathology Division. He was appointed Research Coordinator of the Institute in 1996 and Director in July 2000. He is presently the IUFRO Working Party Coordinator on Diseases of Tropical Plantations. He has had extensive research and consulting experience on diseases and mycorrhizas in eucalypt plantations. He served as an Expert Member on an FAO/IPGRI committee to frame guidelines for the safe movement of eucalypt and pine germplasm and is a Fellow of the Indian Phytopathological Society. B.L. Shearer Department of Conservation and Land Management, 50 Hayman Road, Como, WA 6152, Australia Email: [email protected]

Bryan Shearer obtained a BScAgric(Hons) from the University of Western Australia and a PhD from the University of Minnesota, USA. He is a Principal Research Scientist in the CALM Science Division of the Department of Conservation and Land Management of Western Australia and Adjunct Associate Professor in the Division of Science at Murdoch University. He has investigated the impact, epidemiology and control of Phytophthora species, Armillaria luteobubalina and canker fungi in native plant communities for over 20 years. His current research interests centre on the ecology and control of plant diseases in conservation areas of south-west Western Australia. J.A. Simpson Forest Research and Development Division, State Forests of NSW, PO Box 100, Beecroft, NSW 2119, Australia Email: [email protected]

Jack Simpson is Senior Forest Pathologist with the Research and Development Division of State Forests of

New South Wales, where he has worked for almost 20 years. He obtained an MAgSc from the University of Adelaide for a thesis on mycological aspects of the decomposition of litter of Pinus radiata. During his career Jack has worked on diverse forest disease problems in South Australia, New South Wales, Western Australia, Papua New Guinea and Fiji. He is Chair of Research Working Group 7 (Forest Health), a member of the Forest Health Committee, and the forestry observer on the Plant Health Committee of the Standing Committee on Forestry. He is past president of the Australasian Mycological Society. His research interests include eucalypt foliage pathogens, stem decays in living trees, quarantine issues relating to management of incursions of quarantine pests and imports of wood, and forest declines. I.W. Smith Centre for Forest Tree Technology, Department of Natural Resources and Environment, PO Box 137, Heidelberg, Vic. 3084, Australia Email: [email protected]

Ian Smith obtained a BSc(Hons) from Monash University and is a forest pathologist in the Centre for Forest Tree Technology of the Department of Natural Resources and Environment. He is responsible for investigating the productivity and ecology of native forests, and the biology and control of diseases that threaten the productive capacity of native forests, softwood and hardwood plantations and nurseries. He has over 20 years of experience in the field of forest pathology research in Victoria, much of which was centred on eucalypt dieback caused by Phytophthora cinnamomi. P. Snowdon CSIRO Forestry and Forest Products, PO Box E4008, Kingston, Canberra, ACT 2604, Australia Email: [email protected]

Peter Snowdon is a Principal Research Scientist with the Plantation and Farm Forestry Program of CSIRO Forestry and Forest Products. He majored in plant pathology at the University of Sydney and gained his MSc from the Australian National University for a study of boron nutrition in pines. He has 40 years of experience in various aspects of forest nutrition, including the use of visible symptoms and chemical analyses of soil and foliage samples for identification of nutrient deficiencies and toxicities. He has also been involved in research into the effects of environmental factors such as drought and frost on the growth and health of plantation species. xxi

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J.W. Turnbull

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CSIRO Forestry and Forest Products, PO Box E4008, Kingston, Canberra, ACT 2604, Australia Email: [email protected]

Forestry and Agricultural Biotechnology Institute, University of Pretoria, 74 Lunnon Road, Hillcrest, Pretoria, Republic of South Africa 0002 Email: [email protected]

John Turnbull has a BSc degree in forestry from the University of Wales and a PhD in eucalypt genecology from the Australian National University. As a Senior Principal Research Scientist at CSIRO Forestry and Forest Products he was involved for over 25 years in the exploration and utilisation of eucalypt genetic resources in Australia and many other countries. Subsequently he was Chief Scientist at the Center for International Forestry Research in Indonesia. He is currently based at the Australian Tree Seed Centre, CSIRO Forestry and Forest Products, Canberra.

Mike Wingfield has a PhD from the University of Minnesota and is the Director of the Forestry and Agricultural Biotechnology Institute, University of Pretoria, South Africa. He has 20 years of experience in research on diseases of forest trees and has specialised in the identification and management of diseases of eucalypts, pines and wattles grown as exotics in plantations. He has provided advisory services to forestry companies in South Africa, South and Central America, and south-east Asia.

T.J. Wardlaw Forestry Tasmania, GPO Box 207B, Hobart, Tas. 7001, Australia Email: [email protected]

Tim Wardlaw obtained a BScHons and is completing a PhD at the University of Tasmania. He is Senior Forest Pathologist with Forestry Tasmania. In a career spanning 20 years he has investigated a wide variety of forest diseases including eucalypt crown dieback diseases with complex etiologies, needle cast diseases of Pinus radiata and stem decay of eucalypts in native forests and plantations. Recently much of his work has been focused on quantifying the effects of diseases and developing management strategies to reduce disease losses. He has overseen the introduction and development of health surveillance of eucalypt and pine plantations in Tasmania.

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Z. Yan Plant Research and Development Services, Agriculture Western Australia, Baron Hay Road, South Perth, WA 6151, Australia

Zhaogui Yan studied agricultural science at the Central China University of Agriculture and completed his PhD in mistletoe ecology at Flinders University, South Australia. He currently works for Agriculture Western Australia where his principal research interests are managing annual ryegrass toxicity through biological control, the population dynamics of rangeland plants under various climatic and grazing regimes, and the ecological interactions between mistletoes and their hosts and dispersers.

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For thousands of years eucalypts have been of critical importance in the economy of indigenous Australians. In the last 200 years eucalypts have passed from being a botanical curiosity and nuisance to the early European settlers in Australia, to trees of importance in the local economy, to one of the world’s most important and widely planted forest species. Eucalypts have valuable wood and pulp characteristics and many useful silvicultural properties including high growth rates, adaptability to a wide range of soils and climates, coppicing ability and a tendency not to spread as a weed. In Australia, eucalypt-dominated native forest and woodland communities cover about 124 million hectares but wood and pulp production is restricted to about 13 million hectares. It is estimated that there will be 20 million hectares of eucalypt plantations outside Australia by the year 2010. At present there are more than 10 million hectares in the tropics alone, mainly in South America and Asia. Since the early 1980s, eucalypt planting has expanded rapidly in many parts of the world, including Australia. This expansion has been driven by the world demand for pulpwood, but eucalypts are also being planted widely as a source of charcoal, fuelwood and building materials and for land conservation. The trees can provide a source of financial security for small farmers. Great benefits have accrued from clonal selection and breeding of eucalypts and from more intensive management practices, in which Brazil has led the way. However, it is important to recognise the increased risk of disease epidemics associated with the movement of pathogens to new areas and the establishment of densely planted, genetically homogeneous plantations. Outbreaks of disease in plantations and native forests have stimulated much recent research into the diseases of eucalypts.

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1.1 Introduction The eucalypts (genera Eucalyptus, Corymbia, Angophora), being by far the dominant tree over most of the Australian landscape, have been critical to the economy of indigenous Australians, directly supplying fuel, building materials, medicine and resins, and being habitat for the animals that contributed greatly to their diet. In the late eighteenth century when eucalypts first came to the attention of the scientific world and the French botanist, Charles Louis L’Héritier De Brutelle, applied the name Eucalyptus to an Australian tree, there was little appreciation of the potential of eucalypts to become a major source of industrial forest products. The wood was difficult to saw and season and it was commonly considered to have value only as firewood or as poles. Remarkably, at the beginning of the twenty-first century the natural eucalypt forests are a major source of forest products, and eucalypts have become the most widely planted hardwood species in the world.

1.2 Eucalypts in native forests Eucalypts dominate 124 million hectares of Australia’s natural forests and woodlands (Australian Bureau of Agricultural and Resource Economics 1997) (see Chapter 4) and they have great cultural and environmental significance, as well as being a valuable source of wood products. Most of this area is eucalypt woodland. Only about 28 million hectares is potentially productive forest (Australian Forestry Council 1989). Production of wood for industrial purposes is restricted to about 13 million hectares by factors such as lack of accessibility and conservation reserves (Commonwealth of Australia 1997). Beyond Australia there are small areas of natural eucalypt forests in Indonesia, Papua New Guinea and the Philippines but these are of relatively little economic significance, even locally. When European settlement began in Australia in 1788, trees were considered to be a hindrance to development. Clearing of land for agriculture was essential and large areas of eucalypts were felled. About half of Australia’s forests have been cleared or severely modified by selective logging or uncontrolled fires (Wells et al. 1984; Resource Assessment Commission 1992). Attitudes to the forests changed markedly around the start of the

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twentieth century and State forest services were established to manage public forests for perpetual timber production. By the 1930s the concept of ‘multiple use forestry’ was recognised and forests were dedicated for watershed protection, recreational use and the conservation of native wildlife and flora, in addition to timber production (Carron 1985). The supply of eucalypt timber has generally exceeded demand in Australia and there has been little incentive to manage eucalypts intensively for wood production (Kerruish and Rawlins 1991). In most States the harvest of eucalypt sawlogs increased progressively from about 1930 but is now declining from peaks reached between 1955 and 1980. Today, eucalypt forests meet about half of Australia’s domestic requirements for forest products, the remainder being imported or derived from local plantations of softwood (mainly Pinus species). However, pulpwood production from eucalypt forests increased dramatically from the early 1970s, particularly in Tasmania, Western Australia and New South Wales, with the development of an export market for Australian eucalypt woodchips to meet increased demands for printing, writing and tissue papers. The volume harvested has remained fairly stable through the 1990s. In 1997–98 some 10.3 million cubic metres of native hardwoods (mainly eucalypts) were removed for timber and woodchips and it is predicted that this level will be maintained until 2005 (Australian Bureau of Agricultural and Resource Economics 1999). In 1997, exports of hardwood chips reached 2.5 million tonnes (bone dry). Woodchip, including softwood chips, has generally accounted for just over half of the value of Australian forest product exports in the 1990s and reached a record $646 million in 1997–98 (Australian Bureau of Agricultural and Resource Economics 1999). However, the wood and wood products industry contributes only about 1% of Australia’s gross domestic product. While the eucalypt wood industry is small within the overall Australian economy, the various sectors of the industry together employ about 40 000 people and have great significance in providing employment and economic activity in particular regions (Resource Assessment Commission 1991). Eucalypt growing, harvesting and processing are the major activities of several small rural communities.

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There seems little doubt that the natural eucalypt forests will continue to have considerable economic significance in Australia. By the year 2005 the annual hardwood removals (mainly eucalypt) from Australia’s native forests will be 10.1 million cubic metres (Australian Bureau of Agricultural and Resource Economics 1999). There are also excellent opportunities for the more intensive management of some of the higher-yielding temperate forests in Australia, and a young regrowth eucalypt resource of about 300,000 ha is possibly amenable to intensive management (Wells 1991). The area under eucalypt plantations is being expanded to meet pulpwood needs and possibly some sawlog requirements. As a result of an active eucalypt plantation program with E. globulus and E. nitens, the area of hardwood plantations in Australia rose from 125,000 hectares in 1994 to 287,000 hectares in 1998 (Cromer et al. 1995; Wood et al. 1999). In addition to the economic value of the native eucalypt forests, they have great societal, cultural and environmental significance. Eucalypt forests and woodlands dominate the Australian landscape. They hold particular significance for Aboriginal peoples (Resource Assessment Commission 1991). They are critical for the protection of soil, maintenance of hydrological balance and the survival of wildlife. Excessive clearing of eucalypts and their associated communities has led to decline of remnant trees and salinity problems in many areas. The native forests and woodlands are also the ultimate repository of the great genetic diversity of the eucalypts. In response to community attitudes and changes in government policies, efforts are increasing to modify forest practices to better address conservation values and the maintenance of biological diversity (Turnbull 1996). Although many of the environmental effects of more intensive culture of eucalypts are incompletely understood, there is no doubt that environmental effects will result from the intensification of forestry practices. However, in most cases the costs imposed on the environment by sustainable harvesting and extension of eucalypt planting will be less than those associated with agriculture or other types of intensive land management on similar land. Benefits of intensive culture of eucalypt plantations will accrue from the reduced land area required for wood and pulp production, the use of a renewable resource and

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from the broader socioeconomic effects of such activity (Nambiar and Brown 1997).

1.3 Eucalypts as exotics Outside Australia, eucalypts were initially regarded as botanical curiosities and were sought by botanical gardens and private aboreta in Europe. Once in cultivation, the potential of some eucalypt species to grow rapidly and produce straight stems was recognised and the botanical gardens of southern Europe became centres for the secondary dispersal of eucalypts to other parts of the world, especially Latin America and Africa. Later in the nineteenth century, eucalypts were introduced directly from Australia to many parts of the world. Some were planted for their ornamental value, and others for windbreaks, land reclamation and leaf-oil production. In countries such as Brazil and South Africa, eucalypts were planted along railway lines to provide fuel for woodburning locomotives. The reasons for planting eucalypts have changed significantly, and the end uses to which the various species have been applied are diverse. Eucalypts provide sawn timber, mine props, poles, firewood, pulp, charcoal, essential oils, honey, tannin, shade and shelter (Hillis and Brown 1983). The eucalypt genera Eucalyptus and Corymbia have many favourable characteristics including high growth rates, wide adaptability to soils and climates, ease of management through coppicing, valuable wood properties and absence of any tendency to spread as weeds in most environments. Only a relatively few species from the many in the genera are preferred for fuelwood, pole or pulpwood plantations. The particular species planted depend on the climate. Reliable global estimates for areas of planted eucalypts are difficult to obtain, but published reports (e.g. Davidson 1995) suggest that there were close to 14 million hectares at the end of 1993. Over 90% of these forests have been established since 1955 and about 50% since the mid 1980s (Turnbull 1991). There were over 10 million hectares of tropical eucalypt plantations at the end of 1990, principally in tropical America (4 million ha) and tropical Asia (5 million ha) (Food and Agriculture Organization 1993). The American statistic is dominated by Brazil where there are 3.2 million hectares (EMBRAPA 1996), including part of an area of 2.9 million hectares

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approved for plantation development using government incentives between 1967 and 1984 (Iuseum et al. 1988; Bazett 1993). In tropical Asia, India has over four million hectares including trees planted in various configurations on farms (Davidson 1995). In addition, there are substantial plantations in countries with more temperate climates including Chile 180,000 hectares, China 670,000 hectares, Morocco 200,000 hectares, Portugal 500,000 hectares, South Africa 538,000 hectares and Spain 350,000 hectares (Davidson 1995). Increased areas of eucalypt plantation are projected in several countries. Plantings will continue in Brazil but not at the very high rates of the recent past as there will be more effort to increase the productivity and quality of existing areas. In Portugal too, highly productive clonal plantations of E. globulus are being developed. Both China and India have active reforestation programs, and although there has been some resistance to eucalypt plantations in the latter, the great demand for wood and restrictions on harvesting in native forests will undoubtedly ensure that planting continues. In recent years, eucalypt planting has accelerated in several tropical countries, although extensive planting of eucalypts in the lowland humid tropics has been inhibited by a high incidence of pathogens and insect pests that reduce productivity. Only a few eucalypt species, such as E. deglupta, E. pellita and E. urophylla, are adapted to hot, humid conditions (Werren 1991). Planting of other species tends to result in severe damage by foliar diseases (e.g. Cylindrocladium spp.) associated with trees under stress (see Chapter 9). Despite this, about 200,000 hectares of E. camaldulensis have been established in Thailand (Pousajja 1996) and there are major planting programs in the Congo (Bouillet et al. 1999) and in Vietnam (Tran Xuan Thiep 1996). There are also active plantation programs in the more temperate areas such as those in South America especially in Chile, Paraguay and Uruguay. ‘Opportunities to increase world wood supply in the future will depend on plantations as a consequence of the likely static or decreasing supply from natural forests through deforestation, past overexploitation, greater reservation for nonwood uses or values, and increased costs of access and extraction’ (Kile 1999). If this scenario is 4

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correct, then the current trend to increase the area of eucalypt plantations will continue and the total area will exceed 20 million hectares by 2010.

1.4 Industrial eucalypt plantations There is no sector of world forestry that is expanding as rapidly as the industrial use of eucalypts. Most plantations are being established to provide mediumdensity to low-density short-fibred pulp for paper. Global short-fibre pulp consumption is about 13 million tons per annum and is growing at 3.9% annually (World Resources Institute 1998). Plantation-grown eucalypt wood is usually harvested after 5 to 10 years and provides a uniform material with high brightness, and good opacity and bulk which make the pulp very suitable for the production of copying, printing, writing and tissue papers. Demand for these products is rising and with it the demand for eucalypt pulp. Brazil is the largest producer of eucalypt pulp: its plantations, mainly of E. grandis, yield annually over two million tons of bleached pulp out of a total world production of about five million tons (World Resources Institute 1998). Portugal was the first country to produce eucalypt sulphite pulp in 1906 (Rolo 1988). Increasing interest over the past 20 years has brought E. globulus to prominence as a major source of income in the Portuguese economy. Portugal is the world’s second largest producer of eucalypt bleached pulp and the pulp industry accounts for the majority of Portuguese forestry exports. Other major eucalypt pulp producers are Chile (E. globulus), Morocco (E. camaldulensis), Spain (E. globulus) and South Africa (E. grandis). Very high levels of investment are required for the pulp and paper industry. In Chile, private investment in forestry was about US$4 billion in 1996 and 15% of these funds were invested in eucalypts. Another example of the high level of investment in the eucalypt pulp industry is the Brazilian company, Aracruz Celulose S.A. Since 1973 the company has invested heavily in research, plantation management and processing plant. Tree improvement with an emphasis on clonal forestry increased the productivity of plantations from 5.9 to 10.9 tonnes per hectare per annum (Bertolucci et al. 1995). The company invested US$1.15 billion in 1990 in an expansion of its pulp mill to lift production to one million tonnes per annum and is planning a 20%

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expansion (Aracruz 1991; World Resources Institute 1998). It supplies 22% of the world’s bleached eucalypt pulp and 3% of the world’s total demand for pulp (Campinhos 1999). In 1995, Aracruz Celulose S.A. had a total revenue of US$796 million and is a major contributor to Brazil’s domestic economy. At the same time it contributes health care, housing, education and other benefits to the local communities in and around its plantations (World Resources Institute 1998). However, the greater part of the eucalypt plantations in Brazil is used to provide high quality industrial charcoal for iron and steel production. Minas Gerais State, the centre of Brazil’s iron and steel industry, uses 70% of the wood from its eucalypt forests for production of industrial charcoal. There are several private companies in the State, each managing 150,000 to 200,000 hectares of eucalypt plantations. The main species used in charcoal plantations is E. grandis but C. citriodora, E. camaldulensis, E. cloeziana and E. paniculata are also significant. The latter species yield more charcoal per kilogram than E. grandis but are generally slower growing. Forest managers have long recognised the potential to grow more wood per unit area through the application of tree breeding and more intensive management practices. In Brazil, the company Aracruz Celulose S.A. almost doubled yields from its plantations by species and provenance selection, breeding and the use of clones (Campinhos 1999); the company has 85% of its plantings from clonal cuttings (Bertolucci et al. 1995). Selected clones are also used routinely in eucalypt plantations in the Congo, Morocco and South Africa. Better land preparation, correct use of fertiliser, improved nutrient uptake with selected mycorrhizas and good weed control offer additional opportunities for productivity gains. Domestication of the eucalypts has proceeded faster in countries like Brazil that rely on plantations than in Australia, where industrial wood products have been derived almost entirely from native forests. The countries with long-standing eucalypt plantations (e.g. Brazil, Portugal, Spain, South Africa) are now an important source of eucalypt genotypes adapted for plantation use. Only since the early 1990s have more intensive methods of large-scale eucalypt plantation management been used on a wide scale in Australia, where declining production of wood products from the original native forest and woodland estate due to their

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degradation, clearing for agriculture or protection in conservation reserves has resulted in increasing reliance on plantations. Initially exotic Pinus species were planted over large areas in Australia, but increasingly eucalypts are now being planted (O’Connell and Grove 1999). Great economic benefits will accrue from clonal plantations and more intensive management practices. These potential benefits need to be balanced with the increased risks of loss by pests and diseases, fire, frost, storms or nutrient imbalances in plantations with a high value of investment per unit area. In particular, densely planted, uniform-aged plantations with a narrow genetic base are ecologically prone to outbreaks of pests and diseases. However, the greater economic investment and return involved in plantations allows more intensive control of diseases in the plantations, including selection and breeding for disease resistance which could reduce initially damaging diseases to insignificant levels (see Chapters 18 and 22).

1.5 Eucalypts in the rural landscape Population growth has led to a greater demand for fuelwood, poles, paper and other wood products. To meet these needs, forest exploitation has accelerated to unsustainable levels, resulting in degradation of land, forests and woodlands. In countries like India, where fuelwood is the main source of energy for the rural population, there is an annual shortfall in supply. Palanna (1996) states, ‘Today in India there is enough food for people, thanks to the green revolution, but there is not sufficient wood to cook it’. The scale of wood shortages in many countries is such that government-run, larger scale planting programs alone cannot meet the needs. Increasingly, farmers and other land holders are becoming involved in providing wood from new plantings on small farms. Farmers plant trees for a variety of reasons including: 1

shade and shelter

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Although fuelwood derived from prunings and thinnings is an important product, the trees are more valuable as a source of pulpwood, construction wood, poles and posts that can be sold for cash (Kerkhof 1990; Palanna 1996). Tree planting for shade, shelter and the marking of farm boundaries is also important for some farmers. The use of trees for shading crops like coffee and cocoa can provide an important secondary source of income. Trees are also widely used by smallholders as an important source of long-term financial investment, to be harvested when there is a need for cash. Eucalypts have characteristics that can meet most of these requirements and have proved attractive to farmers in many parts of the world. Some rural landscapes in countries such as Ethiopia, China, Vietnam, India and Peru are dominated by eucalypts established mainly by farmers on small holdings. In Ethiopia, farmers plant E. globulus on small areas of land and may subsequently manage the plot to yield a variety of products including leaves and small branches for fuelwood, and poles and posts for house building, fences and other farm uses. Farmers who have insufficient land to have woodlots nevertheless often grow a few trees which can be harvested and sold when they experience food shortages. Many people in Ethiopia are absolutely dependent on eucalypts as a source of fuel and house building material. Eucalypts are a prominent and important part of the rural landscape in southern China. There are largescale plantations as well as dispersed plantings on small farms and on the borders of roads, railways and waterways. In addition to the estimated 600,000 hectares of eucalypt plantations, some one billion individual trees are planted beside farm houses and along roads and waterways (Wang Huoran et al. 1994). The most widely planted species have been E. exserta, C. citriodora, E. globulus and a hybrid of unknown origin referred to as ‘E. leizhou No. 1’ but these are now being replaced by more desirable species such as E. grandis, E. urophylla and hybrids between the two. The eucalypts are favoured because they grow relatively fast and can tolerate the poor, degraded soils of southern China. The wood is used for posts and poles, pulpwood, furniture, farm tools and fuel; essential oils and tannins are extracted from the leaves, and the trees support honey production. Eucalypts are important in crop production by providing shelter from typhoons in coastal areas and 6

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make a significant contribution to the quality of life and income of the farmers (Zheng Haishui 1988). Eucalypts have been grown on an increasing scale by farmers in India since 1981 and have had a major effect on the rural landscape. As the Indian population approaches one billion, there is an immense requirement for wood for both industrial and domestic use but there is a substantial shortfall in production. The situation is little changed from 1990 when the demand for firewood was 306 million cubic metres and for industrial wood 32 million cubic metres compared with production of only 40 and 12 million cubic metres, respectively (Kumar 1991). Eucalyptus tereticornis, known locally as ‘Eucalyptus hybrid’ or ‘Mysore gum’, is the preferred species for planting in many areas. It is used extensively for village woodlots, on farms and along the boundaries of roads, canals and railways. It has also been planted widely on what are broadly termed ‘wastelands’ or degraded lands. Its popularity is based on its capacity for rapid growth, resistance to cattle browsing, great adaptability to varying environmental conditions, ready market at profitable prices and suitability of the wood for fuel, rural housing and fencing. Farmers have established block plantings and windbreaks on the margins of fields, and sometimes grow eucalypts combined with agricultural crops. Between 1981 and 1988 an estimated eight billion trees were planted on farms, more than 80% of them E. tereticornis, equivalent to about 2.5 million hectares of plantations (Saxena 1991). Eucalypts are often planted to meet future contingencies and have functioned as an important source of savings and long-term investment for the rural poor (Kumar 1991). Economic benefits have generally flowed from eucalypt plantations, although in some areas excessive planting by farmers (e.g. in Haryana and the Punjab) resulted in a local glut of fuelwood and small-sized poles, leading to falling prices. Farmers who planted early made large profits while those planting later did not get similar rewards. In most instances, the trees grown by farmers are to provide products and services to the rural population but there are plantations established by farmers primarily to supply wood to industrial enterprises. In Spain, farmers cooperated with a private pulp and paper company, Celulosas de Asturias, to grow eucalypts on their land for sale to the mill while also making money from the production of honey and essential oils (CEASA 1994). Similar schemes have

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operated in Brazil (e.g. de Freitas 1996), the Philippines (Turnbull 1999) and elsewhere. In India, as in some other countries, there is continuing controversy over the use of eucalypts. There are questions about the diversion of crop land from food production to forestry, reduction in employment and the utilisation of common lands for eucalypt growing by the more powerful members of the community. While from the farmer’s or entrepreneur’s viewpoint eucalypt growing makes economic sense, the landless poor may endure increased hardship and reduced welfare when farmers grow eucalypts (Gregersen et al. 1989). Although the debate is frequently framed in terms of the beneficial and negative ecological effects of eucalypts, the major problem relates to land availability, tenure and management (Poore and Fries 1985; Raintree 1996). Hydrological studies of eucalypt plantings show a complex series of interactions, some of which may be seen as beneficial and others as detrimental (Calder 1992). According to an analysis by Raintree and Lantican (1993), ‘the real crux of the political controversy surrounding eucalyptus planting in India was the opportunity cost of a Social Forestry program which generated such dramatic benefits for the relatively better off segments of society while leaving the originally targeted beneficiaries of the Social Forestry program without benefit’. Clearly, if eucalypts are to realise their full potential to provide benefits to a community there will need to be much more careful analysis of ecological and, particularly, social factors before extensive planting programs are undertaken. While the native eucalypt forests and woodlands have always been a valuable source of fuelwood and building and fencing materials for Australian farmers, degradation of the original natural resources has now led to increasing planting of eucalypts on farmland, particularly to help rectify problems of soil degradation and salinity associated with loss of native vegetation (Marcar 1996). Eucalypts, especially E. globulus, are also now becoming an important source of income for farmers in southwest and south-east Australia who grow small plantations in collaboration with forestry companies interested in producing pulpwood (Butcher 1996).

1.6 Conclusion In the first decades of the new millennium, the shortfall in fuelwood and building materials will be

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desperate, especially in the densely populated countries of Africa, Latin America, and South and East Asia where much of the natural forest has disappeared or is severely degraded. Consumption of fuelwood and poles will increase substantially and natural forest will continue to be degraded by unsustainable harvesting or lost to agriculture. Trees, including eucalypts, will be critically important in providing wood products and assisting sustainable agriculture on the more marginal lands in these countries. Large-scale plantations of eucalypts in many countries, including Australia, will continue to supply a large proportion of the pulp used for paper manufacture, the demand for which continues to expand. The management of these plantations will continue to intensify with increasing selection of highly productive genotypes, clonal propagation, attention to land preparation, use of fertilisers, and use of intensive disease control measures, particularly selection and breeding of disease-resistant genotypes. Eucalypts, because of their adaptation to a wide range of environments, fast growth, ease of management, and the valuable properties of their wood and pulp, will continue to have a major and often expanding role in providing wood products, improved standards of living and environmental protection in many countries.

1.7 References Aracruz Celulose (1991). Aracruz Celulose S.A., Brazil, Annual Report 1990. Aracruz Celulose, Brazil. Australian Bureau of Agricultural and Resource Economics (1997). Australian Forest Products Statistics. June Quarter 1997. ABARE Project 1116. (Australian Bureau of Agricultural and Resource Economics: Canberra.) Australian Bureau of Agricultural and Resource Economics (1999). Forest products: outlook in regional markets to 2003–04. Australian Commodities, Forecasts and Issues 6, 91–102. Australian Forestry Council (1989). Australian Forest Resources Present Areas and Estimates of Future Availability. (Forestry Resources Committee of the Australian Forestry Council: Canberra.) Bazett, M.D. (1993). Industrial Wood. Study No. 3. Shell/ World Wide Fund For Nature Tree Plantation Review. (Shell and WWF: London.) Bertolucci, F.L.G., Demuner, B.J., Garcia, S.L.R. and Ikemori, Y.K. (1995). Increasing fiber yield and quality at Aracruz. In Eucalypt Plantations: Improving Fibre Yield and Quality. Proceedings of the CRCTHF–IUFRO Conference, Hobart, 19–24

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February 1995. (Eds B.M. Potts, N.M.G. Borralho, J.B. Reid, R.N. Cromer, W.N. Tibbits and C.A. Raymond) pp. 31–34. (Cooperative Research Centre for Temperate Hardwood Forestry: Hobart.) Bouillet, J.P., Nzila, J.D., Ranger, J., Laclau, J.P. and Nizinski, G. (1999). Eucalyptus plantations in the Equatorial Zone, on the coastal plains of Congo. In Site Management and Productivity in Tropical Plantation Forests. (Eds E.K.S. Nambiar, C. Cossalter and A. Tiarks) pp. 13–21. (Center for International Forestry Research: Bogor, Indonesia.) Butcher, G. (1996). Establishment of a major hardwood resource in Western Australia. In Environmental Management: The Role of Eucalypts and Other Fast Growing Species. (Eds K.G. Eldridge, M.P. Crowe and K.M. Old) pp. 146–151. (CSIRO Division of Forestry and Forest Products: Canberra.) Calder, I.R. (1992). Water use of eucalypts—a review. In Growth and Water Use of Forest Plantations. (Eds I.R. Calder, R.L. Hall and P.G. Adlard) pp. 167–179. (J. Wiley: New York.) Campinhos, E. (1999). Sustainable plantations of high yield Eucalyptus trees for production of fiber: the Aracruz case. New Forests 17, 129–143. Carron, L.T. (1985). The History of Forestry in Australia. (Australian National University Press: Canberra.) CEASA (1994). Intelligent fibre. World Paper. Nov./Dec. 1994. 2 pp. Commonwealth of Australia (1997). Australia’s First Approximation Report for the Montreal Process. (Department of Primary Industries and Energy: Canberra.) Cromer, R., Smethurst, P., Turnbull, C., Misra, R., LaSala, A., Herbert, A. and Dimsey, L. (1995). Early growth of eucalypts in Tasmania in relation to nutrition. In Eucalypt Plantations: Improving Fibre Yield and Quality. Proceedings of the CRCTHF–IUFRO Conference, Hobart, 19–24 February 1995. (Eds B.M. Potts, N.M.G. Borralho, J.B. Reid, R.N. Cromer, W.N. Tibbits and C.A. Raymond) pp. 331–335. (Cooperative Research Centre for Temperate Hardwood Forestry: Hobart.) Davidson, J. (1995). Ecological aspects of Eucalyptus plantations. In Proceedings of the Regional Expert Consultation on Eucalyptus, Vol. I, pp. 35-72. RAPA Publication 1995/6. (Food and Agriculture Organization Regional Office for Asia and the Pacific: Bangkok.) de Freitas, M. (1996). Planted forests in Brazil. In Caring for the Forest: Research in a Changing World. IUFRO XX World Congress, Tampere, Finland, 6–12 August 1995. Congress Report, Vol. II, pp. 147–154. (International Union of Forestry Research Organizations: Tampare, Finland.) EMBRAPA (1996). Brasil tem banco estrategico de eucalipto. Folha da Floresta No. 8, 6–8.

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Food and Agriculture Organization (1991). Wood and Wood Products. Forestry Statistics Today for Tomorrow. 1961–89 to 2010. (Food and Agriculture Organization: Rome.) Food and Agriculture Organization (1993). Forest Resources Assessment 1990: Tropical Countries. Food and Agriculture Organization Forestry Technical Paper 112. (Food and Agriculture Organization: Rome.) Gregersen, H., Draper, S. and Elz, D. (1989). People and Trees—The Role of Social Forestry in Sustainable Development. (The World Bank: Washington DC.) Hillis, W.E. and Brown, A.G. (Eds) (1983). Eucalypts for Wood Production. 2nd edn. (CSIRO: Melbourne.) Iuseum, A.N., Correa de Lima, J.P. and Mercado, R.S. (1988). Brazil: the forest sector’s participation in international trade. In International Trade in Forest Products. (Ed. A. Nagy) pp. 37–46. (A.B. Academic Publishers: Bicester, UK.) Kerkhof, P. (1990). Agroforestry in Africa: a Survey of Project Experience. (Eds G. Foley and G. Bernard). (Panos: London.) Kerruish, C.M. and Rawlins, W.H.M. (Eds) (1991). The Young Eucalypt Report—Some Management Options for Australia’s Regrowth Forests. (CSIRO: Melbourne.) Kile, G.A. (1999). Planted forests for food, fibre, fuel and fulfillment. Paper to the Crawford Fund Seminar on The Food and Environment Tightrope, 24 November 1999, Canberra, Australia. Kumar, V. (1991). Eucalyptus in the forestry scene of India. In Proceedings of IUFRO Symposium on Intensive Forestry: The Role of Eucalypts. Durban, September 1991. (Ed. A.P.G. Schönau) Vol. 2, pp. 1105–1116. (South African Institute of Forestry: Pretoria, South Africa.) Marcar, N.E. (1996). Eucalypts for salt-affected and acid soils. In Environmental Management: The Role of Eucalypts and Other Fast Growing Species. (Eds K.G. Eldridge, M.P. Crowe and K.M. Old) pp. 90–99. (CSIRO Division of Forestry and Forest Products: Canberra.) Nambiar, E.K.S. and Brown, A.G. (1997). Management of Soil, Nutrients and Water in Tropical Plantations. ACIAR Monograph No. 43. (Australian Centre for International Agricultural Research: Canberra.) O’Connell, A.M. and Grove, T.S. (1999). Eucalypt plantations in south-western Australia. In Site Management and Productivity in Tropical Plantation Forests. (Eds E.K.S. Nambiar, C. Cossalter and A. Tiarks) pp. 53–59. (Center for International Forestry Research: Bogor, Indonesia.) Palanna, R.M. (1996). Eucalyptus in India. In Reports Submitted to the Regional Expert Consultation on Eucalyptus. Vol. II, pp. 46–57. RAP Publication 1996/ 44. (FAO Regional Office for Asia and the Pacific: Bangkok.)

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Poore, M.E.D. and Fries, C. (1985). The Ecological Effects of Eucalyptus. Food and Agriculture Organization Forestry Paper No. 59. (Food and Agriculture Organization: Rome.) Pousajja, R. (1996). Eucalypt plantations in Thailand. In Reports Submitted to the Regional Expert Consultation on Eucalyptus. Vol. II, pp. 213–223. RAP Publication 1996/44. (FAO Regional Office for Asia and the Pacific: Bangkok.) Raintree, J.B. (1996). The great Eucalyptus debate: what is it all about? In Reports Submitted to the Regional Expert Consultation on Eucalyptus. Vol. II, pp. 64–74. RAP Publication 1996/44. (FAO Regional Office for Asia and the Pacific: Bangkok.) Raintree, J.B. and Lantican, C. (1993). Forestry economics research and MPTS development. In Forestry Economics Research in Asia. (Eds Songkram Thammincha, Ladawan Puangchit and H. Wood) pp. 15–31. (Faculty of Forestry, Kasetsart University: Thailand and IDRC: Canada.) Resource Assessment Commission (1991). Forest and Timber Inquiry. Draft Reports Vols 1 and 2. (Resource Assessment Commission, Australian Government Publishing Service: Canberra.) Resource Assessment Commission (1992). Forest and Timber Inquiry. Final Report. Vols 1, 2A and 2B. (Resource Assessment Commission, Australian Government Publishing Service: Canberra.) Rolo, L.B. (1988). The outlook of the Portuguese pulp industry. In Global Issues and Outlook in Pulp and Paper. (Ed. G.F. Schreuder) pp. 142–150. (University of Washington Press: Seattle.) Saxena, N.C. (1991). Marketing constraints for Eucalyptus in farmlands in India. Agroforestry Systems 13, 73–85. Tran Xuan Thiep (1996). Eucalyptus plantations in Vietnam: their history and development process. In Reports Submitted to the Regional Expert Consultation on Eucalyptus. Vol. II, pp. 254–277. RAP Publication 1996/44. (FAO Regional Office for Asia and the Pacific: Bangkok.) Turnbull, J.W. (1991). Future use of Eucalyptus: opportunities and problems. Proceedings of IUFRO Symposium on Intensive Forestry: The Role of Eucalypts. Durban, September 1991. (Ed. A.P.G.

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Schönau) Vol. 1, pp. 2–27. (South African Institute of Forestry: Pretoria, South Africa.) Turnbull, J.W. (1996). Biodiversity in Australian forest ecosystems. In Caring for the Forest: Research in a Changing World. IUFRO XX World Congress, Tampere, Finland, 6–12 August 1995. Congress Report, Vol. II, pp. 90–99. (International Union of Forestry Research Organizations: Tampere, Finland.) Turnbull, J.W. (1999). Eucalypt plantations. New Forests 17, 37–52. Wang Huoran, Jiang Zeping and Yan Hong (1994). Australian trees grown in China. In Australian Tree Species Research in China. (Ed. A.G. Brown) pp. 19–25. ACIAR Proceedings No. 48. (Australian Centre for International Agricultural Research: Canberra.) Wells, K.F. (1991). The young eucalypt resource. In The Young Eucalypt Report. (Eds C.M. Kerruish and W.H.M. Rawlins) pp. 19–27. (CSIRO: Melbourne.) Wells, K.F., Wood, N.H. and Laut, P. (1984). Loss of forests and woodlands in Australia: A summary by State based on rural local government areas. CSIRO Division of Water and Land Resources Technical Memorandum 84/4. (CSIRO: Canberra.) Werren, M. (1991). Eucalyptus plantation development in Sumatra. In Proceedings of IUFRO Symposium on Intensive Forestry: The Role of Eucalypts. Durban, September 1991. (Ed. A.P.G. Schönau) Vol. 2, pp. 1160–1166. (Southern African Institute of Forestry: Pretoria, South Africa.) Wood, M., Howell, C. and Jones, M. (1999). Australia’s national plantation inventory: an interim update. In Australian Forest Products Statistics, September Quarter, pp. 1–2. (Australian Bureau of Agricultural and Resource Economics: Canberra.) World Resources Institute (1998). Aracruz Celulose S.A. and Riocell S.A.: efficiency and sustainability on Brazilian pulp plantations. In The Business of Sustainable Forestry: Case Studies. pp. 5–1 to 5–31. (The John D. and Catherine T. MacArthur Foundation: Chicago.) Zheng Haishui (1988). The role of Eucalyptus plantations in southern China. In Multipurpose Tree Species for Small-Farm Use. (Eds D. Withington, K.D. MacDicken, C.B. Sastry and N.R. Adams) pp. 79–85. (Winrock International and IDRC: Canada.)

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Eucalypts are an assemblage of mainly tree species in the myrtaceous genera Eucalyptus, Corymbia and Angophora. They are generally long-lived, evergreen species that include some of the very tall, fast-growing hardwood species now in great demand for planting around the world. Most are endemic to Australia, with a few species extending into islands to the north, and have evolved largely in isolation in Australia. From north to south, the climate of the vast Australian continent changes from summer to winter rainfall and from warm to cooler seasons which, combined with the effect of variations in altitude, aspect and soils, has resulted in an immense diversity of habitats to which eucalypts have adapted. They show exceptional differentiation and there are often large genetic differences. This variation provides the basis for selection and breeding of variants adapted to a wide range of plantation environments. There are many examples of genetic variation in susceptibility to disease both between and within species and this variation can be exploited for disease management.

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2.1 Introduction Eucalypts belong to the predominantly southern hemisphere family, Myrtaceae (Johnson and Briggs 1984) and have traditionally encompassed the more than 700 species in the genus Eucalyptus L’Hér., as well as the 11 closely related taxa in the genus Angophora Cav. (Pryor and Johnson 1971; Pryor 1976; Pryor and Johnson 1981; Brooker and Kleinig 1994; Hill and Johnson 1995; Ladiges et al. 1995). Angophora has flowers with free sepals and petals whereas in Eucalyptus, with only rare exceptions, these are fused to form one or two opercula which cover the numerous stamens and single style (Ladiges 1997). The eucalypts are virtually all endemic to Australia and together with the monotypic genus Arillastrum from New Caledonia, form the Eucalyptus alliance (subfamily Leptospermoideae) of Johnson and Briggs (1984).

2.2 Morphology Eucalypts are generally long-lived, forest (30–50 m) or woodland (10–25 m) trees, or mallees (several stems 1–10 m high emerging from a common underground woody stock) (Pryor 1976). The genus Eucalyptus contains the tallest hardwood species in the world, E. regnans, which grows in the mountains of Victoria and Tasmania and has attained heights over 100 metres (Mace 1996). Other species such as E. deglupta, E. diversicolor and E. viminalis may grow to more than 70 metres (Boland et al. 1985). At the other extreme, some species are mere shrubs (e.g. E. vernicosa, Potts and Jackson 1986; E. fruticosa, Brooker and Kleinig 1994). Eucalypts are evergreen, except for several northern Australian species that shed most of their leaves during the northern dry season (e.g. Corymbia confertiflora; Brooker and Kleinig 1994). Species exhibit large differences in form, habit, reproductive and foliage characteristics. The foliage may also change dramatically through ontogeny (heteroblasty), with leaf morphology, anatomy, surface waxes, phyllotaxis and orientation often changing considerably between seedling (up to about the 10th node), juvenile and adult stages (Fig. 2.1; Boland et al. 1985; Brooker and Kleinig 1990a; Wiltshire et al. 1991; Hill and Johnson 1995). Ontogenetic changes may also occur in physiology (Cameron 1970; Battaglia and Reid 1993), leaf chemistry (Li et al. 1995), pest (autumn gum moth; Farrow et al. 1994) and disease susceptibility

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Figure 2.1

Branch showing juvenile (larger, lower) and adult (narrow, uppermost) leaves of Eucalyptus globulus ssp. globulus.

(e.g. to Mycosphaerella (M.) spp., see Chapter 9). In some species (e.g. E. cinerea, E. perriniana, E. risdonii), the juvenile foliage type is maintained at reproductive maturity. While many species have a persistent dead outer bark, ranging in appearance from fibrous (‘stringy bark’) to scaly (‘box bark’), the bark of others is decorticating, resulting in smooth stems (‘gum bark’) of variable colour (Boland et al. 1985; Brooker and Kleinig 1990a, 1990b; Brooker and Kleinig 1994). The bark often protects numerous dormant vegetative buds. These sprout to form masses of leafy shoots (epicormic shoots) over the trunk and branches after trees are defoliated or damaged by fire (Fig. 2.2), drought or pests (Jacobs 1955; Pryor 1976). Eucalypts have very efficient mechanisms of branch shedding and occlusion of the resulting wound (Jacobs 1955). A protective layer of tannins or resins is deposited around the part of the moribund branch already included in the stem and kino may be secreted over branch stubs resulting in protection from fungal attack. Most species also

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Figure 2.3 Figure 2.2

A tree of Eucalyptus globulus ssp. globulus regenerating from epicormic shoots following wildfire.

have an unusual organ, the lignotuber, which develops as swellings in the axils of the cotyledons and sometimes the first few seedling leaves and comprises a mass of vegetative buds, vascular tissue and food reserves (Jacobs 1955; Pryor 1976; Fig. 2.3). The lignotuber generally becomes buried and is extremely important in survival where drought and fire are frequent, allowing plants (particularly seedlings) to regenerate after death or damage to the main stem. Continual damage to mature plants may result in the development of the mallee habit and large, clonal copses from underground lignotubers (Lacey and Johnston 1990; Kennington and James 1997). Other vegetative regeneration mechanisms, such as rhizomes or root suckering, are rare (Lacey 1974; Lacey and Johnston 1990; Hill and Johnson 1995). Regeneration is usually from seed which is

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Lignotubers developing on a sapling of Eucalyptus risdonii. Stem diameter immediately above the basal lignotuber is about 1.5 centimetres.

stored in woody, fire-protected capsules in the canopy and shed in mass, especially following wildfire (Boland et al. 1980). Seeds generally have no special mechanisms for dispersal, apart from the terminally winged seed of the red bloodwoods. Except for a few cases of water dispersal (e.g. E. camaldulensis) and a single report of bee dispersal (Wallace and Trueman 1995), seed dispersal is mainly by wind and gravity and normally occurs over short distances (Potts and Wiltshire 1997). The eucalypt flower is normally bisexual (Fig. 2.4), although rare male sterile individuals have been reported (Pryor 1976; Ellis and Sedgley 1993). The numerous stamens and the perigynous arrangement of the outer floral whorls are characteristic of the Myrtaceae. However, the operculum is unique to the group although its derivation differs and it appears

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Flowers of Eucalyptus globulus ssp. globulus showing the inner operculum just about to be shed (right) and fully expanded anthers (left).

to have evolved independently several times (Ladiges 1997). The eucalypt flowers are occasionally solitary (e.g. E. globulus, Fig. 2.4), but generally occur in clusters of regular numbers of 3, 5, 7, 11, 15 or more in an inflorescence, which is effectively a reduced dichasial cyme, but is often called an ‘umbel’ (Johnson 1972; Pryor 1976). Flower clusters may arise singly in the leaf axils (simple axillary inflorescence), as paired axillary inflorescences or compound axillary or terminal inflorescences (Brooker and Kleinig 1990a), with the compound inflorescences developing in a manner unique to eucalypts (Pryor 1976). At anthesis, the operculum is shed and the stamens spread, resulting in a conspicuous floral display (House 1997). Pollination is undertaken by a variety of insects, birds and marsupials (Pryor 1976; Eldridge et al. 1993; House 1997; Potts and Wiltshire 1997). Eucalypts are generally preferential outcrossers with high levels of outcrossing maintained by protandry and various prezygotic and postzygotic barriers to self fertilisation (Pryor 1976; Potts and Wiltshire 1997), coupled with intense, post-dispersal selection against the products of self fertilisation in the regenerating forest (Hardner and Potts 1997).

2.3 Phylogeny As originally defined, the eucalypts are not a natural grouping of taxa. From the early 1990s there has been a major change from a classical to cladistic

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Figure 2.5

Proposed phylogenetic relationships in the Eucalyptus alliance (after Ladiges 1997).

based, phylogenetic treatment of the group (reviewed in Hill and Johnson 1995; Ladiges 1997). In an informal but widely used classification of eucalypts, Pryor and Johnson (1971) divided Eucalyptus into seven subgenera (Corymbia, Blakella, Eudesmia, Gaubaea, Idiogenes, Monocalyptus, Symphyomyrtus), with the genus Angophora considered of equal rank. An eighth subgenus (Telocalyptus) comprising four tropical eucalypts with truly terminal inflorescences (E. deglupta, E. howittiana, E. raveretiana, E. brachyandra) was later suggested by Johnson (1976). Johnson (1976) subsequently proposed that the eucalypts (and Angophora) be rearranged into nine groups or genera (one of which would retain the name Eucalyptus) and these would have about the same degree of distinctness as existed between Eucalyptus and Angophora. Pryor and Johnson (1981) later suggested that the bloodwoods (Blakella and Corymbia) were more closely related to Angophora than to the rest of Eucalyptus and that the eucalypts were polyphyletic, comprising three major evolutionary lineages (or suballiances): 1

Arillastrum, Angophora, Blakella and Corymbia

2

Symphyomyrtus, Telocalyptus and Eudesmia

3

Monocalyptus, Idiogenes and Gaubaea.

The most recent view of eucalypt phylogeny, which is relatively consistent across morphological (Hill and Johnson 1995; Ladiges et al. 1995) and molecular (Sale et al. 1993; Hill and Johnson 1995; Ladiges et al. 1995; Urdovic et al. 1995; Sale et al.

M O RP HO LO GY , P HYL OGENY , O R IGIN , D IST R I BU T I ON

TA BLE 2. 1

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Summary of the key characters differentiating Angophora, Corymbia and the major subgenera of Eucalyptus

After Ladiges (1997) with minor additions from Brooker and Kleinig (1994) and Hill and Johnson (1995). Characteristics of the minor Eucalyptus subgenera Gaubaea, Idiogenes and Telocalyptus are given in Ladiges (1997).

Group

No. of taxa

Angophora/ bloodwood lineage

Characteristics Pinnate venation; raised oil glands (bristle glands) with 4 cap cells of raised oil glands with micropapillae (conspicuous in seedlings); oxalate crystals in embryonic cotelydons; stemonophore absent; pith oil ducts; solitary vessels in the xylem; hemitropous ovules not in regular rows; seed with 2 integuments

Angophora

11–13

Free sepals and petals; corymbioid inflorescences; mop-like stigma with long papillae; pinnate venation; opposite disjunct phyllotaxy; multicellular hairs; cotyledons large and unfolded in embryo; fruits with ridges

Corymbia

113

Calycine operculum; stigmas mop-like or tapering with short papillae; conflorescences terminal corymbioid to axillary; stigmas mop-like with long papillae or tapering with short papillae; opposite disjunct phyllotaxy but alternate adult leaves; unicellular hairs associated with raised oil glands; cotyledons entire, either folded in embryo or not; fruits woody or thin walled

600+

Sepals and petals free or flowers with 1 or 2 opercula; taxa with corolline operculum develop a stamonophore; adult leaves usually with wide spaced, more irregular secondary veins than bloodwoods; opposite disjunct phyllotaxy; if present raised oil glands have 3 cap cells and no micropapillae; stigmas usually with relatively short papillae; regular arrangement of ovules in vertical rows on the placenta; embryos with folded, emarginate or bilobed cotyledons; fruits woody

Subgenus Eudesmia

20

Free sepals (sometimes not obvious); corolline operculum; in some species stemonophore lobed and stamens appear to be in 4 bundles; some subgroups with characteristic hairs radiating from oil glands; hemitropous ovules in 2–4 rows per loculus; seed with 2 integuments

Subgenus Monocalyptus

120+

Single operculum (thought to be derived from petals, lacking sepals); stemophore; axillary conflorescences; anatropous ovules; usually in 2 rows per loculus; seed with 2 integuments; lacking crystalliferous layer in outer integument; reniform cotyledons

Subgenus Symphyomyrtus

300+

Calycine and corolline operculum; stemophore; conflorescences usually axillary; hemitropous ovules in 4–10 rows; seed with 1 integument; emarginate cotyledons

Eucalyptus s. str. lineage

1996) studies, is of two major lineages, one including Angophora, subgenus Corymbia (bloodwoods) and subgenus Blakella (paper fruited bloodwoods or ghost gums), and the other comprising all other subgenera of Eucalyptus (Fig. 2.5). The subgenera Corymbia and Blakella of Pryor and Johnson (1971) have now been formally separated from the rest of Eucalyptus in a new genus, Corymbia K.D.Hill and L.A.S.Johnson (Hill and Johnson 1995), containing 113 species. A detailed classification of these species is provided by Hill and Johnson (1995). Key characteristics of Angophora, Corymbia and Eucalyptus s. str. (and subgenera) are summarised in Table 2.1. In the non-bloodwood eucalypts (Eucalyptus s. str.), the adult leaves have opposite disjunct phyllotaxis,

but with secondary venation more widely spaced and more irregular than in the bloodwoods (Ladiges 1997; Table 2.1). In Eucalyptus, the sepals and/or the petals are also fused into one or two opercula, which appear to have evolved independently from that in the bloodwoods. Within the non-bloodwood eucalypts, three major lineages are recognised (see Ladiges et al. 1995; Ladiges 1997; Fig. 2.5): 1

Eudesmia (eudesmids)

2

Monocalyptus (monocalypts)

3

Symphyomyrtus (symphyomyrts).

The Symphyomyrtus lineage is characterised by the seed coat comprising one integument, rather than two (Table 2.1). Virtually all species have two

15

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Transversaria Maidenaria Exsertaria Adnataria Dumaria Bisectaria Figure 2.6

Proposed phylogenetic relationship among the major sections in the subgenus Symphyomyrtus (after Chappill and Ladiges 1996; Ladiges 1997).

opercula, although they may be closely fused in some species (e.g. section Adnataria, boxes and iron barks) (Pryor and Johnson 1971). Symphyomyrtus is the largest subgenus and includes more than 300 species in six major sections (Fig. 2.6). Most species used in plantation forestry, particularly outside Australia, are from Pryor and Johnson’s (1971) sections Maidenaria (e.g. E. globulus, E. nitens, E. viminalis), Exsertaria (northern and eastern red gums) (e.g. E. camaldulensis, E. tereticornis) and Transversaria (eastern blue gums, red mahoganies, grey gums) (e.g. E. diversicolor, E. saligna, E. grandis, E. urophylla) (Eldridge et al. 1993). The Monocalyptus lineage includes the subgenera Gaubaea, Idiogenes and Monocalyptus. It is characterised by ovules being orientated with the micropile facing the placenta (anatropous) and arranged in two or rarely four rows, and seeds which do not have a crystalliferous layer (Ladiges 1997). The subgenus Gaubaea comprises two species, E. curtisii and E. tenuipes, which have unique features. This subgenus may not be monophyletic and a separate subgenus for E. curtisii has been suggested (Brooker and Kleinig 1994). The subgenus Idiogenes consists only of E. cloeziana, which appears to be the sister taxon to the subgenus Monocalyptus. These three species have small free sepals. In the subgenus Monocalyptus, the sepals are believed to be reduced or absent and the subgenus is characterised by a single operculum derived from

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early fusion of the petals (Drinnan and Ladiges 1989, cf. Pryor and Knox 1971). Monocalyptus is the second largest subgenus and includes groups commonly known as the peppermints (Ladiges et al. 1983), mahoganies, stringy barks (Ladiges and Humphries 1986) and green (Ladiges et al. 1989) and blue (Ladiges et al. 1992) ashes. Many of the monocalypts are important timber species, at least in native forests in Australia (e.g. E. delegatensis, E. diversifolia, E. fastigata, E. obliqua, E. regnans; Eldridge et al. 1993). Cladistic studies of the various Monocalyptus subgroups are reviewed by Ladiges (1997).

2.4 Origins The eucalypt fossil record is reviewed in Hill (1994), Rozefelds (1996) and Ladiges (1997). The ancestors of the Myrtaceae are thought to have migrated into the Australian region of Gondwana from Antarctica, as myrtaceous-like pollen in sediments of the Antarctic Peninsula from the Late Cretaceous [about 90–65 million years ago (MYa)] appears to predate the earliest New Zealand and Australian records from the Paleocene (65–55 MYa) (Dettmann 1994; Specht 1996). This migration was followed by an explosion of myrtaceous genera through the Tertiary, with most extant genera now occurring in the Australasian–Oceanian region and Central and South America (Johnson and Briggs 1981; Johnson and Briggs 1984; Specht 1996). Eucalypts are thought to have evolved from a rainforest or rainforest margin ancestor (Gill et al. 1985; Brooker 1986; Eldridge et al. 1993). Australia has traditionally been accepted as the place of origin and diversification of eucalypts (Carr 1973; Pryor 1976; Pryor and Johnson 1981) and Barlow (1981) considers they originated at least 40 million years ago, in the early Tertiary, on the fragment of Gondwana that formed Australia. This view was held because of the almost total restriction of the extant distribution to Australia, the distribution of related genera in New Guinea and New Caledonia, and the lack of fossil evidence from other countries. However, there are now several reports of eucalyptlike macrofossils occurring in Patagonia, South America (Miocene or Eocene; Frenguelli 1953) and Central Otago, New Zealand (Early Miocene; Pole 1989; Pole 1993 ) which, if correct, provide the first clues that eucalypts may not have been restricted to Australia (Fig. 2.7) and may have a more ancient

M O RP HO LO GY , P HYL OGENY , O R IGIN , D IST R I BU T I ON

Figure 2.7

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The natural distribution of: a) Angophora, b) Corymbia, and the Eucalyptus s. str. subgenera c) Eudesmia, d) Idiogenes and Gaubaea, e) Monocalyptus and f) Symphyomyrtus. Subgenera follow Pryor and Johnson (1971) whereas Corymbia and Angophora follow Hill and Johnson (1995).

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origin. In both cases, the fossils appear to be Symphyomyrtus-like. An ancient, extra-Australian distribution is given further credence by the finding of fossils of another typically Australian group, the she-oaks (Casuarinaceae), in South America and in New Zealand (with the eucalypt fossils); as for Eucalyptus, this group is presently absent from both regions (Hill and Carpenter 1990). Acacia, Casuarina and Eucalyptus-like pollen has also been recorded in Miocene–Early Pleistocene deposits in New Zealand (Mildenhall 1980), suggesting relatively recent extinction of these taxa in New Zealand (Hill 1994). The oldest eucalypt-like macrofossils in Australia appear to be fruits from a Palaeocene or Eocene (65–35 MYa) deposit in south-east Queensland that have affinities to Corymbia or Angophora (Rozefelds 1996). Although evidence is still sparse, eucalypts are believed to have been components of the more xeric vegetation in the interior of Australia during the Early Tertiary (Lange 1982; Martin 1982; Hill 1994). The frequent periods of aridity through the Miocene resulted in expansion of the xerophytic components of the Australian flora and evolution and diversification of xerophytic genera such as Eucalyptus (Martin 1978; Barlow 1981; Martin 1982; Specht 1996; Wardell-Johnson et al. 1997). With the progression of aridity in central Australia, eucalypts were displaced to the continental margins. Indeed, Victorian and New South Wales macrofossil deposits are consistent with a mosaic of eucalypt/ sclerophyllous and rainforest communities in southeast Australia during the Miocene (Holmes et al. 1983; Pole et al. 1993). However, pollen records suggest that the modern eucalypt flora did not become widespread until the Pleistocene (5–1.5 MYa; Martin 1981; Kershaw et al. 1994). The dominance of the Australian landscape by eucalypts appears to be relatively recent. The increase in eucalypt pollen over this period is associated with increased levels of charcoal, suggesting that the genus has undertaken a major spatial radiation in about the last 200,000 years as a response to increasing fire frequency due to the arrival of humans in Australia, coupled with increasing aridity and a remarkable preadaptation to fire (Singh et al. 1981; Kershaw 1986; Hill 1994). An important factor in the evolution of eucalypts is believed to be their adaptation to the nutrient-poor soils of the ancient land surfaces that dominate much

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of the Australian continent (Eldridge et al. 1993). Less oligotrophic environments appear to have become available to eucalypts only after the area of closed forest was reduced by climatic and other changes. Within Corymbia, for example, taxa with the more derived characters tend to occur on less nutrient-deficient soils (Hill and Johnson 1995). Late Miocene (5–10 MYa) fossils from Bacchus Marsh, Vic., provide the first unequivocal evidence of the subgenus Monocalyptus, as well as Symphyomyrtus (Ladiges 1997). However, biogeographical evidence would suggest that the divergence of Monocalyptus and Symphyomyrtus (Specht 1996), and even major lineages within Monocalyptus (Ladiges and Brooker 1987) and the genus Corymbia (Hill and Johnson 1995, p. 210), had occurred much earlier, prior to the Eocene–Miocene marine transgressions into the Eucla and Murray Basins and continental drying that would have isolated eastern and western floras. Geographical isolation appears to have been important in speciation within the genus (Pryor 1976; Pryor and Johnson 1981; Brooker and Hopper 1991; Ladiges 1997). The species of the south-west of Western Australia, particularly from the wetter zones, are very distinct from those of the eastern half of the continent. Most of the south-western species are endemic and have decorative features, including coloured stamens and large sculptured fruits, which are almost absent in eastern Australian species (Brooker and Kleinig 1990b).

2.5 Distribution Only five tropical eucalypts are endemic to areas outside Australia—C. papuana, E. deglupta, E. orophila, E. urophylla and E. wetarensis (Hill and Johnson 1995; Pryor et al. 1995; Ladiges 1997). A small group of species of Symphyomyrtus (E. alba, E. brassiana, E. tereticornis) and Corymbia (C. disjuncta, C. latifolia, C. novoguinensis, C. tessellaris) also extend outside Australia into Papua New Guinea (Chippendale 1988; Hill and Johnson 1995). The latter occurrences are northerly extensions of Australian populations on Cape York Peninsula, which were no doubt continuous across Torres Strait during periods of lower sea levels (Carr 1973; Pryor 1976). Corymbia papuana is endemic to the southern parts of the island of New Guinea and is closely related to the newly described species C. paracolpica from Cape York Peninsula (Hill and

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Johnson 1995), previously considered conspecific with C. papuana (Brooker and Kleinig 1994). Eucalyptus urophylla and the two recently described species, E. orophila and E. wetarensis, occur in Timor and adjoining islands of the Lesser Sunda Islands (House and Bell 1994; Pryor et al. 1995). These three species are related to Australian species such as E. pellita which occurs on Cape York Peninsula (Pryor and Johnson 1981). In contrast, E. deglupta is unlike any other Australian eucalypt. Eucalyptus deglupta is the species with the most northerly distribution, has extremely large disjunctions through its geographical range and has apparently evolved in isolation from the Australian eucalypts. It occurs in northern New Guinea and New Britain in Papua New Guinea, on the Indonesian islands of Sulawesi and Ceram and in the southern Philippines (Eldridge et al. 1993). Cataclysmic wind dispersal is one explanation for the eucalypt distributions that occur beyond the stable edge of the Australian continent (Carr 1973; Pryor and Johnson 1981). However, Ladiges (1997) argues that they could be explained by geological events during the Miocene (for E. deglupta) and Pliocene (e.g. for E. urophylla). Within Australia, eucalypts are ubiquitous and dominate nearly all types of vegetation except rainforest, central arid and high montane vegetation (Pryor 1976; Pryor and Johnson 1981; Specht 1996; Wardell-Johnson et al. 1997). They occur from sea level to the alpine tree line, from high rainfall to semiarid zones, and from the tropics to latitudes as low as 42° south (Pryor and Johnson 1981; Specht 1996; Wardell-Johnson et al. 1997). They occur in tall forest above developing rainforest understoreys in both tropical (e.g. C. torelliana, E. deglupta, E. urophylla) and temperate (e.g. E. obliqua, E. regnans; Jackson 1968) regions. They are the dominant component of open forests and woodlands throughout Australia, and in lower rainfall areas the mallees, with low multistemmed habit and large woody lignotubers, predominate. Several species also extend into the central, arid zone of Australia (e.g. E. rameliana; Sampson et al. 1995), where they may be confined to watercourses (e.g. E. camaldulensis, E. microtheca) or rock outcrops (e.g. E. crucis) (Brooker and Kleinig 1990b). However, while usually originating from Australia, eucalypts are now widely planted throughout the world for timber, fuel and pulp production, and land races and even

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stabilised hybrids have developed in many countries (Eldridge et al. 1993). The natural distributions of Angophora, Corymbia and the major subgenera of Eucalyptus s. str. are shown in Figure 2.7. Monocalyptus species are restricted to the east, south-east and south-west regions and appear to be more competitive than Symphyomyrtus species on less fertile sites (Florence 1981; Pryor and Briggs 1981; Wardell-Johnson et al. 1997). The subgenus Monocalyptus and the section Maidenaria of the subgenus Symphyomyrtus have radiated in the temperate climate of the south-east of the continent and together contain most of the cool temperate species. The more recently evolved species within the Monocalyptus lineage occur in the southeast and south-west of the continent (Ladiges 1997), with species in Tasmania and at high altitudes on the mainland being considered the most specialised (Pryor and Johnson 1981). The most primitive species from this lineage occur in north-east Australia (including the subgenera Gaubaea and Idiogenes; Ladiges 1997). The subgenus Symphyomyrtus is the most widespread, with species occurring throughout Australia. Within Symphyomyrtus, the section Adnataria (boxes, iron barks) is widespread, but predominates in the subtropics. Transversaria (eastern blue gums, red mahoganies, grey gums) is mainly an eastern section, with E. diversicolor (karri) the only species in the south-west (Brooker and Kleinig 1990b). The sections Bisectaria (mallees and gums) and Dumaria (mallees) are centred on the south-west and include many species of mallee habit. Bisectaria is the more diverse and includes species of moister forest sites. Its species dominate or codominate eucalypt communities in a large portion of the medium to dry parts of south-west Australia. Younger and more fertile soils have developed on the inland slopes of ranges both in New South Wales/ Victoria and the Darling Range in Western Australia. In the east these soils are occupied by species from the section Adnataria, but in the west they are occupied by species mainly from Bisectaria and to some extent Dumaria (Pryor and Johnson 1981). The section Exsertaria (northern red gums, eastern red gums) includes mainly tropical and eastern species and, except for E. rudis, is absent from south-west Australia.

19

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The subgenus Eudesmia is a small but diverse group of 20 species, several of which are widespread (Pryor and Johnson 1981). The eudesmid species are mostly tropical, or occur in drier regions of the south-west and across the interior of northern Australia, but are absent from non-tropical regions of the east. Corymbia (bloodwoods) are also relatively diverse and widespread. Tropical and subtropical species predominate, but several red bloodwood species (section Rufaria) extend into the winter rainfall areas of south-west (C. ficifolia, C. calophylla) and southeast (C. maculata) Australia. Within Corymbia, there is a trend for more primitive groups to occur in regions of relatively humid climate and groups with more recently evolved characteristics to occur in more drought-prone regions (Hill and Johnson 1995). At the higher taxonomic level, diversity is greatest in the north-east of the continent, where five subgenera of Eucalyptus s. str. occur along with Corymbia and Angophora (Ladiges 1997). Diversity is low in the south-west where only three subgenera and Corymbia occur, and on the island of Tasmania where only one section of both Symphyomyrtus and Monocalyptus are represented (Williams and Potts 1996; Wardell-Johnson et al. 1997). On a continental scale, eucalypt species richness is greatest in a broad band along the temperate, subcoastal regions of south-east Australia, with secondary concentrations of species in the semiarid south-west and west, and tropical north and north-east regions (Gill et al. 1985; Wardell-Johnson et al. 1997). The transitional rainfall zone of south-west Australia may also prove to be one of the more diverse areas. Species richness is highest in the open forests of south-east Australia, where up to 10 different species may occur per hectare, as species often grow in mixtures and species replacement across the landscape is high (Wardell-Johnson et al. 1997). Within this region, species richness increases on warmer, drier sites (Margules et al. 1987). In natural forests, species frequently occur in a mosaic distribution with their boundaries following a similar mosaic of often fine-scale, environmental variation (e.g. Hogg and Kirkpatrick 1974; Ashton 1976; Kirkpatrick 1981; Austin et al. 1983a; Davidson 1987; Specht 1996). Replacement series often occur along environmental gradients (e.g. altitude, drought) with relatively sharp boundaries delimiting species (Ashton 1981a). Some natural eucalypt forests are dominated

20

by a single species, as with E. regnans in the south-east and E. diversicolor in the south-west (Ashton 1981b). However, eucalypts mostly occur in mixtures of two or more species. Species may co-occur in intermediate, transitional environments (Ashton 1981a) or where fine-scale environmental patchiness occurs (e.g. Battaglia and Williams 1996). In south-east Australia and Tasmania, forests comprising an intimate mix of species from both the Symphyomyrtus and Monocalyptus subgenera are relatively common and species from different subgenera co-occur more frequently than species from the same subgenera (Pryor 1976; Austin et al. 1983b). This trend is believed to be associated with niche displacement because the two subgenera differ in numerous ecological and biological attributes (Noble 1989), including disease susceptibility (see Chapter 9), coupled with complete reproductive isolation between, but not within, the two subgenera (Griffin et al. 1988). An important feature of eucalypt distribution patterns is that many of the recognised taxa intergrade, resulting in species complexes where no clear morphological discontinuity is apparent (Pryor and Johnson 1971; Pryor 1976). Taxa are often separated along altitudinal, continental or simply geographical, gradients. Classic examples of such clinal variation with altitude include the E. pauciflora–niphophila complex in the mountain ranges of south-east Australia (Pryor 1957; reviewed in Pryor 1976; Potts and Wiltshire 1997) and the transition from the tall forest tree E. johnstonii, through E. subcrenulata, to the alpine shrub, E. vernicosa, which occurs on several Tasmanian mountains (Potts and Jackson 1986). Some species have large geographical ranges; for example E. camaldulensis is distributed over most of Australia except for the south-west (Eldridge et al. 1993). Eucalyptus tereticornis also occurs in an extended north-south distribution from Papua to eastern Victoria (Eldridge et al. 1993). However, there are many species with very restricted distributions (e.g. Crisp 1988; Prober et al. 1990a, 1990b; Wiltshire et al. 1990; Sampson et al. 1995; Kennington and James 1997) and many of these are threatened (Pryor and Briggs 1981). There is ample evidence for major changes in species ranges and extinctions through recent geological time (e.g. Pryor 1976; Potts 1986; Martin and Gadek 1988; Potts 1990). Using changes in pollen proportions, Churchill (1968), for example, detailed

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fluctuations in the ranges of three forest species, C. calophylla, E. diversicolor and E. marginata, in south-west Australia over the last 7000 years which were believed to be due to changing rainfall patterns. About 16% of eucalypt species have major disjunctions of more than 140 kilometres in their range (Chippendale and Wolf 1981). With such poor seed dispersal mechanisms, these disjunctions suggest that extant populations are remnants of former, more widespread distributions (Pryor and Johnson 1971; Parsons 1986). Eucalyptus perriniana, for example, occurs as several small populations in the Australian Alps and in three small populations on the island of Tasmania (Wiltshire and Reid 1987). In this case, genetic differentiation across the disjunction is relatively small, although populations can be differentiated. In some other species occurring both in Tasmania and on the mainland, variation appears to be continuous, as in the case of E. obliqua (Brown et al. 1976) and E. regnans (Griffin et al. 1982). However, the Tasmanian and mainland forms of E. delegatensis have distinct morphological differences which have led to subspecific recognition (Boland and Dunn 1985). About 59% of the Tasmanian eucalypts are endemic and concentrated in the south-east of the island (Williams and Potts 1996). The island would have been linked to the mainland of Australia when Pleistocene glacial sea levels were low. The south-east of the island appears to have been a major area of eucalypt speciation in Tasmania (Ladiges et al. 1983), and the endemic groups and relict distributions of species with mainland affinities suggest periods of isolation and reciprocal invasion (Jackson 1965). Other disjunctions in the southern Australian flora appear to be associated with the major geographical and/or ecological barrier arising from the incursion of the Early Miocene sea into the Eucla and Murray Basins (Parsons 1969; Specht 1996). Indeed, the patterns of species distributions within the various eucalypt lineages is consistent with relictual distributions overlaid with distributions suggesting recent radiation and vicariant (allopatric) speciation events (Prober et al. 1990a; Hill and Johnson 1995).

Johnson 1971; Pryor and Johnson 1981; Griffin et al. 1988; Hill and Johnson 1995). Although the importance of hybridisation in eucalypt evolution has yet to be fully understood, there is little doubt that reticulate (anastomosing) evolution is common at lower taxonomic levels and that both vicariant differentiation and hybridisation (secondary intergradation) have been important in shaping extant variation patterns (Pryor and Johnson 1971; Parsons and Kirkpatrick 1972; Ashton 1981a; Pryor and Johnson 1981; Potts and Jackson 1986; Potts and Reid 1988; Potts 1990; Potts and Wiltshire 1997; Steane et al. 1998). Artificial and natural hybridisation in eucalypts has been reviewed by Pryor and Johnson (1971), Pryor (1976), Griffin et al. (1988) and Potts and Wiltshire (1997). In most cases, morphological and physiological traits are inherited in a more-or-less intermediate manner in first generation (F1) hybrids (Fig. 2.8), although there are exceptions and the exact degree of dominance may vary between traits and species combinations. Hybrids may occur:

2.6 Hybridisation

Griffin et al. (1988) analysed records of hybridisation from herbaria and the literature and found that the extent of natural hybridisation between species varies considerably, depending upon numerous factors, including the degree of spatial, ecological and taxonomic separation between putative parents. Using

Hybridisation between recognised eucalypt taxa is frequently reported and, along with often marked clinal variation within species, contributes to difficulties in species identification (Pryor and

1

along species boundaries, as sporadic individuals

2

in hybrid swarms where hybridisation has extended beyond the first generation

3

in zones of introgression.

Some taxonomically intermediate populations, which are isolated from one or both putative parents, are often considered to be the genetic remnants of a past distribution of one or both putative parental species and are termed ‘phantom hybrids’ (Pryor and Johnson 1971; Parsons and Kirkpatrick 1972). For example, a population that is morphologically intermediate between E. cypellocarpa and E. globulus at Mallacoota, Vic., is believed to be a remnant of the E. globulus distribution in this area (Kirkpatrick et al. 1973). However, in other cases such intermediate populations are believed to result from long-distance dispersal (Ashton and Sandiford 1988; Potts and Reid 1988), or to be the remnants of ancestral lineages or other taxa (Watson et al. 1987, cf. Parsons and Kirkpatrick 1972).

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Figure 2.8

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Leaves and capsules of Eucalyptus urnigera (left), E. globulus (right) and their F1 hybrid (centre).

Pryor and Johnson’s (1971) classification, they found that within subgenera the frequency of natural hybrid combinations decreased with increasing taxonomic distance between the two parents (i.e. intersectional < interseries < intraseries). Important exceptions were recorded in the subgenus Monocalyptus and the former subgenus Corymbia where intersectional hybrids were as common as intrasectional hybrids, signalling taxonomic problems (see Ladiges and Brooker 1987; Sale et al. 1993; Hill and Johnson 1995; Ladiges 1997). Across the genus, natural hybridisation was relatively restricted, with only 15% of actual combinations expected on geographical grounds having been recorded. The main subgenera do not hybridise either naturally or artificially (Pryor and Johnson 1971; Griffin et al. 1988; Ellis et al. 1991). However, there are reports of natural intersubgeneric hybrids between the two sister subgenera Idiogenes and Monocalyptus (E. cloeziana × E. acmenoides; Brooker and Kleinig 1994; Hill and Johnson 1995) and between species previously classified in the subgenus Blakella and subgenus Corymbia (Wardell-Johnson et al. 1997). Estimates of the background rate of natural F1 hybridisation in 11 ‘pure’ eucalypt species range from 0.06% to 3.48%

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(mean 1.3%) (Potts and Wiltshire 1997), but this rate may markedly increase in multispecies plantations and ornamental plantings. Differences in flowering time (Drake 1980; Potts and Reid 1985; Williams and Potts 1996), style size (Gore et al. 1990), physiological incongruity (Ellis et al. 1991) and reduced hybrid fitness (Pryor and Johnson 1971; Drake 1981; Potts 1986; Morrow et al. 1994) have all been shown to be important in maintaining species integrity. An important component of reduced hybrid fitness appears to be their increased susceptibility to pests and diseases. Several studies have demonstrated that insect herbivores and fungal pathogens concentrate on natural hybrids (Drake 1981; Whitham et al. 1991; Morrow et al. 1994; Whitham et al. 1994), due to rarity per se (Drake 1981) or increased genetic susceptibility (Dungey et al. 1994) of host trees. The severity of Mycosphaerella leaf blotch in a field trial in north-west Tasmania was higher on juvenile leaves of F1 hybrids between E. nitens and E. globulus than on either pure species, but severity on adult leaves was intermediate between that on the parents (Dungey et al. 1997).

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2.7 Genetic variation The exceptional differentiation observed among eucalypts may be unparalleled for woody plants (Wardell-Johnson et al. 1997). From north to south, the Australian continent changes from summer to winter rainfall and from warm to cooler seasons which, combined with the effect of variations in altitude, aspect and soils, has resulted in an immense diversity of habitats to which eucalypts have adapted (see Eldridge et al. 1993; Specht 1996). Broad ecological trends are evident at higher taxonomic levels (reviewed by Pryor and Johnson 1981; Noble 1989; Specht 1996). Closely related taxa often exhibit marked ecological segregation (e.g. Williams and Potts 1996) and many groups have specialised taxa restricted to unique environments, such as serpentine outcrops (Specht 1996) and saline soils (Wardell-Johnson et al. 1997) over all, or parts, of their range. Within species, marked genetic differentiation between populations is normal rather than the exception (Pryor and Johnson 1971; Pryor 1976; Eldridge et al. 1993; Potts and Wiltshire 1997) and assessment of the performance of a species will often require sampling from throughout its geographical and ecological range (Pederick 1979; Eldridge et al. 1993; Potts and Jordan 1994). Studies of allozyme variation have shown the level of differentiation between populations of eucalypt species to be more than twice that of wind-pollinated conifers and northern hemisphere angiosperm tree species (Moran 1992). Widespread eucalypt species have greater overall and within-population genetic diversity than species with regional and localised distributions, yet population differentiation is greatest in regional species (Moran and Hopper 1987; Moran 1992; Potts and Wiltshire 1997). Variation between populations in quantitative traits is mostly continuous and is often clinal, paralleling environmental gradients associated with changes in, for example, latitude, continentality or altitude (see Pryor 1976; Potts and Jackson 1986; Potts and Wiltshire 1997). Steep environmental gradients may elicit rapid changes in phenotype over short distances, often involving many characters. In E. urnigera, for example, a transition from populations with completely green foliage to populations with completely glaucous foliage occurs over an altitude range of 200 metres on

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Mt Wellington, Tas. (Barber and Jackson 1957; Potts and Jackson 1986). When the progeny of trees selected from E. regnans populations at different altitudes on the southern slopes of Mt Erica, Vic., were grown together on a common test site, their growth rate decreased clinally with increasing altitude of origin (Eldridge 1972) and frost resistance, as determined in the laboratory, increased with increasing altitude of the selected parents (Eldridge 1968). Clinal variation may be more gradual where broadscale climatic changes occur over the geographical range of widespread species. Genetic variation in the widespread E. camaldulensis, for example, has been extensively studied from field trials established around the world for breeding purposes (reviewed in Midgley et al. 1989; Eldridge et al. 1993). A northern and southern form of this species has been detected in several studies, although no distinct boundary exists between them. The northern form has rounded or conical opercula, broad glaucous juvenile leaves, relatively straight stems and white bark. In contrast, the southern form has ‘beaked’ opercula, narrow and non-glaucous juvenile leaves, relatively crooked stems, mottled grey bark and rarely produces lignotubers. Longitudinal clines in several traits have also been demonstrated across northern Australia (Grunwald and Karschon 1982) and E. camaldulensis intergrades with E. tereticornis in northern Queensland (Doran and Burgess 1996) and E. rudis in south-west Western Australia (Pryor and Byrne 1969). Marked climatic adaptation is demonstrated by the better performance in tropical countries of northern provenances from summer rainfall areas such as Katherine, NT, and Petford, Qld, whereas a southern provenance from Lake Albacutya, Vic., with winter rainfall, is best in Mediterranean countries. There is also variation in the polyphenolic constituents of leaves (Banks and Hillis 1969). For example, an unusually high concentration of 1,8-cineole occurs in eucalypt oil distilled from certain populations from Queensland (Doran and Brophy 1991). Intraspecific variation in 1,8-cineole is highly heritable in E. camaldulensis (Doran and Matheson 1994) and is associated with resistance to insect herbivory (Stone and Bacon 1994). The extent and pattern of genetic variation in quantitative traits (i.e. the genetic architecture) is usually determined from common environment

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progeny trials based on open-pollinated seed collected from trees growing in native stands (reviewed in Eldridge et al. 1993; Potts and Wiltshire 1997). The heritability of traits can be estimated where family identity is maintained (see Eldridge et al. 1993). The use of open-pollinated progeny is a cheap and expedient means of studying genetic variation in eucalypts. However, in such cases, the male pedigree is unknown and there may be variable levels of inbreeding due to selfing (e.g. Hardner and Potts 1995a; Hardner and Potts 1997) or the crossing of related neighbours (Eldridge et al. 1993; Hardner et al. 1997) and natural outcrossing may not be random. Open-pollinated progenies may thus yield poor estimates of genetic parameters such as narrow-sense heritability and breeding values (Griffin and Cotterill 1988; Hardner and Potts 1995b; Potts et al. 1995b; Borralho and Potts 1996; Hodge et al. 1996). Accurate estimation of genetic parameters requires the use of controlled pollinated progenies (e.g. Hodge et al. 1996), although for some traits reasonably good estimates may be obtained from open-pollinated progenies. For example, Dungey et al. (1997) demonstrated that breeding values for damage by Mycosphaerella leaf blotch estimated from native stand open-pollinated progenies and controlled crosses (factorial) of E. globulus were highly correlated and heritability estimates were comparable. The level of genetic variability within a species determines the potential gain that can be achieved in breeding programs. Breeding programs are now established throughout the world for numerous tropical and temperate eucalypt species (see Eldridge et al. 1993; Potts et al. 1995a; Dieters et al. 1996b). In some species the emphasis is on use of vegetative propagation by cuttings to establish clonal plantations (e.g. E. grandis, van Wyk 1985; Eldridge et al. 1993; E. gunnii, Potts and Potts 1986; hybrids, Campinhos and Ikemori 1989). In species which are more difficult to clone, genetically improved seed is produced in seed orchards (e.g. E. globulus, Eldridge et al. 1993; E. nitens, de Little et al. 1993).

2.8 Genetic variation in susceptibility to disease Management of diseases and breeding for disease resistance requires a detailed understanding of the genetic variation and taxonomic relationships among and within both the eucalypt hosts and the

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pathogens and ultimately of the genetic control of the host-pathogen interaction. There are increasing numbers of examples that demonstrate genetic variation in disease susceptibility of eucalypts at the species level, as well as within species where differences in susceptibility between populations and between trees within populations have been reported (Alfenas et al. 1983; Dianese et al. 1984; Dungey et al. 1997). In some cases the pathogen can infect many eucalypt species, but in other cases its host range may be limited to a few closely related species. For example, Mycosphaerella cryptica (Cooke) Hansf., a cause of leaf necrosis and defoliation, has been recorded on 38 eucalypt species from both the Monocalyptus and Symphyomyrtus subgenera, and infects both juvenile and adult leaves (Park and Keane 1982a, 1982b, 1984; see Chapter 9). In contrast, Mycosphaerella nubilosa (Cooke) Hansf. was found to infect only juvenile foliage of three related species in the subgenus Symphyomyrtus (E. bridgesiana, E. cypellocarpa, E. globulus) (Park and Keane 1982a). The fungus Sporothrix pitereka (J.Walker & Bertus) U.Braun & Crous, which causes a shoot blight and leaf spot on seedlings of C. maculata in nurseries (see Chapters 8 and 9), and is possibly the same fungus causing canker on naturally occurring C. calophylla and cultivated C. ficifolia in Western Australia, also has a relatively narrow host range (Walker and Bertus 1971). Inoculation experiments showed that only species in the genus Corymbia were susceptible, along with the only species of Angophora tested, Angophora costata. The similarity in response to this pathogen was cited by Pryor and Johnson (1971) as support for the taxonomic association of Angophora and Corymbia. The soilborne pathogen, Phytophthora (Ph.) cinnamomi Rands, is able to infect the fine roots of most eucalypt species, although the disease develops particularly in species of the subgenus Monocalyptus (Podger and Batini 1971; Marks 1979; Marks and Smith 1991; see Chapter 11). Important forest species within Monocalyptus, E. marginata and E. sieberi, are highly susceptible and are associated with severe disease outbreaks in south-west and south-east Australia, respectively. Generally, species of the other main subgenus, Symphyomyrtus and the genus Corymbia, are resistant. A further example illustrates interspecific and intraspecific variation in resistance of eucalypts to a

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pathogen where both are exotics. The stem canker pathogen, Cryphonectria cubensis (Bruner) Hodges, has caused losses in eucalypt plantations in central and northern coastal regions of Brazil and in Cuba, Surinam and Hawaii, on sites with high temperature and humidity throughout the year (see Chapter 10) (Hodges and Reis 1976). Cryphonectria cubensis has been identified as conspecific with Endothia eugeniae (Nutman & F.M.Roberts) J.Reid & C.Booth, a weak pathogen of the myrtaceous species, clove [Syzygium aromaticum (L.) Merr. & L.M.Perry], which is native to the Moluccas area of Indonesia (Hodges et al. 1986). When clove plants were transported to Brazil and other countries to establish commercial plantations, it appears that the pathogen was distributed with its host and has been able to infect susceptible eucalypts when they have been introduced to the same area. Cryphonectria cubensis appears to have a fairly limited host range, with the most susceptible eucalypts being C. maculata and E. saligna (Hodges et al. 1986). Eucalyptus grandis is moderately susceptible but shows intraspecific variation in resistance. This eucalypt species is widely planted as an exotic in the subtropics. In the large plantations on coastal sites in Brazil, freedom from cankers caused by Cryphonectria cubensis is an important selection criterion for breeding and deployment of eucalypts by the Aracruz company (Campinhos and Ikemori 1989). The plantations, managed on a seven-year rotation, have been reported to be now 100% resistant. This has been achieved by the selection of resistant clones which are vegetatively propagated as cuttings. Some of the clones used in the plantation are hybrids between E. urophylla and E. grandis (Campinhos and Ikemori 1989). Eucalyptus urophylla is very resistant to Cryphonectria cubensis and the hybrids have more resistance than E. grandis. Another aspect of the breeding program at Aracruz is based on the finding that selections from the northern-most natural stands of E. grandis in Australia, on the Atherton Tableland in Queensland, are resistant to the disease when grown in Brazil (even though the disease is not known to occur in Australia). Accordingly, collections of seeds of E. grandis in the Atherton district have been grown at Aracruz to provide an additional genetic resource for the breeding program (Campinhos and Ikemori 1989). Intraspecific variation in the disease resistance of eucalypts has been reported for other diseases.

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Several of the 36 provenances of E. regnans in a large trial in New Zealand were severely damaged by M. cryptica, causing heavy defoliation and leader dieback of the young trees (Wilcox 1982). The most susceptible provenance was one that was also the least frost hardy. The author commented that badly frosted trees sometimes resprouted from the base and thus may have been additionally susceptible because of the high proportion of juvenile foliage in the crown. Another of the more susceptible provenances originated from a site north of the Great Dividing Range in Victoria (Rubicon) near stands of E. delegatensis. Wilcox (1982) speculated that the poor disease resistance of this provenance may have been due to some degree of hybridisation with the highly susceptible E. delegatensis, although there was no supportive morphological evidence. Occasional putative hybrids of E. regnans × E. delegatensis that occurred in one of the other provenances were more heavily diseased than pure E. regnans individuals. Provenance variation in the severity of Mycosphaerella leaf blotch has also been reported in field trials of E. globulus (Carnegie et al. 1994; Dungey et al. 1997), E. nitens (Purnell and Lundquist 1986) and E. delegatensis (Dick and Gadgil 1983). In E. globulus, there is evidence that some of the provenance variation results from natural selection favouring genes that confer resistance in disease-prone areas. Outbreaks of Mycosphaerella leaf blotch are favoured by warm, wet weather (Park 1988a, 1988b; Carnegie et al. 1994) and provenances of E. globulus originating from higher summer rainfall areas have greater resistance to the disease than provenances from drier or cooler areas (Carnegie et al. 1994; Dungey et al. 1997). Within populations of E. globulus, the severity of Mycosphaerella leaf blotch in field trials has a low to moderate level of genetic control, with individual narrow-sense heritabilities ranging from 0.1 to 0.3 (Dungey et al. 1997). In a study of controlled crosses, Dungey et al. (1997) showed that heritabilities were consistently higher for disease in adult foliage than juvenile foliage and the variation due to dominance genetic effects was less than half that due to additive genetic effects. Such field assessments may provide reasonably good ranking of families or parental breeding values for breeding purposes as these are based on the average response of progeny, randomly distributed throughout the

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trial. However, studies of natural infection pose problems, firstly, for predicting resistance at the individual level and, secondly, for accurately studying the genetic basis of resistance. Infection levels may not be uniform and susceptible individuals may escape infection. The expression of genetic variation in disease resistance, and hence heritability estimates, may also depend on the overall level of infection (Dieters et al. 1996a; Dungey et al. 1997). Further, in the above examples, damage to the juvenile foliage of E. globulus is due to the combined effects of two pathogens, M. cryptica and M. nubilosa, which usually co-occur on juvenile foliage in south-east Australia and are difficult to distinguish in the field (Carnegie et al. 1994; Dungey et al. 1997; see Chapter 9). The presence of both pathogens may mask a close genetic association between host and pathogen and could explain the generally lower heritabilities and higher levels of damage recorded on juvenile than on adult foliage, in which damage is due only to M. cryptica, recorded in E. globulus by Dungey et al. (1997). Inoculation experiments clearly are required to partition the response to either pathogen. Nevertheless, positive genetic correlations do occur in disease severity between adult and juvenile foliage (Dungey et al. 1997) and seasons (Carnegie et al. 1994), suggesting that similar selections would be made against the different pathogens. Increased disease severity on the juvenile canopy of E. globulus in field trials was found to be genetically correlated with delayed transition from juvenile to adult foliage (rg = 0.54, Dungey et al. 1997). This probably resulted from greater opportunity for disease increase within the larger and longer-lived juvenile canopy. Selection for early transition to adult foliage may thus be one means of reducing damage from Mycosphaerella leaf blotch (Dungey et al. 1997). In Australia, most work has focused on selection and breeding for resistance to Ph. cinnamomi, and this eucalypt–pathogen interaction has been studied more than any other (e.g. Marks 1979; McComb et al. 1987; McComb et al. 1991; Cahill et al. 1992; Cahill and McComb 1992; Cahill et al. 1993; McComb et al. 1994; Stukely and Crane 1994; Bunny et al. 1995; Irwin et al. 1995; see Chapter 11). Genetic variation in susceptibility to Ph. cinnamomi has been reported within many eucalypt species. For example, significantly different rates of disease development occurred in young trees from different families in a

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seedling seed orchard of E. regnans (Harris et al. 1983) and trunk inoculations of trees of similar age and size showed lesions that varied greatly in size from tree to tree depending upon tree genotype (Marks et al. 1981). Such genetic variation is the basis for breeding for disease resistance. There are large differences in the physiological, biochemical and anatomical responses of resistant and susceptible genotypes. Mechanisms of resistance have been best studied in jarrah, E. marginata (McComb et al. 1991; Cahill and McComb 1992; Cahill et al. 1993), in which resistance is under strong genetic control (Stukely and Crane 1994). There is also considerable genetic variation within the pathogen itself (see Irwin et al. 1995) and different isolates have been shown to differ significantly in their pathogenicity against clones of E. marginata and seedlings of several monocalypt species (E. globoidea, E. muelleriana, E. obliqua, E. regnans) (Dudzinski et al. 1993). Significant clone by isolate and species by isolate interactions were detected. In the case of E. marginata, it was only the more pathogenic isolates that allowed resistant and susceptible clones to be distinguished. Different isolates appear to exhibit a differential response to eucalypt host genotypes, but the extent to which gene-for-gene interactions (Keen 1982; Wolfe and McDermott 1994) occur are presently unknown. Nevertheless, Irwin et al. (1995) note that where resistance to Ph. cinnamomi has been detected in native plant species, it is a general or partial resistance.

2.9 Factors affecting disease risk in plantations The risk of disease in plantations is usually considered to be greater than that in natural forests because: 1

there may be less genetic variation present in planted stands

2

site conditions may not suit the requirements of the species, with the result that the trees may grow under stress for all or part of the year.

The main cause of reduced genetic variation in plantations is the use of seed from a limited number of parents or the planting of a limited number of clones. The risk of major losses through disease becomes greater as the genetic base of a plantation is reduced. However, tree breeding does not necessarily reduce genetic variability in deployed populations,

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although a change in the frequency of some genes as a response to selection for desired traits is expected. Most tree breeding programs, involving the production of seed in seed orchards, are designed to maintain genetic variability, partially at the expense of higher gains in economically important characters. A seed orchard with trees derived from several natural populations could produce seed with more genetic variability than would be present in collections from any one natural population, where there may be a degree of inbreeding and limited genetic variation (e.g. Chaisurisri and El-Kassaby 1994). This will provide stability of the crop in the face of risks over long rotations. Nevertheless, growers attracted to the higher yields obtainable from clonal plantations need to be aware of the higher risks of disease due to genetic uniformity. The use of multiclonal plantings has been recommended, particularly if rotations are long (Libby and Ahuja 1993). Indeed, the deployment of a limited number of clones in plantations should be backed by a large, variable breeding population from which alternative clones can be selected to combat various stresses that may occur unexpectedly, including attack by pests and diseases. The environment is also important in determining whether infection is likely to occur. In natural forests an equilibrium is thought to exist between the pathogen, the host species (genotype) and site (environment—both biotic and abiotic), such that disease normally is restricted to fairly low levels, otherwise the host species would be unable to occupy the site. Indeed, disease could be a factor in eliminating species from many potentially suitable sites. Eucalypt plantations, however, have often been planted on sites which differ in some important features, edaphic and/or climatic, from those of the natural distribution of the species involved. As a result, the trees may be growing under stress and are likely to be more susceptible to disease caused by non-specialised pathogens (see Chapter 9). When grown as exotics they may also be exposed to pathogens not present in their natural distribution, as illustrated by Cryphonectria cubensis and the eucalypt rust, Puccinia psidii G.Winter, in Brazil. Plantation managers need to be alert to the many risks. However, there is clear evidence of genetic variation in resistance within eucalypt species with which to combat disease. Selection of well-adapted resistant provenances of a eucalypt species from local

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trials, followed by collection of seeds from the best and healthiest trees in each generation, would be a simple method of developing lines with improved resistance. Many tree improvement programs concentrate on selection for growth rate and form, and assume that in doing so a degree of pest and disease resistance is also selected. More rapid progress to resistance could be obtained from designed breeding programs specifically targeting resistance to diseases as a breeding objective for particular breeding populations. Molecular technology is now being used to find DNA markers associated with quantitative trait loci (QTL) that control disease resistance. This will potentially allow selection for disease resistance in the absence of epidemics and without recourse to complex bioassays (e.g. Young 1996). Nevertheless, the interactions between genotypes of the eucalypt and pathogen, and environmental factors are likely to be complex and understanding these interactions is the challenge for future research and breeding.

2.10 Acknowledgments We thank Dr René Vaillancourt and Dr Greg Jordan for their valued comments on the manuscript.

2.11 References Alfenas, A.C., Jeng, R. and Hubbes, M. (1983). Virulence of Cryphonectria cubensis on Eucalyptus species differing in resistance. European Journal of Forest Pathology 13, 197–205. Ashton, D.H. (1976). The vegetation of Mount Piper, Central Victoria: A study of a continuum. Journal of Ecology 64, 463–483. Ashton, D.H. (1981a). The ecology of the boundary between Eucalyptus regnans F. Muell. and E. obliqua L’Herit. in Victoria. Proceedings of the Ecological Society of Australia 11, 75–94. Ashton, D.H. (1981b). Tall open-forests. In Australian Vegetation. (Ed. R.H. Groves) pp. 121–151. (Cambridge University Press: Cambridge.) Ashton, D.H. and Sandiford, L.M. (1988). Natural hybridisation between Eucalyptus regnans F. Muell. and E. macrorhyncha F. Muell. in the Cathedral Range, Victoria. Australian Journal of Botany 36, 1–22. Austin, M.P., Cunningham, R.B. and Good, R.B. (1983a). Altitudinal distribution of several eucalypt species in relation to other environmental factors in southern New South Wales. Australian Journal of Ecology 8, 169–180. Austin, M.P., Cunningham, R.B. and Wood, J.T. (1983b). The subgeneric composition of eucalypt forest stands

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in a region of south-eastern Australia. Australian Journal of Botany 31, 63–71. Banks, J.C.G. and Hillis, W.E. (1969). The characterization of populations of Eucalyptus camaldulensis by chemical features. Australian Journal of Botany 17, 133–146. Barber, H.N. and Jackson, W.D. (1957). Natural selection in action in Eucalyptus. Nature 179, 1267–1269. Barlow, B.A. (1981). The Australasian flora: its origin and evolution. In Flora of Australia. (Eds R. Robertson, B.G. Briggs, H. Eichler, L. Pedley, J.H. Ross, D.F. Symon and P.G. Wilson) pp. 25–75. (Australian Government Publishing Service: Canberra.) Battaglia, M. and Reid, J.B. (1993). Ontogenetic variation in frost resistance of Eucalyptus delegatensis RT Baker. Australian Journal of Botany 41, 137–141. Battaglia, M. and Williams, K. (1996). Mixed species stands of eucalypts as ecotones on a water supply gradient. Oecologia 108, 518–528. Boland, D.J., Brooker, M.I.H., Chippendale, G.M., Hall, N., Hyland, B.P.M., Johnston, R.D., Kleinig, D.A. and Turner, J.D. (1985). Forest Trees of Australia. (Australian Government Publishing Service: Melbourne.) Boland, D.J. and Dunn, A.T. (1985). Geographic variation in Alpine Ash (Eucalyptus delegatensis R.T. Baker). Australian Forest Research 15, 155–171. Boland, D.J., Brooker, M.I.H., Turnbull, J.W. and Kleinig, D.A. (1980). Eucalyptus Seed. (CSIRO: Melbourne.) Borralho, N.M.G. and Potts, B.M. (1996). Accounting for native stand characteristics in genetic evaluations of open pollinated progeny from Eucalyptus globulus base population. New Forests 11, 53–64. Brooker, M.I.H. (1986). An introduction to the study of characters in Eucalyptus. In Proceedings of a Workshop on Seed Handling and Eucalypt Taxonomy. pp. 119–142. (Eds R.D. Ayling and B.R.T. Seward) (International Development Research Centre: Ottawa.) Brooker, M.I.H. and Hopper, S.D. (1991). A taxonomic revision of Eucalyptus wandoo, E. redunca, and allied species (Eucalyptus series Leucispermae MaidenMyrtaceae) in Western Australia. Nuytsia 8, 1–189. Brooker, M.I.H. and Kleinig, D.A. (1990a). Field Guide to Eucalypts. Volume 1. South-eastern Australia. (Inkata Press: Melbourne.) Brooker, M.I.H. and Kleinig, D.A. (1990b). Field Guide to Eucalypts. Volume 2. South-western and Southern Australia. (Inkata Press: Sydney.) Brooker, M.I.H. and Kleinig, D.A. (1994). Field Guide to Eucalypts. Volume 3. Northern Australia. (Inkata Press: Sydney.) Brown, A.G., Eldridge, K.G., Green, J.W. and Matheson, A.C. (1976). Genetic variation of Eucalyptus obliqua in field trials. New Phytologist 77, 193–203. Bunny, F.J., Crombie, D.S. and Williams, M.R. (1995). Growth of lesions of Phytophthora cinnamomi in

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stems and roots of jarrah (Eucalyptus marginata) in relation to rainfall and stand density in mediterranean forest of Western Australia. Canadian Journal of Forest Research 25, 961–969. Cahill, D.M. and McComb, J.A. (1992). A comparison of changes in phenylalanine ammonialyase activity, lignin and phenolic synthesis in the roots of Eucalyptus calophylla (field resistant) and E. marginata (susceptible) when infected with Phytophthora cinnamomi. Physiological and Molecular Plant Pathology 40, 315–332. Cahill, D.M., Bennett, I.J. and McComb, J.A. (1992). Resistance of micropropagated Eucalyptus marginata to Phytophthora cinnamomi. Plant Disease 76, 630–632. Cahill, D.M., Bennett, I.J. and McComb, J.A. (1993). Mechanisms of resistance to Phytophthora cinnamomi in clonal, micropropagated Eucalyptus marginata. Plant Pathology 42, 865–872. Cameron, R.J. (1970). Light intensity and the growth of Eucalyptus seedlings I. Ontogenetic variation in E. fastigata. Australian Journal of Botany 18, 29–43. Campinhos, E. and Ikemori, Y.K. (1989). Selection and management of the basic population Eucalyptus grandis and E. urophylla established at Aracruz for the long term breeding programme. In Breeding Tropical Trees: Population Structure and Genetic Improvement Strategies in Clonal and Seedling Forestry. Proceedings of the IUFRO Conference, Pattaya, Thailand, November 1988. (Eds G.L. Gibson, A.R. Griffin and A.C. Matheson) pp. 169–175. (Oxford Forestry Institute; Winrock International: Oxford, UK; Arlington, USA.) Carnegie, A.J., Keane, P.J., Ades, P.K. and Smith, I.W. (1994). Variation in susceptibility of Eucalyptus globulus provenances to Mycosphaerella leaf disease. Canadian Journal of Forest Research 24, 1751–1757. Carr, S.G.M. (1973). Problems of the geography of the tropical eucalypts. In Bridge and Barrier: The Natural and Cultural History of Torres Strait. (Ed. D. Walker) pp. 153–182. (Australian National University: Canberra.) Chaisurisri, K. and El-Kassaby, Y.A. (1994). Genetic diversity in a seed production population vs natural populations of Sitka spruce. Biodiversity and Conservation 3, 512–523. Chappill, J.A. and Ladiges, P.Y. (1996). Phylogenetic analysis of Eucalyptus Informal Subgenus Symphyomyrtus Section Maidenaria. Australian Systematic Botany 9, 71–93. Chippendale, G.M. (1988). Eucalyptus, Angophora (Myrtaceae). Flora of Australia. Vol. 19 (Australian Government Publishing Service: Canberra.) Chippendale, G.M. and Wolf, L. (1981). The Natural Distribution of Eucalyptus in Australia. Special Publication No. 6 (Australian National Parks and Wildlife Service: Canberra.)

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chloroplast DNA. Australian Systematic Botany 9, 273–282. Sampson, J.F., Hopper, S.D. and James, S.H. (1995). The mating system and genetic diversity in the Australian arid zone mallee, Eucalyptus rameliana F. Muell. Australian Journal of Botany 43, 461–474. Singh, G., Kershaw, A.P. and Clark, R. (1981). Quaternary vegetation and fire history in Australia. In Fire and the Australian Biota. (Eds A.M. Gill, R.H. Groves and I.R. Noble) pp. 23–54. (Australian Academy of Science: Canberra.) Specht, R.L. (1996). The influence of soils on the evolution of the eucalypts. In Nutrition of Eucalypts. (Eds P.M. Attiwill and M.A. Adams.) pp. 31–60. (CSIRO: Melbourne.) Steane, D.A., Byrne, M., Vaillancourt, R.E. and Potts, B.M. (1998). Chloroplast DNA polymorphism signals complex interspecific interactions in Eucalyptus (Myrtaceae). Australian Journal of Systematic Botany 11, 25–40. Stone, C. and Bacon, P.E. (1994). Relationships among moisture stress, insect herbivory, foliar cineole content and the growth of river red gum Eucalyptus camaldulensis. Journal of Applied Ecology 31, 604–612. Stukely, M.J.C. and Crane, C.E. (1994). Genetically based resistance of Eucalyptus marginata to Phytophthora cinnamomi. Phytopathology 84, 650–656. Urdovic, F., McFadden, G. and Ladiges, P.Y. (1995). Phylogeny of Eucalyptus and Angophora based on 5S rDNA spacer sequence data. Molecular Phylogenetics and Evolution 4, 247–256. van Wyk, G. (1985). Tree breeding in support of vegetative propagation of Eucalyptus grandis (Hill) Maiden. South African Forestry Journal 135, 33–39. Walker, J. and Bertus, A.L. (1971). Shoot blight of Eucalyptus spp., caused by an undescribed species of Ramularia. Proceedings of the Linnean Society of New South Wales 96, 108–115. Wallace, H. and Trueman, S.J. (1995). Dispersal of seeds of Eucalyptus torelliana by the stingless bee, Trigona carbonaria. Oecologia 104, 12–16. Wardell-Johnson, G., Williams, J.E., Hill, K. and Cumming, R. (1997). Evolutionary biogeography and contemporary distribution of Eucalyptus. In Eucalypt Ecology: Individuals to Ecosystems. (Eds J. Williams and J. Woinarski) pp. 92–128. (Cambridge University Press: Cambridge.) Watson, R.J., Ladiges, P.Y. and Griffin, A.R. (1987). Variation in Eucalyptus cypellocarpa L. Johnson in Victoria, and a new taxon from the Grampian Ranges and Anglesea. Brunonia 10, 159–176. Whitham, T., Morrow, P. and Potts, B.M. (1991). The conservation of hybrid plants. Science 254, 779–780. Whitham, T.G., Morrow, P.A. and Potts, B.M. (1994). Plant hybrid zones as centers of biodiversity: the

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herbivore community of two endemic Tasmanian eucalypts. Oecologia 97, 481–490. Wilcox, M.D. (1982). Preliminary selection of suitable provenances of Eucalyptus regnans for New Zealand. New Zealand Journal of Forestry Science 12, 468–479. Williams, K. and Potts, B.M. (1996). The natural distribution of Eucalyptus species in Tasmania. Tasforests 8, 39–164. Wiltshire, R., Potts, B.M. and Reid, J.B. (1990). Phenetic affinities, variability and conservation status of a rare Tasmanian endemic, Eucalyptus morrisbyi R. G. Brett. In Aspects of Tasmanian Botany—A Tribute to Winifred Curtis. (Eds S.J.S.M.R. Banks, A.E. Orchard and G. Kantvilas) pp. 213–229. (Royal Society of Tasmania: Hobart.)

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Wiltshire, R.J.E., Potts, B.M. and Reid, J.B. (1991). A paedomorphocline in Eucalyptus: Natural variation in the E. risdonii/E. tenuiramis complex. Australian Journal of Botany 39, 545–566. Wiltshire, R.J.E. and Reid, J.B. (1987). Genetic variation in the Spinning Gum, Eucalyptus perriniana F. Muell. ex Rodway. Australian Journal of Botany 35, 33–47. Wolfe, M.S. and McDermott, J.M. (1994). Population genetics of plant pathogen interactions: the example of the Erysiphe graminis-Hordeum vulgare pathosystem. Annual Review of Phytopathology 32, 89–113. Young, N.D. (1996). QTL mapping and quantitative disease resistance in plants. Annual Review of Phytopathology 34, 479–501.

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Since European settlement of Australia, eucalypts have been largely cleared from vast areas for agriculture, and residual eucalypt forests subjected to exploitative harvesting. Over the last 50 years much effort has been devoted to restoring damaged landscapes and to developing sustainable forest management and utilisation procedures. Sustainable silviculture is based on an understanding of the unusual growth habits of eucalypts such as their tiny seeds and vulnerable seedlings which require special seedbeds, and their sensitivity to competition (for light, and soil nutrients and water resources). The various alternative silvicultural methods that have been developed and tested experimentally and in practice are reviewed. New directions in eucalypt silviculture for sustainable production and environmental conservation in native forests, and for production in the rapidly expanding plantations, are discussed.

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3.1 Introduction Over many thousands of years, eucalypts have become adapted to the environmental effects, especially the fire regimes, associated with habitation by Australia’s indigenous peoples. Eucalypt forests have provided the bulk of Australian wood and sawn timber needs since first European settlement in 1788. The early European settlers saw the eucalypt forests and woodlands as an impediment to agricultural development and the forest resource as vast and unlimited. Hence, the forests and woodlands were subject to extensive clearing; elsewhere early logging was essentially exploitative. Recurrent wildfires are a feature of the hot, dry environment of the south-east and south-west forests and these degraded both the unlogged forest and residual trees within the harvested forests. Thus, when formed early in the twentieth century, Australian forest services faced three critical tasks: 1

protecting the forests from fire

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regulating cutting in order to sustain sawlog supply to industry

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improving the forest condition by removing the ‘overburden’ of commercially useless trees.

A large part of the more accessible forest had been brought under management in this way by World War II. The demand for timber expanded greatly during the post-World War II decades of rapid economic growth and technological advances in logging. This meant it was now possible to extend logging to the hitherto inaccessible escarpment and mountain forests and to the tall wet sclerophyll (tall open) forests of southern Australia. Generally, these forests were logged at rates well in excess of sustainable yields in order to avoid escalating wood import costs, and to maintain rural industries and communities. The expansion of wood production in this way generated social conflict about the role and management of the native eucalypt forests. This has led, in turn, to the present programs designed to achieve a socially acceptable balance between the production and conservation functions of forests, through the ‘Comprehensive Regional Assessment’ process, and to ensure wood production is sustainable in both ecological and economic terms.

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The development of ecologically sustainable forest management requires both an appreciation of the ecological principles that underpin silvicultural practice and the formulation of silvicultural methods which integrate a wider range of objectives than previously. This chapter develops this theme by examining growth habits of the eucalypts, silvicultural methods that have been used in the eucalypt forests, matters to be considered in formulating ecologically sustainable practice, and silvicultural directions for the forests.

3.2 Growth habits of the eucalypts There are several attributes of eucalypts that determine appropriate silvicultural regimes for the forests. These relate to the requirements for obtaining seedling regeneration (see Chapter 4), the way regrowth responds to competition from residual trees, the effects of species and site on stand dynamic processes, and patterns of stand volume production within even-aged regrowth. These attributes are considered briefly.

3.2.1

The seedbed for seedling regeneration

Regeneration may occur within the eucalypt forest where an opening of sufficient size has been created within the canopy. Regeneration develops from newly establishing seedlings, existing lignotubers and other advance growth or from coppice. New seedlings will normally establish and develop in useful quantities only where there has been sufficient disturbance to the forest floor to expose soil and create a biological environment in the soil favourable for rapid seedling development. A wildfire or a prescribed slash-disposal burn will create such a seedbed. A seedbed may also be produced where the soil has been exposed and disturbed by machinery working during or after logging. A disturbed seedbed is needed as eucalypt seed is small, there is no endosperm and the radicle needs to find its way quickly into moist soil in order to take up water and nutrients. Even when the radicle reaches soil, further seedling growth may be restricted by an unfavourable biological condition that has been noted in many eucalypt forests soils. Within blackbutt (Eucalyptus pilularis) forest this has been attributed by Florence and Crocker (1962) to the long-term incorporation into soil of the more

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refractory (lignified) components of nutritionally poor litter, leading to a decline in the availability of microbial energy sources, low microbial diversity, the dominance of inhibitory soil organisms [e.g. Cylindrocarpon destructans (Zinssm.) Scholten; Evans et al. 1967] and a breakdown in normal processes of nutrient mineralisation. Ashton and Willis (1982) also implicated several soil biological factors in the poor development of E. regnans seedlings in undisturbed forest soil. These include leachates from insect frass, difficulties in competing for a limited pool of ammonium ions before the seedling root has developed a mycorrhizal association, the inhibiting influence of the ubiquitous Cylindrocarpon destructans, and contact between plant roots and lipids in the soil. Waxy lipids of cuticular origin make up as much as 16% of the organic matter in the soil of E. regnans forests. Again, from studies on high altitude soils in Tasmania, it was concluded that ‘late successional’ vegetation is ‘antagonistic’ to eucalypt seedlings through progressive and increasingly unfavourable changes in the soil biological condition with increasing time since fire (Ellis and Pennington 1992). The response of the eucalypt seedlings may have much to do with the effect of fire on the biological condition of the soil. Following an intense fire, an increase in soluble carbon within the soil organic matter will stimulate soil microbial processes, and release nutrients through soil mineralisation (‘the partial sterilisation effect’). Soil heating or drying may also directly affect the microbial populations in the soil. Launonen et al. (1999) suggest that undried and unheated forest soil adversely affects development of effective mycorrhizas on the roots of E. regnans. Whatever the cause, a seedbed favourable for the establishment and vigorous growth of new seedlings is created by fire. Mechanical disturbance of the litter and mineral soil may have an effect on biological processes within the soil comparable to that of fire, providing an alternative means of creating an effective seedbed.

3.2.2

Sensitivity to competition

A dominant eucalypt may be an aggressive competitor for site resources, but where the same species is in a subordinate stand position, it can be highly sensitive to competition. By world standards, eucalypts would be classed as ‘intolerant’ to ‘very intolerant’ of competition. Eucalypts cannot develop

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strongly where the amount of light reaching the leaves is reduced appreciably, or where access to water and nutrients is limited by competition from overtopping or adjacent trees (root competition). Because there is some range in tolerance of competition, there is a tendency to refer to ‘intolerant’ and ‘tolerant’ eucalypts. However, no eucalypt can be classed as ‘tolerant’ in terms of recognised criteria for trees in this category (Jacobs 1955; Florence 1996). It may be more appropriate to refer to some eucalypt species as ‘intolerant but persistent’ rather than ‘tolerant’. Eucalypts do not develop crowns with dense foliage, conforming with the general criterion that intolerant species have thin foliage and open crowns and canopies (Daniel et al. 1979). The intolerance of the eucalypt may also be evident through the accumulation of ‘growth restricted’ trees in the forest, particularly on sites of low to moderate quality. Trees growing in close proximity may bend away from each other, lignotuberous seedlings responding to a small canopy opening may develop weak and unbalanced crowns, and where there is abrasion between the crown of a subordinate tree and the overwood canopy, continuing apical growth ceases. While trees may persist in a growth restricted condition for some time, they quickly lose the capacity to respond appreciably to release.

3.2.3

Growth rates, crown segregation and self-thinning

Compared with many other tree species, most eucalypts are capable of rapid early height growth. This is a particular characteristic of the more intolerant eucalypts such as E. camaldulensis, E. grandis and E. regnans. Within stands of vigorous, fast-growing, intolerant species on high quality sites, there will normally be rapid segregation of stems into dominance or crown classes, and rapid reduction in stocking as suppressed trees die (‘self-thinning’). The death of suppressed trees provides a food base for wood rotting fungi in such native forests (see Chapters 12 and 13). Stands of E. delegatensis, E. diversicolor, E. globulus, E. grandis and E. regnans will self-thin rapidly. For example, the stocking of E. regnans regrowth might decline from around 1700 live stems per hectare at eight years of age to 400 by age 40 (Ashton 1976). Expression of dominance within the canopy trees is not as strong in E. pilularis and E. sieberi stands on

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sites of average quality, and hence the rate of selfthinning is less. The rate of self-thinning of the slower growing or more tolerant or persistent eucalypts will be lower still. For example, the stocking of an E. obliqua stand had declined from 22,000 stems per hectare at age seven to 7000 at age 18 (Borough et al. 1978), far more than the anticipated stocking of around 1300 stems per hectare in an E. regnans stand at the same age.

3.2.4

Volume growth patterns

Eucalypt species also differ appreciably in patterns of stand volume production, often reflecting the relative tolerance and early vigour of the species (Florence 1996). Stands of faster growing eucalypts may have a particularly rapid early growth phase, reaching an early peak in current annual volume production (Current Annual Increment, CAI). For example, on a high quality site, the peak in CAI for E. globulus may be around 12 years when 50 to 60 cubic metres per hectare per annum of wood volume will be produced. However, by 30 years, the CAI will have declined to around 20 cubic metres per hectare per annum. Eucalyptus regnans may not reach a peak in CAI until around 20 years, but at this point a high annual volume production will be achieved. The growth pattern of E. pilularis is similar to that of E. regnans, but the volume of wood produced is much less. The more tolerant or persistent eucalypt species will not only be slower growing than the intolerant species, but also they will lack the distinctive rapid growth phase and early production peak of the fast growing species. Thus, the volume production of an E. obliqua stand on a relatively dry site will build up slowly to only 15 cubic metres per hectare per annum by age 20 to 25 years. However, it will maintain that production over a much greater time than the fast-growing intolerant species. In this way the annual volume production of a 60-year old to 90-year-old E. obliqua stand may exceed that of an E. regnans stand of the same age.

3.3 Sivicultural practice in natural forests The many silvicultural systems or methods described in the literature can be thought of as representing a gradational series in the extent to which the forest floor is exposed to solar radiation and wind, in the degree of root competition to which the developing

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seedlings are subjected and in the supply of seed from the residual stand. The series can be represented by the selection, shelterwood and clearfelling methods, although it is not always possible to place a silvicultural practice into one of these conventional categories.

3.3.1

Selection method

The selection method involves removal at any one harvest of only part of the existing growing stock. The method is normally, although not invariably, applied where there is a range of tree sizes and ages already present within the stand. In its classic or ‘narrow’ sense, the selection method involves the maintenance of a high level of growing stock, a near complete range of tree ages on each hectare of forest, and harvest of sawlogs and thinnings on a short cutting cycle. Because of their growth habits, the eucalypt forests are not amenable to the classic selection system. In Australian practice, the term is applied in a much broader sense, that is, to almost any harvest that creates or maintains some range in tree ages. The method often involves the removal of trees in patches or groups large enough to produce conditions similar to those associated with clearfelling or shelterwood methods. Management of native forests in two States (New South Wales, Queensland) has been based predominantly on selection-type silviculture. Initially, selection was based on ‘diameter-limit cutting’, which involved harvesting only those trees above a prescribed diameter. This was later modified by creating specific openings (or groups) within the forest to encourage regeneration of preferred species in even-aged patches (the ‘Australian Group Selection System’) (Jacobs 1955; Florence 1996). From the 1970s greater industry acceptance of smaller and more defective trees permitted an important modification to the selection prescription. Tree marking could now focus on the retention of trees with good growth potential through a range of sizes, and the harvest of substandard trees that would previously have been retained. This achieved the short-term objectives of sustaining sawlog supply to industry from a limited resource, improving productivity of the growing stock and maintaining a good level of structural and biological diversity throughout the forests. While highly effective use of existing growing stock has been achieved in this way, since the 1970s little emphasis was placed on stand

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regeneration or on establishment of the full range of size classes needed to service industry needs in the long term. It is difficult to maintain full site stocking under the selection method, particularly where the forest is ecologically diverse. More positive steps are needed to ensure complete site regeneration, particularly where the forests continue to be managed in a conservative way.

3.3.2

The shelterwood method

The shelterwood method traditionally has been applied where species require protection from climatic extremes at the regeneration phase (low temperatures, high levels of insolation, strong winds). Under this method the mature timber is removed in a series of cuttings extending over a relatively short part of the rotation, and essentially even-aged regeneration is established under the partial shelter of the residual overwood. Under Australian conditions the shelterwood method has been used in its classic sense only on the high altitude plateaux in northern and central Tasmania where regrowth develops poorly in response to clearfelling (Keenan and Candy 1983; Webb et al. 1983; Ellis et al. 1985; Keenan 1986; Battaglia and Wilson 1990). The term has been used elsewhere in Australia where a shelterwood-type pattern of cutting aims to meet several other objectives, for example, continuing wood increment on the higher quality trees of the stand (Squire and Edgar 1975) and the accumulation of lignotuberous and other advance growth before the final harvest of the overwood (Bradshaw 1986).

3.3.3

Clearfelling

Clearfelling involves removal of all useable elements of the stand, thus increasing site exposure to the maximum and decreasing root competition to the minimum. The technology for large coupe clearfelling was developed in the 1950s and 1960s in Tasmania (Gilbert 1958), Victoria (Cunningham 1960) and Western Australia (White 1971), primarily to cope with the tall wet sclerophyll forests of the temperate region where the species are among the most intolerant of the eucalypts, and intensive seedbed preparation is essential. Clearfelling is by far the most technically efficient method for harvesting and regenerating these forests. An intense slash-disposal burn following clearfelling is widely used to produce a seedbed and to reduce

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the sometimes massive accumulation of logging slash. A seedbed may also be created by mechanically disturbing a large proportion of the surface soil within a logging coupe. Mechanical site disturbance may be more costly than slash burning within larger coupes but can be a viable alternative to slash burning on most sites. The seed source for regeneration may be provided by residual trees retained at a suitable spacing (the ‘seed tree’ method) or seed may be collected and sown onto a disturbed forest floor. Direct seeding may be more expensive but, operationally, is generally more efficient. Planting of nursery raised seedling stock is another option and is used, for example, as one strategy for regenerating the E. diversicolor forest of Western Australia. Clearfelling practice has been subject to continuing investigation in order to develop more efficient clearfelling and seeding technologies and alternative silvicultural methods. The development of more efficient technologies has involved investigation of the effect of seed provenance and appropriate seeding mixtures (Forestry Commission of Tasmania 1991a), seed treatment (Neumann and Kassaby 1986), aerial sowing of seed (Forestry Commission of Tasmania 1991b; Wilson 1993), and different coupe sizes and seedbed preparation methods as well as the relative costs of using helicopters and fixed wing aircraft in seed distribution (King 1991; Wilson 1993; Sharp 1993). Studies on alternative silvicultural methods have been a response to environmental concerns about the effects of clearfelling. For example, Victoria’s ‘Silvicultural Systems Project’ (Squire et al. 1987) has compared clearfelling with seed tree, group selection, shelterwood and strip felling regimes in several forest types. This has demonstrated clear limits to the use of alternative methods in tall wet sclerophyll forest. A range of environmental stresses affect plants in gaps less than about one to two hectares, resulting in suppression and death of seedlings (Walters 1991). Moreover, there are serious operational problems including operational health and safety concerns associated with alternative methods in these forests (King and Cook 1992; Mitchell 1993; Burgess 1993; Dignan 1993). It has been possible to modify the practice of clearfelling in more open forests. Within the Eden area of New South Wales some tree components are

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retained in cut-over coupes, including saplings, poles, larger trees with sawlog potential, seed trees and wildlife habitat trees. In Tasmania, diversity in silvicultural practice is based on structural diversity within the forest, particularly the presence of trees with sawlog potential and useful patches of advance growth (saplings and poles). Similarly, in Victoria’s Otway Ranges, substandard trees may be retained within the coupe where there is no market for pulpwood, and there is environmental benefit in so doing (Bartlett 1983).

3.4 Ecologically sustainable silviculture The major influences on silvicultural practice have been the priority given to maintenance of wood supply for the short term (e.g. through selection regimes), and achievement of technically efficient and low-cost harvesting and regeneration operations (through clearfelling regimes). While these wood supply strategies have served Australia well, circumstances relating both to wood supply and forest management have changed. Now, environmental conservation has become a dominant factor in forest management, and appropriate silvicultural methods need to be developed to address this. There are two requirements for silvicultural practice that need to be met: 1

ecological sustainability

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an ability to respond to a wider range of social and economic circumstances.

The concept of ‘ecological sustainability’ provides the foundation upon which modern forest management needs to be built. This envisages that the naturally occurring species and community patterns will be maintained within the forest, that soil resources will not be depleted to such an extent that the health and productivity of a forest will be jeopardised, that ecosystem processes will be consistent with those of the natural forest environment and that susceptibility to pests and diseases will not be increased.

3.4.1

Natural species and community patterns

Until the 1960s, conventional wisdom held that fire frequency was the primary factor that created ecological patterns in the Australian forests. While there are more specialised situations where fire is

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very important, for example, in the vegetation of the peat soils in south-west Tasmania (Brown and Podger 1982) and the high elevation forest in the same State (Ellis 1985), under most circumstances the pattern represents the outcome of a sensitive ‘ecological sifting’ of species by several site factors (Florence 1981). Within the one forest, eucalypt subgenera and species will be responding to variations in soil fertility, physical properties of soils affecting water storage and availability (which in turn may affect pathogen activity), aspect (through differences in evapotranspiration and soil depth), and position on slope (integrating soil fertility, shelter, water status and, in some situations, the activity of pathogens in the soil). An appreciation of these complex species–site relationships may place constraints on the extent to which the distributions of commercially preferred species might be extended beyond the immediate limits of their natural occurrences, or their frequencies greatly increased within mixed species communities. Where site disturbance is not excessive, and no attempt has been made to alter the species composition, community patterning within the eucalypt forest appears to be robust and resistant to change. The control exerted by site factors on the distribution and association patterns of species might be expected to buffer the forest against undue changes in those patterns. Concerns about the ecological consequences of more radical silvicultural practices (e.g. clearfelling, burning, direct seeding) may be valid where there is little opportunity for ecological sifting of species within the regrowth. This could happen, for example, within a mixed species forest where a single preferred species is encouraged under a seed tree or direct seeding regime, and where there is little advance growth of other species, or that advance growth was largely destroyed in an intense slash-burn.

3.4.2

Forest structure

Although the structure of the natural eucalypt forest and its influence on the health, dynamics and productivity of the forest has been little considered in the silvicultural literature, there are circumstances where this may be important. It has been widely held that before European settlement occasional fires of great intensity maintained eucalypt forests in an even-aged condition. This may be largely true where stands of

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fire sensitive species are killed and replaced within a few years by vigorous, even-aged regrowth, but even in these forests individual mature to senescent trees or patches of trees would normally survive a wildfire. Alternatively, where the species are more fire resistant (and this includes the greater number of eucalypts), regrowth may have developed occasionally within gaps created by the death or senescence of individual trees or small patches of trees. In this case the natural forest would have been uneven-aged, although this might be obscured by the way large-boled trees remain in mature to senescent growth stages for 200 years or more. Where an uneven-aged forest is clearfelled and regenerated, the even-aged regrowth will make a much greater demand on site resources than the natural forest subject only to progressive gap-phase replacement. This demand will be particularly great at the time of peak annual volume production, for example, 20 to 40 years after clearfelling. Where this demand cannot be met from the site resources, expression of dominance within the developing stand might be weak, and the rate of self-thinning slow. There could be circumstances where the forest also becomes susceptible to decline, diseases and dieback as seen in some of the diseases of complex etiology (see Chapter 17).

3.4.3

Loss of nutrients

Inevitably, wood harvesting and the use of an intense fire to create a seedbed will result in loss of part of the nutrient capital of the site. These losses may be compensated for, wholly or in part, by natural inputs to the site where the stand is largely undisturbed during the subsequent rotation. There will also be important inputs of nitrogen through biological fixation by free-living bacteria in the soil and by nodulated plants, particularly in the early fire successional stage which in eucalypt forests is often dominated by Acacia and other nodulated species. Only a small amount of nitrogen is fixed annually in dry sclerophyll forest (e.g. 0.1–1.6 kg/ha in E. marginata forest, Hansen et al. 1987). In contrast, 10 kilograms per hectare was added to an E. pauciflora forest (Raison et al. 1993), and 14 kilograms per hectare to a mature E. diversicolor forest (Grove and Malajczuk 1992). The critical questions concerning these processes are: will nutrient inputs balance outputs over the rotation,

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and if not, will the deficit lead to any reduction in site productivity in the short or long term? There have been several nutrient balance sheets produced for harvested eucalypt forests in Australia. One for an E. regnans forest (Stewart et al. 1985) is based on the effects of clearfelling, an intense slashburn to prepare a seedbed, and a 50-year regrowth rotation. Despite the severity of this regime, net losses of nitrogen and phosphorus were estimated to be relatively small (around 400 kg/ha of N and 4 kg/ha of P, compared with the total available reserves of these elements of 7876 and 323 kg/ha, respectively). Both the available nutrient reserve and the harvesting losses will be smaller within mixed species forest of lower site quality (Turner and Lambert 1986; Stewart et al. 1990). However, the proportionate loss of nutrient capital will be greater on lower quality sites, for example, 18% of the ‘forest accessible’ soil phosphorus. This suggests the lower quality forest might not be as resilient as the higher quality forest in the long term, and should be managed more conservatively in order to avoid any breakdown in ecosystem processes, stand stagnation or increased susceptibility to pests and diseases.

3.4.4

Plant successional processes

Plant and soil processes associated with the early stages of secondary succession, particularly following a fire, may contribute to the long-term health, productivity and stability of a forest. Nitrogen-fixing species commonly make up a large part of the postfire community, and these will contribute, in time, to the organic matter and nitrogen content of the soil. Where the successional crop is dense, it will also help protect the exposed soil from erosion, and take up rapidly the soluble nutrients released in appreciable quantities following a fire. Subsequently, the postfire successional species will cycle a number of nutrients important in eucalypt nutrition, accelerate the decomposition of the eucalypt litter and, through the greater nutrient status of the soil organic matter, help maintain a more diverse and active soil microflora. It follows that periodic fire of at least moderate intensity could help maintain the health and productivity of the eucalypt forest. For example, it has been argued that occasional moderate to intense fire in jarrah (E. marginata) forest can stimulate the development of a crop of the nitrogen-fixing Acacia pulchella R.Br. and, through this, either directly inhibit the root pathogen Phytophthora cinnamomi

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Rands, or restrict its spread and activity through the influence of the acacia on the biological condition of the soil (Shea and Kitt 1976) (see Chapter 19).

3.4.5

Pests and diseases

The decline, dieback and death of trees in eucalypt forests will sometimes be a consequence of historical events that have exposed the environmental threshold of a species or plant community. For example, ‘southern regrowth dieback’ in Tasmania (Podger et al. 1980) (see Chapter 17) and Armillariaassociated death of trees in central Victoria (Edgar et al. 1976; Kile 1981) (see Chapter 12), both involving species of the Eucalyptus subgenus Monocalyptus, might have their origins in unusually severe disturbances to natural ecosystems, the subsequent development of highly stocked even-aged stands and limiting site resources to support them (Florence 1996). Thus, in evaluating any incidence of stand decline or disease, it is necessary to take account of the ecological relationships between species and sites, historical influences on the forest, changes in stand structure these may have generated, and the current stand dynamic processes and tree crown conditions.

delineation of protected and special management zones within the multiple use forest, through greater diversity in silvicultural practice within general wood production zones, and through adoption of silvicultural practices which mimic natural processes in the forests. As a result, natural levels of genetic and structural diversity could be maintained within the forests, thus contributing to avoidance of problems of decline and dieback and outbreaks of pests and diseases, at least on a wide scale. Greater silvicultural diversity will mean determining an appropriate practice for each unit of forest which is more or less homogeneous in composition, structural components and growing stock condition. Biological and structural diversity throughout a forest which has been subject conventionally to a clearfelling regime might be enhanced in the following ways. 1

Planning across the landscape—it is appropriate to plan protection zones, coupe size and shape, and tree and community retention patterns across the landscape. For example, the use of a standard coupe design over a large area might be questioned where wildlife conservation is a management objective, and animals have different habitat requirements, home ranges and minimum population sizes. The retention of wildlife corridors between unlogged areas may have to be considered.

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Protection of specific patches of vegetation within coupes—patches of forest of some vegetational or structural interest might be recognised and protected within coupes (e.g. patches of lower slope forest, or patches with an interesting aspect effect or with a high level of species complexity or diversity).

3

General tree retention within coupes—trees and associated understorey may be retained where appropriate (e.g. where light to moderate regeneration burns or mechanical site disturbance can be used). This may include useful advance growth, larger trees that might make sawlogs at a future harvest, seed trees and wildlife habitat trees. These patterns might be arranged so that unimpeded development of substantial areas of eucalypt regrowth is provided.

Similarly, an enhanced susceptibility of the forest to insect attack may reflect excessive disturbance to forest ecosystems, changes in natural species patterns and frequencies (including changes in populations of predators), loss of plant diversity and decline in the health and vigour of trees (Florence 1996). With current knowledge of, and further research into, patterns and processes in eucalypt forests, it should be possible to recognise those situations where problems may arise and establish the silvicultural and operational limits within which production forestry can be practised without increasing the incidence and severity of pests and diseases.

3.5 New directions in silviculture Silvicultural practice needs to be not only ecologically sustainable but also responsive to a much wider range of circumstances than previously. Notably, conservation objectives embodied in the National Forest Policy Statement (Commonwealth of Australia 1992) and Regional Forest Agreement documents (e.g. Independent Expert Working Group 1998) will be fully realised only where the wood production forest makes a significant contribution to environmental conservation. This can be achieved through the

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Diversity in seedbed preparation—diversity within the understorey may be maintained where several methods are used to create seedbeds (e.g. slash fires of varying intensity and mechanical disturbance of the forest floor and soil).

5

Silviculture for wet sclerophyll forest—it will be more difficult, but not impossible, to develop areas of productive regrowth within the taller wet sclerophyll forest, and yet maintain some biological and structural diversity throughout the forest. Individual trees, or patches of trees, might be left undisturbed during harvesting. In some circumstances the overwood within a mixed eucalypt–rainforest community might be selectively harvested, and the stand left unburnt (favouring growth of temperate rainforest species), or lightly burned in a mosaic pattern to encourage patches of eucalypt regrowth within a vegetationally diverse forest (Hickey and Wilkinson 1994).

6

7

Use of several silvicultural methods—greater ecological and structural diversity might be sought by using several distinct silvicultural methods rather than simply modifying the one (clearfelling) method. There will inevitably be some structural diversity within previously uncut or lightly cutover forests, providing a framework within which use of alternative silvicultural methods might be considered. Silviculture within even-aged regrowth—some diversity in silvicultural practice will be appropriate within large areas of even-aged regrowth. Silvicultural diversity might be based on a careful appreciation of diversity in stand conditions. Some sections may be retained (and thinned if possible) to provide high quality sawlogs for the future, others harvested under shelterwood or patch cutting regimes, and yet others clearfelled and re-established immediately. Not only will greater structural and environmental diversity be created in this way, but the forest may continue to meet the demand for a wider range of forest products, including those at the high-quality end of the market.

3.6 Eucalypt plantations There is a widespread perception that just as we have developed a large plantation softwood resource in Australia, so might we also develop a large

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hardwood plantation program in order to enhance prospects for conserving native forests. However, the extent to which this is possible may be subject to both ecological and economic constraints. The ubiquity of eucalypts in Australia, and their occupancy of an infertile and largely arid land, may obscure the fact that the eucalypt can be more site demanding than Pinus and other coniferous taxa, at least in terms of producing forests of commercial quality. The eucalypt has been described as a ‘drought tolerant mesophyte’ (Florence 1981). This means it must open stomata and transpire for some part of each day, and must be able, through various means, to tolerate the consequences of this. Eucalypt species differ in their capacities to regulate water use or to ‘maximise access to water supply’. This is an important factor contributing to the complexity of species and community patterns within the forests. The more productive species are normally those with inherently fast early rates of growth, relatively early peaks in stand volume production, and consequently high rates of water use. Because of their attributes, these species may occupy only sites within the vegetation and environmental mosaic which have adequate rainfall, soil water storage capacity and shelter from excessive insolation and wind. It follows that planting of eucalypts, particularly for sawlogs, may be justified economically only where faster growing species are used, and ecologically, only where sites are generally consistent with those of their natural environments. There can be some site flexibility with the more environmentally tolerant of the faster growing species (mainly species of Eucalyptus in the subgenus Symphyomyrtus) but tree form, bole quality and site production of any species may be adversely affected, and susceptibility to pests and diseases increased, where species are planted too far off-site. For example, where the Monocalyptus species, E. pilularis, is planted off-site, it becomes more susceptible to termite attack and the early formation of a central ‘pipe’ (Greaves and Florence 1966). And although E. globulus appeared to have wide environmental tolerance when planted on the dry Mediterranean coast of southern Spain, it was all but decimated by the introduced insect Phoracantha semipunctata (Fabricius) as demands on site water resource grew and drought stress developed. Hence, where rainfall and edaphic factors are likely to limit growth, it could be better to err on the side of

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caution in selecting species for planting, at least until there is experience of the performance of species extending over a substantial part of a proposed rotation. This becomes especially critical where sawlog production is planned.

3.7 Conclusion The long-term role in wood production of native forests, particularly the more environmentally significant of those forests, remains uncertain. What is certain, however, is that a diverse and viable forest industry will be possible only where a socially acceptable balance between the production and conservation functions of the forests is established. Undoubtedly, the management of the native forests is moving in this direction, although whether far or fast enough remains a matter of debate. Most silvicultural regimes and harvesting practices are now designed to minimise adverse environmental effects, and to achieve some level of biological, structural and aesthetic diversity throughout the forest. Nevertheless, there is still some way to go in generating public confidence that harvesting of the forest is consistent with multiple use objectives and principles of ecologically sustainable forest management. An extension of more basic ecological research is needed to firmly underpin the case for continuing wood production within native forests. This is despite the fact that the greater part of the forests appears to be ecologically robust and free of epidemic disease. If this is to continue, it will be essential to appreciate, much more than we do currently, the ‘environmental threshold’ of the more site-sensitive species and communities, and the extent to which tree decline and expression of disease may be a consequence of historical events that have exposed that threshold. Thus, ecologically sustainable silviculture demands a more critical understanding of the relationships between the composition and structure of forest stands, the availability of site resources to those stands, the effects of logging and fire on those resources, and the continuing health, dynamics and productivity of the regrowth forests.

3.8 References Ashton, D.H. (1976). The development of even-aged stands of Eucalyptus regnans F. Muell. in central Victoria. Australian Journal of Botany 24, 397–414.

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Ashton, D.H. and Willis, E.J. (1982). Antagonisms in the regeneration of Eucalyptus regnans in the mature forest. In The Plant Community as a Working Mechanism. (Ed. E.I. Newman) pp. 113–128. Special Publications Series of the British Ecological Society. (Blackwell Scientific Publications: Oxford.) Bartlett, A.G. (1983). Multiple use hardwood forest management in the Otway Ranges. Australian Forestry 46, 278–286. Battaglia, M. and Wilson, L.P. (1990). Effect of shelterwoods on stocking and growth of regeneration in dry high altitude Eucalyptus delegatensis. Australian Forestry 53, 259–265. Borough, C.J., Incoll, W.D., May, J.R. and Bird, T. (1978). Yield statistics. In Eucalypts for Wood Production. (Eds W.E. Hillis and A.G. Brown) pp. 201–205. (CSIRO: Melbourne.) Bradshaw, F.J. (1986). Silvicultural guidelines for virgin southern jarrah forest. Technical Report No. 4. (Department of Conservation and Land Management, Western Australia: Perth.) Brown, F.J. and Podger, F.D. (1982). Floristics and fire regimes of a vegetation sequence from sedgelandheath to rainforest at Bathurst Harbour, Tasmania. Australian Journal of Botany 30, 659–676. Burgess, J.S. (1993). A block level simulation study of the application of single silvicultural systems. VSP Internal Report No. 15. (Department of Conservation and Natural Resources, Victoria: Melbourne.) Commonwealth of Australia (1992). National Forest Policy Statement. December 1992. (Government Printer: Canberra.) Cunningham, T.M. (1960). The natural regeneration of Eucalyptus regnans. Bulletin No. 1. (School of Forestry, University of Melbourne: Melbourne.) Daniel, T.W., Helms, J.A. and Baker, S.F. (1979). Principles of Silviculture. McGraw Hill Series in Forest Resources. (McGraw-Hill: New York.) Dignan, P. (1993). Wood production in mountain ash forests: implications of alternative systems for harvesting operations. VSP Technical Report No. 22. (Department of Conservation and Natural Resources, Victoria: Melbourne.) Edgar, J.G., Kile, G.A. and Almond, C.A. (1976). Tree decline and mortality in a selectively logged eucalypt forest in central Victoria. Australian Forestry 39, 288–303. Ellis, R.C. (1985). The relationship among eucalypt forest, grassland and rainforest in a highland area in northeastern Tasmania. Australian Journal of Ecology 20, 297–314. Ellis, R.C. and Pennington, P.I. (1992). Factors affecting the growth of Eucalyptus delegatensis seedlings in inhibitory forest and grassland soils. Plant and Soil 145, 93–105. Ellis, R.C., Webb, D.C., Graley, A.M. and Rout, A.F. (1985). The effect of weed competition and nitrogen

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nutrition on the growth of seedlings of Eucalyptus delegatensis in a highland area of Tasmania. Australian Forest Research 15, 395–408. Evans, G., Cartwright, J.B. and White, N.H. (1967). Nectrolide, a phytotoxic compound produced by some root surface isolates of Cylindrocarpon radicicola. Plant and Soil 26, 253–260. Florence, R.G. (1981). The biology of the eucalypt forest. In The Biology of Australian Plants. (Eds J.S. Pate and A.J. McComb) pp. 147–180. (University of Western Australia Press: Perth.) Florence, R.G. (1996). Ecology and Silviculture of Eucalypt Forests. (CSIRO: Melbourne.) Florence, R.G. and Crocker, R.L. (1962). Analysis of blackbutt (Eucalyptus pilularis Sm) seedling growth on a blackbutt forest soil. Ecology 43, 670–679. Forestry Commission of Tasmania (1991a). Eucalypt seed and sowing. Technical Bulletin No. 1. (Native Forest Silviculture: Hobart.) Forestry Commission of Tasmania (1991b). Aerial Sowing Manual. (Forestry Commission of Tasmania: Hobart.) Gilbert, J.M. (1958). Eucalypt-rainforest relationships and the regeneration of the eucalypts. Report of work carried out under the first Australian Newsprint Mills Forestry Fellowship 1955–58. (Forestry Commission of Tasmania: Hobart.) Greaves, T. and Florence, R.G. (1966). Termite incidence in living blackbutt regrowth and possible relations of termite attack to soil properties and tree vigour. Australian Forestry 30, 153–161. Grove, T.S. and Malajczuk, N. (1992). Production and nitrogen fixation (acetylene reduction) by an understorey legume (Bossiaea laidlawiana) in eucalypt forest. Journal of Ecology 80, 303–314. Hansen, A.P., Pate, J.S., Hansen, A. and Bell, D.T. (1987). Nitrogen economy of post-fire stands of shrub legumes in jarrah (Eucalyptus marginata Donn ex Sm) forest in S.W. Australia. Journal of Experimental Botany 38, 26–41. Hickey, J.E. and Wilkinson, G.R. (1994). Silvicultural options for the maintenance of biodiversity in mixed forest used for wood production in Tasmania. Abstract in Conserving Biological Diversity in Temperate Forest Ecosystems—Towards Sustainable Development. (Centre for Resource and Environmental Studies, Australian National University: Canberra.) Independent Expert Working Group (1998). Assessment of management systems and processes for achieving ecologically sustainable forest management in New South Wales. NSW CRA/RFA Steering Committee Project NA 18/ESFM. (Department of Urban and Regional Planning: Sydney.) Jacobs, M.R. (1955). Growth Habits of the Eucalypts. (Government Printer: Canberra.)

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Keenan, R.J. (1986). Review of the shelterwood system and its potential for application in Tasmanian eucalypt forests. Australian Forestry 49, 226–235. Keenan, R.J. and Candy, S. (1983). Growth of young Eucalyptus delegatensis in relation to variation in site factors. Australian Forest Research 13, 197–205. Kile, G.A. (1981). Armillaria luteobubalina: a primary cause of decline and death of trees in mixed species eucalypt forest in central Victoria. Australian Forest Research 11, 63–77. King, M.R. (1991). An evaluation of regeneration costs under alternative silvicultural systems in mountain ash forests. Silvicultural Systems Project. (Department of Conservation and Environment, Victoria: Melbourne.) King, M. and Cook, J. (1992). The regeneration of Eucalyptus regnans under alternative silvicultural systems. 2. Seedbed descriptions. Value Adding and Silvicultural Systems Program, Internal Report No. 7. (Department of Conservation and Environment, Victoria: Melbourne.) Launonen, T.M., Ashton, D.H. and Keane, P.J. (1999). The effect of regeneration burns on the growth, nutrient acquisition and mycorrhizae of Eucalyptus regnans F.Muell. (mountain ash) seedlings. Plant and Soil 210, 273–283. Mitchell, K. (1993). Safety of forest harvesting under alternative silvicultural systems in mountain ash forest. Silvicultural Systems Project, VSP Technical Report No. 21. (Department of Conservation and Natural Resources, Victoria: Melbourne.) Neumann, F.G. and Kassaby, F.Y. (1986). Effects of commercial pesticides in seed coats on seeds and germinants of Eucalyptus regnans, and their potential as seed protectants in the field. Australian Forest Research 16, 37–50. Podger, F.D., Kile, G.A., Bird, T., Turnbull, C.R.A. and McLeod, D.E. (1980). An unexplained decline in some forests of Eucalyptus obliqua and E. regnans in southern Tasmania. Australian Forest Research 10, 53–70. Raison, R.J., O’Connell, A.M., Khanna, P.K. and Keith, H. (1993). Effects of repeated fires on nitrogen and phosphorus budgets and cycling processes in forest ecosystems. In Fire in Mediterranean Ecosystems. (Eds L. Trabaud and R. Prodon) pp. 347–363. Report 5. (Environmental Research Program of the Commission of European Communities: Brussels.) Sharp, R. (1993). Regeneration costs under alternative silvicultural systems in lowland sclerophyll forest. VSP Technical Report No. 9. (Department of Conservation and Natural Resources, Victoria: Melbourne.) Shea, S.R. and Kitt, R.J. (1976). The capacity of jarrah forest native legumes to fix nitrogen. Research Paper No. 21. Forest Department of Western Australia: Perth.) Squire, R.O. and Edgar, J.G. (1975). A study of natural regeneration of mixed eucalypts under partial cutting

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conditions in the Wombat Forest. Research Branch Report 60. (Forests Commission of Victoria: Melbourne.) Squire, R.O., Dexter, B.D., Smith, R.B., Manderson, A.D. and Flynn, D.W. (1987). Evaluation of alternative silvicultural systems for Victoria’s commercially important mountain eucalypt forests. Project Brief: Working Draft. (Department of Conservation Forests and Lands, Victoria: Melbourne.) Stewart, H.T.L., Flynn, D.W. and Hopmans, P. (1985). On harvesting and site productivity in eucalypt forests. Search 16, 206–210. Stewart, H.T.L., Hopmans, P., Flynn, D.W. and Croatto, G. (1990). Harvesting effects on phosphorus availability in a mixed eucalypt forest ecosystem in south eastern Australia. Forest Ecology and Management 36, 149–162. Turner, J. and Lambert, M.J. (1986). Effects of forest harvesting nutrient removals on soil nutrient reserves. Oecologia 70, 140–148.

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Walters, M. (1991). The regeneration of Eucalyptus regnans F. Muell. under alternative silvicultural systems. 1. Seedling establishment and early height growth (First seasonal replicate). Silvicultural Systems Project Internal Progress Report 2. (Department of Conservation and Environment, Victoria: Melbourne.) Webb, D.P., Ellis, R.C. and Hallam, P.M. (1983). Growth check of E. delegatensis regeneration at high altitudes in north-eastern Tasmania. Canadian Forest Service Information Report 0-X-348. (Reprinted as CSIRO Division of Forest Research Reprint No. 370, Canberra.) White, B.J. (1971). Karri Silvics. Research Note No. 1. (Forest Department of Western Australia: Perth.) Wilson, N.W. (1993). Distribution of raw eucalypt seed by a helicopter-mounted sowing system. Forest Technical Report No. 11. (Department of Conservation and Natural Resources, Victoria: Melbourne.)

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The eucalypts dominate the vegetation of Australia over a wide climatic range. The most important aspects of their persistence at a particular site are their longevity and their ability to regenerate. Drought and fire are the most important factors affecting eucalypts through most of their range, but insect and fungal attack is persistent and can impair survival and competitive ability of the species. Longevity is affected by various factors, including fire and various diseases of mature trees (root rot caused by Phytophthora cinnamomi, woody root rot caused by Armillaria species, stem and butt rots, infection by foliar parasites and mistletoe) but the most critical aspect is the seedling phase which is very susceptible to damage by abiotic (heat, desiccation, flooding, frost) and biotic factors, including damping-off and a range of foliar diseases. The conditions required for regeneration are reviewed and the main modes of regeneration are discussed in relation to the degree of stress of various environments. Finally, the strategies of survival of the eucalypts in the often harsh Australian environment are discussed.

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4.1 Introduction The eucalypt genera Eucalyptus and Corymbia span the continent and dominate communities from the fringe of the north-east rainforests to the fringe of the central desert and the altitudinal tree line at about 1900 metres in the south-east (Fig. 4.1). The environmental range is thus enormous. Mean annual rainfalls range from less than 200 millimetres to more than 2000 millimetres with coefficients of variation from 15% to 80% and seasonal distribution from uniform to summer or winter types. Temperatures range from consistently hot to widely fluctuating or to cool with snowy winters. In the south-east they form the tree line at about 2000 metres. Soils are generally poor but range from nutrient-rich loams to very poor sands and laterites. There is a tendency for species of Eucalyptus subgenus Symphyomyrtus to occur on better soils and those of Eucalyptus subgenus Monocalyptus and genus Corymbia to occur on poorer soils (Florence 1996), although there are many exceptions and, in addition, ecotypic variation may be found in response to such edaphic factors.

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include dieback caused by Phytophthora cinnamomi Rands (see Chapter 11), woody root rots caused by Armillaria species (see Chapter 12) and stem and butt rots caused by a wide range of Basidiomycota (see Chapter 13). The incursion of mistletoes into disturbed vegetation particularly may also affect longevity of trees (see Chapter 15).

The stature of fully grown eucalypts ranges from diminutive shrubs, barely one metre high in the most extreme environments, to the tallest known angiosperms with heights at maturity in excess of 100 metres. A simplified scheme of certain key species in relation to an environmental fabric is shown in Figure 4.2. Eucalypts often form monocultures in either stressful or very favourable sites (see section 4.4) and form mixtures of from two to five species, often from more than one subgenus, in moderate sites. In relatively severe sites other genera may be present or even codominate the stands (e.g. Brachychiton, Callitris, Codonocarpus), whereas in some of the better sites, species of Allocasuarina, Lophostemon, Syncarpia and certain species of Acacia may be subdominant.

The regeneration niche is thus diverse, yet one factor, namely fire, is an important common denominator. Fires may occur whenever heavy fuel accumulation and dry weather coincide. Fire frequency increases to a maximum in the subhumid to semiarid zones; the wet forests only burn during extremely dry weather, and the desert vegetations only burn after periods of extremely wet weather that have promoted a lot of growth. South of latitude 25° south, the centrifugal hot dry winds emanating from the central desert may be associated with severe crown fires in the arc from Brisbane to Perth except for the whole Nullarbor region. In Tasmania, humus fires occur in some forests with devastating results (Cremer 1962). In wet forests in Victoria, heavy litter at the bases of old trees allows fire to burn for long enough to ‘ringbark’ or butt scar the tree. Butt scars are a common infection site for butt rot fungi (see Chapter 13). In this broad spectrum of habitat, eucalypt regeneration may be reliable or erratic and result in even-aged stands or groups in gaps between tree canopies. In unfavourable habitats, seedlings rapidly develop resistant, partly buried lignotubers. Suppressed lignotuberous regrowth (< 1–2 m tall), however, may occur beneath the overstorey as ‘advanced regrowth’ (Jacobs 1955). Such plants, once established, may persist through recurrent stresses for many decades and take advantage of any opening of the canopy. Most eucalypts have a capacity for copious epicormic growth provided fires are not so severe or frequent as to overcome the insulation provided by the bark.

The persistence of eucalypts on a site is a product of both the longevity of individuals and their regeneration. The latter is undoubtedly the more important aspect of their ecology. The seedling is the most vulnerable stage of growth and is frequently susceptible to drought, frost, overheating of surface soil, browsing, insect attack and, most importantly, fungal diseases (see Chapters 8 and 9). However, later growth stages are prone to a wide range of diseases that affect the longevity of trees. These

Biotic factors may affect the success of eucalypts on a particular site directly by predation, herbivory (Burdon and Chilvers 1974; Morrow 1976) or disease, or indirectly through competition among themselves or their understorey associates at particular stages. Generally in typical years, physical factors of the environment are likely to be more important in drier or more exposed sites, whereas biotic factors, including disease, are likely to be more important in wetter and more favourable sites.

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Figure 4.1

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Extent of eucalypt-dominated communities in Australia.

CLIMATE HOT

WARM

porrecta jacobsiana

macrorhyncha siderophloia

SOIL tetrodonta miniata

Figure 4.2

radiata obliqua

30 m pauciflora

60m

pilularis microcorys

regnans 90m

grandis

viminalis

bleeseri WET

COOL

oleosa incrassata

DRY

MOIST

MILD

delegatensis stellulata camphora

ovata camaldulensis

Isolines of eucalypt tree height in relation to some environmental parameters, indicating the occurrence of particular eucalypt species in relation to these factors.

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4.2 Characteristics of eucalypts in relation to their regeneration 4.2.1

Seed

Most eucalypts have small seed (1–2 mm long) with oil storage in the cotyledons. Seed is produced at regular or irregular intervals depending on both the species and climate. Often it is stored in woody capsules, 5 to 30 millimetres in diameter, and held on the tree for several years, thus buffering variations in yearly production. On the tree, seed is consumed by minute beetles or various psittacine birds, and may suffer some loss from fungal infection (see Chapter 7). On the soil, seed is an important food source for insects such as ants and lygaeid bugs (Euander spp., Dieuches spp.) which avidly collect it on the soil or litter surface in most areas of the continent. In good years, seed is shed in enormous numbers, particularly following fires when seed fall exceeds the needs of consumers. Soilborne fungi may also take a toll of fallen seed, particularly on wetter sites.

4.2.2

Seedlings

With eucalypt seed being so small, the pre-emergence and postemergence seedling stage is very susceptible to damping-off in native forests (Mwanza and Kellas 1987) (see Chapter 8). Heavy loss of seedlings can occur at this stage, especially during cool, wet weather. Eucalypts are heteroblastic and the juvenile stages are usually characterised as having opposite dorsiventral leaves for three to five or as many as 30 to 40 pairs or more. The adult form is isobilateral in the Eucalyptus subgenera Monocalyptus and Symphyomyrtus (except E. botryoides and related species) but dorsiventral in Corymbia. Certain species have developed chemical defences in juvenile foliage (e.g. toxins such as cytogenetic glucosides) as a deterrent against insect attack and mammal predation (Pryor 1976). Some glaucous leaves have chemical defences against fungal attack (Heather 1967). Several leaf pathogens [e.g. Mycosphaerella nubilosa (Cooke) Hansf.] are confined to juvenile foliage; others are more common on juvenile than on adult foliage (see Chapter 9). Lignotuber development occurs in most species and commences as woody swellings in the lowermost leaf axils. These fuse and grow down into the soil where they provide a store of buds and carbohydrate

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protected from fires and browsing (Carrodus and Blake 1970). The largest lignotubers, recorded by Mullette (1978) from C. gummifera, formed a complex of 75 square metres. In some cases they have been attributed wrongly to galling caused by Agrobacterium tumefaciens (Smith & Townsend 1907) Conn 1942 (see Chapter 14). In some species, rhizomes (Lacey 1974) or ‘rhizostolons’ (Gillison et al. 1980) develop from these organs and emerge to produce new regrowth one or more metres from the parent. In most of the species that dominate the tall wet forests (wet sclerophyll or tall open forest), lignotubers are not developed and their capacity for vegetative regeneration after damage is meagre.

4.2.3

Tree form

The trunk of the tree varies conspicuously in the type and thickness of bark. In more fire-prone areas, bark is thick and is liberally endowed with dormant buds that sprout as epicormic shoots after fire. Bark thickness increases with stem diameter and is therefore thicker at the butt where the impact of fire is greatest. However, coppice from butts may occur even in some species without lignotubers. Litter is flammable and slow to decay in all but the humid environments, thus accumulating and encouraging fire. The oil content in glands in the foliage is often high especially in Monocalyptus species (e.g. 3% by weight in E. dives; Ewart 1930), producing explosive conditions in crown fires. The great height of trees in the wet climates ensures canopy survival from surface fires, but the sheer biomass of such forest ensures cataclysmic fires when conditions are severe. While fire is the most important factor in most of the Australian eucalyptdominated communities, a point emphasised succinctly by Gill (1975), insect and fungal attack of foliage is persistent in eucalypts and can seriously impair survival of regeneration or its competitive ability in the presence of species not so attacked. In general, gall insects attack expanding leaves, chewing and sap sucking insects attack the current year’s leaves and fungal disease is most evident on older leaves. Although fungi may seriously attack young leaves, the severity of fungal leaf spots becomes progressively greater on two-year-old and three-year-old leaves. Damping-off is common among dense seedling regeneration and foliar diseases can be destructive in seedlings in the first year or two (see Chapter 8). While fungal diseases of foliage are common in native forests, they are

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not usually destructive (see Chapter 9). However, alteration of the forest environment could lead to epidemics.

adequate seed supply following adequate conditions for flowering and seed set

2

sufficient quantities of seed to allow satiation of seed harvesting insects

3

favourable microflora and (premycorrhizal) rhizosphere associations.

Germination conditions: 1

a favourable seedbed, especially bare soil free of litter and ground stratum (grasses, ferns, shrubs)

2

maintenance of suitable conditions of soil moisture and temperature

3

slight burial which reduces predation by seedharvesting insects (ants, lygaeid bugs).

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adequate light to allow development through the juvenile stages of lignotuber production

8

sufficient growth to allow seedlings to endure the stress period of the following season such as seasonal drought, frost, flood inundation or snow cover

9

sufficient light and freedom from root competition, usually as a result of larger canopy gaps, to enable development through the sapling and pole stages to the adult stage.

Seed supply: 1

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4.3 Conditions required for regeneration The ideal conditions required for regeneration (germination to adult seed-bearing stage) of eucalypts are as follows.

OF

4.4 Major modes of regeneration In general the major modes of regeneration are related to climate and the adaptation of the species to the important limiting factors in their environment. The attributes of eucalypts over their climatic range in Australia (Fig. 4.3) as they relate to their modes of regeneration are discussed below. Because of their considerable variability, many eucalypt species may range over more than one habitat type. The climatic range of eucalyptdominated communities and their associated opportunities for regeneration can be categorised as follows: 1

stressful sites (scrub, semiarid woodland, semiarid mallee, many subalpine woodlands, coastal heath)—seedling regeneration rare or erratic

Seedling development: 1

one or more favourable seasons following germination

2

2

early protection from exposure to heat, frost and desiccation, and from rain splash which may carry pathogens (see Chapter 9, especially in relation to winter leaf spot of E. regnans caused by Piggotia substellata Cooke and Ceuthospora innumera Massee)

hazardous sites (woodlands)—seedling regeneration occasional and often at long intervals; vegetative spread possible in tropical regions

3

floodplain sites (open forest to woodland)— regeneration by seed under the control of regular or erratic flood regimes

4

reliable sites (open forest; subhumid to humid; climate relatively favourable for plant growth)— regeneration common especially following fires

5

very favourable, high forest sites (tall open forest; humid to very humid; site conditions very favourable for plant growth)—opportunities for regeneration are infrequent and controlled by disturbances such as fire and wind throw.

3

soil conditions that allow rapid root penetration

4

sufficient air movement and low humidity to reduce damping-off and other diseases (see Chapter 8)

5

low incidence of insect predation of seedling buds and foliage

6

protection from browsing marsupials, including sufficient alternative feed, or sufficient numbers of gaps between seedlings to allow dispersion of browsing and survival of at least some seedlings

4.4.1

Stressful sites

Stressful sites occur in wind-swept coastal or subalpine or regularly drought-prone areas. In these

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750

1000

1250 mm

Stature

Regeneration

Understorey

Lignotuber

Figure 4.3

Stature, regeneration, understoreys and lignotuber development in eucalypts with increasing mean annual rainfall.

sites, eucalypts are low growing (1–8 m) and open spaces between them are large (Plate 4.1). They characteristically have large, conspicuous lignotubers that project above ground and support several stems of equal dominance. They are often gnarled in old age. Regeneration is rare and follows extremely favourable seasons and combinations of seasons. In the semiarid mallee of Victoria, seeds germinate in the winter and spring when they are frost prone. In the first summer they are drought prone (Parsons 1969; Wellington and Noble 1985). High root to shoot ratios in the seedling stages of different species or ecotypes are considered by Parsons (1994) to be an important attribute in successful establishment. After fire, seedlings occur in densities of up to 900 per square metre in hollows where wind and water have collected seed and charred debris. Under these

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conditions the partitioning of moisture resources may be insufficient to allow seedlings to withstand the first summer droughts (Wellington and Noble 1985; Wellington 1989). If they survive and produce lignotubers they will be virtually indestructible and may live for many hundreds of years. Because eucalypts are ‘crown shy’ due to their system of naked buds (Jacobs 1955), stems arising from the lignotuber grow outwards causing increased strain. If the original stem dies, a lignotuberous ring results (Fig. 4.4). Death of the stem may occur when the moment of torque exceeds the strength of the roots, and the rings segments are uprooted. Infection by wood rot fungi such as Phellinus rimosus (Berk.) Pilát (see Chapter 13) may also occur on the exposed upper sides of leaning stems where thin bark may not protect the cambium from damage inflicted by excessive sun scorch.

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Figure 4.4

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Stressful site: Eucalyptus behriana mallee, showing hollow left by the decay of the lignotuber, Melton, Vic.

In the subalpine zone at 1500 to 1800 metres, E. pauciflora develops patches of suppressed growth, each with their own lignotuberous rings. Here, regeneration is limited by snow lie and frost and by severe desiccating winds in winter and spring (Jacobs 1955; Costin et al. 1964; Farrell and Ashton 1973; Ashton and Hargreaves 1983; Ashton and Williams 1989). In snow gum woodlands, regeneration is also dictated by the density of the fine grass tussocks of Poa hiemata Vickery and others of this complex (Plate 4.1). Whereas the seedlings appear to need gaps for establishment they also need the protection of the overhanging grass tussocks against frost. In open situations (e.g. Mt Wellington plains, North Central Gippsland, Vic.), regeneration is commonly restricted to microsites beneath the eucalypt canopy. Suppressed growth is common under the canopy in wetter areas of these forests and woodlands. In some places, snow gums may be killed by fire if humus soils burn and kill the relatively superficial lignotuber (Jacobs 1955). In coastal heaths on deep sands, eucalypts may also develop a mallee form and regeneration is largely prevented by the dense, fire-resistant heath species [e.g. in Victoria Leptospermum myrsinoides Schldtl.

and Allocasuarina pusilla (Macklin) L.A.S. Johnson]. Occasional eucalypts (E. baxteri, E. obliqua) may remain suppressed for many years before emerging above the heath stratum at two metres. Once this occurs, the eucalypts inhibit the heath dominants and form a modified sclerophyll forest or woodland.

4.4.2

Hazardous sites

These occur in subhumid areas with a long severe dry period, annually or lasting many years. Eucalypts in these sites have been shown to regenerate by two modes—seed or rhizomes and root suckers. In tropical areas, several species (C. jacobsiana, C. porrecta) develop dense clones from shallow rhizostolons after fire. Such plants later thin out to form woodland (Lacey 1974) (Plate 4.2). However, in temperate zones, rhizostolons are relatively rare (Gillison et al. 1980). These communities vary considerably in density and size—they are commonly between 10 and 30 metres tall. Gillison (1996) has pointed out the great physionomic variation of woodlands, including monopodial, sympodial and hemisympodial forms. The environments are often unfavourable for seedling establishment, and hence stands may become increasingly open with age until

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Floodplain: seed of Eucalyptus camaldulensis (see arrows) shed on flood deposit in late spring, Tocumwal, NSW.

the right sequence of years enables regeneration to occur. This may be sporadic and scattered, perpetuating the woodland structure, or may result in much denser patches of vegetation with an almost open forest form in the early stages of tree development. Thus, grassy woodlands in the Australian Capital Territory have regenerated only at long intervals, when sequences of three wet years have occurred. According to Jacobs (1955, p. 216) it takes three years to establish the lignotuberous seedling of such tree species. Frequently, regeneration is conspicuously inhibited by the presence of the tree crown and groups occur beyond this up to the distance of seed throw as an asymmetric halo, commonly extending for a distance of from one to three tree heights down wind or down slope. In the tropics (e.g. Arnhem Land), one of the major species, E. tetrodonta, has the capacity to regenerate from root suckers when the stand is damaged or soil is disturbed (Plate 4.3). If cleared or felled by cyclones after being weakened by termite attack, E. tetrodonta can replace its population by this means and grow to 3.8 metres in two seasons. The intact stand up to 24 metres tall may consist of 310 trees per hectare, of which only a very small

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percentage are less than two metres tall; the paucity of shrub regrowth in these forests is probably due to annual or biennial fires and the density of tall annual Sorghum, which itself is promoted by repeated late season fires. In many sites, eucalypts are facultatively deciduous (Plate 4.4).

4.4.3

Floodplain sites

The open forests and woodlands on these sites are epitomised by E. camaldulensis and to a lesser extent E. largiflorens in the Murray River central tract where the moderately low rainfall (300–350 mm per annum) is supplemented to various extents by flooding (Plate 4.5). Floods from the melting of the alpine snows are erratic, occurring every one to five or 15 years depending on the distance from the river and the height of the floodplain above the river. There is thus a gradation of site quality from too little to too much flooding. Trees vary in size and density and mature heights range from 20 to 42 metres. In the best site quality, one to two centimetres of silt is deposited annually and regeneration occurs from seed fall onto this silt (Fig. 4.5). In this site, about 200 trees per hectare are 12 to 30 metres tall and occur above

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regrowth with a density of 360 trees per hectare. In the poorer, more open sites, trees are 12 to 24 metres tall with a density of 100 to 120 trees per hectare. Regeneration following very high floods occurs in these sites and is restricted to positions between the tree crowns. Regeneration follows seed fall at the time of floods (Jacobs 1955) (Plate 4.6). Seed washed or blown to the edge of the flood germinates densely in the worst sites. Seed dropped among flood debris frequently is successful due to the protection offered from surface evaporation. Germination among the grass sedge sward of the intermediate site qualities is disadvantaged by dense root competition. Seed may be washed or blown over the water surface to the edge of the flood. If the flood is extensive, germinants are often stranded in the most unfavourable sites and therefore rarely survive. The best growth of E. camaldulensis occurs where floods occur every two years to three years, thus ensuring a regular replenishment of water reserves and a top dressing of one to two centimetres of fine silt. Regeneration follows floods, soil disturbance or surface fires and in such sites seedlings produce deep root systems which reach watertables in aerated gravel and sand layers (Jacobs 1955). In this way they are sturdy or tall enough to withstand any inundation of the next flood. Weak seedlings inundated for more than three months are seriously affected or killed, or unable to withstand the weight of deposited floating hydrophytes (Azolla and Lemna) following flood recession. Very frequent and prolonged flooding, however, is deleterious to E. camaldulensis and forest is replaced by rampant grasslands (Chesterfield 1986). The behaviour and regeneration of these communities is, therefore, under the control of flood frequency and intensity—without such water supply, gaps may remain unfilled for 15 years or more (Dexter 1978).

4.4.4

Reliable sites

The type of regeneration on these sites is relatively reliable—climatic conditions are adequate in most years and fire frequency is sufficient to permit regeneration to occur in gaps and persist as advanced lignotuberous regrowth one to two metres tall. Seed harvesting by ants is rife. Therefore, establishment usually occurs after fire, when seed fall is greatly in excess of demand, and when transpiration stresses are reduced, soil nutrients more available and light intensity increased during the period of crown repair.

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Advance regrowth is a most important aspect of the forest regeneration cycle which takes advantage of the favourable opportunity for establishment and persists until the appropriate canopy-space becomes available. In E. marginata forests of south-west Western Australia, this understorey of arrested development can quickly grow as a group of ‘evenaged’ saplings and trees when old trees die or are wind thrown (Plate 4.7) (van Noort 1960). The depth of the watertable is of critical importance for survival in this forest. In analogous forests of E. obliqua and E. radiata in central Victoria such regrowth, predominantly of E. radiata, also occurs (Gill and Ashton 1971). Such forest mixtures may show oscillation of dominance if fire does not allow the restoration of E. obliqua regeneration. In somewhat drier environments, soil type may discriminate between overstorey eucalypts and type of understorey. Thus, on poor soils sclerophyll shrubs are predominant (Plate 4.8) but on richer soils these are replaced by graminoids and forbs (Plate 4.11). In Victoria, some low open forests and woodlands of E. macrorhyncha and E. dives may develop a diffuse stratum of suppressed regeneration consisting mainly of E. dives. Such forests appear to be unstable mixtures and given the continuing progress to maturity, this regeneration may assert itself to produce a forest overstorey of changed composition, possibly maintained by the effect of host-specific pathogens (see Chapter 9). The differential success of such regeneration could be the result of relative seed availability at the time of the last fire, the relative ecological tolerance of the species to drought and shade imposed by the overstorey and understorey, and their relative resistance to insect and fungal attack. In these cases, the more ‘tolerant’ species tend to be those in which the dorsiventral, horizontal juvenile foliage persists for a long time. In mixed stands of dry sclerophyll forest at Mallacoota, Vic., C. gummifera and E. botryoides with dorsiventral foliage are conspicuous as a suppressed stratum one to three metres high beneath an overstorey of C. gummifera, E. botryoides, E. globoidea and E. sieberi. Eucalyptus botryoides was severely attacked by the psyllid, Cardiaspina bilobata Taylor, in the 1980s and 1990s and this in the long term may substantially alter the outcome of stand competition. Following the severe fires at Mt Macedon, Vic., in 1983, E. obliqua regenerated prolifically both under

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tree canopy and in gaps. After three years all seedlings were severely attacked by the leaf spotting fungus, Aulographina eucalypti (Cooke & Massee) Arx & E.Müll. (see Chapter 9). Only in the better quality microsites were seedlings able to outgrow these attacks and survive. Under the regenerated tree canopy 10 years after the fire, the demise of all seedling regeneration was undoubtedly hastened by severe leaf spot damage, so that after 15 years, regeneration only survived in overstorey gaps.

4.4.5

Very favourable, tall forest sites

In these forests, the site of most current timber and pulpwood extraction from native forests in Australia, the canopy may be 50 to 100 metres tall with an understorey of dense shrubs, trees, tree ferns, ground ferns and tussock or scrambling grasses (Plates 4.9, 4.10, 4.12 and 4.13). The dense understorey is the primary barrier to regeneration of the eucalypts. The shade tolerance qualities and the density of understorey is enhanced when long absence of fire encourages rainforest elements to establish where they are within dispersal range. Large gaps in the overstorey may be caused by multiple tree falls, or patches of sustained attack in certain areas by lerps or stick insects [Didymuria violescens (Leach)]. Such gaps may be regenerated if the understorey senesces or is temporarily removed by fire. Thus, two or three age classes can occur in some forests although many are even-aged as a result of widespread severe fires. In Tasmania, Bowman and Kirkpatrick (1984) have indicated that many of the tall open forests and tall woodlands of E. delegatensis are multiaged as a result of light fires. Although in Victoria many of the forests of this species are even-aged as a result of very severe wildfires (Grose 1963), regeneration does occur without the intervention of fire in light or senescent understoreys where trees are widely spaced with woodland form. Such tall woodlands may indicate long periods of regeneration difficulty in upper montane sites and be analogous to those situations described previously for hazardous sites. In large, well-lit areas of bracken (one to many hectares) created by recurrent overlapping fires, colonisation by E. regnans and understorey species from surrounding forest can occur without fire provided that the bracken community has developed patchiness of vigour on a microscale, sensu Watt (1955).

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In general, where rainfall is high enough (> 1500 mm/annum) and the probability of severe fires sufficiently low in eastern Australia, tall open forest eucalypts clearly occupy potential rainforest sites (Plates 4.9, 4.10 and 4.12) (Jackson 1968; Ashton and Attiwill 1994). Most of the fast-growing, tall eucalypts of these wet climates are non-lignotuberous and depend upon the enrichment of the ash-bed soil after fire to realise their full height. Under conditions of full light, high soil moisture storage and adequate nutrients they outstrip the understorey associates in one to two years. Under the canopy of the mature trees, however, the success of regeneration is much less assured. If initiated by surface fires, regeneration may be sufficiently stimulated to compete with the understorey and then remain suppressed as saplings of 10 to 20 metres tall for 30 to 40 years until killed by rare periods of drought. Without fire, chance regeneration on bared soil may survive the juvenile stages, only to succumb to understorey competition within five to 10 years. Survival beyond the juvenile stage is particularly hazardous because of attack by insects and damping-off fungi, and browsing by wallabies or possums. Lethal winter leaf spot disease, spread from litter, destroys all but the earliest of the season’s germination of E. regnans in the forest environment (Ashton and Macauley 1972) (see Chapter 9). In the humid microclimate of the mature forest, damping-off of tender cotyledonary seedlings by fungi such as Alternaria may be very common under shady conditions in wet summers. At higher elevations, snow damage and water infiltration as well as leaf and shoot blight caused by Botrytis cinerea Pers. occurs in E. delegatensis when regeneration is insufficiently robust (Grose 1963). In this case, regeneration on warmer slopes and on ashbeds is sufficiently vigorous to survive the critical early years. Seed losses from harvesting ants and lygaeid bugs may account for 60% to 90% of the year’s seed fall of E. regnans (Cunningham 1960; Ashton 1979). Germination may be delayed by overheating of the exposed soil surface; if delayed until autumn in a forest environment, the hazards of winter survival become real. In the montane E. delegatensis forests, seed is dormant because of the necessity for stratification. Hence, germination is delayed until the following spring and thus avoids the lethal frosting of winter. Under regimes of even-aged regeneration, fires in summer kill forest

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over very large areas and establishment of seedlings follows autumn rains. Under these open conditions, hazards of season and of fungal attack are minimised. In south-west Western Australia, the tall forests of E. diversicolor have a similar ecology and the remarkably similar form of the understorey imposes similar restraints (Plate 4.13). Where mixtures with the slower growing, more fire-resistant and lignotuberous C. calophylla occur in this region an unstable mixture is evident (Christensen 1972). Arrested lignotuberous regrowth of C. calophylla may occur commonly in the understorey where, due to its greater shade tolerance, it persists for long periods until an opportunity arises for it to develop further. Without fire for very long periods this species would probably become dominant. The intervention of fire at a time when E. diversicolor is bearing abundant seed would certainly restore dominance of this species. In some of the wettest forest in this region, tall mature E. diversicolor and very large, ancient E. guilfoylei and E. jacksonii occur with a tall second stratum of Allocasuarina decussata (Benth.) L.A.S.Johnson (20–40 m) which shows a wide range of girth classes. One interpretation is that, in the absence of true rainforest, this species may finally dominate the site in the event of a very long absence of fire. However, it could be argued that relatively high fire frequency is endemic to this region (Underwood 1978; WardellJohnson and Coates 1996) and that regeneration of eucalypt forest in some form is assured. In south-east Australia, a similar interpretation could be made of some old E. regnans forests in moderately wet climates where large Acacia melanoxylon R.Br. (30–45 m) forms the second stratum in the absence of rainforest elements. In such instances, a long period of fire absence in excess of 400 to 500 years may allow a complex temperate forest to be dominated by this species and the understorey species, Olearia argophylla (Labill.) Benth. An analogous situation occurs on the Atherton Tableland in North Queensland where wet sclerophyll forest of E. grandis is zoned between rainforest and grassy forest dominated by C. intermedia. Eucalyptus grandis, like E. diversicolor and E. regnans, is both nonlignotuberous and fast growing and is not particularly fire resistant, especially in the young stages. Corymbia intermedia, a bloodwood like

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C. calophylla, is large seeded and relatively slow growing, develops a strong lignotuber and is fire resistant. It can thus withstand fire early in its life and can persist in the presence of tall grasses such as Themeda triandra Forssk. and Imperata cylindrica (L.) P.Beauv. Fires tend to weaken and die out at the rainforest margin. In this niche, E. grandis can assert its height growth superiority and dominate the rainforest elements, for a time. It cannot survive the fire intensity or competition in the sites further away from the rainforest ecotone, although the environment is otherwise suitable (Unwin 1989). The lack of vigour of some eucalypt seedlings in unburnt mature forest of E. regnans or E. pilularis suggests that some antagonistic factors are present. Ellis and Pennington (1992), in studying dieback of E. delegatensis in Tasmania, suggested that these factors may include the age of the dense understorey, a dense grass stratum or the humus type and perhaps the cool microclimate of the root zone. In mature E. pilularis forest soil, Florence and Crocker (1962) suggested that a microbiological antagonism may be the cause of seedling inhibition. This effect was alleviated by fire, heavy fertiliser application, or aeration and desiccation of the soil. In E. regnans forests, the poor growth of young seedlings on soils in unburnt, constantly moist microsites may be spectacularly stimulated by air drying the soil before planting. This results in increases in both available phosphorus and nitrogen and in changes in the microflora in the short term (Ashton and Kelliher 1996). Some effects may be due to exudates from the living root mat of mature E. regnans and Pomaderris aspera A.Cunn. ex DC. (Ashton 1962), to the allelopathic effects of soil lipids (Ashton and Willis 1982) or to the aqueous phase of essential oils from leaves. An interesting development has been the discovery that some strains of the rhizosphere fungus, Cylindrocarpon destructans (Zinssm.) Scholten (Evans et al. 1967), isolated from the roots of moribund E. pilularis seedlings from the mature forest, produce a phytotoxic substance (nectrolide). This fungus has been isolated also from the root surfaces of E. regnans seedlings from the mature forest. The antagonism towards seedlings of mature forest soils can be demonstrated in the glasshouse by growing E. regnans seedlings in freshly collected top soil. Seedlings are unthrifty and purplish. If soil is incubated for three months in warm to hot glasshouse conditions or merely air dried at 20°C to

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45°C, plants are subsequently vigorous and healthy (Ashton and Kelliher 1996). The rhizosphere microflora from numerous root samples of green and purple seedlings was examined by Hin Yuen Yipp (pers. comm.) and results analysed by classificatory programs. Certain species were consistently associated with healthy plants and others with purple plants. The association of health of seedlings with groups of fungal species (and bacteria) suggested that Cylindrocarpon destructans may be an important species in this syndrome and that its effect may be mediated by the presence of other species. However, the appearance of inhibited E. regnans seedling root systems does not suggest damage by microorganisms. Seitz-filtered, aqueous culture medium of Cylindrocarpon destructans certainly caused the death of root tips in vitro (Ashton and Willis 1982), but in glasshouse experiments the effect of inoculation of this species into either sterile or nonsterile soil is neither as consistent as, nor as severe as, the inhibition evident in undried forest soil. Launonen (1995) subsequently demonstrated that although the effect occurred in sterile conditions, it was negated in unsterile soil possibly by the action of the microflora on the fungus. The desiccation of soil greatly increases the availability of phosphorus to seedlings (Ashton and Kelliher 1996 ) and may change the nature of the mycorrhizal relationships (Warcup 1983). R.J. Kelliher and D.H. Ashton (unpubl. data) have shown that although air drying of soil decimates the microbial populations, bacteria and fungal numbers (determined from soil dilution plates) rebound within two to three weeks to their original levels whereas recovery of actinomycete numbers is very slow. Some mycorrhizal fungi, particularly Ascomycota, survive such drying treatment and form symbiotic relationships in four to six weeks. The research into this facet of forest regeneration has only begun. It seems clear that the microflora can be modified by climatic conditions and the composition of the forest community and above all, as shown by Renbuss et al. (1973) and Chambers and Attiwill (1994), by the partial sterilisation wrought by heat and fire.

4.5 In synthesis—the strategies of survival Eucalypts are in general opportunists, producing abundant seed periodically. Their flammable foliage and litter and abundant production of fine, readily

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cast twigs aids the spread of fire. Most are fire resistant, and all are fire tolerant provided fire frequency does not encroach upon their sensitive non-flowering juvenile period nor their early nonlignotuberous stage. However, the latter is usually so short that sufficient fuel to carry a fire does not have time to accumulate during this period. Fire is not the general panacea of ills, although it is a compromise of losses and gains. The more tenacious and dense the understorey, the more necessary is fire to provide the right seedbed for the small and delicate eucalypt seed and seedling. The drier the climate the more success depends on the chance sequence of good years. The soil antagonisms that appear to be common in the wet humid climates are, like all the other factors adverse to regeneration, of little consequence if fire, when it comes, provides nearperfect conditions for establishment. The eucalypts, therefore, behave mostly as C-type strategists (vigorous colonisers, fast-growing, competitive) in the sense of Grime (1979). However, although most species are intolerant of shade beneath their own canopy they have, through the perfection of the lignotuber organ, devised a way of resisting stresses of drought, browsing and fire. This ‘fortress’ of buds (and food reserves) enables eucalypts to persist for very long times in a state of suppression. The extent to which weaker trees may be succoured by root fusion to adjacent vigorous dominant trees is unknown (Ashton 1975). In this sense, some eucalypts possess S-type (slow-growing, stress tolerant) characteristics. Relatively few have developed shade tolerance beyond the early juvenile phase. Many of the more shade-tolerant species are bloodwoods, which are a group some would regard as more primitive, having dorsiventral leaves with transverse venation and horizontal orientation which enables a better interception of overhead light penetrating the canopy. The explosive spread of eucalypts in the Cainozoic in the wake of the demise of the pancontinental rainforests has been in response to the development of colonising characteristics and adaptations to ensure the seizing of regeneration opportunities. The enormous variability inherent in most eucalypt populations could well be a legacy of past climate instability. Although many eucalypts will regenerate in suitable sites without fire, their abundance and vigour are greatly increased by it. Today they exist against a broad canvas between recurrent

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catastrophes in the humid zone and complex but favourable chance events in the dry. The utilisation of this broad ecological base for conservation and management of eucalypts, both within and beyond their natural environments, is a challenge for the future.

4.6 References Ashton, D.H. (1962). Some aspects of root competition. In Proceedings of the Third General Conference. (Institute of Foresters of Australia: Melbourne.) Ashton, D.H. (1975). The root and shoot development of Eucalyptus regnans F. Muell. forests. Australian Journal of Botany 23, 867–887. Ashton, D.H. (1979). Seed harvesting by ants in forests of Eucalyptus regnans F. Muell in central Victoria. Australian Journal of Ecology 4, 265–277. Ashton, D.H. and Attiwill, P.M. (1994). Tall Open Forests. In Australian Vegetation 2nd edn. (Ed. R.H.Groves) (Cambridge University Press: Cambridge.) Ashton, D.H. and Hargreaves, G.R. (1983). Dynamics of subalpine vegetation at Echo Flat, Lake Mountain, Victoria. Proceedings of the Ecological Society 12, 35–60. Ashton, D.H. and Kelliher, K.J. (1996). The effect of soil desiccation on the nutrient status of Eucalyptus regnans F. Muell seedlings. Plant and Soil 179, 45–56. Ashton, D.H. and Macaulay, B.J. (1972). Winter leaf spot disease of seedlings of Eucalyptus regnans and its relation to forest litter. Transactions of the British Mycological Society 58, 377–386. Ashton, D.H. and Williams, R.J. (1989). Dynamics of subalpine vegetation in the Victorian region. In The Scientific Significance of the Australian Alps. (Ed. R. Good) pp. 143–168. (Australian Alps National Parks Liaison Committee: Canberra.) Ashton, D.H. and Willis, E.J. (1982). Antagonisms in the regeneration of Eucalyptus regnans in the mature forest. In The Plant Community as a Working Mechanism. (Ed. E.I. Newman) pp. 113–128. (Blackwell Scientific Publication: Oxford.) Bowman, D.M.J.S. and Kirkpatrick, J.B. (1984). Geographic variation in the demographic structure of stands of Eucalyptus delegatensis R.T. Baker on dolerite in Tasmania. Journal of Biogeography 11, 427–437. Burdon, J.J. and Chilvers, G.A. (1974). Fungal and insect parasites contributing to niche differentiation in mixed species stands of eucalypt saplings. Australian Journal of Botany 22, 103–114. Carrodus, B.B. and Blake, T.J. (1970). Studies on lignotubers of Eucalyptus obliqua L’Herit. 1. The nature of the lignotuber. New Phytologist 69, 1069–1072. Chambers, D. and Attiwill, P.M. (1994). The ashbed effect in Eucalyptus regnans forest: chemical, physical and

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microbiological changes in soil after heating or partial sterilization. Australian Journal of Botany 42, 739–749. Chesterfield, E.A. (1986). Changes in the vegetation of the river red gum forest at Barmah, Victoria. Australian Forestry 49, 4–15. Christensen, P.E. (1972). Plant succession and past and present burning in the karri forest. Forest Notes 10, 7–11. Western Australian Forests Department, Perth. Costin, A.B., Wimbush, D.J. and Cromer, R.N. (1964). Studies in Catchment Hydrology in the Australian Alps V. Soil Moisture Characteristics and Evapotranspiration. Technical Paper No. 20. (CSIRO Division of Plant Industry: Canberra.) Cremer, K.W. (1962). The effects of fire on eucalypts reserved for seeding. Australian Forestry 26, 129–154. Cunningham, M.C. (1960). The Natural Regeneration of Eucalyptus regnans. Bulletin No. 1. (School of Forestry, University of Melbourne.) Dexter, B.D. (1978). Silviculture of the river red gum forests of the Central Murray Flood Plain. Proceedings of the Royal Society of Victoria 90, 175–192. Ellis, R.C. and Pennington, P.I. (1992). Factors affecting the growth of Eucalyptus delegatensis seedlings in inhibitory forest and grassland soils. Plant and Soil 145, 93–105. Evans, G., Cartwright, J.B. and White, N.H. (1967). The production of a phytotoxin, nectrolide, by some root surface isolates of Cylindrocarpon radicicola wr. Plant and Soil 26, 253–260. Ewart, A.J. (1930). The Flora of Victoria. (Victorian Government Printer: Melbourne.) Farrell, T.P. and Ashton, D.H. (1973). Ecological studies on the Bennison High Plains. Victorian Naturalist 90, 286–298. Florence, R.G. (1996). Ecology and Silviculture of Eucalypt Forests. (CSIRO: Melbourne.) Florence, R.G. and Crocker, R.L. (1962). Analysis of blackbutt (Eucalyptus pilularis Sm.) seedling growth on a blackbutt forest soil. Ecology 43, 670–679. Gill, A.M. (1975). Fire and the Australian Flora: a review. Australian Forestry 38, 4–25. Gill, A.M. and Ashton, D.H. (1971). The vegetation and environment of a multi-aged eucalypt forest near Kinglake West, Victoria. Proceedings of the Royal Society of Victoria 84, 159–172. Gillison, A.N. (1996). Woodlands. In Australian Vegetation. 2nd edn (Ed. R.H. Groves) (Cambridge University Press: Cambridge.) Gillison, A.N., Lacey, C.J. and Bennett, R.H. (1980). Rhizostolons in Eucalyptus. Australian Journal of Botany 28, 229–304. Grime, J.P. (1979). Plant Strategies and Vegetative Processes. (Wiley and Sons: New York.) Grose, R.J. (1963). The Silviculture of Eucalyptus delegatensis Part 1. Germination and Seed Dormancy.

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Bulletin No. 2. (School of Forestry, University of Melbourne.) Heather, W.A. (1967). Susceptibility of the juvenile leaves of Eucalyptus bicostata Maiden et al. to infection by Phaeoseptoria eucalypti (Hansf.) Walker. Australian Journal of Biological Sciences 20, 769–775. Jacobs, M.R. (1955). Growth Habits of the Eucalypts. (Forests and Timber Bureau: Canberra.) Jackson,W.D. (1968). Fire, air, water and earth—an elemental ecology of Tasmania. Proceedings of the Ecological Society of Australia 3, 9–16. Lacey, C.J. (1974). Rhizomes in tropical eucalypts and their role in recovery from fire damage. Australian Journal of Botany 22, 29–38. Launonen, T.M. (1995). The effect of air drying of forest soil on the growth of seedlings of Eucalyptus regnans F. Muell. BSc Honours Thesis, La Trobe University, Bundoora, Victoria. Morrow, P.A. (1976). The significance of phytophagous insects in the eucalyptus forests of Australia. In The Role of Arthropods in Forest Ecosystems. (Ed. W,J, Mattson) pp. 19–29. (Springer: New York.) Mullette, K.J. (1978). Studies on the lignotubers of Eucalyptus gummifera (Gaertn.) Hochr. 1. The nature of the lignotuber. Australian Journal of Botany 26, 9–13. Mwanza, E.J.M. and Kellas, J.D. (1987). Identification of the fungi associated with damping-off in the regeneration of Eucalyptus obliqua and E. radiata in a central Victorian forest. European Journal of Forest Pathology 17, 237–245. Parsons, R.F. (1969). Physiological and ecological tolerances of Eucalyptus incrassata and E. socialis. Ecology 50, 386–396. Parsons, R.F. (1994). Eucalyptus scrubs and shrublands In Australian Vegetation, 2nd edn (Ed. R.H. Groves) pp. 291–319. (Cambridge University Press: Cambridge.)

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Pryor, L.D. (1976). The Biology of Eucalypts. The Institute of Biology’s Studies in Biology 61. (Edward Arnold: London.) Renbuss, M. A., Chilvers, G.A. and Pryor, L.D. (1973). Microbiology of an ashbed. Proceedings of the Linnean Society of New South Wales 97, 302–310. Underwood, R.J. (1978). Natural fire periodicity in the karri (Eucalyptus diversicolor F.Muell.) forest. Research Paper 41. (Forest Department of Western Australia: Perth.) Unwin, G.N. (1989). Structure and composition of the abrupt rainforest boundary in the Herberton Highland, North Queensland. Australian Journal of Botany 37, 413–428. van Noort, A. C. (1960). The Development of Jarrah Regeneration. Bulletin No. 65. (Forests Department of Western Australia: Perth.) Warcup, J.H. (1983). Effect of fire and sun-baking on the soil microflora and seedling growth in forest soils. In Soils: An Australian Viewpoint. pp. 741–756. (CSIRO: Melbourne/Academic Press: London.) Wardell-Johnson, G. and Coates, D. (1996). Links to the past: local endemism in four species of forest eucalypts in south-western Australia. In Gondwanan Heritage: Past, Present and Future of the Western Australian Biota. (Eds S.D. Hopper, J.A. Chappill, M.S. Harvey and A.S. George) pp. 137–154. (Surrey Beatty and Sons: Chipping Norton, NSW.) Watt, A.S. (1955). Bracken versus heather; a study in plant sociology. Journal of Ecology 43, 490–506. Wellington, A.B. (1989). Seedling regeneration and population dynamics of eucalypts. In Mediterranean Landscapes in Australia. (Eds J.C. Noble and R.A. Bradstock) pp. 155–167. (CSIRO: Melbourne.) Wellington, A.B. and Noble I.R. (1985). Post-fire recruitment and mortality in a population of Eucalyptus incrassata in semi-arid, south eastern Australia. Journal of Ecology 73, 645–656.

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The key variables that determine the physiological behaviour of eucalypts, including the links established between disease and physiology, are described. Leaf area is a major discriminant of productivity through its effect on light interception. Foliar pathogens reduce the effective leaf area and may further affect productivity by redirecting assimilate. Several diseases can affect also the functioning of stomata. Stomata play a key role in the regulation of transpiration and photosynthesis and provide a useful link between the photosynthetic performance of the plant, its water relations and water stress. This is explored with particular reference to the effect of dieback of eucalypts caused by Phytophthora cinnamomi.

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5.1 Introduction The ultimate effect of disease is to reduce the productivity of the eucalypt forest, although in some instances the opposite effect has been observed. For example, Eucalyptus marginata grew faster in an area infested with Phytophthora (Ph.) cinnamomi Rands than in an adjacent uninfested area: apparently the effect of disease in reducing intraspecific competition was more important than the direct effect of the disease in causing root damage and a loss in productivity (Davison and Tay 1988). This indicates the need to be aware of possible differences between the physiological effect of disease on individual trees and the impact on the whole population. Nevertheless a useful starting point is that disease has a potential effect on above-ground and below-ground production and that this can be measured in physiological terms. Apart from the effects of Ph. cinnamomi on the water relations of eucalypts, there has been little physiological investigation of the diseases of eucalypts.

5.2 Productivity and light interception The productivity of a eucalypt forest can be expressed in terms of its gross primary production (Pg). Net primary production (Pn) is then the total amount of organic matter assimilated minus losses of that matter to respiration (R). Thus: Pn = Pg – R

(5.1)

Net primary production, the total production available to other trophic levels including harvestable yield, is expressed as the dry weight of organic matter. If the effect of a disease is to reduce Pg or increase R, Pn will decrease. An alternative approach to measuring productivity is to consider the total amount of carbon assimilated (i.e. photosynthesis) by the forest (or an individual tree). This has the advantage of describing growth in terms of physiological processes that can be measured readily. Current approaches to mechanistic models of growth quantify the performance of the forest initially in terms of a simple description of the main physiological processes (McMurtrie and Wolf 1983; Sands 1995). Submodels can then be developed to cope with the complex interactions that environmental variables impose on those processes. Such a variable may be a disease.

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Photosynthesis is driven by the fraction of radiation intercepted by the canopy. If it is assumed that radiation is attenuated more or less exponentially through the canopy, this fraction is given by [1 – exp(kL*)] (through Beer’s law) where k is the fraction of incident photons absorbed per unit area and L* is the leaf area index or functional green area of the canopy standing over a unit of ground area (square metre of leaf area per square metre of ground area). For eucalypts it is appropriate to express this as the projected or single-sided area of the leaves. Gross photosynthetic production (Ag) can now be expressed as (McMurtrie and Wolf 1983): Ag = Amax [ 1 – exp ( –kSa L ) ]

(5.2)

Amax is the gross photosynthetic production at full light interception and SaL expresses L* as the product of dry weight of leaf organic matter (L, often approximated as leaf dry weight) and specific leaf area (Sa, ratio of leaf area to leaf dry weight). Amax and Ag are weights of carbon dioxide. The implication of this equation is that there is a proportional relationship between dry matter production and intercepted radiation and that L*(SaL) is a major determinant of the capacity of the stand for photosynthetic production. The slope of this relationship, a measure of the conversion efficiency of light to dry mass, has been found to be 0.4 to 0.5 grams per megajoule for above-ground production of developing stands of temperate eucalypts (Linder 1985; Beadle and Turnbull 1992). Conversion efficiencies for tree crops that are adequately supplied with water and nutrients are potentially similar to those for C3 agricultural crops (1.5 g/MJ; Monteith 1977; Cannell et al. 1988) but depend ultimately on the balance between photosynthesis and respiration and the effect of environmental stress. Diseases such as stem cankers (see Chapter 10), which disrupt the transpiration stream, may lower the water potential of the leaves, disrupt the integrity of the chloroplasts and reduce the conversion efficiency (Fig. 5.1). Alternatively, Mycosphaerella leaf blotch and similar leaf diseases (see Chapter 9) will reduce the percentage of green area (measured as L*) available and growth will decline accordingly, probably in the absence of a change in conversion efficiency. In South Africa, growth of E. nitens was negatively correlated with severity of Mycosphaerella leaf blotch as measured

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The relationship between production and intercepted radiation for a eucalypt canopy. OX, represents the relationship for a healthy canopy and production, is A1 when the level of radiation being intercepted by the canopy is at a maximum. Loss of intercepting area, perhaps to a foliar disease, reduces production along the line XY to A2. Severe stress, perhaps caused by a disease disrupting transport of water, reduces production to A3 along YZ (after Jarvis and Leverenz 1983).

using standard diagrams of percentage of leaf area affected by disease. Percentage of leaf area affected and defoliation were also highly correlated. However, growth did not decline until 25% of the crown was defoliated (Lundquist and Parnell 1987). As the major source of defoliation was in the lower and inner part of the crown, the relative contribution of these leaves to the total carbon budget of the tree would have been low, even in the absence of disease.

5.3 Biomass production, partitioning of dry mass and foliage The naked bud habit of eucalypts permits continuous growth above a critical temperature, given an adequate supply of water and nutrients. Maximum rates of biomass production of eucalypts are the greatest of any broad-leafed species. Published values exceed 40 tonnes per hectare per annum (Jarvis and Leverenz 1983) and may possibly reach higher levels of production given that stem volume increments of 58 (E. globulus, Gasana 1983) and 83 cubic metres per hectare per annum (E. grandis, Campinhos 1980) have been recorded in Rwanda and Brazil,

respectively. To some extent these have been attained in the absence of the pests and diseases prevalent in native forest which often combine with soils of low nutrient status and water-holding capacity to realise very low rates of wood production. Nevertheless, there is little doubt that yields from managed plantations in Australia can match those achieved in other countries (Beadle and Inions 1990; Cromer et al. 1990). The intensive silviculture that may be required in the form of ground preparation, fertiliser and irrigation to increase the nutrient and water supply, and pesticides to protect the foliage and minimise competition from weeds, essentially leads to a marked improvement in the conversion of available energy to dry mass at a given site (Turnbull et al. 1988; Beadle et al. 1995). The eucalypt tree at a given stage of its development is the end result of partitioning processes that distribute the carbon fixed during photosynthesis to leaves, branches, stems and roots. The physiological control of these processes is still poorly understood. The partitioning of carbon is often based on the distribution of dry mass. However, a proper appreciation of carbon balance requires a measure

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of the nutrient content of plant material and of the respiratory costs of producing dry mass (Farrar 1993). Eucalypts appear to differ in their capacity for growth and in a study of three species in a uniformly managed plantation, large differences were observed (Beadle and Inions 1990). However, in each of the first four years of growth, there was little difference in the relative amounts of dry mass partitioned to leaves, branches and stems. The physiological mechanisms controlling partitioning were apparently functioning similarly in the different species. Across a range of sites, even of the same nominal site index (a measure of the potential of the site to support a particular rate of growth), variables such as stocking rate had a marked effect on the distribution of dry mass (and nutrients) in an age-series of trees of E. regnans (Frederick et al. 1985). Site index is likely to have a considerable effect on the distribution of dry mass (Keyes and Grier 1981) and while this has not received any detailed attention in mature stands of eucalypts, studies with seedlings provide evidence that on fertile sites dry matter is allocated preferentially to leaf area development, whereas on non-fertile sites it is allocated preferentially to root development. Cromer and Jarvis (1990) observed a discrete change in the intercept but not in the slope of the allometric relationship between root mass and foliage mass of E. grandis seedlings as the plant nitrogen concentration changed: at high concentrations, plants allocated a high proportion of carbon to leaves. Leaves with a higher nitrogen content also developed a higher area per unit mass, enabling them potentially to intercept more light for rapid growth. The quantity of leaf area or leaf area index is potentially the major discriminant of production at a given site (Equation 5.2; Beadle and Inions 1990). Maximum values of leaf area index for managed eucalypt canopies exceed four square metres per square metre (Beadle and Mummery 1990), and can be as high as eight square metres per square metre at canopy closure in irrigated stands (White 1996). The inherent characteristics of a species and factors such as soil type and the supply of water and nutrients combine to produce a range of values of leaf area index across all types of eucalypt forest (0.8–6 m2 m–2, see Linder 1985; Beadle 1997). Seasonal water stress also has the capacity to cause fluctuations in leaf area index (Roberts et al. 1992).

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Indeed, eucalypts are observed to shed prematurely a large proportion of their canopies as a means of coping with a substantial shortfall in the supply of water needed to meet evaporative demand (Pook 1985). This can be seen as an active mechanism, over and above stomatal closure, for reducing transpiration. Foliar pathogens usually reduce the effective leaf area by killing leaf tissue and causing premature defoliation (see Chapter 9). There have also been studies showing that fungal pathogens infecting eucalypt leaves become a sink for photosynthate (Wall and Keane 1984). Thus, fungal pathogens may directly reduce photosynthetic capacity of leaves by damaging or killing green tissue, and they may have a further effect on plant productivity by redirecting sugar flows. Many species of eucalypts are heteroblastic, having substantially different juvenile and mature foliage. For example, the juvenile leaves of E. globulus ssp. globulus and E. globulus ssp. bicostata are dorsiventral and markedly glaucous, in contrast to the isobilateral, non-glaucous mature leaves. Glaucousness in juvenile leaves has been shown to confer resistance to pest and disease attack (Heather 1967; Edwards 1982). For example, there was a negative correlation between the susceptibility of leaves of E. globulus ssp. bicostata to the leaf spot pathogen Phaeophleospora epicoccoides (Cooke & Massee) Crous, F.A.Ferreira & B.Sutton (see Chapter 9) and the mass per unit area of an ether-soluble fraction from their glaucous coating (Heather 1967). In contrast, and in spite of their glaucous properties, susceptibility of juvenile foliage to Mycosphaerella leaf blotch of E. nitens, E. globulus ssp. globulus and E. globulus ssp. maidenii has restricted the planting of these species in South Africa (Lundquist 1987). The physiological basis of these differences in disease susceptibility between foliage types is not clear but may be related to differences in the chemical as well as the physical properties of the leaf surfaces.

5.4 Gas exchange and stomatal conductance In order to absorb carbon dioxide for photosynthesis, eucalypts, like all terrestrial plants, must expose a wet surface to a dry atmosphere. Transpiration of water is therefore an inevitable corollary to carbon dioxide assimilation. The resultant transfer of carbon dioxide and water vapour across an epidermis with a relatively

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impermeable cuticle occurs through stomata. The variable resistance (or its reciprocal, conductance) which the stomata impose on gas exchange between the atmosphere and the internal tissues of the leaf forms a basis for studying the effect on growth of environmental variables, including disease, and provides a useful link between the photosynthetic performance of the plant and its water relations. The size, density and distribution of stomata vary both within and between eucalypt species (Penfold and Willis 1961). Stomata commonly occur on both sides of the isobilateral adult leaves: the dorsiventral juvenile foliage can show the same pattern as the adult leaves although most stomata occur on the abaxial surface (see Pereira and Koslowski 1976). Besides providing a means of entry into the plant for pathogens, the humidity within the stomatal cavity, which is close to saturation at leaf temperature, is probably conducive to pathogen development. Stomata also provide a site of formation of pseudothecia (e.g. for Mycosphaerella spp.) and distribution of stomata can be reflected in distribution of pseudothecia (see Chapter 9). Further, some diseases have the potential to produce toxins which induce stomatal opening even in the dark (Turner and Graniti 1976). Stomata provide an entry court for Cylindrocladium pathogens of eucalypts (Bolland et al. 1985; Mohanan and Sharma 1986). Penetration by hyphae following inoculation of E. drepanophylla and E. microcorys by Cylindrocladium quinqueseptatum Boedijn & Reitsma occurred only via stomata (Bolland et al. 1985). Stomata are dominant in regulating the total amount of water transpired from stands of eucalypts because, forming tall forests, their canopies are closely coupled to atmospheric conditions (Jarvis 1985). The size of the canopy, the availability of water and the evaporative demand combine to determine rates of transpiration. Given an adequate supply of water, the stomatal conductance (i.e. stomatal opening) of eucalypts is observed to be high in the morning and then to decline during the day; under severe water stress the stomata remain closed throughout the light period (Roberts et al. 1992; White et al. 1994). While these responses can be interpreted as closure in response to increasing atmospheric deficits and/or increasing soil water stress, not all eucalypts exhibit

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this response. Colquhoun et al. (1984) studied several species of eucalypts growing on a range of sites in south-west Australia. Corymbia maculata, E. resinifera, E. saligna and E. wandoo regulated their stomata, so that closure occurred during the day in response to increasing water stress. In contrast, conductance of E. marginata and C. calophylla remained high throughout an extended period of study. Thus, some eucalypts appear to exert little control over water loss, a surprising situation for a plant growing in a dry environment. Several diseases of eucalypts can affect the functioning of stomata (and therefore transpiration), some directly by using the pore as a means of entry (e.g. Cylindrocladium spp.) or as a site of sporulation (e.g. Mycosphaerella spp.), others indirectly by interrupting the supply of water to the leaf (e.g. Armillaria, Ph. cinnamomi). Changes in stomatal conductance at midday following infection of E. marginata by Ph. cinnamomi was the best indicator for separating populations of diebackaffected and healthy trees (Crombie and Tippett 1990). In inoculated plants of E. sieberi, a species which is also susceptible to Ph. cinnamomi, changes in conductance occurred at a late and probably acute stage of infection when root conductivity had already dropped to 9% of that in the controls (Dawson and Weste 1984). Thus, even susceptible species may have a considerable capacity to buffer the effects of a disrupted water supply against changes in conductance. In a further study, conductance could not be used as either an indicator of ‘rural dieback’ (although this syndrome has not yet been ascribed to any root or vascular pathogen, see Chapter 17) or of its severity for three eucalypts growing in northern New South Wales (Crombie and Milburn 1988). Variation in response may well be linked to the apparent differences between species in the way stomatal conductance responds both to the atmospheric demand for water and its supply from the roots. The effect of disease on the parameters that define the photosynthetic processes of eucalypts has not been studied. In view of the scant attention given to disease-free individuals, it is too early even to speculate on the effect of disease other than to say that some parameters will be modified through stomatal conductance and water stress.

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5.5 Water relations Changes in plant water status strongly influence plant growth, particularly through their effect on leaf expansion and shoot and root extension (e.g. Bachelard 1986a). As water deficits intensify, stomatal closure and direct effects of stress on chloroplast processes reduce the rate of photosynthesis. While it is accepted that water moves along gradients of water potential (negative potential gradients) there is still argument as to whether water content or potential has the greater effect on physiological processes. In exploring the effect of diseases of eucalypts on the water relations of the host, it is important to distinguish between changes resulting from a primary event in pathogenesis and simply an expression of disturbed water balance (Ayres 1978). This requires a thorough knowledge of the water relations of healthy tissue, an area which has received considerable attention across a range of eucalypt species. The water content of a leaf is conveniently expressed relative to its saturated or turgid weight (Wt). Thus, the relative water content (R*) is given by: ( Wf – Wd ) R* = ------------------------( Wt – Wd )

(5.3)

where Wf and Wd are, respectively, the fresh and dry weights of the tissue. Water potential (ψ), is defined as the potential energy (joules) per unit volume of water (m3) with reference to pure water at zero potential. Thus: ( µw – µ ow ) ψ = ------------------------Vw

(5.4)

where µw and µow are, respectively, the chemical potentials of water in the tissue and of pure water, and Vw is the volume of a mole of water. Water in most biological systems has less potential energy than pure water. Consequently values of water potential are negative. As 1.0 newton equals 1.0 joule per metre, ψ is expressed in units of pressure, newtons per square metre (the pascal, Pa, or more commonly megapascal, MPa). A measurement of predawn leaf water potential is about equal to water potential at the soil–root interface as it can be assumed that the plant and soil

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will be in equilibrium with little or no net flux of water through the transpiration stream. As predawn water potential estimates the minimal level of stress, midday water potential estimates the maximum level of stress in the tree. The relationship between the water potential and water content of individual leaves, shoots and roots can be explored through the experimental determination of their pressure–volume (p–v) curve (Fig. 5.2). This separates the water potential of the organ in terms of a negative osmotic potential (π) arising from the presence of dissolved solutes in the cell, and a positive turgor potential (P) arising from the pressure exerted on the cells by their walls (i.e. ψ = π + P), and expresses them as a function of the volume of water in the system (R*). Secondly, the p–v curve provides a tool for comparing the strategy of plants (say species of eucalypts) in response to an imposed water stress. In response to the demand for water at the evaporating surface, leaf water potential becomes more negative (i.e. the leaf has a lower ψ). As soil water potential becomes more negative with drying, a simple strategy for maintaining the same flux of water through the plant is to further lower leaf water potential to maintain the potential gradient. To avoid any accompanying drop in turgor potential and consequently potential for growth, plants manipulate their osmotic and elastic properties to sustain positive turgor potential over a wider range of water stress. A much studied phenomenon is osmotic adjustment, the lowering of leaf osmostic potential under an imposed water stress. In a comparative study in a glasshouse, leaf osmostic potential of water-stressed seedlings of C. maculata, E. pilularis and E. sieberi was 0.23, 0.29 and 0.53 megapascals less (more negative), respectively, than those of seedlings maintained at field capacity (Bachelard 1986b). As corresponding reductions in water potential at zero turgor were about the same magnitude, the range of water potential associated with positive turgor potential increased likewise. Osmotic adjustment of seedlings of E. behriana, E. microcarpa and E. polyanthemos subjected to two drought cycles also corresponded closely to the observed change in water potential at the wilting point (Myers and Neales 1986).

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A pressure–volume curve for a shoot of Eucalyptus viminalis. The broken line represents the relationship between the reciprocal of osmotic potential (π) when the turgor potential (P) is zero (i.e. at R* < C). The intercept on the y axis, A at R* = 1.0, is 1/π at full turgor; the intercept B on the x axis is the apoplastic water content (R*a). Both these parameters may change under water stress (see text; after Ladiges 1975).

Several mechanisms, acting together or in isolation, can be activated by plants to ensure a desired change in osmotic potential. Solutes can simply be accumulated in cells with no accompanying change in the geometry or physical properties of the tissue. Reducing the size of cells, particularly in developing tissue, may also reduce leaf osmostic potential, as will an increase in cell wall elasticity or simply a change in tissue hydration. There is evidence that eucalypts can utilise all of these strategies in response to water stress. In the study referred to above, Bachelard (1986b) concluded that solute accumulation was possibly the major cause of osmotic adjustment as the decrease in tissue hydration (Wt : Wd ratio) in the water-stressed seedlings was small (cell size was not measured). In a field experiment, however, the differences between osmostic potential of leaves of irrigated and rainfed E. globulus at the end of the dry season was largely a result of a decrease in cell size of the leaves of the

rainfed trees (Correia et al. 1989). The rainfed trees also had a higher apoplastic water content (R*a, Fig. 5.2) than the irrigated (and irrigated and fertilised) trees. Although apoplastic water content is estimated with limited accuracy from p–v curves, the water holding capacity of cell wall materials, which is measured as apoplastic water content is likely to increase as Wt : Wd decreases. In seedlings of C. maculata, E. pilularis and E. sieberi, apoplastic water content decreased in leaves under water stress (Bachelard 1986b) and while apoplastic water content of the most drought-resistant population of E. viminalis was the greatest, there was no obvious relationship between apoplastic water content and Wt : Wd among the populations studied (Ladiges 1975). Ladiges concluded that apoplastic water content was not a simple function of the amount of cell wall materials but was more related to cell wall composition. Tissue elasticity is expressed as bulk elastic modulus (ε), the change in turgor potential (∆P) for a given

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change in symplastic water content (∆R*). A decrease in bulk elastic modulus in response to a treatment indicates an increase in tissue elasticity. Evidence to date for a consistent pattern of elastic adjustment in eucalypts to water stress is inconclusive. Juvenile leaves of E. globulus that expanded during the dry season had less elastic tissues than those that expanded in the wetter part of the year (Correia et al. 1989). Water stress had no effect on bulk elastic modulus of C. maculata and E. pilularis and bulk elastic modulus increased rather than decreased in E. sieberi (Bachelard 1986b). In an experiment that compared irrigated and rainfed stands of E. globulus and E. nitens, treatment differences in bulk elastic modulus were less important than interspecific differences—bulk elastic modulus of E. globulus was lower than that of E. nitens (White et al. 1996).

has to reach an acute level before abrupt reductions in water content and water potential are experienced (Dawson and Weste 1984).

In linking observed changes in water relations parameters to strategies adopted by eucalypts in their response to water stress, it is reasonable to take the view that the end result ensures that turgor is maintained to lower values of water potential or relative water content compared to well-watered controls. Is there any evidence that diseases which interrupt the supply of water to the shoots elicit a similar response and how is this expressed?

5.6 Conclusion

As yet there are few data available to evaluate changes to the water relations of diseased eucalypts in this detail. Water potential at dawn was lower in areas of forest affected by dieback caused by Ph. cinnamomi than in healthy forest (Crombie and Tippett 1990) but there were no differences in dawn water potential of healthy trees and those affected by rural dieback (Crombie and Milburn 1988). Low relative water contents in the phloem of E. marginata tend to inhibit the growth of Ph. cinnamomi in the tissues of trees on drier sites (Tippett et al. 1989) or in unthinned compared to thinned stands (Bunny et al. 1995), and the extent of lesion development caused by Ph. cinnamomi was less in seedlings and young saplings of E. sieberi subjected to water stress (Smith and Marks 1986). Thus, while water content and water potential are correlated with the spread of Ph. cinnamomi through the tree, they may be poor indicators of any physiological stress directly attributable to the fungus. It may well be that other variables such as stomatal closure and leaf shedding offset the development of water stress as the disease develops (Crombie et al. 1987) or that the disease 68

Similar problems of interpretation have been encountered when diseases apparently causing characteristic changes in the water relations of plants have been investigated (Duniway 1975; Ayres 1978). For disease caused by Ph. cinnamomi, manifestation in terms of a measurable change in plant water status may be linked to reduced transport of cytokinin from the root system (Cahill et al. 1986). Small changes in the rate of synthesis and transport of cytokinin and abscisic acid from the roots into the transpiration stream have been implicated in the control of stomatal conductance even above the wilting point (Blackman and Davies 1985; Zhang and Davies 1990).

While the physiology of healthy eucalypts has been studied extensively, there has been little research on the effect of eucalypt diseases on host physiology. In most cases, the state of knowledge of the diseases is still rudimentary even at the level of identification of causal organisms and study of their basic pathology. There has also been little study on the effect of altered states of host physiology on the susceptibility of eucalypts to disease. There is a general appreciation that seedlings growing under stress may be more heavily infected by certain diseases, especially in the humid tropics, but it is not known whether this is an effect of environment on the pathogen or on the susceptibility of the host. Only in the case of root rot of eucalypts caused by Ph. cinnamomi have there been any detailed physiological studies, and even then it has been difficult to distinguish between subtle direct physiological effects of the pathogen on the host and gross effects associated with massive damage to root systems. The most revealing work was the demonstration that the water content of plant tissues affected the rate of growth of Ph. cinnamomi in the tissues (Tippett et al. 1989).

5.7 References Ayres, P.G. (1978). Water relations of diseased plants. In Water Deficits and Plant Growth. Vol V. (Ed. T.T. Koslowski) pp. 1–60. (Academic Press: New York.) Bachelard, E.P. (1986a). Effects of soil moisture stress on the growth of seedlings of three eucalypt species. II. Growth effects. Australian Forest Research 16, 51–61.

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Bachelard, E.P. (1986b). Effects of soil moisture stress on the growth of seedlings of three eucalypt species. III. Tissue–water relations. Australian Forest Research 16, 155–163. Beadle, C.L. (1997). Dynamics of leaf and canopy development. In Management of Soil, Water and Nutrients in Tropical Plantation Forests. (Eds E.K.S. Nambiar and A.G. Brown) pp. 169–212. (Australian Centre for International Agricultural Research: Canberra.) Beadle, C.L. and Inions, G. (1990). Limits to growth of eucalypts and their biology of production. In Prospects for Australian Forest Plantations. (Eds J. Dargavel and N. Semple) pp. 183–193. (Centre for Resource and Environmental Studies, Australian National University: Canberra.) Beadle, C.L. and Mummery, D.C. (1990). Stand growth and development of leaf area index in young plantations of Eucalyptus nitens at 2 × 2 m spacings. NZ Ministry of Forestry FRI Bull. No. 151, 254–257. (Forest Research Institute: Rotorua.) Beadle, C.L. and Turnbull, C.R.A. (1992). Comparative growth rates of eucalypts in native forest and plantation monoculture. In Growth and Water Use of Forest Plantations. (Eds I.R. Calder, R.L. Hall and P.G. Adlard) pp. 318–331. (Wiley: London.) Beadle, C.L., Honeysett, J.L., Turnbull, C.R.A. and White, D.A. (1995). Site limits to achieving genetic potential. In Eucalypt Plantations: Improving Fibre Yield and Quality. Proceedings of the CRCTHF–IUFRO Conference, Hobart, 19–24 February 1995. (Eds B.M. Potts, N.M.G. Borralho, J.B. Reid, R.N. Cromer, W.N. Tibbits and C.A. Raymond) pp. 325–330. (Cooperative Research Centre for Temperate Hardwood Forestry: Hobart.) Blackman, P.G. and Davies, W.J. (1985). Root to shoot communication in maize plants and the effect of soil drying. Journal of Experimental Botany 36, 39–48. Bolland, L., Tierney, J.W. and Tierney, B.J. (1985). Studies on leaf spot and shoot blight of Eucalyptus caused by Cylindrocladium quinqueseptatum. European Journal of Pathology 15, 385–397. Bunny, F.J., Crombie, D.S. and Williams, M.R. (1995). Growth of lesions of Phytophthora cinnamomi in stems and roots of jarrah (Eucalyptus marginata) in relation to rainfall and stand density in mediterranean forest of Western Australia. Canadian Journal of Forest Research 25, 961–969. Cahill, D.M., Weste, G.M. and Grant, B.R. (1986). Changes in cytokinin concentrations in xylem extrudate following infection of Eucalyptus marginata Donn ex Sm with Phytophthora cinnamomi Rands. Plant Physiology 81, 1103–1109. Campinhos, E. (1980). More wood of better quality through intensive silviculture with rapid-growth improved Brazilian Eucalyptus. Tappi 63, 145–147.

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Cannell, M.G.R., Sheppard, L.J. and Milne, R. (1988). Light use efficiency and woody biomass production of poplar and willow. Forestry 61, 125–136. Colquhoun, I.J., Ridge, R.W., Bell, D.T., Loneragan, W.A. and Kuo, J. (1984). Comparative studies in selected species of Eucalyptus used in rehabilitation of the northern jarrah forest, Western Australia. I. Patterns of xylem pressure potential and diffusive resistance of leaves. Australian Journal of Botany 32, 367–373. Correia, M.J., Torres, F. and Pereira, J.S. (1989). Water and nutrient supply regimes and the water relations of juvenile leaves of Eucalyptus globulus. Tree Physiology 5, 459–471. Crombie, D.S. and Milburn, J.A. (1988). Water relations of rural eucalypt dieback. Australian Journal of Botany 36, 233–237. Crombie, D.S. and Tippett, J.T. (1990). A comparison of water relations, visual symptoms and changes in stem girth for evaluating impact of Phytophthora cinnamomi dieback on Eucalyptus marginata. Canadian Journal of Forest Research 20, 233–240. Crombie, D.S., Tippett, J.T. and Gorddard, D.J. (1987). Water relations of root-pruned jarrah (Eucalyptus marginata Donn ex Smith) saplings. Australian Journal of Botany 35, 653–663. Cromer, R.N. and Jarvis, P.G. (1990). Growth and biomass partitioning in Eucalyptus grandis seedlings in response to nitrogen supply. Australian Journal of Plant Physiology 17, 503–515. Cromer, R.N., Ryan, P.A. and Brown, D.M. (1990). Potential for eucalypt plantations in subtropical to tropical climate zones in north-eastern Australia. In Prospects for Australian Forest Plantations. (Eds J. Dargavel and N. Semple) p. 441. (Australian National University: Canberra.) Davison, E.M. and Tay, F.C.S. (1988). Annual increment of Eucalyptus marginata trees on sites infested with Phytophthora cinnamomi. Australian Journal of Botany 36, 101–106. Dawson, P. and Weste, G. (1984). Impact of root infection by Phytophthora cinnamomi on the water relations of two Eucalyptus species that differ in susceptibility. Phytopathology 74, 486–90. Duniway, J.M. (1975). Water relations in safflower during wilting induced by Phytophthora root rot. Phytopathology 65, 886–891. Edwards, P.B. (1982). Do waxes on juvenile Eucalytpus leaves provide protection from grazing insects? Australian Journal of Ecology 7, 347–352. Farrar, J.F. (1993). Carbon partitioning. In Photosynthesis and Production in a Changing Environment: A Field and Laboratory Manual. (Eds D.O. Hall, J.M.O. Scurlock, H.R. Bolhàr-Nordenkampf, R.C. Leegood and S.P. Long) pp. 232–246. (Chapman and Hall: London.) Frederick, D.J., Madgwick, H.A.I., Jurgensen, M.F. and Oliver, G.R. (1985). Dry matter content and nutrient distribution in an age series of Eucalyptus regnans in

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New Zealand. New Zealand Journal of Forestry Science 15, 158–179. Gasana, J.K. (1983). Site factors limiting growth of Maiden’s gum (Eucalyptus globulus Labill. subsp. maidenii [F. Muell.] Kirkpatr.) in Rwanda. PhD Thesis. University of Idaho, Moscow, Idaho. Heather, W.A. (1967). Leaf characteristics of Eucalytpus bicostata Maiden et al. seedlings affecting the deposition and germination of spores of Phaeoseptoria eucalypti (Hansf.) Walker. Australian Journal of Biological Sciences 20, 1155–1160. Keyes, M.R. and Grier, C.C. (1981). Above- and belowground net production in 40-year-old Douglas fir stands on low and high productivity sites. Canadian Journal of Forest Research 11, 599–605. Jarvis, P.G. (1985). Transpiration and assimilation of trees and agricultural crops: the ‘omega factor’. In Trees as Crop Plants. (Eds M.G.R. Cannell and J.E. Jackson) pp. 460–480. (Institute of Terrestrial Ecology: London.) Jarvis, P.G. and Leverenz, J. (1983). Productivity of temperate, deciduous, and evergreen forests. In Encyclopaedia of Plant Physiology: New series Vol. 12D (Eds O.L. Lange, P.S. Nobel, C.B. Osmond and H. Zeigler) pp. 233–280. (Springer-Verlag: Berlin.) Ladiges, P.Y. (1975). Some aspects of tissue water relations in three populations of Eucalyptus viminalis Labill. New Phytologist 75, 53–62. Linder, S. (1985). Potential and actual production of Australian forest stands. In Research for Forest Management. (Eds J.J. Landsberg and W. Parsons) pp. 11–35. (CSIRO: Melbourne.)

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Pereira, J.S. and Koslowski, T.T. (1976). Leaf anatomy and water relations of Eucalyptus camaldulensis and E. globulus seedlings. Canadian Journal of Botany 54, 2868–2880. Pook, E. (1985). Canopy dynamics of Eucalyptus maculata Hook 3. Effects of drought. Australian Journal of Botany 33, 65–79. Roberts, J.M., Rosier, P.T.W. and Srinivasa Murthy, K.V. (1992). Physiological studies in young Eucalyptus stands in Southern India and their use in estimating transpiration. In Growth and Water Use of Forest Plantations. (Eds I.R. Calder, P.G. Adlard and R.L. Hall) pp. 226–243. (Wiley: London.) Sands, P.J. (1995). Modelling canopy production. II From single leaf photosynthetic parameters to daily canopy photosynthesis. Australian Journal of Plant Physiology 22, 603–614. Smith, I.W. and Marks, G.C. (1986). Effects of moisture stress in Eucalyptus sieberi on growth of lesions caused by Phytophthora cinnamomi. Australian Forest Research 16, 273–279. Tippett, J.T., McGrath, J.F. and Hill, T.C. (1989). Site and seasonal effects on susceptibility of Eucalyptus marginata to Phytophthora cinnamomi. Australian Journal of Botany 37, 481–490. Turnbull, C.R.A., Beadle, C.L., Bird, T. and McLeod, D.E. (1988). Volume production in intensively-managed eucalypt plantations. Appita Journal 41, 447–450. Turner, N.C. and Graniti, A. (1976). Stomatal responses to two almond cultivars to fusicoccin. Physiological Plant Pathology 9, 175–182.

Lundquist, J.E. (1987). A history of five forest diseases in South Africa. South African Forestry Journal 140, 51–59.

Wall, E. and Keane, P.J. (1984). Leaf spot of Eucalyptus caused by Aulographina eucalypti. Transactions of the British Mycological Society 82, 257–273.

Lundquist, J.E. and Parnell, R.C. (1987). Effects of Mycosphaerella leaf spot on growth of Eucalyptus nitens. Plant Disease 71, 1025–1029.

White, D.A. (1996). Physiological responses to drought of Eucalyptus globulus and Eucalyptus nitens in plantations. PhD Thesis. University of Tasmania, Hobart.

McMurtrie, R. and Wolf, L. (1983). Above- and belowground growth of forest stands: a carbon-budget model. Annals of Botany 52, 437–448. Mohanan, C. and Sharma, J.K. (1986). Epidemiology of Cylindrocladium diseases of Eucalyptus. In Eucalypts in India: Past, Present and Future. (Eds J.K. Sharma, C.T.S. Nair, S. Kedharnath and S. Kondas) pp. 388–394. (Kerala Forest Research Institute: Peechi.) Monteith, J.L. (1977). Climate and efficiency of crop production in Britain. Philosophical Transactions of the Royal Society of London, Series B. 281, 277–294. Myers, B.A. and Neales, T.F. (1986). Osmotic adjustment induced by drought, in seedlings of three Eucalyptus species. Australian Journal of Plant Physiology 13, 597–603. Penfold, A.R. and Willis, J.L. (1961). The Eucalypts. (Interscience: New York.)

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White, D.A., Beadle, C.L., Honeysett, J. and Worledge, D. (1994). Stomatal conductance of Eucalyptus globulus and E. nitens in irrigated and rainfed plantations. In Australian Tree Species Research in China. Proceedings No. 48. (Ed. A.G. Brown) pp. 56–63. (Australian Centre for International Agricultural Research, Canberra.) White, D.A., Beadle, C.L. and Worledge, D. (1996). Leaf water relations of Eucalyptus globulus ssp. globulus and E. nitens: seasonal, drought and species effects. Tree Physiology 16, 469–476. Zhang, J. and Davies, W.J. (1990). Changes in the concentration of ABA in xylem sap as a function of changing soil water status can account for changes in leaf conductance and growth. Plant, Cell and Environment 13, 277–285.

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Among the many fungi symbiotic with eucalypts, mutualistic mycorrhiza-forming species are at least as numerous as parasitic, disease-inducing species. Both mycorrhizal and pathogenic fungi raise mostly the same biological issues, including mode of transmission of inoculum, infection processes, spread and abundance in relation to environmental conditions, inherent host specificity of the fungi and fungal acquisition of carbon compounds from the host tissues. Both mutualistic and parasitic symbioses are investigated using the same methods (microscopy, isolation in pure culture, inoculation under controlled conditions, epidemiological analysis, probing with a growing range of chemical and biochemical techniques). This review of eucalypt mycorrhizas not only illustrates the parallels with parasitic systems but also focuses on issues peculiar to the symbiosis (i.e. the mechanisms and magnitude of beneficial effects of mycorrhizas on eucalypts, and the extent to which the mycorrhizal system might be manipulated and exploited in eucalypt forestry practice to maintain tree health and improve forest productivity).

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6.1 Introduction The presence of mycorrhiza in eucalypts was first suspected by van der Bijl (1917), reported formally by Samuel (1926) and confirmed by Smith and Pope (1934) who gave a good description of a typical ectomycorrhiza taken from eucalypt roots. Further reports followed (Fisch 1945; Rawlings 1951), but the first substantial study was that of Pryor (1956a, 1956b) who published a drawing of a eucalypt mycorrhiza and described an inoculation experiment using spores of Scleroderma cepa Pers. sens. lat. (including Scleroderma flavidum Ellis & Everh.) to induce mycorrhizas on Eucalyptus dives, E. macrorhyncha and E. pauciflora. Pryor’s paper stimulated the study of exotic plantings of eucalypts, and ectomycorrhizas were found on eucalypts in England, Scotland, Israel (Levisohn 1958; Neumann 1959), Italy (Rambelli 1962; Anderson 1966, 1967) and India (Bakshi 1966; Thapar et al. 1967).

Figure 6.1

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Meanwhile in Australia, Chilvers and Pryor (1965) surveyed 152 species of eucalypts representing many subsections within the genera Eucalyptus and Corymbia and found that all formed ectomycorrhizas. They illustrated and described in detail the anatomy of a typical eucalypt ectomycorrhiza. Differences in mycorrhizal fungal morphology (Ashton 1956; Anderson 1966, 1967; Chilvers 1968b) indicated that eucalypts had a range of fungal partners. Thus, by the end of the 1960s it was clear that the genera as a whole must be mycorrhizal, that many different fungi were involved and that the phenomenon was widespread. Since the mid 1970s studies of eucalypt mycorrhiza have burgeoned. Several hundred putative ectomycorrhizal fungal species have now been recognised (N.L. Bougher, pers. comm.) and Khan (1978) confirmed earlier indications (Asai 1934; Maeda 1954) that eucalypts can also form endomycorrhizas.

Morphology of eucalypt mycorrhizas: a) and b) simple unbranched ectomycorrhizas; c) and d) pyramidal ectomycorrhizas; e) nodular ectomycorrhizas; f) coralloid ectomycorrhizas; g) superficial and intermediate ectomycorrhizas; h) vesicular-arbuscular endomycorrhiza. Key: M, mycorrhiza; U, uninfected root; R, rhizomorph or hyphal strand; W, weft of loose hyphae.

M Y CORRHIZA S

Research has diversified to explore eucalypt mycorrhizal fine structure, infection processes, physiology of the nutrient flows, effects on plant growth, environmental conditions for mycorrhiza formation and utilisation of mycorrhizas in forestry practice. The consequent advances now provide a reasonably coherent view of the eucalypt mycorrhizas.

6.2 Structure of eucalypt mycorrhizas 6.2.1

Morphology

Ectomycorrhizas of eucalypts are characterised by fungal investment of the fine ultimate lateral roots. In their simplest form they comprise short, blunt ended, cylindrically swollen organs as showed in Figures 6.1a and 6.1b. The most common and typical form is the pyramidal ectomycorrhiza (Figs 6.1c and 6.1d), a compact racemose system having multiple branches at close intervals. Sometimes multiple ectomycorrhizal apices are bound together by fungal tissue into a compact nodular (Fig. 6.1e) or tuberculate (Dell et al. 1990b) form. At other times an irregular system of branching gives rise to a coralloid appearance (Fig. 6.1f). Ectomycorrhizas can be smooth and of similar colour to uninfected roots, or have a fungal covering which has a fluffy or bristly appearance, or be pigmented (e.g. yellow, pink, black). Rhizomorphs and hyphal strands extend from ectomycorrhizas along uninfected roots or radiate out into the surrounding soil (Figs 6.1c and 6.1d). Superficial ectomycorrhizas are roots of normal morphology heavily invested by loose wefts of fungal hyphae that range throughout the adjacent soil or litter (Fig. 6.1g). Endomycorrhizas are morphologically indistinguishable from uninfected roots and the use of stereomicroscopy is needed to detect the sparse external growth or occasional reproductive structures of the endomycorrhizal fungi (Fig. 6.1h).

6.2.2

Anatomy

6.2.2.1

Typical ectomycorrhizas

The anatomy of eucalypt mycorrhizas has been described by Chilvers and Pryor (1965), Chilvers (1968b), Ling-Lee (1976), Ling-Lee et al. (1977a, 1977b) and Massicote et al. (1987a, 1987b, 1987c), among others. A typical eucalypt ectomycorrhizal apex is depicted in longitudinal section in Figure 6.2a. The major feature is the presence of a dense

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sheath of fungal tissue that completely envelopes the root. In plan view (Fig. 6.2c) this tissue consists of branched and twisted hyphal elements compacted together. Monolayers of similar fungal tissue penetrate intercellularly between eucalypt epidermal cells forming the so-called Hartig net (Figs 6.2a, 6.2b, 6.2d and 6.2e). The forward-sloping, radially elongate shape of epidermal cells (Fig. 6.2a) is also a characteristic feature of ectomycorrhizas (epidermal cells of uninfected roots elongate axially, parallel to the direction of root growth). In transverse section (Fig. 6.2b), the single layer of slanting epidermal cells often appears as two layers, which can be a source of confusion. The mycorrhizal root cap (shaded tissue, Fig. 6.2a) is short and hemispherical and along the flanks of the mycorrhiza the cap cells persist as residues trapped within the fungal sheath (in uninfected roots they slough into the soil). The meristematic region is short relative to uninfected roots and cortical, endodermal and xylem cells differentiate quite close to the tip. Other finer structural features of eucalypt ectomycorrhizas have been revealed by electron microscopy (e.g. Chilvers 1968a; Seviour et al. 1978; Rose et al. 1981; Malajczuk et al. 1984; Massicote et al. 1987a, 1987b, 1987c). In particular, this has shown that root cap cells near the apex are invaded by intracellular hyphae (Fig. 6.2f) and those further back are reduced to small fragments. 6.2.2.2

Ectendomycorrhizas

In certain young, otherwise typical ectomycorrhizas, the fungus achieves limited intracellular penetration of epidermal or cortical cells (Chilvers 1968b) to form ectendomycorrhizas as shown in Figure 6.3a. These should not be confused with a more general phenomenon in ageing ectomycorrhizas where the fungi often invade moribund cortical cells. 6.2.2.3

Superficial and intermediate ectomycorrhizas

Superficial mycorrhizas (Ashton 1976; Dell and Malajczuk 1985; Malajczuk et al. 1987a) have the general anatomy of uninfected roots except for the presence of a fungal sheath surrounding them (Fig. 6.3b). Associated with superficial mycorrhizas are mycorrhizas having both a sheath and some Hartig net development, but lacking the radial epidermal cell elongation characteristic of typical ectomycorrhizas (Fig. 6.3c). Malajczuk et al. (1987a) included these within the superficial mycorrhizas, but since they depart significantly from the original 73

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Anatomy of eucalypt ectomycorrhizas: a) median longitudinal section of ectomycorrhizal apex; b) transverse section through Hartig net zone; c) plan view of fungal sheath tissue; d) tangential section through infected epidermis; e) labyrinthine branching of Hartig net hyphae; f) fungal penetration of root cap cells. Key: S, fungal sheath; H, intercellular hyphae of Hartig net; I, intracellular penetration by fungus; C, cap; E, epidermis; X, cortex; T, stele.

definition of superficial mycorrhizas (Clowes 1951), they are best termed ‘intermediate ectomycorrhizas’. 6.2.2.4

Endomycorrhizas

Eucalypt endomycorrhizas are of the vesiculararbuscular (VA) type as shown in Figure 6.3d (Khan 1978; Malajczuk et al. 1981; Zambolim and Barros 1982; Lapeyrie and Chilvers 1985). Except for the initial penetration hyphae, which grow directly through the epidermal cells or root hairs, the fungi are confined to the root cortex. Large diameter intercellular hyphae traverse the cortex and connect to various intracellular structures: hyphal coils, vesicles or arbuscules. Vesicles are large swollen hyphal compartments which tend to endure, full of cytoplasm and storage oils, for considerable periods. By contrast, the finely branched arbuscules are

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usually short lived, degenerating progressively backwards from the tips of the branches a few days after being formed. Ultrastructurally, VA endomycorrhizas of eucalypts are essentially identical to those of many other plants (Boudarga and Dexheimer 1988). In particular, young arbuscules do not breach but merely invaginate the host cell membrane and from the abundance of organelles in adjacent plant and fungal cytoplasm these clearly represent a region of intense physiological activity.

6.3 Functioning of mycorrhizas 6.3.1

The symbiotic interface

The basis of mycorrhizal symbioses is the reciprocal exchange of nutrients (Harley and Smith 1983). In VA endomycorrhizas, the major interface for such

M Y CORRHIZA S

Figure 6.3

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Anatomy of other eucalypt mycorrhizas: a) longitudinal section through outer layers of an ectendomycorrhiza; b) longitudinal section through outer layers of a superficial mycorrhiza; c) longitudinal section through outer layers of an intermediate mycorrhiza; d) longitudinal section through outer layers of a vesicular-arbuscular endomycorrhiza. Key: S, fungal sheath; H, intercellular hyphae of Hartig net; I, intracellular penetration by fungus; E, epidermis; X, cortex; A, arbuscule; V, vesicle.

exchange is the large surface area of the intracellular arbuscule, intimately invested by the cell membrane of the inner cortical cell (Boudarga and Dexheimer 1988). In typical ectomycorrhizas the major interface is the extensive Hartig net tissue penetrating between the elongated anticlinal walls of the epidermal cells (Ashford et al. 1989). The host–fungus interface in superficial mycorrhizas is restricted to the outer surface of epidermal cells, giving only 10% to 20% of the area of contact provided by the Hartig net in an equivalent length of typical ectomycorrhiza (Chilvers and Pryor 1965).

6.3.2

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Transfer of carbon compounds from plant to fungus

Mycorrhizal fungi act as powerful sinks for carbon (Harley and Smith 1983). Simple sugars secreted from the host cells are actively transported across the fungal membrane and inside the hyphae are converted to characteristic fungal compounds such as trehalose, mannitol, glycogen or lipids that cannot readily be reabsorbed by the plant cells (Harley and Smith 1983). The rapidity and magnitude of such carbon transfers in eucalypts was demonstrated in an experiment in which leaves of E. pilularis seedlings with Pisolithus tinctorius (Pers.) Coker & Couch ectomycorrhizas were fed radioactively labelled carbon dioxide and the roots monitored for the tracer shortly afterwards (Cairney et al. 1989). Radioactivity levels in mycorrhizas were

found to be about 20 times the levels in equivalent lengths of uninfected roots.

6.3.3

The fungus–soil interface

VA endomycorrhizal fungi contact the soil through a system of branching hyphae. Although this is somewhat sparse in appearance, individual hyphae can extend up to several centimetres into the soil, with the result that a much greater volume of soil is explored by the roots plus hyphae than by uninfected roots alone (Abbott and Robson 1985). Such hyphae are generally aseptate, generally of large diameter (4–10 µm) and efficiently transport nutrients taken up from the soil (Sanders and Tinker 1973; Sanders et al. 1977). Superficial, intermediate and some typical ectomycorrhizas are characteristically surrounded by dense wefts of hyphae and hyphal strands, which range through the soil and litter. Measurements of the ratio of total hyphal length to the length of ectomycorrhizal root have given values of 104 and even 105, one or two orders of magnitude greater than ratios for VA endomycorrhiza (Francis and Read 1994). This extensive contact with the surrounding environment is further enhanced by selective foraging behaviour, whereby hyphae grow sparsely through regions of low nutrient potential and densely through patches of nutrient-rich organic detritus (Bending and Read 1995).

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Some ectomycorrhizas have a relatively smooth sheath, without obvious hyphal outgrowths, which has led to discussion (e.g. Harley and Smith 1983) about how ectomycorrhizas lacking extraradical hyphal connections might function usefully. However, it seems likely that all ectomycorrhizas must have some such connections, if only to form sporocarps, and that these have somehow escaped detection. Eight distinct types of eucalypt ectomycorrhiza examined in detail, including three smooth sheathed types (Types 2, 4, 6), all exhibited extraradical connections (Chilvers 1968b). These latter had well-organised hyphal strands attached to the sheath, but only at the junction between mycorrhizal and uninfected root. Similar attachments can be seen in good quality stereomicrographs of fir and pine mycorrhizas (e.g. Zak 1971, figs 4d and 7; Zak 1973, figs 2a and 2b).

6.3.4

Phosphate accumulation

6.3.4.1

Effect of mycorrhizal infection on the phosphate status of the plant

Phosphorus is the key element in the mycorrhizal symbiosis (Chilvers and Harley 1980) and it is well documented that mycorrhizal infection enhances phosphate accumulation in eucalypts, with reports covering both ectomycorrhizas (Malajczuk et al. 1975; Mulligan and Patrick 1985; Heinrich and Patrick 1986; Soares 1986; Amorim 1988; Vieira and Peres 1988b) and VA endomycorrhizas (Zambolim et al. 1982; Lapeyrie and Chilvers 1985). Mycorrhizal infection produces the greatest increases in phosphate accumulation and stimulates eucalypt growth, when there is low availability of external phosphate (Malajczuk et al. 1975; Heinrich et al. 1988; Vieira and Peres 1988a; Soares et al. 1989; Bougher et al. 1990). This is important because levels of available phosphate are generally low in Australian soils (Wild 1958) and growth of eucalypts on native forest soils has been shown to be phosphate limited (Beadle 1954). 6.3.4.2

Phosphorus acquisition from the soil

Several mechanisms have been advanced to explain how mycorrhizal fungi acquire phosphorus from the soil more efficiently than uninfected roots: 1

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mycorrhizas are a much more powerful sink for phosphate than uninfected roots, permitting very low concentrations of available phosphate to be scavenged efficiently from the soil

3

fungi appear to be able to access forms of soil phosphorus not readily available to plant roots [e.g. in litter and humus-rich regions of soil, much of the phosphorus can occur in organic forms such as phytate (inositol hexaphosphate)].

Heinrich et al. (1988) compared utilisation of the insoluble iron–aluminium phytate by ectomycorrhizal and control seedlings of E. pilularis and found that infection with Pisolithus tinctorius greatly increased both phosphorus uptake (× 8–12) and dry weight gain (× 5–9) compared with controls. They suggested that surface phosphatase enzymes and/or fungal exudates could have released phosphorus from the phytate. High phosphatase activity has been detected in the outer sheath hyphae of E. fastigata ectomycorrhizas (Ling-Lee 1976). Alternatively, in more alkaline mineral soils, phosphorus can occur as insoluble tricalcium phosphate. Inoculated E. dumosa seedlings growing in calcareous soil developed a high incidence of VA endomycorrhiza and had higher inflow of phosphate (× 4) and dry weight gain (× 9) than uninoculated plants (Lapeyrie and Chilvers 1985). These authors suggested that the mycorrhizal fungi released soluble phosphate by secretion of acidifying hydrogen ions and/or liberation of oxalate which sequesters calcium, freeing some phosphate. Acidification does occur near mycorrhizas (Cairney and Ashford 1989, 1991) and oxalate secretion with consequent formation of calcium oxalate crystals around eucalypt mycorrhizal fungi in calcareous soils is well documented (e.g. Malajczuk and Cromack 1982; O’Connell et al. 1983; Lapeyrie et al. 1984b; Lapeyrie and Bruchet 1986; Lapeyrie et al. 1987; Lapeyrie 1988). 6.3.4.3

Phosphate storage by mycorrhizal fungi

Mycorrhizas are a powerful sink for phosphate because mycorrhizal fungi are able to concentrate phosphate within hyphal vacuoles in the form of polyphosphate, which under some conditions forms granules containing calcium, magnesium, potassium, sodium or organic cations such as glutamate (Ashford et al. 1975, 1986; Lapeyrie et al. 1984a; Chilvers et al. 1985; Moore et al. 1989; Orlovich et al. 1989, 1990; Orlovich and Ashford 1993).

M Y CORRHIZA S

This allows the fungi to store large quantities of this scarce nutrient element at very much higher concentration than could be tolerated in the normal inorganic phosphate pool in the protoplast (Harley and Smith 1983 suggest a one-thousand-fold difference). 6.3.4.4

Translocation of phosphorus to the plant

Active transfer of inorganic phosphate from mycorrhizal fungi to the host tissues occurs more rapidly in VA endomycorrhizas than in ectomycorrhizas. For example 58% of the absorbed radioactive phosphorus (32P) appeared in shoots of VA endomycorrhizal onions within four hours (Bowen et al. 1975) but over 80% of 32P remained in the fungal sheath of beech ectomycorrhizas after seven hours (Harley and Smith 1983). However, this large store of phosphate in the sheath means that the symbiotic supply of phosphate to the plant can be sustained for much longer periods in ectomycorrhizas (Harley and Smith 1983). Mycorrhizal infection of eucalypt seedlings under conditions of low external phosphate leads to parallel gains in shoot phosphorus and shoot dry weights, for both ectomycorrhizas (Heinrich and Patrick 1986; Vieira and Peres 1988b; Bougher et al. 1990) and VA endomycorrhizas (Lapeyrie and Chilvers 1985), indicating that shoot growth is controlled by the supply of phosphorus from the roots.

6.3.5

Acquisition of other plant nutrients

After phosphorus, nitrogen is the most important plant nutrient; indeed under conditions where the special ability of ectomycorrhizas to take up and store phosphorus has satisfied a tree’s current needs for this element, nitrogen may well become the limiting nutrient. There appears to be no specific mechanism for nitrogen storage in mycorrhizas, but there is good evidence for mycorrhizal-enhanced acquisition of this nutrient (e.g. Marschner and Dell 1994; Bending and Read 1995; Turnbull et al. 1995). Again the extensive system of foraging by extraradical mycelium must enhance acquisition of inorganic nitrogen in both endomycorrhizas and ectomycorrhizas. Of special interest is that some ectomycorrhizal fungi can access organic sources of nitrogen in litter residues, such as amino acids, peptides and proteins that cannot be utilised directly by plants (e.g Abuzinadah and Read 1989; Turnbull

OF

E UCA LYPTS

C H A P T E R

6

et al. 1995). Sulphur, calcium, magnesium, potassium, copper and zinc are also reported to be taken up by eucalypt seedlings with Pisolithus ectomycorrhiza in greater quantities than by uninoculated control seedlings (Amorim 1988; Vieira and Peres 1988a, 1988b; Soares et al. 1989). Studies on VA endomycorrhizal systems of other host genera indicate that these are capable of enhancing uptake of potassium, calcium, sulphur, iron and copper (Marschner and Dell 1994).

6.3.6

Other benefits to the plant host

Various other benefits to the plant host have been claimed for the mycorrhizal symbiosis, such as enhanced drought tolerance, screening out toxic ions and protection against pathogens. The main difficulty with studies of these claims has been to distinguish any direct effects from indirect effects operating through improved plant nutrition and growth. For example, there have been suggestions that infection by four different eucalypt ectomycorrhizal fungi stimulated highest seedling growth relative to uninfected controls (188%–221%) at the lowest of four soil water potentials (Bougher and Malajczuk 1990), which could have been due to relative differences in nutrient absorption and transport at low water potential rather than any effect on water movement per se. Mycorrhizal infection may enable some eucalypts to cope with high levels of soil calcium (Ladiges and Ashton 1977; Anderson and Ladiges 1982; Lapeyrie and Bruchet 1982), perhaps by immobilising calcium as calcium oxalate (Lapeyrie et al. 1984b), but it is uncertain whether the problem that the fungi alleviate is one of calcium toxicity per se, or calcium/alkaline immobilisation of phosphate and other essential nutrient ions (Lapeyrie and Chilvers 1985). Marx (1969) found indications that ectomycorrhizal fungi might provide some protection against root pathogens. The compact fungal sheath offers a barrier to pathogens of fine roots and certain ectomycorrhizal basidiomycetes from eucalypt forests have been shown to produce antibiotic substances (Pratt 1971). One type of basidiomycete ectomycorrhiza appeared to prevent infection by Phytophthora cinnamomi Rands but two other mycorrhizal types did not (Malajczuk and Sanfelieu 1984; Malajczuk 1988). On a whole-plant scale, a well-nourished plant with extensive root growth

77

D I S E A S E S

TA B LE 6 . 1

A N D

P A T H O G E N S

O F

E U C A L Y P T S

Fungi recorded as forming mycorrhizas on eucalypts

Fungi

CriterionA

LocationB

Reference(s)C

Ectomycorrhizal fungi Basidiomycota Abstoma sp.

FSe

NZ

21

Amanita gemmata (L.:Fr.) Gillet

F

Chi

30

Amanita grisea Massee & Rodway

FC

Aus

5

Amanita hiltonii D.A.Reid

F

Aus

37

Amanita murina Sacc.

F

Aus

37

Amanita muscaria (L.:Fr.) Lam.

FSn

Por, USA

43, 24

Amanita ochrophylla (Cooke & Massee) Cleland

F

Aus

17

Amanita pagetodes D.A.Reid

F

Aus

17

Amanita phalloides (Vaill.:Fr.) Link

F

Ita

9

Amanita preisii (Fr.) Sacc.

F

Aus

37

Amanita punctata (Cleland & Cheel) D.A.Reid

F

Aus

17

Amanita strobilacea (Cooke) McAlpine

F

Aus

17

Amanita subalbida Cleland

F

Aus

37

Amanita umbrinella E.-J.Gilbert & Cleland

F

Aus

36

Amanita xanthocephala (Berk.) D.A.Reid & R.N.Hilton

FSe

Aus

36, 50

Amanita xanthocephala (Berk.) D.A.Reid & R.N.Hilton (syn. Amanita austropulchella D.A.Reid)

F

Aus

17

Astraeus pteridis (Shear) Zeller

Sn

USA

24

Austroboletus lacunosus (Kuntze) T.W.May & A.E.Wood [syn. Austroboletus cookei (Sacc. & P.Syd.) Wolfe]

F

Aus

37

Austroboletus occidentalis Watling

F

Aus

37

Austrogautieria clelandii E.L.Stewart & Trappe

F

NZ

22

Austrogautieria manjimupana Trappe & E.L.Stewart

F

Aus

36

Boletellus ananas (M.A.Curtis) Murrill

F

Aus

36

Boletellus obscurecoccineus (Höhn.) Singer

F

Aus

37

Boletus edulis Bull.:Fr.

F

Ita

9

Boletus multicolor Cleland

F

Aus

36

Boletus sinapecruentus Cleland

F

Aus

37

Castoreum camphoratum Trappe & Malajczuk (nom. nud.) (N. Malajczuk, pers. comm.)

FC

Aus

42

Cortinarius archeri Berk.

F

Aus

12

Cortinarius australiensis (Cleland & Cheel.) E.Horak

F

Aus

37

Cortinarius basirubescens Cleland & J.R.Harris [= Dermocybe; May and Wood (1997)]

F

Aus

36

Cortinarius castaneofulvus Cleland

F

Aus

38

Cortinarius clelandii A.H.Sm. [= Dermocybe; May and Wood (1997)] (syn. Cortinarius subcinnamomeus Cleland)

FC

Aus

5

Cortinarius erythraeus Berk.

F

Aus

37

Cortinarius fragilipes Cleland

FC

Aus

5

Cortinarius globuliformis Bougher

FCSe

Aus

29

Cortinarius microarcheri Cleland

F

Aus

12

78

M Y CORRHIZA S

OF

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C H A P T E R

6

Fungi

CriterionA

LocationB

Reference(s)C

Cortinarius radicatus Cleland

FCSe

Aus

5

Cortinarius rotundisporus Cleland & Cheel

F

Aus

37

Cortinarius sinapicolor Cleland (syn. Cortinarius ochraceus Cleland)

FSe

Aus

5

Cortinarius subarcheri Cleland

F

Aus

37

Cystangium rodwayi (Massee) A.H.Sm.

F

Aus

37

Dermocybe austroveneta (Cleland) M.M.Moser & E.Horak (syn. Cortinarius austrovenetus Cleland)

FC

Aus

5

Dermocybe cinnabarina (Fr.) Wünsche (syn. Cortinarius cinnabarinus Fr.)

FSe

Aus, NZ

38, 21

Dermocybe cinnamomea (L.:Fr.) Wünsche [syn. Cortinarius cinnamomeus (L.:Fr.) Fr.]

F

Aus, NZ

38, 21

Dermocybe sanguinea (Wulfen:Fr.) Wünsche [syn. Cortinarius sanguineus (Wulfen:Fr.) Fr.]

F

Aus

36

Dermocybe splendida E.Horak

F

Aus

37

Descolea maculata Bougher

FCSe

Aus

28

Descomyces albellus (Massee & Rodway) Bougher & Castellano (syn. Hymenogaster albellus Massee & Rodway)

FSe

Aus, Arg, USA

47, 44, 24

Descomyces albellus (Massee & Rodway) Bougher & Castellano (syn. Hymenogaster zeylanicus Petch)

FSe

Aus

50

Descomyces albus (Klotzsch) Bougher & Castellano (syn. Hymenogaster maurus Maire)

F

NAfrica

47

Descomyces albus (Klotzsch) Bougher & Castellano [syn. Hymenogaster albus (Klotzsch) Berk. & Broome]

FCSe

Aus, Ger, NZ, UK, USA

37, 14, 20, 24

Gymnomyces socialis (Harkn.) Singer & A.H.Sm.

F

USA

47

Gyroporus cyanescens (Bull.:Fr.) Quél.

F

Aus

37

Hebeloma aminophilum R.N.Hilton & O.K.Mill.

F

Aus

37

Hebeloma coarctatum (Cooke & Massee) Pegler [syn. Tricholoma coarctatum FC (Cooke & Massee) Sacc.]

Aus

5

Hebeloma crustuliniforme (Bull.:Fr.) Quél.

Sn

USA

24

Hebeloma mesophaeum (Pers.) Quél.

FC

Aus

5

Hebeloma westraliense Bougher, Tommerup & Malajczuk

FSe

Aus

52, 53

Hydnangium archeri (Berk.) Rodway (syn. Octaviania archeri Berk.)

F

Aus

37

Hydnangium carneum Wallr.

FCSe

Aus, Mex, Per, NZ, UK, USA

37, 19, 24, 47

Hydnangium carneum Wallr. (syn. Hydnangium soederstroemii Lagerh.)

F

Chi

30

Hydnangium sublamellatum Bougher, Tommerup & Malajczuk

FSe

Aus

49

Hydnum repandum L.

FC

Aus

5

Hygrocybe coccinea (Schaeff.:Fr.) P.Kumm. [syn. Hygrophorus coccineus (Schaeff.:Fr.) Fr.]D

FC

Aus

5

Hymenogaster sp.

F

NZ, Ind

20, 45

Hypholoma fasciculare (Huds.:Fr.) P.Kumm. [syn. Naematoloma fasciculare (Huds.:Fr.) P.Karst.]

FCSe

Aus

5

Hysterangium sp.

F

NZ

20

Hysterangium affine Massee & Rodway

F

Aus

37

Hysterangium gardneri E.Fisch.

F

Aus

47

79

D I S E A S E S

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P A T H O G E N S

O F

E U C A L Y P T S

Fungi recorded as forming mycorrhizas on eucalypts (continued)

Fungi

CriterionA

LocationB

Reference(s)C

Hysterangium incarceratum Malençon

F

Ger, USA

14, 24

Hysterangium inflatum Rodway

FSe

Aus, NZ

5, 21

Inocybe sp.

F

NZ

21

Inocybe australiensis Cleland & Cheel

F

Aus

37

Inocybe australiensis Cleland & Cheel (syn. Inocybe granulosipes Cleland)

FC

Aus

5

Inocybe fibrillosibrunnea O.K.Mill. & R.N.Hilton

F

Aus

37 5

Inocybe fulvo-olivacea Cleland

FC

Aus

Inocybe petiginosa (Fr.:Fr.) Gillet

F

Ind

45

Laccaria fraterna (Sacc.) Pegler

FSe

Aus, NZ

48

Laccaria laccata (Scop.:Fr.) Cooke

FSeSn

Aus, NZ USA, Chi

36, 21, 24, 30 32, 26

Laccaria lateritia Malençon [syn. Laccaria ohiensis (Mont.) Singer]

FSe

Aus, Ind

Lactarius clarkeae Cleland

F

Aus

37

Lactarius eucalypti O.K.Mill. & R.N.Hilton

F

Aus

36 37

Leucopaxillus lilacinus Bougher

F

Aus

Lycoperdon gunnii Berk.

F

NZ

22

Lycoperdon perlatum Pers.

F

Ita, NZ

6, 3

Macrolepiota bonaeriensis (Speg.) Singer

F

Chi

30

Martellia sp.

F

Aus

36 24

Melanogaster intermedius (Bark.) Zeller & C.W.Dodge

Sn

USA

Mesophellia arenaria Berk.

FCSe

Aus, NZ

5, 21

Mesophellia labyrinthina Trappe, Castellano & Malajczuk

FC

Aus

39

Mesophellia trabalis Trappe, Castellano & Malajczuk

FC

Aus

9

Octaviania densa (Rodway) G.Cunn. [= Melanogaster; May and Wood (1997)] FC (syn. Hydnangium densum Rodway)

Aus

10

Octavianina tasmanica (Kalchbr.) Pegler & T.W.K.Young (syn. Hydnangium tasmanicum Kalchbr.)

NZ

22

F

Paxillus sp.

F

NZ

21

Paxillus infundibuliformis Cleland

F

Aus

8

Paxillus involutus (Batsch:Fr.) Fr.

Sn

Fra, USA

5, 24

Paxillus muelleri Berk.

F

Aus

36

Phellodon melaleucus (Swartz:Fr.) P.Karst.

F

Aus

37

Phlebopus marginatus (J.Drumm.) Watling & N.M.Greg. [syn. Phaeogyroporus portentosus (Berk. & Broome) McNabb]

F

Aus

2

Phylloporus hyperion (Cooke & Massee) Singer

F

Aus

37

Pisolithus microcarpus (Cooke & Massee) G.Cunn.

F

Aus

36

Pisolithus tinctorius (Pers.) Coker & Couch

FSeSn

Aus, Bra, Por, SAfrica, USA

1, 15, 43, 1, 13, 24

Protoglossum violaceum (Massee & Rodway) T.W.May [syn. Gymnoglossum violaceum (Massee & Rodway) G.Cunn.]

FC

Aus

5

Protoglossum viscidum (Massee & Rodway) T.W.May (syn. Hysterangium viscidum Massee & Rodway)

FSe

Aus

50

Protubera canescens G.W.Beaton & Malajczuk

F

Aus

36

Ramaria sp.

F

NZ

21

80

M Y CORRHIZA S

OF

E UCA LYPTS

C H A P T E R

6

Fungi

CriterionA

LocationB

Reference(s)C

Ramaria formosa (Pers.:Fr.) Quél.

FC

Aus

5

Ramaria ochraceo-salmonicolor (Cleland) Corner

F

Aus

36

Ramaria sinapicolor (Cleland) Corner

FSe

Aus

36

Rozites roseolilacina Bougher, Fuhrer & E.Horak

F

Aus

51

Rozites symeae Bougher, Fuhrer & E.Horak

F

Aus

1

Russula clelandii O.K.Mill. & R.N.Hilton

F

Aus

37

Russula cyanoxantha (Schaeff.) Fr.

F

Aus

38

Russula delica (Paulet) Fr.

F

Aus

46

Russula emetica (Schaeff.:Fr.) Gray

F

Aus

36 36

Russula flocktoniae Cleland & Cheel

F

Aus

Russula mariae Peck

F

Aus

36

Russula purpureoflava Cleland

FC

Aus

5

Scleroderma sp.

F

Bra, Chi

15, 30

Scleroderma albidum Pat. & Trab.

F

Col, USA

16, 24

Scleroderma areolatum Ehrenb.

F

Chi

45

Scleroderma bovista Fr.

F

NZ

3

Scleroderma cepa Pers. sens. lat. (including Scleroderma flavidum Ellis & Everh.)

FCSe

Aus, Ind, NZ

4, 8, 21

Scleroderma citrinum Pers. (syn. Scleroderma aurantium Pers.)

FSn

Fra, Chi

4, 30

Scleroderma geaster Fr.

F

USA

18

Scleroderma laeve Lloyd

Sn

USA

24

Scleroderma paradoxum G.W.Beaton

F

Aus

36 4

Scleroderma texense Berk.

Sn

Congo

Scleroderma verrucosum (Bull.) Pers.

FSe

Aus, Isr, NZ 26, 21

Setchelliogaster sp.

FSe

Aus

50

Setchelliogaster tenuipes (Setch.) Pouzar (syn. Secotium tenuipes Setch.)

F

Aus, USA, Arg, Chi

47, 44, 30

Thaxterogaster sp.

FSe

Aus

50

Tricholoma eucalypticum A.Pearson

F

Aus, SAfrica

37

Tricholoma pessundatum (Fr.:Fr.) Quél.

F

NZ

21

Tricholoma saponaceum (Fr.) P.Kumm.

FSe

NZ

21

Tricholoma tigrinum (Schaeff.) P.Kumm.

F

Ita

9

Xerocomus chrysenteron (Bull.) Quél.

F

Chi

30

Zelleromyces australiensis (Berk. & Broome) Pegler & T.W.K.Young (syn. Hydnangium australiense Berk. & Broome)

F

Aus

37

Zelleromyces daucinus G.W.Beaton, Pegler & T.W.K.Young

F

Aus

37

Zelleromyces malaiensis (Corner & Hawker) A.H.Sm. (syn. Arcangeliella malaiensis Corner & Hawker)

F

Aus

37

FSn

Aus

42

Cenococcum geophilum Fr.:Fr. [syn. Cenococcum graniforme (Sowerby) Ferd. FCSn & Winge]

Aus, Ita, USA

7, 9, 24

Labyrinthomyces varius (Rodway) Trappe

Aus

42

Ascomycota Boudiera tracheia (Gamundí) Dissing & T.Schumach.

FSe

81

D I S E A S E S

TA B LE 6 . 1

A N D

P A T H O G E N S

O F

E U C A L Y P T S

Fungi recorded as forming mycorrhizas on eucalypts (continued)

Fungi

CriterionA

LocationB

Reference(s)C

Lachnea vinoso-brunnea (Berk. & Broome) Sacc.

FSn

Aus

42 40, 42

Muciturbo reticulatus P.H.B.Talbot

FSe

Aus

Muciturbo truncatus P.H.B.Talbot

F

Aus

40

Muciturbo verrucosus P.H.B.Talbot

F

Aus

40

Nothojafnea cryptotricha Rifai

FSn

Aus

42

Peziza whitei (Gilkey) Trappe

FSe

Aus

42

Plicaria alveolata (Rodway) Rifai

FSn

Aus

42

Pulvinula tetraspora (Hansf.) Rifai

F

Aus

42

Reddellomyces westraliensis (G.W.Beaton & Malajczuk) Trappe, Castellano & F Malajczuk (syn. Labyrinthomyces westraliensis G.W.Beaton & Malajczuk)

Aus

37

Ruhlandiella berolinensis Henn. emen. Dissing & Korf [syn. Sphaerosoma mucidum (Rodway) Hansf.]

F

Aus

40

Sphaerosoma trispora McLennan & Cookson

F

Aus

40

FSe

Aus

41

Zygomycota Endogone aggregata P.A.Tandy Endogone tuberculosa Lloyd

FSe

Aus

41

Sclerogone eucalypti Warcup

FSe

Aus

41

VA endomycorrhizal fungi Zygomycota Acaulospora scrobiculata Trappe

FSn

Bra

54, 33

Gigaspora heterogama (T.H.Nicolson & Gerd.) Gerd. & Trappe

Sn

Bra

33

Gigaspora margarita W.N.Becker & I.R.Hall

Sn

NZ

27

Glomus claroideum N.C.Schenck & G.S.Sm.

Sn

Bra

25

Glomus clarum T.H.Nicolson & N.C.Schenck

FSn

Bra

54, 25

Glomus constrictum Trappe

Sn

Bra

25

Glomus fasciculatum (Thaxt.) Gerd. & Trappe emen. C.Walker & Koske

Sn

USA

23 25

Glomus intraradices N.C.Schenck & G.S.Sm.

Sn

Bra

Glomus macrocarpum Tul. & C.Tul.

Sn

Bra

25

Glomus monosporum Gerd. & Trappe

Sn

Bra

25

A

Criterion: F, fruit body association with trees; C, connections traced between mycorrhiza and fruit bodies; S, synthesised (Se— eucalypt fungus; Sn—not eucalypt fungus). Location: Aus, Australia; Arg, Argentina; Bra, Brazil; Chi, Chile; Col, Columbia; Fra, France; Ger, Germany; Ind, India; Isr, Israel; Ita, Italy; Mex, Mexico; NAfrica, North Africa; NZ, New Zealand; Per, Peru; Por, Portugal; SAfrica, South Africa; UK, United Kingdom; USA, United States of America. C Reference(s): 1, Smith and Pope (1934); 2, Fisch (1945); 3, Rawlings (1951); 4, Pryor (1956a); 5, Ashton (1956); 6, Rambelli (1962); 7, Trappe (1964) cited in Chilvers (1968b); 8, Bakshi (1966); 9, Anderson (1966); 10, Chilvers (1968b); 11, Chilvers (1973); 12, 13, 14 Moser (1968), Marx (1977), Gross (1980) all cited in Malajczuk et al. (1982); 15, Barros et al. (1978); 16, Guzman and Varela cited in Zambolim (1990); 17, Reid (1980); 18, Rose et al. (1981); 19, Chu-Chou and Grace (1981a); 20, Chu-Chou and Grace (1981b); 21, Chu-Chou and Grace (1982); 22, Chu-Chou and Grace (1983); 23, Malajczuk et al. (1981); 24, Malajczuk et al. (1982); 25, Zambolim et al. (1982); 26, Raman (1985); 27, Schoeneberger (1985); 28, Bougher and Malajczuk (1985); 29, Bougher and Malajczuk (1986); 30, Garrido (1986); 31, Malajczuk et al. (1987a); 32, Kope and Warcup (1986); 33, Amorim (1988); 34, Garbaye et al. (1988); 35, Lapeyrie (1988); 36, Gardner and Malajczuk (1988); 37, Hilton et al. (1989); 38, Shepherd and Totterdell (1988); 39, Dell et al. (1990a); 40, Warcup and Talbot (1989); 41, Warcup (1990a); 42, Warcup (1990b); 43, N. de Azevedo (pers. comm.); 44, J. Wright (pers. comm.); 45, K. Ingold and P. Mason (pers. comm.); 46, Burgess and Malajczuk (1989); 47, Castellano and Trappe (1990); 48, Tommerup et al. (1991); 49, Bougher et al. (1993); 50, Burgess et al. (1993); 51, Bougher et al. (1994); 52, Bougher et al. (1991); 53, Thomson et al. (1994); 54, Estrada et al. (1993). D Australian records are either Hygrocybe kandora Grgur. & A.M.Young or Hygrocybe miniata (Fr.:Fr.) Kummer (Young and Wood 1997). B

82

M Y CORRHIZA S

could be expected to show greater tolerance of fine root infections anyway.

6.4 The fungal partners of eucalypts 6.4.1

Ectomycorrhizal fungi

Table 6.1 lists over 150 fungal species in over 60 genera believed to be ectomycorrhizal with eucalypts. Most (89%) of these are Basidiomycota; a few are Ascomycota (9%) or Zygomycota (2%). Among the Basidiomycota, most are agarics (e.g. Amanita, Boletellus, Boletus, Cortinarius, Inocybe, Lactarius, Paxillus, Russula, Tricholoma). A substantial minority (23%) of species form hypogeous sporocarps within the genera Arcangeliella, Austrogautieria, Castoreum, Gymnomyces, Hydnangium, Hymenangium, Hymenogaster, Hysterangium, Mesophellia, Octaviania, Protubera, Secotium, Setchelliogaster, Thaxterogaster and Zelleromyces. A further small but significant group are epigeous gasteromycetes in the genera Pisolithus and Scleroderma. The Ascomycota, all Discomycetes, fall within the order Pezizales (Warcup 1990b), except Cenococcum which is believed to be the imperfect stage of Elaphomyces (Elaphomycetales) (Trappe 1971). The Zygomycota are confined to the Endogonales (Warcup 1990a). Many of the ectomycorrhizal fungi, including species of Amanita, Endogone, Hydnangium, Hymenogaster, Labyrinthomyces, Laccaria, Pisolithus and Scleroderma, form typical branching ectomycorrhizas complete with Hartig net and elongate epidermal cells (Malajczuk et al. 1982; Warcup 1990a, 1990b). Cenococcum also forms anatomically typical ectomycorrhizas, but these are mainly limited to single unbranched apices (Chilvers 1968b). Some other fungi, including species of Cortinarius, Hysterangium and Mesophellia, form superficial or intermediate ectomycorrhizas (Malajczuk et al. 1987a; Dell et al. 1990a). While a compilation such as Table 6.1 provides a generally reliable overview of the diversity of eucalypt ectomycorrhizal fungi, some caution is required when interpreting details because the original data of association and taxonomy vary in reliability. Thus, there are three complementary kinds of evidence that a fungus is mycorrhizal on eucalypts:

OF

E UCA LYPTS

C H A P T E R

6

1

observed frequent association of sporocarps with eucalypt trees in the field (Hilton et al. 1989)

2

detection of hyphal connections between sporocarps and mycorrhizal roots (e.g. Ashton 1956; Chilvers 1968b; method of Agerer 1991)

3

experimental synthesis of mycorrhizas following inoculation of eucalypt seedling roots with spores or pure cultures of the fungus taken from sporocarps (e.g. Mullette 1976; Chilvers and Gust 1982b; Chilvers et al. 1986; Grenville et al. 1986; Malajczuk and Hartney 1986; Bailey and Peterson 1988; Battistelli et al. 1989; Boudarga et al. 1990; Brundrett et al. 1996).

Ideally all three kinds of evidence should be collected, since final reisolation of the fungus from synthesised mycorrhizas would be equivalent to satisfying Koch’s rules of proof of causation as applied to pathogens. However, this has been achieved for only eight associates of eucalypts (i.e. FCSe in column 2, Table 6.1). About one-quarter of the fungi satisfy two criteria, but most records (column 2, Table 6.1) are based solely on the criterion of field association. Fortunately, this has proved to be a reasonably reliable indicator where the fungus belongs to a genus already known to contain mycorrhiza-forming species (Hilton et al. 1989). Identification problems result from the incomplete characterisation of Australian mycorrhizal fungi, of which perhaps 90% remain to be described (Bougher 1995), and the current fluid state of their taxonomy due to studies of new species and re-examination of old species (Bougher et al. 1993; Castellano and Bougher 1994). For example, two species originally classified as Octaviania have recently been transferred to Hydnangium, while one Hydnangium species has been reclassified in Octaviania (Table 6.1). Laccaria sporocarps associated with eucalypts have usually been identified as Laccaria laccata (Scop.:Fr.) Cooke or Laccaria lateritia Malençon [syn. Laccaria ohiensis (Mont.) Singer] but Tommerup et al. (1991) suggest that most are Laccaria fraterna (Sacc.) Pegler.

6.4.2

Patterns of specificity of ectomycorrhizal fungi

Within the genera Eucalyptus and Corymbia there is no evidence of host specificity, an ectomycorrhizal mycorrhizal fungus from one eucalypt appearing

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capable of forming mycorrhizas with any other species of eucalypt providing the conditions are suitable (Chilvers 1973; Malajczuk et al. 1982). This is in marked contrast to the situation with parasitic fungi which are often restricted to host species within a particular eucalypt subgenus (Burdon and Chilvers 1974), but is consistent with experience of ectomycorrhizal fungi in the Northern Hemisphere (Harley and Smith 1983). At the other extreme, none of the fungi from eucalypts appears able to infect the exotic Monterey pine, Pinus radiata D.Don, which is grown extensively in plantations in Australia. Many of these plantings have been made in clearings within native woodland and at the boundaries between eucalypts and pines the native eucalypt ectomycorrhizal macrofungi abruptly give way to exotic mycorrhizal species such as Amanita muscaria (L.:Fr.) Lam., Hebeloma hiemale Bres., Hebeloma mesophaeum (Pers.) Quél., Inocybe patouillardii Bres., Lactarius deliciosus (L.:Fr.) Gray, Rhizopogon luteolus Fr., Rhizopogon roseolus (Corda) Th.Fr., Suillus granulatus (L.:Fr.) Roussel, Suillus luteus (L.:Fr.) Roussel, Thelephora terrestris Ehrh.:Fr. and Tricholoma terreum (Schaeff.:Fr.) P.Kumm. (Lamb and Richards 1970; Shepherd and Totterdell 1988). During early attempts to grow plantations of Pinus radiata in new areas, young pines in nursery lots failed to form mycorrhizas and showed signs of serious nutrient deficiency until they were inoculated with pine litter from established pines elsewhere, which resulted in mycorrhiza formation and a dramatic resumption of growth (Kessel and Stoate 1936). This indicates that the pines could not make use of the airborne inoculum emanating from nearby eucalypt stands or the remnant mycelial inoculum of eucalypt forest cleared to make way for the pines. Using a method of pure culture synthesis, Malajczuk et al. (1982) confirmed that eucalypt fungi such as Hydnangium carneum Wallr. and Descomyces albellus (Massee & Rodway) Bougher & Castellano (syn. Hymenogaster albellus Massee & Rodway) would not infect Pinus radiata and conversely that several pine fungi would not form mycorrhizas with eucalypts. However, a few fungi known to have a broad host range covering gymnosperms and angiosperms in the Northern Hemisphere were successfully inoculated on to eucalypts (e.g. Amanita muscaria, Cenococcum geophilum Fr.:Fr., Hebeloma crustuliniforme (Bull.:Fr.) Quél. and Pisolithus

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tinctorius. The last-named is something of a special case. Pisolithus tinctorius occurs widely in association with native gymnosperms and some broadleaf trees in the Northern Hemisphere. In Australia it is widespread among native eucalypts (Shepherd and Totterdell 1988) but is only occasionally reported from exotic pines (Lamb and Richards 1970). In cross-inoculation experiments, an isolate from eucalypts did not form mycorrhizas with pines (Chilvers 1973); different pine isolates inoculated on to eucalypts have sometimes formed mycorrhizas (Malajczuk et al. 1982) and at other times formed mycorrhizas poorly or not at all (Malajczuk et al. 1990; Lei et al. 1990; Burgess et al. 1995). Since there is not only variation in symbiotic behaviour but also considerable structural and physiological variation among isolates (Burgess et al. 1994), it seems likely that the pine and eucalypt isolates of Pisolithus tinctorius represent distinct taxa. There has been discussion of possible host defence reactions to incompatible ectomycorrhizal fungi involving production of polyphenolic compounds, by analogy with defence against plant parasitic fungi, but these compounds are common in successful mycorrhizal infections and uninfected roots, not just in unsuccessful interactions (e.g. Ling-Lee et al. 1977a; Malajczuk et al. 1982). A more recent view is that compatibility depends primarily on the fungus exhibiting a positive chemotropism towards a root and on other positive responses to and by the target host cells (Jacobs et al. 1989; Horan and Chilvers 1990; Lei et al. 1989, 1990; Lapeyrie et al. 1990; Peterson and Bonfante 1994).

6.4.3

Ectomycorrhizal fungi on exotic eucalypts outside Australia

Of about 140 named species of ectomycorrhizal fungi listed as associated with eucalypts in the field (Table 6.1), 104 have been reported from Australia and 37 from outside Australia. Among fungal species from exotic eucalypts, 15 coincide with Australian mycoflora and 22 do not. New Zealand records are currently the most comprehensive. Chu-Chou and Grace (1981a, 1981b, 1982, 1983) distinguished 23 fungi associated with exotic eucalypts in New Zealand and confirmed the mycorrhizal status of most of these by inoculation experiments. Of the 17 fungi they were able to identify to species level, over half (10) were common to Australia; of the

M Y CORRHIZA S

six identified only to genus level, five were from mycorrhizal genera well represented on eucalypts in Australia (Hymenogaster, Hysterangium, Inocybe, Paxillus, Ramaria). This number and coincidence of fungal species probably reflects the relative proximity of New Zealand, just 2000 kilometres downwind from the eucalypt-clad Australian east coast. However, eucalypts also share some mycorrhizal fungi with Nothofagus [e.g. Hydnangium carneum, Descomyces albus (Klotzsch) Bougher & Castellano [syn. Hymenangium album Klotzsch; Hymenogaster albus (Klotzsch) Berk. & Broome] (Chu-Chou and Grace 1983) and it has been suggested from studies on the shared mycorrhizal genera Descolea and Rozites that eucalypts might have originally acquired some mycorrhizal fungi from that ancient Gondwanan genus (Bougher and Malajczuk 1985; Bougher et al. 1994). Accordingly some eucalypt ectomycorrhizal fungi could be native to both countries. Elsewhere in the world the proportion of shared species appears less. Thus, South America and Europe, each with 11 named species of fungi associated with eucalypts, have only four species each in common with Australia (Table 6.1). At this point the quality of data becomes crucial. It is not uncommon for fungi found under exotic eucalypts in the Northern Hemisphere to be described anew, only to be reduced to synonymy when subsequently compared with Australian species [e.g. three Hysterangium species described from eucalypts in France, Equador and the United States of America (USA) are synonyms of Hysterangium inflatum Rodway] (Castellano and Trappe 1990). The species most commonly reported outside Australia are Hydnangium carneum, Descomyces albus (syn. Hymenangium album; Hymenogaster albus), Descomyces albellus (syn. Hymenogaster albellus), Setchelliogaster tenuipes (Setch.) Pouzar (syn. Secotium tenuipes Setch.), Cenococcum geophilum, Laccaria laccata, Laccaria lateritia (syn. Laccaria ohiensis), Pisolithus tinctorius, Scleroderma cepa and Scleroderma verrucosum (Bull.) Pers. All of these are also found within Australia. The first four are almost certainly native Australian fungi which have spread around the world with their specific eucalypt hosts (Malajczuk et al. 1982; Hilton et al. 1989). This is remarkable because no airborne spores have been reported for these hypogean fungi and

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they are not known to have been deliberately introduced. Cenococcum geophilum, Pisolithus tinctorius and some Laccaria and Scleroderma species are generally viewed as cosmopolitan mycorrhizal fungi with broad host ranges (e.g. Trappe 1971; Marx 1977; Malajczuk et al. 1982), which might suggest that eucalypts could readily ‘pick up’ these ectomycorrhizal fungi anywhere in the world. However, there are reasons to doubt this. A consistent feeling among the mycorrhizal workers in other countries with whom I have communicated is that the fungi which they see fruiting with exotic eucalypts are ‘not native’ to their regions. Thus, Laccaria lateritia (syn. Laccaria ohiensis) in India seemed to be associated there specifically with eucalypts (Raman 1985; K. Ingold, pers. comm.) and Pisolithus tinctorius appears to be especially widespread and prominent on eucalypts in South America (Zambolim 1990). Taxonomic uncertainties and the evidence of isolate differences previously alluded to, allow the possibility that these ‘cosmopolitan’ fungi exist as distinct geographical taxa, with some from Australia showing field specificity for eucalypts. The only instances where undeniably local fungi appear to have become associated with exotic eucalypts in the field are reports of Amanita muscaria in Portugal (N. de Azevedo, pers. comm.), Xerocomus chrysenteron (Bull.) Quél. in Chile (Garrido 1986) and Boletus edulis Bull.:Fr. and Amanita phalloides (Vaill.:Fr.) Link in Italy (Anderson 1966). Interestingly, exotic Amanita muscaria, now widely established on Pinus radiata in south-east Australia, has spread to Nothofagus in Tasmania (Bougher 1995), but has not yet been reported on native eucalypts. A latitudinal pattern is evident in exotic eucalypt mycorrhizal fungi. Hydnangium, Hymenangium, Hymenogaster and Secotium species have been reported most commonly in more temperate regions (e.g. Argentina, Chile, Peru, Germany, the United Kingdom, the USA) (Table 6.1). Pisolithus tinctorius and Scleroderma species are the major fungi reported from hotter climates, for example India and Brazil (Thapar et al. 1967; Marx 1977; Yokomizo 1981; Schwan 1984; L. Zambolim and R.C.G. Borges, pers. comm.; Zambolim 1990; V.L. de Oliveira, pers. comm.; G.D. Sharma, pers. comm.).

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6.4.4

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Endomycorrhizal fungi

The fungal species from the genera Acaulospora, Gigaspora and Glomus shown to form VA endomycorrhizas with eucalypts are all from one order, the Glomales. No VA endomycorrhizal fungus has been cultured axenically, and so in most cases spores from defined cultures on roots of graminaceous or herbaceous plants have been used as inoculum on pot-grown eucalypt seedlings (Malajczuk et al. 1981; Zambolim et al. 1982; Schoeneberger 1985). VA endomycorrhizal fungi generally exhibit low host specificity (Harley and Smith 1983) and there is no evidence of a eucalyptspecific species. Rather it seems that endomycorrhizal fungi, which normally persist by cyclical infection of herbs and shrubs, are capable of invading eucalypt roots under suitable conditions in Australia and other countries.

6.5 Mycorrhizal infection cycles 6.5.1

Primary inoculum transmission

Most eucalypt ectomycorrhizal fungi are dispersed as airborne spores produced from mushroom-type sporocarps (e.g. Amanita, Boletus, Cortinarius, Russula) or variations on the puff-ball theme (e.g. Pisolithus, Scleroderma). There is also a significant and important minority that are transmitted by animal vectors (Lamont et al. 1985; Malajczuk et al. 1987b). These fungi (e.g. Hydnangium, Endogone) produce underground sporocarps that are sought out and eaten by small native animals, which digest the sporocarp tissues and void viable spores in faeces. The VA endomycorrhizal fungi produce only soilborne primary inoculum in the form of spores or sclerotia.

6.5.2

The infection process

6.5.2.1

Typical ectomycorrhizas

Spores of ectomycorrhizal fungi are known to germinate in response to a chemical stimulus from active roots (Fries and Swedjemark 1986; Theodorou and Bowen 1987). Using the paper sandwich technique (Chilvers et al. 1986), which allows all parts of a seedling root system to be inoculated simultaneously, Horan et al. (1988) showed that the site of infection of eucalypts is always the apex of one of the fine lateral roots. Differentiated regions of the root system and large fast-growing apices do not become infected. The hyphae are attracted 86

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chemotropically to the root cap (Horan and Chilvers 1990), where they grow over the surface and penetrate between and into the cells (Chilvers 1968a; Massicote et al. 1987a, 1987b; Horan et al. 1988). As the hyphae press inwards through the root cap they become twisted and branched in the confined space, until the whole mass of hyphae and residues of the root cap cells become compacted into a dense sheath tissue enclosing the root apex. On the flanks of the root, just behind the apex, the fungus penetrates right through the cap tissue and contacts the epidermis. Here the fungus forces its way between the epidermal cells in the form of thin sheets of labyrinthine hyphal tissue (Horan et al. 1988). This intercellular penetration only occurs between immature epidermal cells, where the middle lamella is perhaps still inherently weak (Chilvers and Gust 1982b; Horan et al. 1988) and it is brought to a stop at the boundary between epidermis and outer cortex (exodermis) where the middle lamella is suberised (Ling-Lee et al. 1977a). Once established, an ectomycorrhiza can enlarge by linear extension at about one-fifth the rate of an equivalent uninfected root apex (Chilvers and Gust 1982b). The root meristem, which remains uninfected, continues to generate cells and drive apical growth of the root axis. The fungus matches this by sheath extension at the apex and continual invasion of newly formed cap and epidermal cells, perpetuating the mycorrhizal anatomical configuration. The pressure of the elongating root axis pushing forward against the restraining sheath places the sheath under tension, which is responsible for the smooth hemispherical shape of the mycorrhizal apex (Chilvers 1974; Seviour et al. 1978) and by pulling on the Hartig net anchored between epidermal cells, causes these cells to be pulled forward and outward into their characteristic slanted, radially elongate shape (Clowes 1951). An ectomycorrhiza can also enlarge by proliferation of side branches (Chilvers and Gust 1982b), each tip becoming ensheathed as it emerges from the cortex (Massicote et al. 1987b). This can result in a substantial cluster of mycorrhizal apices all derived from the one infection event (Chilvers and Gust 1982a). 6.5.2.2

Endomycorrhizas

Infection of eucalypt roots by VA endomycorrhizal fungi is similar to that in other plants. Spores may germinate in the absence of host roots, but

M Y CORRHIZA S

subsequent hyphal growth requires stimulation by root exudates and there is evidence of chemotropic attraction close to the root surface (Koske and Gemma 1992; Peterson and Bonfante 1994). Most infections probably occur along the young regions of roots just behind the zone of differentiation (Harley and Smith 1983); unlike ectomycorrhizas there is no involvement with cap tissue or undifferentiated epidermal cells (Horan 1991). A hyphal tip contacting the root surface forms an appressorium and infection peg able to penetrate directly into an epidermal cell. The penetration hypha then grows directly inwards through or between the epidermal cells into the cortex (Horan 1991). Once in the cortex the fungus branches and spreads intercellularly for short distances forwards and backwards along the root, forming arbuscules in the inner cortex along the way. There is no anatomical modification of the plant tissues and the infection site is left rapidly behind by the growing apex of the root (Harley and Smith 1983).

6.5.3

Secondary inoculum transmission

6.5.3.1

Ectomycorrhizas

Once a primary focus of infection is well established, satellite infections may be generated by secondary spread of hyphal inoculum, often in the form of organised hyphal strands or rhizomorphs which originate at the base of the primary mycorrhiza (i.e. the site of primary infection) (Chilvers 1968b; Chilvers and Gust 1982a). Spread may occur along root surfaces or through the soil. Such secondary inocula, well-resourced by carbohydrates acquired from the existing primary infection, are very effective in contacting uninfected apices and establishing new mycorrhizas, leading to rapid development of an extended mycorrhizal ‘colony’ of interconnected mycorrhizal clusters (Chilvers and Gust 1982a). Establishment of substantial perennial colonies of ectomycorrhizas is probably a necessary prerequisite for the production of the large sporocarps which characterise ectomycorrhizal fungi. 6.5.3.2

Endomycorrhizas

The relatively short-lived primary infections of VA endomycorrhizas also give rise to secondary infections. Fuelled by carbohydrates from the host, the original infection hypha starts to branch immediately external to its point of entry, and some of these branches spread along the root surface generating secondary infections at intervals of about

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0.5 millimetres (Horan 1991). Other branches radiating into the soil may contact and initiate secondary infections on other nearby roots, but the scale and duration of resulting colonies is limited and they support only small reproductive structures.

6.6 Ecology of mycorrhizas 6.6.1

Natural distribution of mycorrhizas in Australia

6.6.1.1

Geographical and local distribution

VA endomycorrhiza are not significant in established native eucalypts (Gardner and Malajczuk 1988), but ectomycorrhizas can be found wherever eucalypts grow naturally, tending to reach maximum abundance and diversity in cool moist regions where litter and soil organic matter accumulates and plant nutrient cycling is slow (Chilvers and Pryor 1965). Although some of the species may differ [e.g. Descolea maculata Bougher v. Descolea recedens (Cooke & Massee) Singer], west Australia and east Australia share similar ectomycorrhizal fungi (Bougher and Malajczuk 1985; Bougher 1995) and similar patterns of distribution of ectomycorrhizas. The occurrence of fungi within a particular locality is influenced by topographic and edaphic factors. For example, the large gilled fungi are most abundant in moist gullies, the black mycorrhizas formed by Cenococcum are common on dry rocky ridges and Phylloporus is prominent on terra rossa soils over limestone. 6.6.1.2

Stratification of mycorrhizas in tall forest

In tall forest with a well-developed litter layer, there is some stratification of types of ectomycorrhizas and associated fungi (Reddell and Malajczuk 1984; Hilton et al. 1989). The soil proper is dominated by typical pyramidal ectomycorrhizas, which often form substantial clusters representing several years of growth and proliferation. These persistent ectomycorrhizas are often smooth sheathed, but connected to complex hyphal strands having large central conducting hyphae (e.g. Chilvers 1968b, figs 6f and 8g), suggesting that they are equipped for nutrient uptake at a distance. In contrast, the litter layer and the organic soil immediately beneath have many superficial and intermediate ectomycorrhizas. These are commonly surrounded by dense wefts of hyphae or simple hyphal strands which interpenetrate the adjacent organic substrates, giving the impression that these mycorrhizas are mainly 87

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acquiring nutrients close to the root. During the height of summer many of the fine roots near the soil surface dry out and shrivel, requiring that this region be reinvaded periodically by fresh feeder roots. The fast-growing superficial and intermediate mycorrhizas are clearly more suited to exploit these fluctuating conditions than the slow-growing typical mycorrhizas. Different genera of fungi appear to predominate in soil and litter environments: Amanita, Boletus and hypogean fungi generally are characteristic of the soil mycorrhizas; Cortinarius and Tricholoma tend to dominate the litter layer (Reddell and Malajczuk 1984; Malajczuk et al. 1987a; Gardner and Malajczuk 1988; Hilton et al. 1989). 6.6.1.3

Fine-scale horizontal patterning of mycorrhizas in tall forest

Natural distribution of ectomycorrhizas in tall forest is markedly non-random. They invariably occur in clusters, and where the sheath or associated hyphal strands have distinctive features which can be recognised in situ (Chilvers 1968b, 1973; Gardner and Malajczuk 1988), multiple clusters can often be recognised to form collective colonies. Such mycorrhizal colonies range from several centimetres to several decimetres in lateral extent and one exceptionally large colony of mycorrhizas with Octaviania densa (Rodway) G.Cunn. (= Melanogaster; May and Wood 1997) extended over several metres (G.A. Chilvers, pers. obs.). The distribution of mycorrhizal colonies under ground is mirrored in the pattern of sporocarps formed above ground. Hilton et al. (1989, fig. 7) provide maps detailing the positions of sporocarps which emerged over three seasons close to large jarrah (E. marginata) trees. One 25 square metre quadrat shows nearly 300 sporocarps, representing eight ectomycorrhizal species, grouped into some 40 to 50 discrete colonies. Such complex mosaics of mycorrhizal fungal colonies in tall forest change only slowly with time. The large Octaviania densa colony referred to above persisted over five years. A two square metre colony of sporocarps of Laccaria laccata, remapped after two years, remained similar in size but was positioned slightly further away from the reference tree (Hilton et al. 1989, fig. 6). Each colony represents secondary spread from an initial focus of primary infection and the relative stability and large grain-size of the mosaic pattern indicates

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that the niche of the mycorrhizal fungi is substantially saturated, with few opportunities for spores to initiate new primary infections in competition with the abundant and well-nourished secondary hyphal inoculum already present.

6.6.2

Mycorrhizas on eucalypts in new or disturbed sites

6.6.2.1

Mycorrhizal epidemics

When eucalypts are planted into a new (non-forest) site or a disturbed forest site, appropriate hyphal inoculum is initially absent or scarce and this provides maximum opportunities for spores and sclerotia to initiate new primary infections among the expanding network of uninfected roots. Hyphal inoculum spreading from these primary infection foci will encounter many susceptible apices available for secondary infection, favouring a consequent rapid increase in the number of apices converted to mycorrhizas. Using young pot-grown eucalypt seedlings as a model, Chilvers and Gust (1982a) showed that such mycorrhizal population explosions behave in a similar manner and can be analysed in the same terms as plant disease epidemics. In soilgrown seedlings, ectomycorrhizas appeared after two weeks and increased exponentially up to week 12 when more than 75% of root apices were mycorrhizal. The population of ectomycorrhizal apices multiplied at a rate of 0.81 per unit per week, against a background rate of 0.51 for all root apices, giving a net rate of increase of 0.30 per unit per week in the percentage of apices converted to ectomycorrhizas (i.e. doubling every 16 days). In eucalypts grown in peat moss, virtually devoid of primary inoculum, it took much longer for the first infection foci to appear and 24 weeks to achieve comparable infection levels (63% apices converted). 6.6.2.2

Mycorrhizal succession

In various mine reclamation areas (Khan 1978; Gardner and Malajczuk 1988) and disturbed calcareous soil (Lapeyrie and Chilvers 1985), the ubiquitous, non-specific, VA endomycorrhizal fungi have been the first group to form substantial quantities of mycorrhizas (up to 50% root length) on planted eucalypt seedlings. Probably this reflects a higher level of primary inoculum and better adaptation to alkaline conditions than ectomycorrhizal fungi. However, such endomycorrhizal infections do not persist very long,

M Y CORRHIZA S

as they are gradually but inexorably replaced by ectomycorrhizas (Lapeyrie and Chilvers 1985; Chilvers et al. 1987; Gardner and Malajczuk 1988; Boudarga et al. 1990; Bellei et al. 1992). Ectomycorrhizal fungi can invade the root apices of existing endomycorrhizas and take control of these, but endomycorrhizal fungi cannot reciprocate and invade established ectomycorrhizas because the sheath occludes their preferred infection site—the young tissues immediately behind the root apex (Chilvers et al. 1987). The first ectomycorrhizal fungi to establish themselves, either following endomycorrhizal fungi, or acting as pioneers in less extreme situations, are airborne genera such as Laccaria, Pisolithus, Scleroderma and some Amanita species (Chu-Chou and Grace 1982; Gardner and Malajczuk 1988). This pioneer group of ectomycorrhizal fungi form typical pyramidal ectomycorrhizas with hyphal outgrowths and simple undifferentiated hyphal strands extending into the surrounding soil. Hypogean fungi dispersed by animal vectors tend to appear later, along with the first of the most characteristic litter stage mycorrhizal fungi, species of the superficial ectomycorrhizal genus Cortinarius. As forest matures and litter layers consolidate, the characteristic late stage mycoflora of Cortinarius, Paxillus, Ramaria and Russula becomes well developed and the pioneer group is reduced to a minor component (Hilton et al. 1989). 6.6.2.3

Eucalypts outside Australia

VA endomycorrhizas appear to be quite prominent on young plantation eucalypts planted in South America (Zambolim and Barros 1982; Schwan 1984; Bellei et al. 1992; Estrada et al. 1993). Presumably these are indigenous fungi, readily acquired by the eucalypts where suitable ectomycorrhizal inoculum is not abundant. In one study, the VA endomycorrhizas predominated over ectomycorrhizas for the first seven months, and still persisted eight months later, although they were being replaced gradually by the latter (Bellei et al. 1992). It would not be surprising if a search of exotic eucalypts in other countries found VA endomycorrhizas to be common. The ectomycorrhizal fungi, generally exotics originating in Australia, are mostly early stage ‘pioneer’ types such as Pisolithus and Scleroderma. Most of the specialised ‘late stage’ or ‘litter’ eucalypt mycorrhizal

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fungi have not yet been found with exotic eucalypts outside Australia and New Zealand.

6.6.3

Environmental factors influencing formation of mycorrhizas

6.6.3.1

Soil water

Mycorrhizas are formed optimally at moderate soil water potentials, at which fine soil pore spaces are charged with water but larger pore spaces are air filled. In very dry soils, the abundance and diversity of mycorrhizas is greatly reduced, but black mycorrhizas formed by Cenococcum remain common, reflecting its ability to grow at low water potentials (Bowen and Theodorou 1973). In moist soil, the proportion of mycorrhizal roots of eucalypts declined as soil water potential increased from –4.5 to –0.14 kilopascals (Bougher and Malajczuk 1990). In bottle cultures employing a paper wick to moisten eucalypt roots, mycorrhiza formation stopped abruptly at the water line, even though both the roots and hyphae of Pisolithus grew separately below this level (Chilvers and Gust 1982b). These results reflect the need for good aeration of ectomycorrhizas to support their high respiration rates, which are about 50% greater than plant or fungal tissues alone (J.M. Kelly, D.A. Day and G.A. Chilvers, unpubl. data). 6.6.3.2

Light

Pot-grown eucalypt seedlings inoculated with spores had fewer mycorrhizas when grown in heavy shade than when grown in full light (Ashton 1976). Eucalypt mycorrhizal apices synthesised in pure culture in the presence of abundant hyphal inoculum also decreased in number under reduced light conditions, but only in proportion to a general decrease in occurrence of all root apices (McInnes and Chilvers 1994). 6.6.3.3

Plant nutrients

Additions of phosphorus (P) and nitrogen (N) to potgrown eucalypts usually reduce the proportion of root apices converted to ectomycorrhizas (Ashton 1976; Chilvers and Gust 1982a; Reddell and Malajczuk 1984; Marschner and Dell 1994), although small additions of P to soils of low nutrient status can increase the proportion of mycorrhizas (Vieira and Peres 1988a; Bougher et al. 1990; Marschner and Dell 1994). Four different

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categories of response to progressive increases in applied phosphate can be discerned in the data of Bougher et al. (1990) for mycorrhizas formed between E. diversicolor and Descolea maculata: 1

from zero to four micrograms per gram of added P, both total mycorrhizal root length (× 24) and proportion of roots converted to mycorrhiza (× 7) increased markedly, along with seedling dry weight (× 6) and total seedling P (× 14)

2

between four and 20 micrograms per gram of added P, total mycorrhizas continued to increase (× 4) but percentage mycorrhizas decreased (× 0.5), accompanied again by substantial increases in dry weight (× 7) and seedling P (× 8)

3

between 20 and 36 micrograms per gram of added P, total and percentage mycorrhizas both decreased to zero while plant dry weight and total P content increased only slightly

4

above 36 micrograms per gram of added P, dry weight showed no change, although P content continued to increase slightly.

The positive correlation between percentage mycorrhizas and applied phosphate at low phosphate levels (0–4 µg/g) indicates that the mycorrhizal epidemic is rate-limited by density of host apices available for infection. At moderate phosphate levels (4–20 µg/g), there is no shortage of root apices available for infection and the progress of the mycorrhizal epidemic is probably limited by the rate at which the secondary inoculum of the fungus can spread between apices. At high phosphate levels (20–36 µg/g), fungal spread and/or the infection process is inhibited in some way, with the result that as P availability ceases to be limiting for growth the plant no longer expends energy on the mycorrhizal symbiosis. Such apt control of ectomycorrhiza formation was hypothesised by Björkman (1942) to operate through the internal concentration of soluble carbohydrates in the root, where high carbohydrate concentrations accumulating under high light/low nutrient conditions favoured mycorrhiza formation, and low carbohydrate concentrations brought about under low light/high nutrient conditions prevented formation of mycorrhizas. Since low light and high P and N levels produced no discernible reduction in infectibility of eucalypt root apices under conditions of artificially high fungal inoculum potential (McInnes and Chilvers 1994), it is presumed that any variations in the soluble carbohydrate pool must 90

E U C A L Y P T S

operate externally on fungal inoculum potential, perhaps through changed levels in root exudates.

6.7 Manipulating eucalypt mycorrhizas 6.7.1

Experimental manipulation

6.7.1.1

Laboratory studies

Most attempts to manipulate the eucalypt ectomycorrhizal symbiosis have their starting point in the laboratory identification, isolation and culturing of likely fungi as detailed in Brundrett et al. (1996). Another important step is to assess these cultures for capacity to form mycorrhizas by inoculation on the roots of axenically grown eucalypt seedlings (Massicote et al. 1987a; Tonkin et al. 1989; Malajczuk et al. 1990). Eucalypts have proved peculiarly suitable for this because the small hard seeds are readily surface sterilised, most species germinate without difficulty and the small seedlings can be conveniently contained in axenic culture vessels for considerable periods if required (Chilvers and Gust 1982b). Axenically synthesised eucalypt mycorrhizas have provided an ideal model system for controlled experiments on the infection process (e.g. Horan et al. 1988; Burgess et al. 1996) and symbiotic physiology (e.g. Cairney et al. 1989), as well as providing clean, defined material for ultrastructural (e.g. Malajczuk et al. 1984; Jacobs et al. 1989; Lei et al. 1990), chemical and histochemical (e.g. Seviour et al. 1974; Seviour and Chilvers 1972; Ling-Lee et al. 1977a, 1977b; Ashford et al. 1986) and biochemical and genetic studies (e.g. Hilbert and Martin 1988; Martin and Hilbert 1991; Burgess and Dell 1996). The more tractable fungi have then been utilised further in glasshouse and field experiments. 6.7.1.2

Glasshouse and pot experiments

A clear account of glasshouse and nursery experimental procedures for mycorrhizal studies is given in Brundrett et al. (1996). Several types of inocula have been used in pot inoculation experiments, including natural soil impregnated with hyphae or spores (e.g. Ashton 1976; Chilvers and Gust 1982a), faecal pellets containing spores (Lamont et al. 1985), infected plants with attendant spores (Zambolim et al. 1982; Warcup 1990b), spores from sporocarps (Mullette 1976; Heinrich et al. 1988) and pure-cultured mycelial hyphae variously grown on absorbent paper card (Chilvers

M Y CORRHIZA S

TA BLE 6. 2

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Examples of growth enhancement of Eucalyptus and Corymbia seedlings following inoculation with mycorrhizal fungi Mycorrhizal development

Eucalypt

Type of inoculum

Fungus

Control

Inoculated

Dry wt of inoculated plants as % of control

References 5

Pot experiments C. calophylla

Mesophellia trabalis

FPS

24%

56%

210

E. diversicolor

Descolea maculata

HAP

0%

8%

222

11

E. diversicolor

Descolea maculata

HAP

0%

14%

856

11

E. diversicolor

Laccaria laccata

HAP

0%

23%

2111

12

E. diversicolor

Laccaria laccata

HAP

0%

33%

202

11

E. diversicolor

Pisolithus tinctorius

HAP

0%

22%

234

11

E. dumosa

Glomus pallidum I.R.Hall

NSI

20 cm

195 cm

711

4

E. globulus

Hydnangium carneum

HAP

2%

31%

470

14

E. globulus

Descomyces albellus (syn. Hymenogaster zeylanicus)

HAP

2%

30%

328

14

E. globulus

Scleroderma verrucosum

HAP

2%

38%

525

14 11

E. globulus

Setchelliogaster sp.

HAP

0%

64%

350

E. grandis

Glomus clarum

MZR

—

+

400

2

E. grandis

Glomus intraradices

MZR

—

+

380

2

E. grandis

Pisolithus tinctorius

HAP

0%

60%

173

E. grandis

Pisolithus tinctorius

HAP

0%

60%

239

8

E. grandis

Pisolithus tinctorius

HAP

0%

76%

256

8

E. obliqua

Endogone aggregata

MZR

—

+

1628

13

E. obliqua

Endogone tuberculosa

MZR

—

+

2005

13

E. pilularis

‘Black mycorrhizas’

NSI

5 per cm

40 per cm

201

6

E. pilularis

Pisolithus tinctorius

HAP

(0%)

50+%

329

7

E. regnans

Inocybe fulvo-olivacea

HIS

9%

62%

241

1

E. regnans

Laccaria laccata

HAS

—

+

186

3

E. regnans

Mesophellia arenaria

HIS

25%

60%

157

1

E. tereticornis

Glomus clarum

MZR

—

+

288

2

E. tereticornis

Glomus intraradices

MZR

—

+

225

2

Pisolithus tinctorius + Scleroderma cepa

SAS

—

+

380

16 17

Field experiments E. camaldulensis E. diversicolor

Amanita sp.

HAP

?

?

180

E. diversicolor

Protubera sp.

HAP

?

?

172

17

E. globulus

Hebeloma westraliense

HAP

18%

51%

207

18

E. globulus

Setchelliogaster sp.

HAP

18%

46%

179

18

E. urophylla hybrid

Pisolithus tinctorius

HAS

1.8A

3.0A

161B

15

E. urophylla hybrid

Scleroderma citrinum (syn. HAS Scleroderma auranticum)

1.8A

2.3A

137B

15

E. urophylla hybrid

Scleroderma texense

HAS

1.8A

2.0A

139B

15

A

B

An index of mycorrhizal development; a measure of volume growth of young trees. Type of inoculum: FPS, faecal pellet containing spores added to soil; HAP, hyphal inoculum added to young plants before transfer to soil; HAS, hyphal inoculum added to soil; HIS, natural hyphae impregnated soil; MZR, mycorrhizal roots with associated hyphae and spores; NSI, natural soil inoculum containing spores or sclerotia; SAS, spore inoculum added to soil References: 1, Ashton (1976); 2, Zambolim et al. (1982); 3, Schoeneberger (1985); 4, Lapeyrie and Chilvers (1985); 5, Lamont et al. (1985); 6, Heinrich and Patrick (1986); 7, Heinrich et al. (1988); 8, Vieira and Peres (1988a, 1988b); 9, Soares et al. (1989); 10, Burgess and Malajczuk (1989); 11, Bougher and Malajczuk (1990); 12, Bougher et al. (1990); 13, Warcup (1990a); 14, Burgess et al. (1993); 15, Garbaye et al. (1988); 16, Cruz et al. (1990); 17, Grove et al. (1991); 18, Thomson et al. (1996)

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et al. 1986), in a vermiculite/peat-moss mixture (Garbaye et al. 1988), on agar media (e.g. Vieira and Peres 1988a; Bougher et al. 1990; Dell et al. 1994) or in alginate beads within submerged aerated culture (Kuek et al. 1992). Pot cultures have been used for a range of studies including the effect of environmental conditions on mycorrhiza formation (e.g. Bougher and Malajczuk 1990; Aggangan et al. 1995), mycorrhizal population dynamics (Chilvers and Gust 1982a), nutrient uptake (e.g. Malajczuk et al. 1981; Heinrich and Patrick 1986), and especially to determine effects of mycorrhizal inoculation on plant growth. Table 6.2 summarises evidence that mycorrhizal inoculation of young eucalypts can lead to enhanced growth relative to uninoculated controls. The differences between uninoculated and inoculated treatments, commonly two-fold to three-fold but ranging up to 20-fold, confirm that mycorrhizas can be important for eucalypt growth. But the magnitude of these results should be considered in context. Firstly, they probably represent the upper limits of what is possible—some other results, published and unpublished, show modest, negligible or even negative effects of inoculation. Secondly, such large differences are achieved when: 1

the control plants are kept relatively free of mycorrhizas

2

a high incidence of mycorrhizas is produced on the inoculated plants

3

availability of soil phosphate is low.

E U C A L Y P T S

6.7.2

Potential for manipulation of mycorrhizas in forestry practice

6.7.2.1

Australian native forests

There would seem little opportunity to manipulate mycorrhizas in native forests. Assuming that native forests already have a diverse mycorrhizal flora in balance with the needs of the trees, the prime objective should be to avoid unnecessary interference with that community. Quite apart from considerations of tree production, these forests represent a diverse storehouse of endemic plants, fungi and animals which have coevolved in situ and so have important conservation significance (Bougher and Tommerup 1996). Fire is a natural factor that has a periodic effect on the mycorrhizal fungi, negative on some, positive on others (Malajczuk and Hingston 1981; Hilton et al. 1989; Warcup 1990b). A major issue is the practice of clearfelling, which substantially reduces inoculum potential of ‘late stage’ fungi by disrupting established mycelial networks and perhaps also by driving away the small animal vectors of hypogean fungi, but appears to leave adequate inoculum levels of ‘early stage’ fungi (Amaranthus and Perry 1994; Grove and Malajczuk 1994). While the latter inoculum may be appropriate to the regeneration of seedlings in the disturbed situation that results, one would like to see careful comparisons between the effects of clearfelling and other silvicultural practices and natural disturbance by fire upon the subsequent diversity of fungi, development of mycorrhizas and young tree growth. 6.7.2.2

6.7.1.3

Field experiments

So far there have been only a few successful field experiments on inoculation of eucalypts with mycorrhizal fungi; four are listed in Table 6.2. The positive results are encouraging and the experiments demonstrate the practicability of introducing particular mycorrhizal fungi with seedlings into the field. However, some of the introduced fungi have survived for relatively short periods and it has proved difficult to predict when positive responses to inoculation are going to occur in the field because of poor correlation between pot and field results (Grove and Le Tacon 1993; Grove and Malajczuk 1994). This problem no doubt results from the more complex edaphic environment and greater diversity of biological competitors and antagonists in the field. 92

Eucalypts outside Australia

The greatest potential for manipulating mycorrhizas on eucalypts must be in countries other than Australia, where, as we have seen, only a few native Australian mycorrhizal fungi have so far penetrated and where levels of ectomycorrhizal fungal inoculum are not high enough to prevent significant VA endomycorrhizal infection at the first stage in the mycorrhizal succession. Introduction of various Australian mycorrhizal fungi as pure cultures, after careful screening for specificity and effectiveness with eucalypts and against undesirable characteristics such as weediness and toxicity of sporocarps (incidents like the inadvertent introduction of Amanita phalloides into Australia with exotic oaks need to be guarded against), should offer no great technical difficulties. And in a situation where the eucalypt mycorrhizal ecological niche is not filled,

M Y CORRHIZA S

air-dispersed fungi should spread readily. In the somewhat analogous situation with pine plantations in Australia, exotic mycorrhizal fungi periodically spread in epidemic fashion (e.g. Lactarius deliciosus dispersed through southern New South Wales pine plantations during the 1960s and Amanita muscaria during the 1980s). The potential of mycorrhizas for improving establishment and performance of exotic eucalypts is still being explored (e.g. Garbaye et al. 1988; Cruz et al. 1990), with some early indications of growth responses to inoculation. But there has been no example reported from exotic eucalypts which can compare with the dramatic responses to mycorrhizal infection reported for exotic pine seedlings in Australia early this century (Kessel and Stoate 1936). Indeed, many eucalypt species have readily established and have actually grown better in countries other than in Australia (Pryor 1976). Probably, with their more finely branched root systems and evolutionary adaptation to low phosphorus soils, eucalypts are generally less dependent on mycorrhizas than pines. Where establishment difficulties with eucalypts have been encountered, these most often involve species of the subgenus Monocalyptus and/or relate to marginal edaphic conditions (e.g. calcareous soils, or periodically frozen soil). These are areas of particular interest for mycorrhizal studies (Lapeyrie and Bruchet 1982; Lapeyrie 1990). 6.7.2.3

Reclamation of land

In Australia, the most obvious role for mycorrhizal inoculations is in country being reclaimed after mining activities which destroy the normal soil profile, alter soil pH and leave the surface soil denuded of organic matter and sometimes permeated with heavy metal ions. Seedling trees have difficulty establishing in these situations, but pre-inoculated mycorrhizal seedlings have markedly improved survival and growth (Marx and Altman 1979). Mycorrhizal inoculation is also most easily funded in such circumstances, if a satisfactory reclamation process is seen as a normal component of the costs of the mining activity. Inoculation with mycorrhizas might also be important in replanting trees used in recovering salinated agricultural land. 6.7.2.4

Eucalypt plantations in Australia

Establishment of eucalypt plantations is increasing rapidly in Australia. This usually involves

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6

reforestation of land which has become unprofitable for agriculture. Forest plantation management sets a premium on synchrony and rapidity of tree growth, and is prepared to put a reasonable investment into site preparation, seedling production, fertilisers and weed and pest control, provided that the cost is justified by the eventual returns from tree harvests. In this situation, the mycorrhizal inoculation used in seedling production must be reliably infective, physically robust and economical to produce (Tommerup et al. 1987; Miller et al. 1994; Kuek 1994). There already exists a well-developed technology for inoculating eucalypt seedlings with specified ectomycorrhizal fungi (Brundrett et al. 1996), but it is not being widely applied because there is insufficient evidence that such inoculations consistently lead to growth enhancements large enough to be profitable (Grove and Malajczuk 1994; Kuek 1994). While disappointing to the proponents of artificial inoculation, this uncertain position will have the positive effect of stimulating more rigorous field research and some reappraisal of objectives. The main thrust of recent work, mainly aimed at developing procedures to achieve high levels of mycorrhizal infection and rapid seedling growth at a very early stage (Malajczuk 1987; Grove and Le Tacon 1993; Grove and Malajczuk 1994), is epidemiologically sound. Modification of epidemics requires measures to be taken at the earliest possible stage, when changes in inoculum will have the largest influence on subsequent exponential progress of infections (van der Plank 1963). Similarly, a limited period of growth promotion in young trees can give them a time lead over control trees which may persist for years as a separation of their growth curves (e.g. Renbuss et al. 1973). However, in Australia, it is inevitable that inoculation-induced enhancements of mycorrhizal infections and plant growth in the field are going to be reduced to varying extents as a result of background mycorrhizal infections of control plants from endemic ectomycorrhizal inoculum. Rather than trying to predict where, and with which fungus, significant growth promotions might be produced, the objective of inoculations might more realistically be directed towards ensuring a consistently rapid and high conversion of short roots to mycorrhizas regardless of field conditions and background infections. In practice this may require multiple inoculation with a mixture of several different pioneer fungi to ensure that some 93

D I S E A S E S

A N D

P A T H O G E N S

O F

will suit local edaphic conditions and show persistence in the field.

6.7.3

A way forward

Abbott and Gazey (1994) argued that continuous systems computer models are needed to enhance understanding of, and to make predictions about, complex mycorrhizal systems. Experience of continuous systems models in other microbial systems, such as bacterial competition (Legan et al. 1987), plant disease (Mao et al. 1988) and freshwater fungal ecology (Thomas et al. 1990) strongly support the value of this approach, but also emphasises how essential it is to have good information about rates of processes for use in such models. Unfortunately, reliable rate data have been collected only rarely in ectomycorrhizal research. There is a need for experiments and observations specifically designed to collect time-course data at sufficiently frequent intervals to allow reliable rates of change to be calculated for key host, fungal and mycorrhizal parameters under different conditions.

6.8 References Abbott, L.K. and Gazey, C. (1994). An ecological view of the formation of VA mycorrhizas. In Management of Mycorrhizas in Agriculture, Horticulture and Forestry. (Eds A.D. Robson, L.K. Abbott and N. Malajczuk) pp. 69–78. (Kluwer Academic Publishers: Dortrecht.) Abbott, L.K. and Robson, A.D. (1985). Formation of external hyphae in soil by four species of vesiculararbuscular mycorrhizal fungi. New Phytologist 99, 245–255. Abuzinadah, R.A. and Read, D.J. (1989). The role of proteins in the nitrogen nutrition of ectomycorrhizal plants. New Phytologist 103, 507–514. Agerer, R. (1991). Characterization of ectomycorrhizae. In Methods in Microbiology. Vol 23. Techniques for the Study of Mycorrhiza. (Eds J.R. Norris, D.J. Read and A.K. Varma) pp. 25–73. (Academic Press: London.) Aggangan, N.S., Dell, B., Malajczuk, N. and de la Cruz, R.E. (1995). Effects of soil sterilization on the formation and function of two strains of Pisolithus tinctorius on Eucalyptus urophylla. Biotropia 8, 11–22. Amaranthus, M.P. and Perry, D.A. (1994). The functioning of ectomycorrhizal fungi in the field: linkages in space and time. In Management of Mycorrhizas in Agriculture, Horticulture and Forestry. (Eds A.D. Robson, L.K. Abbott and N. Malajczuk) pp. 133–140. (Kluwer Academic Publishers: Dortrecht.) Amorim, E.F. de C. (1988). Compartamento de munas de Eucalyptus grandis na presenca de fungos endo e

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ectomicorrizicos. MS Thesis, Universidade Federale de Viçosa, Brazil. Anderson, C.A. and Ladiges, P.Y. (1982). Lime-chlorosis and the effect of fire on growth of three seedling populations of Eucalyptus obliqua L’Herit. Australian Journal of Botany 30, 46–66. Anderson, J. (1966). Indagini sulla micorrizia in alcune specie de eucalitto nell’italia centrale. Pubblicazioni del Centro di Sperimentazione Agricola e Forestale 8, 261–274. Anderson, J. (1967). Le micorriza dell’eucalitto in piantine allevate in vivaio. Pubblicazioni del Centro di Sperimentazione Agricola e Forestale 9, 81–89. Asai, T. (1934). Über das Vorkommen und die Bedeutung der Wurzelpilze in den Landpflanzen. Japanese Journal of Botany 7, 107–150. Ashford, A.E., Ling Lee, M. and Chilvers, G.A. (1975). Polyphosphate in eucalypt mycorrhizas: a cytochemical demonstration. New Phytologist 74, 447–453. Ashford, A.E., Peterson, R.L., Dwarte, D. and Chilvers, G.A. (1986). Polyphosphate granules in eucalypt mycorrhizas: determination by energy dispersive Xray microanalysis. Canandian Journal of Botany 64, 677–687. Ashford, A.E., Allaway, W.G., Peterson, C.A. and Cairney, J.W.G. (1989). Nutrient transfer and the fungus–root interface. In Plant–Microbe Interface: Structure and Function. (Eds P.A. McGee, S.E. Smith and F.A. Smith) pp. 85–105. (CSIRO: Melbourne.) Ashton, D.H. (1956). Studies on the autecology of Eucalyptus regnans F. Muell. PhD Thesis, University of Melbourne, Melbourne. Ashton, D.H. (1976). Studies on the mycorrhizae of Eucalyptus regnans F. Muell. Australian Journal of Botany 24, 723–741. Bailey, S.R. and Peterson, R.L. (1988). Ectomycorrhiza synthesis between isolated roots of Eucalyptus pilularis and Pisolithus tinctorius. Canadian Journal of Botany 66, 1237–1239. Bakshi, B.K. (1966). Mycorrhiza in eucalypts in India. Indian Forester 92, 19–21. Barros, N.F. de, Brandi, R.M. and Reis, M.S. (1978). Micorriza em eucalipts. Revista Ârvore 2, 130–140. Battistelli, N.J., Oliveira, V.L. de, Espirito Santo, R. and Gomes, N.C. (1989). Uma técnica para síntese ectomicorrizica in vitro com Eucalyptus viminalis e Pisolithus tinctorius. In Proceedings of III Reunião Brasileira Sobra Micorrizas p. 99. Universidade de Sao Paulo, Piracicaba. Beadle, N.C.W. (1954). Soil phosphate and the delimitation of plant communities in eastern Australia. II. Ecology 35, 193–204. Bellei, M.M., Garbaye, J. and Gil, M. (1992) Mycorrhizal succession in young Eucalyptus viminalis plantations in Catarina (southern Brazil). Forest Ecology and Management 54, 205–213.

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Bending, G.D. and Read, D.J. (1995). The structure and function of the vegetative mycelium of ectomycorrhizal plants. V. Foraging behaviour and translocation of nutrients from exploited litter. New Phytologist 130, 401–409. Björkman, E. (1942). Über de bedingungen der mykorrhizabildung bei kiefer und fichte. Symbolae Botanical Upsaliensis 1, 1–90. Boudarga, K. and Dexheimer, J. (1988). Étude ultrastructurale des endomycorhizes à vésicules et arbuscules de jeunes plants de Eucalyptus camaldulensis (Dehnardt) (Myrtacées). Bulletin de la Société Botanique de France, Lettres Botaniques 135, 111–121. Boudarga, K., Lapeyrie, F. and Dexheimer, J. (1990). A technique for dual vesicular-arbuscular endomycorrhizal/ectomycorrhizal infection of Eucalyptus in vitro. New Phytologist 114, 73–76. Bougher, N.L. (1995). Diversity of ectomycorrhizal fungi associated with eucalypts in Australia. In Mycorrhizas for Plantation Forestry in Asia. (Eds M. Brundrett, B. Dell, N. Malajczuk and M.Q. Gong.) pp. 8–15. (Australian Centre for International Research: Canberra.) Bougher, N.L. and Malajczuk, N. (1985). A new species of Descolea (Agaricales) from Western Australia, and aspects of its ectomycorrhizal status. Australian Journal of Botany 33, 619–627. Bougher, N.L. and Malajczuk, N. (1986). An undescribed species of hypogeous Cortinarius associated with Eucalyptus in Western Australia. Transactions of the British Mycological Society 86, 301–304. Bougher, N.L. and Malajczuk, N. (1990). Effects of high soil moisture on formation of ectomycorrhizas and growth of karri (Eucalyptus diversicolor) seedlings inoculated with Descolea maculata, Pisolithus tinctorius and Laccaria laccata. New Phytologist 114, 87–91. Bougher, N.L. and Tommerup, I.C. (1996). Conservation significance of ectomycorrhizal fungi in Western Australia: their co-evolution with indigenous vascular plants and animals. In Gondwanan Heritage: Past, Present and Future of the Western Australian Biota (Eds S.D. Hopper, J. Chappill, M. Harvay and N. Marchant.) pp. 299–308. (Surrey Beatty and Sons: Chipping Norton, NSW.) Bougher, N.L., Grove, T.S. and Malajczuk, N. (1990). Growth and phosphorus acquisition of karri (Eucalyptus diversicolor F. Muell.) seedlings inoculated with ectomycorrhizal fungi in relation to phosphorus supply. New Phytologist 114, 77–85. Bougher, N.L., Tommerup, I.C. and Malajczuk, N. (1991). Nuclear behaviour in the basidiomes and ectomycorrhizas of Hebeloma westraliense sp. nov. Mycological Research 95, 683–688. Bougher, N.L., Tommerup, I.C. and Malajczuk, N. (1993). Broad variation in developmental and mature

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basidiome morphology of the ectomycorrhizal fungus Hydnangium sublamellatum sp. nov. bridges morphologically based generic concepts of Hydnangium, Podohydnangium and Laccaria. Mycological Research 97, 613–619. Bougher, N.L., Fuhrer, B.A. and Horak, E. (1994). Taxonomy and biogeography of Australian Rozites species mycorrhizal with Nothofagus and Myrtaceae. Australian Systematic Botany 7, 353–375. Bowen, G.D., Bevege, D.I. and Mosse, B. (1975). Phosphate biology of vesicular-arbuscular mycorrhizas. In Endomycorrhizas. (Eds F.E.Sanders, B. Mosse and P.B. Tinker) pp. 241–260. (Academic Press: London.) Bowen, G.D. and Theodorou, C. (1973). Growth of ectomycorrhizal fungi around seeds and roots. In Ectomycorrhizae; Their Ecology and Physiology. (Eds G.C. Marks and T.T. Kozlowski) pp. 107–150. (Academic Press: London.) Brundrett, M., Bougher, N., Dell, B., Grove, T. and Malajczuk, N. (1996). Working with Mycorrhizas in Forestry and Agriculture. (Australian Centre for International Agricultural Research: Canberra.) Burdon, J.J. and Chilvers, G.A. (1974). Fungal and insect parasites contributing to niche differentiation in mixed species stands of eucalypt saplings. Australian Journal of Botany 22, 103–114. Burgess, T. and Dell, B. (1996). Changes in protein biosynthesis during the differentiation of Pisolithus Eucalyptus grandis ectomycorrhiza. Canadian Journal of Botany 74, 553–560. Burgess, T. and Malajczuk, N. (1989). The effect of ectomycorrhizal fungi on reducing the variation of seedling growth of Eucalyptus globulus. Agriculture, Ecosystems and Environment 28, 41–46. Burgess, T., Malajczuk, N. and Grove, T.S. (1993). The ability of 16 ectomycorrhizal fungi to increase growth and phosphate uptake of Eucalyptus globulus Labill. and E. diversicolor F. Muell. Plant and Soil 153, 155–164. Burgess, T., Dell, B. and Malajczuk, N. (1994). Variations in mycorrhizal development and growth stimulation by 20 Pisolithus isolates inoculated on to Eucalyptus grandis W. Hill ex maiden. New Phytologist 127, 731–739. Burgess, T., Malajczuk, N. and Dell, B. (1995). Variation in Pisolithus based on basidiocarp and basidiospore morphology, culture characteristics and polypeptide analysis using 1D SDS-PAGE. Mycological Research 99, 1–13. Burgess, T., Dell, B. and Malajczuk, N. (1996). In vitro synthesis of Pisolithus–Eucalyptus ectomycorrhizae: synchronization of lateral tip emergence and ectomycorrhizal development. Mycorrhiza 6, 189–196. Cairney, J.W.G. and Ashford, A.E. (1989). Reducing activity at the root surface in Eucalyptus

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Seviour, R.J. and Chilvers, G.A. (1972). Electrophoretic characterisation of eucalypt mycorrhizas. New Phytologist 71, 1107–1110. Seviour, R.J., Chilvers, G.A. and Crow, W.D. (1974). Characterisation of eucalypt mycorrhizas by pyrolysisgas chromatography. New Phytologist 73, 321–332. Seviour, R.J., Hamilton, D. and Chilvers, G.A. (1978). Scanning electron microscopy of surface features of eucalypt mycorrhizas. New Phytologist 80, 153–156. Shepherd, C.J. and Totterdell, C.J. (1988). Mushrooms and Toadstools of Australia. (Inkata Press: Melbourne.) Smith, V.J.G. and Pope, F.B. (1934). The association between the gasteromycete Polysaccum and Eucalyptus roots. Transactions of the British Mycological Society 19, 95. Soares, I. (1986). Níveis de fósforo no desenvolvimento de ectomicorrizas por Pisolithus tinctorius (Pers.) Coker & Couch e no crescimento de mudas de eucalipto. MSc Thesis, Universidade Federal de Viçosa, Viçosa, Brazil. Soares, I., Borges, A.C., Barros, N.F. de., Neves, J.C.L. and Bellei, M.M. (1989). Teor de fósforo no solo influenciando o desenvolvimento de ectomicorrizas e nutrição e crescimento de mudas de eucalipto. Revista Arvore 13, 140–151. Thapar, H.S., Singh, B. and Bakshi, B.K. (1967). Mycorrhizae in Eucalyptus. Indian Forester 93, 756–759. Theodorou, C. and Bowen, G.D. (1987). Germination of basidiospores of mycorrhizal fungi in the rhizosphere of Pinus radiata. New Phytologist 106, 217–223. Thomas, K., Chilvers, G.A. and Norris, R.H. (1990). A dynamic model of fungal spora in a freshwater stream. Mycological Research 95, 184–188. Thomson, B.D., Grove, T.S. Malajczuk, N. and Hardy G.E. StJ. (1994). The effectiveness of ectomycorrhizal fungi in increasing the growth of Eucalyptus globulus Labill. in relation to root colonization and hyphal development. New Phytologist 126, 517–524. Thomson, B.D., Hardy, G.E.StJ., Malajczuk, N and Grove, T.S. (1996). The survival and development of inoculant ectomycorrhizal fungi on roots of outplanted Eucalyptus globulus Labill. Plant and Soil 178, 247–253. Tommerup, I.C., Kuek, C. and Malajczuk, N. (1987). Ectomycorrhizal inoculum production and utilization in Australia. In Mycorrhizae in the Next Decade, Proceedings of the 7th North American Conference on Mycorrhizae. (Eds D.M. Sylvia, L.L. Hung and J.H. Graham) pp. 293–295. (Institute of Food and Agricultural Science: Gainesville, FA, USA.) Tommerup, I.C., Bougher, N.L. and Malajczuk, N. (1991). Laccaria fraterna, a common ectomycorrhizal fungus with mono- and bi-sporic basidia and multinucleate spores: comparison with the quadristerigmate, binucleate spored L. laccata and the hypogeous

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relative Hydnangium carneum. Mycological Research 95, 689–698. Tonkin, C.M., Malajczuk, N. and McComb, J.A. (1989). Ectomycorrhizal formation by micropropagated clones of Eucalyptus marginata inoculated with isolates of Pisolithus tinctorius. New Phytologist 111, 209–214. Trappe, J.M. (1971). Mycorrhiza-forming Ascomycetes. In Mycorrhizae (Ed. E. Hacskaylo) pp. 19–37. (US Government Printing Office: Washington.) Turnbull, M.H., Goodall, R. and Stewart, G.R. (1995). The impact of mycorrhizal colonization upon nitrogen source utilization and metabolism of seedlings of Eucalyptus grandis Hill ex. Maiden and E. maculata Hook. Plant, Cell and Environment 18, 1386–1394. van der Bijl, P.A. (1917). Note on Polysaccum crassipes D.C.—a common fungus in Eucalyptus plantations around Pretoria. Transactions of the Royal Society of South Africa 6, 209–214. van der Plank, J.E. (1963). Plant Diseases: Epidemics and Control. (Academic Press: New York.) Vieira, R.F. and Peres, J.R.R. (1988a). Seleção de fungos ectomycorrizicos eficientes para Eucalyptus grandis. Revista Brasileira de Ciencia do Solo 12, 231–235. Vieira, R.F. and Peres, J.R.R. (1988b). Definicao do teor de fósforo no solo para máxima eficiencia da associação ectomicorrizica em Eucalyptus grandis. Revista Brasileira de Ciencia do Solo 12, 237–241. Warcup, J.H. (1990a). Taxonomy, culture and mycorrhizal associations of some zygosporic Endogonaceae. Mycological Research 94, 173–178. Warcup, J.H. (1990b). Occurrence of ectomycorrhizal and saprophytic discomycetes after a wild fire in a eucalypt forest. Mycological Research 94, 1065–1069.

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Warcup, J.H. and Talbot, P.H.B. (1989). Muciturbo: a new genus of hypogeous ectomycorrhizal Ascomycetes. Mycological Research 92, 95–100. Wild, A. (1958). The phosphorus content of Australian soils. Australian Journal of Agricultural Research 9, 193–204. Yokomizo, N.K.S. (1981). Associação ectomicorrizica de Pisolithus tinctorius (Pers.) Coker e Couch com espécies de Eucalyptus L’Héritier. MS Thesis, Piracicaba, Escola Superior de Agricultura ‘Luiz de Queiroz’. Young, A.M. and Wood, A.E. (1997). Studies on the Hygrophoraceae (Fungi, Homobasidiomycetes, Agaricales) of Australia. Australian Systematic Botany 10, 911–1030. Zak, B. (1971). Characterization and identification of Douglas-fir mycorrhizae. In Mycorrhizae . (Ed. E. Hacskaylo) pp. 38–53. (US Government Printing Office: Washington, DC.) Zak, B. (1973). Classification of mycorrhizae. In Ectomycorrhizae (Eds. G.C. Marks and T.T. Kozlowski) pp. 43–78. (Academic Press: New York.) Zambolim, L. (1990). Fungos micorrizicas de eucalipto. In Relacao Solo-Eucalipto (Eds N.F. de Barros and R.F. de Novai) pp. 303–322. Zambolim, L. and Barros, N.F. de (1982). Constatação e micorriza vesicular arbuscular em Eucalyptus spp. via regiao de Viçosa, MG. Revista Ârvore 6, 95–97. Zambolim, L., Barros, N.F. de and Costa, L.M. da (1982). Influencia de micorrizas do tipo vesicular–arbuscular no crescimento e absorçã de nutrientes por mudas de Eucalyptus spp. Revista Ârvore 6, 64–73.

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Many fungi have been reported from flowers, capsules and seeds of various species of Corymbia and Eucalyptus. Some fungi such as Ramularia spp., Colletotrichum gloeosporioides and Dothiorella eucalypti have caused diseases of capsules, resulting in reduced seed production, while many others have been reported from capsules without mention of their pathogenicity. The fungi found on eucalypt seed can be classified as field or storage fungi. The field fungi associated with eucalypt seed include common soilborne fungi such as Fusarium spp., Macrophomina phaseolina, Pythium spp. and Verticillium albo-atrum. Their association with seed is probably due to contamination of the seed with soil during harvesting or processing. Other field fungi include known foliar pathogens of eucalypts such as Botrytis cinerea, Coniella australiensis, Curvularia spp., Cylindrocladium scoparium, Dothiorella eucalypti, Fairmaniella leprosa, Harknessia spp. and Pestalotiopsis spp. Storage fungi are those that grow on or infect the seed during storage. They are specialised fungi that are able to grow without free water and on substrates of high osmotic potential. Most storage fungi of eucalypt seed are species of Aspergillus and Penicillium. Appropriate hygiene procedures during seed harvesting and processing, and the storage of seed at low temperatures and humidity will usually provide satisfactory control of seedborne fungi. When necessary, treatment with hot water or hydrogen peroxide can be used to reduce the effect of seedborne fungi on seedling establishment.

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7.1 Introduction Many fungi have been reported from the reproductive structures of eucalypts but often their effect on seed production and quality was not recorded. The range of fungi pathogenic on or associated with flowers, capsules or seed of eucalypts, their effect on seed production, and the control of seedborne fungi will be reviewed.

7.2 Fungi of flowers and capsules and their pathogenicity During studies in south-east Queensland of the reproductive success of natural populations of three ironbark species (Eucalyptus crebra, E. melanophloia, E. populnea) and of hybrids between E. crebra and the other two species, a species of Ramularia and a wasp [Megastigmus sp. (Torymidae)], were observed to cause damage to the developing capsules, resulting in loss of seed of all five genotypes (Drake 1974; 1981a, 1981b). No capsules of any of the populations were found to be infected by both Ramularia and the wasp. Drake (1974) surmised that infection by Ramularia must have occurred at an early stage as young capsules shortly after flowering were heavily infected. Infected capsules opened earlier than healthy ones on the same tree. The fungus became evident as the slits of the capsule opened, and it sometimes grew out of the slits. The contents of the capsules were covered by a white mass of spores and mycelium which bound them together. Very few capsules were only partly infected, and no seeds were produced in capsules infected in all locules. Maximum levels of seed loss caused by the fungus on individual trees were 2.3% for E. crebra, 5.3% for E. populnea, 30% for E. melanophloia, 34% for E. populnea × E. crebra and 83% for E. melanophloia × E. crebra. Eucalyptus crebra, E. melanophloia and a E. crebra × E. melanophloia hybrid have been recorded as hosts of Sporothrix pitereka (J.Walker & Bertus) U.Braun & Crous (syn. Ramularia pitereka J.Walker & Bertus) (Walker and Bertus 1971) (see Chapters 9 and 10) which occurs in south-east Queensland (B.N. Brown, unpubl. data), suggesting that the fungus reported by Drake may be this species. Reduction of seed production due to a capsule disease caused by Colletotrichum gloeosporioides (Penz.) Penz. & Sacc. and a Torula sp. was reported

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in a five-year-old E. camaldulensis plantation in India (Sharma et al. 1985). The infection was widespread only in E. camaldulensis although other species also were in flower. Infection commenced on the operculum which became leathery, dried up and remained attached to the capsule. Stamens inside the capsule were curled and brown, and subsequently the infection spread to the capsules and occasionally to the pedicel. Seed capsule abortion and twig dieback caused by Dothiorella eucalypti (Berk. & Broome) Sacc. has been reported from South Florida (Webb 1983). The disease was observed in three seed orchards of E. camaldulensis (from a Spanish seed source) and caused necrosis and abortion of infected capsules. This resulted in seed-crop failures and lead to the use of vegetative cuttings for commercial plantings of E. camaldulensis. Lesions caused by the fungus were frequently observed on field samples of capsules, pedicels, peduncles and leaf midveins of E. camaldulensis. Examination of the staminal filaments underlying the circular lesions on the capsule surface revealed similar circular, reddish purple staining indicative of infection by Dothiorella eucalypti. Infection of the capsules followed colonisation of the floral parts and frequently preceded fertilisation. The infection often spread from the capsules into the pedicels and peduncles, and ultimately into the twigs, causing dieback. In the three affected seed production areas of E. camaldulensis, only one tree appeared resistant to Dothiorella eucalypti and yielded viable seed. In a nearby seed garden of E. robusta, only one tree out of 750 was severely infected by the fungus, having lesions on capsules, pedicels, peduncles and twigs, and branch and stem cankers. Wound inoculation of succulent stems of one-year-old seedlings showed that Corymbia torelliana, E. camaldulensis, E. robusta and E. viminalis were all potential hosts of the fungus. The basionym of Dothiorella eucalypti is Sphaeropsis eucalypti Berk. & Broome, originally recorded from foliage of a Eucalyptus sp. from Melbourne, Vic. (Berkeley and Broome 1887). Sousa da Câmara (1949) reported a new form of the species (Dothiorella eucalypti forma microspora Sousa da Câmara) on E. globulus in Portugal. Dothiorella eucalypti, which also causes eucalypt leaf spots, has been reported from Australia, Florida and Portugal on E. globulus (Gibson 1975; Farr et al. 1989).

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Webb (1983) regarded Dothiorella eucalypti as an anamorph of Botryosphaeria ribis Grossenb. & Duggar, a concept apparently not supported by Farr et al. (1989) as, in their compilation of fungi on plants in the USA, they made no such connection and listed Fusicoccum sp. as the anamorph of Botryosphaeria ribis. Others list Dothiorella sp. rather than Fusicoccum sp. as the anamorph of Botryosphaeria ribis (Sivanesan 1984). MorganJones and White (1987) discussed the chaotic state of the taxonomy of the anamorph genus Fusicoccum. This genus is considered by some to include the species Fusicoccum aesculi Corda, the possible anamorph of Botryosphaeria dothidea (Moug.:Fr.) Ces. & De Not., and also the Fusicoccum state of Botryosphaeria ribis (Morgan-Jones and White 1987; Farr et al. 1989). Some authors place Botryosphaeria ribis as a synonym of Botryosphaeria dothidea (Barnard et al. 1987; Smith et al. 1994), whereas others keep the two species separate (Farr et al. 1989). Whatever the true taxonomic situation of these fungi, there are several records of Botryosphaeria causing leaf blights that may progress to the stem, and cause twig, shoot or branch cankers on Eucalyptus (but there are no reports of it occurring on Corymbia) (United States Department of Agriculture 1960; Alcorn 1972; Haware et al. 1976; Davison and Tay 1983; Crous et al. 1989b; Farr et al. 1989; Smith et al. 1994). These diseases could result in loss of twigs containing reproductive structures and thus loss of seed. Cankers caused by Botryosphaeria are discussed in Chapter 10 and leaf disease caused by Botryosphaeria ribis is discussed in Chapter 9. Botryosphaeria spp. are usually regarded as weak facultative or opportunistic pathogens (Gibson 1975; Sinclair et al. 1987; Crous et al. 1989a) and stress appears to increase their occurrence on eucalypts (Shearer et al. 1987; Old et al. 1990; Smith et al. 1994). Other fungi reported from capsules of Eucalyptus species (but apparently not Corymbia species) are the coelomycetes Fairmaniella leprosa (Fairm.) Petr. & Syd., Gloeosporium capsularum Cooke & Harkn., Harknessia uromycoides (Speg.) Speg. and Waydora typica (Rodway) B.Sutton, the hyphomycete Polyschema clavulata (Cooke & Harkn.) M.B.Ellis, the discomycetes Polydesmia fructicola Korf, Polydesmia turbinata Raitv. & R.Galán and Pezicula eucalypti Korf. & Iturr., and the agaric, Marasmius eucalypti Berk.

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Fairmaniella leprosa was originally described, as Coniothyrium leprosum Fairm., from capsules of Eucalyptus sp. in California (Millspaugh and Nuttall 1923), but all other records of Fairmaniella leprosa, or its synonym Melanconium eucalypticola Hansf., are as a leaf pathogen on a range of species (see Chapter 9). Gloeosporium capsularum, which is possibly Marssonina carpogena (Cooke & Harkn.) Arx [syn. Gloeosporium carpogenum Cooke & Harkn. (von Arx 1970)], was originally described from ‘capsulis emortis’ on eucalypts in California (Cooke and Harkness 1884a). Apparently based on that record, it has been subsequently reported as occurring on eucalypt capsules (United States Department of Agriculture 1960; Farr et al. 1989) without any mention that the capsules were dead. Harknessia uromycoides has been reported occasionally from eucalypt capsules (Bonar 1928; Nag Raj and DiCosmo 1981; Nag Raj 1993) and is also widespread on eucalypt foliage and twigs (see Chapter 9) (Bonar 1928; Doidge 1950; United States Department of Agriculture 1960; Sutton 1971; Gibson 1975; Sutton 1980; Nag Raj and DiCosmo 1981; Chambers 1982; Cook and Dubé 1989; Farr et al. 1989; Crous et al. 1993). This fungus was first named Melanconium uromycoide Speg. (Spegazzini 1882) from ‘folia dejecta’ of E. globulus in Argentina; a synonym, from Eucalyptus ‘foliis emortuis dejectis’ in California, is Sphaeropsis stictoides Earle (Earle 1902). Harknessia uromycoides has been recorded on several eucalypt species from Africa (Algeria, South Africa), Australia, Europe (Portugal, Spain), South America (Argentina, Bolivia, Peru) and the USA (California, Hawaii) (Spegazzini 1882; Bonar 1928; Doidge 1950; Weiss and O'Brien 1952; Dos Santos De Azevedo 1960; Sutton 1971; Gibson 1975; Sutton 1980; Nag Raj and DiCosmo 1981; Chambers 1982; Cook and Dubé 1989; Farr et al. 1989; Crous et al. 1993; Fisher et al. 1993). Crous et al. (1993) reported that conidiomata of Harknessia uromycoides were found on necrotic leaf tips and leaf litter of Eucalyptus spp., suggesting that it is probably a saprophyte. They also reported that conidiomata were found on petioles and laminae of leaves. In their comparative study of fungal endophytes of E. nitens in Britain and Australia, Fisher et al. (1993) listed Harknessia uromycoides as one of the rare endophytes, without indicating in

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which country or on what tissues it was found. Sutton (1980) and Sutton and Pascoe (1989) indicated that the fungus occurs on dead parts of Eucalyptus spp. Waydora typica (as Pulvinaria typica Rodway) was reported to be common on capsules and opercula of E. globulus in Tasmania (Rodway 1918), thus leaving the unstated possibility that it occurred on living capsules. The same fungus has been recorded on leaves of E. camaldulensis, E. grandis, E. robusta and E. saligna from Hawaii, Florida and South America (Sutton et al. 1976; Sutton 1980; Farr et al. 1989). Although the fungus was occasionally found on leaf laminae, it was usually more abundant on petioles and midribs (Sutton et al. 1976). Polyschema clavulata [syn. Clasterosporium clavulatum (Cooke & Harkn.) Sacc.] was described from decorticated wood of Eucalyptus in California (Cooke and Harkness 1884b; Ellis 1976). Sutton (1979) reported the species from Eucalyptus capsules from western Scotland, at the same time commenting that eucalypt capsules are notoriously poor substrates for microfungi. As the only two previous collections of this fungus were both on Eucalyptus wood (Sutton 1979), it is likely that the record from Scotland was not from living capsules. The discomycete Polydesmia fructicola was found on bark and fallen capsules of E. globulus and a Eucalyptus sp. as well as on peduncles, pods, twigs and wood of Acacia spp. from Madeira and from Tenerife in the Canary Islands (Korf 1978, 1981). Polydesmia fructicola, a new species (Polydesmia turbinata) and an unnamed species of Polydesmia were reported from capsules of E. globulus in Spain (Raitviir and Galán 1995). Another discomycete, Pezicula eucalypti, was described from eucalypt capsules from Tenerife by Iturriaga and Korf (1997). The report by Berkeley (1860) of the agaric, Marasmius eucalypti, on capsules and twigs of some eucalypts from Tasmania probably refers to fallen rather than living capsules and twigs. Cryptococcus neoformans (San Felice) Vuill. var. gattii Vanbreus. & Takashio, the yeast-like anamorph of the basidiomycete Filobasidiella neoformans Kwon-Chung var. bacillispora Kwon-Chung, causes diseases of humans (primarily meningitis and pneumonia), horses and other animals including the koala [Phascolarctos

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cinereus (Goldfuss, 1817)] (Ellis and Pfeiffer 1990b; Riley et al. 1992; Sorrell et al. 1996b; Halliday et al. 1999). The fungus is reported to occur in tropical areas and to have a specific ecological association with several eucalypts, namely E. blakelyi, E. camaldulensis, E. rudis and E. tereticornis (Exsertaria) and E. gomphocephala and E. grandis and also Angophora costata (Halliday et al. 1999). A relatively high incidence of cryptococcosis due to Cryptococcus neoformans var. gattii occurs in some native animal and indigenous human populations in Australia and the disease occurs in other parts of the tropical world where eucalypts, especially E. camaldulensis and E. tereticornis, have been planted (Halliday et al. 1999). Many of the environmental isolates of Cryptococcus neoformans var. gattii are from wood, bark, leaves and litter of eucalypts (Ellis & Pfeiffer 1990a; Halliday et al. 1999). However, the fungus has also been isolated from fruit (capsules) of E. camaldulensis in New South Wales and South Australia (Sorrell et al. 1996a; Halliday et al. 1999) and from flowers of E. camaldulensis in India (Chakrabarti et al. 1997). Although they did not isolate Cryptococcus neoformans var. gattii from the flowers of E. camaldulensis, Ellis and Pfeiffer (1990a) did isolate it from the air spora under flowering E. camaldulensis but not from under non-flowering trees. They further commented that the sudden appearance of Cryptococcus neoformans var. gattii in the environment coincided with the flowering of E. camaldulensis in the study area, that exposure to E. camaldulensis may be required to initiate infection in humans and animals and also that Cryptococcus neoformans var. gattii may have been exported from Australia in association with seed of E. camaldulensis (Ellis and Pfeiffer 1990b).

7.3 Seed fungi of eucalypts Many fungi are capable of destroying seed during its development on the tree, during storage, after sowing or during germination (Chalermpongse 1987; Anderson and Miller 1989). Most of these fungi have been recorded from seed of a range of eucalypt species (Table 7.1). Seed-invading pathogens can be transmitted with the seed into new areas (Chalermpongse 1987). Where seedlings are produced in clean, sterilised containers in relatively pathogen-free media,

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Fungi recorded from eucalypt seed

Fungal species

Eucalypt species

References

Acremomium rutilum W.Gams

E. pellita

Yuan et al. (1997)

Acremomium strictum W.Gams

Eucalyptus spp.

Reddy et al. (1982); Mittal et al. (1990)

Acrostaphylus lignicola Subram.

E. tereticornis, Eucalyptus spp.

Reddy et al. (1982); Mittal et al. (1990)

Alternaria alternata (Fr.) Keissl.

E. camaldulensis, E. grandis, Eucalyptus hybrid, E. nitens, E. pellita, Eucalyptus spp.

Saxena (1985); Mwanza and Kellas (1987); Mittal et al. (1990); Pongpanich (1990); Yuan et al. (1990); Harsh et al. (1992); Yuan et al. (1997)

Alternaria sp.

E. globulus ssp. maidenii, E. grandis

Mittal et al. (1990)

Aspergillus alutaceus Berk. & M.A.Curtis

Eucalyptus spp.

Mehrotra and Singh (1998)

Aspergillus candidus Link

C. citriodora, Eucalyptus spp.

Reddy et al. (1982); Mittal (1985); Mittal et al. (1990)

Aspergillus flavipes (Bainier & Sartory) Thom & Church

Eucalyptus spp.

Reddy et al. (1982); Mittal et al. (1990)

Aspergillus flavus Link

C. citriodora, E. alba, E. deglupta, Eucalyptus hybrid, Eucalyptus spp.

Reddy et al. (1982); Mittal (1985); Saxena (1985); Mittal (1986); Mittal et al. (1990); Pongpanich (1990); Mehrotra and Singh (1998)

Aspergillus fumigatus Fresen.

C. citriodora, E. alba, E. deglupta, Eucalyptus hybrid

Mittal (1985); Mittal (1986); Mittal et al. (1990); Pongpanich (1990)

Aspergillus koningi Oudem.

C. citriodora

Mittal (1985); Mittal et al. (1990)

Aspergillus luchuensis Inui

C. citriodora

Mittal (1985); Mittal et al. (1990)

Aspergillus nidulans (Eidam) G.Winter

E. deglupta, Eucalyptus spp.

Mittal et al. (1990); Pongpanich (1990)

Aspergillus niger Tiegh.

C. citriodora, E. alba, E. camaldulensis, E. deglupta, E. globulus, E. grandis, Eucalyptus hybrid, E. nitens, E. pellita, Eucalyptus spp.

Reddy et al. (1982); Mittal (1985); Saxena (1985); Mittal (1986); Mittal et al. (1990); Yuan et al. (1990); Harsh et al. (1992); Yuan et al. (1997); Mehrotra and Singh (1998)

Aspergillus sulphureus (Fresen.) Thom & Church

C. citriodora; Eucalyptus spp.

Mittal (1985); Mittal et al. (1990); Mehrotra and Singh (1998)

Aspergillus sydowii (Bainier & Sartory) Thom & Church

C. citriodora, Eucalyptus hybrid, Eucalyptus spp.

Reddy et al. (1982); Mittal (1985); Mittal (1986); Mittal et al. (1990)

Aspergillus tamarii Kita

C. citriodora

Mittal (1985); Mittal et al. (1990)

Aspergillus terreus Thom

Eucalyptus spp.

Reddy et al. (1982); Mwanza and Kellas (1987); Mittal et al. (1990)

Aspergillus unguis (Émile-Weil & L.Gaudin) C.W.Dodge

Eucalyptus spp.

Reddy et al. (1982); Mittal et al. (1990)

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Fungi recorded from eucalypt seed (continued)

Fungal species

Eucalypt species

References

Aspergillus sp.

C. citriodora, E. globulus, E. grandis, E. pellita, E. tereticornis

Mittal et al. (1990); Yuan et al. (1997)

Bipolaris tetramera (McKinney) Shoemaker

Eucalyptus spp.

Saxena (1985); Mittal et al. (1990)

Botryodiplodia sp.

E. grandis

Mittal et al. (1990)

Botryotrichum sp.

C. citriodora

Mittal (1985); Mittal et al. (1990)

Botrytis cinerea Pers.

E. camaldulensis, Eucalyptus spp.

Saxena (1985); Mittal et al. (1990); Yuan et al. (1990)

Cephalosporium sp.

C. citriodora, E. deglupta, E. globulus

Mittal et al. (1990)

Chaetomium cochliodes Palliser [this is Chaetomium globosum Kunze]

E. camaldulensis, E. globulus, E. grandis, E. pellita

Yuan et al. (1990); Yuan et al. (1997)

Chaetomium funicola Cooke

E. pellita

Yuan et al. (1997)

Chaetomium globosum Kunze

E. pellita, Eucalyptus spp.

Saxena (1985); Mittal et al. (1990), Yuan et al. (1997)

Chaetomium homopilatum Omvik

C. citriodora

Mittal (1985); Mittal et al. (1990)

Chaetomium sp.

C. citriodora, E. globulus, E. robusta

Mittal et al. (1990); Pongpanich (1990)

Choanephora cf. cucurbitarum (Berk. & Ravenel) Thaxt.

E. pellita

Yuan et al. (1997)

Cladosporium cladosporioides (Fresen.) G.A.de Vries

E. camaldulensis, Eucalyptus hybrid, E. pellita, Eucalyptus spp.

Saxena (1985); Mittal (1986); Mittal et al. (1990); Yuan et al. (1990); Harsh et al. (1992); Yuan et al. (1997); Mehrotra and Singh (1998)

Cladosporium herbarum (Pers.) Link

Eucalyptus spp.

Reddy et al. (1982); Saxena (1985); Mittal et al. (1990)

Cladosporium orchidis E.A.Ellis & M.B.Ellis

E. pellita

Yuan et al. (1997)

Cladosporium oxysporum Berk. & M.A.Curtis

C. citriodora

Mittal (1985)

Cladosporium tenuissimum Cooke

Eucalyptus spp.

Reddy et al. (1982); Mittal et al. (1990)

Cladosporium sp.

C. citriodora

Mittal et al. (1990)

Colletotrichum sp.

C. citriodora

Mittal et al. (1990)

Coniella australiensis Petr.

E. pellita

Yuan et al. (1997)

Coniochaeta ligniaria (Grev.) Cooke

E. pellita

Yuan et al. (1997)

Curvularia eragrostidis (Henn.) J.A.Mey.

E. alba, E. pellita

Pongpanich (1990); Yuan et al. (1997)

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Curvularia fallax Boedijn

E. pellita

Yuan et al. (1997)

Curvularia geniculata (Tracy & Earle) Boedijn

Eucalyptus spp.

Reddy et al. (1982); Mittal et al. (1990)

Curvularia inaequalis (Shear) Boedijn

C. citriodora

Mittal (1985); Mittal et al. (1990)

Curvularia lunata (Wakker) Boedijn

E. camaldulensis, E. deglupta, E. grandis, Eucalyptus hybrid, E. pellita, E. robusta, E. tereticornis, Eucalyptus spp.

Reddy et al. (1982); Mittal et al. (1990); Pongpanich (1990); Yuan et al. (1990); Harsh et al. (1992); Yuan et al. (1997); Mehrotra and Singh (1998)

Curvularia lunata var. aeria (Bat., I.H.Lima & C.T.Vasconc.) M.B.Ellis

Eucalyptus spp.

Saxena (1985)

Curvularia pallescens Boedijn

C. citriodora, E. alba, E. camaldulensis, E. deglupta, Eucalyptus hybrid, E. robusta, Eucalyptus spp.

Reddy et al. (1982); Mittal (1985); Saxena (1985); Mittal (1986); Mittal et al. (1990); Pongpanich (1990)

Curvularia pubescens [(sic) possibly Curvularia pallescens]

C. citriodora

Mittal et al. (1990)

Curvularia senegalensis (Speg.) Subram.

E. camaldulensis, E. laevopinea, E. nitens

Yuan et al. (1990); Yuan et al. (1997)

Curvularia verruculosa M.B.Ellis

Eucalyptus hybrid, Eucalyptus spp.

Saxena (1985); Mittal (1986); Mittal et al. (1990)

Curvularia sp.

E. alba, E. globulus ssp. maidenii, E. grandis

Mittal et al. (1990)

Cylindrocladium scoparium Morgan

Eucalyptus spp.

Mittal et al. (1990)

Dothiorella eucalypti (Berk. & Broome) Sacc.

E. camaldulensis

Farr et al. (1989)

Drechslera australiensis (Bugnic.) M.B.Ellis

E. pellita, Eucalyptus spp.

Saxena (1985); Mittal et al. (1990); Yuan et al. (1997)

Drechslera spicifera (Bainier) Arx

E. camaldulensis

Yuan et al. (1990)

Drechslera sp.

E. grandis

Mittal et al. (1990)

Emericella nidulans (Eidam) Vuill.

Eucalyptus spp.

Reddy et al. (1982)

Epicoccum nigrum Link

E. camaldulensis, E. grandis, E. nitens, Eucalyptus spp.

Mwanza and Kellas (1987); Yuan et al. (1990)

Exserohilum rostratum (Drechsler) K.J.Leonard & Suggs, emen. K.J.Leonard

E. saligna, E. tereticornis, Eucalyptus spp.

Reddy et al. (1982); Saxena (1985); Mittal et al. (1990)

Fairmaniella leprosa (Fairm.) Petr. & Syd.

E. camaldulensis, Eucalyptus spp.

Farr et al. (1989)

Fusarium equiseti (Corda) Sacc.

E. deglupta, Eucalyptus spp.

Saxena (1985); Mittal et al. (1990)

Fusarium graminearum Schwabe

Eucalyptus spp.

Mehrotra and Singh (1998)

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Fungi recorded from eucalypt seed (continued)

Fungal species

Eucalypt species

References

Fusarium moniliforme J.Sheld.

E. camaldulensis, E. grandis, E. tereticornis, Eucalyptus spp.

Reddy et al. (1982); Saxena (1985); Mittal et al. (1990); Pongpanich (1990)

Fusarium oxysporum Schltdl. emen. W.C.Snyder & H.N.Hansen

E. deglupta, Eucalyptus spp.

Saxena (1985); Mittal et al. (1990)

Fusarium poae (Peck) Wollenw.

Eucalyptus spp.

Saxena (1985); Mittal et al. (1990)

Fusarium semitectum Berk. & Ravenel

E. camaldulensis, E. globulus ssp. maidenii, Eucalyptus spp.

Saxena (1985); Mittal et al. (1990); Mehrotra and Singh (1998)

Fusarium solani (Mart.) Sacc.

C. citriodora, E. camaldulensis

Mittal (1985); Michail et al. (1986); Mittal et al. (1990); Yuan et al. (1990)

Fusarium spp.

C. citriodora, E. globulus, Eucalyptus hybrid, E. pellita

Mittal et al. (1990); Yuan et al. (1997)

Fusicoccum sp.

C. citriodora

Mittal et al. (1990)

Gliocephalotrichum sp.

C. citriodora

Mittal et al. (1990)

Gliocladium penicillioides Corda

C. citriodora

Mittal (1985); Mittal et al. (1990)

Gliocladium roseum Bainier

E. camaldulensis, E. pellita

Yuan et al. (1990); Yuan et al. (1997)

Gloeosporium capsularum Cooke & Harkn.

Eucalyptus spp.

Farr et al. (1989)

Harknessia fumaginea B.Sutton & Alcorn

E. pellita

Yuan et al. (1997)

Harknessia hawaiiensis F.Stevens & E.Young

E. pellita

Yuan et al. (1997)

Harknessia uromycoides (Speg.) Speg.

E. globulus, E. odorata, Eucalyptus spp.

Farr et al. (1989)

Humicola cf. fuscoatra Traaen

E. pellita

Yuan et al. (1997)

Lewia infectoria (Fuckel) M.E.Barr & E.G.Simmons (syn. Pleospora infectoria Fuckel)

Eucalyptus spp.

Saxena (1985); Mittal et al. (1990)

Macrophoma sp.

C. citriodora, E. camaldulensis

Michail et al. (1986); Chalermpongse (1987); Mittal et al. (1990)

Macrophomina phaseolina (Tassi) Goid.

Eucalyptus spp.

Saxena (1985); Mittal et al. (1990)

Macrophomina sp.

E. camaldulensis

Pongpanich (1990)

Memnoniella echinata (Rivolta) L.D.Galloway

E. camaldulensis, Eucalyptus hybrid, E. tereticornis, Eucalyptus spp.

Reddy et al. (1982); Mittal (1986); Mittal et al. (1990); Yuan et al. (1990)

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Monocillium sp.

C. citriodora, E. globulus, E. grandis, E. tereticornis

Mittal et al. (1990)

Mucor hiemalis Wehmer

Eucalyptus spp.

Saxena (1985); Mittal et al. (1990)

Mucor plumbeus Bonord.

Eucalyptus spp.

Mwanza and Kellas (1987)

Mucor sp.

E. deglupta, E. globulus, E. grandis, Eucalyptus hybrid, E. tereticornis

Mittal et al. (1990); Pongpanich (1990)

Myrothecium roridum Tode:Fr.

E. grandis, Eucalyptus spp.

Saxena (1985); Mittal et al. (1990)

Nectria sp.

E. pellita

Yuan et al. (1997)

Paecilomyces spp.

C. citriodora, E. alba, E. deglupta, E. globulus

Mittal et al. (1990); Pongpanich (1990)

C H A P T E R

Penicillium albicans Bainier

C. citriodora, Eucalyptus hybrid

Mittal (1985); Mittal (1986); Mittal et al. (1990)

Penicillium arenicola Chalab.

C. citriodora

Mittal (1985); Mittal et al. (1990)

Penicillium brevicompactum Dierckx

Eucalyptus spp.

Mwanza and Kellas (1987)

Penicillium chrysogenum Thom

Eucalyptus hybrid, Eucalyptus spp.

Saxena (1985); Mittal et al. (1990); Harsh et al. (1992)

Penicillium citrinum Thom

Eucalyptus spp.

Reddy et al. (1982); Mittal et al. (1990); Mehrotra and Singh (1998)

Penicillium decumbens Thom

C. citriodora

Mittal (1985); Mittal et al. (1990)

Penicillium dodgei Pitt

C. citriodora, Eucalyptus spp.

Mittal (1985); Mittal et al. (1990); Mehrotra and Singh (1998)

Penicillium expansum Link

C. citriodora, E. pellita

Mittal (1985); Mittal et al. (1990); Yuan et al. (1997)

Penicillium glabrum (Wehmer) Westling

E. camaldulensis, E. grandis, Eucalyptus spp.

Saxena (1985); Mittal et al. (1990); Yuan et al. (1990)

Penicillium kloeckeri Pitt

Eucalyptus spp.

Saxena (1985); Mittal et al. (1990)

Penicillium olsonii Bainier & Sartory

Eucalyptus spp.

Mwanza and Kellas (1987)

Penicillium purpurogenum Stoll

C. citriodora

Mittal (1985); Mittal et al. (1990)

Penicillium spinulosum Thom

Eucalyptus spp.

Mwanza and Kellas (1987)

Penicillium variabile Sopp

C. citriodora

Mittal (1985); Mittal et al. (1990)

Penicillium spp.

C. citriodora, E. camaldulensis, E. deglupta, E. globulus, E. globulus ssp. maidenii, E. grandis, E. pellita, E. tereticornis

Quiniones and Zamora (1987); Mittal et al. (1990); Pongpanich (1990); Yuan et al. (1997)

Periconia spp.

Eucalyptus spp.

Mittal et al. (1990)

Pestalotia sp.

E. deglupta

Quiniones and Zamora (1987); Mittal et al. (1990)

Pestalotiopsis disseminata (Thüm.) Steyaert

E. pellita

Yuan et al. (1997)

Pestalotiopsis funerea (Desm.) Steyaert E. alba, E. grandis

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Fungi recorded from eucalypt seed (continued)

Fungal species

Eucalypt species

References

Pestalotiopsis mangiferae (Henn.) Steyaert

E. tereticornis, Eucalyptus spp.

Reddy et al. (1982); Mittal et al. (1990)

Pestalotiopsis neglecta (Thüm.) Steyaert

E. pellita

Yuan et al. (1997)

Pestalotiopsis sp.

E. globulus ssp. maidenii, E. pellita

Mittal et al. (1990); Yuan et al. (1997)

Phoma eucalyptica Sacc.

E. amplifolia, E. angulosa, E. coccifera, E. dives, E. fastigata, E. kybeanensis, E. laevopinea, E. microcorys, E. nidularisA, E. nova-anglica, E. pauciflora, E. pulverulenta, E. radiata ssp. robertsonii, E. rodwayi, E. saligna, E. stricta, E. tasmanicaB

Girard (1973)

Phoma sp.

E. alba, E. camaldulensis, E. deglupta, E. grandis, E. pellita, Eucalyptus spp.

Mittal et al. (1990); Yuan et al. (1997)

Phomopsis sp.

C. citriodora

Mittal et al. (1990)

Pithomyces maydicus (Sacc.) M.B.Ellis

E. tereticornis, Eucalyptus spp.

Reddy et al. (1982); Mittal et al. (1990)

Preussia sp.

E. pellita

Yuan et al. (1997)

Pythium sp.

C. citriodora

Mittal (1985); Mittal et al. (1990)

Ramularia sp.

E. crebra, E. drepanophylla, E. crebra × E. melanophloia, E. melanophloia × E. crebra, E. populnea × E. crebra, E. melanophloia, E. populnea, Eucalyptus spp.

Drake (1974); Drake (1981a, 1981b); Gill (1981); Mittal et al. (1990)

Rhizopus oryzae Went & Prins. Geerl. (syn. Rhizopus arrhizus A.Fisch.)

C. citriodora, Eucalyptus hybrid, Eucalyptus spp.

Mittal (1985); Saxena (1985); Mittal (1986); Mittal et al. (1990)

Rhizopus stolonifer (Ehrenb.:Fr.) Vuill.

E. camaldulensis, E. globulus, E. grandis, E. pellita, Eucalyptus spp.

Mwanza and Kellas (1987); Yuan et al. (1990); Yuan et al. (1997)

Rhizopus sp.

E. deglupta, E. grandis

Mittal et al. (1990); Pongpanich (1990)

Spicaria sp.

Eucalyptus spp.

Mehrotra and Singh (1998)

Stachybotrys atra Corda

E. nitens, E. tereticornis, Eucalyptus spp.

Reddy et al. (1982); Saxena (1985); Mittal et al. (1990); Yuan et al. (1990)

Stachybotrys sp.

E. globulus

Mittal et al. (1990)

Syncephalastrum racemosum Cohn

E. alba, E. pellita

Mittal et al. (1990); Pongpanich (1990); Yuan et al. (1997)

Thamnostylum lucknowense (J.N.Rai, J.P.Tewari & Mukerji) Arx & H.P.Upadhyay

Eucalyptus hybrid

Mittal (1986); Mittal et al. (1990)

Torula sp.

Eucalyptus hybrid

Harsh et al. (1992)

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Trichoderma viride Pers.

C. citriodora, E. globulus ssp. maidenii, Eucalyptus hybrid, E. pellita

Mittal (1985); Mittal (1986); Mittal et al. (1990); Yuan et al. (1997)

Trichothecium roseum (Pers.) Link

E. camaldulensis, Eucalyptus hybrid, E. pellita, Eucalyptus spp.

Saxena (1985); Mittal et al. (1990); Yuan et al. (1990); Harsh et al. (1992); Yuan et al. (1997)

Ulocladium atrum Preuss

Eucalyptus spp.

Mwanza and Kellas (1987)

Verticillium albo-atrum Reinke & Berthold

Eucalyptus spp.

Saxena (1985); Mittal et al. (1990)

Verticillium sp.

E. grandis, Eucalyptus hybrid

Mittal et al. (1990); Harsh et al. (1992)

Xylaria sp.

Eucalyptus spp.

Mehrotra and Singh (1998)

A

7

B

Unknown taxon; E. tasmanica, identity uncertain, either E. delegatensis R.T.Baker ssp. tasmaniensis Boland or E. tenuiramis Miq.

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contaminated seed can be a major means of pathogen introduction (Campbell and Landis 1990). Seedborne pathogens cause damage by reducing viability of seed or by infecting seedlings after germination (Anderson and Miller 1989) and causing damping-off, blight, wilt, anthracnose, leaf spot, cankers or mosaic diseases (Chalermpongse 1987). A distinction can be made between two categories of seed-invading fungi—‘field fungi’ and ‘storage fungi’ (Neergaard 1979). Field fungi are species that invade seed on the plants in the field. They often invade the maturing seed or the seed after harvesting but before processing, and may be either pathogens or saprophytes. Common field fungi that occur in or on seed are: Alternaria spp. [Alternaria alternata (Fr.) Keissl. (reported as Alternaria tenuis Nees)]; Botryodiplodia spp.; Cladosporium herbarum (Pers.) Link; Curvularia spp. [Curvularia lunata (Wakker) Boedijn and Curvularia pallescens Boedijn]; Exserohilum rostratum (Drechsler) K.J.Leonard & Suggs, emen. K.J.Leonard [reported as both Drechslera halodes (Drechsler) Subram. & B.L.Jain and Drechslera rostrata (Drechsler) M.J.Richardson & E.M.Fraser]; Epicoccum nigrum Link (reported as Epicoccum purpurascens Ehrenb.); Fusarium spp. (Fusarium moniliforme J.Sheld., Fusarium oxysporum Schltdl. emen. W.C.Snyder & H.N.Hansen and Fusarium semitectum Berk. & Ravenel); Pestalotiopsis spp.; a Phoma sp.; and Verticillium albo-atrum Reinke & Berthold. To these may be added a range of other pathogenic fungi reported from eucalypt seed. For example, Chalermpongse (1987) reported 1% infection of E. camaldulensis seed by a Macrophomina sp., and a seedborne Verticillium sp. caused up to 80% damping-off in plants from a seed sample of Eucalyptus hybrid in India (Harsh et al. 1992). The field fungi may cause discolouration of seed, reduced germination and diseases of seedlings or growing plants. The activity of the field fungi is usually arrested during seed storage because they require high relative humidity (above 95%) for growth. Only a small proportion (< 10%) of the seed of E. obliqua and E. radiata collected from mature and semi-mature capsules in the field was contaminated by fungi (Mwanza and Kellas 1987). The most common species isolated was Alternaria alternata, which was also found in seed of E. camaldulensis, E. grandis and E. nitens from Australia (Yuan et al.

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1990), on seed of E. pellita from Indonesia (Yuan et al. 1997) and was associated with seed of E. camaldulensis in Thailand (Mittal et al. 1990). The same species occurred both on and within seed of eucalypts and caused rotting of seed and necrosis of radicles followed by seedling death (Saxena 1985). Fusarium solani (Mart.) Sacc. was shown to be seedborne in E. camaldulensis in Egypt and a seedborne isolate was pathogenic on a range of eucalypt species (Michail et al. 1986). A seedborne Verticillium sp. caused up to 80% mortality of Eucalyptus hybrid seedlings in India (Harsh et al. 1992). In inoculation tests using single isolates of five fungal species, Aspergillus niger Tiegh., Harknessia fumaginea B.Sutton & Alcorn and Pestalotiopsis disseminata (Thüm.) Steyaert reduced germination and killed seedlings of some seed lots of E. pellita. Drechslera australiensis (Bugnic.) M.B.Ellis had no effect on germination but caused the maximum seedling mortality observed in the study and Syncephalastrum racemosum Cohn affected neither germination nor seedling mortality (Yuan et al. 1997). Storage fungi are species that grow on stored products including seed and are generally specialised fungi that are able to grow without free water, and on substrates with a high osmotic pressure. Most storage fungi are species of Aspergillus and Penicillium which are active at relative humidities ranging from 70% to 90%. Well-known species of storage fungi are Aspergillus niger, Aspergillus flavus Link and Aspergillus fumigatus Fresen. (Chalermpongse 1987). Other storage fungi are from genera such as Cladosporium, Chaetomium, Mucor and Rhizopus. Some are able to grow even at low temperatures. Such fungi usually do not invade seeds before harvest although they may be found on the seed at very low levels, perhaps providing inoculum for development of the fungi during storage. They may be present as contaminants on the seed surfaces or as dormant mycelium within the tissues of the pericarp or seed coat.

7.4 Control of seed fungi Seedborne fungi are best controlled by the use of procedures during harvesting and processing of seed that prevent contamination of the seed with soilborne fungi and by use of controlled storage conditions (low humidity and low temperature,

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i.e. 5°C or lower) which reduce the activity of fungi in storage (Chalermpongse 1987).

not recommended because of their toxicity to humans.

Some of the fungi reported from eucalypt seed are common soilborne species (e.g. Fusarium solani, Macrophomina spp., Verticillium spp.), suggesting that their association with the seed derives from contamination during harvesting and processing rather than from invasion of the capsules growing on the tree many metres above ground. Experience in the large eucalypt plantation industries of Brazil and South Africa has shown that with adequate technology and hygiene during the collecting, processing and storage of seed, as well as during seedling production, the effect of diseases of seed and seedlings can be minimised (Donald 1986; Ferreira 1989; Ferreira et al. 1991). Seed should be collected from capsules that are not in contact with the ground or other sources of inoculum of soilborne pathogens, processed under a system of rigorous hygiene, and stored hygienically at temperatures and relative humidities that inhibit fungal activity.

Campbell and Landis (1990) suggested a series of steps for managing seedborne disease. To avoid the unnecessary use of potentially damaging seed treatments, it is first important to determine if seed treatment is warranted. Because it is impossible to identify contaminated seed lots simply by looking at them, samples of seed from problem lots should be assayed in a laboratory for the presence of seedborne pathogens. Once a problem seed lot has been identified it can be treated. Treatment is likely to be necessary for seed that is to be grown in the relatively sterile environment of enclosed container nurseries, and for seed lots with particular problems such as low germination rates, visible mould or a history of poor germination or seedling disease; it is also likely to be necessary for high-risk species that typically suffer high levels of soilborne disease in the nursery and for high value seed such as that arising from tree improvement programs.

Chalermpongse (1987) suggested that the simplest procedure to control seedborne diseases is to check the condition of seed lots before sowing and reject the infected ones or treat them with seed protectants if clean seed lots are not available. Chemical seed protectants such as benomyl, carboxin, triforine, chlorothalonil, thiram and captan have been recommended (Chalermpongse 1987). Seed treatment with 0.2% thiophanatemethyl, carbendazim or mancozeb were effective (in decreasing order of effectiveness) in reducing losses of Eucalyptus hybrid caused by seedborne Verticillium (Harsh et al. 1992). The cost of raising forest nursery seedlings can be reduced 50% to 70% with fungicide treatment of seed (Harsh and Gupta 1993). Fungal development on germinating eucalypt seed was restricted and germinative capacity increased by hot water treatments (50°C for 5, 10 or 20 minutes), surface disinfection (10% sodium hypochlorite or 33% hydrogen peroxide for 1, 2 or 4 minutes) and fungicide application (captan at 1%) (Donald and Lundquist 1988). Several other fungicides used singly [2-methoxyethylmercury chloride, carbendazim (both at 2 g/kg of seed), thiram and mancozeb (both at 4 g/kg of seed)] were also shown to inhibit the seed mycoflora of eucalypts (Mehrotra and Singh 1998). However, the use of mercury compounds is

7.5 Conclusion A wide range of fungi has been reported to be associated with eucalypt capsules and seed. A few are pathogens of living tissues but most appear to be common soilborne fungi that are surface contaminants of the seed. As the latter gain access to the seed during its collection, processing or storage, there are many simple hygiene procedures that can be used to minimise their effects. There are also well-tested seed treatments that can be used to minimise the damage caused by seedborne fungi during production of nursery stock.

7.6 References Alcorn, J.L. (1972). Some new records of Queensland fungi. Queensland Journal of Agricultural and Animal Sciences 29, 71–77. Anderson, R.L. and Miller, T. (1989). Seed fungi. In Forest Nursery Pests. USDA Forest Service, Agriculture Handbook No. 680. (Technical co-ordinators C.E. Cordell, R.L. Anderson, W.H. Hoffard, T.D. Landis, R.S. Smith Jr. and H.V. Toko) pp. 126–127. (USDA Forest Service: Washington, DC.) Arx, J.A. von (1970). A revision of the fungi classified as Gloeosporium. Second Edition, revised and translated from German. Bibliotheca Mycologica Band 24, 106. Barnard, E.L., Geary, T., English, J.T. and Gilly, S.P. (1987). Basal cankers and coppice failure of

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Eucalyptus grandis in Florida. Plant Disease 71, 358–361. Berkeley, M.J. (1860). Fungi. In The Botany of the Antarctic Voyage of H. M. Discovery Ships Erebus and Terror in the Years 1839–1843. Part III. Flora Tasmaniae (Ed. J.D. Hooker) Volume 2, pp. 241–282. (Reprinted 1963, J. Cramer: Kleinheim.) Berkeley, M.J. and Broome, C.E. (1887). XI. List of fungi from Queensland and other parts of Australia; with descriptions of New Species. Part III. The Transactions of the Linnaean Society of London, Second Series (Botany) 2, 217–224. Bonar, L. (1928). Studies on some California fungi. Mycologia 20, 292–300. Campbell, S.J. and Landis, T.D. (1990). Managing seedborne diseases in Western forest nurseries. Tree Planters' Notes 41, 3–7. Chakrabarti, A., Jatana, M., Kumar, P., Chatha, L., Kaushal, A. and Padhye, A.A. (1997). Isolation of Cryptococcus neoformans var. gattii from Eucalyptus camaldulensis in India. Journal of Clinical Microbiology 35, 3340–3342. Chalermpongse, A. (1987). Current potentially dangerous forest tree diseases in Thailand. Biotrop Special Publication 26, 77–90. Chambers, S.C. (1982). List of diseases recorded on ornamentals, native plants and weeds in Victoria, before 30 June, 1980. Technical Report Series No. 61, pp. 1–104. Department of Agriculture, Victoria: Melbourne.) Cook, R.P. and Dubé, A.J. (1989). Host-Pathogen Index of Plant Diseases in South Australia. (South Australian Department of Agriculture: Adelaide.) Cooke, M.C. and Harkness, H.W. (1884a). In Sylloge Fungorum 3, 718. Cooke, M.C. and Harkness, H.W. (1884b). In Sylloge Fungorum 4, 390. Crous, P.W., Knox-Davies, P.S. and Wingfield, M.J. (1989a). A summary of fungal leaf pathogens of Eucalyptus and the diseases they cause in South Africa. South African Forestry Journal 149, 9–16. Crous, P.W., Knox-Davies, P.S. and Wingfield, M.J. (1989b). Newly-recorded foliage fungi of Eucalyptus spp. in South Africa. Phytophylactica 21, 85–88. Crous, P.W., Wingfield, M.J. and Nag Raj, T.R. (1993). Harknessia species occurring in South Africa. Mycologia 85, 108–118. Davison, E.M. and Tay, F.C.S. (1983). Twig, branch, and upper trunk cankers of Eucalyptus marginata. Plant Disease 67, 1285–1287. Doidge, E.M. (1950). The South African fungi and lichens to the end of 1945. Bothalia 5, 1–1094. Donald, D.G.M. (1986). South African nursery practice— the state of the art. South African Forestry Journal 139, 36–47.

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Donald, D.G.M. and Lundquist, J.E. (1988). Treatment of Eucalyptus seed to maximise germination. South African Forestry Journal 147, 9–15. Dos Santos De Azevedo, N.F. (1960). [Eucalyptus diseaes reported in Portugal.] F.Z.O./S.C.M./E.U./60-3 g 4-Portugal. Abstract from Review of Applied Mycology 41, 619–620 (1962). Drake, D.W. (1974). Fungal and insect attack of seeds in unopened Eucalyptus capsules. Search 5, 444. Drake, D.W. (1981a). Reproductive success of two Eucalyptus hybrid populations. I. Generalized seed output model and comparison of fruit parameters. Australian Journal of Botany 29, 25–35. Drake, D.W. (1981b). Reproductive success of two Eucalyptus hybrid populations. II. Comparison of predispersal seed parameters. Australian Journal of Botany 29, 37–48. Earle, F.S. (1902). in Sylloge Fungorum 18, 314 (1906). Ellis, M.B. (1976). More Dematiaceous Hyphomycetes. (Commonwealth Mycological Institute: Kew.) Ellis, D.H. and Pfeiffer T.J. (1990a). Natural habitat of Cryptococcus neoformans var. gattii. Journal of Clinical Microbiology 28, 1642–1644. Ellis, D.H. and Pfeiffer T.J. (1990b). Ecology, life cycle, and infectious propagule of Cryptococcus neoformans. The Lancet 336, 923–925. Farr, D.F., Bills, G.F., Chamuris, G.P. and Rossman, A.Y. (1989). Fungi on Plants and Plant Products in the United States. (American Phytopathological Society Press: St Paul, MI, USA.) Ferreira, F.A. (1989). Patologia Florestal; Principais Doenças Florestais no Brasil. (Sociedade de Investigações Florestais: Viçosa.) Ferreira, F.A., Muchovej, J.J., Demuner, N.L. and Alfenas, A.C. (1991). Biotests for determining fungicide efficacy against conidia and mycelium of Cylindrocladium scoparium and Rhizoctonia solani. In Diseases and Insects in Forest Nurseries. Proceedings of the First Meeting IUFRO Working Party, Victoria, British Columbia, Canada, 22–30 August 1990. (Eds J.R. Sutherland and S.G. Glover) pp. 243–247. (Forestry Canada, Pacific and Yukon Region, Pacific Forestry Centre: Victoria, British Columbia.) Fisher, P.J., Petrini, O. and Sutton, B.C. (1993). A comparative study of fungal endophytes in leaves, xylem and bark of Eucalyptus in Australia and England. Sydowia 45, 338–345. Gibson, I.A.S. (1975). Diseases of Forest Trees Widely Planted as Exotics in the Tropics and Southern Hemisphere. Part 1. Important Members of the Myrtaceae, Leguminosae, Verbenaceae and Meliaceae. (Commonwealth Mycological Institute: Kew, Surrey and Commonwealth Forestry Institute: Oxford.) Gill, A.M. (1981). Adaptive responses of Australian vascular plant species to fire. In Fire and the Australian Biota. (Eds A.M. Gill, R.H. Groves and

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I.R. Noble) pp. 251–271. (Australian Academy of Science: Canberra.) Girard, D.H. 1973. List of Intercepted Plant Pests, 1971. (Animal and Plant Health Inspection Service, United States Department of Agriculture: Washington, DC.)) Halliday, C.L., Bui, T., Krockenberger, M., Malik, R., Ellis, D.H. and Carter, D.A. (1999). Presence of α and a mating types in environmental and clinical collections of Cryptococcus neoformans var. gattii strains from Australia. Journal of Clinical Microbiology 37, 2920–2926. Harsh, N.S.K. and Gupta, B.N. (1993). Economics of chemical control of root diseases in forest nurseries. In Programme and Abstracts, Impact of Diseases and Insect Pests in Tropical Forests. IUFRO Symposium Organized Jointly by S2.07-07: Protection of Forests in the Tropics (Subject Group: Entomology) and S2.06-15: Diseases in Tropical Plantations (Subject Group: Pathology), 23–26 November 1993, Kerala Forest Research Institute, Peechi, Kerala, India. Harsh, N.S.K., Dadwal, V.S. and Jamaluddin (1992). A new post-emergence damping-off disease of Eucalyptus seedlings. Indian Forester 118, 279–283. Haware, M.P., Sharma, N.D. and Joshi, L.K. (1976). Fungi on Eucalyptus globulus from Jabalpur. JNKVV Research Journal 10 Supplement, 96–97. Iturriaga, T. and Korf, R.P. (1997). A preliminary Discomycete flora of Macronesia: Part 10a, Dermataceae. Mycotaxon 61, 223–241. Kamnerdratana, P.-Y., Chalermpongse, A. and Kirtibutr, N. (1987). Forest pests and diseases in Thailand. Biotrop Special Publication 26, 67–76. Korf, R.P. (1978). Revisionary studies in the Arachnopezizoideae: a monograph of the Polydesmieae. Mycotaxon 7, 457–492. Korf, R.P. (1981). A preliminary discomycete flora of Macaronesia: Part 2. Hyaloscyphaceae subf. Arachnopezizoideae. Mycotaxon 13, 137–144. Mehrotra, M.D. and Singh, P. (1998). Study on seed borne fungi of some forest trees and their management. Indian Journal of Forestry 21, 345–354. Michail, S.H., El-Sayed, A.B. and Salem, M.A. (1986). Fusarium post-emergence damping-off of Eucalyptus and its control measures in Egypt. Acta Phytopathologia et Entomologica Hungarica 21, 127–133. Millspaugh, C.F. and Nuttall, L.W. (1923). Flora of Santa Catalina Island. Publication of the Field Museum of Natural History Botanical Series 5 (No. 212), pp. 314–357. [in Index of Fungi 5, 749 1988]. Mittal, R.K. (1985). Tree seed pathology. Science and Culture 51, 291–294. Mittal, R.K. (1986). Studies on the mycoflora and its control on the seeds of some forest trees: III. Eucalyptus Hybrid. The Malaysian Forester 49, 151–159.

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Mittal, R.K, Anderson, R.L. and Mathur, S.B. (1990). Microorganisms associated with tree seeds: World Checklist 1990, Information Report PI-X-96, (Petawa National Forestry Institute, Forestry Canada: Chalk River, Ontario.) Morgan-Jones, G. and White, J.F. (1987). Notes on Coelomycetes. II. Concerning the Fusicoccum anamorph of Botryosphaeria ribis. Mycotaxon 30, 117–125. Mwanza, E.J.M. and Kellas, J.D. (1987). Identification of the fungi associated with damping-off in the regeneration of Eucalyptus obliqua and E. radiata in a central Victorian forest. European Journal of Forest Pathology 17, 237–245. Nag Raj, T.R. (1993). Coelomycetous Anamorphs with Appendage-bearing Conidia. (Mycologue Publications: Waterloo, Ontario, Canada.) Nag Raj, T.R. and DiCosmo, F. (1981). A monograph of Harknessia and Mastigosporella with notes on associated teleomorphs. Bibliotheca Mycologica 80, 1–62. Neergaard, P. (1979). Seed Pathology Volume 1 (Revised Edition). (The Macmillan Press: London.) Old, K.M., Gibbs, R., Craig, I., Myers, B.J. and Yuan, Z.Q. (1990). Effect of drought and defoliation on the susceptibility of eucalypts to cankers caused by Endothia gyrosa and Botryosphaeria ribis. Australian Journal of Botany 38, 571–581. Pongpanich, K. (1990). Fungi associated with forest tree seeds in Thailand. In Proceedings of the IUFRO Workshop on Pests and Diseases of Forest Plantations. RAPA Publication:1990/9:114–120. (Eds C. Hutacharern, K.G. MacDicken, M.H. Ivory and K.S.S. Nair). (Food and Agriculture Organization of the United Nations, Regional Office for Asia and the Pacific: Bangkok.) Quiniones, S.S. and Zamora, R.A. (1987). Forest pests and diseases in the Philippines. Biotrop Special Publication 26, 43–65. Raitviir, A. and Galán, R. (1995). The genus Polydesmia in Spain. Mycotaxon 53, 447–454. Reddy, B.S., Sehgal, H.S. and Manoharachary, C. (1982). Studies on seed mycoflora of certain species of Eucalyptus. Acta Botanica Indica 10, 302–303. Riley, C.B., Bolton, J.R., Mills, J.N. and Thomas, J.B. (1992). Cryptococcosus in seven horses. Australian Veterinary Journal 69, 135–139. Rodway, L. (1918). Botanical notes. Papers & Proceedings of the Royal Society of Tasmania for the Year 1917, 105–110. Saxena, R.M. (1985). Seedling mortality of Eucalyptus spp. caused by seed mycoflora. Indian Phytopathology 38, 151–152. Sharma, J.K., Mohanan, C. and Florence, E.J.M. (1985). Disease survey in nurseries and plantations of forest tree species grown in Kerala. KFRI Research

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Report 36. (Kerala Forest Research Institute: Peechi, Kerala, India.) Shearer, B.L., Tippett, J.T. and Bartle, J.R. (1987). Botryosphaeria ribis infection associated with death of Eucalyptus radiata in species selection trials. Plant Disease 71, 140–145. Sinclair, W.A., Lyon, H.H. and Johnson, W.T. (1987). Diseases of Trees and Shrubs. (Comstock Publishing Associates, Cornell University Press: Ithaca, NY, USA.) Sivanesan, A. (1984). The Bitunicate Ascomycetes and Their Anamorphs. (J. Cramer: Vaduz.) Smith, H., Kemp, G.H.J. and Wingfield, M.J. (1994). Canker and die-back of Eucalyptus in South Africa caused by Botryosphaeria dothidea. Plant Pathology 43, 1031–1034. Sorrell, T.C., Chen, A.A., Ruma, P., Meyer, W., Pfeiffer, T.J., Ellis, D.H. and Brownlee, A.G. (1996a). Concordance of clinical and environmental isolates of Cryptococcus neoformans var. gattii by Random Amplification of Polymorphic DNA Analysis and PCR Fingerprinting. Journal of Clinical Microbiology 34, 1253–1260. Sorrell, T.C., Brownlee, A.G., Ruma, P., Malik, R., Pfeiffer, T.J. and Ellis, D.H. (1996b). Natural environmental sources of Cryptococcus neoformans var. gattii. Journal of Clinical Microbiology 34, 1261–1263. Sousa da Câmara, E. de S. (1949). Agronomia Lusitana 11:52. [in Index of Fungi 2(2):38 1951] Spegazzini, C. (1882). Fungi Argentini: additis Nonnullis Brasiliensibus Montevideensibusque, Pugillus quartus. Anales de la Sociedad Cientifica Argentina. Buenos Aires 13, 11–35, 60–64. Reprinted 1971. pp. 231–260. (Linnaeus Press: Amsterdam.) Sutton, B.C. (1971). Coelomycetes. IV. The genus Harknessia and similar fungi on Eucalyptus. Commonwealth Mycological Institute, Kew, Mycological Papers 123.

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Sutton, B.C. (1979). Exotic fungi from Western Scotland. Bulletin of the British Mycological Society 13, 105–106. Sutton, B.C. (1980). The Coelomycetes, Fungi Imperfecti with Pycnidia, Acervuli and Stroma. (Commonwealth Mycological Institute: Kew.) Sutton, B.C. and Pascoe, I.G. (1989). Addenda to Harknessia (Coelomycetes). Mycological Research 92, 431–439. Sutton, B.C., Rao, V.G. and Mhaskar, D.N. (1976). Kendrickomyces gen. nov. and Waydora nom. nov. two unusual stromatic coelomycetes. Transactions of the British Mycological Society 67, 243–249. United States Department of Agriculture (1960). Index of Plant Diseases in the United States. USDA Handbook No. 165. (US Department of Agriculture: Washington, DC.) Walker, J. and Bertus, A.L. (1971). Shoot blight of Eucalyptus spp. caused by an undescribed species of Ramularia. Proceedings of the Linnean Society of New South Wales 96, 108–115. Webb, R.S. (1983). Seed capsule abortion and twig dieback of Eucalyptus camaldulensis in South Florida induced by Botryosphaeria ribis. Plant Disease 67, 108–109. Weiss, F. and O'Brien, M.J. (1952). Index of Plant Diseases in the United States. Part IV, Guttiferae — Phytolaccaceae. Special Publication No. 1, Part IV, pp. 758–760. (Division of Mycology and Disease Survey; Bureau of Plant Industry, Soils, and Agricultural Engineering; Agriculture Research Administration, United States Department of Agriculture: Beltsville, Maryland.) Yuan, Z.Q., Old, K.M. and Midgley, S.J. (1990). Investigation of mycoflora and pathology of fungi present on stored seeds of Australian trees. In Tropical Tree Seed Research. (Ed. J.W. Turnbull). ACIAR Proceedings 28, 103–110. Yuan, Z.Q., Old, K.M., Midgley, S.J. and Solomon, D. (1997). Mycoflora and pathogenicity of fungi present on stored seeds from provenances of Eucalyptus pellita. Australasian Plant Pathology 26, 195–202.

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B.N. Brown and F.A. Ferreira

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A key aspect of any eucalypt planting program is the nursery system for production of seedlings or cuttings. Losses of planting stock in the nursery can severely affect the planting program. Damage in the nursery can be caused by abiotic and biotic agents. Nurseries provide conditions particularly conducive to the development of disease epidemics caused by pathogens that may originate in nearby forests or from soil, seed or vegetative planting material introduced into the nursery. Most of the nursery diseases of eucalypts are caused by fungi. These diseases include death of germinating seedlings, foliar diseases, stem diseases and root rots. Among the more important are damping-off caused by a range of soilborne fungi, grey mould caused by Botrytis cinerea, especially in temperate and subtropical areas, and a complex of diseases including leaf spots, shoot blight, stem canker, root rot and seedling death caused by several species of Cylindrocladium and Cylindrocladiella, which are particularly prevalent in tropical regions. Other pathogens of mature trees also cause nursery diseases, including Colletotrichum gloeosporioides and species of Coniella, Phaeophleospora and Mycosphaerella. Powdery mildews are common in nurseries but rare on trees in the field. Discohainesia oenotherae (syn. Pezizella oenotherae) or its synanamorphs cause a serious nursery disease known as Hainesia blight. The eucalypt rust, Puccinia psidii, infects eucalypts in nurseries in Brazil. Soilborne fungi such as species of Phytophthora, Pythium and Fusarium, in addition to their role in damping-off, often cause diseases of roots, collars or stems particularly near the soil surface. Thanatephorus cucumeris (Rhizoctonia solani) and Sclerotium rolfsii are soilborne pathogens that can also cause disease of above-ground tissues of eucalypts in nurseries. While there are several potentially destructive diseases of nursery stock, even the most serious can be adequately controlled by management strategies in the nursery.

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8.1 Introduction Forest nurseries provide the stock for the massive eucalypt planting programs for plantations, agroforestry and reforestation. The close spacing of plants, regular watering and high humidity, and heavy use of fertilisers in nurseries can contribute to the development of epidemics of diseases in nurseries that are not usually destructive in forests or plantations. Where nurseries are located within forest areas, most of the diseases occurring in nearby natural forests or plantations become established in the nurseries. Other sources of nursery pathogens are soil and infected or contaminated seed (see Chapter 7), seed debris, leaves, leaf mulch, cuttings or seedlings from other nurseries, or planting material from other countries (Sujan Singh 1985). Nursery diseases can have an important effect on seedling production and on subsequent planting programs. For example, high mortality of eucalypt seedlings caused problems in meeting the planting stock requirements and upset the planting schedule in high rainfall areas of Kerala, India (Kerala Forest Research Institute 1982). Forest nursery diseases can also cause the loss of valuable germplasm developed in tree selection and breeding programs. Other problems resulting from diseases of tree species in nurseries include the need to cull diseased seedlings before planting out, poor seedling establishment after transplanting, the need to replant areas where survival is poor because of the use of diseased seedlings and the possibility of transferring a pathogen on infected seedlings into previously uninfested areas. The number, incidence and severity of diseases that occur in eucalypt nurseries depend largely on the management system in use and the period for which seedlings remain in the nursery. For example, many nursery diseases of eucalypts are soilborne and bare root systems or systems in which seedling containers are held on or close to bare soil will allow development of such diseases. The retention of ‘old’ seedlings in a nursery will allow the development of diseases more typical of early plantation growth, particularly foliage diseases (e.g. Phaeophleospora epicoccoides, see Chapter 9) and will allow the development of common generalist pathogens such as Botrytis cinerea Pers. Diseases such as Cylindrocladium and Rhizoctonia blights can be

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aggravated by extended storage of older seedlings, particularly under crowded conditions. In India, the occurrence of diseases in eucalypt seed beds and containers was clearly related to the age of the seedlings and to differences in microclimatic and macroclimatic conditions (Sharma et al. 1984). Some of these diseases were associated with a particular growth stage of seedlings while others appeared just after the emergence of seedlings and continued on, also affecting container plants. Where nurseries for social forestry plantations are established on agricultural land or on strips of land along roads, soils are often unsuitable for raising tree seedlings because of their neutral or alkaline pH or high salt concentration (Sujan Singh 1985). Under these circumstances damping-off can cause severe losses. A collar rot of Eucalyptus seedlings in such nurseries in Uttar Pradesh, India, was found to be due to high temperature at soil level and the accumulation of salts at the soil surface, apparently because of exposure to hot dry winds in unprotected nurseries (Sujan Singh 1985). Given the environmental situation in some nurseries, abiotic as well as biotic causes of diseases of eucalypt planting stock are common. Both are discussed here, although most diseases of planting stock are caused by fungi. Although most experience has been with diseases of planting stock derived from seed, eucalypts are also propagated commercially by cuttings, especially in the tropics, and diseases of cutting production are also briefly considered.

8.2 Diseases with abiotic causes Even with good nursery technology there can be abiotic problems, some of which produce symptoms similar to those of diseases caused by pathogens. Abiotic problems can be caused by sun scald, burial of seeds and seedlings, excessive moisture in the substrate, hail, frost, drought or irrigation failure. Sun scald is a particular problem of young seedlings growing outside in summer, or in tropical areas, before they develop sufficient foliage to shade their stems. It produces symptoms that resemble dampingoff caused by soilborne fungi, including a dark, collapsed, water-soaked lesion of the collar region, up to one centimetre or more in length. This problem can be minimised by temporary shading for the first 30 days of seedling production in the tropics.

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Seed and seedling burial at excessive depths in the planting medium can cause germination failure and mortality of young seedlings and can predispose seedlings to infection by pathogens. Leaf scorch in the shape of an inverted ‘V’ (in Brazilian “lesão ou necrose em ‘V’ invertido”, Ferreira 1989) is an indication of water deficit due to drought or irrigation failure. The duration of wilting determines the occurrence and extent of leaf scorch, or even seedling death, subject to other conditions such as humidity, temperature and wind. Leaf scorch symptoms develop a few days to a week after a critical water deficit.

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attack only a single part of a tree (root, leaf, stem), others may be associated with a wide range of diseases and habitats. For example, Cylindrocladium quinqueseptatum Boedijn & Reitsma, a fungus of particular importance in eucalypt plantations in the tropics (see Chapter 9), is capable of causing seed rot, damping-off, root rot, leaf spot, stem canker or blight of many species in nurseries. Conversely, damping-off in germinating seedlings is caused by a wide range of fungi. Therefore, both disease syndromes in which numerous fungi are involved and diseases caused by single or related pathogens are considered.

Seedling death can result from excessive substrate moisture due to poor levelling of seedlings in racks or, more commonly, substrates with poor drainage characteristics. In Brazil, mortality of E. grandis seedlings within 60 days has been accompanied by symptoms characteristic of oxygen deficit such as swollen collars, formation of abnormal, thick, whitish secondary roots (aerenchyma) occasionally with negative geotropism, and development of red to purple crowns because of mineral deficiency caused by oxygen deficit in the roots.

8.3.1

Frost or hail can damage or kill eucalypt seedlings. Frost damage appears as a blight of apical tissues. Hail can cause direct physical damage as well as blight due to freezing of tissues. Frost can also predispose seedlings to infection by pathogens.

The pathogens involved in damping-off in eucalypt nurseries are seedborne, soilborne or waterborne fungi in the genera Botrytis, Calonectria, Cylindrocladium, Fusarium, Phytophthora (Ph.), Pythium (P.), Rhizoctonia and Thanatephorus. Damping-off has frequently caused considerable loss of eucalypt seedlings (Magnani 1964; Gibson 1975; Reis and Hodges 1975; Jacobs 1979; Kerala Forest Research Institute 1982; Sharma and Mohanan 1982, 1992a; Sehgal 1983; Sharma et al. 1984, 1985; Kobayashi and De Guzman 1988; Arentz 1991). The species most commonly listed as causing damping-off of eucalypts are Calonectria quinqueseptata Figueiredo & Namek. (usually as the anamorph Cylindrocladium quinqueseptatum), Cylindrocladium scoparium Morgan and Thanatephorus cucumeris (A.B.Frank) Donk (usually as the anamorph Rhizoctonia solani J.G.Kühn). In subtropical Yunnan Province in south-west China, damping-off in eucalypts was caused by Alternaria alternata (Fr.) Keissl. (described as Alternaria tenuis Nees) (Zhou Dequn and Sutherland 1993).

8.3 Fungal diseases The major biotic nursery diseases of eucalypts are damping-off, web blight, seedling blight, leaf blight, seedling wilt, stem infections, leaf spots and root rots caused by a variety of fungal pathogens. Frequently plants in nurseries will be beset by a range of diseases, either simultaneously or in a succession. For example, in high rainfall areas of India, diseases such as damping-off, web blight, seedling blight and leaf blight appear more-or-less in succession on eucalypt seedlings, forming a disease complex which may result in almost 100% mortality (Sharma and Mathew 1991). Since a single pathogen can cause many of these symptoms and a single symptom can be caused by several pathogens, control of a disease complex poses special problems. Sharma and Mathew (1991) commented that while some pathogens cause only a single disease and

Damping-off

Holliday (1990) defined damping-off as ‘the collapse and death of seedlings which results from a lesion caused by a pathogen at about soil level’. A wider concept of damping-off includes girdling diseases, not necessarily occurring at ground level, caused by fungi such as Botrytis cinerea and Cylindrocladium spp. on older seedlings (Ferreira and Muchovej 1991; Blum et al. 1992). Here, damping-off is considered more conventionally as a disease of very young seedlings prior to tissue lignification.

Common seedborne fungi such as Fusarium solani (Mart.) Sacc., Fusarium oxysporum Schltdl. emen. W.C.Snyder & H.N.Hansen, Macrophomina

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phaseolina (Tassi) Goid., Rhizoctonia solani and a Verticillium sp. have caused damping-off of eucalypt species (Michail et al. 1986; Taha et al. 1987; Harsh et al. 1992). It is questionable whether these pathogens are truly seedborne or are contaminants of seed as a result of contact of capsules or seed with the ground during harvesting or processing (see Chapter 7). Because damping-off is caused by a variety of soilborne fungi, it is almost impossible to establish a bare root or container nursery beyond the reach of propagules of these fungi (Kelley and Oak 1989). Damping-off organisms may be endemic in a nursery without causing damage, but may cause serious problems when environmental conditions are favourable for the pathogen (or pathogens) but not for early seeding growth. As the seedlings mature and produce secondary lignified tissues, the diseases may change from damping-off to rot of the young, unlignified roots. Thus, damping-off may be followed by seedling root rots, caused by the same fungi, although several other soilborne fungi also affect older seedlings. Three types of damping-off are generally recognised: 1

Pre-emergence damping-off involving death of seedlings before they emerge from the soil. The seed may fail to germinate or the radicle of the seedling may be attacked as it develops. The most obvious effect of pre-emergence damping-off is poor germination, often in scattered patches.

2

Postemergence damping-off involving death of the very young, succulent seedlings after they have emerged from the soil. There are two forms of postemergence damping-off. In one, seedling tissues at soil level are attacked and die before either the root or top. In the other, the attack starts at the root tip and progresses upwards. The most obvious symptom of both forms is the collapse of seedlings, in patches, so that the affected seedlings are found lying on the soil surface.

3

Top damping-off involving infection of cotyledons retained in the seed coat for extended periods, resulting in death of the seedling. The fungus forms a mat over the seedlings and smothers them. Top damping-off is prevalent

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under conditions of high moisture and seedling density. Damping-off usually occurs in patches which begin at a focus and spread outwards, with the most recent deaths occurring at the perimeter (Sharma and Mohanan 1982). Factors that favour damping-off are continuous use of nursery beds for seedling production, excessive shading, close spacing of germinating seedlings, excessive soil water in the seedbeds or container mixes (resulting from heavy rainfall, overwatering or poor drainage), high content of non-decomposed organic materials in the soil or potting mixture and neutral to alkaline soil pH. Also, tree species vary in their susceptibility to damping-off. Damping-off caused by Rhizoctonia solani was the main establishment problem of tree seedlings in the lowlands of Papua New Guinea, especially for E. deglupta, which suffered a total loss of seedlings when unsterilised soil was used (Arentz 1991). In the Philippines severe damage due to pre-emergence and postemergence damping-off caused by Rhizoctonia solani often occurred in fine-seeded tree species, including eucalypts (Kobayashi and De Guzman 1988). In India pre-emergence damping-off of E. grandis seedlings caused by a Pythium sp. and Rhizoctonia solani was noticed within two or three days of sowing (Sharma et al. 1984, 1985). The disease was associated with high soil water content and heavy shade. Only about 20% of seedlings emerged and the disease was characterised by rotting of the newly emerged radicle and subsequently of the cotyledons within the seed coat. Postemergence damping-off appeared within one week of emergence and was evident as a watersoaked constriction followed by collapse of the stem tissue at the soil surface, causing the seedlings to fall over. Mortality of seedlings was observed for only the first two to three weeks following emergence. Thereafter, the seedlings apparently developed resistance due to formation of bark and protection of susceptible tissues. Species of Cylindrocladium and Cylindrocladiella cause the disease complex of eucalypt seedlings in India, referred to above, that includes damping-off and disease at later growth stages of seedlings (Sharma 1986; Sharma and Mathew 1991). Cylindrocladium scoparium was shown to be a cause of pre-emergence damping-off of several eucalypt species in Japan (Terashita and Takai 1955).

D I S EA SE

In Australia damping-off has been a problem in propagation of eucalypt species in forest nurseries, the main pathogens being Pythium species and Rhizoctonia solani (Brown and Wylie 1991). In laboratory studies using untreated field soil, Phytophthora cinnamomi Rands and Pythium spp. were associated with severe damping-off in seedlings of E. sieberi and E. agglomerata, with Fusarium also being involved (Gerrettson-Cornell 1975). Postemergence damping-off in seedlings of E. obliqua and E. radiata in a native forest in Victoria was primarily caused by five species of Pythium (Pythium mamillatum Meurs, Pythium ultimum Trow, Pythium irregulare Buisman, Pythium paroecandrum Drechsler and Pythium perplexum H.Kouyeas & Theoh.), two species of Fusarium [Fusarium avenaceum (Fr.) Sacc. and Fusarium longipes Wollenw. & Reinking] and Cylindrocarpon destructans (Zinssm.) Scholten (Mwanza and Kellas 1987). It was concluded that the failure of most seeds to germinate in these forests was due to pre-emergence damping-off. The most serious and widespread disease of eucalypts in forest nurseries in Latin America has been damping-off and root rot caused by Cylindrocladium scoparium, which in some cases caused almost complete loss of the seedling crop (Reis and Hodges 1975). Damping-off caused by Rhizoctonia solani or species of Fusarium, Pythium or Phytophthora was of limited importance. This situation has since changed completely, especially in Brazil, where damping-off is no longer a problem in the suspended container and hygiene system now in use (see Chapter 19). Other fungi associated with damping-off of eucalypts are Calonectria ilicicola Boedijn & Reitsma, Calonectria kyotensis Terash., Phytophthora cryptogea Pethybr. & Laff., Pythium deliense Meurs, Pythium intermedium de Bary, Pythium myriotylum Drechsler and Pythium spinosum Sawada.

8.3.2

Grey mould (Botrytis cinerea)

One of the most frequently reported nursery diseases of Eucalyptus species throughout the world is grey mould caused by Botrytis cinerea, the hyphomycete anamorph of Botryotinia fuckeliana (de Bary) Whetzel [syn. Sclerotinia fuckeliana (de Bary) Fuckel] (Birch 1937; Abrahão 1948; Nattrass 1949; Riley 1960; United States Department of Agriculture 1960;

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Magnani 1963; Talbot 1964; Browne 1968; Gibson 1975; Chambers 1982; South African Forestry Research Institute 1985; Gong Mingqin and Ke Jinshan 1988; Cook and Dubé 1989; Brown and Wylie 1991; Zhou Dequn and Sutherland 1993). There are few reports of this disease on Corymbia species. The fungus is ubiquitous, being most prevalent in temperate and subtropical areas where it is common on the phylloplane and is a facultative parasite of a wide range of plants, causing blight or rot of immature, fleshy or senescent tissues (Ellis and Waller 1974; Domsch et al. 1980). It was isolated from the leaf surface of field grown E. stellulata (Lamb and Brown 1970) and has been detected on and within eucalypt seeds (Saxena 1985; Mittal et al. 1990; Yuan et al. 1990; see Chapter 7). It was involved in the fungal succession on leaf litter of E. pauciflora described by Macauley (1979). The fungus is almost universally present on dead and dying vegetable matter (Peace 1962) and can be expected to occur in most nurseries. The occurrence of grey mould or other diseases caused by this fungus (e.g. damping-off) is therefore likely to depend on conditions in the nurseries. Outbreaks of grey mould are often sporadic. For example, it is usually only a minor problem in eucalypt nurseries in subtropical south-east China, but during 1992 it caused the loss of about one million young nursery stock (seedlings, cuttings, tissue-culture explants) in Guangxi Province (Huang Jin Yi and Xue Zhen Nan, pers. comm.). In Yunnan Province the disease caused severe losses of eucalypt seedlings during cold wet weather in 1990 and 1991 (Zhou Dequn and Sutherland 1993). Most reports of Botrytis cinerea on eucalypts are from nurseries but occasionally the fungus has been found on older trees (Nattrass 1949; Gilmour 1966; Lamb and Brown 1970; Gibson 1975). There are several reports that grey mould is particularly common on certain eucalypt species including E. botryoides, E. cladocalyx, E. delegatensis, E. globulus, E. globulus ssp. bicostata and E. globulus ssp. maidenii (Riley 1960; Magnani 1963; Gilmour 1966; Browne 1968; Gibson 1975; Turnbull and Pryor 1978; Jacobs 1979; Marks et al. 1982; Brown and Wylie 1991). Inoculation of E. globulus with conidia and sclerotia of Botrytis cinerea produced typical symptoms

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(Moniz da Maia 1924). After removal of their waxy bloom by gentle rubbing, young leaves became infected by conidial inoculation (Nattrass 1949). Mature leaves were not infected. Inoculation of seed of E. camaldulensis did not reduce seedling emergence (Yuan et al. 1990). The fungus normally invades living tissues of plants after establishing a food base on dead or dying plant material, including shaded, senescent foliage and tissues damaged by fertiliser or frost (Sutherland et al. 1989). The stem lesions are frequently associated with diseased leaves, suggesting initial infection of dead or senescent foliage. The first sign of disease on the stem is the appearance of a water-soaked area that spreads rapidly up and down the plant (Gibson 1962). This is followed by wilting of twigs and foliage followed by rapid collapse and death of the affected parts. The water-soaked stem lesions on eucalypts are usually surrounded by a deep-purple fringe (Marks et al. 1982). In the last stage of disease a web of greyish-white mycelium, conidiophores and conidia develops on dead tissues. The disease occurs in overcrowded beds or under conditions where there is prolonged accumulation of moisture near the host. Under favourable conditions, Botrytis cinerea can spread rapidly from one seedling to another and pockets of disease can develop within the seedling crowns (Landis 1989). Conidia of Botrytis cinerea are dispersed by wind or water splash, often being carried on the surface of drops (Holliday 1980). Grey mould is common at temperatures below optimum for the host (often appreciably below 20°C) (Holliday 1980). Relative humidity is one of the most important environmental factors affecting the disease and rainy or foggy weather favours infection (Mittal et al. 1987). The disease can be controlled by maintaining humidity below 80% to 85% (Mittal et al. 1987).

8.3.3

Cylindrocladiella and Cylindrocladium diseases

Seventeen species of the two, white hyphomycete genera, Cylindrocladiella and Cylindrocladium, cause damping-off and diseases of older eucalypt planting stock in nurseries (Table 8.1). These diseases have often caused severe losses of plants in seedbeds and containers, particularly in the wet tropics (Jacobs 1979; Upadhyaya and Nirwan 1979; Sharma and Mohanan 1982; Sehgal 1983; Quiniones and Dayan 1983; Sharma et al. 1984; Mohanan and

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Sharma 1985; Sharma and Mathew 1991). On occasions several of these species are associated with a single disease syndrome. For example, a complex of nine species caused a disease syndrome affecting different growth stages of seedlings in nurseries in Kerala, India (Sharma and Mohanan 1982; Sharma 1986). Many species of the two genera are also associated with diseases of young eucalypts in plantations (see Chapter 9). 8.3.3.1

Taxonomy of pathogens

The genus Cylindrocladiella Boesew. (teleomorph: Nectria Fr.) was proposed to accommodate several species of Cylindrocladium Morgan (teleomorph: Calonectria De Not.) which differ from the others primarily in having smaller two-celled conidia and lacking septa or having only a basal septum in the sterile filament (stipe extension), a structure of unknown function which extends above the conidiogenous apparatus and terminates in a swollen vesicle which is distinctive for each species (Boesewinkel 1982; Crous and Wingfield 1993). The recent revisions of the taxonomy of species of Cylindrocladium (Crous et al. 1993b; Crous and Wingfield 1994) have resulted in confusing nomenclature of some species (Table 8.2). For example, the common pathogen Cylindrocladium scoparium is the anamorph of Calonectria morganii Crous, Alfenas & M.J.Wingf. while the anamorph of Calonectria scoparia Peerally is now given as Cylindrocladium candelabrum Viégas. Another important aspect of the revised taxonomy is the problem of naming species published prior to these revisions. For example, the isolate reported by Blum and Dianese (1993) and by Blum et al. (1992) as Cylindrocladium scoparium was reported by Crous and Wingfield (1994) to be Cylindrocladium ovatum El-Gholl, Alfenas, Crous & T.S.Schub. The species names used here have been reassigned, as far as possible, from those as published to the current name in light of the above taxonomic changes. 8.3.3.2

Range of diseases

The species of Cylindrocladiella and Cylindrocladium reported to infect eucalypts in forest nurseries, or to infect plants or detached tissue following inoculation, are listed with their distinguishing features in Table 8.1. Although Cylindrocladium ovatum has not been reported from eucalypts in nurseries, it has been shown to infect

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TA BLE 8. 1

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Morphology of the species of Cylindrocladiella and Cylindrocladium reported from eucalypts in nurseries (N), or shown by inoculation to be able to infect eucalypt seedlings (S), plants of unstated age (I) or detached tissue (D)

Data on morphology are from Peerally (1991), Crous and Wingfield (1993, 1994) and Crous et al. (1993a; 1993b, 1993c). Conidia Species

Septa

Length (µm)

Width (µm)

Sterile vesicle

Cylindrocladiella camelliae (Venkataram. & C.S.V.Ram) Boesew.

(0)–1

9–(12.5)–15

1.9–(2.0)–2.5

Ellipsoid to lanceolate N, S, I

Cylindrocladiella infestans Boesew.

(0)–1

10.0–(14.5)–22.5

1.9–(2.5)–3.0

Lanceolate to cylindrical

N

Cylindrocladiella lageniformis Crous, M.J.Wingf. & Alfenas

(0)–1

9.0–(11.5)–15.0

1.5–(1.8)–2.0

Lageniform to ovoid

N

Cylindrocladiella parva (P.J.Anderson) Boesew.

(0)–1

13.5–(17.0)–19.5

2.0–(2.5)–3.0

Clavate to spathulate or pyriform

N, I

Cylindrocladium candelabrum Viégas

1

33–(45)–66

3.5–(4.0)–4.5

Ellipsoid to obpyriform

N

Cylindrocladium colhounii Peerally

3

38–84

3–6

Narrowly clavate

N, S, I

Cylindrocladium curvatum Boedijn & Reitsma

1

40–46

3–4

Globose to subglobose

N

Cylindrocladium floridanum Sobers & C.P.Seym.

1

36–57

3–6

Globose to subglobose

N, S, I

Cylindrocladium gracile (Bugnic.) Boesew.

1

(26)–38–65

(3)–4–6

Narrowly clavate

N, S, I, D

Cylindrocladium ilicicola (Hawley) Boedijn & Reitsma

(1)–3

37–68

4–5

Clavate to spathulate

N, S, D

Cylindrocladium macroconidiale (Crous, M.J.Wingf. & Alfenas) Crous

(1)–3

86–(97)–112

5.5–(6.5)–8

Narrowly clavate

N

Cylindrocladium ovatum El-Gholl, Alfenas, Crous & T.S.Schub.

1(–3)

36–(65)–80

4–(5)–6

Ellipsoid to ovoid

S

Cylindrocladium parasiticum Crous, M.J.Wingf. & AlfenasA

(1)–3

45–(62)–90

4.5–(6)–7

Sphaero-pedunculate

S, I

Cylindrocladium pteridis F.A.Wolf

1 1

61–118 23–48

5 4–5

Clavate

N, I

Cylindrocladium quinqueseptatum Boedijn & Reitsma

(1)–5 (–6) 60–120

5–8

Narrowly clavate

N

Cylindrocladium scoparium Morgan

1

40–(44.5)–66

3.5–(4.0)–4.5

Ellipsoid to pyriform

N, S, I

Cylindrocladium theae (Petch) Subram.

(1)–3

63–103

5–7

Narrowly clavate

N

Cylindrocladium variabile Crous, B.J.H.Janse, D.Victor, G.F.Marais & Alfenas

(1)–3–(4)

48–(60)–75

4–(5)–6

Sphaero-pedunculate or ellipsoid to clavate

N

A

Infection

Nursery records of this species are as the teleomorph Calonectria ilicicola (see Table 8.2).

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TA B LE 8 . 2

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Relationships between anamorphs and teleomorphs of the species of Calonectria, Nectria, Cylindrocladiella and Cylindrocladium reported from species of Corymbia and Eucalyptus in nurseries or shown to infect eucalypt seedlings

Teleomorph Calonectria colhounii Peerally

Anamorph A

Cylindrocladium colhounii PeerallyA

Calonectria gracilis Crous, M.J.Wingf. & Alfenas

Cylindrocladium gracile (Bugnic.) Boesew.A

Calonectria ilicicola Boedijn & ReitsmaA

Cylindrocladium parasiticum Crous, M.J.Wingf. & Alfenas

Calonectria kyotensis Terash.A

Cylindrocladium floridanum Sobers & C.P.Seym.A

Calonectria macroconidialis (Crous, M.J.Wingf. & Alfenas) Crous

Cylindrocladium macroconidiale (Crous, M.J.Wingf. & Alfenas) CrousA

Calonectria morganii Crous, Alfenas & M.J.Wingf.

Cylindrocladium scoparium MorganA

Calonectria ovata D.Victor & Crous

Cylindrocladium ovatum El-Gholl, Alfenas, Crous & T.S.Schul.

Calonectria pteridis Crous, M.J.Wingf. & Alfenas

Cylindrocladium pteridis F.A.WolfA

Calonectria pyrochroa (Desm.) Sacc.

Cylindrocladium ilicicola (Hawley) Boedijn & ReitsmaA

Calonectria quinqueseptata Figueiredo & Namek.A

Cylindrocladium quinqueseptatum Boedijn & ReitsmaA

Calonectria scoparia Peerally

Cylindrocladium candelabrum ViégasA

Calonectria variabilis Crous, B.J.H.Janse, D.Victor, G.F.Marais & Alfenas

Cylindrocladium variabile Crous, B.J.H.Janse, D.Victor, G.F.Marais & AlfenasA

Nectria camelliae (Shipton) Boesew.

Cylindrocladiella infestans Boesew.A Cylindrocladiella camelliae (Venkataram. & C.S.V.Ram) Boesew.A Cylindrocladiella lageniformis Crous, M.J.Wingf. & AlfenasA Cylindrocladiella parva (P.J.Anderson) Boesew.A Cylindrocladium curvatum Boedijn & ReitsmaA

Nectria indusiata SeaverA (= Calonectria; P.W. Crous, pers. comm.) A

Cylindrocladium theae (Petch) Subram.A

Reported from Corymbia or Eucalyptus in a nursery.

seedlings and so must be considered a nursery threat. Although Cylindrocladium parasiticum Crous, M.J.Wingf. & Alfenas has not yet been reported from a eucalypt nursery, its teleomorph, Calonectria ilicicola, is on the list of known nursery pathogens (Sharma and Mohanan 1982, 1991a). Cylindrocladium quinqueseptatum and Cylindrocladium scoparium are the most important species on eucalypts; the former is more important in the tropics, particularly in Asia and Australia, whereas the latter is more important in subtropical and temperate areas. Cylindrocladium blight is the major fungal problem in eucalypt nurseries and on young coppice shoots and first year plants in plantations in Kerala (Jayashree et al. 1986). A disease complex or 126

succession of pathogens is recognised on eucalypts in nurseries (Mohanan and Sharma 1986a; Sehgal 1983; Sharma and Mathew 1991; Sharma and Mohanan 1982). Postemergence damping-off, caused by Pythium, Rhizoctonia and Cylindrocladiella/Cylindrocladium, is the first disease to appear after emergence of seedlings, causing mortality for two weeks until seedlings develop resistance. Within three weeks of emergence, another disease, web blight caused by the Rhizoctonia state of Thanatephorus cucumeris, appears and this may last until the seedlings are pricked into polythene containers. This is followed by a destructive seedling blight caused by species of Cylindrocladiella and Cylindrocladium. The same fungi cause stem canker and leaf and shoot blights

D I S EA SE

after the onset of the monsoon, resulting in further heavy mortality of seedlings. Of the nine species of Cylindrocladium or Cylindrocladiella associated with the disease in Kerala, Cylindrocladium ilicicola (Hawley) Boedijn & Reitsma, along with Cylindrocladium quinqueseptatum, Cylindrocladium gracile (Bugnic.) Boesew. (syn. Cylindrocladium clavatum Hodges & L.C.May) and Cylindrocladium theae (Petch) Subram. were the most serious pathogens (Mohanan and Sharma 1986a). The high incidence of these diseases was mainly because of poor management practices resulting in excessive soil moisture, heavy shade, high density of seedlings and high humidity (Mohanan and Sharma 1986a). The most serious and widespread disease problem in eucalypt nurseries in the Americas was damping-off and root rot of seedlings caused by Cylindrocladium scoparium (Reis and Hodges 1975). This disease was present in all parts of Latin America where eucalypts were grown and in some nurseries caused almost complete loss of the seedling crop. Gibson (1975) regarded Cylindrocladium scoparium as one of the most serious nursery pathogens of eucalypts at all growth stages, causing damping-off in small seedlings and root rot and dieback of later stages. Since those reports, there have been numerous reports of Cylindrocladium scoparium and other species, particularly Cylindrocladium quinqueseptatum, on Corymbia and Eucalyptus species in forest nurseries (Pitkethley 1976; Alfenas et al. 1979; Keirle 1981; Sharma and Mohanan 1982, 1991a, 1992a; Sehgal 1983; Barnard 1984; Sharma et al. 1984, 1985; Mohanan and Sharma 1985; Rattan and Dhanda 1985; Arentz 1991; Ferreira and Muchovej 1991; Sharma and Mathew 1991; Viljoen et al. 1992). In Brazil, Cylindrocladium scoparium and Cylindrocladium gracile both caused disease of pre-emergence and post-thinning stages of eucalypts, while Cylindrocladium scoparium caused disease at the foliage closure stage (Ferreira and Muchovej 1991) and Cylindrocladiella infestans Boesew. and Cylindrocladiella lageniformis Crous, M.J.Wingf. & Alfenas were associated with cutting rot in eucalypt nurseries (Crous and Wingfield 1993). Cylindrocladium ilicicola was isolated from stem lesions on E. alba in Brazil and following inoculation caused damping-off in C. citriodora, E. alba and E. saligna, leaf spots on E. robusta, and stem and branch cankers on E. saligna (Figueiredo and Cruz 1963). Cylindrocladium scoparium caused extensive losses in nursery-grown E. grandis and

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E. robusta in Florida (Barnard 1984). Infections started in the leaves and progressed through the petioles to the stems. As in Kerala, disease was enhanced by overhead irrigation, high temperatures and humidities, and reduced ventilation due to close spacing. Although Cylindrocladium scoparium was generally regarded as a nursery problem, seedling mortality occurred after outplanting as a result of pathogen carryover (Barnard 1981, 1984). A new species, Cylindrocladium macroconidiale (Crous, M.J.Wingf. & Alfenas) Crous (syn. Cylindrocladium coulhounii Peerally var. macroconidiale Crous, M.J.Wingf. & Alfenas), caused serious disease, including leaf spot, root rot and wilt, of E. grandis cuttings in South Africa (Crous et al. 1993c). 8.3.3.3

Disease symptoms

Species of Cylindrocladium and Cylindrocladiella cause a wide range of symptoms on young eucalypts, including seed rots, damping-off, cotyledon infection, seedling blight, leaf spots, foliar and shoot blights, stem lesions, girdling stem cankers, diebacks and root rots, and they can decrease the rooting of cuttings (Kerala Forest Research Institute 1982; Sharma and Mohanan 1982; Barnard 1984; Mohanan and Sharma 1985; Rattan and Dhanda 1985; Ferreira and Muchovej 1991; Sharma et al. 1984, 1985; Crous et al. 1993c). The different species may be associated with one or many of the above symptoms (Sharma and Mohanan 1982, 1991a; Sharma et al. 1984, 1985). Root infection of eucalypts by Cylindrocladiella camelliae (Venkataram. & C.S.V.Ram) Boesew. begins in the collar and the feeder roots and spreads to the entire root system, causing browning and decay (Mohanan and Sharma 1985). Affected seedlings wilt and die within one week. In seedbeds, seedling blight results from infection on the stem near ground level, with the infected seedlings turning brown and drying (Sharma et al. 1984). Small lesions developed on leaves and stems 12 hours after inoculation of E. grandis with Cylindrocladiella camelliae and Cylindrocladium clavatum, and seedling blight, which resulted from leaf blight and stem infection, took five days to kill the seedlings (Mohanan and Sharma 1985). Symptoms appeared on the leaves within three to five days of inoculation of two-month-old seedlings of six eucalypt species with Calonectria ilicicola [reported as Calonectria crotalariae (Loos) D.K.Bell & Sobers] 127

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and developed into irregularly circular, reddish-purple spots (0.5–3 mm in diameter) on all species (Bell and Sobers 1966). Leaf spotting symptoms produced by these species vary with the pathogen species and the species and age of the host. Cylindrocladium scoparium initially produced diffuse, light purple spots on eucalypt leaves and these gradually became darker with a necrotic centre and delimited by a narrow, dark purple halo (Cruz and Figueiredo 1960). However, on older leaves, leaf spots caused by Cylindrocladium scoparium started as minute brown lesions and later enlarged to form lesions with reddish brown margins and light brown centres (Quiniones and Dayan 1983). Symptoms of blight on C. citriodora caused by Cylindrocladium scoparium consisted of irregular dark brown leaf spots which increased rapidly in moist weather (Upadhyaya and Nirwan 1979). On leaves of Eucalyptus hybrid, Cylindrocladium gracile caused small, scattered, angular to circular, brown to light purplish-brown leaf spots on the interveinal area and on the veins (Rattan and Chohan 1983). These spots eventually coalesced to form larger spots. Leaf spots caused by several species [Cylindrocladiella camelliae, Cylindrocladiella parva (P.J.Anderson) Boesew., Cylindrocladium gracile, Cylindrocladium floridanum Sobers & C.P.Seym., Cylindrocladium ilicicola and Cylindrocladium quinqueseptatum] on container seedlings appeared first as minute, greyishblack, water-soaked lesions on young as well as older leaves (Sharma et al. 1984). Later, small lesions coalesced to form large necrotic areas which on drying turned brown, giving a typical leaf blight. Under high humidity, the initial symptoms were generally large greyish-black spots which sometimes covered the entire leaf. Severe leaf infection caused leaf blight and resulted in premature defoliation. Cylindrocladium quinqueseptatum caused leaf spots, leaf blight and seedling blight on 11 eucalypt species in a nursery in Darwin, NT (Pitkethley 1976). Leaf spots were irregular to circular, generally two to six millimetres in diameter, with brown centres and red margins. Lesions developed on leaves within four days of inoculation of E. phoenicea seedlings. ‘Stem strangling’ of young plants of E. alba at a height of about 20 centimetres above the collar was caused by seedborne (or seed-contaminating, see Chapter 7) Cylindrocladium scoparium (Cruz and Figueiredo 1961). In Brazil, stem lesions caused by Cylindrocladium scoparium and Cylindrocladium 128

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gracile are common at the soil line in young eucalypt seedlings and above mature bark on older seedlings (Ferreira and Muchovej 1991). Slow-growing eucalypt species were more susceptible than fastgrowing species to root and collar infection by Calonectria ilicicola (reported as Calonectria crotalariae) (Nishijima and Aragaki 1973). Disease caused by Cylindrocladium spp. on eucalypt stems generally appears as a dark brown to black, spreading, often girdling, sunken lesion, leading to death of the distal portion of the stem and breaking of the stem at the lesion (Cruz and Figueiredo 1961; Upadhyaya and Nirwan 1979; Barnard 1984; Rattan and Dhanda 1985). Stem cankers caused by Cylindrocladium scoparium often occur three to 10 centimetres above the soil line at or near leaf nodes (Barnard 1984). Stem infections are frequently centred on leaf petioles, suggesting that infection begins in the leaves and progresses to the stem through the petioles (Rattan and Dhanda 1985; Cordell et al. 1989). Severe disease leads to defoliation of seedlings, wilting and dieback of branches and stems due to girdling and frequently death of seedlings (Upadhyaya and Nirwan 1979; Quiniones and Dayan 1983; Sharma et al. 1984; Rattan and Dhanda 1985). Secondary shoots may arise from the lower, healthy region of the stem in partly infected seedlings (Sharma et al. 1984; Rattan and Dhanda 1985). Under conditions of high humidity, these pathogens often develop profuse, white to pale fawn coloured tufts of conidiophores and conidia on affected aerial parts of the plant (particularly on the lower stems just above soil level) (Pitkethley 1976; Upadhyaya and Nirwan 1979; Sharma et al. 1984; Rattan and Dhanda 1985). Such structures are readily recognised under magnification with a hand lens and enable preliminary identification of the pathogens. The teleomorphs are often found in association with the anamorphs and perithecia are readily visible as superficial, subglobose to globose, red, red-brown or yellow structures that exude spores in pale yellow slime masses. Perithecia of several of these fungi are formed in culture (Figueiredo and Cruz 1963; Figueiredo and Namekata 1967; Alfenas et al. 1979), on inoculated plants (Figueiredo and Cruz 1963; Figueiredo and Namekata 1967; Alfenas et al. 1979), on natural infections (Reddy 1974; Alfenas et al. 1979), or when naturally infected or inoculated tissues are kept in moist chambers (Figueiredo and Namekata 1967; Alfenas et al. 1979; Sehgal 1983).

D I S EA SE

8.3.3.4

Epidemiology

Wet and humid conditions greatly favour the development of diseases caused by Cylindrocladium spp. (Pitkethley 1976; Keirle 1981; Bolland et al. 1985; Viljoen et al. 1992). In Kerala, Cylindrocladium seedling blight is a very serious problem of eucalypts in nurseries and outplantings during the south-west monsoon season (Sehgal 1983; Nair and Jayasree 1986). Infection spreads rapidly in seedlings when nursery beds are covered, when beds are watered profusely and when seedlings are kept close together (Barnard 1981; Sehgal 1983). The rapid spread of splash-dispersed conidia through crowded seedlings can result in blighting of the whole stock within one week (Nair and Jayasree 1986). In a severe attack, over 50% of seedlings may be killed within 10 to 15 days (Sehgal 1983). Unusually persistent wet and windy weather was associated with the initial outbreak of disease caused by Cylindrocladium quinqueseptatum on eucalypts in a nursery in Darwin, resulting in 100% mortality in some seedling lots (Pitkethley 1976). Seedling blight of E. grandis caused by Cylindrocladium quinqueseptatum occurred one week earlier at higher light intensity under coir matting shade than under the heavier shade provided by coconut leaf thatch, although it generally persisted longer under the latter (Sharma and Mohanan 1992a). Severity of disease caused by Cylindrocladiella parva on E. tereticornis and E. raveretiana in several nurseries in Papua New Guinea was greatest on seedlings suffering nutrient stress (Arentz 1991) and Cylindrocladium blight caused particularly heavy mortality on unthrifty seedlings in India (Nair and Jayasree 1986). Germination of conidia of Cylindrocladium quinqueseptatum on intact leaves of two-month-old E. grandis seedlings began after three hours of incubation. Appressoria were formed over the epidermal cells after four-and-a-half hours on mature leaves and six hours on young leaves (Sharma and Mohanan 1990). Formation of appressoria over stomata was rare and penetration was mostly through epidermal cells, in contrast to the report by Bolland et al. (1985) that leaf penetration was via stomata. Necrotic lesions developed within 12 hours of inoculation and appeared earlier on young leaves than mature leaves even though appressorium formation was slower on the young leaves (Sharma and Mohanan 1990). Young seedlings were more susceptible than older ones to attack by Cylindrocladium gracile, although

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death of infected nursery and transplant seedlings over one year old occurred under highly favourable conditions (Rattan and Dhanda 1985). Although these fungi may be disseminiated as conidia and ascospores over short and longer distances (Peerally 1974a, 1974b), the initial inoculum is often soilborne. Many species form chlamydospores and/or microsclerotia which assist survival and dissemination. Cylindrocladium scoparium forms both chlamydospores and microsclerotia (Booth and Gibson 1973) and is able to survive in soil and infect susceptible plants at and below soil level (Bertus 1976a, 1976b). These infections may lead to foliage infection. Soil artificially infested with a culture of the fungus remained infective for up to seven months. Ants can carry propagules of Cylindrocladium in soil (Hutton and Sanewski 1988). Ferreira and Muchovej (1991) suggested that inoculum of Cylindrocladium in nurseries comes from field soil that contaminates cuttings or from nursery soil, and that rain or irrigation water is the main agent of dispersal. Cylindrocladium gracile was associated with seed of a Eucalyptus hybrid (see Chapter 7) and could be disseminated on seed. Cylindrocladium scoparium may be carried between nurseries on diseased stock (Thies and Patton 1970; Keirle 1981). 8.3.3.5

Host range and variation in resistance

There are considerable differences between species and provenances of eucalypts in their susceptibility to Cylindrocladiella and Cylindrocladium. The pathogens also vary in pathogenicity. For example, in inoculation experiments under field conditions it was evident that Cylindrocladium colhounii Peerally was not as pathogenic as Cylindrocladium quinqueseptatum on E. grandis (Nair and Jayasree 1986). In India, infection of the foliage and tender stems by several species (Cylindrocladiella parva, Cylindrocladium curvatum Boedijn & Reitsma, Cylindrocladium floridanum, Cylindrocladium ilicicola, Cylindrocladium quinqueseptatum, Cylindrocladium scoparium) caused heavy mortality of young plants (Sehgal 1983). Corymbia torelliana and E. deglupta were slightly susceptible and several other species, including C. citriodora, E. camaldulensis, E. grandis, E. saligna and E. tereticornis, were more susceptible. Nursery screening of 38 eucalypt provenances against Cylindrocladium blight in Kerala showed 129

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that Cylindrocladium quinqueseptatum had a much wider host range than Cylindrocladium floridanum (Jayashree et al. 1986). Seven provenances, including provenances of E. deglupta, E. exserta, E. microcorys, E. propinqua and E. resinifera, were completely resistant while two provenances (E. acmenoides, E. drepanophylla) were highly susceptible. Inoculation of detached leaves of 46 provenances of 16 eucalypt species showed that Cylindrocladium quinqueseptatum, Cylindrocladium gracile and Cylindrocladium ilicicola differed in pathogenicity, with Cylindrocladium gracile being the most and Cylindrocladium ilicicola the least pathogenic species (Sharma and Mohanan 1992b). Provenances within eucalypt species sometimes differed widely in their reactions to the three pathogens. For example, while three of the seven provenances of E. tereticornis were resistant to all three fungi, one provenance was susceptible to both Cylindrocladium quinqueseptatum and Cylindrocladium gracile and highly susceptible to Cylindrocladium ilicicola. Among four provenances of E. deglupta only one was rated as resistant, although in other studies the species was regarded as being resistant (Sehgal 1983; Jayashree et al. 1986). In a study of damping-off in 40 provenances of 17 eucalypt species there was variation both within and between species in resistance to Cylindrocladium gracile and Cylindrocladium ovatum (as Cylindrocladium scoparium). Five provenances were moderately resistant to Cylindrocladium gracile, seven were moderately resistant or resistant to Cylindrocladium ovatum and 12 were moderately resistant or resistant to both fungi (Blum et al. 1992). Cylindrocladium gracile was less pathogenic than Cylindrocladium ovatum (as Cylindrocladium scoparium) in leaf inoculations of several eucalypt species (Blum and Dianese (1993). These studies added C. citriodora and E. pellita to the list of eucalypts resistant to Cylindrocladium ovatum and confirmed field observations in Brazil that provenances of C. torelliana, E. saligna and E. microcorys were resistant to leaf blight caused by Cylindrocladium ovatum, while most provenances were resistant to Cylindrocladium gracile. Corymbia citriodora and E. tereticornis were more susceptible than E. saligna to leaf spot caused by inoculation with Cylindrocladium scoparium (probably Cylindrocladium ovatum or Cylindrocladium candelabrum) in Brazil (Cruz and Figueiredo 1960, 130

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1961). Based on foliage damage caused by Cylindrocladium scoparium (again probably Cylindrocladium ovatum or Cylindrocladium candelabrum) following both natural infection and artificial inoculation in Costa Rica, de Segura (1970) concluded that a Eucalyptus hybrid from Bangalore was very susceptible, E. alba and E. saligna moderately susceptible, C. maculata and E. grandis slightly susceptible and E. deglupta highly resistant. Considerable variation in susceptibility to leaf spot and stem lesions caused by Cylindrocladium quinqueseptatum was observed following inoculation of 10 eucalypt species (Bolland et al. 1985). Eucalyptus cloeziana and E. sphaerocarpa were the most susceptible to both forms of disease, while C. citriodora, C. maculata, C. tessellaris and E. nicholii were among the less susceptible species. Although in the laboratory all provenances of E. deglupta were susceptible to infection by Cylindrocladium quinqueseptatum, they differed in the severity of defoliation sustained in the field (Arentz 1991). Five of eight provenances of E. grandis and three of seven provenances of E. tereticornis were moderately resistant to Cylindrocladium quinqueseptatum in a study of nine-month-old seedlings (Mohanan and Sharma 1986a). Seedlings of highly susceptible provenances died after ten to 15 days due to multiple infections of leaves, stems and apical shoots, while seedlings of the moderately resistant provenances recovered from infection. There was wide variation in the pathogenicity of five monoconidial isolates of Cylindrocladium quinqueseptatum on 11 provenances in seven eucalypt species (Sharma and Mohanan 1991b). There was a differential interaction between the isolates and provenances based on susceptibility ranking of the different provenances to the five isolates and seven provenances were suggested as a set of differential hosts for identifying pathotypes of Cylindrocladium quinqueseptatum.

8.3.4

Anthracnose diseases (Colletotrichum gloeosporioides)

The only anthracnose pathogen reported from eucalypts in nurseries is the ascomycete Glomerella cingulata (Stoneman) Spauld. & H.Schrenk and its anamorph Colletotrichum gloeosporioides (Penz.) Penz. & Sacc. This fungus is distributed worldwide, although it is more abundant in the tropics and

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subtropics than in temperate regions (Mordue 1971). The species was found to be common in the phylloplane of E. viminalis (Cabral 1985). It can cause a serious blight of eucalypt seedlings, particularly during wet weather (Brown and Wylie 1991). The pathogen caused a conspicuous leaf spot of E. deglupta in nurseries and plantations in Papua New Guinea (Arentz 1991). It is regarded as an important pathogen of eucalypt cuttings and seedlings in nurseries in Natal, South Africa (Viljoen et al. 1992) and Glomerella cingulata was reported as the cause of death of small seedlings of E. cladocalyx in Tanzania (Gibson 1975). Discrete, round, light brown lesions, usually surrounded by a red-purple border, are formed on infected eucalypt leaves (Viljoen et al. 1992). As lesions expand, concentric rings of acervuli and yellowish to pinkish conidial masses are often visible and the leaves may become yellow and abscise. During wet weather, pink conidial masses exuding from the acervuli break through the leaf surfaces and can be seen easily with a hand lens (Berry 1989). In general, the species persists on and in seed, infected leaf and twig trash, and cankered intact twigs, and in other hosts and soil. It is dispersed locally by water splash, air currents, insects or plant-to-plant contact (Mordue 1971; Berry 1989; Viljoen et al. 1992). The disease is most serious under conditions of high moisture and temperature (Mordue 1971). During rainy periods in the spring, large numbers of ascospores are discharged and are spread by wind or rain splash onto young, developing leaves of seedlings where they germinate and invade under moist conditions (Berry 1989). Rapid increase and spread of anthracnose during summer and autumn occur by wind and rain-splash dispersal of conidia, which are produced in large numbers in the acervuli (Berry 1989).

8.3.5

Diseases caused by Coniella species

Several species of the pycnidial genus, Coniella, have been reported from eucalypts in nurseries, including Coniella castaneicola (Ellis & Everh.) B.Sutton on E. camaldulensis and E. globulus in South Africa (Viljoen et al. 1992), Coniella fragariae (Oudem.) B.Sutton on Eucalyptus spp. in India (Sharma 1986) and Coniella granati (Sacc.) Petr. & Syd. which affected one-month-old to two-month-old seedlings of E. tereticornis in two nurseries in India, where it killed up to 25% of seedlings (Sharma et al. 1985).

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Pathogenicity of both Coniella fragariae and Coniella castaneicola was established by Sharma et al. (1985) using three-month-old container seedlings of Eucalyptus spp. These fungi also cause disease on older eucalypts and are described more fully in Chapter 9.

8.3.6

Diseases caused by Fusarium species

Fusarium avenaceum, Fusarium longipes, Fusarium oxysporum and Fusarium solani cause damping-off in eucalypts and there have been several reports of Fusarium species associated with root rots and wilts of eucalypt seedlings. A nursery wilt of saplings and two-year-old plants of E. gomphocephala was caused by Fusarium oxysporum forma eucalypti Arya & G.L.Jain (Arya and Jain 1962) and a root rot of seedlings in California was attributed to Fusarium oxysporum var. aurantiacum (Link.) Wollenw. (correct name Fusarium oxysporum) (Hepting 1971). Fusarium solani was isolated from the roots of wilted seedlings of E. camaldulensis in Pakistan (Mahmood 1971). Both Fusarium oxysporum and Fusarium solani were associated with nursery root rot of E. deglupta in the Philippines (Kobayashi and De Guzman 1988). Fusarium spp., along with Cylindrocladium spp. and Rhizoctonia solani, were involved in a rot of eucalypt cuttings in glasshouses (Ferreira and Muchovej 1991). Fusarium oxysporum was associated with a vascular wilt of young E. grandis in plantations in Kerala and inoculation studies showed that nine-month-old seedlings were susceptible (Sharma et al. 1985). The pathogen caused brown discolouration of the vascular tissues of roots and stems of one-year-old and two-year-old seedlings of E. grandis. Fusarium sambucinum Fuckel caused root rot of eucalypts in plantations in India and was shown to be pathogenic to five-month-old seedlings of E. deglupta (as E. naudinia, presumably E. naudiniana) (Sushil Sharma et al. 1986). The pathogen caused brownish discolouration of roots just below the soil surface and after three weeks the roots became sticky, leaves turned yellow and abscissed and the whole plant wilted. Fusarium oxysporum forma eucalypti caused wilt of E. gomphocephala which began as a slight drooping of the top of the plant and was followed by general yellowing, drooping of all foliage and ultimate drying of the foliage (Arya and Jain 1962). On the basal portion of affected plants, brown or black coloured streaks were clearly visible 131

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under the bark and the tap root just below the soil surface and lateral roots turned black. Mycelium was present in xylem vessels. In naturally affected plants (6 months to 2 years old) wilting and death of affected plants occurred slowly. Some affected plants showed yellowing of the foliage but were not killed; such plants often regained normal vigour under altered environmental conditions. Eucalyptus gomphocephala and E. rudis were susceptible to Fusarium oxysporum forma eucalypti while C. citriodora, E. camaldulensis, E. melanophloia, E. paniculata, E. robusta and E. tereticornis were resistant. Fusarium species are widely distributed in soil and organic substrates (Booth 1971). In the absence of hosts, most species remain dormant as chlamydospores in soil or decaying organic matter such as roots. As a result, roots of diseased seedlings from previous crops are likely to be a major source of inoculum (Johnson et al. 1989). Contaminated containers that are reused for several crops of seedlings are an important source of Fusarium inoculum in nurseries (James et al. 1991). Species of Fusarium and the other fungi that adversely affected rooting of eucalypt cuttings in Brazil occurred in field soil that contaminated the cuttings or in glasshouse soil and were dispersed by rain or irrigation water (Ferreira and Muchovej 1991). Spores of Fusarium are usually disseminated by water splash, although some are dispersed by air currents, particularly within glasshouses (James et al. 1991).

8.3.7

Hainesia leaf and shoot blight

Most reports of this disease from eucalypts have been as one of its two coelomycete synanamorphs, Hainesia lythri (Desm.) Höhn. or Pilidium concavum (Desm.) Höhn. rather than as the discomycete teleomorph Discohainesia oenotherae (Cook & Ellis) Nannf. [syn. Pezizella oenotherae (Cook & Ellis) Sacc.]. Hainesia lythri forms separate, pale brown conidiomata which are initially globose but become cupulate to discoid at maturity (Palm 1991). Conidia are one-celled, 5–7.5 × 1.5–2 micrometres, hyaline, smooth, thin-walled, cymbiform to allantoid, acute at each end and often guttulate. Pilidium concavum has black, hemispheric, non-ostiolate conidiomata in which the hymenial layer is produced within a locule formed in an erumpent, subcuticular or subepidermal stromatic layer (Palm 1991).

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Hainesia lythri has a worldwide distribution on a wide range of plants, including tree species (Shear and Doige 1921; Sutton and Gibson 1977; Maas 1984). It has been reported from eucalypts in Australia, Africa, south-east Asia and South America. Although the fungus is mainly a problem in forest nurseries, it has been recorded on plantation grown trees in south-east China and Indonesia (B.N. Brown, unpubl. data). A leaf blight caused by the fungus severely damaged a wide range of eucalypt species growing in nurseries in South Africa during 1982 to 1984 (Lundquist and Foreman 1986). The species is common in Brazil as a saprophyte on eucalypt leaves and stems and it caused leaf blight on two-month-old C. citriodora seedlings damaged by fertiliser (F.A. Ferreira, unpubl. data). Lesions develop on expanding leaves of young seedlings and appear as a light brown to tan marginal scorch, resembling drought damage (Lundquist and Foreman 1986). On young plants, the lesions extend into and down the stem, turning it dark brown to black. On older seedlings, symptoms first appear as distinct light brown to dark tan leaf spots (1–5 mm in diameter) more or less evenly distributed over the leaf surface; some seedlings show dieback, often with adventitious shoots developing near the root collar. Leaf symptoms caused by Hainesia lythri often exhibit a rosette pattern of varying shades of brown, apparently due to the convergence of separate leaf spots. Although conidiomata formed on lesions are mostly sessile, stalked conidiomata have been observed on eucalypt leaf spots in plantations in Queensland and south-east China (B.N. Brown, unpubl. data). In inoculation tests, lesions developed only on leaves that had been wounded and the disease developed most rapidly at 25°C, which is consistent with the observation that the disease is most common in summer (Lundquist and Foreman 1986). The occurrence of the disease in nurseries was related to burning of leaves by fertiliser application, and to overhead irrigation, which provided free water for infection. The practice of propagating eucalypts via cuttings from clonal hedges contributed to the relative importance of this pathogen in South Africa (Lundquist and Foreman 1986). Phatak and Payak (1965) observed that Hainesia lythri is a weak pathogen, infecting only through wounds, and they suggested that soil or sand particles may cause

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abrasions through which it can infect. In a forest nursery in south-east Queensland, however, Hainesia lythri infected eucalypts without any evidence of wounding (B.N. Brown, unpubl. data). The fungus, as Hainesia lythri, has been recorded from the following eucalypt species in nurseries: C. maculata, E. camaldulensis, E. cloeziana, E. diversicolor, E. fastigata, E. fraxinoides, E. grandis, E. macarthurii, E. melliodora, E. microcorys, E. nitens, E. oreades, E. smithii, E. tereticornis and E. grandis × E. urophylla hybrid (Lundquist and Baxter 1985; South African Forestry Research Institutue 1985; Lundquist and Foreman 1986; Viljoen et al. 1992; B.N. Brown unpubl. data). All but E. grandis and the hybrid were confirmed as hosts by seedling inoculation (Lundquist and Foreman 1986).

8.3.8

Diseases caused by Phaeophleospora (Kirramyces) species

The coelomycetes Phaeophleospora epicoccoides (Cooke & Massee) Crous, F.A.Ferreira & B.Sutton [syn. Kirramyces epicoccoides (Cooke & Massee) J.Walker, B.Sutton & Pascoe, Cercospora epicoccoides Cooke & Massee, Hendersonia grandispora McAlpine, Phaeoseptoria eucalypti Hansf. emen. J.Walker, Phaeoseptoria luzonensis Tak.Kobay.; Walker et al. 1992; Crous et al. 1997] and Phaeophleospora eucalypti (Cook & Massee) Crous, F.A.Ferreira & B.Sutton [syn. Kirramyces eucalypti (Cooke & Massee) J.Walker, B.Sutton & Pascoe, Cercospora eucalypti Cooke & Massee, Pseudocercospora eucalypti (Cooke & Massee) Y.L.Guo & X.J.Liu, Septoria normae Heather nom. inval., Septoria pulcherrima Gadgil & M.Dick, Stagonospora pulcherrima (Gadgil & M.Dick) H.J.Swart; Walker et al. 1992; Crous et al. 1997] commonly cause leaf diseases of eucalypts in native forests and plantations (see Chapter 9) but they also cause problems in eucalypt nurseries. Phaeophleospora epicoccoides is common in eucalypt nurseries in eastern Australia but it appears to be of no economic significance (Brown and Wylie 1991). However, a serious leaf blight of several eucalypt species in nurseries was caused by the fungus in north-west India (Jamaluddin et al. 1985) and it caused mortality of young plants in Malawi (Chipompha 1987). Although it was reported that this fungus was present, apparently causing little or

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no damage, in most clonal hedge banks in South Africa (Crous 1989), Knipscheer et al. (1990) noted that it could cause death of seedlings and trees in clonal hedges. In Brazil, the disease occurs only on seedlings more than four months old and is not regarded as a problem providing nursery stock is not held past the usual nursery period (5 months) (Ferreira and Muchovej 1991). According to Magnani (1965) young eucalypt nursery plants were unaffected by Phaeophleospora eucalypti (as Cercospora eucalypti) but Raddi et al. (1991) reported that eucalypts in the nursery sometimes become infected by certain weak parasites, including Phaeophleospora eucalypti, when they were under stress due to cold winds. Leaf spot caused by Phaeophleospora eucalypti was found periodically in eucalypt nurseries in New Zealand, but was not considered to be of economic importance (Ray 1991). There must be considerable doubt as to the actual pathogen that has been identified as Cercospora eucalypti (correct name Phaeophleospora eucalypti) in some of these reports, as some have fruiting bodies illustrated as Cercospora-like hyphomycetes rather than as pycnidia characteristic of the coelomycete genus, Phaeophleospora.

8.3.9

Charcoal rot and ashy stem blight (Macrophomina phaseolina)

Macrophomina phaseolina, often reported in the literature under the name of its mycelial form, Rhizoctonia bataticola (Taubenh.) E.J.Butler, is one of the fungi responsible for damping-off in eucalypts. It is also causes root rot (known as charcoal rot) and ashy stem blight of nursery seedlings and young trees. It is a plurivorous species which is widespread in the tropics and subtropics (Holliday and Punithalingam 1970; Holliday 1980). As a soilborne pathogen, Macrophomina phaseolina is a potential problem in soil-based systems but not in hygienic container systems using sterilised container mixes. Macrophomina phaseolina caused wilting of aerial parts and swelling, splitting and gum (possibly kino) production at the crowns of 13-month-old nursery plants of E. globulus in South America (de Segura 1969). It also caused a serious root and stem rot of E. camaldulensis, E. tereticornis and Eucalyptus hybrid seedlings up to five months old in forest

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nurseries in India (Soni et al. 1985; Jamaluddin et al. 1987). The fungus invaded through the roots and spread inside the parenchymatous tissue of the pith and medullary region, producing aggregations of black compact hyphae and sclerotia (Jamaluddin et al. 1987). The infected roots and the stem had a charred appearance due to development of black sclerotia and pycnidia on the surface. Leaves became yellow, then brown, and then shrivelled and dry, leading to death of the seedlings. Mortality of the seedlings varied in different localities and was higher (50%) in nursery beds than in polythene bags (5% to 15%). Sclerotia are black, smooth, hard and 0.1 to 1 millimetre in diameter (they may be larger in culture) (Holliday and Punithalingam 1970). Pycnidia are dark brown, immersed, becoming erumpent, 100 to 200 micrometres in diameter and open by an apical ostiole. Conidia are one-celled, hyaline, ellipsoid to obovoid and 14–30 × 5–10 micrometres. Macrophomina phaseolina invades immature, unthrifty, wounded or senescent roots and healthy plants growing in good conditions are not likely to be seriously affected. The disease is most severe at high temperatures (30°C–39°C), under dry conditions and when plants have been infected by other pathogens (Holliday and Punithalingam 1970; Holliday 1980). The fungus is spread via plant debris in soil (Holliday and Punithalingam 1970). It survives as sclerotia (Holliday 1980) and these are probably the main source of infection although conidia also induce disease (Holliday and Punithalingam 1970). The fungus is reported to be seedborne on some eucalypts (see Chapter 7) and a seedborne isolate was pathogenic on Eucalyptus (Saxena 1985). However, it is difficult to explain the presence of soilborne Macrophomina phaseolina in Eucalyptus seed, which is produced many metres above ground, except by contamination during seed collection or processing.

8.3.10 Mycosphaerella leaf and shoot blight Of the many Mycosphaerella species pathogenic on eucalypt foliage (see Chapter 9), four have been reported from eucalypt nurseries. These are Mycosphaerella cryptica (Cooke) Hansf., Mycosphaerella nubilosa (Cooke) Hansf., Mycosphaerella parkii Crous, M.J.Wingf., F.A.Ferreira & Alfenas and Mycosphaerella swartii R.F.Park & Keane [as Sonderhenia eucalyptorum 134

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(Hansf.) H.J.Swart & J.Walker] (Dingley 1969; New Zealand Forest Research Institute 1977; van Dorsser 1981; Dick 1982, 1990; Keane et al. 1981; Marks et al. 1982; Crous 1989; Crous et al. 1989c, 1991, 1993d; Brown and Wylie 1991; Ray 1991). Mycosphaerella cryptica and M. nubilosa may cause serious damage to foliage and tender shoots of E. obliqua and E. regnans in nurseries and may sometimes kill seedlings (Marks et al. 1982). Early attack by Mycosphaerella spp. can greatly affect the form of the more susceptible host species and repeated dieback of shoots in the early stages of growth can result in a stunted, bushy tree with multiple leaders (Dick and Gadgil 1983).

8.3.11 Root and collar rots caused by Pythiaceae Species of Phytophthora and Pythium commonly cause damping-off in eucalypt seedlings in nurseries and they also cause diseases of older seedlings, including root and stem rots. Surprisingly, although Ph. cinnamomi is the cause of the most serious disease of eucalypts in native forests in southern Australia (see Chapter 11) and was shown to be pathogenic on seedlings of 150 eucalypt species (Titze and Palzer 1969, 1970; Podger and Batini 1971), it only rarely causes disease of eucalypts in nurseries. In south-east Queensland, Ph. cinnamomi was associated with root rot and deaths of containergrown E. pilularis and also with establishment deaths of diseased seedlings that were used for outplanting (Brown and Wylie 1991). When diseased E. obliqua seedlings were used for plantation establishment in Victoria, 27% of a sample of young trees died and 36% were dwarfed, with small leaves and brittle tops that were subject to wind damage (Weste 1980). Phytophthora cinnamomi was recorded on nursery stock of C. citriodora, E. fastigata, E. lehmannii and a Eucalyptus sp. in South Africa (Von Broembsen 1984) and caused a collar rot of C. ficifolia seedlings in New Zealand (Gilmour 1966). Phytophthora cryptogea was associated with root rot of containergrown C. ficifolia in a nursery in Western Australia (Hardy and Sivasithamparam 1988). A survey of container-grown seedlings showing decline or unthriftness from 12 nurseries in the North Island of New Zealand showed that several species of Pythium were associated with

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diseased roots of E. cinerea (Pythium afertile Kanouse & T.Humphrey, P. irregulare, P. spinosum, Pythium splendens Hans Braun), E. leucoxylon (sphaerosporangic forms of Pythium) and a Eucalyptus sp. (Pythium aquatile Höhnk) (Robertson 1973, 1980). A stem disease of Eucalyptus and other seedlings in a nursery in Tasmania was caused by Phytophthora cactorum (Lebert & E.Cohn) J.Schröt., Phytophthora citricola Sawada and Pythium anandrum Drechsler (Wardlaw and Palzer 1985). The disease occurred in small, discrete patches of seedlings and caused a stem rot immediately above the junction of the leaf axil and the main stem. The stem rot extended predominantly up the stem and along the leaf midribs, leading to crown death distal to the lowest point of stem infection. Marks and Kassaby (1974) established that P. ultimum, P. irregulare and Pythium debaryanum R.Hesse were pathogenic on small eucalypt seedlings but that neither these species nor Ph. drechsleri Tucker could kill E. sieberi at the intermediate growth stage. By contrast, Ph. cinnamomi was highly pathogenic, rapidly killing seedlings and saplings. In another study, Phytophthora megasperma Drechsler, Ph. drechsleri and Ph. cryptogea were mildly injurious to E. obliqua and E. sieberi, killing a few intermediate-aged seedlings (Marks and Kassaby 1976). The use of commercial enzyme-linked immunosorbent assay (ELISA) test kits for Phytophthora and Pythium spp. (Ali-Shtayeh et al. 1991; Benson 1991) now offers the possibility of diagnosing these diseases without having to isolate the fungi from diseased plant tissue, or from soil or water samples. Although pythiaceous fungi usually attack only young root tissue of eucalypts (as in damping-off) or the undifferentiated root apices, depending on the species of pathogen and host, infection may spread from young roots into older roots and even into the stem, resulting in root and stem lesions or cankers. A detailed discussion of the root and stem symptoms produced by Ph. cinnamomi can be found in Chapter 11. In the nursery context, species of Phytophthora and Pythium, as suggested by the common name ‘water moulds’, are favoured by high soil water content or

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free water. They can spread into and within nurseries through movement of diseased plants, infested soil or contaminated water. Phytophthora cinnamomi became a serious problem in bare-root Pinus nurseries in Queensland and it is likely that the use of pine needle litter from existing plantations as a source of mycorrhizal inoculum for new nurseries effectively spread the fungus. Robertson (1973) surveyed the major components of nursery potting mixtures in New Zealand and recorded Pythium spp. from one of 23 soil samples and 13 of 20 sand and pumice samples, but from no samples of a local peat or the roots of plants growing in the area. For the sand and pumice, the numbers of Pythium propagules ranged from six to about 5000 per gram and where the organic content of the sand was high, the Pythium populations tended to be high. In view of these results, any plant and soil material introduced into a nursery should be carefully screened for potential pathogens. Irrigation water is an important potential source of inoculum for species of Pythium and Phytophthora in a nursery. In a particular instance in Victoria, disease in nursery stock of E. obliqua was due to Ph. cinnamomi, Ph. cryptogea, Phytophthora spp. and three species of Pythium in a contaminated water supply used for seedling irrigation (Kassaby 1985). Wardlaw and Palzer (1985) considered that the most likely source of Phytophthora spp. and P. anandrum which caused a stem disease of nursery seedlings, including Eucalyptus species, in Tasmania was the untreated water supply from a local river. A disease in transplanted seedlings of several species of Eucalyptus caused by Phytophthora nicotianae Breda de Haan var. nicotianae in Italy was associated with sprinkler irrigation (Belisario 1990, 1993).

8.3.12 Powdery mildews Powdery mildews are obligate, biotrophic parasites which produce white, powdery fungal growth, consisting of superficial mycelium, conidiophores and chains of conidia, on the surface of leaves or young shoots. They can cause significant nursery losses when not recognised and promptly treated (Josiah and Allen-Reid 1991). Although powdery mildews rarely kill eucalypt seedlings, they can cause severe leaf distortion, shoot discolouration and reduction in growth of nursery stock (Magnani 1964; Marks 1981; Marks et al. 1982; Brown and Wylie 1991; De Guzman et al. 1991). In Brazil, powdery mildew is common on juvenile foliage of 135

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six-month-old to 12-month-old seedlings of C. citriodora, causing defoliation and brooming (Ferreira and Muchovej 1991). In southern India, powdery mildew causes distortion, necrosis and ultimately leaf fall on eucalypt hybrid seedlings (Sehgal et al. 1975).

eucalypts are well known on other plants [e.g. Erysiphe polyphaga Hammarl. on cucumber and tobacco, Sphaerotheca aphanis (as Sphaerotheca alchemillae) on strawberries and Sphaerotheca pannosa on roses] and are likely to have transferred to eucalypts from other hosts.

Powdery mildews are most commonly found on young eucalypts growing under intensive cultivation, such as in nurseries or glasshouses, and are rare on eucalypts under field conditions (Heather and Griffin 1978). Mildew can be particularly prevalent on young seedlings and on species from drier regions growing in glasshouses or in wetter regions (Heather 1961). Batches of E. perriniana and E. gunnii growing in a nursery in England became severely infected by powdery mildew (Glasscock and Rosser 1958). In Tasmania, the species most heavily infected is E. nitens and infection occurs in glasshouses or under 50% shade (Wardlaw and Phillips 1990); under 34% shade the disease is less serious and it is undetectable in open beds. Walker (1983) pointed out that all records of conidial powdery mildews on 12 species of eucalypts in Australia were on plants growing in glasshouses, gardens or nurseries; to his knowledge, there were no records of powdery mildew on eucalypts growing in natural communities. There have been no subsequent reports contradicting this statement.

In 1977, Boesewinkel wrote that traditional taxonomy of powdery mildews was based on cleistothecial characteristics and that little use was made of the conidial state, which had not been extensively studied. Takamatsu et al. (1998) also wrote that the anamorph has been neglected. However, recent studies of aspects of the ribosomal DNA (Takamatsu et al. 1998) and morphological characteristics of the anamorphs (Ialongo 1993; Cook et al. 1997) suggest that this state may become more significant in the taxonomy of these fungi. As powdery mildews are most frequently found in the conidial state, many collections are identified on a host basis, and while the identity of the host plant can be a valuable aid to identification, many plants can be infected by more than one species of powdery mildew and in some instances, several species of powdery mildew can occur simultaneously on the one plant, as discussed below. Boesewinkel (1977) developed a key for the identification of species of powdery mildew based on appearance of mycelium, appressoria, fibrosin bodies, haustoria, production of conidia (singly or in chains), conidial characters (size, shape, germination), basal septum of conidiophores and shape and size of conidiophore cells. Detailed descriptions of Erysiphe cichoracearum, Sphaerotheca fuliginea, Sphaerotheca macularis and Sphaerotheca pannosa are given by Kapoor (1967a, 1967b) and Mukerji (1968a, 1968b), respectively.

Seven species of powdery mildew have been identified from eucalypts, these being Erysiphe cichoracearum DC. (anamorph: Oidium asterispunicei Peck; Farr et al. 1989), Erysiphe orontii Castagne emen. U.Braun, Erysiphe paniculata (identity uncertain), Sphaerotheca aphanis (Wallr.) U.Braun [including Sphaerotheca alchemillae (Grev.) L.Junell], Sphaerotheca fuliginea (Schltdt.:Fr.) Pollacci, Sphaerotheca macularis (Wallr.:Fr.) Lind and Sphaerotheca pannosa (Wallr.:Fr.) Lév. (anamorph: Oidium leucoconium Desm.; Hanlin 1990) as well as numerous records naming the pathogen only as ‘Oidium sp.’. Boesewinkel (1981) demonstrated the synonymy of Oidium eucalypti Rostr., commonly recorded from eucalypts in various parts of the world, and Sphaerotheca pannosa. Ferreira (1989) suggested that the name Oidium eucalypti should not be used as a general name for Oidium spp. reported on eucalypts as has frequently happened in Brazil (and possibly elsewhere). The powdery mildews reported from

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Three morphologically different species of powdery mildew caused spotting and malformation of leaves and shoots of five species of Eucalyptus in a nursery in Auckland, New Zealand (Boesewinkel 1981). Sphaerotheca aphanis (as Sphaerotheca alchemillae) occurred from February to October on glasshouse grown E. albens, E. crebra, E. paniculata and E. tereticornis; Sphaerotheca pannosa was found from May to October on outside grown E. albens, E. moluccana and E. tereticornis and glasshousegrown E. moluccana, and Erysiphe polyphaga (a species similar to Erysiphe cichoracearum) was found during a short period in May on outside-

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grown E. crebra and E. moluccana. In a few instances, leaves of E. albens that were infected by Sphaerotheca pannosa became simultaneously infected by Sphaerotheca aphanis on the same or opposite surface and in one case, an outside-grown plant of E. moluccana was found to be simultaneously infected by Erysiphe cichoracearum and Sphaerotheca pannosa. Therefore, careful examination of infected material is necessary for correct identification of powdery mildews on eucalypts. During inoculation experiments, Sphaerotheca aphanis (as Sphaerotheca alchemillae) from E. albens or E. crebra was successfully transferred to Carica papaya L. and Fragaria sp. on which it caused moderate and strong infection, respectively, and Sphaerotheca pannosa was transferred from E. moluccana to Prunus armeniaca L., Punica granatum L., Rosa sp. and Rosa multiflora Thunb. ex Murray (Boesewinkel 1981). In Brazil, it was shown that Sphaerotheca pannosa from both C. citriodora and rose (Rosa sp.) and Erysiphe cichoracearum from Dahlia sp. were able to infect 40-day-old E. pellita (Silva 1994). Infection is caused by conidia that are released in greatest numbers near midday and are dispersed by air currents. The conidia can germinate on dry surfaces, even when atmospheric humidity is low—germination is inhibited by free water. Many powdery mildews produce a new generation of spores in four to six days under favourable conditions (Sinclair et al. 1987). Multiple overlapping disease cycles may develop on plants that continue to produce succulent shoots, as occurs in nurseries continuously producing batches of planting material (Sinclair et al. 1987). There is some evidence of host specificity of powdery mildew on eucalypts. Eucalyptus tereticornis and provenances of E. pellita and E. urophylla were highly susceptible to an isolate of Oidium sp. from E. tereticornis while provenances of E. cloeziana, E. microcorys and E. pilularis were resistant to the same isolate (Blum et al. 1991).

8.3.13 Eucalypt rust (Puccinia psidii) The rust Puccinia psidii G.Winter was described originally from guava (Psidium guajava L.) and has transferred to eucalypts grown as exotics in South America (Walker 1983; Coutinho et al. 1998). It causes damage to a limited number of Corymbia

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and Eucalyptus species in the nursery (Gibson 1975; Reis and Hodges 1975; Navaratnam 1986; Ferreira and Muchovej 1991) and is the main quarantine concern for eucalypts in Australia. There has been an unconfirmed report of Puccinia psidii on Eucalyptus in Taiwan (Wang 1992) although this occurrence does not appear to have developed into an established presence on the island (Coutinho et al. 1998). Under nursery conditions in Brazil, Puccinia psidii is restricted to highly susceptible hosts, particularly E. cloeziana, a few provenances of E. grandis and E. nigra (recorded as E. phaeotricha) (Ferreira and Muchovej 1991). A provenance of E. grandis which had been extensively planted in Brazil up to 1980 is no longer used because of its susceptibility to the rust (Ferreira and Muchovej 1991). On E. cloeziana in nurseries in Brazil, Puccinia psidii produces abundant yellow uredinia on the tender stems and twigs and about 14 days after disease onset, tender parts of diseased seedlings become necrotic and dry (Ferreira and Muchovej 1991). However, the rust is considered a more important problem on plants in the field than in the nursery (see Chapter 9).

8.3.14 Blight caused by Sporothrix pitereka Sporothrix pitereka (J.Walker & Bertus) U.Braun (syn. Ramularia pitereka J.Walker & Bertus; Braun 1995) is a white hyphomycete that causes leaf spots, stem lesions and distortion and twisting of leaves and young shoots of a few eucalypt species (Walker and Bertus 1971). Confirmed records of the fungus are all from Australia, where it causes disease in seedlings over three months old in nurseries and on planted trees up to two years old (see Chapter 9). Leaf spots are brown with a thin purple margin and are from one to two millimetres in diameter up to large irregular areas that often develop along one edge and result in distortion of the leaf. Large infected areas often develop along the midvein. Sunken brown lesions up to 1.5 centimetres long have been seen on stems and leaf petioles. Sporulation occurs abundantly on all diseased tissues, but on leaf spots it is more prominent on the abaxial surface. Diseased shoots appear shining white due to massive production of conidiophores which push up and rupture the epidermis and waxy cuticle. The erumpent pustules are closely packed on

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the affected area, with some coalescence of adjacent pustules. The pustules are composed of a dense layer of conidiophores borne on stromata within the host tissues. On shoots, the pustules rupture the epidermis and cuticle, and are separated by host tissue fragments, while on leaves the conidiophores are formed on substomatal stromata and emerge in clusters through stomata. Conidiophores are non-septate, hyaline and up to 50 micrometres long and 2–2.5 micrometres wide. Conidia are borne singly at the tip of the conidiophore which grows on around the conidial scar; older conidiophores may have up to 14 or more scars. Conidia are hyaline, smooth, strongly vacuolate, very variable in size and shape, generally clavate to elongated-clavate, often cylindrical to narrowly pyriform and measure 5–20 × 2.5–6.5 micrometres. The fungus grows slowly but sporulates readily in culture. Recorded hosts of Sporothrix pitereka are mostly from the genus Corymbia (C. citriodora, C. eximia, C. ficifolia, C. maculata, C. tessellaris) and section Adnataria of the subgenus Symphyomyrtus of Eucalyptus (E. crebra, E. drepanophylla, E. melanophloia, E. crebra x E. melanophloia hybrid). However, the host list also includes Angophora costata. Nursery records for Sporothrix pitereka include C. eximia, C. ficifolia and C. maculata (Walker and Bertus 1971; Walker and McLeod 1972; Gibson 1975; Jacobs 1979; Brown and Wylie 1991). Seedlings of C. eximia, C. ficifolia, C. maculata and Angophora costata were successfully inoculated with Sporothrix pitereka by Walker and Bertus (1971).

8.3.15 Diseases caused by Thanatephorus cucumeris (Rhizoctonia solani) Rhizoctonia solani is frequently parasitic on young tree seedlings, causing root rots, cankers and damping-off, and is an important pathogen in forest nurseries (Browne 1968). Although primarily a soil fungus, during warm, rainy and humid conditions in the tropics and subtropics Rhizoctonia solani may spread through the tops of plants causing a disease known as web blight or thread blight (Mordue 1974a). As plants mature, they become increasingly resistant to Rhizoctonia solani at soil level. However, the fungus is still able to invade and decay the cortical tissues of some species and this decay can girdle the stem. The fungus, as Rhizoctonia solani or

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the basidiomycete teleomorph Thanatephorus cucumeris, has been recorded from many eucalypt species including E. deglupta, E. grandis and E. tereticornis (Ko et al. 1973; Gibson 1975; Reis and Hodges 1975; Bakshi 1976; Jacobs 1979; Kerala Forest Research Institute 1982; Sehgal 1983; Sharma et al. 1984, 1985; Kerala Forest Research Institute 1986; Sharma 1986; Taha et al. 1987; Kobayashi and De Guzman 1988; Arentz 1991; Brown and Wylie 1991; Ferreira and Muchovej 1991; Ferreira et al. 1991; Sharma and Mathew 1991; Sharma and Mohanan 1991a, 1992a). Web blight of eucalypts caused by Rhizoctonia solani is common in humid areas of India (Sharma and Mathew 1991). Although Rhizoctonia solani is not as important as the several species of Cylindrocladium in eucalypt nurseries in Kerala, it has the potential to cause considerable mortality in nurseries and thus cannot be ignored in any disease control strategy (Sharma and Mohanan 1991a). Web blight can occur in seed beds within two weeks of emergence, while postemergence damping-off is still occurring (Sharma et al. 1984) and both diseases can kill seedlings. Initially mycelium of the pathogen emerging from the soil grows epiphytically on the stem and leaves of a few seedlings, and from this develops the characteristic profuse mycelial growth that entangles the affected seedlings, giving the appearance of a cobweb which can best be seen early in the morning when dew droplets are visible on the mycelial strands (Kerala Forest Research Institute 1982; Sharma et al. 1984, 1985). The pathogen may also initiate infection from soil particles carried onto foliage by rain splash (Mehrotra 1990). Highly susceptible weed species, which grow luxuriantly during humid months, may also serve as a source of infection in forest nurseries and in young plantations. Sclerotia and hyphae produced on infected plants provide inoculum in the subsequent growing season if diseased seedling stock is retained in the nursery. The mycelial strands rapidly invade the host tissues, causing affected leaves to develop watersoaked lesions and become necrotic, curled, dry and brown. Affected seedlings soon wilt and die. Stem infection produces characteristic light greyish-black necrotic lesions and although young seedlings are killed outright, older ones remain alive for some time before dying (Sharma et al. 1984). This disease

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usually occurs in irregular patches and spreads rapidly under wet conditions, especially in crowded seedlings, and spreads faster during the night than the day (Kerala Forest Research Institute 1982; Sharma et al. 1984; Mehrotra 1990). Web blight may persist until the seedlings are pricked out into polythene containers (Kerala Forest Research Institute 1982; Sharma et al. 1984). The disease also occurs on seedlings at the closed foliage stage. While young plants in the nursery are susceptible to the disease, they develop resistance with age. The pathogen often produces off-white to light brown irregular sclerotia on affected stems and leaves of older (4-month-old to 5-month-old) seedlings and the Thanatephorus cucumeris stage occasionally develops on diseased stems during the rainy season at temperatures of 20°C to 23°C and relative humidities of 90% to 100% (Sharma et al. 1985). In inoculation studies, a web blight isolate of Rhizoctonia solani caused damping-off in transplanted seedlings of both E. grandis and E. tereticornis at 24°C to 27°C and either 65% to 80% or 95% relative humidity, but web blight developed only at the higher humidity (Sharma et al. 1985).

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found to be completely rotted and were dark brown instead of off-white or yellowish-brown. Occasionally the infection started from the feeder roots and proceeded to the main root and in some specimens the root collar zone was decayed. The fungus also caused a rare collar rot of E. grandis and E. tereticornis in Kerala (Sharma et al. 1984, 1985). The infection appeared near ground level in the form of watersoaked lesions on the stems of two-monthold to three-month-old seedlings and developed under conditions of high humidity and air stagnation due to crowding of seedlings. Stem discolouration was followed by the splitting of the outer bark, stem girdling, callus formation and wilting and death of seedlings. In relation to their broad concept of damping-off (see section 8.3.1), Ferreira and Muchovej (1991) demonstrated girdling caused by Rhizoctonia solani near the collar of eucalypts in the post-thinning stage. Presumably this is ‘wirestem’ or ‘soreshin’ disease as discussed by Baker (1970). Rhizoctonia solani was among the fungi that caused rotting of eucalypt cuttings (Ferreira and Muchovej 1991).

8.3.16 Diseases caused by Sclerotium rolfsii

Incidence and severity of web blight were significantly affected by various nursery practices (Sharma and Mohanan 1992a). Even with species highly susceptible to web blight, the disease was considerably reduced in the high rainfall area of north-east India by decreasing the density of seedlings in seed beds (Mehrotra 1990). It became almost inconsequential when seedlings were raised in polypots and when diseased seedlings were culled without delay. Shading also greatly influenced the development of the disease in highly susceptible species. In north-east India, the disease appeared after the start of the regular monsoon rains and was highly destructive for some weeks. High humidity and incessant heavy monsoon rains for several days followed by a prolonged period (6 to 8 days) of overcast sky provided ideal conditions for development of disease to damaging levels. Night dew on the leaves, after the rains became infrequent, contributed to the progression of the disease.

Sclerotium rolfsii Sacc., the sclerotial state of the basidiomycete Athelia rolfsii (Curzi) C.C.Ju & Kimbr. (syn. Corticium rolfsii Curzi), causes seedling blights, seedling wilts and collar, stem and foot rots of a wide variety of hosts (Browne 1968; Mordue 1974b). It is a facultative parasite capable of extensive saprophytic growth in surface layers of the soil, which, once established, can infect tree seedlings. It is one of the fungi associated with the nursery disease complex of eucalypts recognised in Kerala and although it is not as important as Cylindrocladium, it can cause high seedling mortality (Sharma and Mohanan 1991a). It has caused severe losses in weak, densely planted or poorly nourished seedlings of E. globulus in Yunnan Province, China, following monsoonal rains (Zhou Dequn and Sutherland 1993). The disease has been recorded also on eucalypt seedlings in Zhejiang Province in eastern China (Zhou Dequn and Sutherland 1993).

In Kerala, southwest India, Rhizoctonia solani caused a root rot on four-month-old to five-monthold seedlings of E. tereticornis, resulting in slow wilting of seedlings in scattered patches (Sharma et al. 1984). The root systems of affected plants were

Sclerotium rolfsii causes wilt of 1.5-month-old to two-month-old seedlings of E. grandis and E. tereticornis in Kerala (Sharma et al. 1984, 1985). The first sign of disease is the formation at the base of the stem of a white weft of mycelium which

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spreads up to the leaves and may entangle nearby seedlings. Usually stems and leaves, but not roots, are infected. Wilting of the seedlings is accompanied by the development on affected stems and leaves of smooth, spherical, off-white sclerotia which become light brown with age. Wilted seedlings turn brown and die. The disease occurs in patches and continues to affect seedlings for five to six weeks. At this stage, only the weft of mycelium may be seen on the lower portion of the stem. The fungus also caused a root rot of four-month-old to five-month-old seedlings of E. grandis (Sharma et al. 1985). Woody species rapidly become resistant with age (Browne 1968; Mordue 1974b). Disease is increased by shading and crowding which lead to increased moisture levels at the soil surface (Browne 1968; Mordue 1974b). In dry soil, infection occurs further below the soil surface and wilting is accentuated. High light intensity and temperature favoured shoot wilt of E. grandis caused by Sclerotium rolfsii (Sharma and Mohanan 1992a).

8.3.17 Miscellaneous and minor pathogens Many other pathogens have been reported occasionally from eucalypts in nurseries. Although these are mainly weak, facultative pathogens and have not caused serious problems, they should be considered as having the potential to cause problems under certain circumstances. 8.3.17.1 Crown gall (Agrobacterium tumefaciens) Crown gall caused by the bacterium Agrobacterium tumefaciens (Smith & Townsend 1907) Conn 1942 is known to occur on eucalypts under various circumstances (see Chapter 14). A severe outbreak of crown gall on E. tereticornis (reported as Mysore hybrid) in a nursery was observed by Jindal and Bhardwaj (1986). The disease was characterised by the presence of individual galls or clumps of small galls on the crowns of the seedlings. Seedlings aged from three to 12 months were susceptible, with disease incidence increasing with the age of the seedlings (Jindal and Bhardwaj 1986). However, lignotubers which are common on many eucalypts (see Fig. 2.3) could easily be mistaken for bacterial galls. 8.3.17.2 Alternaria species Alternaria tenuissima (Kunze) Wiltshire was well known in Italy on numerous species, including 140

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E. botryoides, E. globulus, E. globulus ssp. bicostata, E. globulus ssp. maidenii and E. trabutii (the hybrid E. botryoides × E. camaldulensis) (Magnani 1964). The disease caused small leaf spots surrounded by a red border and in the nursery usually caused partial, and occasionally total, defoliation. The same species caused irregular, small leaf spots on older, chlorotic (nutrient-deficient) seedlings of E. grandis in Brazil (Ferreira and Muchovej 1991). Seedlings that were kept too long in the nursery were particularly susceptible, especially if not fertilised adequately. In Argentina, Alternaria alternata affected the early development of eucalypt seedlings in soils with a very high organic matter content when temperatures were above 27°C (Salerno 1991). Leaves of Eucalyptus hybrid were found to be infected by Alternaria alternata (as Alternaria tennuis, sic = Alternaria tenuis) during a survey of nurseries in India (Mittal and Sharma 1982). The disease developed on both leaf surfaces as greyish patches that gradually turned black and formed slightly elevated pustules, leading to discolouration of the whole leaf surface and desiccation and defoliation of the plant. Alternaria alternata was one of the phylloplane fungi isolated at high frequency from different leaf types (young, mature, senescent, dry) from trees of E. viminalis in Argentina (Cabral 1985). Alternaria alternata and Alternaria tenuissima were isolated also from leaf surfaces of E. pauciflora, E. stellulata and E. regnans in Australia (Macauley and Thrower 1966; Lamb and Brown 1970; Parbery 1974; Macauley 1979) and E. globulus in India (Upadhyay 1981, 1986). Alternaria alternata was one of the fungi isolated from the bark disease associated with Cytospora eucalypticola Van der Westh. (van der Westhuizen 1965) (see Chapter 10) and the same species has been reported from eucalypt seeds (see Chapter 7). 8.3.17.3 Bartalinia terricola Bartalinia terricola Luke & S.U.Devi (Luke and Devi 1979) was reported as the cause of a foliar infection of five-month-old E. tereticornis seedlings in forest nurseries (Mohanan and Sharma 1987). The initial symptoms of the disease were small, pale brown to purple angular lesions, usually at the margin of the mature leaves. The lesions later spread and coalesced, giving rise to large necrotic areas. The infection was more severe on mature than on

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young leaves. Pathogenicity of the species was shown by inoculation of seedlings.

Hodges 1975; Sutton 1980; Crous et al. 1989a; Crous and Swart 1995).

8.3.17.4 Cladosporium herbarum

8.3.17.7 Corynespora cassiicola

During a survey of nurseries in India, the leaves of C. citriodora and Eucalyptus hybrid were found to be infected by Cladosporium herbarum (Pers.) Link (Mittal and Sharma 1982). The first symptom of the disease was the development of chlorotic patches on the leaves followed by small blackish-brownish dotlike colonies on the lower surface. Gradually the area of discolouration increased and eventually leaves dried and abscissed. This was another of the phylloplane fungi isolated at high frequencies from E. viminalis (Cabral 1985). It has also been isolated from the surface of leaves of E. stellulata and E. globulus in Australia and India (Lamb and Brown 1970; Upadhyay 1981, 1986) and it has been detected in leaf litter of E. pauciflora, E. regnans and Eucalyptus sp. in Australia and India (Macauley and Thrower 1966; Macauley 1979; Soni and Jamaluddin 1990). It was associated externally and internally with seed of Eucalyptus species in India (Reddy et al. 1982; Saxena 1985) (see Chapter 7).

Corynespora cassiicola (Berk. & M.A.Curtis) C.T.Wei is a plurivorous fungus which is especially abundant in the tropics and usually causes a target spot disease (Ellis and Holliday 1971). Gibson (1975) reported that Corynespora cassiicola had been recorded on E. grandis in India, causing ‘spots with pale brown centre and well-defined dark brown margin, 2 to 6 mm in diameter, which in severe cases may coalesce and cause leaf cast’. Corynespora cassiicola was identified from a leaf spot disease that occurred on E. grandis seedlings in Kerala during the monsoon months (Wilson and Devi 1966). Minute, watersoaked spots were evenly distributed on the leaf lamina. Later they enlarged, becoming more or less round, two to six millimetres in diameter, with a pale-brown centre and a well-defined dark-brown margin. In severe cases, these spots coalesced and formed irregular necrotic areas that ultimately led to considerable defoliation. When they occurred along the margin or adjacent to the midrib the spots were generally oblong or linear and attained a length of 15 millimetres or more. Under conditions of high humidity the disease became very severe, resulting in withering of the young twigs. The pathogen was isolated and pathogenicity established by inoculation of young eucalypt seedlings.

8.3.17.5 Clypeophysalospora latitans Clypeophysalospora latitans (Sacc.) H.J.Swart (as Physalospora latitans Sacc.) (see Chapter 9) was reported on C. citriodora in nurseries in India (Mittal and Sharma 1979). The fungus was associated with discolouration in leaves which developed into sharp, conspicuous, black, circular spots measuring one to 2.5 millimetres in diameter. The leaves showed severe infection on both sides, became dry and finally abscissed. Even when only slightly infected, seedlings did not establish well after transplanting. 8.3.17.6 Codinaea septata Although Codinaea septata B.Sutton & Hodges was reported only from fallen leaves (‘foliis dejectis’) of Eucalyptus species in Brazil (Sutton and Hodges 1975), it was found to occur on stems and petioles of young E. grandis cuttings in South Africa, frequently in association with Cylindrocladium scoparium (Crous et al. 1990). Crous et al. (1989b) regarded it as a saprophyte or weak pathogen on eucalypts. Several other species of Codinaea have been recorded from eucalypts, mainly from leaf litter (Sutton and

8.3.17.8 Curvularia species Curvularia eragrostidis (Henn.) J.A.Mey., Curvularia geniculata (Tracy & Earle) Boedijn, Curvularia lunata (Wakker) Boedijn and Curvularia pallescens Boedijn have been reported to cause disease of eucalypt seedlings (Gibson 1975; Sharma 1986). Curvularia prasadii R.L.Mathur & B.L.Mathur was reported from E. populifolia (identity uncertain: either E. populifolia Desf. which is E. tereticornis, or E. populifolia Hook. which is E. populnea), E. tereticornis and Eucalyptus hybrid in nurseries and plantations in India, causing small, light brown lesions that later coalesced to form slightly larger, dark brown areas surrounded by chlorotic tissue (Jamaluddin et al. 1987). Premature defoliation occurred in severe cases. In the same region, Curvularia lunata infected leaves of Eucalyptus in nurseries and plantations (Jamaluddin et al. 1987). The infection usually started from the leaf margin in 141

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the form of small chlorotic areas and later these spots coalesced to form larger, ash coloured, oval to irregular lesions scattered over the lamina. Lesions were common on coppiced shoots. Curvularia lunata was found in the phylloplane of trees of E. viminalis (Cabral 1985) and E. globulus (Upadhyay 1981, 1986). Curvularia geniculata, Curvularia lunata and Curvularia pallescens have been found in, or in associated with, eucalypt seed in Australia, India and Thailand (see Chapter 7) and Curvularia lunata was one of the fungi isolated from the bark disease associated with Cytospora eucalypticola (van der Westhuizen 1965). 8.3.17.9 Drechslera spicifera and Exserohilum rostratum Two fungi, Drechslera spicifera (Bainier) Arx [as Bipolaris spicifera (Bainier) Subram.], the anamorph of Cochliobolus spicifera R.R.Nelson, and Exserohilum rostratum (Drechsler) K.J.Leonard & Suggs, emen. K.J.Leonard, the anamorph of Setosphaeria rostrata K.J.Leonard, were consistently isolated from foliar infection of three-month-old E. tereticornis in forest nurseries in Karnataka, India (Mohanan and Sharma 1986b). Infection usually began at the margin and tips of mature leaves as minute greyish brown specks that coalesced to form large necrotic areas. The pathogenicity of both fungi was confirmed by spraying conidial suspensions separately onto detached leaves of E. tereticornis and reisolating the respective fungi from lesions. Drechslera spicifera is a cosmopolitan species recorded from over 70 plant species (Mohanan and Sharma 1986b). It was isolated from the phylloplane of E. globulus (Upadhyay 1981; Upadhyay et al. 1980) and has been found in seeds of E. camaldulensis from Australia (Yuan et al. 1990). Exserohilum rostratum is associated both externally and internally with seed of Eucalyptus spp. in India (Reddy et al. 1982; Saxena 1985; Mittal et al. 1990). 8.3.17.10 Fairmaniella leprosa Fairmaniella leprosa (Fairm.) Petr. & Syd., which is discussed in detail in Chapter 9, was reported as a minor leaf pathogen of eucalypts in New Zealand nurseries (Dick 1990). 8.3.17.11 Gnomoniella destruens Barr and Hodges (1987) described a new ascomycete species, Gnomoniella destruens M.E.Barr & Hodges, 142

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as the cause of leaf and stem blight of E. globulus in a small nursery in Hawaii. While no other eucalypt species were naturally infected in the nursery, E. grandis and E. saligna were infected by inoculation. Although E. globulus seedlings were present in the nursery for most of the year, the disease occurred only from late October to December, a pattern that was consistent over several years (Barr and Hodges 1987). The fungus colonised and killed entire leaves without causing discrete leaf spots. It often invaded the stem from the sessile juvenile leaves of E. globulus and then girdled the stem, killing the plant above the lesion. Perithecia of Gnomoniella destruens formed copiously on the dead leaves and stems. The fungus was shown to be extremely pathogenic, with mature perithecia developing on inoculated stems within seven to ten days. 8.3.17.12 Harknessia species Harknessia globosa B.Sutton was found only in nurseries of the Eastern Transvaal where it caused a prominent leaf spot on young E. grandis but was considered of minor importance (Crous et al. 1989a, 1989d). Lesions were round, amphigenous, brown and five to 15 millimetres in diameter. This fungus had previously been found in Brazil and New Zealand on two species of Eucalyptus. Harknessia hawaiiensis F.Stevens & E.Young was reported from leaf spots on E. grandis and E. nitens (Viljoen et al. 1992) and Harknessia uromycoides (Speg.) Speg. from E. amygdalina in seedling nurseries in South Africa (Lundquist and Baxter 1985). Several species of Harknessia have been reported from leaf spots of older eucalypts in the field (see Chapter 9). 8.3.17.13 Pestalotiopsis disseminata A leaf blight of container-grown E. globulus and E. globulus ssp. maidenii (as E. maidenii) caused by Pestalotiopsis disseminata (Thüm.) Steyaert was reported from subtropical Yunnan Province (Zhou Dequn and Sutherland 1993). This fungus can be seedborne in eucalypts (see Chapter 7). The disease caused chlorosis of leaves and occasional brown discolouration of veins. Young stems gradually shrivelled and turned violet-brown. Severely affected seedlings were killed and the disease usually resulted in about 10% loss of seedlings. This disease has also been reported from foliage of trees in the field (see Chapter 9).

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8.3.17.14 Phomopsis eucalypti A severe leaf spot disease caused by Phomopsis eucalypti Zerova was reported in two-year-old seedlings of E. grandis, E. tereticornis, E. exserta and E. urophylla, and in five-month-old seedlings of E. tereticornis (Mohanan and Sharma 1987). The initial symptoms were minute, dull brown to purple spots which later spread and coalesced to form irregular, dark brown to purple lesions. On E. tereticornis lesions were small and restricted while on the other hosts they were fast spreading and resulted in severe infection and premature defoliation. Pathogenicity was confirmed by conidial inoculation and reisolation of the fungus from infected leaves. The original record of Phomopsis eucalypti was from living and dead eucalypt twigs from a greenhouse in the former USSR (Uecker 1988).

8.4 Principal diseases of eucalypt cuttings Increasing areas of eucalypt plantations in the tropics and subtropics are being established using cuttings derived from clonal gardens or hedge banks. In tropical Brazil, the major eucalypt growing companies have established several thousand hectares of clonal eucalypt plantations from cuttings. The cuttings (typically small stem segments) are rooted and raised in modified nursery systems. The first 40 days of cutting production is in a shadehouse, using suspended containers, or on a bed of concrete or crushed rock. It is necessary to maintain high humidities with water sprays at frequent intervals (< 5 minutes). Such conditions are likely to favour the development of fungal pathogens. Although species of Fusarium and Cylindrocladiella are pathogenic on eucalypt cuttings (Alfenas et al. 1988; Carvalho et al. 1989), the most important causes of root rot of cuttings have been Cylindrocladium scoparium, Cylindrocladium gracile and Rhizoctonia solani (Thanatephorus cucumeris). Rot of the stems of cuttings can be caused by cutting failure and by pathogen attack. Disease is evident as development of lesions on the green area of the stem. Most lesions produced by Cylindrocladium on eucalypt cuttings occur at the substrate surface and are black, often with white sporulation. Attack by Rhizoctonia solani begins as web blight followed by leaf mortality and subsequent stem rot.

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Inoculum of the pathogens causing cutting rot comes mainly from glasshouse soil or from field soil that contaminates the cuttings during their collection and transport (Ferreira and Muchovej 1991). Splash dispersal by rain or irrigation water appears to be the main method by which inoculum is spread. The diseases of clonal gardens are the same as those in young plantations (see Chapter 9). These include Cylindrocladium leaf blights, Coniella leaf spots, web blight (Thanatephorus cucumeris), anthracnose (Colletotrichum gloeosporioides), rust (Puccinia psidii), leaf blight caused by Phaeophleospora epicoccoides and leaf diseases caused by species of Mycosphaerella.

8.5 Conclusion The main effect of nursery diseases, in addition to the direct loss of planting stock, is the disruption caused to a planting program by serious losses of seedlings or cuttings in the nursery or soon after transplanting. In certain climates there is only a limited window of opportunity for transplanting into the field and if this is missed through a lack of nursery stock the program can be set back by a full year. Abiotic agencies can cause disease of eucalypts in nurseries but usually these can be readily controlled by improved management practices. The major losses of eucalypt planting material have been caused by fungi, which are often more difficult to control. Fungal diseases can occur at any time from germination (damping-off) right through to the later stages of plant growth in the nursery. They can affect all parts of the planting stock and can range from leaf spots of little consequence to plant death. In some cases, the diseases are caused by a single fungus while others, especially those involving species of Cylindrocladiella or Cylindrocladium, may be caused by a complex or succession of pathogens affecting several plant tissues and persisting over a prolonged period. As several fungi produce basically similar symptoms on eucalypts in nurseries (e.g. damping-off or shoot blight), accurate diagnosis of disease is essential as a basis for effective disease management (see Chapter 21).

8.6 References Abrahão, J. (1948). Botrytis cinerea Pers. parasitando mudas de Eucalyptus spp. O Biológico 14, 172. Alfenas, A.C., Ferreira, F.A., Barbosa, M.M., Demuner, N.L. and Carvalho, A.O. (1988). Fungos associados e

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estacas de eucalipto para enraizemento. Fitopatologia Brasileira 13, 149 (Abstract). Alfenas, A.C., Matsuoka, K., Ferreira, F.A. and Hodges, C.S. (1979). [Identification, cultural characteristics and pathogenicity of three species of Cylindrocladium isolated from leaf spots of Eucalyptus spp.]. Fitopatologia Brasileira 4, 445–459. Ali-Shtayeh, M.S., MacDonald, J.D. and Kabashima, J. (1991). A method for using commercial ELISA tests to detect zoospores of Phytophthora and Pythium species in irrigation water. Plant Disease 75, 305–311. Arentz, F. (1991). Forest nursery diseases in Papua New Guinea. In Diseases and Insects in Forest Nurseries, Proceedings of the First Meeting of IUFRO Working Party S2.07-09, Victoria, British Columbia, Canada, 22–30 August 1990. Information Report BC-X-331. (Eds J.R. Sutherland and S.G. Glover) pp. 97–99. (Forestry Canada, Pacific and Yukon Region, Pacific Forestry Centre: Victoria, British Columbia.) Arya, H.C. and Jain, G.L. (1962). Fusarium wilt of Eucalyptus. Phytopathology 52, 638–642. Baker, K.F. (1970). Types of Rhizoctonia diseases and their occurrence. In Rhizoctonia solani, Biology and Pathology. (Ed. J.R. Parmeter Jr.) pp. 125–133. (University of California Press: Berkeley.) Bakshi, B.K. (1976). Forest Pathology: Principles and Practice in Forestry. (Controller of Publications: Delhi.) Barnard, E.L. (1981). Cylindrocladium scoparium on Eucalyptus spp. in a South Florida tree nursery: Damage and fungicidal control. Phytopathology 71, 201–202. Barnard, E.L. (1984). Occurrence, impact, and fungicidal control of girdling stem cankers caused by Cylindrocladium scoparium on Eucalyptus seedlings in a South Florida nursery. Plant Disease 68, 471–473. Barr, M.E. and Hodges, C.S.Jr. (1987). Hawaiian Forest Fungi. VIII. New species in Gnomoniella and Stigmochora. Mycologia 79, 782–786. Belisario, A. (1990). A new Phytophthora disease of aerial parts of Eucalyptus species. Bulletin EPPO 20, 129–132. Abstract No. 6655 in Review of Plant Pathology 69, 810–811 1990. Belisario, A. (1993). Identification of Phytophthora nicotianae on the aerial portion of eucalypt seedlings. European Journal of Forest Pathology 23, 85–91. Bell, D.K. and Sobers, E.K. (1966). A peg, pod, and root necrosis of peanuts caused by a species of Calonectria. Phytopathology 56, 1361–1364. Benson, D.M. (1991). Detection of Phytophthora cinnamomi in azalea with commercial serological assay kits. Plant Disease 75, 478–482. Berry, F.H. (1989). Anthracnose. In Forest Nursery Pests. Agriculture Handbook No. 680. (Eds C.E. Cordell, R.L. Anderson, W.H. Hoffard, T.D. Landis, R.S.

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Smith Jr. and H.V. Toko) pp. 88–89. (USDA Forest Service: Washington, DC.) Bertus, A.L. (1976a). A fungal leaf spot and stem blight of some Australian native plants. Agricultural Gazette of New South Wales 87, 22–23. Bertus, A.L. (1976b). Cylindrocladium scoparium Morgan on Australian native plants in cultivation. Phytopathologische Zeitschrift 85, 15–25. Birch, T.T.C. (1937). A synopsis of forest fungi of significance in New Zealand. New Zealand Journal of Forestry 4, 109–125. Blum, L.E.B. and Dianese, J.C. (1993). Susceptibility of different Eucalyptus genotypes to artificial leaf inoculations with Cylindrocladium scoparium and C. clavatum. European Journal of Forest Pathology 23, 276–280. Blum, L.E.B., Dianese, J.C. and Costa, C.L. (1992). Comparative pathology of Cylindrocladium clavatum and C. scoparium on Eucalyptus spp. and screening Eucalyptus provenances for resistance to Cylindrocladium damping-off. Tropical Pest Management 38, 155–159. Blum, L.E.B., Boiteux, L.S., Dianese, J.C. and Ferreira, S.B.R.J. (1991). Greenhouse-screening of Eucalyptus provenances for resistance to Oidium sp. Fitopatologia Brasileira 16, 214–217. Boesewinkel, H.J. (1977). Identification of Erysiphaceae by conidial characters. Revue de Mycologie 41, 493–507. Boesewinkel, H.J. (1981). A first recording of rose mildew, Sphaerotheca pannosa, on three species of Eucalyptus. Nova Hedwigia 34, 721–730. Boesewinkel, H.J. (1982). Cylindrocladiella, a new genus to accommodate Cylindrocladium parvum and other small-spored species of Cylindrocladium. Canadian Journal of Botany 60, 2288–2294. Bolland, L., Tierney, J.W. and Tierney, B.J. (1985). Studies on leaf spot and shoot blight of Eucalyptus caused by Cylindrocladium quinqueseptatum. European Journal Forest Pathology 15, 385–397. Booth, C. (1971). The Genus Fusarium. (Commonwealth Mycological Institute: Kew.) Booth, C. and Gibson, I.A.S. (1973). Cylindrocladium scoparium. CMI Descriptions of Pathogenic Fungi and Bacteria No. 362. (Commonwealth Mycological Institute: Kew.) Braun, U. (1995). A Monograph of Cercosporella, Ramularia and Allied Genera (Phytopathogenic Hyphomycetes). Vol. 2. (IHW-Verlag: Munich.) Brown, B.N. and Wylie, F.R. (1991). Diseases and pests of Australian forest nurseries: past and present. In Diseases and Insects in Forest Nurseries, Proceedings of the First Meeting of IUFRO Working Party S2.0709, Victoria, British Columbia, Canada, 22–30 August 1990. Information Report BC-X-331. (Eds J.R. Sutherland and S.G. Glover) pp. 3–15. (Forestry Canada, Pacific and Yukon Region, Pacific Forestry Centre: Victoria, British Columbia.)

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Browne, F.G. (1968). Pests and Diseases of Forest Plantation Trees. (Clarendon Press: Oxford.) Cabral, D. (1985). Phyllosphere of Eucalyptus viminalis: Dynamics of fungal populations. Transactions of the British Mycological Society 85, 501–511. Carvalho, A.O., Alfenas, A.C. and Demuner, N.L. (1989). Patogenicidade de fungos isolados de estacas de eucalipto para enraizamento em casa de vegetaçäo. Fitopatologia Brasileira 14, 122 (Abstract). Chambers, S.C. (1982). List of diseases recorded on ornamentals, native plants and weeds in Victoria, before 30 June, 1980. Technical Report Series 61. (Department of Agriculture, Victoria: Melbourne.) Chipompha, N.W.S. (1987). Phaeoseptoria eucalypti: A new pathogen of Eucalyptus in Malawi. South African Journal Forestry 142, 10–12. Cook, R.P. and Dubé, A.J. (1989). Host-Pathogen Index of Plant Diseases in South Australia. (South Australian Department of Agriculture: Adelaide.) Cook, R.T.A., Inman, A.J. and Billings, C. (1997). Identification and classification of powdery mildew anamorphs using light and scanning electron microscopy and host range data. Mycological Research 101, 975–1002. Coutinho, T.A., Wingfield, M.J., Alfenas, A.C. and Crous, P.W. (1998). Eucalyptus rust: a disease with the potential for serious international implications. Plant Disease 82, 819–825. Cordell, C.E., Barnard, E.L. and Filer, T.H. Jr. (1989). Cylindrocladium diseases. In Forest Nursery Pests, Agriculture Handbook No. 680. (Eds C.E. Cordell, R.L. Anderson, W.H. Hoffard, T.D. Landis, R.S. Smith Jr. and H.V. Toko) pp. 114–117. (USDA Forest Service: Washington, DC.) Crous, P.W. (1989). South African leaf pathogens. Eucalyptus Part 1. Forestry News 4/89, 18–19. Crous, P.W. and Swart, W.J. (1995). Foliicolous fungi of Eucalyptus from Eastern Madagascar: Implications for South Africa. South African Forestry Journal 172, 1–5. Crous, P.W. and Wingfield, M.J. (1993). A re-evaluation of Cylindrocladiella, and a comparison with morphologically similar genera. Mycological Research 97, 433–448. Crous, P.W. and Wingfield, M.J. (1994). A monograph of Cylindrocladium, including anamorphs of Calonectria. Mycotaxon 51, 341–435. Crous, P.W., Knox-Davies, P.S. and Wingfield, M.J. (1989a). A summary of fungal leaf pathogens of Eucalyptus and the diseases they cause in South Africa. South African Forestry Journal 149, 9–16. Crous, P.W., Knox-Davies, P.S. and Wingfield, M.J. (1989b). A list of Eucalyptus leaf fungi and their potential importance to South African forestry. South African Forestry Journal 149, 17–29.

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Crous, P.W., Knox-Davies, P.S. and Wingfield, M.J. (1989c). Mycosphaerella nubilosa on Eucalyptus spp. in South Africa. Phytophylactica 21, 109. (Abstract). Crous, P.W., Knox-Davies, P.S. and Wingfield, M.J. (1989d). Newly-recorded foliage fungi of Eucalyptus spp. in South Africa. Phytophylactica 21, 85–88. Crous, P.W., Wingfield, M.J. and Koch, S.H. (1990). New and interesting records of South African fungi. X. New records of Eucalyptus leaf fungi. South African Journal of Botany 56, 583–586. Crous, P.W., Wingfield, M.J. and Park, R.F. (1991). Mycosphaerella nubilosa, a synonym of M. molleriana. Mycological Research 95, 628–632. Crous, P.W., Alfenas, A.C. and Wingfield, M.J. (1993a). Calonectria scoparia and Calonectria morganii sp. nov., and variation among isolates of their Cylindrocladium anamorphs. Mycological Research 97, 701–708. Crous, P.W., Wingfield, M.J. and Alfenas, A.C. (1993b). Cylindrocladium parasiticum sp. nov., a new name for C. crotalariae. Mycological Research 97, 889–896. Crous, P.W., Wingfield, M.J. and Alfenas, A.C. (1993c). Additions to Calonectria. Mycotaxon 46, 217–234. Crous, P.W., Wingfield, M.J., Ferreira, F.A. and Alfenas, A. (1993d). Mycosphaerella parkii and Phyllosticta eucalyptorum, two new species from Eucalyptus leaves in Brazil. Mycological Research 97, 582–584. Crous, P.W., Ferreira, F.A. and Sutton, B.C. (1997). A comparison of the fungal genera Phaeophleospora and Kirramyces (Coelomycetes). South African Journal of Botany 63, 111–115. Cruz, B.P.B. and Figueiredo, M.B. (1960). [Observations about a disease of Eucalyptus caused by Cylindrocladium]. Arquivas do Instituto Biológico (Sao Paulo) 27, 96–102. Cruz, B.P.B. and Figueiredo, M.B. (1961). [Importance of the fungus Cylindrocladium in eucalypt growing.] O Biológico 27, 106–108. Abstract in Review of Applied Mycology 41, 104 (1962). De Guzman, E.D., Militante, E.P. and Lucero, R. (1991). Forest nursery diseases and insects in the Philippines. In Diseases and Insects in Forest Nurseries, Proceedings of the First Meeting of IUFRO Working Party S2.07-09, Victoria, British Columbia, Canada, 22–30 August 1990. Information Report BC-X-331. (Eds J.R. Sutherland and S.G. Glover) pp. 101–104. (Forestry Canada, Pacific and Yukon Region, Pacific Forestry Centre: Victoria, British Columbia.) Dick, M. (1982). Leaf-inhabiting fungi of eucalypts in New Zealand. New Zealand Journal of Forestry Science 12, 525–537. Dick, M. (1990). Leaf-inhabiting fungi of eucalypts in New Zealand. II. New Zealand Journal of Forestry Science 20, 65–74. Dick, M. and Gadgil, P.D. (1983). Eucalyptus leaf spots. Forest Pathology in New Zealand No. 1. (Forest Research Institute: Rotorua.)

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Ramularia. Proceedings of the Linnean Society of New South Wales 96, 108–115. Walker, J. and McLeod, R.W. (1972). New records of plant diseases in New South Wales, 1970–71. Agricultural Gazette of New South Wales 83, 176–179. Walker, J., Sutton, B.C. and Pascoe, I.G. (1992). Phaeoseptoria eucalypti and similar fungi on Eucalyptus, with description of Kirramyces gen. nov. (Coelomycetes). Mycological Research 96, 911–924. Wang, W.-Y. (1992). Survey of Eucalyptus diseases in Taiwan. Bulletin of the Taiwan Forestry Research Institute New Series 7, 179–194. Wardlaw, T.J. and Palzer, C. (1985). Stem diseases in nursery seedlings caused by Phytophthora cactorum, P. citricola, and Pythium anandrum. Australasian Plant Pathology 14, 57–59. Wardlaw, T. and Phillips, T. (1990). Nursery diseases and their management at the Forestry Commission Nursery, Perth. Tasforests 2, 21–26. Weste, G. (1980). Vegetation changes as a result of invasion of forest on krasnozem by Phytophthora cinnamomi. Australian Journal of Botany 28, 139–150. Wilson, K.I. and Devi, L.R. (1966). Corynespora leaf spot of Eucalyptus grandis (Hill) Maiden. Indian Phytopathology 19, 393–394. Yuan, Z.Q., Old, K.M. and Midgley, S.J. (1990). Investigation of mycoflora and pathology of fungi present on stored seeds of Australian trees. In Tropical Tree Seed Research. (Ed. J.W. Turnbull). ACIAR Proceedings 28, 103–110. Zhou Dequn and Sutherland, J.R. (1993). Diseases of Eucalyptus forest nursery seedlings and their management in forest nurseries in Yunnan Province, China. In Diseases and Insects in Forest Nurseries. (Eds R. Perrin and J.R. Sutherland) pp. 45–49. (Institut National de la Recherche Agronomique: Paris.)

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R.F. Park, P.J. Keane, M.J. Wingfield and P.W. Crous

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Eucalypts have many foliar diseases caused by a wide range of fungi. Foliar diseases are common in native forests but are rarely destructive and have not been regarded as a concern in forest management. However, they have been a problem in eucalypt plantations and there are many examples of destructive epidemics in plantations in Australia, New Zealand, South Africa, Brazil and India. Some have involved highly specialised pathogens such as Mycosphaerella species while others have been caused by less specialised pathogens like Cylindrocladium species attacking trees growing in excessively humid conditions in the wet tropics. Some important new-encounter diseases have been reported and the occurrence of guava rust on eucalypts in Brazil presents a threat to eucalypts around the world. Foliar diseases have prevented the planting of particular eucalypt species in some localities. The study of eucalypt leaf diseases is still in its infancy and, accordingly, is still largely concerned with establishing the identity and basic biology of the causal fungi. Much of this review is devoted to the taxonomy of putative causal fungi about which there is often confusion. For ease of identification, the pathogens are listed in tables with their main characteristics. For some of the more important diseases, preliminary studies have been undertaken on the biology and pathology of the fungi. The study of control measures is still rudimentary but there is ample evidence that selection of disease-resistant genotypes is possible among the great genetic diversity of the eucalypts.

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9.1 Introduction Foliar diseases (overwhelmingly caused by fungi) are common on eucalypts growing in native forests in Australia. On eucalypts in the field it is rare to find mature leaves undamaged by fungi or insects. Only rarely, however, have foliar diseases been of concern in forest management. Coevolution of eucalypts with their foliar parasites in native forests has apparently resulted in a balance between the trees and their parasites (Heather 1967c; Burdon and Chilvers 1974a), although the improved growth rate and form of eucalypts planted in many localities outside Australia indicates that native parasites exact a considerable toll on growth of eucalypts in native communities. Disturbance of the natural communities may result in pest and disease outbreaks. Epidemics of leaf diseases have occurred in native forests but the reasons for their occurrence are poorly understood. For example, fungal leaf spotting caused primarily by Aulographina eucalypti reached epidemic levels in Eucalyptus nitens forests on the Errinundra Plateau, Vic., in 1974 and resulted in defoliation of saplings and mature trees (Neumann and Marks 1976). Epidemics of Aulographina eucalypti were observed in regrowth of ash-type eucalypts at Taggerty and Toolangi, Vic. (Neumann et al. 1975) and in mountain ash (E. regnans) regrowth at Noojee, Vic. (Stefanatos 1993). An epidemic of leaf spotting caused by Aulographina eucalypti and Vermisporium (as Seimatosporium) falcatum possibly associated with drought stress and insect attack occurred in several thousand hectares of E. obliqua growing in valleys in north-west Tasmania during 1973 and many of these trees subsequently died (Felton 1981). Epidemics are more frequent in single-species eucalypt plantations than in mixed-species native forests. Mycosphaerella (M.) nubilosa and M. cryptica seriously damaged E. globulus growing in a small experimental plantation in eastern Victoria, greatly reducing stocking of the site (Park and Keane 1982b); later, M. cryptica severely damaged the adult foliage of the trees at this site (P.J. Keane, unpubl. data). The same fungi caused 90% defoliation of the juvenile foliage of some provenances of E. globulus in planting trials (Carnegie et al. 1994) and were destructive in commercial plantations of E. globulus and E. nitens in Tasmania (Dungey et al. 1997; D. de Little, pers. comm.; see Chapter 22). In New South Wales, leaf

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damage caused by Aulographina eucalypti, Readeriella mirabilis and a species of Mycosphaerella was prevalent on E. agglomerata (but not E. pilularis) in a three-year-old plantation and damage caused by Mycosphaerella was prevalent in another plantation of E. agglomerata (GerrettsonCornell and Dowden 1977). Outside Australia, destructive epidemics of diseases caused by local fungi (‘new-encounter’ pathogens) and coevolved pathogens introduced from Australia have been common in eucalypt plantations. In the tropics, these diseases are often caused by facultative pathogens of wide host range, such as species of Cylindrocladium. Reviews of leaf diseases of exotic eucalypts in the United States of America (USA) (Hedgecock 1926), New Zealand (Dick 1982, 1990), South Africa (Crous et al. 1989b), Brazil (Ferreira 1989), the Mediterranean region (Lanier 1986) and Spain (Ruperez and Munoz 1980) reflect concern about damage caused by these diseases. A species of Mycosphaerella reported from plantations of E. delegatensis in New Zealand (Weston 1957; Gilmour 1966) reached epidemic levels in over 1000 hectares of commercial plantations in the Central North Island (Cheah 1977). In South Africa, Mycosphaerella leaf blotch caused by M. juvenis prevented the commercial planting of E. globulus and several provenances of E. nitens (Crous et al. 1989a; Crous and Wingfield 1996). Species of Cylindrocladium cause destructive blights of young eucalypts growing in warm, humid conditions in Brazil (Ferreira 1989), India (Sharma et al. 1985), South Africa (Crous et al. 1991a) and Vietnam (Old and Yuan 1994). The native guava rust (Puccinia psidii) causes damage in eucalypt plantations in Brazil (Ferreira 1989). Many fungi have been described from eucalypt foliage (Sankaran et al. 1995a), beginning with the studies by Cooke (1892) of material sent to England from Australia in the nineteenth century, but the pathology of relatively few has been studied in detail. Heather (1961, 1965) pioneered the study of the pathology of eucalypt leaf diseases in Australia. With the rapid expansion of eucalypt planting in many regions of the world since the 1970s (see Chapter 1), including Australia during the 1990s, interest in the pathology of leaf diseases has increased greatly. Much of this interest has been focused outside Australia, particularly in New Zealand, South Africa, Brazil and India, where

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cultivation of eucalypts in plantations has been extensive and the effect of leaf diseases most obvious. The study of leaf diseases in native forests in Australia has been very much neglected and no doubt there are many leaf pathogens that remain to be described from these forests. Most of the more specialised fungi infecting eucalypt leaves are Loculoascomycetes, Pyrenomycetes or Coelomycetes. Only now is the diversity of leafinfecting fungi on eucalypts beginning to be adequately catalogued. As Swart (1988) discovered, a mycologist trying to identify leafinhabiting fungi on eucalypts faces two difficulties: 1

many fungi have never been described

2

many of the fungi that have appeared in print need more accurate description, illustration and reclassification.

Harry Swart did much to overcome these difficulties for species found in southern Australia and his clear descriptions and beautiful illustrations are an important starting point for the student of eucalypt leaf diseases (Simpson and Grgurinovic 1996). P.W. Crous and M.J. Wingfield, working in South Africa, have described a wide range of new species from eucalypt plantations outside Australia and have clarified many taxonomic problems of these fungi. A problem highlighted by several workers (e.g. Pascoe 1990) is the difficulty of discerning important taxonomic structures from herbarium specimens. Several taxa require fresh specimens for complete identification. A further complication is that similar leaf spots can be associated with several different fungi and sometimes more than one fungus can occur on a single lesion (Crous 1998). Barber (1998) reported infections by seven different fungi on a single leaf from the lower canopy of E. globulus in a plantation in Victoria. Yet another complexity is the association of insects and fungi observed in leaf spots on E. globulus (Barber 1998; Carnegie and Keane 1998). The nature of the relationship between the insects and fungi in this association is unknown. The extensive literature on the foliar diseases and pathogens of the eucalypts (genera Eucalyptus and Corymbia) is reviewed as a basis for diagnosis, further study and management of the diseases. Because the study of eucalypt leaf diseases is in its infancy, there is much confusion over the identity and nomenclature of causal organisms; accordingly,

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fairly complete taxonomic details have been presented. As many of these pathogens have been reported under several names, we have attempted to include all synonyms of the currently recognised names. Synonyms, anamorphs and authorities of species are presented at the beginning of the section devoted to that species. Diseases caused by Aulographina eucalypti and Mycosphaerella species are among the most common and extensively studied of the specialised leaf diseases and are treated first. The other diseases are grouped according to general symptoms, although this is not always helpful because several species cause rather similar necrotic speckles, spots, blotches or blights and some species cause different symptoms on different hosts. Several pathogens form characteristically angular necrotic lesions restricted by leaf veins. Many fungi infect leaves without causing immediate necrosis and are evident for much of their development only as stromata or discrete sporocarps embedded in the leaf tissue; these are grouped as biotrophic infections. Several fungi that ultimately cause leaf spotting and blighting are clearly biotrophic in the early stages of infection. The extension of eucalypt planting outside the normal environmental range of species has resulted often in diseases caused by a wide range of less specialised pathogens. Within the various symptom categories, diseases are presented by alphabetical order of the pathogen genus primarily associated with the disease. Several diseases affect young stems as well as leaves, leading to tip dieback of young shoots and planting stock in nurseries; these are covered more fully in Chapter 8. Some foliar pathogens affect buds, flowers, capsules and seed (see Chapter 7). Some foliar pathogens are also associated with cankering of twigs and are described in Chapter 10.

9.2 Target spot ( Aulographina eucalypti ) Target spot or corky spot is one of the most common and distinctive leaf diseases of eucalypts in southern Australia (Müller and von Arx 1962; Wall and Keane 1984; Swart 1988). It is caused by the loculoascomycete, Aulographina eucalypti (Cooke & Massee) Arx & E.Müll. (syn. Aulographum eucalypti Cooke & Massee; Lembosiopsis eucalyptina Petr. & Syd.; Müller and von Arx 1962; Lembosiopsis australiense Hansf.; Wall and Keane 1984; Lembosia eucalypti F.Stevens & M.Dixon;

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Swart 1988) [anamorph: Thyrinula eucalypti (Cooke & Massee) H.J.Swart; syn. Leptostromella eucalypti Cooke & Massee; Thyrinula eucalyptina Petr. & Syd.; Swart 1988]. The fungus has been reported from New Zealand (Dick 1982), South Africa (Petrak and Sydow 1924), Hawaii (C.S. Hodges, pers. comm.), Brazil (Ferreira 1989), the United Kingdom (UK) (Spooner 1981) and Vietnam (Old and Yuan 1994). In South Africa, it was associated with severe leaf spotting and defoliation of E. fastigata and E. fraxinoides (Crous and Wingfield 1991). The roughly circular, often raised and corky, necrotic spots (Plates 9.1 and 9.2) are distinctive in developing only part-way through the leaf lamina (Table 9.1), whether they occur on the upper or lower surface. Lesions may extend through the lamina on some hosts, although the sporocarps are formed on only one surface (Swart 1981b). During cooler months a purple margin develops around lesions (Plate 9.1). The disease is most obvious on older leaves and also occurs on petioles, small branches and fruits of certain species, especially E. globulus, E. nitens and E. regnans (Neumann et al. 1975). Initially black, pimple-like pycnidia and later elongate or branched, black thyriothecia with distinctive two-celled ascospores are formed on the lesion surface (Fig. 9.1). The pycnidia are probably a spermatial state—they are always formed before thyriothecia and the very fine, needle-like pycnidiospores have not been observed to germinate (Wall and Keane 1984; Swart 1988). During epidemics in young regrowth, small spots may cover the entire lamina (Plate 9.3). In mixed-species native forests, the occurrence of target spot is characteristic of Eucalyptus species in the subgenus Monocalyptus (Heather 1971; Burdon and Chilvers 1974a; Wall and Keane 1984). However, a severe outbreak of the disease occurred in natural stands of the Symphyomyrtus species, E. denticulata, in eastern Victoria (Neumann and Marks 1976), and in plantations and gardens the disease occurs on eucalypt species in subgenera other than Monocalyptus. The fungus has also been identified on foliage and petioles of Angophora costata (Wall and Keane 1984) and on the leaves of Agonis flexuosa (Willd.) Sweet in Queensland (R.F. Park, unpubl. data). It is common on leaves, petioles and stems in the lower canopy of the Symphyomyrtus species, E. globulus, in plantations

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in Victoria but causes little damage (Carnegie 1991; Barber 1998). In a species and provenance trial in northern New South Wales, the disease was common on species of Monocalyptus and Simpson et al. (1997) concluded that it may be important in the management of plantations of these species on certain sites. The disease reached epidemic proportions in dense populations of regenerating seedlings of E. regnans after logging in native forests in Victoria, causing severe infection on relatively young leaves (Stefanatos 1993). Severe, speckled infection was also common on young regrowth of E. obliqua (Plate 9.3). The speckling was caused by a high density of young infections which did not develop into typical target spots before the heavily infected leaves were shed. There was no evidence of differences in pathogenicity between isolates of the fungus from different eucalypt species (Wall and Keane 1984), although this requires further study. However, there was evidence of variability in resistance to the disease among provenances of E. globulus in field trials (Carnegie 1991). Ascospores shed onto leaves form melanised germ tubes and appressoria from which the fungus penetrates directly through the cuticle, giving rise to subcuticular infection hyphae (Wall and Keane 1984). The fungus also forms a colonising network of melanised surface hyphae. Young, expanding leaves are more susceptible than older, hardened leaves. Following infection of leaves, lesions develop very slowly over several months. This explains why larger lesions are most evident on older foliage in the lower canopy. Development of the distinctive lesions is restricted by a saucer-shaped zone of cork cambium which prevents the infection extending completely through the leaf lamina. However, the cork cambium does not completely restrict growth of the infection hyphae, which extend just beyond it into healthy tissue (Wall and Keane 1984). Severe leaf infection and damage to petioles and small branches leads to premature defoliation (Neumann and Marks 1976). Infection occurs mainly during spring and early summer when susceptible young leaves are present, inoculum is released by wetting of lesions and when temperatures fall within the optimum for sporulation of 15°C to 20°C (Wall and Keane 1984). Ascospore release is most prolific on lesions moistened and kept in the light and it is therefore likely to be more strongly

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Figure 9.1

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Aulographina eucalypti: a) cross section of thyriothecium, b) cross section of pycnidium, c) ascus, d) pycnidiospore and e) ascospores. Bars represent 10 µm. Drawings courtesy of P.A. Barber.

associated with daytime rain than with rain or dew at night (Wall and Keane 1984). As the lesions retain their identity in leaf litter and the fungus continues to sporulate prolifically for several months after leaf fall, leaf litter may be an inoculum source. Lesions on petioles, fruits and smooth bark of some eucalypt species survive for a considerable time and are likely to be important sources of inoculum in the canopy.

Large spots are common on old, lightly infected, attached leaves, which also provide an important inoculum source and allow the fungus to carry over from one year to the next. The disease was more common on trees in low lying, water-gaining sites in association with Phytophthora (Ph.) cinnamomi Rands than on nearby healthy trees (GerrettsonCornell and Dowden 1977; Weste 1980). It is

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Foliar diseases of eucalypts caused by Loculoascomycetes, giving anamorphs, symptoms and distinctive features of the pathogens (see also Table 9.2 for some Mycosphaerella species of minor importance

Pathogen teleomorph (anamorph)

Disease symptoms

Distinctive features of the pathogen

Aulographina eucalypti (Thyrinula eucalypti)

Circular necrotic spots, 1–15 mm diameter, formed only part way through the leaf lamina; with a concentric pattern (‘target spot’); common also on petioles

Black, superficial, pimple-like pycnidia formed first, followed by superficial, black, elongate or branched thyriothecia with longitudinal slit; ascospores 2-celled, guttulate, 9–16 × 3–6 µm, one cell slightly broader and shorter than the other; pycnidiospores needle-like

Botryosphaeria ribis (Fusicoccum sp.)

Grey-brown leaf spot, tip blight and twig canker

Black pseudothecia and pycnidia rupturing epidermis; ascospores hyaline, 1-celled, ovoid, 17–23 × 7–10 µm; conidia 1-celled, hyaline, fusoid, 17–25 × 5–7 µm; spermatia 2–3 × 1 µm

Elsinoë eucalypti (Sphaceloma sp.)

Irregular, circular, raised, sharply defined dark spot with paler centre, with subepidermal stroma covering entire spot (‘scab’)

Conidia hyaline, single-celled, smooth, ovate 4–6 × 3–4 µm; asci formed singly in stroma and piling up in layers on the surface; ascospores hyaline, slipper-shaped with rounded ends, 3 transverse and 1 longitudinal septa, 20–26 × 7–8 µm

Guignardia eucalyptorum (Phyllosticta eucalyptorum)

Small spots (3 mm diameter) to large blotches with red-purple, slightly raised margin

Pseudothecia intermixed with pycnidia; ascospores hyaline, unicellular, fusiform to ellipsoidal, 14–18 × 4–6 µm, wider in middle, with gelatinous plugs; conidia unicellular, ellipsoidal (7–20 × 6–6.5 µm), guttulate, with persistent mucous coats about 1 µm thick, and apical appendages 3–10 µm long

Microthyrium eucalypticola

Circular slightly chlorotic zones, up to 30 mm diameter, visible on leaf when held up to light; circular zones of thyriothecia develop on fallen leaves

Thyriothecia superficial, flat conical with a circular ostiole; paraphyses present but disintegrate as asci formed; ascospores 2-celled, hyaline, fusiform, straight to curved, slightly constricted at septum, tapering to acute ends, surrounded by a gelatinous matrix, 16.5–20 × 4–5 µm (23–25 × 5–6 µm with matrix)

Mycosphaerella (general characteristics)

Amphigenous leaf spots, blotches or distorting blights

Pseudothecia globose, black, subepidermal, substomatal, becoming erumpent in some species; asci bitunicate, aparaphysate; ascospores 2-celled, hyaline, small, guttulate, septum usually median and constricted in some species; germ tubes often emerge from distal ends of ascospore cells either parallel or perpendicular to long axis of spore and spore and germ tubes may become darker and distorted; spermogonia present in some species, similar to pseudothecia; anamorphs various

Mycosphaerella africana

Tiny leaf spots 1–2 mm diameter often with diffuse red-purple margins

Pseudothecia amphigenous, subepidermal; ascospores 8–10 × 2–3 µm, fusoid to ellipsoidal with obtusely rounded ends, constricted at median septum; germ tubes initially parallel, darkening and distorting

Mycosphaerella colombiensis (Pseudocercospora colombiensis)

Irregular to subcircular leaf spots 1–15 mm diameter with raised dark brown borders

Pseudothecia mainly hypophyllous, subepidermal becoming erumpent; ascospores 12–14 × 3–4 µm, not constricted, widest in apical cell, tapering more towards base, germ tubes parallel, not darkening nor distorting; spermogonia present; see Table 9.3 for anamorph

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Pathogen teleomorph (anamorph) Mycosphaerella cryptica (Colletogloeopsis nubilosum)

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Distinctive features of the pathogen

Small, regular spots on juvenile foliage; large irregular spots or blotches causing buckling of leaf lamina (‘crinkle leaf’) on mature foliage of a wide range of eucalypts; initially purplish and water-soaked in appearance, becoming redbrown, then grey as pseudothecia form, with callused border; pseudothecia scattered over lesion except around the border

Pseudothecia immersed under stomata until mature, amphigenous; ascospores with obtusely rounded ends, constricted at median septum, 9–17 × 2–5 µm; germ tubes emerge perpendicular to long axis of ascospores, darkening but not distorting; spermogonia present; spermatia 4–5 × 1–2 µm; acervuli abundant, brown to black rupturing the cuticle to form a slit up to 10 µm long; conidia 10–15 × 4–6 µm, aseptate, subhyaline, smooth, cylindrical, straight or curved, with a rounded apex and truncate base with a distinct frill

Mycosphaerella crystallina Small, subcircular leaf spots (Pseudocercospora crystallina) 2–10 mm diameter coalescing to form larger blotches

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Pseudothecia hypophyllous, becoming erumpent to superficial; ascospores 12–14 × 3–4 µm, not constricted, widest in apical cell, tapering more towards base; germ tubes parallel, not darkening nor grossly distorting; spermogonia amphigenous; spermatia 4–8 × 2 µm; see Table 9.3 for anamorph. Forms red crystals in agar

Mycosphaerella delegatensis (Phaeophleospora delegatensis)

Circular leaf spots 5–10 mm diameter initially with diffuse border and later with sharp, darker border; often surrounding tissue remains green on senescing leaf

Pseudothecia mainly hypophyllous, immersed; ascospores 16–25 × 3–5 µm, not constricted, tapering more towards base; spermagonia numerous; spermatia 5 × 1–2 µm; amphigenous pycnidia formed before pseudothecia, immersed, globose; conidia cylindrical, straight or curved, hyaline, smooth, thin-walled, unevenly 2-celled, 20–50 × 3–5 µm, with a basal hilum

Mycosphaerella ellipsoidea (Uwebraunia ellipsoidea)

Small (2–10 mm) subcircular leaf spots

Pseudothecia amphigenous, inconspicuous; ascospores 8–11 × 2–3 µm, not constricted, widest just above septum and tapering to both ends but more towards base, germ tubes parallel, not darkening nor distorting; spermogonia present; spermatia 2–4 × 1–1.5 µm; brown conidiogenous cells formed singly on external mycelium, giving rise to pale olivaceous, smooth, obclavate, 2-celled conidia, 17–21 × 4–5 µm, widest in lower cell

Mycosphaerella endophytica (Pseudocercosporella endophytica)

Irregular leaf spots 5–20 mm diameter

Pseudothecia amphigenous, subepidermal, becoming erumpent; ascospores 9–10 × 2–3 µm, not constricted, tapering to both ends; germ tubes parallel, not darkening nor distorting; conidia hyaline, smooth, 0–8 septate, 25–45 × 2 µm, with truncate base, formed in slimy masses on sporodochia up to 400 µm wide

Mycosphaerella flexuosa

Leaf spots 1–8 mm diameter on juvenile foliage of E. globulus, with M. suberosa on older foliage

Pseudothecia amphigenous, subepidermal, becoming erumpent; ascospores 10–12 × 2–3 µm, not constricted, widest in middle of apical cell, tapering to both ends; germ tubes initially parallel, not darkening nor distorting

Mycosphaerella gracilis (Pseudocercospora gracilis)

Small (2–6 mm diameter), irregular leaf spots with raised red to brown margin

Pseudothecia amphigenous, immersed, becoming erumpent; ascospores 15–18 × 2–3 µm, not constricted, slightly curved, widest at septum and tapering to both ends; germ tubes parallel, not darkening nor distorting; see Table 9.3 for anamorph

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Pathogen teleomorph (anamorph)

Disease symptoms

Distinctive features of the pathogen

Mycosphaerella grandis

Extensive yellow-brown blighting lesions on leaf margins extending from the tip. On E. grandis

Pseudothecia amphigenous, more prominent on the abaxial surface, immersed, non-erumpent; ascospores 10.5–14.5 × 3–4.5 µm, hyaline, prominently constricted, widest at midpoint of apical cell, initially germinating parallel from one cell, later darkening and distorting

Mycosphaerella gregaria

An occasional secondary invader of parts of more extensive lesions caused by M. grandis, or a primary pathogen

Pseudothecia in dense clusters in restricted areas, amphigenous, erumpent to superficial; ascospores 12.5–15 × 2.5–4 µm, prominently constricted, widest in middle of apical cell; germ tubes parallel, not darkening nor distorting

Mycosphaerella heimii (Pseudocercospora heimii)

Elongate, irregular leaf spots (5–15 mm)

Pseudothecia amphigenous, immersed; ascospores 8–12 × 2–3 µm, not constricted, widest in middle of upper cell; germ tubes initially parallel, not darkening nor distorting; see Table 9.3 for anamorph

Mycosphaerella heimioides Pseudothecia formed in (Pseudocercospora heimioides) otherwise healthy leaves

Pseudothecia amphigenous, subepidermal; ascospores 8–11 × 2–3 µm, not constricted, widest in middle of apical cell, tapering to both ends; germ tubes at angle to long axis of spore, not darkening nor distorting; see Table 9.3 for anamorph

Mycosphaerella irregulariramosa (Pseudocercospora irregulariramosa)

Small subcircular grey leaf spots 3–15 mm in diameter

Pseudothecia amphigenous, subepidermal, becoming erumpent; ascospores 7–10 × 1.5–2.5 µm, not constricted, widest in middle of apical cell, tapering to both ends; germ tubes initially parallel, not darkening nor distorting, then forming lateral branches; spermatia 2–3 × 1 µm; see Table 9.3 for anamorph

Mycosphaerella juvenis (Uwebraunia juvenis)

Lesions irregular, 2–12 mm diameter, becoming confluent to form blotches on juvenile leaves of E. globulus and E. nitens in Africa.

Pseudothecia hypophyllous, subepidermal, becoming slightly erumpent; ascospores 10–15 × 3–4 µm, not constricted, obtuse ends, tapering more toward base; germ tubes parallel, not darkening, later distorting; conidia terminal, solitary, pale olivaceous, smooth, obclavate with an obtuse apex and truncate base, 2-celled with constriction at septum, 25–40 × 4–6 µm

Mycosphaerella lateralis (Uwebraunia lateralis)

Small (3–12 mm diameter) round to irregular leaf spots with raised margins

Pseudothecia amphigenous, subepidermal, becoming erumpent; ascospores 7–16 × 2–3 µm, not constricted, widest in middle of apical cell, tapering to both ends; germ tubes parallel, not darkening nor distorting, later forming lateral branches; conidiophores formed singly on hyphae; conidia olivaceous, smooth, medianly 1-septate, widest in middle of lower cell, 15–35 × 2–4.5 µm

Mycosphaerella longibasalis

Subcircular leaf spots 2–10 mm diameter with a raised brown border

Pseudothecia mainly epiphyllous, subepidermal, becoming erumpent; ascospores 22–30 × 3.5–5 µm, not constricted, widest above middle of apical cell, tapering to both ends, basal cell longer

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Disease symptoms

Distinctive features of the pathogen

Mycosphaerella marksii

Circular to irregular lesions 3–20 mm diameter with redbrown margins; sometimes spots towards leaf margin, coalescing

Pseudothecia mainly epiphyllous, in dense clusters, immersed but becoming erumpent; ascospores 12–22 × 2–5 µm, not constricted, apical cell asymmetrical ; germ tubes parallel, not darkening nor distorting; spermatia 2.5–4 × 1–1.5 µm

Mycosphaerella mexicana

Round to subcircular leaf spots, 1–8 mm diameter with dark brown to black margin

Pseudothecia amphigenous, subepidermal, becoming papillate; ascospores 15–24 × 5–7 µm, olivaceous, smooth to verruculose, not or slightly constricted, widest in middle of apical cell; germ tubes parallel, becoming darker

Mycosphaerella molleriana (Colletogloeopsis molleriana)

Subcircular to irregular leaf spots, 2–10 mm in diameter, becoming confluent

Pseudothecia mainly hypophyllous, subepidermal, becoming erumpent; ascospores 11–17 × 2.5–4.5 µm, straight to curved, not or slightly constricted, widest in middle of apical cell; germ tubes parallel, not darkening nor distorting; acervuli mainly hypophyllous, dark brown to black, subcuticular, erumpent, up to 150 µm wide; conidia aseptate, brown, verruculose, straight to slightly curved, with an obtuse apex and truncate base and marginal frill 7–13 × 2.5–4 µm

Mycosphaerella nubilosa

Circular necrotic lesions or large irregular blotches or blights only on juvenile foliage; pseudothecia scattered across whole lesion

Pseudothecia mainly hypophyllous, immersed, becoming erumpent; ascospores 11–16 × 3–4.5 µm, not constricted, widest near apex of apical cell, tapering more towards base; germ tubes parallel, not darkening

Mycosphaerella parkii (Stenella parkii)

Small to large, light brown, rounded or slightly irregular lesions with red to brown raised margins

Pseudothecia amphigenous, immersed becoming erumpent; ascospores 8.5–15 × 2–3.5 µm, not constricted at median septum, widest in middle of upper cell, tapering more to upper end; germ tubes parallel and perpendicular, not darkening, distorting slightly; conidiophores brown, verruculose, repeatedly geniculate; conidia olivaceous brown, verruculose, 1–8 septate, 25–200 × 2–2.5 µm

Mycosphaerella parva

A secondary invader in lesions of M. nubilosa and M. cryptica

Pseudothecia hypophyllous, immersed, interspersed with those of M. nubilosa or M. cryptica on older lesions; ascospores 7–10 × 1–3 µm, prominently constricted, widest at mid-point of apical cell, germ tubes initially parallel, darkening and distorting slightly

Mycosphaerella suberosa

Corky leaf spot, 5–15 mm diameter with irregular redpurple margin

Pseudothecia mainly hypophyllous, in concentric rings, semi-erumpent to superficial with a distinctive papillate ostiole; ascospores 10–19 × 3–6 µm, constricted, widest in middle of apical cell; 4 germ tubes, darkening and distorting

Mycosphaerella suttoniae (Phaeophleospora epicoccoides)

Angular to irregular spots or smudges, epiphyllous or hypophyllous, up to 3 mm diameter, or brown spots with red-purple margin, 7–25 mm diameter

Pseudothecia hypophyllous, subepidermal, becoming papillate; ascospores 10–13 × 2.5–3.5 µm, not constricted, widest near apex, tapering towards base; germ tubes parallel or perpendicular, darkening and slightly distorting; spermatia 5–7 × 1 µm; pycnidia amphigenous, substomatal— see anamorph in Table 9.5

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Foliar diseases of eucalypts caused by Loculoascomycetes, giving anamorphs, symptoms and distinctive features of the pathogens (see also Table 9.2 for some Mycosphaerella species of minor importance (continued)

Pathogen teleomorph (anamorph) Mycosphaerella swartii (Sonderhenia eucalyptorum)

Disease symptoms

Distinctive features of the pathogen

Leaf speckle (up to 3 mm diameter) with purple margin when young, becoming dark red to brown and raised

Pseudothecia on one surface, immersed; ascospores 20–27 × 4–6 µm, straight or slightly curved, slightly constricted; germ tubes parallel, not darkening nor distorting; pycnidia black, subepidermal, intermingled with pseudothecia; conidia cylindrical, 3-distoseptate, 25–49 × 5–10 µm—see anamorph in Table 9.5

Mycosphaerella tasmaniensis Subcircular leaf spots 2–30 mm (Mycovellosiella tasmaniensis) in diameter, coalescing to form large blotches with raised brown border and diffuse redpurple margin.

Pseudothecia hypophyllous, subepidermal, becoming erumpent; ascospores 10–13 × 2.5–4 µm, not constricted, widest in middle of apical cell, tapering prominently towards base; germ tubes initially parallel, not darkening nor distorting; conidiophores single on superficial mycelium, brown; conidiogenous cells proliferating sympodially; conidia catenulate, olivaceous, smooth, variable in size and shape, occasionally 1-septate, with rounded apex and narrow truncate base, 4–20 × 2–2.5 µm (Cladosporium-like)

Mycosphaerella vespa

Circular to irregular, swollen lesions, hollow, with a hole in one surface; often wasp pupae and mites inside

Pseudothecia amphigenous, substomatal, immersed, scattered; ascospores 9.5–16.5 × 2.5–4 µm, slightly constricted, rounded on ends, widest in middle of apical cell; germ tubes parallel, not darkening nor distorting, occasional third germ tube emerging at an angle from near the septum

Mycosphaerella walkeri (Sonderhenia eucalypticola)

Leaf speckle (up to 3 mm diameter) similar to M. swartii

Teleomorph identical to M. swartii and anamorph similar to Sonderhenia eucalyptorum except conidia ellipsoidal (19–31 × 6–12 µm) and dark brown—see anamorph in Table 9.5

Pachysacca eucalypti (Phomachora eucalypti Syd.)

Circular warty stromata up to 5 mm in diameter

Stroma formed between epidermis and mesophyll; asci develop in locules in stroma; ascospores hyaline, cylindrical, 3-celled, 90–120 × 7 µm, and spermatia 3 × 1 µm formed in smaller locules in stroma

Pachysacca pusilla

Tiny circular stromata up to 1.5 mm in diameter

Stroma formed between epidermis and mesophyll; asci develop in locules in stroma; ascospores hyaline, cylindrical, 4-celled, 38–46 × 4–5 µm

Pachysacca samuelii

Dendritic or large circular warty stromata

Stroma formed between epidermis and mesophyll; asci develop in locules in stroma; ascospores hyaline, elongate, cylindrical, usually 4-celled, 60–65 × 6–7 µm; spermatia 2 × 0.5 µm, formed in locules in stroma

Phaeothyriolum microthyrioides

Large rings of thyriothecia on the leaf, with necrosis only in later stages, sometimes associated with a purple ring, especially in winter

Hyphae subcuticular and intracuticular and superficial; thyriothecia superficial, flat conical, mostly circular, with irregular ostiole; aparaphysate; ascospores 2-celled, slightly constricted, ovoid, with obtusely rounded ends or one end more acute, 15–29 × 5–10 µm but size varies with host, hyaline but darkening after discharge, with a gelatinous matrix

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possible that root rot caused by Ph. cinnamomi may predispose trees to attack by Aulographina eucalypti or that unthrifty, slow-growing trees retain a greater proportion of older, infected leaves.

Mycosphaerella species on eucalypts there (Crous et al. 1993e, 1993f), although one of these (M. suberosa) has been reported also from Western Australia (Carnegie et al. 1997).

Although it causes a necrotic spot, Aulographina eucalypti is a highly adapted leaf parasite with a biotrophic mode of nutrition, as shown by the extension of its subcuticular infection hyphae beyond the necrotic region where they appear to be a sink for photosynthate in infected leaves (Wall and Keane 1984).

There has been confusion over the identification of Mycosphaerella species on eucalypts. The genus is characterised by tiny, black, globoid pseudothecia which are formed individually below stomata in necrotic tissue (Plate 9.8) and contain aparaphysate, bitunicate asci with tiny two-celled, hyaline ascospores (Fig. 9.2). The characters used to separate species, such as ascospore shape and dimensions of pseudothecia, asci and ascospores, vary within, and overlap considerably between, species (Carnegie and Keane 1994; Crous and Wingfield 1996; Crous 1998). Ascospore measurements vary depending on the stain used and the state of the specimen examined (e.g. whether the spores are from a fresh specimen or an older herbarium collection, whether spores are measured dry or after shedding onto the surface of agar and whether spores have been shed onto the lesion surface following complete maturation or have been squashed from asci in an immature state) (Carnegie and Keane 1994). Species are most reliably distinguished when all the characters listed above are used, along with symptoms, host range, pattern of ascospore germination (Fig. 9.3) and identity of the anamorph, if present (Park and Keane 1982b; Crous 1998). The use of ascospore germination creates problems for the comparison of herbarium specimens with freshly collected material. Also, the mode of ascospore germination may vary with the condition of the ascospores and the medium used for germination. For example, germination of freshly shed spores of M. parva (Park and Keane 1982a) differed from that of older, melanised spores that had accumulated on the surface of herbarium specimens (Crous 1998) and the pattern of germination on water agar may be different from that on malt extract agar (Barber 1998). Theodore (1991) was able to differentiate several species using isozymes and there has been some preliminary success with DNA-based methods (A.J. Carnegie, pers. comm.). Crous and Wingfield (1996) reviewed the Mycosphaerella species associated with leaf diseases of eucalypts in South Africa and included a key to all Mycosphaerella species found on eucalypts. More recently, Crous (1998) published a monograph of Mycosphaerella on eucalypts, including many

9.3 Leaf spot, leaf blotch and crinkle leaf blight ( Mycosphaerella species) Nearly 30 species of Mycosphaerella have been described from spots, blotches and blights on eucalypt leaves and the genus, with its anamorphs, is one of the most common causes of foliar diseases of eucalypts (Tables 9.1 and 9.2) (Plates 9.4 to 9.11) (Crous et al. 1995a; Crous and Wingfield 1996; Crous 1998). Many Hyphomycetes and Coelomycetes (Table 9.3 and see Table 9.5) reported from eucalypt leaves are from genera that are common anamorphs of Mycosphaerella, although this link has not been established on eucalypts often (Crous 1998). Diseases caused by Mycosphaerella species are common although rarely severe on regrowth in native forests in Australia, can be destructive in nurseries (see Chapter 8) and are among the most important diseases of eucalypt plantations in Australia (Park and Keane 1982b; Carnegie et al. 1998), New Zealand (Dick 1982) and South Africa (Crous and Wingfield 1991). Of the species reported from outside Australia, some appear to have spread from Australia—these include M. cryptica and M. nubilosa in New Zealand (Dick 1982; Dick and Gadgil 1983), M. cryptica in Chile (Wingfield et al. 1995), M. marksii in Indonesia, Vietnam, South Africa, Portugal and South America, M. walkeri in South America and Portugal and M. suttoniae (Phaeophleospora epicoccoides) in Indonesia and Brazil (Crous 1998). However, many have not been reported from Australia and are likely to have transferred to introduced eucalypts from native myrtaceous hosts (Crous and Wingfield 1996; Crous 1998). Mycosphaerella species certainly occur on myrtaceous hosts other than eucalypts in Brazil (Ferreira 1989; Corlett 1991) and preliminary surveys have shown the occurrence of at least two

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Mycosphaerella species associated with eucalypts as the cause of minor leaf spots, as endophytes or as secondary invaders (most species not mentioned in the text)

Teleomorph (anamorph)

Occurrence

Comments

References

M. africana Crous & M.J.Wingf.

Several eucalypt spp. in southern Africa, Portugal and Colombia

Similar to M. cryptica and M. grandis

Crous and Wingfield (1996); Crous (1998)

M. colombiensis Crous & M.J.Wingf. (Pseudocercospora colombiensis Crous & M.J.Wingf.)

On E. urophylla in Colombia

M. crystallina Crous & M.J.Wingf. (Pseudocercospora crystallina Crous & M.J.Wingf.)

On E. globulus ssp. bicostata and E. grandis × E. camaldulensis hybrid in South Africa

M. ellipsoidea Crous & M.J.Wingf. (Uwebraunia ellipsoidea Crous & M.J.Wingf.)

On E. cladocalyx in South Africa

M. endophytica Crous & H.Sm.ter (Pseudocercosporella endophytica Crous & H.Sm.ter)

On E. grandis and E. nitens in South Africa

M. flexuosa Crous & M.J.Wingf.

On juvenile foliage of E. globulus in Colombia.

Crous (1998)

Similar to M. molleriana and M. juvenis, but differs in its erumpent pseudothecia, anamorph and formation of red crystals in agar

Crous and Wingfield (1996); Crous (1998)

Crous and Wingfield (1997b) The anamorph is formed in culture and has been isolated as an endophyte from healthy leaf tissue

Crous (1998)

Crous (1998)

M. gracilis Crous & Alfenas On E. urophylla in North (Pseudocercospora gracilis Crous Sumatra, Indonesia & Alfenas)

Crous and Alfenas (1995); Crous (1998)

M. heimioides Crous & M.J.Wingf. (Pseudocercospora heimioides Crous & M.J.Wingf.)

On Eucalyptus sp. in Indonesia

M. irregulariramosa Crous & M.J.Wingf. (Pseudocercospora irregulariramosa Crous & M.J.Wingf.)

On E. saligna in South Africa

Crous and Wingfield (1997b); Crous (1998)

M. lateralis Crous & M.J.Wingf. (Uwebraunia lateralis Crous & M.J.Wingf.)

On E. grandis × E. saligna hybrid, E. saligna, E. nitens and E. globulus in South Africa

Crous and Wingfield (1996); Crous (1998)

M. longibasalis Crous & M.J.Wingf.

On E. grandis in Colombia

Crous (1998)

M. marksii Carnegie & Keane

On several species in southeast and south-west Australia, South Africa, Uruguay, Indonesia and Vietnam

M. mexicana Crous

On Eucalyptus sp. in Mexico

M. parva R.F.Park & Keane

In lesions caused by M. nubilosa and M. cryptica

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Pseudothecia formed on otherwise healthy leaf tissue

Distinguished by the asymmetry of the apical cell, which is wider than the basal cell and has a ‘bump’ on one side

Crous and Wingfield (1997b); Crous (1998)

Carnegie and Keane (1994); Carnegie et al. (1997); Crous (1998); Old and Yuan (1994) Crous (1998)

Likely to be a secondary invader of lesions caused by other species

Park and Keane (1982a)

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Teleomorph (anamorph)

Occurrence

Comments

References

M. swartii R.F.Park & Keane (Sonderhenia eucalyptorum (Hansf.) H.J.Swart & J.Walker

On a wide range of species in Australia and New Zealand

Can be distinguished from M. walkeri only by anamorph

Park and Keane (1984)

M. tasmaniensis Crous & M.J.Wingf. (Mycovellosiella tasmaniensis Crous & M.J.Wingf.)

Small to large spots, coalescing to farm large blotches on E. nitens in Tasmania

M. walkeri R.F.Park & Keane (Sonderhenia eucalypticola (A.R.Davis) H.J.Swart & J.Walker

On a wide range of species in Australia and New Zealand

9

Crous (1998)

Can be distinguished from M. swartii only by anamorph

Park and Keane (1984)

conidial genera that are possible anamorphs of Mycosphaerella.

and Mycosphaerella eucalypti (Wakef.) Hansf. (syn. Hypospila eucalypti Wakef.) is uncertain.

Mycosphaerella nubilosa and M. cryptica have been particularly damaging in plantations in Australia (Park and Keane 1982a, 1982b, 1984; Carnegie et al. 1994), while M. cryptica has been destructive in plantations in New Zealand (Ganapathi and Corbin 1979) and M. juvenis has caused damage in plantations in South Africa (Crous and Wingfield 1996). These fungi cause diseases known collectively as ‘Mycosphaerella leaf blotch’ or ‘Mycosphaerella leaf blight’. More than one Mycosphaerella species may be associated with these diseases (e.g. M. nubilosa and M. cryptica on juvenile leaves of E. globulus). The typical symptoms are spots, blotches or buckled blights on leaves, depending on the pathogen species and the stage of development of the leaf at the time of infection (Park and Keane 1982b). Severe infection can cause premature leaf abscission and blighting of the whole shoot tip, resulting in loss of the leader. Many other Mycosphaerella species described from eucalypts cause small leaf spots of minor importance (Table 9.2). Mycosphaerella parva (Park and Keane 1982a) (Fig. 9.3) is a saprophyte, invading lesions caused by other Mycosphaerella species (Tables 9.1 and 9.2). Mycosphaerella gregaria Carnegie & Keane was initially considered a saprophyte, being commonly associated with lesions of M. grandis on E. grandis (Carnegie and Keane 1994, 1997), but it has been found since causing lesions by itself on C. maculata, E. botryoides and E. saligna and is likely to be a primary pathogen (A.J. Carnegie, pers. comm.) (Table 9.1). The taxonomy and pathogenicity of several species including Mycosphaerella didymelloides Petr. (Corlett 1991), Mycosphaerella martinae Hansf. (Hansford 1956)

Because of the damage to plantations caused by Mycosphaerella leaf blotch, there have been several attempts to assess the resistance of species and provenances of eucalypts to the disease, both in Australia (Carnegie et al. 1994, 1998; Dungey et al. 1997), South Africa (Purnell and Lundquist 1986) and New Zealand (Wilcox 1982a, 1982b) (see Chapters 18 and 22). Lundquist and Purnell (1987) developed disease assessment keys for the severity of the disease caused by M. juvenis on eucalypts in South Africa and Carnegie et al. (1994) adapted these for use with the disease caused by M. nubilosa and M. cryptica in southern Australia. In species and provenance trials in eastern Victoria, disease increased rapidly from winter to spring, with incidence in most provenances reaching 100% by the beginning of summer (Carnegie et al. 1994). Eucalyptus globulus and E. nitens, the most important plantation species in southern Australia, were more damaged by the disease than other species. Provenances of E. globulus ssp. globulus and E. globulus ssp. bicostata were the most severely affected, while provenances of E. globulus ssp. maidenii and E. globulus ssp. pseudoglobulus were only slightly affected. When grown in eastern Victoria, where conditions are conducive to disease, provenances from the drier and cooler regions, where the disease may have been less active, were more susceptible than provenances from eastern Victoria, where there has probably been selection for resistance. There is evidence of variation in resistance to Mycosphaerella leaf diseases between eucalypt species (Wilcox 1982a, 1982b; Carnegie et al. 1998), provenances (Wilcox 1982a, 1982b; Lundquist and Purnell 1987; Carnegie et al. 1994, 1998; Dungey et

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The occurrence and distinguishing features of Pseudocercospora species causing leaf spots on eucalypts, including anamorphs of some Mycosphaerella species

Anamorph (teleomorph)

Occurrence

Distinguishing features

References

Pseudocercospora sp.

Tiny (1–4 mm diameter) subcircular to angular leaf spots on E. nitens in Tasmania

Caespituli amphigenous, mostly hypogenous; conidiophores olivaceous, 3–10 per fascicle, emerging through stoma from weakly developed stroma, 1–4 septate; conidia olivaceous to light brown, smooth, thick-walled, cylindrical, tapering from truncate base to obtuse apex, 3–8-septate, 60–130 × 3–5 µm

Yuan (1999)

Pseudocercospora basiramifera Crous

Subcircular or angular leaf spots on E. camaldulensis and E. pellita in Thailand

Conidiophores arising from substomatal stroma; conidia 35–85 × 2–3 µm, smooth, 3–10-septate, with small basal, lateral branches which detach as secondary conidia

Crous (1998)

Pseudocercospora basitruncata Crous

Subcircular to angular leaf spots on E. grandis and Eucalyptus sp. in Colombia

Extremely variable. Conidiophores arising singly from superficial mycelium or from stromata; conidia 25–90 × 2.5–3.5 µm, finely verruculose, 1–11-septate, thickwalled, widest in the basal cell, with truncate base

Crous (1998)

Pseudocercospora cubae Crous

Irregular leaf spots on Eucalyptus sp. in Cuba

Conidiophores arising from suprastomatal stroma; conidia 20–50 × 2–3 µm, smooth to finely verruculose, 0–3-septate, thickwalled, distinguished by the distinct apical taper

Crous (1998)

Conidia light brown, smooth to finely verruculose, cylindrical, 1–5-septate, 25–60 × 2.5–3.5 µm

Crous (1998)

Crous and Wingfield (1996); Crous (1998)

Pseudocercospora Subcircular to irregular leaf colombiensis Crous & spots on E. urophylla in M.J.Wingf. (Mycosphaerella Colombia colombiensis) Pseudocercospora crystallina Crous & M.J.Wingf. (Mycosphaerella crystallina)

Leaf spots or blotches on E. globulus ssp. bicostata and E. grandis × E. camaldulensis hybrid in South Africa

Conidia 50–200 × 2–3 µm, formed on superficial hyphae, smooth, multiseptate, olivaceous, cylindrical

Pseudocercospora deglupta Crous

Subcircular leaf spots on E. deglupta in Malaysia and Papua New Guinea

Caespituli hypophyllous; Crous (1998) conidiophores fasciculate on suprastomatal stroma; conidia 35–80 × 3–4.5 µm, verruculose, thickwalled, 0–8-septate, tapering to truncate base

Pseudocercospora denticulata Crous

Irregular specks to angular leaf spots confined by veins on Eucalyptus sp. in Dominican Republic

Conidiophores arising singly from superficial mycelium or formed in dense fascicles on a suprastomatal stroma; conidiogenous cells denticulate; conidia 25–70 × 2–3 µm, finely verruculose; spermogonia present on lesions

Crous (1998)

Pseudocercospora epispermogoniana Crous & M.J.Wingf.

On leaves of E. grandis × E. saligna hybrid in South Africa

Conidiogenous cells formed on spermogonia; conidia 28–65 × 2–3 µm, smooth, 1–7-septate

Crous and Wingfield (1996); Crous (1998)

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Anamorph (teleomorph)

Occurrence

Distinguishing features

References

Pseudocercospora eucalyptorum Crous, M.J.Wingf., Marasas & B.Sutton

Angular, vein-limited leaf spots on E. nitens in South Africa

Conidiomata amphigenous, conidiophores medium to dark brown, smooth and aggregated into fascicles which emerge through stomata, with larger sporodochial masses of conidiophores also erupting through the leaf surface; conidia 23–100 × 2.5–4 µm, smooth, olivaceous, 1–6-septate, narrow cylindrical

Crous et al. (1989e); Crous (1998)

Pseudocercospora gracilis Crous & Alfenas (Mycosphaerella gracilis)

Irregular leaf spots on E. globulus and E. urophylla in Indonesia

Conidiophores formed singly on superficial mycelium; conidia 35–100 × 2–3 µm, smooth, 3–11septate, pale olivaceous, cylindrical with obtuse apex and truncate base

Crous and Alfenas (1995); Crous (1998)

Pseudocercospora heimii Crous (Mycosphaerella heimii)

Elongate, irregular leaf spots on Eucalyptus sp. in Madagascar

Conidiophores fasciculate or single on secondary mycelium; conidia irregularly curved, guttulate, olivaceous brown, multiseptate, 55–300 × 2.5–3 µm

Crous (1995); Crous (1998)

Pseudocercospora On leaves of Eucalyptus sp. heimioides Crous & in Indonesia M.J.Wingf. (Mycosphaerella heimioides)

Conidiogenous cells inconspicuous on mycelium; conidia in vitro olivaceous to light brown, finely verruculose, irregularly curved; 25–150 × 2–3 µm

Crous and Wingfield (1997b); Crous (1998)

Pseudocercospora Subcircular leaf spots on E. irregulariramosa Crous & saligna in South Africa M.J.Wingf. (Mycosphaerella irregulariramosa)

Conidiophores fasciculate on well developed stroma; conidia medium brown, thick walled, verruculose, multiseptate, variously curved or kinked, 35–85 × 2.5–3 µm in vivo

Crous and Wingfield (1997b); Crous (1998)

Pseudocercospora irregularis Crous

Angular to irregular leaf spots on Eucalyptus sp. in Peru

Conidiophores densely fasciculate, arising from stroma; conidia 17–90 × 3.5–5 µm, thick-walled, verruculose, 1–7-septate, with cells irregularly swollen

Crous (1998)

Pseudocercospora natalensis Crous & T.A.Cout.

Severe infection of subcircular to angular leaf spots on E. nitens in South Africa

Conidiophores fasciculate, arising from stroma; conidia 30–110 × 2–3.5 µm, smooth to verruculose, thick-walled, 4–11-septate; spermogonia present

Crous (1998)

Conidiophores arising from superficial mycelium or in fascicles breaking through epidermis; conidia 28–75 × 2.5–3.5 µm, smooth to finely verruculose, thick-walled, 1–7-septate

Kobayashi (1984); Crous (1998)

Conidiophores arising singly from superficial mycelium or formed on dense fascicles on a well developed dark stroma; conidia 45–110 × 2.5–3.5 µm, medium brown, verruculose, thick-walled, 3–9-septate; spermogonia present

Crous (1998)

Pseudocercospora Angular, vein-limited leaf paraguayensis (Tak.Kobay.) spot on eucalypts in Crous Paraguay, Brazil, Israel and Taiwan

Pseudocercospora robusta Crous & M.J.Wingf.

Subcircular leaf spots on E. robusta in Malaysia

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Fascicle of asci of Mycosphaerella nubilosa squashed from a pseudothecium.

al. 1997) and families (Reinoso 1992; Dungey et al. 1997). Certainly, there is much scope for selection of resistant species, provenances and families for use in plantations. A study of the heritability of resistance to the disease in E. globulus in Tasmania also demonstrated the possibility of breeding for enhanced resistance (Dungey et al. 1997). Resistance was partial and was inherited additively. There was evidence that selection for rapid growth in a location with low disease pressure may result in inadvertent selection for susceptibility.

9.3.1

Mycosphaerella cryptica

This species causes a spot or blotch on juvenile foliage and distinctive blotches or blights on mature foliage, often resulting in buckling and distortion of leaves (crinkle leaf) (Plates 9.4 to 9.7) (Table 9.1). Mycosphaerella cryptica (Cooke) Hansf. (syn. Sphaerella cryptica Cooke) [anamorph: Colletogloeopsis nubilosum (Ganap. & Corbin) Crous & M.J.Wingf., syn. Colletogloeum nubilosum Ganap. & Corbin; Crous and Wingfield 1997a] was originally described by Cooke (1892) from leaves collected near Melbourne. The disease has been destructive in commercial plantations of E. globulus at Woolnorth, Tas. (Park 1984), in dense young regeneration in native forests in Tasmania (Yuan 1999) and in experimental plantings of E. globulus and regenerating E. sieberi in south-east Australia (Park 1984; Carnegie et al. 1994). The fungus was found widely on E. marginata in south-west Australia, causing up to 10% leaf area loss (Abbott et al. 1993); it was particularly damaging on coppice regrowth of E. marginata and E. patens in

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some localities (Carnegie et al. 1997). The disease (initially attributed to M. nubilosa) has been damaging in New Zealand where it reached epidemic levels in over 1000 hectares of commercial forest in the central North Island (Cheah 1977). Epidemics occurred annually in New Zealand in the early 1970s and have occurred occasionally since then, with E. delegatensis and E. regnans being most severely affected (Beresford 1978). Although M. cryptica was found on the leaves and stems of E. delegatensis, E. fastigata and E. regnans in New Zealand, it was of significance only on E. delegatensis, in which leaf and twig infection resulted in dieback and multileadering (Ray 1991). The susceptibility of E. delegatensis was one of the main reasons for replacing this species with E. fastigata in plantations. The disease was most severe on seedlings and saplings (Ganapathi 1979) and adversely affected growth and form of susceptible species (Dick 1982). In Australia, M. cryptica was recorded on the juvenile and/or mature foliage of 14 eucalypt species in the subgenus Monocalyptus and 24 in Symphyomyrtus (Park 1984). On juvenile leaves of E. globulus, spots caused by M. cryptica can co-occur with those caused by M. nubilosa (Park 1984). Mycosphaerella cryptica was also recorded in New Zealand from E. fraxinoides, E. johnstonii and E. saligna (Zandvoort 1977), E. gunnii and E. tenuiramis (Ganapathi 1979), E. ovata (Dick 1982) and E. dendromorpha (Dick 1990). In Chile, M. cryptica was recorded from E. globulus, E. globulus ssp. maidenii (as E. maidenii), E. globulus ssp. bicostata (as E. bicostata) and E. nitens (Wingfield et al. 1995). On juvenile foliage of E. globulus, lesions are either circular and less than 10 millimetres in diameter (Plate 9.8) or large coalescing blotches. On mature foliage of E. globulus and on all leaves of E. obliqua, lesions tend to be large and irregular and sometimes result in blighting of the whole leaf lamina, severe leaf distortion and premature defoliation (Plates 9.5 to 9.7). Symptoms on mature foliage are first visible as a slight distortion and purple discolouration of the infected area (Plate 9.4); eventually this area becomes necrotic and turns initially red-brown and later grey (Park 1984) (Plates 9.5 to 9.7). Distortion appears to be associated with infection of young, expanding leaves. The fungus colonises the full extent of the

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Figure 9.3

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Ascospores and ascospore germination of: a) Mycosphaerella nubilosa, b) Mycosphaerella cryptica, c) Mycosphaerella parva; ascospores from type of d) Mycosphaerella nubilosa and e) Mycosphaerella cryptica. (From Park, R.F. and Keane, P.J., 1982, Transactions of the British Mycological Society 79, 95–100, with permission).

lesion before causing necrosis in the fully expanded leaf (Park and Keane 1982b). Greying of the central part of lesions is associated with the development first of acervuli and later of many mature, black, immersed ascocarps eight to 10 weeks after infection (Plate 9.8). Cankers may develop on petioles and on young shoots, especially at points of attachment of heavily infected leaves. Whole shoot tips may become blighted and distorted. In New Zealand, symptoms included formation of stem cankers up to 25 millimetres long, splitting of bark, exudation of gum and dieback of girdled twigs resulting in thinning, death and malformation of crowns (Dick 1982). In one instance, 70% to 80% of leaves were infected and shed in one month (Cheah 1977).

Leaves of E. delegatensis and E. regnans (Ganapathi 1979) and E. obliqua and E. globulus (Park 1988a) are most susceptible to infection during the first three weeks after emergence and become more resistant with age. Infection of younger leaves typically leads to the formation of larger blights and distortion of the lamina, whereas infection of older leaves produces only small spots or flecks. In coppice regrowth and pole crowns in E. marginata forest in Western Australia, most damage occurred during the first three months after leaf flush, while the young leaves were expanding, with little increase in disease on these leaves over the next 24 months (Abbott et al. 1993). Isolates of M. cryptica from E. regnans (Monocalyptus) infected E. globulus (Symphyomyrtus) and conidia of isolates from

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stages of lesion development, the anamorph (Colletogloeopsis nubilosum) may form abundant brown to black acervuli which rupture the cuticle and form conidia (Table 9.1) (Ganapathi and Corbin 1979; Crous and Wingfield 1996). Pycnidial spermagonia, identified as Asteromella Pass. & Thüm., exude rod-shaped spermatia in a mucilaginous matrix and free water is required for spermatisation and pseudothecial development (Ganapathi 1979; Park 1988a). Mature pseudothecia develop in substomatal cavities on both leaf surfaces; the mouth of the pseudothecium is formed below the stomatal pore and, at maturity, protrudes through it.

Figure 9.4

Germination of ascospore (A) of Mycosphaerella cryptica on water agar, showing formation of conidia (C). (From Park, R.F. and Keane, P.J., 1982, Transactions of the British Mycological Society 79, 95–100, with permission).

E. globulus infected E. obliqua, E. regnans and E. sieberi (Monocalyptus) (Park and Keane 1982b). Inoculation of plants has been possible only by placing heavily infected leaves above seedlings or by collecting freshly shed ascospores into a spore suspension which was then painted or sprayed onto leaves (Park 1988a). Enclosure of inoculated plants in polythene bags for one or two days provided sufficient moisture for leaf infection (Ganapathi 1979; Park 1988a) and ascospores survived up to three days of dryness after deposition on the leaf surface (Park 1988a). Germinating ascospores and conidia form secondary conidia on water agar (Fig. 9.4) and both ascospores and conidia cause infection (Park and Keane 1982a). Penetration of leaves occurs either directly through the cuticle, or less frequently, through stomatal pores. Direct penetration of the cuticle occurs beneath the ascospores or, more usually, from a protoappressorium formed laterally on the spore or at the end of a short germ tube. Initial symptoms are visible three to four weeks after inoculation, by which time the fungus has invaded the leaf extensively in a biotrophic association. In the early

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Mycosphaerella cryptica appears to be a more highly adapted pathogen than M. nubilosa: it infects both mature and juvenile foliage of many eucalypt species in both main subgenera (Monocalyptus and Symphyomyrtus), it penetrates directly through the cuticle and it grows between tightly packed palisade mesophyll cells and forms pseudothecia on both surfaces of isobilateral mature leaves. In contrast, M. nubilosa is confined to dorsiventral juvenile leaves of a limited range of eucalypt species in the subgenus Symphyomyrtus, penetrates only through stomatal pores and grows only in the intercellular spaces of the spongy mesophyll, hence forming pseudothecia mainly on the abaxial surface of the dorsiventral leaves. Windborne ascospores of M. cryptica are actively ejected from pseudothecia following wetting of the lesion surface and maintenance of high humidity over the lesion (Park and Keane 1982a). In detailed epidemiological studies in New Zealand, Cheah (1977) found that ascospore discharge was related to total rainfall, number of hours of rainfall and number of hours above 95% relative humidity, with no evidence of diurnal periodicity. Discharge occurred immediately after start of rainfall and continued for one to two hours after it had ceased (Cheah and Hartill 1987). There was less discharge in winter than in summer for the same amount of rain. The greatest concentrations of airborne ascospores occurred in autumn and early winter. In one instance, a 10-day wet period in early January resulted in prolific discharge of ascospores, followed by a disease outbreak in early February. Half of the lesions continued to actively discharge ascospores for up to 38 weeks after infection (Cheah 1977) and discharge continued for up to 12 months before ascocarps were exhausted (Beresford 1978).

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Infection of E. delegatensis occurred mainly during periods of rainfall, high relative humidity and prolonged leaf wetness in late spring, when many susceptible young leaves were present (Beresford 1978). Higher summer temperatures also favoured disease development and low temperatures limited both leaf and disease development in winter, with overwintering occurring mainly on lightly infected attached leaves. Windborne ascospores were primarily responsible for initiating epidemics in late spring and splash-dispersed conidia were important for disease spread and epidemic development in summer and autumn. The epidemiology of the disease is similar on E. globulus and E. obliqua in south-east Australia (Park 1988b). The disease appeared to be more damaging in the North Island of New Zealand than in south-east Australia and this was attributed to the genetic homogeneity and susceptibility of the E. delegatensis provenances planted, the high stocking density in plantations and the longer growing season in the milder climate of the central North Island (Beresford 1978). In New Zealand, provenances of E. delegatensis and E. regnans differed greatly in susceptibility to the disease (Zandvoort 1977; Beresford 1978; Dick and Gadgil 1983). There is certainly ample scope for selection of disease-resistant genotypes (see section 9.3.8). None of the fungicides tested by Ganapathi (1979) gave significant control of M. cryptica and many exhibited phytotoxicity. Benomyl was the least phytotoxic and gave good control of Mycosphaerella leaf spot in nurseries of E. globulus (Ganapathi 1979). Application of chlorothalonil gave an acceptable level of control of M. cryptica in a nursery of E. delegatensis (Sandberg and Ray 1976). A combination of chlorothalonil and benomyl controlled disease caused by M. cryptica and M. nubilosa on E. globulus in a field trial in Victoria (A.J. Carnegie, pers. comm.).

9.3.2

Mycosphaerella delegatensis

An epidemic of leaf spot caused by Mycosphaerella delegatensis R.F.Park & Keane [anamorph: Phaeophleospora delegatensis (R.F.Park & Keane) Crous; Crous 1998; syn. Stagonospora delegatensis R.F.Park & Keane; Park & Keane 1984] was observed on new season's growth of E. delegatensis in Victoria (Park 1984). Lesions were first visible in late January (mid summer) and further lesions, presumably arising from secondary infection via

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conidia, appeared in late April (autumn). A similar outbreak was observed on coppiced regrowth of E. delegatensis in Tasmania during 1975 (D. de Little, pers. comm.). Mycosphaerella delegatensis appears to occur almost solely on E. delegatensis, on which it causes distinctive circular lesions five to 10 millimetres in diameter (Plate 9.9) which may coalesce and lead to premature defoliation (Park and Keane 1984) (Table 9.1). If leaf senescence occurs before necrosis, tissues surrounding the infections retain some green colouration. Prior to leaf necrosis, hyphae grow predominantly within mesophyll cells. Symptoms developed three to four weeks after inoculation of young expanding leaves with either ascospores or conidia and spermagonia were formed in substomatal cavities before necrosis of leaf tissue (Park and Keane 1984). Pycnidia developed before ascocarps. The anamorph, Stagonospora delegatensis, was not considered to be a true Stagonospora species by Walker et al. (1992). Swart (1988) considered it congeneric with Septoria pulcherrima Gadgil & M.Dick which was reduced to synonymy under Kirramyces eucalypti (Cooke & Massee) J.Walker, B.Sutton & Pascoe by Walker et al. (1992) and more recently under Phaeophleospora eucalypti (Cooke & Massee) Crous, F.A.Ferreira & B.Sutton by Crous et al. (1997). Phaeophleospora delegatensis (Table 9.1) differs in conidial morphology from Phaeophleospora eucalypti (see Table 9.5) (Crous et al. 1997).

9.3.3

Mycosphaerella grandis

Mycosphaerella grandis Carnegie & Keane (anamorph unknown) was common on E. grandis growing in a eucalypt species trial in south-east Australia (Carnegie and Keane 1994). It was associated with blighting lesions which were confined to the leaf margins, often extending back from the tip almost to the petiole (Table 9.1). This species is very similar to M. parva in having immersed pseudothecia and in ascospore shape, size and mode of germination; on this basis Crous (1998) reduced it to synonymy under M. parva. However, the relationship of the two collections requires further study as M. grandis is an aggressive parasite, albeit with a restricted host range (E. grandis) (Carnegie and Keane 1994), while M. parva has been found only as a secondary invader in lesions caused

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by M. nubilosa and, to a lesser extent, M. cryptica (Park and Keane 1982a).

9.3.4

Mycosphaerella heimii

Mycosphaerella heimii Crous (syn. Mycosphaerella heimii Bouriquet, nom. nud.; anamorph: Pseudocercospora heimii Crous) was confirmed from fresh collections of elongate, irregular leaf spots on eucalypts in Madagascar (Crous and Swart 1995). The species was originally described as causing serious leaf withering and occasional seedling mortality of E. obliqua in Madagascar but no type specimen was nominated (Bouriquet 1946). On the basis of host range and morphology, Park and Keane (1984) considered this species to be similar to M. cryptica, although symptoms began as a marginal withering and gradually spread over the whole leaf (Crous 1995), a point of difference from M. cryptica. Pseudothecia are amphigenous and immersed and the distinctive anamorph clearly differentiates the species from M. cryptica (Tables 9.1 and 9.3). As the species has also been associated with extensive leaf spotting on E. urophylla in Indonesia, Crous (1998) has suggested that it may have spread to Madagascar on eucalypt material carried from Indonesia, as suggested also for Calonectria quinqueseptata (Crous and Swart 1995).

9.3.5

Mycosphaerella juvenis

Mycosphaerella leaf blotch caused by Mycosphaerella juvenis Crous & M.J.Wingf. (anamorph: Uwebraunia juvenis Crous & M.J.Wingf.) is one of the most serious diseases of E. nitens in South Africa, causing severe blotching and defoliation solely on juvenile foliage. The species is known only from south and east Africa, where it occurs on juvenile foliage of E. globulus, E. globulus ssp. maidenii, E. grandis and E. nitens (Crous and Wingfield 1996, 1997a, 1997b; Crous 1998). Only certain provenances of E. nitens can be grown in plantations because of the disease (Crous and Wingfield 1996). It was so destructive in South African plantations of E. globulus during the 1930s that it contributed to the abandonment of the species for extensive use in plantations (Purnell and Lundquist 1986; Lundquist and Purnell 1987). Mycosphaerella juvenis was referred to as M. nubilosa by Lundquist (1985) and as M. molleriana by Crous et al. (1991b); it is very

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similar to the former in symptomatology, morphology and occurrence only on juvenile foliage of a somewhat restricted range of eucalypt species (Table 9.1). It differs from M. nubilosa only in its Uwebraunia anamorph and its ability to attack a few species in addition to E. globulus. The anamorph, not reported from the Australian species, is readily produced by single ascospore cultures of M. juvenis on carnation leaf agar at 15°C under near ultraviolet light, despite its rare occurrence in nature (Crous and Wingfield 1996). Ascospores become grossly distorted following germination, a feature that also distinguishes it from M. nubilosa. Disease severity (percentage leaf area diseased) and degree of defoliation were highly correlated in a provenance trial of E. nitens heavily infected by M. juvenis in South Africa (Lundquist and Purnell 1987). Disease severity and defoliation of provenances ranged from 23% to 43% and from 6% to 50%, respectively. Provenances from New South Wales consistently had lower disease severity and defoliation than those from Victoria. Tree growth began to decline markedly at levels of defoliation greater than about 25% and most trees of New South Wales provenances were below this level. Apparently, provenances from areas with uniform or summer rainfall, where similar pathogens (e.g. M. cryptica, M. nubilosa) are likely to be most active, had greater resistance than provenances from areas less conducive to disease. The greater susceptibility of Victorian provenances was associated with their longer susceptible juvenile growth phase and with their higher growth rate (Purnell and Lundquist 1986).

9.3.6

Mycosphaerella marksii

Mycosphaerella marksii Carnegie & Keane occurred commonly on several eucalypt species in a trial in eastern Victoria (Carnegie and Keane 1994) and has since been reported from south-west Western Australia (Carnegie et al. 1997), South Africa, Portugal, Indonesia, Uruguay (Crous 1998) and Vietnam (Old and Yuan 1994; Old et al. 1999a). The species is distinguished by the slight bulge on one side of the uppermost cell of the ascospores and its mode of ascospore germination (Tables 9.1 and Table 9.2) (Carnegie and Keane 1994; Crous 1998). In Vietnam, the pathogen forms distinct marginal lesions on E. camaldulensis (Plate 9.10) (Old and Yuan 1994; Old et al. 1999a). Although it

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is widespread and occurs on several eucalypt species, it appears to be a minor pathogen.

9.3.7

Mycosphaerella molleriana

Mycosphaerella molleriana (Thüm.) Lindau (syn. Sphaerella molleriana Thüm.) (anamorph: Colletogloeopsis molleriana Crous & M.J.Wingf.) was the species of Mycosphaerella most frequently reported from eucalypts growing outside Australia. It was first described from leaves of E. globulus collected in Portugal (von Thümen 1881) and was subsequently reported from California (Wallace 1947; Browne 1968), several African countries (Lundquist and Purnell 1987), Iran (Mirabolfathy 1990), Brazil and Europe (Hedgecock 1926) and Spain (Ruperez and Munoz 1980). Examination of herbarium collections (Park 1984; Park and Keane 1984) and fresh specimens (Crous and Alfenas 1995; Crous and Wingfield 1996; Crous 1998) indicated that most of these records are of taxa which differ from the type of M. molleriana. At one stage, M. nubilosa was considered synonymous with M. molleriana (Crous et al. 1991b) but later this was rejected (Crous and Wingfield 1996). A feature which distinguishes this species from M. nubilosa is the formation in culture of the anamorph, Colletogloeopsis molleriana (Crous and Wingfield 1997a). Following these taxonomic revisions, it is now considered that the species has a much more restricted geographical range; it has been recollected only from Portugal and California, where it is associated with subcircular to irregular leaf spots on E. globulus (Table 9.1) (Crous and Wingfield 1996).

9.3.8

Mycosphaerella nubilosa

In south-east Australia and Tasmania, Mycosphaerella nubilosa (Cooke) Hansf. (syn. Sphaerella nubilosa Cooke; Park and Keane 1982a, 1984) (anamorph unknown) has been very destructive in plantations of E. globulus. It causes circular to irregular leaf spots or blotches only on juvenile or intermediate foliage of E. globulus and a few related species and can be very destructive on some provenances (Carnegie et al. 1994). It can be distinguished from M. cryptica, which can also infect juvenile foliage of E. globulus and is often found in separate lesions on the same leaves as M. nubilosa, by the presence of pseudothecia mainly on the abaxial surface of the lesion while M. cryptica forms pseudothecia on both surfaces (Park and Keane 1982a).

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Mycosphaerella nubilosa infects E. bridgesiana, E. cypellocarpa and E. globulus (Park 1984) and E. quadrangulata (Carnegie 1991) in Australia and also E. gunnii and E. viminalis in New Zealand (Dick and Gadgil 1983), all in the series Viminales, subgenus Symphyomyrtus. Symptoms caused by M. nubilosa vary with host species and with leaf age at the time of infection (Park 1988a). On most hosts studied in Australia, lesions are large, irregular blotches (Plate 9.11), or less frequently, rounded spots five to 10 millimetres in diameter, with pseudothecia confined mainly to the abaxial surface of the dorsiventral juvenile leaves (Table 9.1). Ascospores of M. nubilosa (Figs 9.2 and 9.3) are actively ejected from pseudothecia and are windborne. On young leaves of E. globulus, ascospores form germ tubes which penetrate stomata without forming appressoria and symptoms develop three to four weeks later (Park and Keane 1982b). On water agar, germ tubes emerge from both ends of the spore and cause distortion of the spores. On E. globulus ssp. pseudoglobulus, the fungus infects only young expanding or slightly older, fully expanded leaves. The incubation period increases with leaf age, being three to four weeks on the most susceptible leaves and six months on older, more resistant leaves. Under controlled conditions, optimal infection occurs following five to seven days of leaf wetness at 15°C to 20°C and ascospores survive with little loss of infectivity for up to seven days after deposition on the leaf surface. Two periods of symptom development were observed in each annual disease cycle on saplings of E. globulus in a plantation in east Victoria (Park 1988b). Infection occurred only during or soon after the growing season of the host (October to April; mid spring to mid autumn). High levels of infection coincided with periods of high rainfall on consecutive days. Infections early in the growing season, when inoculum levels were low, gave rise to predominantly small lesions (the first period of disease occurrence). Inoculum levels increased from about January onwards because of the maturation of pseudothecia on lesions from the previous season (Park and Keane 1987), resulting in heavy infection of newly emerged leaves and reinfection of older recently expanded leaves. The incubation period of these infections was prolonged by increasing leaf age and decreasing temperatures and most symptoms did not appear until July to November (the second peak

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in disease incidence, in mid winter to late spring). Symptoms which developed during the second period were often large blights covering most of the leaf and usually resulted in premature leaf drop one to two months after symptom appearance. On average over the three years of the study, 57% of leaf area was affected by the disease and 32% of leaves were shed prematurely. Each year, infection is initiated by ascospore inoculum from lesions on attached leaves of the previous year's growth. Leaves with severe infection generally fell within two to four weeks of symptom development (Park and Keane 1987), while lightly infected leaves often remained attached for longer. Pseudothecia appeared on both attached and prematurely shed leaves about eight weeks after the appearance of the first symptoms and ascospores were first produced eight to 12 weeks after symptom appearance. On prematurely shed leaves, ascocarps continued to shed spores for six to eight months and on attached leaves, for up to 17 months. The durations and quantity of ascospore discharge from prematurely shed leaves indicated that leaf litter may contribute significant quantities of inoculum in addition to that from lesions on attached leaves. The incidence and severity of disease caused by M. nubilosa and M. cryptica on mainly juvenile foliage of 44 provenances of 14 eucalypt species was assessed in a trial in eastern Victoria (Carnegie 1991; Carnegie et al. 1994). Variation in disease severity was detected between and within eucalypt species; E. cypellocarpa, E. globulus and E. nitens were highly susceptible and E. elata and E. oreades were highly resistant. Mycosphaerella nubilosa caused the most damage on E. globulus. Of the nine provenances of E. globulus assessed for resistance to disease associated with both Mycosphaerella species, three were highly susceptible and two were highly resistant. A negative correlation was found between tree growth rate and the incidence and severity of the disease, suggesting that either the disease reduced growth rate or the more susceptible provenances were slower growing. It appeared that provenances from drier or colder regions, which had probably not faced strong selective pressure from the pathogens, were more susceptible than local provenances when tested in the warm, wet environment of eastern Victoria (Carnegie et al. 1994). Selection of resistant provenances of E. globulus has potential for combating the disease in plantations.

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9.3.9

Mycosphaerella parkii

Mycosphaerella parkii Crous, M.J.Wingf., F.A.Ferreira & Alfenas (anamorph: Stenella parkii Crous & Alfenas) was described from small to large, rounded necrotic lesions on E. grandis and E. dunnii in plantations in Espirito Santo, Brazil (Crous et al. 1993f). It was also collected on leaves of E. grandis in Indonesia (Crous and Alfenas 1995) and on leaves of E. globulus and E. grandis in Colombia (Crous 1998), although the Indonesian collections differed from the Brazilian ones in forming conidia in chains (Crous and Wingfield 1997a). Mycosphaerella parkii can be distinguished from other small-spored Mycosphaerella species on Eucalyptus by its ascospores (Table 9.1). The species was shown to be pathogenic on E. grandis by inoculation of seedling leaves with a mycelium and spore suspension, resulting in appearance of prominent lesions two weeks later (Crous et al. 1993f). Most colonies readily formed the anamorph in culture (Crous 1998).

9.3.10 Mycosphaerella suberosa Mycosphaerella suberosa Crous, F.A.Ferreira, Alfenas & M.J.Wingf. (anamorph unknown) was described from a corky, irregular leaf spot on E. dunnii, E. grandis and E. moluccana in the States of Espirito Santo, Minas Gerais and Bahia, Brazil, sometimes occurring on the same leaves as M. parkii (Crous et al. 1993b). Ascospores are similar to those of M. molleriana and M. delegatensis, but M. suberosa can be distinguished by the slight olivaceous pigmentation of the ascospores which intensifies during germination, with each cell forming several highly branched, short, melanised germ tubes which tend to distort the ascospore (Fig. 9.5) (Table 9.1). The same species has been identified as a minor pathogen on E. globulus in plantations in Western Australia, the lesions being blotchy and sectored with irregular, darker margins and a central raised corky region or knob, especially on one surface (Carnegie et al. 1997). Germination of ascospores shed onto malt extract agar from samples collected in Western Australia was distinctive—each cell initially divided into two, the two middle cells became darker and verruculose and a germ tube grew from each of the resulting four cells (Carnegie et al. 1997).

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1 Figure 9.5

Mycosphaerella suberosa on Eucalyptus marginata, showing: 1) leaf spots, 2) asci and ascospores, and 3) germination of ascospores on malt extract agar. Bars represent 10 µm. (From Carnegie, A.J., Keane, P.J. and Podger, F.D., 1997, Australasian Plant Pathology 26, 71–77, with permission).

9.3.11 Mycosphaerella suttoniae Mycosphaerella suttoniae Crous & M.J.Wingf. [anamorph: Phaeophleospora epicoccoides (Cooke & Massee) Crous, F.A.Ferreira & B.Sutton] was described from leaves of a Eucalyptus species from North Sumatra, Indonesia (Crous and Wingfield 1997b) and E. grandis from Brisbane, Australia (Crous 1998) (Table 9.1 and see Table 9.5). Phaeophleospora epicoccoides [as Kirramyces epicoccoides (Cooke & Massee) J.Walker, B.Sutton & Pascoe, Hendersonia grandispora McAlpine, or Phaeoseptoria eucalypti Hansf. emen. J.Walker] is one of the most widely reported foliar pathogens of eucalypts and is discussed in more detail in section 9.7.3.1; its teleomorph is apparently far more restricted.

9.3.12 Mycosphaerella vespa associated with insect invasion Mycosphaerella vespa Carnegie & Keane is associated with small (< 5 mm diameter) leaf spots which are somewhat swollen in the centre due to the presence within the hollow necrotic tissue of the adult or pupal stage of an unidentified wasp (Carnegie and Keane 1998) (Table 9.1). The lesions were found on intermediate and adult foliage of

E. globulus and, less commonly, on E. viminalis in trials and along roadsides in south-east Australia. The lesions are characterised by the presence in one surface of a single, smooth, circular to oblong hole. This is probably the exit hole of the insect, since lesions with holes were observed to contain only empty pupal cases. Similar lesions were among the most common leaf diseases found in a five-year-old E. globulus plantation in south-central Victoria (Barber 1998). The first sign of disease in this case was the slight swelling and discolouration of the leaf lamina in association with the presence of a larva within the leaf. Several fungi, including M. vespa and Propolis emarginata, sporulated in the necrotic tissue. Unidentified dipteran or lepidopteran larvae occurred within developing lesions and empty pupal cases were found within necrotic lesions with a hole in the epidermis. In both cases, mites were commonly observed within the hollow, perforated lesions. These lesions require further study to determine the nature of the relationship between the associated fungi and insects.

9.4 Biotrophic infections This section includes biotrophic parasites which are typically evident as fungal structures or

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discolourations of infected leaf tissue in the absence of necrosis, and which may take the following forms: 1

black or brown sporocarps embedded in apparently healthy leaf tissue (‘pin spots’, ‘tar spots’, ‘blisters’ or ‘scabs’, depending on the size of the sporocarp)

2

darker areas on the leaf surface associated with the presence of superficial melanised mycelium or numerous superficial sporocarps (‘greasy spots’ or ‘black mildews’)

3

concentric rings of sporocarps and/or discolouration on otherwise healthy leaves (e.g. Phaeothyriolum microthyrioides), or

4

slightly paler circular zones visible when leaves are held up to the light (Microthyrium eucalypticola).

The sporocarps may be associated with red or purple discolouration of leaves, particularly in winter and at higher altitudes; this may be caused by accumulation of sugars at the infection site (Wall and Keane 1984). Eventually these infections may result in necrosis of leaf tissue, especially on senescing leaves. Some leaf spotting pathogens are biotrophic in the early stages of their development; for example, Phyllosticta and Sonderhenia may form pycnidia in otherwise healthy leaf tissue which may later become necrotic, and both M. cryptica and M. nubilosa invade leaves biotrophically to almost the full extent of the final lesion before causing necrosis of the invaded tissue (Park and Keane 1982b). Aulographina eucalypti is probably biotrophic throughout much of its parasitic phase (see section 9.2). Phaeophleospora (Kirramyces) species may form biotrophic infections (often purplish in colour) or vein-limited necroses, depending on the host. Eucalypt rusts and powdery mildews, which are typical biotrophic parasites, are treated separately as special cases.

9.4.1

Ascocoma eucalypti

A rarely collected discomycete, Ascocoma eucalypti (Hansf.) H.J.Swart (syn. Pseudopeziza eucalypti Hansf.; Swart 1986c) [anamorph: Coma circularis (Cooke & Massee) Nag Raj & W.B.Kendr.; syn. Pestalozziella circularis Cooke & Massee, Gloeosporiella eucalypti Hansf.; Sutton 1974], produces subcuticular stromata with

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heavily melanised upper layers (Table 9.4). Stromata are either small and unilocular or larger, confluent and containing locules of both the anamorph and teleomorph, depending on the host species (Swart 1986c). On E. dalrympleana, stromata are rounded or irregular and confluent, up to 10 millimetres in diameter and red-brown with a black centre (R.F. Park, unpubl. data). On E. pauciflora, the stromata are minute (1 mm diameter) (Sutton 1974). The fungus is a typical biotroph, forming haustorialike growths in mesophyll cells and causing little necrosis of infected leaf tissue (Swart 1986c). Locules of both the teleomorph and anamorph develop in the stromata and are fully exposed at maturity (Hansford 1956; Sutton 1974; Swart 1986c). A variety of the species, Ascocoma eucalypti (Hansf.) H.J.Swart var. didymospora H.J.Swart, has been recorded from E. pauciflora (Swart 1986c) and E. dalrympleana (R.F. Park, unpubl. data) (Table 9.4).

9.4.2

Leaf scab (Elsinoë eucalypti)

A leaf scab disease associated with Elsinoë eucalypti Hansf. was described originally from leaves of an unidentified eucalypt species collected on Kangaroo Island, SA (Hansford 1954). It appears to be rare and is known only from the type collection (Simpson 1996). The fungus has an acervular anamorph in the genus Sphaceloma. The mycelium ramifies intercellularly through the entire mesophyll and aggregates to form a subepidermal stroma (Hansford 1954). Leaf spots are up to 10 millimetres in diameter and may be confluent; on the opposite side of the leaf, lesions form a smooth, dark brown, raised spot (Hansford 1954) (Table 9.1). The anamorph was recorded from small (1–2 mm diameter), circular to elongate leaf spots on E. delegatensis in New Zealand (Dick 1990). Conidia were slightly longer and thinner (6–8 × 2–2.5 µm) than on the type specimen. The disease was also detected in Brazil (Jenkins and Bitancourt 1955).

9.4.3

Ophiodothella longispora

Infections by Ophiodothella longispora H.J.Swart are evident as discrete ascocarps, surrounded by a pseudoclypeus comprising dark host and fungal cells, embedded in otherwise healthy looking leaf tissue (Fig. 9.6). The ascocarp occupies the whole leaf

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Foliar diseases of eucalypts caused by Pyrenomycetes and Discomycetes, giving anamorphs and distinctive symptoms and features of the pathogens

Pathogen teleomorph (anamorph)

Disease symptoms

Distinctive features of the pathogen

Anthostomella eucalypti

Greyish-white rounded or irregular leaf spots, up to 15 mm diameter, with red-brown or dark brown margins, on senescent leaves in lower crown

Perithecia solitary, scattered, subepidermal, with a brown clypeus and papillate ostiole; asci unitunicate, cylindrical, with an amyloid apical plug; ascospores uniseriate, unicellular, brown, ellipsoid to reniform, 12–18 × 3.5–8 µm, compressed laterally, apex papillate, base truncate with globose appendage in dried material, ascospore with gelatinous sheath in fresh material; paraphyses present

Ascocoma eucalypti (Coma circularis)

Subcuticular stromata with upper layers heavily melanised; no necrosis

Stromata small and unilocular or larger with locules of both teleomorph and anamorph, depending on host; at maturity sporocarps fully exposed; conidia with larger terminal cell (28–38 × 7–9 µm) with apical seta, and smaller basal cell (5–7 × 3–4 µm) with three divergent setae (40–50 × 1–1.5 µm); ascospores hyaline, 1-celled, smooth, fusiform with rounded ends, 25–32 × 7–9 µm

Ascocoma eucalypti var. didymospora

As for Ascocoma eucalypti

Differs from Ascocoma eucalypti in having unevenly 2-celled ascospores

Clypeophysalospora latitans (possibly Idiocercus australis)

Individual ascocarps in green leaf tissue, sharp black spots (1–1.3 mm diameter) or leaf blight

Differentiated from Plectosphaera eucalypti by occurrence of a definite melanised clypeus, the uniseriate arrangement of ascospores in ascus, and the presence of an amyloid apical ring and pulvillus in tip of ascus; ascospores 1-celled, 15–28 × 5–13 µm

Ophiodothella longispora

Discrete black perithecia embedded in healthy-looking leaf tissue, causing localised swelling of leaf

Perithecium surrounded by pseudoclypeus on upper leaf surface, with similar dark region below; lateral walls hyaline; perithecium occupies the whole leaf thickness; ascospores elongate, unicellular, parallel, 150–200 × 4–6 µm

Plectosphaera eucalypti

Slight thickening or reddish discolouration on leaf; from tiny circular to large, elongated distorted infections, depending on the host; biotrophic; usually on only one leaf surface

Pycnidia on younger lesions; perithecia larger, immersed closely packed, visible as glossy black swellings; both with pseudoclypeus; conidia 1-celled, hyaline, obovoid with a flattened base and small marginal frill, 5 × 2 µm; ascospores 1-celled, fusiform, gelatinous with central bulge when mature, 30 × 10 µm. (In fresh specimens, asci bitunicate with annellate barrel-shaped apical apparatus)

Propolis emarginata

Ascocarps on dead leaves or small, irregular, bleached leaf spots

Ascomata apothecioid, 0.2–0.8 mm diameter, initially subepidermal but breaking through the leaf surface and opening by 2–5 radial slits, with paraphyses often branched near the tip; ascospores filiform, 90–105 × 2 µm, 1-septate, with terminal gelatinous caps

Rehmiodothis inaequalis

Tar spot evident as flattened, glossy black stromata originating beneath epidermis in an otherwise healthy leaf

Ascostromata glossy black, dome-shaped, with sparse ostioles emerging through leaf surface as slightly protruding gelatinous structures; ascospores 2-celled, hyaline, with basal cell less than half the length of the apical cell, 22–29 × 6–7 µm

Rehmiodothis eucalypti

Tar spot as for Rehmiodothis inaequalis but with smaller stromata

Crowded ascocarp ostioles; ascospores (25–39 × 8–13 µm) similar to but larger than for Rehmiodothis inaequalis

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Figure 9.6

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Cross section of leaf showing biotrophic infection of Ophiodothella longispora penetrating completely through the leaf and cross section through ostiole. (From Swart, H.J., 1982, Transactions of the British Mycological Society 79, 566–568, with permission).

depth, causes a swelling of the leaf and is most clearly visible on the upper surface; a dark region occurs in the mesophyll and epidermis above and below the ascocarp while the lateral wall is hyaline. The fungus was first described from E. goniocalyx and has been recorded also on E. regnans (Swart 1982c). While it resembles Plectosphaera eucalypti in its parasitic habit and thick, gelatinous ascus wall (Swart 1981a), it differs in forming elongate, unicellular, parallel ascospores (Table 9.4). The fungus is biotrophic and does not initially cause necrosis of leaf tissue, even when actively sporulating (Swart 1988). It may cause some anthocyanin pigmentation in the early stages of development, followed by development of a chlorotic zone which indicates the extent of infection.

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This zone may eventually become necrotic in association with colonisation by one or other of the coelomycetes, Macrohilum eucalypti or Fairmaniella leprosa, which in this situation appear to be secondary invaders of tissue weakened by the presence of the biotrophic parasite (Swart 1988).

9.4.4

Blister diseases (Pachysacca species)

Pachysacca species form subepidermal stromata which appear as brown to black, elevated, blistered regions on one side of the leaf lamina (Swart 1982b). All species appear to be biotrophs and form multilobed, cauliflower-like haustoria in the first three layers of mesophyll cells adjacent to the

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stroma, occasionally with more than one haustorium per cell (Duncan 1989). Asci with thick gelatinous walls are formed in locules within the stroma; ostioles invariably occur under stomatal pores. Often the host tissues show a meristematic response to the presence of the fungus and in older infections the underlying mesophyll may become necrotic and separated from healthy tissue by a cork cambium. Leaf tissues opposite the stroma may be discoloured. Pachysacca eucalypti Syd. emen. H.J.Swart forms small, circular stromata and elongate, cylindrical, three-celled ascospores in locules scattered throughout the stroma (Table 9.1). Thickening of the leaf results from a strong meristematic reaction in the mesophyll tissue and spots are usually visible on both sides of the leaf, with a less well developed stroma being formed on the side opposite the main stroma. Pachysacca samuelii (Hansf.) H.J.Swart forms spreading dendritic or very large circular stromata (Plate 9.12, Fig. 9.7). A characteristic layer of prosenchyma is formed adjacent to the mesophyll, with the hyphae oriented along the dendritic branches in the direction of expansion of the stroma. This species produces smaller spermatia and smaller ascospores (4-celled) than Pachysacca eucalypti (Table 9.1). Haustoria are formed mainly in the layer of palisade mesophyll directly beneath the stroma and are much larger than in Pachysacca eucalypti. There is no stromatic development on the opposite side of the leaf. A third species, Pachysacca pusilla H.J.Swart, produces tiny circular stromata and even smaller four-celled ascospores (Table 9.1). It has been recorded only from E. regnans in Australia, but was reported from four additional eucalypt species in New Zealand, where it has little effect on the health of its hosts (Dick 1990). Pachysacca samuelii was found on E. obliqua and E. odorata in South Australia and Pachysacca eucalypti on several eucalypt species, including E. camaldulensis and E. diversifolia, in South Australia and E. viminalis in Victoria (Swart 1982b). At three study sites in Victoria, Pachysacca samuelii was the most common species, occurring on E. camaldulensis, E. cypellocarpa, E. dives, E. goniocalyx, E. ovata and E. viminalis (Duncan 1989). The disease had a very restricted distribution in the field, usually being common on a few trees in a population but difficult to find on most other nearby trees of the same species. Maturation of locules depended on rainfall and occurred during

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two periods between December 1988 and October 1989. New infections occurred only during the cooler months. On E. dives, the incubation period was estimated to be less than four weeks and after three months, lesions had developed to an average diameter of four millimetres. Attempts to induce infection of seedlings with Pachysacca samuelii were unsuccessful (Duncan 1989).

9.4.5

Sooty blotch (Phaeophleospora species)

Pycnidial fungi in the genus Phaeophleospora (formerly Kirramyces or Phaeoseptoria; Crous et al. 1997) may form black, subepidermal pycnidia in leaf tissue without causing immediate necrosis (Walker 1962), or cause purple blotches (Dick 1982) or necrotic lesions delimited by veins (Heather 1965), depending on the host. The copious extrusion of dark conidia in cirri, characteristic of these fungi, may result in a dark conidial mass spreading over a large part of the leaf surface, giving the appearance of a black flaky coating or sooty mould, with which the infections are often confused (Walker et al. 1992). These diseases are described below in more detail as vein-limited necroses.

9.4.6

Ring infections (Phaeothyriolum microthyrioides and similar fungi)

Several biotrophic Loculoascomycetes form large circular colonies on eucalypt leaves without causing any obvious necrosis of leaf tissues until infections are very old. These infections are evident as a zone of concentric rings of superficial ascocarps (thyriothecia), as an area of slight greying of the leaf surface associated with the presence of ascocarps, or as a slightly chlorotic circular zone (Plate 9.13). Often these fungi are associated with a distinctive ring of reddish pigmentation that is visible long before any fungal structures are evident. Several fungi of this type were reclassified by Swart (1986b) as Phaeothyriolum microthyrioides (G.Winter) H.J.Swart [syn. Asterina microthyrioides G.Winter, Microthyrium amygdalinum Cooke & Massee, Seynesia microthyrioides (G.Winter) Theiss., Phaeothyriolum eucalyptinum Syd., Mycomicrothelia eucalyptina (Syd.) E.Müll., Arnaudiella bancroftii Hansf.]. The species is variable and was recorded on an Angophora species as well as E. delegatensis, E. elata, E. nitens, E. pauciflora, E. polyanthemos, E. tetrodonta and E. viminalis. Ascocarps are

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Figure 9.7

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Pachysacca samuelii on Eucalyptus obliqua, showing: A) cross section through subepidermal infection, B) ascus and ascospores, C) spermatia and phialides, and D) edge of stroma and haustorium. (From Swart, H.J., 1982, Transactions of the British Mycological Society 79, 261–269, with permission).

superficial and dimensions of the two-celled ascospores (Fig. 9.8 and Table 9.1) range from 15–17 × 6–7 micrometres on E. tetrodonta to 24–29 × 9–10 micrometres on E. pauciflora. The fungus has also been recorded on C. ficifolia, E. camphora, E. cephalocarpa, E. dalrympleana, E. dives, E. fastigata, E. rubida and E. sieberi (Park and Keane 1982c; R.F. Park, unpubl. data). It was one of the most commonly encountered leaf-

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infecting fungi in a survey of diseases of plantations of E. globulus and E. nitens in Tasmania (Yuan 1999). A similar fungus, identified as Microthyrium eucalypti Henn., was recorded from several eucalypt species in New Zealand (Dick 1982). Swart (1986b) could not locate a type specimen for Microthyrium eucalypti and was unable to reach a conclusion about its identity. In view of the variable morphology of Phaeothyriolum microthyrioides,

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Figure 9.8

Asci and ascospores of Phaeothyriolum microthyrioides. Photograph courtesy of G. Kalc-Wright.

it is likely that the New Zealand fungus belongs to this species. Infection hyphae of Phaeothyriolum microthyrioides grow within the cuticle (Kalc 1983) (Fig. 9.9) or in the external walls of epidermal cells which they appear to digest without obviously pushing wall layers apart (Swart 1986b). Internal hyphae are connected by fine thread-like pegs to a network of surface hyphae which often extends well beyond the area of the leaf bearing ascocarps (Kalc 1983). Ascocarps are entirely superficial and are linked to the internal mycelium by thin connections. Some host species (e.g. E. globulus) form cork layers in a ring where ascocarps would be expected to form. Like many of the slow-developing leaf parasites of Eucalyptus, this fungus is most commonly seen on the older leaves in the lower crown. The fungus on E. delegatensis appears well adapted to cooler, highland conditions—optimal ascospore discharge occurred at 5°C to 10°C and symptom development in the field was greatest during the cooler months (Kalc 1983). Ascospore germination could not be induced on artificial media even in the presence of leaf extracts; however, germination was observed on inoculated leaves on seedlings and penetration of these leaves occurred by infection pegs produced from protoappressoria, although development of symptoms was not observed in this study (Kalc 1983). The taxonomic affinities of two similar fungi examined by Swart (1986b) remain obscure. A fungus causing a disease often referred to as ‘greasy spot’ appears superficially similar to Phaeothyriolum microthyrioides in ascocarp

Figure 9.9

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Cross section of leaf infected by Phaeothyriolum microthyrioides, showing infection hypha growing within the cuticle. Photograph courtesy of G. Kalc-Wright.

morphology but has smaller ascospores (11–15 × 3.5–4 µm). Infection hyphae are entirely superficial with melanised hyphae growing mainly in the troughs between epidermal cells (Kalc 1983). Ascospores of this fungus germinate readily on water agar and Kalc (1983) concluded that it was most likely an epiphyte. It resembles Schizothyrium Desm. (Swart 1986b) and has been recorded on E. delegatensis, E. globulus, E. nitens and E. pauciflora (R.F. Park, unpubl. data). The second fungus, Microthyrium eucalypticola Speg., is similar to Phaeothyriolum microthyrioides in producing a subcuticular and intracuticular mycelium. Some hyphae enter epidermal and palisade mesophyll cells, but only after the leaf has died. Thyriothecia are formed only on dead leaves (Fig. 9.10) and it has a circular ostiole, in contrast to Phaeothyriolum microthyrioides, which forms thyriothecia on living leaves and has an irregular, often star-shaped ostiole (Table 9.1). Swart (1986b) was unable to comment on the status of Microthyrium eucalypticola because he had only one obscure herbarium specimen; however, a similar fungus was found recently to be one of the most common leaf-infecting fungi on older leaves in several trial plantations of E. globulus in southern Victoria (Barber 1998). The infections appear as faintly chlorotic circular zones, up to 30 millimetres in diameter, that are visible when leaves are held up to the light. On some trees, up to 60% of the lower leaves were infected. In the chlorotic zones, the fungus grows within the cuticle. Distinctive black rings of superficial mycelium and ascocarps become visible on the leaves after they

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Figure 9.10

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Infection of Microthyrium eucalypticola on fallen leaf of Eucalyptus globulus. Photograph courtesy of P.A. Barber.

have senesced and were particularly obvious on leaves in leaf litter or, occasionally, on senescent leaves that remained attached to the tree for an extended period (Barber 1998). A very similar fungus was described as a new species, Arnaudiella eucalyptorum Crous & W.B.Kendr., from eucalypt leaf litter in South Africa (Crous and Kendrick 1994). It was considered to be saprophytic. In culture, this fungus produced a hyaline anamorph, Xenogliocladiopsis eucalyptorum Crous & W.B.Kendr., that formed unicellular, cylindrical conidia (7.5–11 × 1–1.5 µm) on penicillate conidiophores. Another related parasite that does not cause obvious necrosis on eucalypt leaves is Thyriopsis sphaerospora Marasas (Marasas 1966). This fungus is known only from South Africa (Lundquist and Baxter 1985; Crous 1990) and Brazil (Cémara and Dianese 1993), where it is associated with corky lesions on leaves of eucalypts. The ascostromata are raised, brown to black and occur singly or in clusters on both leaf surfaces. These structures are usually found on healthy leaf tissue and subsequently form small, discrete, corky, necrotic lesions, extending through the leaf lamina. This fungus infects both juvenile and mature foliage and severe infection leads to premature defoliation.

9.4.7

Phyllosticta species

Species of the coelomycete genus Phyllosticta are initially biotrophic but later form small leaf spots (Crous et al. 1993f). The species are distinguished by conidial size (Table 9.5). Phyllosticta extensa Sacc. & P.Syd. was described from eucalypt leaves in California and Phyllosticta extensa is regarded as the prior name for Phyllosticta eucalypti Ellis & Everh. (Saccardo 1899). Phyllosticta eucalypti Thüm. was described from E. globulus in Portugal (Saccardo

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1884) and Macrophyllosticta eucalyptina (Pat.) Sousa da Câmara (syn. Phyllosticta eucalyptina Pat.) from E. globulus in Tunisia (Saccardo 1899). Phyllosticta eucalyptorum Crous, M.J.Wingf., F.A.Ferreira & Alfenas (teleomorph: Guignardia eucalyptorum Crous; Table 9.1) was described from small spots and larger blotches with a red-purple, slightly raised margin on leaves of E. grandis in Brazil (Crous et al. 1993f) and was recorded on leaves of E. grandis seedlings in South Africa (Crous 1993). The anamorph has been isolated as an apparent endophyte from healthy leaves of E. grandis and Syzygium cordatum Hochst. (P.W. Crous, unpubl. data).

9.4.8

Plectosphaera eucalypti and Clypeophysalospora latitans

Plectosphaera eucalypti (Cooke & Massee) H.J.Swart [syn. Trabutia eucalypti Cooke & Massee, Phyllachora maculata Cooke, Phyllachora eucalypti (Cooke & Massee) Theiss. & Syd.; Swart 1981a] causes symptoms which vary with the host species but which usually involve a slight thickening and reddish discolouration of the leaf (Table 9.4) in association with the presence of black sporocarps embedded in the leaf tissue (Swart 1981a, 1981b). The fungus forms tiny, circular to irregular colonies a few millimetres in diameter on E. regnans, larger, raised colonies on E. goniocalyx and forms large, elongated, distorting infections up to five centimetres long on E. melliodora. Specimens have also been found on E. leucoxylon, E. obliqua and E. pauciflora (Pascoe 1990). The infections are usually evident only on one leaf surface and cause only slight discolouration on the opposite surface. Vegetative hyphae are irregular, hyaline and grow intracellularly, branching profusely and causing swelling of the invaded regions of the leaf. Pycnidia are visible in younger infections, while the larger ascocarps are clearly visible as glossy black swellings, which are closely packed and cover the colony right to its margin. With both sporocarps, the upper wall is fused with the host epidermis, forming an intensely melanised pseudoclypeus (Fig. 9.11). In fresh specimens, asci appear bitunicate, a feature not apparent in dried herbarium specimens and they have an annellate barrel-shaped apical apparatus, especially in aqueous mounts (Pascoe 1990). In view of these findings, further work is required to determine the correct generic classification of this fungus (Pascoe 1990).

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Foliar diseases of eucalypts caused by pycnidial Coelomycetes, listing recent generic synonyms, teleomorphs, symptoms and and distinctive features of the pathogens

Pathogen anamorph [synonym] (teleomorph)

Disease symptoms

Distinctive features of the pathogen

Aurantiosacculus eucalypti

Small irregular lesions with purple-black margins

Large (0.2–0.9 mm diameter), bright orange, globose, erumpent, gelatinised pycnidia, becoming black with age, with large angular ostiole; conidia (51–81 × 2–3 µm) hyaline, 1-celled, smooth, curved, with slightly swollen base and smaller, thickened truncate basal scar and tapered, acute apex

Ceuthospora innumera (Phacidium eucalypti)

Winter leaf spot of E. regnans. Dull water soaked spots and patches, often at tips of lower leaves, developing a purple margin and becoming necrotic and coalescing to form a blight

Pycnidia formed in immersed multilocular stromata, which protrude through the epidermis by a hyphal plug with one or two ostioles; conidia hyaline, 1-celled, cylindrical or slightly tapering, 16–20 × 2.5–3 µm, with rounded ends and funnelshaped, gelatinous apical appendage, produced on phialides lining the locule

Ceuthospora lauri

Lesions on E. grandis in South Africa; on lower foliage in cooler wetter months

Conidia (11.5–14 × 2.5 µm) are small than those of Ceuthospora innumera and are formed on conidiophores in the locules (Sutton 1980)

Coniella australiensis

Circular, spreading leaf spots with pycnidia irregularly distributed

Pycnidia globose, immersed to semi-immersed, simple, thin-walled; conidia smooth, 1-celled, dark brown, globose to napiform with a truncate base, 10–14 × 7–12 µm

Coniella castaneicola (Schizoparme straminea)

Light brown roundish lesions

Globose, immersed to semi-immersed pycnidia formed in concentric rings or irregularly distributed; conidia smooth, 1-celled, pale brown, navicular, fusiform, falcate with a truncate base, slightly curved, 13–29 × 2.5–3.5 µm. Perithecia with a circumostiolar epistroma often associated with pycnidia; asci with thickening at apex; ascospores hyaline or pale yellow, 1-celled, elliptical, often inequilateral or curved, with thin mucilaginous coat giving appearance of small appendage at end of spore, 11–13 × 3–4 µm

Coniella fragariae

Circular leaf spots beginning on leaf margins and spreading to form large circular lesions with pycnidia in concentric rings; also on petioles and twigs

Numerous light to dark brown pycnidia develop in compact concentric rings; subepidermal and erumpent, exuding dark brown to black conidial ooze; conidia smooth, 1-celled, brown, thick walled, globose to napiform, 7.5–11 × 5.5–7.5 µm

Coniella granati

Initially browning of leaf tips, extending to the entire leaf lamina and stem, killing seedlings. Occasionally lesions only on stems

Numerous black, dot-like pycnidia develop on necrotic tissues; conidia smooth, 1-celled, pale brown, straight or slightly curved, fusiform, 10–15 × 2.5–3.5 µm

Coniella minima

Leaf spots

Pycnidia as for Coniella australiensis; conidia smooth, 1-celled, pale brown, globose to subglobose, 6.5–7.5 × 3.5–4.5 µm

Coniella petrakii

Leaf spots

Pycnidia as for Coniella australiensis; conidia smooth, 1-celled, pale to medium brown, ellipsoid, occasionally slightly curved, apex obtuse, base truncate, 10–15.5 × 4.5–7 µm.

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Foliar diseases of eucalypts caused by pycnidial Coelomycetes, listing recent generic synonyms, teleomorphs, symptoms and and distinctive features of the pathogens (continued)

Pathogen anamorph [synonym] (teleomorph)

Disease symptoms

Distinctive features of the pathogen

Coniothyrium ahmadii

Lesions on branches

Pycnidia as for Coniothyrium eucalypticola; conidia formed holoblastically, dark brown, 1-celled, elliptical, thick-walled and rough-walled, 6–7 × 3.5–4.5 µm

Coniothyrium eucalypticola

Pale brown, more or less veinlimited, circular or irregular leaf spots, 2–10 mm diameter, darkening due to exuded spores

Pycnidia very small (up to 30 µm diameter), thinwalled, globose, brown, amphigenous, substomatal; conidia 8.5–12 × 6–9 µm, dark brown, 1-celled, elliptical or broadly clavate, thick-walled, verruculose, with truncate base and basal marginal frill

Coniothyrium kallangurense

Leaf spots

Differs from Coniothyrium eucalypticola in having smooth to finely verruculose, thin-walled, ovoid to pyriform conidia, constricting at truncate base, 4–10 × 2–7 µm

Coniothyrium ovatum

Small necrotic leaf spots, 1–2 mm diameter

Differs from Coniothyrium eucalypticola in having ellipsoidal conidia, widest at or below the middle, with basal marginal frill, finely verruculose, 5–11 × 2–4 µm

Cryptosporiopsis eucalypti

Discrete warty irregular leaf spots, light to dark brown with dark red-brown margins; leaf rough due to areas of dark, red-brown, erumpent tissue; also stem infection and shoot blight

Conidiomata amphigenous, subepidermal, pycnidial to acervular, cupulate, often opening by an irregular rupture through which conidia exude in a creamyellow mass; conidia 1-celled, hyaline, smooth, thick-walled, eccentric ellipsoidal with an obtuse apex and tapering base with a protruding truncate scar or collar, 11–20 (25) × 4.5–8 µm

Davisoniella eucalypti

Abundant leaf spots on E. marginata

Subepidermal, abaxial, stromatic, unilocular or multilocular conidiomata which raise the epidermis when mature; pycnidia lined with small, flask-shaped conidiogenous cells; conidia 1-celled, thick-walled, verruculose, brown, oval-shaped with a rounded apex and truncate base with a marginal frill, 10–12 × 5–6 µm

Dichomera eucalypti

Black unilocular or multilocular stromata in otherwise green leaf or associated with small leaf spots

Conidia 10–13 × 7–9.5 µm, pale brown, smooth, muriform with 1–3 dark brown transverse septa and one or more longitudinal or oblique septa, subglobose to obpyriform, somewhat irregular, tapered to a truncate base with marginal frill

Dichomera versiformis

Pale, elliptical to rounded or irregular leaf spots with scattered, erumpent pycnidia mainly in the centre of the lesion

Black pycnidia subepidermal to erumpent; conidia brown to black, variable in shape and size, from subglobose to obpyriform (12.5–17.5 × 10–11.5 µm) to elongate ellipsoid (22.5–30 × 7.5–10 µm), muriform with 1–7 transverse septa and occasional longitudinal septa

Hainesia lythri (Discohainesia oenotherae, syn. Pezizella oenotherae)

Light brown to tan marginal scorch develops on expanding leaves and eventually extends down the stems, which become dark brown to black

Separate, pale brown conidiomata, initially globoid but becoming cupulate to discoid, up to 200 µm diameter; conidia 1-celled, hyaline, smooth, thin-walled, cymbiform to allantoid, acute at each end, often guttulate, 5–7.5 × 1.5–2 µm

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Pathogen anamorph [synonym] (teleomorph)

Disease symptoms

Distinctive features of the pathogen

Harknessia eucalypti

Small, vein-limited leaf spots

Pycnidia abundant, amphigenous, separate, immersed, subepidermal, globose, unilocular, erumpent, punctate; conidia 18–25 × 11–14.5 µm, broadly ventricose with bluntly apiculate apex, dark brown, 1-celled, with smooth thick wall and a distinct basal frill or hyaline, stalk-like appendage (2–12 µm long), exuded in black mass

Harknessia eucalyptorum

Leaf and peduncle necrosis; lesions light brown, round to irregular

As for Harknessia eucalypti but conidia (16–29 × 9–24 µm) broadly ventricose with a bluntly apiculate apex and a basal appendage 3–16 µm long

Harknessia fumaginea

Tip blight of young lateral shoots

Immersed pycnidia on leaves and petioles; conidia dark brown, smooth, globose (14 × 9 µm) with a thick wall and hyaline basal appendage 2–7.5 µm long

Harknessia globosa

Small leaf spots or leaf litter

Pycnidia abundant, amphigenous, separate, immersed, subepidermal, globose, unilocular, erumpent, punctiform; conidia 14–16 × 12–13.5 µm, globose, 1-celled, dark brown, with smooth thick wall, hyaline basal appendage 2–7 µm long

Harknessia hawaiiensis

Small irregular leaf spots up to 10 mm diameter or endophytic

Pycnidia separate, immersed, subepidermal, globose, unilocular, erumpent, punctiform, breaking wide open at the leaf surface; conidia 9.5–12.5 × 8–9 µm, globose to broadly elliptical, dark brown, 1-celled, with smooth thick wall, exuded in black mass, hyaline basal appendage 2–7 µm

Harknessia insueta

Small leaf spots

Pycnidia abundant, separate, immersed, subepidermal, globose, unilocular, erumpent; conidia 10–11.5 × 8–9 µm, obliquely napiform to gibbose, dark brown, 1-celled, with eccentric apical appendage 1.5 µm long and basal marginal frill

Harknessia tasmaniensis

Large, irregular, light-brown to dark-brown lesions mainly at the leaf tip; often associated with other fungi such as Harknessia victoriae or Mycosphaerella nubilosa

Pycnidia abundant, separate, immersed to partly erumpent, punctiform, often opening widely onto the leaf surface; macroconidia subcylindrical to elongate-ellipsoid, straight, sometimes narrower in centre, 1-celled, thick-walled, smooth, brown, 29–41 × 13–18 µm, with a distinct apiculus and truncate base and basal appendage 9–15 µm long; microconidia formed in same or separate pycnidia, fusiform with truncate base, 1-celled, hyaline, smooth, 3–7.5 × 2–2.5 µm

Harknessia uromycoides

Small spots on leaves, twigs and fruits; the most common species on eucalypts

Pycnidia abundant, amphigenous, separate, immersed, subepidermal, globose, unilocular, erumpent, punctate; conidia 18–26 × 9–13 µm, broadly or narrowly ventricose with bluntly apiculate apex, 1-celled, dark brown, with smooth thick wall, with longer basal appendage 30–90 µm, several times the length of the conidium, exuded in black mass

Harknessia victoriae

Large pale brown, irregular lesions on margins of senescent leaves in lower crown

Resembles Harknessia globosa but differs by larger subglobose to ellipsoidal conidia (16–21 × 12–15 µm), a longer basal appendage (5–15 µm), a persistent mucilaginous sheath on the conidia, and presence of microconidia

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Foliar diseases of eucalypts caused by pycnidial Coelomycetes, listing recent generic synonyms, teleomorphs, symptoms and and distinctive features of the pathogens (continued)

Pathogen anamorph [synonym] (teleomorph)

Disease symptoms

Distinctive features of the pathogen

Idiocercus australis

Large necrotic lesions or small (3–5 mm diameter) irregular lesions which sometimes drop out leaving a characteristic hole; small, black immersed pycnidia scattered across lesions

Pycnidia separate, immersed but slightly raising the epidermis, globose to broadly ellipsoidal, brown but distinctly darker around the ostiole, with holoblastic conidiogenous cells arising from the inner wall; conidia 1-celled, hyaline, thin-walled, smooth, cylindrical or elliptical, with an obtuse apex and truncate base and minute to small basal frill, 15–29 × 5–7 µm

Macrohilum eucalypti

In necrotic tissue in association with Ophiodothella longispora, or in small pale brown spots with a dark brown margin

Conidiomata with a wide ostiole and single, often convoluted lumen, and generally appear pycnidial although may appear acervular when ostiole has opened wide; mature conidia 2-celled with median septum at which they may be slightly constricted, greenish-brown to dark brown, flattened sideways with a broadly rounded apex and wide base with a large protruding hilum, 15–19 long by 10–12 × 7–9 µm

Microsphaeropsis callista

Circular to elliptical, irregular brown leaf spots with raised purple margin, 3–10 mm diameter, pycnidia on slightly convex centre of lesion

Pycnidia globose, subepidermal, erumpent; conidia ellipsoid, 6–8.5 × 3.5–5.5 µm, 1-celled, brown, darker at both ends and especially the base, smooth, thickwalled, with a central guttule, tapering to truncate base

Microsphaeropsis conielloides

Light to dark brown leaf spots, 1–4 mm diameter, roughly circular to angular with a dark brown or purple raised margin. More common on older leaves

Globose to subglobose amphigenous pycnidia, 30–90 µm diameter; conidia 1-celled, brown, ornamented, 6–19 × 3–4 µm, exuded in dark brown masses onto leaf surface

Phaeophleospora destructans [Kirramyces destructans]

Large subcircular to irregular leaf spots, 10–20 mm in diameter or distorting blight of young leaves, buds and shoots of E. grandis in Indonesia. Conidia form black masses on lesion

Similar to Phaeophleospora eucalypti except for its longer and thinner (30–70 × 2.5–3 µm), variously curved, 1–3-septate conidia. Pycnidia hypophyllous. Spermogonia seen occasionally

Phaeophleospora epicoccoides Necrotic lesions delimited by [Kirramyces epicoccoides] veins or purple blotches up to (Mycosphaerella suttoniae) 7 mm across or pycnidia formed in green tissue. Exudation of dark conidial masses onto leaf surface may give appearance of sooty mould Phaeophleospora eucalypti [Kirramyces eucalypti]

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Blotchy or necrotic lesions, rounded or delimited by veins, 2–12 mm diameter. May cover a large proportion of leaf. Initially only slight paling of patches on young leaves turning pale yellow and carmine red before becoming necrotic

Pycnidia black, subglobose, glabrous, amphigenous or hypophyllous, scattered, substomatal, partly erumpent, exuding a brown to black cirrus of conidia which are brown, cylindric-fusoid (35–60 × 3–6 µm), verruculose, 1–7-septate, with a truncate base and basal frill. Conidiogenous cells prominent, rough-walled and percurrently proliferating. Top of pycnidium may rupture to give acervular appearance Differs from Phaeophleospora epicoccoides by more finely roughened or smooth, paler (hyaline to pale brown), 0–4-septate and more delicate conidia (25–60 × 2–4 µm) and conidiogenous structures. Pycnidia amphigenous, may be deeply embedded. Conidiogenous cells short and flask-shaped, not prominent, rough-walled and percurrently proliferating as in Phaeophleospora epicoccoides

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Disease symptoms

Distinctive features of the pathogen

Phaeophleospora lilianiae [Kirramyces lilianiae]

On C. eximia

Similar to Phaeophleospora epicoccoides but differs in the conidia which are brown, rough-walled, 1–3-septate, cylindrical and slightly wider (35–50 × 4–7 µm)

Phyllosticta eucalypti

Leaf spot on E. globulus in Portugal

Similar to Phyllosticta eucalyptorum but conidia 4 × 1.5 µm.

Phyllosticta eucalyptina [= Macrophyllosticta eucalyptina (Pat.) Sousa da Câmara]

Leaf spot on E. globulus in Tunisia

Similar to Phyllosticta eucalyptorum but conidia 18–20 × 5–6 µm

Phyllosticta eucalyptorum (Guignardia eucalyptorum)

Initially biotrophic but later forming small spots (3 mm diameter) to larger blotches with a red-purple, slightly raised margin on leaves of E. grandis

Mostly aggregated, amphigenous, black pycnidia, immersed but becoming erumpent; conidia 1-celled, guttulate, ellipsoidal, 7.5–20 × 5–6.5 µm, with persistent mucous coat about 1 µm thick, and apical appendages 3–10 µm long; ascocarps obpyriform, intermixed with pycnidia, with bitunicate asci; ascospores hyaline, 1-celled, fusiform-ellipsoidal, 14–18 × 4–6 µm, wider in the mid region, with gelatinous plugs

Phyllosticta extensa

Small leaf spot on eucalypt in California

Similar to Phyllosticta eucalyptorum but conidia 5–8 × 1.5–2.5 µm

Piggotia substellata

Winter leaf spot of E. regnans. As for Ceuthospora innumera above

Pycnidia formed on the leaf surface after the rupture of the cuticle; conidia hyaline, 1-celled, elliptical, 8–13 × 2–2.5 µm

Readeriella mirabilis

Circular or irregular shiny spots up to 15 mm diameter, on some hosts formed on one or other leaf surface only. Common secondary invader of lesions caused by other fungi or insects

Pycnidia scattered in a roughly concentric pattern on spots, subepidermal, dark brown, globose, erupting through the epidermis without forming a definite ostiole; distinctive conidia are 1-celled, thick-walled, smooth, brown, deltoid with a truncate base and basal marginal frill, 7–10 × 6.5–10 µm

Selenophoma eucalypti

Irregular necrotic lesions occurring mainly along the leaf margins

Separate, subepidermal, mainly epigenous pycnidia; conidia hyaline, 1-celled, smooth, fusiform, straight to falcate, tapering to an acute, rounded apex and subtruncate base, 8–15 × 2–3.5 µm

Sonderhenia eucalyptorum (Mycosphaerella swartii)

Tiny leaf spot or leaf speckle, up to 3 mm diameter, slightly raised, with a purple-red margin and a few scattered pycnidia

Pycnidia black, globose, subepidermal, amphigenous, sometimes intermingled with ascocarps; conidia olivaceous, thick-walled, finely verruculose, cylindrical, 25–49 × 4–10 µm, with 3 transverse distosepta, base truncate with marginal frill; borne on smooth-walled, annellidic conidiogenous cells

Sonderhenia eucalypticola (Mycosphaerella walkeri)

Lesions initially purple disolourations that become tiny necrotic spots, light brown, raised, with dark red to brown margins and a few scattered pycnidia. Pycnidia may be formed in green leaf tissue

Pycnidia similar to Sonderhenia eucalyptorum; conidia thick-walled, finely verruculose, with 3 transverse distosepta and truncate base with a marginal frill, but differ from those of Sonderhenia eucalyptorum in being dark brown, ellipsoid to ovoid, 15–28 × 6–13 µm

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Figure 9.11

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Biotrophic infection of eucalypt leaf by Plectosphaera eucalypti, showing: A) embedded pseudothecium with pseudoclypeus, B) ascus, paraphysis and ascus tips, and C) mature ascospores. (From Swart, H.J., 1981, Transactions of the British Mycological Society 76, 89–95, with permission).

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A species identified as ‘Plectosphaera eucalypti Theiss.’ was reported as the main endophytic species colonising seedlings, shoot stems, mature leaves and, to a lesser extent, xylem of E. globulus in Uruguay (Bettucci and Saravay 1993). The fungus occurred in 40% of xylem pieces, 97% of complete stem pieces and in 35% of seedling stem pieces tested from one-year-old to two-year-old shoots of sprouting stumps and seedlings, forming sporocarps only on plant tissues. The relationship of this fungus to Plectosphaera eucalypti (Cooke & Massee) H.J.Swart remains to be determined. A morphologically similar pyrenomycete, Clypeophysalospora latitans (Sacc.) H.J.Swart [syn. Physalospora latitans Sacc., Amerostege latitans (Sacc.) Theiss., Laestadia eucalypti Speg., Physosporella eucalypti (Speg.) Höhn., Phyllachora eucalypti (Speg.) Petr., Laestadia eucalypti Rolland, Laestadia rollandii Sacc. & P.Syd., Physalospora eucalypti (Rolland) Schrantz; Swart 1981a] occurs widely on eucalypts (see Narendra and Rao 1977; Swart 1981a, 1981b; Crous et al. 1990), including nursery stock (see Chapter 8). The fungus was reported from E. globulus and E. obliqua in Victoria and from an unidentified eucalypt in South Australia (Hansford 1956; Chambers 1982; Cook and Dubé 1989). It is differentiated from Plectosphaera eucalypti by the formation of ascocarps with a definite melanised clypeus (Fig. 9.12), the uniseriate arrangement in asci of one-celled ascospores and by the presence of an amyloid apical ring and pulvillus on the tip of the ascus (Table 9.4) (Swart 1981a). Clypeophysalospora latitans is common on fallen eucalypt leaves in Australia and South Africa (Crous et al. 1990) and although recorded as a saprophyte by Swart (1981a), has been reported as parasitic in California where it caused premature defoliation (Hedgecock 1926), in India where it caused sharp, black spots one to 2.5 millimetres in diameter leading to leaf shrivelling and defoliation of C. citriodora (Mittal and Sharma 1979) and leaf blight of E. globulus (Narendra and Rao 1977) and in Portugal and Brazil where it attacked leaves and twigs, causing dieback (Spaulding 1958). There is evidence that Idiocercus australis may be an anamorph of Clypeophysalospora latitans, since both have been found in close association in Australia (Swart 1988).

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Rehmiodothis species

Rehmiodothis inaequalis (Cooke) H.J.Swart [syn. Dothidella inaequalis Cooke, Placostroma inaequalis (Cooke) Theiss. & Syd.; Swart 1987] is a typical ‘tar spot’ fungus, forming flattened dome-shaped glossy black stromata, with ascocarp ostioles emerging through the leaf surface as slightly protruding gelatinous structures (Table 9.4) (Swart 1987). The stromata originate in or beneath the epidermis, become heavily melanised and contain a few ascocarps with oblique necks. Haustoria originate from vegetative hyphae growing between palisade cells. A second species, Rehmiodothis eucalypti (Cooke & Massee) H.J.Swart (syn. Montagnella eucalypti Cooke & Massee), is differentiated from Rehmiodothis inaequalis by its smaller stromata, smaller and more crowded ascocarps within the stromata and larger ascospores. Both species are rare (Swart 1987).

9.4.10 Stigmina species Four species of Stigmina occur in association with brown, partly superficial and partly internal, spreading ‘greasy spot’ colonies on eucalypt leaves. These pathogens are characterised by a dark smudged appearance on the leaf surface because of the dark sporodochial conidiomata that emerge through the stomata and the production of masses of dark, thick-walled conidia in a gelatinous matrix. Stigmina eucalypticola B.Sutton & Pascoe (syn. Peltosoma eucalypti Hansf.) was reported from a mallee eucalypt in South Australia (Hansford 1956; Sutton and Pascoe 1989a). Verruculose brown hyphae grow superficially and are tightly appressed to the leaf surface, following the depressions of the cuticle and forming a reticulate mesh of hyphae (see Table 9.7). Dark plugs of pseudoparenchyma fill the stomatal pores and are attached to hyaline hyphae that penetrate into the mesophyll tissue. The stomatal plugs give rise to suprastomatal masses of dark brown, loose, gelatinous, pseudoparenchyma on which the superficial conidiomata develop. Mature conidiomata are sporodochium-like, giving rise to conidia with one to many distosepta (Sutton and Pascoe 1989a). Stigmina eucalypti Alcorn is readily distinguished from Stigmina eucalypticola by its larger conidia (see Table 9.7). Stigmina hansfordii B.Sutton & Pascoe forms similar infections to Stigmina eucalypticola, also on a mallee eucalypt (Sutton and Pascoe 1989a). A fourth

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Figure 9.12

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Biotrophic infection of eucalypt leaf by Clypeophysalospora latitans, showing: A) embedded perithecium with black clypeus, B) detail of ostiole and perithecium wall, C) asci and ascospores, and D) ascus tip. (From Swart, H.J., 1981, Transactions of the British Mycological Society 76, 89–95, with permission).

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species, Stigmina robbenensis Crous, C.L.Lennox & B.Sutton, was described from lesions on a eucalypt growing on Robben Island, South Africa (Crous et al. 1995c), but has not been reported from mainland South Africa (Crous 1998).

9.5 Powdery mildews ( Oidium species) Powdery mildews occur on eucalypts growing in glasshouses and nurseries in many countries but are rarely seen in the field (see Chapter 8). They are particularly prevalent on young seedlings and on species from drier regions growing in glasshouses or in wetter regions (Glasscock and Rosser 1958). Marks (1981) recorded an Oidium sp. on E. crenulata and E. cypellocarpa and noted that the fungus was common on nursery-grown eucalypts, causing leaf distortion and poor growth. In southern India, powdery mildew causes distortion, necrosis and ultimately leaf fall on eucalypt hybrid seedlings and has been controlled by spraying with a sulphur fungicide (Sehgal et al. 1975). Blum et al. (1991) reported high susceptibility of E. tereticornis and provenances of E. pellita and E. urophylla to an isolate of Oidium sp. from E. tereticornis and demonstrated resistance to the same isolate in provenances of E. cloeziana, E. microcorys and E. pilularis. The identification of powdery mildews on eucalypts has been hampered by the absence of the teleomorph stage. In recent taxonomic studies, more emphasis has been placed on morphological features of the anamorph and further confirmation has come from cross inoculations (see Chapter 8). Using this approach, Boesewinkel (1981) concluded that three species of powdery mildew are present on eucalypts in nurseries in New Zealand. Erysiphe polyphaga Hammarl. (a species similar to Erysiphe cichoracearum DC.) was found on E. crebra and E. moluccana; Sphaerotheca aphanis (Wallr.) U.Braun [as Sphaerotheca alchemillae (Grev.) L.Junell] was found on E. albens, E. crebra, E. paniculata and E. tereticornis; and Sphaerotheca pannosa (Wallr.:Fr.) Lév. was found on E. albens, E. moluccana and E. tereticornis. Boesewinkel (1981) demonstrated the synonymy of Oidium eucalypti Rostr., commonly recorded from eucalypts in various parts of the world, with Sphaerotheca pannosa. These fungi are well known on other plants (e.g. Erysiphe polyphaga on cucumber and tobacco,

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Sphaerotheca alchemillae on strawberries and Sphaerotheca pannosa on rose) and it is likely that they have transferred recently to eucalypts from other hosts. Gibson (1975) reported the susceptibility of E. globulus to Sphaerotheca pannosa. Other powdery mildews recorded on eucalypts are Erysiphe cichoracearum, Erysiphe orontii Castagne emen. U.Braun, Erysiphe paniculata ? (identity uncertain), Sphaerotheca fuliginea (Schltdl.:Fr.) Pollacci and Sphaerotheca macularis (Wallr.:Fr.) Lind.

9.6 Eucalypt rust ( Puccinia psidii ) Although no rust fungus has been described from eucalypts in their area of origin, several have been recorded on the genera in regions to which they have been introduced. Melampsora eucalypti Rabenh. was reported from E. globulus leaves in India but the identity of this species is unconfirmed and it was never described validly (Rabenhorst 1881). A species of Melampsora was reported on C. citriodora in India (Upadhyay and Bordoloi 1975) but this report remains unconfirmed (Coutinho et al. 1998). Additional collections of a Melampsora species from a eucalypt in India were made in 1984 and are lodged at the International Mycological Institute, UK. The status of these reports remains to be determined but it appears that they relate to occasional infections rather than to the development of a damaging new-encounter disease, as occurred with infection of eucalypts in South America by Puccinia psidii G.Winter (guava rust), a neotropical rust of several myrtaceous genera including guava (Psidium guajava L.). This rust is now an important shoot and leaf pathogen of eucalypts in Central and South America and the Caribbean. The disease was reviewed in detail by Coutinho et al. (1998). Puccinia psidii was originally described by Winter (1884) from leaves of a Psidium species in Brazil and was first positively identified on eucalypts by Joffily (1944), although there are reports from 1912 of its occurrence on C. citriodora (Coutinho et al. 1998). Except for one report in Taiwan of a rust with urediniospores identical to those of Puccinia psidii, but which has since disappeared (Wang 1992), Puccinia psidii has not been reported from eucalypts outside the Central and South American region (Coutinho et al. 1998). It is a major quarantine concern for other regions, particularly Australia where it could cause enormous damage to eucalypts in native communities.

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The host range of Puccinia psidii includes many genera in the family Myrtaceae in addition to Corymbia, Eucalyptus and Psidium (Viégas 1961; Hennen et al. 1982). Joffily (1944) reported that the rust was common on species of Myrtaceae in several regions of Brazil and that it damaged seedlings of C. citriodora to the extent that they were unsuitable for planting. The rust is known to infect 14 eucalypt species (Coutinho et al. 1998). The disease was not considered important in Brazil until 1973, when more than 400,000 infected seedlings of E. grandis had to be discarded in the province of Espirito Santo (Ferreira 1981, 1983, 1989). Extensive losses of E. grandis have occurred in Minais Gerais (Dianese et al. 1984; Ferreira 1989). From 1974 to 1980, sporadic but severe epidemics occurred on plants less than two years old in nurseries and commercial plantations. In one epidemic, more than 300 hectares of six-month-old seedlings of E. grandis were killed. The disease remained important between 1980 and 1989, affecting young plantations or the buds of older susceptible eucalypts (Ferreira 1989). Rust is most common on eucalypts up to two years old (Ferreira 1981, 1983) and infection is limited to periods when young susceptible host tissue is present. Leaves are susceptible up to the age of 15 days, after which they become resistant (Ruiz 1988). Older leaves are resistant in the field and could not be infected artificially (Ferreira 1989). The first symptoms of disease are pale yellow flecks followed by development of yellow uredinia on the leaf buds (Plates 9.14 and 9.15). In the field, uredinia are formed on leaves, petioles and young stems and are scattered on both leaf surfaces in groups on discoloured spots up to five millimetres in diameter which may coalesce (Plate 9.16). Young leaves often become distorted (Plates 9.17 and 9.18) and blighting of young stems can follow, resulting in the destruction of shoots two to six months after transplanting (Plate 9.18). Seedlings infected in this way suffer reduced growth and do not compete with healthy plants. One to two weeks after emergence, uredinia lose the characteristic yellow colouration and develop a warty, steel-coloured appearance, making diagnosis more difficult (Ferreira 1989). The rust is macrocyclic and autoecious, although the spermatial state has not been found (Ferreira 1989; Coutinho et al. 1998). Urediniospores (10–20 × 15–25 µm) are ellipsoid to obovoid with a finely echinulate wall, a truncate base and no visible

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germ pores (Fig. 9.13). Urediniospores germinate optimally when in contact with free water in the dark at temperatures from 15°C to 25°C (Ferreira 1989). Germ tubes form an appressorium and penetration of leaves occurs directly through the cuticle and epidermis, often at the junction of two epidermal cells (Hunt 1968). Following penetration of susceptible species, hyphae grow intercellularly in the mesophyll tissue and form haustorial mother cells which give rise to lobe-shaped haustoria within the cells. The two-celled teliospores (30–60 × 15–28 µm) develop in the same pustules as urediniospores or in separate telia and are dark brown (pale fawn in mass) with fragile pedicels which often become detached (Fig. 9.13) (Laundon and Waterston 1965). Teliospores have no dormancy and germinate on water agar, forming basidiospores that germinate while still attached to the metabasidium (J.C. Dianese, pers. comm.). Teliospores and basidiospores are rarely formed on eucalypts in the field (Ferreira 1983), although teliospores have been reported on E. cloeziana during warmer months (Ruiz 1988). However, they are frequently found on Syzygium jambos (L.) Alston. Basidiospores infect only Syzygium jambos; aeciospores, morphologically identical to urediniospores, have been reported only on this species (Coutinho et al. 1998). Primary inoculum is believed to come from native vegetation surrounding eucalypt plantations and the rust spreads within plantations via rain splash, insects and wind (Ferreira 1983). The latent period can be as short as five days, which allows the disease to spread and increase rapidly (Ferreira 1989). Infection occurred in less than 12 hours at 17°C to 25°C (De Castro 1983). Temperatures near 20°C are optimal for infection and sporulation and field conditions from April to August in south-west Brazil are considered favourable for the disease (Ferreira 1989). In field trials, susceptibility to Puccinia psidii was found to vary between and within eucalypt species, with C. citriodora, E. cloeziana and E. grandis being the most susceptible species and E. microcorys, E. pellita and E. saligna the most resistant (Dianese et al. 1984; Ferreira 1989). Rust infection suppressed the growth of some susceptible provenances, leading to the recommendation that planting of the most susceptible provenances be avoided in areas prone to the disease. After severe rust attack in field trials it has been possible to select individual trees with

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whereas Puccinia psidii infects stems as well as leaves. As with the Indian occurrences, this appears to be a chance infection as the fungus has apparently now disappeared from the plantations (Coutinho et al. 1998).

9.7 Angular, vein-limited leaf spots

Figure 9.13

Teliospores (T) and urediniospores (U) of Puccinia psidii. Note pedicels have become detached from some teliospores. Photograph courtesy of F.A. Ferreira.

Several common genera of eucalypt leaf pathogens cause leaf spots that are typically limited by veins, at least in part, giving them an angular appearance, although this symptom is variable.

9.7.1 useful levels of resistance for clonal propagation (Ferreira 1989). Two provenances found to be susceptible or moderately susceptible in one trial were classed as resistant in a study conducted in a neighbouring state (Dianese et al. 1986), possibly reflecting pathogenic differences between rust populations at the two sites. There is evidence of host specialisation within Puccinia psidii, with isolates from one host genus not necessarily infecting other genera within the accepted host range of the species (Coutinho et al. 1998). Urediniospores germinate on both resistant and susceptible species and on young as well as mature leaves. However, on mature leaves germination is retarded and the proportion of spores forming appressoria is reduced compared with young leaves (Coutinho et al. 1998). Hypersensitive cell death occurs following penetration of resistant genotypes. Several fungicides have provided successful control of the rust on eucalypt seedlings (Ruiz et al. 1987). Another rust species on eucalypt leaves was detected in South Africa (Knipscheer and Crous 1990). This rust was confined to the colder areas of Natal Province, where it was found on plants from one seedlot of E. nitens and on E. saligna growing nearby. Pale yellow, distinctly raised pustules occurred mainly on the lower leaf surface on angular, dark brown necrotic areas (Knipscheer and Crous 1990; Crous and Wingfield 1991). Inoculations with urediniospores were unsuccessful and as no teliospore stage was found, the identity of this rust remains uncertain. However, its rather dull yellow urediniospores were distinguishable from the bright yellow urediniospores of Puccinia psidii and the South African rust occurred only on leaves

Harknessia species

About 12 species of the coelomycete genus Harknessia are known from eucalypt leaves (Sutton 1971a, 1975, 1980; Nag Raj and di Cosmo 1981; Galán et al. 1986; Sutton and Pascoe 1989b; Crous et al. 1993d) and although many were collected from dead leaves, at least seven were recorded on leaf spots. Gibson (1975) described four species [Harknessia hawaiiensis F.Stevens & E.Young, Harknessia globosa B.Sutton, Harknessia insueta B.Sutton and Harknessia uromycoides (Speg.) Speg.] as causing leaf spots and one (Harknessia eucalypti Cooke) as causing leaf and shoot necrosis (Table 9.5). Most reports make little reference to disease symptoms, but the review of eucalypt diseases in Spain by Ruperez and Muñoz (1980) clearly illustrates vein-limited leaf spots caused by Harknessia eucalypti. The fungi form separate, immersed, globose pycnidia and brown, smooth, thick-walled, unicellular conidia of variable shape with a distinct basal frill or stalklike appendage formed from the persistent apical part of the conidiogenous cell (Table 9.5) (Sutton 1971a, 1980). The pycnidia erupt through the leaf surface and become somewhat acervular as they open widely and exude black masses of conidia onto the lesion surface. Harknessia uromycoides was reported from leaves, twigs and fruits of eucalypts in California, Spain, Argentina and Australia (Bonar 1928) and is one of the more common Harknessia species on eucalypts (Sutton and Pascoe 1989b) (Fig. 9.14). Harknessia eucalypti has been reported from the USA, New Zealand and Australia (Sutton 1980) and from Italy (Nag Raj and di Cosmo 1981). The conidia of this species are similar in size and shape (with an

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Figure 9.14

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Thick-walled conidia of Harknessia uromycoides. (From Sutton, B.C. and Pascoe, I.G., 1989, Mycological Research 92, 431–439, with permission).

acute apex) to those of Harknessia uromycoides but differ in having a much shorter appendage (Table 9.5) (Sutton and Pascoe 1989b). Both species were recorded also on leaves of Banksia and Lambertia species in Australia (Sutton and Pascoe 1989b). Harknessia eucalyptorum Crous, M.J.Wingf. & Nag Raj is commonly associated with a leaf and peduncle necrosis of various Eucalyptus species in South Africa (Crous et al. 1993d). On E. viminalis, lesions occur mainly on the leaf margins. Harknessia hawaiiensis is considered an important pathogen of eucalypts in South Africa and inoculations have shown it to be pathogenic on a wide range of Eucalyptus species (P.W. Crous, unpubl. data). This species was reported on irregular lesions up to 10 millimetres in diameter with raised reddish-brown

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margins on E. obliqua in Tasmania (Yuan 1999) and as a common endophyte of mature leaves of E. globulus in Uruguay (Bettucci and Saravay 1993). Harknessia fumaginea B.Sutton & Alcorn was associated with a tip blight of young lateral shoots of eucalypts in Australia and was reported from dead leaf tips of Eucalyptus in leaf litter in Brazil (Sutton 1975). Harknessia victoriae B.Sutton & Pascoe, which resembles Harknessia globosa, was described from dead leaves of E. tetraptera in Victoria (Sutton and Pascoe 1989b) and from large, irregular lesions on the margins of senescent leaves in the lower crown of E. nitens in Tasmania (Yuan 1999). Harknessia tasmaniensis Z.Q.Yuan, Wardlaw & C.Mohammed was described from large, irregular lesions occurring mainly at the leaf tips in

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E. globulus and E. nitens plantations in Tasmania (Yuan 1999). Although Harknessia species are common on eucalypts, there is little information on their pathogenicity.

9.7.2

Lecanostictopsis eucalypti

Lecanostictopsis eucalypti Crous was described from small, elongate, vein-limited leaf spots from a species of Eucalyptus in India (Crous 1998). The genus includes several species on leaves of the myrtaceous genus Syzygium (Crous 1998) and it is likely that the species is another example of a pathogen of a myrtaceous species that has the ability to parasitise Eucalyptus.

9.7.3

Phaeophleospora species

Several species now placed in the genus Phaeophleospora (syn. Kirramyces, Phaeoseptoria) may form substomatal pycnidia, reddish discolourations or sooty blotches on otherwise healthy leaves (Walker 1962) or may cause characteristically angular leaf spots (Heather 1965). Phaeophleospora epicoccoides has been destructive in Australia and South Africa and Phaeophleospora eucalypti is common in Australia and New Zealand. 9.7.3.1

Phaeophleospora epicoccoides

Phaeophleospora epicoccoides (Cooke & Massee) Crous, F.A.Ferreira & B.Sutton [syn. Kirramyces epicoccoides (Cooke & Massee) J.Walker, B.Sutton & Pascoe, Cercospora epicoccoides Cooke & Massee, Hendersonia grandispora, Phaeoseptoria eucalypti, Phaeoseptoria luzonensis Tak.Kobay.; Walker et al. 1992; Crous et al. 1997] (teleomorph: M. suttoniae; Crous and Wingfield 1997b) causes lesions delimited by veins (Heather 1965) or small angular, purplish-red spots (Plate 9.19), depending on host species and stage of development of infection (Walker 1962) (Table 9.5). Occasionally, infections appear as irregular, deep purple blotches up to seven millimetres across (Dick 1982). On E. camaldulensis in Vietnam, the lesions are reddish or purple or somewhat chlorotic irregular areas up to about seven millimetres in diameter, with minute black pycnidia evident on the underside in the centre of infected areas (Old et al. 1999a). Pycnidia are formed under stomata (Fig. 9.15) and exude grey-brown to black cirri of conidia, which may appear as hair-like extrusions on the leaf (Old et al. 1999a) or spread over the leaf surface, giving the appearance of a brownish-black woolly mass or

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sooty mould (Walker et al. 1992). Sometimes the top of the pycnidium is ruptured by the pycnidial ooze, resulting in an open, cup-shaped or acervular structure, which may add to the sooty appearance of the infection. The disease is more apparent on mature leaves, which are prematurely shed when heavily infected. In a prolonged epidemic, infection may spread through the canopy on to younger leaves. Phaeophleospora epicoccoides was first described by Cooke (1891) from leaves collected in Victoria and is now regarded as one of the most common and widespread leaf diseases of eucalypts. It caused severe damage to nursery seedlings of several species (C. maculata, E. macarthurii, E. sideroxylon) as well as leaf spots on E. saligna in the field (Walker 1962). The disease is serious in South Africa, where it is one of the three most common leaf pathogens of eucalypts and has caused seedling mortality and complete defoliation of mature trees in plantations (Knipscheer et al. 1990; Nichol et al. 1992a, 1992b). It occurs on eucalypts in many countries, including India (Padaganur and Hiremath 1973), Malawi (Chipompha 1987), Brazil (Ferreira 1989), Italy (Belisario 1993), Chile, Portugal and Taiwan (P.W. Crous and M.J. Wingfield, unpubl. data), New Zealand (Dick 1982) and Vietnam (Sharma 1994; Old et al. 1999a). The teleomorph is much rarer, having been described only from a Eucalyptus species from North Sumatra, Indonesia and from E. grandis from Brisbane, Australia (Crous and Wingfield 1997b; Crous 1998). Phaeophleospora epicoccoides was one of the first foliar pathogens of eucalypts to be studied in detail (Heather 1965, 1967a, 1967b). The disease was readily induced by inoculating seedlings with a conidial suspension and exposing them to high humidity for 48 hours (Heather 1967a). Conidia usually formed two germ tubes from the terminal cells which grew and branched randomly on the leaf surface and formed appressoria over stomatal pores (Heather 1965). After 14 days, extensive intercellular growth of hyphae had occurred and by 17 days cushions of mycelium had formed in substomatal cavities throughout the infected area. Chlorotic spots delimited by veins were visible after 26 days and by 30 days aggregations of hyphae in substomatal cavities had developed into pycnidia. The pathogen has a substantial biotrophic phase prior to development of necrosis of leaf tissue. Spores exuded

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Figure 9.15

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Cross section of leaf showing pycnidia, conidia and conidiophores of Phaeophleospora epicoccoides. (From Swart, H.J. and Walker, J., 1992, Transactions of the British Mycological Society 90, 633–641, with permission).

through the stomatal pore are splash dispersed. Necrosis of 25% to 30% of the total area of a leaf usually results in leaf abscission. Heather (1965) considered that this should break the disease cycle in a mature forest in which there are few regenerating seedlings with leaves close to the inoculum source on fallen leaves. Physiologically older leaves in the lower crown were more susceptible than younger

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leaves of E. globulus ssp. bicostata seedlings (Heather 1967a). In most situations, the disease appears to be confined to species of the subgenus Symphyomyrtus (Walker et al. 1992). In the field in South Africa, it was recorded on 14 species and 7 interspecific hybrids, all from the subgenus Symphyomyrtus (Crous et al.

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1989a). In four eucalypt species trials in Natal, South Africa, all susceptible species belonged to Symphyomyrtus whereas all Monocalyptus species were resistant (Nichol et al. 1992a). It was very common on E. saligna (Symphyomyrtus) in native forest on the north coast of New South Wales but was not reported from the associated Monocalyptus species, E. pilularis (Heather 1965). Within the subgenus Symphyomyrtus, species with non-glaucous foliage are most severely diseased; infection of glaucous species such as E. globulus ssp. bicostata occurs rarely in the field (Heather 1965) and removal of the waxy coating of the juvenile leaves greatly increased their susceptibility (Heather 1967a). Orientation of the leaf lamina and hydrophobicity of leaves were shown to be important in determining the amount of spore deposition on leaves and hence disease severity (Heather 1967b). Leaf glaucousness also confers a degree of resistance because of the presence of an inhibitor of spore germination in the waxy coat (Heather 1967b) and leaves of some species contain water-soluble promoters as well as inhibitors of spore germination (Heather 1965). Nichol et al. (1992a) developed a rating system to assess severity of infection on trees and showed that there is scope for selection of resistant species of Eucalyptus. The most susceptible species were E. camaldulensis, E. grandis, E. saligna and E. tereticornis; several other Symphyomyrtus species and all tested Monocalyptus species were resistant. Eucalyptus tereticornis and E. camaldulensis were also very susceptible in Malawi (Chipompha 1987). A clone derived from the hybrid progeny of E. grandis and E. nitens sustained little infection by this fungus and other leaf pathogens (Crous et al. 1989c). Site preparation and fertilisation had a significant effect on disease severity in trials in South Africa, with severity being reduced in treatments that decreased nutrient and water stress in the trees (Nichol et al. 1992b). The disease has been controlled on eucalypt seedlings by foliar applications of dithiocarbamate fungicides (Jamaluddin et al. 1985; Chipompha 1987; Harsh et al. 1987). 9.7.3.2

Phaeophleospora eucalypti

A biotrophic infection that develops into an irregular leaf spot is caused by Phaeophleospora eucalypti (Cooke & Massee) Crous, F.A.Ferreira & B.Sutton [syn. Kirramyces eucalypti, Cercospora eucalypti

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Cooke & Massee, Pseudocercospora eucalypti (Cooke & Massee) Y.L.Guo & X.J.Liu, Septoria normae Heather nom. inval., Septoria pulcherrima Gadgil & M.Dick, Stagonospora pulcherrima (Gadgil & M.Dick) H.J.Swart; Walker et al. 1992; Crous et al. 1997]. This species differs from Phaeophleospora epicoccoides in having more finely roughened, paler and more delicate conidia and conidiogenous structures (Walker et al. 1992) (Table 9.5). In an early study, it was found to occur extensively on E. dalrympleana and E. viminalis in New South Wales (Heather 1961). Up to 90% of the leaf area became blotchy, especially on E. dalrympleana, but the disease did not occur on E. rubida growing in the same locality. Thirteen species from the subgenus Symphyomyrtus are susceptible to Phaeophleospora eucalypti in Australia and New Zealand. These include E. cephalocarpa, E. cypellocarpa, E. dalrympleana, E. globulus, E. gunnii, E. nitens, E. ovata and E. viminalis. Inoculations of several Symphyomyrtus and species from other subgenera, including E. blakelyi, E. camaldulensis, E. globulus and E. microcorys, were unsuccessful. While it is a serious pathogen, it is less common than Phaeophleospora epicoccoides in mainland Australia, but it was one of the three most common foliar pathogens in young E. globulus and E. nitens plantations in Tasmania (Yuan 1999). In New Zealand, the disease is associated with serious damage, particularly on E. nitens which can be completely defoliated (Dick 1982; Gadgil and Dick 1983). Phaeophleospora eucalypti mostly infects young leaves (Heather 1961) and symptoms first appear in spring as a slight paling of new leaves. Host tissue remains alive for a long time after infection, which becomes visible first as a pale yellow blotch that turns a distinctive carmine red before eventually becoming brown (Dick 1982). Radioactive carbon label has been shown to accumulate in the infected areas to a higher level than in surrounding, uninfected tissue (Burdon and Chilvers 1974a). Lesions are often delimited by large veins, but may coalesce to cover most of the lamina, resulting in shedding of leaves. Necrotic regions with carmine margins slowly develop over two to three months. Black, globose pycnidia of the fungus are produced on both leaf surfaces (Table 9.5) at all stages of disease development, being formed just below the

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epidermis with the ostiole below a stomatal pore and causing little disruption of the epidermis.

is distinctive in having slightly longer and thinner, curved conidia (Table 9.5).

Disease was induced by inoculating seedlings in spring with spore suspensions prepared from cultures and covering them with plastic bags for from one to six days (Heather 1961). Spores germinated on leaves within 36 hours and germ tubes formed infection pegs which penetrated stomatal pores within six to eight days of inoculation. Germ tubes branched and each branch was able to form an infection peg. Hyphae ramified intercellularly through the spongy mesophyll but were often restricted by larger veins. Host cells collapsed in small areas near the site of penetration 18 to 25 days after inoculation and symptoms developed three to five weeks after inoculation, depending on environmental conditions. As with Phaeophleospora epicoccoides, biotrophic infection occurred before the collapse of leaf tissue.

9.7.4

9.7.3.3

Phaeophleospora lilianiae

Walker et al. (1992) examined several other collections of pale-spored fungi resembling Phaeophleospora eucalypti and concluded that further collections and work were needed to fully resolve the identities of these fungi. A third species, Phaeophleospora lilianiae (J.Walker, B.Sutton & Pascoe) Crous, F.A.Ferreira & B.Sutton (syn. Kirramyces lilianiae J.Walker, B.Sutton & Pascoe), is known only from two collections on C. eximia in New South Wales (Walker et al. 1992). This species is closely related to Phaeophleospora epicoccoides, having brown, rough-walled conidia and conidiogenous cells, but its conidia are shorter and one-septate to three-septate (Table 9.5). 9.7.3.4

Phaeophleospora destructans

A fourth species, Phaeophleospora destructans (M.J.Wingf. & Crous) Crous, F.A.Ferreira & B.Sutton (syn. Kirramyces destructans M.J.Wingf. & Crous), was described from irregular to subcircular leaf spots 10 to 20 millimetres in diameter and large blighting lesions on one-year-old to three-year-old E. grandis in North Sumatra, Indonesia (Wingfield et al. 1996). It is an aggressive pathogen that causes distortion of infected leaves and blighting of young leaves, buds and shoots. Spermogonia have been observed on some lesions, although a teleomorph has not been found (Crous 1998). It is similar to Phaeophleospora eucalypti, but

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Pseudocercospora and Cercospora species

Although many leaf-infecting fungi of eucalypts have been placed in the genus Cercospora, very few are now regarded as true cercosporas. The type specimens of Cercospora eucalypti and Cercospora epicoccoides are Coelomycetes rather than Hyphomycetes (Crous et al. 1989e; Walker et al. 1992); they were initially accommodated in the genus Kirramyces (Walker et al. 1992) and are now placed in the genus Phaeophleospora (Crous 1998) (see section 9.7.3). Many other collections lodged in herbaria as Cercospora eucalypti and Cercospora epicoccoides are better placed in the genus Pseudocercospora (Table 9.3) rather than Cercospora because of the presence of non-thickened scars on their conidiogenous cells and the dark pigmentation of their conidia (Crous et al. 1989e). Pseudocercospora species typically form angular, vein-limited lesions on eucalypt leaves. Recently a true Cercospora species (Cercospora eucalyptorum Crous) (see Table 9.7) was described from a lesion in association with a Pseudocercospora species (Crous 1998). Pseudocercospora eucalyptorum Crous, M.J.Wingf., Marasas & B.Sutton (syn. Pseudocercospora eucalypti Goh & W.H.Hsieh) was described by Crous et al. (1989e) from small, subcircular to angular, vein-limited spots on leaves of several eucalypt species in South Africa. Fascicles of conidiophores emerge through stomata (Crous et al. 1989e) (Fig. 9.16), but larger sporodochial masses of conidiophores also erupt through the leaf surface (Table 9.3) (Beilharz 1994). The pathogen is potentially damaging in plantations of E. nitens (Crous et al. 1989e). Older leaves at the base of the crown tend to be more heavily infected. Although Crous et al. (1989e) suggested that Pseudocercospora eucalyptorum has a very wide distribution in Africa, Asia, Europe, South America and Australasia, it was not found in a study (Beilharz 1994) of Australian collections, including those cited by Crous et al. (1989e), which differ significantly from the type of Pseudocercospora eucalyptorum; rather, as many as six undescribed species were represented. An undescribed species of Pseudocercospora was described from tiny

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Figure 9.16

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Conidia and conidiophores of Pseudocercospora eucalyptorum. (From Crous, P.W. et al., 1989, Mycological Research 93, 394–398, with permission).

(1–4 mm diameter), angular to subcircular, vein-limited lesions on E. nitens in Tasmania (Yuan 1999). All Australian collections of the genus on eucalypt leaves are characterised by their association with angular, vein-limited lesions (V. Beilharz, pers. comm.). A fungus tentatively identified as Pseudocercospora eucalyptorum was recorded commonly in surveys of foliar diseases of E. camaldulensis in Vietnam (Old and Yuan 1994; Old et al. 1999a; Thu et al.

1999) and was the most common pathogen in the first year of a large provenance trial in south Vietnam (Dudzinski et al. 1999) (Plate 9.20). On these trees the pathogen caused small to large (up to 2 cm) irregular lesions, often with reddish or chlorotic margins and central areas that appeared dark because of the presence of darkly pigmented fascicles of conidiophores and many dark spores. In Italy, a similar fungus was identified from 45 eucalypt species, the most seriously affected

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including E. botryoides, E. camaldulensis and E. globulus (Magnani 1965). This fungus is probably Pseudocercospora eucalyptorum (Crous 1998). A fungus identified as Cercospora eucalypti was recorded from small (2–8 mm diameter), light brown, angular, vein-limited lesions that were widespread in plantations and nurseries of E. delegatensis, E. fastigata, E. nitens and E. regnans in New Zealand (Dick 1982, 1990). A Cercospora species was identified as a common leaf pathogen in Zimbabwe (Masuka 1990). These fungi are likely to be species of Pseudocercospora, but more work is needed on this complex in Australia and elsewhere before the distribution of Pseudocercospora eucalyptorum and other Pseudocercospora species can be determined (V. Beilharz, pers. comm.). Many species of Pseudocercospora occur on exotic eucalypts in South Africa, South America and Indonesia (Table 9.3). Most cause angular, vein-limited leaf spots of minor importance. Several are the anamorphs of Mycosphaerella species and some are associated with spermogonia on lesions. Pseudocercospora natalensis Crous & T.A.Cout. was described from a severe outbreak of small, subcircular to angular lesions on leaves of E. nitens in South Africa (Crous 1998). The leaf spotting was more serious than that usually caused by Pseudocercospora eucalyptorum and close examination showed that some lesions were caused by Pseudocercospora eucalyptorum while others were caused by Pseudocercospora natalensis. Three other cercosporoid fungi have been described from eucalypt leaves. Mycovellosiella eucalypti Crous & Alfenas was described from small leaf spots on E. saligna in Brazil, Passalora morrisii Crous from small leaf spots on E. morrisii in Australia and Phaeoramularia eucalyptorum Crous (see Table 9.7) was described from specks or small spots on leaves of E. saligna in the Cameron Highlands of Malaysia (Crous 1998).

9.7.5

Sarcostroma and Vermisporium species

Swart (1982a, 1988) and Swart and Williamson (1983) described several species in the genera Seimatosporium and Vermisporium from small angular or larger more rounded leaf spots on various eucalypt species. In small, restricted infections, veins seem to limit the extent of necrosis, while in larger, less restricted infections, the influence of veins is less

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Figure 9.17

Conidia of Sarcostroma brevilatum. (From Swart, H.J., 1982, Transactions of the British Mycological Society 78, 265–269, with permission).

apparent. These fungi produce elongate three to four-celled conidia in acervuli that originate within the epidermis and break through the outer epidermal wall and cuticle, becoming visible as brown, blister-like eruptions in the centre of lesions (Swart 1988). The two genera were differentiated on the basis of their conidia, which in Vermisporium species were uniformly thin-walled with no distinct appendage on the apical cell and which appeared unpigmented under a microscope but were white, orange or pink in mass. Conidia of Seimatosporium species were thicker walled, particularly in the

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Foliar diseases of eucalypts caused by acervular and sporodochial Coelomycetes, listing recent generic synonyms, teleomorphs, symptoms and distinctive features of the pathogens

Pathogen anamorph [synonym] (teleomorph)

Disease symptoms

Distinctive features of the pathogen

Blastacervulus eucalypti

Small spot that develops only part way through leaf lamina

Acervuli formed in single stromatic layer beneath cuticle; acervuli rupture cuticle and form a powdery mass of globose to elliptical, bright brown, thick walled, verruculose, 1-celled conidia (4–5 × 6 µm)

Colletotrichum gloeosporioides

Light brown spots, usually Acervuli exuding yellow-orange or pink, with a purple margin; yellow to sticky mass of cylindrical, hyaline, 1-celled conidia, pink wet conidial masses 10–21 × 3–5 µm, with rounded ends breaking through the surface

Coma circularis (Ascocoma eucalypti)

Biotrophic parasite forming small unilocular or large multilocular subcuticular melanised stromata

Sporocarp locules fully exposed at maturity; conidia consisting of large elongate terminal cell (28–38 × 7–9 µm) with apical seta (up to 40 × 1 µm) and small basal cell (5–7 × 3–4 µm) with 3 divergent setae (40–50 × 1–1.5 µm); ascocarp apothecioid; ascospores 1-celled, hyaline, smooth with rounded ends, 25–32 × 7–9 µm

Coma circularis (Ascocoma eucalypti var. didymospora)

As for Coma circularis

Ascospores unevenly 2-celled

Fairmaniella leprosa

Small, raised, corky lesions similar to those of Aulographina eucalypti; may not extend right through lamina, or large spreading lesions, varying in size and outline with host

Dark acervuli lift and rupture the epidermis, forming a black acervular pustule of conidia; conidia 1-celled, pale brown, thick-walled with fine punctulate ornamentation, broadly elliptical to obclavate with an obtuse to truncate base, 5–9 × 3–5 µm

Lecanostictopsis eucalypti

Small, elongated, angular leaf spots, 2–20 × 2–8 µm, confined by veins

Conidiomata acervular, epidermal to subepidermal, erumpent, amphigenous; conidiophores dark brown, verruculose to tuberculate, with 1–3 percurrent proliferations; conidia brown, coarsely verruculose to tuberculate, 0–3 septate, cylindrical to fusiform, straight to curved, apex rounded, base truncate, 11–35 × 4–6 µm

Pestalotiopsis disseminata

Necrosis of leaf margin; or branch dieback

Acervuli dark, peridermal; conidia 18–23 × 4–5 µm, oozing out in black mass, 4-septate, three median cells dark brown, apical cell hyaline with three appendages (9–12 µm), basal cell hyaline with a single appendage (4–12 µm)

Phloeosporella eucalypticola

Small subcircular to irregular leaf spot up to 11 mm diameter with a dark brown margin

Acervuli subepidermal, hypogenous, rarely epigenous, separate, more or less cupulate; conidia hyaline, 2-celled, filiform, 74–82 × 2–2.5 µm, with apical cell tapering gradually to an obtuse tip and basal cell comprising about 40% of the length with a truncate base

Sarcostroma brevilatum [Seimatosporium brevilatum, Seimatosporium fusisporum]

Angular, vein-limited leaf spots Acervuli originating within the epidermis and with acervuli visible as breaking through the outer epidermal wall and ruptures of surface cuticle to form an irregular rupture in the centre of the lesion; conidia 4-celled, short fusiform, 13–21 × 5–7 µm, two median cells brown, thickwalled, together 8.5–14 µm long, and end cells paler with long, thin hyaline basal (6–16 µm long) and apical (7–18 µm long) appendages

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Foliar diseases of eucalypts caused by acervular and sporodochial Coelomycetes, listing recent generic synonyms, teleomorphs, symptoms and distinctive features of the pathogens (continued)

Pathogen anamorph [synonym] (teleomorph)

Disease symptoms

Distinctive features of the pathogen

Staninwardia breviuscula

Small circular lesions up to 5 mm diameter on leaves and elongated lesions on petioles and stems

Numerous strictly epiphyllous separate acervuli located mainly in epidermis; conidia pale brown, thick-walled, verruculose, 2-celled and often constricted at the median septum, doliiform to clavate, 7–10.5 × 3.5–5 µm, formed in chains of up to 3, intercalary conidia truncate at both ends with the remains of a basal frill, apical conidia truncate only at the base, each conidial chain enveloped in a mucilaginous sheath about 2 µm thick which persists on mature detached conidia

Stilbospora foliorum

Small leaf spots

Conidiomata arise as flattened, closed stromatic structures within the mesophyll and erupt through the epidermis to form an open acervulus with a single locule; young conidia have a gelatinous outer layer that disappears at maturity; mature conidia finely roughened, ellipsoid with a narrowly truncate base, 15–18 × 8–12 µm, with 3 septa which appear to be distosepta that grow thicker and darker with age, eventually giving the appearance of a banded conidium with the median septum forming the thickest band; some conidia become so dark that their inner structure is obliterated

Vermisporium acutum

Probably secondary invader, only on Monocalyptus; uncommon

Acervuli breaking through epidermis in centre of lesion; conidia 53–75 × 2–3 µm, hyaline, 4-celled with apical cell the longest, basal cell the shortest, tapering to sharp point at each end, with exogenous basal appendage 4–8 µm long; spermatia present

Vermisporium biseptatum

Angular, vein-limited leaf spots Acervuli breaking through epidermis in centre of on both Monocalyptus and lesion; conidia 40–70 × 1.5–2.5 µm, hyaline, 3-celled Symphyomyrtus species with central cell by far the shortest, apical cell with short conical tip, exogenous basal appendage 1–3 µm long

Vermisporium brevicentrum

Angular, vein-limited leaf spots Acervuli breaking through epidermis in centre of only on Symphyomyrtus lesion; conidia 46–70 × 2–3 µm, hyaline, 4-celled with species 2 central cells together shorter than end cells, exogenous basal appendage 2–3 µm long

Vermisporium cylindrosporum Angular, vein-limited leaf spots [Seimatosporium on E. behriana; ellipsoid to cylindrosporum] irregular lesions on margins or between veins, with redbrown raised margins, on E. globulus and E. nitens

Vermisporium eucalypti [Seimatosporium eucalypti, Cylindrosporium eucalypti]

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Rounded or angular, often vein-limited leaf spots on E. camaldulensis; similar with purple-brown margins and often at tips on E. nitens

Acervuli brown and blister-like, scattered over lesion, breaking through epidermis, mainly epiphyllous; conidia 30–57 × 3–4.5 µm, straight or slightly curved, longer and thinner than in Vermisporium falcatum, straw coloured, 4-celled, cells slightly longer towards tip, hyaline conical apical appendage up to 5 µm long (or cell attenuated), and conical exogenous basal appendage up to 9 µm long Acervuli brown and blister-like, breaking through epidermis in centre of lesion, sometimes predominanly epiphyllous; conidia 45–55 × 3.5–5 µm, straight or curved, very lightly pigmented, 4-celled, central cells similar and almost colourless, with apical cell tapering to a sharp point and basal cell with an appendage 3–8 µm long also tapering to a sharp point

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Vermisporium falcatum [Seimatosporium falcatum, Cryptostictis falcata]

Tiny angular vein-limited or larger rounded leaf spots, with distinctive dark brown or purple-brown margin, common on several species

Acervuli light-brown to brown and blister-like, breaking through epidermis, scattered over lesion; conidia 22–50 × 3–6 µm, falcate or sigmoid, lightly pigmented, smooth or finely verruculose, 4-celled, constricted at septa, acutely pointed apical appendage 3–22 µm, acutely pointed exogenous basal appendage 3–17 µm, appendages with gel coat when fresh; 2-celled microconidia present

Vermisporium obtusum

Small angular vein-limited or larger rounded leaf spots, with purple raised margins; only on Monocalyptus

Acervuli light brown and blister-like, breaking through epidermis in centre of lesion, in circles; conidia 50–80 × 2–3.5 µm, fusiform to subclindrical, hyaline, smooth, 4-celled, cells longer towards tip, apical cell the longest with blunt tip, exogenous blunt basal appendage 2–10 µm long; 1-celled microconidia present

Vermisporium orbiculare [Stagonospora orbicularis]

Angular leaf spots only on Monocalyptus

Acervuli breaking through epidermis in centre of lesion; conidia 53–59 × 3.5–4 µm, hyaline, 4-celled, apical cell the longest and tapering to conical point, exogenous pointed basal appendage 4–6 µm

Vermisporium samuelii [Seimatosporium samuelii]

Angular, vein-limited leaf spots Acervuli breaking through the outer epidermal wall and cuticle to form an irregular rupture in the centre of the lesion; conidia very long and thin, hyaline, 60–95 × 4–5 µm, with a small knob-like apical appendage and a short asymmetric basal appendage

Vermisporium verrucisporum

Angular leaf spots on E. regnans

Vermisporium walkeri

Angular, vein-limited leaf spots Acervuli breaking through epidermis in centre of lesion; conidia 42–74 × 2–3.5 µm, hyaline, 4-celled, two median cells equal, apical cell twice as long as central cells and tapering to a point, exogenous pointed basal appendage 3–10 µm long; spermatia present

Acervuli breaking through epidermis in centre of lesion; conidia 29–46 × 5–6.5 µm, 4-celled, verruculose, fusiform, falcate or sigmoid, with two median cells golden brown in colour

Sarcostroma brevilatum (H.J.Swart & D.A.Griffiths) Nag Raj (syn. Seimatosporium brevilatum H.J.Swart & D.A.Griffiths, Seimatosporium fusisporum H.J.Swart & D.A.Griffiths) has short, fusiform conidia on E. globulus and larger conidia on E. polyanthemos in Australia (Fig. 9.17) (Table 9.6) (Swart 1988). Vermisporium samuelii (Hansf.) J.A.Simpson & Grgur. [syn. Seimatosporium samuelii (Hansf.) J.Walker & H.J.Swart, Cylindrosporium samuelii Hansf.] has very long, thin, hyaline conidia (Hansford 1956) (Table 9.6).

falcatum (B.Sutton) Shoemaker] is relatively common on several eucalypt species. Conidia collected from a variety of host species were variable in size but could be distinguished by their overall morphology (Swart 1988) (Table 9.6). Vermisporium eucalypti (McAlpine) Nag Raj [syn. Cylindrosporium eucalypti McAlpine, Seimatosporium eucalypti (McAlpine) H.J.Swart] has been reported from E. camaldulensis in southern Australia (Swart 1982a) and from South Africa (Crous et al. 1990). Vermisporium cylindrosporum (H.J.Swart) Nag Raj (syn. Seimatosporium cylindrosporum H.J.Swart) was described from E. behriana in Australia (Fig. 9.18) (Swart 1982a). Nag Raj (1993) described Vermisporium verrucisporum Nag Raj from leaf spots on E. regnans.

Vermisporium falcatum (B.Sutton) Nag Raj [syn. Cryptostictis falcata B.Sutton, Seimatosporium

The six species of Vermisporium described by Swart and Williamson (1983) from necrotic leaf spots on a

central cells, with distinct apical and basal appendages. The Seimatosporium species described by Swart (1982a) were transferred to the genera Sarcostroma or Vermisporium by Nag Raj (1993).

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Vermisporium cylindrosporum showing acervulus breaking through epidermis, conidia and conidiogenous cells. (From Swart, H.J., 1982, Transactions of the British Mycological Society 78, 265–269, with permisssion).

wide range of eucalypt species in southern Victoria are differentiated by the number and relative sizes of cells in each conidium and by the shape of the apical cells (Table 9.6). Vermisporium biseptatum H.J.Swart & M.A.Will. has three-celled conidia (Fig. 9.19). The five other species have four-celled conidia; in two species (Vermisporium brevicentrum H.J.Swart & M.A.Will. and Vermisporium walkeri H.J.Swart & M.A.Will.) the central cells of the conidia are shorter than the apical and basal cells, while three species [Vermisporium acutum H.J.Swart & M.A.Will., Vermisporium obtusum H.J.Swart & M.A.Will. and Vermisporium orbiculare (Cooke) H.J.Swart & M.A.Will. (syn. Stagonospora orbicularis Cooke)] have central cells longer than the

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basal cell and are differentiated by the shape of the apical cell. Vermisporium walkeri is similar to Vermisporium samuelii but has much narrower conidia which lack an apical appendage and any trace of melanisation (Swart 1988). Vermisporium obtusum has been recorded from eucalypts in New Zealand (Dick 1990). Species of both Sarcostroma and Vermisporium grew but did not sporulate readily in culture (Swart 1982a, Swart and Williamson 1983), although Yuan (1999) obtained good sporulation of Vermisporium obtusum on 3% malt extract agar. These fungi are considered to be essentially necrotrophic pathogens of eucalypts, although

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Vermisporium biseptatum, showing: A) and B) acervulus and C) conidia and conidiogenous cells. (From Swart, H.J. and Williamson, M.A., 1983, Transactions of the British Mycological Society 81, 491–502, with permission).

pathogenicity tests have not been reported. Vermisporium acutum and Vermisporium orbiculare have been recorded as secondary invaders (Swart and Williamson 1983). In specimens from E. nitens in Tasmania, Vermisporium eucalypti was found growing with Trimmatostroma excentricum in one collection and Vermisporium falcatum was common on the older leaves in the lower canopy and on leaves infected by M. cryptica (Yuan 1999).

Four species (Vermisporium walkeri, Vermisporium acutum, Vermisporium orbiculare and Vermisporium obtusum) were recorded only on Monocalyptus species, Vermisporium brevicentrum was found only on Symphyomyrtus species and Vermisporium biseptatum was found on species in both subgenera. In Tasmania, Vermisporium cylindrosporum was found on E. globulus and E. nitens in plantations, Vermisporium eucalypti on E. nitens in plantations,

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Vermisporium falcatum on E. nitens in plantations and on E. obliqua, and Vermisporium obtusum was found only on E. obliqua growing within plantations of E. globulus and E. nitens and on E. obliqua in native forests (Yuan 1999).

9.8 White leaf and shoot blight ( Sporothrix pitereka ) A severe shoot and leaf blight disease of seedlings of the Corymbia species, C. eximia, C. ficifolia and C. maculata, is caused by the hyphomycete Sporothrix pitereka (J.Walker & Bertus) U.Braun (syn. Ramularia pitereka J.Walker & Bertus; Braun 1995). The disease was reported widely along the east coast of Australia, often causing severe damage to seedlings and young growth, or being associated with cankering on older trees (Bertus and Walker 1974). The fungus caused losses of over 50% of C. maculata seedlings in a nursery (see Chapter 8). Sporothrix pitereka was found only on seedlings over three months old and, if not controlled, often killed them. The disease was more common in spring and autumn and caused distortion and twisting of young shoots in association with stem lesions, leaf spots and blight (Walker and Bertus 1971). A species of Sporothrix also infects fruit capsules of Eucalyptus (see Chapter 7). In a species and provenance trial in northern New South Wales, all Corymbia but no Eucalyptus species were infected by Sporothrix pitereka, which caused dieback of leaders and shoots and proliferation of branches (Simpson et al. 1997). Only immature tissues were susceptible and infection occurred on new growth in spring each year and persisted through to winter. Repeated infection of new shoots caused a significant loss of height and stem form. It was predicted that successful planting of Corymbia species in the region will require development of methods for managing this disease. In Western Australia, a similar fungus occurs naturally on C. calophylla and causes cankers on cultivated adult trees of C. ficifolia (Cass Smith 1970). Although referred to as ‘Sporotrichum destructor Pittman nom. nud.’ (Macnish 1963), Walker and Bertus (1971) considered it to be Sporothrix pitereka or a very close relative. In Queensland, Sporothrix pitereka was associated with shoot death resulting in multiple shooting of young seedlings of C. maculata in plantations (B.N. Brown,

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pers. comm.). Subsequent infections of the new shoots resulted in multiple dieback and stunting of the trees. Distinctive necrotic areas develop on leaves and stems (Table 9.7). Sunken brown cankers on petioles and stems of C. ficifolia may be up to 15 millimetres long. Dense masses of white conidiophores rupture the cuticle, causing diseased shoots to appear shining white. Sporulation is profuse on all infected tissues, particularly on the abaxial surface of leaves. The fungus grows slowly but sporulates readily in culture (see Chapter 8). The disease was readily induced by inoculating leaves with a spore suspension and keeping the plants in a humid atmosphere for about three weeks (Bertus and Walker 1974). Symptoms developed three weeks to four weeks after inoculation. Pathogenicity tests on 186 species of eucalypt and four species of Angophora showed that the tested Sporothrix isolates were pathogenic only on Angophora, Corymbia and Eucalyptus species in the section Adnataria, subgenus Symphyomyrtus (see Chapter 2). Two further species of Sporothrix are known to parasitise eucalypts. Sporothrix eucalypti M.J.Wingf., Crous & W.J.Swart was recorded as inducing similar symptoms to Sporothrix pitereka but was differentiated from this species on the basis of smaller primary conidia (Table 9.7) and the more frequent production of secondary conidia (Wingfield et al. 1993). To date Sporothrix eucalypti is known only from E. grandis in South Africa. Sporothrix pusilla U.Braun & Crous was recorded from E. camaldulensis in Thailand and is characterised by having secondary mycelium emerging through stomata, with lateral and terminal conidiogenous cells and very small, narrow conidia (Braun 1995) (Table 9.7).

9.9 Winter leaf spot ( Piggotia substellata and Ceuthospora innumera ) A leaf spot that occurs mainly during winter on E. regnans seedlings in the central highlands of Victoria was shown to be caused by the Coelomycetes Piggotia substellata Cooke and Ceuthospora innumera Massee (teleomorph: Phacidium eucalypti G.W.Beaton & Weste; Crous 1993) (Ashton and Macauley 1972). The disease seriously impairs

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Foliar diseases of eucalypts caused by Hyphomycetes, listing recent generic synonyms, teleomorphs, symptoms and distinctive features of the pathogens

Pathogen anamorph [synonym] (teleomorph)

Disease symptoms

Distinctive features of the pathogen

Alternaria spp.

Small leaf spots or pale brown irregular necrotic areas with diffuse margins

Melanised, club-shaped conidia formed on superficial conidiogenous hyphae; conidia multicellular with transverse and some longitudinal septa

Botrytis cinerea (Botryotinia fuckeliana (de Bary) Whetzel; syn. Sclerotinia fuckeliana (de Bary) Fuckel)

Small diffuse leaf spots, grey mould, leaf blight and dieback of seedlings

Creamy brown masses of conidiophores and conidia formed over the entire surface of the lesion; conidiophores up to 2 mm long × 16–30 µm thick, with stipe and open head of branches; conidia 6–18 × 4–11 µm, 1-celled, ellipsoidal or obovoid, with slightly protuberant hilum, hyaline to pale brown, smooth.

Cercospora eucalyptorum

In angular lesions with Pseudocercospora paraguayensis

Caespituli sparse, amphigenous; conidiophores fasciculate, dark brown, sympodial with thick, dark scars; conidia hyaline, 3–7 septate, with thick, dark hilum, 30–80 × 2–3.5 µm

Cylindrocladiella spp. (Nectria spp.)

Damping off, leaf spot or shoot blight of seedlings and stressed trees. Tufts of white to fawn conidiophores and conidia on lesions

Conidiophore penicillate with primary and secondary branches terminating in phialides; branching laterally from a stipe that continues on to form a sterile filament with no septum or one basal septum; conidia cylindrical, hyaline, 2-celled, small (9–23 × 1.5–3 µm)

Cylindrocladiella camelliae (Venkataram. & C.S.V.Ram) Boesew.

Root rot; leaf spot

Sterile filament with one basal septum; vesicle on sterile filament ellipsoid to lanceolate and widest in middle; conidia mainly 1-septate, 9–15 × 2–2.5 µm

Cylindrocladiella infestans Boesew.

Infections on cuttings

Sterile filament with one basal septum; vesicle lanceolate to cylindrical; conidia mainly 1-septate, 10–23 × 2–3 µm

Cylindrocladiella lageniformis Crous, M.J.Wingf. & Alfenas

Infections on cuttings

Sterile filament with one basal septum; vesicle lageniform to ovoid; conidia mainly 1-septate, 9–15 × 1.5–2 µm

Cylindrocladiella parva (P.J.Anderson) Boesew.

Damping-off and seedling blight

Sterile filament with one basal septum; vesicle clavate to spathulate or pyriform; conidia mainly 1-septate, 13–20 × 2–3 µm

Cylindrocladiella peruviana

Common on cuttings in Brazil and South Africa

Similar to Cylindrocladiella camelliae, except vesicle widest in lower third

Cylindrocladium spp. (Calonectria spp.)

Damping off, leaf spot or shoot blight of seedlings and stressed trees. Tufts of white to fawn conidiophores and conidia on lesions

Conidiophore penicillate with primary, secondary and tertiary branches terminating in phialides; branching laterally from a stipe that continues on to form a multicellular sterile filament, with a terminal vesicle, the shape of which varies with the species; conidia cylindrical, hyaline, 1–5-septate, large (24–105 × 2–9 µm)

Cylindrocladium candelabrum Round or irregular leaf spots (Calonectria scoparia) with dark brown borders and clearer centres; shoot blight Cylindrocladium gracile (Calonectria gracilis)

Leaf spot or shoot blight of seedlings and stressed trees. Lesions become covered with white, powdery conidiophores and conidia

Conidia 1-septate, with a slightly swollen upper cell, 33–66 × 3.5–4.5 µm; sterile filament with ellipsoid to obpyriform (widest below the middle) vesicle Conidia 1-septate, 36–60 × 3–5 µm; sterile filament with clavate vesicle

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Foliar diseases of eucalypts caused by Hyphomycetes, listing recent generic synonyms, teleomorphs, symptoms and distinctive features of the pathogens (continued)

Pathogen anamorph [synonym] (teleomorph)

Disease symptoms

Distinctive features of the pathogen

Cylindrocladium ovatum (Calonectria ovata)

Round or irregular leaf spots with dark brown borders and clearer centres; shoot blight

Conidia 1-septate, with a slightly swollen upper cell, 50–60 × 4.6–6 µm; sterile filament with ovoid vesicle

Cylindrocladium quinqueseptatum (Calonectria quinqueseptata)

Leaf and shoot blight of seedlings and stressed trees

Conidia cylindrical, characteristically 5-septate, 60–120 × 5–7 µm

Cylindrocladium scoparium (Calonectria morganii)

Damping off, leaf spot or shoot blight of seedlings and stressed trees

Conidia 1-septate, with a slightly swollen upper cell, 40–66 × 3.5–4.5 µm; sterile filament with ellipsoid to pyriform vesicle

Cylindrotrichum sp.

Tiny (1–5 mm) slightly raised, brown, aggregated leaf spots, with prominent black conidiophores

Conidiophores dark, 2–4 in a group, 80–160 × 4–5 µm; conidiogenous cells polyphialidic, proliferating sympodially; conidia light brown, smooth, thin-walled, 1–3 septate, subcylindrical to narrowly obclavate, apex obtuse, base truncate, 30–40 × 4–5.5 µm

Mycovellosiella eucalypti

Subcircular to irregular leaf spots, 1–15 mm diameter, with red-brown border

Caespituli amphigenous, up to 70 µm wide, emerging from stomata; conidiophores light brown, finely verruculose, densely fasciculate, arising from brown stroma; conidia pale olivaceous, smooth, cylindrical, with thick hilum, in branched or unbranched chains, 1–3-septate, 14–40 × 1.5–2.5 µm

Passalora morrisii

Small subcircular to angular leaf spots 1–4 mm in diameter

Caespituli amphigenous, brown; conidiophores fasciculate, brown, thick-walled, verruculose, proliferating sympodially, arising in loose clusters from the upper cells of a stroma; conidia olivaceous to light brown, thick-walled, verruculose, base obconic-truncate, 1–7-septate, 30–55 × 4–5 µm

Phaeoramularia eucalyptorum Specks to small leaf spots, 1–5 mm diameter, along leaf margin

Caespituli amphigenous, brown; conidiophores fasciculate, arising from dark brown stroma; conidia catenulate, pale olivaceous to subhyaline, smooth, thin-walled, with thickened hilum, 1–6-septate, 15–90 × 2–3 µm

Pseudocercospora spp.

Angular, vein-limited necrotic lesions on several species in Australia and elsewhere

See Table 9.3 for details of species. Conidiophores medium to dark brown, smooth and aggregated into fascicles, which may emerge through stomata; conidial scars not thickened; conidia elongate, usually multiseptate, dark

Sporothrix pitereka [Ramularia pitereka]

Leaf and shoot blight and shoot canker of seedlings and young foliage; necrotic regions brown with reddish-purple margins and range from spots (1–2 mm diameter) to large irregular areas developing along one edge, distorting the leaf, or along the midvein

Dense masses of white conidiophores push up and eventually rupture the cuticle, forming closely packed white pustules which give a shining white appearance to diseased areas; pustules composed of dense layer of hyaline, aseptate conidiophores (up to 50 × 2.5 µm) borne on a stroma which develops either below the epidermis in shoots or in substomatal cavities in leaves; conidia 1-celled, hyaline, vacuolate, variable in shape but generally clavate to cylindrical, 5–20 × 2.5–6.5 µm

Sporothrix eucalypti

Similar to those induced by Sporothrix pitereka

Conidiophores similar to those of Sporothrix pitereka; primary conidia 6–12 × 2.5–4 µm, frequently with single or several secondary conidia, 3–5 × 1.5–2.5 µm

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Distinctive features of the pathogen

Sporothrix pusilla

Leaf spots amphigenous, subcircular to angular, often vein-limited, small 0.5–4 mm diameter, occasionally confluent

Primary mycelium internal; secondary mycelium external, emerging through stomata; primary conidia narrowly ellipsoid-ovoid, cylindrical-fusiform, 1-celled, 4–10 × 1–2 µm; secondary conidia 1.5–3.5 × 0.5–1.5 µm

Stigmina eucalypti

As for Stigmina eucalypticola

Similar to Stigmina eucalypticola except that it lacks a gelatinous matrix over conidiomata, and has larger (20–36 × 7.5–12 µm), cylindrical, markedly verruculose conidia

Stigmina eucalypticola

Brown to olivaceous, partly superficial, partly internal, spreading greasy spot colonies up to 10 mm diameter on leaves of mallee eucalypts; colonies discrete and maintain identity when confluent; purple discolouration of veins, especially in centre of colony

Verruculose, brown, superficial hyphae form a reticulate network; dark plugs of pseudoparenchyma fill stomatal pores and form sporodochia-like conidiomata, amphigenous but more abundant when hypogenous; conidia formed in a gelatinous matrix, dark brown, ellipsoidal to fusiform, 13–20 × 7–8 µm, rounded at apex and slightly truncate at the base with a slight marginal frill, indistinctly verruculose, with 1–3 transverse distosepta, occasionally with a longitudinal distoseptum, not constricted at distosepta

Stigmina hansfordii

As for Stigmina eucalypticola; brown with green-brown chlorotic centre and distinct purple outer zone that becomes paler and more diffuse towards the margin

Similar to Stigmina eucalypticola except that the superficial mycelium is restricted to the gelatinous matrix associated with the sporodochial conidiomata formed above the stomata, and conidia (10–17 × 5–8 µm) consistently have only one median distoseptum with an occasional oblique distoseptum

Stigmina robbenensis

Similar to Stigmina eucalypticola; differs by predominantly hypophyllous, 2–5 mm diameter infections that do not extend right through lamina; on leaves of eucalypt on Robben I., South Africa

Similar to Stigmina eucalypticola except that conidia ellipsoid to cylindrical, verruculose, 10–30 × 6–9 µm, with 1–9 distosepta

Trimmatostroma bifarium

Brown, roughly circular lesions, 2–15 mm diameter often with raised or crusty centre; larger lesions have concentric zones of different shades of brown; more common on older leaves in lower crown

Brown superficial mycelium and amphigenous, dark brown to black powdery, loose sporodochia, often in a circular pattern; heavily melanised conidia are 12–24 × 6–14 µm, smooth, 6–10-celled, with cells formed in two parallel rows on a common, thickened base

Trimmatostroma excentricum

As for Trimmatostroma bifarium

As for Trimmatostroma bifarium except that conidia are 9–11 × 6.5–8.5 µm, 4-celled, with two primary basal cells (9–11 × 3–4 µm combined) separated by a thick brown septum, and two secondary cells 2.5–4.5 µm in diameter

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survival of seedlings during the first year of growth and is an important factor in the regeneration cycle. It is confined to cooler months when lower light intensities, shorter day lengths and consistently high humidity from rain, fog, dew or snow prevail and is most severe in persistently wet winters. The disease appears initially in autumn as dull water-soaked spots and patches, often at the tip of the lower, fully expanded leaves. Within two or three weeks conspicuous purple margins form around the patches, which become necrotic and coalesce to cover much of the leaf, often resulting in leaf abscission. In mid winter to spring, minute black pycnidia of the fungi are formed on both surfaces of necrotic regions on attached or fallen leaves. Piggotia substellata forms single pycnidia on the leaf surface after the rupture of the cuticle, whereas Ceuthospora innumera forms pycnidia in multilocular stromata which are immersed in the dead mesophyll and are not clearly delimited (Swart 1988) (Table 9.5). The fungi may occur together or separately on infected leaves. Ceuthospora innumera is more common on leaf spots during autumn to early winter, while Piggotia substellata is more common in winter because it grows faster at lower temperatures. Ceuthospora innumera appears to be widely distributed in Australia, having been isolated from eucalypt leaf litter from Tasmania and Central Australia (Swart 1988). Seedlings up to the four-leaf stage may be killed within three weeks of infection and larger seedlings at the six to 12-leaf stage die gradually as the disease spreads to the uppermost leaves and terminal bud. Generally, only the taller seedlings of the spring and summer germination survive. Piggotia substellata and Ceuthospora innumera are colonisers of E. regnans leaf litter and are common on partially decayed leaf litter and in soil (Macauley and Thrower 1966). Soil splash to the lower leaves of seedlings is the main source of initial inoculum (Ashton and Macauley 1972) and accounts for the restriction of disease to lower leaves and its absence from seedlings older than two to three years. Symptoms were induced by inoculating plants with spore suspensions of both fungi and keeping them at high humidity for four to seven days, especially if the leaves were wounded by pricking or scratching. Under certain conditions, infection by Piggotia substellata alone occurred readily, but infection by

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Ceuthospora innumera was at best slight unless Piggotia substellata was present. Severe infection by Botrytis cinerea often obscured winter leaf spot development in mature forests during very wet periods. Both Ceuthospora innumera and a similar species, Ceuthospora lauri (Grev.) Grev., occur on eucalypt leaves in South Africa (Crous 1991, 1993). The conidia of Ceuthospora lauri are smaller than those of Ceuthospora innumera and are produced on conidiophores, unlike those of Ceuthospora innumera which are produced directly on phialides lining the locules (Swart 1988). In a relationship similar to that observed for winter leaf spot in southern Australia, Ceuthospora lauri co-occurs with Pilidium acerinum Kunze on lesions on lower branches of E. grandis during the cooler, wetter months (Crous 1991). Both fungi are weakly pathogenic on older leaves and appear to have little effect on the host.

9.10 Leaf spots and speckles of minor importance While several pathogens (e.g. M. nubilosa) that commonly cause large blights may also cause small leaf spots (depending on the species of host, the stage of development of leaves when they become infected and the environmental conditions), many others, including many of the Mycosphaerella spp. listed above, only ever cause small circular spots or speckles. Most of these pathogens have been of taxonomic interest only but some may reach epidemic levels in response to local conditions. These pathogens are discussed briefly here.

9.10.1 Anthostomella eucalypti The unitunicate ascomycete, Anthostomella eucalypti H.Y.Yip, was described from round to irregular, greyish-white lesions with reddish-brown margins on E. camaldulensis collected in Melbourne (Yip 1989) and was found on E. globulus in plantations in Tasmania (Yuan 1999) (Table 9.4). The species is distinguished by solitary and widely scattered subepidermal ascomata and uniseriate, one-celled, ellipsoid to reniform, melanised ascospores. When fresh, ascospores have a gelatinous sheath (Yuan 1999), which appears to contract to a gelatinous globose basal appendage in dried specimens (Yip 1989).

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9.10.2 Aurantiosacculus eucalypti Aurantiosacculus eucalypti (Cooke & Massee) Dyko & B.Sutton (syn. Protostegia eucalypti Cooke & Massee) is a rare but distinctive coelomycete occurring on lesions on leaves of E. obliqua and some mallee eucalypts (Dyko et al. 1979). In a survey of leaf diseases on eucalypts in east Victoria, it was found on one occasion, causing an irregular lesion with a thick purple-black margin on E. baxteri (Marshall 1997). It has been reported only from Australia and is distinguished by its large, erumpent, bright orange pycnidia that are visible to the unaided eye (Plate 9.21) (Table 9.5).

9.10.3 Blastacervulus eucalypti Blastacervulus eucalypti H.J.Swart (Table 9.6) causes leaf spots that develop only part way through the leaf lamina, being divided from living tissue by a saucer-shaped meristematic region (Swart 1988). Acervular conidiomata form beneath the cuticle, with plugs of hyphae penetrating between the epidermal cells. The acervuli rupture the cuticle and form branched chains of conidia in a powdery mass interspersed with sterile hyphae. The disease has been reported only from E. obliqua in Victoria (Swart 1988).

9.10.4 Coniothyrium species Small leaf spots, one to 10 millimetres in diameter, are caused by several species of the coelomycete genus Coniothyrium (Sutton 1980). The fungi produce minute, substomatal, globose pycnidia (Table 9.5). Coniothyrium eucalypticola B.Sutton was described from pale brown more or less vein-limited lesions (Sutton 1971a). A second species, Coniothyrium ahmadii B.Sutton (syn. Coniothyrium eucalypti S.Ahmad), from eucalypt branches collected in Pakistan (Sutton 1980), has thick, rough-walled conidia (Sutton 1975). Swart (1986a) described two species, Coniothyrium ovatum H.J.Swart (Fig. 9.20) and Coniothyrium parvum H.J.Swart, from small necrotic leaf spots on eucalypts in Australia; the former was also reported from New Zealand (Ridley 1995). The conidia of Coniothyrium parvum are only slightly smaller than those of Coniothyrium ovatum (Swart 1986a) and Crous (1998) has since reduced the species to synonymy under Coniothyrium ovatum. This species is distinguished from Coniothyrium eucalypticola and Coniothyrium

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ahmadii by conidial shape. A fifth species, Coniothyrium kallangurense B.Sutton & Alcorn, was described from leaves of E. microcorys in Queensland (Sutton 1975). An unidentified Coniothyrium species was reported from widely occurring leaf spots on E. urophylla in Vietnam (Sharma 1994). A leaf spot caused by Coniothyrium ovatum occurs on immature leaves on young growth and lower branches of mature trees of E. cladocalyx and E. lehmannii in South Africa, but is relatively unimportant (Crous et al. 1989a). There is now doubt, based on its wider conidia, that the South African fungus is the same as Coniothyrium ovatum from Australia (Crous 1998). Attempts to infect eucalypt seedlings with conidia of South African isolates of Coniothyrium ovatum collected from naturally infected leaves were unsuccessful (Crous et al. 1989c).

9.10.5 Cylindrotrichum sp. A species of the dematiaceous hyphomycete, Cylindrotrichum Bonord., was found rarely in plantations of E. nitens in Tasmania (Yuan 1999). The fungus was associated with tiny, slightly raised, red-brown, aggregated leaf spots with prominent, erect, black conidiophores (Table 9.7).

9.10.6 Davisoniella eucalypti The pycnidial fungus, Davisoniella eucalypti H.J.Swart, causes abundant leaf spots on saplings and mature trees of E. marginata in Western Australia (Swart 1988) (Table 9.5).

9.10.7 Dichomera species Dichomera eucalypti (G.Winter) B.Sutton [syn. Camarosporium eucalypti G.Winter, Camarosporellum eucalypti (G.Winter) Tassi, Coryneum viminale Cooke & Massee] forms subepidermal, unilocular (pycnidia-like) stromata or multilocular stromata in otherwise healthy leaf tissue (Cooke 1892; Sutton 1975). A similar fungus with larger conidia of variable shape and size was described as Dichomera versiformis Z.Q.Yuan, Wardlaw & C.Mohammed from rare, elliptical to irregular, pale leaf spots on E. nitens in Tasmania (Table 9.5) (Yuan et al. 1999). A similar fungus with even larger, variable conidia (15–29 × 8–13 µm, compared with 12.5–17.5 × 10–11.5 µm in Dichomera versiformis and 10–13 × 7–9.5 µm in

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Figure 9.20

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Pycnidium of Coniothyrium ovatum below a stoma, with conidiophores and conidia. (From Swart, H.J., 1986, Transactions of the British Mycological Society 86, 494–496, with permission).

Dichomera eucalypti) was associated with small, round to irregular, light brown leaf spots on E. globulus in a plantation in southern Victoria (Barber 1998). All fungi are characterised by dark muriform conidia with several transverse and occasional longitudinal septa (Table 9.5).

9.10.8 Fairmaniella leprosa Fairmaniella leprosa (Fairm.) Petr. & Syd. (syn. Coniothyrium leprosum Fairm., Melanconium eucalypticola Hansf.; Sutton 1971a) is a common but minor pathogen that was first described from fruits and stalks of a eucalypt in California (Sutton 1971a). It has also been recorded as a leaf pathogen from several eucalypt species in Australia, Chile, Hawaii, Zambia and New Zealand (Hansford 1956;

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Sutton 1971a; Swart 1988; Dick 1990) and from older leaves and petioles of E. globulus, sometimes in association with a Mycosphaerella species, in South Africa (Crous et al. 1989a, 1990). It is common on a wide range of eucalypts in southern Australia, often causing small, raised corky lesions similar to those caused by Aulographina eucalypti. Depending on the host species, leaf spots vary in size, shape and colour and acervular pustules vary in diameter and height (Swart 1988). Lesions on E. fasciculosa and E. globulus are circular to elliptical or irregular and up to 20 millimetres in diameter, while on C. citriodora they vary from minute circular flecks to irregular lesions one to seven millimetres in diameter (Sutton 1971a). On E. nitens, the fungus was associated with large

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Figure 9.21

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Acervulus, conidiophores and conidia of Fairmaniella leprosa. (From Swart, H.J., 1988, Transactions of the British Mycological Society 90, 279–291, with permission).

spreading lesions at the tips and margins of leaves (Yuan 1999). In some cases, hypophyllous acervuli were not associated with necrosis of leaf tissues (Sutton 1971a) or the fungus was associated with necrosis around infections of Ophiodothella longispora (Swart 1988). On E. globulus in South Africa, the fungus causes hard, round, corky lesions that usually do not extend right through the lamina. The dark acervuli (100–200 µm diameter) arise from a stroma in the mesophyll and eventually lift and rupture the epidermis, forming black pustules of thick-walled, finely-ornamented conidia (Sutton 1971a; Swart 1988) (Table 9.6) (Fig. 9.21).

9.10.9 Idiocercus australis Idiocercus australis (Cooke) H.J.Swart [syn. Phoma australis Cooke; Macrophoma australis (Cooke) Berl.

& Voglino; Dothiorella australis (Cooke) Petr. & Syd.] (Table 9.5) was associated with large necrotic lesions on leaves of two-year-old E. regnans which had regenerated after a bush fire (Swart 1988). It was not clear whether the fungus was a primary pathogen or a saprophytic invader of leaves killed by other factors. The fungus was found in close association with Clypeophysalospora latitans and is a possible anamorph of that species (Swart 1988). A similar association was observed in South Africa (Crous et al. 1990). In Tasmania, Idiocercus australis was found in small (3–5 mm diameter), irregular lesions that occurred commonly but at low incidence on eucalypt species, including E. globulus, in both plantations and native forests (Yuan 1999). Some lesions dropped out, leaving characteristic holes in the leaves. There is some confusion about the generic

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Figure 9.22

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Pycnidium beneath a stoma, and conidiophores and conidia of Sonderhenia eucalypticola. (From Swart, H.J. and Walker, J., 1992, Transactions of the British Mycological Society 90, 633–641, with permission).

placement of this species as Nag Raj (1993) excludes it from Idiocercus.

9.10.10 Microsphaeropsis species Sutton (1980) listed four species of Microsphaeropsis that are known to cause small spots on eucalypt leaves. The genus is similar to Coniothyrium but is differentiated by the mode of conidiogenesis, which

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is phialidic in Microsphaeropsis and holoblastic in Coniothyrium (Sutton 1980). The Microsphaeropsis species produce ornamented conidia and are differentiated from one another by conidial size and morphology (Table 9.5). Microsphaeropsis conielloides B.Sutton was reported from leaf spots on E. viminalis ssp. viminalis, E. obliqua, E. regnans and E. delegatensis in New Zealand (Dick 1990).

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The fungus is most commonly associated with older leaves in the lower crown and is weakly pathogenic. Microsphaeropsis callista (Syd.) B.Sutton was reported to be parasitic on eucalypt leaves in Australia (Sutton 1971a, 1980) and South Africa, where it was associated with brown, raised lesions on leaves of E. nitens (Crous and van der Linde 1993). Conidia of Microsphaeropsis callista are characterised by a central guttule (Sutton 1980). This species was common on small, circular to elliptical lesions on E. obliqua and E. nitens in Tasmania (Yuan 1999). Other species recorded from eucalypts are Microsphaeropsis globulosa (Sousa da Câmara) B.Sutton from E. globulus in Portugal and Microsphaeropsis olivacea (Bonord.) Höhn. from a wide range of hosts and locations (Sutton 1980). A species of Microsphaeropsis was commonly isolated as an endophyte from healthy xylem of young shoots and seedlings of E. globulus in Uruguay (Bettucci and Saravay 1993).

9.10.11 Phloeosporella eucalypticola The acervular coelomycete, Phloeosporella eucalypticola H.Y.Yip, was reported from a small subcircular or irregular leaf spot on a hybrid between E. radiata and E. dives in Victoria (Table 9.6) (Yip 1997).

9.10.12 Selenophoma eucalypti Selenophoma eucalypti Crous, C.L.Lennox & B.Sutton was described from irregular necrotic lesions occurring mainly along leaf margins of eucalypts in South Africa (Crous et al. 1995c) (Table 9.5).

9.10.13 Sonderhenia species A relatively common tiny leaf spot (‘speckle’) up to three millimetres in diameter with a purple-red margin on eucalypt leaves is caused by two species of Sonderhenia (formerly Hendersonia) (Plate 9.22). Swart and Walker (1988) reviewed the taxonomic status of five of the seven Hendersonia species previously described from eucalypt leaves. Hendersonia eucalypti Cooke & Harkn., reported from dead leaves and twigs of E. globulus in California, was shown to be a species of Seimatosporium, probably Seimatosporium lichenicola (Corda) Shoemaker & E.Müll. Hendersonia grandispora was shown to be Kirramyces (now Phaeophleospora) epicoccoides. Two species were accepted—Sonderhenia

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eucalyptorum (Hansf.) H.J.Swart & J.Walker (syn. Hendersonia eucalyptorum Hansf.) and Sonderhenia eucalypticola (A.R.Davis) H.J.Swart & J.Walker (syn. Hendersonia eucalypticola A.R.Davis; Hendersonia fraserae Hansf. as ‘fraseri’). The conidia of Sonderhenia species differ from those of Phaeophleospora epicoccoides in being shorter and wider, more so for Sonderhenia eucalypticola (Fig. 9.22) than Sonderhenia eucalyptorum (Fig. 9.23), distoseptate and borne on smooth-walled anellidic conidiogenous cells (Table 9.5) (Walker et al. 1992). Park and Keane (1982c) reported Hendersonia isolates from small leaf speckles (1–2 mm diameter) on E. globoidea and E. obliqua. The isolates varied considerably in conidial size (e.g. 27–44 × 6–9 µm from E. globoidea) and were considered to be Sonderhenia (as Hendersonia) eucalyptorum. Pycnidia were often intermingled with ascocarps of an undescribed species of Mycosphaerella, which was shown to be the teleomorph of the Sonderhenia species. Mycosphaerella swartii and M. walkeri, two morphologically identical fungi, were subsequently described as the teleomorphs of Sonderhenia (as Hendersonia) eucalyptorum and Sonderhenia eucalypticola (as Hendersonia fraserae), respectively (Park and Keane 1984). Sonderhenia eucalyptorum was identified from leaf spots on 17 eucalypt species but the teleomorph was found on only five of these; Sonderhenia eucalypticola was identified on only three eucalypt species, with the teleomorph occurring on only one of these. The anamorphs formed similar pycnidia but could be distinguished reliably by differences in size, morphology and mode of germination of conidia and by growth in culture (Table 9.5) (Hansford 1954). On agar, conidia of Sonderhenia eucalyptorum tend to germinate mainly from the terminal cells, whereas those of Sonderhenia eucalypticola germinate from the central cells as well as the terminal cells. On E. globulus, Sonderhenia eucalypticola was observed to form pycnidia in green leaf tissue, which subsequently became necrotic and formed a leaf spot (Plates 9.23 and 9.24) (Barber 1998). It appears that this species, like several well-adapted eucalypt leaf pathogens, may have a biotrophic phase of parasitism prior to development of a necrotic lesion. In Tasmania, Sonderhenia eucalypticola was found commonly on E. obliqua in natural stands and on E. globulus and E. nitens in plantations, causing tiny, dark-purple

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Figure 9.23

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Pycnidia beneath stomata, conidiophores and conidia of Sonderhenia eucalyptorum. (From Swart, H.J. and Walker, J., 1992, Transactions of the British Mycological Society 90, 633–641, with permission).

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spots that became necrotic, whereras Sonderhenia eucalyptorum occurred commonly on E. globulus in plantations (Yuan 1999). There have been several studies of the host specificity of these pathogens on eucalypts. Burdon and Chilvers (1974a) found an unidentified Hendersonia species on six eucalypt species (four Monocalyptus, two Symphyomyrtus). In a study of isolates obtained from leaf spots on eight eucalypt species (four Monocalyptus species and four Symphyomyrtus species) collected from one location, conidial dimensions varied significantly between isolates from the two subgenera and also between isolates from several of the eucalypt species (Fripp and Forrester 1981). Similar differences were observed among conidia produced in culture, although in general these were longer and narrower than those from field collections. The authors did not identify the isolates to species level. Using polyacrylamide gel electrophoresis, Burdon et al. (1982) studied the soluble proteins of 14 isolates and obtained six different protein patterns; identical patterns were obtained for isolates from two or three different eucalypt species. On the basis of variation in protein patterns and conidial dimensions, it was suggested that several different races or even species of Hendersonia were present. In view of the morphological similarity of Sonderhenia eucalyptorum and Sonderhenia eucalypticola and their teleomorphs, cross inoculations were conducted with conidia from single conidial isolates of each species (Park and Keane 1984). These tests showed conclusively that the two species were distinct: each showed greater infectivity on the host species with which they were normally associated in the field and the conidia produced on inoculated seedlings showed the same differences as those from naturally infected trees. Both Sonderhenia eucalyptorum and Sonderhenia eucalypticola are present in New Zealand (Dick 1990) but are considered to be of minor importance (Dick and Gadgil 1983). As in Australia, Sonderhenia eucalyptorum is found on a wider range of eucalypt species, but the teleomorph is not present on all of these. The teleomorph of Sonderhenia eucalypticola has not been recorded from New Zealand (Dick 1990).

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9.10.14 Staninwardia breviuscula Staninwardia breviuscula B.Sutton was described from small circular lesions on leaves and elongated, often confluent, lesions (up to 10 mm long) on the stems and petioles of an unidentified eucalypt species in Mauritius (Sutton 1971b). The margin of younger leaf lesions is raised, somewhat irregular and chocolate brown in colour on the upper leaf surface. On the lower surface, the lesions are slightly smaller with a narrow, diffuse, pale brown halo. Numerous epiphyllous acervuli are formed mainly in the epidermis and conidia are formed in chains of up to three, with conidial shape depending on position in the chain (Table 9.6) (Sutton 1971b).

9.10.15 Stilbospora foliorum Stilbospora foliorum Cooke is a minor leaf pathogen reported from a stringybark eucalypt near Melbourne (Swart 1988) and from E. sieberi in East Gippsland (D.A. Marshall, pers. comm.). The fungus described from Eucalyptus (Fig. 9.24) is atypical of the genus, but could not be better placed at the time (Swart 1988) (Table 9.6).

9.10.16 Trimmatostroma species Trimmatostroma bifarium Gadgil & M.Dick and Trimmatostroma excentricum B.Sutton & Ganap. cause small brown, roughly circular, discrete or confluent lesions, the centre of which is often raised or crusty (Sutton and Ganapathi 1978; Dick 1982; Gadgil and Dick 1983). Larger lesions are composed of concentric rings of differing shades of brown, giving the appearance of a target spot (Dick 1982). During wet periods in summer and autumn, the fungus forms spore masses which appear as black dots on lesions (Beresford 1978). While the two species cannot be distinguished macroscopically, their heavily melanised conidia are very distinctive (Table 9.7). In New Zealand both fungi are found mainly on E. delegatensis, E. regnans and E. sieberi and are most common on older leaves in the lower crown where they cause little damage (Dick 1982). Trimmatostroma excentricum has been reported from mature foliage of E. globulus (Park and Keane 1982c) and E. perriniana (R.F. Park, unpubl. data) in Australia and from C. citriodora in Brazil (Ferreira 1989).

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Figure 9.24

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Conidiomatum and conidia of Stilbospora foliorum. (From Swart, H.J., 1988, Transactions of the British Mycological Society 90, 279–291, with permission).

9.11 Leaf spots and blights of stressed plants Many leaf spot or leaf blight diseases, associated with less specialised pathogens and often leading to twig cankers and dieback of young shoots, have been reported from eucalypts growing in plantations under conditions to which the trees are not well adapted, especially in the wet tropics. Many such diseases are common in nurseries (see Chapter 8) and some are more appropriately discussed as canker diseases (see Chapter 10).

9.11.1 Alternaria leaf spot Several species of Alternaria have been described from leaf spots on eucalypts, more commonly on seedlings (see Chapter 8) than on mature plants in the field. Alternaria leaf spot was commonly observed at low incidence in young plants or coppice shoots of E. grandis and E. tereticornis in plantations in India (Sharma et al. 1985). The disease usually appeared during the dry period as minute

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greyish-brown spots which developed near the tip and along the margin of the leaf (Table 9.7). These spots coalesced to form large dull-brown to pale-brown irregular necrotic areas with diffused margins. The necrotic area along the leaf margins often showed splitting due to the action of the wind. Alternaria tenuissima (Kunze) Wiltshire is a common cause of small leaf spots on several eucalypt species in Italy (Magnani 1964). Alternaria alternata (Fr.) Keissl. and Alternaria tenuissima occur as phylloplane fungi on various eucalypt species in several countries including Australia (Macauley and Thrower 1966; Lamb and Brown 1970; Parbery 1974; Macauley 1979; Upadhyay 1981, 1986; Cabral 1985).

9.11.2 Botryosphaeria ribis Botryosphaeria ribis Grossenb. & Duggar (anamorph: Fusicoccum sp.; syn. Dothiorella sp.) (Table 9.1) is a relatively minor, non-specialised pathogen of wide occurrence in temperate and

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tropical regions, causing a range of symptoms (leaf spot, tip blight and twig canker) in stressed trees (Punithalingam and Holliday 1973). The confusing state of the taxonomy of the species is discussed in Chapter 7. Lesions are grey-brown with black ascocarps and pycnidia erupting through the epidermis (Punithalingam and Holliday 1973; Crous et al. 1989d). In South Africa, the species occurs in lesions caused by other pathogens on eucalypt leaves, but was also identified as the cause of tip blight on stressed trees of E. camaldulensis, E. cladocalyx, E. grandis, E. globulus and E. nitens and was isolated as an endophyte from apparently healthy, surface-sterilised leaves and twigs (Crous et al. 1989d; Smith et al. 1996). In Brazil, the fungus is often associated with cankers on shoots with dieback caused by a variety of factors (Ferreira 1989) and it causes a distinctive leaf spot on eucalypts in Spain (Ruperez and Munoz 1980). The anamorph was isolated from necrotic seed capsules, pedicels, peduncles, twigs and leaf veins of E. camaldulensis in Florida (Webb 1983) and from leaf spots and stem cankers associated with shoot dieback on E. globulus in India (Haware et al. 1976); in both cases, pathogenicity was confirmed by inoculations. Botryosphaeria ribis is frequently associated with cankering and dieback of E. marginata in Western Australia (Davison and Tay 1983) and elsewhere (see Chapter 10).

9.11.3 Grey mould (Botrytis cinerea) Grey mould, leaf blight and dieback of eucalypt seedlings and saplings caused by Botrytis cinerea Pers. have been reported from many localities, including Central America (Abrahão 1948), Brazil (Ferreira 1989, Ferreira and Muchovej 1991), Spain (Ruperez and Munoz 1980), South Africa (Crous et al. 1989a) and Australia (Marks et al. 1982; Wardlaw and Phillips 1990) (Table 9.7). Infection by Botrytis cinerea often causes a blight on seedlings of E. regnans in mature forests in the central highlands of Victoria during very wet periods in winter, when it may obscure winter leaf spot (see section 9.9) (Ashton and Macauley 1972). In New Zealand, Botrytis cinerea caused leaf blight leading to seedling death in several eucalypt species in the glasshouse and severe dieback on saplings of E. delegatensis up to 10 years old (Gilmour 1966). Seedlings of E. globulus about one metre high were severely

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attacked on their leaves, branches and stems during a very wet year in Kenya (Nattrass 1949). Lesions on leaves ranged from small diffuse spots, developing from leaf tips or margins, through to blights covering large areas of the leaf. Mittal et al. (1987) reviewed Botrytis as a hazard to reforestation. Epidemics caused by Botrytis are known to occur in cool, wet and humid weather; such conditions favour the fungus and also predispose the host to infection. Plants grown in sunny, well-aerated situations do not suffer as badly from grey mould as plants in shady or protected situations (Jones and Elliot 1986). The disease on eucalypts is most common towards the end of the growing season (autumn) when plants are large, foliage is usually crowded and growthsuppressed plants and dead tissue are present (Brown and Wylie 1991). However, the disease is mainly a problem in nurseries (see Chapter 8).

9.11.4 Colletotrichum gloeosporioides Colletotrichum gloeosporioides (Penz.) Penz. & Sacc. is a common facultative pathogen that causes leaf spots and cankers of stressed plants of many species, including eucalypts. It was associated with a leaf spot and stem canker of eucalypt seedlings in India (Sharma et al. 1985), a leaf spot of clonal cuttings in South African nurseries (Viljoen et al. 1992) and a canker and leaf and seedling blight on E. pellita in Brazil (Dianese et al. 1985). A species of Colletotrichum was associated with leaf blight of clonal cuttings of E. urophylla in Brazil (Batista et al. 1985). Lesions are light brown and usually surrounded by a purple margin and cause leaves to become yellow and drop off. Acervuli occur on leaves and stems and exude pink to yellow conidial masses under humid conditions (Table 9.6). Conidia are mainly dispersed by water splash and wind. This disease is more common in nurseries than in the field (see Chapter 8).

9.11.5 Coniella species Six species of Coniella are associated with leaf spots on eucalypts in plantations and nurseries (see Chapter 8) (Sutton 1980; Sharma et al. 1985). Most have wide host ranges, including nonmyrtaceous species, and occur on eucalypts growing under excessively humid conditions. The fungi produce immersed to semi-immersed pycnidia and the species are differentiated by conidial size and shape (Table 9.5) (Sutton 1980).

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Coniella castaneicola (Ellis & Everh.) B.Sutton (syn. Coniella eucalypticola Nag Raj; Embolidium eucalypti Bat. & Peres) (teleomorph: Schizoparme straminea Shear) is widely distributed, being reported from Brazil, Cuba, the USA, Australia, the UK (Sutton 1980), India (Sharma et al. 1985) and South Africa (Viljoen et al. 1992; Crous and van der Linde 1993). Perithecia of the teleomorph are frequently associated with pycnidia (Shear 1923). Coniella fragariae (Oudem.) B.Sutton (syn. Coniella pulchella Höhn.) is pathogenic on eucalypts in Brazil (Ferreira 1989), India (Sharma et al. 1985; Sharma 1986), China and Australia (B.N. Brown, pers. comm.) and Vietnam (Sharma 1994) and was reported from Canada, the UK and several African countries (Sutton 1980). It was observed on E. grandis and E. urophylla in south-east China and on 27 of 33 eucalypt species during an outbreak in trial plots in tropical north Queensland during 1989 and 1990 (B.N. Brown, pers. comm.). It occurs in both nurseries and plantations, although in Brazil it was reported only in plantations six months after planting, where all Coniella infections followed insect damage or infection by rust or other pathogens (F.A. Ferreira, pers. comm.), frequently Cylindrocladium species (Ferreira 1989). It usually forms circular, marginal leaf spots which are initially greyish-black but become pale brown during dry weather (Sharma et al. 1985; B.N. Brown, pers. comm.). Leaves with large areas affected are shed. Numerous pycnidia, arranged in more or less concentric rings, develop even in small spots and as the spots enlarge, new rings of pycnidia develop. During wet weather pycnidia produce an off-white to pale yellow or brown conidial ooze that is dispersed by rain splash. Lesions also occur on petioles and twigs (B.N. Brown, pers. comm.). The disease is favoured by wet and humid conditions. At one location in Kerala, India, it caused extensive defoliation of lower branches of E. grandis during a period of heavy and incessant monsoon rains, but in the following year when rainfall was less and intermittent, the incidence of disease was low (Sharma et al. 1985). On the island of New Britain, Papua New Guinea, Coniella australiensis Petr. (Batista et al. 1964; Sutton 1980) occurred on dead branches of E. deglupta following insect damage (Shaw 1984). Two types of leaf spot associated separately with Coniella australiensis and Coniella fragariae occur

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commonly on E. camaldulensis in Vietnam (Sharma 1994; Old et al. 1999a) (Plate 9.25). Coniella fragariae causes circular necrotic areas along the leaf margin with concentric rings of brown pycnidia evident even on small lesions. Eventually large circular necrotic lesions with many concentric rings of pycnidia may be formed (Table 9.5). In contrast, Coniella australiensis forms pycnidia irregularly over the lesions (Sharma 1994). In Vietnam, Coniella leaf blight is common on E. camaldulensis but is not regarded as a serious problem (Old et al. 1999a). Other species of Coniella reported from eucalypts are Coniella granati (Sacc.) Petr. & Syd., reported only from Eucalyptus in India (Sharma et al. 1985; Soni and Jamaluddin 1990) and Coniella petrakii B.Sutton, reported from several countries in Asia and Africa (Sutton 1980) (Table 9.5). Coniella minima B.Sutton & Thaung occurred on leaf lesions on E. camaldulensis in Burma but because it was associated with several other fungi, its status as a primary pathogen is doubtful (Sutton 1975, 1980). It was commonly isolated as an endophyte from seedling stems and leaves of E. globulus in Uruguay (Bettucci and Saravay 1993). Infection by Coniella granati appears initially on leaf tips in the form of browning, which gradually extends and covers the entire leaf, spreading to the stem and killing the seedlings (Sharma et al. 1985). Occasionally, the infection occurs only on the stem.

9.11.6 Cryptosporiopsis eucalypti Cryptosporiopsis eucalypti Sankaran & B.Sutton has been recorded from leaf spots, shoot blight and stem cankers on several eucalypt species in many countries, mainly in the wet tropics (Sankaran et al. 1995b; Old et al. 1999a, 1999b). Leaf spots caused by the species occur widely on eucalypts in Brazil (F.A. Ferreira, unpubl. data), Indonesia (M.J. Wingfield and P.W. Crous, unpubl. data) and Thailand, Vietnam and Japan (Old and Yuan 1994). Damage caused by this fungus has sometimes been attributed to Cylindrocladium, but unlike Cylindrocladium, which can cause severe defoliation over a short period and then be difficult to detect, Cryptosporiopsis forms longer-lived infections on the trees (Old et al. 1999a). In Vietnam and Thailand, the pathogen causes discrete, irregularly shaped, reddish-brown to dark chocolate-brown, erumpent lesions which give the leaf a roughened surface (Table 9.5) (Plate 9.26). Cream-coloured droplets of

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Figure 9.25

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Cylindrocladium candelabrum, showing: A) conidiophore and stipe, B) and E) sterile vesicle, C) and E) conidia and D) chlamydospore. Bar represents 10 µm. (From Crous, P.W. et al., 1993, Mycological Research 97, 701–708, with permission).

spores can be seen exuding from cup-shaped sporocarps during wet weather. The fungus grows and sporulates readily in culture. In Thailand, the species is the most serious pathogen of E. camaldulensis and E. urophylla (Old and Yuan 1994; Pongpanich 1999). Variation in resistance to the disease was evident among different clones of E. camaldulensis; susceptible clones suffered chronic defoliation, shoot blight and canker development, culminating in shoot and even tree death. Sankaran et al. (1995b) confirmed pathogenicity on leaves of six-month-old seedlings of E. grandis and E. tereticornis. Symptoms were obtained on wounded and unwounded leaves, but leaf spots in the field are most frequently associated with insect or wind damage, or with lesions caused primarily by Cylindrocladium spp. In this regard the pathogen is very similar to Coniella fragariae and in Brazil the two frequently occur together (F.A. Ferreira, unpubl. data). Both Cryptosporiopsis eucalypti and a Coniella species occurred in association with a serious defoliating disease of E. camaldulensis in north Queensland (Old and Yuan 1994). In Vietnam, the two fungi are common but not particularly damaging in young plantings of E. camaldulensis

(Old et al. 1999a). An unidentified species of Cryptosporiopsis caused root and collar rot leading to mortality in young plantations of E. nitens in Tasmania (Yuan 1999).

9.11.7 Cylindrocladium and Cylindrocladiella species At least 15 species of Cylindrocladium and five species of Cylindrocladiella (Crous and Wingfield 1993, 1994) are associated with a wide range of diseases including damping-off, root rot, shoot blight and leaf spot of seedlings in nurseries (see Chapter 8) and blight, stem canker and death of mature trees growing in plantations under humid conditions (Sharma et al. 1985; Ferreira 1989; Crous et al. 1991a). The main species involved and their distinguishing features are summarised in Table 9.7 and discussed more fully in relation to nursery diseases in Chapter 8. Conidiophores are scattered over the lesion surface and consist of conidiogenous branches formed laterally from a stipe which grows on past the penicillate conidiogenous structure to form the long sterile appendage characteristic of the genera (Fig. 9.25) (Booth and Gibson 1973). Originally all species were included in

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Cylindrocladium but Boesewinkel (1982) established a new genus, Cylindrocladiella, for the species with smaller spores and stipes lacking a septum or with a single septum near the point of emergence of the conidiogenous branches. This separation was confirmed by Crous and Wingfield (1993). Cylindrocladium and Cylindrocladiella species are non-specialised pathogens with wide host ranges, which under conditions of high temperature and humidity in the wet tropical lowlands and crowding of plants in nurseries and young plantations, may include many eucalypt species. Isolates from other plant genera are pathogenic on eucalypts under certain conditions (Bell and Sobers 1966; Sobers and Seymour 1967; Sobers 1968; Almeida and Bolkan 1981). In some cases, a destructive disease is associated with several species. The species grow readily in culture.

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Cylindrocladium isolates possessing one-septate conidia with a slightly swollen upper cell (Booth and Gibson 1973). These fungi are now allocated to at least three species on the basis of the shape of the terminal cell on the sterile stipe or filament (Crous et al. 1993a; El-Gholl et al. 1993). Cylindrocladium scoparium was retained for species with ellipsoid to pyriform vesicles on its sterile filaments, Cylindrocladium candelabrum Viégas (teleomorph: Calonectria scoparia Peerally) for species with ellipsoid to obpyriform vesicles (Fig. 9.25) and Cylindrocladium ovatum El-Gholl, Alfenas, Crous & T.S.Schub.; El-Gholl et al. 1993) (teleomorph: Calonectria ovata D.Victor & Crous; Victor et al. 1997) for species with ovoid vesicles (Table 9.7). This discussion is based on names as published in the literature, some of which may prove to be incorrect in the light of this taxonomic revision.

9.11.7.1 Leaf blight caused by Cylindrocladium scoparium, Cylindrocladium candelabrum and Cylindrocladium ovatum

In Australia, Cylindrocladium scoparium caused seedling death in nurseries and young eucalypt plantations in northern New South Wales, mainly as a result of root infection (Keirle 1981). It was thought to have been introduced into the field with nursery stock and disease outbreaks were associated with high rainfall, relative humidity and temperature. The main species affected were E. grandis, E. microcorys, E. pilularis and E. pyrocarpa. In an earlier study, an isolate of Cylindrocladium scoparium from Agonis flexuosa was shown to be pathogenic when inoculated onto about 60 eucalypt species and Angophora costata, although the disease was not reported from these species in the field (Bertus 1976). Certain eucalypt species were also subject to root and stem rot as a result of soil infestation with this fungus. It was concluded that the fungus survives in soil and infects susceptible plants at soil level and below and may later cause foliar infection under suitable conditions (Bertus 1976). The leaf spots are initially red with distinct margins and eventually develop into blights. Control of root infection and, to a lesser extent leaf infection, was achieved with soil drenches or foliar sprays of fungicides such as benomyl and thiophanate-methyl.

Until recently the name Cylindrocladium scoparium Morgan [syn. Cylindrocladium pithecolobii Petch; Cylindrocladium brasiliense (Bat. & Cif.) Peerally; Cylindrocladium ellipticum Alfieri, C.P.Seym. & Sobers; Diplocladium cylindrosporum Ellis & Everh.] (teleomorph: Calonectria morganii Crous, Alfenas & M.J.Wingf. 1993a) was given to all

Cylindrocladium scoparium was reported as a serious eucalypt pathogen in Brazil (Cruz and Figueiredo 1960, 1961) and Costa Rica (Segura 1970) and has been recorded on eucalypts in Argentina (Jauch 1943). Morphological and electrophoretic studies of Cylindrocladium scoparium-like isolates from South Africa, Brazil and

Diseases caused by species of Cylindrocladium and Cylindrocladiella pose a serious threat to eucalypts in tropical India and in equatorial regions of Brazil due to the prevailing humid conditions (Mohanan and Sharma 1986; Blum and Dianese 1993). In Kerala, Cylindrocladium leaf blight is the major disease in eucalypt plantations—with the onset of the southwest monsoon, the disease assumes epidemic proportions and causes devastating damage to seedlings in the nursery and to young coppice shoots and one-year-old plants in the field (Jayashree et al. 1986). High incidence of leaf infection by Cylindrocladium spp. was observed only during the monsoon; during drier periods only root infection was prevalent (Sharma and Mohanan 1982). The most destructive disease of E. camaldulensis in the hot, humid conditions of lowland south and central Vietnam is leaf blight caused by Cylindrocladium quinqueseptatum (Old and Yuan 1994; Old et al. 1999a).

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North America showed that most Brazilian isolates were Cylindrocladium candelabrum, with some being Cylindrocladium scoparium, while all South African isolates were Cylindrocladium candelabrum (Crous et al. 1993a). Cylindrocladium ovatum also causes leaf disease on eucalypts in Brazil (El-Gholl et al. 1993). Cylindrocladium leaf blight is so serious in Brazil that selection for resistance to the disease is important in the Brazilian eucalypt breeding program (Blum and Dianese 1993). Ferreira (1989) listed 13 eucalypt species as being highly resistant. Inoculation studies showed that C. citriodora, C. torelliana, E. microcorys and E. saligna and a provenance of E. pellita were resistant and that E. camaldulensis, E. cloeziana, E. grandis, E. pilularis, E. resinifera, E. robusta, E. tereticornis and three other provenances of E. pellita were susceptible (Blum and Dianese 1993). Field observations and inoculations in Costa Rica indicated that C. citriodora and E. alba were very susceptible, C. maculata, E. grandis and E. saligna susceptible and E. deglupta highly resistant to Cylindrocladium leaf blight (Segura 1970). 9.11.7.2 Leaf spot and blight caused by Cylindrocladium quinqueseptatum Cylindrocladium quinqueseptatum Boedijn & Reitsma (teleomorph: Calonectria quinqueseptata Figueiredo & Namek.), with characteristic cylindrical, five-septate conidia (Table 9.7), is the most common Cylindrocladium species on eucalypts in south-east Asia, India and northern Australia. It is widespread on eucalypts in central and south Vietnam, where it is the most serious disease of eucalypts, causing death of 60% to 100% of seedlings in high rainfall areas of some provinces (Sharma 1994; Old et al. 1999b). Foliar diseases caused by Cylindrocladium quinqueseptatum or Cylindrocladium scoparium start as grey-green, irregular, water-soaked spots which may spread and kill large areas of the leaf, leading to distortion of leaves, premature defoliation and dieback of the shoots (B.N. Brown, unpubl. data) (Plates 9.27 and 9.28). Cylindrocladium quinqueseptatum typically affects the foliage and green shoots of young trees (Ivory 1999). On some eucalypt species, the species may form smaller rounded to irregular lesions, sometimes with purple margins (Old et al. 1999a) (Plate 9.27). White hyphae, conidiophores and clusters of conidia can be seen with a hand lens on the underside of lesions (Ivory 1999; Old et al.

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1999a). Inoculation studies with young plants have shown that the disease cycle is completed in less than five days (Ivory 1999). Often the lower crown is more affected, although in severe epidemics the disease can move into the upper crown (Old et al. 1999a). On older, chlorotic foliage, the necrotic area often has a green margin. In India, leaf spots on eucalypts caused by these species are irregular to circular, mostly two to six millimetres in diameter, with brown centres and red margins (Rattan and Dhanda 1985). The foliar symptoms are characteristic, often allowing diagnosis of the disease in the field. Cylindrocladium quinqueseptatum was responsible for outbreaks of leaf spot and shoot blight in nursery seedlings of several eucalypt species in Darwin (Pitkethley 1976; see Chapter 8) and in a young plantation of E. microcorys in north Queensland (Bolland et al. 1985). Glasshouse inoculations using one isolate indicated that the fungus was pathogenic on seedlings of E. microcorys and caused varying degrees of leaf spot and shoot blight on 10 eucalypt species. An unusual extended period of wet and windy weather was associated with the outbreak of the disease in Darwin (Pitkethley 1976). Cylindrocladium quinqueseptatum was also the principle cause of severe defoliation and shoot and tree death during late summer to autumn in experimental plots established in the wet tropics of north Queensland (B.N. Brown, pers. comm.). The pathogen was found on all 33 eucalypt species growing in the plots. Species with only slight to moderate infection included C. torelliana, E. cloeziana, E. deglupta, E. nigra, E. pellita, E. resinifera and E. signata. In young plantations in north Queensland, the species affects mainly E. camaldulensis, E. grandis, E. microcorys and E. urophylla but is less damaging on E. pellita (Ivory 1999). The pathogen was observed to be similarly less damaging on E. pellita than E. camaldulensis in south Vietnam (Nghia 1999a, 1999b; K.M. Old, pers. comm.). In Vietnam, several provenances and families of E. camaldulensis show field resistance to the disease (Sharma 1994; Nghia 1999a, 1999b). Severe disease caused by Cylindrocladium spp. in young planted eucalypts may result from the carry over of pathogens from the nursery or from infection after planting out. In tropical Queensland during the summer wet season of 1988–89, severe damage was caused by

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Cylindrocladium quinqueseptatum on two-year-old E. grandis and other species but there was little disease in a forest nursery only 25 kilometres away (Brown and Wylie 1991). Using simple climatic limits derived from published studies (mean minimum temperature of the coldest month greater than or equal to 16°C and mean annual precipitation greater than or equal to 1400 mm) (Sharma and Mohanan 1982; Bolland et al. 1985) and broad patterns of disease occurrence in south-east Asia, Booth et al. (1999) developed a computer-based model to predict locations with a high risk of leaf blight caused by Cylindrocladium quinqueseptatum. Cylindrocladium quinqueseptatum is one of the most common and destructive pathogens of eucalypts in tropical India (Anahosur et al. 1977; Sharma and Mohanan 1982). In several instances, more than one species of Cylindrocladium was recorded from the same specimen. For example, a complex of nine species was associated with a disease syndrome affecting seedlings in nurseries in Kerala (see Chapter 8) and several of these species caused root rot, severe to complete defoliation, branch dieback and even death of plants up to two years old in plantations (Sharma and Mohanan 1982; Sharma 1986). Cylindrocladium quinqueseptatum was isolated from eucalypt specimens collected from throughout Kerala, irrespective of host species or geographical location (Sharma and Mohanan 1982). Other species had a more limited distribution and narrower host range; for example, Cylindrocladium ilicicola occurred only at high altitudes on E. grandis. Fungicides were used to control the disease on seedlings of E. tereticornis in the Punjab (Rattan and Dhanda 1985). Seedling inoculations indicated variation in susceptibility of eucalypt species to Cylindrocladium quinqueseptatum and Cylindrocladium floridanum (Jayashree et al. 1986) and of provenances of two species to Cylindrocladium quinqueseptatum (Mohanan and Sharma 1986). Sharma and Mohanan (1991) found a differential interaction between several isolates of Cylindrocladium quinqueseptatum and selected eucalypt provenances. Cylindrocladium quinqueseptatum was also recorded from Brazil, where it caused damping-off and leaf spotting of E. saligna and E. tereticornis (Figueiredo and Namekata 1967).

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9.11.7.3 Leaf and shoot blight caused by Cylindrocladium gracile Molecular studies showed that the type culture of Cylindrocladium clavatum Hodges & L.C.May was the same as the earlier described Cylindrocladium gracile (Bugnic.) Boesew. (teleomorph: Calonectria gracilis Crous, M.J.Wingf. & Alfenas) (Crous et al. 1995b). This pathogen was associated with nursery diseases of eucalypts in South Africa (Crous et al. 1993b) and the death of 15-year-old eucalypts in Brazil (Hodges and May 1972). While Cylindrocladium gracile is normally a root pathogen of eucalypts in Brazil, it infected leaves following their inoculation with spore suspensions (Blum and Dianese 1993). The species (as Cylindrocladium clavatum) was widespread and caused serious root, stem and leaf infection of seedlings in nurseries in Kerala (Mohanan and Sharma 1985). Both Cylindrocladium gracile and Cylindrocladium scoparium caused leaf blight and stem canker of seedlings and leaf spot and blight of saplings in plantations of C. citriodora, E. macarthurii and E. tereticornis in north India (Pandotra et al. 1971; Upadhyaya and Nirwan 1979; Rattan and Dhanda 1985). Small reddish leaf spots with a distinct margin appeared in large numbers on leaves, became grey-brown to dark brown and gradually enlarged and coalesced to give a blight covering up to 75% of the leaf lamina. In some cases, the laminae were distorted, premature defoliation occurred and infection spread to the stem, causing stem cankers and dieback of young seedlings. Young seedlings were more affected than older ones. The lesions became covered with white, powdery conidiophores and conidia, particularly during high temperatures and humidity (Table 9.7) (Rattan and Dhanda 1985). The disease spread rapidly in humid weather, particularly when growing conditions reduced air circulation within the canopy (Sehgal et al. 1975). 9.11.7.4 Miscellaneous Cylindrocladium species Several other Cylindrocladium species have been recorded on eucalypts in Brazil. These include Cylindrocladium reteaudii (Bugnic.) Boesew. (El-Gholl et al. 1989; Crous and Wingfield 1992, 1994), Cylindrocladium pteridis F.A.Wolf, Cylindrocladium floridanum Sobers & C.P.Seym., Cylindrocladium heptaseptatum Sobers, Alfieri &

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Knauss (Ferreira 1989), Cylindrocladium ilicicola (Hawley) Boedijn & Reitsma [teleomorph: Calonectria pyrochroa (Desm.) Sacc.] (as Cylindrocladium spathulatum El-Gholl, Kimbr., E.L.Barnard, Alfieri & Schoult.; El-Gholl et al. 1986), Cylindrocladium parasiticum Crous, M.J.Wingf. & Alfenas (teleomorph: Calonectria ilicicola Boedijn & Reitsma; Crous et al. 1993c) and Cylindrocladium variabile Crous, B.J.H.Janse, D.Victor, G.F.Marais & Alfenas; Crous et al. 1993c) (teleomorph: Calonectria variabilis Crous, B.J.H.Janse, D.Victor, G.F.Marais & Alfenas; Crous et al. 1993g). In India, Cylindrocladium ilicicola and its teleomorph have been reported as the cause of a serious leaf spot disease of eucalypts (Reddy 1974) and Cylindrocladium colhounii Peerally was identified as the cause of stem lesions and leaf spots (Nair and Jayasree 1986). 9.11.7.5 Leaf blight caused by Cylindrocladiella species Five species of Cylindrocladiella have been reported from living tissues of eucalypts, causing damping-off, leaf spots or infections on the stems of cuttings (Crous and Wingfield 1993; Victor et al. 1998) (see Chapter 8). The species are distinguished from one another by the shape of the vesicle on the sterile filament (Table 9.7). Three species tested were less pathogenic on eucalypt seedlings than three Cylindrocladium species (Crous et al. 1993a, 1993b, 1993c). Cylindrocladiella peruviana (Bat., J.L.Bezerra & M.M.P.Herrera) Boesew. is common on eucalypt cuttings in Brazil and South Africa (P.W. Crous, unpubl. data).

9.11.8 Dothiorella eucalypti Dothiorella eucalypti (Berk. & Broome) Sacc. infects capsules (see Chapter 7) and also causes leaf spots on E. globulus. The fungus has been reported from Australia, Florida and Portugal (Gibson 1975; Farr et al. 1989) and is possibly the anamorph of Botryosphaeria ribis (see Chapter 8).

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and Foreman 1986) but it can also infect older plants in plantations. The species is common on seedlings in nurseries in New South Wales and also occurred on trees in a species and provenance trial in northern New South Wales (Simpson et al. 1997). A scorch develops on the margins of expanding leaves and eventually spreads to the shoots of young seedlings (Table 9.5) (see Chapter 8). Records of eucalypt hosts outside nurseries include C. torelliana, E. globulus, E. pauciflora, E. regnans, E. robusta, E. saligna and E. urophylla. The teleomorph and both synanamorphs of the fungus have been reported from E. globulus (Spegazzini 1882; Saccardo 1884; Shear and Doige 1921; United States Department of Agriculture 1960; Farr et al. 1989). The only other reports of Pilidium concavum have been those on E. pauciflora (Macauley and Thrower 1966) and E. regnans (Macauley 1979), both as Sclerotiopsis australasica Speg. The only additional report of Discohainesia oenotherae was on E. robusta and E. saligna (Sutton and Gibson 1977). The disease also occurs on eucalypts in plantations in southern China and India (B.N. Brown, unpubl. data). Hainesia lythri was isolated as an endophyte from seedling stems of E. globulus in Uruguay (Bettucci and Saravay 1993).

9.11.10 Macrohilum eucalypti Macrohilum eucalypti H.J.Swart was described from necrotic tissue associated with the biotrophic ascomycete Ophiodothella longispora on E. polyanthemos (Swart 1988) and is regarded as a weak pathogen which invades and kills leaf tissue weakened by this pathogen. Conidiomata are generally pycnidial although some may appear acervular when the ostiole has opened widely (Table 9.5). The species was subsequently recorded in New Zealand on pale brown, roughly circular lesions (1–4 mm diameter) with a dark brown margin on E. delegatensis, where they had no association with Ophiodothella longispora (Dick 1990).

9.11.9 Hainesia lythri The coelomycete Hainesia lythri (Desm.) Höhn. [teleomorph: Discohainesia oenotherae (Cooke & Ellis) Nannf.; syn. Pezizella oenotherae (Cooke & Ellis) Sacc; synanamorph: Pilidium concavum (Desm.) Höhn.] has been a particular problem in nurseries in South Africa (Lundquist

9.11.11 Pestalotiopsis disseminata Pestalotiopsis disseminata (Thüm.) Steyaert has been reported from necrotic spots and blights on eucalypt leaves in Australia and elsewhere. This distinctive fungus (Table 9.6) was recorded on several eucalypt species at one site in a species and provenance trial in

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Pycnidium and distinctive conidia of Readeriella mirabilis. Bars represent 10 µm. Drawing courtesy of P.A. Barber.

northern New South Wales (Simpson et al. 1997). It also caused leaf spots on E. grandis in India (Sharma et al. 1985) and a serious leaf margin necrosis of E. camaldulensis and E. urophylla and a dieback disease of E. camaldulensis in Vietnam, where it sporulated prolifically on affected stems (Sharma 1994).

9.11.12 Propolis emarginata Propolis emarginata (Cooke & Massee) Sherwood (syn. Stictis emarginata Cooke & Massee) has been found on pale-brown lesions on fallen leaves of eucalypts in Australia, New Zealand, Africa, India and North America (Table 9.4) (Sherwood 1977; Cannon and Minter 1986). Recently it was found in small, circular to irregular, bleached lesions, sometimes in association with an insect, on E. globulus growing in a plantation in southern Victoria (Plate 9.29) (Barber 1998). Its widespread

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occurrence suggests it may be an endophyte which sporulates in tissue killed by other factors (Cannon and Minter 1986).

9.11.13 Readeriella mirabilis Macauley and Thrower (1965) redescribed Readeriella mirabilis Syd. & P.Syd. from leaf spots on E. capitellata, from type material on E. capitellata and from cultures derived from apparently symptomless senescent and recently dead leaves of E. regnans. Macauley and Thrower (1965) considered the fungus to be a weakly competitive saprophyte. The fungus is very common on leaf spots in Australia (Park and Keane 1982c) and New Zealand (M. Dick, pers. comm.) and has been recorded from Brazil and the UK (Sutton 1980). In the type material on E. capitellata, circular, shiny spots up to 12 millimetres in diameter occur on one

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or other leaf surface. The fungus forms pycnidia in subepidermal stromata and has distinctive tetrahedral conidia (Fig. 9.26) (Table 9.5). Sutton (1971a) examined the type specimen and regarded Readeriella mirabilis as a secondary invader in lesions caused by Tracylla aristata (Cooke) Tassi (syn. Leptothyrium aristatum Cooke). Park and Keane (1982c) commonly found the fungus on small leaf spots (10–15 mm diameter) in association with insect damage or on lesions with M. cryptica on E. baxteri, E. globulus, E. obliqua and E. pauciflora. Symptoms failed to develop on leaves of seedlings of E. obliqua inoculated with a spore suspension prepared from culture, even when leaves were pricked with a needle before inoculation, providing evidence that the fungus is a secondary invader. The fungus was found commonly on E. nitens in a survey of foliar diseases of plantation species in Tasmania, often in lesions with other fungi (Yuan 1999) and it was common in leaf spots on E. globulus in plantations in Victoria (Barber 1998). Its common occurrence in leaf spots on eucalypts indicates an association with these trees but the precise nature of this association is still to be determined.

9.12 Conclusion Many other fungi have been reported from leaves of eucalypts (see Cooke 1892 and lists in Hedgecock 1926, Gibson 1975, Crous et al. 1989b, Sankaran et al. 1995a). In most cases, little information other than a basic description of the fungus is available. In some cases, it is not clear whether the fungus was found on living, attached leaves or in leaf litter. It is to be expected that with closer study some of these fungi will prove to be saprophytes or only weak parasites. Also, some fungi may have been described on more than one occasion under different names, as is the case with several reviewed here. The role and importance of endophytic fungi in eucalypts is yet to be fully explored. Several well-known pathogens (e.g. Phyllosticta eucalyptorum, Plectosphaera eucalypti, Hainesia lythri, Microsphaeropsis sp.) are commonly isolated as endophytes from apparently healthy stem and leaf tissue of E. globulus (P.W. Crous, unpubl. data; Crous et al. 1989d; Bettucci and Saravay 1993; Smith et al. 1996). The mode of infection of seedlings and young shoots by these fungi and the course of their development in older tissues is unknown.

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Many of the leaf-inhabiting fungi recorded from eucalypts are associated with leaf spots of minor importance on older, weakened leaves, perhaps reflecting the fact that leaves can remain on eucalypts for up to three years (Jacobs 1955). This may account for the number of new-encounter pathogens causing small leaf spots on trees growing outside Australia and for the number of complex fungal associations found in certain leaf spots. Most of the specialised fungal parasites of eucalypt leaves are indigenous to Australia, having coevolved with eucalypts and adapted in various ways to the peculiarities of eucalypts. Many fungal pathogens show specialised adaptations to the characteristically thick cuticle of eucalypt leaves, growing immediately beneath or even within the cuticle and many form sporocarps directly below stomata. Presumably, the fungi have also become adapted to the high content of potentially fungitoxic volatile oils and flavonoids in eucalypt leaves. The carryover between seasons of many pathogens on lightly infected leaves that remain attached to the tree may be an adaptation to the non-deciduous nature of the eucalypts. Many of these highly adapted eucalypt pathogens (e.g. Aulographina eucalypti, M. cryptica, Phaeophleospora epicoccoides, Plectosphaera eucalypti, Pseudocercospora eucalyptorum) occur widely outside Australia and have probably been distributed on vegetative planting material. It is highly unlikely that the specialised leaf pathogens are transmitted by seed, although some of the less specialised pathogens may be carried in debris accompanying poorly cleaned seed (see Chapter 7). Some quite specialised pathogens (e.g. several Mycosphaerella species, Puccinia psidii) have transferred to eucalypts from other hosts outside Australia, especially in southern Africa and South America, possibly reflecting the common occurrence of myrtaceous relatives of the eucalypts on the southern continents. Other species have been described recently from plantations in Indonesia, raising the possibility that these fungi have transferred to introduced eucalypts from the few eucalypt species indigenous to the Indonesian Archipelago. Management decisions require an estimate of the economic effect of leaf diseases in eucalypt plantations and forests. Parasites probably reduce the growth of eucalypts in their natural environment—seedlings grown in the absence of

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pathogens in glasshouses retain a larger proportion of their leaves than field-grown seedlings with leaf infections and growth rates of pest-free and disease-free eucalypts in plantations in other countries have generally outstripped those of the same species growing with their coevolved parasites in their natural environment (Heather 1971). However, it has proved difficult to assess the extent of growth reduction associated with moderate or even severe levels of these diseases. In some cases, heavy infection of seedlings and saplings has resulted in greatly reduced establishment rates in plantations (Park 1984; Crous and Wingfield 1996) but growth losses caused by more moderate levels of disease, especially in older trees, have rarely been quantified. Even the extent of infection is difficult to quantify, particularly on older trees, because of the inaccessibility of the active foliage and the associated sampling problems. Even the occurrence of identified diseases on the foliage of mature trees is poorly known, let alone their incidence and severity. Abbott et al. (1993) made an exemplary study of the extent of damage caused by insects and fungi, especially M. cryptica (Carnegie et al. 1997), on coppice regrowth and pole crowns in E. marginata forest in Western Australia. They discussed the methodological problems involved in such a study and provided a firm basis for further studies in this neglected area of research. Interestingly, in their study about 7% of the average proportion of leaf area damaged on the eight eucalypt species comprising the forest was caused by insects and only about 4% was caused by fungi, predominantly M. cryptica. The proportion of leaf area damaged on E. marginata, the dominant species, measured over several years at three locations on coppice and poles, ranged from about 8% to 39% for insects and about 1% to 10% for fungi (again, mainly M. cryptica). In a study of growth losses associated with fungal diseases and insect pest attack in northern New South Wales, Monocalyptus species generally suffered less leaf damage from fungi and insects than Symphyomyrtus species (Simpson et al. 1997). The main leaf pathogens observed in this study were Aulographina eucalypti, Colletotrichum gloeosporioides, Hainesia lythri, Harknessia spp., M. cryptica, Phomopsis sp., Pestalosphaeria sp., Sporothrix pitereka and Vermisporium falcatum. The mean heights and diameters of 27-month-old saplings were greater in untreated Monocalyptus

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than in untreated Symphyomyrtus species, but when fungicides and insecticides were applied, the mean growth of Symphyomyrtus species equalled or exceeded that of the Monocalyptus species, even though the chemical treatments only partially controlled the fungus and insect damage. In a study of four dense stands of sapling regeneration, each consisting of two dominant eucalypt species, Burdon and Chilvers (1974a) found that parasite damage was responsible for an average of more than 20% effective leaf area loss, with a range of 7% to 44%. A large proportion of this loss, up to 30%, was attributable to fungal pathogens. Studies of the effects on eucalypt growth of artificial defoliation and bud removal and defoliation by phasmatids (Bamber and Humphreys 1965; Mazanec 1966, 1967, 1968; Burdon and Chilvers 1974a) and protection against defoliating insects (Morrow and La Marche 1978) have indicated that loss of effective leaf area as a result of parasitism can significantly reduce tree growth. There was a negative correlation between growth of provenances of E. globulus and disease severity, even when overall disease severity was low (Carnegie et al. 1994; Barber 1998). In reviewing many studies of the effect of natural or artificial defoliation in trees in general, Kulman (1971) concluded that the overwhelming majority of studies showed a direct correlation between the severity of defoliation and reduction in tree growth. The well-known ability of eucalypts to regenerate crowns following defoliation could reduce the effect of leaf parasites and may indicate adaptation of eucalypts to regular or sporadic defoliation by parasites (Heather 1971). Native eucalypt stands usually consist of two or more codominant eucalypts from genetically isolated subgenera, which appear to share the same niche and yet remain in equilibrium (Pryor 1959). Host-specific foliar parasites (insects and fungi) may help maintain the equilibrium between eucalypt species in these mixed stands (Burdon and Chilvers 1974a, 1974b). While many foliar parasites have a wide host range, they often display a degree of host specificity towards trees of particular eucalypt subgenera in natural stands. If one eucalypt species in a mixed stand becomes more common at the expense of the other, parasites specific to the dominant species may increase in number and reduce its competitive ability. Relatively few of the foliar pathogens of eucalypts have been studied in sufficient detail to permit firm

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conclusions about their host specificity in natural stands. In their study of parasite damage in mixedspecies stands of sapling regrowth, Burdon and Chilvers (1974a) concluded that of the total of 27 leaf parasites (insects and fungi) collected, 11 occurred specifically on species of one eucalypt subgenus or the other. Some fungi appear to display considerable host specificity (e.g. M. delegatensis, M. nubilosa, M. walkeri, Pachysacca spp., Phaeophleospora spp., Sporothrix pitereka), while others have wide host ranges that include eucalypt species from several subgenera (e.g. M. cryptica, M. swartii, Phaeothyriolum microthyrioides) or even other genera (e.g. Aulographina eucalypti on Angophora and Agonis). However, many collections of these fungi have been made from ornamental trees, nurseries, roadside regrowth or young plantations, where conditions differ from those in native forests and the functional host specificity of trees in their native communities may not be evident, as was reported for Phaeophleospora epicoccoides (Heather 1967a). When inoculated in the laboratory, M. cryptica and M. nubilosa caused lesions on eucalypt species on which they were not found in forests (Park 1984). Aulographina eucalypti was found to have a wide host range on planted eucalypts (Wall and Keane 1984) although in native forests it occurs primarily on species of the subgenus Monocalyptus and can be used to identify such species (Heather 1971). While host specific parasites may contribute to the maintenance of diversity of eucalypt species in lowland native forests, the diversity of species and the consequent wider spacing of trees of each species in the forests probably reduces the occurrence of epidemics of leaf parasites. Selection of a degree of resistance to leaf parasites probably contributes to their control in forests. While there has been little study of disease resistance mechanisms in eucalypt leaves, several pathogens (e.g. Aulographina eucalypti, Blastacervulus eucalypti, Coniothyrium sp.) are restricted by the formation of wound cork barriers (Heather 1961). Within the outbreeding eucalypt species in these forests there is great variation in the resistance of individual trees to leaf parasites (Burdon and Chilvers 1974a; Duncan 1989). Strong selection for disease resistance is to be expected during the reduction of the plant population from hundreds of thousands of seedlings per hectare to a few hundred mature trees per

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hectare (Heather and Griffin 1978). There is evidence that the selection pressure is greater, resulting in greater resistance, in provenances from localities where environmental conditions favour a particular pathogen than from localities unfavourable for disease development (Carnegie et al. 1994). Selection of species, provenances, families and clones with higher levels of disease resistance from within the great diversity of eucalypts in native communities in Australia (see Chapter 2) will contribute greatly to control of foliar diseases of eucalypts in plantations (see Chapter 18). Selection of resistant genotypes from within the pool of genetic resources collected in various countries outside Australia has already been important in disease management in those countries (see Chapter 22). Accordingly, it is critical that we conserve the greatest range possible of this priceless genetic resource, including diversity within provenances. Epidemics of Mycosphaerella species in eucalypt plantations in New Zealand and South Africa have clearly shown the destructive potential of foliar pathogens of eucalypts. Heather and Griffin (1978) considered that the potential for epidemics of leaf pathogens in eucalypt plantations in Australia is even greater than in plantations outside Australia: within Australia, plantations are exposed to a wider range of well-adapted parasitic fungi than plantations elsewhere. Heather and Griffin (1978) warned of the likelihood of greatly increased incidence and severity of leaf diseases in plantations consisting of a single species, provenance or clone of eucalypts than in the more genetically diverse native forests. Initial observations in eucalypt plantations in southern Australia confirm these predictions and indicate that these diseases, along with insect pests, are likely to have an important effect in plantations (Park 1984). The severity of leaf diseases caused by less specialised pathogens such as Cylindrocladium species on eucalypts growing under stress in environments outside their natural range, particularly in the wet tropics, is also instructive. Matching eucalypt genotypes to plantation sites in order to reduce stress on the trees and the occurrence of associated stress-induced diseases will be an important aspect of plantation practice and is a further reason for the conservation of the genetic diversity of eucalypts within their natural range. Exclusion of the new-encounter pathogens, particularly the eucalypt rust (Puccinia psidii) and

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M. juvenis, already adapted to exotic eucalypts, will be important for the health of both the native eucalypt-dominated vegetation in Australia and the fledgling eucalypt plantation industries in Australia and elsewhere.

9.13 Acknowledgments We thank Mr Carlos Reinosa and Professor Luiz Carlos Federizzi for translating Spanish and Portuguese papers, Dr M.J. Duncan and Mr A.J. Carnegie for obtaining references and Drs D.R. Burgess, J.C. Dianese, M. Dick and V. Beilharz for reviewing the manuscript. The chapter is dedicated to the memory of Dr H.J. Swart, whose detailed studies of the leaf-infecting fungi of the eucalypts greatly facilitated their investigation by others.

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Sobers, E.K. (1968). Morphology and host range of Cylindrocladium pteridis. Phytopathology 58, 1265–1270. Sobers, E.K. and Seymour, C.P. (1967). Cylindrocladium floridanum sp. n. associated with decline of peach trees in Florida. Phytopathology 57, 389–393. Soni, K.K. and Jamaluddin (1990). Eucalyptus litter decomposition in tropical dry deciduous forest of Madhya Pradesh. Indian Forester 116, 286–291. Spaulding, P. (1958). Diseases of Foreign Forest Trees Growing in the United States. An annotated list. USDA Agriculture Handbook 139. (US Department of Agriculture: Washington, DC.) Spegazzini, C. (1882). Fungi Argentini: additis Nonnullis Brasiliensibus Montevideensibusque Pugillus quartus. Anales de la Sociedad Cientifica Argentina. Buenos Aires 13, 11–35, 60–64. Reprinted 1971, Linnaeus Press, Amsterdam, Holland pp. 231–260. Spooner, B.M. (1981). New records and species of British microfungi. Transactions of the British Mycological Society 76, 265–301. Stefanatos, A. (1993). A study of the severity of leaf parasites on Eucalyptus globulus in a progeny trial and E. regnans in a silvicultural systems trial. BSc Honours Thesis, School of Botany, La Trobe University, Bundoora, Victoria. Sutton, B.C. (1971a). Coelomycetes . IV. The genus Harknessia, and similar fungi on Eucalyptus. Mycological Papers, No. 123. (Commonwealth Mycological Institute: Kew.) Sutton, B.C. (1971b). Staninwardia gen. nov. (Melanconiales) on Eucalyptus. Transactions of the British Mycological Society 57, 539–542. Sutton, B.C. (1974). Miscellaneous coelomycetes on Eucalyptus. Nova Hedwigia 25, 161–172. Sutton, B.C. (1975). Eucalyptus microfungi. Satchmopsis gen. nov., and new species of Coniella, Coniothyrium and Harknessia. Nova Hedwigia 26, 1–16. Sutton, B.C. (1980). The Coelomycetes. Fungi Imperfecti with Pycnidia, Acervuli and Stromata. (Commonwealth Mycological Institute: Kew.) Sutton, B.C. and Ganapathi, A. (1978). Trimmatostroma excentricum sp. nov. , on Eucalyptus from New Zealand and Fiji. New Zealand Journal of Botany 16, 529–533. Sutton, B.C. and Gibson, I.A.S. (1977). Pezizella oenotherae (conidial state Hainesia lythri). CMI Descriptions of Pathogenic Fungi and Bacteria No. 535. (Commonwealth Mycological Institute: Kew.) Sutton, B.C. and Pascoe, I.G. (1989a). Reassessment of Peltosoma, Stigmina and Batcheloromyces and description of Hyphothyrium gen. nov. Mycological Research 92, 210–222. Sutton, B.C. and Pascoe, I.G. (1989b). Addenda to Harknessia (Coelomycetes). Mycological Research 92, 431–439.

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Swart, H.J. (1981a). Australian leaf-inhabiting fungi XI. Phyllachora eucalypti. Transactions of the British Mycological Society 76, 89–95. Swart, H.J. (1981b). Taxonomic problems of leaf pathogens of eucalypts. In Eucalypt Dieback in Forests and Woodlands. (Eds K.M. Old, G.A. Kile and C.P. Ohmart) pp. 147–150. (CSIRO: Melbourne.) Swart, H.J. (1982a). Australian leaf-inhabiting fungi XIII. Seimatosporium species on Eucalyptus. Transactions of the British Mycological Society 78, 265–269. Swart, H.J. (1982b). Australian leaf-inhabiting fungi XIV. The genus Pachysacca. Transactions of the British Mycological Society 79, 261–269. Swart, H.J. (1982c). Australian leaf-inhabiting fungi XV. Ophiodothella longispora sp. nov. Transactions of the British Mycological Society 79, 566–568. Swart, H.J. (1986a). Australian leaf-inhabiting fungi XXI. Coniothyrium on Eucalyptus. Transactions of the British Mycological Society 86, 494–496. Swart, H.J. (1986b). Australian leaf-inhabiting fungi XXII. Microthyrium -like fungi on Eucalyptus. Transactions of the British Mycological Society 87, 81–91. Swart, H.J. (1986c). Australian leaf-inhabiting fungi XXIV. Coma circularis and its teleomorph. Transactions of the British Mycological Society 87, 603–612. Swart, H.J. (1987). Australian leaf-inhabiting fungi XXV. Dothidella inaequalis and Montagnella eucalypti. Transactions of the British Mycological Society 89, 483–488. Swart, H.J. (1988). Australian leaf-inhabiting fungi XXVI. Some noteworthy coelomycetes on Eucalyptus. Transactions of the British Mycological Society 90, 279–291. Swart, H.J. and Walker, J. (1988). Australian leafinhabiting fungi XXVIII. Hendersonia on Eucalyptus. Transactions of the British Mycological Society 90, 633–641. Swart, H.J. and Williamson, M.A. (1983) Australian leaf inhabiting fungi XVI. Vermisporium, a new genus of coelomycetes on Eucalyptus leaves. Transactions of the British Mycological Society 81, 491–502. Theodore, M.L. (1991). Inoculation and isozyme studies of fungal leaf pathogens of Eucalyptus. Honours Thesis, La Trobe University, Bundoora, Victoria. Thu, Pham Quang, Old, K.M., Dudzinski, M.J. and Gibbs, R.J. (1999). Results of eucalypt disease surveys in Vietnam. In Proceedings of Workshop on Eucalypt Diseases. ACIAR, Ho Chi Minh City, Vietnam, p. 6. (CSIRO Forestry and Forest Products, Canberra and Forest Science Institute of Vietnam, Hanoi.) Thümen, F. von (1881). Contributiones ad floram mycologicum lusitanicum. Instituto Coimbra 28, 1–54. United States Department of Agriculture (1960). Index of Plant Diseases in the United States. USDA Handbook No. 165. (US Department of Agriculture: Washington, DC.)

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Upadhyay, R.K. (1981). Sporostasis between phylloplane microfungi fungi and a foliar pathogen. Experientia 37, 833–835. Upadhyay, R.K. (1986). Effect of zineb and copper oxychloride on leaf inhabiting microfungi of Eucalyptus globulus. Pesticides 20, 34–39. Upadhyay, D.N. and Bordoloi, D.N. (1975). New records of diseases in cultivated essential oil bearing plants from North-East India. Indian Phytopathology 28, 532–534. Upadhyaya, J. and Nirwan, R.S. (1979). Cylindrocladium blight of Eucalyptus citriodora. Indian Phytopathology 32, 118–120. Victor, D., Crous, P.W., Janse, B.J.H. and Wingfield, M.J. (1997). Genetic variation in Cylindrocladium floridanum and other morphologically similar Cylindrocladium species. Systematic and Applied Microbiology 20, 268–285. Victor, D., Crous, P.W., Janse, B.J.H., van Zyl, W.H., Wingfield, M.J. and Alfenas, A.C. (1998). Systematic appraisal of species complexes within Cylindrocladiella. Mycological Research 102, 273–279. Viégas, A.P. (1961). Indice de fungos da América do Sul. Seá o de Fitopatologia Instituto Agronìmico de Campinas, Brazil. Viljoen, A., Wingfield, M.J. and Crous, P.W. (1992). Fungal pathogens in Pinus and Eucalyptus seedling nurseries in South Africa: a review. South African Forestry Journal 161, 45–51. Walker, J. (1962). Notes on plant parasitic fungi. I. Proceedings of the Linnean Society of New South Wales 87, 162–176. Walker, J. and Bertus, A.L. (1971). Shoot blight of Eucalyptus spp. caused by an undescribed species of Ramularia. Proceedings of the Linnean Society of New South Wales 96, 108–115. Walker, J., Sutton, B.C. and Pascoe, I.G. (1992). Phaeoseptoria eucalypti and similar fungi on Eucalyptus, with description of Kirramyces gen. nov. (Coelomycetes). Mycological Research 96, 911–924. Wall, E. and Keane, P.J. (1984). Leaf spot of Eucalyptus caused by Aulographina eucalypti. Transactions of the British Mycological Society 82, 257–273. Wallace, G.B. (1947). Annual Report of Plant Pathologist. In Report of the Department of Agriculture, Tanganyika. Wang, W.-y. (1992). Survey of Eucalyptus diseases in Taiwan. Bulletin of the Taiwan Forest Research Institute, New Series 7, 179–194. Wardlaw, T. and Phillips, T. (1990). Nursery diseases and their management at the Forestry Commission Nursery, Perth. Tasforests 2, 21–26.

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Webb, R.S. (1983). Seed capsule abortion and twig dieback of Eucalyptus camaldulensis in South Florida induced by Botryosphaeria ribis. Plant Disease 67, 108–109. Weste, G. (1980). Vegetation changes as a result of invasion of forest on krasnozem by Phytophthora cinnamomi. Australian Journal of Botany 28, 139–150. Weston, G.C. (1957). Exotic forest trees in New Zealand. Statement prepared for the Seventh British Commonwealth Forestry Conference, Australia and New Zealand. (Reissued as New Zealand Forest Service Bulletin 13). Wilcox, M.D. (1982a). Preliminary selection of suitable provenances of Eucalyptus regnans for New Zealand. New Zealand Journal of Forestry Science 12, 468–479. Wilcox, M.D. (1982b). Selection of genetically superior Eucalyptus regnans using family tests. New Zealand Journal of Forestry Science 12, 480–493. Wingfield, M.J., Crous, P.W. and Swart, W.J. (1993). Sporothrix eucalypti (sp. nov.), a shoot and leaf pathogen of Eucalyptus in South Africa. Mycopathologia 123, 159–164. Wingfield, M.J., Crous, P.W. and Peredo, H.L. (1995). A preliminary, annotated list of foliar pathogens of Eucalyptus spp. in Chile. South African Forestry Journal 173, 53–57. Wingfield, M.J., Crous, P.W. and Boden, D. (1996). Kirramyces destructans sp. nov., a serious leaf pathogen of Eucalyptus in Indonesia. South African Journal of Botany 62, 325–327. Winter, G. (1884). Rabenhostii Fungi europaei et extraeuropaei exsiccati cura Dr Winter. Centuria XXI et XXXII. Hedwigia 23, 164–175. Yip, H.Y. (1989). Four species of Anthostomella from Australia. Mycological Research 93, 75–82. Yip, H.Y. (1997). Phloeosporella eucalypticola sp. nov. from a hybrid between Eucalyptus radiata and E. dives in Australia. Australasian Plant Pathology 26, 26–27. Yuan, Z.Q. (1999). Fungi Associated with Diseases Detected During Health Surveys of Eucalypt Plantations in Tasmania. (School of Agricultural Science, University of Tasmania: Hobart.) Yuan, Z.Q., Wardlaw, T. and Mohammed, C. (1999). A new species of Dichomera (Mitosporic fungus) described on eucalypt leaves from Tasmania, Australia. Nova Hedwigia (in press). Zandvoort, A. (1977). Mycosphaerella nubilosa on five different provenances of Eucalyptus delegatensis in Kaingaroa Forest. New Zealand Forest Service Report No. 54 (unpublished).

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Cankers are infections of the bark or bark and cambium that can occur on all parts of a tree. In severe cases they cause twig and branch death, coppice death and stem distortion. Cankers are extremely common and are usually of limited extent because fungal invasion triggers a suite of cellular and tissue responses in the phloem, cambium and wood that restrict fungal invasion. In eucalypts, damage to the cambium often results in the formation of kino veins. The rate at which the tree responds to invasion by canker fungi can be modified by environmental conditions, so that stress, such as that caused by defoliation, can result in increased canker size. The two most severe canker diseases of eucalypts growing outside Australia are caused by Erythricium (Corticium) salmonicolor and Cryphonectria cubensis. Both diseases are controlled by selecting resistant species, provenances and genotypes. Although both Erythricium salmonicolor and Cryphonectria cubensis occur in Australia, either they have not been recorded from eucalypts or do not cause significant disease. Common canker diseases of eucalypts in Australia are caused by opportunistic pathogens such as Botryosphaeria spp. and Endothia gyrosa.

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10.1 Introduction If a living tree is examined carefully, small superficial fungal infections often can be found in the bark of the main stem and roots, and in some cases these infections may be deep enough to cause the death of the vascular cambium, killing twigs in the lower crown or killing roots. Unless the tree is severely stressed these lesions are usually limited in size by the defence mechanisms of the host. Many fungi can be isolated from them and when these are inoculated into healthy bark they are able to persist in wounds and have a limited ability to invade adjacent healthy tissue. These superficial infections are referred to as ‘cankers’, defined as ‘sunken necrotic lesion(s) of main root, stem or branch arising from disintegration of tissues outside the xylem cylinder, but sometimes limited in extent by host reactions which can result in more or less massive overgrowth of surrounding tissues’ (Federation of British Plant Pathologists 1973). Fungi that cause cankers grow primarily in the bark, or bark and cambium. If invasion of the wood occurs it is usually of very limited extent and the fungi are unable to spread extensively through the xylem and reinfect the phloem (Boyce 1961). Cankers may be annual, in which case the inciting organism is active for one year only and the damaged host tissue is sloughed off or overgrown (Plates 10.1 and 10.2), or perennial, in which case the pathogen is active for many years although fungal invasion is repeatedly checked by the response of the host (Boyce 1961). In perennial cankers the cambium, bark external to the cambium and adjacent wood are killed (Plates 10.3 to 10.6). Dead bark sloughs off and the underlying wood is exposed. New wood may be formed by the surrounding healthy tissue but not in the canker, so that with time the canker appears to penetrate deeply into the wood (Plates 10.5 and 10.6) (Boyce 1961). Manion (1981) recognised four types of canker: saprophytic, annual, perennial and diffuse. The fungi that cause these different cankers have a range of pathogenicity. Those that cause saprophytic cankers can invade only weakened tissue because they cannot overcome the chemical or mechanical defences of healthy tissue. Greater pathogenicity is exhibited by the fungi that cause annual and perennial cankers, although Manion considered that all of these fungi

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are opportunistic invaders of damaged plant tissue. Diffuse cankers are caused by the most pathogenic fungi, which invade rapidly and provoke a minimal or ineffectual response from the host. These cankers cause extensive death of bark and cambium, resulting in discoloured or sunken lesions which may girdle stems or branches (Plates 10.3 and 10.4). The ability of the fungus to cause a canker is determined therefore partly by the pathogenicity of the fungus and partly by the rapidity of the host’s response to infection.

10.2 Fungal invasion and host responses Although many of the investigations discussed in this section have been carried out on trees other than eucalypts, they are, however, pertinent because they describe the non-specific responses of bark, cambium and sapwood to damage, including that triggered by pathogenic invasion. Where eucalypts have been studied, the responses appear similar and damaged tissue is either sloughed off or localised within the stem or root.

10.2.1 Barriers to invasion Desiccation of woody plants is prevented by the periderm, and this suberised tissue may also prevent invasion by fungi. Wounding is usually a prerequisite for infection, so that cankers are associated with mechanical damage, branch stubs, insect damage or bark splits (Boerboom and Maas 1970; Hodges et al. 1979; Davison and Tay 1983). Wound inoculation is usually used to demonstrate pathogenicity of fungi isolated from cankers, although infection may occur through stomata and lenticels (Michailides 1991). Although Lasiodiplodia theobromae (Pat.) Griffon & Maubl. (as Botryodiplodia theobromae Pat.) invaded Eucalyptus tereticornis in the absence of wounding (Sharma et al. 1984a), and zoospores of Phytophthora (Ph.) cinnamomi Rands infected unwounded woody roots (Dell and Malajczuk 1989) and stems (O’Gara et al. 1996) of E. marginata, in all cases more infections occurred when the plants were wounded. Bark tissues internal to the periderm contain antimicrobial chemicals. These are present in an effective form and in sufficient concentration to inhibit invasions by microorganisms (Stoessl 1983), so that if the periderm is breached, most organisms colonising the wound are unable to persist.

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10.2.2 Cellular and tissue responses to invasion

Symphyomyrtus and the genus Corymbia (Tippett et al. 1985).

10.2.2.1 Phloem

10.2.2.2 Vascular cambium

When the periderm is damaged and the underlying phloem is exposed to the air there are rapid cellular and tissue responses that result in the formation of a new, necrophylactic periderm. These responses were studied in conifers by Mullick (1977), and his interpretation was modified and developed by Biggs (1985a, 1985b), who described these general responses in many dicotyledonous trees. Within three days of wounding, cellular changes, indicated by the appearance of distinctly visible nuclei and tissue hypertrophy, occur within phloem ray parenchyma about one millimetre internal to the wound. These changes spread centripetally, being observed last in the phellogen and phelloderm cells of the damaged periderm. They are the first indication of the formation of a boundary zone around the wound. Initially lignin and then suberin are deposited in the walls of the boundary zone cells, preventing desiccation of underlying tissue. Finally a periderm develops internal to this lignosuberised boundary zone and spreads centripetally so that a new, necrophylactic periderm is formed around the wound (Biggs 1992a).

The characteristic response to cambial damage in eucalypts is the formation of kino, an exudate rich in a range of polyphenolics including leucoanthocyanins, catechins and ellagitannins (Hillis 1962, 1972). Ellagitannins formed in heartwood of Quercus alba L. have been shown to be fungistatic (Hart and Hillis 1972). Within a few days of wounding, periclinal cell divisions in the vascular cambium result in a broad band of traumatic parenchyma (Skene 1965; Tippett 1986). Polyphenols accumulate within these parenchyma cells. The cells within the putative kino vein collapse and release their contents into the vein lumen, whereas cells around the vein begin to divide, forming a peripheral cambium. Cells produced by this cambium contain polyphenols, and they also eventually collapse, releasing their contents into the lumen (Skene 1965). When the vascular cambium recommences division, kino veins are included in either the xylem or phloem, the eventual position depending on the eucalypt species (Tippett 1986).

When the periderm is damaged and underlying tissues are invaded by a pathogen the response of the host may be very similar to the response to wounding (Biggs 1992b). Tippett et al. (1983) and Tippett and Hill (1984) described cellular and tissue responses which occurred in stem and root phloem of E. marginata following wound inoculation with Ph. cinnamomi. In the necrotic area during the first three weeks after infection, starch accumulated in axial parenchyma and ray cells, and was then replaced by tannins and other polyphenols. Sieve tubes were blocked by callose deposited on sieve plates. Polyphenols also accumulated in the phloem adjacent to the developing lesion. Cellular hypertrophy preceded the formation of a necrophylactic periderm which delimited living and dead tissue. In some, but not all, lesions an exophylactic periderm, similar in structure to the normal periderm of E. marginata bark, formed internal to the necrophylactic periderm. This pattern of response to invasion was observed in stems of the Eucalyptus subgenera Monocalyptus and

Eucalypts are able to rapidly regenerate both cambium and bark even when large areas of bark are damaged down to the cambium. Chudnoff (1971) found that 18 out of 40 eucalypt species tested had regenerated at least two-thirds of the bark in the girdled region within two weeks of damage. Kino veins are also, but not invariably, formed following pathogenic invasion of phloem and death of the vascular cambium (Tippett et al. 1985). When E. marginata coppice stems were inoculated with Ph. cinnamomi at different times of the year, kino veins formed when the inner phloem was invaded in summer and autumn, but only rarely in winter and spring (Tippett et al. 1983). Kino veins formed more rarely in roots than in stems. 10.2.2.3 Sapwood Some of the most destructive eucalypt cankers are caused by fungi such as Cryphonectria cubensis and Erythricium salmonicolor that are able to invade sapwood as well as bark (Hilton 1958; Boerboom and Maas 1970; Hodges and Reis 1976). Sapwood invasion often results in discolouration of the wood underlying the canker, reduced water movement through the colonised wood and wilting of leaves

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distal to the canker (Bramble 1938; Nutman and Roberts 1952). Sapwood usually responds rapidly to pathogen invasion (Blanchette 1992). Stress metabolites and phytoalexins, believed to be formed by lysing parenchyma cells, appear in the sapwood (Kemp and Burden 1986), and xylem internal to the wound becomes non-conducting (Coutts 1977; Mullick 1977). Plugging of vessels and tracheids by tyloses, gums and resins protects the functioning of undamaged sapwood and reduces the axial spread of opportunistic microorganisms in wounds. Radial and tangential spread of microorganisms is restricted by the accumulation of phenols in axial and ray parenchyma (Shortle 1979) and suberin may be deposited in walls of tyloses and parenchyma cells (Biggs 1987; Schmitt and Liese 1991). In addition to these modifications of existing cells, a new tissue consisting of a barrier zone of axial parenchyma or axial parenchyma and resin ducts is formed at the vascular cambium (Sharon 1973; Tippett and Shigo 1981; Tippett et al. 1982). Cell walls in this barrier zone may become heavily suberised (Pearce and Holloway 1984; Pearce 1990), preventing invasion of xylem formed in subsequent years by opportunistic microorganisms localised within the damaged tissue. Boddy (1992) and her coworkers have suggested that, following damage, non-specific responses which maintain sapwood function also limit invasion by microorganisms because functional sapwood is an inhospitable environment for most fungi. Shigo and his coworkers (Shigo 1979) have proposed a model of compartmentalisation of decay in trees (CODIT) in which host responses are interpreted as being largely triggered by invasion of pathogens and other microorganisms. When eucalypt sapwood is wounded, phenols are formed rapidly in the tissue adjacent to the injury (Mireku and Wilkes 1988). These phenols persist in highest concentration at the boundary between normal and discoloured sapwood (Wilkes 1985; Mireku and Wilkes 1989). The rapidity with which phenols are formed depends on the time of the year of wounding (Mireku and Wilkes 1989). A barrier zone of traumatic parenchyma forms in the cambium; in some species this barrier zone develops into a kino vein (Tippett 1986; Wilkes 1986).

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The parenchyma cells in this zone may become lignified (Wilkes 1986).

10.3 Effect of plant stress on the development of cankers Eucalypts, particularly in plantations (Plates 10.7 and 10.8) but sometimes in native stands (Plates 10.3 to 10.6), can be severely affected by cankers. This may be the result of the susceptibility of particular species or provenances to a particular pathogen (Hodges and Reis 1976; Alfenas et al. 1983), the pathogenicity of particular local isolates of a pathogen (Alfenas et al. 1983; Sharma et al. 1988), or the build up of inoculum on alternate hosts (Sharma et al. 1984b). Commonly, however, high incidence and severity of cankers are associated with environmental stress, particularly drought (van der Westhuizen 1965; Shearer et al. 1987). Host responses that are triggered following tissue damage and invasion by microorganisms are enzymemediated so that their rate will depend on ambient temperature, tissue hydration and availability of ATP and substrates. As plants do not always grow in ideal conditions, host responses following tissue damage are often modified by temperature, nutrient status and water supply (Schoeneweiss 1975). Houston (1981, 1987) and Manion (1981) have developed this concept to interpret many decline and dieback diseases of trees (see Chapter 17). Houston (1987) has drawn attention to the effects of environmental stress in the production, transport and storage of carbohydrates, as well as the absorption of water and mineral nutrients from soil. The effect of water stress on canker development and size has been assessed by several workers. In many species cankers are larger on drought stressed than on unstressed plants (Schoeneweiss 1975). Mullick (1977) showed that this occurred because of the slower formation of the boundary zone in the phloem of water-stressed trees. The invading fungi may also penetrate more deeply into xylem in drought-stressed trees (McPartland and Schoeneweiss 1984; Chou 1987). There is evidence, however, that eucalypts do not follow this pattern. When Old et al. (1990) subjected seedlings of several eucalypt species to drought stress, they found no effect on canker size, although they pointed out the need for studies with larger trees in the field. Cryphonectria cubensis caused smaller lesions on potted, drought-stressed

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E. grandis than on non-stressed seedlings (Swart et al. 1992). Cankers caused by Ph. cinnamomi in stems of E. marginata were longer when bark was well hydrated than when bark moisture content was low (Tippett and Hill 1983; Tippett et al. 1987). It was shown experimentally that eucalypt defoliation results in reduced soluble carbohydrates and starch in E. regnans and E. grandis, and that cankers caused by Endothia gyrosa on defoliated E. regnans saplings, and by Botryosphaeria ribis on defoliated E. regnans and E. delegatensis seedlings were significantly longer than on similar, nondefoliated control trees (Old et al. 1990). Defoliation of Quercus rubra L. infected with Pezicula cinnamomea (DC.) Sacc. resulted in larger cankers being formed than on non-defoliated trees because defoliated trees were less able to produce effective wound barriers (Kehr 1991). Pathogenicity tests indicate that canker fungi such as Botryosphaeria ribis and Endothia gyrosa are generally opportunists which have limited ability to invade the tissues of healthy eucalypts, while field observations show that these fungi are often associated with larger or deeper lesions (Shearer et al. 1987; Old et al. 1990; van der Westhuizen et al. 1993). Stress factors such as defoliation may be invoked to explain discrepancies (Old et al. 1990) but the mechanisms by which such factors affect the host’s response on a cellular and tissue level remain to be explained. Another possibility is that some pathogenic canker fungi exist as latent infections, symptoms developing only when the host is stressed (Nathaniels and Taylor 1983). For example, stem end rot of Mangifera indica L. is caused by several fungi including species of Botryosphaeria. These fungi can persist as latent infections in branches and pedicels, and fruit invasion frequently originates from these sources (Johnson et al. 1992). Smith et al. (1996a) have observed both Botryosphaeria dothidea and Sphaeropsis sapinea (Fr.) Dyko & B.Sutton to be endophytic in species of Pinus and Eucalyptus in South Africa and have suggested that the rapid ingress of both fungi in stressed or damaged trees may be explained by their presence as endophytes in healthy tissue prior to damage. Fisher et al. (1993) compared endophytes in leaves, xylem and bark collected from E. nitens trees in Canberra, Australia, and Exeter, England. The most common endophyte in Australian twig samples was Cytospora eucalypticola Van der Westh., and the most common

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fungus in samples from the trees in Exeter was Botryosphaeria dothidea. Carroll (1988) suggested that endophytes have evolved from plant pathogens which have a long latent period. Latent pathogens and endophytes may be much more common in woody plants than is generally recognised. For example, Wildman and Jones (1991) isolated 189 fungal species from the roots of 139 wind-thrown trees. The role of latency and environmental stress in symptom development in trees infected by canker fungi requires further research.

10.4 Major canker diseases of eucalypts Canker diseases caused by Erythricium salmonicolor and Cryphonectria cubensis are sufficiently severe in plantation-grown eucalypts in several tropical and subtropical countries to warrant their control by the selection of resistant species, provenances or genotypes. Although Erythricium salmonicolor is common on fruit trees in New South Wales (Penrose 1956), this fungus has not been recorded on eucalypts in Australia and Cryphonectria cubensis is known in Australia only as a cause of root cankers on E. marginata in native forest (Davison and Coates 1991).

10.4.1 Pink disease (Erythricium salmonicolor) 10.4.1.1 Symptoms and epidemiology Erythricium salmonicolor (Berk. & Broome) Burds. [syn. Corticium salmonicolor Berk. & Broome, Phanerochaete salmonicolor (Berk. & Broome) Jülich, Pellicularia salmonicolor (Berk. & Broome) Dastur, Botryobasidium salmonicolor (Berk. & Broome) Venkatarayan] (anamorph: Necator decretus Massee), the cause of pink disease, is an important pathogen of many plantation crops such as rubber and cocoa in tropical and subtropical regions (Hilton 1958; Mordue and Gibson 1976). The disease is named for the pink to salmoncoloured, scattered or coalescent pustules and corticioid basidiocarps that are formed on the surface of branches and stems of trees with advanced infections. Bark cracks and girdling cankers develop, causing death of branches above the cankers. Erythricium (Corticium) salmonicolor is described by Mordue and Gibson (1976), and symptoms of the

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disease are described in detail by Seth et al. (1978). The fungus produces four distinct growth forms on the stems and branches, namely ‘cobweb’, ‘pustule’, ‘necator’ and ‘pink encrustation’ forms. The cobweb stage appears as superficial arachnoid mycelium shortly after infection during periods of high rainfall. Pustules of pink cellular tissue about one millimetre in diameter develop shortly after. These develop into the conidiomata (sporodochia) of the necator stage, which are orange-red and are formed on the upper side of affected branches late in the development of the disease when dieback is well advanced. Fragmentation of the conidiogenous cells produces hyaline, unicellular, ellipsoid conidia, 10–18 × 6–12 micrometres. The final symptom of infection is the basidiocarp (Erythricium) stage which is a thin, light pink hymenial encrustation originating at forks and extending across the underside of dead and dying branches. The smooth hymenial surface consists of crowded basidia only. The disease on eucalypts in India is most severe when plantations are established in areas where a high level of disease occurs on other trees and plantation crops, and rainfall exceeds 2000 millimetres per annum. Hilton (1958) stressed the importance of high rainfall in disease severity on rubber, temperature variation being relatively slight in these areas. Environmental factors affecting the level of disease in eucalypts are detailed by Sharma et al. (1985a). In Brazil, the disease has recently been very severe in some clones of E. grandis planted commercially in high rainfall areas (> 1500 mm/ annum) with high ambient temperatures (> 25oC) (A.C. Alfenas, pers. comm.). 10.4.1.2 Economic importance Although the fungus is present in warm, temperate regions in New Zealand, New South Wales, Australia and southern Japan (Sakaguchi et al. 1980) as well as the lowland humid tropics, most reports of severe pink disease on eucalypts come from India (Seth et al. 1978; Singh et al. 1979; Sehgal 1984; Sharma et al. 1984b). Infection has resulted in largescale mortality of E. tereticornis and E. grandis in high rainfall areas of Kerala, Karnataka and Goa States. For example, mortality in five-year-old to 11year-old plantations of E. tereticornis was estimated at 55% to 95% (Seth et al. 1978). Eucalyptus globulus and C. citriodora are also susceptible.

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In Brazil, the disease on eucalypts was first described by Ferreira and Alfenas (1977). There the pathogen causes economically important stem and branch cankers on many eucalypt species (Ferreira 1989) and has limited the use of some clones of E. grandis (or hybrids). In these clones, the main damage is the death of the leading stem and breakage in the vicinity of canker lesions (A.C. Alfenas, pers. comm.). Other disease records are on young E. robusta × E. tereticornis (reported as E. kirtoniana) in Costa Rica (de Segura 1970), E. grandis and E. saligna in the Philippines (H.M. Soriano, pers. comm.), E. camaldulensis in Vietnam (Sharma 1994) and E. diversicolor in Zambia (O. Shakacite, pers. comm.). 10.4.1.3 Control Control measures for pink disease on high value crops such as rubber, cocoa and fruit trees include pruning of affected limbs and treatment with fungicides. Such measures are unlikely to be feasible in eucalypt plantations (Sharma et al. 1985a) and options are reduced to silvicultural practices, especially the removal of affected trees aimed at reducing the sources of inoculum within the plantation, and the planting of resistant species, provenances or selections. In this regard, C. torelliana and E. deglupta have been found to be significantly more resistant to pink disease than E. grandis and E. tereticornis (Seth et al. 1978). Sharma et al. (1988) described a rapid assessment test for the susceptibility of cut shoots of eucalypts to culture filtrates of Erythricium salmonicolor. Differences were found between species and provenances in responses to toxins in the filtrates but the relationship of these responses to susceptibility to disease in the field was not established. A.C. Alfenas (pers. comm.) has observed variation in resistance among species and clones of eucalypts in Brazil, Indonesia and South Africa. Inoculation trials are to be established to select resistant clones suitable for plantations in the south-east of Bahia, Brazil.

10.4.2 Cryphonectria canker (Cryphonectria cubensis) 10.4.2.1 Symptoms and epidemiology Cryphonectria canker is the most important stem canker disease of eucalypts grown as plantation crops in the tropics and subtropics. Symptoms of the disease have been described (e.g. Hodges et al. 1979; Barnard and English 1980; Sharma et al. 1985a;

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Ferreira 1989; Wingfield et al. 1989) and the causal fungus has been reported as Diaporthe cubensis Bruner by Bruner (1917) and Hodges and Reis (1976), as Cryphonectria cubensis (Bruner) Hodges by Hodges (1980) and as Endothia eugeniae (Nutman & F.M.Roberts) J.Reid & C.Booth by Booth and Gibson (1973). This fungus was first described as Diaporthe cubensis from eucalypts in Cuba by Bruner (1917). In the previous year, Bruner (1916) described a somewhat similar fungus, Endothia havanensis Bruner from eucalypts. When a severe canker disease of E. grandis and E. saligna was reported from Surinam by Boerboom and Maas (1970), it was attributed to Endothia havanensis, and in preliminary reports an identical disease in Brazil was attributed to the same fungus (Hodges and Reis 1976). Comparison of the fungi from Surinam and Brazil with authentic specimens of Endothia havanensis and descriptions of Diaporthe cubensis showed that Diaporthe cubensis was the correct name (Hodges and Reis 1976). Hodges (1980) questioned the generic affinity of Diaporthe cubensis and transferred this species to Cryphonectria. This placement has been supported by Micales and Stipes (1987) and has gained general acceptance. Hodges et al. (1986) speculated that Cryphonectria cubensis may be a common pathogen of other closely related plants and showed that it is conspecific with Endothia eugeniae, a pathogen of cloves [Syzygium aromaticum (L.) Merr. & L.M.Perry]. This observation was confirmed by Micales et al. (1987). Hodges et al. (1986) suggested that Cryphonectria cubensis may have been spread widely on cloves throughout the areas where it is now a pathogen of plantation eucalypts. On trees less than two years old commonly the first symptoms are sunken areas in the bark near the base of the tree (Plate 10.7). The origin of these infections is uncertain. A.C. Alfenas (pers. comm.) considers that fine cracks in the bark may be an avenue for fungal invasion. In older trees, cankers higher up the stem may be associated with branch stub infections. Removal of the outer bark reveals a sharp demarcation line between healthy and diseased tissue (Plate 10.7). There is considerable variation among trees in response to infection. In some trees the outer bark is sloughed off before the cambium is killed, in others the infection stimulates cambial activity

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resulting in swelling and development of rough, thickened bark at the base of the tree, and in still others the cambium is killed, wood is invaded and spreading cankers are produced which can girdle the tree, or predispose the tree to stem breakage during high winds (Plate 10.8). Pycnidia and perithecia are produced either together or separately on dead bark near the cankers, and their clumps of protruding necks are visible under a hand lens (Booth and Gibson 1973). Sporocarps are formed in a stroma which develops in the cortical tissue of the host. Conidia are hyaline, oval, aseptate and 3.5–5 × 1.2–2 micrometres. Asci are unitunicate (20–30 × 4–6.5 µm) and ascospores are ellipsoid, two-celled, widest in the upper cell, and 6–8.5 × 2–3 micrometres. Common features of stem cankers induced by Cryphonectria cubensis are extensive formation of kino in veins and pockets between the bark and sapwood, and the subsequent flux of kino from cracks in the bark of affected trees (Boerboom and Maas 1970; Sharma et al. 1985b). As discussed above, copious kino secretion, although a common symptom of fungal infection, is of limited use in diagnosis, being caused in eucalypts by a wide range of biotic and abiotic agencies. Cryphonectria canker is favoured by temperatures above 23oC and high rainfall (1500–2400 mm) (Hodges et al. 1979; Sharma et al. 1985b). Laboratory studies have shown that Cryphonectria cubensis has an optimum growth rate at about 30oC (Hodges et al. 1976) and an isolate from Western Australia has a similar growth optimum (F.J. Bunny, pers. comm.). Trees subjected to water stress (Swart et al. 1992) were found to be less susceptible to infection and lesion development than were nonstressed trees. This is consistent with the disease being most severe in wetter parts of South Africa. 10.4.2.2 Economic importance Cryphonectria canker is widespread and serious in plantation eucalypts in the tropics and subtropics, and has been recorded from Surinam (Boerboom and Maas 1970), Brazil (Hodges and Reis 1974), Venezuela (Sharma et al. 1985b), Cuba (Bruner 1917), Puerto Rico, Florida and Hawaii (Hodges et al. 1979), Trinidad and Western Samoa (Hodges 1980), Hong Kong and Thailand (Pongpanich, K.M. Old and M.J. Wingfield, unpubl. data), Sumatra (A.C. Alfenas, pers. comm.) and India and the Cameroons (Sharma et al. 1985b). The only records

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from more temperate regions are from South Africa (Wingfield et al. 1989; Conradie et al. 1990) and the south-west of Western Australia (Davison and Tay 1995). The main economic effect of the disease results from reduced growth rate (Camargo et al. 1991), reduced coppicing (Hodges and Reis 1976; Sharma et al. 1985a; Barnard et al. 1987) and increased mortality (Boerboom and Maas 1970; Hodges et al. 1979). Wood yield was significantly reduced when cankers extended for more than 25% of the commercially useful stem length (Ferrari et al. 1984). Compared with normal wood, cankered wood contains more extractives and lignin and is denser with shorter fibres and thinner cell walls (Foekkel et al. 1976). Although the main problem in processing wood from affected stands is the loss in pulp yield, the increased content of extractives adversely affects bleaching. It was possible to produce pulp of a quality similar to that from healthy stands provided infection levels were below 34%. Stands with more than 50% of trees infected were not recommended for pulping (Foekkel et al. 1981). In Australia, Cryphonectria cubensis has been recovered from root cankers and a crown canker of E. marginata in native forest in Western Australia (Davison and Tay 1995; E.M. Davison, unpubl. data). 10.4.2.3 Control Many of the reports of Cryphonectria canker in eucalypt plantations indicate that there is considerable intraspecific and interspecific variation in susceptibility to this disease (Hodges et al. 1976; Conradie et al. 1992). Planting of moderately or highly resistant species is practised in Brazil (Alfenas et al. 1983). A summary of the relative susceptibility of species was given by Hodges et al. (1979) who considered that E. saligna and C. maculata are highly susceptible; E. grandis, E. propinqua and E. tereticornis moderately susceptible; E. microcorys, E. paniculata and E. robusta moderately resistant; and C. citriodora, E. paniculata and E. urophylla highly resistant. Eucalyptus grandis, possibly the most widely planted subtropical plantation species, shows a high level of between-provenance variation (Krugner 1983) and offers opportunities for selection at the family and clonal level (Borges and Brune 1981).

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10.5 Opportunistic pathogens associated with cankers in eucalypts Isolation of fungi from minor stem lesions yields a range of species such as Botryosphaeria spp., Coniothyrium spp., Cytospora eucalypticola, Endothia gyrosa, Lasiodiplodia theobromae (Pat.) Griffon & Maubl., Pestalotiopsis spp. and saprophytic moulds. More serious cankers can also be found on eucalypts in native forests and plantations in association with crown dieback of dominant trees (Davison and Tay 1983; Old et al. 1990; Shearer 1994; Yuan 1996; Yuan and Mohammed 1997) or as extensive girdling cankers of suppressed trees (Walker et al. 1985). These cankers usually yield the same fungi as the minor lesions (Plates 10.1 to 10.6), suggesting that the physiological state of the tree is important in disease expression (Crist and Schoeneweiss 1975; Appel and Stipes 1984; Smith et al. 1994). For example, stem cankers of eucalypts in Vietnam were associated with, in one case, Acremonium sp., Botryodiplodia sp., Phialophora sp., Verticillium sp. and in another case with Cytospora sp. and Botryodiplodia sp. (J.K. Sharma, pers. comm.). A stem canker (known as ‘Botryodiplodia stem canker’) caused by Lasiodiplodia theobromae severely affected two-year-old to four-year-old plantations of E. camaldulensis in the dry climate of Andhra Pradesh, India (J.K. Sharma, pers. comm.). Although the growth of E. camaldulensis is much superior to that of E. tereticornis, it is no longer planted because of its susceptibility to this disease. Opportunist canker pathogens can be frequently found associated with the dieback syndromes discussed in Chapter 17. Recommendations for control concentrate on relieving tree stress by matching species to site, drought avoidance and control of defoliating insects rather than on controlling the fungi directly.

10.5.1 Botryosphaeria ribis One of the most common fungi causing cankers on eucalypts is a species of Botryosphaeria, occurring most frequently as its Fusicoccum or Dothiorella anamorph. Botryosphaeria is variously identified as Botryosphaeria ribis Grossenb. & Duggar or Botryosphaeria dothidea (Moug.:Fr.) Ces. & De Not. These are considered synonyms by von Arx and Müller (Morgan-Jones and White 1987), but not by

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Farr et al. (1989). The confusing state of the taxonomy of Botryosphaeria and its anamorphs is discussed more fully in Chapter 7. Botryosphaeria ribis causes fruit rot, cankers and dieback on many woody plants in temperate and tropical regions. It is described by Punithalingam and Holliday (1973). Cankers on stems are commonly sunken and elongated (lens shaped) and infected tissue may be darkly pigmented. Bark cracking and kino exudation are often present. Cankers are most obvious on the smooth bark of twigs and young branches, on which black, solitary conidiomata are embedded in dead periderm. When girdling occurs, the cankers extend down the branches as necrotic stripes. Conidiomata produce hyaline, unicellular, fusoid macroconidia (17–25 × 5–7 µm) and tiny hyaline, allantoid microconidia (spermatia) (2–3 × 1 µm). Black ascostromata up to four millimetres wide are formed in the cortex and become erumpent. Ascogenous locules form bitunicate asci among filiform paraphyses, and ascospores are unicellular, hyaline, ovoid (17–23 × 7–10 µm). Eucalypt species differ in their response to infection. For example, Botryosphaeria ribis was associated with death of E. radiata, a native of moderately wet forests of temperate eastern Australia, growing in species selection trials in the strongly mediterranean climate of Western Australia (Shearer et al. 1987). In inoculation trials, both seedlings and plantation trees of E. radiata developed damaging cankers, whereas two species native to Western Australia were much less susceptible to the disease. Botryosphaeria ribis causes important stem base and root cankers on several eucalypt species in Argentina (Frezzi 1952; S.E. Lopez, pers. comm.), stem cankers of C. citriodora and branch cankers of E. grandis and E. urophylla in Brazil (C.G. Auer, pers. comm.; A.C. Alfenas, pers. comm.), twig and branch cankers of E. botryoides, E. delegatensis and E. saligna, and dieback of E. cypellocarpa, E. delegatensis and E. regnans in New Zealand (M. Dick, pers. comm.), and root cankers on E. urophylla and E. grandis in the Solomon Islands (P. Zekele, pers. comm.). It has been reported from South Africa to attack coppice, stems and roots of many species (Smith et al. 1994), from Malawi (T.S. Zulu, pers. comm.) and from Zimbabwe where it causes stem cankers on E. grandis (A.J. Masuka, pers. comm.).

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Botryosphaeria ribis was isolated together with Cryphonectria cubensis from cankers on E. grandis coppice shoots and stumps in Florida (Barnard et al. 1987). It has also been recorded on eucalypts in Western Australia (Davison and Tay 1983; Shearer et al. 1987), eastern Australia (Old et al. 1990), India (Jamaluddin and Dadwal 1987) and Japan (K.M. Old, unpublished data) and as an endophyte of E. nitens in southern England (Fisher et al. 1993) and South Africa (Smith et al. 1996b).

10.5.2 Coniothyrium sp. A new canker disease caused by a species of Coniothyrium Corda (Coniothyrium canker) was discovered in the Zululand region of South Africa in 1991 and has subsequently spread throughout the wetter subtropical areas of the country, causing substantial damage to seedlings and clonal stands of eucalypts, especially E. grandis (Kemp et al. 1991). Early infections are typified by development of small necrotic lesions on young, green stem tissue (P.W. Crous and M.J. Wingfield, pers. comm.). These lesions develop abundant pycnidia of the pathogen and coalesce to form large lesions with cracks exuding copious amounts of kino. Infections persist in the wood and result in spindle-shaped malformations of the stems which ultimately girdle trees and result in cessation of apical growth and dead tops. Clones of E. grandis and hybrids of this and other species differ considerably in their susceptibility to Coniothyrium canker and work is under way to replace susceptible with resistant planting material (see Chapter 22).

10.5.3 Cryphonectria gyrosa Endothia tropicalis Shear & N.E.Stevens is a synonym of Cryphonectria gyrosa (Berk. & Broome) Sacc. (Barr 1978), and both Kobayashi (1970) and Hodges (1980) regard Cryphonectria gyrosa as also being synonymous with Endothia havanensis Bruner [which was transferred by Barr (1978) to Cryphonectria havanensis (Bruner) M.E.Barr]. However, Walker et al. (1985) argue that adequate comparisons of type material have not been made to confirm the synonymy of Cryphonectria havanensis and Cryphonectria gyrosa and until this is done they should be retained as separate species. Cryphonectria gyrosa occurs widely on eucalypts grown as exotics. It has been recorded on E. globulus

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and many other trees in Japan (Kobayashi 1970), in Florida sporulating on dead and cankered coppice of E. grandis (Barnard et al. 1987), and has been associated with stem cankers on young E. camaldulensis in Vietnam. The latter trees had been severely defoliated by Cylindrocladium quinqueseptatum Boedijn & Reitsma (K.M. Old and Z.-Q. Yuan, unpubl. data). Cryphonectria gyrosa has been observed on dead twigs and branches of C. torelliana, E. alba, E. deglupta, E. grandis and E. tereticornis in Kerala, India, by Sharma et al. (1985a), who conducted disease surveys and artificial inoculations. Although up to 10% mortality of C. torelliana was recorded, Cryphonectria gyrosa was considered to be a weak pathogen, offering no serious threat to plantation eucalypts. Cryphonectria gyrosa was associated with cankers caused by Cryphonectria cubensis in Florida (Barnard et al. 1987). The importance of this opportunist fungus lies in its morphological similarity to more aggressive pathogens.

10.5.4 Cryphonectria parasitica Cryphonectria parasitica (Murrill) M.E.Barr [syn. Diaporthe parasitica Murrill; Endothia parasitica (Murrill) P.J.Anderson & H.W.Anderson] (anamorph: Endothiella parasitica Roane) is well known as the cause of chestnut blight, but it can also infect eucalypts. It is described in detail by Sivanesan and Holliday (1981). The fungus forms scattered yellow to yellowish-brown stromata up to three millimetres wide in which are formed deeply embedded perithecia connected to the surface by long necks passing through the stromatic disc. Unitunicate asci become free floating within the perithecial cavities, and ascospores (7–12 × 3–5.5 µm) are hyaline, one septate, elliptical, straight and rounded at the ends. Conidiomata are pseudostromatic, immersed, erumpent, and yellow to yellowish-brown, and form hyaline, one celled, ellipsoidal to bacilliform conidia (3–5 × 1–1.5 µm) on branched conidiophores. Severe cankers were formed on seedlings of five Eucalyptus spp. inoculated with this fungus (Old and Kobayashi 1988) (Plate 10.9). The teleomorph of Cryphonectria parasitica was found in Japan on two unidentified eucalypt species in amenity plantings in two separate locations, and a further eight collections of a species of Endothiella morphologically identical to the anamorph of

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Cryphonectria parasitica were obtained from E. cornuta, E. globulus, E. mannifera and E. pauciflora ssp. niphophila (reported as E. niphophila). Symptoms of disease in the field included minor twig cankers and death of coppice shoots, elongate bark cankers and main stem dieback of saplings. In one instance, pycnidia were found at the base of an apparently healthy tree. Anamorphs of Cryphonectria spp. and Endothia spp. cannot be distinguished morphologically with any certainty and, while at least seven species within these genera have been recorded in Japan (Kobayashi 1970) (Plate 10.10), only the teleomorph collections were confirmed as Cryphonectria parasitica. The potential status of Cryphonectria parasitica as a eucalypt pathogen is not clear, as the geographical ranges of the pathogen and exotic eucalypt plantations do not generally coincide and no isolations of the fungus from eucalypts have been recorded other than from Japan. Expansion of eucalypt cultivation, especially of frost-tolerant species, into areas of Europe and Asia where Cryphonectria parasitica is endemic could result in wider occurrence of infection on eucalypts.

10.5.5 Cytospora eucalypticola One of the commonest fungi isolated from eucalypt cankers in Australia is Cytospora eucalypticola Van der Westh. [teleomorph: Valsa ceratosperma (Tode:Fr.) Maire]. This fungus forms perithecia embedded in the bark. There may be some stromatic development, and perithecia are black, up to 700 micrometres in diameter, with long necks that often emerge collectively. Asci are unitunicate, and ascospores (5.5–9 × 1–2 µm) are allantoid, unicellular and hyaline. Conidiomata are eustromatic, black, immersed, erumpent, often with long necks; conidiophores are hyaline, septate and branched irregularly, and conidia (3–6 × 0.5–1.5 µm) are hyaline, unicellular and allantoid. The fungus occurs in Argentina (S.E. Lopez, pers. comm.), Brazil (A.C. Alfenas, C.G. Auer, J.L. da S. Maia, pers. comm.), India (Sharma et al. 1985b), New Zealand (M. Dick, pers. comm.), Solomon Islands (P. Zekele, pers. comm.), South Africa (van der Westhuizen 1965; M.J. Wingfield, pers. comm.) and Zambia (O. Shakacite, pers. comm.). It was the only endophyte found by Fisher et al. (1993) in twigs of E. nitens collected in both Australia and England.

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Although commonly isolated from wounded stems, from the full spectrum of cankers from annual to diffuse (Plates 10.1 to 10.6) and from trees suffering from shoot dieback (Plate 10.11), Cytospora eucalypticola is a very weak pathogen. However, it is able to persist for a long time in wounds, and as an endophyte in healthy tissue. When inoculated into seedlings or larger trees it is only capable of limited invasion of bark and sapwood (Fraser and Davison 1985; Old et al. 1986; Shearer et al. 1987). Old et al. (1991) found a Valsa sp. on eucalypts in Australia and Japan; it was identified as Valsa ceratosperma and was considered to be the teleomorph of Cytospora eucalypticola. Valsa ceratosperma is widely distributed in the northern hemisphere in association with cankers on many broad-leaved hosts (Spielman 1985). Several other collections of Valsa have been made on eucalypts and usually these have been called Valsa eucalypti Cooke & Harkn. The first use of this name was by Cooke and Harkness (1881) for a collection on E. globulus in California. Spielman (1985) suggested that this collection was a Leucostoma sp. However, Sharma et al. (1985b, 1989) also used the name Valsa eucalypti and separated other collections as Valsa eucalypticola J.K.Sharma, C.N.Mohanan & Florence. In view of the wide host range and distribution of Valsa ceratosperma it may be possible to accommodate these taxa in Valsa ceratosperma but further studies of worldwide collections of Valsa and their anamorphs from eucalypts are needed to resolve this question.

10.5.6 Endothia gyrosa Endothia gyrosa (Schwein.:Fr.) Fr. (anamoph: Endothiella gyrosa Sacc.) is well known from North America as a canker pathogen of Quercus spp. (Stipes and Phipps 1971; Roane et al. 1974), Liquidambar formosana Hance (Snow et al. 1974) and several other hosts including chestnut and beech (Sinclair and Hudler 1980). It is described in detail by Snow et al. (1975). Perithecia and conidiomata are formed in distinctive orange stromata one to two millimetres in diameter and up to two millimetres high, irregularly spaced on the surface of dead bark. When wetted, conidiomata exude bacilliform conidia (3–4 × 0.7–1 µm). Perithecia form long necks which protrude from the stromata, asci are unitunicate, and ascospores (6–10 × 2–2.5 µm) are one celled and allantoid with tapering ends. The report of Endothia gyrosa on eucalypts by Walker et al. (1985) has been

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followed by many isolations of this fungus in Australia and its association with significant disease of both forest and woodland eucalypts (Old et al. 1986; Old et al. 1990). The Endothiella anamorph of this fungus found in Western Australia to cause branch and stem cankers of E. marginata was originally named Endothia havanensis (Davison 1982; Davison and Tay 1983). Isozyme studies have since shown that this fungus is the anamorph of Endothia gyrosa (Alfenas et al. 1988; Davison and Coates 1991) (Plates 10.12 to 10.14). The fungus is associated with cankers of a range of severities (Plates 10.1 to 10.6) and is particularly damaging on trees which have been repeatedly defoliated, either artificially or by insect feeding (Old et al. 1990). Wardlaw (1999) found that Endothia gyrosa was associated with severe cankers on plantation-grown E. nitens in Tasmania. Incidence and severity were not associated with pruning or thinning treatments and the affected stand had no known history of environmental stress that could predispose trees to disease. There was, however, a clear provenance effect that appeared to be related to bark roughness. This fungus is a significant pathogen of Eucalyptus spp. in South Africa, where there are species and clonal differences in disease severity in inoculated and naturally infected trees (van der Westhuizen et al. 1993). Lesions caused by Endothia gyrosa, especially active cankers on young trees, may be reddish-brown in colour due to the formation of pigments in the outer bark. The fungus often sporulates profusely on dead bark over necrotic sunken lesions, and both the teleomorph and anamorph can be present, singly or concurrently. K.M. Old and M.J. Dudzinski (unpubl. data) have found Endothia gyrosa to be a common coloniser of sapwood of regrowth E. sieberi and E. globoidea following wounding. The fungus could be isolated from discoloured wood for at least two years after wounding but no cankers were recorded.

10.5.7 Hypoxylon mediterraneum Hypoxylon mediterraneum (De Not.) Ces. & De Not. [syn. Sphaeria mediterranea De Not.; Nummularia mediterranea (De Not.) Sacc.; Numulariola mediterranea (De Not.) P.Martin] causes charcoal disease of Quercus suber L. but is associated with canker diseases of many trees including other species of oak and Shorea robusta

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Gaertner.f. It is described by Hawksworth (1972). The fungus forms shiny, black, erumpent, carbonaceous stromata (2–5 × 1–1.5 mm) in the bark. Ascospores are dark brown to black and ellipsoidal, 12.5–23 × 5–10 micrometres, with a distinct longitudinal furrow. The hyphomycete anamorph forms hyaline conidiophores, often aggregated into tufts, with branches mainly in the upper parts, and hyaline, unicellular, smooth ellipsoidal to ovoid conidia, 2.5–7.5 × 2.5–3.5 micrometres. Infection is most severe on droughtstressed trees (Boyce and Bakshi 1959; Ragazzi et al. 1989). Eucalypts can be infected, and in Portugal Hypoxylon mediterraneum is associated with stem cankers of E. globulus (M.T. Cabral, pers. comm.). Two further species of Hypoxylon, namely Hypoxylon nummularium Bull.:Fr. var. pseudopachiloma (Speg.) J.H.Mill. and Hypoxylon stygium (Lév.) Sacc., were described by Ferreira (1989) as causing significant disease on eucalypts in Brazil.

10.5.8 Seiridium eucalypti Species of the coelomycete genus Seiridium are well known as significant canker pathogens of conifers, especially Cupressaceae (Sutton and Gibson 1972; Swart 1973; Sasaki and Kobayashi 1975). Seiridium eucalypti Nag Raj was isolated from a cankered branch of E. delegatensis in northern Tasmania (Yuan and Old 1995). The fungus was shown to be pathogenic on seedlings. A survey of native stands and plantations at locations throughout Tasmania confirmed that it can be associated with severe cankers in the field (Yuan and Mohammed 1997). The fungus forms inconspicuous, separate, immersed, erumpent acervuli in the bark, and distinctive six-celled, cylindric-fusoid, slightly curved conidia (22.5–35 × 6.3–10.5 µm) with four brown intermediate cells, and hyaline basal and apical cells each with an unbranched appendage. The pathogenic status of this fungus is not clear and its relationship to the cypress canker pathogens remains to be determined. However, in a pathogenicity test it was the most pathogenic of five fungi tested, including Botryosphaeria ribis, Cytospora eucalypticola and Endothia gyrosa (Yuan and Old 1995).

10.6 Conclusion Eucalypts are being increasingly grown as plantation species in the tropics, subtropics and temperate

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regions of the world, including Australia. The incidence and severity of damage caused by the important canker-inducing fungi, Cryphonectria cubensis and Erythricium salmonicolor, together with opportunistic pathogens with wide host ranges such as Botryosphaeria ribis, Lasiodiplodia theobromae, Coniothyrium spp., Endothia gyrosa, Hypoxylon mediterraneum and Valsa spp., are likely to increase, particularly if plantations are subject to physiological stresses induced by drought, waterlogging, temperature extremes or defoliation by insects or pathogens. There are recent examples of opportunistic pathogens responding to changing silviculture. For example, extensive clonal trials of E. grandis in South Africa have been notable for the appearance of stem cankers, stem deformation and mortality caused by several opportunistic pathogens such as a species of Coniothyrium (M.J. Wingfield, pers. comm.) and Endothia gyrosa. In addition, genera such as Seiridium, which include important pathogens of other plantation species, may become important on eucalypts in the future. As many of these fungi are extremely widespread, it is essential that species, provenances and clones being grown in plantations are matched to both climate and site so that environmental stress of the trees is minimised. Genotypes can also be selected for resistance to canker, and plantations can be established with a broad genetic base to reduce vulnerability to particular pathogens.

10.7 Acknowledgments Many records of the occurrence of canker-causing fungi are unpublished and we thank the following colleagues for making their records available to us: A.C. Alfenas (Universidade Federal de Viçosa, Brazil), C.G. Auer (EMBRAPA/CNPF, Curitiba, Brazil), E. Avcioglu (Poplar and Fast-growing Forest Tree Directorate, Tarsus, Turkey), A. Belisario (Centro di Sperimentazione Agricola e Forestale, Rome, Italy), S.J. Bosco (Institut des Sciences Agronomiques du Burundi), M.T. Cabral, (Forest Research Centre, Lisbon, Portugal), M. Diabangouaya (U.A.I.C., Pointe-Noir, Congo), M. Dick (Forest Research Institute, Rotorua, New Zealand), Y.A.C. Doo (Forest Research Institute, Yezin, Pyinmana, Myanmar), J. Francis (Institute of Tropical Forestry, Río Piedras, Puerto Rico), S.S. Lee (Forest Research Institute, Kuala Lumpur, Malaysia), A. Leslie (Lesotho Woodlot

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Project, Maseru Lesotho), S.E. Lopez (Ciudad Universitaria, Buenos Aires, Argentina), J.L. da S. Maia (Duraflora Silvicultura e Comercio Ltda, Jundiai, Brazil), A.J. Masuka (Forest Research Centre, Highlands, Harare, Zimbabwe), L. Nshubemuki (Tanzania Forestry Research Institute, Morogoro, Tanzania), C.H. Sandoral (Corporación Hondureña de Desarrollo Forestal, Tegucigalpa, Honduras), N. Sam (Papua New Guinea Forest Research Institute, Lae, Papua New Guinea), O. Shakacite (Forest Department, Kitwe, Zambia), J.K. Sharma (Kerala Forest Research Institute, Peechi, India), H.M. Soriano (Institute of Forestry and Environmental Studies, Camiling, Tarlal, the Philippines), S.P. Soteriou (Department of Forests, Nicosia, Cyprus), R.G. Strouts (Forest Research Station, Alice Holt, England), M. Sudin (Jabatan Perhutanan, Sabah, Malaysia), M. Suharti (Forest Research Development Centre, Bogor, Indonesia), H. Wang (Chinese Academy of Forestry, Beijing, China), W.-Y. Wang (Taiwan Forestry Research Institute, Taipei, Taiwan), M.J. Wingfield (University of Pretoria, Pretoria, South Africa), P. Zekele (Forestry Research, Munda, Solomon Islands), T.S. Zulu (Forest Research Institute, Zomba, Malawi). We also thank Drs Wingfield and Alfenas for reviewing the manuscript.

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Tippett, J.T., Hill, T.C. and Shearer, B.L. (1985). Resistance of Eucalyptus spp. to invasion by Phytophthora cinnamomi. Australian Journal of Botany 33, 409–418. Tippett, J.T., Crombie, D.S. and Hill, T.C. (1987). Effect of phloem water relations on the growth of Phytophthora cinnamomi in Eucalyptus marginata. Phytopathology 77, 246–250. van der Westhuizen, G.C.A. (1965). A disease of young Eucalyptus saligna in Northern Transvaal. South African Forestry Journal 54, 12–16. van der Westhuizen, I.P., Wingfield, M.J., Kemp, G.H.J. and Swart, W.J. (1993). First report of the canker pathogen Endothia gyrosa on Eucalyptus in South Africa. Plant Pathology 42, 661–663. Walker, J., Old, K.M. and Murray, D.I.L. (1985). Endothia gyrosa on Eucalyptus in Australia with notes on some other species of Endothia and Cryphonectria. Mycotaxon 23, 353–370. Wardlaw,T.J. (1999). Endothia gyrosa associated with severe stem cankers on plantation grown Eucalyptus nitens in Tasmania. European Journal of Forest Pathology 29, 199–208. Wildman H.G. and Jones R.J. (1991). Isolation of fungal endophytes from root samples of trees blown over at the Royal Botanic Gardens, Kew, during the 1987 hurricane. The Mycologist 5, 180–182. Wilkes, J. (1985). Host attributes affecting patterns of decay in a regrowth eucalypt forest. IV. The responses of sapwood to injury. Holzforschung 39, 321–326. Wilkes, J. (1986). Host attributes affecting patterns of decay in a regrowth eucalypt forest. V Barrier zones. Holzforschung 40, 37–42. Wingfield, M.J., Swart, W.J. and Abear, B.J. (1989). First record of Cryphonectria canker of Eucalyptus in South Africa. Phytophylactica 21, 311–313. Yuan, Z.-Q. (1996). Fungi and associated tree diseases in Melville Island, Northern Territory, Australia. Australian Systematic Botany 9, 337–360. Yuan, Z.-Q and Mohammed, C. (1997). Investigation of fungi associated with stem cankers of eucalypts in Tasmania, Australia. Australian Plant Pathology 26, 78–84. Yuan, Z.-Q. and Old, K.M. (1995). Seiridium eucalypti, a potential stem canker pathogen of eucalypts in Australia. Australasian Plant Pathology 24, 173–178.

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Many soilborne species of Phytophthora and Pythium have been isolated from eucalypt forests. Some cause damping-off in seedlings but the most serious disease is dieback of eucalypts and their associated understorey caused by Phytophthora cinnamomi. While several species of Phytophthora have been isolated from native eucalypt forests, only Ph. cinnamomi has been associated with significant damage to the forests. Research into the biology and control of Ph. cinnamomi has dominated eucalypt pathology in Australia for nearly four decades. However, this pathogen has had little effect in plantations of eucalypts, either in Australia or elsewhere, mainly because the preferred species are largely resistant to it. There is strong evidence that Ph. cinnamomi was introduced to the vulnerable forests of southern Australia, probably from tropical regions further north. This accounts for the dramatic effect of the pathogen in these forests and the susceptibility of key elements of the plant communities, including certain eucalypt species and many understorey species. In natural eucalypt forests, the roles of species of Pythium are less well known. It is likely that as elsewhere they are primarily agents of pre-emergence damping-off of seedlings and postemergence losses of seedlings.

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11.1 Introduction Although diseases in eucalypt communities now known to be caused by species of Phytophthora (Ph.) and Pythium (P.) have been observed since the beginning of the twentieth century, their causes have been determined only comparatively recently. In 1949, Phytophthora cinnamomi Rands was associated with the death of understorey species in eucalypt woodland near Sydney (Fraser 1956). Deaths of eucalypts later shown to be associated with Ph. cinnamomi were first observed in the early 1920s in south-west Australia (Podger 1968) and in the 1950s in south-east Australia (Weste and Marks 1974; Marks and Idczak 1977). However, the first association of Ph. cinnamomi with death of Eucalyptus marginata (jarrah) and the understorey vegetation in forests of south-west Australia (Podger et al. 1965; Podger 1968) undoubtedly stimulated much of the research which forms the basis of our knowledge of diseases caused by pythiaceous fungi in indigenous eucalypt communities. The occurrence and biology of Ph. cinnamomi in forests has been given priority in research and has been extensively reviewed (Newhook and Podger 1972; Marks and Idzcak 1973; Marks and Idczak 1977; Old 1979; Zentmyer 1980; Weste and Marks 1987; Davison and Shearer 1989; Dell and Malajczuk 1989; Shearer and Tippett 1989; Marks and Smith 1991). Knowledge of the role of pythiaceous fungi in other eucalypt communities is limited. Species of Pythium and Phytophthora are the only members of the Pythiaceae recorded as pathogens of eucalypts and are the most frequently reported soilborne pathogens of eucalypts in plantations and forests. These species are also important causes of damping-off and other diseases in eucalypt nurseries (see Chapter 8). Phytophthora species isolated from native eucalypt communities include Phytophthora boehmeriae Sawada, Ph. cinnamomi, Phytophthora citricola Sawada, Phytophthora cryptogea Pethybr. & Laff., Phytophthora drechsleri Tucker, Phytophthora gonapodyides (H.E.Petersen) Buisman, Phytophthora megasperma Drechsler var. megasperma, Phytophthora megasperma Drechsler var. sojae A.A.Hildebr. and Phytophthora nicotianae Breda de Haan var. parasitica (Dastur.) G.M.Waterh. (Newhook and Podger 1972; Pratt and Heather 1973b; Weste 1975; Gerrettson-Cornell

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1980; Fagg 1987; Shearer et al. 1987a; Shearer 1990). Phytophthora cinnamomi is the species most frequently isolated from areas of dying vegetation and is a widespread but not ubiquitous pathogen in native eucalypt communities of south-west and south-east Australia. It has been described as ‘the most destructive plant pathogen ever recorded in native vegetation of this and possibly any region’ (Newhook and Podger 1972). The next most frequently isolated species are Ph. drechsleri in the mixed eucalypt forests of south-east Australia (Pratt and Heather 1973b) and Ph. citricola in E. marginata forests of south-west Australia (Shearer et al. 1987a). Phytophthora boehmeriae, Phytophthora cambivora (Petri) Buisman, Ph. cinnamomi, Ph. cryptogea, Phytophthora heveae A.W.Thomps., Ph. nicotianae var. parasitica and Phytophthora palmivora (E.J.Butler) E.J.Butler have been isolated from eucalypt plantations throughout the world but have not been associated with serious losses (Arruda 1943; Frezzi 1950; Wattle Research Institute 1973; Gerrettson-Cornell 1976; Gerrettson-Cornell and Dowden 1977; Gerrettson-Cornell 1978; Wingfield and Knox-Davis 1980; Lundquist and Baxter 1985). In Australia, death and poor growth of eucalypts in plantations associated with Phytophthora species have occurred only in localised areas, often areas subject to occasional soil saturation. Mortality from Ph. cinnamomi infection is limited in South African plantations because the commonly grown eucalypt species are resistant to the pathogen (Wingfield and Knox-Davis 1980). It is possible to avoid diseases caused by pythiaceous fungi in plantations by the correct choice of site and species and appropriate management practices. At least thirteen Pythium species have been recorded from native eucalypt forests. These include Pythium (?)acanthicum Drechsler, Pythium (?)acanthophoron Sideris, Pythium (?)deliense Meurs, Pythium intermedium de Bary, Pythium irregulare Buisman, Pythium mamillatum Meurs, Pythium middletonii Sparrow, Pythium (?)oedochilum Drechsler, Pythium paroecandrum Drechsler, Pythium perplexum H.Kouyeas & Theoh., Pythium splendens Hans Braun, Pythium ultimum Trow, Pythium ultimum Trow var. sporangiferum Drechsler (Pratt and Heather 1973b; Mwanza 1986; Mwanza and Kellas 1987) and unidentified Pythium species (Marks and Kassaby 1974; Gerrettson-Cornell et al. 1979;

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Fagg 1987). Many of these species have been associated with pre-emergence and postemergence damping-off of seedlings (Mwanza 1986; Mwanza and Kellas 1987) (see Chapter 8). Unidentified Pythium species have been isolated from eucalypt plantations (Gerrettson-Cornell and Dowden 1977; Gerrettson-Cornell 1978). In northern Natal, South Africa, P. splendens has caused severe losses of six-month-old to 18month-old plantings of E. grandis (Linde et al. 1994) but only in unthrifty stock planted on difficult sites (C. Linde, pers. comm.).

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particularly its association with human ingress, the susceptibility of many floristic components, including in some cases dominant components of the native vegetation, widespread occurrence of the A2 but not the A1 mating type and lack of genetic variation in the pathogen (Podger 1972; Weste and Marks 1974; Old et al. 1984a; Old et al. 1988; Podger and Brown 1989). Circumstantial evidence suggests that Phytophthora species other than Ph. cinnamomi may also be relatively recent introductions to native plant communities in Australia (Shearer and Tippett 1989).

11.2 Origin of the pathogens

11.3 Host range

The origins of Phytophthora and Pythium species in native communities or plantations of eucalypts are obscure. More information is required on the occurrence of species other than Ph. cinnamomi to determine whether they are indigenous components of eucalypt communities.

Certain Phytophthora species attack an extraordinarily wide range of woody plants. Phytophthora cinnamomi is pathogenic on at least 805 plant species from 273 genera (Zentmyer 1980). Nearly half of these hosts are indigenous to native plant communities in Australia. Worldwide, Ph. nicotianae var. parasitica attacks plant species from 72 genera in 42 angiosperm families, Ph. cryptogea 25 genera in 11 families and Ph. megasperma 14 genera in nine families (Hickman 1958). Host lists for all species of Phytophthora and Pythium from native eucalypt communities are clearly incomplete. They also consist mainly of isolation records which do not separate hosts that are symptomless carriers from those that died following infection.

While it is now generally agreed that Ph. cinnamomi is an exotic wherever it causes disease in native eucalypt communities, there has been much debate and speculation about the region of origin of the species and its introduction to Australia (Newhook and Podger 1972; Shepherd 1975). An analysis by Zentmyer (1988) of the effect, relative frequency of occurrence of the A1 and A2 mating types, variation in the pathogen and occurrence of human disturbance suggests that Ph. cinnamomi may have originated in the tropical region of Papua New Guinea–Indonesia–Malaysia, possibly including north-east Australia and Taiwan. Phytophthora cinnamomi occurs in remote, apparently undisturbed sites at high altitudes in the South West Cape, South Africa, without causing appreciable plant death (Von Broembsen and Kruger 1985) and on this basis it was concluded that the pathogen is indigenous to the region. However, as only the A1 mating type is found there (Von Broembsen 1989), South Africa is considered a less likely region of origin of than the south-east Asian tropics (Zentmyer 1988) and recent isozyme and molecular evidence (C. Linde, pers. comm.) suggests that the fungus is not indigenous to South Africa. Evidence that Ph. cinnamomi is a comparatively recent introduction to native plant communities of south-west and south-east Australia comes from the patterns of disease distribution within the forests,

Zentmyer (1980) listed 152 species of eucalypts as hosts of Ph. cinnamomi. However, various inoculation studies and field observations have shown that the eucalypt genera and subgenera differ in their responses to Ph. cinnamomi infection (Podger 1968; Titze and Palzer 1969; Podger and Batini 1971; Weste and Taylor 1971; Marks et al. 1972, 1973; Pratt and Heather 1973a; Weste et al. 1973; Brown 1977; Tippett et al. 1985). Species of the Eucalyptus subgenus Monocalyptus (Pryor and Johnson 1971) are more severely affected by Ph. cinnamomi than are species of the subgenus Symphyomyrtus and the genus Corymbia (Fig. 11.1). Phytophthora cinnamomi is destructive on certain species of the subgenus Monocalyptus, particularly E. marginata in the jarrah forests of south-west Australia (Plate 11.1) and E. baxteri, E. consideniana (Plate 11.2), E. radiata, E. globoidea, E. macrorhyncha, E. obliqua and

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Seedlings of species of eucalypts of the Eucalyptus subgenus Monocalyptus are more sensitive to root rot caused by Phytophthora cinnamomi than species of the subgenus Symphyomyrtus and the genus Corymbia. Histograms show the percentage of species having a root rot rating ranging from 1 (little damage) to 4 (severely damaged) (after Table 1.3 in Brown 1977).

E. sieberi in the mixed eucalypt forests of south-east Australia (Podger 1973; Weste and Marks 1974). In south-west Australia, C. calophylla is field resistant and continues to survive, and in some places to increase, in infested areas long after E. marginata has died (Podger 1968; Shearer and Dillon 1995, 1996). Eucalypts of the subgenus Symphyomyrtus such as E. diversicolor, E. globulus, E. gomphocephala and E. wandoo are resistant. In south-east forests, species of the subgenus Symphyomyrtus such as E. aromaphloia, E. sideroxylon and E. viminalis are resistant and E. ovata and E. goniocalyx are apparently highly resistant (Podger 1973). Considerable intraspecific variation exists in the ability of individual plants within the generally susceptible subgenus Monocalyptus to restrict Ph. cinnamomi infection. Seedling survival following infection differed between provenances of E. marginata and E. obliqua (Podger 1972; Brown 1977). Eucalyptus regnans exhibited variation in resistance, assessed as the degree of lesion extension in wound-inoculated stems (Marks et al. 1981) and root collar infection (Harris et al. 1985). Lesion length induced by wound inoculation of stems was normally distributed in E. marginata trees in the forest (Shearer and Tippett 1989) and

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varied continuously from low to high values in seedlings inoculated in the glasshouse (Stukely and Crane 1994). Resistant lines of micropropagated clones of E. marginata have been selected in glasshouse and forest trials (Cahill et al. 1992; Bennett et al. 1993; Stukely and Crane 1994). There is some evidence from seedling inoculation studies that species of eucalypts that are susceptible to Ph. cinnamomi may also be more susceptible to other pythiaceous fungi. Susceptibility to preemergence and postemergence damping-off and root necrosis caused by Pythium species and by Phytophthora cactorum (Lebert & E.Cohn) J.Schröt., Ph. citricola, Ph. drechsleri and Ph. nicotianae var. parasitica appears to be greater for species of Monocalyptus than for Symphyomyrtus and the genus Corymbia (Marks and Kassaby 1974; Sedgley 1974; Brown 1977).

11.4 Distribution patterns and effect of disease The damaging consequences of an epidemic of root rot disease in the E. marginata forests of Western Australia, proved later (in 1964) to be caused by Ph. cinnamomi, first came to notice in 1921. By

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1946 the disease known as ‘jarrah dieback’ was viewed by T.N. Stoate, the Conservator of Forests of the day, as a very disturbing phenomenon. Between 1962 and 1977 similar problems were recognised successively in Victoria, Tasmania and South Australia. In some cases basal area, an index of accumulated biomass, was reduced to a few per cent of its original pre-infection status (see figure 9 in Podger 1968). At the other end of the spectrum of effect, Ph. cinnamomi invaded communities and persisted beneath them for many decades with no discernable effect. Since the first association of Ph. cinnamomi with death of E. marginata in south-west Australia, Phytophthora species have been detected in a wide range of eucalypt communities in Australia. Little is known of the distribution of Pythium species in eucalypt communities. Disease caused by Phytophthora species occurs mainly in south-west and south-east Australia in communities ranging from shrub-heath to tall forest. There have been no reports of Phytophthora affecting natural stands of eucalypts in the wet–dry tropics of northern Australia, although Ph. cinnamomi was reported to have been associated with death of E. tetrodonta growing in a poorly drained, disturbed area in an urban environment in the Northern Territory (Weste 1983a). The most striking and widespread expression of disease caused by a Phytophthora species occurs in the E. marginata forest and associated plant communities in south-west Australia (Podger 1968, 1972; Shearer 1990, 1994). The destructive effect of Ph. cinnamomi in these forests (Plate 11.1) has been described as ‘an exceptional example of an introduced pathogen with a wide host range causing great damage to a diverse but mainly susceptible plant community’ (Shearer and Tippett 1989). The most vulnerable plant communities are the diverse shrublands and woodlands occurring on sandplains derived from leached sand or laterite (Shearer 1994). About 14% of the E. marginata forest is infested with Ph. cinnamomi (Davison and Shearer 1989), although the percentage of forest trees infected varies greatly throughout the forest, with more than 50% of some forest blocks being infested (e.g. figure 5 in Shearer and Tippett 1989). Incidence and effect of Ph. cinnamomi infestation is greatest in the western

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and southern high rainfall forest (up to 1400 mm per annum) and less in the eastern low rainfall forest (< 800 mm per annum). Diseased areas occur as a mosaic within the forest in association with roading and water gaining areas (Podger 1968), similar to the pattern of disease occurrence observed in Victoria (Weste and Taylor 1971). Disease effect is greatest in plant communities occurring on shallow soils with impeded drainage and lowest on the free-draining fertile soils on steep slopes of the Darling Scarp and major valleys on the western edge of the forest (Shearer and Tippett 1989). The decreasing incidence of Ph. cinnamomi with distance eastward is associated with decreasing rainfall and decreasing occurrence of susceptible hosts, impeding lateritic soils and disturbance from human activity (Shearer and Tippett 1989). There is also a north–south gradient with southern forests being less affected than northern forests (Shearer 1992). Infections in southern forests are mainly associated with drainage lines or roading before 1970 (Shearer 1992). Historically, southern E. marginata forests have been exposed to less of the sort of disturbance that favours spread and intensification of Ph. cinnamomi than northern forests (Shearer 1992). Phytophthora cinnamomi was first recorded in eucalypt forest in Victoria in 1969 (Podger and Ashton 1970) and has since been found to be widely distributed in Victoria (Weste and Marks 1974; Marks and Idczak 1977). About 10% of the area of State forests and national parks is infested (Marks and Smith 1991). Badly diseased native vegetation (Plate 11.2) has a mosaic-like distribution among healthy areas in association with shallow soils on water gaining sites and with roading. Greatest damage in eucalypt forests and woodlands has occurred parallel to the coast in eastern and southern Gippsland, in the Brisbane Ranges, the Grampians, a small area in the Otway Ranges, Wilsons Promontory and the southern foothills of the Great Dividing Range (Weste and Taylor 1971; Weste and Law 1973; Weste and Marks 1974; Marks and Idczak 1977; Weste 1981; Kennedy and Weste 1986). The effect of Ph. cinnamomi is greater in eucalypt forest on shallow duplex soils than on the deeper more fertile krasnozems of the southern foothills of the Great Dividing Range (Weste 1980). Infestation of the Brisbane Ranges National Park by Ph. cinnamomi increased from 1% of the area in 1970 to 31% 10 years later (Dawson

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and Weste 1985). Although only 1% of the Grampians National Park was infested in 1976, about 30% of the total area of 200,000 hectares was classified as disease prone (Marks and Smith 1991). While seedlings of several of the dominant eucalypt species in mountain forests, such as the Monocalyptus species E. delegatensis and E. regnans and the Symphyomyrtus species E. nitens, are susceptible to Ph. cinnamomi, incidence of disease in these forests is low because the activity of the fungus is limited by low soil temperatures (Marks and Idczak 1977). Although Ph. cinnamomi is widely distributed in Tasmania (Podger et al. 1990), it is not an important cause of disease in eucalypt forests, except for susceptible E. amygdalina, E. obliqua and E. sieberi growing in small, localised, poorly drained areas on the east coast (Wardlaw and Palzer 1988). Climatic analysis has enabled presently healthy plant communities that are vulnerable to infection and damage by Ph. cinnamomi to be identified (Podger et al. 1990). Phytophthora cinnamomi and other Phytophthora species are widely distributed in eucalypt forests in New South Wales (Fraser 1956; Pratt and Heather 1973a; J.A. Simpson, unpubl. data) and the Australian Capital Territory (Jehne 1970; Blowes et al. 1982). However, disease is localised and minor, even in association with disturbance (Gerrettson-Cornell et al. 1979; Bridges et al. 1980). Although localised minor damage has been recorded on sites grossly disturbed by human activity in the montane region above 800 metres along elevated parts of the southern Great Dividing Range and on the Central Highlands of Tasmania, no damage has been reported in essentially intact communities. In these places, the pathogen seems unable to survive winter cold or the soil temperature rarely rises to levels favourable for activity of the pathogen and active management of Ph. cinnamomi is not required. The possible role of several other Phytophthora species tolerant of low soil temperatures, as a possible cause of dieback in native alpine communities in the Central Highlands of Tasmania, is being investigated. In Western Australia, Victoria and Tasmania, the problems are now widely accepted as being due to ongoing and destructive colonisation of healthy communities that had not been exposed to the 264

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selective force of either Ph. cinnamomi or any close analog prior to European settlement. The occurrence of disease within these regions is uneven, being determined by local factors of topography, soil and patterns of distribution of the pathogen. The observed pattern of disease expression has resulted from multiple interactions between the pathogen, climate, soils, vegetation, time since infection and intensity of human activity. It reflects how factors of the environment have interacted to create niches available for destructive interactions between pythiaceous pathogens and their hosts.

11.5 Host–pathogen interactions 11.5.1 Symptoms The primary symptom is rot of fine roots and then larger roots. Secondary symptoms such as decline and death of branches and whole trees follow root damage. Pythiaceous pathogens do not form readily visible structures in infected tissues and so recognition of their occurrence in vegetation depends on recognition of macrosymptoms on infected plants. Lesions in fleshy primary roots are usually evident as discoloured and water-soaked lesions although asymptomatic infection has been demonstrated (O'Gara et al. 1997). Infection by Pythium rarely proceeds beyond this stage. Once aggressive species of Phytophthora have invaded host roots, primary symptoms of infection are evident as advancing fronts of necrotic lesions in the inner bark of roots and lower stems (Fig. 11.2). In lignified tissues, lesions are hidden by the outer protective bark and often go unobserved. Further detail on lesion formation, the infection process and host resistance is presented in sections 11.5.2, 11.8.2 and 11.9. Secondary symptoms of disease caused by Phytophthora species, especially Ph. cinnamomi, are evident in all growth phases of eucalypts. By contrast, disease caused by Pythium species appears to be restricted to non-lignified tissues in young roots and stems of seedlings (see Chapter 8) and undifferentiated feeder roots of mature trees. Postemergence damping-off, associated with infection by Pythium species, caused mortality of seedlings up to eight weeks after germination in a mixed eucalypt forest in Victoria (Mwanza and Kellas 1987). Mortality was significantly greater on disturbed or bare soil than on ash beds. Damping-off occurred in localised pockets or was scattered across the seedbed.

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The outer bark has been removed to show lesions of Phytophthora cinnamomi in Eucalyptus marginata. Healthy tissue is white while infected tissue is discoloured. a) The chisel indicates the lesion edge in the stem of a mature tree. b) A lesion edge in an infected lateral root. (From Shearer, B.L. and Tippett, J.T. 1989, Research Bulletin 3, Department Conservation and Land Management: Western Australia, with permission).

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There have been few studies on seedling infection in areas of forest infested with Phytophthora species. Few eucalypt seedlings survived in infested jarrah forest (Podger 1968) or mixed eucalypt forest and woodland in Victoria (Weste 1981; Weste 1986). However, in other trials susceptible species have been satisfactorily established by sowing or natural seedfall on prepared seedbeds on infested sites (Fagg 1987; Wardlaw and Palzer 1988). In other infested areas subject to clearfelling in East Gippsland, Vic., occasional seedlings of E. sieberi are killed by Ph. cinnamomi (P.J. Keane, pers. comm.). There are very few detailed reports of symptoms in the ground vegetation, understorey and dominant layers of eucalypt forest associated with other Phytophthora species. In south-east Australia, Ph. citricola and Ph. drechsleri have occasionally been isolated from eucalypt forests and plantations with dying or unthrifty trees (Pratt and Heather 1973b; Weste 1975; Gerrettson-Cornell 1980). Phytophthora citricola, a widely distributed species in forests of E. marginata in south-west Australia, has been associated rarely with mortality. The appearance of sites infested with Ph. cinnamomi varies according to the time elapsed since the fungus was introduced and site characteristics. Disease is evident as a mosaic of affected patches of vegetation that increase in size and number (Podger 1968, 1972; Marks et al. 1972). The rate of development and severity of symptom expression is greatest in infertile, water-gaining sites asssociated with concave topography and soils with dense subsoils that temporarily impede drainage. Death of the susceptible understorey species of the important Australian plant families Epacridaceae, Papilionaceae, Proteaceae and Xanthorrhoeaceae (Podger 1968; Weste et al. 1973; Weste 1986; Shearer and Dillon 1995) is the first indication that the pathogen has spread into a new area. In sites favourable for disease development, a sharp boundary or front of dead and dying understorey species, such as Banksia grandis Willd. in E. marginata forest and Xanthorrhoea australis R.Br. in certain Victorian mixed eucalypt forests, marks the boundary between infested and uninfested forest. The effect of disease is much less in free-draining fertile sites, where there is often no clear demarcation between infested and uninfested forest. The

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susceptible understorey species often die many years before symptoms appear in the eucalypt overstorey. The rate at which symptoms develop in susceptible eucalypts following infestation is variable. Above-ground symptoms on trees resemble drought damage and have been classified as chronic or acute symptoms (Podger 1968; Marks and Idczak 1977). Symptoms of the chronic form are gradual deterioration of crowns, starting with leaf chlorosis and death of primary leaf-bearing branches. New leaves formed on epicormic shoots are reduced in size, resulting in thinning of the crown. As the condition progresses, both epicormic shoot production and leaf area decline. Trees exhibiting such symptoms may survive for many years. These sublethal chronic symptoms are often confused with the effects of other damaging agencies. In the acute type of injury, the leaves of apparently healthy individuals or groups of trees wilt and turn brown, and the trees die suddenly with the leaves still attached (Plate 11.1). The trees may reshoot from epicormic buds along the stem, but do not survive the following summer. Trees of different age classes may die or the incidence of mortality may vary greatly within an area. ‘Islands’ of survivors may exist in varying degrees of health. Sometimes dead trees may occur adjacent to living trees. Temporal and spatial patterns of symptom development reflect the dynamic interactions between pathogen, host and environment. This is especially so for species of Monocalyptus which may suffer acute injury after infection by Ph. cinnamomi, but can also resist invasion by the fungus and show little damage. The balance between resistance and susceptibility depends on site and environmental conditions (see sections 11.9 and 11.10). Severe epidemics of mortality in some species of Monocalyptus over large areas have occurred periodically in years of high rainfall and on soil types with impeded drainage (Tregonning and Fagg 1984). In south-west Australia, there is some evidence of extensive death of E. marginata in 1921, 1928, the late 1940s, the late 1950s, 1964, 1973 and 1982 (Davison 1988). In the East Gippsland region of Victoria, extensive death of susceptible eucalypts was noted in 1953, 1956, 1967 and 1971 by Tregonning and Fagg (1984) who calculated that extensive mortality of susceptible eucalypts may occur once every 42 ± 16 years on infested sites.

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Although relatively few deaths occur in most years, the pathogen may still be damaging eucalypt communities on infested sites. The consequences of disease symptoms more subtle than tree death are described in section 11.7.

11.5.2 Effects of infection on host physiology Knowledge of the effects of infection by pythiaceous species on physiological processes of eucalypts is based mainly on infection of seedlings and saplings by Ph. cinnamomi. Infection of eucalypt seedlings by Ph. cinnamomi disrupts uptake, transport and utilisation of mineral nutrients by roots (Weste and Chaudhri 1982; Cahill et al. 1986b). Infection reduces mineral concentration in plant tissue of susceptible eucalypts and understorey species but not of resistant species (Halsall 1980; Weste and Chaudhri 1982; Cahill et al. 1986b), possibly reflecting the failure of mineral uptake and conduction by damaged root systems (Weste and Marks 1987). Respiration and cell wall permeability, with associated leakage of electrolytes, increased in eucalypt seedling roots following infection by Ph. cinnamomi (Cahill and Weste 1983b; Cahill et al. 1985). Increases in both root leakage and respiration followed infection and were therefore greater in susceptible than in resistant eucalypts. Most of the increase in total respiration rate of infected roots was due to accumulation of photosynthetic sugars, characteristic of metabolically inactive tissue (Cahill and Weste 1983b). Symptoms in the crowns of eucalypts infected by Ph. cinnamomi are similar to those caused by drought (Plate 11.1; Podger 1972). However, the mechanisms whereby root infection by Ph. cinnamomi can induce water stress are obscure. At least 90% of the surface roots of E. marginata saplings need to be removed before severe water stress is induced (Crombie et al. 1987). By contrast, in seedlings of E. sieberi hydraulic conductance failed and severe stress developed throughout the root system when only 8% to 15% of the root system was infected with Ph. cinnamomi (Dawson and Weste 1984). The resistant species, C. maculata, showed no change in water relations when grown in soil infested by Ph. cinnamomi.

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The observed failure in water transport when only a small proportion of the root systems of susceptible eucalypts is infected may be due to systemic induction of tyloses in xylem vessels, to toxins or to fungus-mediated hormonal imbalance (Dawson and Weste 1984). Tyloses have been seen in Ph. cinnamomi infected eucalypts, but with as few as 4% of the vessels blocked in the zone of active root growth of wilting seedlings (Marks and Tippett 1978). Tyloses also form in roots of waterlogged E. marginata seedlings in the absence of a pathogen (Davison and Tay 1985) and may be a general host reaction to stress. The role of tyloses in causing eucalypt root dysfunction in both infected and uninfected plants needs to be clarified. Glucans secreted by Ph. cinnamomi, Ph. cryptogea and Ph. nicotianae have been shown to cause wilt of both susceptible and resistant eucalypt seedlings (Woodward et al. 1980). The wilt-inducing toxin was not related to pathogenicity of the fungal species. By contrast, addition of sterile cell-free extracts of Ph. cinnamomi to either water or sand cultures of seedlings resulted in greater root discolouration and reduction in root growth in susceptible than resistant eucalypt species (Halsall 1978). The role of toxins in the pathogenicity of Phytophthora species to eucalypts is not clear. Fungus mediated hormonal imbalance may be a factor in symptom expression. A large reduction in cytokinin levels occurs in the sap of infected seedlings of susceptible E. marginata but not the resistant C. calophylla (Cahill et al. 1986a). Hormonal imbalance may be a major cause of the secondary symptoms caused by Ph. cinnamomi in seedlings of susceptible eucalypts (Cahill et al. 1986a). How this relates to symptom expression in mature trees is unknown.

11.6 Pathogenicity of Pythiaceae on eucalypts There have been innumerable studies of pathogenicity of isolates of Ph. cinnamomi on a wide variety of native species including eucalypts in liquid culture and in greenhouse trials of potted plants growing in artificial substrates or their natural soils. These tests demonstrate a much wider range of susceptible taxa than is found in the field. More certain evidence of the pathogenicity and host range of Ph. cinnamomi has been obtained from

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deliberate field inoculation with pure cultures in healthy stands. These studies include E. marginata forest communities in Western Australia (Podger 1968), heathland in Tasmania (F.D. Podger, unpubl. data) and post fire regeneration of temperate rainforest in Tasmania (Podger and Brown 1989). In most of these cases, the rigorous tests required to satisfy Koch's postulates of cause have been satisfied. Together these field inoculations form a body of unequivocal evidence that Ph. cinnamomi is an aggressive primary pathogen of an extraordinary range of higher plant species.

caused extensive pre-emergence and postemergence damping-off in most of the six Eucalyptus species tested.

Knowledge of the comparative pathogenicity of Pythium and Phytophthora species on a range of eucalypt species is incomplete. Most pathogenicity tests have used juvenile seedlings under glasshouse conditions, with few involving mature plants in forest or woodland environments.

The pathogenicities of nine species of Phytophthora to intermediate-aged eucalypt seedlings have been compared under glasshouse conditions (Marks and Kassaby 1976; Brown 1977). Only Ph. cinnamomi caused destructive root rot and consistently killed seedlings. Marks and Kassaby (1976) rated Ph. megasperma, Ph. drechsleri and Ph. cryptogea as mildly injurious to seedlings of Monocalyptus species in comparison to Ph. cinnamomi. Five Phytophthora species tested by Brown (1977) were all shown to be pathogenic to young seedlings of several eucalypt species. Phytophthora cinnamomi caused significantly greater root rot than Ph. cactorum, Ph. citricola, Ph. cryptogea or Ph. nicotianae var. parasitica.

A study of seedling mortality in a mixed eucalypt forest in Victoria found that the Pythium species isolated most frequently from Eucalyptus seedlings with damping-off were also the most pathogenic (Mwanza 1986). In pathogenicity tests on juvenile seedlings of four Eucalyptus species, the isolated Pythium species could be ranked in order of decreasing ability to cause pre-emergence dampingoff as P. intermedium > P. irregulare > P. mamillatum > P. paroecandrum > P. perplexum and P. ultimum. The ranking of these species for their ability to cause postemergence damping-off was generally similar to that for pre-emergence dampingoff. Damping-off symptoms were not expressed after the two-leaf stage of seedling development when tissues became lignified. However, P. paroecandrum caused significant feeder root necrosis in 10-weekold seedlings, reducing their vigour. The pathogenicity of isolates of Pythium and Phytophthora from diseased eucalypt forest was tested against several eucalypt species in a glasshouse (Sedgley 1974). Extensive pre-emergence damping-off in most of the Eucalyptus species tested was induced by P. (?)acanthicum, P. (?)acanthophoron, P. (?)deliense, P. irregulare, Pythium myriotylum Drechsler, P. splendens and several unidentified Pythium species. However, their ability to cause postemergence damping-off was variable. In the same experiments, isolates of Ph. cinnamomi, Ph. citricola, Ph. cryptogea, Ph. drechsleri and Ph. nicotianae var. parasitica

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In glasshouse tests, Pythium species isolated from agricultural and forest soils were far less pathogenic to eucalypt seedlings than was Ph. cinnamomi (Marks and Kassaby 1974). Pythium debaryanum R.Hesse and P. irregulare killed juvenile (2-leaf stage) but not intermediate (5-month-old) seedlings of Monocalyptus species; these species and P. vexans de Bary reduced growth of seedlings in both age groups.

The pathogenicity of eight species of Phytophthora were compared in wound inoculated stems of E. marginata in the forest (Shearer et al. 1988). Based on the linear growth rates of lesions induced in the phloem, the Phytophthora species could be divided into two distinct groups within which differences were not significant. Mean lesion extension rates for the first group comprising Ph. cactorum, Ph. cinnamomi, Ph. citricola, Ph. cryptogea (A1 mating type), Ph. nicotianae var. nicotianae and Ph. nicotianae var. parasitica were 2.3–4.0 millimetres per day, significantly greater than the 0.6 to 1.8 millimetres per day for the second group of Ph. cambivora, Ph. cryptogea (A2 mating type), Ph. megasperma var. sojae and an unidentified Phytophthora sp. Confident estimates of the relative pathogenicity of Phytophthora species can only be made when the pathogens are tested under a range of conditions. Whereas Ph. cinnamomi caused greater root rot of eucalypt seedlings than other Phytophthora species in glasshouse tests, wound inoculations in the forest

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Schematic representation of the direct and indirect impact of pythiaceous pathogens on eucalypt communities.

showed that several Phytophthora species caused similar rates of phloem necrosis to Ph. cinnamomi in E. marginata. Observations and inoculation studies have shown that Ph. cinnamomi is an aggressive primary pathogen of eucalypts. Further pathogenicity testing and ecological assessment of effect is required before accurate estimates can be made of the relative threats that pythiaceous species other than Ph. cinnamomi pose to the health of native plant communities in Australia.

11.7 Effects of disease on wood production and conservation values Change in biomass is the best indicator of disease effect. Although changes of an order of magnitude are self evident in many severely effected forests, there has been relatively little quantification of such changes. Kennedy and Weste (1986) contrasted changes in biomass in open eucalypt woodland infested with Ph. cinnamomi with uninfested woodland consisting of similar species. The infested area had only 65% of the plant mass found on the uninfested area. Furthermore the plant mass of the monocotyledonous component was increased

from 17% of the total biomass in the uninfested area to 42% in the infested area. Infestation by Ph. cinnamomi significantly alters the floristic composition and structure of vulnerable eucalypt communities and grossly degrades their conservation value. In contrast, changes to natural ecosystems caused by other soilborne fungi are often not detected (Hendrix and Campbell 1973; Sewell 1981). Soilborne fungi are nonetheless an important component of natural communities (Hendrix and Campbell 1973; Sewell 1981). According to Sewell (1981), the ‘the apparent “healthiness” (normality) of vegetation is no indication of freedom from soil-borne disease, nor is it evidence that disease is not imperceptibly but continually modifying the patterns of plant populations’. The damage to conservation and production values caused by disease in native plant communities is rarely quantified. The potential direct and indirect effects of infection by pythiaceous pathogens on the flora and fauna of eucalypt communities are shown in Figure 11.3. Many of the effects of these pathogens are interrelated and changes induced by disease can induce complex feedback loops.

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During the 1940s, mortality and crown decline of eucalypts in infested areas of south-west and southeast Australia gave rise to concern that the problem of jarrah dieback (later shown to be due to Ph. cinnamomi) would reduce timber production. This threat to the harvestable forest resource provided the stimulus for much of the research on diseases caused by pythiaceous fungi in eucalypt communities. Despite this, estimates of past losses or prognoses of potential losses are difficult to obtain. The accurate assessment of rates of regeneration, mortality and growth of eucalypts in infested compared with uninfested areas is an expensive task and, except for illustrative sample, is not often affordable. Estimates of tree mortality following Ph. cinnamomi infection vary greatly. Up to 50% of the number of E. obliqua trees per hectare died in infested forest and woodland in Victoria (Fig. 11.4). Mortality in Ph. cinnamomi-infested areas in Gippsland reduced sawlog volumes by about 7% and pulpwood volumes by about 10% over about five years. Some of these losses could have been reduced by salvage cutting (Marks and Smith 1991). In south-west Australia, almost total mortality of E. marginata occurred in some infested forests in the 1940s and 1960s (Podger 1968; Davison and Shearer 1989) but the area infested is not known. Mortality rates for E. marginata were estimated to range from 1.7% to 6% per annum at three sites over two to six years (Podger 1972), 1.5% per annum at three sites over three to five years (Crombie and Bunny 1994) and 0.84% per annum at two sites over five years (Davison and Tay 1988). The number of recently dead E. marginata trees recorded in three forest blocks assessed using aerial photography on two occasions increased from four to five trees per 100 hectares prior to 1984 to nine to 13 trees per hectare in 1984 to 1985 (Shearer and Tippett 1989). In an aerial photographic survey of over 130,000 hectares between 1978 and 1983, a low rate of death of E. marginata of 0.05 trees per hectare per annum was recorded (E. Davison, pers. comm.), which was three times the death rate in healthy forest (Davison and Shearer 1989). The use of death rates calculated over short intervals, however, can be misleading. As noted previously, individual trees of susceptible eucalypts die each year in Ph. cinnamomi-affected sites, but death of large numbers of trees occurs periodically on

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shallow, infertile sites following particular climatic conditions. Further monitoring of eucalypt mortality over time in areas infested by pythiaceous pathogens is required to provide a sound basis for management decisions. We are not aware of estimates of mortality caused by Phytophthora species other than Ph. cinnamomi. Other pythiaceous fungi contribute to poor regeneration of eucalypt stands. In Victoria, seedlings of susceptible E. obliqua failed to survive in some woodlands infested with Ph. cinnamomi (Weste 1981; Weste 1986). In a seeding trial in forest sites infested with Ph. cinnamomi and Pythium species, the number of seedlings of susceptible E. sieberi decreased more rapidly than those of resistant eucalypts (Fagg 1987). However, after seven years it appeared unlikely that E. sieberi would be eliminated, even in a high hazard site. Damping-off in a mixed eucalypt forest in Victoria, caused mainly by Pythium species, reduced seedling establishment by 10% (Mwanza 1986). Death of seedlings from other causes such as insect damage, frost heave and freezing was four times that caused by damping-off (Mwanza 1986). Further estimates of the relative effects of pythiaceous fungi and other factors on seedling regeneration are needed for a range of eucalypt communities. Fungicides could be used in studies of indigenous communities to help quantify seedling loss through disease (Paul et al. 1989). The effects of sublethal infections that reduce root development and decrease growth are often ignored. Susceptible eucalypts can suffer infection and root loss for several years before final symptom expression and death occur. Current estimates of the effect of Ph. cinnamomi on tree growth are imprecise because of the difficulty of separating confounding effects on tree growth of disease, rainfall, soil, topography, and tree vigour, age, dominance class and genetic variation in growth potential and resistance to Ph. cinnamomi (Crombie and Bunny 1994)—this accounts for the contrasting estimates of effect on growth (Podger 1972; Davison and Tay 1988; Crombie and Tippett 1990; Crombie and Bunny 1994). Gross basal area increment of infected stands of E. sieberi on well-drained foothills of East Gippsland was not related to the frequency of isolation of Ph. cinnamomi (Incoll and Fagg 1975). Sublethal root damage may interact with other factors to affect the productivity of forests. For

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Survival of Eucalyptus obliqua over time in Phytophthora cinnamomi disease centres at three locations in Victoria (circles, Narbethong; squares, Wilson's Promontory; diamonds, Brisbane Ranges) (after Weste 1980; Weste 1981; Weste and Ashton 1994).

example, root damage from infection can increase wind throw of trees in areas infested with Ph. cinnamomi (Marks et al. 1972; Weste and Law 1973; Wardlaw and Palzer 1988). However, assessment of the extent of root damage is difficult. Improved understanding is needed of the severity of root damage sustained by eucalypts following infection by pythiaceous pathogens, and of interactions with genotype, abundance of inoculum in the soil, site characteristics and environment. Excavation of the root system of E. marginata trees has clarified the extent and location of the amount of damage to fine and large root systems on several sites (Shea et al. 1982; Shearer and Tippett 1989; Davison and Tay 1995). In sites of high impact, Ph. cinnamomi was isolated from lesions in 66% of vertical roots compared to 30% of lateral roots of recently dead trees (Shea et al. 1982). On sites of low impact, 2% of vertical roots and about 5% of lateral roots of living trees were infected (Shearer and Tippett 1989; Davison and Tay 1995). Low levels of root infection probably have minimal effect on tree health unless lesions girdle the trunk collar or a significant number of vertical tap roots. The long-term effect of root infection on tree health and

growth in sites where tree mortality is low needs to be determined. Eucalypt canopy cover is reduced in infested areas following tree mortality and reduction in leaf area. In woodlands in the Brisbane Ranges, canopy cover in areas infested with Ph. cinnamomi was reduced by one-third over 20 years (Dawson et al. 1985). However, canopy cover lost through death of susceptible eucalypts can be replaced to some extent by that of resistant eucalypts increasing on infested areas. Usually the effect of Ph. cinnamomi in forest is not as evident as it is in shrubland and woodland communities. Although the susceptible shrub species are severely affected, the eucalypt overstorey in forests often survives. Within susceptible families that are important components of eucalypt communities, there is considerable interspecific variation in response to Ph. cinnamomi infection (Shearer and Dillon 1995, 1996).The most severe and extensive effects of Ph. cinnamomi on the composition and structure of eucalypt communities is on unrelated flora of the understorey and ground layers. In many places, the effect of disease is similar in south-east and south-west Australia (Podger 1972;

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Weste 1981; Weste 1986; Kennedy and Weste 1986; Shearer and Dillon 1995). The floristic composition is distinct at the species level but very similar at the generic level. Many species of the families Dilleniaceae, Epacridaceae, Myrtaceae, Papilionaceae, Proteaceae and Xanthorrhoeaceae that make up a large component of the understorey and shrub layer of eucalypt communities are commonly killed, resulting in irreversible decline in the species diversity of vegetation in infested areas. Some understorey species, mainly graminoides such as grasses, reeds and sedges, are resistant. These and resistant eucalypts colonise old dieback sites. Open woodlands with a grass-dominated lower stratum are characteristic of old diseased areas. The changes in plant community structure caused by Phytophthora infection have yet to be quantified for many eucalypt woodlands and shrublands. By permanently decreasing the density and altering the composition of the vegetation, Ph. cinnamomi may affect the temperature and water budget of eucalypt forests (Shea 1975; Shearer and Tippett 1989; Kinal 1993). Increased temperature and throughfall of rain associated with reduced cover may result in increased rates of decomposition and decreased accumulation of litter (Postle et al. 1986). Reduced ground cover caused by Ph. cinnamomi infection can lead to increased erosion (Podger 1968; Kennedy and Weste 1986). Reduced transpiration rates and rainfall interception in infested areas can result in raised watertables and increased stream salinity in salt-prone areas of the eastern E. marginata forest (Schofield et al. 1989). Increased soil water status in infested areas can also favour intensification of pythiaceous pathogens in the soil profile and may further change community structure to moisture-tolerant plant species. Pythiaceous pathogens may already be a factor in natural selection within eucalypt species. Intraspecific variation in resistance to Ph. cinnamomi has been observed in eucalypt species that are considered generally susceptible (Harris et al. 1985; Shearer and Tippett 1989; Stukely and Crane 1994). Natural selection of resistant types may partly explain survival of susceptible species on infested sites (Weste 1986) and the regeneration of susceptible eucalypts on high effect sites in Victoria (Fagg 1987; Marks and Smith 1991), although this might also reflect an element of disease escape. Mortality of seedlings caused by pythiaceous

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pathogens may lead to faster genetic change in the host population than disease in mature plants (Burdon 1982). The genetics of tree populations may also be affected by reduction of pollinator populations dependent on the nectar and pollen of affected plants (Sampson et al. 1990). The analysis of the major losses from pythiaceous pathogens shows that our inability to put monetary values on losses from disease does not mean they are unimportant. Many losses are vital to ecosystem dynamics and need quantification. Prevention of potential losses through protection of catchments and healthy communities needs to be a high priority in disease management (see Chapter 19).

11.8 Pathogen dynamics The life cycle depicted in Figure 11.5 is a simple conceptual model of the survival and dispersal of the pathogen, the infection of the host and of disease development. Changes in populations of soilborne pythiaceous pathogens result from a series of cycles consisting of non-parasitic and parasitic phases (Gilligan 1987) as shown in Figure 11.6. Populations outside a living host increase or decrease in the nonparasitic phase, which may involve saprophytic growth and sporulation in dead organic substrates in the soil. Surviving inoculum initiates primary infection in the parasitic phase and infected host tissue may initiate secondary infection. Table 11.1 summarises characteristics of the sporangia and survival spores (chlamydospores, oospores) of Phytophthora species isolated from eucalypt communities. Each of the spores mentioned in Table 11.1 and illustrated in Figure 11.5 can complete the cycle depicted in Figure 11.6. However, there have been few attempts to identify the spores of pythiaceous fungi isolated from the soil of eucalypt communities. Circumstantial evidence suggests that zoospores are probably the main type of inoculum of Ph. cinnamomi. The A2 mating type predominates in southern Australia (Shepherd and Cunningham 1978) and oospores have not been found in roots or soil in Victorian eucalypt communities (Weste and Vithanage 1978). The occurrence of oospores of homothallic Phytophthora species (Table 11.1) in eucalypt communities needs to be determined. Chlamydospores of Ph. cinnamomi have been isolated from infested soil of eucalypt woodlands in

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Reproductive structures

Sporangium Mycelium

Chlamydospore

Zoospore

Oospore

Cyst formation and germination

Lesion in root bark Figure 11.5

Spores can be dispersed in infested soil or water

Infection of roots

Generalised life cycle of pythiaceous pathogens in eucalypt communities (not drawn to scale). Microscopic mycelium oversummering in infected roots forms sporangia, chlamydospores or oospores when soil is warm and moist. In the life cycle of Phytophthora cinnamomi in south-east and south-west Australia, only sporangia and chlamydospores are formed in any numbers. Chlamydospores may germinate directly to form sporangia; these release motile zoospores which are actively or passively dispersed, leading to infection of roots. Following infection, the fungus invades root bark to form lesions that may extend into the tree collar resulting in crown decline or death of the host.

Victoria (Weste and Vithanage 1978; Weste and Vithanage 1979a) and from lowland water-gaining sites but not from freely draining upland sites in northern E. marginata forest (Shea et al. 1980; Schild 1995). Formation of sporangia and zoospores is probably the main sporulation phase influencing host infection and population density of pythiaceous pathogens in the soil. Other spore types germinate to produce sporangia (Fig. 11.5). Sporangia can produce many infectious zoospores in a short time. For example in warm, moist soil each sporangium of Ph. cinnamomi can produce 10 to 30 zoospores within one hour (Zentmyer 1980). Rapid increase in inoculum density of Ph. cinnamomi in eucalypt communities occurs following periods when warm, moist conditions favour sporangium production and zoospore release (Weste and Ruppin 1977; Shearer and Tippett 1989). Therefore, zoospores released from sporangia produced on infected roots probably function most

often as secondary inoculum in the reinfection of healthy roots of infected plants or in the infection of nearby healthy plants. They also serve as primary inoculum when they are carried in moist soil or in moving water to uninfested areas, although they have a very short life span before encysting.

11.8.1 Non-parasitic phase 11.8.1.1 Sporulation Sporulation of pythiaceous fungi depends on many factors including water potential, temperature, aeration, light, soil microflora, nutrient balance and the concentration of sterols, cations, root exudates and soil extracts. More information on the factors affecting sporulation can be found in detailed reviews by Zentmyer and Erwin (1970), Zentmyer (1980), Duniway (1983), Ribeiro (1983), Weste (1983b); Erwin and Ribeiro (1996) and Hardham and Hyde (1997).

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Figure 11.6

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Schematic representation of the non-parasitic and parasitic phases of the life cycle of pythiaceous pathogens in eucalypt communities.

In contrast to other Phytophthora species isolated from eucalypt communities, Ph. cinnamomi does not readily form sporangia in axenic culture and appears to require some inherent soil factor to stimulate the formation of sporangia. The precise nature of the stimulatory factor(s) is unknown but the effect can be influenced by soil type and soil microflora. Sandy soils from E. obliqua woodland and the E. marginata forest stimulated sporangium production of Ph. cinnamomi more than loamy soils from forested areas (Weste and Vithanage 1979b; Sochacki 1982). The stimulatory capacity of all soil types changed with season, being greatest in summer and least in winter in the E. marginata forest (Sochacki 1982) and greatest in spring and least in summer for soils of eucalypt communities in

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south-east Australia (Weste and Vithanage 1979b). Stimulation of chlamydospore and sporangium production may be a response to nutrient depletion caused by microbial competition for organic substrates (Kelley 1977; Murray 1987). In stimulatory soils, sporangium production is favoured by moist, warm, aerobic conditions. Soil water content is one of the most important factors determining sporulation of Pythiaceae, as reviewed by Duniway (1979, 1983). Sporangia are formed prolifically in soil following short periods of saturation which provide the free water necessary for sporangium formation and zoospore release without creating anoxic conditions that are inimical to sporulation. When soil water is not limiting,

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Some characteristics of sporangia, chlamydospores and oospores of Phytophthora species isolated from eucalypt communities

Compiled from Waterhouse (1963) and Newhook et al. (1978).

Spore structure

Phytophthora Phytophthora Phytophthora Phytophthora Phytophthora Phytophthora megasperma nicotianae cinnamomi citricola cryptogea drechsleri sojae parasitica

Sporangia Length (µm)

27–114

21–70

37–55

36–70

32–51

38–50

Width (µm)

20–71

15–39

23–30

26–40

23–35

30–40

Production

+/–

+/–

—

+/–

—

+

Diameter (µm)

31–50

Chlamydospores

60

Oospores Production Homothallic Heterothallic Diameter (µm)

+ + 19–54

18–38

+ +

+

27–35

33–50

+ 24–46

22–29

+, Occurrence; +/–, in some isolates only.

temperature is a determining factor for sporulation of pythiaceous pathogens in the soil. The Phytophthora species isolated from eucalypt communities require higher temperatures for sporulation than for growth.

period in spring when soils are wet and soil temperature and soil factors that stimulate sporulation are increasing as the soil warms up after winter. Although temperatures are optimal for sporangium production in summer, soil water is limiting unless summer rains occur.

11.8.1.2 Seasonal variation in sporulation Eucalypt communities of southern mainland Australia experience a Mediterranean climate—cool wet winters during which most of the annual rainfall occurs, followed by hot dry summers. This marked seasonal pattern is reflected in a cyclical variation in sporangium and chlamydospore production by Ph. cinnamomi. Seasonal changes in sporulation of other Phytophthora species in eucalypt communities has not been determined. The greatest number of sporangia of Ph. cinnamomi form in surface soil of the E. marginata forest in autumn and spring, with low numbers in winter and summer (Shea et al. 1980). Rain falling on warm, stimulatory soil creates conditions conducive to sporangium production in autumn. Few sporangia form in winter because, although soil water is not limiting, the temperature of the surface soil rapidly falls to suboptimal levels following frontal rains. Sporangia can form in the often relatively short

In the E. marginata forest, production of sporangia of Ph. cinnamomi at depth in the soil profile, just above an impeding layer, was greater and the decline in sporulation in winter and summer was less than in surface soil (Shearer and Tippett 1989). This is due to temporary ponding of water on the dense subsoil but also reflects the buffered temperature and moisture conditions at depth compared with the widely fluctuating environment at the surface. The food base provided by a concentration of roots above the impeding horizon provides a favourable niche for the fungus within the soil profile. 11.8.1.3 Survival in dead host material and soil Pythiaceous pathogens persist by continual parasitic growth within hosts. This is an important mode of survival in eucalypt communities composed mainly of susceptible, woody perennial hosts. In the absence of a host, these fungi survive adverse conditions by saprophytic colonisation of dead tissues infected

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during the parasitic phase, as saprophytes in organic substrates in soil and as spores. Based on inoculum increase and distribution in eucalypt forest soils in Victoria, Marks et al. (1975) considered Ph. cinnamomi a poor saprophytic coloniser of dead organic matter. Malajczuk (1983) concluded that ‘the competitive saprophytic ability of Phytophthora spp. is extremely low’. However, Ph. cinnamomi showed some degree of saprophytic ability in dead remains of susceptible hosts in the E. marginata forest (Schild 1995). Pythium species are also considered poor competitors with restricted saprophytic ability (Hendrix and Campbell 1973). Infected roots and stem bases provide a buffered environment for the survival of Phytophthora species during adverse conditions and a food base for inoculum increase when conditions are favourable. In the E. marginata forest, Ph. cinnamomi was isolated from 50% of the stem bases of Banksia grandis trees that had been dead for about one year, compared to only 3% of soil samples from the same site (Shea 1979). At another disease site, Ph. cinnamomi was isolated from the stem bases of 33% of Banksia grandis that had been dead for about one year, compared to only 0.1% of soil samples taken from the site (Blowes et al. 1982). Survival of the fungus is low in long dead trees (Shea 1979). This is possibly due to desiccation and competition from specialised saprophytic microorganisms in the highly lignified tissues. Saprophytic persistence of Pythiaceae probably occurs mainly when competition from other microorganisms is low, such as during rapid colonisation of virgin substrates, and when conditions are unfavourable for other organisms. For example, soils of the E. marginata forest have extremely low microbial activity (Podger 1972). This may partly account for 40% to 70% of Ph. cinnamomi colonies from infested soil originating from pieces of organic matter (Shea et al. 1980) and the persistence of the pathogen in infested areas for many years despite the great reduction in susceptible hosts (Podger 1968). Provided competition from the microflora was low, chlamydospores of Ph. cinnamomi could persist and multiply for up to eight months at matric potentials of –500 kilopascals in non-sterile soil free of a host and containing an organic substrate (Weste and Vithanage 1979a). Competition in organic substrates already colonised

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by other organisms possibly restricts pythiaceous pathogens to being opportunistic pioneers in an ecological succession of microorganisms on decaying substrates. Of the various morphological stages (Fig. 11.5), germ tubes and mycelium are least able to survive in the long term. Hyphae are rapidly lysed as their food sources are depleted or become colonised by antagonistic organisms (e.g. during advanced stages of root colonisation). Sporangia and encysted zoospores survive longer than mycelium, while chlamydospores and oospores can survive for even longer periods (Stanghellini 1974; Malajczuk 1983). Soil temperature and water content, floristic composition of the understorey, antagonistic microflora and soil type affect survival of propagules of Pythiaceae and these effects are detailed in Weste (1983b) and Stanghellini (1974). Temperatures less than freezing or greater than 35°C are unfavourable for the survival of spores and mycelium of Phytophthora species isolated from eucalypt communities. In southern Australia, the effect of high soil temperatures in summer is compounded by the occurrence of extended periods of low soil water content unfavourable for survival. Soil water content is probably the most important factor affecting survival of pythiaceous fungi in eucalypt communities, but precise information is lacking. There is only a general understanding that pythiaceous fungi will survive longer when soils are moist than when they are dry. Prediction of survival under a range of conditions requires a much better understanding of the relationships between soil water content and survival than is presently available. Chlamydospores and oospores of Pythiaceae are considered to persist under relatively harsh conditions (Duniway 1983; Malajczuk 1983). Although chlamydospores of Ph. cinnamomi persisted for up to eight months in non-sterile, host-free gravels and soils at matric potentials of –300 and –500 kilopascals (Weste and Vithanage 1979a), other studies indicate that these structures persist longer under moist conditions. Phytophthora cinnamomi survived in 70% to 90% of infected E. marginata root fragments for 56 days following incubation in lateritic soil held at soil water potentials of –2 and –10 kilopascals (Old et al. 1984b); sporangia were formed mainly at

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–2 kilopascals and chlamydospore production was favoured at –10 kilopascals. Chlamydospores of Ph. cinnamomi produced in culture did not survive in surface soil of upland sites of the E. marginata forests at matric potentials less than –100 kilopascals (Schild 1995). Changes in the composition of the understorey of the E. marginata forest alters the chemical and physical environment of the soil and affects survival of Ph. cinnamomi. In glasshouse experiments, survival of the fungus was greatest in soil amended with roots of Banksia grandis and least in soil amended with roots of Acacia pulchella R.Br. (Cary 1982). Survival was inversely correlated with ammonium levels in the soil. However, in the forest, differences in soil water content beneath different vegetation types had a greater influence on survival than did ammonium levels. Changes in the physical and chemical soil environment associated with changes in understorey composition affect both the population size and composition of the soil microflora, which in turn influence survival of Ph. cinnamomi (Malajczuk 1983). The activity of bacteria, actinomycetes, fungi and amoebae may directly or indirectly pose the greatest hazard to the survival of spores of pythiaceous fungi in warm, moist, organically rich surface soil (Malajczuk 1983). These organisms reduce survival by causing perforation and lysis of mycelium and spores, and abortion and lysis of sporangia resulting in failure of spore release. Often the mechanisms by which the microflora affect survival of spores are not known or are counteracted by other effects. For example, hyphal lysis stimulates sporangium production of Ph. cinnamomi (Malajczuk et al. 1983). Thus, although leachates of E. marginata leaf litter caused lysis of hyphae and reduced hyphal survival, stimulation of sporangium production increased overall survival of the fungus (Nesbitt et al. 1979). Microorganisms have been implicated in enforced dormancy of chlamydospores and oospores of Pythiaceae, possibly by competing for nutrients required for germination or by releasing inhibitory compounds (Malajczuk 1983). Enforced dormancy of spores increases the opportunity for their degradation by microoorganisms but also aids longterm survival by maintaining a low but continuing pathogen population (Malajczuk 1983).

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11.8.1.4 Temporal and spatial dynamics of inoculum Factors that affect survival and sporulation interact to produce fluctuations in inoculum levels in the soil. Changes in inoculum density of Ph. cinnamomi have been recorded in soils of eucalypt forests and woodlands of Victoria (Marks et al. 1973, 1975; Weste and Ruppin 1977) and south-west Australia (Shearer and Shea 1987; Shearer et al. 1989). This information has been used in the development of hygiene prescriptions for management of disease in native forests (see Chapter 19). In Victoria, inoculum levels of Ph. cinnamomi are greatest in summer. In the northern E. marginata forest of south-west Australia, it is difficult to isolate the pathogen from surface soil in dry summers, when low soil water contents reduce survival and prevent sporulation of the fungus. In this region, inoculum survives dry summers in infected hosts which are foci of inoculum production when soils become wet in autumn. Inoculum densities reach a maximum in moist soils in winter and rapidly fall as the soils dry out in summer in the E. marginata forest (Shearer and Shea 1987), but rapidly decline during winter in eucalypt forests and woodlands in Victoria (Marks et al. 1973, 1975; Weste and Ruppin 1977). Although the occurrence of low inoculum densities in winter in Victoria has been attributed to the direct effect of low temperatures, the soil temperatures experienced were not inhibitory to survival of the pathogen and were about the same as those in south-west Australia. Differences in winter inoculum levels of Ph. cinnamomi between Victoria and Western Australia may reflect differences in population levels of antagonistic microflora (Shearer and Shea 1987). In Victorian soils, populations of antagonistic microflora peaked in winter (Weste and Vithanage 1977) when temperatures and inoculum densities of Ph. cinnamomi were lowest. The seasonal pattern of inoculum increase varies from year to year depending on site and seasonal occurrence of rain (Shearer and Shea 1987). In the E. marginata forest, viable inoculum occurs in infested, water-gaining lowland areas and in the soil at depth throughout the year, reflecting extended periods of moist conditions favourable for survival and maximum coincidence of warm and moist conditions favourable for sporulation. Occasional late spring or summer rains allow inoculum to survive well into summer.

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11.8.1.5 Dispersal of inoculum Pythiaceous pathogens are actively dispersed as motile zoospores in free water and by growth through roots. Details of zoospore release and active dispersal can be found in reviews by Duniway (1979, 1983), Carlile (1986) and Erwin and Ribeiro (1996). Passive dispersal of encysted zoospores occurs in moist soil or flowing water. Pythium species actively extend through the soil by mycelial growth from one seedling to another (Garrett 1970). Although Ph. cinnamomi can grow up to three centimetres through non-sterile soil (Zentmyer and Mircetich 1966), growth through roots is more important for active extension of the fungus. Phytophthora cinnamomi can grow up to one centimetre per day in roots of susceptible Banksia grandis in summer when temperatures are optimal for fungal growth (Shearer et al. 1987b). Thus in E. marginata forest, although activity of the fungus in dry soil can cease during summer, disease centres will continue to expand through growth of the fungus in roots of susceptible hosts. Upslope spread of Ph. cinnamomi associated with growth through infected roots varied from an average of 0.8 metres per annum in the E. marginata forest (Shea and Dillon 1980) to 6.6 metres per annum in stringybark eucalypt forest in the Brisbane Ranges of Victoria (Weste et al. 1976). Vectored dispersal, in contrast to autonomous dispersal, can result in transport of inoculum of soilborne pythiaceous pathogens over very large distances. New centres of infection can originate from movement of inoculum in moist soil and infected plant tissue. Human activity is the most important vector agent and is probably the main mechanism by which species of Phytophthora and possibly Pythium have been disseminated widely. Restriction of human access is important in controlling Ph. cinnamomi in forests in south-west Australia (Shearer and Tippett 1989) and Victoria (Marks and Smith 1991) (see Chapter 19). Use of pathogen-infested gravel in road construction is a major potential means of spread of these fungi (Podger 1968). Chlamydospores of Ph. cinnamomi are believed to survive for up to eight months in gravel free of host tissue (Weste and Vithanage 1979a). Prior to knowledge of the association between Ph. cinnamomi and dieback in eucalypt forests in southern Australia, gravel for roads was

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taken selectively from areas with dead and dying vegetation (Podger 1968). This practice dispersed inoculum of Ph. cinnamomi over large areas and initiated many new infections; it accounts for the common association of eucalypt dieback with roads in these forests. Vehicular traffic in forests and along unsealed roads is an effective mechanism of dispersal in addition to dispersal during road construction. Batini (1973) demonstrated that vehicles can pick up and move infested soil. The results of passive dispersal of Ph. cinnamomi in water are noticeable as rapid spread of disease along drainage lines and the development of fanshaped diseased areas below road drains. The rate of downhill spread of disease associated with drainage water varied from 40 metres per annum in E. marginata forest (Podger 1972) to 400 metres per annum in eucalypt woodland and forest in Victoria (Weste et al. 1976; Weste 1983b). Lateral seepage of near-surface water is one of the main mechanisms of passive dispersal of inoculum at depth in soils of the E. marginata forest where coarse textures or aggregate structures occur over an impeding layer (Shea et al. 1983; Kinal 1986; Shearer and Tippett 1989; Kinal et al. 1993). Vertical dispersal in water flowing down fissures and root channels is probably important for the infection of the deep root systems of eucalypts. Subsurface hydrology explains spread along contours which can vary from four metres per annum in E. marginata forest (Podger 1972) to 171 metres per annum in shallow soils and 12 metres per annum in deeper soils in eucalypt forests of Victoria (Weste and Law 1973). These processes link disease development with specific site characteristics that affect sporulation, survival and dispersal of Ph. cinnamomi and infection of E. marginata at depth in the soil (Shea et al. 1983; Shearer and Tippett 1989). 11.8.1.6 Germination of survival structures and attraction of zoospores Prior to the infection of plant roots by soilborne pythiaceous pathogens, surviving sporangia and spores must germinate either directly to form a germ tube or indirectly by the production of zoospores (Fig. 11.5). Although these alternative germination strategies allow spore structures to rapidly adapt to changing conditions, specific information on the environmental factors favouring one form of germination over the other is lacking. Soil water status, temperature and nutrition are the main

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factors affecting the germination behaviour of survival structures (see reviews by Zentmyer and Erwin 1970; Hendrix and Campbell 1973; Stanghellini 1974; Duniway 1983; Ribeiro 1983; Erwin and Ribeiro 1996). Motile zoospores are attracted to the root surfaces or their rhizospheres, where they accumulate, encyst and germinate, leading to penetration of host tissue by the emerging germ tube. Zoospores of Ph. cinnamomi are attracted chemically to the root surface of eucalypts and are trapped within a zone close to the source of the chemical attractant, accumulating around the zone of elongation or wounds within minutes after roots are immersed in a zoospore suspension (Palzer 1976; Brown 1977). Zoospores frequently germinate within minutes of encystment on the root surface (Tippett et al. 1976). Roots of most plant species of the eucalypt communities studied attract zoospores of Ph. cinnamomi, irrespective of the susceptibility of the species (Palzer 1976; Tippett et al. 1976; Brown 1977; Malajczuk and McComb 1977; Halsall 1978; Hinch and Weste 1979). Although in some studies there were no quantitative differences in attraction of zoospores to roots of different plant species from eucalypt communities (Malajczuk and McComb 1977; Hinch and Weste 1979), some host specificity may occur, as originally reported by Zentmyer (1961) for agricultural crops. For example, more zoospores are attracted to roots of species of Monocalyptus than to those of Symphyomyrtus (Tippett et al. 1976; Brown 1977; Halsall 1978).

11.8.2 Parasitic phase 11.8.2.1 Infection Germ tubes enter young unsuberised eucalypt roots by rapid penetration between epidermal cells (Tippett et al. 1976; Malajczuk et al. 1977; Cahill et al. 1989). The minimum number of zoospores of Ph. cinnamomi resulting in infection of eucalypt seedlings ranged from five to 20 spores when applied just behind the root tip under aseptic conditions (Byrt and Holland 1978; Weste and Cahill 1982) to over 200 spores (Palzer 1976). This agrees with estimates by Mitchell (1978) that the lowest number of zoospores per plant resulting in significant percentages of infection was 50 for a range of Pythium and Phytophthora species on agricultural crops. Estimates of the probability of a single

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zoospore of Ph. cinnamomi infecting a plant ranged from greater than 0.032 for susceptible Banksia grandis to 0.011 for resistant C. calophylla, 0.009 for susceptible E. marginata, and 0.002 for resistant E. diversicolor (Palzer 1976). Direct penetration of the outer epidermal cell walls is associated with swellings of the germ tubes which have been described as appressoria (Palzer 1976; Brown 1977). Dissolution of cell walls near penetrating hyphae indicates that root penetration by Ph. cinnamomi is aided mainly by enzymic action rather than mechanical pressure (Tippett et al. 1976; Malajczuk et al. 1977). Several hours after penetration the germ tube is sealed off from the outside by a plug of pectin-like material. As hyphae of pythiaceous fungi have no cross walls, the formation of such plugs may be important in preventing entry of antagonistic microorganisms from the rhizosphere (Tippett et al. 1976). Infection of root tissues may be moderated by ectomycorrhial symbionts and the mycorrhizosphere population associated with the roots (Malajczuk 1988) (see Chapter 6). Some ectomycorrhiza have no effect on Ph. cinnamomi infection while the mantles of others prevent germ tube penetration. Although root contact is thought to be an important mechanism by which Phytophthora species spread in infested eucalypt communities, the importance of mycelial infection of roots by root to root contact has not been evaluated. In axenic experiments, hyphae of Ph. cinnamomi commonly entered roots of eucalypt seedlings by penetrating root hairs in the zone just behind the root cap (Tippett et al. 1976). The mycelium grew on the root surface and may be responsible for spread of infection along the roots (Tippett et al. 1976). In young seedling roots of eucalypts inoculated with Ph. cinnamomi, intercellular hyphae invaded the root cortex within 12 hours of infection (Halsall 1978). Tissue at the site of penetration turned brown and lesion formation occurred between eight and 16 hours after inoculation (Cahill et al. 1989). Lesion expansion in seedling roots of a resistant eucalypt stopped within 48 to 72 hours and such lesions remained limited in size. In young roots of susceptible E. marginata, Palzer (1976) observed diminished lesion extension after five days and limited invasion from primary into secondary root tissue. However, in other studies lesions increased in length in roots of susceptible eucalypts and eventually entered the collar region of the

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seedlings (Batini 1974; Smith and Marks 1982; Cahill et al. 1989). Studies of the infection process of Phytophthora species have been conducted mainly with seedling roots. There have been no definitive studies of entry through mature woody roots of eucalypts. It is possible that Ph. cinnamomi enters woody roots through wounds (Shearer and Tippett 1989), by direct invasion between layered periderms (Dell and Malajcuk 1989), via adventitious roots emerging through bark (Marks et al. 1981; Dell and Malajcuk 1989) or by gradual progression up lateral roots and thence into the stem (Smith and Marks 1982; Cahill et al. 1989; Shearer and Tippett 1989). Zoospores of Ph. cinnamomi may infect soft suberised tissues of flooded stem bases of one-year-old E. marginata seedlings (O’Gara et al. 1996, 1997). In small primary roots, Ph. cinnamomi extended most rapidly in the phloem (Tippett et al. 1976). The hyphae penetrated intercellularly and intracellularly with cell death evident in advance of invading hyphae. Infection of the root cortex resulted in diffuse hydrolysis of cell walls. Establishment of Ph. cinnamomi and initial disruption of undifferentiated root tissues occurred in both resistant and susceptible species of eucalypt (Tippett et al. 1977). As lesions of Ph. cinnamomi extend into more mature, differentiated roots, the phloem is discoloured (Fig. 11.2) due to the accumulation and oxidation of polyphenols (Tippett et al. 1983). In secondary roots of E. marginata, spread is most rapid in the expanded spongy tissue of the outer phloem. Invasion of the inner phloem results in death of the cambium. Infection also occurs in xylem adjacent to the cambium, but is much less there than in the phloem (Tippett et al. 1983; Tippett and Hill 1984). Tyloses develop in xylem vessels and tannins accumulate in ray cells (Marks and Tippett 1978; Smith and Marks 1982; Tippett et al. 1983). Wound periderms of suberised and lignified cells restrict lesion development (Tippett et al. 1983; Fig. 11.7). Radial walls of necrophylactic periderm (a band of suberised cells formed as a result of disordered division of tissue adjacent to necrotic phloem) often form the boundary between living and dead tissue. Following the establishment of necrophylactic periderm, exophylactic periderm

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can form by the same process as normal bark to protect healthy tissue (Tippett and Hill 1984). The rate of periderm formation and width of suberised bands varies greatly both between and within eucalypt species. 11.8.2.2 Sporulation In pot trials, sporangia of Ph. cinnamomi were formed on hyphae re-emerging from infected primary roots within one to two days of infection of eucalypt seedlings (Batini 1974; Palzer 1976; Brown 1977; Halsall 1978; Cahill et al. 1989). Sporangium production was more prolific on tap roots than lateral roots of E. marginata seedlings (Davison and Tay 1987). Chlamydospores of Ph. cinnamomi form in infected seedling roots at later stages of infection (Malajczuk et al. 1977; Byrt and Holland 1978; Cahill et al. 1989). The ability of Phytophthora species to sporulate on a range of eucalypt species in the field has not been assessed.

11.9 Resistance mechanisms Observation of forests and woodlands infested with Ph. cinnamomi and the results of inoculation tests on seedlings allow classification of eucalypt species into resistant and susceptible types. This is reflected at the cellular level where there is a gradient from highly susceptible to highly resistant responses (Cahill et al. 1989). The morphological, biochemical and genetic bases of resistance operating in eucalypt hosts against pythiaceous pathogens have not been resolved. In in vitro experiments, zoospores of many species of Pythiaceae are attracted indiscriminately to the roots of resistant as well as susceptible plant species (Hickman and Ho 1966). However, significantly more zoospores of Ph. cinnamomi were attracted to roots of susceptible eucalypts of the subgenus Monocalyptus than to those of the resistant Symphyomyrtus species (Tippett et al. 1976; Brown 1977; Halsall 1978). Whether differences in attraction of zoospores are important in the expression of resistance in the forest is not known. Expression of resistance also depends on plant age. Roots of seedlings of several resistant species of Symphyomyrtus were susceptible to Ph. cinnamomi when seven days old but were resistant at 14 days (Brown 1977). Cahill and Weste (1983a) found that none of the species examined, including some with

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Expression of resistance to Phytophthora cinnamomi during invasion of coppice stems of Corymbia calophylla. K, kino vein; C, vascular cambium; X, xylem; EP, exophylactic periderm around lesion; P, new layer of spring periderm; arrowhead indicates where cambium has been killed by the fungus. 1) Lesion confined by periderms, but xylem callus curls have not closed the gap where the cambium has been killed. Kino has oozed into space below the lesion. 2) Lesion contained in a stem at a later stage of recovery than shown in (1). 3) Lesion almost shed. (From Tippett, J.T. et al. 1985, Australian Journal of Botany 33, 409–418, with permission).

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high field resistance species, were completely resistant at the seedling stage, even to a small dose of 10 to 20 zoospores. Resistance to invasion is expressed as limited colonisation and necrosis following infection (Byrt and Holland 1978; Cahill et al. 1989). The rate of growth of Ph. cinnamomi in roots of seedlings of resistant Symphyomyrtus species was about half that in susceptible Monocalyptus species (Byrt and Holland 1978). No specific anatomical or histological feature in primary root tissues has been consistently associated with resistance of mature trees (Cahill et al. 1989). Callose deposits or papillae formed on root cell walls in response to infection were observed encasing hyphae of Ph. cinnamomi in resistant plant species (Cahill and Weste 1983a). Papillae also formed in susceptible E. marginata when low temperatures restricted fungal growth (Cahill et al. 1989). Although there is little evidence that papilla formation prevents fungal growth through the root, it may delay or reduce intercellular penetration (Cahill and Weste 1983a). The resistance of many species of Symphyomyrtus to Ph. cinnamomi was expressed in secondary root tissue as complete inhibition of fungal colonisation at points of inoculation. Accumulation of phenolic compounds may contribute to this type of resistance (Tippett et al. 1985). The resistant reaction of roots of C. calophylla seedlings to Ph. cinnamomi has been linked to the activity of phenylalanineammonia lyase in the phenylpropanoid pathway, together with increased lignification and synthesis of new phenolic compounds (Cahill and McComb 1992). Formation of morphological barriers such as necrophylactic and exophylactic periderms in secondary tissue may be important in resistance to Ph. cinnamomi (Tippett and Hill 1984). Lesions formed following initial establishment of the fungus in the phloem of roots of resistant C. calophylla are confined by periderm layers and are shed in a manner typical of annual cankers (Tippett et al. 1985; Fig. 11.7). Susceptibility was associated with the inability of eucalypt species to prevent ‘break-out’ from lesions that periodically have been confined by periderm formation or by unsuitable physiological status of the host. As resistance can be expressed in roots of young seedlings of some eucalypt species (Brown 1977;

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Cahill et al. 1989) without the formation of morphological barriers (Cahill et al. 1989), physiological and biochemical mechanisms of resistance are also likely to be of importance (Tippett et al. 1985; Cahill et al. 1989). The ability of pythiaceous fungi to sporulate on or survive in infected host tissue may be a factor in the susceptibility of eucalypt species (Tippett et al. 1985). Although sporangia of Ph. cinnamomi are formed on infected roots of both susceptible and resistant eucalypts (Batini 1974; Palzer 1976; Brown 1977; Malajczuk and McComb 1977; Byrt and Holland 1978; Halsall 1978; Cahill et al. 1989), they develop more rapidly and in greater numbers on roots of susceptible Monocalyptus species than of resistant Symphyomyrtus species (Brown 1977). Chlamydospores of Ph. cinnamomi were formed in 35% of infected seedlings of two Monocalyptus species but none were formed in infected seedlings of three Symphyomyrtus species (Byrt and Holland 1978). Sporulation on roots of susceptible eucalypt species favours secondary infection.

11.10 Effects of environment on disease development in established infections Environmental factors affect the pathogen directly and also influence host physiology and the ongoing interaction between fungus and host.

11.10.1 Temperature Little attention has been given to the variable effects of temperature on penetration of the host and growth within host tissue (Duniway 1983; Shearer et al. 1987b). Infection of seedling roots of susceptible and resistant eucalypts, for example, can occur at temperatures as low as 6°C but optimal temperatures for infection are usually in the range of 18°C to 22°C (Halsall and Williams 1984). Lesions of Ph. cinnamomi in seedling roots of C. calophylla increased in length for up to four days after zoospore inoculation in the temperature regime 14°C (night) to 28°C (day), but did not increase thereafter (Grant and Byrt 1984). In contrast, rate of lesion extension of Ph. cinnamomi in E. marginata seedling roots increased across the range 17°C to 28°C. Optimal temperatures for growth of the fungus in secondary phloem of woody roots of E. marginata were 25°C to 30°C (Shearer et al.

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1987b), with estimates of the minimum and maximum temperatures for growth being 5°C and 34°C, respectively.

11.10.2 Soil water Soil water conditions affect not only development of Ph. cinnamomi in the soil but also plant water status and, consequently, the growth rate of the fungus in the secondary phloem of eucalypts (Smith and Marks 1983, 1985, 1986; Tippett and Hill 1983; Tippett et al. 1987; Bunny et al. 1995). Trees of susceptible eucalypts suffering water stress were less susceptible to invasion by Ph. cinnamomi than well watered trees. Inhibition of lesion development occurs at levels of water stress that have no permanent adverse effects on trees adapted to drought. Growth of Ph. cinnamomi in phloem of E. marginata was completely halted at a water potential of –1500 kilopascals (Tippett et al. 1987).

11.10.3 Soil temperature–water interactions Lesions in roots of E. marginata in the forest were shorter than predicted if only temperature influenced the rate of fungal growth; this was particularly the case in summer (Shearer et al. 1987b). In summer, higher temperatures may enhance the ability of the host to confine lesions or the lesions may be constrained by the low water status of the tree (Tippett and Hill 1983; Tippett et al. 1987).

11.10.4 Nutrition Nutrient status affects growth, vigour and survival of eucalypts infected with Ph. cinnamomi. In a forest trial, a single fertiliser treatment increased seedling mortality of susceptible and resistant eucalypts compared to the non-fertilised treatment (Marks et al. 1973). Greatest mortality occurred in eucalypts of the subgenus Monocalyptus. The addition of macronutrients in pot trials increased mortality of E. marginata seedlings, the number of seedlings infected with Ph. cinnamomi and the extent of infection in infected plants (Dell and Malajczuk 1989). Nutritional imbalance between nitrogen and phosphorus caused greatest reduction in the growth of infected seedlings of susceptible and resistant eucalypts, and resulted in increased isolation of Ph. cinnamomi from infected roots (Halsall et al. 1983). Calcium nutrition may affect resistance of trees to Ph. cinnamomi. Amendment of acid sand culture

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with calcium reduced infection of seedling roots of E. marginata (Boughton et al. 1978), and liming of four soils in a pot trial reduced E. marginata seedling mortality and plant and root infection in three gravel soils, but not in a loam (Dell and Malajczuk 1989). Further study is required under both controlled and conditions experienced in eucalypt communities to evaluate the importance of nutrition in the response of eucalypts to pythiaceous pathogens.

11.10.5 Predisposition by environmental stress Flooding, drought and salinity stress can predispose plants in cultivation to disease caused by a number of Phytophthora species (MacDonald 1982; Duniway 1983; Sulistyowati and Keane 1992; Erwin and Ribeiro 1996). The effects of environmental stress on the field susceptibility of eucalypts to pythiaceous fungi has not been extensively investigated, although in E. marginata development of lesions caused by Ph. cinnamomi is restricted by water stress (Tippett and Hill 1983). Seedlings are commonly predisposed to infection by pythiaceous fungi if drainage is poor (Duniway 1983) and the same may be true of mature trees. Eucalypts vary in their tolerance to waterlogging, with many Monocalyptus species being intolerant and many Symphyomyrtus species being tolerant (Brown 1977). Susceptibility to Ph. cinnamomi and sensitivity to waterlogging may be related in eucalypts (Newhook and Podger 1972; Brown 1977), although the physiological basis for the relationship is not known. For E. marginata, waterlogging at the same time as, or after inoculation, increased infection of seedling roots by zoospores of Ph. cinnamomi (Davison and Tay 1987). Flooding of E. marginata seedlings before inoculation did not increase infection. Davison (1997) proposed that dieback of E. marginata is attributable to the direct effects of waterlogging and not to infection by Ph. cinnamomi. However, it is important to distinguish between the effects of short periods of soil saturation with aerated waters, which favour the activity of pythiaceous fungi without affecting plant roots, and prolonged periods of soil saturation leading to anoxia (i.e. waterlogging). The latter inhibits both the activity of fungi and adversely affects the health of roots. Although many diseased sites in southern Australia are water-gaining sites, they are often dominated by eucalypts sensitive

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to waterlogging (e.g. E. marginata and E. sieberi) suggests that the effect on these sensitive eucalypts of periodic soil saturation had little influence on their health prior to the introduction of Ph. cinnamomi. Trees of E. marginata and E. sieberi suffering drought stress are less susceptible to invasion by Ph. cinnamomi than well-watered trees (Smith and Marks 1985, 1986; Tippett et al. 1987). This contrasts with the finding that drought stress predisposes resistant and susceptible rhododendron cultivars to root rot caused by Ph. cinnamomi (Blaker and MacDonald 1981). The difference could be because these particular eucalypts are highly tolerant to drought stress. Salinity stress predisposes ornamental and citrus trees to Phytophthora root rot (MacDonald 1982; Sulistyowati and Keane 1992). The relevance of these observations is of interest, particularly in view of the consequences for remnant vegetation affected by salinisation of soils following excessive vegetation clearance in southern Australia.

11.11 Conclusion Recognition of the threat that Ph. cinnamomi posed to eucalypt communities in the mid 1960s greatly stimulated research into forest pathology in Australia. There is no doubt that its introduction to the forests of south-east and south-west Australia has caused one of the greatest ecological disasters affecting eucalypt communities in recent times. ‘There are no comparable records in the history of plant pathology of a pathogen invading native forests and destroying whole natural communities on the scale observed in Australia’ (Weste and Marks 1987). Changes in community structure and composition following infestation by Ph. cinnamomi have been well documented in woodlands and forests in Victoria, but improved understanding of the effect of Ph. cinnamomi on both production and conservation values is required for eucalypt communities in other areas of Australia. Estimation of past or potential losses to the harvestable forest resource is difficult as there have been no adequate assessments of death over time, or regeneration and growth rates of eucalypts in diseased sites compared to healthy forest. A sound basis for management decisions would be provided by further monitoring of changes in vegetation health, composition and density

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following infestation of eucalypt communities by Ph. cinnamomi. The relative importance of other pythiaceous fungi in causing disease in native forests remains to be determined. Further understanding is required of the effect of forestry management practices on the soil environment and the activity of Ph. cinnamomi and other pythiaceous fungi. There is evidence of wide variation in susceptibility of genotypes within species regarded as generally field susceptible. Further work is required on selection of resistant genotypes for use in rehabilitation of diseased areas.

11.12 Acknowledgment Our thanks to Catherine Shearer for drawing Figure 11.5.

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Shea, S.R. (1979). Phytophthora cinnamomi Rands—a collar rot pathogen of Banksia grandis Willd. Australasian Plant Pathology 8, 32–34. Shea, S.R. and Dillon, M.J. (1980). Rate of Spread of Phytophthora cinnamomi Rands Infection in the Jarrah (Eucalyptus marginata Sm.) Forest. Research Paper 65. (Forests Department: Western Australia.) Shea, S.R., Gillen, K.J. and Leppard, W.I. (1980). Seasonal variation in population levels of Phytophthora cinnamomi Rands in soil in diseased, freely drained Eucalyptus marginata Sm sites in the northern jarrah forest of south–western Australia. Protection Ecology 2, 135–156. Shea, S.R., Shearer, B. and Tippett, J. (1982). Recovery of Phytophthora cinnamomi Rands from vertical roots of jarrah (Eucalyptus marginata Sm.). Australasian Plant Pathology 11, 25–28. Shea, S.R., Shearer, B.L., Tippett, J.T. and Deegan, P.M. (1983). Distribution, reproduction, and movement of Phytophthora cinnamomi on sites highly conducive to jarrah dieback in south western Australia. Plant Disease 67, 970–973. Shearer, B.L. (1990). Dieback of native plant communities caused by Phytophthora species—a major factor affecting land use in south-western Australia. Land and Water Research News 5, 15–26. Shearer, B.L. (1992). The ecological implications of disease in the southern forest of south-western Australia. In Research on the Impact of Forest Management in South Western Australia. (Ed. M. Lewis) CALM Occasional Paper No. 2/92, pp. 99–113. (Department of Conservation and Land Management: Como.) Shearer, B.L. (1994). The major plant pathogens occurring in native ecosystems of south-western Australia. Journal of the Royal Society of Western Australia 77, 113–122. Shearer, B.L. and Dillon, M. (1995). Susceptibility of plant species in Eucalyptus marginata forest to infection by Phytophthora cinnamomi. Australian Journal of Botany 43, 113–134. Shearer, B.L. and Dillon, M. (1996). Susceptibility of plant species in Banksia woodlands on the Swan Coastal Plain, Western Australia, to infection by Phytophthora cinnamomi. Australian Journal of Botany 44, 433–445. Shearer, B.L. and Shea, S.R. (1987). Variation in seasonal population fluctuations of Phytophthora cinnamomi within and between infected Eucalyptus marginata sites of south western Australia. Forest Ecology and Management 21, 209–230. Shearer, B.L. and Tippett, J.T. (1989). Jarrah dieback: The dynamics and management of Phytophthora cinnamomi in the jarrah (Eucalyptus marginata) forest of south-western Australia. Research Bulletin 3. (Department of Conservation and Land Management: Western Australia.)

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Shearer, B.L., Michaelsen, B.J. and Warren, H.J. (1987a). Comparative behaviour of Phytophthora species in the secondary phloem of stems and excised roots of Banksia grandis and Eucalyptus marginata. Australian Journal of Botany 35, 103–110. Shearer, B.L., Shea, S.R. and Deegan, P.M. (1987b). Temperature and growth relationships of Phytophthora cinnamomi in the secondary phloem of roots of Banksia grandis and Eucalyptus marginata. Phytopathology 77, 661–665. Shearer, B.L., Michaelsen, B.J. and Somerford, P.J. (1988). Effects of isolate and time of inoculation on invasion of secondary phloem of Eucalyptus spp. and Banksia grandis by Phytophthora spp. Plant Disease 72, 121–126. Shearer, B.L., Dillon, M.J. and Buehrig, R.M. (1989). Population dynamics of Phytophthora cinnamomi in Banksia woodlands and the jarrah forest of southwestern Australia. Abstract 181. Proceedings of the Australasian Plant Pathology Society Seventh National Conference, University of Queensland, Brisbane. (Australasian Plant Pathology Society: Brisbane.) Shepherd, C.J. (1975). Phytophthora cinnamomi—an ancient immigrant to Australia. Search 6, 484–490. Shepherd, C.J. and Cunningham, R.B. (1978). Mating behaviour of Australian isolates of Phytophthora species. II Phytophthora cinnamomi. Australian Journal of Botany 26, 139–151. Smith, I.W. and Marks, G.C. (1982). Observations of the infection process of Phytophthora cinnamomi on Eucalyptus sieberi. Australasian Plant Pathology 11, 2–3. Smith, I.W. and Marks, G.C. (1983). Influence of Acacia spp. on the control of Phytophthora cinnamomi root rot of Eucalyptus sieberi. Australian Forest Research 13, 231–240. Smith, I.W. and Marks, G.C. (1985). Inhibition of Phytophthora cinnamomi lesion development in Eucalyptus sieberi through moisture stress. Australasian Plant Pathology 14, 55–56. Smith, I.W. and Marks, G.C. (1986). Effect of moisture stress in Eucalyptus sieberi on growth of lesions caused by Phytophthora cinnamomi. Australian Forest Research 16, 273–279. Sochacki, S.J. (1982). A comparative study of four northern jarrah forest soil types in relation to Phytophthora cinnamomi Rands. Honours Thesis, Murdoch University, Western Australia. Stanghellini, M.E. (1974). Spore germination, growth and survival of Pythium in soil. Proceedings of the American Phytopathological Society 1, 211–214. Stukely, M.J.C. and Crane, C.E. (1994). Genetically based resistance of Eucalyptus marginata to Phytophthora cinnamomi. Phytopathology 84, 650–656. Sulistyowati, L. and Keane, P.J. (1992). Effect of soil salinity and water content on stem rot caused by Phytophthora citrophthora and accumulation of

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phytoalexin in citrus rootstocks. Phytopathology 82, 771–777. Tippett, J.T. and Hill, T.C. (1983). The relationship between bark moisture and invasion of Eucalyptus marginata by Phytophthora cinnamomi. Australasian Plant Pathology 12, 40–41. Tippett, J.T. and Hill, T.C. (1984). Role of periderm in resistance of Eucalyptus marginata roots against Phytophthora cinnamomi. European Journal of Forest Pathology 14, 431–439. Tippett, J.T., Holland, A.A., Marks, G.C. and O'Brien, T.P. (1976). Penetration of Phytophthora cinnamomi into disease tolerant and susceptible eucalypts. Archives of Microbiology 108, 231–242. Tippett, J.T., O'Brien, T.P. and Holland, A.A. (1977). Ultrastructural changes in eucalypt roots caused by Phytophthora cinnamomi. Physiological Plant Pathology 11, 279–286. Tippett, J.T., Shea, S.R., Hill, T.C. and Shearer, B.L. (1983). Development of lesions caused by Phytophthora cinnamomi in the secondary phloem of Eucalyptus marginata. Australian Journal of Botany 31, 197–210. Tippett, J.T., Hill, T.C. and Shearer, B.L. (1985). Resistance of Eucalyptus spp. to invasion by Phytophthora cinnamomi. Australian Journal of Botany 33, 409–418. Tippett, J.T., Crombie, D.S. and Hill, T.C. (1987). Effect of phloem water relations on the growth of Phytophthora cinnamomi in Eucalyptus marginata. Phytopathology 77, 246–250. Titze, J.F. and Palzer, C.R. (1969). Host list of Phytophthora cinnamomi Rands with special reference to Western Australia. Technical Note 1. (Forestry and Timber Bureau: Canberra.) Tregonning, K.C. and Fagg, P.C. (1984). Seasonal rainfall and Eucalyptus dieback epidemics associated with Phytophthora cinnamomi in Gippsland, Victoria. Australian Forest Research 14, 219–234. von Broembsen, S.L. (1989). Biogeography of Phytophthora cinnamomi mating types in South Africa. Phytopathology 79, 1185. von Broembsen, S.L. and Kruger F.J. (1985). Phytophthora cinnamomi associated with mortality of native vegetation in South Africa. Plant Disease 69, 715–717. Wardlaw, T.J. and Palzer, C. (1988). Regeneration of Eucalyptus species in an Eastern Tasmanian coastal forest in the presence of Phytophthora cinnamomi. Australian Journal of Botany 36, 205–215. Waterhouse, G.M. (1963). Key to the species of Phytophthora de Bary. Mycological Papers No. 92. (Commonwealth Mycological Institute: Kew.) Wattle Research Institute (1973). Report of the Wattle Research Institute, 1972–1973. (University of Natal: Pietermaritzburg.)

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Weste, G. (1975). Phytophthora drechsleri and Eucalyptus viminalis. Australian Plant Pathology Society Newsletter 4, 38. Weste, G. (1980). Vegetation changes as a result of invasion of forest on krasnozem by Phytophthora cinnamomi. Australian Journal of Botany 28, 139–150. Weste, G. (1981). Changes in the vegetation of sclerophyll shrubby woodland associated with invasion by Phytophthora cinnamomi. Australian Journal of Botany 29, 261–276. Weste, G. (1983a). Dieback and death of Eucalyptus tetrodonta due to Phytophthora cinnamomi in native forest at Nhulunbuy, N.T. Australasian Plant Pathology 12, 42–44. Weste, G. (1983b). Population dynamics and survival of Phytophthora. In Phytophthora: Its Biology, Taxonomy, Ecology, and Pathology. (Eds D.C. Erwin, S. Bartnicki-Garcia and P.H. Tsao) pp. 237–257. (The American Phytopathological Society: St Paul, MN, USA.) Weste, G. (1986). Vegetation changes associated with invasion by Phytophthora cinnamomi of defined plots in the Brisbane Ranges, Victoria, 1975–1985. Australian Journal of Botany 34, 633–648. Weste, G. and Ashton, D. H. (1994). Regeneration and survival of indigenous dry sclerophyll species in the Brisbane Ranges, Victoria, after a Phytophthora cinnamomi epidemic. Australian Journal of Botany 42, 239–283. Weste, G. and Cahill, D. (1982). Changes in root tissue associated with infection by Phytophthora cinnamomi. Phytopathologische Zeitschrift 103, 97–108. Weste, G. and Chaudhri, M.A. (1982). Changes in the mineral composition of plants infected with Phytophthora cinnamomi. Phytopathologische Zeitschrift 105, 121–141. Weste, G. and Law, C. (1973). The invasion of native forest by Phytophthora cinnamomi. III. Threat to the National Park, Wilson's Promontory, Victoria. Australian Journal of Botany 21, 31–51. Weste, G. and Marks, G.C. (1974). The distribution of Phytophthora cinnamomi in Victoria. Transactions of the British Mycological Society 63, 559–572. Weste, G. and Marks, G.C. (1987). The biology of Phytophthora cinnamomi in Australasian forests. Annual Review of Phytopathology 25, 207–229. Weste, G. and Ruppin, P. (1977). Phytophthora cinnamomi: Population densities in forest soils. Australian Journal of Botany 25, 461–475. Weste, G.M. and Taylor, P. (1971). The invasion of native forest by Phytophthora cinnamomi. I Brisbane Ranges, Victoria. Australian Journal of Botany 19, 281–294. Weste, G. and Vithanage, K. (1977). Microbial populations of three forest soils: Seasonal variation

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and changes associated with Phytophthora cinnamomi. Australian Journal of Botany 25, 377–383. Weste, G. and Vithanage, K. (1978). Seasonal variation in numbers of chlamydospores in Victorian forest soils infected with Phytophthora cinnamomi. Australian Journal of Botany 26, 657–662. Weste, G. and Vithanage, K. (1979a). Survival of chlamydospores of Phytophthora cinnamomi in several non-sterile, host-free forest soils and gravels at different soil water potentials. Australian Journal of Botany 27, 1–9. Weste, G. and Vithanage, K. (1979b). Production of sporangia by Phytophthora cinnamomi in forest soils. Australian Journal of Botany 27, 693–701. Weste, G., Cook, D. and Taylor, P. (1973). The invasion of native forest by Phytophthora cinnamomi. II. Postinfection vegetation patterns, regeneration, decline in inoculum and attempted control. Australian Journal of Botany 21, 13–29. Weste, G., Ruppin, P. and Vithanage, K. (1976). Phytophthora cinnamomi in the Brisbane Ranges: Patterns of disease extension. Australian Journal of Botany 24, 201–208.

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Wingfield, M.J. and Knox-Davies, P.S. (1980). Observations on diseases in pine and Eucalyptus plantations in South Africa. Phytophylactica 12, 57–63. Woodward, J.R., Keane, P.J. and Stone, B.A. (1980). ßglucans and ß-glucan hydrolases in plant pathogenesis with special reference to wilt-inducing toxins from Phytophthora species. In Fungal Polysaccharides (Eds P.A. Sandford and K. Matsuda) pp. 113–141. Advances in Chemistry Series. (American Chemical Society: Washington, DC.) Zentmyer, G.A. (1961). Chemotaxis of zoospores for root exudates. Science 133, 1595–1596. Zentmyer, G.A. (1980). Phytophthora cinnamomi and the Diseases it Causes. Monograph 10. (The American Phytopathological Society: St Paul, MN, USA.) Zentmyer, G.A. (1988). Origin and distribution of four species of Phytophthora. Transactions of the British Mycological Society 91, 367–378. Zentmyer, G.A. and Erwin, D.C. (1970). Development and reproduction of Phytophthora. Phytopathology 60, 1120–1127. Zentmyer, G.A. and Mircetich, S.M. (1966). Saprophytism and persistence in soil by Phytophthora cinnamomi. Phytopathology 56, 710–712.

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Woody root rots of eucalypts can be locally or regionally important in both native forests and plantations. The woody roots of eucalypts can be infected by species from at least 12 genera of Basidiomycota. Species of Armillaria are the most important and may act as primary or secondary pathogens. Species of Pseudophaeolus and Ganoderma have been recorded as locally severe in Africa and India. The identity, pathogenicity, epidemiology and management options for woody root rots are reviewed. It is possible that these diseases could become more important in planted eucalypt forests.

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12.1 Introduction Specialised pathogens (sensu Garrett 1970) which kill the cambium and cause subsequent decay of woody roots have been recorded on a range of eucalypt species from temperate, mediterranean and tropical environments. Some are new host-pathogen associations that have developed as a consequence of the movement of eucalypts to new locations around the world; others, such as Armillaria (A.) luteobubalina Watling & Kile in native eucalypt forests in Australia, are undoubtedly host-pathogen interactions of long standing. The economic importance of the different woody root rot diseases varies and Koch's postulates have not been completed for some of the putative causal organisms discussed in this chapter. Armillaria species are the best known and most comprehensively studied of the woody root rot pathogens. The Basidiomycota capable of infecting and killing the woody roots of living eucalypts are able to infect roots from resting structures or from mycelial inoculum in infected wood; infection may be via either mycelium (sometimes ectotrophic) or rhizomorphs. The fungi may persist for long periods as saprophytes in colonised host tissue. They cause similar, generally non-specific, above-ground symptoms in the host, including crown dieback and reduced growth, and diseased trees tend to be clustered in patches or foci in forest stands as a consequence of the dependence of the pathogens on a woody inoculum source to overcome active host defences. Individual fungal species may cause either a brown or white rot of the root wood and some also have the ability to grow into the inner stem tissues causing butt rot (see Chapter 13). The host responses invoked by infection with these pathogens are similar to those caused by wounding and invasion of decay fungi in stems and branches (Shaw and Kile 1991; see Chapter 13) but the root rotting organisms are not dependent on wounds for entry to the host.

12.2 Armillaria root disease Armillaria root disease has been recorded in many regions around the world where eucalypts are grown and is the single most important woody root rot disease of eucalypts in terms of economic loss and the range of species affected. Armillaria species are primary pathogens in some native forests in Australia, as well as in plantations or amenity

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plantings in Australia and elsewhere. They are secondary pathogens in some eucalypt dieback and decline syndromes in particular native forests. Species of Armillaria recorded on eucalypts worldwide include Armillaria fumosa Kile & Watling, Armillaria hinnulea Kile & Watling, A. luteobubalina, Armillaria mellea (Vahl:Fr.) P.Kumm., Armillaria novae-zelandiae (G.Stev.) Herink, Armillaria tabescens (Scop.) Emel [syn. Clitocybe tabescens (Scop.) Bres.] and possibly Armillaria fellea (Hongo) Kile & Watling and Armillaria fuscipes Petch. Numerous host records of unidentified Eucalyptus species, or of records aggregated under A. mellea also exist. The generic characteristics of Armillaria are described by Watling et al. (1991). Symptoms of Armillaria infection in eucalypts include the development of white mycelial sheets or fans permeating through the inner bark or growing in the cambium of the roots, root collar or lower stem, development of an initially firm white rot of the sapwood, formation of pseudosclerotial tissue within or at the surface of decayed wood, formation of rhizomorphs attached to roots or on the cambium when bark has been loosened, development of basal cankers and kino formation and, at certain times of the year, the presence of clusters of brown or honeycoloured basidiocarps at the base of trees (Plates 12.1 to 12.4) (Podger et al. 1978; Kile 1981; Pearce et al. 1986; Shearer and Tippett 1988; Shaw and Kile 1991). Armillaria butt rot has been reported in young plantation eucalypts in Papua New Guinea (Arentz and Simpson 1989) and in 22-year-old to 34-year-old regrowth of E. regnans and E. delegatensis (Wardlaw 1996).

12.2.1 Primary Armillaria root disease in native eucalypt forests Four Armillaria species (A. fumosa, A. hinnulea, A. luteobubalina, A. novae-zelandiae) have been recorded from several eucalypt forest types in Australia (Kile and Watling 1981, 1988), and more than 35 eucalypt species have been identified as hosts (Table 12.1). However, only A. luteobubalina is a proven primary pathogen in native forests (Kile 1981). Armillaria pallidula Kile & Watling, another species described from Australia, has been found only in a pine plantation but most probably also occurs naturally in eucalypt forests (Kile and Watling 1988; B.N. Brown, pers. comm.).

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Eucalyptus and Corymbia species recorded as hosts of Armillaria species in forests, plantations and amenity plantings in Australia

After Edgar et al. (1976), Kile and Watling (1981, 1988), Kile et al. (1983), Pearce et al. (1986), Shearer and Tippett (1988), Shivas (1989), M. Pearce (pers. comm.), T. Wardlaw (pers. comm.), J.W. Tierney (pers. comm.).

Armillaria fumosa E. amygdalina, E. drepanophylla, E. obliqua, E. ovata, E. pilularis, E. propinqua, E. punctata, E. rubida, E. signata

Armillaria hinnulea E. delegatensis, E. obliqua, E. regnans

Armillaria luteobubalina C. calophylla, C. citriodora, C. ficifolia, C. gummifera, E. camaldulensis, E. cladocalyx, E. cypellocarpa, E. diversicolor, E. dives, E. erythrocorys, E. forrestiana, E. globulus ssp. bicostata , E. gomphocephala, E. leucoxylon, E. macrorhyncha, E. marginata, E. megacarpa, E. melliodora, E. nicholii, E. nitens, E. obliqua, E. ovata, E. patens, E. radiata, E. rubida, E. rudis, E. viminalis, E. wandoo

Armillaria novae-zelandiae E. delegatensis, E. obliqua, E. regnans

Armillaria luteobubalina affects many eucalypt and understorey species in dry sclerophyll mixedspecies forests in central Victoria, and in E. diversicolor (karri) and E. marginata (jarrah) forests and E. wandoo woodland in south-west Australia (Kile 1981; Kile et al. 1983; Pearce et al. 1986; Shearer and Tippett 1988; Shearer et al. 1997). The affected forests or woodlands occur mainly between 500 and 1200 metres altitude on soils of variable fertility, and receive average annual rainfall of 500 to 1200 millimetres. Most have a long history of logging. Hosts in these forests include over 80 eucalypt, understorey and ground cover species (Shaw and Kile 1991). The evidence for the primary pathogenicity of A. luteobubalina includes the constant association of the fungus with disease, a pattern of contagion consistent with that of an organism dependent on a woody food base, a correlation between infection and symptom development in large trees, and pathogenicity of the fungus in pot and field inoculations of some host tree species (Kile 1981; Pearce et al. 1986; Shearer and Tippett 1988). In Victorian forests, diseased trees tend to occur in roughly circular foci although the pattern of disease development is often obscured by multiple infections, harvesting and burning (Plate 12.5). Within patches, which may range from a few trees to one hectare or more, the disease usually spreads outward progressively, with the more recently dead and dying trees towards the margin and the long dead

and often wind thrown trees towards the centre. Eucalypts of all ages are attacked. The chronic nature of infection is indicated by the death of eucalypt or understorey regeneration established following death or removal of the previous, diseased overstorey. Typically A. luteobubalina or other Armillaria species are not found in healthy forest surrounding diseased areas. Similar disease development occurs in E. marginata forest and E. wandoo woodland (Shearer and Tippett 1988; Shearer et al. 1997). In E. diversicolor forest, the disease is most active in young stands; with increasing stand age, mortality is restricted mostly to suppressed or subdominant trees although larger trees may be infected and killed (Pearce et al. 1986). Young infected trees often die suddenly with the major proportion of their foliage still attached (Plate 12.6). In contrast, large, mature trees generally show progressive crown dieback before eventual death (Plate 12.7) (Kile 1981; Pearce et al. 1986; Shearer and Tippett 1988). In all eucalypts studied, Armillaria attack may result in the formation of basal cankers (Plate 12.3) which limit fungal infection and promote host survival (Kile 1981; Pearce et al. 1986; Shearer and Tippett 1988). These cankers may have an inverted ‘V’ shape and extend up to two to three metres above ground, although in Corymbia calophylla basal lesions were less clearly delineated and had greater marginal kino formation than in E. marginata (Shearer and Tippett 1988). Although the patterns of discolouration and decay resulting from A. luteobubalina infection

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reflect the process of compartmentalisation (Kile 1981; Shearer and Tippett 1988), there are differences in the relative susceptibility to invasion of inner bark and sapwood which may result in interspecific and intraspecific variation in host response to infection (Shearer and Tippett 1988). Eucalyptus wandoo does not show evidence of resistance and the species is invariably killed once the fungus reaches the root collar (Shearer and Tippett 1988; Shearer et al. 1997). In forest soils the fungus forms few rhizomorphs, although they may be formed readily on agar and in pot culture (Podger et al. 1978; Kile 1981; Pearce et al. 1986; Shearer and Tippett 1988). Underground spread between hosts occurs via root contact, with an average spread rate of one to three metres per annum (Kile 1983; Shearer et al. 1997). Limited development of rhizomorphs of A. luteobubalina occurred in E. diversicolor forest soils because soil temperature and water content were unsuitable for rhizomorph growth for most of the year (Pearce and Malajczuk 1990b). As a result of long-term belowground spread, individual genotypes of the fungus may infect trees in large contiguous areas (up to 2–3 ha or more), while some genotypes may infect trees in areas occurring hundreds of metres apart (Plate 12.9) (Kile 1983). Basidiocarps of A. luteobubalina develop mainly in autumn and early winter, depending on seasonal conditions (Kile and Watling 1981; Pearce et al. 1986; Shearer and Tippett 1988). In these relatively dry eucalypt communities, there appears to be limited opportunity for basidiospores to cause infection in the total forest area although such infections would be significant in establishing new disease foci. In central Victorian forests, where 36 genotypes of A. luteobubalina were identified in 24 hectares of forest, the average rate of infection resulting from basidiospores was estimated at less than one per annum (Kile 1983). In wet sclerophyll eucalypt forest in Tasmania, infection arising from basidiospores of A. hinnulea and A. novae-zelandiae may be much more frequent (Kile 1986). All eucalypt species exposed to A. luteobubalina appear susceptible to infection and mortality, although quantification of intraspecific and interspecific variation in host resistance under standard conditions is lacking. Shearer and Tippett (1988) noted anatomical differences between several

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eucalypt species in their reaction to infection in E. marginata forest. In Victorian forests there was no evidence of major differences in mortality of several eucalypt species caused by A. luteobubalina (Edgar et al. 1976; Kile 1981; Kellas et al. 1987), although E. obliqua showed greater mortality than E. globulus ssp. bicostata on the same sites (Kellas et al. 1987). Within a region there may be differences in the epidemiology of disease caused by A. luteobubalina on the same hosts. Crown decline and mortality following infection of E. marginata and C. calophylla was less severe in the higher rainfall zones of the western E. marginata forest than in the intermediate and low rainfall zones to the east (Shearer and Tippett 1988). The fungus also appeared less damaging in the wetter E. diversicolor forests in the same region (Pearce et al. 1986). Further studies of the influence of climatic and soil factors on the host and pathogen are required to explain such differences. Several thousand hectares of Australian eucalypt forest are seriously affected by A. luteobubalina (Edgar et al. 1976; Shearer and Tippett 1988; Shearer et al. 1997). Edgar et al. (1976) estimated that mature stands with moderate to severe disease had sawlog increments of two-thirds to one-half of that in an average healthy stand, respectively, with annual growth losses of 0.3 to 2.0 cubic metres per hectare depending on site and disease severity. Besides these losses, scattered and small patch mortality was evident in regrowth stands. In 30-year-old E. obliqua regrowth, with 51% to 75% of the total ground-level stem circumference infected by A. luteobubalina, average monthly girth increment was only 41% of that of healthy trees (Kile et al. 1982a). The wide distribution of A. luteobubalina in southern and eastern Australia and its intimate association with eucalypt forest communities indicate that it is an indigenous species. Although Kile (1983) reported evidence of its pathogenic activity in unlogged eucalypt forest, the most severe Armillaria root disease in dry sclerophyll eucalypt forest in Victoria occurred in forests subjected to repeated selection cutting of the larger trees at about 10-year intervals (Edgar et al. 1976). There is a strong relationship between incidence of infected stumps and disease incidence (Plate 12.8) (Edgar et al. 1976; Kile 1981; Pearce et al. 1986; Kellas et al. 1987).

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Subsequently, Kellas et al. (1987) showed that cutting intensity per se did not affect disease incidence, but that the frequency of cutting within infected forests is probably the critical factor promoting disease development. The regular creation of stumps by harvesting increased inoculum levels and the probability of residual trees being close to inoculum, and thus favoured infection by the pathogen. Unless A. luteobubalina infects stumps within three to four years of cutting, it is excluded from the stumps as a result of their colonisation by other microorganisms (Kile 1981). Practical control of A. luteobubalina is aimed at reducing inoculum levels within affected stands (see Chapter 19). In some central Victorian forests, an initial attempt at control has involved alteration of the silvicultural practice in diseased forest from selection logging to clearfelling with the aim of minimising inoculum buildup, reducing the chance of contact between healthy trees and inoculum sources, and maximising the chance of maintaining an adequately stocked stand through the rotation. A long-term trial of site preparation techniques, including stump and root removal, was established in central Victorian forests (Kile et al. 1982b). Analysis after 18 years of the mortality of the three species E. obliqua, E. globulus ssp. bicostata and Pinus radiata D.Don planted on the sites indicated that treatments involving extensive removal of stumps and roots were not effective in reducing mortality due to Armillaria on high disease hazard sites (Kellas et al. 1997). In Western Australia, investigations of biological control using fungi which can compete with or are antagonistic to A. luteobubalina have been undertaken (Pearce 1990; Pearce and Malajczuk 1990a, 1990c). A stump inoculation trial together with ammonium sulphamate treatment of stumps (Pearce et al. 1995) indicated that Phanerochaete filamentosa (Berk. & M.A.Curtis) Burds. was more effective than a Hypholoma species in reducing colonisation of stumps by A. luteobubalina and that both fungi were more effective than the non cord-forming fungi used by Pearce and Malajczuk (1990a). Fungi such as Trichoderma species, which are capable of killing or seriously weakening A. luteobubalina through hyperparasitism or antibiosis, may also assist biological control (Nelson et al. 1995). While these studies have demonstrated

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the potential value of selected fungi in reducing inoculum of A. luteobubalina in eucalypt forests, no operational biocontrol strategy has been developed.

12.2.2 Secondary Armillaria root disease in native eucalypt forests Biotic or abiotic stress of native eucalypt forests may transform indigenous Armillaria species of low primary pathogenicity into vigorous secondary pathogens (Shaw and Kile 1991). The best known example of this phenomenon is the dieback of regrowth E. obliqua/E. regnans in wet sclerophyll and mixed eucalypt–rainforest communities observed in several regions in Tasmania since the mid 1960s (Podger et al. 1980). The disease was first recognised in 30-year-old to 100-year-old second growth forests in south-east Tasmania in 1964 (Bowling and McLeod 1968). Symptoms in individual dominant and codominant trees include reduced growth rate, and branch dieback and death of residual foliage, with decline of individual trees occurring over several years (Plate 12.10). During the initial stages of disease, affected trees are scattered diffusely among apparently healthy trees (Podger et al. 1980). In the advanced stage of dieback many trees may be affected, although even then diseased trees remain randomly distributed (Ratkowsky et al. 1980). Armillaria novae-zelandiae and A. hinnulea are weakly pathogenic species that are widely distributed in the affected forests as a mosaic of genotypes and survive saprophytically in the roots and stumps of the previous stand for up to several decades (Kile 1981, 1986; Kile and Watling 1983, 1988). From this inoculum, these species form epiphytic rhizomorph associations with roots of living eucalypts and understorey species, and infect roots and cause local lesions of varying size (Plate 12.11). Kile (1980) found that 74% of 300 partially excavated eucalypt root systems in 15 stands had Armillaria associations or infections. Minor root infections have little effect on growth and survival of the host until the advent of stress, which in this case was believed to be caused by a succession of unusually dry summers (West 1979; Podger et al. 1980). New infections may then develop from epiphytic rhizomorph associations, or Armillaria may spread from pre-existing infections and colonise large portions of the root systems and root collar zones. Tree decline accelerates and many trees die

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that may have survived the stress in the absence of Armillaria (Kile 1981). Increased susceptibility to Armillaria is related to biochemical changes in the host tissues induced by stress, which lower host resistance and stimulate development of the fungus (Shaw and Kile 1991). More than 90% of the dead trees in affected forests were colonised by the two species of Armillaria. With the amelioration of drought stress, crown dieback and tree death decreased during the 1980s (Wardlaw 1989). Armillaria species have been associated with dieback development in other forests affected by stresses, including severe drought (Ashton et al. 1975; Palzer 1981), insect attack (Moore 1959, 1962) and possibly an epidemic of a leaf pathogen (Palzer 1978). With the exception of gully dieback (Palzer 1981), where the species was identified as A. luteobubalina, the species involved and their precise contributions to the disease syndromes have not been assessed.

12.2.3 Armillaria root disease in eucalypt plantations and amenity plantings Armillaria root disease has been reported in plantations and amenity plantings of eucalypts in several countries. Armillaria luteobubalina and its effects were initially described from a plantation of E. regnans in Victoria (Podger et al. 1978) and this species has subsequently been reported in plantings of E. diversicolor and E. saligna in Western Australia (Pearce et al. 1986; Shearer 1995) and E. delegatensis in Victoria (Plate 12.12) (Shaw and Kile 1991). This species is also an important pathogen of eucalypts and other species in parks and gardens in several Australian urban areas including Sydney, Melbourne, Adelaide and Perth (Smith and Kile 1981; Kile and Watling 1988). Outside Australia more than 30 eucalypt species have been recorded as hosts of Armillaria species (Table 12.2), with A. mellea (southern Europe, California) and A. tabescens (Tunisia, France, Florida) being the most important pathogens. (There is evidence that the European A. tabescens could be a separate species from the exannulate species found in south-east United States and previously referred to as A. (Clitocybe) tabescens (Shaw and Kile 1991). Losses in plantations have been reported from Portugal (Azevedo 1971;

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Sampaio 1975) and Tunisia (Delatour 1969a, 1969b), and in hedges, shelterbelts or amenity plantings in other regions. Whereas both A. mellea and A. tabescens occurred in natural vegetation in Tunisia, only the latter species was pathogenic on eucalypts (Delatour 1969a, 1969b). Quantification of host susceptibility is generally lacking, although Raabe (1969) in California reported, based on artificial inoculation studies, that E. camaldulensis and E. polyanthemos were highly resistant and moderately resistant, respectively, to A. mellea, while C. citriodora, E. gracilis, E. pulverulenta, E. rudis and E. sideroxylon (as E. sideroxylon var. rosea) were susceptible. Whether such ratings are valid for the native Australian species, A. luteobubalina, is unknown. In pot trials in New Zealand, plants of E. delegatensis, E. regnans, E. fastigata and E. saligna were infected by A. novae-zelandiae and Armillaria limonea (G.Stev.) Boesew. but only the first two species were killed (Benjamin and Newhook 1984). In contrast, on Pinus radiata in New Zealand A. novae-zelandiae and A. limonea can be aggressive primary pathogens (Shaw 1976; Shaw and Calderon 1977). Disease in plantations typically affects single trees or small patches of trees. Losses may be locally severe (Gibson 1967; Delatour 1969b; Podger et al. 1978) but worldwide losses to Armillaria root disease in commercial eucalypt plantations are very minor given the large areas of established plantations (see Chapter 1). This may be because in many countries plantations were established on already cleared land or when plantations were established on sites cleared of indigenous vegetation, the Armillaria species were only weakly pathogenic or restricted in distribution. Armillaria species are known, however, to establish disease foci in plantations of other tree species on former arable sites (Rishbeth 1988); hence future disease development may occur in some eucalypt plantations where the environment is suitable for the establishment of pathogenic Armillaria species. Whether all reports of disease in plantations represent primary pathogenicity cannot be determined but it is likely that physiological stress imposed by ‘off-site’ plantings, climatic events or other biotic agents may have increased the susceptibility of hosts in some cases.

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TAB LE 12 . 2

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Eucalyptus and Corymbia species recorded as hosts of Armillaria spp. causing root disease in countries other than Australia

Other records occur on unidentified eucalypt species.

Species

Location

Reference

C. citriodora

Tanzania

Wallace (1935)

C. citriodora

Tunisia

Delatour (1969a,1969b)

C. ficifolia

Florida

Rhoads (1956)

E. alba

Zimbabwe

Piearce (1990)

E. angulosa

Tunisia

Delatour (1969a)

E. camaldulensis

California

Raabe (1969)

E. camaldulensis

Cyprus

Soteriou (pers. comm.)

E. camaldulensis

Italy

Magnani (1964)

E. camaldulensis

Tunisia

Delatour (1969a,1969b)

E. cinerea

Tunisia

Delatour (1969a,1969b)

E. crebra

Zimbabwe

Piearce (1990)

E. dalrympleana

France

Lung-Escarmant & Taris (1989)

E. delegatensis

New Zealand

Gilmour (1966)

E. globulus

Portugal

Sampaio (1975)

E. globulus

California

Miller (1940)

E. globulus

Florida

Rhoads (1956)

E. globulus

Portugal

Azevedo (1971)

E. globulus

South Africa

Lundquist (1987)

E. globulus

Tanzania

Wallace (1935)

E. globulus

Tunisia

Delatour (1969a)

E. globulus ssp. bicostata

Papua New Guinea

Arentz & Simpson (1989)

E. globulus ssp. maidenii

Africa

Browne (1968)

E. globulus ssp. maidenii

Malawi

Zulu (pers. comm.)

E. gomphocephala

Cyprus

Browne (1968)

E. gomphocephala

Zimbabwe

Piearce (1990)

E. gracilis

California

Raabe (1969)

E. grandis

Papua New Guinea

Arentz & Simpson (1989)

E. leptophleba

Zimbabwe

Piearce (1990)

E. leucoxylon

Florida

Rhoads (1956)

E. nitens

Zimbabwe

Piearce (1990)

E. occidentalis

Tunisia

Delatour (1969a,1969b)

E. ochrophloia

Zimbabwe

Piearce (1990)

E. ovata

Tunisia

Delatour (1969a,1969b)

E. ovata

Zimbabwe

Piearce (1990)

E. paniculata

South Africa

Pole-Evans (1932)

E. paniculata

Tunisia

Delatour (1969a,1969b)

E. paniculata

Zimbabwe

Piearce (1990)

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E. pilularis

Zimbabwe

Masuka (1990)

E. polyanthemos

California

Raabe (1965)

E. polyanthemos

Florida

Rhoads (1956)

E. pulverulenta

California

Raabe (1965)

E. resinifera

Zimbabwe

Piearce (1990)

E. robusta (multiflora)

Florida

Rhoads (1956)

E. robusta (multiflora)

Papua New Guinea

Arentz & Simpson (1989)

E. rudis

Califomia

Raabe (1959)

E. rudis

Florida

Rhoads (1956)

E. saligna

Tanzania

Nshubemuki (pers. comm.)

E. saligna

Tunisia

Delatour (1969a,1969b)

E. sideroxylon

California

Raabe (1965)

E. sideroxylon

Florida

Rhoads (1956)

E. viminalis

Florida

Rhoads (1956)

E. viminalis

Tunisia

Delatour (1969a,1969b)

12.3 Pseudophaeolus root disease Pseudophaeolus baudonii (Pat.) Ryvarden [syn. Phaeolus manihotis Heim; Polyporus baudonii Pat., Laetiporus baudonii (Pat.) Ryvarden] is widely distributed in the warm climates of central and southern Africa and Madagascar where it is a notable pathogen of broadleaved trees, including Eucalyptus species, and a minor pathogen of pines (Gibson 1979; Ivory 1987). While some specimens and disease reports have been attributed to Ganoderma colossum (Fr.) C.F.Baker (Magnani 1964; van der Westhuizen 1973; Lundquist 1987), there are distinct differences between the two species (van der Westhuizen 1973). Basidiocarps of Pseudophaeolus baudonii are annual, 12 to 70 centimetres in diameter, typically forming after summer or autumn rains, and occurring singly or as several originating from a common base (Plate 12.13). The upper surface is initially orange, later becoming more brownish but with a thick, even undulating or partly lobed margin and an orange–yellow pore surface beneath. Basidiocarps emerge above the ground from buried roots or hypogeous pseudosclerotia or more rarely on stumps or at the base of trunks (van der Westhuizen 1973, 1975; Ofosu-Asiedu 1975). The fungus infects the woody roots up to the root collar and the roots become encased in a thick, yellow to creamy-white net of mycelium

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(Plate 12.14). It causes a brown rot of the wood. Infected eucalypts decline slowly, exhibiting chlorosis and abscission of the foliage, dieback of twigs and shoots and kino exudation from stems and root collars. In plantations, gradually expanding patches of dead and dying trees may form with mortality continuing for many years (Ofosu-Asiedu 1973, 1975). Disease foci are associated with cleared forest or woodland in which the fungus is endemic. Initial infection may be from mycelium growing from pseudosclerotia, with secondary spread via root contacts and grafts (Ofosu-Asiedu 1975). In the absence of a suitable host, the fungus may survive as pseudosclerotia in the soil. Although basidiospores are liberated in large numbers, their role in the epidemiology of the disease is unclear. No quantitative information on the rate of spread of the disease in eucalypt plantations is available although it has been described as quite rapid (Ofosu-Asiedu 1975). Disease effects may be locally severe and in a two-hectare, nine-year-old plantation of C. citriodora in Ghana nearly 50% of trees were killed (Ofosu-Asiedu 1975). Although some earlier unsuccessful experiments on disease control were undertaken in South Africa (Lundquist 1987), systematic attempts at control have not been reported for eucalypt plantations.

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The host range of Pseudophaeolus baudonii includes C. citriodora, C. maculata, C. torelliana, E. microcorys, E. paniculata, E. punctata and certain hybrids (Lückhoff 1955, 1964; Magnani 1965; Ofosu-Asiedu 1975; Lundquist 1987). Possible variation in interspecies and intraspecies susceptibility has not been assessed.

Ganoderma spp. are endemic in native forests and inoculum derives initially from residual stumps and roots in poorly cleared plantation sites. Patch mortality is associated with this primary inoculum but later spread may occur along planting rows through lateral root contact from infected to healthy hosts.

Field observation suggests that Pseudophaeolus baudonii may act as a vigorous primary pathogen of eucalypts although particular soil types or host stress may favour attack (Ofosu-Asiedu 1975). There is a need for pot and field inoculation studies to provide further information on pathogenicity, species susceptibility and epidemiology.

Hosts in India include C. citriodora, E. tereticornis (including Mysore hybrid), E. odorata (as E. fruticetorum) and E. staigerana (Bakshi et al. 1972; Bakshi 1976). Eucalyptus globulus has been recorded as a host in Argentina (Spaulding 1961), E. pilularis in Australia (Browne 1968) and E. grandis in Zimbabwe (Masuka and Nyoka 1995).

12.4 Ganoderma root rot Ganoderma lucidum (Curtis) P.Karst. has a wide geographical distribution and an extensive host range among broad-leaved species (Anon. 1975). Most records of the species as a pathogen of eucalypts derive from India where eucalypts are considered some of the most susceptible exotic hosts (Bakshi 1976; Rajan 1987). Although called ‘Ganoderma lucidum’, the correct identify of this pathogenic Ganoderma in India and elsewhere is apparently uncertain (Moncalvo et al. 1995). In Zimbabwe, Ganoderma root rot has been associated with Ganoderma sculpturatum (Lloyd) Ryvarden (Masuka and Nyoka 1995). Ganoderma spp. are spread by root contact and may infect through intact bark or wounds and cause a soft white rot of the root and butt sapwood (Bakshi 1976). Although a white mycelial mat develops between the bark and the wood, the fungus may grow ectotrophically as thin mycelial strands on the bark of roots or the surfaces of solid objects in contact with roots. Crown symptoms include foliage chlorosis, dieback and wilting. Infected trees are susceptible to wind throw, and stems may show cankering and kino exudation (Masuka and Nyoka 1995). Mortality may commence from an early age. Basidiocarps are sessile or laterally stipitate with a corky-woody texture, and may develop at the base of infected trees or from decayed roots. The pileus is subplane to very irregular, with a shiny, lacquered, blackish brown and irregularly lumped upper surface, and a white pore surface which becomes tawny with age (Anon. 1975).

12

Detailed assessment of disease effect in eucalypt plantations in India is lacking although Bakshi (1967) attributed losses of 10% to 15% in eucalypts to Ganoderma root rot, and Khara (1992) found 4% of trees (Eucalyptus hybrid) infected. In Zimbabwe, a disease incidence of 7.5% and 18% was reported in E. grandis plantations and seed orchards, respectively (Masuka 1990, 1992). Recommended control measures for Ganoderma root rot include prevention through complete removal of potential inoculum during stand establishment, isolation of disease foci by trenching, and planting of mixtures of resistant and susceptible species. There appears to be evidence of both interspecific and intraspecific variation in resistance to Ganoderma root rot in eucalypts. In Zimbabwe, 170 half sib families in 23 provenances of E. grandis were assessed for symptoms and death associated with Ganoderma sculpturatum infection in a 7.5year-old field trial where the fungus was present on residual host material from the previous vegetation (Masuka and Nyoka 1995). There were significant differences among provenances and families for deaths associated with Ganoderma sculpturatum and family heritability estimates were sometimes high, suggesting the opportunity to select or breed for more resistant genotypes if economically justified.

12.5 Other woody root diseases Several other organisms have been reported as causing root or root and butt rot in eucalypts in various regions of the world, although definitive studies of pathogenicity, symptom development and epidemiology are usually lacking and losses generally appear to be minor.

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P A T H O G E N S

O F

Rosellinia necatrix Prill., the cause of white root rot of a wide range of hosts (Sivanesan and Holliday 1972), has been reported as a pathogen of several eucalypt species in New Zealand (Pennycook 1989). Although originally identified by Birch (1937) as Rosellinia radiciperda Massee causing damage to trees in poorly drained areas, this species is probably non pathogenic (Gilmour 1966), and Dingley (1969) attributed the disease to Rosellinia necatrix. Azevedo (1971) recorded the species as a pathogen in plantations of E. globulus in Portugal, but subsequent reports from Portugal and Spain indicate it is probably only of local significance (Sampaio 1975; Ruperez and Munoz 1980). It was most common on coppice stumps and shoots. The invading mycelium proliferated in the cambial zone and over the bark, forming stromatic masses on which the fructifications of the anamorph and teleomorph developed. Infection extended into the base of new shoots and caused their separation from stumps. Infected wood became darkened and moist and later showed white rot symptoms. The lack of records from other eucalypt-growing areas of the world suggests that overall this species is of minor importance on eucalypts. Dextrinocystidium sacratum (G.Cunn.) Sheng H.Wu [syn. Amylostereum sacratum (G.Cunn.) Burds., Peniophora sacrata G.Cunn., Gloeocystidiellum sacratum (G.Cunn.) Stalpers & P.K.Buchanan] has been recorded as a root and stem pathogen in young plantings of E. botryoides, E. ovata and E. saligna in New Zealand (Gilmour 1966; Dick 1983; Pennycook 1989). It causes patch mortality resulting from root infections or girdling of the root collar or butt by cankers associated with a spongy white rot. Cankers develop from mycelial growth arising from inoculum left from the clearing of native vegetation. Control is not considered necessary (Dick 1983). Junghuhnia vincta (Berk.) Hood & M.Dick [syn. Poria vincta (Berk.) Cooke, Rigidoporus vinctus (Berk.) Ryvarden] has caused localised root disease (white crown canker) in shelter belts and farm plantings in New Zealand (Taylor and Sale 1980; Taylor 1984). The causal agent was initially identified as Rigidoporus lineatus (Pers.) Ryvarden (Taylor and Sale 1980) but Junghuhnia vincta has been accepted as the correct identification (Taylor 1984; Hood and Dick 1988). Species field susceptible to Junghuhnia vincta include E. botryoides, E. fraxinoides, E. johnstonii and E. saligna

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(Taylor 1984). In pathogenicity tests, E. regnans was infected but not E. delegatensis, E. nitens and E. saligna (Hood and Dick 1988). Eucalyptus pulchella was reported to be field-resistant (Taylor and Sale 1980). Although normally confined to conifers, Phaeolus schweinitzii (Fr.) Pat. (syn. Polyporus schweinitzii Fr.) was reported as causing a red-brown cubical root and butt rot of E. globulus in California (Spaulding 1958). Spaulding (1961) and Browne (1968) also noted this species from E. obliqua in Australia, a record probably originating from Cleland (1934–35). This and subsequent records of Phaeolus schweinitzii from Australia, including one on E. fastigata in New South Wales (J.A. Simpson, pers. comm.), were transferred to Phaeolus albertinii (Lloyd) D.A.Reid (Reid 1963) and later to its synonym Inonotus albertinii (Lloyd) P.K.Buchanan & Ryvarden. It is thus uncertain whether Phaeolus schweinitzii occurs in Australia. Further investigation of Inonotus albertinii is required to determine if it causes root rot of living hosts. Abortiporus biennis (Bull.:Fr.) Singer [syn. Heteroporus biennis (Bull.:Fr.) Lázaro Ibiza] and Rigidoporus lineatus were isolated from roots and butts of E. robusta growing in waterlogged soils in the highlands of Papua New Guinea (Arentz and Simpson 1989). The pathogenicity of these species is uncertain. Corymbia citriodora, C. tessellaris, E. deglupta and E. drepanophylla have been recorded as hosts of Phellinus noxius (Corner) G.Cunn. (Davidson 1974; Bolland 1984). The fungus typically produces encrusting mycelium on the roots or lower stem and a white pocket rot of woody tissues. Losses in eucalypts appear minor but the fungus may kill individual trees (L. Bolland, pers. comm.) and cause heart rot (see Chapter 13). Purple root rot caused by Helicobasidium compactum Boedijn has been recorded on Eucalyptus spp. in Nigeria (Browne 1968) and possibly South Africa (Lückhoff 1964; Gibson 1967) but losses were apparently minor.

12.6 Conclusion Woody roots of eucalypts may be infected by species from at least 12 genera of Basidiomycota. Armillaria root disease is an important problem in natural

W OODY R OOT R OTS

eucalypt forests and woodland in Australia but most of the woody root rots reported in eucalypt plantations appear at present to be of local or minor importance. The exact identity of some of the species reported as associated with or causing woody root rots requires further attention and the nature of the association requires further study in several cases. With the exception of some Armillaria species, there is little knowledge of the silvicultural, site or environmental factors influencing disease development. Woody root rots could become more important as a cause of disease in eucalypt plantations. The intensive short-rotation management regimes typically used for eucalypts, the increasing number of eucalypt species being planted, the range of environments in which they are grown, and the potential for some pathogens to develop new disease foci through airborne infection of stumps could promote greater disease development.

12.7 References Anon. (1975). Ganoderma lucidum. CMI Descriptions of Pathogenic Fungi and Bacteria No. 445. (Commonwealth Mycological Institute: Kew.) Arentz, F. and Simpson, J.A. (1989). Root rot diseases of exotic plantation tree species in Papua New Guinea. In Proceedings of the 7th IUFRO International Conference on Root and Butt Rots, Vernon and Victoria, British Columbia, 1988. (Ed. D.J. Morrison) pp. 83–91. (Forestry Canada: Victoria, British Colombia.) Ashton, D.H., Bond, H. and Morris, G.C. (1975). Drought damage on Mount Towrong, Victoria. Proceedings of the Linnaean Society of New South Wales 100, 44–69. Azevedo, N.F.S. (1971). Diseases of Eucalyptus. In Forest Tree Diseases. pp. 10–33. (Laboratorio de Patologia Florestal: Oeiras, Portugal.) Bakshi, B.K. (1967). Quantification of forest disease losses. In Report for Asia for 14th IUFRO Congress, Vol. 5, Munich, 1967, pp. 361–372. Bakshi, B.K. (1976). Forest Pathology: Principles and Practice in Forestry. (Forest Research Institute Press: Dehra Dun, India.) Bakshi, B.K., Ram Reddy, M.A., Puri, Y.N. and Singh, S. (1972). Forest Disease Survey. Survey of the diseases of important native and exotic forest trees in India. Final Technical Report 1967–1972. (Controller of Publications: Delhi.) Benjamin, M. and Newhook, F. (1984). The relative susceptibility of various Eucalyptus spp. and Pinus radiata to Armillaria grown on different food bases.

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In Proceedings of the 6th IUFRO International Conference on Root and Butt Rots of Forest Trees (IUFRO Working Party S2.06.01). (Ed. G.A. Kile) pp. 140–147. (CSIRO: Melbourne.) Birch, T.T.C. (1937). A synopsis of forest fungi of significance in New Zealand. New Zealand Journal of Forestry 4, 109–125. Bolland, L. (1984). Phellinus noxius: cause of a significant root–rot in Queensland hoop pine plantations. Australian Forestry 47, 2–10. Bowling, P.J. and McLeod, D.E. (1968). A note on the presence of Armillaria in second growth eucalypt stands in southern Tasmania. Australian Forest Research 3, 38–40. Browne, F.G. (1968). Pests and Diseases of Forest Plantation Trees. An Annotated List of the Principal Species Occurring in the British Commonwealth. (Clarendon Press: Oxford.) Cleland, J.B. (1934–35). Toadstools and Mushrooms and Other Larger Fungi of South Australia. Parts I and II. Handbooks of the Flora and Fauna of South Australia. (Government Printer: Adelaide.) Davidson, J. (1974). Decayed wood in living trees of Eucalyptus deglupta Blume. Tropical Forestry Research Note SR. 18, Papua New Guinea (Department of Forests: Boroko, Papua New Guinea.) Delatour, C. (1969a). Quelques observations de phytopathologie forestiere faites en tunisie. Variété Scientifique No. 2. Institut Reboisement de Tunis Tunis 2. Delatour, C. (1969b). Quelques observations sur le pourridié des Eucalyptus dans le nord de la Tunisie. Annales de L'Institut National de Recherches Forestieres de Tunisie 2 Institut Reboisement de Tunis Tunis. Dick, M. (1983). Peniophora root and stem canker. Forest Pathology in New Zealand No. 3. (Forest Research Institute: Rotorua, New Zealand.) Dingley, J.M. (1969). Records of Plant Diseases in New Zealand. New Zealand Department of Scientific and Industrial Research. Bulletin 192, pp. 1–298. (Wellington, New Zealand.) Edgar, J.G., Kile, G.A. and Almond, C.A. (1976). Tree decline and mortality in selectively logged eucalypt forests in central Victoria. Australian Forestry 39, 288–303. Garrett, S.D. (1970). Pathogenic Root-infecting Fungi. (Cambridge University Press: London.) Gibson, I.A.S. (1967). The influence of disease factors on forest production in Africa. In Report for Asia for 14th IUFRO Congress, Vol. 5, Munich, 1967, pp. 327–360. (IUFRO: Rome.) Gibson, I.A.S. (1979). Diseases of Forest Trees Widely Planted as Exotics in the Tropics and Southern Hemisphere. II. The Genus Pinus. pp. 30–33. (Commonwealth Mycological Institute/ Commonwealth Forestry Institute: Kew/Oxford.)

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Gilmour, J.W. (1966). The pathology of forest trees in New Zealand. The fungal, bacterial, and algal pathogens. Technical Paper No. 48. (Forest Research Institute, New Zealand Forest Service: Wellington.) Hood, I.A. and Dick, M. (1988). Junghuhnia vincta (Berkeley) comb. nov., root pathogen of Pinus radiata. New Zealand Journal of Botany 26, 113–116. Ivory, M.H. (1987). Diseases and Disorders of Pines in the Tropics. A Field and Laboratory Manual. Overseas Research Publication Series No. 31. (Overseas Development Administration, Oxford Forestry Institute: Oxford, England.) Kellas, J.D., Kile, G.A., Jarrett, R.G. and Morgan, B.J.T. (1987). The occurrence and effects of Armillaria luteobubalina following partial cutting in mixed eucalypt stands in the Wombat Forest, Victoria. Australian Forest Research 17, 263–276. Kellas, J.D., Kile, G.A., Oswin, D.A. and Ashton, A.K. (1997). Growth and mortality, 1978 to 1996, in an Armillaria root rot control experiment in the Mount Cole State Forest, Victoria. Research Report. (Department of Natural Resources and Environment/ Centre for Forest Tree Technology: Melbourne.) Khara, H.S. (1992). Incidence of Ganoderma lucidum root rot on some tree species around Ludhiana. Plant Disease Research 8, 136–137. Kile, G.A. (1980). Behaviour of an Armillaria in some Eucalyptus obliqua – Eucalyptus regnans forests in Tasmania and its role in their decline. European Journal of Forest Pathology 10, 278–296. Kile, G.A. (1981). Armillaria luteobubalina: a primary cause of decline and death of trees in mixed species eucalypt forests in central Victoria. Australian Forest Research 11, 63–77. Kile, G.A. (1983). Identification of genotypes and the clonal development of Armillaria luteobubalina Watling & Kile in eucalypt forests. Australian Journal of Botany 31, 657–671. Kile, G.A. (1986). Genotypes of Armillaria hinnulea in wet sclerophyll eucalypt forest in Tasmania. Transactions of the British Mycological Society 87, 312–314. Kile, G.A. and Watling, R. (1981). An expanded concept of Armillaria luteobubalina. Transactions of the British Mycological Society 77, 75–83. Kile, G.A. and Watling, R. (1983). Armillaria species from south-eastern Australia. Transactions of the British Mycological Society 81, 129–140. Kile, G.A. and Watling, R. (1988). Identification and occurrence of Australian Armillaria species, including A. pallidula sp. nov. and comparative studies between them and non-Australian tropical and Indian Armillaria. Transactions of the British Mycological Society 91, 305–315. Kile, G.A. Kellas, J.D. and Jarrett, R.G. (1982a). Electrical resistance in relation to crown dieback symptoms, Armillaria infection and growth in Eucalyptus obliqua

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and E. globulus subsp. bicostata. Australian Forest Research 12, 139–149. Kile, G.A., Squire R.O. and Edgar J.G. (1982b). An Armillaria root rot control experiment in the Mount Cole State Forest, Victoria. 1. Establishment and Progress Report. Research Branch Report No. 197. (Forests Commission Victoria: Melbourne.) Kile, G.A., Watling, R., Malajczuk, N. and Shearer, B.L. (1983). Occurrence of Armillaria luteobubalina Watling and Kile in Western Australia. Australasian Plant Pathology 12, 18–20. Lückhoff, H.A. (1955). Two hitherto unrecorded fungal diseases attacking pines and eucalypts in South Africa. Journal of the South African Forestry Association 26, 47–61. Lückhoff, H.A. (1964). Diseases of exotic plantation trees in the Republic of South Africa. In Diseases of Widely Planted Forest Trees, Proceedings of the FAO/IUFRO Symposium on Internationally Dangerous Forest Diseases and Insects, Oxford, July 1964. (USDA Forest Service: Washington, DC.) Lundquist, J.E. (1987). A history of five forest diseases in South Africa. South African Forestry Journal 140, 51–59. Lung-Escarmant, B. and Taris, B. (1989). Methodological approach to assess host response (resinous and hardwood species) to Armillaria obscura infection in the south-west French pine forest. In Proceedings of the 7th IUFRO International Conference on Root and Butt Rots, Vernon and Victoria, British Columbia, 1988. (Ed. D.J. Morrison) pp. 226–236. (Forestry Canada: Victoria, British Colombia.) Magnani, G. (1964). Diseases of Eucalyptus. In Diseases of Widely Planted Forest Trees, Proceedings of the FAO/ IUFRO Symposium on Internationally Dangerous Forest Diseases and Insects, Oxford, July 1964. pp. 159–167. (USDA Forest Service: Washington, DC.) Masuka, A. (1990). A new canker of Eucalyptus grandis Hill ex Maid. in Zimbabwe. Commonwealth Forestry Review 69, 195–200. Masuka, A. (1992). Diseases and disorders of eucalypts with emphasis on the canker of Eucalyptus grandis. In Forestry Research Advances in Zimbabwe, Proceedings of the Anniversary Seminar, Mutare, 1990. (Eds G.D. Piearce and P. Shaw) pp. 243–248. (The Forestry Commission: Harare, Zimbabwe.) Masuka, A.J. and Nyoka, B. I. (1995). Susceptibility of Eucalyptus grandis provenances to a root rot associated with Ganoderma sculpturatum in Zimbabwe. European Journal of Forest Pathology 25, 65–72. Miller, P.A. (1940). Notes on diseases of ornamental plants in southern California. Plant Disease Reporter 24, 219–222. Moncalvo, J.-M., Wang, H.-F. and Hseu, R.-S. (1995). Gene phylogeny of the Ganoderma lucidum complex based on ribosomal DNA sequences. Comparison

W OODY R OOT R OTS

with traditional taxonomic characters. Mycological Research 99, 1489–1499. Moore, K.M. (1959). Observations on some Australian forest insects. 4. Xyleborus truncatus Erichson 1842 (Coleoptera : Scolytidae) associated with dying Eucalyptus saligna Smith (Sydney Blue Gum). Proceedings of the Linnaean Society of New South Wales 84, 186–193. Moore, K.M. (1962). Entomological research on the cause of mortalities of Eucalyptus saligna Smith (Sydney Blue Gum). New South Wales Forest Commission Research Note No. 11, Sydney. Nelson, E.E., Pearce, M.H. and Malajczuk, N. (1995). Effects of Trichoderma spp. and ammonium sulphamate on establishment of Armillaria luteobubalina on stumps of Eucalypts diversicolor. Mycological Research 99, 957–962. Ofosu-Asiedu, A. (1973). Root rot of Eucalyptus citriodora Hook. In Abstracts of Papers. Second International Congress of Plant Pathology, Minneapolis, 1973. (American Phytopathological Society: St Paul, MN, USA.) Ofosu-Asiedu, A. (1975). A new disease of eucalypts in Ghana. Transactions of the British Mycological Society 65, 285–289. Palzer, C. (1978). Defoliation and death in Eucalyptus obliqua forests. Australian Forestry Research Newsletter 5, 71. Palzer, C. (1981). Aetiology of gully dieback. In Eucalypt Dieback in Forests and Woodlands (Eds K.M. Old, G.A. Kile and C.P. Ohmart) pp. 174–178. (CSIRO: Melbourne.) Pearce, M.H. (1990). In vitro interactions between Armillaria luteobubalina and other wood decay fungi. Mycological Research 94, 753–761. Pearce, M.H. and Malajczuk, N. (1990a). Inoculation of Eucalyptus diversicolor thinning stumps with wood decay fungi for control of Armillaria luteobubalina. Mycological Research 94, 32–37. Pearce, M.H. and Malajczuk, N. (1990b). Factors affecting growth of Armillaria luteobubalina rhizomorphs in soil. Mycological Research 94, 38–48. Pearce, M.H. and Malajczuk, N. (1990c). Stump colonization by Armillaria luteobubalina and other wood decay fungi in an age series of cut-over stumps in karri (Eucalyptus diversicolor) regrowth forests in south-western Australia. New Phytologist 115, 129–138. Pearce, M.H., Malajczuk, N. and Kile, G.A. (1986). The occurrence and effects of Armillaria luteobubalina in the karri (Eucalyptus diversicolor F. Muell.) forests of Western Australia. Australian Forest Research 16, 243–259. Pearce, M.H., Nelson, E.E. and Malajczuk, N. (1995). Effects of the cord-forming saprotrophs Hypholoma australe and Phanerochaete filamentosa and of ammonium sulphamate on establishment of Armillaria

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luteobubalina on stumps of Eucalyptus diversicolor. Mycological Research 99, 951–956. Pennycook, S.R. (1989). Plant Diseases Recorded in New Zealand; Vol. 1. Plant Diseases Division, DSIR, Auckland, New Zealand, pp. 85–88. Piearce, G.D. (1990). Armillaria root-rot. Presented at a Deciduous Fruit Workshop, Chimanimani, Zimbabwe, 30 July–1 August 1990. (Typescript, 10 pp.) Podger, F.D., Kile, G.A., Watling, R. and Fryer, J.M. (1978). Spread and effects of Armillaria luteobubalina Watling and Kile sp. nov. in an Australian Eucalyptus regnans plantation. Transactions of the British Mycological Society 71, 77–87. Podger, F.D., Kile, G.A., Bird, T., Turnbull C.R.A. and McLeod, D.E. (1980). An unexplained decline in some forests of Eucalyptus obliqua and E. regnans in southern Tasmania. Australian Forest Research 10, 53–70. Pole-Evans, I.B. (1932). Arable farming and pasture problems. Farming in South Africa 7, 341–352. Raabe, R.D. (1959). Additional unrecorded hosts of Armillaria mellea. Plant Disease Reporter 43, 1270. Raabe, R.D. (1965). Some previously unreported hosts of Armillaria mellea in California. Plant Disease Reporter 49, 81. Raabe, R.D. (1969). Plants Resistant or Susceptible to Armillaria Root Rot. (Cooperative Extension Service, University of California: Berkeley, CA, USA.) Rajan, B.K.S. (1987). Fungal diseases. In Versatile Eucalyptus. pp. 160–163. (Diana Publications: Bangalore, India.) Ratkowsky, D.A., Myers B.J. and Bird, T. (1980). Analysis of pattern of crown damage in forests. Forest Ecology and Management 3, 245–253. Reid, D.A. (1963). New or interesting records of Australasian Basidiomycetes: V. Aphyllophorales (Coniophoraceae). Kew Bulletin 17, 267–308. Rhoads, A.S. (1956). The occurrence and destructiveness of Clitocybe root rot of woody plants in Florida. Lloydia 19, 193–240. Rishbeth, J. (1988). Stump infection by Armillaria in firstrotation conifers. European Journal of Forest Pathology 18, 401–408. Ruperez, A. and Muñoz, C. (1980). Enfermedades de los eucaliptos en España. Boletin del Servicio de Plagas Forestales 6, 193–217. Sampaio, M.H. (1975). Doenças do Eucalipto em Portugal. Boletin do Instituto Productos Florestais (Madeiras) 7, 11–20. Shaw, C.G. (1976). Armillaria root rot. New Zealand Forest Research Institute. What's New in Forest Research 36, 1–4. Shaw, C.G. and Calderon, S. (1977). Impact of Armillaria root rot in plantations of Pinus radiata established on sites converted from indigenous forest. New Zealand Journal of Forest Science 7, 359–373.

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Shaw, C.G. III and Kile, G.A. (1991). Armillaria Root Disease. Agriculture Handbook No. 691. (USDA Forest Service: Washington, DC.) Shearer, B.L. (1995). Impact and symptoms of Armillaria luteobubalina in rehabilitation plantings of Eucalyptus saligna in forests of Eucalypts marginata in south-western Australia. Australasian Plant Pathology 24, 77–81. Shearer, B.L. and Tippett, J.T. (1988). Distribution and impact of Armillaria luteobubalina in the Eucalyptus marginata forest of south-western Australia. Australian Journal of Botany 36, 433–445. Shearer, B.L., Byrne, A., Dillon. M. and Buehrig. R. (1997). Distribution of Armillaria luteobubalina and its impact on community diversity and structure in Eucalyptus wandoo woodland of southern Western Australia. Australian Journal of Botany 45, 151–165. Shivas, R.G. (1989). Fungal and bacterial diseases of plants in Western Australia. Journal of the Royal Society of Western Australia 72, 1–62. Sivanesan, A. and Holliday, P. (1972). Rosellinia necatrix. CMI Descriptions of Pathogenic Fungi and Bacteria No. 352. (Commonwealth Mycological Institute: Kew.) Smith, L. and Kile, G.A. (1981). Distribution and hosts of Armillaria root rot in Melbourne suburban gardens. Australasian Plant Pathology 10, 41–42. Spaulding, P. (1958). Diseases of Foreign Forest Trees Growing in the United States. Agriculture Handbook No. 139. (US Department of Agriculture: Washington, DC.) Spaulding, P. (1961). Foreign Diseases of Forest Trees of the World. Agriculture Handbook No. 197. (US Department of Agriculture: Washington, DC.)

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Taylor, J.B. (1984). White crown canker in shelter belts: significance and control. Horticultural Produce and Practice 131. (NZ Ministry of Agriculture and Fisheries: Wellington, New Zealand.) Taylor, J.B. and Sale, P.R. (1980). White crown canker in shelter belts: significance and control. Horticultural Produce and Practice 131. (NZ Ministry of Agriculture and Fisheries: Wellington, New Zealand.) van der Westhuizen, G.C.A. (1973). Polyporus baudonii Pat. on Eucalyptus spp. in South Africa. Bothalia 11, 143–151. van der Westhuizen, G.C.A. (1975). Polyporus baudonii. CMI Descriptions of Pathogenic Fungi and Bacteria No. 442. (Commonwealth Mycological Institute: Kew.) Wallace, G.B. (1935). Armillaria root rot in East Africa. East African Agricultural Journal 6, 182–192. Wardlaw, T.J. (1989). Management of Tasmanian forests affected by regrowth dieback. New Zealand Journal of Forest Science 19, 265–276. Wardlaw, T.J. (1996). The origin and extent of discolouration and decay in stems of young regrowth eucalypts in southern Tasmania. Canadian Journal of Forest Research 26, 1–8. Watling, R., Kile, G.A. and Bursdall, H.H. Jr. (1991). Nomenclature, taxonomy, and identification. In Armillaria Root Disease. Agricultural Handbook No. 691. (Eds C.G. Shaw III and G.A. Kile) pp. 1–9. (USDA Forest Service: Washington, DC.) West, P.W. (1979). Date of onset of regrowth dieback and its relation to summer drought in eucalypt forests in southern Tasmania. Annals of Applied Biology 93, 337–350.

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G.A. Kile and G.C. Johnson

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Stem and root decay in standing trees reduces life span of the trees and the commercial value of the timber, and makes trees hazardous to human life and property—it also creates nesting hollows for animals. Information on decay in eucalypts is limited and often not well documented. In this chapter, the decay process is reviewed beginning with the infection of exposed sapwood and heartwood and continuing through tissue responses and patterns of decay. Factors affecting decay development in individual trees and in stands are also discussed. The fungi associated with heartwood rot of over 80 species of eucalypts are tabulated according to their occurrence in Australia and elsewhere and in butts, major roots, upper trunks and branches. These data are based on both published and unpublished information. Over 75% of the eucalypt heart rot species are associated with white rot or white pocket rot. Species of Phellinus and Inonotus are most commonly implicated in Australia, and Phellinus and Stereum elsewhere. An improved understanding of the decay process, the organisms involved and the environmental, genetic and silvicultural factors affecting decay development will be important for the production of high quality wood in intensively managed eucalypt forests.

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13.1 Introduction Decay of above-ground and below-ground woody tissues of eucalypts may reduce the tree's growth rate, diminish the amount and quality of products that can be obtained from discoloured or incipiently decayed wood, and shorten the life span of the tree by either direct pathogenesis or mechanical failure. Decay may also render a tree hazardous to people and property. However, decay in the native forests and woodlands is important in providing nesting hollows for birds, reptiles and mammals. Losses from decay have rarely been estimated in Australia (Greaves et al. 1965), even for the most commercially valuable forests. Although Australian forest management agencies estimate total losses from various causes (fire, termites, decay, poor tree form) when assessing timber yields, these estimates are based on previous experience of timber recoveries rather than forest survey information relating to the various types of losses. However, if judged from assessments in other forests, the losses are likely to be of considerable economic significance (Hepting 1971; Singh 1989). For example, in the United States of America (USA) heart rot had the greatest effect on recovery of sawtimber (Hepting and Jemison 1958). Stem and butt rots occurring in natural eucalypt forests were regarded as diseases of mature and overmature trees (Heather and Griffin 1978). In these forests, decay in young trees, having naturally durable heartwood, was confined to a small core of wood surrounding the pith. As harvesting is now being directed away from old-growth forests and is increasingly being carried out in regrowth forests and plantations managed under shorter rotations, it has been assumed that stem rots would become less important (Heather 1962; Manion and Zabel 1979; Wilkes 1982). However, Da Costa (1973) and Heather and Griffin (1978) observed that young trees, even of species reputed to have durable heartwood, can suffer extensive heart rot when grown rapidly in plantations. This heart rot was attributed to such factors as the reduced content of natural antifungal components of the inner heartwood of rapidly grown trees and the impaired shedding of branches (associated with rapid growth) which can provide a direct infection route to this less durable heartwood. In some respects the heart of a tree might be considered a protected environment for a pathogen. Temperature and moisture fluctuations within the 308

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host, and contact with other microorganisms, are less than in twigs or slash. That only a small proportion of the species of Basidiomycota are able to cause heart rots (Wagener and Davidson 1954) indicates limiting conditions inside the host. Unlike other wood decay fungi, heart rotting fungi are able to ‘penetrate into, survive in and cause decay in the living tree's interior’ (Highley and Kirk 1979). Whether a species can cause heart rot in a particular tree species will be determined by the effect of the chemical and microbial environment inside the host. Although Highley et al. (1983) were unable to demonstrate what features make heart rot fungi unique, they concluded that concentration and type of volatiles (e.g. oxygen, carbon dioxide, acetic acid) and extractives, as well as microbial interactions, temperature, moisture content and pH, would be powerful selective forces for determining what fungi grow in the heartwood. Scheffer (1986) demonstrated that a higher proportion of heart rot fungi were tolerant of low oxygen concentrations than were product-rotting fungi that attack better aerated wood. According to Rayner and Boddy (1988), the characteristics of heart rot fungi are slow growth rate, lack of competitive ability and strong selectivity for particular tree taxa. Most ‘true heart rotting fungi’ are unable to decay sound wood in vitro unless the wood has been colonised previously by non-hymenomycetes or partially decayed by another hymenomycete (Merrill 1970). The important stem decays have been classified as ‘stem heart rots’ (of the top and butt). Whereas ‘top rots’ are initiated in the branches or upper trunk and progress downwards, ‘butt rots’ establish in the roots or at the base of the stem and spread upwards. We have used ‘heart rot’ to refer to heartwood decomposition of living eucalypts. In this chapter information on the organisms involved and the damage they cause is brought together and reviewed. For convenience, the taxonomic authorities for the decay fungi discussed in the chapter are listed in the accompanying tables.

13.2 Causal organisms and hosts Few attempts have been made to collate data on fungi associated with heartwood and sapwood rot of eucalypts. Although some limited information was assembled by Spaulding (1961) in an annotated list and by Browne (1968), Gibson (1975) provided considerably more information in his table of ‘principal heart rot fungi recorded on Eucalyptus

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spp.’. We believe that the latter reference unfortunately refers to some fungi not associated with heart rot of live eucalypts. In her paper on forest tree diseases, Azevedo (1971) listed 52 species as causing ‘stump and heart rots’, although she believes that only three of these species are associated with heart rot of living eucalypts (N.F.S. Azevedo, pers. comm.). Many more than these three species appear in Gibson's (1975) table. Such differences in interpretation have resulted in our list of eucalypt stem rotting fungi (Tables 13.1 to 13.3) being quite different from that of Gibson (1975). Over 80 species of eucalypts (Eucalyptus, Corymbia) are recorded in Tables 13.1 to 13.3 as hosts of one or more heart rot fungi. These species represent a very small proportion of the approximately 500 species of eucalypts (Bamber 1985). The lack of a record should not be interpreted as indicating that the species is immune to attack by heart rot fungi. It is much more likely due to our ignorance. Our expectation is that ‘the heartwood of practically every tree species is subject to decay in the living tree by one or more heart-rot fungi adapted to grow there’ (Wagener and Davidson 1954).

13.2.1 Source of tabulated information Tables 13.1 to 13.3 were assembled from the literature and from personal communications. Significant sources of information were Tamblyn (1937) and Marks et al. (1982). Information was also obtained from floristic studies (Cleland 1934–35; Spaulding 1961; Azevedo 1971) and taxonomic works (Cunningham 1965). Not surprisingly, the detail relevant to our interest in heart rots was often lacking, and so we have adopted a very conservative approach to the inclusion of data in the tables. An entry was made in the tables if: 1

the host was a living eucalypt

2

at least the genus of the fungus was given

3

the heartwood of the host was decayed.

If it was impossible to be certain whether the host was alive, whether the heartwood was attacked or whether the host was old enough to have formed heartwood (heartwood formation in most eucalypts probably begins at about year 4 or 5 as measured from the cambium; Bamber 1985), then an entry was made but the host was bracketed in the table. For example, when Cunningham (1965) reports that

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basidiomes of a certain fungus occurred on dead or dying eucalypt trunks and lists four eucalypt species, as we cannot be sure if the eucalypt species were alive when colonised, the four host species are bracketed in our tables. A substantial body of Australian data on fungi causing heart rot of eucalypts has never been published. This information has been made available to us through the generosity of the mycologists and pathologists acknowledged later. The tables contain few references to heart rot fungi from the Northern Territory, the Australian Capital Territory or Tasmania where, until recently, little work on eucalypt stem and butt rots has been carried out.

13.2.2 Fungi associated with heart rots We have been unable to determine many cases where fungi suspected of causing heart rots of living eucalypts have been confirmed as the cause by completion of Koch’s postulates. In 1936, Tamblyn tested a version of Koch’s postulates in which he isolated and compared the heart rot fungus from the basidiome and from decayed wood (Tamblyn 1936). If the isolates were similar, he used the basidiome culture to cause in vitro decay and the decay was compared with that from the tree. This procedure was carried out with several fungi associated with heart rot. According to Koch’s postulates, the isolates should have been used to inoculate living trees that had no heart rot. Davison and Tay (1990), following a conventional approach to Koch’s postulates, recovered fungi associated with brown discolouration and incipient decay in the transition wood and heartwood of living, regrowth Eucalyptus diversicolor. They grew each fungus in pure culture and inoculated unaffected trees to establish whether that fungus could cause heartwood discolouration and decay. Heartwood of inoculated trees was sampled at regular intervals to determine the incidence and type of decay. Attempts were also made to recover the inoculated fungus. Using these methods they showed that Stereum hirsutum and a species of Hymenochaete caused white rot in heartwood within two years. Castro and Krügner (1984a) also isolated fungi from decayed heartwood, in this case from E. urophylla. Two unnamed isolates, both hymenomycetes, were observed to have caused decay 115 days after the host was inoculated. 309

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Fungi closely associated with heartwood rot in the butt and major roots of living eucalypts in Australia Geographical occurrence

Fungi implicated [Synonyms]

Rot typeA Eucalypt hostsB

ReferencesC

Remarks

Amauroderma rude (Berk.) G.Cunn.

WR

(E. camaldulensis, Vic. E. cypellocarpa, E. globoidea, E. regnans)

Marks et al. (1982)

Found in most parts of Victoria except the arid areas

Armillaria novae-zelandiae (G.Stev.) Herink

WR

E. delegatensis, E. regnans

Tas.

TJW

Associated with butt rot of 30year-old trees

Aurantioporus pulcherrimus (Rodway) P.K.Buchanan & Hood [syn. Tyromyces pulcherrimus (Rodway) G.Cunn.]

WPR

E. pauciflora

NSW

JAS

Aurantioporus pulcherrimus (Rodway) P.K.Buchanan & Hood [syn. Tyromyces pulcherrimus (Rodway) G.Cunn.]

WPR

E. delegatensis, E. pauciflora

Vic.

Marks et al. (1982)

Aurantioporus pulcherrimus (Rodway) P.K.Buchanan & Hood [syn. Tyromyces pulcherrimus (Rodway) G.Cunn.]

WPR

(E. delegatensis)

Tas.

TJW

Coniophora olivacea (Fr.) P.Karst.

BR

E. marginata

WA

Tamblyn (1944); Da Costa (1973)

Coprinus micaceus (Bull.:Fr.) Fr.

WR

C. maculata, E. nicholii

NSW

JAS

Fistulina spiculifera (Cooke) D.A.Reid

BR

E. pilularis, E. saligna

NSW

JAS

Fistulina spiculifera (Cooke) D.A.Reid

?BR

(C. calophylla, E. guilfoylei, E. jacksonii, E. marginata)

WA

Tamblyn (1937); Hilton (1982); Hilton et al. (1989); RNH

Probably the most common fungus on living E. marginata stems in south-west of Western Australia. Causes pencilling.

Ganoderma lucidum (Curtis) P.Karst. sens. lat.

WR

C. citriodora

Qld

JWT

Widely distributed in Queensland

Gymnopilus crociphyllus (Sacc.) Pegler (syn. Flammula crociphylla Sacc.)

WR

E. obliqua

NSW

JAS

Gymnopilus spectabilis (Fr.:Fr.) A.H.Sm. [syn. Pholiota spectabilis (Fr.:Fr.) P.Kumm.]

WR

E. mannifera

ACT

JAS

310

A rare fungus, restricted in Victoria to alpine regions

Initially reported as Coniophora cerebella (Pers.) Pers.

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Gymnopilus spectabilis (Fr.:Fr.) A.H.Sm. [syn. Pholiota spectabilis (Fr.:Fr.) P.Kumm.]

WR

C. citriodora, C. maculata, E. robusta, E. viminalis

NSW

JAS

Gymnopilus spectabilis (Fr.:Fr.) A.H.Sm.

WR

E. macrorhyncha, E. viminalis

Vic.

Marks et al. (1982)

Distributed throughout southeast Australia

Hapalopilus mutans (Peck) Gilb. & Ryvarden [syn. Poria mutans (Peck) Peck, Poria healeyi N.Walters]

WR

E. regnans

Vic.

Walters 1958

This column heart rot can continue to develop after tree death

Hapalopilus mutans (Peck) Gilb. & Ryvarden [syn. Poria mutans (Peck) Peck, Poria healeyi N.Walters]

WR

(E. guilfoylei, E. jacksonii, E. staeri), E. marginata

WA

Tamblyn (1937); Hilton (1982); Hilton et al. (1989)

Usually associated with a butt and stem rot which occasionally extends well up mature E. marginata

Hapalopilus sp.

WR

E. microcorys

NSW

JAS

Hexagonia vesparius (Berk.) Ryvarden [syn. Hexagonia gunnii Berk., Osmoporus gunnii (Berk.) G.Cunn.]

WR

(E. odorata, E. viminalis)

SA

Cleland (1934–35); Cunningham (1965)

Basidiomes found 3 m or more above the ground on stems of dead or dying eucalypts

Hexagonia vesparius (Berk.) Ryvarden [syn. Hexagonia gunnii Berk., Osmoporus gunnii (Berk.) G.Cunn.]

?WR

(E. bridgesiana, E. cypellocarpa, E. macrorhyncha, E. microcarpa, E. moluccana, E. ovata, E. viminalis)

Vic.

Marks et al. (1982); NEMW

Occurs throughout Victoria and is suspected of causing heartwood decay

Hexagonia vesparius (Berk.) Ryvarden [syn. Hexagonia gunnii Berk., Osmoporus gunnii (Berk.) G.Cunn.]

WR

(E. gomphocephala)

WA

Cunningham (1965)

Basidiomes on standing dead or dying stems of eucalypts

Hymenochaete sp.

WPR

E. diversicolor

WA

Davison and Tay (1990)

Causes brown wood and decay in regrowth E. diversicolor

Inonotus albertinii (Lloyd) P.K.Buchanan & Ryvarden

BR

(E. obliqua)

SA

Cunningham (1965)

Basidomes on stems of living tree or roots at base of stem

Inonotus chondromyelus Pegler [syn. Inonotus dryadeus (Pers.:Fr.) Murrill]

WPR

(E. saligna)

NSW

Cunningham (1965)

Inonotus chondromyelus Pegler [syn. Inonotus dryadeus (Pers.:Fr.) Murrill]

WPR

E. eugenioides, E. drepanophylla, E. microcorys, E. resinifera, C. tessellaris

Qld

JWT

Inonotus chondromyelus Pegler [syn. Inonotus dryadeus (Pers.:Fr.) Murrill]

WPR

(E. obliqua, E. viminalis)

SA

Cleland (1934–35); Cunningham (1965)

Inonotus chondromyelus Pegler [syn. Inonotus dryadeus (Pers.:Fr.) Murrill]

WPR

(E. macrorhyncha, E. obliqua, E. regnans)

Vic.

Cunningham (1965)

Common in wet lowlands or high altitude forests

Basidiomes at base of living or standing dead stems

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Fungi closely associated with heartwood rot in the butt and major roots of living eucalypts in Australia (continued)

Fungi implicated [Synonyms]

Rot typeA Eucalypt hostsB

Geographical occurrence

ReferencesC

Inonotus rheades (Pers.) Bondartsev & Singer

WR

(E. macrorhyncha)

Vic.

Cunningham (1965)

Inonotus rheades (Pers.) Bondartsev & Singer

WR

(E. obliqua)

SA

Cunningham (1965)

Inonotus rheades (Pers.) Bondartsev & Singer

WR

(E. tereticornis)

Qld

Cunningham (1965)

Mycena subgalericulata Cleland

WR

(E. obliqua)

SA

Cleland (1934–35)

Omphalotus nidiformis (Berk.) O.K.Mill. [syn. Pleurotus nidiformis (Berk.) Sacc.]

WR

C. maculata, E. obliqua

NSW

JAS

Omphalotus nidiformis (Berk.) O.K.Mill. [syn. Pleurotus nidiformis (Berk.) Sacc.]

WR

E. pilularis, E. saligna, E. macrorhyncha, E. radiata

Vic.

Marks et al. (1982)

Distributed throughout the wetter mountainous areas of Victoria, and wooded lowlands

Omphalotus nidiformis (Berk.) O.K.Mill. [syn. Pleurotus nidiformis (Berk.) Sacc.]

WR

C. calophylla

WA

Hilton et al. (1989); RNH

Throughout south-west of Western Australia

Panellus pusillus (Pers.:Lév.) Burds. & O.K. Mill. [syn. Dictyopanus rhipidium (Berk.) Pat.]

WR

E. pilularis, E. sieberi

NSW

JAS

On fire-scarred trees

Perenniporia medulla-panis (Jacq.:Fr.) Donk [syn. Poria medulla-panis (Jacq.:Fr.) Bres.]

WPR

E. obliqua, E. regnans

Tas.

TJW

Decay associated with butt wounds

Phellinus extensus (Lév.) Pat.

WR

E. piperita

NSW

JAS

Phellinus gilvus (Schwein.) Pat. [syn. Fomes gilvus (Schwein.) Lloyd]

WPR

E. crebra

NSW, Qld

JAS, JWT

Found in south-east Queensland (rare)

Phellinus gilvus (Schwein.) Pat. [syn. Fomes gilvus (Schwein.) Lloyd]

WPR

(C. calophylla), E. diversicolor, E. marginata

WA

Tamblyn (1936, 1937); Hilton et al. (1989), RNH

Found in south-west of Western Australia. Tentative identification as Phellinus gilvus or Fomes lineato-scaber Berk. & Broome. Associated with butt rot of young E. marginata coppice.

Phellinus noxius (Corner) G.Cunn.

WPR

C. citriodora, C. ptychocarpa

Qld

JWT

Found in wet, former rainforest sites. Attacks sapwood and heartwood.

312

Remarks

Basidiomes develop from fissures in bark

STEM

AND

BUTT ROT

OF

EUCALYPTS

C H A P T E R

13

Phellinus noxius (Corner) G.Cunn.

WPR

C. calophylla

WA

Hilton et al. (1989); RNH

Throughout south-west of Western Australia

Phellinus rimosus (Berk.) Pilát [syn. Fomes rimosus (Berk.) Cooke including Phellinus badius (Berk.) G.Cunn.]

WPR

E. crebra, E. dealbata, E. pilligaensis, E. populnea

NSW

JAS; Wilkes (1985b)

Phellinus rimosus (Berk.) Pilát [syn. Fomes rimosus (Berk.) Cooke including Phellinus badius (Berk.) G.Cunn.]

WPR

C. maculata

Qld

JWT

Found throughout Queensland

Phellinus rimosus (Berk.) Pilát [syn. Fomes rimosus (Berk.) Cooke including Phellinus badius (Berk.) G.Cunn.]

WPR

(E. odorata, E. oleosa)

SA

Cleland (1934–35)

Found in living stems

Phellinus rimosus (Berk.) Pilát [syn. Fomes rimosus (Berk.) Cooke including Phellinus badius (Berk.) G.Cunn.]

WPR

E. wandoo

WA

Tamblyn (1936); Hilton (1982); Hilton et al. (1989); Shivas (1989)

Found in south-west region of Western Australia. Mainly causes a top rot but may extend into butt.

Phellinus robustus (P.Karst.) Bourdot & Galzin (syn. Fomes robustus P.Karst.)

WPR

E. grandis, E. nicholii, E. resinifera, E. saligna

NSW

JAS

Phellinus robustus (P.Karst.) Bourdot & Galzin (syn. Fomes robustus P.Karst.)

WPR

(E. camaldulensis, E. fasciculosa, E. odorata, E. oleosa, E. ovata, E. viminalis)

SA

Cleland (1934–35)

Phellinus wahlbergii (Fr.) D.A.Reid [syn. Phellinus zealandicus (Cooke) Teng, including Phellinus setulosus (Lloyd) Imazeki]

WPR

E. dalrympleana, E. globulus ssp. bicostata

ACT

JAS

Phellinus wahlbergii (Fr.) D.A.Reid [syn. Phellinus zealandicus (Cooke) Teng, including Phellinus setulosus (Lloyd) Imazeki]

WPR

E. globulus ssp. globulus, E. globulus ssp. bicostata, E. nova-anglica, E. viminalis

NSW

JAS

Phellinus wahlbergii (Fr.) D.A.Reid [syn. Phellinus zealandicus (Cooke) Teng, including Phellinus setulosus (Lloyd) Imazeki]

WPR

E. drepanophylla

Qld

JWT

Phellinus wahlbergii (Fr.) D.A.Reid [syn. Phellinus zealandicus (Cooke) Teng, including Phellinus setulosus (Lloyd) Imazeki]

WPR

E. delegatensis, E. obliqua, E. regnans, E. viminalis

Tas.

TJW

On stems of living trees from the base to about 3 m

Found in wetter forests of Queensland

313

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Fungi closely associated with heartwood rot in the butt and major roots of living eucalypts in Australia (continued)

Fungi implicated [Synonyms]

Rot typeA Eucalypt hostsB

Geographical occurrence

ReferencesC

Remarks

Phellinus wahlbergii (Fr.) D.A.Reid [syn. Phellinus zealandicus (Cooke) Teng, including Phellinus setulosus (Lloyd) Imazeki]

WPR

E. obliqua, E. ovata, E. regnans

Vic.

Marks et al. (1982)

Probably attacks most eucalypts in Victoria, except those in the arid areas

Phellinus wahlbergii (Fr.) D.A.Reid [syn. Phellinus zealandicus (Cooke) Teng, including Phellinus setulosus (Lloyd) Imazeki]

WPR

E. diversicolor

WA

MHP

Piptoporus australiensis (Wakef.) G.Cunn. BR (syn. Polyporus australiensis Wakef.)

E. botryoides, E. camaldulensis, E. fastigata, E. robusta

NSW

JAS

Piptoporus maculatissimus (Lloyd) G.Cunn.

BR

E. delegatensis, E. pauciflora, Vic. E. regnans

Piptoporus portentosus (Berk.) G.Cunn. (syn. Polyporus eucalyptorum Fr., Piptoporus portentosus Berk.)

BR

E. mannifera

ACT

JAS

Piptoporus portentosus (Berk.) G.Cunn. (syn. Polyporus eucalyptorum Fr., Piptoporus portentosus Berk.)

BR

E. amplifolia, E. blakelyi, E. camaldulensis, E. cinerea, E. dalrympleana, E. oreades, E. parramattensis, E. propinqua, E. tereticornis, E. viminalis

NSW

JAS

Associated with majority of heart rots in New South Wales red gums

Piptoporus portentosus (Berk.) G.Cunn. (syn. Polyporus eucalyptorum Fr., Piptoporus portentosus Berk.)

BR

(E. baxteri, E. camaldulensis, E. goniocalyx, E. leucoxylon, E. obliqua, E. viminalis)

SA

Cleland (1934–35); Cunningham (1965)

Common and produces basidiomes up to 1 m from the ground or high up on stems

Piptoporus portentosus (Berk.) G.Cunn. (syn. Polyporus eucalyptorum Fr., Piptoporus portentosus Berk.)

BR

E. camaldulensis, Vic. E. cypellocarpa, E. globoidea, E. macrorhyncha, E. microcarpa, E. obliqua, E. ovata, E. polyanthemos, E. radiata, E. regnans, E. sieberi, E. smithii, E. viminalis

Marks et al. (1982); NEMW

Found in most Victorian forests and exclusively on eucalypts. Able to attack all parts of stem.

314

Marks et al. (1982)

Common in Victoria's alpine region

S

TEM AND

BUTT ROT

OF

EUCALYPTS

C H A P T E R

13

Piptoporus portentosus (Berk.) G.Cunn. (syn. Polyporus eucalyptorum Fr., Piptoporus portentosus Berk.)

BR

C. calophylla, E. gomphocephala, E. marginata, E. patens, E. rudis

WA

Tamblyn (1936, 1937); Hilton et al. (1989); RHN

In E. marginata, associated with majority of decay in top and upper stem but occasionally also a butt rot. The most destructive heart rot of live E. marginata in south-west Western Australia.

Polyporus tumulosus Cooke & Massee

?BR

(E. macrorhyncha, E. obliqua)

Vic.

Marks et al. (1982)

Widely distributed in Victoria and may cause brown rot of heartwood

Polyporus tumulosus Cooke & Massee

BR

(E. diversicolor), E. marginata

WA

Tamblyn (1936; 1937)

The variety "westraliensis" was never described. Common in south-west Western Australia, but only once isolated from living E. marginata.

Postia pelliculosa (Berk.) Rajchenb. [syn. Polyporus pelles Lloyd, Polyporus pelliculosus Berk., Tyromyces pelliculosus (Berk.) G.Cunn.]

BR

E. blaxlandii, E. obliqua

NSW

JAS

Postia pelliculosa (Berk.) Rajchenb. [syn. Polyporus pelles Lloyd, Polyporus pelliculosus Berk., Tyromyces pelliculosus (Berk.) G.Cunn.]

BR

E. microcorys

Qld

JWT

Common in south-east Queensland

Postia pelliculosa (Berk.) Rajchenb. [syn. Polyporus pelles Lloyd, Polyporus pelliculosus Berk., Tyromyces pelliculosus (Berk.) G.Cunn.]

BR

(E. obliqua)

SA

Cleland (1934–35)

Common on living stems

Postia pelliculosa (Berk.) Rajchenb. [syn. Polyporus pelles Lloyd, Polyporus pelliculosus Berk., Tyromyces pelliculosus (Berk.) G.Cunn.]

BR

E. baxteri, E. consideniana, E. dives, E. elata, E. globoidea, E. macrorhyncha, E. obliqua, E. ovata, E. polyanthemos, E. regnans, E. sieberi

Vic.

Cunningham (1965); Marks et al. (1982)

Widespread in south and east Australia

Postia pelliculosa (Berk.) Rajchenb. [syn. Polyporus pelles Lloyd, Polyporus pelliculosus Berk., Tyromyces pelliculosus (Berk.) G.Cunn.]

BR

C. calophylla, E. marginata

WA

Tamblyn (1936); Hilton et al. (1989); RNH

Common in Darling Ranges of Western Australia

Pulcherricium caeruleum (Lam.: St.Amans) Parmasto

WR

E. grandis

NSW

JAS

315

D I S E A S E S

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O F

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Fungi closely associated with heartwood rot in the butt and major roots of living eucalypts in Australia (continued)

Fungi implicated [Synonyms]

Rot typeA Eucalypt hostsB

Geographical occurrence

ReferencesC

Remarks

Punctularia strigoso-zonata (Schwein.) P.H.B.Talbot

WR

C. torelliana

NSW

JAS

Found on a coppiced tree

Rigidoporus laetus (Cooke) P.K.Buchanan & Ryvarden [syn. Coltricia laeta (Cooke) G.Cunn., Polyporus lateritius Lloyd]

WR

(E. viminalis)

SA

Cleland (1934-35)

Found once on a living tree

Ryvardenia campyla (Berk.) Rajchenb. [syn. Grifola campyla (Berk.) G.Cunn.]

BR

C. calophylla, E. diversicolor

WA

MHP

Ryvardenia cretacea (Lloyd) Rajchenb. [syn. Piptoporus cretaceus (Lloyd) G.Cunn.]

BR

E. microcorys

NSW

JAS

Ryvardenia cretacea (Lloyd) Rajchenb. [syn. Piptoporus cretaceus (Lloyd) G.Cunn.]

BR

E. delegatensis, E. regnans

Vic.

Marks et al. (1982)

Ryvardenia cretacea (Lloyd) Rajchenb. [syn. Piptoporus cretaceus (Lloyd) G.Cunn.]

BR

E. amygdalina, (E. delegatensis, E. regnans)

Tas.

TJW

Stereum hirsutum (Willd.:Fr.) Gray

WR

E. diversicolor

WA

Davison and Tay (1990); RNH

Trechispora mollusca (Pers.:Fr.) Liberta [syn. Fibuloporia mollusca (Pers.:Fr.) Bondartsev & Singer, Poria mollusca (Pers.:Fr.) Cooke]

WR

E. obliqua

NSW

Edwards (1982); DWE Tentative identification of species by NEMW

Tyromyces merulinus (Berk.) G.Cunn. [syn. Poria merulina (Berk.) Cooke]

WR

(E. obliqua)

SA

Cleland (1934-35)

Basidiomes found on living stems

Xylobolus spectabilis (Klotzsch) Boidin (syn. Stereum radiato-fissum Berk. & Broome)

WPR

(E. baxteri)

SA

Cleland (1934-35)

Found on stems

A

Found in wet, mountain forests of Victoria

Causes brown wood and decay in regrowth E. diversicolor in south-west Western Australia

Rot types: BR, brown rot; WPR, white pocket rot; WR, white rot. The brackets indicate that the reference did not state whether the host was alive, or that heartwood was attacked, or that the host was old enough to have heartwood. If unbracketed, the live eucalypt host showed heartwood decay. C Personal communications: DWE, the late D.W. Edwards (State Forests of New South Wales); JAS, J.A. Simpson (State Forests of New South Wales); JWT, the late J.W. Tierney (Queensland Forest Service); MHP, M.H. Pearce (formerly of CSIRO Forestry and Forest Products); NEMW, N.E.M. Walters (CSIRO Forestry and Forest Products, retired); RNH, R.N. Hilton (Botany Department, University of Western Australia, retired); TJW, T.J. Wardlaw (Forestry Tasmania). B

316

STEM

T ABLE 1 3 . 2

AND

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EUCALYPTS

C H A P T E R

13

Fungi closely associated with heartwood rot in the upper trunk and major branches of living eucalypts in Australia

Fungi implicated [Synonyms]

Rot typeA Eucalypt hostsB,C

Geographical occurrenceC

ReferencesD

Aleurodiscus sp.

WR

E. delegatensis, E. obliqua, E. regnans

Tas.

TJW

Amauroderma rude (Berk.) G.Cunn.

WR

As for Table 13.1 for Vic.

Vic.

Marks et al. (1982); NEMW

Usually attacks butt although may attack top

Australoporus tasmanicus (Berk.) P.K.Buchanan & Ryvarden (syn. Polyporus tasmanicus Berk.)

WR

E. regnans

Vic.

Cunningham (1965); Marks et al. (1982)

Restricted to alpine regions of Victoria

Hexagonia vesparius (Berk.) Ryvarden

WR

As for Table 13.1 for SA, Vic. & WA

Heterobasidion hemitephrum (Berk.) G.Cunn.

WR

(Eucalyptus spp.)

Vic.

Cunningham (1965)

None of the existing generic names is appropriate for this fungus

Hymenochaete sp.

WPR

E. diversicolor

WA

Davison and Tay 1990 Causes brown wood and decay in regrowth E. diversicolor

Inonotus chondromyelus Pegler

WPR

E. baxteri, E. camaldulensis, E. delegatensis, E. dives, E. globoidea, E. macrorhyncha, E. obliqua, E. radiata, E. rubida, E. viminalis

Vic.

Marks et al. (1982)

Inonotus luteo-contextus D.A.Reid

WR

E. pilularis

NSW

JAS

Inonotus victoriensis (Lloyd) Pegler

WR

E. obliqua

NSW

JAS

Laetiporus sulphureus (Bull.:Fr.) Murrill [syn. Polyporus sulphureus (Bull.:Fr.) Fr., Grifola sulphurea (Bull.:Fr.) Pilát]

BR

E. tereticornis

Qld

JWT

Meruliopsis sp.

WR

E. regnans

Tas.

TJW

Perenniporia ochroleuca (Berk.) Ryvarden WR

E. grandis, E. pilularis

NSW

JAS

Phellinus rimosus (Berk.) Pilát

As for Table 13.1 for NSW & WA

WPR

Remarks

Found in most Victorian forests

Uncommon

317

D I S E A S E S

T A BLE 1 3 . 2

A N D

P A T H O G E N S

O F

E U C A L Y P T S

Fungi closely associated with heartwood rot in the upper trunk and major branches of living eucalypts in Australia (continued)

Fungi implicated [Synonyms]

Rot typeA Eucalypt hostsB,C

Geographical occurrenceC

ReferencesD

Remarks

Phellinus rimosus (Berk.) Pilát

WPR

E. drepanophylla, C. intermedia, C. maculata, E. microcarpa, E. populnea

Qld

JWT

Widely distributed in Queensland

Phellinus rimosus (Berk.) Pilát

WPR

E. camaldulensis, E. microcarpa, E. moluccana

Vic.

Marks et al. (1982); NEMW

Widely distributed in Victoria

Phellinus robustus (P.Karst.) Bourdot & Galzin (syn. Fomes robustus P.Karst.)

WPR

As for Table 13.1 for NSW

Phellinus robustus (P.Karst.) Bourdot & Galzin (syn. Fomes robustus P.Karst.)

WPR

E. crebra, E. drepanophylla, E. melanophloia, E. moluccana, E. resinifera, E. sideroxylon, E. thozetiana

Qld

JWT

Widely distributed in Queensland

Phellinus robustus (P.Karst.) Bourdot & Galzin (syn. Fomes robustus P.Karst.)

WPR

E. amygdalina, E. globulus, E. ovata, E. viminalis

Tas.

TJW

Entry associated with branch stubs

Phellinus robustus (P.Karst.) Bourdot & Galzin (syn. Fomes robustus P.Karst.)

WPR

E. bosistoana, E. camaldulensis, E. dumosa, E. microcarpa, E. viminalis

Vic.

Marks et al. (1982); Parkin (1942); GCJ

Widely distributed in Victoria

Phellinus robustus (P.Karst.) Bourdot & Galzin (syn. Fomes robustus P.Karst.)

WPR

E. wandoo

WA

Tamblyn (1936)

Fungus tentatively identified as Fomes robinsoniae Lloyd. Probably most common cause of heart rot in E. wandoo.

Phellinus wahlbergii (Fr.) D.A.Reid

WPR

E. dalrympleana, E. globulus ssp. bicostata

ACT, NT

JAS

Phellinus wahlbergii (Fr.) D.A.Reid

WPR

E. drepanophylla

Qld

JWT

Found in south-east Queensland (rare)

Phellinus wahlbergii (Fr.) D.A.Reid

WPR

E. bosistoana, E. botryoides, E. camaldulensis, E. cypellocarpa, E. melliodora, E. microcarpa, E. obliqua, E. ovata, E. polyanthemos, E. radiata, E. regnans, E. viminalis

Vic.

Marks et al. (1982)

Fungus found in most parts of Victoria

Qld

JWT

Common in Queensland

Piptoporus australiensis (Wakef.) G.Cunn. BR

As for Table 13.1 for NSW

Piptoporus australiensis (Wakef.) G.Cunn. BR

E. drepanophylla, E. microcarpa

318

STEM

AND

BUTT ROT

OF

EUCALYPTS

C H A P T E R

13

Piptoporus australiensis (Wakef.) G.Cunn. BR

E. bosistoana, E. botryoides, E. bridgesiana, E. cypellocarpa, E. globulus ssp. maidenii, E. melliodora, E. muelleriana, E. obliqua, E. polyanthemos, E. regnans, E. sideroxylon

Vic.

Marks et al. (1982)

Found exclusively on eucalypts and in most Victorian forests

Piptoporus australiensis (Wakef.) G.Cunn. BR

C. calophylla, E. diversicolor, (E. gomphocephala, E. guilfoylei, E. wandoo)

WA

Tamblyn (1936); Hilton (1982); Hilton et al. (1989); RNH

Common in south-west Western Australia

Piptoporus portentosus (Berk.) G.Cunn.

BR

As for Table 13.1 for ACT, NSW, SA, Vic. & WA

Piptoporus portentosus (Berk.) G.Cunn.

BR

E. camaldulensis, E. propinqua, E. tereticornis

Qld

JWT

Common in Queensland

Piptoporus portentosus (Berk.) G.Cunn.

BR

E. diversicolor

WA

MHP

Postia pelliculosa (Berk.) Rajchenb.

BR

As for Table 13.1 for NSW & WA

Postia pelliculosa (Berk.) Rajchenb.

BR

E. amygdalina

Tas.

TJW

Ryvardenia campyla (Berk.) Rajchenb. [syn. Grifola campyla (Berk.) G.Cunn.]

BR

E. cypellocarpa, E. delegatensis, E. obliqua, E. pauciflora, E. radiata, E. regnans, E. viminalis

Vic.

Marks et al. (1982)

Found throughout Victoria

Ryvardenia campyla (Berk.) Rajchenb. [syn. Grifola campyla (Berk.) G.Cunn.]

BR

C. calophylla, E. diversicolor

WA

MHP

Found in wind thrown mature trees

Schizopora flavipora (Cooke) Ryvarden [syn. Schizopora carneolutea (Rodway & Cleland) Kotl. & Pouzar]

WR

E. grandis

NSW

JAS

Stereum hirsutum (Willd.:Fr.) Gray

WR

E. diversicolor

WA

Davison and Tay (1990); RNH

Stereum sp.

WR

E. delegatensis, E. regnans

Tas.

TJW

Vararia sp.

WR

E. delegatensis, E. obliqua, E. regnans

Tas.

TJW

Xylobolus sp.

BR

E. obliqua

Tas.

TJW

Associated with brown wood and decay in regrowth E. diversicolor

A

Rot types: BR, brown rot; WPR, white pocket rot; WR, white rot. B The brackets indicate that the reference did not state whether the host was alive, or that heartwood was attacked, or that the host was old enough to have heartwood. If unbracketed, the live eucalypt host showed heartwood decay. C Personal communications: GCJ, G.C. Johnson (formerly CSIRO Forestry and Forest Products); JAS, J.A. Simpson; JWT, J.W. Tierney; MHP, M.H. Pearce; NEMW; N.E.M. Walters; RNH, R.N. Hilton; TJW, T.J. Wardlaw.

319

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O F

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Fungi associated with decay in the butt, trunk and major branches of eucalypts in countries other than Australia

Fungi implicated [Synonyms]

Rot typeA Eucalypt hostsB

Geographical occurrenceC

Armillaria sp.

WR

E. grandis

Armillaria sp.

WR

Armillaria sp. Chondrostereum purpureum (Pers.:Fr.) Pouzar

ReferencesD

Remarks

PNG

Arentz and Simpson (1989)

Heart rotted

E. globulus ssp. bicostata

PNG

Arentz and Simpson (1989)

Root and butt rot of < 20-yearold trees

WR

E. robusta

PNG

Vigus (1986)

Butts of sapling and pole trees attacked

WR

(E. delegatensis)

New Zealand

Gadgil and Bawden (1981)

Branch stubs of 4-year-old trees attacked

Fistulina hepatica (Schaeff.:Fr.) Fr.

BR

(Eucalyptus sp.)

Portugal

Spaulding (1961)

Heart rotted

Fomes fomentarius (L.:Fr.) J.J.Kickx

WR

E. globulus

Portugal

N.F.S. Azevedo (1971, pers. comm.)

Butt rotted

Fomes fomentarius (L.:Fr.) J.J.Kickx

WR

Eucalyptus sp.

Portugal

Sampaio (1975)

Infection occurred via wounds

Fomitopsis feei (Fr.) Kreisel [syn. Trametes feei (Fr.) Pat., Polyporus rubidus Berk.]

BR

C. citriodora

India

Bakshi et al. (1956)

Infection occurred via pruning wounds. Heart rotted

Ganoderma applanatum (Pers.) Pat.

WR

(E. globulus)

USA

Baxter (1967)

Ganoderma applanatum (Pers.) Pat.

WR

(Eucalyptus sp.)

Portugal

Spaulding (1961)

Ganoderma lucidum (Curtis) P.Karst.

WR

C. citriodora

India

Spaulding 1961

Butt and heartwood attacked

Ganoderma lucidum (Curtis) P.Karst.

WR

E. globulus

Argentina

Spaulding (1961)

Butt and heartwood attacked

Ganoderma lucidum (Curtis) P.Karst.

WR

Eucalyptus spp.

Worldwide

Foster (1964)

Roots, butt and stem attacked

Hymenochaete floridea Berk. & Broome

WPR

E. deglupta

PNG

JAS

Butt rotted

Hymenochaete rhabarbarina (Berk.) Cooke

WPR

E. deglupta

PNG

JAS

Butt rotted

Inonotus rheades (Pers.) Bondartsev & Singer

WR

(E. camaldulensis, E. grandis, E. saligna)

Brazil

Castro and Krügner (1984b)

Attacked trees 6–10 years old

Laetiporus discolor (Klotzsch) Corner

BR

E. grandis

PNG

JAS

Butt, stem and major branches attacked

Laetiporus sulphureus (Bull.:Fr.) Murrill

BR

(E. amygdalina, E. globulus)

Argentina

Bonar (1942)

Laetiporus sulphureus (Bull.:Fr.) Murrill

BR

E. camaldulensis

Portugal

Pimentel (1982)

Laetiporus sulphureus (Bull.:Fr.) Murrill

BR

E. globulus

PNG

JAS

Laetiporus sulphureus (Bull.:Fr.) Murrill

BR

E. globulus

Portugal

N.F.S.Azevedo (1971, pers. comm.)

Laetiporus sulphureus (Bull.:Fr.) Murrill

BR

E. globulus

USA

Bonar (1942)

320

Butt, stem and major branches attacked

Lower stem and large roots attacked

STEM

AND

BUTT ROT

OF

EUCALYPTS

C H A P T E R

13

Laetiporus sulphureus (Bull.:Fr.) Murrill

BR

E. grandis, E. saligna

South Africa

Lückhoff (1964)

Most damage seen in unthrifty stands

Laetiporus sulphureus (Bull.:Fr.) Murrill

BR

E. saligna

Brazil

May (1962)

Infection occurred via heartwood wounds

Laetiporus sulphureus (Bull.:Fr.) Murrill

BR

E. saligna

South Africa

van der Westhuizen (1959)

Older (37-year) trees attacked, younger (8-year) were not

Laetiporus sulphureus (Bull.:Fr.) Murrill

BR

Eucalyptus sp.

Portugal

Sampaio (1975)

Trees killed in a few years

Lentinus squarrosulus Mont.

WR

(C. citriodora)

India

Sharma et al. (1985)

Associated with wounded 6-year-old trees

Microporus xanthopus (Fr.) Kuntze

WR

(C. citriodora)

India

Sharma et al. (1985)

As above

Phellinus conchatus (Pers.:Fr.) Quél. [syn. Fomes conchatus (Pers.:Fr.) Gillet]

WR

Eucalyptus sp.

Portugal

Spaulding (1961)

Stem heart rotted

Phellinus ferruginosus (Schrad.:Fr.) Pat. [syn. Phellinus salicinus (Fr.) Quél.]

WR

Eucalyptus sp.

Portugal

Azevedo (1971 pers. comm.)

Stem heart rotted

Phellinus gilvus (Schwein.) Pat.

WPR

E. grandis, E. saligna

Zambia

Gibson (1975)

Severe rot in trees as young as 4 years old

Phellinus gilvus (Schwein.) Pat.

WPR

(E. cloeziana, E. grandis, E. pilularis, E. resinifera)

Zambia

Piearce (1987)

Butt rot associated with mechanical injury. Infection occurred via pruning wounds.

Phellinus gilvus (Schwein.) Pat.

WPR

C. maculata

Zimbabwe

Masuka 1990; Masuka Fungus associated with minor and Ryvarden (1992) heart rot of overmature trees

Phellinus ignarius (L.:Fr.) Quél.

WR

(Eucalyptus sp.)

Widespread

Bakshi (1964)

Phellinus ignarius group

WR

E. alba

PNG

JAS

Phellinus noxius (Corner) G.Cunn.

WPR

(E. deglupta)

PNG, Solomon Islands

Davidson 1974; Mukiu Infection of young trees 1992; JAS occurred via pruned branches. Butt, stem and major branches attacked.

Phellinus noxius (Corner) G.Cunn.

WPR

(E. deglupta)

Vanuatu

JAS

Phellinus resinaceus Kotl. & Pouzar

WR

C. papuana

PNG

Kotlaba and Pouzar (1979); JAS

Upper stem and major branches attacked

Phellinus rimosus (Berk.) Pilát

WPR

E. grandis

PNG

JAS

Butt, stem and major branches attacked

Phellinus robiniae (Murrill) A.Ames

WPR

C. confertiflora

PNG

JAS

Provisional identification of fungal species by F. Kotlaba (JAS). Upper stem and major branches attacked.

Upper stem and major branches attacked

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Fungi associated with decay in the butt, trunk and major branches of eucalypts in countries other than Australia (continued)

Fungi implicated [Synonyms]

Rot typeA Eucalypt hostsB

Geographical occurrenceC

ReferencesD

Phellinus robustus (P.Karst.) Bourdot & Galzin

WPR

E. tereticornis

PNG

JAS

Phellinus robustus (P.Karst.) Bourdot & Galzin

WPR

Eucalyptus spp.

USA

Bakshi (1964)

Infection via branch stubs

Phellinus robustus (P.Karst.) Bourdot & Galzin

WPR

Eucalyptus spp.

USA

Overholts (1953)

Butt, stem and major branches attacked

Phellinus torulosus (Pers.) Bourdot & Galzin

WR

E. globulus

Portugal

Azevedo (1971, pers. comm.)

Stem heart rotted

Phellinus torulosus (Pers.) Bourdot & Galzin

WR

Eucalyptus sp.

Portugal

Sampaio (1975)

Piptoporus australiensis (Wakef.) G.Cunn. BR

E. deglupta

PNG

JAS

Provisional identification of species by JAS. Upper stem and major branches attacked

Piptoporus portentosus (Berk.) G.Cunn.

BR

E. tereticornis

PNG

JAS

Commonly attacks this species. Butt, stem and major branches attacked

Stereum hirsutum (Willd.:Fr.) Gray

WR

(E. diversicolor)

South Africa

Food and Agriculture Organization (1958)

Trees > 40 years old attacked

Stereum hirsutum (Willd.:Fr.) Gray

WR

E. globulus

South Africa

Bottomley & Carlson 1920; Food and Agriculture Organization (1958)

Stool shoots (2-6 years old) attacked from infected stumps

Stereum hirsutum (Willd.:Fr.) Gray

WR

(E. globulus ssp. maidenii)

South Africa

Spaulding (1961)

Heart rotted

Stereum hirsutum (Willd.:Fr.) Gray

WR

(E. saligna)

South Africa

Food and Agriculture Organization (1958)

Shoots from old stumps attacked

Trametes cubensis (Mont.) Sacc.

WR

C. citriodora

India

Bagchee (1953)

Sap and heart rot originating from wounds

Trametes scabrosa (Pers.) G.Cunn.

WR

E. deglupta

PNG

JAS

Upper stem and major branches attacked

A

Remarks

Rot types: BR, brown rot; WPR, white pocket rot; WR, white rot. The brackets indicate that the reference did not state whether the host was alive, or that heartwood was attacked, or that the host was old enough to have heartwood. If unbracketed, the live eucalypt host showed heartwood decay. C PNG, Papua New Guinea; USA, United States of America. D Personal communications: Azevedo, N.S.F. Azevedo (Estacao Florestal nacional—INIAER, Portugal); as in Tables 13.1 and 13.2; JAS, J.A. Simpson. B

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Until a given fungus is shown, using the steps in Koch’s postulates, to cause heart rot, it should be considered as being ‘associated’ with the heart rot. Nearly all of the species in Tables 13.1 to 13.3 need to be considered as having this status. Despite the thousands of species of Basidiomycota and Ascomycota capable of decaying wood, few are known to decay heartwood of living trees (Wagener and Davidson 1954). All the fungi listed in Tables 13.1 to 13.3 are members of the Aphyllophorales or Agaricales and are associated with the cell wall degradation stage of heart rot of eucalypts. None belongs to the Ascomycota. Over 80% of the species in each table are Aphyllophorales, with the rest being Agaricales, most of which are associated with butt rot. Most fungi appearing in Tables 13.1 and 13.2 were associated with heart rot in a few host species and in a few Australian States. This distribution may relate to the geographical range of the fungus (including where it produces basidiomes), geographical range of the host and/or the location and field of interest of a particular mycologist or pathologist. Some of these fungi (such as Rigidoporus laetus) are probably opportunistic and rare colonisers of wounded wood and may not be able to decay substantially beyond the wound-altered zone. Others, such as species mentioned in the following paragraph, are able to produce long decay columns within the heartwood. From Table 13.1 Piptoporus portentosus (Plate 13.1) has the widest reported host range of all the fungi associated with heart rot in the butt and major roots of eucalypts in Australia. Also reported from four Australian States and associated with heart rot of the butt in many eucalypts are Phellinus rimosus, Phellinus wahlbergii (Plate 13.2), Postia pelliculosa (Plate 13.3) and Inonotus chondromyelus. For heart rot in the upper stem and major branches (Table 13.2), Piptoporus portentosus has the widest recorded host and geographical range, followed by Piptoporus australiensis (Plate 13.4), Phellinus robustus (Plate 13.5) and Phellinus rimosus, and then by Phellinus wahlbergii and Inonotus chondromyelus.

13.3 The decay process Breaks within the protective bark mantle that expose sapwood and heartwood are the commonest points of entry for decay fungi, which are usually

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saprophytic or weakly parasitic. This entry initiates a complex of interactions which may lead to significant decay of at least part of the tree's stem. Aspects of the decay process are discussed in the following sections.

13.3.1 Infection courts Spaulding (1961) considered that most heart rot fungi were able to invade trees only through wounds. A wound may be superficial, in which case the bark is dislodged and outer sapwood exposed, or it may penetrate into the heartwood. Above ground, unshed dead branches, poorly occluded branch stubs or deep wounds (e.g. fire scars) may expose the heartwood directly to infection. Shallow wounds, such as mechanical injuries caused by forestry operations or animals, may damage the bark and expose the biologically responsive sapwood. Below ground, wounds that expose heartwood are less frequent, and entry into the host depends more on active pathogenesis, as seen with the woody root rot fungi (see Chapter 12). Heart rot fungi have been reported to infect live eucalypts via the following infection courts: 1

scars resulting from either wildfire or prescribed burning (Tamblyn 1937; Greaves et al. 1965; Abbott and Loneragan 1983; McCaw 1983; Perry et al. 1985)

2

dead branches and branch stubs (Tamblyn 1937; Gibson and Waller 1972; Davidson 1974; Edwards 1982; Marks et al. 1982; Wilkes 1985a; Hilton et al. 1989; Wardlaw 1996)

3

branch crotches (Wardlaw 1996)

4

scars from forestry operations such as thinning, pruning, felling and snigging (Tamblyn 1937; Gadgil and Bawden 1981; Marks et al. 1982; Perry et al. 1985; Wilkes 1985a; Hilton et al. 1989)

5

colonised stumps from which coppice is infected (Bottomley and Carlson 1920; Bakshi et al. 1972;Wilkes 1985a)

6

damaged roots (Davidson 1974; Marks et al. 1982; Hilton et al. 1989)

7

wounds caused by insects including longicorn borers and wood moths (Walters 1958; Edwards 1973; Perry et al. 1985; Wilkes 1985a; Wardlaw 1996)

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8

wounds caused by branch abrasion (Wardlaw 1996)

9

scars caused by lightning and sunscorch (Bagchee 1953).

O F

Although not reported for eucalypts, wounds caused by freezing, cankers, mistletoe and animals can be infection courts in some tree species (Bakshi 1964; Bakshi and Singh 1970). The inoculum of any heart rotting fungus reaching an above-ground wound is likely to consist of winddispersed basidiospores or asexual spores. Infection is likely to be controlled by the presence of extractives and other microorganisms in the infection court (Merrill 1970). At the butt or below ground, the inoculum may take the form of spores, mycelium or hyphae aggregated into a strand or rhizomorph. Root contacts also allow ready transfer of a pathogen from an infected to an uninfected tree. There is circumstantial evidence that spores or mycelium, transported as faecal pellets, nest building material or as a surface contaminant, may be introduced into an uninfected host by insects. Webb and Simpson (1991) showed that a range of beetles in Australia consume basidiomes of heart rot fungi, although no attempt was made to prove that these insects act as vectors.

13.3.2 Patterns of decay and tissue responses Decay in stems and roots of eucalypts develops in patterns that reflect the interaction between the microbial populations and host tissues as affected by aeration and moisture loss following wounding. These patterns, at least in eucalypt sapwood, conform to those expected within the framework of the model for compartmentalisation of decay in trees (CODIT) (Shigo and Marx 1977; Shigo 1979). This model proposes that three types of wall restrict the progression of decay in tissues extant at the time of wounding: 1

wall 1 restricts longitudinal spread

2

wall 2 restricts centripetal spread

3

wall 3 restricts tangential spread.

A fourth wall, termed the barrier zone and formed by the vascular cambium, restricts the centrifugal spread of decay into tissues formed after wounding. Compartmentalisation has been noted in several

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eucalypt species following both wounding (including fire damage, branch shedding, mechanical wounds) and active pathogenesis by organisms such as Armillaria (A.) luteobubalina Watling & Kile (Kile 1981; Wilkes 1982, 1985a, 1986a; McCaw 1983; Shearer and Tippett 1988; Mireku and Wilkes 1989; White and Kile 1993, 1994). In heartwood, compartmentalisation may operate but as a more passive response linked to the content, toxicity and location of extractives as well as to physical barriers (Wilkes 1982). The factors that result in consistent patterns of discolouration and decay in living trees are disputed (Boddy and Rayner 1983; Rayner and Boddy 1988). The CODIT model explains the spatial distribution of discolouration and decay by the imposition of barriers to microbial spread. These barriers may include physical features (e.g. wall 2 where rows of high density cells in growth rings may limit centripetal spread, wall 1 where the formation of tyloses and the aspiration of pits limit longitudinal spread), unfavourable biochemical changes in differentiated sapwood (reaction zones) or the formation of anatomically and biochemically modified tissues by the vascular cambium (barrier zone). However, Rayner and Boddy (1988) argue that the formation of reaction and barrier zones in sapwood is open to different interpretations and that aeration following wounding (not wounding per se) is of primary significance in promoting host responses. These barriers are seen as sealant layers limiting aeration and drying, and marking the divide between microenvironmental conditions inhospitable to fungi in water-filled xylem and more favourable conditions for fungal growth in aerated tissues. Therefore, the spread of microorganisms is only indirectly contained by these layers. In eucalypts, the barrier zone is often macroscopically visible as a kino vein (Shigo and Hillis 1973) and shares some features in common with those formed in other hardwood species (Wilkes 1986a). In E. bancroftii, E. dealbata, E. macrorhyncha and E. sideroxylon, barrier zones examined eight months after artificial injury usually contained abundant undifferentiated parenchyma cells and lacked vessels, fibres and identifiable ray cells. Regions of collapsed, undifferentiated cells were often filled with kino. Barrier zone tissues were only weakly lignified and, in the absence of kino veins, the content of hot water extractives was

S TEM

similar to that of sapwood. The development of barrier zones was more evident in the vertical than the lateral direction (Wilkes 1985a, 1986a). The nature of the response of differentiated sapwood to wounding and microbial infection has been studied in only a few eucalypt species. Wilkes (1985d) and Mireku and Wilkes (1988, 1989) identified a zone of intensified physiological activity separating strongly discoloured and infected tissue from clear sapwood in five eucalypt species. In the reaction zone of E. bancroftii, E. dealbata, E. macrorhyncha and E. sideroxylon, abundant formation of tyloses and increased levels of polyphenols were evident compared with adjacent tissues. In Corymbia maculata the concentration of phenols and phenol-oxidising enzymes (peroxidase, tyrosinase, laccase) was higher than in clear or lightly discoloured wood. The discolouration of sapwood was not accompanied by marked increases in moisture content, potassium level or pH, although calcium, magnesium and manganese content were greater than that of clear sapwood. The responsiveness of eucalypt heartwood to decay appears to be variable. In E. microcorys, moisture content, pH and extractives (methanol soluble, hot water soluble, phenolics) decreased during decay and there was no evidence of mineral accumulation or intense discolouration of heartwood in advance of visible decay as has been found in some other hardwood species (Wilkes 1982, 1985c). White and Kile (1993), however, noted extensive discolouration in advance of decay in E. regnans although the chemical and microbial features of such tissue and normal heartwood were not analysed. Following wounding, exposed sapwood dies and may become incorporated into the heartwood as the wound is occluded. Included sapwood (Cummins 1937; Dadswell and Hillis 1962) may provide some heart rot fungi with the inoculum potential to invade heartwood tissue centripetally (Wilkes 1986b). The low decay resistance of such sapwood was attributed to low levels of fungitoxic polyphenols (Wilkes 1985a, 1986b). Although consistent patterns of discolouration and decay are observed in eucalypts, breakdown of barrier zones was observed by Wilkes (1985a) and White and Kile (1994). Disruption of these zones may occur through insect activity, but a more common cause is likely to be mechanical stresses in

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stems and around wounds, particularly those associated with wound-wood development (White and Kile 1994). In E. regnans and E. obliqua, barrier zone breakdown commonly occurred 16 to 18 years after wounding and resulted in significant increases in stem volumes affected by decay fungi which had spread into wood formed after wounding (White and Kile 1994). The time-limited effectiveness of barrier zones has implications for the management of rotation length in stands that may have a high incidence of stem wounds such as those caused by thinning (White and Kile 1991).

13.3.3 Rot types Fungi that decay cell walls and are associated with heart rot may produce brown, white, white pocket or soft rots. Brown rot fungi degrade all wood carbohydrates, including crystalline cellulose, and leave behind a modified lignin matrix (Blanchette 1991). As it dries, brown rotted wood shrinks and cracks across the grain to form cubical structures (Plate 13.6). White rot fungi either simultaneously degrade lignin and other cell wall components or attack lignin preferentially to cellulose (Blanchette 1991). The decayed wood may shrink when dry but it does not crack across the grain. Viewed macroscopically, the white rotted wood may appear spongy (Plate 13.7), stringy or fibrous (indicated in Tables 13.1–13.3 by WR) or contain pockets (Plate 13.8) or streaks (WPR) separated by areas of sound wood (Boyce 1961). Over 75% of the eucalypt heart rot species recorded from Australia (Tables 13.1 and 13.2) and over 80% of those from other countries (Table 13.3) are associated with one of the white rots (WR or WPR). Hardwoods exposed under service conditions and inground field tests tend to be degraded by white rot rather than brown rot fungi (Scheffer 1964; Thornton and Johnson 1988). The genera of white rot fungi most commonly implicated in heart rot of eucalypts are Phellinus and Inonotus in Australia, and Phellinus and Stereum in other countries; the genera of brown rot fungi most commonly implicated are Piptoporus and Postia in Australia, and Laetiporus in other countries (Tables 13.1–13.3). Tamblyn (1937) reported a ‘black straw rot’ of living E. marginata, apparently caused by a basidiomycete, in which ‘large bore holes … run for long distances

325

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down the secondary fibre walls’ in the butt region. However, photomicrographs and drawings in Tamblyn's thesis (1936) indicate that what is now known as a soft rot was involved, probably in concert with a basidiomycete. Later Tamblyn (1944) associated black straw rot with a Stemphylium sp. One of his isolates was recently (G.C. Johnson, unpubl. data) identified as Bispora betulina (Corda) S.Hughes, a species known to produce soft rot in forest products (Duncan and Eslyn 1966).

13.3.4 Microbial interactions leading to decay The development of decay following wounding, particularly of sapwood, may involve microorganisms in a succession or a well-defined pattern of community development, as the conditions within invaded tissues are modified (Rayner and Boddy 1988). The establishment of the dominant decay fungus in eucalypts may also be independent of other microorganisms, as is probably the case with a necrotroph such as A. luteobubalina (see Chapter 12), but for most host and decayer combinations, the nature of these interactions has not been elucidated. For sapwood, the results of Gadgil and Bawden (1981) illustrate the probable complexity of the interactions leading to decay. Only 27% of fungi isolated from pruned branch stubs on four-year-old E. delegatensis were species capable of causing decay. A seasonal pattern was also evident, with fewer decay fungi being isolated from wounds made in winter compared with spring, summer and autumn. In a more detailed study in E. bancroftii and E. macrorhyncha, Wilkes (1987) found Cytospora eucalypticola Van der Westh. and Phialophora bubakii (Laxa) Schol-Schwarz were the pioneer invaders of the injured sapwood, being found at the margins of discoloured wood, while Paecilomyces variotii Bainier was recovered only from older, discoloured wood. The role of these organisms in relation to the establishment of particular decay fungi was not investigated, however. In heartwood, Wilkes and Toole (1987) suggested there were no major synergistic effects with microfungi in the invasion of E. bancroftii and E. macrorhyncha by a Piptoporus species. Although Paecilomyces variotii and Phialophora bubakii were commonly present at the margin of decay, in other cases only the decay fungus was isolated. Similarly,

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Wardlaw (1990a) was able to isolate only Perenniporia medulla-panis from the margin of a white pocket heart rot in E. regnans and E. obliqua. Wilkes and Heather (1983), however, believed microfungi were important in detoxifying heartwood extractives to favour decay by a Polyporus species in E. microcorys. Edwards (1982) isolated a number of pioneer microfungi associated with ‘pencil streak’ discolouration and subsequent decay in the heartwood of several eucalypt species. The initial wood staining (pencil streak) was associated with insect attack. Wilkes (1983a) failed to isolate bacteria from the acidic heartwood of four eucalypt species, suggesting that they are not involved in mediating decay in heartwood. Collectively, these results demonstrate the need for further studies of the microbial interactions involved in the establishment of infection and spread of decay fungi if forest managers are to develop the capacity to minimise decay in managed eucalypt forests through biocontrol strategies.

13.3.5 Rates of decay The rates of defect (discolouration and decay) development were measured in E. regnans and E. obliqua in south-east Australia (Webb 1966; White and Kile 1993, 1994). These species are recognised to have heartwood of low durability (Thornton et al. 1997) and presumably have low resistance to heart rot in the standing tree (Rudman 1964a). Longitudinal rates of defect column extension in the heartwood of these species ranged from 0.18 to 0.44 metres per annum when measured on a range of wound sizes, tree ages and times since wounding. In E. regnans and E. obliqua, defect volume in wounds five to 23 years old increased at a mean rate of 1.7 to 3.4 × 10–3 cubic metres per annum for up to 14 years after wounding, at which time the breakdown of barrier zones led to a rapid increase in defect volume. Time since wounding was the best predictor of defect volume and defect column length (White and Kile 1994). How representative these rates of defect development are for the broader range of commercial eucalypt species is unknown, but they appear comparable with results reported for other tree species (see review in Peace 1962). Rates of wound closure may affect the extent of decay and have been assessed in eucalypts by Perry and Hickman (1987) and White and Kile (1993).

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Initial seasonal differences between treatments tend to disappear with time and in E. regnans rates of circumferential wound wood development of 11 to 15 millimetres per annum were recorded (White and Kile 1993).

13.3.6 Detection of decay No specific methods have been developed for the detection of decay in standing eucalypts. In forestry operations, external indicators of the likely extent of stem decay (fire scars, broken branches, basidiocarps) or empirical tests such as the type of sound when the stem is struck with an axe, may be used to select the most commercially valuable trees. An electrical conductivity meter, the Shigometer, was tested as a means of detecting decay in several eucalypt species (Wilkes and Heather 1982; Wilkes 1983b; Costello and Peterson 1989). Wood condition was correctly predicted in about 55% to 80% of cases, but the disagreement percentage was considered too large for reliable decay detection and care was required in applying the technique. Wilkes and Heather (1983) concluded that some decayinduced changes in eucalypt wood properties may not be reflected in changes in resistance readings. Costello and Peterson (1989) compared the Shigometer with a drilling and a pick test method in E. globulus and E. viminalis. The Shigometer and drilling methods detected decay at a higher proportion of the test points than the pick test. A plant impedance ratio meter (PIRM), which has been used to determine the extent of lesions caused by Phytophthora cinnamomi Rands in E. marginata (Tippett and Barclay 1987), has potential for the detection of decay in stems.

13.3.7 Decay of forest products by heart rot fungi Although based on very limited data, it is generally believed that most heart rot fungi do not survive the conversion of their host into forest products (Tamblyn 1937; Boyce 1961; Highley and Kirk 1979). The product in which heart rot fungi are most likely to survive is the pole. Eslyn (1970) reported that many of the heart rot fungi decaying softwood poles in Canada were species associated with the standing tree. In Australia, N.E.M. Walters (pers. comm.) isolated species of Piptoporus from eucalypt poles whose sapwood had been treated with

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creosote. The Piptoporus species are known to be heart rot fungi of living eucalypts and are unlikely to infect converted timber (Tamblyn 1939). Laetiporus sulphureus, one of the most commonly reported eucalypt heart rot fungi, is considered by May (1962) to be of great economic importance because it not only causes heart rot but is able to continue its growth after the tree is felled. Tamblyn (1944) carried out the only significant study to determine whether eucalypt heart rots were capable of continuing to cause decay after timber was converted and buried in the ground. In sleepersized billets of E. marginata, brown rot associated with at least two fungal species rarely extended beyond the preinstallation decayed zone, even after five years. However, the white rots associated with two fungal species and brown rot associated with another species were able to continue to cause decay in up to 50% of test specimens in moist soil but not in any specimens in dry soil.

13.4 Factors affecting decay development From laboratory and field studies of heartwood cut from a range of eucalypt species, an appreciation has been gained of many of the factors that affect resistance to decay. However, much less is known about the rate of decay and the effect of site, stand and silvicultural factors on the incidence of decay.

13.4.1 Variation in decay resistance The decay resistance of the outer heartwood of oldgrowth eucalypts has been extensively evaluated, with interspecies and intertree variation having been determined by laboratory tests (Da Costa et al. 1962; Da Costa 1979; Johnson et al. 1996) and in-ground field trials (Thornton et al. 1983; Johnson et al. 1986). The tentative durability ratings of 52 eucalypt species given in Thornton et al. (1983) have been confirmed or modified in line with long-term field testing (Thornton et al. 1996, 1997). The durability of eucalypt heartwood is attributed primarily to the deposition of biologically active compounds, particularly polyphenols, during heartwood formation. These compounds, which are fungitoxic, can be extracted with solvents. In general, variation in natural durability depends on the type, quantity and distribution of these extractives. Structural features of mature eucalypt heartwood,

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although significant in preventing decay by some fungi (Da Costa et al. 1962), are relatively unimportant in determining decay resistance (Rudman and Da Costa 1961; Rudman 1964a). The decay resistance rating of eucalypt heartwood varies from non-durable to very durable, depending on the tree species (Da Costa 1949). In relatively durable species, decay resistance is usually greatest at the butt and decreases with height up the stem (Rudman 1964a). Also, the outer heartwood (i.e. wood close to the sapwood–heartwood boundary), containing the greatest concentration of extractives, is more durable than the middle heartwood, which, in turn, is more durable than the heartwood nearest the pith (i.e. inner heartwood) (Rudman 1963, 1964b). In the standing tree, the progressive detoxification of heartwood extractives over time reduces their biological activity and probably accounts for the reduction in decay resistance of the inner heartwood and, in some cases, middle heartwood (Rudman 1963, 1964a, 1964b; Da Costa 1975). This radial variation in durability has given rise to apparent anomalies because, in some cases, the high decay resistance determined in vitro contrasts with losses from heart rot in standing trees (Manion and Zabel 1979; Wilkes 1982, 1985b; van der Kamp 1986; Rayner and Boddy 1988). Whereas the reputation of a highly durable species is generally based on studies of outer heartwood, heart rot generally occurs in the less durable inner heartwood. The only study that compares equivalent heartwood zones in the laboratory with those in live eucalypts is that of Wilkes (1985b). He reported that the species (E. dealbata, E. sideroxylon) which showed the greatest in vitro differences in decay resistance between inner and outer heartwood were those characterised by the most pronounced radial variation in resistance to heart rot in vivo. However, interspecies variations in the rate of extension of heart rot in vivo did not correspond closely with variations in decay resistance in vitro (Wilkes 1985b). Other factors suggested as influencing the development of heart rot in standing trees, and which complicate close comparisons between in vitro and in vivo results, include possible changes (e.g. discolouration) of heartwood in response to microbial invasion, activities of pioneer microorganisms and the degree of tissue aeration and drying. The situation in forests is

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further confounded by the number and size of infection courts and the involvement of a complex community of decay fungi. Da Costa (1949, 1975), Da Costa et al. (1961) and Wilkes (1984) stated that there is a widespread belief that slow-grown wood is more durable than fastgrown wood of the same species. The relevant literature on the effect of growth rate on durability (Findlay 1956; Rudman 1964a) and on the amount of extractives present (Hillis 1987) has been reviewed. While few of the published studies deal with eucalypts and allow us to compare the decay resistance of heartwood from eucalypts with different growth rates, three studies do not support the conventional wisdom. Rudman (1964b) observed that there was no significant difference in decay resistance between E. marginata trees of the same age (> 45 years) but with different growth rates. Similarly, Wilkes (1984, 1985b) noted a negligible effect of growth rate on resistance of heartwood to deterioration in vitro of four species of coppiced eucalypts (40 years old), despite a pronounced positive association between growth rate and extractive accumulation. Wardlaw (1990a) found no significant differences in extractive content or decay resistance of the outer heartwood of 44-year-old plantation-grown E. regnans compared with that of slow-grown E. regnans of comparable age in naturally regenerated forest. Any differences in the decay resistance of young fastgrown or slow-grown trees of the same species could be confounded by the presence of juvenile wood (Rudman 1964a; Wilkes 1984). Juvenile wood, which is low in fungitoxic extractives, surrounds the pith. It is produced by young trees, is associated with low decay resistance (Rudman 1964a; Nelson and Heather 1972) and is characterised by low basic density, short fibre length and thin cell walls. Eucalypts, regardless of rate of their growth, produce juvenile wood for eight to 13 years (Nelson and Heather 1972; W.E. Hillis, pers. comm.) and may not produce mature heartwood until the tree is up to 35 years old (Bamber and Curtin 1974; Wilkes 1984). A higher proportion of the wood in fastgrown than in slow-grown trees is juvenile and hence more susceptible to heart rot (Rudman 1964a; Da Costa 1975). Eucalypts grown rapidly in short rotations may be subject to significant losses due to heart rot because they lack mature heartwood

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rich in fungitoxic extractives (Da Costa 1975; Wilkes 1982, 1985b). Da Costa (1973) suggested that in vitro evaluation of the decay resistance of the first formed heartwood in fast-grown eucalypts could be used as a guide to the susceptibility to heart rots in standing trees and hence for genetic improvement of this characteristic. Heritability of the susceptibility of eucalypts to discolouration and decay has been studied in E. regnans and E. nitens. White et al. (1999) found that heritability estimates for longitudinal extension of discolouration in artificially wounded stems of E. nitens (0.17 ± 0.17) and cross-sectional area affected (0.13 ± 0.16) were similar to estimates of heritability for diameter at breast height (0.19 ± 0.18) in E. nitens and for height and diameter growth in the closely related species E. globulus (Volker et al. 1990). Provenances of E. regnans differed in the degree of spread of decay in the radial and tangential directions but no differences were found in longitudinal spread.

13.4.2 Effect of site, stand and silvicultural factors on decay Studies which relate the incidence of discolouration and decay in eucalypt forests to factors such as soil type, climatic variables, management practices, and age, history and composition of stands are generally lacking. Such studies are important for the future management of eucalypt regrowth forests and plantations, particularly those managed on longer rotations for solid wood products. One of the most consistent relationships demonstrated in the investigations of heart rots in living trees in northern hemisphere forests has been an increase in incidence and volume of decay with stand age (Boyce 1932; Wagener and Davidson 1954). Although eucalypt forests are unlikely to be an exception, timber assessments in Australia have not normally determined decay volumes. Some evidence for increasing volumes of decay with age is suggested by the study of Greaves et al. (1965) in E. delegatensis in New South Wales, where decay caused 13% to 36% of total losses in merchantable volume, with the greatest losses in the oldest (> 90 years) trees. However, although it is known that the incidence of decay in young, fast-growing plantation trees and regrowth stands may also be high (Da Costa 1973), volume losses are generally low (Hardie 1974; Gibson 1975). Although up to

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28% of seven-year-old E. grandis trees in Zambia showed decay, volume losses were less than 0.02% (Ivory 1975). In Brazil, Castro and Krügner (1982) found a decay incidence in E. grandis and E. saligna trees less than 10 years old of 61% and 40%, respectively, although volume losses were small. Wardlaw (1996) recorded that decay in 22-year-old to 34-year-old E. regnans and E. delegatensis varied from 0% to 17.5% of total volume, with a mean of 1.3%. Gadgil and Bawden (1981) estimated that 46% of seven-year-old, pruned E. delegatensis in New Zealand had decay. Davidson (1974) and Lamb et al. (1974) reported that decay was common in four-year-old to 20-year-old stems of E. deglupta in New Britain, Papua New Guinea, and that decay volumes increased with age but were unlikely to affect utilisation, at least for pulpwood. Edwards (1973), referring to work by Humphreys and Bootle, reported significant incidence of heart rot in plantation-grown eucalypts in New South Wales. Humphreys found wood rots in 70% of the E. grandis trees he examined, while Bootle found heart rot prevalent in 20-year-old E. pilularis and E. grandis. Of the E. grandis trees examined in one stand, 90% were affected by heart rot associated with insect larva holes to the extent that economic utilisation of logs from these trees was difficult. Fire damage is one of the major determinants of incidence and extent of decay in many eucalypt forests (Greaves et al. 1965; Perry et al. 1985), but studies relating amount of defect in a stand to its fire history have not been undertaken. McCaw (1983) found a positive correlation in E. marginata between height of decay (and termite attack) in the stem and the size of the original fire scar. High intensity fires cause more physical damage to the stand than do low intensity fires (McArthur 1968; Abbott and Loneragan 1983). Perry et al. (1985) indicated that termite attack in eucalypt heartwood is probably secondary to fungal decay, which in turn often depends substantially on fire scarring. Protection of trees from wildfire through the use of low intensity fuel reduction burns should limit fire scarring and the subsequent decay (Wallace 1966; Perry et al. 1985; Abbott and Loneragan 1986; Wardlaw 1990b). The influence of site factors on the incidence and extent of decay in eucalypts is poorly documented. Davidson (1974) and Lamb et al. (1974) suggested that decay in E. deglupta was greater on poorly than

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on well-drained sites in New Britain. A possible interaction between planting method and site fertility, leading to unusual patterns of root development, weak unions between root and butt increment wood, and root and butt decay, has been observed in some eucalypts in plantations on the North Island of New Zealand (I.A. Hood, pers. comm.). Affected trees are susceptible to windsnap. The organisms that cause decay have not been identified. Another aspect of stand history is the vegetation present before the plantation was developed. The incidence of heart rot in E. grandis in Brazil was greater on sites which previously supported acacia or scrub vegetation than on grassy sites (Castro and Krügner 1982). Eucalypts have a characteristic branch shedding mechanism (Jacobs 1955) which usually results in branch stubs being encased in the stem with minimal defect. According to Jacobs (1955), when a branch of up to 13 to 19 millimetres in diameter becomes moribund, a zone of brittle wood develops near the union of branch and stem. Most of the branch breaks away by a fracture across the outer part of the brittle wood. The remaining stub is ejected after a second fracture across the lower part of this wood. Stub removal, sometimes down to solid stemwood, is caused in part by pressure of stem growth and kino secretions. Dead, unshed branches or branch stubs that have not been completely occluded are important points of entry for decay organisms in eucalypts (Gadgil and Bawden 1981; Marks et al. 1986; White and Kile 1991; Wardlaw 1996) and the interaction between tree vigour and spacing in pure or mixed species stands may be important in determining the incidence and extent of defect through effects on branch shedding. Marks et al. (1986) found that tree spacing in pure stands of E. regnans affected the relationship between mean height and crown depth such that higher stand densities resulted in trees with greater lengths of branch-free boles after age 12 to 15 years. Trees grown at closer spacings also had smaller, more successfully (defect free) encased branch stubs. The probability of defect occurring in the main stem as a result of branch shedding increased rapidly as branch diameters exceeded 10 millimetres and the shedding mechanism became less effective (Marks et al. 1986). Humphreys (reported by Edwards 1973) concluded that reducing branch and knotty core size of E. grandis by silvicultural means (increased

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stocking, postponement of early thinning) reduced the incidence of wood rot and improved log values. Also, observations in fast-growing eucalypt plantations indicate that rapid growth in stem diameter causes the retention of dead branches leading to greater opportunities for the entry of decay organisms (G.A. Kile, unpubl. data; Waugh and Yang 1994). Competition between species of different growth habits may also affect branching and hence defect. There was a significantly greater length of branchfree stem in E. sieberi competing with Acacia verniciflua A.Cunn. than in E. sieberi competing with itself (Marks et al. 1986). On the basis of these results, there are opportunities for silvicultural manipulation of the size of the defect core (the portion of the tree stem containing branch stubs) and the potential volume of decay. Although decay may develop through artificial pruning wounds in eucalypts (Gadgil and Bawden 1981; Glass and McKenzie 1989), the incidence and extent of decay in artificially and naturally pruned stands has not been compared. Dead branches, however, may be a more common entry point for decay fungi than pruned stubs (Gadgil and Bawden 1981). Length of pruning stub, branch diameter, season of pruning and height above ground level of pruned branches may all influence infection and decay development after pruning (Gadgil and Bawden 1981; Glass and McKenzie 1989). The approximate size of the defect core can be predicted (Glass and McKenzie 1989). Regeneration via coppicing may lead to the direct infection of shoots by the decay fungi colonising stumps (Bottomley and Carlson 1920; Tamblyn 1936; Food and Agriculture Organization 1958; Azevedo 1971; Sampaio 1975; Table 13.3). Attempts to prevent Stereum hirsutum from establishing on coppice stumps by coating them with carbolineum and tar, or by burning, failed (Bottomley and Carlson 1920). Bakshi et al. (1972) recommend killing the stumps by application of herbicide and replanting with seedlings. Other silvicultural approaches may minimise the effect of decay. Because the greatest losses to decay are generally associated with older trees, attack by decay fungi may be reduced by shortening the rotation length (Food and Agriculture Organization 1958; van der Westhuizen 1959). Also, volume losses

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to heart rot may be lessened by reducing the growth rate early in the rotation and hence decreasing the volume of the less durable core (Wilkes 1982). Another long-term solution suggested by Wilkes (1982) is to select trees for their ability to compartmentalise wounds. Mireku and Wilkes (1989) reported that wounding of C. maculata sapwood in spring and summer resulted in shorter columns of discolouration and decay, and lower diversity and abundance of invading organisms, than wounding in other seasons. They believe that forest operations such as prescribed burning and thinning are best carried out in seasons when compartmentalisation is most effective. White and Kile (1993) noted that differences in defect development following wounding in different seasons diminished over two years and such effects may not be significant in the long term.

13.5 Particular heart rots and stem conditions Examples of fungi associated with eucalypt heart rots (Fistulina spiculifera, Laetiporus sulphureus) and various stem conditions (‘brown wood’, canker rots, ‘pencilling’) are described in the following sections. Each condition was chosen because of its widespread occurrence and likely economic significance or because it illustrates aspects of the biology of a heart rot fungus in eucalypts.

13.5.1 Pencilling and decay associated with Fistulina spiculifera Fistulina hepatica causes the heartwood of certain Quercus spp. to turn reddish brown, thereby producing a material (‘brown oak’) considered highly desirable for decorative woodwork (Cartwright 1937). Brown oak is believed to be characteristic of a stage in the slow development of the heart rot, especially in overmature trees (Cartwright and Findlay 1946). Boyce (1961) reports that the decay develops so slowly that it rarely produces the cubical cracking and softness typical of most brown rotted timber. Furthermore, even after year-long laboratory bioassays of sterilised oak blocks, little decay is found (Cartwright and Findlay 1946). The related fungus, Fistulina spiculifera (Tables 13.1, 13.2, Plate 13.9), is believed to cause a very common condition known as pencilling in the heartwood

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(and occasionally sapwood) of E. marginata (Tamblyn 1937). On a transverse face, the pencilling is seen as a dark streak of pencil-line thickness running radially (Tamblyn 1936). Tamblyn forwarded samples of pencilled E. marginata to W.P.K. Findlay in England who compared it with brown oak. Findlay concluded that pencilling was very likely to be the early stage of a slowly developing rot caused by Fistulina spiculifera (then known as Fistulina hepatica). We believe that the rot known as ‘black stringy rot’ is caused by the combined attack of Fistulina spiculifera and a soft rotting microfungus. Because of the latter, the rot produced is so unlike that seen in oak that Tamblyn (1936) felt only a tentative association between black stringy rot and Fistulina spiculifera was justified. Such conservatism was not shown by Rothberg (1937, 1938) who, after isolating fungi from decayed E. marginata, expressed the view that what we now know as Fistulina spiculifera was responsible for heart rot. M.H. Pearce (pers. comm.) noted Fistulina spiculifera actively fruiting on dead E. marginata stumps and N.E.M. Walters (pers. comm.) observed that the fungus was associated with heartwood not sapwood. We are not aware of any studies in which Fistulina spiculifera has been inoculated into sound E. marginata. Such a study would be complicated by the large proportion of trees of this species already colonised by this fungus and by the very slow rate of decay, which in oak is checked once the wound heals over (Cartwright and Findlay 1946). Several year-long bioassays of E. marginata heartwood with Fistulina spiculifera failed to show that the fungus could cause decay in vitro (Rothberg 1938; G.C. Johnson, unpubl. data). Merrill (1970) considers the inability of a fungus to decay sound wood in vitro to be a characteristic of a true heart rot fungus. Despite these and other failures to demonstrate the ability of the fungus to cause decay under controlled conditions, it is generally considered that Fistulina spiculifera produces brown rot of several hardwoods (Rothberg 1937; Roth and Sleeth 1939; Cartwright and Findlay 1946; Gilbertson and Ryvarden 1986; J.A. Simpson, pers. comm.). Thus, we feel justified in including Fistulina spiculifera in Tables 13.1 and 13.2 as being associated with heart rot in E. marginata and other eucalypts.

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Cartwright and Findlay (1946) stated that in oak ‘there is no evidence to show that Fistulina hepatica can continue its activity in converted timber’. However, Rothberg (1938) was able to isolate the closely related Fistulina spiculifera from E. marginata 22 weeks after it was felled, and G.C. Johnson (unpublished) isolated this fungus from E. marginata poles installed at least 10 years previously.

13.5.2 ‘Brown wood’ of Eucalyptus diversicolor ‘Brown wood’ is the name given to heartwood of karri (E. diversicolor) discoloured, at the incipient decay stage, by white rot or white pocket rot fungi (Plate 13.10). The role, if any, of brown rot fungi has yet to be determined. Thus far, Stereum hirsutum, a Hymenochaete species and several as yet unidentified fungi are able to cause brown wood. Stereum hirsutum produced brown wood within six months of heartwood inoculation and white rot within two years. Natural infections leading to brown wood are associated with branch stubs, gum rings and insect damage (Davison and Tay 1990; Hewett and Davison 1995). Brown wood was recognised in mature karri in the 1950s, but was probably not common. Donnelly et al. (1994) indicated that the incidence of sawlogs with either brown wood or decay was significantly greater in thinnings of 50-year-old regrowth stands than in sawlogs from mature stands. Moreover, sampling in 12-year-old to 14-year-old regrowth karri showed that in some stands brown wood and decay occurred in 83% of the dominant and codominant trees, whereas only 28% of the subdominant and suppressed trees were affected (Hewett and Davison 1995). Volume affected was not determined. Studies were also carried out to determine the natural durability of brown wood. When exposed to in-ground contact, brown wood is significantly less durable than unaffected karri heartwood (i.e. wood without brown wood) (Johnson and Thornton 1992).

13.5.3 Laetiporus sulphureus Laetiporus sulphureus, a Basidiomycota with a broad geographical distribution (Spaulding 1961; van der Westhuizen 1975), is associated with brown rot of the heartwood (heart and butt rot) of a wide range of softwoods and hardwoods (Hepting 1971).

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The fungus produces large basidiomes (up to 40 cm wide) with an orange to lemon-yellow pileus (Gilbertson and Ryvarden 1986). Spaulding (1961) and Sampaio (1975) consider the fungus to be a parasite that invades trees through wounds that expose inner living tissues. In most cases, Laetiporus sulphureus is associated with heartwood rot at the butt or near the base of the stem (Bonar 1942; Magnani 1964; Berry 1982; Costello and Peterson 1989; Kim et al. 1991). In the only Australian report of this fungus on eucalypts, it was associated with heartwood rot in the upper trunk and major branches (Table 13.2). Gibson (1975) considers Laetiporus sulphureus to be one of the few heart rots ‘that seem to have achieved some importance’ in eucalypts as exotics. This point of view is supported by observations that in the space of a few years the rot may bring about the death of the attacked trees (Sampaio 1975) and that the fungus is able to continue its growth after the tree is felled (May 1962). Unfortunately, there are few data on the proportion of the stand or log volume affected. Van der Westhuizen (1959) reported that eight-year-old E. saligna trees were free of heart rot but that 37-year-old trees had lost 5% of total sawn volume.

13.5.4 Canker rot Canker rots, caused by repeated localised killing of the vascular cambium and bark by wood decay fungi, eventually produce a concentric lesion and decayed wood. Although known to afflict eucalypts (Shigo 1986), their incidence, origin and causal organisms are poorly known. It is likely that some of the fungi mentioned in Tables 13.1 to 13.3 cause canker rots. Phellinus robustus is one such species (Plate 13.11).

13.6 Conclusion In 1937 Tamblyn lamented that in Australia ‘many of our heart rot fungi are endemic and their biology unknown’. This situation remains largely unchanged as indicated by Wilkes’ (1982) statement that ‘the gaps in our knowledge are countless’. In particular, we lack comprehensive information on the identity of the fungi causing heart rot, their economic effect, the principles of rot establishment and development, and the silvicultural or other methods needed to manage them.

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The nature of the concern about the effect of stem decay is, however, changing. Tamblyn's (1937) perspective was from the effect of decay on timber recovery from large trees in old growth forests. In native forest management in Australia today, a major issue emerging is the effect of decay on the recovery rate and quality of products from the smaller trees harvested from regrowth forests after 50-year to 100-year rotations. In addition, commercial thinning in regrowth stands to increase the recovery of merchantable wood and accelerate the growth of residual crop trees may, through stem damage, further increase the volumes of discoloured and decayed wood. In other countries where eucalypts generally have been harvested on very short rotations (7–15 years), mainly for pulp or fuelwood, there is some developing interest in longer rotations to produce larger trees for conversion to solid wood products. Losses to stem decay may be more important in these circumstances. In all these situations, greater emphasis will be placed on producing the maximum volumes of clear wood, which will lead to renewed interest in minimising eucalypt stem decay through management practices, breeding and biological control.

13.7 Acknowledgments With forest pathologists already carrying heavy workloads, one might have expected limited assistance from them in the production of this chapter. On the contrary, colleagues were enthusiastic and generous in providing information and data (much of it not previously published), photographs and constructive comments. We gratefully acknowledge N.F.S. Azevedo, Estacao Florestal Nacional-INIAER, Portugal; E.M. Davison, Curtin University of Technology, Western Australia; the late D.W. Edwards, State Forests of New South Wales; R.N. Hilton (retired), University of Western Australia; I.A. Hood, New Zealand Forest Research Institute; M.A. Pearce, formerly of CSIRO Forestry and Forest Products; R. Robinson, Western Australia Department of Conservation and Land Management; J.K. Sharma, Kerala Forest Research Institute, India; J.A. Simpson, State Forests of New South Wales; the late J.W. Tierney, Queensland Forest Service; N.E.M. Walters (retired), CSIRO Forestry and Forest Products; and T.J. Wardlaw, Forestry Tasmania. In particular, we wish to express our appreciation to J.A. Simpson for providing unpublished information

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on fungi associated with heartwood rot of living eucalypts, both in Australia and other countries. We are also grateful to E.M. Davison, B.A. Fuhrer, S. Morton, and T.J. Wardlaw for superb photographs.

13.8 References Abbott, I. and Loneragan, O. (1983). Influence of fire on growth rate, mortality and butt damage in Mediterranean forest of Western Australia. Forest Ecology and Management 6, 139–153. Abbott, I. and Loneragan, O. (1986). Ecology of jarrah (Eucalyptus marginata) in the northern jarrah forest of Western Australia. Bulletin Number 1. (Western Australia, Department of Conservation and Land Management: Perth.) Arentz, F. and Simpson, J.A. (1989). Root rot diseases of exotic plantation tree species in Papua New Guinea. In Proceedings of the 7th IUFRO International Conference on Root and Butt Rots, Vernon and Victoria, British Columbia, 1988. (Ed. D.J. Morrison) pp. 83–91. (Forestry Canada: Victoria, British Columbia.) Azevedo, N.F.S. (1971). Forest Tree Diseases. (Laboratorio de Patologia Florestal. Secretaria de Estado da Agricultura Direcção Geral des Serviços. Filorestais e Aquicolas: Oeiras, Portugal.) Bagchee, K. (1953). New and noteworthy diseases in India. The sap and heartrot diseases of Eucalyptus maculata Hook., var. citriodora Bailey due to the attack of Trametes cubensis (Mont.) Sacc. Indian Forester 79, 341–343. Bakshi, B.K. (1964). Known and potential hazards from stem diseases—heart rots. In Diseases of Widely Planted Forest Trees, FAO/IUFRO Symposium on Internationally Dangerous Forest Diseases and Insects, Oxford, July, 1964. (USDA Forest Service: Washington, DC.) Bakshi, B.K. and Singh, S. (1970). Heart rots in trees. International Review of Forest Research 3, 197–251. Bakshi, B.K., Puri, Y.N., Sharma, R.P., Singh, S. and Singh, B. (1956). New and noteworthy diseases of trees of India. Indian Forester 82, 449–454. Bakshi, B.K., Ram Reddy, M.A., Puri, Y.N. and Singh, S. (1972). Survey of the diseases of important native and exotic forest trees in India. Final Technical Report 1967–1972. (Forest Research Institute: Dehra Dun, India.) Bamber, R.K. (1985). The wood anatomy of eucalypts and papermaking. Appita 38, 210–216. Bamber, R.K. and Curtin, R.A. (1974). Some properties of wood in blackbutt trees of two ages. Australian Forestry 36, 226–234. Baxter, D.V. (1967). Disease in Forest Plantations: Thief of Time. Bulletin 51. (Cranbrook Institute of Science: Bloomfield Hills, MI, USA.)

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Berry, F.H. (1982). Butt rot in oak in the central hardwood region. Phytopathology 72, 958. Blanchette, R.A. (1991). Delignification by wood-decay fungi. Annual Review of Phytopathology 29, 381–398. Boddy, L. and Rayner, A.D.M. (1983). Origins of decay in living deciduous trees: the role of moisture content and a re-appraisal of the expanded concept of tree decay. New Phytologist 94, 623–641. Bonar, L. (1942). Studies on some California fungi. II. Mycologia 34, 180–192. Bottomley, A.M. and Carlson, K.A. (1920). Parasitic attack on Eucalyptus globulus: a note on Stereum hirsutum in plantations in the Transvaal. Bulletin Number 3. (Union of South Africa Forests Department: Pretoria.) Boyce, J.S. (1932). Decay and other losses in Douglas Fir in Western Oregon and Washington. US Department of Agriculture, Technical Bulletin Number 286. Boyce, J.S. (1961). Forest Pathology. 3rd edn. (McGrawHill: New York.) Browne, F.G. (1968). Pests and Diseases of Forest Plantation Trees. An Annotated List of the Principal Species Occurring in the British Commonwealth. (Clarendon Press: Oxford.) Cartwright, K.T. StG. (1937). A reinvestigation into the cause of ‘brown oak’, Fistulina hepatica (Huds.) Fr. Transactions of the British Mycological Society 21, 68–83. Cartwright, K.T. StG. and Findlay, W.P.K. (1946). Decay of Timber and its Prevention. (Department of Science and Industrial Research, His Majesty's Stationery Office: London.) Castro, H.A. and Krügner, T.L. (1982). Incidéncia de apodrecimento de cerne em árvores vivas de Eucalyptus na regiao de GuaÌba – RS. Summa Phytopathologica 8, 3–11. Castro, H.A. and Krügner, T.L. (1984a). Avaliaçao da capacidade de apodrecimento de cerne por himenomicetos isolados de árvores vivas de Eucalyptus spp. na Regiao de GuaÌba, RS. Fitopatologia Brasileira 9, 233–239. Castro, H.A. and Krügner, T.L. (1984b). Microorganismos associados á podridao do cerne de árvores vivas de Eucalyptus spp. na regiao de GuaÌba, RS. Fitopatologia Brasileira 9, 227–232. Cleland, J.B. (1934–35). Toadstools and Mushrooms and Other Larger Fungi of South Australia. Parts I and II. Handbooks Committee, Adelaide. Reprinted 1976. Costello, L.R. and Peterson, J.D. (1989) Decay detection in Eucalyptus: an evaluation of two methods. Journal of Arboriculture 15, 185–188. Cummins, J.E. (1937). ‘Included Sapwood’ in karri (E. diversicolor). Journal of the Council for Scientific and Industrial Research 10, 29–32. Cunningham, G.C. (1965). Polyporaceae of New Zealand. Bulletin 164. New Zealand Department of Science

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and Industrial Research. (Government Printer: Wellington, NZ.) Da Costa, E.W.B. (1949). The decay resistance of Australian timbers. Commonwealth Scientific and Industrial Research Organisation, Forest Products Newsletter 175, 1–2. Da Costa, E.W.B. (1973). Natural durability and heart rots. Sixteenth Forest Products Research Conference, Melbourne. Topic 1/15: 1–2. (CSIRO Division of Forest Products: Melbourne.) Da Costa, E.W.B. (1975). Natural decay resistance of wood. In Biological Transformations of Wood by Microorganisms. (Ed. W. Liese) pp. 103–117. (Springer-Verlag: Berlin.) Da Costa, E.W.B. (1979). Comparative decay resistance of Australian timbers in accelerated laboratory tests. Australian Forest Research 9, 119–135. Da Costa, E.W.B., Rudman, P. and Gay, F.J. (1961). Relationship of growth rate and related factors to durability in Tectona grandis. Empire Forestry Review 40, 308–319. Da Costa, E.W.B., Rudman, P. and Deverall, F.J. (1962). Inter-tree variation in decay resistance of karri (Eucalyptus diversicolor F. Muell.) as related to colour, density and extractive content. Journal of the Institute of Wood Science 10, 48–55. Dadswell, H.E. and Hillis, W.E. (1962). Wood. In Wood Extractives and Their Significance to the Pulp and Paper Industries. (Ed. W.E. Hillis) pp. 3–55. (Academic Press: New York.) Davidson, J. (1974). Decayed wood in living trees of Eucalyptus deglupta Blume. Tropical Forestry Research Note SR. 18, Papua New Guinea (Department of Forests: Boroko, Papua New Guinea.) Davison, E.M. and Tay, F.C.S. (1990). Brown wood in karri. Interim report. (Department of Conservation and Land Management: Como, WA.) Donnelly, D.J., Rule, R. and Davison, E.M. (1994). Incidence of brown wood (incipient rot) and rot in regrowth karri: comparison of medium and first grade sawlogs. Unpublished report. (Department of Conservation and Land Management: Como, WA.) Duncan, C.G. and Eslyn, W.E. (1966). Wood-decaying Ascomycetes and Fungi Imperfecti. Mycologia 58, 642–645. Edwards, D.W. (1973). Defects of fast-grown eucalypts in New South Wales, Australia. Proceedings IUFRO Division 5 Meeting 2, South Africa. pp. 256–270. (IUFRO: Cape Town, South Africa.) Edwards, D.W. (1982). Pencil streak, stain and decay in Eucalyptus and Syncarpia in New South Wales. Research Paper Number 1. (Forestry Commission of New South Wales: Sydney.) Eslyn, W.E. (1970). Utility pole decay. Part II. Basidiomycetes associated with decay in poles. Wood Science and Technology 4, 97–103.

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D ISEASES OF E UCALYPTS A SSOCIATED WITH V IRUSES , P HYTOPLASMAS , B ACTERIA AND N EMATODES

14

T.J. Wardlaw, G.A. Kile and J.C. Dianese

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U M M A R Y

Very few diseases of eucalypts have been associated with viruses, phytoplasmas, bacteria or nematodes. In most cases the causal role of viruses and phytoplasmas associated with disorders of eucalypts has not been proven conclusively. Only bacterial wilt caused by Ralstonia solanacearum in Brazil is an important disease for which the causal agent has been clearly established. This disease killed up to 17% of eucalypt seedlings within six months of planting in certain areas. The particular biotype of Ralstonia solanacearum pathogenic on eucalypts in Brazil is not known to be present in Australia. Very few nematodes associated with eucalypts have been shown to cause serious damage. Nematodes of the genus Fergusobia, together with the fly Fergusonina, are associated with disease of the above-ground parts of eucalypts.

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14.1 Introduction

E U C A L Y P T S

6

The first report of a suspected virus disease of eucalypts in Australia identified spherical particles in the sap of young nursery-grown trees of E. macrorhyncha with mosaic symptoms (Brzostowski and Grace 1974). No attempt was made to transmit the disease to healthy plants.

7

Guy (1982) was the first to attempt to obtain evidence of viral diseases of eucalypts in their natural habitat. He examined a number of species of eucalypts, collected from throughout mainland Australia, which had symptoms of mosaic, chlorosis, stunting or witches’ broom (Plate 14.1). Three of the pathogens were transmitted in sap or by grafting and produced symptoms in healthy indicator plants (Table 14.1). Similar symptoms were observed on C. gummifera in Brazil (Plate 14.2).

The taxonomically diverse pathogens considered in this chapter cause a range of diseases. They have been grouped together because they are poorly known and are as yet generally minor pathogens of eucalypts when compared with the fungi. The literature on diseases of eucalypts associated with viruses, phytoplasmas, bacteria and nematodes reflects recent knowledge, with 70% of reports occurring only in the last two decades. Most of these reports are from situations where the eucalypts are being grown as exotics; there is almost no knowledge of these diseases in native stands.

14.2 Virus-like diseases 14.2.1 Earlier reports There have been seven published reports of possible viral diseases in eucalypts, as follows. 1

A graft transmissible disease that caused chlorosis and stunting of nursery seedlings of Eucalyptus propinqua and, to a lesser extent, E. saligna, Corymbia citriodora and C. maculata in Argentina (Fawcett 1941).

2

A graft transmissible disease that produced symptoms of mosaic, microphylly, leaf asymmetry and witches’ broom in E. camaldulensis (reported as E. rostrata) in Sardinia (Foddai and Marras 1963).

3

A sap transmissible mosaic disease of one-year-old to two-year-old nursery seedlings of C. citriodora in India (Sastry et al. 1971). The virus associated with this disease was thought to belong to the tobacco mosaic group based on host range and physical attributes. The authors also described little leaf and leaf crinkle symptoms in C. citriodora which were graft transmissible.

4

Mosaic, leaf curl and leaf spot symptoms on E. tereticornis which could not be transmitted to healthy plants by grafting (Sharma et al. 1985).

5

A stunt disease in seedlings and saplings of E. deglupta in the Philippines (Anino 1987). Sap transmission to Chenopodium amaranticolor H.J.Coste & A.Reyn. provided evidence that a virus might be involved.

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14.2.2 Difficulties in purifying viruses from eucalypts A major impediment to proof of causation has been the difficulty of purifying viral particles from the sap of eucalypts. The attempts of Brzostowski and Grace (1974) from leaf sap of E. macrorhyncha were unsuccessful possibly because the particles were precipitated by sap constituents. This is consistent with the work of Guy (1982) who showed that acidity, high phenolic content and the presence of certain protein fractions in the leaf sap of E. globulus ssp. bicostata inhibited transmission of galinsoga mosaic virus (GMV) and tobacco necrosis virus (TNV) to Phaseolus vulgaris L. The antiviral activity of extracts of eucalypts demonstrated by Tripathi and Tripathi (1982) provides some indirect evidence of the involvement of viruses. The inhibitory effects of eucalypt sap might be reduced by dilution, buffering, chemical inactivation and precipitation techniques.

14.2.3 Role of vectors None of the above putative viral diseases of eucalypts has been shown to be transmitted by a vector. Anino (1987) suspected that insect transmission was responsible for the natural spread of stunt disease in plantations of E. deglupta as neither graft nor sap transmission of the pathogen was successful. Many viruses of trees are confined to, or occur in highest concentrations in, root tissue (Nienhaus and Castello 1989). Root extracts of E. globulus ssp. bicostata were found to be less

D IS EASES

OF

TAB LE 14 . 1

E UCAL YPTS A S S OCIATED

W ITH

V IR US E S , P HY TOPLA SMA S , B A CTE RIA

A ND

N EMA TODE S

C H A P T E R

14

Graft and mechanical transmission of suspected virus symptoms in three eucalypt (Corymbia and Eucalyptus) species (after Guy 1982)

Host

Symptoms

Method of transmission

C. ficifolia

Leaf chlorosis

Graft

Indicator species testing positive

Symptoms on test plant (proportion of successful transmissions)

C. calophyllaA

Leaf chlorosis (2/6)

B

C. gummifera

Interveinal chlorosis Leaf sap

E. amplifolia

C. gummifera

Interveinal chlorosis Leaf sap

Gossypium hirsutum L.C

Systemic vein clearing

C. gummifera

Interveinal chlorosis Leaf sap

Godetia amoena G.Don

Faint systemic mottle

E. cloeziana

Vein clearing

Phaseolus aureus Roxb.

Flecks of vein clearing (1/11)

Leaf sap

Systemic flecking, leaf distortion (2/19)

E. cloeziana

Vein clearing

Root sap

E. cloeziana

Vein clearing (2/38)

E. cloeziana

Vein clearing

Graft

E. cloezianaD

Vein clearing (1/9)

A

Four inoculated trees each of C. calophylla, E. tetragona and C. tessellaris remained symptomless. Six inoculated trees each of E. tenuipes and C. tessellaris remained symptomless, no virus-like particles observed in sap from symptomatic plants, and symptoms could not be transmitted from graft inoculated C. calophylla to herbaceous test plants. C Symptomatic leaves contained virus-like particles about 30 nanometres in diameter. D Symptoms could be transmitted from symptomatic Gossypium hirsutum to healthy Gossypium hirsutum. In none of the above cases was there conclusive evidence that the disease was caused by a virus. In particular, there was no demonstrated pathogenicity of purified viral inoculum. Guy (1982), however, showed that cotyledons of four species of eucalypt were susceptible to infection when inoculated with purified preparations of known viruses. He transmitted tobacco necrosis virus (TNV) to cotyledons on young seedlings of C. calophylla and C. gummifera, causing necrotic local lesions, and cacao yellow mosaic virus (CoYMV) to E. cloeziana, C. gummifera and E. howittiana, causing latent infections. B

inhibitory to the transmission of GMV and TNV, both of which are soilborne, than were extracts of leaves or flowers (Guy 1982). Clearly, any future attempts to mechanically transmit viruses from eucalypts should include root extracts.

14.2.4 Importance and prognosis The incidence of suspected viral diseases in eucalypt populations is within the range of 1% to 5% of trees being affected (Sastry et al. 1971; Guy 1982). While the incidence of stunting increased to 16% in a plantation of four-year-old E. deglupta in the Philippines and resulted in a 50% reduction in height and diameter growth of affected trees, the total effect was considered to be not economically important (Anino 1987). The effect of apparent viral disease in eucalypts may be transitory and often decreases with age. Symptoms of ‘mosaic’ in C. citriodora disappeared once plants reached four to five years old, and the disease was no longer transmissible (Sastry et al. 1971). Similarly three putative virus diseases observed in Australia were less severe in older plants and in mature foliage (Guy 1982). Viruses may contribute to plant decline in diseases of complex etiology, as has been suggested for other forest species (Nienhaus 1985). Such a role for viruses has not been demonstrated in any eucalypt

dieback syndrome of complex etiology in Australia (Podger et al. 1980; Palzer 1981, 1983, 1990; see Chapter 17). Unless significant effects can be demonstrated as a result of an outbreak of a particular viral disease, it is unlikely that our knowledge of such diseases in eucalypts will increase greatly in the near future.

14.3 Diseases associated with phytoplasmas 14.3.1 Occurrence and etiology Disease in eucalypts associated with phytoplasmas (formerly known as ‘mycoplasma-like organisms’— MLOs) is consistently described as general plant stunting and an extreme reduction in leaf size (microphylly), giving rise to the name ‘little leaf disease’. The lamina of affected leaves becomes thinner and narrower, and more brittle, glabrous and chlorotic. Internodes are shorter and axillary bud activity is stimulated, resulting in a bushy, witches’ broom habit (Plate 14.3). Flowers are sterile and reduced in size (Ghosh et al. 1985; Dafalla et al. 1986). Trees may also show yellowing, stunting and dieback, and may decline and die prematurely (Nayar and Ananthapadmanabha 1977; Ghosh et al. 1984; Marcone et al. 1996). No visible abnormalities

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were evident in the roots of affected seedlings of E. tereticornis, E. grandis and E. globulus (Sharma et al. 1983). Little leaf and witches’ broom in eucalypts has been reported from Australia (Palzer 1983), China (Zhing et al. 1982), India (Sastry et al. 1971; Sharma et al. 1983; Ghosh et al. 1984, 1985), Italy (Ragozzino and Cristinzio 1980; Marcone et al. 1996, 1997), the Sudan (Dafalla et al. 1986), Syria (Bos et al. 1990) and Taiwan (Wang 1992). Symptoms described from the different geographical regions and eucalypt species are basically similar. Sastry et al. (1971) were first to demonstrate the biotic nature of little leaf disease of eucalypts in India by transmitting the disease through grafts from diseased to healthy C. citriodora. However, they thought the pathogen was a virus. Sharma et al. (1983), Ghosh et al. (1984) and Ali et al. (1987) provided indirect evidence that a phytoplasma caused the disease when they found histopathological and cytopathological aberrations of phloem tissue of diseased eucalypts using light and fluorescence microscopy. Using transmission electron microscopy, Ali et al. (1984) found a phytoplasma in the phloem of affected plants. The reports by Nayar and Ananthapadmanabha (1977) and Dafalla et al. (1986) of the presence of pleomorphic bodies bound by a tripartite unit membrane in the sieve elements of diseased E. grandis and E. microtheca, respectively, confirmed the association of a phytoplasma with little leaf disease. Palzer (1983) noted that some declining shoots of E. obliqua with ‘regrowth dieback’ in Tasmania had little leaf and witches’ broom-like symptoms. Attempts to transmit disease from witches’ broom and dieback affected shoots of E. obliqua to Catharanthus roseus (L.) G.Don (syn. Vinca rosea L.) occasionally resulted in rapid wilting, phloem collapse and death of the test plants within three to six weeks of grafting (T.J. Wardlaw and C. Palzer, unpubl. data). These symptoms could not be explained by the presence of any fungal or bacterial pathogen and appeared similar to those ascribed to Spiroplasma citri (Saglio et al. 1973) by Calavan and Oldfield (1979). However, no evidence of a pleomorphic phytoplasma or spiroplasma was detected in diseased plants. Similarly, examination by light, fluorescence and transmission electron microscopy failed to demonstrate the presence of a

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phytoplasma in shoots of E. obliqua with witches’ broom (T.J. Wardlaw and C. Palzer, unpubl. data). A phytoplasma in eucalypts (possibly E. robusta and E. rudis) in Italy associated with little leaf and witches’ broom symptoms was identified using polymerase chain reaction (PCR) assays as a member of the the elm yellows group and was named the eucalypt little leaf (ELL) phytoplasma (Marcone et al. 1996). The same phytoplasma was found in several trees and was present in both root and stem tissues. Phytoplasmas were not detected with fluorescence microscopy of sections of petioles, shoots, branches or roots stained with 4'-6-diamidino-2-phenylindole (DAPI), nor with direct PCR using universal and group-specific phytoplasma primers. However, phytoplasma DNA was detected when the initial amplification products were reamplified with universal or group-specific nested primers. No phytoplasmas were detected in trees showing yellowing and decline that did not also show little leaf and witches’ broom symptoms. The host specificity of ELL remains to be determined and while symptoms on eucalypts in Italy were similar to those described from India, China and the Sudan, this does not allow the conclusion that all little leaf diseases in eucalypts are caused by ELL. Similar symptoms may be induced by several other phytoplasmas (Marcone et al. 1996). As with virus diseases of eucalypts, the causal role of a phytoplasma in little leaf disease of eucalypts has not been proven conclusively. However, the remission of symptoms following tetracycline therapy has often been used to demonstrate the link between phytoplasmas and plant disease (Nienhaus and Sikora 1979). Temporary remission of little leaf symptoms has been demonstrated in E. tereticornis and E. grandis following treatment with tetracycline (as oxytetracycline hydrochloride or tetracycline hydrochloride), and the presence of phytoplasma in the sieve elements of diseased plants and their absence in healthy plants has also been demonstrated by transmission electron microscopy (Ghosh et al. 1985; Ali et al. 1987; Balasundaran et al. 1988). A disease suspected to be due to phytoplasma in two-year-old to three-year-old Eucalyptus hybrid plants was supressed by antibiotic sprays (Dhanda and Bansal 1983). Nayar and Ananthapadmanabha (1977) suggest that the phytoplasma which causes the sandal spike

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disease of sandalwood (Santalum album L.), a shrubby hemiparasite on the roots of many other tree species including eucalypts, may be the same as that associated with little leaf disease of E. grandis. The primary pathogenic role of the now characterised Mycoplasma sp. in causing spike disease of sandalwood has been demonstrated (Nayar 1984).

eventually affect the entire tree (Plate 14.5). The syndrome was first observed in 1973 by G. Cotton and in recent years has been observed widely in temperate Australia (see Chapter 19). Preliminary studies using DNA probes indicate that the disease may be caused by a phytoplasma (Randles 1999). Virus-like particles but not phytoplasmas have been observed by electron microscopy.

14.3.2 Effect and importance

14.4 Diseases caused by bacteria

Although little leaf disease occurs widely, its incidence is low. Sastry et al. (1971) observed an incidence of 3% to 5% in four-year-old to five-year-old plantings of C. citriodora. The incidence was less than 1% in one-year-old to five-year-old plantations of E. tereticornis, E. grandis and E. globulus and nursery crops of E. tereticornis and E. grandis (Sharma et al. 1983). A low incidence was also reported in E. grandis, E. eugenioides and E. microtheca (Ghosh et al. 1984; Dafalla et al. 1986). The incidence of eucalypts with symptoms in the field has been reported to fluctuate from season to season. Balasundaran et al. (1988) reported ‘spontaneous remission of little leaf’ of E. tereticornis following dry summers, only to see the disease reappear in moist seasons. In Zambia, I.A.S. Gibson (cited in Ghosh et al. 1985) observed natural recovery of young eucalypts with little leaf in the field.

Only three bacterial species have been recorded as pathogens of eucalypts and they are uncommon. Wilt caused by Ralstonia solanacearum (Smith 1896) Yabuuchi et al. 1995 [syn. Pseudomonas solanacearum Smith (1896) Smith 1914, Burkholderia solanacearum (Smith 1896) Yabuuchi et al. 1993; Yabuuchi et al. 1995] has been significant in newly established plantations in Amazonian Brazil. Crown gall caused by Agrobacterium tumefaciens (Smith & Townsend 1907) Conn 1942 and shoot blight caused by Xanthomonas campestris (Pammel 1895) Dowson 1939 pv. eucalypti (Truman 1974) Dye 1978 are considered to be of only minor or sporadic, local importance. Bacterial wilt and crown gall appear to be new encounter diseases that have arisen as eucalypt species have been moved from their natural habitats to new environments.

Because of the low incidence and effect of diseases of eucalypts associated with phytoplasmas, strategies to control them have not received much attention. Nayar and Ananthapadmanabha (1977) suggest that any measure to control sandal spike disease in commercially valuable sandalwood should also consider control of the disease in the plants, including eucalypts, which are parasitised by the sandalwood. Variation in susceptibility to little leaf disease between provenances of E. tereticornis has been reported (Sharma et al. 1983). The use of less susceptible species or provenances could reduce the effect of the disease.

The most important bacterial disease affecting eucalypt species is wilt caused by Ralstonia solanacearum in tropical regions. Death rates of up to 16% of plants within six months of transplantating have been reported on sites in Brazil infested with the bacterium (Table 14.2). Pathogenicity of the bacterium has been demonstrated by fulfilment of Koch’s postulates using several methods of inoculation (Dianese et al. 1990).

14.3.3 Mundulla yellows There has been much interest in a disorder of eucalypts in south-east South Australia in which the leaves turn yellow in a characteristic pattern (Plate 14.4) and dieback develops in the tree, ultimately leading to mortality. Symptoms may develop on only one or a few branches on a tree and

14.4.1 Bacterial wilt

The degree of specificity to eucalypts of races and biovars within Ralstonia solanacearum remains to be determined. Although disease has been linked to biovars 1 (Brazil) and 3 (Australia, China), artificial inoculation with isolates of biovars 2 and 3 resulted in wilt and death of E. grandis in Brazil (Dianese and Dristig 1993). Isolates of biovar 1 from eucalypts in Brazil were also pathogenic to tomato, pepper and eggplant. Investigation of the occurrence of the pathogen in native forests in Australia and the pathogenicity on eucalypts of the Australian biovars

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Incidence of bacterial wilt in two species of Eucalyptus at three sites in the Brazilian Amazon planted in January 1985, each with a different history prior to planting (from Dianese et al. 1990)

Species/provenance

Prior crop

Observation date

Wilt (%)

E. pellita (Morada Nova)

Native forest

5/85

16.0

E. pellita (Morada Nova)

Gmelina arborea Roxb. for 7 years

5/85 7/85 10/85 1/86

0.8 0.2 0.1 0.1

E. urophylla (Duratex)

Gmelina arborea for 6 years, plus E. deglupta for 6 years

5/85 7/85 1/86

0.3 2.3 1.4

2, 3 and 4 (Hayward 1975) could help elucidate the relationship between eucalypts and Ralstonia solanacearum. The first record of the disease was on E. grandis in south-east Brazil (Sudo et al. 1983). The isolate obtained was also pathogenic on C. citriodora, E. saligna, E. trabutii (a hybrid of E. botryoides and E. camaldulensis), and E. urophylla. Later, the disease was reported in the Jari Valley of equatorial Brazil where it was severe (Dianese and Takatsu 1985; Dianese 1986), although it had been known to occur in the Jari Valley since 1983 (F.C. Albuquerque, pers. comm.). Traditionally Ralstonia solanacearum has been divided into five races on the basis of host range and five biovars on the basis of biochemical properties (Hayward 1964, 1991; Saddler 1994). The Brazilian isolates all belonged to biovar 1. Bacterial wilt has been known to occur in the Guangxi Province of China since 1983 and in Guangdong since 1986 (Wu and Liang 1988a, 1988b). The casual organism in China was identified as biovar 3 and was considered similar to isolates from Casuarina sp., sweet potato and tomato based on studies of esterase isozymes and pathogenicity. Biovar 3 has also caused some minor losses in E. pellita and E. urophylla in north Queensland (Akiew and Trevorrow 1994; Sun et al. 1996; E. Akiew, pers. comm.). In Brazil the disease mainly affects seedlings planted on areas recently cleared of forest, and on newly planted sites infection may be widespread or concentrated in irregular patches. In these areas the bacterium is apparently associated with the root systems of the native tropical plants. Transplanting

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of susceptible eucalypts on to these sites results in infection of the roots and later the xylem vessels in the stem. There is evidence that infection occurs through wounds in the roots of transplanted seedlings, and avoidance of wounding of roots during nursery and transplanting operations has been recommended for disease control (Robbs et al. 1988) (see Chapter 22). Wilting of infected plants may start one to two months after transplanting in areas where the daytime temperatures usually exceed 30oC. Bacterial slime (Plate 14.6) fills the xylem vessels and is observed at the distal cut end of a piece of infected stem when its base is placed in water for two to three minutes. The leaves of infected seedlings wilt and finally become dry, sometimes only on particular branches, sections of the crown or even sections of a single branch (Plate 14.7). Some leaf drop occurs but dead leaves are usually retained until the whole plant finally wilts. Tap roots are usually killed in affected plants (Plate 14.8), although sublethal infections can occur in which taproots weakened by infection are replaced by secondary roots. As crowns enlarge, two-year-old to four-year-old infected plants become susceptible to wind throw which can cause losses of up to 5%. The inner stem wood of trees with sublethal infections may also be invaded by secondary fungi and termites via root tissue infected by the bacterium (Plates 14.9 and 14.10). In the Brazilian Amazon, disease losses of less than 2% to 3% occur in areas previously cultivated with other plant species or even with eucalypt species resistant to the bacterium (Table 14.2). At least, the first eucalypt crop on newly cleared native forest sites must be resistant to the bacterium to avoid heavy losses after stand establishment. A similar relationship has also been observed with the ‘campo

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Selections of eucalypt species and seed sources which show useful resistance to bacterial wilt in Brazil and in China

Species (seed lot)

MethodA

Seed source (Brazil) or origin (China)

Brazil E. camaldulensis C. citriodora E. cloeziana E. deanei E. deglupta E. grandis E. grandis E. grandis E. pellita E. pellita E. resinifera E. tereticornis E. tereticornis E. tereticornis C. torelliana C. torelliana

GC GC GC GC FP GC GC GC FP GC GC FP FP GC GC GC

Ibitira CSIRO 11762 Carbonita L1-CB Jarf Ibitira Orchard CPAC-EMBRAPA Coen (13˚53'S) Quartel Geral Zimbabwe Palmer River (16˚10'S) Kennedy River (16˚05'S) CSIRO Fazenda Engenho Texeira de Freitas

ChinaB C. citriodora E. exserta E. saligna (7651) E. saligna (7451)

Long Men Long Men Leichin No. 1 (Ben Di) Leichin No. 1 (Ben Di)

A

Selections were based on severity of disease observed in field plots (FP) or by screening of inoculated plants in temperature controlled growth chambers (GC) at 28°C to 30°C (Dianese et al. 1990; Dianese and Dristig 1993). Data of Wu and Liang (1988a).

B

bio’ disease of potato caused by biovars 1 and 2 of Ralstonia solanacearum (Lopes and Reifschneider 1983). Interspecific and intraspecific resistance in eucalypts to bacterial wilt has been reported from Brazil (Cruz and Dianese 1986; Dianese et al. 1990; Dianese and Dristig 1993) and China (Wu and Liang 1988a, 1988b) (Table 14.3). In particular, E. deglupta, a native of the wet tropical regions of south-east Asia and Melanesia, performed well in tests in Brazil, and more importantly, no case of wilt was reported in more than 20,000 hectares of commercial plantings of the species in the Jari Valley (Dianese et al. 1990). Although none of the other species tested were from equatorial regions, and their test plantings might be regarded as being outside their natural range of climatic adaptation, the responses of the species and provenances (e.g. of E. tereticornis) were not related to the latitudes from which they originated. In spite of variability in the pathogen, the existence of significant variation in host resistance and the availability of screening methods indicate that

interspecific and intraspecific selection is a useful means of avoiding losses to this disease.

14.4.2 Crown gall There is some confusion in the literature between lignotuber formation in eucalypts and crown gall caused by Agrobacterium tumefaciens (Gibson 1967), and there are also uncertain diagnoses because of failure to isolate the bacterium (Arruda 1943). Lignotubers are features of the normal development of many species of eucalypts. They start as very small swellings of the axillary bud tissue in the axils of the first leaf pair of young seedlings and finally develop into a woody complex of dormant bud tissues (Dufrenoy 1922) morphologically similar to the crown galls produced by Agrobacterium tumefaciens. The report of crown gall on C. citriodora in the Seychelles indicates that the swellings observed were almost certainly lignotubers (Squibbs 1936). The symptoms of crown gall on eucalypts are similar to those on many other dicotyledonous hosts and consist of tumours, overgrowths or warty

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protuberances of variable size on roots or at the base of the stem. The gall may develop to a large size with lethal or sublethal effect upon the seedlings. The bacterium transfers the Ti (tumour inducing) plasmid to cells in wounded host tissue (Zaenen et al. 1974). The plasmid DNA is incorporated into the genome of the plant cells which are thus genetically transformed into primary tumourigenic cells (Chilton et al. 1977) and may multiply in an disorganised manner to give rise to a gall that develops independently of the presence of the bacterium. Crown gall of eucalypts has been reported from South America, Europe, Africa and Asia. The first record was on E. robusta and C. citriodora in the State of Sao Paulo, Brazil (Navarro de Andrade 1928). Later the occurrence of crown gall on an unidentified species of Eucalyptus in Poland was reported by Siemaszko (1929). Arruda (1943) referred to the frequent occurrence of crown gall on Eucalyptus in Brazil but emphasised the difficulty of proving the parasitic origin of the syndrome by isolating the bacterium. The occurrence of tumours on a species of Eucalyptus at East Malling, England, thought to be due to Agrobacterium tumefaciens was mentioned by Wormald (1945). Fernandez-Valiela et al. (1954) found the disease on E. camaldulensis and demonstrated the pathogenicity of the bacterium. Crown gall has been reported from Madagascar (Gibson 1967), listed as a disease of C. maculata in Taiwan (Hsieh 1980) and reported on Eucalyptus species in Chile (Herrera-Autter 1964). Crown gall on eucalypts is considered to be a minor disease, mostly recorded on seedlings in nurseries. However, Jindal and Bhardwaj (1986) reported severe losses of E. tereticornis in India where disease increased as seedling age increased from three to 12 months. Infection reached 12% in three-month-old seedlings, but in nine-month-old seedlings losses rose to 70%. Most reports of suspected crown gall on Eucalyptus species come from nurseries and seedlings but Hepting (1971) noted the disease on stems of Eucalyptus spp. in the field in California. Interspecific differences in resistance to crown gall in eucalypts appear likely and Fernandez-Valiela et al. (1954) considered E. saligna to be immune and E. camaldulensis susceptible. The hairy root bacterium [Agrobacterium rhizogenes (Riker et al. 1930) Conn 1942] has not been

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reported from field plantings of eucalypts (De Cleene and De Ley 1981). However, this pathogen can transfer its Ri (root inducing) plasmid to seedlings of E. gunnii, inducing typical hairy root symptoms (White and Nester 1980). Eucalyptus dunnii, E. grandis and E. nitens are also susceptible to infection in vitro by Agrobacterium rhizogenes (MacRae 1991). It was concluded that transformation by the bacterium has potential for improving the rooting of cuttings of some eucalypts that are otherwise difficult to propagate vegetatively.

14.4.3 Xanthomonas shoot blight and dieback Shoot blight and dieback of C. citriodora caused by Xanthomonas campestris pv. eucalypti has been reported from New South Wales, Australia (Truman 1974). Three outbreaks of the disease were recorded in suburbs of Sydney, New South Wales, in 1963, 1967 and 1970, affecting trees ranging from three to seven metres high. The bacterium is a typical xanthomonad originally described as Xanthomonas eucalypti by Truman (1974). Pathogenicity of the bacterium was demonstrated by inoculation of seedlings of C. citriodora and C. maculata, while inoculations of E. haemastoma, E. grandis, E. saligna and E. laevopinea produced no apparent infection (Truman 1974). Infections in C. citriodora resulted in blackened areas on the distal five to 10 centimetres of the twigs. These diseased areas increased in size until blight and death of the terminal buds occurred. Epicormic shoots along the lower branches produced new growth, giving a characteristic bushy appearance to the infected plants. Artificial inoculation of C. citriodora can also result in the formation of small cankers that produce droplets of resinous exudate.

14.5 Diseases associated with nematodes There are few records of disease in eucalypts associated with plant parasitic nematodes. Evidence of pathogenicity is lacking for most of the eucalypt–nematode associations reported. Parasitic nematodes may be relatively common in the soils of native eucalypt forests and woodlands. Apart from the study of Reay and Wallace (1981b), which indicated that potentially parasitic species were

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abundant in wetter environments in the central highlands of South Australia, no studies have been undertaken to determine whether nematode populations might reach densities that could affect tree growth. Khair (1987) recorded 41 species in 22 genera of nematodes associated with 45 named eucalypt species from a range of forest types. Eighteen nematode species were from the genera Hemicriconemoides, Hemicycliophora and Radopholus. Other species have been recorded from eucalypt forests and woodlands (Andrassy 1986; Reay 1986; Reay and Colbran 1986; Reay 1987a, 1987b; Reay 1991; Decraemer and Reay 1991). More detailed investigations of the association of nematodes with native eucalypts in Australia are limited. Colbran (1966) described females of Cryphodera eucalypti Colbran (eucalypt cystoid nematode) partially embedded in small roots of E. major. This species was also found to reproduce on E. crebra, E. punctata and E. sideroxylon and was associated with E. andrewsii, apparently being widespread in eucalypt forest in south-east Queensland. Acontylus vipriensis Meagher was described from a Eucalyptus species in a Victorian forest where sessile, partly swollen females formed colonies on roots (Meagher 1968). No other pathological effects were noted in either case. The root lesion nematode Pratylenchus coffeae (Zimmerman) Filipjev & Schuurmans Stekhoven was found by Beaumont (1975) on dead E. globulus, E. microcorys and E. obtusiflora but no details were provided on plant growing conditions, plant size or symptoms. Nematodes have been associated with disease and mortality of eucalypts in several exotic plantings. A species of Meloidogyne was associated with an unidentified eucalypt species in East Africa (Whitehead and Kariuki 1960) and E. gunnii in Latin America (Garces 1964). In Brazil, the root lesion nematode Pratylenchus brachyurus (Godfrey) Filipjev & Schuurmans Stekhoven caused a reduced root system and root necrosis and cracking in seedlings and young trees of E. alba and E. saligna (Lordello 1967). Field infection was associated with stunting, foliage chlorosis and plant death. Nematode species in 24 genera were associated with mortality of eucalypt seedlings in nurseries and plantations in Pakistan (Shah and Chaudrey 1975). The nematodes most frequently isolated from soil and roots were species of Paratylenchus,

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Pratylenchus, Tylenchorhynchus, Ditylenchus and Longidorus. The contribution of the nematodes to seedling mortality was not clarified. Eight nematode species known to be parasitic on other genera were associated with certain disease symptoms on 11 eucalypt species in Sao Paulo State, Brazil (Ferraz et al. 1984). However, on sandy soils in Natal, South Africa, with a previous history of sugarcane cropping including routine nematode control, Atkinson et al. (1991) found no growth response consistent with a nematicidal effect in trials of aldicarb in newly established plantations of E. grandis and E. grandis × E. camaldulensis hybrid; while species of many nematode genera were present in the soils, their populations were generally low, a finding confirmed in a survey of nematode populations in South African eucalypt plantations by Marias and Buckley (1993). Inoculation studies have demonstrated that some common plant parasitic nematodes are able to infect certain eucalypt species and that eucalypt species vary in susceptibility to infection by some nematode species. Radopholus similis (Cobb) Thorne was shown to infect E. robusta in Florida (van Weerdt et al. 1959). Root tips of E. obliqua became swollen following feeding by Tylodorus fisheri Reay, although this species, which also fed on the roots of E. regnans, did not attack E. fasciculosa or E. camaldulensis (Teare and Wallace 1974; Reay 1991). Corymbia citriodora was apparently resistant to Pratylenchus brachyurus where E. alba and E. saligna were susceptible (Lordello 1967). Meloidogyne javanica (Treub) Chitwood caused no infection on three eucalypt species and minor infection on two others inoculated by Stirling (1976), and caused gall formation on six of 13 eucalypt species inoculated by Reay and Wallace (1981a). Eucalyptus camaldulensis was resistant to 11 local populations of Meloidogyne spp. in Senegal (Netscher 1981), a result confirmed by Ibrahim and Kandeel (1986) who reported that eucalypts were resistant to Meloidogyne incognita (Kofoid & White) Chitwood, Meloidogyne javanica and Meloidogyne arenaria (Neal) Chitwood. Corymbia citriodora, reported as possibly resistant to Pratylenchus brachyurus (Lordello 1967), was shown to be susceptible to Meloidogyne javanica (Ferraz 1982). Giant cells were observed to develop in the stele of roots, and mature females formed egg masses which disrupted the epidermis.

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O F

Only nematodes of the genus Fergusobia (Tylenchida: Sphaerulariidae), together with the fly Fergusonina (Diptera: Fergusoninidae), have been associated with disease of the above-ground parts of eucalypts. Morgan (1933) and Currie (1937) described the development on the flower and vegetative buds and stem tips of C. maculata, E. macrorhyncha and other eucalypts of galls resulting from invasion of host tissues by the fly and the nematode. These galls are capable of reducing shoot growth and seed production. Some Fergusobia species, of which Fergusobia tumifaciens (Currie 1937) Wachek 1955 [syn. Fergusobia curriei (Johnson 1938) Christie 1941] is the best known (Fisher and Nickle 1968; Siddiqui 1986), are associated with different species of Fergusonina. The nematode species are likely to be specific to insect host species, although each insect-nematode association is not necessarily restricted to one eucalypt species (Davies and Lloyd 1996). The nematodes parasitise both the insect and the plant, and are oviposited into the host plant tissue by the insect. Currie (1937) considered this type of gall formation to be common on many Eucalyptus spp. in all parts of Australia. The host list in Australia has been extended to 19 eucalypt species (Khair 1987), and species of Fergusobia have also been described from flower bud galls on E. deglupta in Papua New Guinea and the Philippines (Siddiqi and Mousa 1997). As a parasite of the fly, developmental stages of Fergusobia are associated with the fly throughout its life cycle. Currie (1937) believed the feeding of Fergusobia on the plant host contributed to cell proliferation and gall development as galling started where nematodes occurred and not around the eggs or larvae of the fly. While the role of Fergusobia spp. in gall development could not be confirmed by Fisher and Nickle (1968), Siddiqi (1986) argued that they are indeed plant parasites although they are primarily parasites of the insect rather than of the plant. The constant relationship between Fergusobia and Fergusonina makes demonstration of the causation of galling difficult and the relationship is regarded as one of the most complex gall associations known (Giblin-Davis 1993; Taylor et al. 1996). The size and morphology of the galls varies with the species of fly and the plant tissue affected, but they may be up to 25 millimetres in diameter and

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50 millimetres long (Currie 1937; Taylor et al. 1996). Large fluctuations were observed in the number of galls from season to season, with irregular bud formation being considered the main factor responsible for these fluctuations in the species that cause galling of flower buds (Currie 1937). While galling may be severe on individual trees or branches and can suppress flower and seed production (Morgan 1933), it is unlikely to greatly affect regeneration in natural forests. However, severe galling could affect honey production (Currie 1937) and could affect silvicultural management where regeneration may depend on seed from retained trees or seed production in managed seed orchards.

14.6 Conclusion Although eucalypts have been exposed to potentially pathogenic viruses, phytoplasmas, bacteria and nematodes in their natural range (Reay and Wallace 1981a; Guy 1982), most eucalypt diseases attributed to these agents have been reported from exotic cultivation. The exposure of eucalypts to alien pathogens no doubt accounts for some of these diseases. For example, bacterial wilt of Eucalyptus spp. in Brazil and little leaf of E. grandis in India following parasitism by Santalum album naturally infected with a phytoplasma are almost certainly new encounter diseases. It is also likely that the development of some of these diseases is enhanced by intensive cultivation of eucalypts in nurseries and plantations where the potential for disease is often increased as a result of greater genetic uniformity in the host and favourable conditions for development of disease (Cowling 1978). Furthermore, there is a greater likelihood of detection of disease at low incidence or with non-lethal symptoms than would be the case in native forests or woodlands. In native communities early mortality is naturally high and activities of other pests and diseases are likely to obscure minor symptoms. There has been a recent rapid expansion of eucalypt plantations in Australia involving higher intensity of management, greater surveillance and lower tolerance of disease losses. It is therefore to be expected that more frequent reports of diseases caused by these agents might emerge. A theme through most of this chapter has been the lack of reports in which the pathogenicity of particular agents has been demonstrated. Only Ralstonia solanacearum has been shown to be a

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pathogen of eucalypts; on present evidence the other organisms mentioned in this chapter can only be considered to be associated with disease. The study of these diseases requires specialised knowledge, methodology and equipment; as a result it is unlikely that our knowledge of them will increase dramatically without the collaboration of virologists, bacteriologists, nematologists and molecular biologists from other disciplines. With the exception of bacterial wilt, the incidence of eucalypt diseases associated with viruses, phytoplasmas, nematodes and bacteria has been low and their economic effects small, particularly as the diseases are confined mainly to young plants. Such diseases have stimulated little research and this situation is likely to remain unless there are destructive outbreaks of disease caused by these agents.

14.7 References Akiew, E. and Trevorrow, P.R. (1994). Management of bacterial wilt of tobacco. In Bacterial Wilt. The Disease and its Causative Agent, Pseudomonas solanacearum. (Eds A.D. Hayward and G.L. Hartman) pp. 179–198. (CAB International: Wallingford, Oxford.) Ali, M.I.M., Balasundaran, M. and Ghosh, S.K. (1984). Histopathological detection of little leaf disease of eucalypts in Kerala. In Eucalypts in India. Past, Present and Future, Proceedings of the National Seminar held at Kerala Forest Research Institute, Peechi, Kerala, India, 30–31 January 1984. (Eds J.K. Sharma, C.T.S. Nair, S. Kedharnath and S. Kondas) pp. 404–408. (Kerala Forest Research Institute: Peechi, Kerala.) Ali, M.I.M., Balasundaran, M. and Ghosh, S.K. (1987). Association of mycoplasma-like organisms with little leaf disease of eucalypts in Kerala, India. Indian Journal of Forestry 10, 159–162. Andrassy, I. (1986). Fifteen new nematode species from the southern hemisphere. Acta Zoologica Hungarica 32, 1–33. Anino, E.O. (1987). Stunt disease affecting the Eucalyptus deglupta Blume plantations in the Paper Industries Corporation of the Philippines (Picop). Sylvatrop 12, 129–132. Arruda, S.C. (1943). Observações sobre algumas doenças do eucalipto no Estado de São Paulo. O Biológico 9, 140–144. Atkinson, P.R., van den Berg, E. and van Rensburg, N.J. (1991). Response of Eucalyptus to aldicarb in coastal sandy soils in Natal, South Africa. South African Forestry Journal 158, 5–9.

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Balasundaran, M., Ali, M.I.M. and Ghosh, S.K. (1988). Little leaf disease of eucalypts. In Mycoplasma Diseases of Woody Plants. (Eds S.P. Raychaudhuri and N. Rishi) (Malhotra Publishing House: New Delhi, India.) Beaumont, P.B. (1975). Nematodes. Australian Plants 8, 183–188. Bos, L., Makkouk, K.M. and Bayaa, B. (1990). Witches’ broom and decline of Eucalyptus, a serious disease in Syria, likely caused by mycoplasma. Arab Journal of Plant Protection 8, 133–135. Brzostowski, H.W. and Grace, T.D.C. (1974). Virus-like particles isolated from diseased eucalypts. Plant Disease Reporter 58, 92–93. Calavan, E.C. and Oldfield, G.N. (1979). Symptomatology of spiroplasmal plant diseases. In The Mycoplasmas. Volume III. Plant and Insect Mycoplasmas. (Eds R.F. Whitcomb and J.G. Tully) pp. 37–64. (Academic Press: New York.) Chilton, M.D., Drummond, M.H., Merlo, D.J., Sciaky, D. Montoya, A.L., Gordon, M.P. and Nester, E.W. (1977). Stable incorporation of plasmid DNA into higher plant cells: the molecular basis of crown gall tumorigenesis. Cell 11, 263–271. Colbran, R.C. (1966). Studies of plant and soil nematodes. 12. The eucalypt cystoid nematode Cryphodera eucalypti n.g., n.sp. (Nematoda: Heteroderidae) a parasite of eucalypts in Queensland. Queensland Journal of Agricultural and Animal Sciences 23, 41–47. Cowling, E.B. (1978). Agricultural and forest practices that favor epidemics. In Plant Disease: An Advanced Treatise. Volume II. How Disease Develops in Populations. (Eds J.G. Horsfall and E.B. Cowling) (Academic Press: New York.) Cruz, A.P. da and Dianese, J.C. (1986). Tolerância á murcha bacteriana em eucalípto. Fitopatologia Brasileira 11, 396. Currie, G.A. (1937). Galls on Eucalyptus trees: A new type of association between flies and nematodes. Proceedings of the Linnean Society of New South Wales 62, 147–174. Dafalla, G.A., Theveu, E. and Cousin, M.T. (1986). Mycoplasma-like organisms associated with little leaf disease of Eucalyptus microtheca Muell. Journal of Phytopathology 117, 83–91. Davies, K.A. and Lloyd, J. (1996). Nematodes associated with Diptera in South Australia: a new species of Fergusobia Currie from a fergusoninid and a new record of Syrphonema Laumond & Lyon from a syrphid. Transactions of the Royal Society of South Australia 120, 13–20. Decraemer, W. and Reay, F. (1991). Trichodorid nematodes from Australia with description of two new species from native vegetation. Australasian Plant Pathology 20, 52–66.

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M ISTLETOES AND O THER P HANEROGAMS P ARASITIC ON E UCALYPTS

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Three main types of parasitic phanerogam (mistletoes, native cherries, dodder-laurels) infect eucalypts in Australia and are part of the natural landscape. However, the levels of mistletoe infestation and associated debility or death of trees have concerned many observers for more than one hundred years. Amyema miquelii is the most widespread and damaging parasite of eucalypts in southern and eastern Australia and Amyema pendula achieves pest status in parts of south-east Australia. Progressive infection of hosts leads to the point where little or no host foliage remains on heavily infected trees. The apparent increase in mistletoe populations has been associated with land clearance and thinning of trees for agriculture and other purposes. In temperate Australia, mistletoe infestation is especially apparent on isolated trees or trees in small stands or on forest margins. The mistletoe problem in rural Australia lends itself to long-term strategies based on promoting natural regeneration of remnant vegetation. Selection of mistletoe-resistant plant species and provenances is a priority. Because of the need to conserve local biodiversity, revegetation activities should concentrate on using local provenances of trees. Germplasm of non-host species and of individuals of host species that appear (based on their uninfected state despite their close proximity to heavily infected individuals) to be resistant to mistletoe infestation, should be collected for propagating mistletoe-resistant plants. The native cherries or ballarts (Exocarpos) are santalacean shrubs or small trees that parasitise the roots of plants including eucalypts. The dodder-laurels (Cassytha) in the Lauraceae are superficially leafless, wiry perennial herbs that form dense masses of intertwined stems and can smother woody and herbaceous vegetation. Neither group of parasites has been a widespread problem in management of eucalypt vegetation.

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15.1 Introduction Parasitic phanerogams are flowering plants that have evolved specialised organs called haustoria by which they attach themselves to host plants and absorb water and chemicals from the vascular tissues of the host. Three principal kinds of parasitic phanerogam infect eucalypts in Australia: mistletoes, native cherries and dodder-laurels. Mistletoes are shrubby angiosperms in the Santalales that parasitise the aerial stems of perennial plants. About 1400 species occur almost worldwide and they are most diverse in the tropics. As tree parasites, they cause severe damage to tree crops and managed forests, and inflict significant economic losses in many countries (Hawksworth 1983). The native cherries or ballarts (Exocarpos) are santalacean shrubs or small trees that parasitise the roots of plants. Twenty-six species of Exocarpos occur from Malesia to Hawaii, with nine species in Australia (George 1984). Less is known about the root parasites than the mistletoes because they differ little in general appearance from the rest of the vegetation, the haustoria are concealed below ground and few taxa are of economic importance (Fineran 1991). Unlike the mistletoes, native cherries do not cause serious damage in Australian forests and woodlands. The dodderlaurels (Cassytha) in the Lauraceae are superficially leafless, wiry perennial herbs that form dense masses of intertwined stems and can smother woody and herbaceous vegetation. About 20 species of Cassytha occur worldwide, mainly in tropical and subtropical regions, with 14 species in Australia (Harden 1990). At least three species are parasitic weeds in agriculture and forestry (Parker and Riches 1993). Australia's mistletoe flora includes species that preferentially parasitise eucalypts. Mistletoes are not generally a problem in old growth and regenerating eucalypt forests managed for timber production (Hartigan 1960; McKinnell et al. 1991; Turner 1991; Fagg 1997) or in forest and woodland managed for nature conservation. In such areas, mistletoe populations are usually in equilibrium with host populations and individual trees are seldom killed (Barlow 1986). Moreover, mistletoes provide food resources and habitat for many species of forest and woodland fauna. However, in the box-ironbark eucalypt forests of north-central Victoria and the agricultural and pastoral districts of temperate Australia, mistletoes contribute to the premature death of native trees (Kellas 1991; Kahn 1993;

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Reid 1995; Fagg 1997) (Plates 15.1 and 15.2). Infestations of the common eucalypt parasites, Muellerina eucalyptoides (DC.) Barlow, Amyema pendula (Spreng.) Tiegh. and Amyema miquelii (Miq.) Tiegh. have concerned rural communities since the early twentieth century (Ewart and Tovey 1909; May 1941; Calder et al. 1979) and various mistletoe control methods have been tested. Eucalypt species planted in other countries are occasionally infected by local mistletoes, but infection of these eucalypts has not yet been reported to cause serious debility or mortality. Six species of Exocarpos are widespread in eucalypt-dominated communities in Australia. Some species can kill their woody shrub and tree hosts but their effect on forest production and other values of the vegetation is negligible. Cassytha is a locally severe pest of coppice growth in the boxironbark eucalypt forests of north-central Victoria (Kellas 1991) and smothers roadside and low woody vegetation in parts of southern Australia.

15.2 Mistletoes parasitic on eucalypts Of the 1400 species of mistletoe, most belong to the Loranthaceae (950 species) and Viscaceae (400 species). The remainder occur in the Misodendraceae, Eremolepidaceae and Santalaceae (Phacellaria and Henslowia) (Kuijt 1990). The Australian mistletoe flora comprises 74 species (12 genera) of Loranthaceae and 16 species (3 genera) of Viscaceae (Barlow 1984, 1992, 1993, 1996). Loranthaceous mistletoes occur throughout mainland Australia in a wide variety of wooded habitats including eucalypt forests and woodlands. Viscaceous mistletoes, however, occur predominantly in coastal and subcoastal humid forests in the north and east of the continent. The 13 species (four genera) of Loranthaceae that commonly parasitise eucalypts (Eucalyptus and Corymbia) in Australia are listed in Table 15.1. Most of these species have extensive geographical distributions and parasitise many different eucalypt species. No species of Australian Viscaceae is a major eucalypt parasite, but at least three viscaceous and 23 loranthaceous mistletoe species not listed in Table 15.1 occasionally infect eucalypts (Downey 1997); for example, Decaisnina petiolata (Barlow) Barlow subsp. angustata Barlow (Barlow 1993) and Nuytsia

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The principal hosts, distribution and habitats of Australian mistletoes that commonly parasitise eucalypts (after Barlow 1966, 1984, 1992 and Downey 1997)

Mistletoe

Principal hosts

Distribution and habitat

Amyema bifurcata (Benth.) Tiegh.

Almost exclusively Corymbia (15 spp.), Eucalyptus (7 spp.) and Angophora (5 spp.)

North, east and central Australia in open forest

Amyema bifurcata (Benth.) Tiegh. var. eburnea Barlow

Exclusively Corymbia: only recorded hosts C. dichromophloia and C. papuana

Kimberley region, WA

Amyema biniflora Barlow

Exclusively Corymbia (4 spp.) and Eucalyptus (2 spp.)

Coastal and subcoastal Queensland in sclerophyll forest

Amyema miquelii (Miq.) Tiegh.

Usually on Eucalyptus (102 spp.) or Corymbia (8 spp.); locally common on Acacia (5 spp.).

Throughout mainland Australia in open forest, woodland and scrub

Amyema pendula (Spreng.) Tiegh.

Usually on Eucalyptus (52 spp.); recorded on C. gummifera; locally common on Acacia (14 spp.)

South-east Australia in mesic forest and semiarid woodland

Amyema pyriformis Barlow

Exclusively Eucalyptus: only recorded host E. rupestris

Kimberley region, WA

Amyema sanguinea (F. Muell.) Danser

Mostly Corymbia (17 spp.) and Eucalyptus (16 spp.); occasionally Melaleuca and Lophostemon

Central, north and north-west Australia in open forest and woodland

Dendrophthoe glabrescens (Blakely) Barlow

Various genera but commonly Eucalyptus (14 spp.) and Corymbia (4 spp.); also Melaleuca, Lophostemon, Barringtonia, Brachychiton and Acacia

North and east Australia in open forest and woodland

Dendrophthoe homoplastica (Blakely) Danser

Eucalyptus (4 spp. but especially E. shirleyi), Corymbia (2 spp.), Lophostemon, Tristania and Melaleuca

North-east Queensland in open forest and woodland

Dendrophthoe odontocalyx (Benth.) Tiegh.

Various genera but especially Eucalyptus (3 spp.), Corymbia (3 spp.), Grevillea and Syzygium

North NT in monsoon forest and woodland

Dendrophthoe vitellina (F.Muell.) Tiegh.

Many genera but frequently Eucalyptus (16 spp.), Corymbia (7 spp.) and other Myrtaceae

Coastal and subcoastal eastern Australia in open forest

Diplatia grandibractea (F.Muell.) Tiegh.

Almost exclusively Eucalyptus (13 spp.)

North and inland central-eastern Australia in open forest and woodland

Muellerina eucalyptoides (DC.) Barlow

Usually on Eucalyptus (53 spp.), South-east Australia in humid and Corymbia (6 spp.) and Angophora (5 subhumid forest and woodland spp.); also Acacia, casuarinas and exotics

floribunda (Labill.) R.Br. (Göbel 1975). Nine species (10%) of Australian mistletoes in three genera (Muellerina, Amyema, Diplatia) are largely or entirely host-specific to eucalypts (Table 15.1). Given that most Australian mistletoes show some degree of host specificity (Barlow and Wiens 1977) and that eucalypts dominate vegetation over about 30% of the continent, the Australian mistletoe flora might be considered extraordinary for the number of species that do not parasitise eucalypts.

The paradox is explained by the relatively recent emergence of eucalypt dominance. Because of the late onset of aridity in Australia in the Tertiary (Lange 1980) and of human burning of vegetation in the late Quaternary (favouring fire-tolerant genera such as Eucalyptus and Corymbia), the eucalypts have diversified and expanded relatively recently, with the result that the Australian mistletoe flora has had relatively little opportunity to adapt to them.

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Frequency of infection of common host trees by three eucalypt-parasitising mistletoes along roadsides within 50 kilometres of Armidale, NSW

Data were collected by recording mistletoe infestation of all species of only dominant and codominant trees at 83 roadside stops (from N. Reid, Z. Yan & C. Nadolny, unpubl. data)

Frequency (%) of trees infected by: Host species Angophora floribunda Eucalyptus albens E. blakelyi E. bridgesiana

No. of trees 126

Amyema miquelii

Amyema pendula

Muellerina eucalyptoides

1.6

0

1.6

28

39.3

0

0

255

49.0

3.1

5.1

98

32.7

11.2

2.0

244

3.3

27.1

2.1

E. dalrympleana

81

13.6

23.5

2.5

E. dealbata

29

44.8

0

3.4

E. caliginosa

E. laevopinea

94

3.2

21.3

3.2

E. melliodora

320

40.9

0.6

2.8

E. nova-anglica

62

0

1.6

0

E. viminalis

89

0

4.5

0

Mistletoes vary in their degree of host specificity. Downey (1997) listed all the known hosts of Australian mistletoes from herbarium records, which helps quantify and clarify earlier comments (e.g. Barlow 1984) about mistletoe host preferences from a national perspective. However, national lists of host species do not indicate the specificity of local mistletoe populations because of regional variation in host preference. Regional or local studies demonstrate the varying degrees of host specificity exhibited by different mistletoe species. The frequency of occurrence of three species of eucalypt-parasitising mistletoe on a range of tree species near Armidale, NSW, is shown in Table 15.2. Muellerina eucalyptoides was the least abundant of the three mistletoes and exhibited the least host specificity. It parasitised eight of the 11 tree species, all in low frequency. Amyema miquelii and Amyema pendula, however, showed greater specificity, each parasitising a subset of potential eucalypt hosts more frequently than other species. Amyema miquelii preferentially parasitised the red gums (Eucalyptus blakelyi, E. dealbata) and boxes (E. melliodora, E. albens, E. bridgesiana), while Amyema pendula most frequently infected the stringybarks (E. caliginosa, E. laevopinea) and mountain gum (E. dalrympleana). The Amyema species commonly co-occurred only on E. bridgesiana and

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E. dalrympleana and were otherwise absent from each other's major hosts. These patterns of infection suggest the phenomenon of ‘host exclusion’ (i.e. the tendency for species of sympatric mistletoes to infect mutually exclusive subsets of host species), hitherto known only from North America (Hawksworth and Wiens 1996). Host exclusion may be due to the historical presence of a primary parasite that selected for higher levels of resistance to mistletoe infection in local host populations, rendering the hosts less susceptible (less compatible) to secondary parasite species (Reid et al. 1995). Table 15.2 also highlights the tree species near Armidale that are naturally resistant to infection by mistletoes. Although E. nova-anglica and E. viminalis both appear to be resistant to infection, some stands of the latter species in the region are frequently parasitised by Amyema pendula. Only E. nova-anglica is resistant to infection across the region, although some specimens of even this species are parasitised by Amyema pendula. Eucalypts have been planted in many parts of the world and Table 15.3 lists records of mistletoe infection of eucalypts outside Australia. Although infection of Eucalyptus by Psittacanthus calyculatus (DC.) G.Don can be severe in southern Mexico (F.G. Hawksworth, pers. comm.), eucalypts are probably relatively resistant to infection by

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Records of mistletoe infection of eucalypts outside Australia (from Hawksworth 1974; F.G. Hawksworth, pers. comm. and Kuijt 1989)

Eucalypt species

Mistletoe species

Locality

Corymbia citriodora

Dendrophthoe falcata

India

Eucalyptus sp.

Psittacanthus calyculatus (DC.) G.Don

Michoacán, Mexico

Eucalyptus sp.

Struthanthus polystachys (Ruiz & Pav.) Eichler

Costa Rica

Eucalyptus sp.

Tapinanthus erianthus (Sprague) Danser

Zaire

Eucalyptus sp.

Tripodanthus acutifolius (Ruiz & Pav.) Tiegh.

Bolivia

E. camaldulensis

Dendrophthoe falcata (L.f.) Ettingsh.

India

E. globulus

Dendrophthoe nilgherrensis (Wright & Arn.) Tiegh.

Sri Lanka; India

E. globulus

Scurrula parasitica L.

Sri Lanka

E. robusta

Dendrophthoe falcata

India

E. saligna

Dendrophthoe falcata

India

mistletoes with generalised host preferences. Of the host generalist genera in Australia, only Dendrophthoe commonly parasitises eucalypts. Other mistletoes of open forest and woodland that parasitise many host genera, such as Lysiana and Decaisnina, tend not to infect eucalypts.

15.2.1 The basis of host specificity Several factors have been suggested to explain the host specificity exhibited by mistletoes, including the behaviour of avian dispersers and host water relations (Lamont 1985). Disperser behaviour may explain some aspects of mistletoe distribution (Lamont 1985; Yan 1990), but the genetic adaptation of mistletoe populations to particular host populations is probably the major mechanism accounting for mistletoe–host specificity (Atsatt 1983). This has been demonstrated for mistletoe populations on mesquite in North America (May 1971). Because mistletoes adapt to local populations of host species, their host preferences vary geographically (Hawksworth and Wiens 1996) and non-local provenances of host species may not be as susceptible to infection as local host populations. We recently tested this possibility in arid South Australia, using Amyema quandang (Lindl.) Tiegh. and its principal host, Acacia papyrocarpa Benth. Individuals of different populations of Acacia papyrocarpa were inoculated along the highways between Whyalla and Coober Pedy with seeds of Amyema quandang from near Whyalla. Mistletoe establishment varied among the host populations (N. Reid and Z. Yan, unpubl.

data). Infection was highest (21%–22%) among trees of the Whyalla host population where the mistletoe seeds were collected. Infection of host populations fell to 4% to 9% between 70 and 120 kilometres from Whyalla, and to 0% to 2% between 200 and 320 kilometres from Whyalla. Although environmental differences between sites could not be ruled out, we suspect that the result is largely attributable to the adaptation of Whyalla mistletoes to local hosts and to genetic differentiation between the populations of Acacia papyrocarpa. Among conspecific eucalypt populations, variation in susceptibility to mistletoe infection probably exists on a similar geographical scale.

15.2.2 Mistletoe biology 15.2.2.1 Ecophysiology Most mistletoes are aerial parasites of stems, obtaining water, nutrients and organic solutes from the xylem stream of their hosts. Exceptions include the two Australian loranths, Nuytsia floribunda and Atkinsonia ligustrina (Lindl.) F.Muell., which are xylem-tapping parasites of roots (Fineran 1991), and the viscaceous dwarf mistletoes (Arceuthobium spp.) which tap both host xylem and phloem (Hull and Leonard 1964; Knutson 1983). Although xylemtapping mistletoes are often regarded as hemiparasitic autotrophs (i.e. they depend on the host xylem stream for water and minerals but are self-sufficient in organic carbon from photosynthesis), recent studies have demonstrated that most, if not all, mistletoes are at least partly heterotrophic (Marshall and Ehleringer 1990;

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Fineran 1991). Labelled carbon fixed by host foliage was detected in the leaves of Tapinanthus bangwensis (Engl. & K.Krause) Danser (Room 1971). Raven (1983) calculated that at least 20% of the carbon in a xylem-tapping parasite with a carbon to nitrogen ratio of 15 must be derived from the host in the form of organic nitrogen compounds dissolved in the xylem sap. Apoplastic translocation of host 3 H-lysine from host to parasite was demonstrated in Korthalsella lindsayi (Oliv. ex Hook.f.) Engl. (Viscaceae) (Coetzee and Fineran 1989). Pate et al. (1991) measured amino acid concentrations in host and mistletoe xylem sap and estimated that 24% of the carbon requirements for dry matter production in Amyema linophylla (Fenzl) Tiegh. is met by intake of organic solutes from the host (Casuarina obesa Miq.). Marshall and Ehleringer (1990) used carbon isotope and gas exchange data to estimate that 62% of the carbon in Phoradendron juniperinum Engelm. ex Gray is derived from amino acids and organic acids dissolved in the host xylem sap, and Schulze et al. (1991) calculated the degree of carbon heterotrophy of Tapinanthus oleifolius (J.C.Wendl.) Danser on a range of hosts to be 47% to 67%. Despite the assumption that the organic carbon flux is from host to parasite, experimental evidence for the phloem-tapping dwarf mistletoe, Arceuthobium americanum Nutt. ex Engelm. in A.Gray, suggests that considerable movement of photosynthate from parasite to host sometimes occurs (Raven 1983). In the case of eucalypt-parasitising mistletoes, Calder et al. (1979) speculated that reverse translocation of organic materials might sometimes occur from mistletoe to host because eucalypts whose canopy consists entirely of Amyema, or virtually so, can survive for up to three years (Kerr 1925). Given the lack of continuity between the phloem of eucalypts and xylem-tapping mistletoes (discussed below), such trees are more likely to survive on carbohydrates stored in the host wood and bark, or translocated from surrounding eucalypts or stems via root grafts and lignotuber connections. Mistletoes typically exhibit low leaf water potentials, high transpiration rates and low water use efficiencies (assimilation/transpiration) compared with their hosts (Fisher 1983; Ullmann et al. 1985; Marshall and Ehleringer 1990). High transpiration rates may be necessary to satisfy a requirement for either mineral nitrogen (Schulze et al. 1984; Ehleringer et al. 1985), heterotrophic carbon

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(Stewart and Press 1990) or both (Marshall and Ehleringer 1990). Despite the profligate use of water, stomatal control in mistletoes is good and regulation of leaf conductance is coordinated with the stomatal responses of the host (Ullmann et al. 1985; Whittington and Sinclair 1988). Control over water use and growth is an important adaptation for long-lived mistletoes in drought-prone environments and helps prevent the premature death of the host and parasite (Ullmann et al. 1985; Tennakoon and Pate 1996). Since xylem-tapping mistletoes are obligate parasites dependent on the water, nutrient and organic compounds provided by their hosts, it is likely that well-watered, well-fertilised host trees provide better habitat for mistletoes than stressed trees with water and nutrient deficits (Hawksworth 1961; Norton et al. 1995). The assumption is sometimes made that stressed trees are selectively attacked by mistletoes because such trees are less able to resist infection (Gehring and Whitham 1992) or conversely that vigorous trees are better able to withstand the effects of parasites (Parsons et al. 1991). Paradoxically, vigorous hosts are likely to suffer the greatest growth reductions as a result of heavy mistletoe infection. 15.2.2.2 Seedling establishment and the haustorium The seeds of most mistletoes germinate immediately upon excision from the epicarp. The emerging radicle is club-shaped and tends to grow toward the branch irrespective of initial orientation, probably as a result of negative phototropism and negative geotropism (Kuijt 1969; Lamont 1983). Upon making contact with the branch, the tip of the radicle flattens against the branch surface to form a club-shaped holdfast. From the undersurface of the holdfast, a wedge of haustorial tissue penetrates the host bark by a combination of mechanical pressure and enzymic digestion, and makes contact with the host xylem in the cambial zone. Seedling establishment may take from a few weeks to six months (Yan 1990). During this time the free-living seedling depends on endosperm reserves and photosynthate from the chlorophyllous embryo. The diaspore, radicle and holdfast are coated in an oily viscin which may restrict water loss, but the free-living seedling is susceptible to desiccation and high temperatures. Branch diameter and bark thickness determine establishment success in most mistletoe species (Reid 1991). In the case of Amyema quandang

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30

Frequency (%)

25

20 Tree 1 Tree 2

15

Tree 3

10

5

0 1-5 Figure 15.1

6-10

11-15

16-20

21-25

26-30

31-35

36-40

41-45

46-50

51-55

56-60

61-65

Distribution of host branch diameters of mistletoes on three trees of Eucalyptus melliodora heavily infected by Amyema miquelii near Armidale, NSW, in February 1990. The minimum diameter of the host branch was measured proximal to the mistletoe haustorium. Sample sizes for trees 1 to 3 were 45, 160 and 274 mistletoes, respectively, and infestation percentages (proportion of total canopy foliage contributed by mistletoes) were 70%, 90% and 95%, respectively.

parasitic on Acacia papyrocarpa, establishment is maximal on stems one to six millimetres in diameter and seedlings fail to establish on stems greater than 16 millimetres in diameter. In eucalypts, bark thickness is positively correlated with branch diameter (A.M. Gill, P. Moore and N. Reid, unpubl. data), but the evidence that bark thickness limits establishment of eucalypt-parasitising mistletoes is equivocal. In two experiments on infection of E. blakelyi and E. melliodora by Amyema miquelii, seedling establishment varied significantly with branch size in only one of four host–cohort combinations (Yan and Reid 1995). For each cohort and host, however, maximum establishment occurred on intermediate-sized branches, seven to 20 millimetres in diameter. The frequency distribution of diameters of branches supporting Amyema miquelii on three heavily infected trees of E. melliodora exhibited a modal class of mistletoes on branches of diameter 16 to 20 millimetres (Fig. 15.1). The decline in frequency of mistletoes on

branches greater than 20 millimetres in diameter could indicate that seedling establishment is inhibited by bark thickness on larger branches. In xylem-tapping mistletoes, the haustorial xylem and host xylem grow in a coordinated radial fashion to produce a convoluted disc-shaped surface within the host branch. Infection and haustorial development produce a hypertrophic growth response in the host near the point of infection so that host branch diameter is usually greatest immediately proximal to the haustorium. With Amyema pendula and Amyema miquelii, the exaggerated radial growth of the host xylem soon subsumes the entire cambial activity of small host branches at the point of infection and the host branch distal to the haustorium dies. Other Australian mistletoes of open forest and woodland also commonly come to occupy the distal position on infected branches [e.g. Amyema preissii (Miq.) Tiegh., Tennakoon and Pate 1996].

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Figure 15.2

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P A T H O G E N S

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Various types of haustorium in eucalypt-parasitising mistletoes. Mistletoe tissue is stippled, and the vascular cambium is indicated by a dashed line. a) ‘Ball and socket’ union of Amyema miquelii on Eucalyptus populnea: external view (left) and transverse section of a young attachment; b) elongate haustorial connection of Amyema pendula ssp. longifolia on E. melliodora: external view (right) and longitudinal section showing attachment with a longitudinal strand; and c) haustoria of Muellerina eucalyptoides: transverse section of older attachment on E. acmenoides (left) and external view of runners and a secondary haustorium on Betula platyphylla Sukaczev (from Hamilton and Barlow 1963).

The haustorium is the physical and physiological bridge between the host and parasite and becomes large and woody with age. In xylem-tapping mistletoes, the haustorium contains abundant vessel elements for water conduction but no phloem elements (Kuijt 1977) and is the base from which the aerial shoots of the mistletoe develop. The structure of the haustorium differs among eucalyptparasitising mistletoes. The haustorium of Amyema miquelii develops only at the primary point of infection, forming a globose ‘ball and socket’ union with the host (Fig. 15.2a). Amyema pendula (Spreng.) Tiegh. ssp. longifolia (Hook.) Barlow forms an elongate attachment, with longitudinal strands of

360

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haustorial tissue under the host bark (Fig. 15.2b). From the primary haustorium, Muellerina eucalyptoides produces vine-like runners which spread on top of the bark along the host branches and trunk and subtend secondary haustoria and branch systems (Fig. 15.2c). One individual (genet) of Muellerina eucalyptoides can produce many plants (ramets) as a result of senescence and abscission of connecting runners. 15.2.2.3 Growth and reproduction Information about the growth and longevity of Australian mistletoes is scant. In summarising 15 years of observations of mistletoes in New South

M IS TL ETOES

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Seedling growth rates of Amyema spp. Data are the mean (± 1 s.e.) maximum canopy diameters for an Alice Springs, NT, population of Amyema preissii (deployed in May 1992, open circle) and three cohorts of Amyema quandang: Middleback, SA (March 1983, hatched square); Middleback (July–August 1983, open square) and Atartinga, NT (June 1986, solid square). For Amyema miquelii (Armidale, NSW, October 1990, open triangle), data are the mean (± 1 s.e.) length of the longest shoot.

Wales, particularly eucalypt-parasitising species such as Amyema miquelii, Hartigan (1960) reported that a seedling of two to four leaves grows to a plant with a canopy diameter of one metre in three years and that average life expectancy is 10 years. We have monitored the growth and population dynamics of several species of Amyema in different environments. In Figure 15.3 growth of Amyema miquelii on E. blakelyi and E. melliodora is compared with that of Amyema preissii on a fast-growing acacia and Amyema quandang on a slow-growing acacia. During the first 12 months after seed deployment when early development of the mistletoe endophyte occurs, foliage growth in the slower growing Amyema miquelii and Amyema quandang is minimal. By 24 months, the mean size of the longest shoot of Amyema miquelii is 20 to 30 centimetres. Mistletoes of this size on a shrub or small tree are readily detectable from the ground, but are less easily detected high in the canopy of a mature tree. Eucalypt-parasitising mistletoes reproduce seasonally in temperate Australia. The annual flowering and fruiting seasons of Amyema species in southern

South Australia and Victoria are protracted (Bernhardt 1982; Reid 1986). Amyema miquelii flowers over several months from late summer to late autumn and produces ripe fruit in spring and early summer, while Amyema pendula flowers from mid winter to early summer and fruits from late summer to early winter. Similar phenological patterns are encountered near Armidale at least for Amyema miquelii (Figs 15.4a and 15.4b). In comparison with Amyema, Muellerina eucalyptoides has short annual flowering and fruiting seasons of about two months (Fig. 15.4c). Less is known about the reproductive phenology of arid zone mistletoes but in some species at least, reproduction is strongly seasonal (Reid 1990). In arid South Australia, Amyema miquelii may flower in winter rather than summer–autumn (Reid 1986). Australian Loranthaceae are generally pollinated by birds and tend to have large, yellow to red flowers, 20 to 30 millimetres long (Barlow 1986). The flowers are visited by a variety of honeyeaters (Meliphagidae) and other nectar-feeding birds (Reid 1986; Turner 1991). The suite of pollinating species

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Figure 15.4

A N D

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E U C A L Y P T S

The relative abundance of open flowers (open circle) and ripe fruit (solid circle) on large plants of a) Amyema miquelii, b) Amyema pendula and c) Muellerina eucalyptoides between November 1989 and November 1992 near Armidale, NSW. Data are scaled so that the maximum number of flowers or fruits recorded is equal to 100%. Sample sizes are 33, 25 and 15 plants, respectively, for the three species.

often changes through the flowering period in response to floral density and season (Bernhardt and Calder 1979, 1980; Bernhardt 1983). In open forest remnants near Armidale the floral nectar of eucalyptparasitising mistletoes is a keystone resource determining the structure of the bird community (Barrett and Ford 1993). In summer–autumn, honeyeaters congregate in E. blakelyi and E.

362

melliodora woodland to feed on flowering Amyema miquelii. In winter–spring, the same species are present in E. caliginosa open forest, attracted by flowering Amyema pendula. Reid (1986) described other instances where Amyema pendula and Amyema miquelii become keystone mutualists in providing nectar for temperate honeyeater communities during otherwise lean periods.

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The fleshy fruits of mistletoes (Plate 15.3) consist of a single diaspore within an epicarp. The diaspore consists of the embryo, endosperm and endocarp, surrounded by a nutritive, viscous tissue. In the case of bird-dispersed species, the viscous tissue serves the dual function of attracting dispersers and sticking the seed to the host branch (Barlow 1986). Birds are the main dispersal agents of almost all Australian stem-parasitic mistletoes. The mistletoebird [Dicaeum hirundinaceum (Shaw, 1792)] is the principal disperser (Liddy 1983) and occurs throughout mainland Australia in association with fruiting mistletoes. Other birds, particularly the painted honeyeater [Grantiella picta (Gould, 1838)], spiny-cheeked honeyeater [Acanthagenys rufogularis (Gould, 1838)] and striped honeyeater [Plectorhyncha lanceolata (Gould, 1838)] are effective dispersers in arid and subhumid regions (Reid 1986, 1989; Yan 1993; N. Reid, unpubl. data). In eucalypt forests and woodlands in south and east Australia, pied currawongs [Strepera graculina (Shaw, 1790)] are abundant and consume large quantities of mistletoe fruit, but their status as mistletoe dispersers is doubtful (Brittlebank 1908). Mistletoebirds are efficient dispersers of large-fruited mistletoes. Large seeds stick to the cloaca, requiring the bird to wipe the seed string onto the perch (Reid 1991). If the perch is a living branch of a host species, establishment can be as high as 72% (Lamont 1985). Mistletoebirds mostly perch on branches five to 10 millimetres in diameter and rarely on branches greater than 20 millimetres (Reid 1989). Hence the seedlings of large-fruited mistletoes dispersed by mistletoebirds, including species that parasitise eucalypts, generally establish on branches of diameter less than 20 millimetres. To the extent that all branches in a host population grow at uniform rates, host branch diameter provides an index of mistletoe age. 15.2.2.4 Disperser behaviour and mistletoe population dynamics Mistletoe fruits are retained in the gut of avian dispersers for only a short time. The minimum, mean and maximum passage time of Amyema quandang seeds through the gut of mistletoebirds and spiny-cheeked honeyeaters is 3, 14 and 38 minutes and 16, 41 and 84 minutes, respectively (Murphy et al. 1993). The fruits and seeds of Amyema miquelii and Amyema pendula are similar

ON

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to those of Amyema quandang. Because of the territorial behaviour of both mistletoebirds and honeyeaters (Reid 1990) and the amount of time spent resting in or near mistletoes (Reid 1997a), mistletoe seed shadows probably decline sharply with increasing distance from the maternal plant and are likely to be biased towards existing fruiting mistletoes or special features in the disperser’s home range, such as perch and roost trees, or nests. Most seed dispersal probably occurs over distances of one to 500 metres. Long distance (>10 km) dispersal is likely to be rare but significant, given the propensity for mistletoebirds and honeyeaters to move over longer distances in search of food or territories. The extensive continental distributions of most Australian mistletoe species of open forest and woodland (Barlow 1984) testify to the efficacy of avian dispersal over land. As a result of disperser behaviour, mistletoe populations are often distributed patchily in relation to preferred host species. Mistletoes almost invariably display contagious distributions, with a small percentage of hosts supporting a disproportionately large percentage of parasites (Reid and Lange 1988, but see Hoffmann et al. 1986). Heavily infected eucalypts can host more than 250 mistletoes (Fig. 15.1). Hosts close to neighbours with mistletoes may bear more mistletoes than more distant hosts (Lamont 1985). The age distributions of mistletoes can be ascertained from inventories of host branch diameter, assuming that host branch diameter is an index of parasite age. Figure 15.1 represents the age distribution of an expanding population of Amyema miquelii. Young plants on branches less than 20 millimetres in diameter are most abundant, with decreasing numbers of progressively older mistletoes. Hartigan (1960) described how such an age distribution might be generated. A mistletoe establishes on a young host tree by chance. Once mature, its fruit attracts sporadic visits from dispersers. As the plant grows and annual fruit crops increase in size, birds spend more time in and near the plant and new mistletoe seedlings establish in the host canopy near the original plant, producing satellite infections. Once these seedlings grow to maturity, the enlarged fruit resource leads to increased visitation by dispersers, increased dispersal of mistletoe seed to the host canopy and further cohorts of seedlings.

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15.2.2.5 Mistletoe host resemblance About three-quarters of the mistletoe species of open forest and woodland in Australia closely resemble in vegetative characteristics their usual hosts or a widespread tree species which they commonly infect (Barlow and Wiens 1977) (Plate 15.3). Usually the leaves of the host and parasite have similar shapes and dimensions and are presented in a visually similar way. Consequently, the mistletoe is difficult to distinguish against the background of the host, unless the colour of the foliage differs from that of the host (Plate 15.4). All of the eucalypt-parasitising mistletoes, Amyema miquelii, Amyema pendula and Muellerina eucalyptoides, have leaf shapes and foliage presentation similar to eucalypts. A likely explanation for the phenomenon is the protection afforded to cryptic mistletoes by concealment from their predators (Barlow and Wiens 1977). Ehleringer et al. (1986) showed that Australian mistletoes that mimic host foliage tend to have higher leaf nitrogen contents than the host, unlike non-mimics, supporting the notion that mimics gain a selective advantage from reduced herbivory through crypsis. Mistletoes are predated by a variety of herbivores. Australian mistletoes are heavily predated by jezebel (Pieridae) and azure (Lycaenidae) butterfly larvae (Canyon and Hill 1997), tortricid moths (Olethreutinae) and fruitfly (Tephritidae) larvae, arboreal marsupials (Phalangeridae and Petauridae) and broad-tailed parrots (Platycercidae). Insects use chemical cues to locate food plants and so visual mimicry is unlikely to have evolved in relation to their grazing pressure (Barlow 1986; cf. Canyon and Hill 1997). Nocturnal marsupials and parrots use visual cues to locate food, at least from a distance, and marsupials have monochromatic vision and so they are unlikely to be able to detect differences in foliage colour at night. Arboreal marsupials consume large quantities of mistletoe foliage in certain situations. Heavy browsing of foliage by koalas [Phascolarctos cinereus (Goldfuss, 1817)] killed Amyema pendula at Healesville, Vic. (Campbell 1948). Foliage of Muellerina eucalyptoides comprised 3% of the diet of the greater glider [Petauroides volans (Kerr, 1792)] in Boola Boola State Forest, Vic., increasing to 10% to 12% of the diet during drought (Henry 1985). Greater gliders sometimes eat the foliage of Amyema

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pendula (Kavanagh and Lambert 1990; Porter 1990). Muellerina eucalyptoides was highly sought after, despite being uncommon, by common ringtail possums [Pseudocheirus peregrinus (Boddaert, 1795)] in E. laevopinea forest near Armidale (Porter 1990) and was defoliated by ‘possums’ at Healesville (Coleman 1949). In Porter's (1990) study, ringtails also ate more foliage of Amyema pendula and less eucalypt foliage than expected due to chance alone. Mistletoe leaves are a principal dietary component of common brushtail possums [Trichosurus vulpecula (Kerr, 1792)] in central Australia (Evans 1992; J. Foulkes, pers. comm.) and brushtails preferred the foliage of Amyema miquelii to that of a common host and foodplant, E. fasciculosa, in feeding trials with captive animals (Choate et al. 1987). Young (1937) considered that brushtail possums prefer mistletoe foliage, flowers and fruit and exert a controlling influence on mistletoe spread in south-east Queensland. Arboreal herbivores such as possums have been common in Australian forests since the late Tertiary (Barlow 1986). Since folivorous possums and gliders have well-developed detoxication mechanisms, the cryptic mimicry of mistletoes may be a better defence against herbivores than toxicity. Several species of broad-tailed parrot have been recorded feeding on and destroying the flowers and fruits of Australian mistletoes (Reid 1986). Rosellas (Platycercus) and Australian king-parrots [Alisterus scapularis (Lichtenstein, 1816)] are significant predispersal and postdispersal seed predators of Amyema miquelii and Amyema pendula. They ate an average of 48% of the seeds of both species deployed on eucalypt branches on nine occasions over 14 months near Armidale (Yan and Reid 1995). Broad-tailed parrots ate 23% of the fruit crop of Amyema quandang during peak fruiting in January to February 1991 at Middleback, SA (unpubl. data). Parrots have colour vision and some mistletoes that otherwise mimic their hosts have foliage of a noticeably different colour. Thus the likelihood that parrot predation has influenced the evolution of cryptic mimicry in Australian mistletoes is less convincing than that for nocturnal marsupials, but cannot be discounted, especially in the case of mistletoe species with cryptic fruit (e.g. the yellowish-brown fruit of Amyema pendula) and floral colours [e.g. the green flowers of Amyema maidenii (Blakely) Barlow] (Reid 1986).

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15.2.3 Mistletoe pathology Various mistletoe species were abundant in temperate (Coleman 1950) and arid (Moore 1899; White 1913) Australia early in the history of European settlement. The levels of mistletoe infestation and the resulting debility or death of trees have concerned many observers (Turner 1904; Brittlebank 1908; Anderson 1941; May 1941; Coleman 1949; Greenham and Brown 1957; Hartigan 1960; Kenneally 1973; Lamont 1985; McCarter 1986; Hart 1987; New South Wales Farmers’ Association 1990; Cremer 1990; Reid 1995; Barlow 1996; Thomas 1997). Mistletoes were proclaimed ‘noxious plants’ in Victoria as early as 1904 (Ewart and Tovey 1909). The mistletoe species causing concern and the host trees and districts affected are listed in Table 15.4. Amyema miquelii is the most widespread and damaging parasite of eucalypts in southern and eastern Australia. Amyema pendula also achieves pest status in parts of south-east Australia, particularly Victoria. The effect of mistletoes on host growth and survival depends on the severity of infection. In North America, tree ring analysis in conifers has been used to establish the relationship between severity of infection by dwarf mistletoes and tree growth (Hawksworth and Shaw 1984). Lightly infected trees (i.e. with less than one-third of the canopy infected) show no measurable effects. Moderately infected trees exhibit significant reductions in radial increment, while wood production in heavily infected trees may be reduced by more than 50%. In general, height growth rates are more markedly reduced than diameter growth rates. Moderately and heavily infected trees also suffer increased mortality (Hawksworth and Geils 1990). Effects of dwarf mistletoe on host growth may also depend on tree age. Large trees in an old-growth stand of Pinus contorta Douglas ex Loud. suffered less reduction in growth rate than younger trees in regenerating and mature stands nearby (Hawksworth et al. 1992). The only comparable Australian data pertain to the effects of Amyema miquelii on three species of eucalypt, although heavy mistletoe infection is thought to kill many species of host tree in Australia (Table 15.4). Heavily infected E. blakelyi trees (mean crown infection of 59%) were significantly more likely to survive 33 months after mistletoe removal than matched control trees with a mean crown

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infection of 63% (Reid et al. 1994). In the same experiments, the mean increase in host foliage biomass over the same period attributable to removal of Amyema miquelii was 22% in E. blakelyi and 24% in E. melliodora (mean crown infection of 48% to 49%). The average increase in radial growth attributable to mistletoe removal was 55% in E. blakelyi and 49% in E. melliodora. Trees of E. polyanthemos with an average crown infection of 38% had a 55% reduction in stem diameter increment over 15 months, whereas trees with an average crown infection of 15% had an 11% reduction in radial increase over 18 months (Nicholson 1955). The pathogenicity of ‘pest’ mistletoes is curious, given the biological adage that well-adapted parasites do not kill their hosts. Eucalypt-parasitising mistletoes with a ‘ball and socket’ haustorial structure (e.g. Amyema miquelii and Amyema pendula ssp. pendula) assume a terminal position over time and suppress the activity of dormant buds and vegetative growth along the host branch proximal to the haustorium (Jacobs 1955). The mode of suppression of host buds proximal to the haustorium is unknown. Hormonal suppression cannot be supported currently because a reverse flux of organic compounds from parasite to host has not been detected in xylem-tapping mistletoes (e.g. Raven 1983; cf. Nicholson 1955). The simplest hypothesis to account for the rapid debility and death of the host's distal branch must therefore postulate that through tight regulation of water use, the mistletoe becomes a powerful sink for the host's transpiration stream so that the distal host foliage attracts few resources and host buds proximal and distal to the sink remain dormant. This hypothesis is based on the assumption that host buds are activated by the absence of a strong sink for xylem sap along a branch, rather than being suppressed by hormonal control originating in an apical meristem. If the mistletoe is removed from the branch, dormant host buds frequently resprout below the cut despite the absence of distal foliage (Jacobs 1955; Reid et al. 1994). In ‘pest’ mistletoes such as Amyema miquelii, Amyema pendula ssp. pendula and Amyema preissii, progressive infection of host branches leads to the point where little or no host foliage remains on heavily infected trees because host branches distal to mistletoes die and host buds proximal to infections

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Mistletoe species (Loranthaceae and Viscaceae) responsible for debility or death of host trees and shrubs in Australia

Mistletoe

Hosts

District

References

Amyema congener (Sieber ex Schult. & Schult. f.) Tiegh.

Fruit trees

Coastal NSW

May (1941)

Amyema miquelii (Miq.) Tiegh.

E. wandoo

Mt Barker, WA

Kenneally (1973)

Amyema miquelii

Mallee eucalypts

Bute and N. Yorke Peninsula, SA

McCarter (1986); Rudd (1990)

Amyema miquelii

E. leucoxylon

Keyneton, SA

Cleland (1940b)

Amyema miquelii

E. leucoxylon

Clare, SA

Anon. (1993); Kahn (1993)

Amyema miquelii

Eucalypts

Southern Flinders Ranges (Pitchi Ritchi Pass, Port Germein Gorge, Wilmington and Quorn), SA

J. Choate (pers. comm.)

Amyema miquelii

E. camaldulensis, E. leucoxylon, E. melliodora, E. microcarpa, E. polyanthemos, E. sideroxylon

Victoria

Coleman (1949); Calder et al. (1979); Calder (1981, 1997); DCFL (no date); Fagg (1997); Thomas (1997)

Amyema miquelii

Eucalypts

NSW

May (1941)

Amyema miquelii

E. polyanthemos

Southern Tablelands, ACT and NSW (e.g. Canberra, Tharwa, Gundaroo)

Greenham and Brown (1957); Brown (1959); N. Reid, pers. obs.

Amyema miquelii

E. blakelyi, E. melliodora, E. sideroxylon

Northern Tablelands and North-west Slopes, NSW

N. Reid & Z. Yan, pers. obs.

Amyema miquelii

C. maculata, E. tereticornis, E. microcorys

South-east Qld

Young (1937); Anon. (1945)

Amyema pendula (Spreng.) Tiegh. ssp. pendula

Mostly eucalypts

Victoria

Calder et al. (1979); Calder (1981, 1997); Fagg (1997)

Amyema pendula ssp. pendula

E. laevopinea

Uralla, NSW

N. Reid & Z. Yan, pers. obs.

Amyema pendula ssp. pendula

E. pauciflora

Ebor, NSW

N. Reid, pers. obs.

Amyema pendula ssp. pendula

E. polyanthemos

Heyfield, Vic.

Fagg (1997)

Amyema pendula ssp. pendula

E. viminalis

Armidale, NSW

N. Reid, pers. obs.

Amyema quandang (Lindl.) Tiegh.

Acacia spp. including Acacia terminalis (Salisb.) J.F.Macbr.

Victoria

Coleman (1949); Calder (1981, 1997)

Kalamunda, WA

Lamont (1985)

Acacia victoriae Benth.

Alice Springs, NT

Reid et al. (1992)

Acacia acuminata Benth.

WA Wheatbelt

Lamont and Perry (1977); Lamont and Southall (1982)

Amyema preissii (Miq.) Tiegh. Several Acacia species

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Mistletoe

Hosts

District

References

Amylotheca dictyophleba (F.Muell.) Tiegh.

Cypress pine (Callitris)

Fraser I., Qld

Young (1937)

Dendrophthoe glabrescens (Blakely) Barlow

Fruit trees

Coastal NSW

May (1941)

Dendrophthoe glabrescens

Brachychiton populneus (Schott & Endl.) R.Br.

North-west Slopes and Plains, NSW

May (1941)

Korthalsella rubra (Tiegh.) Endl. ssp. geijericola Barlow

Geijera parviflora Lindl.

Quambone, Nyngan, Gunnedah, NSW

May (1941); N. Reid, pers. obs.

Lysiana exocarpi (Behr) Tiegh.

Casuarina, Acacia melanoxylon R.Br.

Myrniong, Vic.

Brittlebank (1908)

Muellerina eucalyptoides (DC.) Barlow

Eucalypts and several other native and introduced trees

Victoria

Ewart and Tovey (1909); Calder (1981)

Muellerina eucalyptoides

Fruit trees

Coastal NSW

May (1941)

Muellerina bidwillii (Benth.) Barlow

Cypress pine (Callitris)

South-east Qld

Young (1937)

remain dormant (Jacobs 1955; Tennakoon and Pate 1996). The death of heavily infected hosts often occurs with the onset of water stress in late spring or early summer (N. Reid, unpubl. data), presumably because the tree's fine-root system is starved of photosynthate and insufficiently developed to provide water and mineral nutrients to the host's tissues. On the other hand, drought and water stress may disadvantage mistletoes more than lightly infected hosts. Amyema pendula is sensitive to severe water stress, and mistletoe defoliation and death frequently occur after drought (Calder et al. 1979). The effect of ‘pest’ mistletoes on eucalypt survival contrasts with the effects of benign mistletoes such as Amyema quandang on Acacia papyrocarpa (Reid and Lange 1988) and creeping mistletoe (Muellerina eucalyptoides) on eucalypt hosts near Armidale. These benign species are characterised by vegetative resprouting and secondary haustoria either in the form of a ramifying subcortical haustorium (Amyema quandang) or external runners (Muellerina eucalyptoides). Both species permit the host branch distal to infections to survive so that field evidence of dead, heavily parasitised hosts is rare. The pathogenicity of Muellerina eucalyptoides varies geographically, however, as in Victoria it allegedly spreads through the host canopy which is eventually killed (Ewart and Tovey 1909). Variations in the pathogenicity of mistletoes are related partly to between-habitat differences in fire regimes and host longevity (Reid et al. 1995). In fire-prone

15

environments such as eucalypt woodlands and open forests, it is likely to be selectively advantageous for fire-sensitive mistletoes such as Amyema miquelii and Amyema pendula (Kelly et al. 1997) to extract as many resources as possible from hosts prior to the next fire, in order to grow quickly and initiate sexual reproduction early, irrespective of the medium-term consequences for the host. On long-lived hosts in stable environments in which fire does not occur, a more benign parasitic strategy is likely to evolve (Reid and Lange 1988). Since host-mistletoe interactions vary with species of host and parasite and with environment, experiments are needed to establish whether mistletoe infection is responsible for host debility or death in particular field situations.

15.2.4 Factors contributing to expanding mistletoe populations Many authors have claimed that mistletoe populations have increased in rural districts since about 1900 (Turner 1904; Brittlebank 1908; Anderson 1941; May 1941; Coleman 1949; Greenham and Brown 1957; McCarter 1986; Fagg 1997; Thomas 1997). Mistletoe increase has been associated with land clearance and thinning of trees for agriculture, housing and roads. In temperate Australia, mistletoe infestation is especially apparent on trees that are isolated, in thinned stands, in small stands in paddocks, around stockyards and

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homesteads, along roadsides or on the edge of large stands and forest margins (May 1941; Hartigan 1960; Kenneally 1973; Calder et al. 1979; Lamont and Southall 1982; Lamont 1985; Hart 1987) (Plates 15.1 and 15.2). In arid Australia, mistletoes are often abundant along rivers, creeks and washes and near stockwaters (May 1941; Beadle 1948). The popular impression of expanding mistletoe populations in managed semi-natural landscapes needs to be tempered by two caveats: 1

no long-term datasets have been published that demonstrate that mistletoe populations are increasing or spreading

2

sharp reductions in local mistletoe populations sometimes occur due to fire (see following paragraph), drought, or insect or fungal attack (Blakely 1922a, 1922b; May 1941; Chaffer 1966; Keast 1995). The extent to which local population increases are balanced by declines elsewhere is unclear.

Five hypotheses have been proposed to explain increases in mistletoe abundance in temperate Australia. The hypotheses are not mutually exclusive and each may operate to varying degrees in different districts and at different times. The first postulates that fire is a natural control agent of mistletoe distribution and abundance, and that fire suppression in agricultural districts since European settlement has permitted fire-sensitive mistletoe populations to increase (May 1941; Reid 1997b). Liddy (1982) ascribed high population densities of Amyema cambagei (Blakely) Danser and hyperparasitic Notothixos subaureus Oliv. in coastal Casuarina glauca Spreng. open-forest in south-east Queensland to the cessation of annual burning 12 years previously. Most of the open forests and woodlands that occur in agricultural districts would have been burnt frequently before European settlement, either as a result of wildfire or human activity (Gill et al. 1981). Most eucalypt species can survive fires by sprouting from lignotubers or epicormic buds. In comparison, eucalypt-parasitising mistletoes are killed by intense fires (Cleland 1940a; Gill and Moore 1993). In South Australia, Amyema miquelii was abundant on gums in Belair Recreation Park near Adelaide and on E. leucoxylon in the Clare Valley before the February 1983 bushfires. Most of the eucalypts but

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few mistletoes survived in the burnt areas (Anonymous 1993; Z. Yan, unpubl. data). In trials with a portable kerosene flamethrower, thorough burning resulting in complete canopy scorch killed all but one of 21 individuals of Amyema miquelii and Amyema pendula within two years (Table 15.5). By chance, 2% to 5% of the canopies of another three Amyema miquelii plants were not scorched by the flamethrower and all three survived. In a second series of experiments with similar equipment (Kelly et al. 1997), burning involving either single or double passages of flame across the mistletoe canopy killed 38% of mistletoes (Amyema miquelii, Amyema pendula) compared to 11% mortality resulting from severe branch pruning and none resulting from complete defoliation. After two years, leaf-pruned Amyema miquelii had almost managed to recover their pretreatment dimensions, but burnt and pruned plants were still markedly smaller. After intense wildfires, mistletoes must recolonise from beyond the limits of the fire or from scattered survivors (Gill 1996). The second hypothesis to account for mistletoe increase in fragmented habitats is a decline in abundance of the arboreal marsupials that feed on mistletoes (May 1941; Reid 1997b). Mistletoe increase in the early part of the twentieth century coincided with the decline of possums and koalas as a result of uncontrolled hunting (Young 1937; May 1941; Troughton 1965) and the reduction and fragmentation of forested and wooded habitats in agricultural districts. In cleared pastoral country in western Victoria, common ringtail possums occur only in forest remnants larger than three hectares (Bennett 1990) and in the central wheatbelt of Western Australia common brushtail possums are extinct owing to habitat loss and fragmentation (Hobbs et al. 1994). Isolated trees and small stands in paddocks and along fences and roads do not provide sufficient food or protection for either species. Predation by foxes in temperate districts (A. Smith, pers. comm.), the scarcity of old-growth (habitat) trees in stands of native timber as a result of past ringbarking and clearfelling, and the susceptibility of common brushtail possums to poison (sodium monofluroacetate) baits laid for rabbits, have also contributed to the low density or disappearance of larger arboreal marsupials in many agricultural districts. The behaviour of

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Resprouting and survival of two species of mistletoe after complete canopy scorch using a portable pump-action flamethrower (weedburner)

Burning experiments were conducted near Armidale, NSW, in January and February 1990. Resprouting was measured on three occasions up to 18 months after burning and survival was measured 24 months after burning. Canopy heights and widths of large mistletoes ranged from 0.9 to 2.6 metres and 0.6 to 1.7 metres, respectively. The maximum canopy diameter of small mistletoes was ≤ 0.5 metre.

Duration of scorch (s)

No. of mistletoes

Mistletoe

No. burnt

Size

Mean (± s.e.)

Range

Resprouters

Survivors

Amyema miquelii

16

Large

65 ± 8.9

30–120

4

1

Amyema miquelii

6

Small

16 ± 2.6

10–25

0

0

Amyema pendula

2

Large

60 ± 42.4

30–90

0

0

arboreal marsupials may also partly explain the concentrations of mistletoes along forest margins and at the edges of woodlots. Near Armidale, common ringtail possums frequently feed on mistletoes in trees in the forest but seldom at the forest edge or in isolated trees, despite the high abundance of mistletoes there (Porter 1990). Arboreal marsupials may be reluctant to venture into edge habitats due to the greater risk of predation. A third hypothesis that may explain the pattern of mistletoe infestation in rural landscapes relates to the behaviour of mistletoe dispersers. On an evolutionary time scale, the mistletoebird is a recent arrival in Australia from south-east Asia (Reid 1987), and may therefore prefer reduced competition in disturbed landscapes to competing with the many bird species found in native forests and woodlands. Since mistletoebirds are unlikely to spend long in either disturbed or undisturbed habitats lacking fruiting mistletoes, this hypothesis is difficult to test: the greater abundance of mistletoebirds in disturbed landscapes may simply reflect the greater abundance of food plants in such habitats. Several authors have suggested that, as the number of potential host trees is reduced through land clearance and tree decline, the activities of dispersers are restricted to fewer trees, causing aggregation of mistletoes on remaining trees (Anderson 1941; Greenham and Brown 1957; Barlow 1986). In a recently cleared or thinned landscape, host tree abundance is unlikely to decline without concomitant reductions in mistletoe density and disperser abundance, due to the stochastic nature of clearing of infected host trees (cf. Turner 1991). Nevertheless, in long-cleared landscapes, the few remaining paddock and edge trees necessarily attract most use by birds (Hartigan 1960).

The fourth hypothesis concerns the effect of semideveloped landscapes on host tree physiology and the consequent quality of such trees as mistletoe habitat. Trees that are isolated, at the edge of stands, or in thinned stands have greater access to water and nutrients than interior trees in unthinned forest and woodland because of release from competition with neighbours. Roadside trees have increased water and nutrients from road runoff, and trees in improved pasture have access to greater quantities of phosphorus and nitrogen. These changes to the water and nutrient balance of eucalypts in agricultural districts predispose farm trees to chronic insect defoliation in parts of south-east Australia (see Chapter 17). The same changes may also encourage mistletoe infestation of farm trees that escape chronic insect attack. Mistletoe seedlings establishing on such trees must sequester a larger quantity of water and nutrients than seedlings attempting to establish on trees in forest and woodland interiors. During drought, the severity of water stress will be reduced in host trees freed from competition with neighbours. Thus, mistletoe growth and survival is likely to be higher on edge and isolated trees than on interior trees. Light may be important in the context of mistletoe habitat quality. Some mistletoe species are shade-intolerant (Kuijt 1969) and so mistletoes may prosper under high light conditions associated with the exposure of isolated or edge trees (Greenham and Brown 1957; Barlow 1986). No experiments have been conducted to evaluate this possibility. The fifth hypothesis concerns the growth habit of host trees and the persistence of tree branches in semideveloped landscapes. Forest tree species growing in isolation or on the edge of forests develop the deliquescent habit of woodland trees. Branches

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survive longer than in a regenerating forest where, due to shading and competition from neighbours, lower branches are continuously shed by actively growing trees. The branches of isolated and edge trees on which mistletoe seedlings establish have a higher probability of persistence than those of a forest tree, leading to increased longevity of mistletoes. Indeed, the difference in branch demography between woodland and forest trees may partly explain why mistletoes are more abundant or conspicuous in Australian woodlands than forests.

15.2.5 A conceptual model of mistletoe population abundance in agricultural districts The information reviewed in the preceding sections permits the development of a conceptual model of mistletoe infestation of eucalypts and their management in agricultural districts in south and east Australia (Fig. 15.5). The model presumes that the eucalypt hosts of the mistletoe population are widespread in the district and are reasonably long lived. Before land clearance and development, the abundance of mistletoes at a landscape level is low because of frequent fires, droughts and suppression by high densities of natural predators. The effect of land clearance on mistletoe abundance is initially negative because of the death of most of the host trees and mistletoes (e.g. Turner 1991). Over time, as factors such as fire suppression, increased vigour of remnant trees and the decline or extinction of arboreal marsupials, broad-tailed parrots and mistletoe-specific moths and butterflies take effect, mistletoe populations start to increase and expand, slowly at first, and then at an increasing rate as a result of increasing populations of avian dispersers. The degree of mistletoe infestation peaks (at point A in Fig. 15.5) for one of several reasons. With increasing mistletoe abundance, heavily infected host trees die at an increasing rate, counteracting the growth in mistletoe numbers on lightly infected trees. Continuing land clearance or phenomena such as dieback (Heatwole and Lowman 1986) reduce tree density to a critical level that no longer provides adequate cover and habitat for dispersers. Finally, stands of trees become functionally although not physically saturated with mistletoes because avian vectors disperse virtually all seeds to mistletoes or infected trees rather than to uninfected trees.

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From point A (Fig. 15.5), two scenarios are possible. Scenario B envisages continuing land clearance or tree decline, reducing tree density to the extent that disperser populations are unable to survive. In other words, mistletoe populations will decline to extinction in landscapes with very low densities of trees. This is happening in the central wheatbelt of Western Australia where original vegetation has been reduced to 7% of the landscape, mostly in small fragments (< 100 ha), the mistletoebird is probably now extinct, and Amyema miquelii faces regional extinction (Norton et al. 1995). The remaining patches of mistletoe are the ‘living dead’ unless active and costly propagation and management of salmon gum (E. salmonophloia) habitat is undertaken and mistletoes are assisted to disperse from tree to tree by human agency. Scenario C, however, envisages adoption of management strategies based on principles outlined below, to create resilient vegetation stands which contain checks and balances to avoid the buildup of excessive mistletoe infestations and permit moderate levels of mistletoe to be sustained regionally.

15.2.6 Management of mistletoes In the agricultural districts of south and east Australia, land clearance, rural tree decline and modification of understorey vegetation have been substantial. Loss of native vegetation has contributed to land degradation and dwindling biodiversity (State of the Environment Advisory Council 1996). Many landholders are attempting to restore woody perennial vegetation to croplands and pasture in order to sustain or increase agricultural productivity, encourage wildlife and maintain an attractive environment (Cremer 1990; Thomas 1997). The damage caused by mistletoes in largely deforested rural landscapes is important because the scattered remnant trees and stands that are valuable for agricultural production and nature conservation are preferentially infected (Hartigan 1960). In the short term, direct control methods are required to save heavily infected trees. In the longer term, preventative management strategies are needed that avoid the buildup of serious mistletoe infestations and permit moderate infestations to be tolerated. 15.2.6.1 Biological control Classical biological control is limited to situations where a pest species has prospered outside its natural geographical range and therefore outside the range of

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A conceptual model of the relative abundance of mistletoe (continuous line) on a widely distributed host species in agricultural districts in temperate Australia. The shaded zone indicates a major period of land clearance, resulting in reduced abundance of native trees (broken line). A indicates the peak in mistletoe infestation. In scenario B, land clearance and tree decline eliminate almost all host trees from the area. In scenario C, a substantial proportion (> 20%) of the district is maintained under native tree cover and is managed to permit natural regeneration and to control severe mistletoe infestations.

its natural predators, parasites and pathogens. The mistletoe, Scurrula cordifolia (Wall.) G.Don, was previously confined to the western Himalayas, but spread to the Sivalik Hill region in northern India in the 1970s where it damaged valuable fruit and timber trees (Pundir 1981). In 1972, a second mistletoe, Viscum loranthi Elmer, was observed to hyperparasitise Scurrula cordifolia. In the ensuing eight years, Viscum loranthi spread rapidly, resulting in a sharp decrease in the abundance of Scurrula cordifolia. Viscum loranthi is an obligate hyperparasite, only infecting other mistletoes (Pundir 1981). In a similar vein, Kahn (1993) suggested that the abundance of the hyperparasitic harlequin mistletoe, Lysiana exocarpi (Behr) Tiegh., might be encouraged to help control Amyema miquelii in the Clare Valley, SA. Since Australian mistletoes have become pests within their normal geographical range, natural predators and control agents have presumably declined in abundance or efficacy. In these situations, the simple reintroduction of a formerly abundant predator or hyperparasite is unlikely to be helpful because the original reason for their decline may remain. The reintroduction of common brushtail possums in Pitchi Ritchi Pass, SA, in the 1940s failed because of lack of habitat for the animals (Coleman 1949). Long-term mistletoe management strategies will need to focus on providing opportunities for formerly abundant predators such as arboreal marsupials or hyperparasites such as Lysiana exocarpi.

15.2.6.2 Surgical methods Lopping is the most effective means of treating mistletoe infections but it is labour intensive and expensive. Lopping involves cutting the infected host branch proximal to the mistletoe haustorium so that all mistletoe tissue is removed to prevent resprouting. In the past, the treatment of tall trees was difficult, but the widespread availability of hydraulic bucket hoists (‘cherrypickers’) means that treatment is now generally possible, if costly (Fagg 1997). Eucalyptus blakelyi and E. melliodora with 90% of the canopy consisting of Amyema miquelii foliage can be treated successfully (Reid et al. 1994). Lopping Amyema miquelii from heavily infected eucalypts requires a follow-up treatment because the many seedlings usually present on such trees are not obvious at the time of treatment. A second lopping is desirable two to three years after the first, by which time the young plants are conspicuous but have not yet grown to a size capable of significant fruit production. Lopping is usually impractical where many trees require treatment. Mistletoes such as Muellerina eucalyptoides, which have multiple, often widely spaced haustoria, may be difficult to treat surgically. For eucalypt species that can resprout from the main limbs, trunk or lignotuber, the pollarding or felling of infected trees is a viable if severe alternative to lopping infected branches. Pollarding involves removal of the canopy, leaving the bases of the main limbs and trunk. Pollarding of mallee eucalypts in roadside vegetation was authorised by the local

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authorities in South Australia to treat Amyema miquelii infestations (Rudd 1990). The work was carried out by contractors who sold the timber for firewood. The mallees resprouted and trees with large hollow branches were left for wildlife. Near Armidale, NSW, landholders are pollarding E. blakelyi and E. melliodora infected by Amyema miquelii and have reported less than 5% host deaths (Curtis and Wright 1993; T. Wright and B. Coop, pers. comm.). When infected trees are pollarded or felled in grazing areas, it is important that they be cut above browsing height to ensure that eucalypt regrowth is not impaired by livestock. In commercial coniferous forests in North America, silvicultural treatment of stands infected with dwarf mistletoe is a preferred management option (Hawksworth and Shaw 1984). In Australia, silvicultural management involves removing one or a few heavily infected trees where the trees are a potential seed source for the infection of adjacent younger or uninfected trees (Fagg 1997). This is a suitable option in eucalypt forests managed for timber production. However, in rural districts where landholders wish to retain remaining trees, pollarding and pruning will be the preferred means of treating heavily infected eucalypts (Thomas 1997). A final variant of the surgical approach for mistletoe control is the use of a rifle to shoot infected branches that are beyond the reach of other methods. This method is practised to a limited extent on the Northern Tablelands of New South Wales. 15.2.6.3 Chemical treatments Hormone-based herbicides, principally 2,4-dichlorophenoxyacetic acid (2,4-D), were sprayed to control eucalypt-parasitising mistletoes (mainly Amyema miquelii) in South Australia, New South Wales and Western Australia in the 1940s and 1950s (Anonymous 1949; Harding 1959; Hartigan 1962). Mistletoes are more susceptible than eucalypts to 2,4-D and can be sprayed at an appropriate dose without damaging the host. Nevertheless, hormone sprays are not popular for several reasons: 1

the need to treat tall trees with a mobile high pressure pump and spray unit

2

the use and cost of large quantities of herbicide

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3

the problem of herbicide drift for operator safety and non-target foliage

4

non-eucalypt hosts of problem mistletoes (e.g. casuarinas, acacias and Brachychiton) are susceptible to 2,4-D and therefore cannot be treated if their foliage is likely to be sprayed

5

the method results in only about 90% mortality of mistletoes from one application.

A second method of herbicide application is injection into the host stem (Greenham et al. 1951). The underlying principle is that dilute solutions of certain herbicides injected into the trunk will be translocated throughout the canopy and will kill or damage mistletoes but not seriously impair the host tree. Between 1948 and 1963 many different organic and inorganic compounds were tested in several localities for control of Amyema spp. and acceptable results were obtained with seven out of eight eucalypt species (Greenham and Brown 1957; Brown and Greenham 1965). Mistletoe mortality of between 70% and 100% was recorded using the triethanolamine or hydrazine salt of 2,4-D, with temporary defoliation of some of the host trees and up to 5% host mortality. A method of rapidly applying the correct doses of herbicide to trees of a range of sizes using a modified axe was developed and costed at A$0.05 per tree in 1959 (Brown 1959) and A$7.13 per hectare in commercial forests of E. tereticornis at Imbil, Qld, in 1988 (J.C. Murphy, pers. comm.). Trunk injections of glyphosate and triclopyr (ester) were also trialled for the control of Amyema miquelii and Amyema pendula on 11 species of eucalypt near Myrtleford, Vic. (Minko and Fagg 1989). Some injections of particular eucalypt species on specific dates achieved modest levels of mistletoe control, with no tree mortality (Table 15.6). Mistletoe mortality ranged from 20% to 83% depending on the species, with an average of 57%. At a 20% host death rate, average mistletoe kill increased to 71%. The advantages of trunk injection over spraying are that the former requires smaller amounts of chemical, can be carried out by individuals with inexpensive equipment and can be used to treat infections that are inaccessible by spraying. Nevertheless, the trunk injection approach has several limitations, as follows.

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TA BLE 15. 6

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Best results achieved by stem injections of triclopyr (480 g/L) and glyphosate (360 g/L) for mistletoe (Amyema pendula and Amyema miquelii) control with no host mortality, on 11 species of eucalypt near Myrtleford, Vic. (from Minko and Fagg 1989) Herbicide (dilution in water)

Application date

Mistletoe mortality (%) Treatment

ControlA

E. bridgesiana

Triclopyr (1:4)

Jan. 1985

80

—

E. camaldulensis

Triclopyr (1:4)

Apr. 1985

40

—

E. dives

Glyphosate (1:3)

June 1984

60

21

E. globulus

Triclopyr (1:4)

Oct. 1985

83

—

E. goniocalyx

Triclopyr (1:4)

Jan. 1985

71

—

E. macrorhyncha

Glyphosate (1:3)

June 1984

59

18

E. melliodora

Triclopyr (1:4)

Jan. 1985

62

—

E. ovata

Glyphosate (1:3)

Jan. 1985

35

—

E. polyanthemos

Glyphosate (1:3)

Jan. 1985

57

—

E. radiata

Glyphosate (1:3)

June 1984

65

16

E. sideroxylon

Glyphosate (1:4)

Oct. 1985

20

—

A

Control data by species were reported only for June 1984. Mean mistletoe mortality (%) over all eucalypt species on control (untreated) trees was 5% in January 1985, 5% in April 1985, 6% in July 1985 and 1% in October 1985.

1

2

3

Host and mistletoe responses can be unpredictable and may vary with species of mistletoe and host, location, herbicide and season (trials should be conducted before large-scale application of the method; Minko and Fagg 1989). Most of the experimental work has been conducted on trees with a few large mistletoes rather than on heavily infected trees (Brown 1959; Brown and Greenham 1965; Minko and Fagg 1989). Since heavily infected trees are more likely to succumb to the herbicide treatment (Greenham and Brown 1957), the method is least appropriate for the trees most in need of treatment. Although some species of eucalypt have responded similarly to given doses of herbicide, others have responded differently perhaps because of variable crown width to trunk diameter ratios (Brown 1959). Similarly, although herbicide doses have been calibrated for trunk size (Greenham and Brown 1957), Minko and Fagg (1989) found that small trees (with trunks less than 30 cm diameter) were more susceptible to death from trunk injections than larger trees, suggesting that further

refinement of the dose to trunk diameter relationship is needed. 4

Complete control is unlikely, treatment may take two years to be fully effective and young mistletoes are less susceptible than older plants (Greenham and Brown 1957).

5

Infected trees should not be treated in drought or unusually wet conditions because host and mistletoe responses are unpredictable (Greenham and Brown 1959; Brown and Greenham 1965).

6

As with the spray method, non-eucalypt hosts may be as susceptible as mistletoe to trunk injections of dilute herbicide and so cannot be treated.

15.2.6.4 Fire Fire may be a cheap and effective means of controlling fire-sensitive mistletoes. Prescribed burning successfully controls dwarf mistletoe infestation in North America (Koonce and Roth 1980, 1985; Harrington and Hawksworth 1990), but little work has been conducted in Australia on the use of fire for mistletoe control. A blowlamp-type weed burner (with a 75 cm flame, 1100°C) was used on Yorke Peninsula, SA, to control low Amyema miquelii on mallee and gums, with reportedly

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excellent results (Anonymous 1949). ‘Flame throwers’ were trialled in 1947 near Canberra, but the approach was not promising for unstated reasons (Greenham and Brown 1957). A flame thrower and cherrypicker were used in suburban Adelaide to burn Amyema miquelii on street trees with satisfactory results (E. Robertson, pers. comm.). Small flamethrowers of the kerosene weedburner type are unlikely to be popular for mistletoe control because the flame is small (up to 3 m) and the approach offers no advantage over surgical treatment with a chainsaw. Military flamethrowers, in which the flame engulfs the entire tree, may have practical application for treating severe infections. Trials are also required to evaluate the efficacy of individual bonfires beneath heavily infected trees to control mistletoes in the canopy above.

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trees are heavily infected, the mistletoes can be removed easily. 3

Revegetation of large stands of trees is preferable to small stands, in order to create stand interiors where trees are less prone to mistletoe infection.

4

Large stands of trees are also likely to support larger arboreal marsupials and broad-tailed parrots that may be instrumental in mistletoe control, particularly if some of the trees are hollow-bearing. Corridors of suitable habitat between large stands of trees need to be maintained or revegetated to facilitate the movement of wildlife.

5

Mistletoe-resistant plants can be used for revegetation in addition to susceptible stocks. Resistant trees and shrubs can be planted around susceptible individuals to act as barriers to local buildup of mistletoe populations. Selection of mistletoe-resistant plant species and provenances is a common silvicultural practice in the United States (Hawksworth and Johnson 1989). Because of the need to conserve local biodiversity, revegetation activities should concentrate on using local provenances of trees and shrubs where local environmental conditions have not been altered by farming. Hence, the germplasm of non-host species and of individuals of host species that appear (based on their uninfected state despite their close proximity to heavily infected individuals) to be resistant to mistletoe infection, should be collected for propagating mistletoe-resistant local plants.

6

The early removal of large mistletoes will prevent future severe infestations. Despite this, eucalypts can be left until an advanced state of infection before control is necessary to prevent tree death.

15.2.6.5 Long-term strategies Mistletoes take from several to many years to severely infect host eucalypts (Hartigan 1960). The mistletoe problem in rural Australia thus lends itself to long-term strategies that prevent the buildup of mistletoe populations or enable moderate levels of mistletoe infestation to be tolerated. Strategic planning of native vegetation management and restoration at the property, landscape and catchment level offers the best long-term strategy and should be based on the following principles. 1

2

In semicleared grazing lands where mistletoe infestation has or is likely to cause tree mortality, the natural regeneration and planting of trees will provide or maintain beneficial tree cover for livestock, pastures, wildlife and aesthetics. Managing for natural regeneration (i.e. the continual or periodic recruitment of young trees) is important because mature trees will eventually die anyway (because of mistletoes, dieback or old age). The managed regeneration of naturally occurring tree populations avoids the periodic need for expensive revegetation works, preserves local biodiversity and regional character and may provide a source of fence posts, strainers, fuelwood and other products. Stands of young regenerating trees will not tend to be infected by mistletoes because large trees are the natural focus for bird activity. If young

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15.2.6.6 Conclusions There are no easy solutions to the mistletoe problem in the rural districts of southern and eastern Australia. The infection of isolated trees and small stands is attributable to the complex interplay of deforestation and tree thinning, grazing-induced suppression of natural tree regeneration, local extinction of mistletoe predators, the lack of prescribed burning in more intensively developed landscapes, suppression of wildfires and bird

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behaviour. Unfortunately, the relative contribution of these factors to the dynamics of local populations of mistletoes is unknown. Experiments are required to disentangle the effects of host genotype, growth habit, branch longevity, nutrition, water status and canopy irradiation on mistletoe establishment, growth, fecundity and survival. Careful observations are required of the behaviour of avian dispersers during the fruiting seasons of mistletoes to determine the factors that influence the birds' movements and use of space. In particular, the importance of the density and dispersion of hosts and fruiting mistletoes, tree and mistletoe size and the location of nests, song trees, perch trees and territorial boundaries need to be determined in order to predict disperser movements and seed dispersal. Finally, a landscape ecology perspective will be helpful in determining the influence of patterns of habitat fragmentation and host density and configuration on mistletoe population dynamics. In the short term, surgical control methods, herbicides and fire offer expensive means of saving heavily infected individual trees. Pollarding is a more severe means of treating eucalypts and other tree and shrub species capable of resprouting, over larger areas. There seems considerable potential for the development of novel approaches to treating heavy infections on individual trees. We foresee further interest in ultralight surgical equipment operated from the ground, mistletoe-specific herbicides, remotely controlled aerial herbicide-delivery systems, military flamethrowers and individual bonfires for mistletoe control. Progress with such research and development will be slow, however, given the low priority afforded to rural vegetation management. Lasting solutions for avoiding or tolerating mistletoe infestations need to be based on a planned approach to the management of native vegetation. Guidelines for treating, avoiding and tolerating mistletoe infestations need to be developed and incorporated in property and catchment planning schemes. Long-term plans for mitigating the effect of mistletoes on farms will: 1

require the natural regeneration of native tree and shrub populations in pastures and croplands

2

make provisions for habitat for arboreal marsupials, parrots and insects that depend on mistletoes as a food source

3

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specify the judicious use of mistletoe-resistant plant stocks as barriers to mistletoe spread in stands and landscapes prone to infestation.

Two important priorities for research are indicated. First, we need to understand how landscape patterns in tree cover affect the abundance and dispersion of mistletoes. This work will need to focus both on bird behaviour and the water and nutrient status of host trees and mistletoes, and their response to changes in land use and tree density and configuration. The second research priority is to better understand the genetics and pathology of mistletoe infection of local and non-local provenances of susceptible tree species. The work will need to evaluate the utility of mistletoe-resistant provenances of susceptible species in revegetation and the possibility of selecting and breeding mistletoe-resistant trees.

15.3 Native cherries parasitic on eucalypts Of the nine species of native cherry (Exocarpos) in Australia, six are widespread in eucalypt forest, woodland or shrubland (mallee and coastal scrub) in south, east or north Australia and are likely to frequently parasitise eucalypts: Exocarpos aphyllus R.Br., Exocarpos cupressiformis Labill., Exocarpos latifolius R.Br., Exocarpos sparteus R.Br., Exocarpos strictus R.Br. and Exocarpos syrticolus (Miq.) Stauffer. They are woody shrubs (to 5 m) or small trees (to 10 m) (George 1984) and judging from field observations of their size through time, some species live for several decades. The fruit of Exocarpos is a drupe with a coloured swollen fleshy receptacle (George 1984). The succulent fruit is attractive to frugivorous birds (Forde 1986; Reid 1990) which are the principal dispersal agent. As mentioned in section 15.1, little is known about the root-parasitic Santalales in comparison to mistletoes, partly because their parasitism is concealed below ground and few species achieve economic importance. Benson (1910) first reported root parasitism in Exocarpos and described the haustorium of Exocarpos cupressiformis. The following information is based largely on Fineran's (1991) excellent review of root-parasitic Santalales and his detailed studies on the New Zealand Exocarpos bidwillii Hook.f. Most species of Exocarpos have yet to be studied.

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15.3.1 Infection biology and pathology A feature of root-parasitic Santalales is that they have normal roots, sometimes with root hairs (Fineran 1991). Seedlings can absorb water and nutrients from the soil as plants may live for several months before contacting a host. However, in the absence of a host, growth diminishes and the plant dies. This was demonstrated experimentally for Exocarpos bidwillii (Fineran 1963): well-established parasites were maintained in cultivation if they were transplanted from the field in a large ball of earth containing host plants, but they died within a few months when transplanted without hosts. The native cherries are therefore presumed to be obligate root hemiparasites, which after the seedling stage, depend on haustorial connections with host plants to meet their nutritional demands. Like other xylemtapping parasites, they presumably sequester water, minerals and organic compounds from host xylem and presumably need to allocate less resources to root growth than free-living plants as a result. All native cherry roots are probably capable of forming haustoria but only during primary growth (Fineran 1991). The stimulus to initiate haustoria is the proximity (a few millimetres) of a host root. If the haustoria developed by short lateral roots of primary growth meet suitable hosts, the roots may become secondarily thickened and persist. But if the haustoria fail to contact functional hosts and full development of the haustoria is not achieved, the original fine lateral root may die once it has ceased to function in direct absorption from the soil. This ephemeral status of many roots is largely responsible for the lack of branching in older parts of the parasite's root system. Because haustoria are initiated on young roots, their formation is closely coordinated with seasonal root growth (Fineran 1991). In its temperate subalpine habitat, Exocarpos bidwillii produces new roots and haustoria between spring and autumn. The haustorium of Exocarpos and other rootparasitic Santalales is a rounded to conical-shaped organ between the parasite and host roots (Fineran 1991). The organ is six to eight millimetres in diameter in Exocarpos bidwillii and the internal endophytic portion extends as a tongue of tissue from beneath the organ into the host. The distal end of the organ against the host root is sometimes called the apex. When a large root is attacked, the apex

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forms a pad against the host, but if the host root is small, the apex grows partly around it and forms clasping or cortical folds. The clasping folds seldom encircle the host root and never form a continuous collar encircling the whole root as in the root-parasitic mistletoe, Nuytsia floribunda (Fineran 1991). Root-parasitic Santalales attack a wide variety of plants (Fineran 1991); for example, 12 host species are listed for Exocarpos bidwillii in open, subalpine vegetation. Numerous haustoria are produced, apparently to ensure that sufficient meet suitable host roots (Fineran 1991). The extent to which all haustorial contacts represent functional connections remains to be determined. In the case of Exocarpos bidwillii, almost every plant in the surrounding vegetation may support the growth of haustoria up to a certain stage, but only woody roots allow full development of the organ (Fineran and Hocking 1983). The weak host specificity for initiation of haustoria is also demonstrated by the habit of self-parasitism, contacts usually developing into graft-like unions between the roots of the same individual or between conspecifics. The haustoria in many genera of root-parasitic Santalales are short-lived (≤ 15 months), but growth ring analysis of Exocarpos bidwillii haustoria indicates a maximum age of eight years (Fineran 1991). These long-lived haustoria appear to provide the parasite's main source of mineral nutrition. Haustorial colour may be a useful indicator of age, the actively differentiating tissue in the young haustorium being white. As the organ ages, it becomes creamy and finally, in old organs, brown like the periderm of the root because of accumulation of phenolic compounds. At the seedling stage, the parasite may have young haustoria present in high density over the entire root system (e.g. 15 haustoria and haustorial rudiments per 2.5 cm of root in Exocarpos bidwillii), provided host roots are available for contact. As a root ages, the density of haustoria decreases and those that occur are usually found on host roots two millimetres or more in diameter. Sectioning reveals that the haustoria usually form after secondary thickening of the host root begins. The roots at the base of long-established parasites support few haustoria, these usually being graft-like self-infecting haustoria.

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The effects of infection and haustorial development on the host may include the death of the distal portion of host root and the proliferation of host xylem around the endophyte (Fineran 1991). The hypertrophic host response increases the absorptive contact between the xylem tissues of the parasite and host. Free-living trees and shrubs growing alongside native cherries (e.g. Exocarpos aphyllus, Exocarpos cupressiformis, Exocarpos strictus) in Australian forests and woodlands are sometimes dead or appear debilitated (Jacobs 1955; Parsons et al. 1991; N. Reid, pers. obs.). Jacobs (1955) argued that the mechanism of host debility induced by Exocarpos parasitism was similar to that of mistletoes (Amyema): new buds in the crown of the parasitised tree remain dormant and fail to replace the host foliage as it senesces, resulting in the death of the host. Jacobs argued that a chemical suppressant must be translocated from parasite to host to maintain bud dormancy, but as for mistletoes, this hypothesis remains to be tested. The only report of serious damage to native cherries in commercially managed forests in Australia is that of Parsons et al. (1991), who reported that Exocarpos strictus occasionally reaches ‘plague proportions and requires control measures’ in E. camaldulensis forests on the central Murray River valley, but did not specify management actions. Native cherries are not known to be a management problem in forest, bushland or remnant vegetation elsewhere in Australia.

15.4 Dodder-laurels parasitic on eucalypts Of the 20 or so species of Cassytha (Lauraceae), at least three species are locally important parasites of woody vegetation in different parts of the world (Parker and Riches 1993). Cassytha ciliolata Nees completely overgrows trees in South Africa; Cassytha filiformis L. infests roadside and forest trees in Kenya and China, shrub and herbaceous ground vegetation in the Bahamas and citrus in India and Tanzania; and Cassytha melantha R.Br. damages eucalypts in Victoria. Little is known about the biology of the 14 Australian species, but Parker and Riches (1993) reviewed information about Cassytha filiformis, which occurs throughout the coastal tropics, including Australia.

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15.4.1 Infection biology The host range of most if not all species of Cassytha is broad, individual stems potentially parasitising the stems of many different host plants of various species (Harden 1990; Parker and Riches 1993). Ferns, gymnosperms, monocotyledons and dicotyledons may all be infected by the twining wiry stems, along which develop multiple haustoria that attach to host plant tissue with which the parasite stems come into contact. Frequency of successful establishment by the parasite diminishes with increasing host bark thickness (Gill 1936). Some Australian species of Cassytha flower seasonally, others throughout the year (Harden 1990). The fruit is fleshy with a single hard-coated seed and is dispersed by birds (Forde 1986; Parker and Riches 1993). The seedlings of Cassytha filiformis can survive for up to two months, reaching a length of 30 centimetres or more, without a host. Cassytha filiformis, at least, appears not to tolerate shade.

15.4.2 Pathology and management Heavy infestations of Cassytha smother and kill coppice regrowth in the box-ironbark forests of central and central-west Victoria (Kellas 1991), trees and shrubs in roadside mallee vegetation in the West Wyalong district of New South Wales (N. Reid, pers. obs.), Casuarina, Banksia and Hibbertia in Tasmania (Lawrence 1994) and cause economic losses in forestry and horticulture in other countries (Parker and Riches 1993). Parker and Riches (1993) suggested that Cassytha infestations be removed manually as early as possible to prevent spread. This may involve the pruning of infected branches or the use of non-selective herbicides or fire as spot applications in herbaceous vegetation. In some situations, shading might be used to reduce the parasite’s vigour. Management of the forests dominated by E. microcarpa and E. sideroxylon for timber production in Victoria relies on coppice regrowth from harvested eucalypt stumps, as eucalypt seedling regeneration is rare in such forests (Kellas 1991). The coppice regrowth, however, is susceptible to attack by dodder-laurel (Cassytha melantha) spreading from the adjacent ground flora. Repeated thinning of the coppice growth for silvicultural purposes increases the opportunity for spread of the parasite. Trees infected by dodder-laurel were routinely removed in thinning operations in the box-ironbark

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forests up to 1921 and additional areas were treated in the 1920s (up to 5000 ha per annum, Kellas 1991). Infected trees were felled and the vines heaped and sometimes burnt. Gill (1936) observed that dodder-laurel was again significant in areas which had not been burnt in previous operations. Control operations started again in 1948 with over 3000 hectares treated annually in the early 1950s, but Pederick and Zimmer (1961) found 3200 hectares of the Wellsford State Forest heavily infested by 1961. Subsequently, sheep grazing combined with slashing of residual dodder-laurel clumps was found to be an effective and relatively cheap means of control. Thinning operations in Wellsford forest are now restricted to areas that are relatively dodder-laurel free (Kellas 1991).

15.5 Acknowledgments The research of the authors was funded by the Australian Research Council large grants scheme (AO893025), UNE-Armidale Internal Research Grants Committee and the UNE-Armidale Newholme Funds Allocation Scheme. Richard Bird, Barry Coop, Ross Delaney and John Prior kindly permitted access to their properties for fieldwork and Chris Nadolny and Jim Fittler assisted in the field. Bryan Barlow, Peter Fagg, Rob French, Job Kuijt, David Norton, Mark Stafford Smith and the three editors offered constructive criticisms of earlier drafts. N. Reid would especially like to thank the Sra Doña Alicia de la Garza de De la Mora and Sr Don Raymundo de la Mora for very kindly providing the perfect haven for preparing the first draft of the manuscript. This chapter is dedicated to the memory of Frank Hawksworth, whose lifetime of mistletoe research was exemplary and an inspiration to us.

15.6 References Anderson, R.H. (1941). The effect of settlement upon the New South Wales flora. Proceedings of the Linnean Society of New South Wales 66, 5–23. Anonymous (1945). The mistletoe problem. (Bureau of Investigation: Brisbane.) Anonymous (1949). Blowlamp-type weed burners used to destroy mistletoe. Australian Timber Journal 15, 299. Anonymous (1993). Bush research: mallee fowl … and mistletoe. The Bush Chronicle 9, 9.

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This chapter describes the symptoms and diagnosis of disorders in eucalypts caused by nutrient deficiencies and other abiotic factors. As a basis for understanding the symptoms and their development, the basic nutrition of the eucalypts is discussed. The symptoms of toxicities resulting from excessive nutrients, heavy metals, salinity, agricultural chemicals and air pollutants are described. Damage associated with frost, drought, waterlogging and exteme conditions in artificial environments are also discussed. It is concluded that eucalypts in their native environments are adapted to a wide range of conditions of nutrient and water availability, frost and salinity and that eucalypt species and provenances may be selected to suit particular planting conditions. Symptoms of damage by most abiotic agencies generally indicate either poor management practice or that the species or provenance is unsuited to the particular environment.

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16.1 Introduction Eucalypts (Eucalyptus and Corymbia) are long-lived species which during their lives may be exposed to stress factors that interfere with their normal development. Stress factors include biotic factors such as pathogens and pests, and abiotic factors such as fire and extremes of soil and climate. Tree pathology deals with those stress factors that cause disease or injury. Disease is the result of a prolonged interaction between the tree and a stress factor that leads to detrimental changes in physiological processes. Injury refers to short-term interactions with stress factors that cause damage and have little effect on physiological processes other than those involved in healing. This chapter is concerned with diseases, disorders or injuries of eucalypts caused by abiotic factors. Effects of nutrient deficiencies and toxicities, excessive salts and pollutants of various kinds are discussed. Particular attention is given to those disorders which produce visible symptoms. Injuries such as those caused by fire, breakages from wind or snow and damage caused by grazing insects and mammals are not considered but injuries caused by drought and frost are discussed because physiological mechanisms in the trees can influence the severity of damage caused by these factors.

16.2 Diagnosis Accurate diagnosis of a disorder is essential before effective corrective action can be taken. Similar visible symptoms may be produced by completely different factors and consequently symptoms alone are often inadequate for diagnosis. It is therefore necessary to use a systematic approach which considers the progressive development of symptoms and their pattern of development within the plant and the community, as well as any specific tests or analyses which may be required to identify probable causes (Green et al. 1990). Although specific symptoms can be developed in response to particular abiotic disorders, there are also generalised responses to stress. In eucalypts, these include the production of anthocyanins and kinos. In some eucalypt species, red or blue anthocyanin pigments are produced in young, healthy tissues. The pigments are also produced in response to stress (e.g. in response to invasion by

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some foliar pathogens), or they may become more noticeable when they are unmasked by the disintegration of chlorophyll as a result of stress or senescence. Anthocyanins are glycosides formed by reactions between various sugars and cyclic compounds called anthocyanidins. Stress factors which lead to the accumulation of soluble carbohydrates, low temperatures, high light intensity and drought all favour the production of anthocyanins. Sharma and Crowden (1974) identified 17 compounds in young tissues from 23 species of Tasmanian eucalypts and concluded that divergence in anthocyanin types appeared to parallel divergence in taxonomic groups. The type and degree of anthocyanin production can vary between provenances (Banks and Hillis 1968; Wilcox 1982) and between tissues (Hillis 1956a, 1956b). When the cambium is injured kino veins are often produced. These are formed by lysigenous breakdown of traumatic parenchyma bands produced by the cambium shortly after stimulation (Skene 1965). The cell contents form the kino, which contains polyphenols such as tannin and leucoanthocyanins. In many species, the kino veins are retained in the wood, but in certain species, particularly members of three sections (Adnataria, Bisectaria, Dumaria) of the subgenus Symphyomyrtus, the kino veins become included in the phloem, then the rhytidome and are eventually shed (Tippett 1986). Kino vein production in trees is a mechanism of resistance against fungal invasion and insect attack and they can also be induced by mechanical damage, fire, frost, sun scorch and boron deficiency. They can be used as a useful marker within stems and branches of time elapsed since injury. Kino production is a common response to canker diseases in eucalypts (see Chapter 10).

16.3 Nutrient deficiencies 16.3.1 Nutritional physiology Much of our knowledge of the nutrition of higher plants comes from studies of annual species, whereas the nutrition of trees has been a neglected area of study. The general principles of nutrition of higher plants are reviewed here as a preface to their application to eucalypts. Arnon and Stout (1939) proposed that three criteria should be used to establish whether or not a mineral element was an ‘essential nutrient’ for plant growth. These were:

N UTR ITIONAL D IS OR DE R S

A ND OTHER

1

the plant could not complete its life cycle without it

2

its action must be specific and not replaceable by another mineral element

3

its effect on the plant must be direct.

It became evident that concept 2 was too rigid because sets of elements were found which could substitute for each other. Subsequently Nicholas (1961) proposed the term ‘functional nutrient’ which included any mineral nutrient that functions in plant metabolism irrespective of whether or not its action is specific. The macronutrients that are essential for all higher plants (in order of importance) are: nitrogen (N), phosphorus (P), sulphur (S), potassium (K), calcium (Ca) and magnesium (Mg). Iron (Fe), manganese (Mn), copper (Cu), zinc (Zn), molybdenum (Mo), boron (B) and chlorine (Cl) are essential elements, while sodium (Na), silicon (Si) and cobalt (Co) are essential for some higher plants. A more appropriate classification (modified from Clarkson and Hanson 1980; Mengel and Kirkby 1982) according to biochemical behaviour and physiological function is: Group 1

N and S, which in reduced form are covalently bonded constituents of plant organic matter

Group 2

P, which, as orthophosphate, is esterified with hydroxyl groups of sugars and alcohols

Group 3

K, Na, Mg, Ca and Mn which are important in osmotic and ion balance and more specific functions in enzyme activation and catalysis in which they maintain their ionic identity or are reversibly bound to organic compounds

Group 4

Fe, Zn, Cu and Mo which occur as structural chelates or metalloproteins

Group 5

B and Cl for which specific function is still uncertain.

The ability of plants to remobilise nutrients from leaves and transport them in the phloem to other organs is an important aspect of plant nutrition. The major nutrients N, P, K and Mg, together with Na and Cl, are readily mobile within the plant. Typically these nutrients are withdrawn from older leaves during senescence and redistributed to

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developing tissues, but they may also be withdrawn from non-senescent leaves during nutrient stress. Species such as Eucalyptus baxteri, which are adapted to nutrient-poor soils, may redistribute a higher fraction as their leaves senesce than do crop plants (Specht and Groves 1966). In contrast, once B and Ca are deposited in plant leaves they become virtually immobile. Some nutrients (Fe, Zn, Cu, Mo, S) have limited mobility. Others have variable phloem mobility depending on plant species, environmental conditions and on the stage of plant growth. For example, Cu and S, which are incorporated into proteins, behave as immobile nutrients when nitrogen status is adequate but act as mobile nutrients when nitrogen stress leads to the hydrolysis of proteins (Loneragan et al. 1976). The complex behaviour of Mn in plant phloem does not fit the prevailing classification into these groups (Loneragan 1988). The nutritional health of a plant depends upon the maintenance of a balance of the supply of nutrients to their sites of action, as determined by nutrient acquisition, remobilisation and translocation, with the demand for nutrients as determined by photosynthesis and plant growth. The eucalypts have evolved mechanisms which enable them to cope with low levels of key plant nutrients, particularly P (Bowen 1981). They have a high rooting density which increases physical exploration of the soil. They also form mycorrhizal associations which further increase nutrient absorption (see Chapter 6). The eucalypts have efficient mechanisms for the ‘re-use’ of absorbed nutrients. This involves the withdrawal of nutrients such as N, P and K from wood when heartwood is being formed and from leaves just before they senesce. The relative importance of these mechanisms changes as seedlings develop into mature trees. Thus large trees are highly buffered against temporal changes in nutrient availability whereas seedlings and small trees are poorly buffered. The latter are more subject to nutrient deficiencies but are also more responsive to addition of fertilisers. For example, it has been shown that when young seedlings, including those of eucalypts (Cromer et al. 1984; Cromer and Jarvis 1990), are grown with an exponentially increasing supply of balanced nutrients, both seedling nutrient status and relative growth rate can be stabilised to where nutrient requirement is saturated (Ingestad 1982). Within the

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responsive range there is a linear relationship between relative growth rate and the relative addition of nutrients. One of the mechanisms whereby stability is maintained is a change in the proportions of photosynthates allocated to root and foliage production: with low relative nutrient supplies, a greater proportion is allocated to root production than to leaf production. Growth responses to fertiliser application (e.g. Schönau and Herbert 1989), which often occur in the absence of deficiency symptoms, can be interpreted as an upward shift in relative nutrient addition and relative growth rates. While such responses are of great importance to forest management, the emphasis in this chapter is on those cases where nutrient deficiency is sufficiently severe to produce visible symptoms of disorder.

16.3.2 Diagnosis of deficiency Deficiency symptoms occur when there is an imbalance among the nutrients available for growth or when the relative rate of supply of a balanced set of nutrients is reduced. The symptoms produced in eucalypts by most nutrient deficiencies have been described. In most cases, the deficiencies have been induced experimentally but in some the symptoms have been confirmed by field observations also. Relatively few species have been examined and consequently some care is required in the general application of the following descriptions. For example, species differ in their ability to produce anthocyanins. Symptoms may also be masked by the presence of waxes on the leaf surface. Some variation in symptom development would also be expected depending upon the experimental or field conditions under which the deficiency develops. The development of a nutrient deficiency depends partly on the mobility of the nutrient within the plant. Thus deficiency symptoms for mobile nutrients occur first in the older leaves when the particular nutrient is remobilised and translocated to young growing organs. Care needs to be taken to distinguish such symptoms from those produced by natural senescence when there is a general withdrawal of nutrients from the old leaves. With an increasing degree of deficiency, progressively younger leaves begin to exhibit symptoms. In contrast, the symptoms of deficiency for immobile nutrients first appear in immature organs and, under some circumstances, may be alleviated by

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continued accumulation of the nutrient as the tissues grow older. Chemical analysis of plant organs is often used to confirm the diagnosis of deficiency. Loneragan (1968) drew attention to the need to define two concepts about the nutrient requirements of plants. Firstly, there is a functional requirement, which is the minimal concentration of a nutrient at the site of function which can sustain that function at rates that do not limit growth. Secondly, there is a critical nutrient concentration for the plant or tissue, which represents the nutrient concentration at which maximal growth is attained. The latter depends on both the functional requirement and the ability of the plant to redistribute nutrients. While the functional requirements will remain constant with changing conditions of nutrient supply, the critical concentrations, particularly for immobile elements, may vary depending on the history of plant growth and nutrient supply. Critical concentrations will also vary depending on whether the whole plant or a particular organ is sampled and whether the function of interest (e.g. cell formation in the stem for Cu, or at the terminal meristem for B) occurs in the organ sampled. Leaf age is an important factor affecting concentrations of nutrients in foliage because the concentrations of mobile nutrients tend to decline with age whereas those of the immobile nutrients tend to increase (e.g. Lamb 1976). Seasonal fluctuations in nutrient concentrations also occur (Lamb 1976; Schönau 1981; Bell and Ward 1984; Knight 1988). In view of these types of variation, it is important to standardise methods of foliar sampling and their timing. The concentrations of nutrients in the youngest fully expanded leaves is often used to diagnose nutrient status. The concentrations of mobile nutrients in old leaves and the concentrations of immobile nutrients in immature leaves also can be useful indicators of deficiency. Guidelines are available for the optimum foliar nutrient concentrations for field-grown E. grandis (Herbert and Schönau 1990; Dell et al. 1995), E. globulus and E. urophylla (Dell et al. 1995) and for deficient and healthy seedlings of C. maculata (Dell and Robinson 1993), E. globulus, E. grandis, E. pellita and E. urophylla (Dell et al. 1995). A compendium of foliar analyses obtained from plantation species has been produced by Boardman et al. (1997). Caution

N UTR ITIONAL D IS OR DE R S

TAB LE 16 . 1

A ND OTHER

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Eucalypt species for which deficiency symptoms for major and minor nutrients have been described

C., Corymbia; E., Eucalyptus; B, boron; Ca, calcium; Cu, copper; Fe, iron; Mg, magnesium; Mn, manganese; Mo, molybdenum; S, sulphur; Zn, zinc; nutrients have been listed in order of importance.

Species

Medium

Nutrients

References

C. citriodora

Sand

N, P, K, Ca, Mg, S

Kaul et al. (1970b)

C. maculata

Sand

N, P, Ca

Halsall et al. (1983)

C. maculata

Sand

Zn

Dell and Wilson (1985)

C. maculata

Various

N, P, K, Ca, Mg, S, Fe, Mn, Zn, Cu

Dell and Robinson (1993); Dell (1996)

E. baxteri

Sand

N, P, K, Mg, S, B

P. Snowdon (unpubl. data)

E. botryoides

Perlite

N, P, K, Ca, Mg

Will (1961)

E. camaldulensis

Soil

N

Esparcia and Nuno (1964)

E. camaldulensis

Various

N, P, K

P. Snowdon (unpubl. data)

E. cypellocarpa

Sand

N, P, K, Mg, S, B

P. Snowdon (unpubl. data)

E. diversicolor

Various

N, P, K, Ca, Mg, Fe, Mn, Zn

P. Snowdon (unpubl. data)

E. globulus

Sand

N, P, K, Ca, Mg, S

Kaul et al. (1970a)

E. globulus

Soil

N

Esparcia and Nuno (1964)

E. globulus

Various

N, P, K, Ca, Mg, Fe, Mn, Zn, B

P. Snowdon (unpubl. data)

E. globulus

Various

N, P, K, Ca, Mg, S, Fe, Mn, Zn, Cu, B

Dell et al. (1995)

E. globulus

Water

N, P, K, Ca, Mg

Marcos de Lanuza and Marzo Muñoz-Cobo (1968)

E. gomphocephala

Sand

N, P, K, Ca, Mg, Fe, Mn, Zn, B

P. Snowdon (unpubl. data)

E. grandis

Sand

N, P, K, Ca, Mg, Fe, Mn, B

P. Snowdon (unpubl. data)

E. grandis

Sand

N, P, K, Ca, Mg, S

Kaul et al. (1968)

E. grandis

Soil

N, P, K, Ca, S

Zhong and Reddell (1994)

E. grandis

Various

N, P, K, Ca, Mg, S, Mn, Zn, Cu, B, Mo

Dell et al. (1995)

E. grandis

Water

P, K, Ca

Zeijlemaker (1973)

E. marginata

Sand

N, P, K

P. Snowdon (unpubl. data)

E. marginata

Sand

Zn

Dell and Wilson (1985); Wallace et al. (1986)

E. obliqua

Sand

N, P, K, Mg, S, B

P. Snowdon (unpubl. data)

E. patens

Sand

Zn

Dell and Wilson (1985)

E. pellita

Various

N, P, K, Mg, S, Zn, B

Dell et al. (1995)

E. pilularis

Perlite

N, P, K, Ca, Mg

Will (1961)

E. pilularis

Sand

N, P, Ca

Halsall et al. (1983)

E. pilularis

Sand

N, P, K, Ca, Mg, S, Fe

Truman and Turner (1972)

E. pilularis

Various

N, P, K, Ca, Fe, Mn, Zn

P. Snowdon (unpubl. data)

E. regnans

Sand

N, P, K

P. Snowdon (unpubl. data)

E. saligna

Perlite

N, P, K,Ca, Mg

Will (1961)

E. saligna

Sand

N, P, K

P. Snowdon (unpubl. data)

E. sieberi

Sand

N, P, K

P. Snowdon (unpubl. data)

E. tereticornis

Sand

N, P, K, Ca, Mg, S

Hussain and Theagarajan (1966)

E. tereticornis

Sand

N, P, K, Ca, Mg, S

Kaul et al. (1966)

E. urophylla

Sand

N, P, K, Ca, Mg

Cheng and Horng (1992)

E. urophylla

Solution

N, P, K, Ca, Mg, S, Fe, B

Rocha Filho et al. (1978)

E. urophylla

Various

N, P, K, Ca, Mg, S, Fe, Mn, Zn, Cu, B, Mo Dell et al. (1995)

E. viminalis

Various

Fe

Ladiges (1977)

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should be used when extrapolating results obtained with seedlings to established trees.

16.3.3 Deficiencies of specific nutrients Under field conditions, new plantings of eucalypts commonly give growth responses after application of fertiliser containing N, P or, to a lesser extent, K (Schönau and Herbert 1989). The most commonly occurring micronutrient problems are lime chlorosis (usually due to Fe deficiency) and B deficiency. Deficiencies of Mg (Karschon 1963b) and Cu (Dell and Bywaters 1989; Turnbull et al. 1994) have also been described under field conditions. For other nutrients our knowledge of the symptoms produced by deficiency depends on studies carried out in glasshouses. The symptoms produced by deficiencies of the major and minor nutrients have been described for several species (Table 16.1). Only a few studies include coloured illustrations of the symptoms (Malavolta et al. 1962; Esparcia and Nuno 1964; Marcos de Lanuza and Marzo MuñozCobo 1969; Truman and Turner 1972; Nichols et al. 1981; Will 1985; Cheng and Horng 1992; Dell and Robinson 1993; Dell et al. 1995; Dell 1996). Keys to the symptoms developed in E. gomphocephala (Karschon 1963a), E. pilularis (Truman and Turner 1972) and for eucalypts generally (Malavolta et al. 1962) have been prepared to aid identification of deficiencies. 16.3.3.1 Nitrogen In green plant tissue about 85% of the N content occurs in proteins, 10% in nucleic acids and 5% in soluble forms such as amino acids, amides and amines. The major proportion of the proteins are enzymes but there are also structural proteins, which occur mainly in biological membranes, and storage proteins. Protein in older leaves can be hydrolysed to amino acids which are redistributed to newly developing tissues. Proteolysis results in a collapse of the chloroplasts and, hence, the yellowing of older leaves which is the first symptom of inadequate N nutrition. Nitrogen is considered to be the key element required for leaf production and, hence, for controlling growth rates (Plate 16.1). Thus, growth responses to fertiliser application (Schönau and Herbert 1989) need not always be seen as the alleviation of deficiency. Nitrogen deficiency in eucalypts is characterised first by the restriction of height growth and branching,

390

and later by chlorosis of the foliage. Chlorosis begins in the older leaves and is usually a uniform pale yellow–green, but interveinal chlorosis or yellow spots may be evident. Anthocyanin colouration often develops on the veins and leaf margins. Development of colouration over the leaf surface may be either uniform or blotched and can be accentuated by low temperatures and/or high light intensity (Plate 16.2). Some necrosis may occur before leaf shed. Nitrogendeficient foliage in seedlings often has concentrations of less than 0.7% N (e.g. Kaul et al. 1970b; Rocho Filho et al. 1978; Cheng and Horng 1992; P. Snowdon, unpubl. data). Vigorous growth of young trees in the field is often associated with foliar concentrations of greater than 2.0% N (e.g. Lamb 1977; Will 1985; Herbert and Schönau 1990). The availabilities of N and P in soils are closely linked, as are requirements for them in plants. Good health depends on a balanced supply of both nutrients. Nitrogen tends to be the major nutrient required by young trees grown on alluvial soils, recent sands, volcanic soils and other relatively young soils low in organic matter (Schönau and Herbert 1989). Nitrogen deficiency is exacerbated by the addition of P-containing fertilisers. Such a situation occurs commonly in nurseries, particularly in potted stock grown in a medium containing large amounts of peat or sawdust. 16.3.3.2 Sulphur Cysteine and methionine are the most important Scontaining amino acids in plants and are important constituents of proteins. Sulphur deficiency results in an inhibition of protein synthesis, with the consequence that non-sulphur containing amino acids, particularly asparagine, glutamine and arginine, are accumulated in affected tissues. Since both N and S are involved in protein synthesis it is sometimes difficult to distiguish the visible symptoms of these two elements. Sulphur deficiency is characterised by chlorosis which appears first in the expanding leaves and may later spread to the old leaves. In advanced stages, there can be some distortion of young leaves in some species, the leaves can become bronze coloured and necrotic patches may develop at the tips and margins (Plate 16.3). Under severe deficiency, dieback of the shoots can occur. In C. maculata, the expanding leaves from deficient plants may contain 0.12% to 0.13% S whereas those from healthy seedlings contain

N UTR ITIONAL D IS OR DE R S

A ND OTHER

0.18% to 0.42% S (Dell and Robinson 1993). Sulphur deficiency has been observed in E. globulus grown in Western Australia and in E. urophylla grown in southern China (Dell et al. 1995). 16.3.3.3 Phosphorus The unique function of phosphate in metabolism is its formation of pyrophosphate bonds which allow energy transfer. The most important phosphatecontaining compound is adenosine triphosphate (ATP). Other triphosphates are important for the synthesis of sucrose, phospholipids, cellulose, ribonucleic acids and deoxyribonucleic acids. Organic phosphates are also important as intermediary compounds in metabolism. Much of the phosphate present in plants is in the inorganic form. Under deficient conditions the concentration of inorganic P is depressed while the organic P levels are little affected. Deficiency in eucalypts is characterised by restricted height growth and branching. Visible symptoms of deficiency first appear on the older leaves which are often darker green than normal. Purple colouration develops as spots or blotches on the leaf lamina or at the margins or sometimes most noticeably on the veins (Plate 16.4). The leaves fade and often become dull red or orange before being shed. Necrosis of the leaf tips sometimes occurs. Under field conditions nutrient withdrawal from the lower crown followed by leaf shed results in trees with sparse crowns. The P concentration in eucalypt leaves displaying symptoms is often about 0.02% to 0.05% P (e.g. Malavolta et al. 1962; Rocha Filho et al. 1978; Dell et al. 1987; Cheng and Horng 1992; P. Snowdon, unpubl. data). Vigorous growth of young trees is often associated with foliar concentrations greater than 0.14% P (Will 1985; Herbert and Schönau 1990). Phosphorus deficiency would be expected in soils developed from parent materials such as sands or sandstones which are low in P or in soils containing high amounts of active Al or Fe which can reduce the availability of P for plants. 16.3.3.4 Potassium Potassium is the most abundant cellular cation. High concentrations are required for the active conformation of many enzymes and for the neutralisation of soluble and macromolecular anions. Potassium is also important in determining osmotic potential and is specifically involved in membrane transport processes (Clarkson and Hanson 1980).

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Deficiency in some eucalypt species is characterised by slight chlorosis followed by the development of purple blotches or spots on the older leaves. In other species, the progressive development of chlorosis is more typical. The veins become red or purple and sometimes leaves become uniformly and brightly coloured with orange or red before they are shed. Later, necrotic spots and patches develop. Necrosis sometimes begins from the base of the leaf but it is more usual for it to begin from the leaf tip or margin (Plate 16.5). In advanced cases, the immature leaves can be mottled by chlorotic or anthocyanin patches, and can become cupped and distorted. Potassium deficiency can stimulate branch production in some species (Will 1961; Dell and Robinson 1993). This, coupled with short internodes, can give the seedling a bushy appearance (Plate 16.6). Leaves of seedlings exhibiting symptoms often have concentrations less than 0.6% K (e.g. Malavolta et al. 1962; Kaul et al. 1968, 1970a; Cheng and Horng 1992; P. Snowdon, unpubl. data). Similarly low concentrations are found in leaves of deficient field-grown trees (Zech and Kaupenjohann 1990). Potassium deficiencies would be expected to occur in acid, sandy to loamy sand soils that are low in organic matter, low in total cation exchange capacity and have a low base saturation. Growth responses by E. gomphocephala to applications of potassium fertilisers were first obtained in Morocco (Beaucorps 1959; Marion 1960). Deficiency has been observed in C. torelliana and E. camaldulensis grown on sandy soils in South Benin (Zech and Kaupenjohann 1990). It has also been observed in E. globulus grown in Western Australia, E. grandis in southern China and E. urophylla in the Philippines (Dell et al. 1995). 16.3.3.5 Magnesium Often over 70% of total Mg in plant tissues is diffusible and associated with inorganic and organic acid ions. About 20% is associated with the chlorophyll molecule. Besides this function, Mg2+ is a cofactor in almost all enzymes actuating phosphorylation processes. Deficiency of Mg inhibits protein synthesis. Deficiency symptoms appear first in the older leaves, usually as interveinal chlorosis. In E. diversicolor, irregular sectors of the lamina, often with distinct margins, become bleached and necrotic. In other species such as E. baxteri, E. globulus and E. obliqua , chlorosis spreads across the lamina, then

391

D I S E A S E S

A N D

P A T H O G E N S

O F

anthocyanin production followed by necrosis progresses inward from the leaf margin prior to premature leaf shed (Plate 16.7). Immature leaves can sometimes be chlorotic and distorted. Deficient seedling leaves often have concentrations less than 0.07% Mg (e.g. Rocho Filho et al. 1978; Cheng and Horng 1992; P. Snowdon, unpubl. data). A possible case of Mg deficiency has been recorded for E. gomphocephala growing on calcareous soils formed on travertines (Karschon 1963b). Deficiencies would be expected in highly leached acid humus soils and sandy soils. Uptake of magnesium ions can be depressed in the presence of high levels of hydrogen, potassium, ammonium, calcium and possibly aluminium ions. 16.3.3.6 Calcium Calcium is required for cell division and cell elongation. It is important in ion uptake and is also of fundamental importance for membrane permeability and maintenance of cell integrity. It occurs in plant tissues as free Ca2+ and as Ca2+ adsorbed to indiffusible ions and is also present as oxalates, carbonates and phosphates which often occur as deposits in cell vacuoles (e.g. Buttrose and Lott 1978). In cell walls, Ca is associated with the free carboxylic groups of the pectins. The youngest leaves of deficient eucalypt seedlings become wrinkled, with the leaf margins turned under. In the early stages of deficiency, the leaves expand to full size but remain with the margins turned under. This can lead to a marked reduction in water usage because stomata in juvenile leaves are concentrated on the underside of the leaf. At later stages the young leaves fail to expand. Chlorotic patches develop on the leaf margins and extend inwards. This is followed by necrosis from the margin until finally the whole leaf dies (Plate 16.8). Terminal shoots die back and new shoots are stimulated in the axils of young leaves. Occasionally chlorosis, development of blotches of anthocyanin pigmentation or necrosis can occur in old leaves. Affected leaves and shoot apices have concentrations in the range 0.05% to 0.15% Ca. Deficiencies of Ca are unlikely to occur under natural conditions. 16.3.3.7 Manganese The biochemical functions of Mn2+ resemble those of Mg2+ and in many activities they can substitute for each other. Manganese also has specific roles.

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It activates indole acetic acid oxidation–reduction processes in the photosynthetic electron transport system. The chloroplasts are the most sensitive of all organelles to deficiency. In E. tereticornis, deficiency begins as interveinal chlorosis of young leaves with tissue near the veins remaining green. As the deficiency becomes more acute the tips and margins of the leaves begin to wither and show a sandy colour which spreads throughout the blade (Malavolta et al. 1962). In C. maculata, small white or brown spots may become widespread in the chlorotic interveinal areas (Dell and Robinson 1993). In E. globulus, the first symptom is the development of interveinal anthocyanin colouration in the expanding leaves. In E. globulus and E. pilularis, the developing leaves may be distorted with undulate margins or with leaf tips and margins curved under (Plates 16.9 and 16.10). Later the leaf margins become chlorotic and may become necrotic (P. Snowdon, unpubl. data). Concentrations of Mn in the youngest fully expanded leaf and younger tissues of deficient seedlings are usually less than 15 micrograms per gram dry weight. The deficiency has been observed in E. globulus grown in Western Australia (Dell et al. 1995). A localised occurrence of lime-induced Mn deficiency in E. nitens has been reported in Tasmania (Plate 16.11) (J.L. Honeysett, pers. comm.). Deficiency is usually associated with soils of high pH or with organically rich soils of neutral to alkaline reaction. 16.3.3.8 Iron Most of the active Fe in plants is implicated in reduction or oxidation reactions of the chloroplasts, mitochondria and peroxisomes. Another requirement is for porphyrin synthesis, the absence of which results in iron chlorosis (Clarkson and Hanson 1980). Deficiency in E. pilularis grown in sand culture is first characterised by interveinal chlorosis of young leaves (Plate 16.12). As the deficiency becomes more acute, newly formed leaves become progressively more chlorotic until the last formed leaves are almost white with anthocyanin production along the veins and mid rib. In older leaves, the interveinal regions are yellow while the veins remain dark green (Malavolta et al. 1962; Dell and Robinson 1993). Under field conditions necrotic spotting and leaf death may occur (Stewart et al. 1981). The concentration of Fe in plant tissues is a poor

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indicator of their Fe status because often the concentration in affected leaves is higher than in healthy leaves. Confirmation of deficiency by application of a foliar spray containing an Fe salt such as ethylenediaminetetraacetic acid ironpotassium salt (Fe-K-EDTA) can also be unreliable unless the cuticle is damaged sufficiently to allow absorption of the active ingredient (Andrew and David 1959; Winterhalder 1963). Iron deficiency is a common problem with potted nursery stock (Will 1985).

(Anderson and Ladiges 1978, 1982) and E. viminalis (Ladiges 1977; Ladiges and Ashton 1977) but tests with E. diversifolia (Parsons and Specht 1967) and E. ovata (McCoy and Parsons 1974) failed to demonstrate such differences. There is also considerable between-species variation in tolerance to Fe deficiency on acidic soils when there is an excessive uptake of Mn (Andrew and David 1959; Winterhalder 1963).

In the field, chlorotic symptoms of Fe deficiency commonly occur in eucalypts grown on calcareous or alkaline soils. This is often called ‘lime-chlorosis’ because other nutrients such as Mn, Zn and Cu are also commonly near deficiency levels under these conditions (Plate 16.13). Calcareous and siliceous beach sands in southern Australia each carry a distinctive assemblage of eucalypts. Eucalyptus diversifolia is widespread on calcareous beach sands but E. baxteri is restricted to acid soils. When E. baxteri seedlings are grown in alkaline calcareous sand they become stunted by severe lime chlorosis, but E. diversifolia is unaffected (Parsons and Specht 1967). Similarly, E. ovata seedlings are little affected while E. obliqua becomes chlorotic when planted on alkaline calcareous sands (McCoy and Parsons 1974). These results imply that the absence of some species from alkaline calcareous sands is due to physiological intolerance of the alkaline conditions.

Zinc and its importance in forestry has been reviewed by Boardman and McQuire (1990). Primarily, Zn is involved in the fundamental processes of cell replication and gene expression associated with nucleic acid and protein metabolism. Deficiency results in drastic effects on enzyme activity, chloroplast development and nucleic acid and protein contents.

Plantings of E. botryoides, E. camaldulensis, E. globulus and E. grandis on calcareous earths at Robinvale in north-west Victoria have been affected by Fe deficiency (Stewart et al. 1981). Lime chlorosis in eucalypts has also been observed in Cypress (Thirgood 1955), France (Lacaze 1963; Marien and Thibout 1981), India (Ghosh et al. 1978; Kaul et al. 1982), Israel (Karschon 1958a), Italy (Giulimondi and Arru 1959) and Sudan (Booth 1965). There is considerable variation between species for tolerance to alkaline conditions, with some slight evidence that Symphyomyrtus species are more tolerant than Monocalyptus species (Marien and Thibout 1981). Within species, differences between populations in tolerance to alkaline soils have been shown for E. dalrympleana (Lacaze 1963), E. globulus (Marien and Thibout 1981), E. obliqua

16.3.3.9 Zinc

In E. marginata seedlings, Zn deficiency first appears as bronzing on the adaxial surface of young leaves (Wallace et al. 1986). As bronzing intensifies the adaxial surface becomes slightly chlorotic and salt may be deposited at the leaf tips by guttation. With ageing the leaves and cotyledons become red at the tips and margins. The affected areas spread to cover most of the leaf and in severe cases become necrotic. The size of leaves and length of internodes are reduced. This is also the case with E. pilularis (Plate 16.14). Observations on E. tereticornis (Malavolta et al. 1962; Kamala et al. 1986) and C. maculata and E. patens (Dell and Wilson 1985) indicate that old leaves may become purple rather than red and that leaf distortion may occur. The critical concentration for Zn in the shoot apex lies between 10 and 12 micrograms per gram of dry matter in temperate species (Wallace et al. 1986; Dell and Wilson 1989) but may be higher (21 mg/g) in tropical species (Dell and Xu 1995). Deficiency would be expected to occur on calcareous soils, podzolised sands, lateritic podzolic soils and peats. Zinc deficiency has been implicated in the failure of E. pauciflora to colonise peats on the Lake Mountain plateau in Victoria (Ashton and Hargreaves 1983), it has been induced in E. pellita seedlings grown in rudimentary soils developed from mine waste (Reddell and Milnes 1992) and it has been observed in E. urophylla grown in the Philippines (Dell et al. 1995).

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16.3.3.10 Copper The role of Cu in forest nutrition has been reviewed by Turvey and Grant (1990). Copper-containing proteins are involved in several electron transfer reactions including those involved in photosynthesis, although it appears that the activity of Cu metalloenzymes involved in the production of secondary metabolites, such as lignins and plant hormones, is more sensitive to low Cu levels. Deficiency occurs most often in acid sandy soils high in organic matter and in calcareous soils. It is exacerbated by poor drainage and soil salinity. In E. tereticornis seedlings, Cu deficiency results in deformation of young leaf blades and an irregular appearance of the leaf margins (Malavolta et al. 1962). Leaves can become chlorotic and later reddish, and seedlings can become stunted (Kamala et al. 1986). In C. maculata , early stem bleeding from the nodes coincides with reduced lignification of the secondary xylem (Dell and Robinson 1993). Later, the leaves lose their lustre and undulate margins develop on expanding leaves. At an advanced stage, the petioles show epinastic curvature and necrosis of young leaves, lateral buds and shoot apices occurs. In C. maculata grown on revegetated bauxite mine sites in Western Australia, the first expression of deficiency is deformation of the leaf blade which is followed by gradual loss of function at the shoot apex, shedding of young organs and eventually by tip dieback (Dell and Bywaters 1989). Trees with severe dieback develop enlarged nodes which often produce a proliferation of shoots. Thus, highly branched dwarf shrubs lacking a dominant shoot are formed. Normal shoot growth in affected trees was restored after application of copper sulphate as a foliar spray or to the soil. Serious malformation of E. nitens grown on an improved pasture site in Tasmania has been attributed to Cu deficiency induced by the application of high rates of nitrogenous and phosphorous fertilisers (Turnbull et al. 1994). The critical concentration of Cu in young foliage lies between 0.5 and 1.5 micrograms per gram dry weight. The deficiency has also been observed in E. globulus grown in Western Australia (Dell et al. 1995). 16.3.3.11 Molybdenum Nitrate reductase is the only established Mocontaining enzyme in higher plants (Clarkson and Hanson 1980). Deficiency induced in E. tereticornis

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seedlings is characterised by yellowish spots between the veins of young mature leaves. Narrow bands adjacent to the veins remain green while purplish colouration develops along the leaf margins (Malavolta et al. 1962). Stunting and distortion of the leaves of E. tereticornis may also occur (Kamala et al. 1986). Growth reduction due to Mo deficiency has been observed in E. grandis grown in a nutrient omission experiment on a soil developed on beach ridges in north Queensland (Zhong and Reddell 1994). 16.3.3.12 Boron A common feature in B deficiency is the disturbance in the development of meristematic tissues, whether these are root or shoot apices or tissues of the cambium. The precise function of this nutrient is unknown. Since B is largely immobile within the plant, a continuous supply is required for the maintenance of meristematic activity. Symptoms of B deficiency appear first in young tissues. Newly developed leaves are small, cupped and often distorted. Leaves can become chlorotic with necrotic patches. Red colours develop as the leaves grow older. Shoots developing in the leaf axils die and under severe deficiency dieback proceeds from the top of the plant (Plate 16.15). Deficiency symptoms are usually associated with foliar concentrations of B in the range 4 to 8 micrograms per gram but may also occur at concentrations up to 16 micrograms per gram (P. Snowdon, unpubl. data). Boron deficiency has been linked with increased susceptibility to drought (Savory 1962) and frost (Cooling 1967; Cooling and Jones 1970). Deficiency of B in plants commonly occurs on soils developed from volcanic or granitic rocks and from sedimentary rocks formed in freshwater environments. Within these geological provinces, deficiency tends to occur on skeletal or eroded soils and soils that have been extensively leached. Boron deficiency is unlikely to occur in coastal regions where there can be considerable accession of B from the ocean via rainfall and atmospheric deposition (Hingston 1986). Overt manifestations of B deficiency and/or reduced foliar B concentrations may be induced by the addition of macronutrient fertilisers (Stone 1990). The most productive species and provenances are often the most affected (Althoff et al. 1991). Boron deficiency in eucalypts has been reported in Brazil (Knudson et al. 1970;

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Tokeshi et al. 1976), southern China (Yang et al. 1991; Malajczuk et al. 1994; Dell et al. 1995), Columbia (Ladrach 1980), Nepal (Jackson 1987), New Zealand (Will 1985), Nigeria (Kadeba 1978), Papua New Guinea (Hartley 1977; Lamb 1977), the Philippines (Dell et al. 1995), Upper Volta (Delwaulle 1979), Zambia (Savory 1962; Cooling and Jones 1970) and Zimbabwe (Steyn and Straker 1969).

16.4 Toxicities 16.4.1 Nutrient and heavy metal toxicities The growth and health of eucalypts can be adversely affected when abnormally high concentrations of nutrient or other mineral elements occur in the soil or growing medium. There is some evidence that high levels of Mg and heavy metals in soils developed from ultramafic rocks have influenced the development of eucalypt species and communities. For example, in the humid subtropics of Queensland and northern New South Wales there are three species of eucalypts restricted to ultramafic sites: C. xanthope, E. fibrosa and E. serpentinicola (Batianoff and Reeves 1991). Conversely, E. melliodora woodland is excluded from the Coolac Serpentine Belt in southern New South Wales (Lyons et al. 1974). Near Kalgoorlie, WA, eucalypts can occur on greenstone deposits but where there are excessive amounts of nickel (Ni) in the soil and low pH they are replaced by Ni-tolerant shrubs (Cole 1973). Forest communities dominated by E. delegatensis, E. nitida or E. obliqua inhabit ultramafic sites in Tasmania but there are obvious substrate-correlated morphological differences in leaf form in E. nitida grown on and off the ultramafic substrate (Gibson et al. 1992). In Zimbabwe, E. grandis has been found to grow poorly on soils derived from serpentine (Barrett et al. 1975). In the Philippines, there is evidence for Fe deficiency and Ni toxicity in eucalypts grown on soils derived from ultramafic rocks (Dell et al. 1995). Almost all elements will induce deleterious physiological and metabolic consequences when present in the plant in excess of optimal quantities. Nutrient toxicities induced in seedlings of E. globulus have been described for N, P, K, Ca and Mg (Marcos de Lanuza and Marzo Muñoz-Cobo 1968, 1969). Often the visible symptoms produced by these

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imbalances were similar to those produced by deficiencies of other nutrients. For example, excess N caused symptoms similar to K deficiency while excess K caused symptoms similar to P deficiency. Toxicity symptoms have also been described for Mn (Zeijlemaker 1973) and B in E. grandis (Rocha Filho et al. 1979; Novelino et al. 1982), Cu in E. sieberi (Hanger and Bjarnason 1976) and cadmium (Cd), Zn and lead (Pb) for several species (Davey 1977). Problems could be expected when eucalypts are planted on mine spoils, on sites where industrial or municipal wastes have accumulated or on soils contaminated by prolonged use of fungicides containing heavy metals. Zinc toxicity can be caused by galvanised products such as planting tubes (Worsnoop 1955). Toxicity can also occur when fertilisers are applied at excessive rates or when the composition of the fertiliser is inappropriate. For example, seedlings of E. agglomerata and E. macrorhyncha shed a high proportion of their juvenile leaves when their nitrogen source is from nitrate only (Moore and Keraitis 1971; Moore et al. 1973).

16.4.2 Salinity Saline and sodic soils occupy about one-third of the total area of Australia. Disturbance of natural ecosystems has led to changes in hydrological regimes with the consequence that salt formerly distributed in deeper subsoil and substrate layers has, through secondary salinisation, been mobilised and concentrated in vulnerable parts of the landscape (Loveday and Bridge 1983). This results in adverse physical conditions in the soil such as reduced permeability to water and air, and increased mechanical resistance to root penetration, as well as the toxic effects of soluble salts. This in turn can lead to decreased vigour and increased mortality of affected vegetation (Froend et al. 1987) (Plate 16.16). Eucalypts are being evaluated for utilisation and reclamation of salt-affected sites both in Australia (Morris and Thomson 1983; Biddiscombe et al. 1985) and other countries (Midgley et al. 1986) (Plate 16.17). While few Monocalyptus species have been tested for salt tolerance in field trials (Noble 1989), glasshouse studies indicate that Monocalyptus species are very salt sensitive whereas Symphyomyrtus species vary from sensitive to tolerant (Blake 1981; Marcar 1989).

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In general the presence of soluble salts in the nutrient medium can affect growth in two ways. Firstly, soluble salts depress the water potential of the nutrient medium and, hence, restrict water uptake by the plants. A degree of osmotic adjustment can occur because the higher salt concentration also results in an increased uptake of ions. The second effect is due to physiological disorders induced by toxicities of specific ions such as Na+, Mg2+, Cl– or borate [B(OH)4–]. For example, Cl– and Mg2+ ions have been shown to have specific effects on E. globulus ssp. bicostata (Marcar and Termaat 1990). Severe salinity stress can also affect enzymes and organelles present in the cytoplasm. Development of symptoms in seedlings varies according to their salt tolerance (van der Moezel et al. 1988; Marcar 1989). In sensitive species, young expanding leaves are affected by marginal necrosis which quickly spreads to the whole leaf (Plate 16.18). Wilting and necrosis of the shoot apices occur at the same time. Later, necrosis and senescence of the older leaves occur. In more tolerant species, the older basal leaves show necrosis and senescence earlier than the younger leaves. With high chloride concentrations, the young expanding leaves of E. globulus ssp. bicostata become reddened and curl before becoming necrotic (Marcar and Termaat 1990). Eucalypts are also adversely affected by wind-blown salt (Karschon 1958b). Intolerance to salt spray might exclude eucalypts from exposed coastal locations (Parsons and Gill 1968). Necrosis begins at the leaf tip or margins and extends inward until most of the leaf is affected. There is usually a well-defined margin between affected and healthy tissue and anthocyanin may develop along the edges of the necrotic zone. Death of branches occurs on the exposed side of the tree. The amount of wind penetration into the edge of forest stands determines the extent of damage from airborne salt (Offor 1992). If the wind can penetrate beneath the canopy, dieback will be more extensive and can result in dead trees on the windward side. Young leaves can be readily damaged by strong winds alone and this can be confused with salt damage (Offor 1992).

16.4.3 Agricultural chemicals There is considerable use of agricultural chemicals in eucalypt nurseries and plantations. Some, such as germination inhibitors and herbicides, are specifically

396

toxic to higher plants and are used to control weeds. Others are used to control organisms such as fungi, nematodes, molluscs or insects. Some of these chemicals can become phytotoxic if they are applied at high rates or in adverse conditions (Plate 16.19). For example, many insecticides and fungicides can be moderately to severely phytotoxic when used as seed protectants (Neumann and Kassaby 1986). At high dosages benomyl, which is used as a systemic fungicide for control of Cylindrocladium pteridis F.A.Wolf in eucalypt seedlings, is phytotoxic, causing marginal and interveinal chlorosis of the leaves and reducing growth (Bedendo and Krugner 1988; Ferreira 1989).

16.4.4 Air pollution The growth and health of many native forests, plantations and urban trees are threatened by a wide diversity of air pollutants (Kozlowski and Constantinidou 1986a, 1986b). Sulphur dioxide (SO2) and ozone (O3) probably cause more injury than all other air pollutants combined. Near large point sources of pollution, however, severe injury to trees is caused by fluorides, dusts and acidic aerosols. Adverse metabolic changes and injuries are induced in plant cells, depending on both the concentration and frequency of exposure to the pollutant. Absorption of sublethal amounts of gaseous air pollutants leads to chronic injury characterised by chlorosis and early leaf senescence. Higher levels of pollution cause cell collapse and necrosis, although in some cases acute exposure may result in heavy defoliation within a few hours without the formation of injury symptoms (e.g. Taylor 1984). Both vegetative and reproductive growth may be reduced by air pollution. Eventually entire forest ecosystems can be affected by reduction in structural complexity, productivity and species diversity. Gaseous pollutants enter the plant through open stomata. Thus, young leaves with partially developed stomata and old leaves with a high proportion of degenerate, non-functional stomata are more resistant to damage than recently matured leaves. There have been several laboratory studies comparing the sensitivity of eucalypt species to specific gaseous pollutants (Table 16.2). These used relatively high concentrations of pollutant and sensitivity was rated on the basis of acute injury. Much less is known about chronic injury caused by low levels of pollution (Murray 1984). Even less is

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TAB LE 16 . 2

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Degrees of tolerance shown by eucalypt species to various air pollutants

In each study the number of species in each category is shown.

Pollutant

Tolerant

Intermediate

Sensitive

References

Sulphur dioxide

7

15

21

O’Connor et al. (1974)

Fluoride

6

13

21

Horning and Mitchell (1982)

Fluoride

17

22

21

Doley (1986)

Ozone

50

10

1

O'Connor et al. (1975)

Smog

20

—

9

Hanson (1972)

known about the effects of combinations of gases (Elkiey and Ormond 1987; Murray and Willson 1988a, 1988b) and the effects of environmental variables, such as temperature, on sensitivity to air pollution (Norby and Kozlowski 1981). Only a few studies have been made of the effects of pollutants on field-grown trees (Hanson 1972; Murray 1981). 16.4.4.1

Sulphur dioxide

In 1990, the annual global mass emission of SO2 was about 2.2 megatonnes and increasing rapidly (Clarke and Murray 1990). From 1990 to 2000, pollution from industrial sources was reduced to 1.3 megatonnes by the installation of pollution control equipment in heavy industry but there is still a high output from other sources such as transport, domestic usage and light industry (F. Murray, pers. comm.). This high level of emission of SO2 combined with the area affected and its toxicity makes SO2 the most important air pollutant in the natural environment. The main source of SO2 pollution is the combustion of fossil fuels but mineral roasting and smelting operations are also important sources. When the gas is absorbed by leaves it dissolves on the moist surfaces of mesophyll cells in the stomatal cavities to form sulphurous acids which dissociate to form H+, HSO3– and SO32–. These products accumulate and eventually uncouple phosphorylation. The chloroplast membranes can also be disrupted. Symptoms appear first on newly mature leaves while old leaves show little sign of injury and expanding leaves are most tolerant. The leaves may be mildly chlorotic or distorted at first. This is quickly followed by a sharply delineated tip or marginal necrosis in some species, by marginal, interveinal or irregular flecks of necrotic tissue, or, in a few species, by basal necrosis. This is followed by leaf abscission.

In a study using 131 species of Australian woody shrubs and trees, eucalypts were found to be more sensitive to exposure to high (1–3 µg/g) levels of SO2 than species of Acacia, Callitris, Casuarina or Melaleuca (O'Connor et al. 1974). However, there was a wide range in sensitivity so that some eucalypt species such as C. maculata, E. botryoides, E. tetraptera and E. urnigera were extremely resistant. Variation in susceptibility also occurs at lower levels of exposure (Howe and Wolz 1981; Norby and Kozlowski 1981; Murray 1984; Wilson and Murray 1994). Under some circumstances exposure to low levels can have an apparent fertilisation effect whereby growth is increased (Murray and Wilson 1989; Clarke and Murray 1990; Fulford and Murray 1990). 16.4.4.2 Fluorides These are the most toxic of the common pollutants. The major industrial sources of airborne F (used here in a generic sense to refer to the fluoride ion and to combined forms of fluoride) are aluminium smelting, manufacture of steel, conversion of fluorapatite to phosphates, and glass, ceramic and brick production. Excess F inhibits photosynthesis, affects respiratory enzymes and inhibits the oxidation of free fatty acids. When leaves absorb F it dissolves in the aqueous phase and is transported acropetally to the end of the vascular system. The first visible symptom of toxicity is a slight chlorotic mottling near the leaf margins. The severity of chlorosis intensifies and marginal necrosis occurs. Distortion of the leaves may occur and in some species, red anthocyanin colours are produced. Susceptibility to visible injury is enhanced by the presence of SO2 (Murray and Wilson 1988a, 1988b). The relative tolerance of several species has been determined by experimental fumigations but the levels of susceptibility determined by the formation of visible symptoms

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may differ from those determined from other effects such as such as those on photosynthesis (Doley 1981; Rutherford et al. 1993). There is a degree of segregation in fluoride tolerance among the subgenera and species of the eucalypts (Doley 1986). Some Symphyomyrtus species (E. brevifolia, E. crebra, E. fibrosa, E. gomphocephala) are tolerant to exposure to fluoride (Horning and Mitchell 1982). Corymbia calophylla, C. citriodora, C. tessellaris and E. cloeziana (in the subgenus Idiogenes) are very sensitive to exposure to fluoride (Doley 1986). Mathematical simulations of atmospheric spread of hydrogen fluoride (HF) and its subsequent deposition on and absorption by a eucalypt forest indicate that the atmospheric concentration falls rapidly with increasing distance from the source and that half of the HF may be deposited within 80 kilometres of the source (Murphy and Ares 1982). Visible symptoms of F toxicity and elevated foliar F concentrations have been observed in E. cladocalyx and E. gomphocephala growing more than two kilometres from the fluoride source (Botha et al. 1989). Observations on an open forest near an aluminium smelter have indicated that tolerant species such as E. fibrosa could be killed depending on the degree of exposure (Murray 1981). The annual sink efficiency of this ecosystem has been estimated as 21 to 23 kg F per hectare (Murray 1982). This is quite small compared with the average annual output (480,000 kg F) from the smelter. 16.4.4.3 Photochemical oxidants Photochemical oxidants include ozone (O3), oxides of N and peroxyacetylnitrate (PAN). They are secondary pollutants which form as the result of sunlight acting on products of combustion, particularly those emanating from internal combustion engines. Injury to eucalypts by photochemical oxidants is most likely to occur in urban environments (Hanson 1972; Krishnamurthy et al. 1986). Ozone disrupts the plasmalemma, allowing leakage of cell contents into the intercellular spaces. The injured leaf develops areas that appear dark-green or water-soaked. These areas may become chlorotic if the chloroplast membranes are also disrupted and bleached as the palisade membrane dries out. In resistant plants, injury may appear as flecks or stippling of the upper leaf surface due to desiccation of small islands of cells. More heavily injured leaves

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form irregular bleached areas which, particularly when they become bifacial, resemble sulphur dioxide injury. Heavily injured leaves abscise. Eucalypts as a group tend to be insensitive to ozone but some species are susceptible to injury (O’Connor et al. 1975). A variety of nitrogen oxides, including the important pollutants nitric oxide (NO) and nitrogen dioxide (NO2), occur in the atmosphere. The concentrations vary diurnally and seasonally. At low concentrations plants are able to assimilate nitrogen oxides and to incorporate them into various compounds such as amino acids with the result that, under some circumstances, growth is enhanced. At higher concentrations toxicity is induced and growth is inhibited. Growth of eucalypt seedlings exposed under field conditions to a mixture of NO and NO2 at a range of concentrations and frequencies is consistent with this bivariant response model (Murray et al. 1994). At low rates of exposure the growth of E. microcorys was increased by about 25% but the response curve had a broad plateau region at higher rates of exposure. Growth of E. globulus and E. pilularis was also stimulated at low exposures but this effect was reversed at higher exposure rates. A similar pattern was observed with E. marginata.

16.5 Water as an abiotic factor 16.5.1 Water stress Water stress can be induced by low water availability due to high matric or osmotic potentials in the rooting medium, by root loss due to mechanical damage or pathogens or physicochemical processes, or by disruption to the transpiration pathways (e.g. by insect or pathogen damage), high temperatures or high vapour pressure deficits. Seedlings subjected to moderate sustained water stress can respond by developing higher root to shoot ratios (Bachelard 1986), fewer, smaller leaves (Myers and Landsberg 1989) or by increasing the concentration of solutes in leaf cells (Myers and Neales 1986). The distribution of eucalypt species in Australia is determined partly by their water requirements (Florence 1981; Gill et al. 1985; see Chapter 4). Monocalyptus species are restricted to the higher rainfall zones and do not occur where annual rainfall is less than about 600 millimetres. Symphyomyrtus

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species occur widely in all parts of the continent but individual sections of the subgenus may have more restricted distributions. Thus, Maidenaira and Transversaria are restricted to high rainfall zones while Bisectaria, Dumaria, Exsertaria and Adnataria extend through the drier regions. There are also local distributional differences whereby Monocalyptus species are often restricted to sites with better water availability than those occupied by Symphyomyrtus. Species in the subgenera Blakella and Eudesmia and in the genus Corymbia tend to occur in the summer rainfall regions in the northern half of Australia with extensions down the east and west coasts. Variation in drought tolerance also occurs within species (Ladiges 1974). Mature leaves of eucalypts are sclerophyllous, tolerant to water deficit and tend to have a more or less vertical alignment that helps reduce leaf temperature and avoid excessive transpiration in the middle of the day. These and various combinations of other attributes result in a wide spectrum of drought tolerance among eucalypt species (Florence 1981). Studies of water use indicate that some species tend to exert limited stomatal control of water loss while others exhibit marked stomatal regulation (Colquhoun et al. 1984). The development of an extensive vertical root system which maximises access to water supplies (Dell et al. 1983; Talsma and Gardener 1986) rather than regulation of water losses may be the key feature of drought tolerance (Florence 1981). However, in semiarid environments where water supply is very limited, water potentials of mallee eucalypt shoots remain very low over long periods without any visible damage to leaves (Myers and Neales 1984). Drought is a characteristic and recurrent feature of climate over much of Australia. Much of the native flora is adapted to drought, but dieback and death of dominant tree species can occur if the drought is prolonged (Cremer 1966; Pook et al. 1966; Ashton et al 1975; Pook and Forrester 1984). There is increasing evidence that drought is also involved in eucalypt diebacks of varying complexity in different parts of Australia (see Chapter 17). The effects of drought are most severe on soils which prevent deep penetration of water and/or roots, on shallow or stony soils with low moisture holding capacity and on slopes exposed to strong radiation and drying winds. They are exacerbated on sites where the natural flow of subterranean water has been

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disturbed by construction of roads, buildings or other works and in trees with roots damaged by disease or other factors. The development of symptoms of drought varies according to the particular combination of climatic circumstances. For example, when relatively high temperatures and large vapour pressure deficits were experienced during a spring drought in 1980, the shedding of mature leaves in a coastal forest dominated by C. maculata was 3.5 times higher than normal with the result that the leaf area index fell from 4.3 to 0.8 (Pook 1985). Despite similar drought circumstances, but with relatively low temperatures and vapour pressure deficits, in 1982 there was no massive shedding of foliage and leaf fall continued at a low rate (Pook 1986). Leaf shedding is an important mechanism whereby plants may reduce their transpiring surface. Its significance in eucalypts is uncertain because most studies of the effect of drought in native forests have not begun until the stands have shown signs of severe water stress. The foliage of dry sclerophyll forest species such as E. macrorhyncha and E. rossii is usually of normal appearance while leaf water potentials are above –3 megapascals but becomes dull and obviously wilted in the range –3 to –5 megapascals and appears severely wilted and chlorotic below –5 megapascals (Pook and Forrester 1984). After wilting, the leaves die and become brown. Individual leaves may die back gradually and only part of the lamina may be affected (Cremer 1966). The dead leaves are persistent and are gradually removed by mechanical abrasion and weathering rather than by abscission. Dieback of twigs, branches and occasionally whole trees may occur. In advanced stages of dehydration in gum-barked species, the bark may shrink, become fissured and eventually become separated from the wood at the cambium (Day 1959; Cremer 1966; Pook et al. 1966). Damage can then be exacerbated by secondary biotic agents (see Chapter 17). Naked buds are often killed during droughts, and consequently recovery depends upon accessory buds from living twigs or, if damage has been severe, from dormant buds protected by thick bark (Cremer 1966). Recovery of the crown is usually good except in cases of extensive defoliation when epicormic growth can be too weak to sustain life. Kino veins

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develop near injured areas of cambium in the stem and branches (Day 1959). In Western Australia, drought has been a particular problem in plantations of E. globulus established on shallow, rocky soils (Plate 16.20). During extended dry periods in summer mortality was high in these plantations but not in nearby plantations on deeper soils. It is highly recommended that shallow soils on hill tops be avoided when planting E. globulus in drought-prone areas. Drought can also be a problem in plantations in Africa (Plate 16.21).

16.5.2 Waterlogging Waterlogging of soils triggers physical, chemical and biological processes which profoundly influence the quality of soil as a medium for plant growth (Ponnamperuma 1984). Within a few hours of flooding, microorganisms and roots use up most of the oxygen present and nitrogen, carbon dioxide, methane and hydrogen then begin to accumulate. Anaerobic decomposition of organic matter leads to the production of phytotoxic products such as ethylene and hydrogen sulphide. Anaerobic respiration also leads to the reduction of Fe and Mn to more soluble forms which may then accumulate to levels toxic to plant roots. Flooding also results in shifts in the populations of soil organisms and in the morphology and function of plant roots. As a consequence, roots may be rendered more susceptible to attack by pathogens such as Phytophthora cinnamomi Rands (see Chapter 11). Most eucalypts of swampy and flood-prone areas belong to the Eucalyptus subgenus Symphyomyrtus but, since most experimental studies have been confined to this subgenus, no firm conclusions can be drawn about the comparative physiological properties of the genera and subgenera (Noble 1989). Symphyomyrtus species differ in the degree to which they produce adventitious roots as a survival mechanism. They also differ in the degree to which they respond to waterlogging by producing ethylene, which in turn stimulates the production of aerenchyma (Blake and Reid 1981). The symptoms of waterlogging in Symphyomyrtus seedlings include leaf epinasty, anthocyanin production and the chlorosis, death and premature fall of older leaves (Parsons 1968; Clemens and Pearson 1977; Ladiges and Kelso 1977; Sena Gomes and Kozlowski 1980; Blake and Reid 1981). Near

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water level the stem may become swollen and split because of hypertrophy of the stem cortex and production of aerenchyma tissue. Adventitious roots may also be produced from this region of the stem (Clucas and Ladiges 1979; Sena Gomes and Kozlowski 1980; Blake and Reid 1981) but are inhibited under saline conditions (van der Moezel et al. 1988). In E. marginata (Monocalyptus), waterlogged seedlings are characterised by wilting, marginal leaf scorching and leaf necrosis (Davison and Tay 1985). Blockages of the lumen of xylem vessels caused by tyloses, particularly in the tap root, also occur and increase in number with the duration of flooding.

16.6 Frost Germinating seeds and newly emergent seedlings are the most frost sensitive stages of the eucalypt life cycle (Cremer and Mucha 1985; Battaglia and Reid 1993). Frost tolerance increases with seedling age but damage, especially of unhardened seedlings, may still occur with temperatures as mild as –4°C. The large photoperiod–temperature interactions that increase frost tolerance or induce dormancy in many northern hemisphere plants are absent in the eucalypt species so far examined. Provided that night temperatures are close to freezing, hardening of eucalypts is independent of photoperiod, light source or day–night temperature differentials (Paton 1981). Although hardening at a rate of –2°C per day has been reported for E. viminalis (Paton 1981), hardening rates are usually slow (e.g. daily: –0.25°C for E. pauciflora, Harwood 1981; –0.7°C for E. nitens, Tibbits and Reid 1987a, 1987b; –0.07°C for E. delegatensis, Hallam and Reid 1989). Some Monocalyptus species have shown a reduced ability to harden under waterlogged conditions whereas such a reduction was not shown by Symphyomyrtus species (Davidson and Reid 1987). Fertilisation with major nutrients may reduce frost tolerance (Ashton 1958; Grose 1960) but addition of B can increase it (Grose 1960; Cooling 1967). After hardening, many Eucalyptus species are damaged if exposed to temperatures below about –10°C but a few may survive temperatures between –15°C and –18°C (Paton 1981). Dehardening can be rapid once the shoots are exposed to mild temperatures (Harwood 1981; Hallam and Reid 1989) but can be delayed if roots are exposed to low temperatures or waterlogging (Paton et al. 1979; Paton 1981).

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Frost damage is caused by the formation of ice in the tissues, with subsequent damage to cell membranes and leakage of ions (Steponkus 1984; ScarasciaMugnozza et al. 1989; Valentini et al. 1990). Leaves may be more severely damaged if they are wet at the time of freezing (Grose 1960; Thomas and Barber 1974; Harwood 1980). Lethal frost damage can be diagnosed by a change in leaf colour and a flaccid appearance immediately after the frost, but clear symptoms are usually not apparent until several days later (Paton 1972). The first symptoms are watersoaked regions and small local lesions. Under some circumstances these areas may recover from injury (Paton 1981) but usually necrosis occurs, giving rise to speckles, spots or scattered patches of dead tissue. Senescence of older leaves is accelerated by frost and severely injured leaves abscise. In small trees, the symptoms appear in the outer, exposed part of the crown (Plate 16.22). Axillary buds are less hardy than leaves (Harwood 1980) and roots are less hardy than shoots (Cremer 1985), while the sensitivity of the cambium varies with bark thickness. In cases of severe defoliation, recovery may occur from secondary buds often from the lower stem or lignotuber and recurrent frost damage can result in the eucalypts becoming shrub-like in form (Farrell and Ashton 1973; Wardle 1985; Gilfedder 1988). In Australia, critically low temperatures occur near tree lines in mountainous terrain (Turnbull and Eldridge 1983). Natural upper limit tree lines are determined by low temperatures. Intermontane tree lines in valleys are determined by inversion layers due to cold air drainage and entrapment. In these localities, there are frequent radiation frosts during winter which reduce leaf temperatures several degrees below air temperature (Leuning and Cremer 1988). The survival, growth and distribution of eucalypt species in these situations depends largely on the depth of the inversion layer and the frequency and severity of frosts (Harwood 1983; Paton 1983; Davidson and Reid 1985). Thus, establishment of eucalypt seedlings is hazardous in frost-prone locations but as the trees grow taller and forest stands develop they are damaged only by unusually severe frosts (Banks and Paton 1993). Frost hollows may also develop in clearings or gaps after harvesting or destruction of forest by fire, with the consequence that regeneration can be seriously affected and changes in species composition can occur (Bond 1945).

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Although eucalypts from the subalpine woodlands are the most frost tolerant, there is greater economic potential for species which combine fast growth rates and good form with a useful degree of frost tolerance (Turnbull and Eldridge 1983). Both Monocalyptus and Symphyomyrtus species occur at the tree line and in high altitude forest. Many of these species have considerable variation in their tolerance of frost (e.g. Ashton 1958; Paton 1972; Tibbitts and Reid 1987b; Hallam and Reid 1989). Freezing resistance in interspecific F1 hybrids is highly heritable and is inherited in a predominantly additive manner (Tibbits et al. 1991). In studies of eucalypts outside Australia, Symphyomyrtus species tend to be listed as highly frost-tolerant more frequently than Monocalyptus species (Noble 1989). This tendency is also apparent on sites subject to waterlogging (Davidson and Reid 1987).

16.7 Artificial environments 16.7.1 High relative humidity Leaves of many eucalypt species develop blister-like galls (intumescences, enations, oedemata) when grown in controlled environment chambers (Warrington 1980). This disorder is induced by high (> 65%) relative humidity. Under these conditions the margins of expanding and recently expanded leaves roll inwards toward the midrib. Galls develop on both leaf surfaces but are most marked on the lower surface (Plate 16.23). The galls are caused by hypertrophy and hyperplasia of mesophyll cells which disrupt the cuticle and stomata. Damage is extensive on young leaves and stem tissue but is restricted to individual galls on old leaves. If the mesophyll cells become isolated from the interior of the leaf there may be extensive development of anthocyanin (La Rue 1933). Similar galls occur in shoots grown in vitro (J.G.P. Svensson, pers. comm.). Galls can also be induced by localised restriction in diffusion of air, water or other substances in leaves associated with psyllid attack or application of greases, pastes, sugar solutions or adhesive tape (Madden and Stone 1984). Monocalyptus species were more sensitive to applied treatments than Symphyomyrtus species. In E. camaldulensis early initiation of phellogen by the stems can be stimulated by high humidity and/or exposure to oxygen or by binding of the stem with polythene strips beneath which condensation of

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water occurs (Liphschitz and Waisel 1970). The first reaction is the development of irregular swellings caused by the division and elongation of cortical cells beneath the epidermis. Distortion and rupture of the twig surface enables oxygen to diffuse into the twigs at higher rates. Meristematic activity begins within the tissues and when phellogen is initiated, several cork layers may form. An apparently related phenomenon occurs when seeds of the mistletoe Phoradendron macrophyllum (Engelm.) Cockerell are germinated on the non-host E. grandis. Typical holdfasts fail to form but wound periderm develops beneath the germlings (Lichter and Berry 1991). Identical layers develop when viscin removed from the mistletoe seeds is applied to the stem.

16.7.2 High temperatures When seedlings are grown at high, sublethal temperatures (36°C/31°C, day/night) growth abnormalities can be induced (Paton 1980). These often involve dense ramifications of short lateral shoots bearing greatly reduced leaves. These shoots are derived from accessory bud tissue following abortion of all primary buds and loss of apical dominance. When this pattern persists the plants develop ‘witches’ broom’ symptoms.

16.7.3 Light quality When light has an imbalanced composition, especially with respect to the red and far-red bands of the spectrum, eucalypt seedlings can be dwarfed due to the inhibition of internode elongation (Cremer 1972).

16.8 Miscellaneous abnormalities On rare occasions leaf abnormalities that may be confused with symptoms of nutrient deficiency or toxicity may be caused by genetic chimeras (Plate 16.24) or ericoid mites (Plate 16.25).

16.9 Conclusion Since the Mid Tertiary the eucalypts have been subject to many selection pressures. The most important adaptations have been to soils of low fertility and to arid climates. To a lesser extent there are species and provenances that are tolerant to frost, or to waterlogged, saline or calcareous soil. Eucalypt genera and major subgenera vary in their general tolerance to several environmental factors but individual species and provenances can be quite

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sensitive to small changes in some factors. These adaptations influence the presence or absence of eucalypts in natural ecological systems and vegetation formations, and on a smaller scale, lead to complex patterns of associations between various eucalypt species. In both natural and exotic environments, the eucalypts are subject to abiotic stress factors which influence their health and survival. In natural ecosystems, evidence for stress is often most apparent near the boundary of the ecosystem or in locations where natural or artificial disturbance has occurred. Of greater concern are cases where managed forests show signs of stress because these may indicate poor management practices or, in the case of plantations or ornamental plantings, that the species or provenance is not well adapted to the particular site. Accurate diagnosis of a disorder needs to be made before effective corrective action can be taken. It is therefore necessary to have a systematic approach which combines investigative skills with careful observation. The first step is to establish the appearance of a 'normal' plant and then to define the ‘abnormality’ and the way it develops over time. It is important to establish the pattern of damage both within the plant and within its community. A non-uniform or scattered damage pattern which spreads progressively within the plant and the community over time is indicative of damage caused by living organisms. Damage which has a uniform pattern within the plant and community, or damage which does not spread within the plant or community is likely to be caused by abiotic factors. The occurrence and severity of stress owing to abiotic factors can sometimes be related to particular topographic or edaphic features or to differences in management practices. For example, dieback and damage resulting from frost or waterlogging is often associated with low lying parts of the landscape whereas dieback due to drought tends to be worse on shallow soils and on aspects exposed to afternoon sun. On soils developed from volcanic or granitic materials, B deficiency tends to occur both in the low-lying areas and on the exposed slopes. Observations such as these form an important part of the diagnostic process. When an abiotic factor is suspected as the cause of the damage, the following key (Key 16.1) can be used in the first step of identifying the factor

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responsible. This key is necessarily very general because: 1

specific visible symptoms are commonly the exception rather than the rule

2

symptoms and the degree of damage can vary according to species, the stage of plant development and according to other non-causal environmental conditions.

More detailed information on visual symptoms is available for nutrient deficiencies in some species (see sections 16.3.2 and 16.3.3). In most cases, visual symptoms will be insufficient for accurate diagnosis. Supplementary microscopic observation of affected plant parts will sometimes be useful. For nutrient deficiency and toxicity, or damage by air pollution, specific chemical analyses of plant tissues or soils may be required to narrow the range of probable causes. In some cases, for example nutrient deficiencies, confirmation of the diagnosis may be obtained by observing a positive response to the application of an ameliorative treatment. Key 16.1 Key for the first phase of identifying the abiotic stress factors which have resulted in specific visible symptoms 1.

Symptoms appear first on the outer exposed portions of the crown. Typically the foliage wilts and later dies... Desiccation due to frost damage, root damage (waterlogging, disease), drought, high salinity.

2.

Symptoms appear first in immature leaves or shoots A. Leaves bronzed or chlorotic, not deformed... Lime chlorosis; iron, manganese or zinc deficiency; sulphur deficiency. B.

Leaf blades cupped or curled, leaf margins distorted, dieback of shoots... Boron, calcium or copper deficiency.

3.

Symptoms occur first in recently matured leaves. Chlorotic mottling, necrotic spots or patches... Air pollution; sulphur dioxide, fluoride or ozone injury.

4.

Symptoms appear first in old leaves

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A. Leaves chlorotic, spots or blotches of red anthocyanin, premature leaf shed... Nitrogen or magnesium deficiency. B.

Leaves not markedly chlorotic, blotches of purple anthocyanin develop... Phosphorus or potassium deficiency.

16.10 References Althoff, P., de Oliveira, A.C., de Morais, E.J. and da Fonseca, S. (1991). Eucalypt dieback in ‘Cerrado’ areas in north-northwest of Minas Gerais. In Proceedings of IUFRO Symposium on Intensive Forestry: The Role of Eucalypts. (Ed. A.P.G. Schönau) pp. 598–609. (South African Institute of Forestry: Pretoria.) Anderson, C.A. and Ladiges, P.Y. (1978). A comparison of three populations of Eucalyptus obliqua L'Herit. growing on acid and calcareous soils in southern Victoria. Australian Journal of Botany 26, 93–109. Anderson, C.A. and Ladiges, P.Y. (1982). Lime-chlorosis and the effect of fire on the growth of three seedling populations of Eucalyptus obliqua L'Herit. Australian Journal of Botany 30, 47–66. Andrew, W.D. and David, D.J. (1959). Iron deficiency in Eucalyptus dives Schauer. Proceedings of the Linnean Society of New South Wales 84, 256–258. Arnon, D.I. and Stout, P.R. (1939). The essentiality of certain elements in minute quantity for plants with special reference to copper. Plant Physiology 14, 371–375. Ashton, D.H. (1958). The ecology of Eucalyptus regnans F. Muell: the species and its frost resistance. Australian Journal of Botany 6, 154–176. Ashton, D.G. and Hargreaves, G.R. (1983). Dynamics of subalpine vegetation at Echo Flat, Lake Mountain, Victoria. Proceedings, Ecological Society of Australia 12, 35–60. Ashton, D.H., Bond, H. and Morris, G.C. (1975). Drought damage on Mount Towrong, Victoria. Proceedings of the Linnean Society of New South Wales 100, 44–69. Bachelard, E.P. (1986). Effects of soil moisture stress on the growth of seedlings of three eucalypt species. II Growth effects. Australian Forest Research 16, 51–61. Banks, J.C.G. and Hillis, W.E. (1968). A survey of the anthocyanins in Eucalyptus camaldulensis. Australian Forest Research 3, 50–53. Banks, J.C.G. and Paton, D.M. (1993). Low temperature as an ecological factor in the cool-climate eucalypt forests. Studia Forestalia Suecica 191, 25–32. Barrett, R.L., Carter, D.T. and Seward, B.R.T. (1975). Eucalyptus grandis in Rhodesia. Research Bulletin 6. (Rhodesia Forestry Commission: Salisbury.) Batianoff, G.N. and Reeves, R.D. (1991). The serpentine flora of the humid subtropics of eastern Australia.

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Proceedings of the Royal Society of Queensland 101, 137–157. Battaglia, M. and Reid, J.B. (1993). Ontogenetic variation in frost resistance of Eucalyptus delegatensis R.T. Baker. Australian Journal of Botany 41, 137–141. Beaucorps, G. de (1959). Rapports entre les peuplements d’eucalyptus et les sols sableux de la Mamora et du Rharb. Annales de la Recherche Forestiere au Maroc 1957, 27–216. Bedendo, I.P. and Krugner, T.L. (1988). Persistence of benomyl in seedlings of Eucalyptus cloeziana and Eucalyptus grandis after soil application. Fitopatologia Brasileira 13, 227–230. Bell, D.T. and Ward, S.C. (1984). Seasonal changes in foliar macronutrients (N, P, K, Ca and Mg) in Eucalyptus saligna Sm. and E. wandoo Blakely growing in rehabilitated bauxite mine soils of the Darling Range, Western Australia. Plant and Soil 81, 377–388. Biddiscombe, E.F., Rogers, A.L., Greenwood, E.A.N. and De Boer, E.S. (1985). Growth of tree species near salt creeps, as estimated by leaf area, crown volume and height. Australian Forest Research 15, 141–154. Blake, T.J. (1981). Salt tolerance of eucalypt species grown in saline solution culture. Australian Forest Research 11, 179–183. Blake, T.J. and Reid, D.M. (1981). Ethylene, water relations and tolerance of waterlogging of three Eucalyptus species. Australian Journal of Plant Physiology 8, 497–505. Boardman, R. and McQuire, D.O. (1990). The role of zinc in forestry. 1. Zinc in forest environments, ecosystems and tree nutrition. Forest Ecology and Management 37, 167–205. Boardman, R., Cromer, R.N., Lambert, M.J. and Webb, M.J. (1997). Forest plantations. In Plant Analysis and Interpretation Manual. 2nd edn. (Eds D.J. Reuter and J.B. Robinson) pp. 505–566. (CSIRO Publishing: Melbourne.) Bond, R.W. (1945). Frost damage to Victorian mountain forest areas. Australian Forestry 9, 21–25. Booth, G.A. (1965). Forestry in the Khashm el Girba scheme. Sudan Silva 2, 3–5. Botha, A.T., Visser, J.H. and Moore, L.D. (1989). Evaluation of possible fluoride injury to vegetation in the vicinity of an industrial site near Cape Town. South African Journal of Science 85, 741–745. Bowen, G.D. (1981). Coping with low nutrients. In The Biology of Australian Plants. (Eds J.S. Pate and A.J. McComb) pp. 33–64. (University of Western Australia Press: Nedlands.) Buttrose, M.S. and Lott, J.N.A. (1978). Calcium oxalate druse crystals and other inclusions in seed protein bodies: Eucalyptus and jojoba. Canadian Journal of Botany 56, 2083–2091. Cheng, W. and Horng, F. (1992). Effect of macronutrient deficiency on the growth and nutrient status of

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Eucalyptus urophylla seedlings. Bulletin, Taiwan Forest Research Institute, New Series 7, 111–120. Clarke, K. and Murray, F. (1990). Stimulatory effects of SO2 on growth of Eucalyptus rudis Endl. New Phytologist 115, 633–637. Clarkson, D.T. and Hanson, J.B. (1980). The mineral nutrition of higher plants. Annual Review of Plant Physiology 31, 239–298. Clemens, J. and Pearson, C.J. (1977). The effect of waterlogging on the growth and ethylene content of Eucalyptus robusta Sm. (Swamp mahogany). Oecologia (Berlin) 29, 249–255. Clucas, R.D. and Ladiges P.Y. (1979). Variations in populations of Eucalyptus ovata Labill., and the effects of waterlogging on growth. Australian Journal of Botany 27, 301–315. Cole, M.M., (1973). Geobotanical and biogeochemical investigations in the sclerophyllous woodland and shrub associations of the eastern goldfields of Western Australia, with particular reference to the role of Hybanthus floribundus (Lindl.) F. Muell. as a nickel indicator and accumulator plant. Journal of Applied Ecology 10, 269–320. Colquhoun, I.J., Ridge, R.W., Bell, D.T., Loneragan, W.A. and Kuo, J. (1984). Comparative studies in selected species of Eucalyptus used in rehabilitation of the northern jarrah forest, Western Australia. 1. Patterns of xylem pressure and diffusive resistance of leaves. Australian Journal of Botany 32, 367–373. Cooling, E.N. (1967). Frost resistance in Eucalyptus grandis following application of fertilizer borate. Rhodesia, Zambia, Malawi Journal of Agricultural Research 5, 97–100. Cooling, E.N. and Jones, B.E. (1970). The importance of boron and NPK fertilizers to Eucalyptus in the southern province, Zambia. East African Agriculture and Forestry Journal 36, 185–194. Cremer, K.W. (1966). Field observations of injuries and recovery in Eucalyptus rossii after a record drought. Australian Forest Research 2, 3–21. Cremer, K.W. (1972). Internode extension of eucalypts reduced in artificial light. Australian Journal of Biological Sciences 25, 849–854. Cremer, K.W. (1985). Effects of freezing the roots and shoots of seedlings of Pinus radiata and three Eucalyptus species. Australian Forest Research 15, 253–261. Cremer, K.W. and Mucha, S.B. (1985). Effects of freezing temperatures on mortality of air-dry, imbibed and germinating seeds of eucalypt and radiata pine. Australian Forest Research 15, 243–251. Cromer, R.N. and Jarvis, P.G. (1990). Growth and biomass partitioning in Eucalyptus grandis seedlings in response to nitrogen supply. Australian Journal of Plant Physiology 17, 503–515. Cromer, R.N., Wheeler, A.M. and Barr, N.J. (1984). Mineral nutrition and growth of Eucalyptus seedlings.

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New Zealand Journal of Forestry Science 14, 229–239. Davey, A.S. (1977). The effects of heavy metals on tree seedlings growth. Honours Thesis, Department of Forestry, Australian National University, Canberra. Davidson, N.J. and Reid, J.B. (1985). Frost as a factor influencing the growth and distribution of subalpine eucalypts. Australian Journal of Botany 33, 357–367. Davidson, N.J. and Reid, J.B. (1987). The influence of hardening and waterlogging on the frost resistance of subalpine eucalypts. Australian Journal of Botany 35, 91–101. Davison, E.M. and Tay, F.C.S. (1985). The effect of waterlogging on seedlings of Eucalyptus marginata. New Phytologist 101, 743–753. Day, W.R. (1959). Observations on eucalypts in Cyprus. 1. The character of gum veins and anatomical indications for their origin. Empire Forestry Review 38, 35–44. Dell, B. (1996). Diagnosis of nutrient deficiencies in eucalypts. In Nutrition of Eucalypts. (Eds P.M. Attiwill and M.A. Adams) pp. 417–440. (CSIRO Publishing: Melbourne.) Dell, B. and Bywaters, T. (1989). Copper deficiency in young Eucalyptus maculata plantations. Canadian Journal of Forest Research 19, 427–431. Dell, B. and Robinson, J.M. (1993). Symptoms of mineral nutrient deficiencies and the nutrient concentration ranges in seedlings of Eucalyptus maculata Hook. Plant and Soil 155/156, 255–261. Dell, B. and Wilson, S.A. (1985). Effect of zinc supply on growth of three species of Eucalyptus seedlings and wheat. Plant and Soil 88, 377–384. Dell, B. and Wilson, S.A. (1989). Zinc nutrition and leaf carbonic anhydrase activity of Eucalyptus maculata seedlings and Trifolium subterraneum. Plant and Soil 113, 287–290. Dell, B. and Xu, D.P. (1995). Diagnosis of zinc deficiency in seedlings of a tropical eucalypt (Eucalyptus urophylla S.T. Blake). Plant and Soil 176, 329–332. Dell, B., Bartle, J.R. and Tacey, W.H. (1983). Root occupation and root channels of jarrah forest subsoils. Australian Journal of Botany 31, 615–627. Dell, B., Jones, S. and Wilson, S.A. (1987). Phosphorus nutrition of jarrah (Eucalyptus marginata) seedlings. Use of bark for diagnosing phosphorus deficiency. Plant and Soil 97, 369–379. Dell, B., Malajczuk, N. and Grove, T.S. (1995). Nutrient Disorders in Plantation Eucalypts. (Australian Centre for International Agricultural Research: Canberra.) Delwaulle, J.C. (1979). Plantations forestières en Afrique tropicale sèche. Techniques et espèces à utiliser. Bois et Forêts des Tropiques 184, 45–59. Doley, D. (1981). Fluoride and the Australian flora. In Proceedings of the Seventh International Clean Air Conference, Adelaide, August 1981. (Eds K.A. Webb

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and A.J. Smith) pp. 463–477. (Ann Arbor Science Publishers: Ann Arbor, MI, USA.) Doley, D. (1986). Plant–Fluoride Relationships. An Analysis with Particular Reference to Australian Vegetation. (Inkata Press: Melbourne.) Elkiey, T. and Ormrod, D.P. (1987). Casuarina and Eucalyptus response to single and multiple gaseous air pollutants. Water, Air and Soil Pollution 36, 365–370. Esparcia, E.G. and Nuño, J.J.G. (1964). Algunos aspectos de la nutricion nitrogenada en plantitas de eucalipto. Spain. Instituto Forestal de Investigaciones & Experiencias, Annales, 82–99. Farrell, T.P. and Ashton, D.H. (1973). Ecological studies on the Bennison High Plains. Victorian Naturalist 90, 286–298. Ferreira, F.A. (1989). Patologia Florestal, Principais Doenças Florestais no Brasil. (Sociedade de Investigacoes Florestais:Viçosa, Brasil.) Florence, R.G. (1981). The biology of the eucalypt forest. In The Biology of Australian Plants. (Eds J.S. Pate and A.J. McComb) pp. 147–180. (University of Western Australia Press: Nedlands.) Froend, R.H., Heddle, E.M., Bell, D.T. and McComb, A.J. (1987). Effects of salinity and waterlogging on the vegetation of Lake Toolibin, Western Australia. Australian Journal of Ecology 12, 281–298. Fulford, G.B. and Murray, F. (1990). Morphogenic changes in Eucalyptus gomphocephala exposed to SO2. Environmental and Experimental Botany 30, 343–347. Ghosh, R.C., Singhal, R.M. and Suri, R.K. (1978). Mortality of Eucalyptus at Haldwani (U.P.) and its relation with soil iron. Indian Forester 104, 240–245. Gibson, N., Brown, M.J., Williams, K. and Brown, A.V. (1992). Flora and vegetation of ultramafic areas in Tasmania. Australian Journal of Ecology 17, 297–303. Gilfedder, L. (1988). Factors influencing the maintenance of an inverted Eucalyptus coccifera tree-line on the Mt Wellington Plateau, Tasmania. Australian Journal of Ecology 13, 495–503. Gill, A.M., Belbin, L. and Chippendale, G.M. (1985). Phytogeography of Eucalyptus. In Australia: Australian Flora and Fauna Series No. 3. (Australian Government Publishing Service: Canberra.) Giulimondi, G. and Arru, G.M. (1959). Primi risultati di esperienze di correzione di terreni argillosi per limpianto dell' eucalitto. Pubblicazioni del Centro di Sperimentazione Agricola e Forestale 3, 257–264. Green, J.L., Maloy, O. and Capizzi, J. (1990). A systematic approach to diagnosing plant damage. Ornamentals Northwest Newsletter 13, 1–24. Grose, R.J. (1960). The silviculture of Eucalyptus delegatensis R.T Baker. PhD Thesis, University of Melbourne, Melbourne.

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Hallam, P.M. and Reid, J.B. (1989). Seasonal and genetic variation in frost hardiness of Eucalyptus delegatensis. Canadian Journal of Forest Research 18, 595–600. Halsall, D.M., Forrester, R.I. and Moss, T.E. (1983). Effects of nitrogen, phosphorus and calcium nutrition on growth of eucalypt seedlings and on the expression of disease associated with Phytophthora cinnamomi infection. Australian Journal of Botany 31, 341–355. Hanger, B.C. and Bjarnason, E.N. (1976). Copper toxicity in Eucalyptus sieberi. Victorian Plant Research Institute Report No. 8, Jan. 1974–Dec. 1975, 46. (Department of Agriculture: Melbourne.) Hanson, G.P. (1972). Relative air pollution sensitivity of some Los Angeles Arboretum plants. Lasca Leaves 22, 86–89. Hartley, A. (1977). The establishment of Eucalyptus tereticornis on tailings from the Bougainville copper mine, Papua New Guinea. Commonwealth Forestry Review 56, 239–245. Harwood, C.E. (1980). Frost resistance of subalpine Eucalyptus species. I. Experiments using a radiation frost room. Australian Journal of Botany 28, 587–599. Harwood, C.E. (1981). Frost resistance of sub-alpine Eucalyptus species. II. Experiments using the resistance index method of damage assessments. Australian Journal of Botany 29, 209–218. Harwood, C.E. (1983). Studies on Eucalyptus frost resistance in a sub-alpine frost hollow. In Proceedings, IUFRO Colloque International sur les Eucalyptus Resistants au Froid, pp. 126–144. (Association FôretCellulose: Nangis, France.) Herbert, M.A. and Schönau, A.P.G. (1990). Fertilising commercial forest species in southern Africa: research progress and problems (Part 2). South African Forestry Journal 152, 34–42. Hillis, W.E. (1956a). Leucoanthocyanins as the possible precursors of extractives in woody tissues. Australian Journal of Biological Sciences 9, 263–280. Hillis, W.E. (1956b). The anthocyanins of the leaves and young bark of Eucalyptus sieberiana F. Muell. Australian Journal of Chemistry 9, 544–546. Hingston, F.J. (1986). Biogeochemical cycling of boron in native eucalypt forests of southwestern Australia. Australian Forest Research 16, 73–83. Horning, D.S. and Mitchell, A.D. (1982). Relative resistance of Australian native plants to fluoride. In Fluoride Emissions. Their Monitoring and Effects on Vegetation and Ecosystems. (Ed. F. Murray) pp. 157–176. (Academic Press: New York.) Howe, T.K. and Woltz, S.S. (1981). Symptomology and relative susceptibility of various ornamental plants to acute airborne sulphur dioxide exposure. Proceedings, Florida State Horticultural Society 94, 121–123. Hussain, A.M.M. and Theagarajan, K.S. (1966). Preliminary studies in the mineral nutrition of

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Eucalyptus "hybrid" seedlings. Indian Forester 92, 285–292. Ingestad, T. (1982). Relative addition rate and external concentration; driving variables used in plant nutrition research. Plant, Cell and Environment 5, 443–453. Jackson, J.K. (1987). Manual of Afforestation in Nepal. Nepal-United Kingdom Forestry Research Project, Forest Survey and Research Office. (Department of Forest: Kathmandu.) Kadeba, O. (1978). Nutritional aspects of afforestation with exotic tree species in the Savannah region of Nigeria. Commonwealth Forestry Review 57, 191–199. Kamala, B.S., Angani, V.G., Parthasarathi, K. and Rai, S.N. (1986). Symptoms of deficiency of trace elements and the associated changes in peroxidase isoenzyme pattern in the seedlings of teak, mahogany and eucalyptus. Van Vigyan 24, 49–55. Karschon, R. (1958a). Investigations on iron chlorosis in Eucalyptus gomphocephala A.DC. La-Yarran 8, 30–32. Karschon, R. (1958b). Leaf absorption of wind-borne salt and leaf secretion in Eucalyptus camaldulensis Dehn. Ilanoth No. 4 (Department of Forests: Israel.) Karschon, R. (1963a). Key to leaf symptoms of mineral deficiencies in Eucalyptus gomphocephala A.DC. Israel Journal of Agricultural Research 13, 177–181. Karschon, R. (1963b). A probable case of magnesium deficiency in Eucalyptus gomphocephala A. DC. Israel Journal of Agricultural Research 13, 173–175. Kaul, O.N., Srivastava, P.B.L. and Bora, N.K.S. (1966). Nutrition studies on Eucalyptus. 1. Diagnosis of mineral deficiencies in Eucalyptus hybrid seedlings. Indian Forester 92, 264–268. Kaul, O.N., Srivastava, P.B.L. and Tandon, V.N. (1968). Nutrition studies on Eucalyptus. 3. Diagnosis of mineral deficiencies in Eucalyptus grandis seedlings. Indian Forester 94, 831–834. Kaul, O.N., Srivastava, P.B.L. and Tandon, V.N. (1970a). Nutrition studies on Eucalyptus. 4. Diagnosis of mineral deficiencies in Eucalyptus globulus seedlings. Indian Forester 96, 453–456. Kaul, O.N., Srivastava, P.B.L. and Negi, J.D.S. (1970b). Nutrition studies on Eucalyptus. 5. Diagnosis of mineral deficiencies in Eucalyptus citriodora seedlings. Indian Forester 96, 787–790. Kaul, R.N., Jha, M.N. and Pande, P. (1982). Lime induced chlorosis in Eucalyptus. Indian Forester 108, 461–463. Knight, P.J. (1988). Seasonal fluctuations in foliar nutrient concentrations in a young nitrogen-deficient stand of Eucalyptus fastigata with and without applied nitrogen. New Zealand Journal of Forestry Science 18, 15–32.

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Knudson, D., Yahner, J.E. and Correa, H. (1970). Fertilizing eucalypts on Brazilian savanna soils. Commonwealth Forestry Review 40, 30–40. Kozlowski, T.T. and Constantinidou, H.A. (1986a). Responses of woody plants to environmental pollution. Part 1. Sources and types of pollutants and plant responses. Forestry Abstracts 47, 5–51. Kozlowski, T.T. and Constantinidou, H.A. (1986b). Responses of woody plants to environmental pollution. Part 2. Factors affecting responses to pollution and alleviation of pollution effects. Forestry Abstracts 47, 105–132. Krishnamurthy, R., Ramesh Babu, Anbazhagan, M., Banerjee, G. and Bhagwat, K.A. (1986). Physiological studies of the leaves of some avenue trees exposed to chronic low levels of air pollutants. Indian Forester 112, 503–511. Lacaze, M. (1963). La resistance des eucalyptus au calcaire actif dans le sol. Compte - rendue dun test precoce. Proceedings of the World Consultation on Forest Genetics and Tree Improvement, Stockholm, Sweden, 23–30 August 1963. Vol. 1, 4/8, 1–10. (Food and Agriculture Organization of the United Nations: Rome.) Ladiges, P.Y. (1974). Variation in drought tolerance in Eucalyptus viminalis Labill. Australian Journal of Botany 22, 489–500. Ladiges, P.Y. (1977). Differential susceptibility of two populations of Eucalyptus viminalis Labill. to iron chlorosis. Plant and Soil 48, 581–597. Ladiges, P.Y. and Ashton, D.H. (1977). A comparison of some populations of Eucalyptus viminalis Labill. growing on calcareous and acid soils in Victoria, Australia. Australian Journal of Ecology 2, 161–178. Ladiges, P.Y. and Kelso, A. (1977). The comparative effects of waterlogging on two populations of Eucalyptus viminalis Labill. and one population of E. ovata Labill. Australian Journal of Botany 25, 159–169. Ladrach, W.E. (1980). Tree growth response to the application of phosphorus, nitrogen and boron at the time of planting in the Departments of Cauca and Valle. Carton de Columbia Investgación Forestale Research Report 59, 1–13. Lamb, D. (1976). Variations in the foliar concentrations of macro and micro nutrients in a fast-growing tropical eucalypt. Plant and Soil 45, 477–492. Lamb, D. (1977). Relationship between growth and foliar nutrient concentration in Eucalyptus deglupta. Plant and Soil 47, 495–508. La Rue, C.D. (1933). Intumescences on leaves of Eucalyptus cornuta, E. coccifera, Hieracium venosum, Mitchella repens and Thurberia thespesiodes. Phytopathology 23, 281–289. Leuning, R. and Cremer, K.W. (1988). Leaf temperatures during radiation frost. Part 1. Observations. Agricultural and Forest Meteorology 42, 121–133.

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Savory, B.M. (1962). Boron deficiency in eucalypts in Northern Rhodesia. Empire Forestry Review 41, 118–126. Scarascia-Mugnozza, G., Valentiny, R., Kuzminski, E. and Giordano, E. (1989). Freezing mechanisms, acclimation processes and cold injury in Eucalyptus species planted in the Mediterranean region. Forest Ecology and Management 29, 81–94. Schönau, A.P.G. (1981). Seasonal changes in foliar nutrient content of E. grandis. South African Forestry Journal 119, 1–4. Schönau, A.P.G. and Herbert, M.A. (1989). Fertilizing eucalypts at plantation establishment. Forest Ecology and Management 29, 221–244. Sena Gomes, A.R. and Kozlowski, T.T. (1980). Effects of flooding on Eucalyptus camaldulensis and Eucalyptus globulus. Oecologia 46, 139–142. Sharma, P.J. and Crowden, R.K. (1974). Anthocyanins in some Eucalyptus species. Australian Journal of Botany 22, 623–627. Skene, D.S. (1965). The development of kino veins in Eucalyptus obliqua L'Herit. Australian Journal of Botany 13, 367–378. Specht, R.L. and Groves, R.H. (1966). A comparison of the phosphorus nutrition of Australian heath plants and introduced economic plants. Australian Journal of Botany 14, 201–221. Steponkus, L.P. (1984). Role of the plasma membrane in freezing injury and cold acclimatisation. Annual Review of Plant Physiology 35, 353–384. Stewart, H.T.L., Flinn, D.W., Baldwin, P.J. and James, J.M. (1981). Diagnosis and correction of iron deficiency in planted eucalypts in north-west Victoria. Australian Forest Research 11, 185–190. Steyn, J.J. and Straker, M.F.B. (1969). The application of boron to gum trees. Rhodesian Agricultural Journal 66, 148. Stone, E.L. (1990). Boron deficiency and excess in forest trees: a review. Forest Ecology and Management 37, 49–75. Talsma, T. and Gardner, E.A. (1986). Soil water extraction by a mixed eucalypt forest during a drought period. Australian Journal of Soils Research 24, 25–32. Taylor, O.C. (1984). Organismal responses of higher plants to atmospheric pollutants: photochemical and other. In Air Pollution and Plant Life. (Ed. M. Theshow) pp. 215–238. (John Wiley and Sons: Chichester.) Thirgood, J.B. (1955). Forest Research. Cyprus, Forest Report 1955, 57–68. (Cyprus Government Printing Office: Nicosia.) Thomas, D.A. and Barber, H.N. (1974). Studies on leaf characteristics of a clone of Eucalyptus urnigera from Mount Wellington, Tasmania. 1. Water repellency and the freezing of leaves. Australian Journal of Botany 22, 501–512.

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Tibbits, W.N. and Reid, J.B. (1987a). Frost resistance in Eucalyptus nitens (Deane and Maiden) Maiden: physiological aspects of hardiness. Australian Journal of Botany 35, 235–250. Tibbits, W.N. and Reid, J.B. (1987b). Frost resistance in Eucalyptus nitens (Deane & Maiden) Maiden: genetic and seasonal aspects of variation. Australian Forest Research 17, 29–47. Tibbits, W.N., Potts, B.M. and Savva, M.H. (1991). Inheritance of freezing resistance in interspecific F1 hybrids of Eucalyptus. Theoretical and Applied Genetics 83, 126–135. Tippett, J.T. (1986). Formation and fate of kino veins in Eucalyptus L’Hérit. IAWA Bulletin (New Series) 7, 137–143. Tokeshi, H., Guimarães, R.F. and Tomazello, F. (1976). Deficiência de boro em Eucalyptus em São Paulo. Summa Phytopatologica 2, 122–126. Truman, R. and Turner, J. (1972). Mineral deficiency symptoms in Eucalyptus pilularis. Technical Paper No. 18. (Forestry Commission of New South Wales: Sydney.) Turnbull, J.W. and Eldridge, K.G. (1983). The natural environment of Eucalyptus as the basis for selecting frost resistant species. In Proceedings, IUFRO Colloque International sur les Eucalyptus Resistants au Froid, pp. 43–62. (Association Fôret-Cellulose: Nangis, France.) Turnbull, C.R.A., Beadle, C.L., West, P.W. and Cromer, R.N. (1994). Copper deficiency: a probable cause of stem deformity in fertilised Eucalyptus nitens. Canadian Journal of Forest Research 24, 1434–1439. Turvey, N.D. and Grant, B.R. (1990). Copper deficiency in coniferous forests. Forest Ecology and Management 37, 95–122. Valentini, R., Scarascia-Mugnozza, G., Giordano, E. and Kuzmitsky, E. (1990). Influence of cold hardening on water relations of three Eucalyptus species. Tree Physiology 6, 1–10. Wallace, I.M., Dell, B. and Loneragan, J.F. (1986). Zinc nutrition of jarrah (Eucalyptus marginata Donn ex Smith) seedlings. Australian Journal of Botany 34, 41–51. Wardle, P. (1985). New Zealand timberlines. 1. Growth and survival of native and introduced species in the

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Craigieburn Range, Canterbury. New Zealand Journal of Botany 23, 219–234. Warrington, I.J. (1980). Humidity-induced gall formation on Eucalyptus species. Australian Forest Research 10, 185–189. Wilcox, M.D. (1982). Anthocyanin polymorphism in seedlings of Eucalyptus fastigata Deane & Maid. Australian Journal of Botany 30, 501–509. Will, G.M. (1961). Some changes in the growth habit of Eucalyptus seedlings caused by nutrient deficiencies. Empire Forestry Review 40, 301–307. Will, G.M. (1985). Nutrient deficiencies and fertilizer use in New Zealand exotic forests. New Zealand, Bulletin 97. (Forest Research Institute: Rotorua.) Wilson, S.A. and Murray, F. (1994). The growth response of sclerophyllous Eucalyptus species to SO2 exposure compared to Pinus radiata. Forest Ecology and Management 68, 161–172. Winterhalder, E.K. (1963). Differential resistance of two species of Eucalyptus to toxic soil manganese levels. Australian Journal of Science 25, 363–364. Worsnop, F.E. (1955). The growth of zinc-sensitive tree seedlings in tinplate and galvanized iron tubes. Australian Forestry 19, 74–86. Yang, P., Bai, R., Jiang, M. and Dong, C. (1991). A study on the withered and red leaves disease of eucalypts. Yunnan Linye Keyi 1, 41–44. Zech, W. and Kaupenjohann, M. (1990). Carences en potassium et an phosphore chez Casuarina equisetifolia, Eucalyptus sp., Acacia auricularformis et Tectona grandis au Sud-Bénin (Afrique occidentale). Bois et Forêts des Tropiques 226, 29–36. Zeijlemaker, F.C.J. (1973). Plant physiology and pathology. Project 424.7P: Investigations into nutrient deficiencies. Wattle Research Institute, Report for 1972–1973, 47–48. (University of Natal: Pietermaritzburg.) Zhong, C. and Reddell, P. (1994). Determining soil nutrient limitations to tree growth: nutrient omission experiments with Eucalyptus grandis on six forest soils. In Australian Tree Species Research in China. (Ed. A.G. Brown) pp. 96–100. (Australian Centre for International Agricultural Research: Canberra.)

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K.M. Old

S

U M M A R Y

Native eucalypt forests and woodlands in Australia and some eucalypt plantations established in other parts of the world suffer from a range of diseases of complex, often poorly known, etiology. Although the causes of these diseases often differ, the symptoms are commonly a progressive dieback of the crown of the tree, death of major crown components and in many cases tree death. The major dieback syndromes of eucalypts that are not attributable to a clearly identifiable pest or pathogen are described for both native forests and woodlands and eucalypt plantations. Hypotheses for the causes of some of the more important dieback syndromes are outlined, including the predisposing role of environmental stresses of physical (drought) and biotic origin (insect defoliation) and the wide range of contributory factors that can result in significant disease. Management strategies devised to reduce the incidence of dieback in affected stands or in forest communities at risk are described.

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17.1 Introduction This chapter is an acknowledgment of the difficulties experienced by forest pathologists in the diagnosis of the causes of several eucalypt diseases. Long-lived organisms such as trees are exposed to many environmental stresses, both abiotic and biotic, that are inimical to vigorous growth and survival. The separation of these factors and assessment of their role in disease is a challenge, especially when coupled with a need to predict the outcome of an outbreak and to recommend management practices to mitigate or remedy the condition (Podger 1981a). Any stand of trees will have a proportion of unthrifty individuals, but where the number of affected trees is excessive, management actions may be needed. As with other tree genera in many parts of the world, planted eucalypts and those which dominate Australian native forests and woodlands have commonly been affected by tree decline and mortality on a large scale (Newhook and Podger 1972; Marks and Idczak 1973; Old et al. 1981). In several examples documented elsewhere in this book, notably dieback of eucalypts and understorey vegetation induced by Phytophthora cinnamomi Rands (see Chapter 11) and dieback of eucalypts induced by Armillaria luteobubalina Watling & Kile (Kile 1981a) (see Chapter 12), primary causal agents have been identified. While the severity of these diseases is modulated by several factors, infection by highly pathogenic organisms is of primary importance. This chapter is restricted to a discussion of some other disease syndromes for which it has not been possible to provide wholly satisfactory explanations and in which disease expression appears to result from complex interactions among biotic and abiotic agents. For some of these diseases, further research may well demonstrate primary causal agents; others, notably certain ‘dieback diseases’, seem to have truly complex etiologies.

17.2 Etiology of diebacks and declines Forest diebacks have been reviewed (Manion 1981; Mueller-Dombois 1983a, 1983b; Innes 1993), as has the influence of stress on susceptibility of trees to pathogens and the etiology of disease (Schoeneweiss 1975; Houston 1981, 1984). Houston considered

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that ‘none of these problems involve a virulent, aggressive or obligate primary pathogen. Rather, each results when trees stressed by some adverse abiotic or biotic environmental factor or factors are rendered susceptible to attacks by organisms of secondary action’. These comments apply to the etiology of eucalypt diseases of complex etiology described in this chapter. Manion (1981) classified the various factors contributing to decline syndromes into three categories. 1

Predisposing factors which put a permanent stress on the tree. Examples can be found in trees planted off site and in naturally regenerated stands where disturbance or change in land use has resulted in a major environmental shift.

2

Inciting factors which are typically short in duration and may be physical (e.g. drought) or biological (e.g. insect defoliation). The tree may recover completely unless it has been predisposed by other factors.

3

Contributing organisms including leaf parasites, stem borers, canker fungi and root pathogens. These organisms feature in most diseases of complex etiology and many examples follow in this chapter. They invade the tissues of trees stressed by other agencies and reduce the chances of recovery (see Chapters 9 and 10).

These concepts are useful in attempting to diagnose and manage diseases of complex etiology, but separation of predisposing from inciting factors may be difficult. For example, the chronic annual defoliation by insect herbivores of some eucalypt species in rural environments in Australia (see below) may assume the status of a predisposing factor. Drought may be short in duration, but the evidence from studies of regrowth dieback in Tasmania is that its effect may be long lasting. In this latter disease syndrome there was no evidence for a predisposing factor other than drought. Mueller-Dombois (1983a, 1983b) has advanced a theory for the etiology of dieback in certain forests where even-aged stands regenerate after rare and cataclysmic events (wildfire, flood, volcanic activity), proposing that dieback may be a natural aspect of stand succession. In Manion’s terminology the ‘predisposing’ factor here is the synchronous (cohort) senescence of even-aged areas of the forest. Drought,

E UCA LYPT D ISEA SES

TAB LE 17 . 1

Dieback

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C OMPLE X E TIOLOGY

C H A P T E R

17

Dieback conditions of complex or undetermined etiology in native eucalypt forests and woodlands Tree species affected

Region of occurrence

Agents implicated

Comments

References

Forest diebacks associated with drought Regrowth dieback

E. obliqua, E. regnans

Tasmania

Drought, defoliators, Management Armillaria spp. prescriptions developed

Kile (1974); West (1979); Podger et al. (1980); Wardlaw (1989)

Gully dieback

E. obliqua

North-east Tasmania

Drought, defoliators, Rare event, no Armillaria spp. recurrence

Felton (1972); Palzer (1981)

Woodland dieback

E. macrorhyncha, E. rossii

ACT and adjoining New South Wales

Drought, stem borers

Rare event, no recurrence

Pook (1981); Pook and Forrester (1984)

Mount Towrong dieback

E. radiata, E. obliqua

Central Victoria

Drought, Armillaria sp.

Rare event, no recurrence

Ashton et al. (1975)

Forest diebacks associated with successional changes High altitude dieback

E. delegatensis

North-east Tasmania

Rainforest succession, understorey competition, possible allellopathy

Can be ameliorated by understorey burning

Ellis (1964); Ellis et al. (1980); Ellis (1981)

Eucalypt crown decline

E. deglupta

Papua New Guinea

Drought or waterlogging, rainforest succession

Riverbanks and floodplains

Arentz (1988)

Forest and woodland diebacks associated with chronic insect herbivory Bell miner dieback

E. saligna

Coastal New South Wales

Insect defoliators and psyllids, weed invasion

Widely distributed in sclerophyll forest, locally severe

Stone (1996); Stone (2000)

Dieback of rural eucalypts

Many species

All States and Territories

Defoliators, pasture management, salinity, canker fungi, old age

Widespread and locally very severe

Kile (1981b); Mackay et al. (1984); Heatwole and Lowman (1986); Landsberg et al. (1990); Old et al. (1991); Neyland (1996)

flood or nutrient depletion act as a trigger for decline and suites of fungi and insects contribute to the widespread death of trees. Some syndromes (e.g. high altitude dieback of Eucalyptus delegatensis in Tasmania and death of E. deglupta in Papua New Guinea) are congruous with the cohort senescence concept.

well-researched examples of significant diseases where one or more biotic agencies interact in a complex but poorly understood way with environmental factors to induce disease of eucalypts. The topic will be dealt with in two parts: 1

diseases of native forests and woodlands of Australia (primarily diebacks)

The above discussion provides a conceptual background for the following discussion of some

2

unexplained or complex maladies of eucalypts grown as exotics in plantations.

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17.3 Diebacks of native forests and woodlands Podger (1981a) pointed out that in less than 30 years Australian forest pathology had moved from the mistaken belief that native forests and woodlands were generally healthy, to a recognition that several serious problems, especially dieback diseases, occur in these forest types. However, the causes of several diebacks, collectively described at the 1973 Lakes Entrance seminar (Marks and Idczak 1973) and discussed at the 1980 Canberra conference (Old et al. 1981), remain equivocal. Table 17.1 lists diebacks of complex etiology that have been observed and studied in native forests, woodlands and pastoral areas of Australia since the 1970s.

17.4 Forest diebacks associated with drought A thread that runs through many of the research findings and their interpretation is the influence of drought as a cause or inciting factor of dieback and its effect on the susceptibility of eucalypts to attack by insects and fungi. This is illustrated by ‘regrowth dieback’ (Table 17.1) which affected dominant and codominant trees of E. regnans and E. obliqua in about 16,000 hectares of high quality stands in southern Tasmania, a further 1000 hectares in the Castra area in the north-west and several locations in the north-east of the State. In the early 1970s a localised drought-related condition also affecting E. obliqua was identified in north-east Tasmania and referred to as ‘gully dieback’ (Table 17.1). Dieback of dry sclerophyll forest in the Australian Capital Territory and adjoining areas of New South Wales was associated with a severe drought in 1964–65 and similar damage occurred three years later at Mount Towrong in central Victoria.

17.4.1 Regrowth dieback The symptoms of regrowth dieback are slow decline, expressed as crown dieback and proliferation of crown epicormic shoots (Plate 17.1), reduced growth rates and higher than average mortality (West and Podger 1980). After a detailed study of many site and stand factors, including the presence of potential pathogens, Podger et al. (1980) were unable to identify a causal agent. An important clue to the cause of regrowth dieback is that only trees aged more than 30 to 40 years were affected. The onset of disease coincided with a series of unusually dry

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summers between 1959 and 1964, and the hypothesis was advanced that the disease was triggered by successive droughts (West 1979). Further episodes of crown dieback have since been observed following droughts in the southern forests in 1972 and in forests in northern Tasmania during 1967, 1972 and 1982. Supporting data for the hypothesis that drought was the inciting factor was provided by Podger (1981b), who nevertheless pointed out the difficulties in the diagnosis of drought as a cause of dieback. Although there is strong circumstantial evidence of the importance of drought as a principle causal factor of regrowth dieback, there is also evidence that stressed trees were predisposed to defoliation by the paropsine beetle, Chrysophtharta bimaculata (Olivier) (Kile 1974), and more significantly, to root rot caused by Armillaria spp. (Kile 1980). In healthy wet sclerophyll forest, more than 70% of excavated roots were infected by Armillaria hinnulea Kile & Watling or Armillaria novae-zelandiae (G.Stev.) Herink (Kile and Watling 1983) in restricted lesions (Kile 1980). The relationship between host stress and susceptibility to Armillaria root disease was reviewed by Wargo and Harrington (1991). In dieback-affected trees, these widely distributed opportunistic pathogens invaded root systems and probably accounted for much of the observed mortality. Witches’ broom-like symptoms also occurred in the upper crowns of trees affected by regrowth dieback (Palzer 1983). Using sap and graft transmission, electron microscopy and staining techniques, evidence was sought for the presence of viruses and mycoplasmas but these agents were not detected (T.J. Wardlaw, pers. comm.). The connection between drought and the onset of regrowth dieback was maintained through studies during the 1980s. A brief synthesis of relationships between drought incidence, tree growth, crown condition and mortality was presented by Wardlaw (1989). Consequently there was enough confidence in the definition of the problem and the prognosis of the effects of the disease on stand productivity for the development of management prescriptions, which were reviewed for Tasmania by Wardlaw (1989). Affected stands are assessed for the severity and extent of dieback and yield predictions and harvesting schedules are adjusted to minimise the losses of merchantable timber.

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17.4.2 Gully dieback Felton (1972) reported death of E. obliqua in gullies in north-east Tasmania. The condition, subsequently called ‘gully dieback’, affected some 2800 hectares and it was apparent that the trees had died in large numbers during the late 1960s and early 1970s. Investigation of the problem following Felton's report showed that no further deaths were occurring. In an account of the etiology of the disease, Palzer (1981) tentatively concluded that the major cause was drought associated with concurrent defoliation by a common leaf skeletoniser, Uraba lugens Walker, followed by secondary attack of some trees by A. luteobubalina. As in the case of regrowth dieback, the extreme nature of the drought was regarded as a critical predisposing factor. The return period of the 1967 drought was estimated to be 250 years which approaches the life span of the affected species. In support of the Felton hypothesis, the affected species (E. obliqua) was shown experimentally to be less drought tolerant than E. viminalis, which occurred in the gullies and was unaffected by gully dieback (Palzer 1981). The evidence for extreme insect defoliation was anecdotal, but the association of A. luteobubalina (a primary pathogen) with some dieback-affected trees suggested a contributory role for this fungus. The etiology of both regrowth and gully diebacks remains hypothetical but the research carried out on these diseases has provided evidence that a rare, intense event may be a limiting factor in tree health.

17.4.3 Drought and dieback in woodlands and dry sclerophyll forests Whereas regrowth dieback and gully dieback are conditions of tall, wet sclerophyll forest and drier tall forests, respectively, drought-related dieback has also been documented for dry sclerophyll forests and woodland of inland Australia, most notably by Pook (1981) and Pook and Forrester (1984) for stands of mixed eucalypts in the Australian Capital Territory (Table 17.1). The etiology was complicated, not by defoliators, but by stem-boring longicorn beetles. Longicorns, especially Phoracantha spp., are eucalypt pests of both native stands and plantations in Australia (Curry 1981) and elsewhere in plantations, for example in California

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(Scriven and Luck 1986), Brazil (Berti Filho et al. 1997) and Europe (Anon. 1981). The distribution of the several eucalypt species that dominate dry sclerophyll woodland and forest communities is markedly influenced by slope, soil depth and aspect. In the Australian Capital Territory, E. macrorhyncha, E. polyanthemos and E. rossii are the major tree species on hill tops and upper slopes not cleared for grazing. The second and third species usually occupy the drier northerly to westerly aspects. Where continuous forest gives way to woodlands and pasture, soils are deeper with more favourable moisture-retaining properties, and species such as E. blakelyi and E. melliodora are common. In the summer of 1964–65 a record drought extended from southern Queensland through to Victoria. Only six millimetres of rainfall were recorded in the Australian Capital Territory during the first quarter of 1965 (the driest for 95 years) and the first six months were the driest on record for Canberra. Wilting of terminal shoots, dieback of major branch components and even tree death were widespread, especially on dry north-facing slopes (Pook 1981; Pook and Forrester 1984). The most severely affected species (about 14% mortality) was E. rossii, paradoxically the species which typically occupies the most drought-prone sites; the woodland/savannah species, E. blakelyi and E. melliodora, which tend to occur on deeper soils, were little affected. The dieback syndrome was complicated by invasion of stems by a species of Phoracantha (Pook 1981). The smooth-barked Symphyomyrtus species, E. rossii, developed severe bark cracks that extended to the cambium of some trees and provided ideal sites for oviposition. Recovery after the drought appeared to be impaired by these longicorns, whose feeding in the live underbark was in some cases extensive enough to girdle the tree. The fibrous barked species, E. polyanthemos, suffered few bark splits and only minor stem borer damage. At first examination this woodland dieback appears to be a simple example of drought-induced death. However, the syndrome encompasses subtle relationships between tree community structure, morphology and physiology of contrasting species and their responses to water stress, compounded by predisposition of trees to insect attack.

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A further example of drought damage to montane sclerophyll forest was reported by Ashton et al. (1975) who studied the effects of a severe drought on codominant trees and shrubs on the slopes of Mt Towrong, Vic. Damage was chiefly confined to exposed westerly slopes and the margins of creeks and dry gullies. The distribution of the damaged patches of vegetation could be explained largely by the moisture-supplying capacity of the sites, stand density and the relative responsiveness of tree species to water stress. As with ‘gully dieback’ in Tasmania, some drought-stressed trees later succumbed to Armillaria infection [reported as A. mellea (Vahl:Fr.) P.Kumm.], later identified as A. luteobubalina (Kile 1981a).

17.5 Forest diebacks associated with successional changes Some dieback conditions of forest species are associated with natural successional changes, particularly the transition from tall eucalypt forest with a developing rainforest understorey to climax rainforest from which eucalypts are absent. The timing and rate of transition may be affected by environmental factors. Examples of this syndrome are the dieback of E. delegatensis in the high altitude forests of Tasmania and dieback of E. deglupta in the lowlands of New Britain, Papua New Guinea.

17.5.1 High altitude dieback Eucalyptus delegatensis is one of the principal timber species in south-east Australia. In north-east Tasmania it occurs in association with temperate rainforest species which eventually form the climax vegetation. For many decades stands in this region above 800 metres were observed to be declining in vigour, leading to the term ‘high altitude dieback’ (Ellis 1964). Eucalypt decline in these highland areas is nearly always associated with the development of a dense understorey of rainforest species including myrtle [Nothofagus cunninghamii (Hook.) Oerst.], the dominant tree species in mature rainforest. Dieback of eucalypts in these communities seems not to be new as some stands of myrtle more than 200 years old contain remnants of decaying eucalypts on the forest floor although no standing eucalypts remain (Ellis 1981). Ellis (1981) summarised the events leading to dieback and considered the death of the eucalypts, pioneer colonisers of burnt or otherwise disturbed sites, as part of the succession to climax rainforest.

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The unravelling of the mechanisms contributing to eucalypt decline over extended periods is difficult, but the severity of dieback appears to be related to fire history. Stands where frequent fires have prevented the development of a vigorous rainforest understorey show little dieback, whereas those unburnt since the beginning of the twentieth century, and which therefore contain vigorous rainforest understorey, are severely affected. Also soils beneath long unburnt stands showing dieback appeared to be inhibitory to eucalypt seedling growth, suggesting a possible allelopathic effect. Ellis et al. (1980) have shown experimentally that by felling and burning understorey, dieback can be checked and eucalypt tree growth stimulated. They recommend that if the aim of management is to grow E. delegatensis for commercial timber harvest, then controlled burning at intervals of 30 to 50 years is probably necessary to maintain the health of the eucalypts.

17.5.2 Crown decline of Eucalyptus deglupta in Papua New Guinea Although occurring in a tropical environment, crown dieback of E. deglupta, as reported in Papua New Guinea by Arentz (1988), has some features in common with the high altitude dieback syndrome discussed in the previous section. While E. delegatensis regenerates after fire and is eventually replaced by temperate rainforest, E. deglupta regenerates on river banks and floodplains following catastrophic flood damage and is eventually replaced by tropical rainforest. Senescence of the even-aged E. deglupta stands, evidenced by crown dieback, may be triggered by extreme events such as droughts or inundations that result in accelerated return to climax forest. Arentz was unable to provide further information on the etiology of the condition but suggested that it was an example of stress-induced cohort senescence (Mueller-Dombois 1983a,1983b).

17.6 Forest and woodland diebacks associated with chronic insect herbivory 17.6.1 Bell miner dieback Eucalypt stands within moist coastal regrowth forest in eastern Australia from south-central Victoria to southern Queensland are often colonised by native bell miners [Manorina melanophrys (Latham, 1802)] (Loyn et al. 1983; Stone 1996). These are

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insectivorous birds that live in colonies of up to 200 individuals occuping an area that can extend to several hectares (Clarke and Fitz-Gerald 1994). They are aggressive toward other insectivorous birds and predators, the populations of which are drastically diminished within bell miner territories. Areas of colonised forest commonly show crown decline with some species, especially E. saligna and E. paniculata, being more severely affected than others (e.g. E. pilularis). Results from two study sites in New South Wales indicated that susceptible E. saligna trees were subjected to a relatively high and chronic level of damage from high populations of a large suite of phytophagous insects, especially psyllids. At least 16 different species of psyllid were found on affected E. saligna foliage (Stone 1996). Interference in the effectiveness of both vertebrate (e.g. insectivorous birds) and invertebrate (e.g. parasitoids, spiders) regulatory agents by the bell miners appears to enable some phytophagous insect populations to remain at damaging levels over prolonged periods. Affected trees are unable to sustain repeated cycles of foliage loss and replacement, and over time develop symptoms of dieback. Several predisposing stresses for tree dieback have been proposed, including climate variation, site quality or tree species growing off site, composition and age of stands, and site disturbance including logging and fire history. The inciting factor appears to be associated with colonisation by bell miners, which in turn results in an increase in populations of leaf sucking and chewing insects in the crowns of susceptible tree species. Affected trees then suffer from attack by various contributory agents, including insect borers and fungal pathogens. Gap development through tree death and crown thinning encourages the invasion of the stands by exotic weeds (e.g. lantana or native vines) and provides favourable nesting sites for the expanding population of bell miners. The complex etiology of this widespread syndrome, illustrated in Stone (2000), requires further study to validate several of its components. At present no control measure has been developed that is consistent with the multiple-use objectives in these highly valuable mixed eucalypt forests.

17.6.2 Dieback of rural eucalypts Dieback of remnant eucalypts on intensively managed pastoral and cropping land in Australia

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(Plates 17.2 and 17.3) is undoubtedly the most widespread, serious form of dieback of native trees on the continent. During the late 1980s and 1990s there has been an increased awareness of the value of trees on agricultural land. Research on rural dieback has been strongly supported by rural communities in which previously wholesale clearing of land was actively encouraged by tax incentives. An appreciation of the scope of the problem and the hypotheses of cause that have been advanced can be gained from reviews by Old et al. (1981), Heatwole and Lowman (1986), Landsberg and Wylie (1983), White (1986), Landsberg and Wylie (1988), Landsberg et al. (1990), Jones et al. (1990) and Neyland (1996). Widespread death of trees in the pastoral tablelands of eastern Australia is certainly not a new phenomenon. In 1886, Norton read to the Royal Society of Queensland a paper entitled ‘On the decadence of Australia’s forests’ (Norton 1886). He reported seeing thousands of acres ‘chiefly in the New England district of New South Wales, where a plague seems to have carried death through the forest’. One hundred years later the same region has shown an extreme manifestation of the rural dieback problem (referred to as ‘New England dieback’), although the relationship between the historic dieback events and the modern problem is not clear. The research into forest diebacks during the 1970s led to the identification of many factors of the altered environment that were potentially damaging to the health of remnant eucalypts (Kile 1981b). Yet, one century after Norton's paper was delivered, a definitive description of its etiology was not yet possible (Landsberg and Wylie 1988). Subsequent reviews of tree decline have identified climatic and biotic factors which appear to be regionally important; for example, browsing of eucalypts by the common brushtail possum [Trichosurus vulpecula (Kerr, 1792)] is a contributory factor in rural tree decline in central and eastern Tasmania (Neyland 1996). Many conceptual models of rural tree decline have been developed. One model is that recurrent defoliation by phytophagous insects leads to exhaustion of starch reserves in the trees and their consequent decline (Mackay et al. 1984). This suggestion was further refined by Richards (1981), who considered that the decline resulted from a change in energy flow to the soil. Instead of

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the normal flow through the tree, he considered that energy flowed through insects to the soil. Root dysfunction was proposed as the ultimate cause of tree death, but the hypothesis has not been tested experimentally. White (1986) considered that weather, especially the juxtaposition of extreme wet and dry periods, induced stress in trees and led to dieback. He showed that a calculated stress index had increased markedly during two major surges of dieback incidence in the Armidale area of New South Wales and suggested that the dieback recorded in the 1800s had a similar explanation. Increased insect feeding resulted from higher nitrogen levels in stressed foliage and stressed trees were also likely to be more susceptible to fungal attack (although such pathogens were not identified). No differences were detected in predawn water potentials of diebackaffected and healthy eucalypts in the Australian Capital Territory during the extremely dry summer of 1982–83 (Landsberg 1985) and Crombie and Milburn (1988) found no differences in water relations between healthy and dieback-affected trees in the New England tablelands. Research by Lowman and Heatwole (1992) in the same region suggested that dieback is more severe during a sequence of moist summers, which favours increased abundance of scarab beetles (Bell 1985). Extrapolating from a well-researched example of retrogressive changes in the vegetation of dune systems, where soils had been reduced over the millenia to a low nutrient status, Walker et al. (1983) proposed that vegetation dieback on the tablelands of New South Wales could have been induced by reduced nutrient status of the soils, accelerated by farming systems. However, this hypothesis has not been tested. Indeed, research by Landsberg et al. (1990) suggests that irregular nutrient enhancement of paddocks by stock camping under trees may exacerbate dieback. Duggin (1981) and Jones et al. (1990) sought the solution in relationships between dieback, land forms and land use. They found evidence that dieback is not necessarily lessened by an increase in species diversity, or increased by superphosphate application, although no causal relationships emerged from their study. From the available information, several key factors emerge. Firstly, the influence of weather, especially drought, can undoubtedly predicate tree death, as shown by Pook (1981). However, it also depresses insect populations, notably the pasture scarabs that

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are major defoliators of woodland eucalypts (Roberts et al. 1982). Drought also influences the stocking rates and probably reduces grass competition, especially from the exotic herbage species predominant in ‘improved’ pasture, and so the relationship of drought to rural dieback remains equivocal. Secondly, insect feeding, which varies in local intensity and the importance of particular insect species (Ohmart and Edwards 1991) is a constant part of the disease syndrome. In eastern Australia, scarab beetles are major eucalypt pests. Other groups of defoliators, including leaf skeletonisers (Roberts and Sawtell 1981) and psyllids (Clark and Dallwitz 1975; Ward and Neumann 1982; Morgan and Taylor 1988), are also commonly associated with death of young trees and dieback of established woodland eucalypts. Thirdly, changing land management practices, especially the high stocking intensity of introduced grazing animals, influences soil chemistry and reduces the natural regeneration of seedlings required to replace senescent trees. The most persuasive and unifying hypothesis yet to emerge is that of Landsberg and coworkers (Landsberg and Wylie 1988; Landsberg 1990a, 1990b, 1990c; Landsberg et al. 1990). The hypothesis encompasses the three key factors listed above and has been refined by research carried out in the Australian Capital Territory and adjacent New South Wales. The research project involved detailed study of paired woodland communities matched in all respects except their grazing history which was linked to contrasting structure of understorey vegetation. One of each pair was regularly grazed, whereas the other was rarely subjected to grazing by sheep. The hypothesis is centred on the importance of chronic defoliation of eucalypts in pastures and remnant woodlands as a cause of dieback. Five possible explanations were explored: 1

Periods of high levels of defoliation may be natural in eucalypt woodlands, and rural dieback is a naturally occurring phenomenon (White 1986).

2

Trees in remnant woodlands may be chronically stressed by factors such as soil degradation, increased physical exposure or old age, and are less able to replace foliage lost to defoliators (Landsberg and Wylie 1988).

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Selective removal of trees to promote pasture may have resulted in increased abundance of

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insects, especially scarabs with larvae feeding on tree roots, on the remaining trees (Roberts et al. 1982).

depleted carbohydrate reserves. Although no claims were made for a primary role for these fungi, they probably hasten death of infected branches.

4

Floristic and structural simplification of remnant woodlands may have reduced the diversity and abundance of natural predators (parasitoids, insectivores) of defoliating insects, allowing their numbers to increase (Davidson 1980).

5

Increasing soil fertility associated with pasture improvement may have improved the dietary quality of tree foliage sufficiently to allow increased abundance of defoliating insects (Landsberg 1988). Chronic defoliation by these insects then stressed the trees beyond their capacity to recover.

Because of the extent of rural dieback, its complex etiology and the multiplicity of factors that affect the health of trees on farms, no ready prognosis is possible. Severe doubts have been expressed that the characteristic landscape of the eastern tablelands of New South Wales, of pasture complemented by isolated shade trees and remnant woodland, will survive more than a few decades (Heatwole and Lowman 1986). More particularly, Landsberg et al. (1990) have concluded that the E. blakelyi–E. melliodora woodlands of the southern tablelands of New South Wales are now only a severely degraded remnant of a once widespread vegetation type. If Landsberg's hypothesis is valid, then conservation of this vegetation type could be achieved by the enclosure or minimal grazing of remnant woodlands. Replanting of trees in the pastoral areas of Australia is widely advocated and is being implemented on an increasing scale as a way of reducing or even reversing processes of land degradation such as erosion and dryland salinity. Landcare groups favour the planting of local species and provenances of trees as a means of conserving biodiversity. There is a considerable risk that these initiatives will have limited success due to the same dieback processes that affect remnant trees.

Landsberg et al. (1990) concluded that explanation 5 was the only one to fit the observed patterns of dieback and insect damage. As drought-stressed trees also show altered foliar nitrogen concentrations (Landsberg and Wylie 1983), the hypothesis does not exclude the influence of drought as a factor predisposing eucalypts to feeding. The hypothesis (Fig. 17.1) needs further testing, especially with regard to the effects of enhanced levels of leaf nutrients on a broader range of defoliators. Defoliation need not lead to tree death. Eucalypts, through epicormic growth responses, can quickly replace lost shoots and leaves, but this represents a drain of carbohydrate reserves. Mackay et al. (1984) suggested that successive cycles of epicormic growth and defoliation exhaust starch reserves. This depletion is compounded by late flushing followed by autumn frosts and results in crown decline and eventual death. Note that repeated insect defoliation leading to tree decline is also a feature of bell miner dieback discussed above, although in the latter case the affected stands are in wetter coastal forests. Crowns of trees suffering from rural dieback had many cankers which wholly or partially girdled main branches (Old et al. 1991). A range of fungi, notably Endothia gyrosa (Schwein.:Fr.) Fr., Botryosphaeria ribis Grossenb. & Duggar and Cytospora eucalypticola Van der Westh., were associated with these cankers and the first two species showed enhanced pathogenicity in experimentally defoliated trees (see Chapter 10). Such opportunistic pathogens appeared to be responsible for girdling limbs of trees suffering from chronic defoliation (Plate 17.2) and

In order to increase the survival chances of replanted eucalypts, it may be possible to select genotypes with resistance to insect attack. Foliage on individual trees of several woodland eucalypts and in one instance on a single branch of E. melliodora varies in its cineole content to such an extent that some high cineole types are extremely resistant to insect defoliation (Edwards et al. 1990). Seed was selected from these ‘chemotypes’ and propagated with the aim of providing resistant material for establishment in dieback-prone areas. Two distinct populations of E. camaldulensis were observed in a native forest in southern New South Wales which differed in total foliar terpenoid and cineole content (Stone and Bacon 1994). Trees with high 1,8-cineole content suffered less herbivory than those with lower oil content. They proposed that tree selection for high 1,8-cineole content could be a means of reducing herbivory in E. camaldulensis plantations and restoring native eucalypt species to cleared land.

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planting exotic pasture species

removing trees fertiliser application

camping at provide more base of trees roots for larvae of some defoliating insects damage to improved soil saplings nutrient status no new growth of trees attraction of insects to nutrient-rich leaves

loss of habitat for predators and parasites possible increased salinity

increase in leaf nutrients enhanced insect reproduction rate increased local population of tree-feeding insects long-term defoliation tree stress probable increase in susceptibility to damage by fungi

climate fluctuations

tree death Figure 17.1

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Flow diagram of an hypothesis to explain the complex causes of rural dieback associated with the transformation of native eucalypt woodland to improved pastures for livestock (from Landsberg et al. 1990). Figure redrawn from Ecos 62 with permission of CSIRO and the authors.

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17.7 Plantation diseases of complex etiology 17.7.1 Australian plantations There are no examples in Australia of diseases of complex etiology in eucalypt plantations comparable in severity to those described above in native eucalypt forests and woodlands. This probably reflects the limited extent of plantations in Australia. However, the area planted to eucalypts has increased greatly during the 1990s and is approaching 250,000 hectares (see Chapter 1). The greatest proportion of this estate has been established on former agricultural and grazing land, with E. globulus being the most commonly grown species in southern mainland Australia and E. nitens being the most common species in Tasmania. The various factors contributing to diseases of complex etiology in native forests also apply to plantations. It is to be expected that such diseases will be encountered as eucalypts are planted more widely in Australia, especially where trees are grown outside their natural range and where planting occurs on more marginal sites as the land base suitable for eucalypt planting dwindles. For example, in the Australian Capital Territory a trial planting of a tall wet forest species, E. nitens, on ex pasture was virtually destroyed by a combination of defoliating insects (Farrow, pers. comm.) and canker fungi (Kubono, unpublished data). These organisms are commonly associated with rural dieback of native woodland species in the same area and readily adapted to the plantation species. Moisture stress was probably a predisposing factor as the local rainfall is about half of that in the natural environment of E. nitens. The recent increasing interest in plantation establishment in Australia, especially on former grazing lands, is likely to result in some failures from ‘off site’ planting. Such mistakes can be minimised by systematic matching of species and provenances to site through the use of climatic mapping programs (Booth 1996). With the large investment involved in plantations and the consequent need to monitor growth and damage from pests and diseases, factors contributing to disease probably will be identified more readily in plantations than in native forests and remedies should be feasible. For example, selection for enhanced or improved resistance will usually be an option in plantations, even in the absence of a full understanding of the etiology of the disease.

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Where insects combine with fungi to damage trees, it may be possible to control one or the other by chemical, genetic or silvicultural means.

17.7.2 Plantations outside Australia 17.7.2.1 Mal do Rio Dôcé As implied by its colloquial name, this is a disease of unknown etiology locally severe in the Rio Dôcé valley of Minais Gerais State, Brazil. Since first being recognised in 1974, about 30,000 hectares of eucalypt plantation have been affected. Despite detailed knowledge of symptomology (Dianese and Moraes 1986), the cause of the disease remains obscure. Symptoms (Plate 17.4) include defoliation and shoot dieback followed by branching which results in poor tree form, girdling branch cankers and reduced stem increment. A wide range of eucalypts is affected including those of most commercial value. Dianese et al. (1984) summarised the various hypotheses as to the cause, including unfavorable soil and water factors, air pollution and acid rain. No evidence has been found suggesting a primary causal role for fungi, including root pathogens. Although foliar and stem pathogens, notably Colletotrichum gloeosporioides (Penz.) Penz. & Sacc., may contribute to some of the dieback and girdling of trees affected in the field (Dianese et al. 1985), they are probably secondary. Certain provenances of E. camaldulensis, E. pellita, E. punctata, E. resinifera and E. saligna and a clone of E. grandis appear to be field resistant (Dianese et al. 1984). Corymbia torelliana appears to be highly resistant (J.C. Dianese, pers. comm.). Use of resistant species, provenances or clones offers the opportunity for disease management even if the etiology remains obscure. 17.7.2.2 Gummosis and canker of Eucalyptus grandis in Zimbabwe Since 1986 gummosis and canker of E. grandis have been a cause of concern in Zimbabwe (Masuka 1990). The term ‘gummosis’ for eucalypts is strictly incorrect, as the secretion which forms in cambial tissue and exudes from wounds is phenolic in nature and is more correctly termed ‘kino’ (Hillis 1972). Surveys have established that the condition is widespread in Zimbabwe and is the most important eucalypt disease in the country (Masuka 1990). Trees aged two years and older are affected by kino exudation, stem swelling and cankers. In the worst

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affected stands, up to 30% of trees have been affected and indications are that diseased trees eventually die. Several contributory organisms have been noted, including the ascomycete, Botryosphaeria dothidea (Moug.:Fr.) Ces. & De Not., an unidentified basidiomycete and the longicorn beetle, Phoracantha semipunctata (Fabricius). The condition has not increased its range and is likely to be of complex or abiotic cause (A. Masuka, pers. comm.) with the above organisms being secondary. 17.7.2.3 Sudden death of Eucalyptus globulus in California Eucalypts (mostly E. globulus) have been planted widely in the San Francisco Bay area of California for more than 100 years, and apart from occasional frost damage, have been relatively healthy. Since 1986 there have been regular reports of deaths often of large trees (> 70 cm diameter), with the time to death from first symptoms of wilted foliage being only two to four months. The condition has been called ‘sudden death of eucalypts’ and has so far been restricted to E. globulus (McCain et al. 1989). Brown streaking of xylem occurs in major roots and upper branches of some trees. There is circumstantial evidence for root-to-root spread of the disease. An unidentified fungus was readily isolated from discoloured xylem, and stem, root and branch inoculation of E. grandis, E. camaldulensis and E. globulus produced cankers, although these healed after several months (A.H. McCain, pers. comm.). Although the longicorn, Phoracantha semipunctata, a well-known insect pest of eucalypts (Hadlington and Johnston 1988), now occurs in the Bay area (Scriven and Luck 1986), the condition predates its first record and longicorn attack may be secondary. The etiology of sudden death disease remains unclear. 17.7.2.4 Other diebacks of eucalypts in plantations The following eucalypt diebacks have been reported also. 1

Dieback and mortality of E. grandis associated with drought in Uganda (Karani 1975). Unsuccessful attempts were made to relieve this problem by fertilisation as minor element deficiency was suspected.

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Dieback of seedlings of tropical eucalypts in the Solomon Islands caused by the coreid bug

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Amblypelta cocophaga China (Macfarlane et al. 1976). The problem was reportedly controlled by clearance of understorey vegetation and establishment of the predacious ant Oecophylla smaragdina (Fabricius) which preys on the bug. As the eucalypts presumably benefited from weed control, the cause of the dieback and the mechanism of amelioration remain unclear. 3

Dieback of E. globulus in Colombia (Orozco Jaramillo and Copete Perdomo, undated) is reportedly due to potassium deficiency and secondary infection by Pestalotiopsis sp. (as Pestalotia sp.).

It is likely that the above diseases may have complex etiology, in which trees predisposed by abiotic stresses are further damaged by secondary fungal or insect attack.

17.8 Conclusion The diseases discussed in this chapter share features with those discussed in other chapters of this book in that the incidence and expression of disease invariably results from interactions between pathogen(s), the host, and physical and biotic factors of the environment. For diseases of complex etiology, however, it is very difficult, given our present knowledge, to apportion causal roles and establish the relationship between predisposing factors (stresses) and pathogenesis. The forest manager seeks to mitigate the disease and its economic effect and a detailed knowledge of all aspects of the syndrome may be unnecessary for the development of adequate control prescriptions. For native forests, the determination of relationships between changing forest management practices and disease incidence may give the opportunity to prescribe remedies or avoid losses. Examples discussed here of means to reduce the level of dieback in affected stands include modified harvesting plans (regrowth dieback), prescribed burning (high altitude dieback) and modified pasture and woodland grazing regimes (rural dieback) (see Chapter 19). For plantations, selection of the most appropriate species and provenance for the environment is the starting point for stand health management (see Chapter 22). Some diseases of complex etiology occurring during establishment and stand development are probably due to ‘off site’ plantings. In such situations, stressed trees are subjected to

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secondary factors, especially insect and fungal attack, which result in puzzling ‘diseases’ which may never be adequately characterised. Research on Mal de Rio Dôcé in Brazil illustrates that selection for resistance can provide a management solution even when the cause of a serious disease is not well understood. Such selection probably involves, fundamentally, selection for species or provenances that are better adapted to the particular site.

17.9 References Anonymous (1981). Europe-insect pests on eucalyptus. Plant Protection Bulletin FAO 29, 77. Arentz, F. (1988). Stand-level dieback etiology and its consequences in the forests of Papua New Guinea. GeoJournal 17, 209–215. Ashton, D.H., Bond, H. and Morris, G.C. (1975). Drought damage on Mount Towrong, Victoria. Proceedings of the Linnean Society of New South Wales 100, 44–69. Bell, H.L. (1985). Seasonal variation and the effects of drought on the abundance of arthropods in savannah woodland on the Northern Tablelands of New South Wales. Australian Journal of Ecology 10, 207–221. Berti Filho, E., Perecin, M.F. and Bernadi, E.B. (1997). Possibility of classical biological control of Phoracantha semipunctata Fabricius (Coleoptera, Cerambicidae). Revista de Agricultura 72, 350 (Piricicaba-SP) Brazil. Booth, T.H. (1996). The development of climatic mapping programs and climatic mapping in Australia. In Matching Trees and Sites. Proceedings of an International Workshop held in Bangkok, 27–30 March 1995, ACIAR Proceedings No. 63 (Ed. T.H. Booth) pp. 38–42. (Australian Centre for International Agricultural Research: Canberra.) Clark, L.R and and Dallwitz, M.J. (1975). The life system of Cardiaspina albitextura (Psyllidae). Australian Journal of Zoology 23, 523–561. Clarke, M.F. and Fitz-Gerald, G.F. (1994). Spatial organisation of the cooperatively breeding bell miner, Manorina melanophrys. Emu 94, 96–105. Crombie, D.S. and Milburn, J.A. (1988). Water relations of rural dieback. Australian Journal of Botany 36, 233–237. Curry, S.J. (1981). The association of insects with eucalypt dieback in south western Australia. In Eucalypt Dieback in Forests and Woodlands. (Eds K.M. Old, G.A. Kile and C.P. Ohmart) pp. 130–133. (CSIRO: Melbourne.) Davidson R.L. (1980). Local management. In Focus on Farm Trees. (Eds N.M. Oates, P.J. Greig, D.G. Hill. P. A. Langley and A.J. Reid) pp. 89–98. (Capitol Press: Box Hill, Vic.)

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Dianese, J.V.A. and Moraes, T.S.A. (1986). Sintomatologia do ‘Mal do Rio Dôcé’: Enfermidade do Eucalipto. Fitopatologia Brasileira 11, 49–258. Dianese, J.C., Haridasan, M. and Moraes, T.S. de A. (1984). Tolerance to ‘Mal do Rio Dôcé’ a major disease of Eucalyptus in Brazil. Tropical Pest Management 30, 247–252. Dianese, J.C., Ribeiro, W.R.C. and Moraes, T.S. de A. (1985). Colletotrichum gloeosporioides associated with lesions on branches of Eucalyptus pellita affected by the ‘Mal do Rio Dôcé’ disease. Turrialba 35, 29–32. Duggin, J.A. (1981). The use of ecological provinces and land systems in the study of eucalyptus dieback on the New England tablelands. In Eucalypt Dieback in Forests and Woodlands. (Eds K.M. Old, G.A. Kile and C.P. Ohmart) pp. 245–260. (CSIRO: Melbourne.) Edwards, P., Wanjura, W.J. and Brown, W.V. (1990). Mosaic resistance in plants. Nature 347, 434. Ellis, R.C. (1964). Dieback of alpine ash in northern Tasmania. Australian Forestry 28, 75–90. Ellis, R.C. (1981). High altitude dieback and secondary succession as influenced by controlled burning. In Eucalypt Dieback in Forests and Woodlands. (Eds K.M. Old, G.A Kile and C.P. Ohmart) pp. 205–211. (CSIRO: Melbourne.) Ellis, R.C., Mount, A.B. and Mattay, J.P. (1980). Recovery of E. delegatensis from high altitude dieback after felling the understorey. Australian Forestry 43, 29–35. Felton, K.C. (1972). Eucalypt diebacks in Tasmania. Appita 26, 207–208. Hadlington, P. and Johnston, J. (1988). Australian Trees— Their Care and Repair. (New South Wales University Press: Sydney.) Heatwole, H. and Lowman, M. (1986). Dieback: Death of an Australian Landscape. (Reed Books: Frenchs Forest, NSW.) Hillis, W.E. (1972). Properties of eucalypt woods of importance to the pulp and paper industry. Appita 26, 113–122. Houston, D.R. (1981). Stress-triggered Tree Diseases: The Diebacks and Declines. (USDA Forest Service: Washington, DC.) Houston, D.R. (1984). Stress related to diseases. Arboricultural Journal 8, 137–149. Innes, J.L. (1993). Forest Health Its Assessment and Status. (CAB International: Wallingford, Oxford.) Jones, A.D., Davies, H.I. and Sinden, J.A. (1990). Relationships between eucalypt dieback, land, and land use in southern New England, New South Wales. Australian Forestry 53, 13–23. Karani, P.K. (1975). Fertiliser trials and dieback of Eucalyptus grandis in Uganda. Technical Note, 207/ 1975. (Uganda Forest Department: Kampala, Uganda.) Kile, G.A. (1974). Insect defoliation in the regrowth forests of Tasmania. Australian Forest Research 6, 9–18.

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Kile, G.A. (1980). Behaviour of an Armillaria in some Eucalyptus obliqua–Eucalyptus regnans forests in Tasmania and its role in their decline. European Journal of Forest Pathology 10, 248–296. Kile, G.A. (1981a). Armillaria luteobubalina. A primary cause of tree decline and death in mixed species eucalypt forests in central Victoria. Australian Forest Research 11, 63–77. Kile, G.A. (1981b). An overview of eucalypt dieback in rural Australia. In Eucalypt Dieback in Forests and Woodlands. (Eds K.M. Old, G.A. Kile and C.P. Ohmart) pp. 13–26. (CSIRO: Melbourne.) Kile, G.A. and Watling, R. (1983). Armillaria species from south eastern Australia. Transactions of the British Mycological Society 81, 129–140. Landsberg, J. (1985). Drought and dieback of rural eucalypts. Australian Journal of Ecology 10, 87–90. Landsberg, J. (1988). Dieback of rural eucalypts: tree phenology and damage caused by leaf-feeding insects. Australian Journal of Ecology 13, 251–267. Landsberg, J. (1990a). Dieback of rural eucalypts: does insect herbivory relate to dietary quality of tree foliage? Australian Journal of Ecology 15, 73–87. Landsberg, J. (1990b). Dieback of rural eucalypts: response of foliar dietary quality of herbivory to defoliation. Australian Journal of Ecology 15, 89–96. Landsberg, J. (1990c). Dieback of rural eucalypts: the effect of stress on the nutritional quality of foliage. Australian Journal of Ecology 15, 97–107. Landsberg, J. and Wylie, F.R. (1983). Water stress, leaf nutrients and defoliation: a model of dieback of rural eucalypts. Australian Journal of Ecology 8, 27–41. Landsberg, J. and Wylie, F.R. (1988). Dieback of rural trees in Australia. GeoJournal 17, 231–237. Landsberg, J., Morse, J. and Khanna, P. (1990). Tree dieback and insect dynamics in remnants of native woodlands on farms. Proceedings of the Ecological Society of Australia 16, 149–165. Lowman, M.D. and Heatwole, H.H. (1992). Spatial and temporal variability in defoliation of Australian eucalypts. Ecology 73, 129–142. Loyn, R.H., Runnals, R.G., Forward, G.Y.and Tyers, J. (1983). Territorial bell miners and other birds affecting the populations of insect prey. Science 221, 1411–1412. Macfarlane, R., Jackson, G.V.H. and Marten, K.D. (1976). Die-back of Eucalyptus in the Solomon Islands. Commonwealth Forestry Review 55, 133–139. Mackay, S.M., Humphreys, F.R., Clark, R.V., Nicholson, D.W. and Lind, P.R. (1984). Native Tree Dieback and Mortality on the New England Tablelands of New South Wales. Research Paper No.3, Forestry Commission of N.S.W. Manion, P.D. (1981). Tree Disease Concepts. (Prentice Hall: Engelwood Cliffs, NJ, USA.)

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Marks, G.C. and Idczak, R.M. (1973). Eucalypt Dieback in Australia. Proceedings of the Lakes Entrance Seminar, 1973. (Forests Commission Victoria: Melbourne.) Masuka, A. ( 1990). A new canker of Eucalyptus grandis Hill ex Maiden in Zimbabwe. Commonwealth Forestry Review 69, 195–200. McCain, A.H. Costello, L.R. and Correll, J.C. (1989). Sudden death of eucalypts. California Plant Pathology 84, 4–5. Morgan, F.D. and Taylor, G.S. (1988). The white lace lerp in southeastern Australia. In Dynamics of Forest Insect Populations. (Ed. A.A. Berryman) pp. 129–140. (Plenum Press: New York.) Mueller-Dombois, D. (1983a). Stand-level dieback in New Zealand forests and the theory of cohort senescence. Hawaiian Botanical Society Newsletter 22, 33–42. Mueller-Dombois, D. (1983b). Canopy dieback and successional processes in Pacific forests. Pacific Science 37, 317–325. Newhook, F.J. and Podger, F.D. (1972). The role of Phytophthora cinnamomi in Australian and New Zealand forests. Annual Review of Phytopathology 10, 299–326. Neyland, M. (1996). Tree Decline in Tasmania. (Land and Water Management Council: Hobart, Tas.) Norton, A.M.L.A. (1886). On the decadence of Australian forests. Proceedings of the Royal Society of Queensland 3, 15–22. Ohmart, C.P. and Edwards, P.B. (1991). Insect herbivory on Eucalyptus. Annual Review of Entomology 36, 637–657. Old, K.M., Kile, G.A. and Ohmart, C.P. (Eds) (1981). Eucalypt Dieback in Forests and Woodlands. (CSIRO: Melbourne.) Old, K.M., Gibbs, R., Craig, I., Myers, B.J. and Yuan Z.-Q. (1991). Effect of drought and defoliation on the susceptibility of eucalypts to cankers caused by Endothia gyrosa and Botryosphaeria ribis. Australian Journal of Botany 38, 571–581. Orozco Jaramillo, C. and Copete Perdomo, A. (undated). Possible causes of dieback of Eucalyptus globulus in Narino, Colombia. Research Report. (National Institute of Natural Renewable Resources: Bogota, Colombia.) Palzer, C. (1981). Aetiology of gully dieback. In Eucalypt Dieback in Forests and Woodlands. (Eds K.M. Old, G.A. Kile and C.P. Ohmart) pp. 174–178. (CSIRO: Melbourne.) Palzer, C. (1983). Crown symptoms of regrowth dieback. Pacific Science 37, 465–470. Podger, F.D. (1981a). Definition and diagnosis of diebacks. In Eucalypt Dieback in Forests and Woodlands. (Eds K.M. Old, G.A. Kile and C.P. Ohmart) pp.1–8. (CSIRO: Melbourne.) Podger, F.D. (1981b). Some difficulties in the diagnosis of drought as the cause of dieback. In Eucalypt Dieback

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in Forests and Woodlands. (Eds K.M. Old, G.A. Kile and C.P. Ohmart) pp.167–173. (CSIRO: Melbourne.) Podger, F.D., Kile, G.A., Bird, T., Turnbull, C.R.A. and McLeod, D.E. (1980). An unexplained decline in some forests of Eucalyptus obliqua and E. regnans in southern Tasmania. Australian Forest Research 10, 53–70. Pook, E.W. (1981). Drought and dieback of eucalypts in dry sclerophyll forests and woodlands of the southern tablelands New South Wales. In Eucalypt Dieback in Forests and Woodlands. (Eds K.M. Old, G.A. Kile and C.P. Ohmart) pp. 179–189. (CSIRO: Melbourne.) Pook, E.W. and Forrester, R.I. (1984). Factors influencing dieback of drought–affected dry sclerophyll forest tree species. Australian Forest Research 14, 201–217. Richards B.N. (1981). A theoretical framework for a research program on New England Dieback. In Eucalypt Dieback in Forests and Woodlands. (Eds K.M. Old, G.A. Kile and C.P. Ohmart) pp. 261–272. (CSIRO: Melbourne.) Roberts, R.J. and Sawtell, N.L. (1981). Survival and growth of local and other eucalypts planted on the northern tablelands. In Eucalypt Dieback in Forests and Woodlands. (Eds K.M. Old, G.A. Kile and C.P. Ohmart) pp. 87–94. (CSIRO: Melbourne.) Roberts, R.J., Campbell, A.J., Porter, M.R. and Sawtell, N.L. (1982). The distribution and abundance of pasture scarabs in relation to Eucalyptus trees. In Proceedings of 3rd Australasian Conference on Grassland Invertebrate Ecology, pp. 207–214. (SA Government Printer: Adelaide.) Schoeneweiss, D.F. (1975). Predisposition, stress and plant disease. Annual Review of Phytopathology 13, 193–211. Scriven, G.T. and Luck, R.F. (1986). Beetle from Australia threatens eucalyptus. California Agriculture 40, 4–6. Stone, C. (1996). The role of psyllids (Hemiptera: Psyllidae) and bell miners (Manorina melanophrys) in

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canopy dieback of Sydney blue gum (Eucalyptus saligna Sm.). Australian Journal of Ecology 21, 450–458. Stone, C. (2000). Assessment and monitoring of decline and dieback of forest eucalypts in relation to ecologically sustainable forest management; a review with a case study. Australian Forestry (in press). Stone, C. and Bacon, P.E. (1994). Relationships among moisture stress, insect herbivory, folioar cineole and the growth of river red gum Eucalyptus camaldulensis. Journal of Applied Ecology 31, 604–612. Walker, J., Thompson, C.H. and Jehne, W. (1983). Soil weathering stage, vegetation succession and canopy dieback. Pacific Science 37, 471–481. Ward, B.K. and Neumann, F.G. (1982). Eucalypt dieback in foothill forests of the Dandenong Ranges. Forestry Technical Papers, No. 29, 10–14. (Forests Commission, Victoria: Melbourne.) Wardlaw, T.J. (1989). Management of Tasmanian forests affected by regrowth dieback. New Zealand Journal of Forestry Science 19, 265–276. Wargo, P.M. and Harrington T.C. (1991). Host stress and susceptibility. In Armillaria Root Disease. Agricultural Handbook No. 691. (Eds G.C. Shaw and G.A. Kile) pp. 88–101. (USDA Forest Service: Washington, DC.) West, P.W. (1979). Date of onset of regrowth dieback and its relation to summer drought in eucalypt forest of southern Tasmania. Annals of Applied Biology 93, 337–350. West, P.W. and Podger, F.D. (1980). Loss in timber volume and value due to regrowth dieback of eucalypts in southern timber. Australian Forestry 43, 20–28. White, T.C.R. (1986). Weather, eucalyptus dieback in New England, and a general hypothesis of the cause of dieback. Pacific Science 40, 1–4.

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4.1

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4.1 Stressful site: Eucalyptus pauciflora subalpine woodland in the thaw, Mt Hotham, Vic. 4.2 Hazardous site: Corymbia porrecta regeneration from rhizostolons after fire, NT. 4.3 Hazardous site: Eucalyptus tetrodonta—root sucker developing on an older plant in a sand dune, Groote Eylandt, NT.

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4.4 Hazardous site: Eucalyptus alba—‘autumnal’ colour before the deciduous phase in the dry season, Katherine, NT. 4.5 Floodplain: Eucalyptus camaldulensis forest along the Murray River at full flow after catchment snow thaw, Tocumwal, NSW.

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4.6 Floodplain: dense regeneration of Eucalyptus camaldulensis from seed shed on water and blown to the lee shore, Lake Bambruk, N.W. Vic. 4.7 Dry sclerophyll forest, Eucalyptus marginata, Darling Scarp, near Perth, WA. 4.8 Dry sclerophyll forest, Eucalyptus obliqua– E. macrorhyncha, Brisbane Ranges, Vic.

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4.9 Mature Eucalyptus regnans, 250-year-old wet sclerophyll forest with younger even-aged understorey, Wallaby Creek, north north-east of Melbourne, Vic. 4.10 Old Eucalyptus regnans with mature Nothofagus cunninghamii (Hook.) Oerst. late stage succession, Cement Creek, Warburton, Vic. 4.11 Grassy woodland, Eucalyptus viminalis– E. pauciflora–E. ovata, Brisbane Ranges, Vic. 4.12 Even-aged Eucalyptus delegatensis with post-fire coppice Nothofagus cunninghamii, Mt Donna Buang, Vic.

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4.13 Mature Eucalyptus diversicolor and E. jacksonii wet sclerophyll forest with mature understorey, Walpole, WA.

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9.1 Larger spots caused by Aulographina eucalypti on Eucalyptus obliqua, showing purple margins around spots in winter. Photograph E.J. Minchinton. 9.2 A lesion caused by Aulographina eucalypti, showing elongate thyriothecia and pimplelike pycnidia. Photograph E.J. Minchinton. 4.13

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9.3 Heavy infection of Aulographina eucalypti on Eucalyptus obliqua.

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9.4 Early stage of development of crinkle leaf caused by Mycosphaerella cryptica on Eucalyptus obliqua, showing discolouration of mesophyll tissue. 9.5 Crinkle leaf caused by Mycosphaerella cryptica on Eucalyptus obliqua. The darker colour on the lesions is caused by development of pseudothecia.

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9.6 Crinkle leaf caused by Mycosphaerella cryptica on a mature leaf of Eucalyptus globulus. 9.7 Crinkle leaf caused by Mycosphaerella cryptica on tip leaves of a seedling of Eucalyptus obliqua.

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9.8 Pseudothecia of Mycosphaerella cryptica formed in a leaf spot (about 10 mm in diameter) on a juvenile leaf of Eucalyptus globulus. 9.9 Leaf spots on Eucalyptus delegatensis caused by Mycosphaerella delegatensis. 9.10 Marginal necrosis caused by Mycosphaerella marksii on leaves of Eucalyptus camaldulensis in Vietnam. 9.11 Leaf blotch caused by Mycosphaerella nubilosa on juvenile leaf of Eucalyptus globulus.

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9.12 Infections of leaf of Eucalyptus goniocalyx by Pachysacca samuelii. Photograph M.J. Duncan. 9.13 Infection of leaf of Eucalyptus delegatensis by Phaeothyriolum microthyrioides. Photograph G. Kalc-Wright.

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9.14 First symptoms of Puccinia psidii on young shoots of Eucalyptus. Photograph F.A. Ferreira. 9.15 Infection by Puccinia psidii on young shoot of Eucalyptus. Photograph F.A. Ferreira. 9.16 Uredinia of Puccinia psidii on leaves of Eucalyptus. Photograph F.A. Ferreira. 9.17 Distortion of shoot of Eucalyptus, caused by Puccinia psidii. Photograph F.A. Ferreira.

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9.18 Damage to shoots of seedling of Eucalyptus caused by Puccinia psidii. Photograph F.A. Ferreira. 9.19 Small purple-red leaf spots caused by Phaeophleospora epicoccoides on Eucalyptus camaldulensis in Vietnam.

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9.20 Pseudocercospora eucalyptorum on leaves of Eucalyptus camaldulensis in Vietnam. 9.21 Lesion caused by Aurantiosacculus eucalypti on Eucalyptus baxteri, showing distinctive orange pycnidia. Photograph D.A. Marshall.

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9.22 Leaf speckle on Eucalyptus globoidea caused by Sonderhenia eucalyptorum. 9.23 Pycnidia of Sonderhenia eucalypticola formed in green leaf tissue of Eucalyptus globulus. Photograph P.A. Barber. 9.24 Necrotic spot on mature leaf of Eucalyptus globulus with pycnidia of Sonderhenia eucalypticola. Photograph P.A. Barber.

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9.25 Coniella sp. causing a circular blight on a leaf of Eucalyptus camaldulensis in Vietnam. Note pycnidia formed in concentric circles. 9.26 Lesions caused by Cryptosporiopsis eucalypti on leaves of Eucalyptus camaldulensis in Vietnam. 9.27 Leaves of Eucalyptus grandis X E. urophylla hybrid at Meunga, N. Qld, showing early stages of infection by Cylindrocladium quinqueseptatum. Note purple margins around lesions. Photograph K.M. Old.

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9.28 Leaves of Eucalyptus grandis X E. urophylla hybrid at Meunga, N. Qld, showing leaf spots caused by Cylindrocladium quinqueseptatum. Photograph K.M. Old. 9.29 Propolis emarginata on lesion on mature leaf of Eucalyptus globulus. Photograph P.A. Barber. 10.1 Annual canker on a stem of Eucalyptus mannifera, with bark cracking and kino secretion. The diseased bark (from which Endothia gyrosa was isolated) will be sloughed. 10.2 Section of canker shown in Plate 10.1 showing bark splits but no invasion of the sapwood.

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10.3 Diffuse perennial canker on Eucalyptus blakelyi caused by Endothia gyrosa. The tree had been repeatedly defoliated and showed advanced crown dieback.

10.3

10.4 Section of canker shown in Plate 10.3 showing invasion of the sapwood (arrows). 10.5 Many perennial cankers on Eucalyptus rossii. Endothia gyrosa can be readily isolated from the canker margins but its role in the etiology of this condition is unclear. 10.6 Section through one of the cankers shown in Plate 10.5. Discolouration and some decay of the sapwood and heartwood has occurred. 10.4

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10.7 Eucalyptus grandis, growing in a plantation, showing early symptoms of infection by Cryphonectria cubensis. Note the discolouration of the inner bark. 10.8 Eucalyptus grandis, growing in a plantation, showing advanced stem canker caused by Cryphonectria cubensis. Note the severe bark splitting and stem deformation. 10.9 Eucalyptus camaldulensis seedling, inoculated with Cryphonectria parasitica, showing canker symptoms. 10.10 Eucalyptus sp. with stem canker in Japan and found to be infected by Cryphonectria parasitica.

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10.11 Dead main stem of a young Eucalyptus nitens extensively colonised by Cytospora eucalypticola. The tree has branched vigorously but form has been affected.

10.11

10.12 Endothiella anamorph of Endothia gyrosa showing pycnidia. 10.13 Teleomorph of Endothia gyrosa. Surface view showing perithecial necks embedded in orange stromata. Stromata are 0.5 to 1.5 millimetres in diameter. 10.14 Teleomorph of Endothia gyrosa showing longitudinal section of a perithecium. Vertical axis of the perithecium is about 300 micrometres long.

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11.1 Effect of Phytophthora cinnamomi in eucalypt forests. Recent and old deaths of Eucalyptus marginata in a disease centre near Dwellingup, WA. The view is from the disease centre towards healthy forest. Most susceptible hosts have been killed in the disease centre. 11.2 Effect of Phytophthora cinnamomi in eucalypt forests. Patch death of Eucalyptus consideniana in the Mullundung State Forest, South Gippsland, Vic. 12.1 Mycelial sheets and fans of Armillaria luteobubalina in the bark of Eucalyptus globulus ssp. bicostata.

12.1

12.2 Mycelial sheets and developing rhizomorphs of Armillaria novae-zelandiae or A. hinnulea beneath loosened bark on the stem of Eucalyptus regnans.

12.2

12.3 Large basal canker formed in response to Armillaria luteobubalina infection in Eucalyptus cypellocarpa. 12.4 Basidiocarps of Armillaria luteobubalina at the base of a Eucalyptus globulus ssp. bicostata. 12.3

12.5 A focus of disease caused by Armillaria luteobubalina in mixed species eucalypt forest. 12.6 Sudden death of a Eucalyptus cypellocarpa sapling caused by Armillaria luteobubalina infection. 12.5

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12.7 Crown dieback (central trees) in Eucalyptus obliqua caused by Armillaria luteobubalina. 12.8 A cluster of dead and infected saplings of Eucalyptus obliqua around a stump from the previous crop infected by Armillaria luteobubalina. Trees were infected as a result of root contact with the inoculum. 12.9 Distribution of seven genotypes of Armillaria luteobubalina in 32 hectares of mixed species eucalypt forest. 12.10 Crown decline typical of that observed in trees of Eucalyptus obliqua/E. regnans affected by regrowth dieback and Armillaria infection (A. novaezelandiae/A. hinnulea).

12.9

12.11 Lesion on a root of Eucalyptus regnans caused by Armillaria novae-zelandiae or A. hinnulea.

12.10

12.12 Scattered-clustered mortality in a plantation of Eucalyptus delegatensis caused by Armillaria luteobubalina. 12.13 Basidiocarps of Pseudophaeolus baudonii on a eucalypt coppice stump. 12.14 Ectotrophic mycelium of Pseudophaeolus baudonii spreading over the stem base of a eucalypt.

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13.1 Piptoporus portentosus basidiocarp on burned stringybark eucalypt. Photograph B.A. Fuhrer. 13.2 Phellinus wahlbergii basidiocarp on ironbark eucalypt. Photograph B.A. Fuhrer. 13.3 Postia pelliculosa basidiocarps. Photograph B.A. Fuhrer.

13.5

13.4 Piptoporus australiensis basidiocarp. Photograph B.A. Fuhrer.

13.6

13.5 Phellinus robustus basidiocarp on Eucalyptus dumosa. Photograph S. Morton. 13.6 Brown rot. Photograph S. Morton. 13.7 White rot. Photograph S. Morton. 13.8 White pocket rot of heartwood of a Eucalyptus paniculata pole. 13.7

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13.9 Fistulina spiculifera basidiocarp. Photograph B.A. Fuhrer. 13.10 ‘Brown wood’ of Eucalyptus diversicolor. Note the pink colour of the unaffected and discoloured heartwood. The latter is referred to as ‘brown wood’. Photograph E.M. Davison.

14.3

13.11 Canker rot of Eucalyptus globulus associated with Phellinus robustus. Photograph T.J. Wardlaw. 14.1 Foliar symptoms of virus-like diseases in juvenile leaves of Eucalyptus cloeziana. Healthy leaves (upper) and leaves with vein clearing (lower). Photograph P.L. Guy.

14.2

14.2 Foliar symptoms of virus-like diseases in juvenile leaves of Corymbia gummifera with patchy interveinal chlorosis. Material from the Jari Valley in equatorial Brazil. Photograph P.L. Guy.

14.4

14.5

14.3 Foliage of Eucalyptus grandis with microphylly symptom of little leaf disease. Vottavada, Kerala, India. 14.4 Shoot of Eucalyptus camaldulensis near Mundulla, SA, showing interveinal chlorosis of leaves typical of Mundulla yellows. Photograph I.W. Smith. 14.5 Symptoms of Mundulla yellows on Eucalyptus camaldulensis near Penola, SA. Photograph P. Keane.

14.6

14.8

14.7

14.9

14.6 Bacterial slime on a cross section of the stem of six-monthold Eucalyptus urophylla with wilt symptoms caused by Ralstonia solanacearum. 14.7 Eucalyptus urophylla showing mild symptoms caused by Ralstonia solanacearum—wilting and death of leaves on a lateral branch. 14.8 Discolouration and death of the tap root of a three-month-old Eucalyptus sp. seedling caused by Ralstonia solanacearum.

14.10

15.1

14.9 Stem discolouration caused by the infection of six-month-old Eucalyptus urophylla by Ralstonia solanacearum. 14.10 Stem discolouration in twoyear-old Eucalyptus urophylla caused by infection with Ralstonia solanacearum and subsequent secondary fungal infection. 15.1 Remnant clumps of drooping mistletoe (Amyema pendula) on recently killed Eucalyptus viminalis, Hindmarsh Valley, SA.

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15.2

15.2 A roadside Blakely’s red gum (Eucalyptus blakelyi) heavily infected by box mistletoe (Amyema miquelii) near Invergowrie, NSW, pictured two years prior to death. 15.3 The immature fruits of box mistletoe (Amyema miquelii).

15.4

15.4 Large brownish clumps of box mistletoe (Amyema miquelii) in the canopy of Eucalyptus blakelyi near Armidale, NSW.

16.1

16.1 Nitrogen is a key element for leaf production. Eucalyptus globulus grown with all nutrients (right) or all nutrients except nitrogen (left). 16.2 Expression of symptoms due to nitrogen deficiency can depend on light intensity. Nitrogen deficient Eucalyptus grandis grown in a glasshouse (left) and a shadehouse (right).

16.2

16.3 Sulphur deficiency in Eucalyptus obliqua. Note general chlorosis and death of leaf tips. 16.4 Phosphorus deficiency in Eucalyptus baxteri. Note purple discolouration and the presence of necrotic spots. 16.3

16.5 Potassium deficiency in Eucalyptus grandis. Note tip and marginal necrosis of older leaves.

16.4

16.6 Potassium deficiency in Eucalyptus pilularis. Note stimulation of branching and distortion of young leaves. 16.7 Magnesium deficiency in Eucalyptus globulus. Note recurved tips of leaves and necrosis beginning from the leaf margins.

16.5

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16.6

16.8

16.9

16.10

16.11

16.9

16.8 Calcium deficiency in Eucalyptus globulus. Note leaf rolling and death of axillary shoots. 16.9 Manganese deficiency in Eucalyptus pilularis. Note chlorosis of young leaves. 16.10 Manganese deficiency in Eucalyptus globulus. Note development of interveinal patches of purple anthocyanin colouration.

16.12

16.11 Manganese deficiency in Eucalyptus nitens. Photograph J.L. Honeysett. 16.12 Mild iron deficiency in Eucalyptus pilularis. Note interveinal chlorosis. 16.13 Combined deficiency of iron, manganese and zinc in Eucalyptus pilularis. Note strong development of chlorosis. 16.13

16.14

16.14 Zinc deficiency in Eucalyptus pilularis. Note development of small leaves and interveinal patches of purple anthocyanin colouration. 16.15 Boron deficiency in Eucalyptus grandis. Note distorted leaves, stems and shoots; proliferation of axillary shoots; shoot and leaf necrosis.

16.15

16.17

16.16

16.18

16.19

16.16 Death of Eucalyptus occidentalis near Katanning, WA, caused by a rising saline watertable. Photograph M. McDonald. 16.17 Effects of salinity on Eucalyptus brassiana in Thailand. Note damaged foliage. Photograph N. Marcar. 16.18 Salt damage on seedlings in a glasshouse.

16.20

16.21

16.19 Effects of paclobutrazol. 16.20 Drought affected Eucalyptus globulus seedlings. 16.21 Death of Eucalyptus grandis due to drought in Swaziland. Photograph B.V. Gunn. 16.22 Frost damage results in death of leaves on the outer, exposed part of the crown.

16.22

16.23

16.23 Leaf rolling and intumescences of Eucalyptus grandis leaves caused by high humidity. Photograph J. Oros. 16.24 Genetic chimera in Eucalyptus nitens. 16.25 Terminal shoot of a eucalypt with leaves infested by ericoid mites.

16.24

16.25

17.1

17.2

17.3

17.1 Eucalyptus regnans in Tasmania showing advanced dieback and epicormic shoots. Photograph G.A. Kile. 17.2 Eucalyptus blakelyi affected by crown dieback in the Australian Capital Territory. 17.3 Eucalypts in the Australian Capital Territory showing various stages of rural dieback. Many trees have cankers with Endothia gyrosa.

17.4 19.1

19.1 Aerial photograph (scale 1 to 4500) above Bandicoot Road, Walpole District, 19 March 1994. Lighter area in centre is severe dieback of Eucalyptus marginata due to Phytophthora cinnamoni. Healthy E. marginata forest at upper left and centre right; healthy E. diversicolor forest lower left and top right. Photograph DOLA, Perth, WA. 19.2 One-year-old leaves from adjacent branchlets of a tree of Eucalyptus marginata, showing healthy leaf (left), leaf with interveinal chlorosis diagnostic of Mundulla yellows (centre), and senescent leaf (right). Photograph F.D. Podger, D. Sarson.

19.2

19.3

17.4 Eucalypt stands affected by Mal do Rio Dôcé in the Rio Dôcé valley of Minais Gerais State, Brazil. Photograph J.C. Dianese.

19.4

19.3 Symptoms of Mundulla yellows in avenue of Euclayptus camaldulensis near Mundulla, SA, showing canopy dieback. Photograph R. Beever. 19.4 Symptoms of Mundulla yellows on Euclayptus todtiana, Perth, WA. Parts of the crown are dead (top right), yellowed (top) and healthy (bottom left). Photograph D. Sarson.

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J.A. Simpson and F.D. Podger

S

U M M A R Y

The options available for integrated management of the diverse diseases in eucalypt forests, woodlands and plantations, and constraints upon their use are summarised. The importance of knowledge of the basic biology of pathogens and its incorporation into general management strategies is emphasised. Choice among options varies according to whether the trees are growing in native forests and woodlands, in short or long rotation plantations, in amenity and social plantings, or in remnant vegetation in agricultural landscapes. Effective management of disease in native forests requires a clear understanding of the various functions of the vegetation, particularly its value for conservation, whereas management options are less constrained in plantations grown solely for timber or fibre production. In native forests, disease management is based on modifications to forest management practices used in healthy forest. Manipulation of fire and silvicultural treatments for example, may be required to reduce the vulnerability of the forest to disease. Control of tree decline and mortality in remnant eucalypts on grazing and farm land involves restoration of areas of forest or woodland communities or the planting of eucalypt genotypes better adapted to the changed environmental conditions. Planting of disease resistant genotypes of eucalypts produced by selection and breeding is important in management of disease in plantations and in regeneration of areas of native forest badly damaged by particular diseases. The economic returns from short-rotation plantations may be sufficient to justify the use of fungicides in integrated disease management programs, while the high value of nursery stock allows for the application of highly intensive management options, including fungicides. Properly conducted forest health surveys are important for determining the occurrence, effect and cause of disease in native forests and plantations. Because of the restricted distribution of many eucalypt diseases, quarantine measures are important in preventing the spread of these diseases between countries and between infested and uninfested forests within a country. For example, quarantine restrictions are important in preventing the spread of eucalypt rust, Puccinia psidii, from South America to Australia and elsewhere, while local quarantine measures have been important in reducing the spread of Phytophthora cinnamomi from diseased to healthy forests in Western Australia. A variety of social, economic and political constraints determine choice among strategies that theoretically might be available.

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18.1 Introduction Much of this book comprises an account of the causes and biology of the major diseases of eucalypts. However, the main concern of eucalypt pathology is the amelioration of diseases as they affect the survival and productivity of the trees in the various communities in which they grow. Fundamentally, this is an exercise in applied ecology as developed over recent decades under the heading of ‘Integrated Pest Management’. Ultimately, knowledge of the biology of particular diseases needs to be incorporated into realistic management strategies that enable us to maintain the health of the trees and their associated communities. In this and subsequent chapters, the development of integrated management strategies and their potential for success is discussed, and disease management strategies in native forests and woodlands, eucalypt nurseries and commercial plantations are reviewed. There are two basic objectives in disease management: 1

to predict and measure the effect of the range of diseases present in a plant community (Teng 1987)

2

to contain damage from these diseases within acceptable limits in a way that is cost-effective and consistent with other management objectives (Lester 1986).

A sound knowledge of the growth and development of healthy trees and their responses to changed environmental conditions is required for diagnosis, prediction of disease and determination of disease effects (Walker 1992). This applies particularly to eucalypts, many species of which have irregular growth habits, and to trees in complex plant communities such as forests. A familiarity with the book by Jacobs (1955) on eucalypt growth habits is a good beginning. For example, ignorance of the propensity of some eucalypt species to form lignotubers has led some observers to confuse these natural structures with crown gall (see Chapter 14). Regenerating forests of shade-intolerant eucalypts often undergo a process of self-thinning throughout the life of the forest, resulting in debility and death of trees which are part of the forest’s normal ecological processes. Some dieback conditions of eucalypts are expressed as the symptoms of natural senescence of trees undergoing normal successional processes in the transition from tall eucalypt forest to temperate 428

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rainforest (see Chapter 17). Severe infection by fungi such as Aulographina eucalypti (Cooke & Massee) Arx & E.Müll. on older, senescing leaves (up to 3 years old) retained in the lower canopy is common in eucalypts and probably has little effect on growth (see Chapter 9). In many forests there are distinctive difficulties for disease management resulting from: 1

very long rotations (often many decades)

2

changing forest environment and tree architecture as the stand ages and progresses through the natural ageing sequence from seedling to sapling, pole, mature tree and overmature tree

3

uncertainties of projected market returns for forest products that may not be harvested for many years

4

effect of compound interest over the long rotations on the real cost of disease control measures

5

relatively small monetary returns per hectare per annum through much of the rotation

6

unpredictable effects of pests and diseases

7

the possibility, during the life of the forest, of dramatic damage by abiotic agents such as wildfire, drought, storm, frost or flood, any of which could reduce yield directly or predispose the forest to disease.

A major impediment to the implementation of particular control measures in forests results from the difficulty of determining whether a measure that is effective in experimental studies of the first few years of forest growth will retain its efficacy throughout the long life and complex developmental stages of the forest. This applies, for instance, to the regeneration of susceptible eucalypt species on sites infested by Phytophthora (Ph.) cinnamomi Rands in Victoria (see Chapter 19). Because of these complexities, disease management in forests is necessarily multidisciplinary and involves the integration of inputs from many specialists, including forest pathologists, ecologists, silviculturalists, nursery managers, tree breeders and economists. The management options for disease in eucalypts depend greatly on the diverse situations in which trees grow, including native forests and woodlands covering vast areas and a wide range of climatic and

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edaphic circumstances, remnants of woodlands and forests on land largely cleared for farming and grazing in Australia, and large commercial plantations and small amenity and social forestry plantings in many parts of the world (see Chapter 1). In south-east and south-west Australia the effect of disease caused by Ph. cinnamomi in both the eucalypt overstory and non-eucalypt understorey components of native plant communities has threatened large areas of these communities. It has required a management response in both multipurpose production forests and national parks and reserves (see Chapters 11 and 19). This epidemic has highlighted the need for disease management strategies in native forests, woodlands and heathlands in which, previously, little heed was paid to the health of the vegetation. The disease management options and constraints in native vegetation (see Chapter 19) are vastly different from those in eucalypt nurseries (see Chapter 21) or in small plantings and extensive commercial plantations (see Chapter 22). Except in nurseries, small amenity and social plantings and short-term plantations, management of disease in eucalypts is essentially an exercise in silviculture and applied ecology rather than an application of particular disease control methods (e.g. spraying fungicides). The objectives of quantifying disease effects and economically containing damage both pose serious problems for management of native eucalypt forests. Long-lived forests usually show evidence of great stress imposed by components of the abiotic and biotic environment, including a range of pests and diseases. Except in the case of obvious premature mortality (as caused by Ph. cinnamomi in the Eucalyptus marginata forests in Western Australia), it is difficult to quantify the effect of a particular disease. Even then it is difficult to reduce the impact within the constraints imposed by the low and often unpredictable economic returns from the forest. In native forests and woodlands, options are limited to manipulation of the usual range of silvicultural practices (e.g. burning, harvesting, regeneration practices) in a way that reduces the vulnerability of the communities to disease. If the productivity and ecological sustainability of multipurpose eucalypt forests is to be optimised, management of disease needs to be an integral part of the management of the forests throughout the harvesting cycle. In slowgrowing native eucalypt forests (i.e. all but the most

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productive tall forests), disease management is rarely a primary consideration (McKinnell et al. 1991). Control of dieback in remnant eucalypts on grazing and farm land (see Chapter 17) will require restoration of areas of natural woodland or the planting of eucalypts selected for their adaptation to the changed environmental conditions (see Chapter 19). In response to a growing appreciation of the value of eucalypt vegetation in providing shelter for crops and livestock and in reducing the problem of dryland salinity which extends over large areas of farmland in south-east and south-west Australia, some farmers are replanting and restoring areas of native woodland and forest on their properties, often using seed from surviving local eucalypts (W. Twigg, pers. comm.). Eucalypt plantations (e.g. E. globulus in south-east and south-west Australia) are being established increasingly on farms under contract arrangements with forestry companies and pulp mills. These plantations provide additional income to the farmers but are also likely to have environmental benefits in a landscape that has been cleared excessively of trees over the last 200 years. Disease management options in eucalypt plantations vary in several important ways from those in native forests. Plantations often grow at a faster rate than native forests and involve a much greater expenditure in establishment and maintenance. Thus, management will often have a greater commitment to disease control in plantations. Selection pressure for development of disease resistance in the plant community is less in plantations than in natural forests (Heather and Griffin 1978). Plantations usually consist of a single species and so have a less diverse genetic base than mixed-species native forests, possibly increasing their vulnerability to disease (Heather and Griffin 1978; Chau 1981). This applies particularly to clonal plantations and less so to seedlings established from open-pollinated seed orchards. However, if the plantation has been established from stock selected for resistance to the prevalent pathogens, it may have a reduced risk of disease. Short rotations reduce the risk of catastrophic disease losses, as does the existence of markets for diverse sizes of log (e.g. pulp, poles, sawlogs). Plantation management practices that contribute to a high level of tree vigour often result in reduced losses from disease. Such practices include careful site selection, matching of genotypes to site, fertilising, weed suppression, 429

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control of herbivores, thinning and removal of unthrifty or malformed trees. Maintaining a healthy forest is predicated on sound forest management, regular monitoring of forest health, prompt remedial action against economically important pathogens, priority for salvage of diseaseaffected timber and research on the biology, epidemiology and control of diseases. Management of forest diseases mainly involves disease avoidance, use of disease resistant stock and manipulation of silvicultural practices (Hepting and Cowling 1977). In the formulation of a disease management strategy, the following matters need to be considered: 1

recognition that a problem exists

2

extent and degree of damage caused by the disease

3

regional variation in the nature and importance of disease

4

identity of the causal agents (or processes)

5

origins of the agents (native or exotic)

6

biological characteristics of the causal agents

7

influence of environmental factors

8

how pathogens interact with the plants and communities they damage

9

stage of development of the epidemic on a broad scale

10 prognosis for the further development of disease 11 consideration of disease control technologies potentially available 12 selection of practicable disease management strategies and the tactics necessary for their implementation within the constraints imposed by the type of forest, the nature of its control and management, and the social framework.

18.2 Environmental concerns In recent years, concerns about the effects of forest management practices on conservation of biodiversity, water management and conservation, and ecological sustainability have assumed increasing importance and must be considered in disease management (Whitehead 1982; Howarth and

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Norgaard 1990; Zwolinski 1990; Probst and Crow 1991; Bishop 1993; Squire 1993). This applies particularly to native eucalypt forests which usually have multiple functions, including conservation of biodiversity and water management. In some countries, legislative action has been taken to ensure that the genetic diversity of forests is maintained. For example, in Germany there was a legal requirement that reforestation projects over large areas using clonal material must use a minimum of 100 to 500 clones per mixture depending upon the species being planted (Muhs 1986). Management actions to protect rare and threatened species and communities in many places need to be integrated with established management programs directed to broader scale protection of whole communities. Retention of habitat trees for cavity-inhabiting birds and mammals may result in retention of sources of inoculum of heart rot fungi (Shigo and Hillis 1973) and in reduced vigour and growth of stands (Mackowski 1984). Many birds and mammals utilise cavities in eucalypt trees for shelter or breeding (Tyndale-Biscoe and Calaby 1975; McIlroy 1978). As animals of different sizes preferentially use cavities of different depths and volumes and with entrance holes of different diameters (Saunders et al. 1982; Smith and Lindenmeyer 1988), it is necessary, if biodiversity of fauna is to be maintained, to have a succession of trees developing a succession of cavities. Hollows suitable for wildlife develop only in old trees, older than 200 years for E. pilularis (Mackowski 1984) and 120 years for E. regnans (Gibbons and Lindenmayer 1997). Perry et al. (1985) have noted the close association between fire injury, decay and termite attack. Mackowski (1984) observed that fungal decays alone did not provide hollows suitable for animals, although trees with decay were more prone to termite attack which in turn opens up hollows. Thus, any management option that decreases the incidence of fire injury, fungal decay, termite attack and hollow formation in trees is likely to be incompatible with management of the forest for conservation values and maintenance of biodiversity. In forests where these values are paramount, it may be necessary to actively encourage decay and termite attack by wounding and inoculation of trees. Such a practice is obviously incompatible with management of a forest primarily for fibre and wood production, which involves strategies to reduce the incidence of decay in the trees.

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18.3 Quarantine and eradication The first line of defence against disease is the exclusion of potentially damaging pathogens. This can be achieved by banning or controlling the movement into disease-free areas of plants, propagative material, pathogens or vectors from biogeographical areas in which the pathogens occur (Waterworth 1981). The boundaries between such areas may be between or within nations. For example, the damage done by Ph. cinnamomi in E. marginata forest in south-west Australia has been limited by imposition of strict quarantine measures to restrict the spread of the pathogen from diseased to healthy parts of the forest (see Chapter 19). Quarantine is particularly important for restriction of diseases of the eucalypts, given the origin of the trees in an isolated region and the great movement of eucalypt species around the world in relatively recent times. No eucalypt growing area is exempt from the threat of exotic pathogens. Many of the native pathogens known from Australia have not yet been spread widely to other countries and Australia and other regions are free from several important exotic pathogens, including the guava rust, Puccinia psidii G.Winter (in Central and South America), Mycosphaerella (M.) juvenis Crous & M.J.Wingf. (in South Africa), Ralstonia solanacearum (Smith 1896) Yabuuchi et al. [syn. Burkholderia solanacearum (Smith 1896) Yabuuchi et al. 1993 and Pseudomonas solanacearum (Smith 1896) Smith 1914] Biotype 1 (in Brazil) and Pseudophaeolus baudonii (Pat.) Ryvarden (in central and southern Africa and Madagascar). These pathogens are a serious threat to the biodiversity and productivity of the native eucalypt-dominated communities in Australia, although there has been little effort to evaluate their potential damage. Quarantine at a subspecies, biotype or pathovar level may be important (e.g. with Ralstonia solanacearum). Hosts other than species of Myrtaceae may be important (Walker 1987). Cryphonectria parasitica (Murrill) M.E.Barr is also a destructive pathogen of some species of eucalypt (Old and Kobayashi 1988) while species of Calonectria De Not. can have wide host ranges. Once a pathogen has been introduced and become established in an area with a large population of susceptible hosts, experience indicates that it is unlikely to be eradicated (Eldridge and Simpson 1987). Fungi are eight times more likely than insects

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to be introduced and to become established successfully on Pinus radiata D.Don in New Zealand (Carter 1989). Quarantine inspection and eradication procedures are far more difficult in forests than in agricultural crops. Forests tend to cover vast areas with often difficult access and forest trees tend to be large and difficult to examine closely. Numbers of trained staff are low on a per hectare basis and inspections of trees for health are usually infrequent. Consequently there is only a low likelihood of detection of a pathogen in the early stages of its establishment in a new region. In the effort to increase forest productivity and quality it is inevitable that there will be a substantial international trade in propagation material of eucalypts. Certification (Organization for Economic Cooperation and Development 1971) goes partway to ensuring this material is not contaminated but an effective quarantine system is still essential (Parliman and White 1985; Foster 1988). Seed or plantlets in tissue culture are less likely to carry pathogens than normal vegetative material. However, our present knowledge of seedborne pathogens of the eucalypts is inadequate for quarantine purposes (see Chapter 7). Likewise our knowledge of the effect of most eucalypt pathogens is not sufficient to permit a thorough disease risk analysis (Kahn 1979; Shrum and Schein 1983). In many cases our knowledge of the taxonomy of eucalypt pathogens is insufficient as a basis for quarantine decisions. For example, there is uncertainty as to whether the destructive Mycosphaerella foliar pathogens in South Africa are the same as those in Australia (see Chapter 9). The logical course is to determine the various pathways by which such organisms can be introduced into a country and then devise measures that aim to exclude all eucalypt pathogens by closing these pathways as far as possible, bearing in mind the legitimate requirements of trade. Although this should lessen considerably the introduction of unwanted organisms, such incursions can never be completely eliminated, particularly in continental countries where political boundaries seldom coincide with biological barriers. Even a remote, island country such as New Zealand is subject to regular, uncontrollable airborne incursions of pests and pathogens because of its geographical location downwind of Australia.

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If outbreaks of exotic pathogens are to be eradicated or if serious outbreaks of established pathogens are to be contained and managed effectively, it is essential to have detailed contingency plans. Furthermore, there must be high quality teams in key locations trained in disease diagnosis and control techniques. The eradicability of a newly introduced pathogen depends on the promptness of its detection (as indicated by the area of forest it has infected prior to detection), the degree of isolation of the first infected community and the rate and mode of spread of the pathogen (Carter 1989). However, a windborne pathogen such as Puccinia psidii is unlikely to be amenable to eradication unless it is detected very early or the infected stand is very isolated. Eradication and control measures may include clearfelling and burning of infected trees, or the use of chemical control measures that would not normally be economical in forest management. The expense of eradication and containment are justifiable only as long as there is a reasonable prospect of success and the potential effect of the disease is likely to be great.

E U C A L Y P T S

surveys can be incorporated into bioclimatic distribution models of hosts and pathogens (Booth et al. 1988, 1989), risk prediction models (Caulfield 1987; Hicks et al. 1987; Caulfield et al. 1991) and Geographic Information Systems (Daniel et al. 1983). Because of previous lack of attention to the health of native eucalypt forests, the long-term survey data required are rarely available for Australian forests and this has compounded the difficulty of diagnosis of diseases of complex etiology and the assessment of the effects of all diseases in these forests.

Regular forest health surveys are important for early detection of new diseases and for monitoring the incidence and severity of diseases of long standing. An understanding of the normal state of health of trees is essential for the early detection of disease outbreaks, which may allow eradication or the implementation of control measures to minimise losses. Assessment of the state of health of native eucalypt forests is particularly difficult because the trees are commonly attacked by a wide range of natural herbivores and parasites. For example, detection of the guava rust, Puccinia psidii, on native eucalypts in Australia, if it is ever introduced, will be difficult among the profusion of ‘rust-like’ symptoms (epidermal eruptions, blisters, small spots) caused by native insects and fungi. Periodic assessments of the incidence and severity of disease allow prediction of its long-term effects and the cost effectiveness of control measures.

The methods of surveying for diseases are diverse and will vary according to the resources and technologies available, the area, remoteness and isolation of the forests and the kind of disease (Bloomberg et al. 1980a, 1980b; Bousfield et al. 1985; Baddeley 1989; Carter 1989; Bulman et al. 1999). Qualitative estimates of disease are subject to wide variation among observers unless they have been carefully trained using well-documented standards (Innes 1988). As far as possible, quantitative measures should be used, although this may be impractical in large-scale surveys. Quantitative severity ratings depend on some knowledge of the epidemiology of the pathogen (Seem 1984) but are reliable and repeatable. Carter (1989) and Bulman et al. (1999) compared the costs and effectiveness of observation by forest staff, random point sampling, drive-through roadside surveys, aerial surveys and surveys of port environs. Cost per percentage point of probability of detection increased greatly from aerial to roadside to random survey. Maximum net monetary benefit was found to be achieved at a survey level detecting 95% of new introductions. This was achieved by using a combination of aerial, roadside and random survey methods. Effectiveness of aerial surveys can be maximised by timing surveys to coincide with peak periods of damage by the disease of interest, which must be based on a sound knowledge of the epidemiology of the disease and phenology of the hosts. For eucalypt diseases, much of this basic knowledge is only now being gathered.

Surveys of forests for disease should be an integral part of forest management and often disease surveys can be combined with insect and weed surveys to reduce costs. Survey data collected consistently over many years will provide a sound basis for diagnosis and management of diseases, especially diseases of complex etiology (see Chapter 17). Information from

Prior to plantation establishment in a new area it is desirable that the site be surveyed for potentially devastating pathogens (e.g. Ph. cinnamomi, species of Armillaria). If certain pathogens are present and widely distributed, appropriate resistant species, provenances or clones can be used or the site conditions ameliorated by, for example, mounding

18.4 Forest health surveillance

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and ripping to improve drainage for control of Ph. cinnamomi (see Chapter 19) or stump and root removal for control of Armillaria (see Chapter 12). Eucalyptus nitens is very susceptible to Ph. cinnamomi whereas the closely related E. globulus is not; if Ph. cinnamomi is widespread in the proposed planting area then E. globulus can be used, significantly reducing the likelihood of plantation failure. Outside Australia, serious diseases usually have become evident only after the establishment of plantations on a large scale, resulting in a period of evaluation and selection of resistant genotypes and replanting to replace susceptible with resistant genotypes. In Australia, eucalypts are ubiquitous and so there are always likely to be sources of inoculum of many pathogens, especially airborne pathogens, close to newly established plantations.

18.5 Approaches to disease management 18.5.1 Silviculture Appropriate silviculture is essential for the good health of trees in both native forests and more intensively managed plantings and has been the only option for management of diseases of eucalypts in native forests and woodlands. This applies particularly to the dieback diseases that have been the major disease problem in these communities. These diseases are of little concern in plantations, except where a species has been planted in an environment to which it is not well adapted, in which case the solution is obvious. In many cases, management of dieback diseases in native forests is limited by the lack of understanding of the underlying causes (see Chapter 17). Very little can be done to ameliorate dieback resulting from unusual weather patterns (e.g. ‘regrowth dieback’ and ‘gully dieback’ associated with prolonged drought in Tasmania, see Chapter 17), although an understanding of the etiology of the condition is important in predicting and coping with the problem (e.g. through salvage logging). Management options for control of dieback caused by Ph. cinnamomi in native forests are limited mainly to use of quarantine and hygiene measures to restrict the further vectored spread of the pathogen and replanting of damaged areas with rapidly growing trees, including trees selected for resistance to the pathogen (see Chapter 19). While dieback caused by Ph. cinnamomi has preoccupied forest

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pathologists in Australia, largely because of its effect on important timber species (E. marginata in southwest Australia and E. sieberi in south-east Australia) and its damage to a wide range of understorey species (see Chapter 11), dieback of remnant eucalypts on intensively managed pastoral and cropping land in Australia (‘rural dieback’) is a widespread and serious problem (Old et al. 1981; Landsberg and Wylie 1983; Heatwole and Lowman 1986; White 1986; Landsberg and Wylie 1988; Jones et al. 1990; Landsberg et al. 1990) (see Chapter 17). The increased effect of mistletoe infestation in remnant woodland is linked to this syndrome (see Chapter 15). Management of rural dieback requires a reassessment of the importance of eucalypts on farm and grazing land in Australia and the extent to which their survival has been imperilled by excessive clearing of native vegetation and alteration of the natural edaphic environment. In some locations, dieback is linked to the increasing problem of dryland salinity resulting from excessive tree clearing over large areas. Management of this problem will involve extensive replanting of trees, including genotypes selected for adaptation to the altered environments, and reduced clearing of existing forests and woodlands. The revegetated areas will have to be managed so that the communities are self sustaining, otherwise they will again go through a cycle of degradation and decline. For example, they will have to be large enough to reduce the effect of problems associated with exposure of trees on the edge of the community (e.g. mistletoe infestation). In the case of decline and mortality associated with natural successional changes in the forest (e.g. ‘high altitude dieback’, see Chapter 17) and for most stem and butt rots and woody root rots (e.g. Armillaria) that are part of the natural ecological cycle within the forest, all that can be done is to ensure that the major silvicultural activities in the forest do not exacerbate the problems. Outbreaks of disease caused by Armillaria and other root rotting Basidiomycota typically occur in natural stands that are thinned or selectively harvested on a regular basis or in plantations established on recently cleared natural forest or woodland (see Chapter 12). Thus, the harvesting regime (selective logging, clearfelling) or the extent and type of thinning (natural, silvicultural) may affect disease incidence. Stumps and other woody material are infected by spread of mycelium from root to root or by airborne spores. Infected stumps and roots remaining after 433

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clearing or harvesting provide the inoculum for infection of living trees. Inoculum can be reduced by removal of stumps, roots and other woody material prior to planting, although in an 18-year field trial in central Victoria (Kile et al. 1982) this was not shown to be effective in controlling the disease on high hazard sites (Kellas et al. 1997). The size and distribution of disease foci is determined by the occurrence of the pathogen in the previous plant community and by the distribution of stumps available for infection. Methods for surveying root rots are described by Bloomberg et al. (1980a, 1980b) and Bloomberg (1983b). Various models have been developed for Armillaria species (McNamee et al. 1989; Stage et al. 1990; Shaw et al. 1991) and for Phellinus weirii (Murrill) Gilbn. (Bloomberg 1983a, 1988) that relate disease effect to the biology and epidemiology of the pathogen in a predictive manner. Such models can be used to provide information for both short-term and longterm planning and for site specific management. Similar models could be developed for species of Rigidoporus, Oxyporus, Ganoderma and Pseudophaeolus in eucalypt forests. Methods of controlling root decay pathogens have been discussed at length by Fox (1977) and Shaw and Kile (1991). Stem and butt rot is rarely an important problem in short rotation stands grown for fibre or fuelwood (Davidson 1974; White and Kile 1991b) but is of concern for timber production in native eucalypt forests and long-term plantations. Decay-causing organisms enter the trunks of trees through basal injuries, branch stubs or bole wounds (Wagener and Davidson 1954). Common basal injuries include fire scars, logging injuries and cracks in the aboveground union of coppice stems with parent stumps. Retained branch stubs, particularly on fast-growing trees, and pruned branch stubs can be important entry sites (Davidson 1974; Gadgil and Bawden 1981), particularly in trees being managed for high quality sawlogs or veneer. Bole wounds resulting from fire, logging, windthrow, breakage of large branches, cankers or attack by larvae of cerambycid beetles or cossid moths can also be important. White and Kile (1991a) found that, 24 months after wounding, defect volume per unit of wound width was inversely related to wound width. Thus, even small wounds may provide suitable infection courts for decay fungi. They also reported that defect volume after 24 months was greater under barkcovered wounds than open wounds. Australian 434

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cerambycid beetles such as Phoracantha semipunctata (Fabricius) cause wounds that may allow infection, and the spread of these insects to other countries (Chararas 1968; Powell 1978) is likely to result in an increase in decay in eucalypt stands in those countries. The severity of attack by this kind of insect is amenable to silvicultural manipulation (see Chapter 19). Incidence of infection of pruning wounds varies greatly with season of pruning in regions with a seasonal climate (Gadgil and Bawden 1981). Presumably the same could apply to infection of coppice stumps. Also, the ability to compartmentalise infections may vary with season and forest type (Mireku and Wilkes 1989; White and Kile 1991a). Therefore, it may be possible to time pruning operations to reduce the incidence of decay arising from this source. Jacobs (1955) established relationships between branch diameter and the probability of defect-free occlusion of branch stubs. Marks et al. (1986) confirmed that the incidence of decay and other defects increases with the diameter of the occluded branch and they found also that the ratio of tree height to crown depth provided a method of predicting defect in the upper part of the bole. High stocking rates or competition with acacias reduced crown depth, diameter of occluded branches and incidence of decay. Thus, it is possible that manipulation of stocking rates can be used to reduce the incidence of decay. However, as eucalypt species differ considerably in their tolerance of between-tree competition and onset of suppression, this kind of information will have to be developed for particular species and site combinations. There is apparently no information on whether the incidence of decay in stands of species which tend to be self thinning is greater if they are thinned from below or allowed to self thin (Horne and Robinson 1990). McCaw (1983) found a strong correlation between extent of defect, tree diameter and wound size. Thus, it should be possible to develop predictive models to allow salvage logging of trees unlikely to grow to produce merchantable boles. Eucalypts depend on fire for regeneration and to maintain site occupancy and many species have adaptations that facilitate survival in fires (Mount 1964; Jackson 1968). In native eucalypt forests, fire is an important silvicultural tool (Wilkinson et al. 1993) and various models are available to help

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predict fire behaviour (Crane 1982). However, even with fire tolerant species, recovery after fire can be slow. Gill (1980) reported that restoration of normal bark thickness on the trunk of fire damaged E. dalrympleana was not complete even after seven years. Thus, for a long period after fire, eucalypts can be at increased risk of infection by decay fungi. In a stand of E. delegatensis, fire damage directly accounted for only 5% of defect but was the major cause of most of the scars through which decay fungi and termites entered the trees (Greaves et al. 1965). The co-occurrence of fire scars, decay and termites is a common feature in eucalypts in Australia (Perry et al. 1985). Low intensity fires, even if frequent, did not result in fire scars on jarrah trees unless branches had fallen close to the trees. High intensity fires which killed all the leaves on the trees did cause scars (Abbott and Loneragan 1983). Careful management of fire regimes in eucalypt forests, especially through the use of controlled, fuel reduction burns, can reduce the incidence of wild fires and hence minimise fire scars and subsequent development of decay. In the event of severe fire damage, high incidence of decay and termite damage can be expected and so it is probably better to clearfell the site and re-establish the stand (Wilkinson and Jennings 1993). There has been little study of the rate of progress of decay in eucalypt stands and there is little published information for eucalypts on the increase with stand age in decay as a proportion of standing volume (Rayner and Turner 1990a, 1990b). There is no standard methodology for selecting sites or trees for decay sampling. External indicators of decay such as presence of basidiocarps or scars are likely to be of only limited use. The number of trees to be sampled and the number of survey sites will depend on the number of eucalypt species growing on the site, the range of site variation and the range of tree ages. Decay and termite damage commonly occur together in eucalypt trees in Australia (Greaves et al. 1965, 1967) and quantifying their separate effects is difficult. Defect resulting from damage during thinning is, however, recognised as a factor to be included in economic analyses of intensive forestry management (Bostrom 1982) and in weighing the relative merits of selective logging and clearfelling. In general, decay as a percentage of gross volume in the standing trees increases with age (Wagener and Davidson 1954). From studies of stand growth and predictions of decay incidence it should be possible to predict the optimum time to harvest. In summary,

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many aspects of sound siviculture can reduce losses due to decay. Many foliar and canker pathogens are endemic in native eucalypt forests and woodlands, but epidemics of disease are rare and little attention has been paid to them in forest management. However, many of these pathogens are common and destructive in eucalypt plantations and are of major concern in plantation management. Eucalyptus globulus plantations in south-east Australia are often heavily infected by Mycosphaerella nubilosa (Cooke) Hansf. and Mycosphaerella cryptica (Cooke) Hansf. Destructive foliar diseases are common in plantations outside Australia. For example, planting of E. globulus was greatly restricted by Mycosphaerella leaf blotch caused by M. juvenis in South Africa (see Chapter 9) and Cryphonectria canker is a serious problem in eucalypt plantations in Brazil (see Chapters 10 and 22). Management of disease outbreaks depends on sound knowledge of pathogen biology and disease epidemiology (see Chapters 9 and 10). Unlike stem and butt rots, woody root rots and dieback diseases, which generally develop and spread slowly, foliar and canker diseases can develop rapidly and cause problems even in short rotation plantations. For example, M. juvenis and M. nubilosa are destructive on the juvenile growth phase of their hosts (see Chapter 9). The severity of foliar and canker diseases can vary widely depending on weather conditions and the environment in particular localities. Therefore, management strategies must be flexible in order to anticipate localised epidemics. Foliar and canker diseases are sensitive to microclimate, and so alteration of the forest environment or planting of eucalypt genotypes in different environments can result in disease outbreaks. Some silvicultural practices may influence disease severity. For example, spacing of plants and the extent of pruning and thinning can affect air movement and the rate of drying of foliage, thereby affecting the time during which conditions will be favourable for sporulation and infection by foliar and twig pathogens. Ground preparation, control of weeds and fertilising may improve tree vigour, which may reduce susceptibility and disease incidence. Adult and juvenile foliage of some eucalypts differ markedly in susceptibility to some pathogens (e.g. M. nubilosa attacks only juvenile leaves of E. globulus and related species, see Chapter 9). Thus, conditions which promote early maturity of foliage can reduce the effect of such 435

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diseases. Trees could also be selected and bred for this attribute.

18.5.2 Selection of resistant genotypes The very wide genetic diversity of the eucalypts (see Chapter 2) offers great scope for selection of types adapted to particular environments and, more specifically, of types with a degree of resistance to particular pests and diseases. Species and provenance trials are of critical importance in matching genotypes to sites during plantation development. Selection of disease resistant species and provenances, based on their performance in such trials, is important for management of most diseases. Such trials are also useful in giving forewarning of potentially damaging pests and diseases at the site. Often their effect may not become fully evident until plantations have been established on a wide scale for several years. The growth rate and quality of stands and tree health can be increased dramatically by careful phenotypic selection and subsequent genetic improvement, as evident in the research on Pinus radiata (Burdon 1992). Clonal forestry is being used increasingly as a viable alternative to natural regeneration or seedlingbased forestry. The potential advantages of clonal forestry are well documented (Libby and Rauter 1984; Carson 1986; Mullins and Park 1992). By using clonal techniques, higher yielding, healthier forests can be developed within a much shorter time than with breeding methods based only on seedlings (Mullins and Park 1992; Eldridge et al. 1993). The success of an accelerated selection and breeding strategy using clonal selection depends heavily on reliable methods of vegetative propagation and, increasingly, on reliable in vitro regeneration systems, which are now becoming available for a wide range of eucalypt species (although not yet for E. globulus). Intensive selection of resistant trees, development of inexpensive vegetative propagation techniques and careful breeding programs have resulted in the virtual elimination of Cryphonectria cubensis (Bruner) Hodges, a serious canker pathogen, from commercial eucalypt plantations in Brazil where it had previously caused epidemic disease (Alfenas et al. 1983; Campinhos and Ikemori 1983). An imperative in eucalypt selection and breeding programs is the development of methods for the early screening of trees for disease resistance. Genotypes can be screened for resistance to some diseases by inoculation of potted plants in a 436

greenhouse or by exposure of tissue culture lines to a pathogen (e.g. Harvey and Grasham 1969; Hrib and Rypacek 1981; van den Bulk 1991) or a pathogen metabolite (such as a toxin) if this is the sole determinant of pathogenicity (e.g. Belanger et al. 1989; Hammerschlag 1989). However, ultimately resistance selected in this way has to be expressed in the field in the face of highly variable pathogen populations and must be stable over a long period of widespread exposure to the pathogen. Breakdown of narrowly based resistance due to adaptation of pathogen populations, as has occurred commonly in agriculture, could be disastrous in eucalypt forests where replanting with new, more resistant genotypes is difficult and expensive. The surest way of selecting for durable field resistance is by exposure of a range of genotypes of the tree to natural or augmented inoculum of the pathogen in the field (e.g. in species, provenance or clonal trials). Even when genotypes with resistance against a certain disease are selected, it is prudent to plant a diversity of genotypes in case of breakdown of resistance due to adaptation of the pathogen or of an increase in the effect of other pests and diseases. The best option for low cost, long-term management of foliar and canker diseases is by selection and breeding of resistant genotypes. Significant differences in susceptibility to some foliage and canker diseases have been reported between eucalypt species and between provenances within species. Some of the more noteworthy examples are resistance to canker caused by Cryphonectria cubensis in E. grandis (Campinhos and Ikemori 1978) and E. urophylla (Eldridge 1984), resistance to Mal de Rio Dôcé in Brazil (Dianese et al. 1984a), to Puccinia psidii in Brazil (Dianese et al. 1984b), to M. juvenis in E. nitens in South Africa (Nixon and Hagedorn 1983; Purnell and Lundquist 1986), to Mycosphaerella spp. on E. globulus in southern Australia (Dungey et al. 1997), to Ralstonia solanacearum in Brazil (Dianese et al. 1990) and to Cylindrocladium spp. in Brazil (Blum and Dianese 1993) (see Chapter 22). Most of these reports are based on observations of the performance of eucalypts in the field rather than on quantitative measurement of disease in replicated trials. However, in several cases, variation between species and provenances in their field response to disease has been sufficient for the plantation industry to undertake successful selection, breeding and replanting programs to control diseases. In only one

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study of eucalypt pathogens, to our knowledge, has heritability of resistance been estimated in a series of carefully designed and well-replicated trials. Dungey et al. (1997) found resistance to M. cryptica and M. nubilosa in E. globulus to be highly heritable (0.3) with no significant genotype by site interaction. If breeding for resistance to disease is to progress rapidly, more experimental data of this kind are needed. Selection of resistance to particular diseases can be used for disease management in native forests and woodlands. If a disease is particularly destructive, as in the case of Ph. cinnamomi in some coastal forests in south-east Australia and more extensively in E. marginata forests in south-west Australia, it is possible to replant damaged areas with resistant species or even with genotypes of susceptible species selected for resistance to the pathogen (Stukely and Crane 1994). Generally, if a diversity of seed is applied to the sites in the normal regeneration processes, natural selection will ensure that sites are occupied by genotypes with a degree of resistance to the prevalent diseases. In the coastal forests in eastern Victoria, it is possible that there is a degree of selection of resistance to Ph. cinnamomi among the populations of susceptible E. sieberi surviving on severely affected dieback sites which have been replanted, although this is yet to be shown experimentally and the survival of the trees in the long term is yet to be determined. Although species such as Armillaria luteobubalina Watling & Kile have a wide host range in native forests (Shaw and Kile 1991), there have been no detailed studies of variation in resistance of different eucalypt genotypes. By planting resistant genotypes it may be possible to rehabilitate areas damaged by Armillaria. Selection of eucalypt genotypes adapted to the altered rural environments, including saline areas, will be important in the restoration of the health of remnant eucalypts in rural landscapes. In some cases, it may be necessary to replant with eucalypt species resistant to the local pests and diseases. Some species (e.g. Corymbia citriodora, C. maculata) show wide adaptability beyond their natural range and exhibit high levels of resistance to, for example, leaf spot diseases and psyllids that can be damaging on indigenous eucalypts like E. botryoides and E. camaldulensis in south-east Australia. Planting of species resistant to mistletoe may be necessary to allow the regeneration of areas of woodland badly infested by these parasites (see Chapter 15).

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Eucalypt species vary greatly in the decay resistance of their heartwood, although this is not necessarily reflected in the decay resistance of standing trees (see Chapter 13). Stem decay patterns in eucalypts vary with the natural decay resistance within the bole heartwood (Rudman 1964; Wilkes 1982, 1985a), with the compartmentalising responses of the sapwood (Wilkes 1985a, 1985d) and with the formation of barrier zones by cambial activity (Wilkes 1985a, 1986). While sapwood of eucalypts shows typical compartmentalising responses (Shigo and Marx 1977; Shortle 1979; Wilkes 1985a), the heartwood does not (Wilkes and Heather 1983; Wilkes 1985a, 1985c). In angiosperms, there is a positive correlation between volumetric heat content of the wood and resistance to decay but a negative correlation between growth rate and resistance. This has been interpreted as indicating that increased decay resistance requires an increased proportion of the energy budget of the tree to be directed towards protective measures such as fungitoxic heartwood chemicals or thick protective bark (Loehle 1988). Selection and breeding of decay resistance probably could be used in establishment of long-term plantations for sawlog production. However, there appears to be no published information on the heritability of resistance to decay in standing trees or of durability of heartwood. In the future it is likely that, to reduce pulping costs, eucalypts grown in plantations for pulpwood will be selected for late formation of heartwood and for low concentrations of the extractives which determine natural decay resistance of heartwood (Rudman 1964; Nelson and Heather 1972; Hart and Hillis 1974). Fast-growing eucalypts with these attributes are known to be susceptible to decay (Davidson 1974; Gadgil and Bawden 1981). While there is a negligible influence of growth rate on decay resistance of heartwood tested in vitro, the diameter of the juvenile core, which is more susceptible to decay, is larger in faster than in slower growing trees of a given species (Wilkes 1985b). Furthermore, branch shedding and occlusion of the resulting stubs may be poorer in faster growing trees (Jacobs 1955), providing greater opportunity for infection by stem rotting fungi. Thus, selection of trees for pulping quality probably will result in greater problems with decay in the plantations, although the short-term nature of these plantations should minimise the effect of decay. 437

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18.5.3 Chemical control The use of fungicides in native eucalypt forests is not cost effective and they are almost never used. They may be used to control disease in plantations, especially plantations managed for short-term production of fibre and in seasons unusually favourable for development of disease epidemics. Use of fungicides to protect the juvenile growth stage of E. globulus from destructive Mycosphaerella spp. may be justifiable in plantation establishment (see Chapter 9). Seed orchards and clone banks, being the result of long and expensive research programs, have high economic value and justify a very high level of disease management including use of fungicides (see Chapter 21). This may apply particularly where disease-free shoots are required for clonal propagation. Treatment of seed with fungicides may be important where the seed is being transferred between regions, even though our knowledge of seedborne diseases in the eucalypts is limited (see Chapter 7). The use of fungicides in forest nurseries is often feasible and justifiable, particularly for preventing disruption of planting programs, minimising the introduction of diseases to new areas and reducing the occurrence of disease in the early stages of plantation development. The use of healthy, diseasefree stock for forest and plantation establishment may be important for the long-term health of the planting and may give an economic return out of all proportion to the value of the initial planting stock. The danger of development of resistance to fungicides in populations of pathogens needs to be considered, and strategies, such as use of mixtures of fungicides and alternation of fungicides with different modes of action, are employed to reduce the likelihood of buildup of resistant strains. Chemical treatment of nematode infestations or soilborne diseases such as woody root rot caused by Armillaria may be feasible where these diseases are localised, spread slowly from foci of relatively restricted area and are likely to lead eventually to infestation of a much larger area of forest. Various fungicides and fumigants have been recommended for control of root rot in foci but none has been shown to be cost effective for use in plantations or native forests on a broad scale.

18.5.4 Biological control Biological control has been little used in control of diseases in eucalypt forests, although one of the 438

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earliest methods of biological control of a plant pathogen involved a forest disease. Root rot of conifers caused by Heterobasidion annosum (Fr.:Fr.) Bref. was controlled by pre-emptive inoculation of freshly cut stumps with the competitive saprophyte, Phanerochaete gigantea (Fr.:Fr.) S.S.Rattan, Abdullah & Ismail [syn. Peniophora gigantea (Fr.:Fr.) Massee] (Rishbeth 1963). Use of a competitive saprophyte to colonise dead stumps and roots or an antagonistic or mycoparasitic fungus to prevent further spread of the pathogen will possibly prove to be the most effective approach to control of woody root rot caused by Armillaria (Rishbeth 1976; Shaw and Roth 1978). Studies in Western Australia (Pearce 1990; Pearce and Malajczuk 1990a, 1990b; Nelson et al. 1995; Pearce et al. 1995) have shown the potential of certain fungi to reduce inoculum of Armillaria, although effective biocontrol methods are not yet available for commercial use.

18.6 Political and legislative considerations The last two decades of the twentieth century saw a burgeoning of community and political interest at local, state, national and international level in the manner in which forests are managed. Management of forest health has been an important issue in these developments.

18.6.1 Multiple forest use at a local scale The growth of concern that multiple forest use be delivered at a localised scale has resulted in significant changes to forestry practices. To optimise the regeneration of some eucalypt species (e.g. E. diversicolor, E. regnans, E. sieberi) or to minimise impacts of Ph. cinnamomi in jarrah forests, the optimum strategy might have involved clearfelling in clusters of large coupes. The current practices of selection cutting on small, widely dispersed coupes, while desirable for many other reasons including reduced impacts on aesthetic landscape values, greatly increases the area of forest harvested and the extent of roads with attendant risk of increased breakdown of hygienic access. Roading also increases access to forest wildlife by foxes, a destructive introduced predator in Australia. Concern for public health and quiet, and for preservation of conservation values has complicated the process and increased the cost of application of fungicides for example. The number of community,

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health, environment and air safety agencies with whom it is necessary to consult, and from whom approvals must be sought has increased significantly. There is increasing recourse to litigation in disputes with managers of forested lands. Expert opinion supplied to the court by qualified and experienced forest pathologists acting for the plaintiff or the defendant may be contradictory.

18.6.2 International conventions The concept of Ecologically Sustainable Forest Management is an integral part of the management of all commercial and conservation forests in Australia. The Working Group on Criteria and Indicators for the Conservation and Sustainable Management of Temperate and Boreal Forests (Montreal Process 1995) identified seven categories of conditions or processes (criteria) by which sustainable forest management might be assessed. For each criterion a set of quantitative or qualitative variables (indicators) was nominated that demonstrate trends when observed periodically (Brand 1997). The third Montreal Process criterion is assessment and monitoring of forest ecosystem health. Rapport et al. (1998) identified three components of ecosystem health: vigour, resilience and organisation. A common indicator used for forest health has been tree health, which is defined as the incidence of biotic and abiotic factors (stresses) affecting trees (Innes 1993; Ferretti 1997). Most forest health surveys assess tree appearance or condition rather than tree health. To overcome this possible problem there has been a move internationally to use of physiological rather than phenotypic or morphological attributes to monitor forest health (Vora 1997; Innes 1998). Demonstrated sustainable forest management is critical to national and international forest and forest product certification schemes and to development of an Australian Forest Standard for forests managed for wood production. National Forest Policy and Regional Forest Agreements reflect this diverse community interest in forests and forest management. Liberalisation of international trade under World Trade Organisation auspices following the Uraguay Round of negotiations has important implications for international plant quarantine. In an effort to introduce greater transparency of processes and increased consistency in application of the rules, the International Plant Protection Convention and the Sanitary and Phytosanitary Standards have been

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given greater importance. The result in Australia is an increasing number of formal Import Risk Analyses. The desire of plantation managers to increase tree growth and pest and disease resistance quickly has meant increasing demand for approval to import germplasm from other countries either as seed or tissue cultures. The quarantine risks associated with imports of eucalypt germplasm in either form are as yet poorly understood. Imports of untreated eucalypt timber either as lumber or as packaging and dunnage is another high-risk potential entry route for exotic pathogens or decays of eucalypts (Bulman 1998).

18.7 Conclusion The management options available for disease control in eucalypts depend on the situation in which the trees are grown. In native forests, options are limited to manipulation of the natural forest environment using silvicultural treatments, while in plantations a wider range of options is available, including careful selection of sites for planting (e.g. to avoid drought prone sites and areas infested with Ph. cinnamomi), selection of eucalypt genotypes for adaptation to the site and for disease resistance, creation of environmental conditions less favourable for disease (e.g. by deep ripping and mounding of soil, fertilisation, pruning, thinning) and even carefully targeted use of fungicides. Disease management in nurseries may be even more intensive and can include exclusion of pathogens by strict quarantine and hygiene measures, manipulation of environmental conditions within glasshouses, control of water supply, and regular application of fungicides. Management of disease in remnant eucalypts on grazing and farm land will rely mainly on restoration of areas of these predominantly woodland areas to something approaching their natural ecological state. Management options also depend on the types of disease threatening the forest. For some dieback diseases, woody root rots and stem rots that are part of the natural ecological cycle of a forest or are the result of unusual weather, little can be done except to incorporate predictions of disease effects into normal forest management strategies and to develop silvicultural practices that ameliorate or do not exacerbate the diseases. For control of destructive epidemic diseases, the wide genetic variability of the eucalypts is a firm basis for selection of better adapted and disease resistant genotypes. While 439

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selection for resistance is likely to be useful for most diseases, it has already proven useful for management of foliar and canker diseases, especially in plantations where the choice of planting material is not restricted. Chemical treatments are only likely to be feasible in nurseries or where potentially destructive soilborne diseases are found to be spreading slowly from restricted foci. International quarantine is important in preventing the spread of several destructive pathogens that appear to have adapted to eucalypts growing outside Australia. Only a few of the many native Australian pathogens of eucalypts have spread to other countries. These pathogens may have little effect in native forests, but are well adapted to eucalypts and could be destructive in plantations in other countries or other environments. Within Australia, quarantine and hygiene measures are important in restricting the further spread of Ph. cinnamomi, a pathogen that has been introduced in relatively recent times. Such measures will also be important if another destructive exotic pathogen (e.g. Puccinia psidii) is introduced to indigenous forests. In long-lived forests, regular surveillance is important to detect outbreaks of diseases, including those that may invade despite quarantine, to provide the basis for correct diagnosis of disease, to increase information on spread and impact, and to build the long-term ecological understanding of forest diseases needed to develop appropriate management strategies for reducing their impact. Regular surveillance of forest health is also needed to fulfil monitoring and reporting requirements for demonstrating sustainable forest management. Social and political constraints are likely to make management increasingly difficult.

18.8 Acknowledgments John Walker and the late Jack Warcup taught J. Simpson the value of close observation of detail. M.R. Jacobs, author of Growth Habits of the Eucalypts, taught F.D. Podger that the history of trees and forests is writ large in their architecture for those who observe carefully. To each we are profoundly grateful.

18.9 References Abbott, I. and Loneragan, O. (1983). Influence of fire on growth rate, mortality, and butt damage in

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Mediterranean forest of Western Australia. Forest Ecology and Management 6, 139–153. Alfenas, A.C., Jeng, R. and Hubbes, M. (1983). Virulence of Cryphonectria cubensis on Eucalyptus species differing in resistance. European Journal of Forest Pathology 13, 197–205. Baddeley, C. (1989). Detection of new insects and diseases in indigenous forests in New Zealand. New Zealand Journal of Forestry Science 19, 250–255. Belanger, R.R., Manion, P.D. and Griffin, D.H. (1989). Tissue culture and leaf spot bioassays as variables in regression models explaining Hypoxylon mammatum incidence on Populas tremuloides clones in the field. Phytopathology 79, 318–321. Bishop, R.C. (1993). Economic efficiency, sustainability, and biodiversity. Ambio 22, 69–73. Bloomberg, W.J. (1983a). A ground survey method for estimating loss caused by Phellinus weirii root rot III. Simulation of disease spread and impact. Canadian Forest Service, Pacific Forest Research Centre Report BC-R-7. (Forestry Canada, Pacific Forestry Centre: Victoria, British Columbia.) Bloomberg, W.J. (1983b). A ground survey method for estimating loss caused by Phellinus weirii root rot IV. Multiple disease recording and stratification by infection intensity. Canadian Forest Service, Pacific Forest Research Centre, Report BC-R-8. (Forestry Canada, Pacific Forestry Centre: Victoria, British Columbia.) Bloomberg, W.J. (1988). Modelling control strategies for laminated root rot on managed Douglas-fir stands: model development. Phytopathology 78, 403–409. Bloomberg, W.J., Cumberbich, P.M. and Wallis, G.W. (1980a). A ground survey method for estimating loss caused by Phellinus weirii root rot I. Development of survey design. Canadian Forest Service, Pacific Forest Research Centre, Report BC-R-3. (Forestry Canada, Pacific Forest Research Centre: Victoria, British Columbia.) Bloomberg, W.J., Cumberbirch, P.M. and Wallis, G.W. (1980b). A ground survey method for estimating loss caused by Phellinus weirii root rot II. Survey procedures and data analysis. Canadian Forest Service, Pacific Forest Research Centre, Report BC-R4. (Forestry Canada, Pacific Forest Research Centre: Victoria, British Columbia.) Blum, L.E.B. and Dianese, J.C. (1993). Susceptibility of different Eucalyptus genotypes to artificial leafinoculations with Cylindrocladium scoparium and C. clavatum. European Journal of Forest Pathology 23, 276–280. Booth, T.H., Nix, H.A., Hutchinson, M.F. and Jovanovic, T. (1988). Niche analysis and tree species introduction. Forest Ecology and Management 23, 47–59. Booth, T.H., Stein, J.A., Nix, H.A. and Hutchinson, M.F. (1989). Mapping regions climatically suitable for particular species: an example using Africa. Forest Ecology and Management 28, 19–31.

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F.D. Podger and P.J. Keane

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Only since the 1960s, with the diagnosis of Phytophthora cinnamomi as the cause of a destructive epidemic in the eucalypt overstorey and in many other taxa in the understorey of Eucalyptus marginata forests of south-west Australia, have disease problems been studied seriously in native plant communities. Many diseases with a variety of causes, some complex and poorly understood, are now recognised in eucalypts in native forests and woodlands and in remnant trees on farming and grazing land. Appropriate management strategies for these diseases have been developed within the constraints imposed by the ecological situation of native communities, their relatively low economic productivity, and their multiple functions including wildlife conservation and water catchment (see Chapter 18). Because of its destructiveness in a wide range of vegetation types in south-east and south-west Australia, diebacks caused by Ph. cinnamomi have received most attention. This disease has provided a model for the diagnosis, monitoring and development of management options for other diseases in native forests and woodlands. Direct attack upon Ph. cinnamomi or major modification of environments to constrain its effects are unaffordable, with the possible exception of use of the inorganic chemical, potassium phosphonate, to protect selected elements of susceptible flora on lands that are already infested. The key management strategy to constrain further development of the epidemic is based on control of human access to forests in order to reduce the chance of further human-vectored spread of the pathogen. Management of dieback and mistletoe infestation in remnant eucalypts on grazing and farm land requires restoration of self-sustaining areas of woodland and forest communities and the replanting of eucalypts adapted to the grossly altered environments. Management options for the wide range of dieback diseases of complex etiology, foliar and canker diseases, woody root rots, and stem and butt rots in native forests are in the early stages of development and are limited to application of silvicultural practices so as not to exacerbate diseases that occur at low incidence and severity in relatively undisturbed forests. Regeneration of forests with the full range of eucalypt genotypes previously on the site allows for selection of types with resistance to the prevalent diseases, albeit with expected further losses of susceptible genotypes. Planting of genotypes of eucalypts selected for resistance to Ph. cinnamomi has potential for regeneration of small areas of forest severely damaged by this pathogen.

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19.1 Introduction Awareness of disease in natural woody vegetation in Australia increased greatly in the 1960s following reports (Podger et al. 1965; Podger 1968; Podger 1972) of the causal role of Phytophthora (Ph.) cinnamomi Rands in a serious epidemic of tree deaths and deaths of an extraordinarily wide range of understorey taxa in the jarrah (Eucalyptus marginata) forests of south-west Western Australia. This disease came to be known as ‘jarrah dieback’ (Figs 19.1 and 19.2) (see Chapter 11). Later, a similar dieback disease was reported from forests in south-east Australia. This was followed by numerous reports of tree decline with a range of causes in native plant communities in many localities across Australia (Podger and Ashton 1970; Marks and Idczak 1973; Podger 1973). An analysis of this wide variety of dieback diseases indicated that, within a predominantly healthy matrix of native forests and woodlands, a significant and widespread but patchy mosaic of unhealthy stands extended over extensive areas of the winter rainfall regions of Australia (Podger 1972). Some are now known to be caused by episodic or local outbreaks of native parasites which form a natural and integral component of the natural biota. For example, the native agaric, Armillaria (A.) luteobubalina Watling & Kile, causes a root rot resulting in death of patches of trees in some forests of southern Australia (Kile 1981; Kile et al. 1991). Foliar and canker diseases are endemic in the native eucalypt forests and undoubtedly reduce productivity, as shown by the improved growth and form of species grown outside Australia in the absence of coevolved foliar parasites (see Chapters 9 and 10). However, only on rare occasions have these diseases reached epidemic proportions and they have not caused damage to mature trees on the scale of the epidemics due to Ph. cinnamomi. Stem and butt rots cause significant losses in native forests, especially in natural ‘old growth’ forests that have suffered repeated episodes of damage by fire and other stress factors during a long life (see Chapter 13). Other diseases are associated with rare environmental events. For example, regrowth dieback at lower elevations in tall open forests of the high rainfall zone in Tasmania is associated with rare, protracted drought (see Chapter 17). Other dieback problems such as high altitude (c. 1000 m) dieback of E. delegatensis over thousands of hectares on the plateaux in north-east and north-west Tasmania are a

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Figure 19.1

Jarrah forest 45 years old arising from clearcutting in the early 1920s (Karnet compartment 7), uninfested by Phytophthora cinnamomi.

consequence of natural succession towards temperate rainforest (see Chapter 17). Other diseases are a consequence of human disruption of the natural balance between the plant communities, their physical environment and other components of the natural biota (see Chapter 17). This is thought to be the fundamental cause of the progressive decline known as ‘rural dieback’ in remnant eucalypts in partly cleared grazing and farm lands. This decline is a problem in many parts of eastern and south-west Australia. In some areas, the general decline in such eucalypt populations is associated with rising watertables and increasing soil salinity. A serious tree decline over the last few decades in the open woodland of partially cleared country in the low rainfall zone in Tasmania is

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Contemporaneous mass collapse of overstorey and understorey caused by Phytophthora cinnamomi in unlogged natural jarrah forest (Cooke Forest Block 1975).

associated with an increase in browsing pressure of brush possums [Trichosurus vulpecula (Kerr, 1792)]. The occurrence of patches of severe defoliation in grossly altered eucalypt forests in moist habitats along the eastern seaboard between Lakes Entrance, Vic., and Cunninghams Gap, Qld, has been attributed to high populations of leaf sucking psyllids and associated bell miners [Manorina melanophrys (Latham, 1802)] (see Chapter 17). The decline of eucalypts and other trees and shrubs in remnant and roadside vegetation in the south-east of South Australia, now referred to as ‘Mundulla yellows’ (see section 19.3 and Chapter 14), is of increasing concern. While none of these diseases has matched the severity of impact of the ongoing epidemic of dieback caused by Ph. cinnamomi in the jarrah forests of Western Australia, they represent a major problem of decline in eucalypt-dominated vegetation across southern Australia and a major challenge for vegetation management. It is important to note the long lapse of time between the first observation of dieback diseases and their definitive diagnosis and the first implementation of disease management strategies. Jarrah dieback was first noted in 1921 (Wallace and Hatch 1953) but its cause was not diagnosed until 1964 (Podger et al. 1965) and a disease management system was not put in place until about 1972. A similar situation has occurred with Mundulla yellows, which was first

observed in about 1975 (G. Cotton, pers. comm.) but whose cause has yet to be diagnosed. The management of disease in native eucalypt forests and woodlands is a complex and challenging task for several reasons, as follows. 1

Native forests and woodlands are complex communities. The overstorey trees often consist of several species in different age classes and arrays. These may be affected differently by particular diseases. Disease control is often as important in the understorey species as in the overstorey eucalypts, not least because disease in understorey species may affect disease in the overstorey. In particular, management of disease caused by Ph. cinnamomi is directed at the entire plant community.

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Native forests and woodlands cover vast areas.

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Native vegetation occurs in varied situations of land tenure and management, ranging from forests managed by government for production of wood and fibre or for conservation purposes, to natural woodlands and woodland remnants created by tree clearing on private land. Often, forests have multiple functions. Large areas of native forest in Australia are managed mainly as water catchments. A dieback disease such as that caused by Ph. cinnamomi can adversely affect

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Areas affected by dieback (solid shading) (after Shearer and Tippett 1989; based on Forests Department pre 1976 aerial photographic interpretation and other best available Forest Department information; isohyets provided by WA Water Authority and coastline by AUSLIG; compiled by C. Pearce, Information Management Branch, Department of Conservation and Land Management, Western Australia).

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the quality of water flowing from these forests while increasing their yield of water (Shea et al. 1975; Shea and Herbert 1977; Bartle et al. 1981). 4

5

There is widespread confusion over the causes of death and debility in native vegetation (see Chapter 17). This is very largely because of the difficulty of diagnosis of cause among many unrelated problems which share common symptoms (fundamentally, ‘dieback’ symptoms resulting in tree death after a longer or shorter period). Diagnosis of dieback diseases in native vegetation requires detailed ecological and pathological observation over an extended period. The direct economic return from native forests and woodlands is often too low to support anything but minimal intervention to control diseases.

Disease management strategies will be affected by the overall aim of vegetation management, whether for timber production on long rotation, pulp or pole production on short rotation, water catchment, conservation or land protection. For example, while it is important to reduce losses from stem and butt rots in production forests, these rots are considered to be an important natural process providing hollows for animal shelter in forests set aside for conservation (see Chapter 18). Diseases require different management strategies according to their cause. If the underlying cause is ecological disturbance of the community, the strategy will be to address that disturbance. If the disturbance is part of a natural cycle (e.g. severe but infrequent drought) there is little to be done except to understand the problem and incorporate action into the overall vegetation management strategy. If the syndrome is part of a natural successional change from tall open forest to temperate rainforest, a management decision is required as to whether the succession should be allowed to take its natural course or whether the forest should be burnt to allow reassertion of eucalypt dominance. This decision will depend on whether the forest is being managed for timber production or for conservation. If the disease is caused by an identifiable destructive pathogen such as Ph. cinnamomi or A. luteobubalina, there are two possible management strategies. One strategy is to attempt abatement of disease in areas already

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affected by the pathogen. In native forest the choices for abatement are few and, except in small areas of unique value, unaffordable. This situation applies to many areas already infested as a result of introduction of Ph. cinnamomi. It also applies to most of the forests to which A. luteobubalina is indigenous. The second broad strategy is to constrain the rate of invasion of yet uninfested native plant communities (which may contain susceptible species and are also environmentally vulnerable to the disease). This situation applies to many areas of vulnerable forests which are still free of Ph. cinnamomi.

19.2 Management of dieback caused by Phytophthora cinnamomi Because of its destructiveness, dieback caused by Ph. cinnamomi, among all the diseases of native eucalypt forests, has had the greatest effect on forest management particularly in south-west Australia. The development and application of management strategies for this disease are therefore discussed in detail and provide an example of the problems associated with the diagnosis, mapping and management of diseases in native forests, even when the primary cause of the disease is clearly identified. Substantial management programs to combat the threat have been implemented in Western Australia, Victoria and Tasmania, and lately in South Australia. These programs, progressively modified with experience, reflect regional differences in the nature of the vegetation, the expression of the disease and the relative difficulty of addressing the problem under particular local administrative and legislative circumstances. The programs reflect all the problems of managing a disease in native forests referred to in the previous section. The basic biology and pathology of Ph. cinnamomi are discussed in Chapter 11. Where inherent susceptibility to Ph. cinnamomi root rot exists among important elements of certain native plant communities, including particular eucalypt species, and is coincident with environmental conditions conducive to disease, an epidemic is inevitable upon introduction of the pathogen. Plants in such circumstances are said to be both genetically susceptible and environmentally vulnerable—with the presence of the pathogen this combination usually results in major disruption of community

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structure, extinction of populations of some species of the flora, a massive reduction in primary productivity, including that of eucalypts, and drastic consequences for the capacity of the affected communities to provide habitat for dependent flora and fauna. The vegetation assemblages of resistant species, particularly grasses and sedges, which often colonise devastated lands, are generally less productive, less diverse and more open and provide poorer habitat for fauna that depended on the original forest. Colonisation of Australian landscapes by Ph. cinnamomi is almost certainly in its third century and the pathogen is now established in a mosaic over millions of hectares of native vegetation.

3

a distinct patchiness in the distribution of the disease and association of its occurrence with evidence of prior human movement through the forest (Fig. 19.4 and Plate 19.1)

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clear evidence of an ongoing extension of the boundaries of the patches of damaged forest marked in the understorey by a sharp boundary with healthy forest

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clear symptoms of differences in the time of onset of disease among individual plants in the ground layer, indicative of ongoing disease rather than calamitous impact of a physical factor

The ultimate goal of management of the disease is to maximise the long-term survival in nature of those plant species (including eucalypts) and their dependent biota that are threatened by the epidemic. The steps involved in management of the disease in native plant communities have been (see sections 19.2.1 to 19.2.5) to:

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temporally and spatially irregular extension of the patches, seldom averaging more than one metre per annum upslope but being greater downslope.

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diagnose the cause of the disease

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determine the process of disease development

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map the extent of disease

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determine hazard ratings for particular communities

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devise and test options for disease control.

19.2.1 Diagnosis Often accurate diagnosis of disease has been a difficult problem for forest and woodland dieback syndromes where diseases of different cause have similar symptoms, particularly when observed only once (see Chapter 17). The following characteristics, based initially on the most clear-cut expressions of the disease in the E. marginata forests of Western Australia during the 1960s, are associated with epidemics of disease caused by Ph. cinnamomi in native vegetation and allow diagnosis of the disease (Podger 1973): 1

sudden wilt followed by mass deaths in the E. marginata overstorey, preceded or accompanied by similar collapse in the understorey of Banksia and Persoonia and many other species of the shrub and ground layers (Fig. 19.2)

2

no comparable deaths in the codominant Corymbia calophylla canopy and certain other resistant floristic elements in the lower storeys

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With experience it is possible to recognise similar patterns in areas where symptoms are expressed more subtly. From the 1970s, similar syndromes were observed in Victoria, Tasmania and South Australia, although in these areas the eucalypt and understorey species are different from those in the E. marginata forest and the expression of symptoms in the overstorey often involved dieback rather than mass deaths of trees. In certain forests in Victoria, mass collapse of the understorey shrub, Xanthorrhoea australis R.Br., is the most diagnostic feature of dieback caused by Ph. cinnamomi (Weste and Taylor 1971). In exceptionally wet years, localised mass collapse of the eucalypt overstorey has occurred (Marks et al. 1972).

19.2.2 Development of disease In one of the most readily interpretable circumstances, that of stands dominated by Banksia grandis Willd. and E. marginata in the high rainfall zone (800–1200 mm) in south-west Australia, two distinct epidemics occur. The two epidemics, one in the very susceptible understorey, the other among the E. marginata trees, have distinctive courses and characteristics. The epidemic in the understorey results in mass mortality of Banksia grandis, which except rarely, completely eliminates the species, progresses steadily from year to year, is insensitive to variation in soil characteristics and is followed by a severe decline in populations of the pathogen. A similar epidemic occurs in the dominant understorey species, Xanthorrhoea australis, in certain forests in south-east Australia (Weste and Taylor 1971). The epidemic in the

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Aerial view from 6000 metres over jarrah forest near Willowdale (19/1/65 by Western Australian Lands Department—WA 909 Pinjarra Run 17 number 5063 6"). The white lines indicate forest roads and tracks; the dark, closely matted areas, dense ti-tree flats along watercourses; mid-grey areas with granular texture, uninfested forest; pale-grey blotchy textured areas, forest of greatly reduced canopy cover following infestation by Phytophthora cinnamomi. Note the tendency for diseased areas to be associated with roads and drainage lines.

E. marginata overstorey is much more variable. On some sites the effect is severe and contemporaneous with that on Banksia grandis. This response is said to be a ‘mass collapse’ on sites of high hazard and leads in time to a ‘graveyard’ condition of tall dead stags among which many of the smaller lignotuberous advance-growth plants may persist for long periods. However, in most places it is unusual for all E. marginata plants to die. More commonly, mortality in the eucalypt overstorey is episodic and rare. Eucalypt deaths often follow unseasonal heavy summer rains of erratic and limited distribution. The extent of mortality is very sensitive to site. The variable patterns of eucalypt death in a stand are thought to be a function of both sensitivity to local variations in soil characteristics and to innate resistance within the populations. On long-infested areas epidemics are followed by a phase of endemic disease. On these old mass collapse sites, advance growth of E. marginata may develop slowly into the sapling

and small pole stages. This has lead casual observers to believe that the community might be in a state of recovery, but there is little evidence of its long-term persistence or of significant seedling regeneration of E. marginata. However, advance-growth and seedling regeneration of C. calophylla increases on some severely damaged sites and eventually produces a woodland of open-grown, low-branching trees. In some such places, a dense stand of Dryandra sessilis (Knight) Dômin may develop. These populations may in turn be severely damaged in wetter than normal years. Unlike Banksia grandis, they are not eliminated and, with time, again increase in density. In this phase of episodic pulsing of disease, the pathogen interacts with its hosts in a manner characteristic of endemic disease.

19.2.3 Mapping the extent and spread of disease Assessment of the location and extent of the disease is required for development of management strategies in native forests. The most extensive 451

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surveys, now totalling some 30,000 hectares per year, have been made in the E. marginata forests of Western Australia, principally in association with planning for hygienic access to uninfested areas for timber harvesting and mining exploration (see Chapter 20) and in several major National Parks. Figure 19.3 shows the distribution of the disease in south-west Western Australia as at 1976. Because of the occurrence of cryptic infestation ahead of symptom expression, it would be ideal if mapping could be based on the precise location of the boundaries between areas infested with the pathogen and those free of it. This requires direct mapping of the pathogen but is never practical in the wild because of problems of sampling and cost which relate to the very low levels of propagules of the pathogen usually present in soil. In a two-year sampling program during the wet years of 1965 to 1967, Ph. cinnamomi was recovered from only 10% of 650 samples, each about one kilogram, from the active disease invasion front in E. marginata forest (Podger 1968). In the drought year of 1972, only a single isolate was recovered from more than 500 samples from the E. marginata forests in the same general area (W.M. Blowes, unpubl. data). Because of cost, use of soil sampling in Western Australia is largely restricted to verification of doubtful evidence of symptoms, especially in association with planning for access to the forest for timber harvesting or bauxite mining (see Chapter 20). Unfortunately, for technical reasons, the more modern molecular and antigen techniques are limited to samples smaller than one gram. Consequently the costs are about three magnitudes more than for traditional methods. None of these molecular methods, although useful in research and survey in high value row crops, is affordable in wildland management. Delineation of boundaries in the field has devolved, therefore, to recognition of characteristic symptoms of the disease in plant communities (see section 19.2.1). Mapping uses various combinations of ground inspection and location with geographical positioning systems. A review of a range of remote sensing technologies, including Landsat imagery, for the detection of jarrah dieback is reported by Behn (1995). Standard technique is based on colour aerial photography at a scale of 1 to 4500 (Plate 19.1) under shadow-free conditions afforded by complete intermediate cloud cover. Techniques of aerial

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photographic interpretation and mapping of the distribution of disease symptoms were refined from 1 to 40,000 scale black-and-white film (Fig. 19.4) (Williamson 1973), and large scale 70 millimetre colour with requisite navigational systems (Bradshaw 1974; Bradshaw and Chandler 1978). Initially interpreters tended to overestimate the extent of infestation as most areas of high light reflectance in black and white and recently dead crowns of understorey were taken to be due to Ph. cinnamomi when, in some cases, these proved to be caused by other agencies (e.g. A. luteobubalina or drought). Therefore, the method requires adequate on-ground calibration of the photographic images. A further problem with the technique is that its use is sometimes limited by cost and by restricted opportunity for shadow-free photography. Despite the problems involved in measurement, the total area affected by Phytophthora root rot exceeds many hundreds of thousands of hectares in Western Australia, Victoria and Tasmania and tens of thousands of hectares in South Australia. An indicative map of distribution of damaged areas in south-west Western Australia is presented in Shearer and Tippett (1989) (Fig. 19.3). The 1982 estimate of Davison and Shearer (1989) of 250,000 hectares of damaged forest is now outdated and almost certainly conservative. However, these figures indicate the scale of the management problem. Repeated mapping of the extent of disease in certain regions is important for monitoring the rate and pattern of spread of disease. This is fundamental information for implementation of measures aimed at restricting further spread and protecting vulnerable plant communities (Havel 1979). Knowledge of the mode of dispersal of Ph. cinnamomi is critical for predicting disease spread. While local spread mainly involves dispersal of zoospores in moving water and spread of mycelium through roots, the most common long distance dispersal involves movement of infested soil (see Chapter 11). The relative importance of different dispersal agents has been equivocal. Among the numerous vectors, human transport of soil either deliberately or accidentally during road building and maintenance, timber harvesting and mineral exploration are the most important. The risk of establishing new centres of infestation is proportional to the population levels of

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Ph. cinnamomi in the soil at the point of pick up and the quantity of soil transferred. Survival, establishment and further epidemic increase depend upon conditions at the point of delivery especially freedom from desiccation and the availability of susceptible host tissue. In some circumstances, infested soil may be moved by animals (Brown 1976). This movement is likely to be greater on sticky clay soils and wet peats than on drier, welldrained soils of low organic matter content.

19.2.4 Rating forests for disease hazard and risk An important step in managing any disease in forests is to establish disease hazard ratings for particular parts of the forest so that management efforts can be directed at the most threatened communities. Based on topography, climate, presence of susceptible hosts, proximity to roads, geology of bedrock and soil type, it is possible to predict hazard posed by Ph. cinnamomi in some forests (Havel 1979). Detailed mapping of these factors in the E. marginata forest in Western Australia (Havel 1979; Shearer and Tippett 1989) and in the coastal mixed forests of eastern Victoria (Marks and Smith 1991) has enabled hazard ratings to be established. In eastern Victoria, the frequency of occurrence of the pathogen was found to be related to the intensity of forestry activity, internal soil drainage and soil temperatures (Marks et al. 1975). High altitude forests were found to be relatively free of disease even though they include many susceptible species (Neumann et al. 1981). Therefore, it has been possible to concentrate management action in the coastal and foothill forests most threatened by the disease. If hazard ratings can be established for a particular area of forest, these can be combined with ratings of the risk of spread or introduction of the pathogen to uninfested areas to give a sound basis for a practical disease management strategy (Shearer and Tippett 1989). Unfortunately hazard assessment systems have been difficult to develop in practice (F.D. Podger, unpubl. data). In the E. marginata forests, the risk of disease spread into an area has been determined from factors such as the proximity of the area to infested sites and whether it is downhill from those sites, its proximity to roads and the sort of human activity proposed for the area. A practical management outcome from such assessments has been the realignment of fire protection and walking tracks away from infested

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areas (Weste 1994) and restriction of access to vulnerable areas (see section 19.2.5).

19.2.5 Disease management options Development of responses by land management authorities to the presence of Ph. cinnamomi began in 1968 in Western Australia and soon followed in other States. Very substantial expenditures have occurred to: 1

understand the nature of the disease caused by Ph. cinnamomi

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evaluate the practicability of various control procedures

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plan strategic approaches to disease management

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formulate prescriptions for their delivery

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develop legislation to ensure authority exists to implement policies and to audit for compliance

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integrate disease management with other land use where legislation requiring multiple use and conservation of environmental values exists

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develop policies appropriate to the above aims and constraints.

These elements of management have been developed largely in parallel, with adjustment as knowledge, experience and changing sociopolitical considerations have required. With a disease as complex as the one caused by Ph. cinnamomi in native forests, there is rarely available a single clear and universally appropriate set of actions. Management of such a disease requires the choice of methods appropriate to local circumstances. Some methods have proved affordable and effective in management of high-value nurseries, row crops and orchards. Unfortunately very few have proved to be both practical and affordable in broadacre management of disease in native vegetation. Also, appropriate techniques for amelioration of the effects of established infection are usually not the same as those for constraining the further colonisation of native vegetation by the pathogen. In the following sections, the applicability to wildland management of various control options is briefly assessed. 19.2.5.1 Eradication attempts There have been several attempts to eradicate Ph. cinnamomi in Australian wildlands. The first

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unsuccessful experimental effort was reported from Victoria by Weste et al. (1973). An attempt to eradicate small roadside infestations of Ph. cinnamomi in a jarrah forest with applications of copper oxychloride was unsuccessful (Shea 1979a). A more optimistic report by Hill and Tippett (1989) from Western Australia, based on a large experiment in Banksia woodlands, suggested that eradication could be achieved inexpensively. It was recommended that eradication be attempted in small centres of infection newly recognised in areas predominantly free of the pathogen. This recommendation was based on the low cost of chemicals and took no account of the greater costs of survey, deployment of staff and associated costs in delivering the treatment. Examination of the experimental sites some years after the published report showed that success of the treatment was not sustained and severe disease broke out again in the treated areas and at their boundaries. 19.2.5.2 Containment of infestation within existing boundaries In the 1970s in Western Australia, a large experiment was conducted in which trenches were dug around the perimeter of a dieback affected patch (P.C. Kimber, unpubl. data; Shea 1979a). The experiment failed to contain spread, probably because the trenches did not sever the root connections in clays beneath the dense indurated cap rock (duricrust) and the roots of susceptible species that regenerated on silt washed into the trenches by heavy rain provided bridges between infested and uninfested areas. Other containment treatments tested in the jarrah forest included creation of zones of dead vegetation using herbicides, ploughing, planting of barriers of resistant species and the burning of windrows of cleared vegetation to create zones of high intensity fire (Shea 1979a). None effectively contained the pathogen. 19.2.5.3 Measures to reduce the activity of the pathogen Soil mounding and drainage proved vital to the establishment of plantations of Pinus radiata D.Don on infested and poorly drained sites in Western Australia and have also been effective in reestablishment of E. marginata on infested sites mined for bauxite in lateritic profiles (see Chapter 20). Clearly it is not compatible with management of wildlands. Roads and other sources of inoculum in

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native forests can be engineered to move water quickly in narrow channels away from areas to be protected or into sumps, as described in Chapter 20. Reduction of the food base available to the pathogen in dense stands of highly susceptible Banksia grandis is theoretically desirable where the objective is to protect eucalypt species (e.g. E. marginata) in which the average level of resistance is moderate (Shea 1979a, 1979b). Extensive operational experiments that reduced the stocking of Banksia grandis have provided only short-lived advantage. The method has not been applied on a broad scale (Shearer and Tippett 1989). The benefit of physical removal of larger banksias was negated by rapid growth of numerous small lignotuberous plants released from competition by removal of the larger plants (Burrows 1985). 19.2.5.4 Fire as a disease management tool Wildfire has been a feature of the Australian landscape to which the eucalypt dominated vegetation has adapted. During the twentieth century, the use of fuel reduction burns during the cooler, moister autumn and spring months has been an important management tool for reducing the frequency and intensity of severe wildfires in summer. The use of fire as a heat sterilant for eradication of Ph. cinnamomi from soil has been tested (Shea 1979a) and found to be ineffective for several reasons: 1

the insulating capacity of soils which prevents transmission of heat to the depths needed to eradicate the pathogen

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the barriers to heat transmission even at shallow depth afforded by rocks and the root systems and stems of trees

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the inadequacy of fuel quantities usually available even on land cleared for mining.

As a consequence, all that is achieved by such burning is a mosaic of soils sterilised to less than one metre depth and pockets of unaffected inoculum under rocks and trees from which reinvasion inevitably occurs. Even the most severe wildfires do not entirely cleanse areas of the pathogen. In contrast, in cool temperate rainforests of Tasmania where soils are normally too cool for zoospore formation, the loss of canopy cover and blackening of soil following fires allow solar heating of soils to temperatures favourable for zoospore

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formation and infection. It has been argued (e.g. Shea 1979a) that fuel reduction burns in the dieback affected forests increase soil temperature and reduce microbial activity as a result of removal of shrubby ground cover and leaf litter, with the result that activity of Ph. cinnamomi is increased. In the E. marginata forests, however, the epidemic seems insensitive to variation in both time since last burn (from one to 80 years) and fine fuel loads (from one to 20 t/ha) (F.D. Podger and N. Burrows, unpubl. data). Considerable effort has been focused on the prospect of control of Ph. cinnamomi by the use of fire to decrease the food base for the pathogen in Banksia grandis understoreys and to promote field resistant Acacia species, some of which are antagonistic to Ph. cinnamomi (Shea 1979a). It was also observed that in forests subject to regular ‘cool’ fuel reduction burns, the understorey was dominated by the Phytophthora-susceptible Banksia grandis, while after severe wildfire the niche was occupied by Acacia species, in which germination of buried seed is stimulated by the heat of the more intense fire. Under Banksia grandis, the population of Ph. cinnamomi tended to be high while under Acacia species the population was low. The intensity of fire required both to kill Banksia grandis, which is relatively fire resistant and a vigorous resprouter, and to stimulate the germination of Acacia seed, usually stored deeply in the soil by ants, proved to be both unmanageable and severely damaging to the E. marginata overstorey. The maintenance of naturally accumulated loads of litter, theoretically conducive to microbial diversity, proved to have no effect on the advance of Ph. cinnamomi or the extent of its deleterious effects on the understorey in the E. marginata forests (F.D. Podger and N. Burrows, unpubl. data). Moreover, organic matter content in E. marginata forests was not significantly reduced by regular fuel reduction burns (Hatch 1959) and high levels of sporangia production by the pathogen occurred in forest soils with a seven-year accumulation of litter (Shea et al. 1978). Therefore, this approach to disease management has not been applied operationally (Shearer and Tippett 1989). 9.2.5.5

Biological control

The literature records examples of lysis, predation and parasitism of Ph. cinnamomi by a range of

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organisms (Malajczuk 1979b; Old and Oros 1980; Nesbitt et al. 1981; Postle et al. 1986) mostly in vitro. Increases in microbial antagonism to Ph. cinnamomi and in vigour of root regeneration contributes to control of root rot following extravagant additions of organic matter and fertilisers to the soil in infested avocado groves (Broadbent and Baker 1974). There may be an element of biological control in this management regime; however, its effectiveness probably rests on an integration of numerous physical and microbiological factors which improve regeneration of the new root systems following feeder root necrosis and contain progress of infection within the smaller roots. The quantities of organics and fertilisers used in avocado orchards will never be available nor their delivery affordable or desirable in native forests. Although it might be possible to transfer antagonistic microbes, presumed to be effective in controlling the level of activity of the pathogen in areas of low impact, to places where the pathogen is damaging (Malajczuk 1979a, 1983; Shearer and Tippett 1989), such an approach is unlikely to be successful. Where biological control of Ph. cinnamomi is evident (e.g. in mountain kraznozem soils in Victoria; Marks and Smith 1981) the effect is probably a result of several biological and physical (e.g. cold) agents rather than to any dominant species among the numerous microbes known to have deleterious effects on the pathogen. The dieback suppressive mountain soils in Victoria have microbial populations several orders of magnitude greater than those in conducive soils (Weste and Vithanage 1978). However, the role of these organisms in contributing to control of Ph. cinnamomi in areas of low impact of the pathogen in native forests, as against the effects of the environment and plant resistance, remains equivocal. Furthermore, any proposal to import and disseminate exotic biological agents will need to meet strict tests to prove that there will be no deleterious effects on any elements of the native biota. Another potential problem is the fitness of such organisms to compete with indigenous organisms, particularly in the harsh soil environments so conducive to Ph. cinnamomi. While such organisms might contribute in some degree to attenuation of the deleterious activity of the pathogen in areas already infested, it is much more difficult to envisage how biological antagonists specific to Ph. cinnamomi might be

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deployed ahead of or at the invasion front. There is no evidence of autonomous movement of indigenous putative agents of biological control from susceptible communities on non-conducive sites to their susceptible neighbours on conducive sites in native eucalypt forests, even where the latter are downslope of the former. In the seminal work of Marx (1972) with Pinus, particular ectomycorrhizas provided physical and chemical barriers to infection by Ph. cinnamomi. This possibility was explored for species of Eucalyptus by Malajczuk (1988) and Malajczuk and Hingston (1981). Unfortunately, there were serious practical difficulties involved in sustaining in the field particular protective ectomycorrhizal symbioses beyond the first year after their synthesis in the nursery. This was due, apparently, to displacement of the protective mycorrhizas by native ectomycorrhizal fungi which do not confer the same level of protection against Ph. cinnamomi. Furthermore, Ph. cinnamomi is able to infect newly initiated roots ahead of complete mycorrhizal colonisation of the roots. 9.2.5.6

Chemical treatment of infected plants

The use of fungicides on a broad scale in native forests is prohibitive on the basis of cost and on ecological and conservation grounds, even for those shown to be effective in controlling Ph. cinnamomi root rot in eucalypts (Shearer and Tippett 1989). Far more encouraging is the use of the relatively cheap inorganic salt, potassium phosphonate (phosphorous acid partly neutralised with potassium hydroxide). It is the only affordable and benign chemical treatment yet devised for use against Ph. cinnamomi in native vegetation (Shearer and Tippett 1989). Phosphonate combines several very desirable properties. It is nontoxic with a complex mode of action in the plant, involving slight inhibition of the pathogenesis of the invading fungus and consequent enhancment of the resistance of the plant (Smillie et al. 1989; Guest and Grant 1991). It is effective in protecting plants when injected or sprayed on the foliage at low dosages (Pegg et al. 1990; El-Hamalawi and Menge 1995). Its effect is highly persistent, sometimes lasting several years after an initial dose or two. It has very low mammalian toxicity and is converted rapidly in soil into naturally occurring compounds. Finally, it can be effectively applied as low volume aerosols by

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hand or by micronair application from low flying aircraft or helicopters. The one disadvantage to the use of phosphonate appears to be some phytotoxicity if used at levels above the tolerances of particular plant species, although these effects are seldom lethal (Pilbeam et al. 2000). Because significant variation between plant species in tolerance to the chemical has been reported, uniform prescriptions for entire communities may not be possible (Komorek and Shearer 1997). For this reason and those of cost of application, its principal use is likely to be on threatened populations of selected species which are listed as rare or in danger of extinction (Pilbeam et al. 2000). Land managers in Western Australia are developing schedules and methods, including aerial application, for treatment of populations and species in the field (Shearer and Tippett 1989). The prospective use of phosphonate to delay the advance of the epidemic at the upslope boundaries with healthy forest is under consideration. The expectation is that protection of plants by phosphonate will deny to Ph. cinnamomi the sheltered environment for mycelial growth in the root systems of Banksia, thereby protecting the eucalypt overstorey. 19.2.5.7 Use of resistant eucalypts There is a very clear distinction between eucalypt taxa that are highly resistant to dieback caused by Ph. cinnamomi (particularly the genus Corymbia and the major Eucalyptus subgenus, Symphyomyrtus) and taxa regarded as susceptible (mainly in the Eucalyptus subgenus, Monocalyptus—although in the field susceptibility to lethal disease is much less common than in pot trials) (Marks et al. 1972; Podger 1973). Among Monocalyptus species there is also a clear variation in the degree of susceptibility. For example, E. marginata and E. sieberi are highly susceptible, while other stringybark species are somewhat less susceptible. Therefore, an important consideration in management of lowland eucalypt forests, which often consist of a mixture of species from these eucalypt subgenera, is maintenance of the natural, adapted mixture of species. Silvicultural practices that favour the regeneration of susceptible species may increase the vulnerability of the forest to damage by Ph. cinnamomi. This may have occurred already in the coastal forest of East Gippsland with the selective logging of Symphyomyrtus species

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during the early decades of exploitation of these forests, resulting in forests dominated by the more susceptible E. sieberi and stringybarks (G.C. Marks, pers. comm.). In the field, there is strong circumstantial evidence of variable resistance within many eucalypt species regarded as generally susceptible. The most extensively studied resistance is that in E. marginata in which a considerable range of resistance has been demonstrated and has been shown to be continuously variable and additively inherited (Stukely and Crane 1994). However, there is a strong interaction between resistance and the environment in disease expression. Thus, the proportion of the host population in which resistance is sufficient to ward off further progress of disease following first infection decreases as conditions become more favourable to the pathogen. This is reflected in both variable rates of mortality depending on hazard of the site and sudden mortality following high summer rainfall events of trees which had survived for many years after first arrival of the pathogen. The recognition of the existence of resistance in E. marginata has been followed by vegetative propagation of resistant lines and the establishment of seed orchards to produce resistant seedlings. The progeny will be used principally in the rehabilitation of bauxite pits (see Chapter 20). It should also be possible to establish resistant E. marginata seedlings more widely on the very fractious graveyard sites in the broader forest and, possibly, to initiate natural recolonisation of affected areas from resistant plantings. Natural selection of resistant genotypes may have been involved in rehabilitation of diebackaffected sites in eastern Victoria, although this has yet to be demonstrated experimentally. 19.2.5.8 Rehabilitation Early attempts to reforest the graveyard sites in Western Australia using commercial timber species of exotic origin have not proved viable. Attempts to improve drainage using heavy machinery to rip the duricrust have been disappointing. However, efforts to restore native forests on dieback sites in Victoria have been much more encouraging (Marks and Smith 1991). This program has been based on the following three expectations. 1

Once the advancing edge of disease has removed the food base for the pathogen provided by the

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most highly susceptible elements of the vegetation, the damaged sites will not support high populations of the pathogen, as has been shown in a dry sclerophyll forest with understorey dominated by Xanthorrhoea australis (Duncan and Keane 1996; Weste et al. 1999). 2

Regeneration practices involving clearfelling, mechanical disturbance or burning of the site and seeding with a mixture of eucalypt species indigenous to the site lead to establishment of high densities of rapidly growing eucalypt and Acacia seedlings, resulting in increased transpiration of water by the vegetation. Soils under largely undisturbed mature and overmature forest tend to become saturated readily. Densely stocked vigorous regrowth tends to become somewhat drier, which mitigates against activity of the pathogen both in the soil and in the host (Smith and Marks 1986).

3

Establishment of high densities of eucalypt seedlings of a mixture of species (both resistant and susceptible) will allow selection of types that have a degree of resistance to the pathogen.

Twenty years of experience with field trials and regeneration of dieback sites have shown that restocking of these sites, even with a susceptible species such as E. sieberi, is possible. However, it has not yet been established that the regeneration will withstand the pressure of extraordinarily wet years which in eastern Victoria occur on average every 15 years and are thought to have resulted in outbreaks of dieback in the past (Tregonning and Fagg 1984). There is also no clear evidence that the improved circumstances will promote the re-establishment of highly susceptible understorey species. However, the incidence and severity of disease in young rapidly growing forests that have developed following clearfelling appear to be much less than in older forests subject to selective logging and thinning. In some vulnerable Victorian forests, selective logging and thinning have been suspended and drainage controlled as part of a disease management strategy (Weste and Marks 1987). 19.2.5.9 Reduction of vectored dispersal Scientists and land managers in Western Australia have found that the only practical options for disease management are actions related to quarantine and

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hygiene (Underwood and Murch 1984). Generally, only that part of the vectored dispersal of Ph. cinnamomi that results from human activity is amenable to change. This can be approached in two ways: to reduce the area over which human movement occurs and to ensure that entry to uninfested areas is conducted so that transfer of the pathogen to such areas is minimised (hygiene). In the late 1960s, two actions were recommended for application in the E. marginata forest with the aim of achieving the first objective (F.D. Podger, unpubl. data). 1

The use of gravel obtained from dieback-affected areas for road construction through uninfested areas was banned. This constraint applies to gravels in which plants are rooted but not to crushed rock or river gravels. Clearly the relatively few sources of uninfested gravels should not be wasted on infested areas.

2

The lower per hectare yielding silvicultural system of group selection was replaced. Clearcutting in contiguous blocks was recommended so that the annual timber supply commitment could be obtained from the smallest possible area, the opportunity for quarantine of uninfested forests was maximised, and risk of failure of hygiene systems was minimised.

The first arm of this strategy has been sustained. The second has been overwhelmed by pressures associated with increasing practice of multiple use of forests to meet aesthetic, stream protection, conservation and habitat requirements. These pressures have led to a need to extend annual timber harvesting, necessary to honor contractual arrangements, over increasingly large areas of land. As a consequence, the cost of quarantine and the risk of spread of the pathogen to uninfested areas has been increased considerably. In Western Australia, large areas of apparently disease free forest are gazetted as ‘Disease Risk Areas’. Access is excluded except on a permit system for hygienic entry. Subsequently it has become evident that judgments as to the disease status of some areas of forest were based on a precautionary approach in the absence of reliable survey data. The implementation of hygienic access has involved imposition of controls on a wide array of activities in the forest. For example, access for suppression of

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wildfires and fuel reduction burning is controlled and waters used in fire suppression are treated to eliminate Ph. cinnamomi. Road building and maintenance programs involve demarcation of boundaries between infested and uninfested areas and associated cleaning of heavy earth-moving machinery. Timber havesting and mining equipment (see Chapter 20) is washed down on entry to uninfested areas and access to uninfested areas is denied when soils are likely to be picked up from timber harvest coupes and spread further within them. This requires an elaborate and protracted system of mapping and demarcation in planning access of heavy equipment so that inadvertent movement of machinery from uninfested into infested areas and back is kept to a minimum. Barriers, accompanied by signs with direct and unequivocal messages, are used to exclude access from infested to uninfested areas. For sound management of hygienic access to uninfested areas, it is necessary to delineate, map and mark boundaries between infested and uninfested areas. Once the field interpretation of boundaries for hygienic operations is completed, lines are marked inside the adjacent healthy vegetation with flagging tapes at distances appropriate to circumstance, usually about 15 metres upslope and a greater distance downslope to account for cryptic infections and the hydrological characteristics of the land. The application of hygienic access to forests for the purposes of harvesting and other silvicultural operations is extremely complex. Of the 64 managerial steps involved over three or more years, 32 require movement of humans on the ground, and each of these activities must be conducted hygienically to reduce the risk of infestation of pathogen-free areas. Guidelines for control of Ph. cinnamomi in forested public lands in Victoria are outlined in forest management plans based on a threat evaluation for specific areas. These plans combine a knowledge of the susceptibility of components of the communities, the terrain as it determines vulnerability of the forest and the risk of introduction of the pathogen. These guidelines focus on protection of uninfested lands through reduction of the frequency of vectored spread of infested material and involve requirements for planning access, hygienic access requiring washdown of machinery before entry, testing to

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ensure infested gravels are not used in pathogen-free areas, exclusion of access (quarantine) and signage (I.W. Smith, pers. comm.). Throughout eastern Tasmania, the distribution of infested vegetation is related almost constantly to human movement, particularly involving heavy machinery. The peaty soils of western Tasmania and the heavy clays of much of the high rainfall areas of south-west and north-west Tasmania are highly conducive to transfer on bushwalkers’ boots and by native fauna. While there are detailed management plans for Ph. cinnamomi in the Tasmanian Wilderness World Heritage Area and State Forests, prescriptions are generally applied on a case-by-case basis as proposals for development or access are lodged. The requirements of conservation and hygienic access constrain commercial activity and add to its costs in several ways. Mineral exploration access and operations are scheduled so that hygienic entry to uninfested areas is completed ahead of entry to adjacent infested areas. Cleaning of small items (e.g. boots, tools, helicopter skids) is required. For larger items this procedure needs to be followed by use of a chemical spray to sterilise soil lodged in places difficult to access with high pressure sprays. With a few localised exceptions, including Kangaroo Island, SA, mapping the boundaries of infestations elsewhere in Australia is more difficult than in the E. marginata forest and in many cases is not feasible. In most regions, the interface between infested and non-infested areas is hundreds of thousands of kilometres and the precise definition of the location of interfaces, so necessary to ensure hygienic movement between infested and non-infested areas, is not everywhere practicable. Furthermore, control of unlawful destruction of barriers and illegal entry to quarantined areas appears to be extremely difficult over large areas of wildlands. Public education in relation to the implementation of quarantine and hygiene measures has been more extensively addressed in Western Australia than elsewhere. Considerable expenditure has been directed at the use of audiovisual instruction kits and school visits. The development of regional coordination groups is being encouraged to promote good hygiene practice among those industries, local government and other organisations that use the forests. Policy advice to government is provided by the independent Dieback Consultative Council.

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In the severely affected States, management responses to the problem have involved constraint of access to public lands. The number of stakeholders (e.g. public institutions, private enterprises, citizen interest groups) whose activities must be constrained is extraordinarily large, and this creates problems for implementation of the strategy. Even if measures to eliminate the inadvertent vectoring by humans prove to be successful, there appears to be no prospect of affordable interference with autonomous spread on any significant scale. Both passive dispersal and vectored spread resulting from uncontrollable movement of soil by feral and native fauna also seem to be beyond realistic address. In the implementation of hygiene measures, a clear distinction needs to be made between abatement of further epidemic colonisation by Ph. cinnamomi and abatement of the deleterious effects in places where the pathogen is already established. There would seem to be little prospect of abatement of the existing disease caused by Ph. cinnamomi in most of the places already colonised. The exceptions appear to be: 1

the prospect of protective chemical treatment with phosphonate of those small parts of the conservation estate which are rare and threatened

2

major amelioration of hazard by physical alteration of soil structure to remove impervious layers (as occurs in bauxine mining, see Chapter 20)

3

use of strategically placed barriers to drainage such as those employed in association with bauxite mining and subsequent restoration of native vegetation in Western Australia (see Chapter 20)

4

reversal of rising watertables associated with excessive land clearance by replanting with vigorous and rapidly transpiring trees in parts of catchments above the threatened populations— an understanding of the hillslope hydrological cycle is important in attempting to manipulate the soil water environment in a way that disfavours the pathogen and favours the host (Shearer and Tippett 1989).

5

rehabilitation of dieback sites in eastern Victoria associated with clearfelling of old, diseased forest and establishment of a vigorous young

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forest by replanting with mixtures of the eucalypt species previously growing on the site, including resistant species (see section 19.2.5.8). Until recently it has been argued within land management agencies that their purpose should be to prevent any further spread of the pathogen, an aim since shown to be unattainable (Podger et al. 1996). At the other extreme, pessimists have argued a case for viewing the epidemic as an expression of an irreversible evolutionary process on which no public resource should be expended because efforts will inevitably be doomed to failure. Neither of these approaches is likely to attract widespread support in the community. A policy which embraces both realism and a rational degree of optimism is based on the hope that abatement of the human vectored spread of the pathogen will delay the epidemic and allow time for scientific advance to provide a general solution. Such a solution is not yet in prospect. This policy implies that such resources as are available should be directed to those areas which are most likely to remain free of infestation in the longer term. It will also require that resources are not wasted on futile exercises on unprotectable areas under imminent threat. This policy, recently adopted in Western Australia following the recommendations of the W.A. Dieback Review Panel (Podger et al. 1996), requires identification of areas that are: 1

free of infestation

2

significant for conservation either as single purpose reserves or for other multiple land uses

3

so located topographically that they are unlikely to be entirely colonised by autonomous spread of the pathogen in some definable medium-term time frame

4

physically amenable to affordable and socially acceptable constraints on human access and are not likely to be vulnerable to early infestation by the actions of other uncontrollable vectors.

A necessary corollary is that resources should not be expended in constraints of legitimate access where such constraints offer only short-term benefit at considerable expense and cost to longer term protection of protectable areas elsewhere. Measures to evaluate the extent to which any one area of uninfested vegetation meets these criteria and,

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therefore, can be deemed ‘protectable’ are being developed (K. Vear and F.D. Podger, pers. comm.). Unless novel and inexpensive solutions emerge, it is to be expected that the autonomous colonisation of native vegetation by Ph. cinnamomi will continue and the pathogen will come eventually to occupy all environments suitable for its survival whether or not those environments are conducive to the development of severe disease. Given these considerations, the disease management strategies appropriate to particular regions will range from no action, to various combinations of quarantining of ‘protectable’ areas, restriction of access between infested areas and protectable areas, use of phosphonate to protect selected susceptible species in infested stands and the rehabilitation of damaged areas based on planting or natural selection of resistant eucalypt genotypes and on regeneration of vigorously growing stands which remove water from the soil and reduce pathogen activity.

19.3 Management of dieback diseases of complex etiology Across the forests and woodlands of southern Australia there is a range of dieback diseases of complex etiology that must be addressed in vegetation management (see Chapter 17). Some appear to result from unusual weather. Regrowth dieback in tall E. obliqua and E. regnans forests of the high rainfall zone (>1000 mm) in southern Tasmania, first observed in 1956 (Bowling and McLeod 1968), has affected some thousands of hectares of stands which regenerated after harvest of virgin forests from the 1860s (Podger et al. 1980) (see Chapter 17). Several species of wood rotting fungi, including Armillaria species, are believed to be secondary agents of decline (Kile 1980, 1981) following damage by an unusually protracted drought. The drought closely preceded the first recorded evidence of loss of vigour in permanent growth plots (West 1979). Gully dieback on the eastern slopes of the north-east highlands in Tasmania was first observed in 1962 on several thousand hectares in tall open E. obliqua forest in gullies of the intermediate rainfall zone (see Chapter 17). While A. luteobubalina is commonly associated with the problem (C.A. Palzer, pers. comm.), it appears that this disease was triggered by an extremely rare, protracted drought immediately prior

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to its first notice (C.A. Palzer, unpubl. data). There is little that can be done to manage these problems, although an understanding of their cause has allowed their effect to be included in the planning of forest management and broader managment strategies (Wardlaw 1989). Early recognition of their occurrence is important in implementation of salvage logging to reduce their economic effect. Other dieback problems are a consequence of natural successional processes in the vegetation. High altitude dieback occurs over thousands of hectares on the plateaux above 800 metres in the north-east and north-west of Tasmania. It begins as a slow decline and dieback of E. delegatensis in the middle stages of succession toward temperate rainforest (see Chapter 17). In long unburnt stands, the eucalypt is eliminated and replaced by callidendrous closed rainforest dominated by Nothofagus cunninghamii (Hook.) Oerst. in a sequence consistent with the successional theory of Jackson (1968). The decline was reversed following burning to remove the fire intolerant understorey (Ellis 1964, 1981; Ellis et al. 1980). A decline in semi-mature and mature forests of E. obliqua and E. regnans over a developing rainforest understorey in Tasmania is a low elevation analog of high altitude dieback except that there is a strong association with the native leaf spotting fungus Aulographina eucalypti (Cooke & Massee) Arx & E.Müll. (Palzer 1978). It is known only from the fog-prone valley bottoms and slopes of the Calder and Ingliss River valleys of north-west Tasmania. In these situations it is clear that fire management is the key to the problem. If the forests are to be managed mainly for wood production, regular burning or regular clearfelling and burning is required to maintain the dominance of the eucalypt overstorey. If they are to be managed mainly for conservation, it will be necessary to decide what is being conserved and to manage the forests accordingly—if the objective is to conserve tall eucalypt forests, the forests will have to be managed as for production forests; if to conserve the natural successional processes and temperate rainforests, nature should be allowed to take its course, resulting in continued dieback and decline of the eucalypts and their gradual replacement by temperate rainforest elements. Thought will have to be given to where and in what proportions these conservation communities will be maintained in a shifting mosaic.

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Yet other dieback diseases are a consequence of human disruption of the natural vegetation (see Chapter 17). A widespread decline and dieback of remnant eucalypts occurs in pastoral areas of the high rainfall zone in south-west, south-east and eastern Australia. These declines have been generally known as rural dieback and the best known has been dubbed ‘New England dieback’ because of its widespread occurrence on the New England Tableland in northern New South Wales (see Chapter 17). The trees suffer repeated episodes of defoliation, appear unthrifty and may eventually die. Often, the trees have heavy infestations of mistletoe (see Chapter 15). These syndromes are associated with excessive and repeated damage by defoliating insects, but the factors leading to this situation are complex. Trees of remnant woodlands used for farming and grazing may be stressed as a result of changes to the edaphic environment, increased physical exposure or old age, and may be less able to replace foliage lost to defoliators (Landsberg and Wylie 1988). In some areas, clearing of a large proportion of trees and establishment of improved pastures has resulted in increased abundance of certain insects such as scarabs whose larvae damage the roots of the remaining trees (Roberts et al. 1982). Lack of diversity in the remnant woodlands has reduced the diversity and abundance of natural predators of defoliating insects, allowing their numbers to increase to destructive levels (Davidson 1980). Increased levels of soluble nitrogen and phosphorus that have resulted from planting introduced leguminous pasture species and application of phosphate fertiliser have increased the nutrient levels of tree foliage, allowing increased abundance of defoliating insects (Landsberg 1988). While Landsberg et al. (1990) concluded that the last explanation best fitted the observed patterns of dieback and insect damage, all of the factors are interrelated and, depending on the locality and particular situation, may contribute to the onset of dieback. Over large areas of south-east and south-west Australia, excessive clearing of deep-rooted native forest and woodland has resulted in a rise in the watertable, bringing saline water into the root zone, greatly reducing the productivity of the land, and causing salt-induced dieback in remnant eucalypts. A tree decline in Tasmania has developed to serious proportions in the last few decades in the open

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TA B LE 1 9 . 1

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Eucalypts recorded as exhibiting symptoms of ‘Mundulla yellows’ in semimature and mature trees in modified landscapes in several temperate regions of southern Australia

Regions: SA, South Australia; NSWH, Hunter Valley to Mudgee, New South Wales; NSWS, Wollongong South Coast, New South Wales; WA, Western Australia Swan Coastal Plain Guilderton to Bunbury. Numbers 1 to 6 represent sources of unpublished data: 1, G. Cotton; 2, D. Paton; 3, D. Hart; 4, J. Simpson and F. Podger; 5, J. Simpson; 6, F. Podger.

Species

SA

NSWH

NSWS

4

Angophora floribunda

6

Corymbia calophylla Corymbia calophylla var. rosea

3 EC

A

6 EC

Corymbia maculata

4

Eucalyptus amplifolia

4

Eucalyptus baxteri

1 6 EC

Eucalyptus botryoides Eucalyptus camaldulensis

1, 2

Eucalyptus cladocalyx

1, 2 6 EC

Eucalyptus conferruminata 4

Eucalyptus crebra Eucalyptus diversifolia

1

Eucalyptus fasciculosa

1, 2

Eucalyptus foecunda

1 EC

Eucalyptus globulus

1 EC

Eucalyptus incrassata

1, 2

Eucalyptus largiflorens

1

Eucalyptus leptophylla

2

Eucalyptus leucoxylon

1, 2

Eucalyptus mannifera ssp. maculosa

4 6

Eucalyptus marginata Eucalyptus microcarpa

1

Eucalyptus obliqua

1

Eucalyptus odorata

1 4

Eucalyptus paniculata Eucalyptus platypus

3 EC 5

Eucalyptus pilularis Eucalyptus porosa

1

Eucalyptus rugosa

1

Eucalyptus saligna

4

Eucalyptus sclerophylla

4

Eucalyptus steedmanii Eucalyptus tereticornis

1 EC 4

Eucalyptus todtiana A

EC, in exotic cultivation, otherwise in naturally occurring specimens in partially cleared woodland and forests.

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WA

6

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Change between 1994 and 1999 in the percentages of trees exhibiting symptoms of ‘Mundulla yellows’ for each of five disease classes among a sample of 475 individual eucalypt trees

Figures are derived from unpublished data of D.C. Paton and J. Cutten for dominantly mature trees in partly cleared forest in the upper south-east of South Australia—Eucalyptus camaldulensis, 245 individuals; E. incrassata, 78; E. fasciculosa, 77; E. leucoxylon, 66; E. leptophylla, 9. Disease rating—0, symptom free; 4, dead.

Disease rating 0

1

2

3

4

1994

26

14

21

18

11

1999

4

33

23

16

23

TAB LE 19 . 3

Average disease ratings (0 to 4) and percentage mortality assessed in 1994 and 1999 for each of five species of Eucalyptus with symptoms of ‘Mundulla yellows’ in the upper south-east of South Australia (derived from unpublished data of D.C. Paton and J. Cutten) 1994

1995

Species

No. of trees

Average disease rating

Mortality (%)

Average disease rating

Mortality (%)

E. camaldulensis

245

2.0

20

2.5

35

E. incrassata

78

1.5

3

2.3

19

E. fasciculosa

77

1.3

0

1.7

4

E. leucoxylon

66

1.7

3

1.9

6

E. leptophylla

9

1.0

0

2.3

33

woodland of partially cleared land in the low rainfall zone of the midlands. The decline is linked to drought and is associated with an increase in browsing pressure of possums (Trichosurus vulpecula). Recovery of the crowns has followed placement of metal sleeves on the lower stems to deny possums access to the crown. In the south-east of South Australia, the widespread decline and death of eucalypts associated with characteristic leaf symptoms (interveinal chlorosis), referred to as ‘Mundulla yellows’ (Plate 19.2), is of great concern (Cotton 1998). There is an urgent need to resolve the cause of this disease which affects many eucalypt species of all age classes across extensive rural landscapes (Table 19.1 and Plates 19.3 and 19.4). In the upper south-east of South Australia, there has been a dramatic increase in numbers of trees exhibiting high levels of disease severity and mortality (Tables 19.2 and 19.3). Preliminary evidence indicates that a phytoplasma or virus might may be involved (Randles 1999).

A general hypothesis of cause, which is useful in devising management strategies for rural dieback, is that disease is the result of disruption of natural balances among native eucalypt species and dependent herbivores and parasites following excessive clearing of native vegetation and changes to the soil environment associated with the development of farming and grazing. Recent evidence of a resurgence of eucalypt regeneration in the Northern Tablelands of New South Wales, coincident with a reduction in stocking levels and fertiliser applications after a downturn in the profitability of grazing, is consistent with this hypothesis. On this analysis, active measures to manage the syndrome could involve a moratorium on further clearing of native vegetation on farming and grazing land and exclusion of remnant areas of woodland (e.g. corners of paddocks, roadsides, land around buildings, unproductive paddocks, public land) from further heavy grazing and fertilisation. Many farmers, realising that they are losing a source of shelter for livestock and crops and one of the most

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attractive features of the landscape, are now protecting remnant woodlands and replanting native vegetation. Ideally, seed for this purpose is collected from a range of the local, adapted remnant eucalypts and associated genera (especially Acacia). The planting of many seedlings provides an opportunity for further selection of locally adapted types, including selection for resistance to the defoliating insects that tend to cause excessive damage. There is a degree of variation in resistance to these insects among species such as E. camaldulensis and E. melliodora, based upon variation in foliar content of particular oils and flavonoids (Edwards et al. 1990; Stone and Bacon 1994). Species of Corymbia (e.g. C. citriodora and C. maculata) introduced from New South Wales are highly resistant to the main local species of psyllid in the Melbourne region. Such nonlocal species may be necessary to initiate revegetation in certain circumstances. Seedlings derived from selected resistant trees could be used to restore badly affected areas. In salt-affected areas, planting of salt tolerant species of eucalypts may be required initially to lower the water table and allow the establishment of a range of species indigenous to the site. However, planting of too narrow a range of genotypes selected on the basis of only one character should be avoided. What is required in this situation is a restoration of the functional processes of natural regeneration and adaptation, on a sufficient scale, to ensure that stable, self-perpetuating communities result. Mistletoe populations are an important cause of decline and death in woodlands across the agricultural lands of southern Australia (see Chapter 15). In the first instance, direct control measures, including lopping of heavily infected branches, pollarding of heavily infected trees and trunk injection with selective herbicides (Minko and Fagg 1989), may be necessary to reduce heavy infestations. In the long term, the general restoration of reasonably large areas of natural vegetation is likely to result in a reduction in mistletoe infestation. Younger trees and trees within larger stands are less prone to excessive mistletoe infestation than the isolated, overmature trees that are typical of many current rural landscapes. Selection of mistletoeresistant genotypes, based on lower levels of infection of individual trees evident in heavily infested stands, will be an important aspect of the careful selection of locally adapted eucalypt genotypes for revegetation of rural lands.

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19.4 Management of root rot caused by Armillaria luteobubalina Several thousand hectares of low elevation, mixed species eucalypt forest in south-east Australia and E. diversicolor forest in south-west Australia are seriously affected by A. luteobubalina, which infects the woody roots of the trees and kills small patches of forest (see Chapter 12) (Edgar et al. 1976; Kile 1981; Shearer and Tippett 1988; Shearer et al. 1997). In E. diversicolor forest it damages both regeneration established after harvest and retained trees in selectively cut stands (Pearce et al. 1986; Shearer and Tippett 1988). Management options for A. luteobubalina are affected by it being an indigenous component of the south-east and southwest eucalypt forests, having an intimate association with the trees and being distributed widely in the forests (not always in association with disease). Although there is evidence of its pathogenic activity in unlogged eucalypt forests (Kile 1983), the most severe disease in central Victoria occurred in forests subjected to repeated selection cutting of the larger trees (Edgar et al. 1976). The stumps are colonised by the fungus within three to four years of cutting (Kile 1981) and provide a high inoculum potential for infection of adjacent trees, resulting in foci of disease around the infected stumps. The damaging effects of A. luteobubalina contrast with the benign occurrence of two related species, Armillaria hinnulea Kile & Watling and Armillaria novaezelandiae (G.Stev.) Herink, which are ubiquitous as epiphytic rhizomorphs or occur in restricted lesions on the root systems of eucalypts in wetter forests in Tasmania but cause little mortality, even after logging or wildfire results in extensive root and stump invasion among regenerating trees (Kile et al. 1991). Initially, management of Armillaria-affected stands of eucalypts involved repeated salvage of dead or dying trees (Kellas et al. 1997). However, it was considered that this practice may have increased the likelihood of infection of remaining trees by increasing the food base for the pathogen. One of the most commonly advocated methods for control of Armillaria in orchards, forests and plantations has been the physical removal of stumps and large roots to deny the pathogen a food base and roots (Roth et al. 1980). Experimental removal of stumps and roots by pushing over trees with a bulldozer and by

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ripping to a depth of 60 to 90 centimetres was not effective over the first 18 years in reducing mortality due to A. luteobubalina in three species (E. obliqua, E. globulus ssp. bicostata, Pinus radiata) planted on high disease hazard sites in a central Victorian forest (Kellas et al. 1997). Also there have been attempts to reduce the chance of contact between healthy trees and inoculum built up in the stumps and roots remaining after logging by changing from selective logging to clearfelling of larger areas (Kile et al. 1982). Although Kellas et al. (1987) concluded that frequency rather than intensity of cutting affected disease incidence, the high intensity fires used to clear debris and prepare the seedbed following clearfelling may reduce the effect of Armillaria (Kile 1980, 1981). In an experimental planting on a high hazard site in central Victoria, mortality caused by Armillaria was about 14% in E. obliqua compared with only 2% in E. globulus ssp. bicostata (Kellas et al. 1997). It appears, therefore, that there is variation in susceptibility of eucalypt species to Armillaria and this must be borne in mind during silvicultural operations (Benjamin and Newhook 1984). A shift from the natural mixture of indigenous species to dominance by more susceptible species as a result of silvicultural operations could result in increased incidence of disease. However, management practices that increase the occurrence of more resistant species could reduce the incidence of disease in high hazard sites. Use of seed sources from locally adapted species with a degree of resistance to the disease is a general recommendation for management of Armillaria disease of conifers in the north-west United States of America and western Canada (Hagle and Shaw 1991) and a similar precaution is probably advisable in eucalypt forests in southern Australia. There is also general acceptance that stresses in trees predispose them to development of Armillaria root rot, even in situations where the fungus is an aggressive primary pathogen (Wargo and Harrington 1991). The intensification of the disease following partial cutting (Edgar et al. 1976) may be related to the phenomenon of ‘thinning shock’ as well as to an increase in inoculum in the cut stumps (Wargo and Harrington 1991). Armillaria luteobubalina is associated with gully dieback in the north-east highlands in Tasmania, which is thought to be primarily caused by drought (see Chapter 17). Since A. luteobubalina is a native component of the

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affected eucalypt forests, Florence (1996) has postulated that the outbreaks of patch deaths caused by the fungus in recent decades are fundamentally due to disturbance of the natural ecological processes in the forests, resulting in increased activity of the pathogen or reduced resistance of the host trees. Maintenance of natural ecological and evolutionary processes and functional diversity is essential for general health of the forests and is likely to be important in management of Armillaria root rot. Unless A. luteobubalina can invade stumps within three to four years of cutting, it is excluded as a result of colonisation of the stumps by saprobic microorganisms (Kile 1981). Competitive colonisation of stumps and roots has long been advocated as a means of reducing the inoculum potential of root rot pathogens of trees, and one of the earliest biological control treatments—control in Britain of root rot of pine caused by Heterobasidion annosum (Fr.:Fr.) Bref.—involves stump treatment with an aggressive saprophytic fungus, Phanerochaete gigantea (Fr.:Fr.) S.S.Rattan, Abdullah & Ismail (Rishbeth 1963). It is likely that slow decline and death of senescent trees allows progressive invasion of the roots and butts of trees by saprobes that deplete the food resources required by Armillaria, whereas felling of healthy trees leaves behind nutrient-rich stumps and roots in which the pathogen increases its inoculum base. A trial in E. diversicolor forests in Western Australia indicated that stump inoculation with cord-forming wood decay fungi, Phanerochaete filamentosa (Berk. & M.A.Curtis) Burds. and Hypholoma sp., contemporaneously with herbicide (ammonium sulphamate) treatment of stumps, was effective in reducing their colonisation by A. luteobubalina inoculated into the stumps (Pearce et al. 1995). Inoculation with the fungi alone was ineffective and treatment of stumps with the herbicide alone tended to increase their below-ground colonisation by the pathogen. Killing of stumps with ammonium sulphamate may result in their rapid colonisation by wood rotting fungi and exclusion of Armillaria provided they are initially free of Armillaria. This may also apply to ringbarking of trees at some time prior to logging, which has been suggested as a control measure for the pathogen (Swift 1970). Trichoderma species applied as spores to drill holes in E. diversicolor stumps at the same time as they were inoculated with A. luteobubalina reduced

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colonisation by the pathogen (Nelson et al. 1995). Some isolates of Trichoderma were more effective than others, indicating potential for selection of more useful isolates for broad-scale application. While the potential value of several fungi as biocontrol agents has been demonstrated in stumps inoculated with A. luteobubalina, more research is required on their efficacy in reducing natural infection and spread in the field. This approach merits further development.

19.5 Management of foliar and canker diseases A wide range of fungal parasites that cause foliar and canker diseases are endemic and common in native eucalypt forests and woodlands. While these diseases undoubtedly affect the growth of trees, destructive epidemics are rare and generally these diseases have been of little concern in forest management (see Chapters 9 and 10). Coevolution of eucalypts with their parasites in native forests has resulted in a balance between the trees and their parasites (Heather 1967; Burdon and Chilvers 1974a). The ability of eucalypts to regenerate crowns following defoliation indicates adaptation of eucalypts to sporadic defoliation by parasites or fire (Heather 1971). However, disturbance of the natural communities may result in disease outbreaks, although the underlying reasons for these outbreaks are poorly understood. For example, an outbreak of leaf spotting caused mainly by Aulographina eucalypti in E. denticulata (as E. nitens) forest in eastern Victoria resulted in defoliation of saplings and mature trees (Neumann and Marks 1976). Severe leaf spotting caused by Aulographina eucalypti and other fungi, possibly associated with drought stress and insect attack, occurred over several thousand hectares of E. obliqua growing in valleys in north-west Tasmania and resulted in the death of many trees (Felton 1981). Epidemics of foliar disease appear to be more common in seedling and coppice regrowth than in mature foliage. Epidemics of Aulographina eucalypti are common and cause substantial defoliation in seedling regrowth of ash-type eucalypts in Victoria (Neumann et al. 1975; Stefanatos 1993) (see Chapter 9). Leaf blight caused by Mycosphaerella cryptica (Cooke) Hansf. was severe on coppice regrowth of E. marginata and E. patens in some forests in Western Australia (Carnegie et al. 1997). A winter leaf spot caused by the coelomycetes Piggotia

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substellata Cooke and Ceuthospora innumera Massee can be destructive on E. regnans seedlings in the highlands of central Victoria (Ashton and Macauley 1972). The disease impairs survival of seedlings during the first year of growth and is an important factor in the regeneration cycle. During regrowth, foliage is dense, close to the ground and protected from the drying effect of wind, all of which are likely to contribute to leaf wetness periods more favourable for infection by foliar pathogens than occur in the foliage high on older trees. Before foliage and canker diseases are considered in a general forest management program, it is necessary to assess the extent of damage caused by these diseases. This has rarely been done in mature eucalypt forests. The study by Abbott et al. (1993) in the E. marginata forests of Western Australia provides a methodological basis for monitoring damage by foliar pests and diseases in native forests. While there is practically no active management for control of foliar diseases in native forests, there is an awareness that some silvicultural practices may influence disease severity. For example, thinning of native forest can increase air movement and the rate of drying of foliage, thereby reducing the time during which conditions are favourable for infection. Juvenile foliage of some eucalypts is more susceptible than adult foliage to some pathogens [e.g. Mycosphaerella nubilosa (Cooke) Hansf. attacks only juvenile leaves of E. globulus and related species] and some diseases are more common in dense seedling or coppice regrowth, as mentioned above. Conditions that promote rapid seedling growth and early maturity of foliage may reduce the effect of such diseases. Native eucalypt forests in the lowlands usually consist of two or more codominant eucalypts from different genera or subgenera (Pryor 1959). It is thought that this contributes to the balance between the trees and their parasite populations in these forests. Whereas host-specific foliar parasites may help maintain the equilibrium between eucalypt species in these mixed stands (Burdon and Chilvers 1974a, 1974b), the mixture of eucalypt species may reduce the incidence and severity of damage caused by host-specific parasites. It could be expected that, if a sufficient diversity of seed is applied to sites in the normal regeneration process, either from selected seed trees or through collection and broadcasting of

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seed mixtures, natural selection would ensure that sites are occupied by genotypes with sufficient resistance to the prevailing diseases. This may have happened on sites seriously affected by Ph. cinnamomi in eastern Victoria, and it is likely that it also contributes to the control of endemic foliar and canker diseases. It is, therefore, imperative that silvicultural practices, especially those associated with thinning and regeneration, sustain the functional diversity of native forests. This principle is commonly recognised during regeneration of forests in eastern Victoria when care is taken to restock coupes with at least the same range and relative frequency of species as occupied the site prior to logging (P.W. Geary, pers. comm.). An option for management of foliar and canker diseases where particular diseases are destructive is to replant damaged forests with genotypes selected for disease resistance. The genetic diversity of the eucalypts offers great scope for selection of types with a degree of resistance to particular pests and diseases (see Chapter 2), including resistance of E. globulus to Mycosphaerella spp. in southern Australia (Dungey et al. 1997). Significant differences in susceptibility to some foliage and canker diseases have been shown to exist among eucalypt species and provenances (Dianese et al. 1984; Purnell and Lundquist 1986; Carnegie et al. 1994). These differences have been exploited in management of diseases in plantations (see Chapters 18 and 22). Many reports of Cryphonectria canker caused by Cryphonectria cubensis (Bruner) Hodges in eucalypt plantations indicate that there is considerable intraspecific and interspecific variation in susceptibility to this disease (Hodges et al. 1976; Campinhos and Ikemori 1978; Conradie et al. 1992). While these reports are based largely on observations of the performance of different genotypes during disease epidemics in the field rather than on detailed genetic or physiological analysis of resistance, obvious variation between species and provenances in their field response to disease has been sufficient for the plantation industry to undertake successful selection, breeding and replanting programs to control diseases. This is a sound way of proceeding as it avoids the danger of selecting resistance with a narrow genetic and physiological base that can be overcome by adaptation of the pathogen population. Canker fungi such as Botryosphaeria ribis Grossenb. & Duggar and Endothia gyrosa (Schwein.:Fr.) Fr.,

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both of which occur in the E. marginata forests, are opportunists which have limited ability to invade the tissues of healthy eucalypts (Shearer et al. 1987; Old et al. 1990; van der Westhuizen et al. 1993). Stress factors such as defoliation and drought may contribute to their development and the rate at which the tree responds to invasion by canker fungi is affected strongly by environmental conditions. Defoliation due to outbreaks of pests or foliar pathogens may result in larger cankers. Defoliation results in reduced soluble carbohydrates and starch in E. regnans and E. grandis and this may reduce resistance of the trees to extension of canker diseases—cankers caused by Endothia gyrosa on E. regnans saplings and by Botryosphaeria ribis on E. delegatensis and E. regnans seedlings were significantly longer on defoliated than on nondefoliated plants (Old et al. 1990). Canker pathogens are often associated with the dieback syndromes discussed above. The main management options are to avoid tree stress by ensuring that the eucalypt species are matched to the site and that silvicultural practices do exacerbate stresses on the trees. Seeding of logged sites with the same diversity of species as previously occupied the site will allow adaptation of the trees to the site and contribute to a reduction in damage by canker-causing fungi. For example, Botryosphaeria ribis was associated with death of E. radiata (a native of temperate eastern Australia) growing in species selection trials in the strongly mediterranean climate of Western Australia (Shearer et al. 1987). In inoculation trials, seedlings and saplings of E. radiata developed damaging cankers, whereas two species native to Western Australia, and presumably better adapted to the site, were much less damaged by the disease.

19.6 Management of stem and butt rots Stem and butt rots have long been considered a serious problem for timber production in native eucalypt forests (Da Costa 1973; Davidson 1974; Heather and Griffin 1978; Wilkes 1982; White and Kile 1991b), more so than in short rotation plantations. Decay-causing fungi, which are usually wood rotting saprobes or weak, facultative parasites, invade the trunks of trees through wounds that expose the sapwood or heartwood (Spaulding 1961). Such wounds have a variety of causes, including logging machinery and falling trees and branches

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resulting from logging, fire, wind throws and wind damage, late shedding and poor occlusion of branch stubs, lightning, canker fungi and insect larvae (see Chapter 13) (Wagener and Davidson 1954; Davidson 1974; Gadgil and Bawden 1981). These wounds are mostly above ground and are accessible to the windborne spores of decay-causing fungi. Even small wounds may provide infection courts for decay fungi (White and Kile 1991a). The incidence of wounding on trees in native forests can be reduced by silvicultural means, for example through control of wildfires and by changing from selective logging to clearfelling. Selective logging and thinning of stands are both likely to cause widespread butt and stem wounding and increase the incidence of decay (Bostrom 1982), although cable thinning systems can greatly reduce the damage sustained by remnant trees (H. Elliott, unpubl. data). Fire is one of the major causes of wounding leading to decay in eucalypt forests (Greaves et al. 1965; Perry et al. 1985), and high intensity fires cause more wounding than low intensity fires (McArthur 1968; Abbott and Loneragan 1983). Following high intensity fire, eucalypts can be at increased risk of infection by decay fungi for a prolonged period (Gill 1980). In an alpine stand of E. delegatensis, fire caused most of the scars through which decay causing fungi and termites entered the trees (Greaves et al. 1965). The size of the original fire scar is directly proportional to the extent of stem decay in E. marginata (McCaw 1983). Termite attack in eucalypt heartwood follows upon fungal decay (Perry et al. 1985). The two are usually directly proportional (McCaw 1983). Careful management of fire in eucalypt forests, mainly through the use of fuel reduction burns to reduce the occurrence of wildfires, can minimise the incidence of severe fire scars and subsequent development of decay (Wallace 1966; Perry et al. 1985; Abbott and Loneragan 1986; Wardlaw 1990). The severity of attack by insects such as cerambycids, whose larvae are favoured by water stress and cause trunk wounds that allow the entry of decay fungi, could be reduced by silvicultural means. For example, attack on E. diversicolor by the cerambycid Phoracantha acanthocera (Macleay) [syn. Tryphocaria acanthocera (Macleay)] was reduced by thinning after a certain age, exclusion of

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fire until after the first thinning and removal of old growth trees (Abbott et al. 1991). Eucalyptus regnans trees grown at high density tend to shed branches when they are smaller than trees grown at lower density, with the result that stub occlusion is more successful, reducing the incidence of decay in branch stubs in the denser plantings (Marks et al. 1986). The probability of defect occurring in the main stem as a result of branch shedding increases substantially when branch diameters exceed one centimetre. Branch shedding also occurred earlier in E. sieberi seedlings competing with rapidly growing acacias than in E. sieberi seedlings growing alone (Marks et al. 1986). It is, therefore, possible that the extent of defect-free branch shedding can be increased by planting at higher densities and burning logged coupes to encourage regeneration of acacias along with eucalypts. Because eucalypt species differ in their tolerance of competition, silvicultural management needs to be tailored to each species. An improved understanding of the environmental, genetic and silvicultural factors affecting the incidence and severity of decay is crucial for improved management of decay and production of high quality wood in native eucalypt forests. Because of the extended time over which decay occurs and the lack of rapid methods for measurement of decay in standing eucalypts, the progress of decay in eucalypts has been little studied. The rough external indicators of the likely extent of stem decay (e.g. extent of fire scars or distortions of the trunk), or empirical tests such as the echo produced when the stem is struck with the back of an axe, may be useful for selecting decay-free trees during harvesting, but they are neither sufficiently precise nor reliable for long-term studies. There have been few studies of the effect of fire history or edaphic, climatic and stand factors on the rate of development of decay in eucalypt trees. Furthermore, there is little information on the rates of decay as stands age or on the losses from decay in different eucalypt species (Rayner and Turner 1990a, 1990b). In general, the amount of decay as a proportion of gross volume of standing trees increases with age (Wagener and Davidson 1954). The extent of attack by decay fungi may be reduced by shortening the rotation length (van der Westhuizen 1959). While stem and butt rots are regarded as a particular problem in mature and

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overmature trees in eucalypt forests (Heather and Griffin 1978), they are also considered to be a problem in regrowth trees now being harvested at intervals as short as 50 years (see Chapter 13). Detailed studies of stand growth and incidence and severity of decay such as those conducted in Tasmania (Wardlaw 1996) should enable development of models that can be used to predict the optimum time to harvest particular species in different forest types. Development of such models for decay incidence could facilitate salvage logging of trees with decay, although selective removal of trees could damage remaining trees and so increase the overall incidence of decay in the forest. Laboratory tests (Da Costa et al. 1962; Da Costa 1979; Johnson et al. 1996) and in-ground field tests (Thornton et al. 1983, 1996, 1997; Johnson et al. 1986) have shown considerable variation in resistance to rot of outer heartwood of eucalypts both between and within species (see Chapter 13). However, results of in vitro tests using outer heartwood and selected fungi sometimes do not reflect incidence of decay in standing trees in which rot occurs mainly in the less rot-resistant inner heartwood, is affected by environmental factors and the occurrence of infection courts, and involves a complex community of decay fungi and other microorganisms (Wilkes 1982, 1985a, 1985b). There is no doubt that there is great variation between eucalypt species in stem and butt rot resistance in standing trees, with incidence of decay in a study in New South Wales ranging from 9% of trees in E. sideroxylon to 84% in E. bancroftii (Wilkes 1985a). There was significant variation in incidence and extent of discolouration and decay among individual trees of E. regnans in Tasmania (Wardlaw 1996). It may be possible, therefore, to select for genotypes of eucalypts with resistance to decay and use these for regeneration on sites in native forests identified as having a high incidence of stem and butt rot. It is important also to ensure that forest management practices do not alter species composition of forests in a way that would make them more vulnerable to stem and butt rot. A complication in native forests being managed for conservation of wildlife as well as for timber production is that the hollows in trees resulting from decay and termite attack are important in providing shelter for wildlife (see Chapter 18). Silvicultural

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systems aimed at greatly reducing the incidence of decay in native forests may be incompatible with management aimed partly at conservation of wildlife.

19.7 Conclusion The most direct intervention for management of disease in native eucalypt forests has been the attempt to restrict the further spread of Ph. cinnamomi in the forests of south-east and south-west Australia. This has involved significant expenditure on basic research, mapping occurrence of the pathogen, drafting legislation to restrict access to vulnerable areas of forest and ensuring that hygiene measures are implemented. Initial success with the use of the inorganic salt, potassium phosphonate, to control the disease in native vegetation in Western Australia offers the possibility of protecting those rare species threatened by Ph. cinnamomi. The selection of genotypes of E. marginata with a degree of resistance to the pathogen is likely to be useful for rehabilitating severely damaged sites. There has been initial success in rehabilitation of severely damaged forests in eastern Victoria using conventional silvicultural practices to encourage rapid regeneration of a mix of local eucalypt species, including susceptible as well as resistant eucalypts, and acacias. Management of the many other dieback diseases of eucalypts in native forests has been hampered by a lack of knowledge of their etiology and ecology. Only in the cases of rural dieback and increased mistletoe invasion of altered woodlands has there been sufficient understanding of the syndromes to allow development of appropriate remedial measures. These have mainly involved restoration of patches of the woodlands to something approaching their original diversity and structure. While there has been little active management directed at control of various forest diebacks of complex etiology, Armillaria root rot, foliage and canker diseases, and stem and butt rots, there is increasing awareness of the incidence and severity of these diseases and how sound silvicultural practices aimed at maintaining general health and diversity of the forests might alleviate them. Increased damage by endemic diseases is often associated with disturbance of the natural structure and functioning of forests and woodlands. Given that most commonly it is

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impracticable to intervene actively to control these diseases, it is important that the native plant communities be managed so that natural ecological and adaptive processes are disturbed as little as possible. In particular, the silvicultural practices involved in fire control, harvesting and regeneration need to be conducted so as to ensure that the natural diversity of adapted genotypes, both between and within species, is maintained. Most forest management practices are now directed at maintaining this diversity, for example through the careful selection of seed mixtures for sowing on logged sites or of seed trees to be left after logging. In the coastal forests of eastern Victoria, restoration of the natural ecological and adaptive processes of the forests, even on sites badly affected by an aggressive introduced pathogen like Ph. cinnamomi, can be effective in limiting disease and restoring productive forest following disease outbreak.

19.8 Acknowledgments In writing this chapter we gratefully acknowledge the influence of our many colleagues, but especially David Ashton, Mick Brown, Syd Shea, Jack Simpson and our late friends and mentors, Frank Newhook and Geoff Marks.

19.9 References Abbott, I. and Loneragan, O. (1983). Influence of fire on growth rate, mortality, and butt damage in Mediterranean forest of Western Australia. Forest Ecology and Management 6, 139–153. Abbott, I. and Loneragan, O. (1986). Ecology of jarrah (Eucalyptus marginata) in the northern jarrah forest of Western Australia. Bulletin Number 1. (Western Australia, Department of Conservation and Land Management: Perth.) Abbott, I., Smith, R., Williams, M. and Voutier, R. (1991). Infestation of regenerated stands of karri (Eucalyptus diversicolor) by bullseye borer (Tryphocaria acanthocera, Cerambycidae) in Western Australia. Australian Forestry 54, 66–74. Abbott, I., Van Heurck, P., Burbidge, T. and Williams, M. (1993). Damage caused by insects and fungi to eucalypt foliage: spatial and temporal patterns in Mediterranean forest of Western Australia. Forest Ecology and Management 58, 85–110. Ashton, D.H. and Macauley, B.J. (1972). Winter leaf spot disease of seedlings of Eucalyptus regnans and its relation to forest litter. Transactions of the British Mycological Society 58, 377–386.

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Bartle, J.R., Shea, S.R. and Kimber, P.C. (1981). Management of tree cover on water catchments in Western Australia. In Eucalypt Dieback in Forests and Woodlands. (Eds K.M. Old, G.A. Kile and C.P. Ohmart) pp. 212–226. (CSIRO: Melbourne.) Behn, G.A. (1995). Evaluation of the effectiveness of remote sensing in geographic information system technologies for mapping and monitoring dieback. MSc Thesis, Curtin University, Perth, Western Australia. Benjamin, M. and Newhook, F. (1984). The relative susceptibility of various Eucalyptus spp. and Pinus radiata to Armillaria grown on different food bases. In Proceedings of the 6th IUFRO International Conference on Root and Butt Rots of Forest Trees (IUFRO Working Party S2.06.01). (Ed. G.A. Kile) pp. 140–147. (CSIRO: Melbourne.) Bostrom, C. (1982). Profitability of thinning: short and long term considerations. New Zealand Journal of Forestry Science 12, 364–379. Bowling, P.J. and McLeod, D.E. (1968). A note on the presence of Armillaria in second growth eucalypt stands in southern Tasmania. Australian Forest Research 3, 38–40. Bradshaw, F.J. (1974). Large scale 70mm colour photography as an aid to detecting jarrah dieback. In Proceedings, Symposium on Remote Sensing and Photo Interpretation. Commission VII, Banff, Alberta, Canada. pp. 439–448. (International Society for Photogrammetry: Banff, Alberta.) Bradshaw, F.J. and Chandler, R.J. (1978). Full coverage at large scale. In Symposium on Remote Sensing for Vegetation Damage Assessment. Archived as 913777 Forest Science Library, Conservation and Land Management, Como, WA 6152, Australia. Broadbent, P. and Baker, K.F. (1974). Behaviour of Phytophthora cinnamomi in soils suppressive and conducive to root rot. Australian Journal of Agricultural Research 25, 121–137. Brown, B.N. (1976). Phytophthora cinnamomi associated with patch death in tropical rainforests in Queensland. Australian Plant Pathology Society Newsletter 5, 1–4. Burdon, J.J. and Chilvers, G.A. (1974a). Fungal and insect parasites contributing to niche differentiation in mixed species stands of eucalypt saplings. Australian Journal of Botany 22, 103–114. Burdon, J.J. and Chilvers, G.A. (1974b). Leaf parasites on altitudinal populations of Eucalyptus pauciflora Sieb. ex Spreng. Australian Journal of Botany 22, 265–269. Burrows, N.D. (1985). Reducing the abundance of Banksia grandis in the jarrah forest by the use of controlled fire. Australian Forestry 48, 63–70. Campinhos, E. and Ikemori, Y.K. (1978). Tree improvement program of Eucalyptus spp.: preliminary results. In Documents FAO Third World Consultation on Forest Tree Breeding 2, 717–735.

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Carnegie, A.J., Keane, P.J., Ades, P.K. and Smith, I.W. (1994). Variation in susceptibility of Eucalyptus globulus provenances to Mycosphaerella leaf disease. Canadian Journal of Forest Research 24, 1751–1757. Carnegie, A.J., Keane, P.J. and Podger, F.D. (1997). The impact of three species of Mycosphaerella newly recorded on Eucalyptus in Western Australia. Australasian Plant Pathology 26, 71–77. Conradie, E., Swart, W.J. and Wingfield, M.J. (1992). Susceptibility of Eucalyptus grandis to Cryphonectria cubensis. European Journal of Forest Pathology 22, 312–315. Cotton, G. (1998). A background to Mundulla yellows. In Proceedings of Workshop. 16 September 1998. Mundulla, South Australia. (South Australian Department for the Environment, Heritage and Aboriginal Affairs: Adelaide.) Da Costa, E.W.B. (1973). Natural durability and heart rots. Sixteenth Forest Products Research Conference, Melbourne. Topic 1/15: 1–2. (CSIRO Division of Forestry and Forest Products: Melbourne.) Da Costa, E.W.B. (1979). Comparative decay resistance of Australian timbers in accelerated laboratory tests. Australian Forest Research 9, 119–135. Da Costa, E.W.B., Rudman, P. and Deverall, F.J. (1962). Inter-tree variation in decay resistance of karri (Eucalyptus diversicolor F. Muell.) as related to colour, density and extractive content. Journal of the Institute of Wood Science 10, 48–55. Davidson, J. (1974). Decayed wood in living trees of Eucalyptus deglupta Blume. Research Note SR. 18. (Department of Forests: Boroko, Papua New Guinea.) Davison, E.M. and Shearer, B.L. (1989). Phytophthora spp. in indigenous forests in Australia. New Zealand Journal of Forestry Science 19, 277–289. Davidson R.L. (1980). Local management. In Focus on Farm Trees. (Eds N.M. Oates, P.J. Greig, D.G. Hill. P. A. Langley and A.J. Reid) pp. 89–98. (Capitol Press: Box Hill, Vic.) Dianese, J.C., Moraes, T.S. de A. and Silva, A.R. (1984). Response of Eucalpytus to field infection by Puccinia psidii. Plant Disease 68, 314–316. Duncan, M.J. and Keane, P.J. (1996). Vegetation changes associated with Phytophthora cinnamomi and its decline under Xanthorrhoea australis in Kinglake National Park, Victoria. Australian Journal of Botany 44, 355–369. Dungey, H.S., Potts, B.M., Carnegie, A.J. and Ades, P.K. (1997). Mycosphaerella leaf disease: genetic variation in damage to Eucalyptus nitens, E. globulus and their F1 hybrid. Canadian Journal of Forest Research 27, 750–759. Edgar, J.G., Kile, G.A. and Almond, C.A. (1976). Tree decline and mortality in selectively logged eucalypt forests in central Victoria. Australian Forestry 39, 288–303.

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Control of Phytophthora cinnamomi in association with a large-scale bauxite mining operation in the Eucalyptus marginata forests of Western Australia provides an example of intensive management of this disease in native forest. In particular, it shows that the most intensive use of disease mapping and hygiene and rehabilitation measures can restrict the spread of the disease and result in the re-establishment of E. marginata forest on the mined sites.

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20.1 Introduction

20.2 The mining operation

Alcoa World Alumina Australia (Alcoa) operates two bauxite mines in the Western Australian Eucalyptus marginata (jarrah) forest where dieback caused by Phytophthora (Ph.) cinnamomi Rands is widespread. Bauxite mining, by necessity, moves large volumes of soil and markedly alters the surface drainage of the area being mined, both of which can potentially spread the pathogen and exacerbate the disease (Fig. 20.1). The commitment of the company and the government to the protection of the environment around the mines has led to the development of an intensive dieback management program (Colquhoun and Hardy 2000). This program is fully integrated with all planning and operational practices and was developed in collaboration with the State Department of Conservation and Land Management (CALM). The economic return from mining allows a much greater expenditure on dieback management than occurs in the bulk of the affected forest. The company has also conducted some experimentation at an operational level that provides insights useful for management of the broader forest (Colquhoun and Hardy 2000).

Bauxite of mineable quality is found in less than 5% of the jarrah forest. The ore deposits occur in areas from one to 100 hectares and tend to occur on the mid and upper flanks of hills. Most ore deposits typically underlie infested forest on the lower slopes and uninfested forest towards the ridges. Annual production of bauxite is 20 million tonnes, which requires mining of about 550 hectares of forest.

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After harvest of the timber, the remaining forest is cleared and the topsoil (0–15 cm) and overburden (16–40+ cm) are removed separately. The topsoil is either replaced ‘fresh’ onto a previously mined site prepared for revegetation or stockpiled near the remote edge of the ore deposit or in another minepit. The overburden is stockpiled separately. Below the overburden is a one to two metre deep, concreted laterite layer (duricrust), with a more friable laterite layer below. Water can pond on the duricrust, providing ideal conditions for infection of roots by Ph. cinnamomi. Open-cut mining extracts the top three to five metres of laterite. Following ore extraction, major earthworks reshape the pit to

Bauxite ore being extracted at an Alcoa mine using a front-end loader and tip truck, showing concretions from the duricrust and Eucalyptus marginata forest.

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Topsoil being returned at an Alcoa mine using scrapers to place soil on a mine pit that has been landscaped after mining.

blend with local topography. The overburden and then topsoil are replaced separately (Fig. 20.2) and the pit is ripped to remove compaction and prevent erosion. Finally, seed collected from local E. marginata forest, of many native species taken from overstorey, understorey and ground shrub layers, is broadcast on the area and fertilised. Seeding rates are designed to result in 2000 to 2500 tree seedlings per hectare, with E. marginata as the dominant tree. Nichols et al. (1985) and Ward et al. (1993) provide more detailed descriptions of the mining and rehabilitation process.

The revegetation must also be able to sustain a range of other forest values such as supplying potable water, timber production and conservation.

20.3 Objectives of rehabilitation and the dieback management program

These objectives need to be met while maintaining an economically viable mining operation.

The overall objective of the rehabilitation program is to re-establish an E. marginata forest community with plant diversity as similar as possible to that of the surrounding forest and comprised of species indigenous to the locality of the mine.

The major objectives of Alcoa’s dieback management program are to: 1

prevent the spread of Ph. cinnamomi from mining areas to uninfested forest

2

maximise the area of mine rehabilitation that is not infested with Ph. cinnamomi and to meet criteria for successful restoration of botanical diversity and land use needs.

20.4 The management strategy The strategy has six major operational objectives: 1

To know the location of Ph. cinnamomi infested soils—this is the foundation of all dieback management and is based on the

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Figure 20.3

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Bunting and signs as used throughout Alcoa’s bauxite mining operations to mark the boundary of infested and uninfested areas. The site is ready for seeding and fertilising.

diagnosis and mapping procedures applied in the broader E. marginata forests (see Chapter 19). Detailed maps are prepared and sampling carried out for each exploration area before a drilling program is initiated and also for each mine pit before clearing and mining. The locations of boundaries between infested and uninfested areas of forest are followed at each stage of mining and are clearly marked (Fig. 20.3). The locations of soil and overburden stockpiles, and whether they originated from infested or uninfested sites, are also recorded. 2

3

To target dieback control measures at operations with a high risk of spreading Ph. cinnamomi— because many dieback control operations have a substantial cost, it is important to assess the risk of spread associated with each stage of mining. The most stringent control measures are applied where the risk is judged to be greatest. To integrate dieback control measures with all other mining operations so that the risk of spread and the level of disruption to mining are

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minimised—at the Huntly mine, the selection of the best integration option resulted in a major change in the operations. In the past, much of the area cleared for mining was infested, so mining roads were built using the closest gravel source and the roads were deemed to be infested. Vehicles needed to be cleaned before leaving the road and entering an uninfested area. At Huntly over 80% of the ore is in uninfested forest so the frequency of cleaning vehicles was predicted to be very high. Consequently, to reduce this frequency the roads were built with uninfested gravel. This change to standard procedures affected all subsequent mining operations. 4

To undertake a dieback research program to support and improve the field operations and to contribute to the understanding and management of dieback throughout the forest— part of this program has been the selection of E. marginata individuals with high resistance to Ph. cinnamomi. This is a collaborative project with CALM and Murdoch University.

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Early research showed that resistance to Ph. cinnamomi is a highly heritable trait (Stukely and Crane 1994). This project has involved screening of plants for disease resistance, micropropagating resistant individuals, validating resistance in the field and glasshouse, and establishing clonal seed orchards. Dieback rehabilitated mine pits and severely diebackaffected forest sites will be revegetated using plants from this project. 5

6

To educate the workforce on dieback management procedures and their necessity— the dieback control strategy and procedures were developed by a team composed of mine management staff, field supervisors, environmental officers and research scientists. When the procedures were introduced there was a strong commitment because of the direct involvement of managers and field supervisors in their development. All operators are trained in the control procedures relevant to their duties. There is strong senior management commitment to the procedures. Any breach of rules is regarded as important and serious breaches attract disciplinary action. Contractors are also trained in the procedures. Any breach by a contractor can lead to cancellation of their contract. To monitor compliance and success of the program in achieving the above objectives— this is achieved by auditing the procedures throughout the mining operation and in followup studies of the spread of dieback in forest adjacent to mining and in rehabilitated sites. The results of audits and investigations into the causes of spread are used to improve the dieback management procedures.

20.5 Procedures for disease control 20.5.1 Planning of mine operations and rehabilitation planting The mine planner and mine environmental scientist work together to develop operational plans to ensure that mining is economic but appropriate scheduling of operations decreases the risk of spreading Ph. cinnamomi. The risk of infested soil adhering to vehicles and mine machinery is low when the soil is dry. High-risk operations can be scheduled for the

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hot, dry months from November to May. For example, haul roads are usually built during this dry period. Good planning to reduce the chance of spreading the pathogen also encompasses location of roads, length of time that a mine pit is left active, sequence of mining a large mine pit, location of stockpiles and a wide range of other issues.

20.5.2 Control of access Success of the uninfested haul road system used at the Huntly mine is indicated by the uninfested areas remaining free of Ph. cinnamomi. The ‘unknown’ presence of Ph. cinnamomi on a wet haul road has the potential to introduce Ph. cinnamomi to every dieback-free area the vehicles visit. Controlling access to all dieback-free areas is essential at all mines and most stages of mining. This is achieved by: 1

blocking tracks so they cannot be used

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displaying signs and bunting to limit access and inform users of access conditions (Fig. 20.3)

3

erecting gates on all entry points to the mine

4

constructing ‘bridges’ across infested areas using gravel and rocks from uninfested sites.

20.5.3 Cleaning of vehicles and machinery As operations occur in both infested and uninfested sites, procedures are needed to minimise the risk of spreading infested soil across boundaries. Before any vehicle or mobile equipment moves from infested to uninfested sites, as much soil as possible is removed (Fig. 20.4). Because the most effective cleaning occurs in the workshop, scheduling is optimised to exploit workshop cleaning. For example, after ripping an infested area, the bulldozer is transported back to the workshop where it is cleaned. It is then sent to rip uninfested areas, after which it may move directly into an infested area. It is then cleaned at the workshop again, ready for its next task. Cleaning occurs at all stages of mining where vehicles are required to cross dieback boundaries. Large, trailer-mounted, high-pressure water pumps are used in the field and special cleaning facilities are constructed where necessary (Fig. 20.5). Because effective cleaning of vehicles in the field is difficult and time consuming, the need for this task is reduced as much as possible by strategic planning. 481

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Figure 20.4

Washing the soil from the wheels of a scraper before the vehicle crosses into a dieback-free area.

Figure 20.5

Automatic vehicle cleaning facility at the entrance to a bauxite mine.

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A stockpile of topsoil uninfested with Phytophthora cinnamomi showing the type of sign used in all Alcoa bauxite mines.

20.5.4 Infested and uninfested soil is moved separately The location of boundaries between infested and uninfested areas is noted throughout all operations. This enables the infested and uninfested soils to be moved and stored separately. In some cases, the boundary needs to be moved further into the uninfested area for practical reasons (e.g. the uninfested area may be too small to enable a large mining vehicle to turn). This boundary change is marked in the field so that all the soil can be moved and stored as infested soil. All overburden and topsoil stockpiles are distinctively marked (Fig. 20.6) to show if they are overburden (OB) or topsoil (T) and if they are infested (red) or uninfested (green). Dieback control measures associated with soil movement and storage are discussed in detail in Colquhoun and Petersen (1994).

20.5.5. Controls of drainage Because zoospores of Ph. cinnamomi are transported in water, surface water movement from infested to uninfested areas needs to be controlled. Surface water is not allowed to drain freely into the forest from any mine works, irrespective of the dieback status of the water or forest—discharge is always controlled. In the rehabilitated mine pits the

landscape design and the ripping pattern direct all surface water back into the mine pit, away from the forest. If an infested ore body is located upslope of an uninfested site, then the duricrust in the lowest part of the boundary is disrupted (by blasting or ripping with a bulldozer). This ‘drainage slot’, as it is termed, intercepts and prevents surface water running into the forest. The haul roads shed significant quantities of water. A system of drains and high bunds directs the runoff water into sumps and prevents surface water flowing directly into the forest. ‘Infiltration sumps’ are constructed in upper slope areas. These are stabilised, deep holes through which water can drain vertically into the profile. In lower slope areas, threestage sedimentation sumps, designed to remove sediments before the water discharges into the stream zone, are used.

20.6 Success in management of disease In 1996, forest classified as uninfested prior to mining was remapped for the presence of dieback. Only about six hectares of recently infested forest, assumed to be attributable to mining, was found adjacent to 1253 hectares of land which had been

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Figure 20.7

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A five-year-old rehabilitated mine pit showing regeneration of Eucalyptus marginata.

cleared for mining up to 10 years previously (Crosbie and Colquhoun 1999). If dieback management procedures are effective, then uninfested soil removed before mining should be returned during rehabilitation in the same uninfested condition. To check this, every one-year-old rehabilitated area with uninfested soil is searched for dead or unhealthy plants of dieback-susceptible species. These plants, with the soil surrounding the roots, were screened in the laboratory for the presence of Ph. cinnamomi. Only four of the 29 rehabilitated mine pits monitored were found to have Ph. cinnamomi present, indicating that, in most cases, the dieback management procedures have been effective. Major audits of the dieback management procedures occurred in 1994 and 1997. The audits assessed the mine’s compliance with documented procedures and the level of knowledge and understanding of the procedures. The results from the audits are used to identify opportunities to improve procedures. The survival of E. marginata trees in rehabilitated mine pits is high (> 80%, Alcoa of Australia 1994), with no instances of mass deaths after 11 years of 484

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routine use of this species (Fig. 20.7). It was expected that the presence of Ph. cinnamomi would decrease the species richness of rehabilitated mine pits. However, recent monitoring has indicated that this is not the case. Fifty monitoring plots (five 4 by 4 m quadrats) are established routinely every year in rehabilitated mine pits in each mine. Fifteen months after revegetation, species richness is monitored. The method of topsoil handling has the biggest effect on species richness, with sites where topsoil was stockpiled having fewer species than those that received fresh topsoil (Table 20.1). Surprisingly, the use of soil infested with Ph. cinnamomi did not significantly affect species richness. The outcome of the vegetation monitoring programs and opportunistic sampling of recently dead plants is encouraging. Susceptible plants are killed by Ph. cinnamomi but not as frequently as expected based on knowledge of the pathogen in the forest. Probably this is because mining removes the duricrust, thus preventing water-ponding, which provides ideal conditions for infection of sinker roots (see Chapters 11 and 19). The procedures continue to be revised. The need for revision is based on four factors:

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Mean plant species richness of rehabilitated bauxite mine pits with varying topsoil history and presence of Phytophthora cinnamomi, monitored 15 months after rehabilitation

The data are for two years of monitoring.

Topsoil history

Pathogen status of soil

Mean species richness (No. species per 80 m2 ± s.e.)

No. of plots observed

Topsoil directly returned to minepit

Uninfested Infested

51.7 ± 1.6 51.0 ± 2.1

56 26

Topsoil stockpiled

Uninfested Infested

39.5 ± 0.9 39.8 ± 0.9

112 110

1

improved information about the risk of spreading the pathogen

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practical problems associated with procedures

3

improved costing of implementation

4

introduction of new stages to the mining process.

20.7 Conclusion Spread of Ph. cinnamomi has been kept to a minimum during Alcoa’s mining operations through a combination of initiatives:

plant health management objectives, provided there is a strong commitment to disease control from the operators and managers, close collaboration with the land management authority, and a sufficient commitment of resources to allow development and application of intensive disease management procedures. The research and experience underpinning the development of successful disease management procedures in the mining operation have wider application in disease management.

20.8 References

1

mapping of the occurrence of the pathogen in forests subject to exploration and mining

Alcoa of Australia (1994). Wagerup Alumina Refinery— Consultative Environmental Review. (Alcoa of Australia Limited: Applecross, WA.)

2

forward planning of mining operations based on the behaviour of the pathogen

Colquhoun, I.J. and Petersen, A.E. (1994). Impact of plant disease on mining. Journal of the Royal Society of Western Australia 77, 151–158.

3

training of all field and managerial staff in disease awareness and control procedures

4

a commitment to incorporating disease management procedures into the mining process

Colquhoun, I.J. and Hardy, G.E.St.J. (2000). Managing the risks of Phytophthora root and collar rot during bauxite mining in the Eucalyptus marginata (jarrah) forest of Western Australia. Plant Disease 84, 116–127.

5

continual improvement of procedures following the results of compliance auditing and monitoring of disease spread

Crosbie, J.A. and Colquhoun, I.J. (1999). Assessment of dieback spread associated with bauxite mining. Alcoa World Alumina Australia Research Bulletin No. 28, Applecross, WA.

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conduct of ongoing research into the ecology of the disease.

Restoring E. marginata on the minepits, even infested pits, has been very successful (Fig. 20.7). Establishing E. marginata genotypes selected for resistance to the pathogen should further improve the success rate. Overall, Alcoa’s bauxite mining operation demonstrates how an intensive production activity can proceed in a forest without seriously jeopardising

Nichols O.G., Carbon B.A., Colquhoun I.J., Croton J.T. and Murray N.J. (1985). Rehabilitation after bauxite mining in south-western Australia. Landscape Planning 12, 75–92. Stukely M.J.C. and Crane C.E. 1994. Genetically based resistance of Eucalyptus marginata to Phytophthora cinnamomi. Plant Pathology 84, 650–656. Ward, S.C., Slessar, G.C. and Glenister, D.J. (1993). Environmental resource management practices of Alcoa of Australia Limited. In Australasian Mining and Metallurgy, Vol. 1, 2nd edn (Eds J.T. Woodcock and J.K. Hamilton) pp. 104–108. (University of New South Wales Press: Sydney.)

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The nursery is a key element in any eucalypt planting program and control of diseases in the nursery is essential. While nursery diseases are best avoided, the management of those that threaten a planting program depends on their early recognition and on knowledge of their cause and the interaction between host, environment and causal agent. The management of nursery diseases needs to be seen as only one aspect of the total nursery system which also involves irrigation, nutrition, shading, and insect and weed control. Often poor cultural practices are the cause of, or a contributing factor in, both abiotic and biotic diseases. Many of the diseases that affect eucalypt planting material in forest nurseries are caused by soilborne or waterborne microorganisms and these can often be prevented, or at least minimised, by the use of good cultural procedures, especially those likely to exclude pathogens. There can also be a role for direct physical controls of nursery diseases such as the use of heat, either by direct application to soil of steam or dry heat, or by soil solarisation. Toxic fumigants have been used widely to eliminate plant pathogens from soils or container mixtures used in nurseries, but strict post-fumigation hygiene is needed to avoid the risk of severe disease losses that may occur when treated soils are contaminated by soilborne pathogens. It is often feasible to use fungicides for disease control in eucalypt nurseries. The principles of disease control applicable to all nursery situations are reviewed and recommendations for the control of specific eucalypt nursery diseases are summarised.

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21.1 Management of nursery diseases—general principles 21.1.1 Introduction A fundamental maxim of disease control in the nursery is that it is far better to avoid disease than to have to apply controls after disease has broken out. It is important to identify the actual and potential disease problems facing a eucalypt propagation program (see Chapters 7 and 8) as a basis for implementing an economical and effective disease management strategy. Disease problems must be detected early, even though they may then appear only minor. The effective implementation of any disease control practice depends on detailed information on the disease agent and its interaction with its host and environment. Information on where the pathogen comes from, how it spreads, its severity, what environmental and host factors favour its development and its response to fungicides contributes to the development of control strategies. Disease management cannot stand alone; it must be considered in relation to the general management of the nursery, including container management, shading, irrigation, fertiliser application, and insect and weed control. In Brazil, general nursery management is important in the incidence of nursery diseases and a significant decrease in damping-off was brought about by changes in nursery practices (Ferreira and Muchovej 1991). Until 1970 the use of a seedbed system resulted in severe damping-off; from 1970 to 1984 direct seeding into containers on the ground was associated with some damping-off; after 1984 direct seeding into suspended containers resulted in virtual elimination of damping-off (see section 21.2.2). Most diseases in forest nurseries can be adequately managed by application of sound nursery practices. Poor cultural practices such as uneven seed distribution in beds or containers, incorrect sowing depth, high seedling density and inappropriate shade levels can increase the incidence and severity of nursery diseases. In Kerala, India, crowding of plants allowed the development of many nursery diseases which were much reduced or disappeared altogether after the stock was transplanted to the field (Sharma 1986). Occurrence of nursery diseases will be affected by whether plants are raised in glasshouses, under shade or under the open sky. Excessive shade resulting in low light intensities in nurseries of

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Eucalyptus grandis lowered the ambient and soil temperatures but raised the soil water potential, favouring the development of web blight and damping-off diseases (Sharma and Mohanan 1992). Conversely, seedbeds under higher light intensities had higher ambient and soil temperatures and lower soil water potentials, conditions which favoured the development of seedling blight and shoot blight. Closed glasshouses can result in raised humidity, a condition likely to favour many foliar and shoot diseases. The selection of the growing medium is important in nursery disease management. Seedbed soils and container mixes need to have a good structure and be well drained and slightly acid (pH 5–6). Poor levelling of trays of containers and poorly draining substrates can cause direct waterlogging damage or can aggravate soilborne diseases. An ideal substrate for container production of eucalypts is one with an organic base to support the full production phase (5 months in Brazil), with sufficient added fertiliser to reduce follow-up fertiliser applications to a minimum (F.A. Ferreira, pers. comm.). Nutrients are not as readily leached from organic-based substrates as from materials such as vermiculite and the organic-based substrates also provide a receptive base if there are to be inoculations with mycorrhizal fungi or biocontrol agents. In South Africa, although damping-off was considered to be potentially the most important nursery disease of exotic plantation species including eucalypts (Lückhoff 1964), it and other nursery diseases were of minor importance and any outbreaks were almost invariably traced to incorrect nursery practice. In Brazil, which produces more eucalypt nursery stock than any other country, there are few diseases in eucalypt nurseries because of the nursery management techniques used (F.A. Ferreira, pers. comm.). The use of direct seeding, suspended containers and rapid turn-over of stock in Brazil has allowed the production of eucalypt planting stock in tropical areas without recourse to fungicides (Ferreira and Muchovej 1991). Plant growth is generally restricted after three months by reduced irrigation and fertilisation and seedlings are retained in the nursery for no longer than five months. If seedlings are retained for more than five months, severe diseases can occur, particularly in the tropical

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regions. However, in cooler, subtropical and temperate areas, grey mould of leaves and shoots caused by Botrytis cinerea Pers. is a problem which requires a combination of cultural and chemical control measures (F.A. Ferreira, pers. comm.). The forest nursery is an area of comparatively high value production where costly methods of disease control may be economically viable. There will be occasions where disease control is so important that the financial aspects may not be given serious consideration, or where losses caused by delays in the planting program, the potential disease loss in the plantation or the high genetic or economic value of the particular seedling crop justify additional expenditure on disease control in the nursery. Physical and chemical control measures can be used in diverse ways to suppress nursery diseases. Physical control measures include hand roguing, the use of heat, either by direct heating or solarisation, and the use of ultraviolet light and/or filtration to sterilise water supplies. Chemicals can be applied to soil (either as soil fumigants or fungicides), to irrigation water, seed or other propagative material, or foliage (as sprays or dusts). Free radical scavengers have also been used to control nursery diseases (Elad 1992). Much research is now being directed at the inclusion of biocontrol agents in growing mixtures.

21.1.2 Quarantine and hygiene Quarantine regulations are important in preventing the entry of new diseases into a country or into a region within a country. Everyone involved with a plantation program that includes introductions of planting material should recognise the importance of quarantine and ensure that the appropriate regulations are followed and that source material is free of disease. Every precaution should be taken to exclude disease from the nursery. Experience in southern Queensland has shown that long-term operations based on strict hygiene principles can be used to maintain a nursery free of soilborne pathogens (Brown and Baxter 1991). The use of direct seeding and suspended containers, as in Brazil, allows the adoption of a practical hygiene system which almost totally excludes pathogens, while providing the benefit of allowing automation of some nursery procedures (F.A. Ferreira, pers. comm.). Measures taken to exclude pathogens from nurseries should also include the prohibition of transfer of seedlings or rooted

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cuttings from one nursery to another—if such material has to be brought into an area, it should be kept away from existing nurseries. Possible sources of Fusarium and Phytophthora (Ph.) problems in forest nurseries are the use of old agricultural fields for nursery sites, the incorporation of cull plants into seedbeds, composting of culls at a site that drains into the nursery, reuse of peat moss from an infested nursery, the lack of culling for disease and the movement of infested stock within and between nurseries (Hansen et al. 1979; Johnson et al. 1989). As many of the nursery diseases of eucalypts are soilborne, they can be eliminated by use of appropriate hygienic containers as shown in Brazil. Seedling containers should preferably be suspended in racks, or held in trays that allow free drainage from the bottom of the container, at a height of about one metre above the nursery floor, which should be gravel or crushed rock. A soil floor is a potential source of pathogen propagules which can be splashed onto the seedlings. If seedlings in containers are to be placed at ground level, the surface should be material like concrete or deep, well-drained gravel or crushed rock, that can be regularly cleaned and treated with chlorinated water or fungicides. The use of sterilants on benches, plant containers and the floor can help to reduce disease. The practice of carrying over planting stock in the nursery should be minimised or eliminated as such stock may allow pathogens to persist or even to build up in the nursery environment. For example, in the eucalypt cutting program in Brazil, glasshouses are filled and then emptied in single operations and a sterilant is used regularly on benches and soil (Ferreira and Muchovej 1991; Ferreira 1993). Mature trees around nurseries should be considered as a potential source of inoculum of certain pathogens and the trees may have to be removed or the nursery located at a distance from them. Removal of alternative hosts of a pathogen and the elimination of weeds which may be alternative hosts or which may create conditions favourable for a particular disease are also important. In existing nurseries with disease problems, particularly in seedbeds, infested areas should be excluded from operation or the entire nursery should be abandoned in favour of a new, pathogen-free site (Brown and Baxter 1991).

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21.1.3 Physical control methods Soil can be heated by either steam or dry heat to temperatures lethal to soilborne pathogens but not high enough to cause chemical or physical damage to the soil. For both steam and dry heat, the soil must be kept moist and temperatures of 80°C to 85°C must be maintained throughout the mixture for 30 minutes. Soil solarisation can be used to raise the soil temperature to a level high enough to inactivate plant pathogens (Katan 1981, 1985). When clear polythene film is spread over soil exposed to the sun, solar energy is trapped beneath the film and heats the soil. Although the incoming radiation can penetrate the film, the longer wavelength energy reradiated from the soil cannot pass out through the film. Solar heating is effective only when used on moist soils for some days or weeks. Nursery plots given a solarisation treatment for up to 55 days were found to have 64% to 75% lower incidence of the damping-off pathogens Pythium (P.) and Fusarium (Hildebrand 1985), indicating the potential of this technique in disease management. Solarisation of potting mixes was effective in controlling soilborne pathogens in Australia (Duff and Barnaart 1992). During solarisation of a nursery potting mixture under single and double layers of clear 50 micrometre polythene sheeting in the tropical environment of Darwin, temperatures followed an annual pattern with the highest temperatures at 25 cm depth ( 51°C, 44.6°C, 37°C under double and single layers of polythene and the uncovered control, respectively) occurring during summer (November) (Duff and Connelly 1993). Covering soil with 40 micrometre thick transparent polythene sheets during the hot period of May in Pakistan increased soil temperatures to 65°C and 52°C in the top five centimetres of moist (field capacity) and dry soil, respectively (Sheikh and Ghaffar 1984). Solarisation of seedbeds for 60 days at Dehra Dun, India, apparently eliminated a Pythium sp. and Fusarium solani (Mart.) Sacc., Fusarium moniliforme J.Sheld. and Fusarium chlamydosporum Wollenw. & Reinking, and significantly improved subsequent germination of seed of a Eucalyptus hybrid (Shukla et al. 1990).

21.1.4 Soil fumigation and chemical sterilisation Soil fumigation with gaseous (or gas-forming) chemicals such as methyl bromide, chloropicrin, 490

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formaldehyde or metam has been used commonly in the control of root rot and damping-off diseases in seedbeds, or for sterilisation of container mixes before use. Treatments have to be applied before planting and sufficient time must be allowed for adequate soil aeration so that any residual chemical vapours can dissipate, as fumigants are toxic to plants. Methyl bromide is being phased out for environmental reasons (Ristaino and Thomas 1997; Champ 1999; Collinson et al. 1999; Porter et al. 1999) and so its long-term availability as a soil treatment is in doubt.

21.1.5 Post-sterilisation hygiene Where seedbeds or growing mixes have been sterilised, strict attention to hygiene is essential during all subsequent stages of nursery management. The introduction of pathogens after sterilisation may result in very heavy losses due to the absence from the soil or container mix of natural competitors or antagonists of pathogens (e.g. natural biological control organisms). For example, the use in Haiti of commercial imported potting media which had been sterilised resulted in more serious problems with damping-off than did the non-sterile local mixes (Josiah and Allen-Reid 1991). Rhizoctonia solani J.G.Kühn caused damping-off of several tree species, including E. deglupta, following soil fumigation in Hawaii, emphasising the need to practise sanitation following soil sterilisation (Ko et al. 1973). In a study of the use of solarisation for control of damping-off in E. obliqua, while both steaming and solarisation of a sandy loam potting mixture reduced the disease, damping-off was increased when nursery water from a contaminated source (containing Phytophthora cinnamomi Rands, Phytophthora cryptogea Pethybr. & Laff. and three species of Pythium) was used on either steamed or untreated potting mixture but not when used on solarised mixture (Kassaby 1985). Possibly the solar treatment did not eliminate all the saprophytic microorganisms in the soil, rendering the soil at least partly suppressive to the pathogens. Strict post-sterilisation hygiene measures for seedbeds should include the sort of measures adopted in the Queensland system to reduce the likelihood of contamination of the area (Brown 1985). Similarly, measures should be taken to avoid contamination of sterilised container mixes from untreated soil, dirty containers and nursery equipment, and contaminated water.

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21.1.6 Water treatment Pathogen inoculum has been found in the water supply used for irrigation in a eucalypt nursery (see Chapter 8). Where the water supply is recycled from the nursery via a storage dam, the inoculum can increase to damaging levels. In Brazil, there have been problems of salt buildup as a result of recycling of nursery water (F.A. Ferreira, pers. comm.). There are several ways to ensure that a nursery water supply is free of inoculum of pathogens (Brown and Baxter 1991). These include use of a clean reticulated water supply, filtration, irradiation with ultraviolet light or chlorination.

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of triadimefon for powdery mildew and alternating sprays of benomyl and iprodione for grey mould (Wardlaw and Phillips 1990). [Fungicides will be referred to by their common chemical name according to Tomlin (1997)]. Triadimefon could be mixed with either benomyl or iprodione without phytotoxic effects, thus allowing the application of mixtures. In other situations a single chemical may control two diseases. For example, prochloraz gave good control of powdery mildew and also offered the prospect of controlling grey mould (Wardlaw and Phillips 1990).

21.1.8 Biological control

‘In-line’ filtration (5 µm pore size cartridge) of water used for seed germination, propagation and glasshouse work resulted in a very large decrease in damping-off in eucalypts grown in steam-sterilised soil mixes (Palzer 1980). The only damping-off pathogen which persisted in the nursery was the airborne Botrytis cinerea. Ultraviolet irradiation, in combination with water filtration (sand and cartridges of 100, 20 and 5 µm pore sizes) eliminated fungi, including Fusarium spp. and pythiaceous species, from river water used for irrigation in citrus and subtropical fruit nurseries (Grech et al. 1989). A reduction in the levels of propagules occurred with each stage in water treatment, but only after filtration and irradiation combined were no pythiaceous fungi detected. Filtration of the water supply for eucalypt nurseries has been used in Brazil (F.A. Ferreira, pers. comm.).

The use of biological control involving living microorganisms, byproducts of microorganisms or organic amendments is applicable in the nursery. Certainly, good nursery management requires an awareness that saprophytic microorganisms in container mixes may contribute to natural biological control of certain pathogens. Container mixes that have been sterilised should not be used for at least two weeks after sterilisation to allow aerial recolonisation of the mixes by saprophytic microorganisms; alternatively they could be inoculated with selected strains of microorganisms antagonistic to pathogens like Cylindrocladium spp. and Rhizoctonia solani (Ferreira 1993). Because of environmental concerns about the use of fungicides and soil fumigants, greater emphasis should be given to the use of biocontrol agents in forest nurseries.

Chlorination of water supplies using calcium hypochlorite, sodium hypochlorite or chlorine gas (Rochecouste 1985) requires a pH in the water of below 7.0 and should result in a minimum residual chlorine level of two micrograms per gram after treatment. It is best carried out in an open tank from which the excess chlorine is able to escape before use of the treated water so as to avoid damage to seedlings.

21.2 Two minimal-disease nursery systems

21.1.7 Fungicide use Although chemical control treatments generally differ between diseases, often a chemical control strategy is aimed at more than one disease, and, depending on the diseases to be controlled, it is sometimes possible to apply mixtures of fungicides (Sharma et al. 1984). For example, control of a powdery mildew (Oidium spp.) and grey mould (Botrytis cinerea) on E. nitens required applications

The two nursery systems discussed here show how disease prevention can be incorporated into nursery management protocols. One was developed in southern Queensland for bare root Pinus seedling production in areas where Ph. cinnamomi caused serious problems in seedbed nurseries. The system would be equally applicable in a eucalypt nursery. The other was developed in Brazil for container production of eucalypt planting stock.

21.2.1 The Queensland bare-root nursery system Soil fumigation was an effective, but costly, means of producing Pinus planting stock free from Ph. cinnamomi, even in nurseries with a serious disease problem (Brown 1985). One significant problem associated with seedbed fumigation in the 491

D I S E A S E S

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P A T H O G E N S

O F

subtropical to tropical environment in Queensland was the growth of soft succulent Pinus seedlings (Brown and Baxter 1991). Therefore, a nursery system based on ‘hygiene’ was developed in the late 1960s to replace soil fumigation for the control of Phytophthora root rot of bare-root seedlings of Pinus spp. and also to allow extensive mechanisation of nursery operations. This system involves exclusion of the pathogen by quarantine and hygiene measures, and cultural practices such as crop rotation and regular deep ripping of seedbeds. Experience with this system has shown that long-term mechanised nursery operations (more than 25 years of production in a 20 ha nursery) using strict hygiene principles can maintain a seedbed nursery free from soilborne pathogens such as Ph. cinnamomi (Brown 1985; Brown and Baxter 1991; A.G.M. Baxter, pers. comm.). The basis of hygiene in the nursery starts with selection of the site, which must have suitable soils for seedling growth and preferably be sited on a ridge top with outward drainage in all directions. The site must be free from serious soilborne pathogens. Once selected, the site is subject to hygiene management. Thus for all operations starting with clearing of the site, access by machinery, vehicles and staff is kept to a minimum and under no circumstances is unfumigated soil taken either deliberately or accidentally onto the site. During the initial clearing and construction of the nursery, machines and vehicles are cleaned away from the site before use. Secure perimeter fencing with controlled access points and, if necessary, drainage away from the site, is established as early as possible. The fencing is intended to prevent access by large animals and to control access by machines, vehicles and staff. Ancillary nursery facilities such as machinery storage sheds and seedling sorting and packing facilities are fully within, or form part of, the perimeter fencing. Access to the nursery by machines and vehicles is restricted to essential needs only, and as far as possible, nursery machinery remains within the nursery perimeter fence. Machines and vehicles taken into the nursery are free of soil and are driven through a wheel bath containing formaldehyde. Staff going into the nursery have to walk through a formaldehyde boot bath. Irrigation water should be free from potential pathogens; if necessary this can be ensured by chlorination.

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Special precautions are taken to ensure that pathogens are not introduced with nursery-bed additives of any type. If soil or organic material has to be introduced then it is fumigated. Inorganic fertilisers do not need to be treated but care is taken to ensure that no soil is introduced to the nursery on bags or other containers. Where the use of mycorrhizal inoculum is necessary, the source must not be directly from an existing plantation or similar area. Historical records in Queensland leave little doubt of widespread distribution of Ph. cinnamomi into new Pinus nurseries with pine needle litter used to introduce mycorrhizas (B.N. Brown, unpubl. data). Culture-based inoculum would be ideal, but in one Queensland nursery, remote from existing Pinus stands, macerated suspensions from surface sterilised sporocarps of Suillus and Rhizopogon were applied to seed just before sowing, resulting in successful inoculation of the new seedbeds. Crop rotation is integral to the ‘hygiene’ nursery system. The Queensland system allows a three-year cycle for each 10-month Pinus crop. During the intervening period a green manure crop is grown and then worked into the soil. The beds are then prepared for the subsequent pine crop. The soils used in Queensland develop hard pans as result of longterm use as nursery beds, a condition believed to favour the development of root rot problems. Thus, a deep ripping is performed during bed preparation for each pine crop.

21.2.2 The Brazilian eucalypt container system Eucalypt diseases in seedling and cutting production programs in Brazil are controlled through an integrated container nursery system aimed at maintaining healthy plants with minimal fertiliser and fungicide usage under hygienic conditions (Ferreira and Muchovej 1991; Ferreira 1993). The management of eucalypt seedling diseases can be divided into four plant growth stages: 1

pre-emergence or sowing

2

prethinning or abiotic disease

3

post-thinning or disease free

4

closure.

These stages usually last 10, 30, 20 and 60 days, respectively. The main pathogens encountered are Cylindrocladium scoparium Morgan (possibly

M ANAGEMEN T

OF

D ISEA SE

Cylindrocladium candelabrum Viégas—see Chapter 9), Cylindrocladium gracile (Bugnic.) Boesew. (syn. Cylindrocladium clavatum Hodges & L.C.May) and Rhizoctonia solani during the pre-emergence and prethinning stages, and Botrytis cinerea and Cylindrocladium spp. during the closure stage. Disease control practices used in the hygiene regime include the use of seed, substrates and water free from soilborne pathogens and management practices to control Botrytis cinerea during the closure stage. Plants are produced in containers suspended one metre above a crushed rock ground cover to avoid contact with water-splashed soil particles. Container substrates consist of materials (e.g. vermiculite) free from soilborne pathogens, or organic-based substrates which are sterilised with methyl bromide or steam. Sterilised substrates are allowed a post-treatment period of at least two weeks to allow recolonisation by airborne saprophytic microorganisms or are inoculated with microorganisms antagonistic to Cylindrocladium spp. and Rhizoctonia solani. Growing racks and containers are washed and immersed for three minutes in a chlorinated-fungicide mixture (Table 21.1). Seeds are collected and processed so that they do not have contact with soil which could carry soilborne pathogens and are sown directly into the containers. In smaller nurseries, Botrytis disease during the closure stage is effectively controlled by thinning seedlings twice for uniform height and at the same time culling diseased or dead seedlings and removing senescent and fallen leaves. However, in larger nurseries this manual rouging is not feasible and chemical control is used.

21.3 Control of particular nursery diseases 21.3.1 Damping-off Although damping-off was considered to be the most important nursery disease of exotic plantation species in South Africa (Lückhoff 1964), it was easily controlled by appropriate nursery management practice. Later, Donald (1986) discussed protection against damping-off and root rot problems in South African forest nurseries and indicated that emphasis is placed on prevention of disease, rather than cure. In Australia, where damping-off has been a problem with eucalypt species in forest nurseries, losses are

DURING

E UCA LY PT P ROPA GA TION

C H A P T E R

21

now avoided by the use of composted potting mixtures, sterilised soil in germination trays and nursery hygiene systems and by alteration in the time of sowing. The virtual elimination of damping-off in Brazil by using a suspended container system as discussed in the previous section (Ferreira and Muchovej 1991) clearly shows that nursery procedures, without resort to the use of fungicides, can greatly reduce losses from damping-off. Other preventative and control measures effective against damping-off include avoiding overuse of seedbeds and not reusing germination mixtures. Soil or container mixes should be light textured with good drainage and be slightly acidic (an inorganic acid such as dilute sulphuric acid, or granular sulphur or ammonium sulphate can be used to lower the pH to 5–6). Only well-rotted organic materials should be used in container mixtures or soils (e.g. peat, composted rice hulls or coconut husk) (Kijkar 1991) and materials high in nitrogen such as poultry manure should be avoided. Fumigants used for control of damping-off include dazomet, chloropicrin, formaldehyde (Norani 1987), methyl bromide (Reis and Hodges 1975) and vorlex (a mixture which contains methyl isothiocyanate, a chemical that is released in the soil by the breakdown of dazomet). Unless sterilised container mixes and good hygiene are being used, very susceptible tree species should not be sown during or just before periods of high rainfall or humidity. Sharma et al. (1985) and Sharma and Mathew (1991) recommended that once damping-off appears, watering should be reduced to a bare minimum, even being stopped for a day or two, depending on the weather conditions, until fungicides can be applied. Avoidance of overwatering, the prevention of overshading of the seedbeds and frequent weeding will reduce the incidence of damping-off disease. Biological control agents can be added directly to the potting medium, or, as shown by Huang and Kuhlman (1991a, 1991b), the potting medium can be amended to promote the growth of antagonistic microorganisms. In laboratory tests, Trichoderma viride Pers. inhibited the growth of all pathogenic fungi associated with damping-off in Eucalyptus and in glasshouses it was effective in controlling Macrophomina phaseolina (Tassi) Goid. and Rhizoctonia solani (Taha et al. 1987).

493

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Specific uses of chemicals for disease prevention and/or control in eucalypt nurseries

Types of application: GS, general sterilant; FS, foliar spray, FG, fumigant, presowing; PS, presowing; SD, seed dressing; SDR, soil drench @ = interval between applications; ( ) = longevity of effectiveness.

Active chemical

Strength (%A)

Type of application

Sterilant mixture

Chlorine + Captan

0.08 + 0.12

GS

Ferreira (1997)

Sterilant for racks and containers

Chlorine + Thiram + Captan

0.078 + 0.21 + 0.12

GS for 3 minutes

Ferreira (1993); Ferreira and Muchovej (1991)

Chlorine solution

Chlorine

0.0002 (free residual chlorine level)

GS

Rochecouste (1985); Brown and Baxter (1991)

Formalin solution

Formaldehyde

5.0

GS

Brown (1985); Brown and Baxter (1991)

Methyl bromide

Methyl bromide ± 2% Chloropicrin

FG—plant beds under plastic

490 kg/ha

Brown (1985)

Methyl bromide

Methyl bromide

FG—potting substrate under plastic

150 mL/m3

Ferreira (1989)

Methyl bromide

Methyl bromide

FG—potting substrate under plastic

30–40 mL/m2

Ferreira (1989)

Methyl bromide

Methyl bromide

FG—rice straw under plastic

50–100 mL/m3

Ferreira (1989)

Chloropicrin

Chloropicrin

FG soil injection and then under plastic

270 L/ha

Brown (1985)

MBR–CP

Methyl bromide + Chloropicrin

50 + 50

FG soil injected and then under plastic

390 kg/ha

Brown (1985); Brown and Baxter (1991)

MBR–CP

Methyl bromide + Chloropicrin

33 + 66

FG soil injected and then under plastic

390 kg/ha

Brown (1985)

Di-Trapex

Methyl isothiocyanateB

23.5

FG soil injected and then under plastic

610 L/ha

Brown (1985)

Mixture/formulation

Rate

References

General

Alternating fungicide mixes when pathogen unknown 1989 mixture

Thiabendazole + Captan then Benomyl + Captan

0.12 + 0.1

First FS

0.035 + 0.1

Second FS

1991 mixture

Thiabendazole + Captan alt. Benomyl + Thiram

0.035 + 0.1

4 alternating FS @ 3 or 4 days for 2 weeks

494

0.035 + 0.1

Ferreira (1989)

Ferreira and Muchovej (1991)

MANAGEMENT

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DISEASE

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21

Prophylactic schedule for container nursery Schedule

Carbendazim then Mancozeb then Methyl ethyl mercuric chloride followed 2–3 months laterC with Carbendazim

0.01 0.1 0.005

Three separate SDR on day of sowing

0.02–0.05D

FS

Sharma and Mohanan (1986)

Damping-off Di-Trapex Methyl bromide

Methyl isothiocyanate Methyl bromide + Chloropicrin

FG covered with plastic sheet

55 mL/m2 2

Sharma and Mohanan (1991) Sharma and Mohanan (1991)

98.0 + 2.0

FG covered with plastic sheet

100 g/m

Formalin (commercial) Formaldehyde

38.0

SDR

250 mL in 4 L of water/m2

Norani (1987)

Cheshunt solutionE

Copper sulphate Ammonium carbonate (fine powders)

Ratio of 2 to 11

SDR

35 g per 10 L over 3 m2

Queensland Forestry Department (1963)

Bavistin Dithane M-45 Emisan-6

Carbendazim then Mancozeb then Methyl ethyl mercuric chloride

0.01 0.01 0.0025

SDR separately @ 4 hour intervals

Sharma et al. (1985); Sharma and Mathew (1991)

Sharma and Mohanan (1991)

Kerala schedule (a) (see below) Chlorothalonil

Chlorothalonil

0.006–0.033

Regular spraying

Zhou Dequn and Sutherland (1993)

Carbendazol

Carbendazol

0.050–0.063

Regular spraying

Zhou Dequn and Sutherland (1993)

Pre-emergence and postemergence damping-off caused by Thanatephorus cucumeris (Rhizoctonia solani) Brassicol

PCNB 0.05 (pentachloronitrobenzene)

SDR 3 times

Sharma and Mohanan (1991)

Postemergence damping-off caused by Thanatephorus cucumeris (Rhizoctonia solani) Captan

Captan

0.05

SDR 3 times

Sharma and Mohanan (1991)

Vitavax

Carboxin

0.05

SDR 3 times

Sharma and Mohanan (1991)

Mixture

Thiabendazole + Thiram

0.12 + 0.15

Ferreira (1989)

0.13

Ferreira (1989)

Postemergence damping-off caused by Pythium Captan

Captan

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Specific uses of chemicals for disease prevention and/or control in eucalypt nurseries (continued)

Mixture/formulation

Active chemical

Strength (%A)

Type of application

Rate

References

Postemergence damping-off caused by Fusarium solani Benlate

Benomyl

0.01

SDR

57 g/kg soil

Michail et al. (1986)

TBZ

Thiabendazole

0.01

SDR

57 g/kg soil

Michail et al. (1986)

Postemergence damping-off caused by Verticillium spp. Bavistin

Carbendazim

0.2

SD—dipped for 5 minutes prior to sowing

Harsh et al. (1992)

Topsin-M

Thiophanate methyl

0.2

SD—dipped for 5 minutes prior to sowing

Harsh et al. (1992)

Kerala nursery disease complex (damping-off, web blight, Cylindrocladium blight) Mixture

Five applications as SDR & FS

Sehgal (1983)

0.005 + 0.02 + 0.02

SDR just after sowing

Sharma and Mohanan (1991)

0.01 + 0.01

SDR & FS 54 days after emergence

0.01

SDR & FS 117 days after emergence

Benomyl Carbendazim Captafol

Prophylactic Methyl ethyl mercuric sequential treatments chloride + Mancozeb + Carbendazim then Methyl ethyl mercuric chloride + Carbendazim then Carbendazim

Botrytis cinerea Standard fungicides

Captan + Benomyl alternated with Chlorothalonil

Alternating fungicide mixes

Benomyl + Thiram alternated with Benomyl + Captan

0.035 + 0.15

Alternating sprays

Chlorothalonil then Carbendazim then Fenaminosulf

0.15 0.25 0.14

Alternating sprays

Benomyl then Iprodione

496

470 to 940 L of water/ha FS @ 10–14 days 940 L of water/ha

0.56 kg/ha + 0.56 kg/ha 0.95–1.9 L/ha

Russell (1990)

4 alternating FS @ 3 or 4 days for 2 weeks

Ferreira and Muchovej (1991)

Alternate FS @ 7 days

Zhou Dequn and Sutherland (1993)

Alternate @ 14 days

Wardlaw and Phillips (1990)

0.035 + 0.1

MANAGEMENT

OF

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DURING

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21

Cylindrocladium blights and leaf spots SD (90 days)

Argoll-3 0.01–0.02

10 mg /g seed

Rattan and Dhanda (1985) Sharma et al. (1985); Sharma and Mathew (1991)

Bavistin

Carbendazim

Bavistin

Carbendazim

Captafol

Captafol

SD (30 days)

10 mg /g seed

Rattan and Dhanda (1985)

Captaf

Captan

SD (90 days)

10 mg /g seed

Rattan and Dhanda (1985)

Captan

Captan

Ceresan

PMA (phenyl mercuric acetate)

SD (90 days)

0.2

Deuter Dithane M-45

Mancozeb

Panoram

Fenfuram

1 or 2 FS and SDR @ 7 days

0.5

FS

Rattan and Dhanda (1985)

Sehgal (1983)

SD (30 days)

10 mg /g seed

Rattan and Dhanda (1985)

SD (30 days)

10 mg /g seed

Rattan and Dhanda (1985)

3 FS @ 7 days SD (90 days)

0.2

10 mg /g seed

Rattan and Dhanda (1985) 10 mg /g seed

Rattan and Dhanda (1985) Sehgal (1983)

Thiram

Thiram

Thiram

Thiram

SD (90 days)

FS 10 mg /g seed

Rattan and Dhanda (1985)

Topsin-M

Thiophanate methyl

SD (30 days)

10 mg /g seed

Rattan and Dhanda (1985)

Cylindrocladium scoparium Benlate 50WP

Benomyl

0.084

FS @ 14 days

Barnard (1984)

Benlate 50WP

Benomyl

0.084

SDR @ 14 days

Barnard (1984)

Daconil 2787

Chlorothalonil

0.192

FS @ 7 days

Barnard (1984)

Thiram

Thiram

0.2

Alfenas et al. (1988)

Leaf spots caused by Cylindrocladium quinqueseptatum Mancozeb

Mancozeb

0.16

FS

+ WAF

Bolland et al. (1985)

Stem lesions caused by Cylindrocladium quinqueseptatum Benomyl

Benomyl

0.025

FS

+ WA

Bolland et al. (1985)G

Captan

Captan

0.108

FS

+ WA

Bolland et al. (1985)

Mancozeb

Mancozeb

0.16

FS

+ WA

Bolland et al. (1985)

Cylindrocladium root rot (Cylindrocladium curvatum) Bavistin

Carbendazim

0.02

1 or 2 SDR

Sharma et al. (1985)

Cylindrocladium pteridis Benomyl

Benomyl

SDR (53 days)

2–4 g/m2

Bedendo and Krügner (1988)

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Specific uses of chemicals for disease prevention and/or control in eucalypt nurseries (continued)

Mixture/formulation

Active chemical

Strength (%A)

Type of application

Rate

References

335 kg/ha

Cordell and Skilling (1975); Cordell et al. (1989)

Cylindrocladium species MBR-CP

Methyl bromide + Chloropicrin

67 + 33

FG soil injected and then under plastic

Alternating fungicide mixes

Benomyl + Thiram then Benomyl + Captan

0.035 + 0.15 0.035 + 0.1

4 alternating FS @ 3 to 4 days for 2 weeks

Ferreira and Muchovej (1991)

Phaeophleospora (Kirramyces) epicoccoides Benlate

Benomyl

0.035

FS @ 14 days

Ferreira and Muchovej (1991)

Bavistin

Carbendazim

0.05

FS @ 14 days

Ferreira and Muchovej (1991)

Bavistin

Carbendazim

0.02

2 FS @ 7 days

Sharma et al. (1985)

Dithane M-45

Mancozeb

0.2

FS @ 10 days

Harsh et al. (1987)

Dithane M-45

Mancozeb

0.2

2 FS @ 90 days

Jamaluddin et al. (1985)

Zineb 65WP

Zineb

0.13

FS @ 7 days

Chipompha (1987)

Macrophomina phaseolina MBR-CP

Methyl bromide + Chloropicrin

57 + 43

FG injected then covered with plastic

360 kg/ha

Smith and Krugman (1967)

MBR-CP-PBR

Methyl bromide + Chloropicrin + Propargyl bromide

61 + 31 + 8

FG injected then covered with plastic

230 kg/ha

Smith and Krugman (1967)

Bavistin

Carbendazim

0.1 – 0.2

SDR

Soni et al. (1985); Jamaluddin et al. (1987)

Dithane M-45

Mancozeb

0.2

SDR

Soni et al. (1985); Jamaluddin et al. (1987)

Mycosphaerella species Daconil 2787 (75WP)

Chlorothalonil

FS @ 14 days

3.4 kg/ha + WA

New Zealand Forest Service (1977); Dick and Gadgil (1983); Ray (1991)

Chlorothalonil

Chlorothalonil

FS @ 21 days

2.55 kg/ha

van Dorsser (1981)

Root rot caused by Phytophthora cinnamomi Various soil fumigantsH

498

Brown (1985)

MANAGEMENT

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Basamid

Dazomet

FG granules worked in and then covered with polythene sheet or soil watered daily for 7 days

30 g/m2

Donald and von Broembsen (1977)

Vapoweeder

VapamI

Covered with polythene sheet or soil watered daily for 7 days

100 mL/m2

Donald and von Broembsen (1977)

Methyl bromide

Methyl bromide

FG under polythene sheet

0.125 kg/m2 J

Donald and von Broembsen (1977)

ETMT

Etridiazole

SDR

To concentration of 50 µg/g in soil

Bertus (1974)

Aliette

Fosetyl-Al

80% WP

SDR

4–16 g a.i./m2

Bertus and Wood (1979)

Fongarid

Furalaxyl

25% WP

SDR

1.0 g a.i./m2

Bertus and Wood (1979)

2

Bertus and Wood (1979)

Ridomil

Metalaxyl

25% WP

SDR

0.5 g a.i./m

Ridomil 5W

Metalaxyl

0.001–0.007

SDR

25 mL per 5 cm pot

0.6 mg a.i/mL

SDR

21

Cho (1981)

Stem lesions caused by Phytophthora cinnamomi Dimethomorph

Dimethomorph

Marks and Smith (1990)

Aliette

Fosetyl-Al

1.0 mg a.i/mL

SDR

Marks and Smith (1990)

Ridomil

Metalaxyl

2.0 mg a.i/mL

SDR

Marks and Smith (1990)

Stem disease (Phytophthora cactorum, Phytophthora citricola and Pythium anandrum) Ridomil

Metalaxyl

FS @ 14 days

Wardlaw and Palzer (1985)

Powdery mildews Benlate

Benomyl

FS @ 14 days

Ferreira and Muchovej (1991)

Bayleton

Triadimefon

FS @ 14 days

Wardlaw and Phillips (1990); J.A. Simpson (pers. comm.)

Octave then Bayleton

Prochloraz then Triadimefon

FS alternate

Wardlaw and Phillips (1990)

Sulphur

Wettable sulphur

Sulphur

Colloidal sulphur

0.035

0.25

FS @ 14 days

Ferreira and Muchovej (1991)

FS

Marks et al. (1982)

Rust (Puccinia psidii) Copper

Copper oxychloride

0.16–0.2

FS @ 7 days

Ferreira and Muchovej (1991)

Mancozeb

Mancozeb

0.16–0.2

FS @ 7 days

Ferreira and Muchovej (1991); Ferreira (1997a)

Triadimenol

Triadimenol

0.07; 0.075

FS @ 7 days

Ferreira and Muchovej (1991); Ferreira (1997a)

Triforine

Triforine

0.028

FS @ 7 days

Ferreira and Muchovej (1991); Ferreira (1991)

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Specific uses of chemicals for disease prevention and/or control in eucalypt nurseries (continued)

Mixture/formulation

Active chemical

Strength (%A)

Type of application

Rate

References

Web blight caused by Thanatephorus cucumeris (Rhizoctonia solani) Di-Trapex

FG under plastic sheet

Methyl isothiocyanate

55 mL/m2 100 g/m

2

Sharma and Mohanan (1991) Sharma and Mohanan (1991)

Methyl bromide

Methyl bromide + Chloropicrin

98.0 + 2.0

FG under plastic sheet

Emisan-6

Methyl ethyl mercuric chloride

0.005

SDR

Sharma et al. (1985); Sharma and Mathew (1991)

Carbendazim

Carbendazim

0.05

PS SDR

Sharma and Sankaran (1987); Sharma and Mathew (1991)

Bayleton

Triadimefon

0.08

FS

Mehrotra (1998)

Kerala schedule (b) (see below)

Sharma and Mohanan (1991)

Kerala schedule (c) (see below)

Sharma and Mohanan (1991)

Root and stem rots caused by Thanatephorus cucumeris (Rhizoctonia solani) Kerala schedule (a)

Kerala schedule (b)

Kerala schedule (c)

500

Copper oxychloride + Carbendazim + Quintozene

0.025 + 0.025 + 10 g/m2

FS on 2–4-day-old plants

Carbendazim + Quintozene

0.1 +15 g/m2

FS on 26–28-day-old plants

Carbendazim

0.05

FS on 73–75-day-old plants 2

7 days PS

Quintozene

10 g/m

Copper oxychloride + Carbendazim

0.025 + 0.05

FS on 2–4-day-old plants

Copper oxychloride + Carbendazim

0.05 + 0.1

FS on 26–28-day-old plants FS on 73–75-day-old plants

Carbendazim

0.05

Captan + Carbendazim

0.025 + 0.025

FS on 2–4-day-old plants

Captan

0.1

FS on 26–28-day-old plants

Carbendazim

0.05

FS on 73–75-day-old plants

Sharma and Mohanan (1991)

Sharma and Mohanan (1991)

Sharma and Mohanan (1991)

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PS mixed into soil to 10 cm depth

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50–100 kg/ha

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Terrachlor

PCNB (Pentachloronitrobenzene)

Ko et al. (1973)

Fungicide mix

Thiabendazole + Thiram

0.12 + 0.15

4 FS @ 3–4 days for 2 weeks

Ferreira and Muchovej (1991)

Emisan-6

Methyl ethyl mercuric chloride

0.005

1 or 2 SDR @ 7 days

Sharma et al. (1985)

Fungicide mix

Benomyl + Captan

0.035 + 0.120

4 FS @ 3–4 days for 2 weeks

Ferreira (1997b)

0.005

1 or 2 SDR @ 7 days

Sharma et al. (1985)

0.2

FS @ 7 days

Ferreira and Muchovej (1991)

0.2

FS

Jamaluddin et al. (1987)

Root rot caused by Athelia rolfsii Emisan-6

Methyl ethyl mercuric chloride

Leaf spots caused by Alternaria tenuissima Dithane-M45

Mancozeb

Curvularia prasadii and Curvularia lunata Dithane M-45

Mancozeb

General control of diseases in eucalypt cutting programs Chlorine solution

Chlorine

0.08

Fully immerse new cuttings for 3 minutes and rinse with water

Ferreira and Muchovej (1991); Ferreira (1993); Ferreira (1997b)

Alternating fungicide sprays

Benomyl + Thiram alt. Benomyl + Captan

0.035 + 0.15 0.035 + 0.1

Alternating FS @ 3–4 days

Ferreira and Muchovej (1991); Ferreira (1993)

Fungicide mix sprays

Benomyl + Captan

0.035 + 0.1

4 FS @ 3–4 days for the first 2 weeks in the shadehouse

Ferreira (1997b)

Control when Rhizoctonia solani disease or sclerotia observed on shoots before cuttings taken Cutting dip

Chlorine + Captan + WA

0.08 + 0.12 + 0.05

Immerse new cuttings for 3 minutes and rinse in water

Ferreira (1993); Ferreira (1997b)

Alternating fungicide sprays

Benomyl + Thiram alt. Benomyl + Captan

0.035 + 0.15

Alternating FS @ 3–4 days

Ferreira (1993)

Floor sterilant

Chlorine + Thiram + Captan

0.078 + 0.21 + 0.12

Soak floors every 40 or 80 days

Ferreira (1993)

0.035 + 0.1

A

% a.i. (active ingredient) unless otherwise specified. Di-Trapex = methyl isothiocyanate at 235 g/L in mixture of dichloropropanes and dichloropropenes. C Before onset of monsoon. D 0.02% in low rainfall areas. E Cheshunt mixture is prepared by grinding copper sulphate and ammonium carbonate separately into fine powders and mixing in the ratio of 2 to 11, respectively. The mixture is stored in a tightly stoppered glass or earthenware container (not metal) for at least 24 hours before use. After storage, the dry mixture is dissolved at the rate of 35 g in 10 L water, which is sufficient for 3 m2 of seed bed. Any metal equipment used for mixing or applying Cheshunt mixture should be well washed after use as the mixture is corrosive. F +WA=plus wetting agent. G Only effective on E. cloeziana. H See near top of table under ‘General’. I Sodium N-methyl dithiocarbamate dihydrate. J In 1.69 L water/m2. B

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The use of new and high quality seed to increase the rate and uniformity of seed germination has been reported to reduce damping-off (Chalermpongse 1987). Seed should be sown evenly and excessive seedling density avoided. Seed can be treated with a fungicide (e.g. captan, quintozene, thiram) prior to sowing. For some species the results may be inconsistent and sometimes seed dressing fungicides may be phytotoxic. Thus, it is advisable to conduct trials with particular tree species and available fungicides before seed treatment is practised on a large scale. Appropriate fungicides (Table 21.1) can be applied as a drench (with about 10 L water per m2) at least once per week when damping-off occurs. Cheshunt mixture (Table 21.1) is a simple but useful formulation which provides an alternative to commercial fungicides (Queensland Forestry Department 1963). Damping-off in Eucalyptus was effectively controlled by soil drenching with benomyl (Taha et al. 1987) and treating seedbeds with carbendazim, mancozeb and methyl ethyl mercuric chloride separately as soil drenches at intervals of four hours between treatments, instead of normal watering (Sharma et al. 1985; Sharma and Mathew 1991) (Table 21.1). However, methyl ethyl mercuric chloride is highly toxic and is therefore not recommended. Spot treatment with quintozene-based fungicides was used to control damping-off which occurred despite heat sterilisation of nursery soil and post-treatment hygiene measures (Arentz 1991). Damping-off in eucalypts may be reduced by the use of mycorrhizal inoculum. In pot studies, addition of the mycorrhizal basidiomycetes, Rhizopogon luteolus Fr. and Pisolithus tinctorius (Pers.) Coker & Couch, reduced damping-off in E. tereticornis caused by Pythium aphanidermatum (Edson) Fitzp. to the same extent as the fungicide metalaxyl (Narayana Bhat et al. 1997).

21.3.2 Grey mould caused by Botrytis cinerea To control grey mould, cultural measures should be emphasised (Peace 1962; Ellis and Waller 1974; Marks et al. 1982; Mittal et al. 1987; Landis 1989; Sutherland et al. 1989; Russell 1990; Brown and Wylie 1991; Ferreira and Muchovej 1991). Such measures include using pathogen-free growing medium, containers and irrigation water, sterilising containers and growing surfaces between

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crops and using growing media with a good initial base of nutrients to minimise the need for later fertiliser applications (Landis 1989; Ferreira and Muchovej 1991; F.A. Ferreira, pers. comm.). Removal of dead plant debris and roguing of infected plants help reduce inoculum within a crop (Landis 1989; Brown and Wylie 1991; Ferreira and Muchovej 1991). Botrytis cinerea is seedborne in eucalypts (see Chapter 7) and the use of pathogen-free seed is advised (Ferreira and Muchovej 1991). Surface cleaning, sterilisation and fungicide treatment of forest tree seeds are possible control strategies for Botrytis (Mittal et al. 1987). However, because of the small size of eucalypt seed and the quantity of non-viable material in most eucalypt seed lots, these options may not be of value in commercial nurseries. Direct seeding can contribute to the reduction of problems due to Botrytis. The role of high humidity and free water on foliage in promoting this disease cannot be overemphasised. Srago and McCain (1989) advise less frequent irrigation to reduce disease, and it is important to reduce the duration of leaf wetness by encouraging air circulation, irrigating early in the day, using surfactants in the irrigation water, providing under-bench heating, or by force-drying foliage with fans (Landis 1989; Russell 1990). Hausbeck and Pennypacker (1991) showed that the activity of irrigation itself could increase the concentration of airborne conidia of Botrytis cinerea. Cultural procedures should be designed to avoid conditions that predispose eucalypt seedlings to Botrytis attack. In particular, seedlings should be kept healthy and vigorous and good ventilation should be maintained within a seedling crop (Gibson 1962; Peace 1962; Marks et al. 1982; Forestry Canada 1989; Landis 1989; Sutherland et al. 1989; Russell 1990; Brown and Wylie 1991). For example, in cooler areas of Brazil, lower temperatures combined with incorrect nutrient balance can result in seedlings with several weak or thin branches at their base; such seedlings are more susceptible to abiotic stress and Botrytis attack. These growth problems are avoided and Botrytis attack reduced during cold weather by growing eucalypt container stock in glasshouses for the first 40 to 50 days and by the use of organic substrates with a good initial base of nutrients in order to minimise the need for

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follow-up fertiliser applications (F.A. Ferreira, pers. comm.). Substrates such as vermiculite are not recommended as they are readily leached of nutrients, necessitating additional fertiliser applications. Ventilation can be improved by avoiding crowding, by improvement of glasshouse ventilation (removal of sidewalls and roof coverings), by use of ventilated styrofoam block containers (Forestry Canada 1989) or by keeping containerised plants off the ground. Improved lighting in nurseries reduces etiolation of shoots, a condition which is particularly favourable for development of grey mould (Sutherland et al. 1989). There are numerous reports that crowding of eucalypt nursery stock favours Botrytis disease (Riley 1960; Gibson 1962, 1975; Magnani 1964; Bakshi 1976; Marks et al. 1982; Neumann and Marks 1989; Brown and Wylie 1991). Much can be done to control the disease by thinning beds or by planting the stock into the field at the earliest opportunity (Gibson 1962). Ferreira and Muchovej (1991) advocate thinning before stock becomes too large and regular selection (at least twice after the seedling canopies have closed and crowding occurs) of stock for uniformity in size and removal of diseased and dead seedlings. Reduction in wounding of nursery stock is also important in reducing the incidence of Botrytis disease. In South Africa, Botrytis cinerea, along with Hainesia lythri (Desm.) Höhn., was shown to attack E. fastigata seedlings through wounds caused by fertiliser damage (South African Forestry Research Institute 1985). Protection of nursery plants against injury by autumn frost, which favours the disease, is recommended (Peace 1962; Mittal et al. 1987), although Phillips and Burdekin (1982) warned that covering the plants should be minimised to avoid raising the humidity of the beds, which also favours the disease. Chemical control of grey mould (Table 21.1) is virtually impossible without an integrated program of cultural control (Landis 1989; Sutherland et al. 1989). Botrytis cinerea frequently develops resistance to fungicides such as benomyl, dichloran, iprodione, quintozene, tecnazene, thiophanate-methyl and vinclozolin (Washington 1977; Holliday 1980; Ghini and Krügner 1987; Mittal et al. 1987; Landis 1989; Srago and McCain 1989; Moorman and Lease 1992; Latorre et al. 1994). Thus, prophylactic

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chemical use is to be discouraged unless there is a serious problem or a particularly susceptible species. If spraying is necessary, alternation of different types of fungicide is recommended. Protectant fungicides need to be applied so that they penetrate within the canopy, where grey mould mostly develops, and at regular intervals of one to two weeks because of new foliage growth and the rinsing effect of irrigation (Landis 1989; Russell 1990). Two-component, three-component or four-component mixtures of vinclozolin, chlorothalonil, cupric hydroxide and mancozeb at reduced rates were more effective and had longer residual efficacy (up to 21 days) than the fungicides applied singly against a benomyl-resistant, vinclozolin-sensitive strain of Botrytis cinerea (Moorman and Lease 1992). In Western Australia, a rotating schedule of iprodione, vinclozolin, benomyl and chlorothalonil was used to control Botrytis on eucalypts and in Tasmania benomyl and iprodione are alternated (Brown and Wylie 1991). The use of leaf wetness sensors allows monitoring for conditions favourable for infection as a basis for more timely application of fungicides (Russell 1990). Control of grey mould was achieved using free radical scavengers (antioxidants) (Elad 1992) and by application of Gliocladium roseum Bainier, a Penicillium sp., Trichoderma harzianum Rifai, Trichoderma viride and saprophytic yeasts as biocontrol agents (Elad et al. 1993, 1994; Sutton and Peng 1993).

21.3.3 Diseases caused by Cylindrocladium Early detection, diagnosis and evaluation of damage are essential for the control of Cylindrocladium diseases (Cordell et al. 1989). For example, if remedial measures are not taken immediately on the appearance of Cylindrocladium leaf blight in India [caused by a complex of species, including Cylindrocladium quinqueseptatum Boedijn & Reitsma, Cylindrocladium ilicicola (Hawley) Boedijn & Reitsma, Cylindrocladium gracile (syn. Cylindrocladium clavatum), Cylindrocladium scoparium and Cylindrocladium colhounii Peerally], mortality of up to 100% may result within one month (Sharma and Mathew 1991). Again, quarantine and hygiene measures are an important foundation for control of these diseases in eucalypt nurseries. It is important to identify and avoid infested nursery sites, to avoid contamination of

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clean sites through movement of infected seedlings or contaminated machinery between and within nurseries, to remove plant material following lifting of seedlings (Cordell et al. 1989; Sutherland et al. 1991) and to remove susceptible hosts within and around the nursery (Peerally 1974). The severity of Cylindrocladium root rot in seedbeds can be significantly reduced by soil fumigation before seeding or transplanting. Also, improving air circulation in the seedling crop will help to reduce the risk of these diseases (Gibson 1975; Sehgal 1983). Keirle (1981) concluded that Cylindrocladium scoparium can be controlled in container nurseries by soil pasteurisation, sanitation measures, systemic fungicides, manipulation of the environment or raising stock when weather was less favourable for the disease. Control of Cylindrocladium scoparium (Cylindrocladium candelabrum) is achieved in the eucalypt seedling and cutting production program in Brazil by using the integrated nursery system described above. The intensity of Cylindrocladium root rot in seedbeds can be reduced by soil fumigation before seeding or transplanting (Rowe et al. 1974; Cordell and Skilling 1975; Cordell et al. 1989; Phipps 1990; Sutherland et al. 1991). Fumigation of seedbeds with methyl bromide or spraying of plants with certain fungicides at three-day to five-day intervals controlled damping-off and root rot caused by Cylindrocladium scoparium (Reis and Chaves 1967). Fungicides have been used extensively against Cylindrocladium diseases in eucalypt nurseries (Table 21.1), reflecting the severity of these diseases in many countries. Partial control of leaf spots caused by Cylindrocladium scoparium in Australia was obtained by protective and eradicant soil drenches of benomyl, carbendazim or thiabendazole or foliar sprays of benomyl or thiophanate-methyl (Bertus 1976). Weekly foliar sprays of chlorothalonil and drenches every two weeks of benomyl were the most effective of several fungicides tested for control of Cylindrocladium scoparium on eucalypts in Florida (Barnard 1984). Weekly foliar sprays of copper oxychloride also showed promise. In one nursery, an operational schedule of alternate weekly sprays of benomyl and chlorothalonil throughout the life of the plants in the nursery was effective in controlling the disease. Three sprays of mancozeb at seven-day intervals was very effective against seedling blight [Cylindrocladium gracile (syn.

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Cylindrocladium clavatum), Cylindrocladium scoparium] on naturally infected six-month-old seedlings of E. tereticornis and seed treatments with several fungicides were effective for up to 90 days after germination against seedling blight due to these fungi (Rattan and Dhanda 1985) (Table 21.1). Foliar sprays of carbendazim were used for the control of cotyledon infection of E. grandis by Cylindrocladium quinqueseptatum and are highly effective in controlling the leaf blight and leaf spot of eucalypts caused by various species of Cylindrocladium (Sharma et al. 1985; Sharma and Mathew 1991). Seedling blight in the seedbeds was controlled with carbendazim as a foliar spray and soil drench and soil drenching with carbendazim was recommended for control of root rot of eucalypts caused by Cylindrocladium curvatum Boedijn & Reitsma (Sharma et al. 1985; Sharma and Mathew 1991). The eucalypt nursery disease complex described from Kerala (Mohanan and Sharma 1986; see Chapter 8), which includes postemergence damping-off caused by Pythium, Rhizoctonia and Cylindrocladium, web blight caused by Rhizoctonia solani and Cylindrocladium blight, can be controlled by five applications of benomyl, carbendazim and captafol as soil and foliar drenches (Sehgal 1983). Following soil application, benomyl persisted in Eucalyptus seedlings for up to 53 days from sowing, reducing infection induced by Cylindrocladium pteridis F.A.Wolf (Bedendo and Krügner 1988). Alfenas et al. (1988) reported that constant use of benomyl to control Cylindrocladium scoparium (possibly Cylindrocladium candelabrum) in nursery cuttings led to the development of strains of the fungus with tolerance to doses of the fungicide up to 1000 micrograms per gram. They reported that excellent control was obtained with thiram at 2000 micrograms per gram and suggested that fungicides with different modes of action should be used in rotation to avoid the buildup of tolerant strains of the pathogen. Some Bacillus isolates from the leaves of E. grandis were antagonistic to Cylindrocladium scoparium (Cylindrocladium candelabrum) (Bettiol et al. 1988) and a 10-day-old liquid culture of a Bacillus sp. provided protection but not postinfection control of disease caused by Cylindrocladium scoparium on detached leaves of both E. grandis and E. urophylla. Experimental studies in Brazil, using strains of Trichoderma sp. in a eucalypt bark compost/soil

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substrate, have shown a high level of protection of seedlings against both pre-emergent and postemergent attack by Cylindrocladium scoparium (Cylindrocladium candelabrum).

21.3.4 Anthracnose diseases caused by Colletotrichum gloeosporioides Mordue (1971) indicated that cultural practices are important in control of anthracnose caused by Glomerella cingulata (Stoneman) Spauld. & H.Schrenk [anamorph: Colletotrichum gloeosporioides (Penz.) Penz. & Sacc.]. Berry (1989) recommended elimination of the overwintering fungus in plant material in and around the nursery for control of anthracnose diseases in hardwoods. As irrigation water can disseminate spores (Mordue 1971), attention needs to be paid to the purity of the water supply for nursery irrigation. Field control of anthracnose often requires several applications of fungicidal sprays (Mordue 1971). Bordeaux mixture has been registered in the United States of America (USA) for anthracnose control on several hardwood species and dodine and benomyl could be used to control this disease (Berry 1989).

21.3.5 Diseases caused by Fusarium species Fusarium root rot is a difficult disease to manage as there is no satisfactory way to predict outbreaks (Sutherland 1990). However, cultural practices, including preventative and cultural measures, offer some protection against the disease (Johnson et al. 1989; Sutherland 1990). Fusarium diseases should be of little importance in container production when effective hygiene measures are used. Preventative measures include avoiding sites with heavy soils or poorly drained soils with a hardpan and sites that were used for agricultural crops and which therefore may have high levels of Fusarium. Areas of the nursery with a history of heavy losses to Fusarium root rots could be used for transplants rather than for seedbeds. Appropriate cultural measures include selecting the sowing season so as to avoid heavy mortality, the use of sawdust mulching and frequent irrigation for well drained soils, both of which reduce soil temperature and thus may help reduce disease, and the use of a balanced fertiliser (high levels of nitrogen appear to increase the amount of disease while high potassium seems to reduce seedling losses).

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The most effective control of Fusarium root rot is soil fumigation with chemicals such as methyl bromide plus chloropicrin prior to planting. Soil fumigation is recommended only for nurseries in which control of Fusarium is part of an overall pest control program targeted at weeds, insects and other diseases (Sutherland 1990). Although the growing medium for container seedlings is a potential source of Fusarium inoculum, this should not be fumigated or steam treated unless severe disease problems are known to occur (James et al. 1991). Some commercially prepared media may be pathogen-free and contain populations of antagonistic organisms. Treating styroblock containers for 10 minutes in hot water (86°C) or with very dilute sodium hypochlorite and detergent effectively reduced populations of Fusarium and Cylindrocarpon on the surface of the containers as well as in seedling roots which had penetrated walls of the container cells (James and Woollen 1989). The treatment of equipment (e.g. washed containers, storage racks) with chlorinated fungicide suspensions of thiram, iprodione or captan for three minutes as recommended by Ferreira (1993) (Table 21.1) against Cylindrocladium and Rhizoctonia is also effective. Sutherland (1990) indicated that there was no value in treatment of seeds with fungicides to control Fusarium root rot as the fungicide loses its effectiveness before infection occurs and the application of fungicide drenches when symptoms appear on seedlings does little good, as by that time the fungus is already in the root. However, it may be important to reduce inoculum carried on seed (James et al. 1991). As in Brazil, the careful collection and processing of eucalypt seed to avoid contact with soil and potential pathogens (Ferreira 1993) is far more effective in preventing seed contamination by Fusarium spp. than any follow-up treatments. Treating seeds with pesticides has produced mixed results; surface sterilants such as hydrogen peroxide and sodium hypochlorite have reduced amounts of seed-borne Fusarium but may affect seed germination or growth of young germinants. Problems with reduced germination and phytotoxicity have precluded the widespread use of fungicides as seed treatments. Other possible methods of reducing seedborne Fusarium include the use of running water rinses and the use of microwave energy to heat water in which the seeds have been placed, although care must be taken to ensure that

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water temperatures do not become lethal to the seeds (James et al. 1988, 1990, 1991). Use of fungicides has given inconsistent results against Fusarium root rot and thus is not recommended. Kassaby (1985) showed that solar heating (45°C–52°C) of moist soil under clear polythene sheeting (50 µm thick) during summer eliminated Fusarium oxysporum Schltdl. emen. W.C.Snyder & H.N.Hansen from inoculated pine roots. Solarisation for 60 days at Dehra Dun, India, of seedbeds infested by Fusarium solani, Fusarium moniliforme and Fusarium chlamydosporum apparently eliminated the pathogens and significantly improved germination of Eucalyptus hybrid (Shukla et al. 1990).

21.3.6 Hainesia leaf and shoot blight During the months when temperatures are around the optimum for development of shoot blight caused by Hainesia lythri (i.e. 25°C), growers should be especially careful to prevent water droplets and fertiliser granules from collecting on leaf surfaces— these cause fertiliser burns which have been associated with outbreaks of shoot blight (Lundquist and Foreman 1986). Provision of adequate initial levels of nutrients in the container medium avoids the need for follow-up fertilisation, as has been recommended as a measure to minimise activity of Botrytis cinerea in eucalypt nurseries (F.A. Ferreira, pers. comm.). Reducing the density of eucalypt seedlings and planting them out before they become too large has also been suggested (South African Forestry Research Institute 1985). Cultural practices such as mulching, weed control and removal of plant debris may help control the disease (Maas 1984). There are no reports of the use of chemicals to control this disease on eucalypts although mancozeb, captan and thiram were shown to restrict mycelial growth of the pathogen in culture (South African Forestry Research Institute 1985).

21.3.7 Diseases caused by Phaeophleospora (Kirramyces) epicoccoides Leaf spot caused by Phaeophleospora epicoccoides (Cooke & Massee) Crous, F.A.Ferreira & B.Sutton [syn. Kirramyces epicoccoides (Cooke & Massee) J.Walker, B.Sutton & Pascoe, Phaeoseptoria eucalypti Hansf. emen. J.Walker] is regarded as a

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disease of ‘old seedlings’ and is of no consequence in the five-month production system used in Brazil (F.A. Ferreira, pers. comm.). Management of the disease in nurseries in India involved removal of infected material from below the seedlings, removal and destruction of infected seedlings, avoiding overcrowding of stock, avoiding waterlogging by using appropriate irrigation and use of mancozeb sprays (Jamaluddin et al. 1985) (Table 21.1). Disease has also been managed by pruning and burning of infected branches (Chipompha 1987) or by the early removal of infected leaves, avoidance of frequent irrigation during winter and by regulation of plant spacing so as to avoid dense growth which favours disease development (Harsh et al. 1987). Crous (1989) advised the removal of the most severely infected seedlings from a nursery to avoid spread of the splash-dispersed conidia. Spraying with mancozeb (Harsh et al. 1987) or zineb (Chipompha 1987) controlled the disease (Table 21.1). Benomyl and carbendazim were also effective fungicides as twice-monthly sprays (Ferreira and Muchovej 1991).

21.3.8 Charcoal rot and ashy stem blight (Macrophomina phaseolina) Holliday and Punithalingam (1970) discussed the control of Macrophomina phaseolina, indicating that the aim should be to correct conditions which favour infection (e.g. inappropriate cultural conditions, extreme moisture levels, nutritional problems). This is obviously a disease that can be avoided in well-managed container systems with pathogen-free growing media. Presowing fumigation with a mixture of methyl bromide and chloropicrin greatly reduced levels of dormant sclerotia in soil (Smith and Krugman 1967; Kliejunas 1990) (Table 21.1). Soil solarisation for one week during the hot days of May in Pakistan resulted in elimination of sclerotia at five centimetre depth in both moist (field capacity) or dry soil artificially infested with Macrophomina phaseolina but at 20 centimetres only 50% of the sclerotia lost viability in wet soil and none were affected in dry soil (Sheikh and Ghaffar 1984). In a naturally infested soil, the sclerotia were reduced to such an extent that, after one week of solarisation in both wet and dry soil, no disease was observed in the subsequent crop.

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Macrophomina root rot disease of Eucalyptus may be checked by applying carbendazim or mancozeb as a soil drench in seedlings growing in polythene bags or in seedbeds (Soni et al. 1985; Jamaluddin et al. 1987) (Table 21.1). Various organic amendments to soil apparently increased the populations of soil microorganisms antagonistic to Macrophomina phaseolina, and thus reduced Macrophomina diseases of some crops, while other amendments were less effective (Ghaffar et al. 1969; Byadgi and Hegde 1988; Osunlaja 1990). The antagonistic effect increased as time between the addition of amendments and sowing increased from 15 to 60 days (Byadgi and Hegde 1988). Pelleting of seeds with carbendazim in combination with the antagonist Trichoderma viride and treatment of seeds with cell and spore suspensions of actively growing cultures of Trichoderma harzianum, Gliocladium virens J.H.Mill., Giddens & A.A.Foster, Paecilomyces lilacinus (Thom) Samson or a Streptomyces sp. have reduced seedling mortality caused by Macrophomina phaseolina in some crop species (Alagarsamy and Sivaprakasam 1988; Hussain et al. 1990). Similar treatments could be useful for eucalypts.

21.3.9 Mycosphaerella leaf and shoot blight

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The inoculum of the pathogen usually came from an older infected stand growing adjacent to the nursery, and thus growing seedlings in an area well removed from such trees, or sanitation felling of trees near the nursery, will control the disease in such situations (Ray 1991).

21.3.10 Root and collar rots caused by Pythiaceae The general principles for prevention of root rot diseases caused by species of Phytophthora and Pythium (known as water moulds) are similar to those for prevention of damping-off. A strict hygiene system (see section 21.2.1) is applicable to any eucalypt nursery threatened by diseases caused by water moulds (Boughton and Crane 1984). It is important that water used for nursery irrigation be free from waterborne pythiaceous pathogens. Various water treatments can be used to remove pythiaceous pathogens from water supplies (see section 21.1.6). Smith (1979) tested some fungitoxic compounds for their effect on Ph. cinnamomi in water. Mycelium was killed when immersed for 24 hours in suspensions containing copper (13–45 mg/L) or a solution containing free residual chlorine (100 mg/L) and exposing zoospores for 60 seconds to water containing two milligrams of free residual chlorine per litre reduced subsequent colony production on agar plates by 96% to 100%. As relatively few zoospore cysts can be detected in water samples using commercial enzyme-linked immunosorbent (ELISA) test kits (Ali-Shtayeh et al. 1991; Benson 1991b), it may be possible to screen water supplies as a basis for decisions about their suitability or the need for decontamination.

Because the lesions of Mycosphaerella leaf blight, caused on juvenile foliage of E. globulus in Australia by Mycosphaerella (M.) cryptica (Cooke) Hansf. and Mycosphaerella nubilosa (Cooke) Hansf. (see Chapter 9), appear between one and two months after infection, spraying of fungicides on diseased nursery seedlings is likely to be less effective than their application as prophylactic sprays on foliage early in the growing season (Marks et al. 1982). As new flush leaves are most susceptible to infection, Park (1988) indicated that the disease could be most effectively controlled in the field by spraying only during new leaf formation, and possibly only after rainfall on two or more consecutive days. The same approach would be beneficial in nurseries.

Hot water treatments (50°C for 5 minutes, 41°C for 25 minutes) have been used to eradicate Ph. cinnamomi from dormant and actively growing Vitis sp. (von Broembsen and Marais 1978) and Pinus radiata D.Don seedlings (Theron et al. 1982). Small increases in either temperature or time of exposure resulted in damage to plants and so this treatment would have to be studied carefully for its applicability to eucalypts.

Regular frequent spraying with chlorothalonil (Table 21.1) from undercutting to lifting gave satisfactory control of Mycosphaerella leaf blotch (M. nubilosa) in New Zealand (New Zealand Forest Service 1977; van Dorsser 1981; Ray 1991).

Soil fumigation with methyl bromide, chloropicrin, mixtures of methyl bromide and chloropicrin or Di-trapex can control Ph. cinnamomi in seedbeds (Brown 1985) and can be used for potting mixtures as necessary. However, the great problem with the

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use of such treatments is the risk of severe disease should a pathogen such as Ph. cinnamomi contaminate beds after fumigation. Solarisation of nursery soils with clear polythene films was shown to control various Phytophthora and Pythium species (Kassaby 1985; Garibaldi and Tamietti 1989). Infectious propagules of Ph. cinnamomi were undetectable in solar-heated soil for up to 16 months after treatment, although infectious propagules of Pythium were detected at a low level (Kassaby 1985). Solar heating of a potting mixture temporarily suppressed disease incidence in nursery stock of E. obliqua due to Ph. cinnamomi, Ph. cryptogea, Phytophthora spp. and three species of Pythium from a contaminated water supply used for irrigation of seedling trays, suggesting that solarisation resulted in an increase in the populations of antagonistic microorganisms. Solarisation of seedbeds used for a Eucalyptus hybrid apparently eliminated Pythium and significantly improved germination (Shukla et al. 1990). Chemicals that have been used to effectively control Ph. cinnamomi in horticulture include metalaxyl, fosetyl-Al and partly neutralised phosphorous acid (phosphonate) (Allen et al. 1980; Sivasithamparam and Hawson 1982; Pegg et al. 1985; Whiley et al. 1986) (Table 21.1). Root rot of E. marginata caused by Ph. cinnamomi was controlled with soil drenches of etridiazole one day before transplanting (Bertus 1974). Although metalaxyl was phytotoxic to some plants at 50 and 100 micrograms per gram of active ingredient in a soil mix low in organic matter, the phytotoxicity was reduced with increasing levels of peat moss in the potting mix and metalaxyl provided good control of root rot at concentrations as low as 25 micrograms per gram (Greenhalgh 1979). Marks and Smith (1990) compared several systemic fungicides, applied as root drenches, for control of stem lesions of E. sieberi caused by Ph. cinnamomi. Dimethomorph, metalaxyl and fosetyl-Al all resulted in a significant reduction in lesion extension, but a single application was not able to eliminate Ph. cinnamomi from an established infection. Stem disease of seedling eucalypts caused by Phytophthora cactorum (Lebert & E.Cohn) J.Schröt., Phytophthora citricola Sawada and Pythium anandrum Drechsler was controlled with a schedule of sprays of metalaxyl every two weeks (Wardlaw and Palzer (1985).

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Biological control offers an attractive, viable alternative to the use of chemicals for the control of the water moulds. Boehm and Hoitink (1992) reported that root rot and population development of Pythium ultimum Trow were highest in potting mixes containing the most decomposed, dark sphagnum peat (conducive), intermediate in a slightly decomposed peat and lowest in the least decomposed peat (suppressive). Microbial activity was highest in the suppressive and lowest in the conducive potting mixes. Suppression was negated by heating, suggesting that the effect was biological, and both the microflora in, and the microbial carrying capacity of, the peat contributed to sustained suppression of the pathogen. Hardy and Sivasithamparam (1991) have shown that a potting medium containing composted Eucalyptus bark was suppressive to, in decreasing order of effectiveness, Ph. cryptogea, Phytophthora nicotianae Breda de Haan var. nicotianae, Ph. citricola, Phytophthora drechsleri Tucker and Ph. cinnamomi. Suppressiveness appeared to be biological, as the mix became conducive to root rot after steam sterilisation.

21.3.11 Powdery mildews Several different species of powdery mildew are common on eucalypts growing in glasshouses (see Chapter 8). Chemicals used to control powdery mildews include sulphur preparations (sulphur dust, lime sulphur, wettable sulphur), benomyl, chlorothalonil, dinocap, maneb, prochloraz, triadimefon and zineb. Horst et al. (1992) reported successful control of powdery mildew of roses with weekly sprays of 0.06 moles per litre of aqueous solution of sodium bicarbonate plus 1% (v/v) of an ultrafine spray oil. Because of its low mammalian and environmental toxicities, the sodium bicarbonate/oil mix could be considered for trial on eucalypt seedlings. Powdery mildews can be controlled by exposing diseased plants to direct sunlight for an extended period (Josiah and AllenReid 1991). In Australia, powdery mildews have been controlled on eucalypt seedlings with colloidal sulphur compounds or triadimefon (Marks et al. 1982; Wardlaw and Phillips 1990; J.A. Simpson, pers. comm.) (Table 21.1). Prochloraz also gave good control (Wardlaw and Phillips 1990). Weekly sprays of wettable sulphur or benomyl twice per month

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were recommended in Brazil for control of powdery mildew on C. citriodora (Ferreira and Muchovej 1991).

21.3.12 Rust (Puccinia psidii) Weekly sprays of copper oxychloride, mancozeb, triadimenol or triforine were recommended in Brazil to control rust caused by Puccinia psidii G.Winter on E. cloeziana (Ferreira and Muchovej 1991) (Table 21.1).

21.3.13 Blight caused by Sporothrix pitereka Walker and Bertus (1971) indicated that the hyphomycete Sporothrix pitereka (J.Walker & Bertus) U.Braun (syn. Ramularia pitereka J.Walker & Bertus) could be controlled on plants older than three months by spraying but did not indicate what chemical was used. Gibson (1975), quoting a personal communication from J. Walker, indicated that the disease was controlled by appropriate hygiene and a thiram/copper oxychloride spray.

21.3.14 Diseases caused by Thanatephorus cucumeris (Rhizoctonia solani) Web blight caused by Thanatephorus cucumeris (A.B.Frank) Donk (mycelial state Rhizoctonia solani J.G.Kühn) can best be managed through an integrated approach involving sanitation, cultural practices and the use of chemicals (Mehrotra 1990). Sanitation measures recommended are the disposal of leaf litter by burning and the segregation of diseased seedlings soon after disease is detected. The latter helps prevent lateral spread of the disease through foliar contact. Cultural practices discussed by Mehrotra (1990) include the raising of seedlings in polypots instead of seedbeds, the keeping of seedlings in lots of 250 to 300 seedlings instead of 1000 as had been the practice in Indian nurseries, the removal of the lower branches on seedlings before the regular monsoon rains set in, weeding during the vulnerable period to reduce humidity around the plants and to preclude the possibility of infection from susceptible weeds, and avoiding the use of infested soil for raising seedlings. Solarisation of soil in closed glasshouses with either single-layer or double-layer polythene film was effective against Rhizoctonia solani in northern Italy (Garibaldi and Tamietti 1989).

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Several fungicides, including benomyl, chlorothalonil, flutolanil, iprodione, metalaxyl plus benomyl and tebuconazole alone or in an alternating schedule with chlorothalonil, have been used to control Rhizoctonia solani on a range of plants and these could be useful for control of web blight of eucalypts (Benson 1991a; Brenneman et al. 1991). Control of web blight in forest nurseries in India was achieved by applying a prophylactic drench of carbendazim one week before seed sowing (Sharma and Sankaran 1987) (Table 21.1). Once this disease appears, it can be controlled with at least two applications of carbendazim at weekly intervals (Sharma and Mathew 1991) or by the reduction of watering and application of Emisan-6 (methyl ethyl mercuric chloride) as a soil drench (Sharma et al. 1985; Sharma and Mathew 1991). Rhizoctonia aerial blight of forest tree seedlings was controlled with foliar sprays of triadimefon (Mehrotra 1998). Sharma and Mohanan (1991) reported that various schedules (Kerala schedules a, b and c) were effective in controlling root rot, damping-off and web blight caused by Rhizoctonia solani in eucalypt seedlings (Table 21.1). In Brazil, the recommended fungicide mixture for control of Rhizoctonia solani in eucalypt seedlings is thiabendazole plus thiram (Ferreira and Muchovej 1991). Ferreira (1993) amended these recommendations for control of pathogens in the eucalypt cutting program (see section 21.4), including those situations where sclerotial strains of Rhizoctonia solani caused leaf blight in clonal eucalypt gardens in tropical Brazil.

21.3.15 Diseases caused by Athelia rolfsii (Sclerotium rolfsii) Control measures recommended against Athelia rolfsii (Curzi) C.C.Tu & Kimbr. (anamorph: Sclerotium rolfsii Sacc.) include chemical disinfection of cuttings, increasing soil pH by liming and adjustment of the fertiliser regime (Mordue 1974). Recommended cultural control methods include removal or deep burial of crop residues and weed hosts, use of herbicides for weed control and avoidance of mechanical injury. Fumigation of seedbeds (Gibson 1975) and application of quintozene, Emisan-6 and terbucanazole (alone or alternated with chlorothalonil) provided good control (Sharma et al. 1985; Kobayashi and de Guzman 1988; Brenneman et al. 1991).

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21.3.16 Miscellaneous and/or minor diseases There is little information on control of the minor diseases reported on nursery eucalypts. Alternaria tenuissima (Kunze) Wiltshire causes leaf spots of older, chlorotic (nutrient-deficient) seedlings of E. grandis in Brazil, especially seedlings kept too long in the nursery (Ferreira and Muchovej 1991). Weekly sprays of mancozeb when the disease first appears were recommended (Table 21.1). Proper production and planting schedules to avoid the longterm holding of stock should reduce the problem. Diseases of Eucalyptus caused by Curvularia prasadii R.L.Mathur & B.L.Mathur and Curvularia lunata (Wakker) Boedijn in Madhya Pradesh, India, were successfully controlled by foliar application of mancozeb (Jamaluddin et al. 1987) (Table 21.1).

21.4 Control of principal diseases of eucalypt cutting programs Special measures are taken in Brazil to eliminate pathogens, including Cylindrocladium spp., on and within material used for vegetative production of eucalypts by cuttings. The precautions used to avoid diseases of cuttings under frequent irrigation during the first 40 days in the shadehouse can be separated into those relating to the cultural environment, to the growing medium and to the cuttings themselves. The procedures relating to the cultural environment are: 1

use of concrete or crushed rock for the shadehouse floor

2

use of washed racks and containers (tubettes) that have been immersed for three minutes in a chlorinated fungicide-water mixture (Table 21.1)

3

use of irrigation water that is free of soilborne pathogens

4

removal of all cuttings every 40 days from the glasshouse and their replacement with a new crop (the glasshouse is filled in one operation to avoid transfer of disease between cutting crops of different ages in the glasshouse)

5

limiting access to the shadehouse to essential staff, who wear specific shoes when they enter.

The growth medium is a pathogen-free substrate such as vermiculite, or organic based substrates that have been sterilised with methyl bromide or steam.

510

Sterilised substrates are allowed to stand for at least two weeks to allow their recolonisation by saprophytic organisms or, alternatively, they are inoculated with selected microorganisms antagonistic to Cylindrocladium spp. and Rhizoctonia solani. New cuttings are immersed in chlorine solution (Table 21.1) for three minutes and then rinsed in fresh water. Cuttings are then sprayed with fungicides twice per week (see following paragraph) and fallen leaves and tubettes with dead cuttings are removed. However, if leaf blight or lesions caused by Rhizoctonia solani, or sclerotia of Rhizoctonia solani, are observed on the eucalypt sprouts before taking the cuttings, the treatment is immersion of the cuttings in chlorinated water with added captan and surfactant (Silveira et al. 1992; Ferreira 1993). Ferreira et al. (1991) reported that spores and mycelium of Cylindrocladium scoparium were killed by a three minute exposure to 780 parts per million (µg/g) chlorine and that its mycelium was killed by a two minute exposure to benomyl (120 ppm) or thiram (2100 ppm). Cuttings are held in the glasshouse for only 40 days and during that time fungicide sprays are applied twice per week (Ferreira and Muchovej 1991; Ferreira et al. 1992; Ferreira 1993). Mixtures of benomyl plus thiram or benomyl plus captan are alternated for these twice-weekly sprays. During the subsequent outside nursery phase, diseases such as grey mould (Botrytis cinerea) and Cylindrocladium blight and stem girdling are controlled as in seedlings. Despite these measures there are occasions where high cutting losses occur. The rooting of cuttings is a very sensitive physiological process, affected by several internal and external factors. If a high percentage of cuttings do not produce callus tissue and roots and sprouts within the first 15 to 20 days, the cuttings will rot due to factors other than disease (F.A. Ferreira, pers. comm.).

21.5 Conclusion The forest nursery is an integral aspect of any eucalypt planting program. There is great potential for substantial losses of planting stock, and thus of important germplasm in some situations, from diseases in the nursery phase. Experience throughout the world has shown that close attention to sound cultural practices can minimise, if not eliminate,

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nursery diseases. The Queensland bare-root system and Brazilian eucalypt container system are excellent examples of this. However, while such systems are excellent for managing soilborne and waterborne pathogens, foliar pathogens can still cause serious problems. Although there are indications that biological control can be important in disease management, the use of chemicals can be an effective management tool for disease in the nursery environment. Chemicals can be used to sterilise equipment, containers and the water supply as well as for treating soil, seed and plants.

21.6 Acknowledgments I wish to thank Professor F.A. Ferreira, Universidade Federal de Viçosa, Viçosa, MG, Brazil, for his valued comments on disease avoidance and control as practised in the eucalypt nurseries of Brazil.

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in a South Florida nursery. Plant Disease 68, 471–473. Bedendo, I.P. and Krügner, T.L. (1988). Persistence of benomyl in seedlings of Eucalyptus cloeziana and Eucalyptus grandis after soil application. Fitopatologia Brasileira 13, 227–230. Abstract No. 2569 in Review of Plant Pathology 69, 320 (1990). Benson, D.M. (1991a). Control of Rhizoctonia stem rot of Poinsettia during propagation with fungicides that prevent colonization of rooting cubes by Rhizoctonia solani. Plant Disease 75, 394–398. Benson, D.M. (1991b). Detection of Phytophthora cinnamomi in azalea with commercial serological assay kits. Plant Disease 75, 478–482. Berry, F.H. (1989). Anthracnose. In Forest Nursery Pests. Agriculture Handbook No. 680. (Technical coordinators C.E. Cordell, R.L. Anderson, W.H. Hoffard, T.D. Landis, R.S. Smith Jr. and H.V. Toko) pp. 88–89. (USDA Forest Service: Washington, DC.) Bertus, A.L. (1974). Control of Phytophthora cinnamomi root rot with soil drenches of sodium p(dimethylamino)benzenediazosulfonate and 5-ethoxy3-(trichloromethyl)-1,2,4-thiadiazole. Plant Disease Reporter 58, 437–438. Bertus, A.L. (1976). Cylindrocladium scoparium Morgan on Australian native plants in cultivation. Phytopathologische Zeitschrift 85, 15–25. Bertus, A.L. and Wood, J.E. (1979). Protective treatments with six soil fungicides to control root rot caused by Phytophthora cinnamomi Rands. Phytopathologische Zeitschrift 96, 277–280. Bettiol, W., Auer, C.G., Camargo, L.E.A. and Kimati, H. (1988). Controle da macha foliar de Eucalyptus grandis e E. urophylla induzida por Cylindrocladium scoparium com Bacillus sp. [Control of leaf spot of Eucalyptus grandis and E. urophylla induced by Cylindrocladium scoparium with Bacillus sp.]. Summa Phytopathologica 14, 210–218. Abstract No. 5955 in Review of Plant Pathology 69, 728 (1990). Boehm, M.J. and Hoitink, H.A.J. (1992). Sustenance of microbial activity in potting mixes and its impact on severity of Pythium root rot of poinsettia. Phytopathology 82, 259–264. Bolland, L., Tierney, J.W. and Tierney, B.J. (1985). Studies on leaf spot and shoot blight of Eucalyptus caused by Cylindrocladium quinqueseptatum. European Journal Forest Pathology 15, 385–397. Boughton, T.J. and Crane, C.E. (1984). Assessment of Phytophthora disease risk at the Nannup nursery. Forests Department of Western Australia, Research Paper 77, 8 pp. Brenneman, T.B., Murphy, A.P. and Csinos, A.S. (1991). The activity of tebuconazole on Sclerotium rolfsii and Rhizoctonia solani, two soilborne pathogens of peanut. Plant Disease 75, 744–747. Brown, B.N. (1985). Phytophthora cinnamomi root rot in Pinus nurseries: soil fumigation and disease

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P.D. Gadgil, T.J. Wardlaw, F.A. Ferreira, J.K. Sharma, M.A. Dick, M.J. Wingfield and P.W. Crous

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The climate of a region and the occurrence of pests and pathogens have a major influence on the selection of the species of eucalypts that can be successfully grown as exotics and on the management of eucalypt plantations. Frost and drought are the two most important climatic factors that determine whether certain species can be grown in a region. The major diseases that have restricted the use of commercially desirable species are Mycosphaerella leaf blotch in Australia, New Zealand and South Africa, Cryphonectria stem canker in Brazil and South Africa, eucalypt rust in Brazil and Phytophthora root rot in parts of Australia and in South Africa. Successful management of disease in plantations can be achieved by a combination of plant quarantine measures, silvicultural practices and the use of disease resistant planting stock. Many eucalypt pests and pathogens occur in some regions of the world but not others; the threat to yet uninfested areas can be reduced, although never eliminated, by quarantine practices aimed at reducing the opportunity for the spread of such organisms between regions. Silvicultural practices can be modified to create conditions unfavourable for disease development. The incidence of stem decay, for example, can be considerably reduced by avoiding damage during thinning. Losses from bacterial wilt can be prevented by avoiding injury to the roots of containerised seedlings. The use of resistant stock has minimised the effect of Cryphonectria canker in Brazil and South Africa. Very promising material resistant to Cylindrocladium leaf blight and pink disease is becoming available in India and the management of Mycosphaerella leaf blotch in South Africa is achieved primarily through the planting of disease resistant species and provenances. A prudent manager should seek to combine the advantages of all available control methods. The selection of species adapted to the site, combined with the use of silvicultural regimes that maintain stand hygiene and the use of a mix of productive clones or provenances with enduring field resistance to the major diseases will provide the most successful disease management strategy in eucalypt plantations.

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22.1 Introduction Disease is recognised as one of the major constraints in the long-term development of eucalypt plantations, both of species planted as exotics in many parts of the world outside their natural range and of species established within their natural range. Eucalypts have been very widely planted as exotics in tropical, subtropical and temperate regions (see Chapter 1). In the transition of species from natural forests in Australia to intensively cultivated plantations elsewhere, few of the native pathogens of these species were transferred from Australia to the new regions. As a consequence, most exotic eucalypts grew in a largely disease-free environment at least in the earlier years of their introduction. With time and the rapid expansion of planted areas, more native eucalypt pathogens have spread to new areas (e.g. species of Mycosphaerella have spread to Chile, New Zealand and South Africa). Eucalypt species grown outside Australia have also come into contact with local pathogens and some of these, particularly pathogens of myrtaceaous plants (e.g. the guava rust, Puccinia psidii G.Winter), have transferred from their native hosts to eucalypts. When eucalypts have been planted outside their natural climatic range, especially in the humid tropics, they have suffered damage from pathogens such as Cylindrocladium species, which often have a broad host range. In plantations, eucalypts are usually grown in singlespecies monocultures suited to large-scale industrial handling. While trees in genetically uniform monocultures are ecologically more vulnerable to host specific pathogens than trees in mixed species forests, as shown by experience with plantations of Eucalyptus globulus in southern Australia (Park and Keane 1982; Carnegie et al. 1994), New Zealand (Dick 1982) and South Africa (Lundquist and Purnell 1987), in practice the occurrence of disease in exotic plantations need not be any greater than in natural forests (Gadgil and Bain 1999). The occurrence of disease in a plantation depends on how well the particular species or provenance is matched to its new environment, the occurrence of particular destructive pathogens in the region, the appropriateness of stand management practices and the nature of the genetic base of the planted material. Some diseases of eucalypt plantations have constrained the choice of species that can be planted, limited the expression of the full potential of some species and presented a challenge to plantation 520

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management. For example, diseases have had a substantial effect on the eucalypt plantation industry (Wingfield 1990) and have caused the abandonment of certain species and provenances of eucalypts in South Africa (Lundquist and Purnell 1987; Linde et al. 1994a, 1994b). In Australia, where experience with eucalypt plantations is more limited than in many other countries where eucalypts have been grown as exotics for a century or more, plantation managers still face the problems of matching species and provenances to particular sites (Carnegie et al. 1994) and of developing both appropriate genetic bases for plantations and appropriate management practices to reduce disease effect. In Australia, there is no doubt about the occurrence of potentially destructive pathogens, which abound in the native forests and woodlands, and have already revealed their destructiveness in the early stages of plantation development in some areas (Park and Keane 1982; Carnegie et al. 1994; D. de Little, pers. comm.). Even in Tasmania, which has the longest history of eucalypt plantation establishment in Australia, disease effects are still being evaluated and management strategies to ameliorate disease problems are still in their infancy. We review the effect of disease on the selection of species for planting in a given area and the disease management strategies in use for the important diseases in plantations in various countries.

22.2 Disease and the selection of species The climate of a region is obviously a major factor in deciding which eucalypt species and which provenances of these species are likely to grow well in that region. Establishment of particular eucalypt genotypes in plantations has often depended on the planting materials available locally. Most large plantations in new regions (e.g. in South America) are now planted with seed collected from precisely matched climatic regions in Australia. The choice of species is further limited by variation in the microclimate within a region and by the pests and pathogens that occur there.

22.2.1 Abiotic factors The incidence and severity of frosts and droughts are the two main abiotic factors affecting the selection of species for planting. For example, in southern Brazil,

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where frosts are light and infrequent, most plantations are of E. grandis and E. saligna from local or regional seed. In areas where frosts are frequent, E. saligna is preferred to E. grandis at present but is being replaced by more frost-tolerant genotypes of E. dunnii, derived from improved local seed sources, which have silvicultural and wood properties similar to those of E. grandis and E. saligna. Eucalyptus viminalis is virtually the only species to be planted in areas with severe and frequent frosts. While the Brazilian genotypes of this species are inferior in growth compared with E. grandis, a current breeding program should provide improved selections of the species. In Brazil, losses due to frost are rare in areas where frosts are severe and frequent. This is because the plantation companies use only frost-tolerant planting material. Generally, losses are significant only in the areas where frosts are occasional and less frost-tolerant material has been used. Eucalyptus nitens is the preferred species in South Africa, New Zealand and Tasmania for areas with frost-prone winters; in France, where frosts can be severe and prolonged, E. gunnii is favoured. There is wide variation in frost tolerance within species that are regarded as being frost tolerant so that careful selection of provenances is essential. The importance of using drought-tolerant species in areas subject to prolonged drought is exemplified by experience in Brazil where over 1.5 million hectares in areas of the State of Minas Gerais subject to annual droughts of six to eight months duration were planted for charcoal production with provenances of E. grandis that were not drought tolerant. The growth of these plantations was most unsatisfactory and the trees suffered repeated annual gummosis, dieback and sometimes total desiccation of the tops (Ferreira 1989). They are gradually being replanted with drought-tolerant provenances of E. camaldulensis, E. tereticornis, E. urophylla and E. pilularis. Hybrids of E. camaldulensis × E. grandis and E. urophylla × E. grandis selected for drought tolerance have also been clonally propagated and used successfully in drought-prone areas. Where in India E. tereticornis is planted widely from the sea to the Himalayan foothills in both wet and dry areas, on the hot, dry plains of South India, with annual rainfall less than 1000 millimetres, E. camaldulensis is superior to E. tereticornis and is the preferred species. Eucalyptus grandis and E. globulus are

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planted in the wetter areas at higher elevations in Tamil Nadu, Kerala and Karnataka States. In certain areas, heat scorch results in girdling of the stems of seedlings and cuttings at the point where they emerge from the ground and can be a serious problem. For example in some years in Espirito Santo State, northern São Paulo State and northern Minas Gerais State in Brazil, heat scorch killed up to 38% of four-month-old to eight-month-old plants (F.A. Ferreira, unpubl. data). The problem is readily recognised by the development of a dark, slightly or deeply depressed lesion around the stem at ground level. Periderm and cambium tissues are killed and a ring of callus tissue is commonly formed immediately above and below the lesion. In these particular regions of Brazil, temperatures at soil level on sunny days in summer can reach 60°C, well above the 50°C known to cause physiological injury. It is possible that species selection could be used to address this problem, as similarly high soil surface temperatures are common in many localities in Australia.

22.2.2 Interaction between abiotic stress and pathogens Abiotic factors also affect the severity of disease on eucalypts in plantations. Plants growing under stress can be more susceptible than unstressed plants to the pathogens. It is important, therefore, that site and local climatic factors are matched with the ecophysiological requirements of individual species so as to avoid stress in the trees and consequent serious problems with opportunistic pathogens. For example, in New Zealand E. regnans planted on sites with high (> 2000 mm a year), uniformly distributed rainfall suffered serious attack by a complex of fungi, whereas E. fastigata grew reasonably well on such sites. In Tasmania, expansion of the planting of E. nitens into lowland areas, particularly those exposed to hot, drying winds, has led to damaging attack by Armillaria luteobubalina Watling & Kile. The management solution is to plant such areas with better adapted species or provenances. Provenances of E. urophylla from high altitudes when planted at sea level in the tropical areas of Brazil suffered badly from pink disease (caused by Erythricium salmonicolor (Berk. & Broome) Burds.] (Ferreira 1989). In South Africa, clones of E. grandis susceptible to Coniothyrium canker cannot be planted in high rainfall areas. When seedlings of E. nitens susceptible to Mycosphaerella leaf blotch are grown at altitudes below 1400 metres, not only is 521

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the disease severe but losses can be aggravated by other pathogens such as Pseudocercospora eucalyptorum Crous, M.J.Wing., Marasas & B.Sutton, Aulographina eucalypti (Cooke & Massee) Arx & E.Müll. and Phaeophleospora epicoccoides (Cooke & Massee) Crous, F.A.Ferreira & B.Sutton [syn. Kirramyces epicoccoides (Cooke & Massee) J.Walker, B.Sutton & Pascoe and Phaeoseptoria eucalypti Hansf. emen. J.Walker] (Crous et al. 1997). In Brazil, planting material normally resistant to Cryphonectria stem canker [caused by Cryphonectria cubensis (Bruner) Hodges] (see Chapter 10) has been severely attacked by the common strain of the pathogen when stems have been damaged by heat scorch at ground level (F.A. Ferreira, unpubl. data).

22.2.3 Biotic factors The choice of species for planting is also restricted by primary attack by certain pests and pathogens. For example, E. camaldulensis, which is much preferred in the dry areas of southern India, is of restricted use because of its susceptibility to Botryodiplodia stem canker [caused by Lasiodiplodia theobromae (Pat.) Griffon & Maubl., syn. Botryodiplodia theobromae Pat.]. Similarly, Cylindrocladium leaf blight (caused by Cylindrocladium quinqueseptatum Boedijn & Reitsma) has severely limited the use in Vietnam of the favoured Petford provenance of E. camaldulensis which is highly susceptible to this pathogen in several parts of the country, depending on the rainfall and humidity. In South Africa, the planting of E. globulus (and some provenances of E. nitens) was abandoned because of the ravages of Mycosphaerella leaf blotch associated with a range of Mycosphaerella species (Purnell and Lundquist 1986; Lundquist and Purnell 1987; Crous and Wingfield 1996) (see Chapter 9). In New Zealand, early choices of species for plantations based on growth potential had to be revised when susceptibility of the species to frost and a range of insect pests and pathogens became apparent. Because the preferred species, E. globulus, E. macarthurii and E. viminalis, were highly susceptible to insect defoliation, particularly by the chrysomelid beetle Paropsis charybdis Stål, focus shifted to members of the ash group. However, Mycosphaerella leaf blotch [caused by Mycosphaerella cryptica (Cooke) Hansf.] limited the use of E. regnans, which in high rainfall areas was also severely affected by a disorder, known locally as ‘Barron Road syndrome’, involving several

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leaf pathogens (Kay 1993). In view of such limitations, E. regnans is no longer planted in New Zealand and its successor, E. nitens, could only be used after Paropsis charybdis, which causes severe defoliation in this species, was controlled successfully by the release in 1987 of a biocontrol agent (Bain and Kay 1989). Initially there was a high level of interest in E. delegatensis in New Zealand, but its increasingly poor performance in the face of severe infection by Mycosphaerella leaf blotch caused it to fall into disfavour (Fry 1983; Cheah and Hartill 1987). Lowland plantations of E. globulus in northern Tasmania, particularly the far north-west, have been subject to periodic defoliation due to epidemics of Mycosphaerella leaf blotch [caused on juvenile foliage by Mycosphaerella nubilosa (Cooke) Hansf.)]; this was one of the main reasons why it was replaced by E. nitens which is highly resistant. The other reasons were the frost tolerance of E. nitens and its relative resistance to defoliation by the chrysomelid beetle Chrysophtharta bimaculata (Olivier). Cryphonectria stem canker has had a major influence on species selection. This disease led to the abandonment of E. saligna in some parts of Brazil (Ferreira 1979) and the replacement of susceptible plantations of Corymbia maculata, E. grandis, E. propinqua and E. saligna by clones and seedling lines selected for resistance. As a result the disease is now under control. Cryphonectria stem canker was first recorded in South Africa in 1986 (Wingfield et al. 1989) and is one of the most important diseases of eucalypts there (Conradie et al. 1990; Wingfield et al. 1991; Wingfield and Kemp 1993), being most serious in subtropical areas with high rainfall where it commonly girdles young trees rather than causing cankers higher on the stem as observed in Brazil. Susceptible species such as E. grandis, E. saligna and E. tereticornis are being replaced by clones of hybrids selected for resistance. Further, the discovery of a new canker disease caused by a species of Coniothyrium in a limited area of the Zululand Forest region in 1991 (Wingfield et al. 1997; see Chapter 10) and its rapid spread throughout the subtropical areas of South Africa, particularly areas of higher rainfall, has led to the abandonment of many valuable clones of E. grandis and hybrid clones of this and other Eucalyptus species. In Brazil, a widely planted provenance of E. grandis (from a South African seed source) had to be

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abandoned because of its susceptibility to Puccinia psidii (Ferreira 1989). Plantations of E. cloeziana established in Bahia State suffered severe attacks of rust in young coppice shoots which regenerated after clear cutting, resulting in a high proportion of dead stumps and the necessity for premature replanting of the stock after the first clear cutting (Alfenas et al. 1993). While dieback caused by Phytophthora (Ph.) cinnamomi Rands is a major problem in certain native forests in south-east and south-west Australia (see Chapters 11 and 19), it has not often been a problem in eucalypt plantations in these areas, largely because they are planted with resistant species of the eucalypt subgenus, Symphyomyrtus, particularly E. globulus. However, in South Africa E. fraxinoides, which was favoured for its excellent pulping characteristics, cannot be grown successfully because of its susceptibility to Ph. cinnamomi (Linde et al. 1994a, 1994b).

22.3 Disease management strategies In large-scale plantation forestry, the methods that can be used for disease control are often restricted by economic considerations, although there are some basic strategies of plant quarantine, selection of disease-resistant planting material and silviculture that are fundamental for disease control and the establishment of a successful plantation industry (see Chapter 18). The major disease control strategies used in various parts of the world are outlined below.

22.3.1 Quarantine Quarantine measures designed to reduce the likelihood of the introduction of foreign pathogens (and pests) are fundamental to plantation management; this is especially so for eucalypts which are widely planted as exotics in countries largely free of the native parasites of the species. In addition, certain new-encounter pathogens (e.g. Puccinia psidii) that have adapted to exotic eucalypt plantations in certain regions have not yet been introduced to other regions, including Australia (see Chapter 18). Countries so far free from Cryphonectria cubensis, Cylindrocladium quinqueseptatum and Puccinia psidii would be well advised to institute quarantine regulations to exclude these species. The wide variation in pathogenicity

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between isolates of a taxon and the taxonomic confusion surrounding many pathogenic species, however, make it more prudent to have general quarantine measures aimed at a broad range of pathogens rather than measures designed to exclude specific organisms. For example, Cryphonectria cubensis is reported from Australia (Davison and Coates 1991) but causes little damage there, while Ph. cinnamomi is a major pathogen in Australia (Podger 1975) and South Africa (Linde et al. 1994a, 1994b) but is of little importance in New Zealand. The taxonomy of the genus Mycosphaerella, which contains many pathogenic species, is in a state of flux which makes it inadvisable to target particular species for quarantine. This type of confusion points to the futility of compiling and relying on lists of ‘excluded organisms’ which can never be complete and are frequently misleading. It is more important to implement quarantine measures that aim to prevent the movement between regions of materials which might carry any of the multitude of pests and pathogens of eucalypts. However, one has to be ready to manage pathogens that breach the quarantine barriers.

22.3.2 Silviculture In managed forests, silvicultural practices can be used to create conditions unfavourable for disease development. Some disorders, such as stem decay, arise largely as a result of silvicultural activity (e.g. thinning) and so can be controlled by modifying such activity. Stem decay arising from natural damage (e.g. branch shedding) and damage inflicted during pruning and thinning has been identified as a major problem in plantations managed for sawlog production under a clearwood regime in Australia and New Zealand (see Chapter 13). Silvicultural practices required to reduce the incidence of natural decay include both site selection for intensively managed native forests or plantations to avoid areas subject to high levels of decay and identification and culling (during thinning) of severely decayed trees. Significant differences have been found in the level of stem decay between sites selected for intensive management in Tasmania (Wardlaw 1996). While some stand factors such as stocking rate were associated with these differences, a wider range of site factors (e.g. soil type, drainage, vegetation type) needs to be evaluated before high risk sites can be identified. Reducing the level of

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naturally occurring decay in thinned stands by selectively culling trees with severe stem decay requires the modification of criteria used to select retained trees; current selection criteria usually fail to identify decayed trees for culling. A non-destructive method to detect decay in the lower trunks (1.5–2.5 m) is required. No such reliable method is available at present but a torsion drilling apparatus (Resistograph) is being evaluated for this purpose in Tasmania (T.J. Wardlaw, unpubl. data).

Because the incidence and severity of pink disease on E. tereticornis in India is higher at a spacing of one metre by one metre than two metres by two metres (Anon. 1985), the wider spacing is now recommended. The severity of Cylindrocladium leaf blight was greater when an intercrop of tapioca (Manihot esculenta Crantz) was cultivated during the first two years in eucalypt plantations in India (Sharma and Mohanan 1994); this practice had to be discontinued.

Stem decay that becomes established through natural and artificial pruning wounds has been identified as a serious problem in E. nitens plantations in Tasmania and on a range of species including E. botryoides, E. fastigata, E. macarthurii, E. pyrocarpa, E. regnans and E. viminalis in New Zealand (A. Zandvoort, pers. comm.). The principal fungus found infecting pruning wounds in a trial in New Zealand was Chondrostereum purpureum (Pers.:Fr.) Pouzar (Gadgil and Bawden 1981). About 75% of sampled trees had visible sapwood rot or stain indicating early stages of decay 12 months after pruning had taken place; the incidence of stub infection was highest in spring and summer and lowest in autumn and winter. Infection was significantly reduced by pruning flush with the main stem. As the main factors governing the release of the basidiospores of Chondrostereum purpureum are rainfall and high relative humidity (> 95%) (Dye 1967, 1974), it is recommended that eucalypts should be pruned during fine, dry weather in winter (Nicholas 1992). As a result of these studies, a strategy aimed at reducing the risk of infection of pruning wounds by decay fungi includes:

Bacterial wilt caused by Ralstonia solanacearum (Smith 1896) Yabuuchi et al. 1995 [syn. Pseudomonas solanacearum (Smith 1896) Smith 1914 and Burkholderia solanacearum (Smith 1896) Yabuuchi et al. 1993 and Iibuchi et al. 1995] has caused considerable losses (up to 17%) in young seedlings in regions in north and north-east Brazil where eucalypt plantations have replaced tropical rainforest (Dianese et al. 1990). As the pathogen infects through damaged roots, the disease can be reduced by avoiding injury to seedling roots during lifting from the nursery. Accordingly, the seedling containers are suspended above ground to ensure that the roots do not grow through the bottom of the containers into the soil and suffer damage when the containers are moved (Robbs et al. 1988). Any practice such as mulching, which prevents injury through high temperatures at the stem-soil interface in young plantations, also lessens bacterial attack (Ferreira 1997a).

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reducing the size of pruning wounds by pruning early when branches are still alive and are small

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avoiding pruning branches larger than 2.5 centimetres in diameter and those making an acute angle with the stem (Glass and Mackenzie 1989; Nicholas and Hay 1990)

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conducting pruning in autumn and winter when the risk of infection is lowest (Gadgil and Bawden 1981).

Although application of a fungicide (Captafol, 2% aqueous) to pruning wounds also significantly reduced infection, the practice was not feasible on an operational scale.

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In order to minimise damage by Puccinia psidii in Brazilian plantations of E. cloeziana intended for coppicing, it is recommended that clear cutting of the trees be undertaken in the warmer months when conditions are less favourable for infection of the young shoots (Ferreira 1989; Alfenas 1991; Ferreira 1997b).

22.3.3 Genetic manipulation In the medium to long term, the most effective strategy for management of disease in eucalypt plantations is exploitation of the wide range in disease resistance evident within and between species. An excellent example is the control of Cryphonectria canker of eucalypts in Brazil by the selection and planting of resistant trees (Ferreira 1989). The emergence of Cryphonectria stem canker led to the rapid development of techniques for rooting eucalypt

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cuttings on a large scale so that plantations could be planted with resistant clones selected from genetically heterogeneous plantations mainly of E. alba (‘Rio Claro hybrid’), E. grandis, E. urophylla, E. camaldulensis and E. tereticornis (Ferreira 1989). Susceptible species in plantations were also replaced with moderately resistant provenances of E. grandis and less frequently by resistant to highly resistant provenances of C. citriodora, C. torelliana, E. cloeziana, E. pellita and E. urophylla propagated from seed. Cryphonectria canker (Cryphonectria cubensis) is controlled in South Africa by the replacement of susceptible species (E. grandis, E. saligna, E. tereticornis) with hybrid clones selected for resistance to the disease. Eucalyptus camaldulensis and E. urophylla show particular promise as parental material for breeding resistant hybrids. Clonal selection is based on disease assessments in trial plantings as well as the response to inoculation which has been shown to reliably reflect field resistance (Conradie et al. 1992; van der Westhuizen et al. 1992). Sexual outcrossing and genetic diversity among isolates of the pathogen in South Africa have been shown to be extremely limited (van der Westhuizen et al. 1993), supporting the conclusion that the pathogen has been introduced to the country only recently. Clones of E. grandis and of hybrids of this with other species differ considerably in their resistance to the relatively new canker disease caused by a Coniothyrium species in South Africa; indeed, the disease pressure is sufficient for very susceptible clones to be recognised under forest conditions and eliminated within one year of planting. Considerable efforts are being made to introduce resistant clones, especially in the higher rainfall areas. Major trials based on the Brazilian (Aracruz) model of eucalypt improvement have been carried out in India to select field resistance to Cylindrocladium leaf blight and pink disease among local seed sources and Australian provenances (Sharma and Mohanan 1992). Selections of apparently disease-resistant trees of E. grandis and E. tereticornis were made by forest departments and other research organisations throughout India. Selected trees were coppiced and one-noded cuttings prepared from the coppice shoots were vegetatively propagated and initially screened for resistance to the two diseases in glasshouses. Resistant clones were planted in a clonal orchard to test their field resistance to both diseases. Clones

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with the desired traits were further tested for disease resistance and productivity in multilocational trials and seed collected from the clonal orchard was planted in progeny trials to determine the inheritance of the traits. Elite trees were clonally propagated for large-scale planting. In the long term these trees will also supply seed for commercial plantations. Results obtained by a private company have demonstrated amply the success of this strategy in selecting resistant clones with high productivity. To broaden the genetic base, 61 Australian provenances of E. camaldulensis, E. grandis, E. pellita, E. tereticornis and E. urophylla were screened for resistance to Cylindrocladium leaf blight and pink disease in further multilocational trials, with some provenances from all species showing adequate levels of resistance and productivity. Similar multilocational species and provenance trials in south Vietnam have provided information on the variation in susceptibility to Cylindrocladium leaf blight of different provenances of E. camaldulensis and E. tereticornis and promising resistant provenances have been identified. A bioassay involving exposure of cut shoots to toxin has been developed in India to assess susceptibility to pink disease, with the results showing significant variation in response among provenances of E. grandis and E. tereticornis which could be exploited for disease control (Sharma et al. 1988). Severe leaf spot diseases caused by Cylindrocladium spp., Coniella fragariae (Oudem.) B.Sutton and a species of Mycosphaerella have caused extensive defoliation in plantations in Brazil but no measures to control them have been taken because most often they affect trees in the early stages of growth (phenologic stage B, Ferreira 1997a). Once the trees commence natural branch pruning in the basal and intermediate thirds of the trunk (phenologic stage C), they are not at risk from these diseases, nor from eucalypt rust (Ferreira 1989; Ferreira 1997b). An understanding of the developmental stages of the eucalypts is important for understanding the incidence of particular diseases (F.A. Ferreira, unpubl. data). The microclimate near the shoot varies as the seedlings develop and this affects disease incidence. This helps to explain why a typical plantation disease such as Cylindrocladium leaf spot and blight is rarely reported from nurseries in countries (e.g. Brazil) where seedlings are transplanted early while being reported from

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nurseries in other countries where seedlings are transplanted at a later stage. Thus provenances or clones selected for faster initial growth suffer less damage from these pathogens. A new situation arose in Brazil in the late 1990s with the occurrence in clonal plantations of a damaging leaf spot caused by Cylindrocladium pteridis F.A.Wolf. In the south-east of Bahia State, about 10% of the clonal genotypes are highly susceptible and so use of this material on a commercial scale has been suspended (Ferreira et al. 1995). Management of Mycosphaerella leaf blotch in South Africa is primarily achieved through the planting of disease-resistant provenances of E. nitens. The tendency of Victorian provenances of E. nitens to grow for a longer period in the juvenile phase than New South Wales provenances was reported from Australia (Pederick 1979) and South Africa (Nixon and Hagedorn 1978). As this disease is most prevalent on the juvenile foliage, the New South Wales provenances have been preferred in plantations (Lundquist and Purnell 1987). There is, however, recent evidence that certain collections from New South Wales are beginning to show a higher level of susceptibility to the disease (C. Clarke, pers. comm.). Whether this is due to development of more aggressive strains of the fungus that can infect mature as well as juvenile foliage, or the incursion of a new species of Mycosphaerella, has yet to be determined. Where it has not been possible to plant resistant seedlings of E. nitens, losses have been aggravated by other pathogens as mentioned above. Botryosphaeria canker [caused by Botryosphaeria dothidea (Moug.:Fr.) Ces. & De Not.] in South Africa (Smith et al. 1994) is managed through selection of disease-resistant clones and hybrids. Stem canker caused by Endothia gyrosa (Schwein:Fr.) Fr. and decay arising from stem wounds in plantation-grown E. nitens in Tasmania could potentially be controlled by selection of resistant genotypes. The incidence of stem canker was related to bark roughness in provenances of E. nitens and this could be used as a selection criterion for disease resistance. Selection of planting material with traits such as small branches, low branch angles and general decay resistance has potential for control of decay associated with pruning.

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It is now commonly accepted that in selection and breeding for disease resistance it is sufficient to avoid the most susceptible genotypes, particularly if disease control relies also on appropriate cultural and hygiene practices. In South Africa, management strategies to avoid losses attributable to Phytophthora root disease have relied almost entirely on the avoidance of susceptible species, although considerable progress is being made in developing techniques to identify disease-resistant families within some of the susceptible species. Similarly, control of rust in Brazil is primarily achieved by excluding the few highly susceptible eucalypt clones and provenances, and by rejecting rust susceptible clones during selection for resistance to Cryphonectria canker (Ferreira 1989).

22.3.4 Chemical control Chemical control measures are available for several serious eucalypt diseases but they are not in general use because of their high cost relative to the value of the crop. Control of Mycosphaerella leaf blotch with sprays of 3.4 kilograms of Daconil (chlorothalonil) 2787 (75W) + multifilm X77 in 1000 litres of water per hectare is occasionally undertaken in New Zealand nurseries (Dick and Gadgil 1983) and regular applications (every 3–4 weeks for 6 months) to young trees of a broad spectrum fungicide gave reasonable control of the Barron Road syndrome associated with several leaf-infecting pathogens, although the control was not considered practical (Kay 1993). In South Africa, the use of a limited number of fungicide applications to control Mycosphaerella species and associated pathogens on juvenile foliage of E. nitens in the first few years of growth is being seriously considered. In India, Cylindrocladium leaf blight in the nursery can be controlled effectively with fungicides. Although Calixin (tridemorph) has been found to be very effective against pink disease in E. tereticornis, the chemical control of this disease in plantations is not economic. Control of Puccinia psidii by the application of three sprays of tridimenol (0.5 g/L) or diniconozole (0.15 g/L) every 20 days after the initial attack on coppice regrowth of E. cloeziana in southern Brazil has been recommended (Alfenas et al. 1993), although it is not widely used. Although it is unlikely that fungicide applications alone will be used to control disease in eucalypt plantations, their highly targeted use together with a range of other control measures is feasible.

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22.3.5 Biological control Although there are many examples of successful biological control of insect pests of eucalypts, there are no examples of biological control of eucalypt diseases on a broad scale. Double-stranded (ds) RNA mediated hypovirulence has been identified in the South African population of Cryphonectria cubensis (van der Westhuizen et al. 1994) which might give rise to use of hypovirulent strains as biological control agents for Cryphonectria canker.

22.4 Conclusion Selection of provenances and clones which are resistant to disease has been the most useful strategy for the management of disease in eucalypt plantations (e.g. Cryphonectria canker in Brazil). However, the limitations of this approach must be recognised. Clones and provenances resistant to one disease may be highly susceptible to another and the narrowing of the genetic base in order to gain an advantage in productivity or disease resistance may prove disadvantageous in the long term. For example, the planting of many valuable clones of E. grandis and hybrids between this and other Eucalyptus species had to be abandoned in South Africa after the appearance of Coniothyrium canker, and the use of a single provenance (Petford) of E. camaldulensis over large areas allowed the epidemic development of Cylindrocladium leaf blight in central and southern Vietnam. Some clones of E. grandis selected for good growth and resistance to Cryphonectria canker and Puccinia psidii suffered severely from pink disease in coastal eastern Brazil following two consecutive years of abnormally high rainfall (Alfenas and Silveira 1995). As field assessment of disease resistance is usually time consuming, the use of more rapid methods such as the cut-shoot toxin bioassay for pink disease (Sharma et al. 1988) and artificial inoculation for Cryphonectria canker (Conradie et al. 1992) is very attractive. It is, however, most important to be certain that the results of such methods accurately reflect field resistance and do not result in selection of a non-durable form of resistance with a narrow genetic base. For diseases that do not cause mortality, the replacement of fast-growing, susceptible provenances or clones by less productive but putatively diseaseresistant genotypes has to be carefully considered; if

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damage caused by the disease is moderate, at the end of the rotation the faster-growing, susceptible genotypes may still prove to be more productive. The selection in South Africa of New South Wales provenances of E. nitens because of their apparent resistance to Mycosphaerella leaf blotch to replace the susceptible but faster-growing Victorian provenances is an example. The resistance of the New South Wales provenances is apparently not as great as at first predicted and it is possible that the Victorian provenances could outyield them (M.J. Wingfield, unpubl. data). In provenance trials of E. globulus in eastern Victoria, the main selection criteria are growth rate and tree form, which are considered to reflect, among other things, the degree of resistance to pests and diseases. A prudent manager will seek to combine the advantages of the various control methods that are available for disease management. The selection of species adapted to the site, combined with the use of silvicultural regimes that maintain stand hygiene and create conditions unfavourable for disease development, and the use of a mix of clones or provenances of good productivity and with proven field resistance to the prevalent major diseases, should allow successful disease management. Chemical control measures may be a useful addition to this strategy but only if they are used for a short, defined period (e.g. to control a disease affecting only the juvenile foliage or to limit inoculum buildup in a year when the weather has been particularly favourable for rapid disease development).

22.5 Acknowledgments We are very grateful for the most helpful comments on the manuscript by Heather Mackenzie and Mike Wilcox.

22.6 References Alfenas, A.C. (1991). Controle integrado da ferrugem causada por Puccinia psidii em Eucalyptus cloeziana no sudeste de Bahia. Fitopatologia Brasileira 16, 6 (Abstract). Alfenas, A.C. and Silveira, S.F. (1995). Epidemia a mancha rosada do euclipto causada por Corticium salmonicolor. Fitopatologia Brasileira 20, 375 (Abstract). Alfenas, A.C., Maffia, A.C., Macabeu, A.J. and Sartorio, R.C. (1993). Eficiência de triadimenol, oxicarboxine diniconazole para controle da ferrugem (Puccinia

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Ferreira, F.A. (1979). Situação do reflorestamento até julho de 1976, nas regiões de maior ocorrência do cancro do eucalipto, nos Estados do Espirito Santo e Minas Gerais, em termos de escolha de espécies e procedências de Eucalyptus. Revista Arvore 2, 104–110. Ferreira, F.A. (1989). Patologia Florestal; Principais Doenças Florestais no Brasil. (Sociedade de Investigações Florestais: Viçosa, Brazil.) Ferreira, F.A. (1997a). Enfermidades do eucalipto no Brasil. Informe Agropécuário (A cultura do Eucalypto II) 136, 5–19 and 31–51. Ferreira, F.A. (1997b). Eucalipto (Eucalyptus spp.)— Controle de doenças. In Controle de Doenças de Plantas—Grandes Culturas. Vol. I. (Eds F.X. Ribeiro do Vale and L. Zambolim) pp. 289–333. (Universidade Federal de Viçosa: Viçosa, Brazil.) Ferreira, F.A., Alfenas, A.C., Moreira, A.M. and Demunner, N.L. (1995). Mancha de pteridis-doença foliar do eucalipto. Fitopatologia Brasileira 20, 107–110. Fry, G. (1983). Eucalypts in New Zealand: a position report. New Zealand Journal of Forestry 28, 394–411. Gadgil, P.D. and Bain, J. (1999). Vulnerability of planted forests to biotic and abiotic distrubances. New Forests 17, 227–238. Gadgil, P.D. and Bawden, A.D. (1981). Infection of wounds in Eucalyptus delegatensis. New Zealand Journal of Forestry Science 11, 262–270. Glass, B.P. and McKenzie, H. (1989). Decay distribution in relation to pruning and growth stress in plantationgrown Eucalyptus regnans in New Zealand. New Zealand Journal of Forestry Science 19, 210–222. Kay, M.K. (1993). Barron Road syndrome. New Zealand Forestry 38, 44. Linde, C., Kemp, G.H.J. and Wingfield, M.J. (1994a). Diseases of pines and eucalypts in South Africa associated with Pythium and Phytophthora species. South African Forestry Journal 169, 25–32. Linde, C., Kemp, G.H.J. and Wingfield, M.J. (1994b). Pythium and Phytophthora species associated with exotic forest trees in South Africa. European Journal of Forest Pathology 24, 345–346. Lundquist, J.E. and Purnell, R.C. (1987). Effects of Mycosphaerella leaf spot on growth of Eucalyptus nitens. Plant Disease 71, 1025–1029. Nicholas, I.A. (1992). Pruning eucalypts. New Zealand Tree Grower 13, 18–20. Nicholas, I.A. and Hay, A.E. (1990). Selection of special purpose species: effect of pests and diseases. New Zealand Journal of Forestry Science 20, 279–289. Nixon, K.M. and Hagedorn, S.F. (1978). South African Wattle Research Institute Report for 1977–1978, pp. 67–69. (South African Wattle Research Institute: Pietermarizburg.)

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Park, R.F. and Keane, P.J. (1982). Leaf diseases of Eucalyptus associated with Mycosphaerella species. Transactions of the British Mycological Society 79, 101–115. Pederick, L.A. (1979). Natural variation in shining gum (Eucalyptus nitens). Australian Forest Research 9, 41–63. Podger, F.D. (1975). The role of Phytophthora cinnamomi in dieback disease of Australian eucalypt forests. In Biology and Control of Soil-borne Plant Pathogens. (Ed. G.W. Bruehl) pp. 27–36. (American Phytopathological Society: St Paul, MN, USA.) Purnell, R.C. and Lundquist, J.E. (1986). Provenance variation of Eucalyptus nitens on the Eastern Transvaal Highveld in South Africa. South African Forestry Journal 138, 23–31. Robbs, C.F., Cruz, A.P. and Neto, J.R. (1988). Algumas estratégias do controle da murcha bacteriana (Pseudomonas solanacearum) em eucaliptos jaguariana. Comunidado Técnico No. 3. (EMBRAPA, CNPDA: Brasilia, São Paulo.) Sharma, J.K. and Mohanan, C. (1992). Relative susceptibility of Eucalyptus provenances to Cylindrocladium leaf blight in Kerala, India. European Journal of Forest Pathology 22, 257–265. Sharma, J.K. and Mohanan, C. (1994). Cylindrocladium leaf blight in relation to taungya crop, Manihot utilissima and climatic conditions in eucalypt plantations. Indian Forester 120, 1104–1107. Sharma, J.K., Maria Florence, E.J., Sankaran K.V. and Mohanan, C. (1988). Differential phytotoxic response of cut shoots of eucalypts to culture filtrates of pink disease fungus, Corticium salmonicolor. Forest Ecology and Management 24, 97–111. Smith, H., Kemp, G.H.J. and Wingfield, M.J. (1994). Canker and dieback of Eucalyptus in South Africa caused by Botryosphaeria dothidea. Plant Pathology 43, 1031–1034.

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van der Westhuizen, I.P., Wingfield, M.J., Kemp, G.H.J. and Swart, W.J. (1992). Comparison of the susceptibility of Eucalyptus clones to Cryphonectria cubensis under field and glasshouse conditions. Phytophylactica 24, 107 (Abstr.) van der Westhuizen, I.P., Smit, W.A., Wingfield, M.J. and Kemp, G.H.J. (1993). Population study of South African isolates of Cryphonectria cubensis. Phytophylactica 25, 170 (Abstr.) van der Westhuizen, I.P., Smit, W.A., Wingfield, M.J. and Kemp, G.H.J. (1994). Hypovirulence associated with dsRNA discovered in Cryphonectria cubensis. Phytopathology 84, 1127 (Abstr.). Wardlaw, T.J. (1996). The origin and extent of discolouration and decay in stems of young regrowth eucalypts in southern Tasmania. Canadian Journal of Forest Research 26, 1–8. Wingfield, M.J. (1990). The current status and future prospects of forest pathology in South Africa. South African Journal of Science 86, 60–62. Wingfield, M.J. and Kemp, G.H.J. (1993). Diseases of Pines, Eucalypts and Wattles. Forestry Handbook. 3rd edn. (South African Forestry Institute: Pretoria.) Wingfield, M.J., Swart, W.J. and Abear, B.J. (1989). First record of Cryphonectria canker of Eucalyptus in South Africa. Phytophylactica 21, 311–313. Wingfield, M.J., Swart, W.J. and Kemp, G.H.J. (1991). Pathology considerations in clonal propagation of Eucalyptus with special reference to the South African situation. In Proceedings of IUFRO Symposium on Intensive Forestry: The Role of Eucalypts (Ed. A.P.G. Schonau) pp. 811–820. (South African Institute of Forestry: Pretoria.) Wingfield, M.J., Crous, P.W. and Coutinho, T.A. (1997). A serious canker disease of Eucalyptus in South Africa caused by a new species of Coniothyrium. Mycopathologia 136, 139–145.

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Animal Index

Birds and Mammals Scientific Names Acanthagenys rufogularis Gould, 1838 (Bird) 363 Alisterus scapularis (Lichtenstein, 1816) (Bird) 364 Dicaeum hirundinaceum (Shaw, 1792) (Bird) 363 Grantiella picta (Gould, 1838) (Bird) 363 Manorina melanophrys (Latham, 1802) (Bird) 416, 447 Petauroides volans (Kerr, 1792) (Mammal) 364 Phascolarctos cinereus (Goldfuss, 1817) (Mammal) 106, 364 Platycercus (Bird) 364 Plectorhyncha lanceolata (Gould, 1838) (Bird) 363 Pseudocheirus peregrinus (Boddaert, 1795) (Mammal) 364 Strepera graculina (Shaw, 1790) (Bird) 363 Trichosurus vulpecula (Kerr, 1792) (Mammal) 364, 417, 446, 463

Birds and Mammals Common Names Please refer to the index of scientific names to obtain the corresponding page numbers. Australian king parrot Alisterus scapularis (Lichtenstein, 1816) Bell miner Manorina melanophrys (Latham, 1802) Common brushtail possum Trichosurus vulpecula (Kerr, 1792) Common ringtail possum Pseudocheirus peregrinus (Boddaert, 1795) Greater glider Petauroides volans (Kerr, 1792) Koala Phascolarctos cinereus (Goldfuss, 1817) Mistletoebird Dicaeum hirundinaceum (Shaw, 1792) Painted honeyeater Grantiella picta (Gould, 1838) Pied currawong Strepera graculina (Shaw, 1790) Spiny-cheeked honeyeater Acanthagenys rufogularis (Gould, 1838) Striped honeyeater Plectorhyncha lanceolata (Gould, 1838)

Insects Amblypelta cocophaga China 422 Cardiaspina bilobata Taylor 55

Chrysophtharta bimaculata (Olivier) 414, 522 Didymuria violescens (Leach) 56 Dieuches 50 Euander 50 Fergusonina 339, 348 Megastigmus 104 Oecophylla smaragdina (Fabricius) 422 Paropsis charybdis Stål 522 Phoracantha 415 Phoracantha acanthocera (Macleay) 468 Phoracantha semipunctata (Fabricius) 43, 422, 434 Tryphocaria acanthocera (Macleay) [this is Phoracantha acanthocera (Macleay)] 468 Uraba lugens Walker 415

Nematodes Acontylus vipriensis Meagher 1968 347 Cryphodera eucalypti Colbran 1966 347 Ditylenchus 347 Fergusobia 339, 348 Fergusobia curriei (Johnson 1938) Christie 1941 [this is Fergusobia tumifaciens (Currie 1937) Wachek 1955] 348 Fergusobia tumifaciens (Currie 1937) Wachek 1955 348 Hemicriconemoides 347 Hemicycliophora 347 Longidorus 347 Meloidogyne 347 Meloidogyne arenaria (Neal 1889) Chitwood 1949 347 Meloidogyne incognita (Kofoid & White 1919) Chitwood 1949 347 Meloidogyne javanica (Treub 1885) Chitwood 1949 347 Paratylenchus 347 Pratylenchus 347 Pratylenchus brachyurus (Godfrey 1929) Filipjev & Schuurmans Stekhoven 1941 347 Pratylenchus coffeae (Zimmerman 1898) Filipjev & Schuurmans Stekhoven 1941 347 Radopholus 347 Radopholus similis (Cobb 1893) Thorne 1949 347 Tylenchorhynchus 347 Tylodorus fisheri Reay 1991 347

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Fungi and other Microorganisms (Actinomycetes, Bacteria, Oomycota, Phytoplasmas) Index Abortiporus biennis (Bull.:Fr.) Singer 302 Abstoma 78 Acaulospora 86 Acaulospora scrobiculata Trappe 82 Acremomium 248 Acremomium rutilum W.Gams 107 Acremomium strictum W.Gams 107 Acrostaphylus lignicola Subram. 107 Agrobacterium rhizogenes (Riker, Banfield, Wright, Keitt & Sagen 1930) Conn 1942 (Bacterium) 346 Agrobacterium tumefaciens (Smith & Townsend 1907) Conn 1942 (Bacterium) 50, 140, 343, 345, 346 Aleurodiscus 317 Alternaria 56, 107, 114, 140, 207, 218 Alternaria sp. [teleomorph Lewia infectoria (Fuckel) M.E.Barr & E.G.Simmons] Alternaria alternata (Fr.) Keissl. 107, 114, 121, 140, 218 Alternaria tenuis Nees [this is Alternaria alternata (Fr.) Keissl.] 114, 121, 140 Alternaria tenuissima (Kunze) Wiltshire 140, 218, 501, 510 Amanita 83, 86, 88, 89, 91 Amanita austropulchella D.A.Reid [this is Amanita xanthocephala (Berk.) D.A.Reid & R.N.Hilton] 78 Amanita gemmata (L.:Fr.) Gillet 78 Amanita grisea Massee & Rodway 78 Amanita hiltonii D.A.Reid 78 Amanita murina Sacc. 78 Amanita muscaria (L.:Fr.) Lam. 78, 84, 85, 93 Amanita ochrophylla (Cooke & Massee) Cleland 78 Amanita pagetodes D.A.Reid 78 Amanita phalloides (Vaill.:Fr.) Link 78, 85, 92 Amanita preisii (Fr.) Sacc. 78 Amanita punctata (Cleland & Cheel) D.A.Reid 78 Amanita strobilacea (Cooke) McAlpine 78 Amanita subalbida Cleland 78 Amanita umbrinella E.-J.Gilbert & Cleland 78 Amanita xanthocephala (Berk.) D.A.Reid & R.N.Hilton 78 Amauroderma rude (Berk.) G.Cunn. 310, 317 Amerostege latitans (Sacc.) Theiss. [this is Clypeophysalospora latitans (Sacc.) H.J.Swart] 189 Amylostereum sacratum (G.Cunn.) Burds. [this is Dextrinocystidium sacratum (G.Cunn.) Sheng H.Wu] 302 Anthostomella eucalypti H.Y.Yip 177, 210 Arcangeliella 83 Arcangeliella malaiensis Corner & Hawker [this is Zelleromyces malaiensis (Corner & Hawker) A.H.Sm.] 81 Armillaria 42, 47, 48, 65, 293, 294, 295, 296, 297, 298, 303, 320, 413, 414, 416, 432, 433, 434, 437, 438, 460, 464, 465, Plate 12.10 Armillaria fellea (Hongo) Kile & Watling 294 Armillaria fumosa Kile & Watling 294, 295 Armillaria fuscipes Petch 294

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Armillaria hinnulea Kile & Watling 294, 295, 296, 297, 414, 464, Plates 12.2, 12.10, 12.11 Armillaria limonea (G.Stev.) Boesew. 298 Armillaria luteobubalina Watling & Kile 294, 295, 296, 297, 298, 324, 326, 412, 415, 416, 437, 446, 449, 452, 460, 464, 465, 466, 521, Plates 12.1, 12.3, 12.4, 12.5, 12.6, 12.7, 12.8, 12.9, 12.12 Armillaria mellea (Vahl:Fr.) P.Kumm. (mycelial form Rhizomorpha subcorticicalis Pers.) 294, 298, 416 Armillaria novae-zelandiae (G.Stev.) Herink 294, 295, 296, 297, 298, 310, 414, 464, Plates 12.2, 12.10, 12.11 Armillaria pallidula Kile & Watling 294 Armillaria tabescens (Scop.) Emel 294, 298 Arnaudiella bancroftii Hansf. [this is Phaeothyriolum microthyrioides (G.Winter) H.J.Swart] 179 Arnaudiella eucalyptorum Crous & W.B.Kendr. (anamorph Xenogliocladiopsis eucalyptorum Crous & W.B.Kendr.) 182 Ascocoma eucalypti (Hansf.) H.J.Swart [anamorph Coma circularis (Cooke & Massee) Nag Raj & W.B.Kendr.] 176, 177, 201 Ascocoma eucalypti (Hansf.) H.J.Swart var. didymospora H.J.Swart 176, 177, 201 Aspergillus 103, 108, 114 Aspergillus alutaceus Berk. & M.A.Curtis 107 Aspergillus candidus Link 107 Aspergillus flavipes (Bainier & Sartory) Thom & Church 107 Aspergillus flavus Link 107, 114 Aspergillus fumigatus Fresen. (teleomorph Fennellia flavipes B.J.Wiley & E.G.Simmons) 107, 114 Aspergillus koningi Oudem. 107 Aspergillus luchuensis Inui 107 Aspergillus nidulans (Eidam) G.Winter [teleomorph Emericella nidulans (Eidam) Vuill.] 107 Aspergillus niger Tiegh. 107, 114 Aspergillus sulphureus (Fresen.) Thom & Church 107 Aspergillus sydowii (Bainier & Sartory) Thom & Church 107 Aspergillus tamarii Kita 107 Aspergillus terreus Thom 107 Aspergillus unguis (Émile-Weil & L.Gaudin) C.W.Dodge (teleomorph Emericella unguis Malloch & Cain) 107 Asterina microthyrioides G.Winter [this is Phaeothyriolum microthyrioides (G.Winter) H.J.Swart] 179 Asteromella Pass. & Thüm. 170 Asteromella sp. [teleomorph Mycosphaerella cryptica (Cooke) Hansf.] Astraeus pteridis (Shear) Zeller 78 Athelia rolfsii (Curzi) C.C.Tu & Kimbr. (sclerotial state Sclerotium rolfsii Sacc.) 139, 501, 509 Aulographina eucalypti (Cooke & Massee) Arx & E.Müll. [anamorph Thyrinula eucalypti (Cooke & Massee) H.J.Swart] 56, 154, 155, 157, 158, 163, 176, 201, 212, 227, 228, 229, 428, 461, 466, 522, Plates 9.1, 9.2, 9.3 Aulographum eucalypti Cooke & Massee [this is Aulographina eucalypti (Cooke & Massee) Arx & E.Müll.] 155 Aurantioporus pulcherrimus (Rodway) P.K.Buchanan & Hood 310

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Aurantiosacculus eucalypti (Cooke & Massee) Dyko & B.Sutton 183, 211, Plate 9.21 Australoporus tasmanicus (Berk.) P.K.Buchanan & Ryvarden 317 Austroboletus cookei (Sacc. & P.Syd.) Wolfe [this is Austroboletus lacunosus (Kuntze) T.W.May & A.E.Wood] 78 Austroboletus lacunosus (Kuntze) T.W.May & A.E.Wood 78 Austroboletus occidentalis Watling 78 Austrogautieria 83 Austrogautieria clelandii E.L.Stewart & Trappe 78 Austrogautieria manjimupana Trappe & E.L.Stewart 78 Bacillus (Bacterium) 504 Bartalinia terricola Luke & S.U.Devi 140 Bipolaris spicifera (Bainier) Subram. [this is Drechslera spicifera (Bainier) Arx] 142 Bipolaris tetramera (McKinney) Shoemaker 108 Biscogniauxia capnodes (Berk.) Y.M.Ju & J.D.Rogers [syn. Hypoxylon nummularium Bull.:Fr. var. pseudopachiloma (Speg.) J.H.Mill.] Biscogniauxia mediterranea (De Not.) Kuntze (anamorph Botrytis sylvatica Malençon) [syn. Hypoxylon mediterraneum (De Not.) Ces. & De Not.] Bispora betulina (Corda) S.Hughes 326 Blastacervulus eucalypti H.J.Swart 201, 211, 229 Boletellus 83 Boletellus ananas (M.A.Curtis) Murrill 78 Boletellus obscurecoccineus (Höhn.) Singer 78 Boletus 83, 86, 88 Boletus edulis Bull.:Fr. 78, 85 Boletus multicolor Cleland 78 Boletus sinapecruentus Cleland 78 Botryobasidium salmonicolor (Berk. & Broome) Venkatarayan [this is Erythricium salmonicolor (Berk. & Broome) Burds.] 245 Botryodiplodia 108, 114, 248 Botryodiplodia theobromae Pat. [this is Lasiodiplodia theobromae (Pat.) Griffon & Maubl.] 242, 522 Botryosphaeria 105, 241, 245, 248, 249 Botryosphaeria dothidea (Moug.:Fr.) Ces. & De Not. (anamorph Fusicoccum aesculi Corda) 105, 245, 248, 422, 526 Botryosphaeria rhodina (Berk. & M.A.Curtis) Arx [anamorph Lasiodiplodia theobromae (Pat.) Griffon & Maubl.] Botryosphaeria ribis Grossenb. & Duggar (anamorph Fusicoccum sp.) 105, 158, 218, 219, 225, 245, 248, 249, 252, 419, 467 Botryotinia fuckeliana (de Bary) Whetzel (anamorph Botrytis cinerea Pers.) 123, 207 Botryotrichum 108 Botrytis 121, 219, 502, 503 Botrytis cinerea Pers. [teleomorph Botryotinia fuckeliana (de Bary) Whetzel] 56, 103, 108, 119, 120, 121, 123, 124, 207, 210, 219, 489, 491, 493, 496, 502, 503, 506, 510 Botrytis sylvatica Malençon [teleomorph Biscogniauxia mediterranea (De Not.) Kuntze] Boudiera tracheia (Gamundí) Dissing & T.Schumach. 81

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Burkholderia solanacearum (Smith 1896) Yabuuchi, Kosako, Oyaizu, Yano, Hotta, Hashimoto, Ezaki & Arakawa 1993 [this is Ralstonia solanacearum (Smith 1896) Yabuuchi, Kosako, Yano, Hotta & Nishiuchi 1995] (Bacterium) 343, 431, 524 Calonectria De Not. 121, 124, 126, 207, 431 Calonectria colhounii Peerally (anamorph Cylindrocladium colhounii Peerally var. colhounii) 126 Calonectria crotalariae (Loos) D.K.Bell & Sobers (this is Calonectria ilicicola Boedijn & Reitsma) 127, 128 Calonectria gracilis Crous, M.J.Wingf. & Alfenas [anamorph Cylindrocladium gracile (Bugnic.) Boesew.] 126, 207, 224 Calonectria ilicicola Boedijn & Reitsma (anamorph Cylindrocladium parasiticum Crous, M.J.Wingf. & Alfenas) 123, 125, 126, 127, 128, 225 Calonectria indusiata Seaver [this is Nectria indusiata Seaver (= Calonectria P.W. Crous pers. comm.)] Calonectria kyotensis Terash. (anamorph Cylindrocladium floridanum Sobers & C.P.Seym.) 123, 126 Calonectria macroconidialis (Crous, M.J.Wingf. & Alfenas) Crous [anamorph Cylindrocladium macroconidiale (Crous, M.J.Wingf. & Alfenas) Crous] 126 Calonectria morganii Crous, Alfenas & M.J.Wingf. (anamorph Cylindrocladium scoparium Morgan) 124, 126, 208, 222 Calonectria ovata D.Victor & Crous (anamorph Cylindrocladium ovatum El-Gholl, Alfenas, Crous & T.S.Schub.) 126, 208, 222 Calonectria pteridis Crous, M.J.Wingf. & Alfenas (anamorph Cylindrocladium pteridis F.A.Wolf) 126 Calonectria pyrochroa (Desm.) Sacc. [anamorph Cylindrocladium ilicicola (Hawley) Boedijn & Reitsma] 126, 225 Calonectria quinqueseptata Figueiredo & Namek. (anamorph Cylindrocladium quinqueseptatum Boedijn & Reitsma) 121, 126, 172, 208, 223 Calonectria reteaudii (Bugnic.) C.Booth [anamorph Cylindrocladium reteaudii (Bugnic.) Boesew.] Calonectria scoparia Peerally (anamorph Cylindrocladium candelabrum Viégas) 124, 126, 207, 222 Calonectria spathulata El-Gholl, Kimbr., E.L.Barnard, Alfieri & Schoult. (anamorph Cylindrocladium spathulatum El-Gholl, Kimbr., E.L.Barnard, Alfieri & Schoult.) Calonectria theae Loos [this is Nectria indusiata Seaver (= Calonectria P.W. Crous pers. comm.)] Calonectria variabilis Crous, B.J.H.Janse, D.Victor, G.F.Marais & Alfenas (anamorph Cylindrocladium variabile Crous, B.J.H.Janse, D.Victor, G.F.Marais & Alfenas) 126, 225 Camarosporellum eucalypti (G.Winter) Tassi [this is Dichomera eucalypti (G.Winter) B.Sutton] 211 Camarosporium eucalypti G.Winter [this is Dichomera eucalypti (G.Winter) B.Sutton] 211 Castoreum 83 Castoreum camphoratum Trappe & Malajczuk (nom. nud.) 78 Cenococcum 83, 87, 89

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Cenococcum geophilum Fr.:Fr. 81, 84, 85 Cenococcum graniforme (Sowerby) Ferd. & Winge (this is Cenococcum geophilum Fr.:Fr.) 81 Cephalosporium 108 Cercospora 133, 198, 200 Cercospora epicoccoides Cooke & Massee [this is Phaeophleospora epicoccoides (Cooke & Massee) Crous, F.A.Ferreira & B.Sutton] 133, 195, 198 Cercospora eucalypti Cooke & Massee [this is Phaeophleospora eucalypti (Cooke & Massee) Crous, F.A.Ferreira & B.Sutton] 133, 197, 198, 200 Cercospora eucalyptorum Crous 198, 207 Cercostigmina sp. [teleomorph Mycosphaerella suttoniae Crous & M.J.Wingf.; synanamorph Phaeophleospora epicoccoides (Cooke & Massee) Crous, F.A.Ferreira & B.Sutton] Ceuthospora innumera Massee (teleomorph Phacidium eucalypti G.W.Beaton & Weste) 51, 183, 187, 206, 210, 466 Ceuthospora lauri (Grev.) Grev. 183, 210 Chaetomium 108, 114 Chaetomium cochliodes Palliser (this is Chaetomium globosum Kunze) 108 Chaetomium funicola Cooke 108 Chaetomium globosum Kunze 108 Chaetomium homopilatum Omvik 108 Choanephora cf. cucurbitarum (Berk. & Ravenel) Thaxt. 108 Chondrostereum purpureum (Pers.:Fr.) Pouzar 320, 524 Cladosporium 108, 114, 162 Cladosporium cladosporioides (Fresen.) G.A.de Vries 108 Cladosporium herbarum (Pers.) Link [teleomorph Mycosphaerella tassiana (De Not.) Johanson] 108, 114, 141 Cladosporium orchidis E.A.Ellis & M.B.Ellis 108 Cladosporium oxysporum Berk. & M.A.Curtis 108 Cladosporium tenuissimum Cooke 108 Clasterosporium clavulatum (Cooke & Harkn.) Sacc. [this is Polyschema clavulata (Cooke & Harkn.) M.B.Ellis] 106 Clitocybe tabescens (Scop.) Bres. [this is Armillaria tabescens (Scop.) Emel] 294, 298 Clypeophysalospora latitans (Sacc.) H.J.Swart 141, 177, 182, 189, 190, 213 Cochliobolus australiensis (Tsuda & Ueyama) Alcorn [anamorph Drechslera australiensis (Bugnic.) M.B.Ellis] Cochliobolus eragrostidis (Tsuda & Ueyama) Sivan. [anamorph Curvularia eragrostidis (Henn.) J.A.Mey.] Cochliobolus geniculatus R.R.Nelson [anamorph Curvularia geniculata (Tracy & Earle) Boedijn] Cochliobolus lunatus R.R.Nelson & F.A.Haasis [anamorph Curvularia lunata (Wakker) Boedijn] Cochliobolus pallescens (Tsuda & Ueyama) Sivan. (anamorph Curvularia pallescens Boedijn) Cochliobolus spicifera R.R.Nelson [anamorph Drechslera spicifera (Bainier) Arx] 142 Cochliobolus verruculosus (Tsuda & Ueyama) Sivan. (anamorph Curvularia verruculosa M.B.Ellis) Codinaea 141 Codinaea septata B.Sutton & Hodges 141

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Colletogloeopsis molleriana Crous & M.J.Wingf. [teleomorph Mycosphaerella molleriana (Thüm.) Lindau] 161, 173 Colletogloeopsis nubilosum (Ganap. & Corbin) Crous & M.J.Wingf. [teleomorph Mycosphaerella cryptica (Cooke) Hansf.] 159, 168, 170 Colletogloeum nubilosum Ganap. & Corbin [this is Colletogloeopsis nubilosum (Ganap. & Corbin) Crous & M.J.Wingf.] 168 Colletotrichum 108, 219 Colletotrichum gloeosporioides (Penz.) Penz. & Sacc. [teleomorph Glomerella cingulata (Stoneman) Spauld. & H.Schrenk] 103, 104, 119, 130, 143, 201, 219, 228, 421, 505 Coltricia laeta (Cooke) G.Cunn. [this is Rigidoporus laetus (Cooke) P.K.Buchanan & Ryvarden] 316 Coma circularis (Cooke & Massee) Nag Raj & W.B.Kendr. [teleomorph Ascocoma eucalypti (Hansf.) H.J.Swart] 176, 177, 201 Confistulina hepatica (Sacc.) Stalpers [teleomorph Fistulina hepatica (Schaeff.:Fr.) Fr.] Coniella 119, 131, 219, 220, 221, Plate 9.25 Coniella australiensis Petr. 103, 108, 183, 220 Coniella castaneicola (Ellis & Everh.) B.Sutton (teleomorph Schizoparme straminea Shear) 131, 183, 220 Coniella eucalypticola Nag Raj [this is Coniella castaneicola (Ellis & Everh.) B.Sutton] 220 Coniella fragariae (Oudem.) B.Sutton 131, 183, 220, 221, 525 Coniella granati (Sacc.) Petr. & Syd. [teleomorph Schizoparme versoniana (Sacc. & Penz.) Nag Raj & Lowen] 131, 183, 220 Coniella minima B.Sutton & Thaung 183, 220 Coniella petrakii B.Sutton 183, 220 Coniella pulchella Höhn. [this is Coniella fragariae (Oudem.) B.Sutton] 220 Coniochaeta ligniaria (Grev.) Cooke 108 Coniophora cerebella (Pers.) Pers. [this is Coniophora puteana (Schumach.:Fr.) P.Karst.] 310 Coniophora olivacea (Fr.) P.Karst. 310 Coniophora puteana (Schumach.:Fr.) P.Karst. [syn. Coniophora cerebella (Pers.) Pers.] Coniothyrium Corda 211, 214, 229, 248, 249, 252, 522, 525 Coniothyrium ahmadii B.Sutton 184, 211 Coniothyrium eucalypti S.Ahmad (this is Coniothyrium ahmadii B.Sutton) 211 Coniothyrium eucalypticola B.Sutton 184, 211 Coniothyrium kallangurense B.Sutton & Alcorn 184, 211 Coniothyrium leprosum Fairm. [this is Fairmaniella leprosa (Fairm.) Petr. & Syd.] 105, 212 Coniothyrium ovatum H.J.Swart 184, 211, 212 Coniothyrium parvum H.J.Swart (this is Coniothyrium ovatum H.J.Swart) 211 Coprinus micaceus (Bull.:Fr.) Fr. 310 Coriolopsis aspera (Jungh.) Teng (syn. Fomes lineatoscaber Berk. & Broome) Corticium rolfsii Curzi [this is Athelia rolfsii (Curzi) C.C.Tu & Kimbr.] 139

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Corticium salmonicolor Berk. & Broome [this is Erythricium salmonicolor (Berk. & Broome) Burds.] 241, 245 Cortinarius 83, 86, 88, 89 Cortinarius archeri Berk. 78 Cortinarius australiensis (Cleland & Cheel) E.Horak 78 Cortinarius austrovenetus Cleland [this is Dermocybe austroveneta (Cleland) M.M.Moser & E.Horak] 79 Cortinarius basirubescens Cleland & J.R.Harris (= Dermocybe; May & Wood 1997) 78 Cortinarius castaneofulvus Cleland 78 Cortinarius cinnabarinus Fr. [this is Dermocybe cinnabarina (Fr.) Wünsche] 79 Cortinarius cinnamomeus (L.:Fr.) Fr. [this is Dermocybe cinnamomea (L.:Fr.) Wünsche] 79 Cortinarius clelandii A.H.Sm. (= Dermocybe; May & Wood 1997) 78 Cortinarius erythraeus Berk. 78 Cortinarius fragilipes Cleland 78 Cortinarius globuliformis Bougher 78 Cortinarius microarcheri Cleland 78 Cortinarius ochraceus Cleland (this is Cortinarius sinapicolor Cleland) 79 Cortinarius radicatus Cleland 79 Cortinarius rotundisporus Cleland & Cheel 79 Cortinarius sanguineus (Wulfen:Fr.) Fr. [this is Dermocybe sanguinea (Wulfen:Fr.) Wünsche] 79 Cortinarius sinapicolor Cleland 79 Cortinarius subarcheri Cleland 79 Cortinarius subcinnamomeus Cleland [this is Cortinarius clelandii A.H.Sm. (= Dermocybe; May & Wood 1997)] 78 Corynespora cassiicola (Berk. & M.A.Curtis) C.T.Wei 141 Coryneum viminale Cooke & Massee [this is Dichomera eucalypti (G.Winter) B.Sutton] 211 Cryphonectria 247, 250 Cryphonectria cubensis (Bruner) Hodges 25, 27, 241, 243, 244, 245, 246, 247, 248, 249, 250, 252, 436, 467, 522, 523, 525, 527, Plates 10.7, 10.8 Cryphonectria gyrosa (Berk. & Broome) Sacc. 249, 250 Cryphonectria havanensis (Bruner) M.E.Barr (anamorph Endothiella havanensis Roane) 249 Cryphonectria parasitica (Murrill) M.E.Barr (anamorph Endothiella parasitica Roane) 250, 431, Plates 10.9, 10.10 Cryptococcus neoformans (San Felice) Vuill. var. gattii Vanbreus. & Takashio (teleomorph Filobasidiella neoformans Kwon-Chung var. bacillispora KwonChung) 106 Cryptosporella sp. [anamorph Harknessia uromycoides (Speg.) Speg.] Cryptosporiopsis 220, 221 Cryptosporiopsis eucalypti Sankaran & B.Sutton 184, 220, 221, Plate 9.26 Cryptosporiopsis quercina Petr. [teleomorph Pezicula cinnamomea (DC.) Sacc.] Cryptostictis falcata B.Sutton [this is Vermisporium falcatum (B.Sutton) Nag Raj] 203 Curvularia 103, 109, 114, 141

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Curvularia eragrostidis (Henn.) J.A.Mey. [teleomorph Cochliobolus eragrostidis (Tsuda & Ueyama) Sivan.] 108, 141 Curvularia fallax Boedijn 109 Curvularia geniculata (Tracy & Earle) Boedijn (teleomorph Cochliobolus geniculatus R.R.Nelson) 109, 141, 142 Curvularia inaequalis (Shear) Boedijn 109 Curvularia lunata (Wakker) Boedijn (teleomorph Cochliobolus lunatus R.R.Nelson & F.A.Haasis) 109, 114, 141, 142, 501, 510 Curvularia lunata (Wakker) Boedijn var. aeria (Bat., I.H.Lima & C.T.Vasconc.) M.B.Ellis 109 Curvularia pallescens Boedijn [teleomorph Cochliobolus pallescens (Tsuda & Ueyama) Sivan.] 109, 114, 141, 142 Curvularia prasadii R.L.Mathur & B.L.Mathur 141, 501, 510 Curvularia pubescens [(sic) possibly Curvularia pallescens] 109 Curvularia senegalensis (Speg.) Subram. 109 Curvularia verruculosa M.B.Ellis [teleomorph Cochliobolus verruculosus (Tsuda & Ueyama) Sivan.] 109 Cylindrocarpon 505 Cylindrocarpon destructans (Zinssm.) Scholten (teleomorph Nectria radicola Gerlach & L.Nilsson) 37, 57, 58, 123 Cylindrocladiella Boesew. 119, 122, 124, 125, 126, 127, 129, 143, 207, 221, 222, 225 Cylindrocladiella camelliae (Venkataram. & C.S.V.Ram) Boesew. 125, 126, 127, 128, 207 Cylindrocladiella infestans Boesew. [teleomorph Nectria camelliae (Shipton) Boesew.] 125, 126, 127, 207 Cylindrocladiella lageniformis Crous, M.J.Wingf. & Alfenas 125, 126, 127, 207 Cylindrocladiella parva (P.J.Anderson) Boesew. 125, 126, 128, 129, 207 Cylindrocladiella peruviana (Bat., J.L.Bezerra & M.M.P.Herrera) Boesew. 207, 225 Cylindrocladium Morgan 4, 65, 119, 121, 122, 124, 125, 126, 127, 128, 129, 131, 138, 139, 143, 153, 154, 207, 220, 221, 222, 223, 224, 225, 229, 436, 491, 493, 498, 503, 504, 505, 510, 520, 525 Cylindrocladium brasiliense (Bat. & Cif.) Peerally (this is Cylindrocladium scoparium Morgan) 222 Cylindrocladium candelabrum Viégas (teleomorph Calonectria scoparia Peerally) 124, 125, 126, 130, 207, 221, 222, 223, 493, 504, 505 Cylindrocladium clavatum Hodges & L.C.May [this is Cylindrocladium gracile (Bugnic.) Boesew.] 127, 224, 493, 503, 504 Cylindrocladium colhounii Peerally var. colhounii (teleomorph Calonectria colhounii Peerally var. colhounii) 125, 126, 129, 225, 503 Cylindrocladium colhounii Peerally var. macroconidialis Crous, M.J.Wingf. & Alfenas [this is Cylindrocladium macroconidiale (Crous, M.J.Wingf. & Alfenas) Crous] 127 Cylindrocladium curvatum Boedijn & Reitsma 125, 126, 129, 497, 504

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Cylindrocladium ellipticum Alfieri, C.P.Seym. & Sobers (this is Cylindrocladium scoparium Morgan) 222 Cylindrocladium floridanum Sobers & C.P.Seym. (teleomorph Calonectria kyotensis Terash.) 125, 126, 128, 129, 130, 224 Cylindrocladium gracile (Bugnic.) Boesew. (teleomorph Calonectria gracilis Crous, M.J.Wingf. & Alfenas) 125, 126, 127, 128, 129, 130, 143, 207, 224, 493, 503, 504 Cylindrocladium heptaseptatum Sobers, Alfieri & Knauss 224 Cylindrocladium ilicicola (Hawley) Boedijn & Reitsma [teleomorph Calonectria pyrochroa (Desm.) Sacc.] 125, 126, 127, 128, 129, 130, 224, 225, 503 Cylindrocladium macroconidiale (Crous, M.J.Wingf. & Alfenas) Crous [teleomorph Calonectria macroconidialis (Crous, M.J.Wingf. & Alfenas) Crous] 125, 126, 127 Cylindrocladium ovatum El-Gholl, Alfenas, Crous & T.S.Schub. (teleomorph Calonectria ovata D.Victor & Crous) 124, 125, 126, 130, 208, 222, 223 Cylindrocladium parasiticum Crous, M.J.Wingf. & Alfenas (teleomorph Calonectria ilicicola Boedijn & Reitsma) 125, 126, 225 Cylindrocladium pithecolobii Petch (this is Cylindrocladium scoparium Morgan) 222 Cylindrocladium pteridis F.A.Wolf (teleomorph Calonectria pteridis Crous, M.J.Wingf. & Alfenas) 125, 126, 224, 396, 497, 504, 526 Cylindrocladium quinqueseptatum Boedijn & Reitsma (teleomorph Calonectria quinqueseptata Figueiredo & Namek.) 65, 121, 125, 126, 127, 128, 129, 130, 208, 222, 223, 224, 250, 497, 503, 504, 522, 523, Plates 9.27, 9.28 Cylindrocladium reteaudii (Bugnic.) Boesew. [teleomorph Calonectria reteaudii (Bugnic.) C.Booth] 224 Cylindrocladium scoparium Morgan (teleomorph Calonectria morganii Crous, Alfenas & M.J.Wingf.) 103, 109, 121, 122, 123, 124, 125, 126, 127, 128, 129, 130, 141, 143, 208, 222, 223, 224, 492, 497, 503, 504, 505, 510 Cylindrocladium spathulatum El-Gholl, Kimbr., E.L.Barnard, Alfieri & Schoult. (teleomorph Calonectria spathulata El-Gholl, Kimbr., E.L.Barnard, Alfieri & Schoult.) 225 Cylindrocladium theae (Petch) Subram. [teleomorph Nectria indusiata Seaver (= Calonectria P.W. Crous pers. comm.)] 125, 126, 127 Cylindrocladium variabile Crous, B.J.H.Janse, D.Victor, G.F.Marais & Alfenas (teleomorph Calonectria variabilis Crous, B.J.H.Janse, D.Victor, G.F.Marais & Alfenas) 125, 126, 225 Cylindrosporium eucalypti McAlpine [this is Vermisporium eucalypti (McAlpine) Nag Raj] 202, 203 Cylindrosporium samuelii Hansf. [this is Vermisporium samuelii (Hansf.) J.A.Simpson & Grgur.] 203 Cylindrotrichum Bonord. 208, 211 Cystangium rodwayi (Massee) A.H.Sm. 79 Cytospora 248 Cytospora eucalypticola Van der Westh. [teleomorph Valsa ceratosperma (Tode:Fr.) Maire] 140, 142, 245, 248, 250, 251, 252, 326, 419, Plate 10.11

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Davisoniella eucalypti H.J.Swart 184, 211 Dematophora necatrix R.Hartig (teleomorph Rosellinia necatrix Prill.) Dermocybe austroveneta (Cleland) M.M.Moser & E.Horak 79 Dermocybe cinnabarina (Fr.) Wünsche 79 Dermocybe cinnamomea (L.:Fr.) Wünsche 79 Dermocybe sanguinea (Wulfen:Fr.) Wünsche 79 Dermocybe splendida E.Horak 79 Descolea 85 Descolea maculata Bougher 79, 87, 90, 91 Descolea recedens (Cooke & Massee) Singer 87 Descomyces albellus (Massee & Rodway) Bougher & Castellano 79, 84, 85, 91 Descomyces albus (Klotzsch) Bougher & Castellano 79, 85 Dextrinocystidium sacratum (G.Cunn.) Sheng H.Wu 302 Diaporthe cubensis Bruner [this is Cryphonectria cubensis (Bruner) Hodges] 247 Diaporthe parasitica Murrill [this is Cryphonectria parasitica (Murrill) M.E.Barr] 250 Dichomera 211 Dichomera eucalypti (G.Winter) B.Sutton 184, 211, 212 Dichomera versiformis Z.Q.Yuan, Wardlaw & C.Mohammed 184, 211 Dictyopanus pusillus (Pers.:Lév.) Singer [syn. Panellus pusillus (Pers.:Lév.) Burds. & O.K.Mill.] Dictyopanus rhipidium (Berk.) Pat. [this is Dictyopanus pusillus (Pers.:Lév.) Singer] 312 Diplocladium cylindrosporum Ellis & Everh. (this is Cylindrocladium scoparium Morgan) 222 Discohainesia oenotherae (Cooke & Ellis) Nannf. [synanamorphs Hainesia lythri (Desm.) Höhn. and Pilidium concavum (Desm.) Höhn.] 119, 132, 184, 225 Discostroma corticola (Fuckel) Brockmann [anamorph Seimatosporium lichenicola (Corda) Shoemaker & E.Müll.] Dothidella inaequalis Cooke [this is Rehmiodothis inaequalis (Cooke) H.J.Swart] 189 Dothiorella 105, 218, 248 Dothiorella australis (Cooke) Petr. & Syd. [this is Idiocercus australis (Cooke) H.J.Swart] 213 Dothiorella eucalypti (Berk. & Broome) Sacc. 103, 104, 105, 109, 225 Dothiorella eucalypti (Berk. & Broome) Sacc. forma microspora Sousa da Câmara 104 Drechslera 109 Drechslera australiensis (Bugnic.) M.B.Ellis [teleomorph Cochliobolus australiensis (Tsuda & Ueyama) Alcorn] 109, 114 Drechslera halodes (Drechsler) Subram. & B.L.Jain [this is Exserohilum rostratum (Drechsler) K.J.Leonard & Suggs, emen. K.J.Leonard] 114 Drechslera rostrata (Drechsler) M.J.Richardson & E.M.Fraser [this is Exserohilum rostratum (Drechsler) K.J.Leonard & Suggs, emen. K.J.Leonard] 114 Drechslera spicifera (Bainier) Arx (teleomorph Cochliobolus spicifera R.R.Nelson) 109, 142

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Elaphomyces 83 Elsinoë eucalypti Hansf. (anamorph Sphaceloma sp.) 158, 176 Embolidium eucalypti Bat. & Peres [this is Coniella castaneicola (Ellis & Everh.) B.Sutton] 220 Emericella nidulans (Eidam) Vuill. [anamorph Aspergillus nidulans (Eidam) G.Winter] 109 Emericella unguis Malloch & Cain [anamorph Aspergillus unguis (Émile-Weil & L.Gaudin) C.W.Dodge] Endogone 83, 86 Endogone aggregata P.A.Tandy 82, 91 Endogone tuberculosa Lloyd 82, 91 Endothia 250 Endothia eugeniae (Nutman & F.M.Roberts) J.Reid & C.Booth [this is Cryphonectria cubensis (Bruner) Hodges] 25, 247 Endothia gyrosa (Schwein.:Fr.) Fr. (anamorph Endothiella gyrosa Sacc.) 241, 245, 248, 251, 252, 419, 467, 526, Plates 10.1, 10.3, 10.5, 10.12–10.14, 17.3 Endothia havanensis Bruner [this is Cryphonectria havanensis (Bruner) M.E.Barr] 247, 249, 251 Endothia parasitica (Murrill) P.J.Anderson & H.W.Anderson [this is Cryphonectria parasitica (Murrill) M.E.Barr] 250 Endothia tropicalis Shear & N.E.Stevens [this is Cryphonectria gyrosa (Berk. & Broome) Sacc.] 249 Endothiella 250, 251, Plate 10.12 Endothiella gyrosa Sacc. [teleomorph Endothia gyrosa (Schwein.:Fr.) Fr.] 251 Endothiella havanensis Roane [teleomorph Cryphonectria havanensis (Bruner) M.E.Barr] Endothiella parasitica Roane [teleomorph Cryphonectria parasitica (Murrill) M.E.Barr] 250 Epicoccum nigrum Link 109, 114 Epicoccum purpurascens Ehrenb. (this is Epicoccum nigrum Link) 114 Erysiphe cichoracearum DC. (anamorph Oidium asterispunicei Peck) 136, 137, 191 Erysiphe orontii Castagne emen. U.Braun (anamorph Oidium violae Pass. emen. U.Braun) 136, 191 Erysiphe paniculata (unknown taxon) 136, 191 Erysiphe polyphaga Hammarl. (this is Erysiphe orontii Castagne emen. U.Braun) 136, 191 Erythricium 246 Erythricium salmonicolor (Berk. & Broome) Burds. (anamorph Necator decretus Massee) (syn. Corticium salmonicolor Berk. & Broome) 241, 243, 245, 246, 252, 521 Eupenicillium brefeldianum (B.O.Dodge) Stolk & D.B.Scott (anamorph Penicillium dodgei Pitt) Exserohilum rostratum (Drechsler) K.J.Leonard & Suggs, emen. K.J.Leonard (teleomorph Setosphaeria rostrata K.J.Leonard) 109, 114, 142 Fairmaniella leprosa (Fairm.) Petr. & Syd. 103, 105, 109, 142, 178, 201, 212, 213 Fennellia flavipes B.J.Wiley & E.G.Simmons (anamorph Aspergillus fumigatus Fresen.) Fibuloporia mollusca (Pers.:Fr.) Bondartsev & Singer [this is Trechispora mollusca (Pers.:Fr.) Liberta] 316

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Filobasidiella neoformans Kwon-Chung var. bacillispora Kwon-Chung [anamorph Cryptococcus neoformans (San Felice) Vuill. var. gattii Vanbreus. & Takashio] 106 Fistulina hepatica (Schaeff.:Fr.) Fr. [anamorph Confistulina hepatica (Sacc.) Stalpers] 320, 331, 332 Fistulina spiculifera (Cooke) D.A.Reid 310, 331, 332, Plate 13.9 Flammula crociphylla Sacc. 310 Fomes conchatus (Pers.:Fr.) Gillet [this is Phellinus conchatus (Pers.:Fr.) Quél.] 321 Fomes fomentarius (L.:Fr.) J.J.Kickx 320 Fomes gilvus (Schwein.) Lloyd [this is Phellinus gilvus (Schwein.) Pat.] 312 Fomes lineato-scaber Berk. & Broome [this is Coriolopsis aspera (Jungh.) Teng] 312 Fomes rimosus (Berk.) Cooke [this is Phellinus rimosus (Berk.) Pilát] 313 Fomes robinsoniae (Murrill) Sacc. & Trotter [this is Phellinus robustus (P.Karst.) Bourdot & Galzin] 318 Fomes robustus P.Karst. [this is Phellinus robustus (P.Karst.) Bourdot & Galzin] 313, 318 Fomitopsis feei (Fr.) Kreisel 320 Fusarium 103, 110, 114, 119, 121, 123, 131, 132, 143, 489, 490, 491, 505 Fusarium avenaceum (Fr.) Sacc. (teleomorph Gibberella avenacea R.J.Cooke) 123, 131 Fusarium chlamydosporum Wollenw. & Reinking 490, 506 Fusarium equiseti (Corda) Sacc. (teleomorph Gibberella intricans Wollenw.) 109 Fusarium graminearum Schwabe [teleomorph Gibberella zeae (Schwein.:Fr.) Petch] 109 Fusarium longipes Wollenw. & Reinking 123, 131 Fusarium moniliforme J.Sheld. [teleomorph Gibberella fujikuroi (J.Sawada) S.Ito] 110, 114, 490, 506 Fusarium oxysporum Schltdl. emen. W.C.Snyder & H.N.Hansen 110, 114, 121, 131, 506 Fusarium oxysporum Schltdl. emen. W.C.Snyder & H.N.Hansen forma eucalypti Arya & G.L.Jain 131, 132 Fusarium oxysporum Schltdl. emen. W.C.Snyder & H.N.Hansen var. aurantiacum (Link) Wollenw. (this is Fusarium oxysporum Schltdl. emen. W.C.Snyder & H.N.Hansen) 131 Fusarium pallidoroseum (Cooke) Sacc. (syn. Fusarium semitectum Berk. & Ravenel) Fusarium poae (Peck) Wollenw. 110 Fusarium sambucinum Fuckel [teleomorph Gibberella pulicaris (Fr.) Sacc.] 131 Fusarium semitectum Berk. & Ravenel [this is Fusarium pallidoroseum (Cooke) Sacc.] 110, 114 Fusarium solani (Mart.) Sacc. (teleomorph Nectria haematococca Berk. & Broome) 110, 114, 115, 121, 131, 490, 496, 506 Fusicoccum sp. (teleomorph Botryosphaeria ribis Grossenb. & Duggar) 105, 110, 158, 218, 248 Fusicoccum aesculi Corda [teleomorph Botryosphaeria dothidea (Moug.:Fr.) Ces. & De Not.] 105

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Ganoderma 293, 301, 434 Ganoderma applanatum (Pers.) Pat. 320 Ganoderma colossum (Fr.) C.F.Baker 300 Ganoderma lucidum (Curtis) P.Karst. 301, 310, 320 Ganoderma sculpturatum (Lloyd) Ryvarden 301 Gibberella avenacea R.J.Cooke [anamorph Fusarium avenaceum (Fr.) Sacc.] Gibberella fujikuroi (J.Sawada) S.Ito (anamorph Fusarium moniliforme J.Sheld.) Gibberella intricans Wollenw. [anamorph Fusarium equiseti (Corda) Sacc.] Gibberella pulicaris (Fr.) Sacc. (anamorph Fusarium sambucinum Fuckel) Gibberella zeae (Schwein.:Fr.) Petch (anamorph Fusarium graminearum Schwabe) Gigaspora 86 Gigaspora heterogama (T.H.Nicolson & Gerd.) Gerd. & Trappe 82 Gigaspora margarita W.N.Becker & I.R.Hall 82 Gliocephalotrichum 110 Gliocladium penicillioides Corda 110 Gliocladium roseum Bainier [teleomorph Nectria ochroleuca (Schwein.) Berk.] 110, 503 Gliocladium virens J.H.Mill., Giddens & A.A.Foster 507 Gloeocystidiellum sacratum (G.Cunn.) Stalpers & P.K.Buchanan [this is Dextrinocystidium sacratum (G.Cunn.) Sheng H.Wu] 302 Gloeosporiella eucalypti Hansf. [this is Coma circularis (Cooke & Massee) Nag Raj & W.B.Kendr.] 176 Gloeosporium capsularum Cooke & Harkn. 105, 110 Gloeosporium carpogenum Cooke & Harkn. [this is Marssonina carpogena (Cooke & Harkn.) Arx] 105 Glomerella cingulata (Stoneman) Spauld. & H.Schrenk [anamorph Colletotrichum gloeosporioides (Penz.) Penz. & Sacc.] 130, 131, 505 Glomus 86 Glomus claroideum N.C.Schenck & G.S.Sm. 82 Glomus clarum T.H.Nicolson & N.C.Schenck 82, 91 Glomus constrictum Trappe 82 Glomus fasciculatum (Thaxt.) Gerd. & Trappe emen. C.Walker & Koske 82 Glomus intraradices N.C.Schenck & G.S.Sm. 82, 91 Glomus macrocarpum Tul. & C.Tul. 82 Glomus monosporum Gerd. & Trappe 82 Glomus pallidum I.R.Hall 91 Gnomoniella destruens M.E.Barr & Hodges 142 Grifola campyla (Berk.) G.Cunn. [this is Ryvardenia campyla (Berk.) Rajchenb.] 316, 319 Grifola sulphurea (Bull.:Fr.) Pilát [this is Laetiporus sulphureus (Bull.:Fr.) Murrill] 317 Guignardia eucalyptorum Crous (anamorph Phyllosticta eucalyptorum Crous, M.J.Wingf., F.A.Ferreira & Alfenas) 158, 182, 187 Gymnoglossum violaceum (Massee & Rodway) G.Cunn. [this is Protoglossum violaceum (Massee & Rodway) T.W.May] 80 Gymnomyces 83 Gymnomyces socialis (Harkn.) Singer & A.H.Sm. 79 Gymnopilus crociphyllus (Sacc.) Pegler 310 Gymnopilus spectabilis (Fr.:Fr.) A.H.Sm. 310, 311 Gyroporus cyanescens (Bull.:Fr.) Quél. 79

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Hainesia lythri (Desm.) Höhn. [teleomorph Discohainesia oenotherae (Cooke & Ellis) Nannf.; synanamorph Pilidium concavum (Desm.) Höhn.] 132, 133, 184, 225, 227, 228, 503, 506 Hapalopilus 311 Hapalopilus mutans (Peck) Gilb. & Ryvarden 311 Harknessia 103, 142, 193, 195, 228 Harknessia eucalypti Cooke 185, 193 Harknessia eucalyptorum Crous, M.J.Wingf. & Nag Raj (teleomorph Wuestneia eucalyptorum Crous, M.J.Wingf. & Nag Raj) 185, 194 Harknessia fumaginea B.Sutton & Alcorn 110, 114, 185, 194 Harknessia globosa B.Sutton 142, 185, 193, 194 Harknessia hawaiiensis F.Stevens & E.Young 110, 142, 185, 193, 194 Harknessia insueta B.Sutton 185, 193 Harknessia tasmaniensis Z.Q.Yuan, Wardlaw & C.Mohammed 185, 194 Harknessia uromycoides (Speg.) Speg. (teleomorph Cryptosporella sp.) 105, 110, 142, 185, 193, 194 Harknessia victoriae B.Sutton & Pascoe 185, 194 Hebeloma aminophilum R.N.Hilton & O.K.Mill. 79 Hebeloma coarctatum (Cooke & Massee) Pegler 79 Hebeloma crustuliniforme (Bull.:Fr.) Quél. 79, 84 Hebeloma hiemale Bres. 84 Hebeloma mesophaeum (Pers.) Quél. 79, 84 Hebeloma westraliense Bougher, Tommerup & Malajczuk 79, 91 Helicobasidium compactum Boedijn 302 Hendersonia 215, 217 Hendersonia eucalypti Cooke & Harkn. [probably Seimatosporium lichenicola (Corda) Shoemaker & E.Müll.] 215 Hendersonia eucalypticola A.R.Davis [this is Sonderhenia eucalypticola (A.R.Davis) H.J.Swart & J.Walker] 215 Hendersonia eucalyptorum Hansf. [this is Sonderhenia eucalyptorum (Hansf.) H.J.Swart & J.Walker] 215 Hendersonia fraserae Hansf. [this is Sonderhenia eucalypticola (A.R.Davis) H.J.Swart & J.Walker] 215 Hendersonia grandispora McAlpine [this is Phaeophleospora epicoccoides (Cooke & Massee) Crous, F.A.Ferreira & B.Sutton] 133, 175, 195, 215 Heterobasidion annosum (Fr.:Fr.) Bref. 438, 465 Heterobasidion hemitephrum (Berk.) G.Cunn. 317 Heteroporus biennis (Bull.:Fr.) Lázaro Ibiza [this is Abortiporus biennis (Bull.:Fr.) Singer] 302 Hexagonia gunnii Berk. [this is Hexagonia vesparius (Berk.) Ryvarden] 311 Hexagonia vesparius (Berk.) Ryvarden 311, 317 Humicola cf. fuscoatra Traaen 110 Hydnangium 83, 85, 86 Hydnangium archeri (Berk.) Rodway 79 Hydnangium australiense Berk. & Broome [this is Zelleromyces australiensis (Berk. & Broome) Pegler & T.W.K.Young] 81 Hydnangium carneum Wallr. 79, 84, 85, 91 Hydnangium densum Rodway [this is Octaviania densa (Rodway) G.Cunn. (=Melanogaster; May & Wood 1997)] 80

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Hydnangium soederstroemii Lagerh. (this is Hydnangium carneum Wallr.) 79 Hydnangium sublamellatum Bougher, Tommerup & Malajczuk 79 Hydnangium tasmanicum Kalchbr. [this is Octavianina tasmanica (Kalchbr.) Pegler & T.W.K.Young] 80 Hydnum repandum L. 79 Hygrocybe coccinea (Schaeff.:Fr.) P.Kumm. [Australian records are either Hygrocybe kandora Grgur. & A.M.Young or Hygrocybe miniata (Fr.:Fr.) Kummer] 79 Hygrocybe kandora Grgur. & A.M.Young 82 Hygrocybe miniata (Fr.:Fr.) Kummer 82 Hygrophorus coccineus (Schaeff.:Fr.) Fr. [this is Hygrocybe coccinea (Schaeff.:Fr.) P.Kumm.] 79 Hymenangium 83, 85 Hymenangium album Klotzsch [this is Descomyces albus (Klotzsch) Bougher & Castellano] 85 Hymenochaete 309, 311, 317, 332 Hymenochaete floridea Berk. & Broome 320 Hymenochaete rhabarbarina (Berk.) Cooke 320 Hymenogaster 79, 83, 85 Hymenogaster albellus Massee & Rodway [this is Descomyces albellus (Massee & Rodway) Bougher & Castellano] 79, 84, 85 Hymenogaster albus (Klotzsch) Berk. & Broome [this is Descomyces albus (Klotzsch) Bougher & Castellano] 79, 85 Hymenogaster maurus Maire [this is Descomyces albus (Klotzsch) Bougher & Castellano] 79 Hymenogaster zeylanicus Petch [this is Descomyces albellus (Massee & Rodway) Bougher & Castellano] 79, 91 Hypholoma 297, 465 Hypholoma fasciculare (Huds.:Fr.) P.Kumm. 79 Hypospila eucalypti Wakef. [this is Mycosphaerella eucalypti (Wakef.) Hansf.] 165 Hypoxylon 252 Hypoxylon mediterraneum (De Not.) Ces. & De Not. [this is Biscogniauxia mediterranea (De Not.) Kuntze] 251, 252 Hypoxylon nummularium Bull.:Fr. var. pseudopachiloma (Speg.) J.H.Mill. [this is Biscogniauxia capnodes (Berk.) Y.M.Ju & J.D.Rogers] 252 Hypoxylon stygium (Lév.) Sacc. 252 Hysterangium 79, 83, 85 Hysterangium affine Massee & Rodway 79 Hysterangium gardneri E.Fisch. 79 Hysterangium incarceratum Malençon 80 Hysterangium inflatum Rodway 80, 85 Hysterangium viscidum Massee & Rodway [this is Protoglossum viscidum (Massee & Rodway) T.W.May] 80 Idiocercus 214 Idiocercus australis (Cooke) H.J.Swart 177, 186, 189, 213 Inocybe 80, 83, 85 Inocybe australiensis Cleland & Cheel 80 Inocybe fibrillosibrunnea O.K.Mill. & R.N.Hilton 80 Inocybe fulvo-olivacea Cleland 80, 91

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Inocybe granulosipes Cleland (this is Inocybe australiensis Cleland & Cheel) 80 Inocybe patouillardii Bres. 84 Inocybe petiginosa (Fr.:Fr.) Gillet 80 Inonotus 307, 325 Inonotus albertinii (Lloyd) P.K.Buchanan & Ryvarden 302, 311 Inonotus chondromyelus Pegler 311, 317, 323 Inonotus dryadeus (Pers.) Murrill (this a valid species but has been included in Inonotus chondromyelus Pegler) 311 Inonotus luteo-contextus D.A.Reid 317 Inonotus rheades (Pers.) Bondartsev & Singer 312, 320 Inonotus victoriensis (Lloyd) Pegler 317 Junghuhnia vincta (Berk.) Hood & M.Dick 302 Kirramyces 133, 176, 179, 195, 198 Kirramyces destructans M.J.Wingf. & Crous [this is Phaeophleospora destructans (M.J.Wingf. & Crous) Crous, F.A.Ferreira & B.Sutton] 186, 198 Kirramyces epicoccoides (Cooke & Massee) J.Walker, B.Sutton & Pascoe [this is Phaeophleospora epicoccoides (Cooke & Massee) Crous, F.A.Ferreira & B.Sutton] 133, 175, 186, 195, 215, 498, 506, 522 Kirramyces eucalypti (Cooke & Massee) J.Walker, B.Sutton & Pascoe [this is Phaeophleospora eucalypti (Cooke & Massee) Crous, F.A.Ferreira & B.Sutton] 133, 171, 186, 197 Kirramyces lilianiae J.Walker, B.Sutton & Pascoe [this is Phaeophleospora lilianiae (J.Walker, B.Sutton & Pascoe) Crous, F.A.Ferreira & B.Sutton] 187, 198 Labyrinthomyces 83 Labyrinthomyces varius (Rodway) Trappe 81 Labyrinthomyces westraliensis G.W.Beaton & Malajczuk [this is Reddellomyces westraliensis (G.W.Beaton & Malajczuk) Trappe, Castellano & Malajczuk] 82 Laccaria 83, 85, 89 Laccaria fraterna (Sacc.) Pegler 80, 83 Laccaria laccata (Scop.:Fr.) Cooke 80, 83, 85, 88, 91 Laccaria lateritia Malençon 80, 83, 85 Laccaria ohiensis (Mont.) Singer (this is Laccaria lateritia Malençon) 80, 83, 85 Lachnea vinoso-brunnea (Berk. & Broome) Sacc. 82 Lactarius 83 Lactarius clarkeae Cleland 80 Lactarius deliciosus (L.:Fr.) Gray 84, 93 Lactarius eucalypti O.K.Mill. & R.N.Hilton 80 Laestadia eucalypti Rolland [this is Clypeophysalospora latitans (Sacc.) H.J.Swart] 189 Laestadia eucalypti Speg. [this is Clypeophysalospora latitans (Sacc.) H.J.Swart] 189 Laestadia rollandii Sacc. & P.Syd. [this is Clypeophysalospora latitans (Sacc.) H.J.Swart] 189 Laetiporus 325 Laetiporus baudonii (Pat.) Ryvarden [this is Pseudophaeolus baudonii (Pat.) Ryvarden] 300 Laetiporus discolor (Klotzsch) Corner 320 Laetiporus sulphureus (Bull.:Fr.) Murrill 317, 320, 321, 327, 331, 332

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Lasiodiplodia theobromae (Pat.) Griffon & Maubl. [teleomorph Botryosphaeria rhodina (Berk. & M.A.Curtis) Arx] 242, 248, 252, 522 Lecanostictopsis eucalypti Crous 195, 201 Lembosia eucalypti F.Stevens & M.Dixon [this is Aulographina eucalypti (Cooke & Massee) Arx & E.Müll.] 155 Lembosiopsis australiense Hansf. [this is Aulographina eucalypti (Cooke & Massee) Arx & E.Müll.] 155 Lembosiopsis eucalyptina Petr. & Syd. [this is Aulographina eucalypti (Cooke & Massee) Arx & E.Müll.] 155 Lentinus squarrosulus Mont. 321 Leptostromella eucalypti Cooke & Massee [this is Thyrinula eucalypti (Cooke & Massee) H.J.Swart] 156 Leptothyrium aristatum Cooke [this is Tracylla aristata (Cooke) Tassi] 227 Leucopaxillus lilacinus Bougher 80 Leucostoma 251 Lewia infectoria (Fuckel) M.E.Barr & E.G.Simmons (anamorph Alternaria sp.) 110 Lycoperdon gunnii Berk. 80 Lycoperdon perlatum Pers. 80 Macrohilum eucalypti H.J.Swart 178, 186, 225 Macrolepiota bonaeriensis (Speg.) Singer 80 Macrophoma 110 Macrophoma australis (Cooke) Berl. & Voglino [this is Idiocercus australis (Cooke) H.J.Swart] 213 Macrophomina 110, 114, 115 Macrophomina phaseolina (Tassi) Goid. 103, 110, 121, 133, 134, 493, 498, 506, 507 Macrophyllosticta eucalyptina (Pat.) Sousa da Câmara 182, 187 Marasmius eucalypti Berk. 105, 106 Marssonina carpogena (Cooke & Harkn.) Arx 105 Martellia 80 Melampsora 191 Melampsora eucalypti Rabenh. 191 Melanconium eucalypticola Hansf. [this is Fairmaniella leprosa (Fairm.) Petr. & Syd.] 105, 212 Melanconium uromycoide Speg. [this is Harknessia uromycoides (Speg.) Speg.] 105 Melanogaster intermedius (Berk.) Zeller & C.W.Dodge 80 Memnoniella echinata (Rivolta) L.D.Galloway 110 Meruliopsis 317 Mesophellia 83 Mesophellia arenaria Berk. 80, 91 Mesophellia labyrinthina Trappe, Castellano & Malajczuk 80 Mesophellia trabalis Trappe, Castellano & Malajczuk 80, 91 Microporus xanthopus (Fr.) Kuntze 321 Microsphaeropsis 214, 215, 227 Microsphaeropsis callista (Syd.) B.Sutton 186, 215 Microsphaeropsis conielloides B.Sutton 186, 214 Microsphaeropsis globulosa (Sousa da Câmara) B.Sutton 215 Microsphaeropsis olivacea (Bonord.) Höhn. 215

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Microthyrium amygdalinum Cooke & Massee [this is Phaeothyriolum microthyrioides (G.Winter) H.J.Swart] 179 Microthyrium eucalypti Henn. 180 Microthyrium eucalypticola Speg. 158, 176, 181, 182 Monocillium 111 Montagnella eucalypti Cooke & Massee [this is Rehmiodothis eucalypti (Cooke & Massee) H.J.Swart] 189 Muciturbo reticulatus P.H.B.Talbot 82 Muciturbo truncatus P.H.B.Talbot 82 Muciturbo verrucosus P.H.B.Talbot 82 Mucor 111, 114 Mucor hiemalis Wehmer 111 Mucor plumbeus Bonord. 111 Mycena subgalericulata Cleland 312 Mycomicrothelia eucalyptina (Syd.) E.Müll. [this is Phaeothyriolum microthyrioides (G.Winter) H.J.Swart] 179 Mycoplasma (Phytoplasma) 343 Mycosphaerella 12, 65, 119, 134, 143, 153, 154, 155, 158, 163, 164, 165, 166, 173, 174, 200, 210, 212, 215, 227, 229, 431, 436, 438, 467, 498, 520, 522, 523, 525, 526 Mycosphaerella africana Crous & M.J.Wingf. 158, 164 Mycosphaerella colombiensis Crous & M.J.Wingf. (anamorph Pseudocercospora colombiensis Crous & M.J.Wingf.) 158, 164, 166 Mycosphaerella cryptica (Cooke) Hansf. [anamorphs Asteromella sp. and Colletogloeopsis nubilosum (Ganap. & Corbin) Crous & M.J.Wingf.] 24, 25, 26, 134, 154, 159, 161, 163, 164, 165, 168, 169, 170, 171, 172, 173, 174, 176, 205, 227, 228, 229, 435, 437, 466, 507, 522, Plates 9.4–9.8 Mycosphaerella crystallina Crous & M.J.Wingf. (anamorph Pseudocercospora crystallina Crous & M.J.Wingf.) 159, 164, 166 Mycosphaerella delegatensis R.F.Park & Keane [anamorph Phaeophleospora delegatensis (R.F.Park & Keane) Crous] 159, 171, 174, 229, Plate 9.9 Mycosphaerella didymelloides Petr. 165 Mycosphaerella ellipsoidea Crous & M.J.Wingf. (anamorph Uwebraunia ellipsoidea Crous & M.J.Wingf.) 159, 164 Mycosphaerella endophytica Crous & H.Sm.ter (anamorph Pseudocercosporella endophytica Crous & H.Sm.ter) 159, 164 Mycosphaerella eucalypti (Wakef.) Hansf. 165 Mycosphaerella flexuosa Crous & M.J.Wingf. 159, 164 Mycosphaerella gracilis Crous & Alfenas (anamorph Pseudocercospora gracilis Crous & Alfenas) 159, 164, 167 Mycosphaerella grandis Carnegie & Keane 160, 164, 165, 171 Mycosphaerella gregaria Carnegie & Keane 160, 165 Mycosphaerella heimii Bouriquet, nom. nud. (this is Mycosphaerella heimii Crous) 172 Mycosphaerella heimii Crous (anamorph Pseudocercospora heimii Crous) 160, 167, 172

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Mycosphaerella heimioides Crous & M.J.Wingf. (anamorph Pseudocercospora heimioides Crous & M.J.Wingf.) 160, 164, 167 Mycosphaerella irregulariramosa Crous & M.J.Wingf. (anamorph Pseudocercospora irregulariramosa Crous & M.J.Wingf.) 160, 164, 167 Mycosphaerella juvenis Crous & M.J.Wingf. (anamorph Uwebraunia juvenis Crous & M.J.Wingf.) 154, 160, 164, 165, 172, 230, 431, 435, 436 Mycosphaerella lateralis Crous & M.J.Wingf. (anamorph Uwebraunia lateralis Crous & M.J.Wingf.) 160, 164 Mycosphaerella longibasalis Crous & M.J.Wingf. 160, 164 Mycosphaerella marksii Carnegie & Keane 161, 163, 164, 172, Plate 9.10 Mycosphaerella martinae Hansf. 165 Mycosphaerella mexicana Crous 161, 164 Mycosphaerella molleriana (Thüm.) Lindau (anamorph Colletogloeopsis molleriana Crous & M.J.Wingf.) 161, 164, 172, 173, 174 Mycosphaerella nubilosa (Cooke) Hansf. 24, 26, 50, 134, 154, 161, 163, 164, 165, 168, 169, 170, 171, 172, 173, 174, 176, 185, 210, 229, 435, 437, 466, 507, 522, Plate 9.11 Mycosphaerella parkii Crous, M.J.Wingf., F.A.Ferreira & Alfenas (anamorph Stenella parkii Crous & Alfenas) 134, 161, 174 Mycosphaerella parva R.F.Park & Keane 161, 163, 164, 165, 169, 171, 172 Mycosphaerella suberosa Crous, F.A.Ferreira, Alfenas & M.J.Wingf. 159, 161, 163, 174, 175 Mycosphaerella suttoniae Crous & M.J.Wingf. [synanamorphs Cercostigmina sp. and Phaeophleospora epicoccoides (Cooke & Massee) Crous, F.A.Ferreira & B.Sutton] 161, 163, 175, 186, 195 Mycosphaerella swartii R.F.Park & Keane [anamorph Sonderhenia eucalyptorum (Hansf.) H.J.Swart & J.Walker] 134, 162, 165, 187, 215, 229 Mycosphaerella tasmaniensis Crous & M.J.Wingf. (anamorph Mycovellosiella tasmaniensis Crous & M.J.Wingf.) 162, 165 Mycosphaerella tassiana (De Not.) Johanson [anamorph Cladosporium herbarum (Pers.) Link] Mycosphaerella vespa Carnegie & Keane 162, 175 Mycosphaerella walkeri R.F.Park & Keane [anamorph Sonderhenia eucalypticola (A.R.Davis) H.J.Swart & J.Walker] 162, 163, 165, 187, 215, 229 Mycovellosiella eucalypti Crous & Alfenas 200, 208 Mycovellosiella tasmaniensis Crous & M.J.Wingf. (teleomorph Mycosphaerella tasmaniensis Crous & M.J.Wingf.) 162, 165 Myrothecium roridum Tode:Fr. 111 Naematoloma fasciculare (Huds.:Fr.) P.Karst. [this is Hypholoma fasciculare (Huds.:Fr.) P.Kumm.] 79 Necator decretus Massee [teleomorph Erythricium salmonicolor (Berk. & Broome) Burds.] 245 Nectria camelliae (Shipton) Boesew. (anamorph Cylindrocladiella infestans Boesew.) 126 Nectria Fr. 111, 124, 126, 207

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Nectria haematococca Berk. & Broome [anamorph Fusarium solani (Mart.) Sacc.] Nectria indusiata Seaver (= Calonectria P.W. Crous pers. comm.) [anamorph Cylindrocladium theae (Petch) Subram.] 126 Nectria ochroleuca (Schwein.) Berk. (anamorph Gliocladium roseum Bainier) Nectria radicola Gerlach & L.Nilsson [anamorph Cylindrocarpon destructans (Zinssm.) Scholten] Nothojafnea cryptotricha Rifai 82 Nummularia mediterranea (De Not.) Sacc. [this is Biscogniauxia mediterranea (De Not.) Kuntze] 251 Numulariola mediterranea (De Not.) P.M.D.Martin [this is Biscogniauxia mediterranea (De Not.) Kuntze] 251 Octaviania 83 Octaviania archeri Berk. [this is Hydnangium archeri (Berk.) Rodway] 79 Octaviania densa (Rodway) G.Cunn. (= Melanogaster; May & Wood 1997) 80, 88 Octavianina tasmanica (Kalchbr.) Pegler & T.W.K.Young 80 Oidium 136, 137, 191, 491 Oidium asteris-punicei Peck (teleomorph Erysiphe cichoracearum DC.) 136 Oidium eucalypti Rostr. 136, 191 Oidium leucoconium Desm. [teleomorph Sphaerotheca pannosa (Wallr.:Fr.) Lév.] 136 Oidium ruborum Rabenh. [teleomorph Sphaerotheca aphanis (Wallr.) U.Braun] Oidium violae Pass. emen. U.Braun (teleomorph Erysiphe orontii Castagne emen. U.Braun) Omphalotus nidiformis (Berk.) O.K.Mill. 312 Ophiodothella longispora H.J.Swart 176, 177, 178, 186, 213, 225 Osmoporus gunnii (Berk.) G.Cunn. [this is Hexagonia vesparius (Berk.) Ryvarden] 311 Oxyporus 434 Pachysacca 178, 229 Pachysacca eucalypti Syd. emen. H.J.Swart (anamorph Phomachora eucalypti Syd.) 162, 179 Pachysacca pusilla H.J.Swart 162, 179 Pachysacca samuelii (Hansf.) H.J.Swart 162, 179, 180, Plate 9.12 Paecilomyces 111 Paecilomyces lilacinus (Thom) Samson 507 Paecilomyces variotii Bainier 326 Panellus pusillus (Pers.:Lév.) Burds. & O.K.Mill. [this is Dictyopanus pusillus (Pers.:Lév.) Singer] 312 Passalora morrisii Crous 200, 208 Paxillus 80, 83, 85, 89 Paxillus infundibuliformis Cleland 80 Paxillus involutus (Batsch:Fr.) Fr. 80 Paxillus muelleri Berk. 80 Pellicularia salmonicolor (Berk. & Broome) Dastur [this is Erythricium salmonicolor (Berk. & Broome) Burds.] 245 Peltosoma eucalypti Hansf. (this is Stigmina eucalypticola B.Sutton & Pascoe) 189 Penicillium 103, 111, 114, 503

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Penicillium albicans Bainier 111 Penicillium arenicola Chalab. 111 Penicillium brevicompactum Dierckx 111 Penicillium chrysogenum Thom 111 Penicillium citrinum Thom 111 Penicillium decumbens Thom 111 Penicillium dodgei Pitt [teleomorph Eupenicillium brefeldianum (B.O.Dodge) Stolk & D.B.Scott] 111 Penicillium expansum Link 111 Penicillium glabrum (Wehmer) Westling 111 Penicillium kloeckeri Pitt [teleomorph Talaromyces wortmannii (Klöcker) C.R.Benj.] 111 Penicillium olsonii Bainier & Sartory 111 Penicillium purpurogenum Stoll 111 Penicillium spinulosum Thom 111 Penicillium variabile Sopp 111 Peniophora gigantea (Fr.:Fr.) Massee [this is Phanerochaete gigantea (Fr.:Fr.) S.S.Rattan, Abdullah & Ismail] 438, 465 Peniophora sacrata G.Cunn. [this is Dextrinocystidium sacratum (G.Cunn.) Sheng H.Wu] 302 Perenniporia medulla-panis (Jacq.:Fr.) Donk 312, 326 Perenniporia ochroleuca (Berk.) Ryvarden 317 Periconia 111 Pestalosphaeria 228 Pestalotia 111, 422 Pestalotiopsis 103, 112, 114, 248, 422 Pestalotiopsis disseminata (Thüm.) Steyaert 111, 114, 142, 201, 225 Pestalotiopsis funerea (Desm.) Steyaert 111 Pestalotiopsis mangiferae (Henn.) Steyaert 112 Pestalotiopsis neglecta (Thüm.) Steyaert 112 Pestalozziella circularis Cooke & Massee [this is Coma circularis (Cooke & Massee) Nag Raj & W.B.Kendr.] 176 Pezicula cinnamomea (DC.) Sacc. (anamorph Cryptosporiopsis quercina Petr.) 245 Pezicula eucalypti Korf & Iturr. 105, 106 Peziza whitei (Gilkey) Trappe 82 Pezizella oenotherae (Cooke & Ellis) Sacc. [this is Discohainesia oenotherae (Cooke & Ellis) Nannf.] 119, 132, 184, 225 Phacidium eucalypti G.W.Beaton & Weste (anamorph Ceuthospora innumera Massee) 183, 206 Phaeogyroporus portentosus (Berk. & Broome) McNabb [this is Phlebopus marginatus (J.Drumm.) Watling & N.M.Greg.] 80 Phaeolus albertinii (Lloyd) D.A.Reid [this is Inonotus albertinii (Lloyd) P.K.Buchanan & Ryvarden] 302 Phaeolus manihotis R.Heim [this is Pseudophaeolus baudonii (Pat.) Ryvarden] 300 Phaeolus schweinitzii (Fr.) Pat. 302 Phaeophleospora 119, 133, 176, 179, 195, 198, 229 Phaeophleospora delegatensis (R.F.Park & Keane) Crous 159, 171 Phaeophleospora destructans (M.J.Wingf. & Crous) Crous, F.A.Ferreira & B.Sutton 186, 198 Phaeophleospora epicoccoides (Cooke & Massee) Crous, F.A.Ferreira & B.Sutton (teleomorph Mycosphaerella suttoniae Crous & M.J.Wingf.; synanamorph Cercostigmina sp.) 64, 120, 133, 143, 161, 163, 175,

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186, 187, 195, 196, 197, 198, 215, 227, 229, 498, 506, 522, Plate 9.19 Phaeophleospora eucalypti (Cooke & Massee) Crous, F.A.Ferreira & B.Sutton 133, 171, 186, 195, 197, 198 Phaeophleospora lilianiae (J.Walker, B.Sutton & Pascoe) Crous, F.A.Ferreira & B.Sutton 187, 198 Phaeoramularia eucalyptorum Crous 200, 208 Phaeoseptoria 179, 195 Phaeoseptoria eucalypti Hansf. emen. J.Walker [this is Phaeophleospora epicoccoides (Cooke & Massee) Crous, F.A.Ferreira & B.Sutton] 133, 175, 195, 506, 522 Phaeoseptoria luzonensis Tak.Kobay. [this is Phaeophleospora epicoccoides (Cooke & Massee) Crous, F.A.Ferreira & B.Sutton] 133, 195 Phaeothyriolum eucalyptinum Syd. [this is Phaeothyriolum microthyrioides (G.Winter) H.J.Swart] 179 Phaeothyriolum microthyrioides (G.Winter) H.J.Swart 162, 176, 179, 181, 229, Plate 9.13 Phanerochaete filamentosa (Berk. & M.A.Curtis) Burds. 297, 465 Phanerochaete gigantea (Fr.:Fr.) S.S.Rattan, Abdullah & Ismail 438, 465 Phanerochaete salmonicolor (Berk. & Broome) Jülich [this is Erythricium salmonicolor (Berk. & Broome) Burds.] 245 Phellinus 307, 325 Phellinus badius (Berk.) G.Cunn. (this a valid species but has been included in Phellinus rimosus (Berk.) Pilát) 313 Phellinus conchatus (Pers.:Fr.) Quél. 321 Phellinus extensus (Lév.) Pat. 312 Phellinus ferruginosus (Schrad.:Fr.) Pat. 321 Phellinus gilvus (Schwein.) Pat. 312, 321 Phellinus igniarius (L.:Fr.) Quél. 321 Phellinus noxius (Corner) G.Cunn. 302, 312, 313, 321 Phellinus resinaceus Kotl. & Pouzar 321 Phellinus rimosus (Berk.) Pilát 52, 313, 317, 318, 321, 323 Phellinus robiniae (Murrill) A.Ames 321 Phellinus robustus (P.Karst.) Bourdot & Galzin 313, 318, 322, 323, 332, Plates 13.5, 13.11 Phellinus salicinus (Pers.) Quél. (this a valid species but has been included in Phellinus ferruginosus (Schrad.:Fr.) Pat.) 321 Phellinus setulosus (Lloyd) Imazeki (this a valid species but has been included in Phellinus wahlbergii (Fr.) D.A.Reid) 313, 314 Phellinus torulosus (Pers.) Bourdot & Galzin 322 Phellinus wahlbergii (Fr.) D.A.Reid 313, 314, 318, 323, Plate 13.2 Phellinus weirii (Murrill) Gilb. 434 Phellinus zealandicus (Cooke) Teng [this is Phellinus wahlbergii (Fr.) D.A.Reid] 313, 314 Phellodon melaleucus (Swartz:Fr.) P.Karst. 80 Phialophora 248 Phialophora bubakii (Laxa) Schol-Schwarz 326 Phlebopus marginatus (J.Drumm.) Watling & N.M.Greg. 80 Phloeosporella eucalypticola H.Y.Yip 201, 215

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Pholiota spectabilis (Fr.:Fr.) P.Kumm. [this is Gymnopilus spectabilis (Fr.:Fr.) A.H.Sm.] 310, 311 Phoma 112, 114 Phoma australis Cooke [this is Idiocercus australis (Cooke) H.J.Swart] 213 Phoma eucalyptica Sacc. 112 Phomachora eucalypti Syd. (teleomorph Pachysacca eucalypti Syd. emen. H.J.Swart) 162 Phomopsis 112, 228 Phomopsis eucalypti Zerova 143 Phyllachora eucalypti (Cooke & Massee) Theiss. & Syd. [this is Plectosphaera eucalypti (Cooke & Massee) H.J.Swart] 182 Phyllachora eucalypti (Speg.) Petr. [this is Clypeophysalospora latitans (Sacc.) H.J.Swart] 189 Phyllachora maculata Cooke [this is Plectosphaera eucalypti (Cooke & Massee) H.J.Swart] 182 Phylloporus 87 Phylloporus hyperion (Cooke & Massee) Singer 80 Phyllosticta 176, 182 Phyllosticta eucalypti Ellis & Everh. (this is Phyllosticta extensa Sacc. & P.Syd.) 182 Phyllosticta eucalypti Thüm. 182, 187 Phyllosticta eucalyptina Pat. [this is Macrophyllosticta eucalyptina (Pat.) Sousa da Câmara] 182, 187 Phyllosticta eucalyptorum Crous, M.J.Wingf., F.A.Ferreira & Alfenas (teleomorph Guignardia eucalyptorum Crous) 158, 182, 187, 227 Phyllosticta extensa Sacc. & P.Syd. 182, 187 Physalospora eucalypti (Rolland) Schrantz [this is Clypeophysalospora latitans (Sacc.) H.J.Swart] 189 Physalospora latitans Sacc. [this is Clypeophysalospora latitans (Sacc.) H.J.Swart] 141, 189 Physosporella eucalypti (Speg.) Höhn. [this is Clypeophysalospora latitans (Sacc.) H.J.Swart] 189 Phytophthora (Oomycota) 119, 121, 123, 134, 135, 259, 260, 261, 263, 264, 266, 267, 268, 270, 272, 274, 275, 276, 278, 279, 280, 283, 455, 489, 507, 508 Phytophthora boehmeriae Sawada (Oomycota) 260 Phytophthora cactorum (Lebert & E.Cohn) J.Schröt. (Oomycota) 135, 262, 268, 499, 508 Phytophthora cambivora (Petri) Buisman (Oomycota) 260, 268 Phytophthora cinnamomi Rands (Oomycota) 24, 26, 41, 47, 48, 61, 62, 65, 68, 77, 123, 134, 135, 157, 163, 242, 243, 245, 259, 260, 261, 262, 263, 264, 265, 266, 267, 268, 269, 270, 271, 272, 273, 274, 275, 276, 277, 278, 279, 280, 281, 282, 283, 284, 327, 400, 412, 427, 428, 429, 431, 432, 433, 437, 438, 439, 445, 446, 447, 449, 450, 451, 452, 453, 454, 455, 456, 458, 459, 460, 467, 469, 470, 477, 478, 479, 480, 481, 483, 484, 485, 490, 491, 492, 498, 499, 507, 508, 523, Plates 11.1, 11.2 Phytophthora citricola Sawada (Oomycota) 135, 260, 262, 266, 268, 275, 499, 508 Phytophthora cryptogea Pethybr. & Laff. (Oomycota) 123, 134, 135, 260, 261, 267, 268, 275, 490, 508 Phytophthora drechsleri Tucker (Oomycota) 135, 260, 262, 266, 268, 275, 508

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Phytophthora gonapodyides (H.E.Petersen) Buisman (Oomycota) 260 Phytophthora heveae A.W.Thomps. (Oomycota) 260 Phytophthora megasperma Drechsler (Oomycota) 135, 261, 268 Phytophthora megasperma Drechsler var. megasperma (Oomycota) 260 Phytophthora megasperma Drechsler var. sojae A.A.Hildebr. (Oomycota) 260, 268, 275 Phytophthora nicotianae Breda de Haan (Oomycota) 267 Phytophthora nicotianae Breda de Haan var. nicotianae (Oomycota) 135, 268, 508 Phytophthora nicotianae Breda de Haan var. parasitica (Dastur) G.M.Waterh. (Oomycota) 260, 261, 262, 268, 275 Phytophthora palmivora (E.J.Butler) E.J.Butler (Oomycota) 260 Piggotia substellata Cooke 51, 187, 206, 210, 466 Pilidium acerinum Kunze 210 Pilidium concavum (Desm.) Höhn. [teleomorph Pezizella oenotherae (Cooke & Ellis) Sacc.; synanamorph Hainesia lythri (Desm.) Höhn.] 132, 225 Piptoporus 325, 326, 327 Piptoporus australiensis (Wakef.) G.Cunn. 314, 318, 319, 322, 323, Plate 13.4 Piptoporus cretaceus (Lloyd) G.Cunn. [this is Ryvenardia cretacea (Lloyd) Rajchenb.] 316 Piptoporus maculatissimus (Lloyd) G.Cunn. 314 Piptoporus portentosus (Berk.) G.Cunn. 314, 315, 319, 322, 323, Plate 13.1 Pisolithus 77, 83, 86, 89 Pisolithus microcarpus (Cooke & Massee) G.Cunn. 80 Pisolithus tinctorius (Pers.) Coker & Couch 75, 76, 80, 84, 85, 91, 502 Pithomyces maydicus (Sacc.) M.B.Ellis 112 Placostroma inaequalis (Cooke) Theiss. & Syd. [this is Rehmiodothis inaequalis (Cooke) H.J.Swart] 189 Plectosphaera eucalypti (Cooke & Massee) H.J.Swart 177, 178, 182, 188, 189, 227 Plectosphaera eucalypti Theiss. 189 Pleospora infectoria Fuckel [this is Lewia infectoria (Fuckel) M.E.Barr & E.G.Simmons] 110 Pleurotus nidiformis (Berk.) Sacc. [this is Omphalotus nidiformis (Berk.) O.K.Mill.] 312 Plicaria alveolata (Rodway) Rifai 82 Polydesmia 106 Polydesmia fructicola Korf 105, 106 Polydesmia turbinata Raitv. & R.Galán 105, 106 Polyporus 326 Polyporus australiensis Wakef. [this is Piptoporus australiensis (Wakef.) G.Cunn.] 314 Polyporus baudonii Pat. [this is Pseudophaeolus baudonii (Pat.) Ryvarden] 300 Polyporus eucalyptorum Fr. [this is Piptoporus portentosus (Berk.) G.Cunn.] 314, 315 Polyporus lateritius Lloyd [this is Rigidoporus laetus (Cooke) P.K.Buchanan & Ryvarden] 316 Polyporus pelles Lloyd 315 Polyporus pelliculosus Berk. [this is Postia pelliculosa (Berk.) Rajchenb.] 315

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Polyporus portentosus Berk. [this is Piptoporus portentosus (Berk.) G.Cunn.] 314, 315 Polyporus rubidus Berk. [this is Fomitopsis feei (Fr.) Kreisel] 320 Polyporus schweinitzii Fr. 302 Polyporus sulphureus (Bull.:Fr.) Fr. [this is Laetiporus sulphureus (Bull.:Fr.) Murrill] 317 Polyporus tasmanicus Berk. [this is Australoporus tasmanicus (Berk.) P.K.Buchanan & Ryvarden] 317 Polyporus tumulosus Cooke & Massee 315 Polyschema clavulata (Cooke & Harkn.) M.B.Ellis 105, 106 Poria healeyi N.Walters [this is Hapalopilus mutans (Peck) Gilb. & Ryvarden] 311 Poria medulla-panis (Jacq.:Fr.) Bres. [this is Perenniporia medulla-panis (Jacq.:Fr.) Donk] 312 Poria merulina (Berk.) Cooke [this is Tyromyces merulinus (Berk.) G.Cunn.] 316 Poria mollusca (Pers.:Fr.) Cooke [this is Trechispora mollusca (Pers.:Fr.) Liberta] 316 Poria mutans (Peck) Peck [this is Hapalopilus mutans (Peck) Gilb. & Ryvarden] 311 Poria vincta (Berk.) Cooke [this is Junghuhnia vincta (Berk.) Hood & M.Dick] 302 Postia 325 Postia pelliculosa (Berk.) Rajchenb. 315, 319, 323, Plate 13.3 Preussia 112 Propolis emarginata (Cooke & Massee) Sherwood 175, 177, 226, Plate 9.29 Protoglossum violaceum (Massee & Rodway) T.W.May 80 Protoglossum viscidum (Massee & Rodway) T.W.May 80 Protostegia eucalypti Cooke & Massee [this is Aurantiosacculus eucalypti (Cooke & Massee) Dyko & B.Sutton] 211 Protubera 83, 91 Protubera canescens G.W.Beaton & Malajczuk 80 Pseudocercospora 166, 198, 200, 208 Pseudocercospora basiramifera Crous 166 Pseudocercospora basitruncata Crous 166 Pseudocercospora colombiensis Crous & M.J.Wingf. (teleomorph Mycosphaerella colombiensis Crous & M.J.Wingf.) 158, 164, 166 Pseudocercospora crystallina Crous & M.J.Wingf. (teleomorph Mycosphaerella crystallina Crous & M.J.Wingf.) 159, 164, 166 Pseudocercospora cubae Crous 166 Pseudocercospora deglupta Crous 166 Pseudocercospora denticulata Crous 166 Pseudocercospora epispermogoniana Crous & M.J.Wingf. (teleomorph Mycosphaerella sp. similar to Mycosphaerella marksii Carnegie & Keane) 166 Pseudocercospora eucalypti (Cooke & Massee) Y.L.Guo & X.J.Liu [this is Phaeophleospora eucalypti (Cooke & Massee) Crous, F.A.Ferreira & B.Sutton] 133, 197 Pseudocercospora eucalypti Goh & W.H.Hsieh (this is Pseudocercospora eucalyptorum Crous, M.J.Wingf., Marasas & B.Sutton) 198

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Pseudocercospora eucalyptorum Crous, M.J.Wingf., Marasas & B.Sutton 167, 198, 199, 200, 227, 522, Plate 9.20 Pseudocercospora gracilis Crous & Alfenas (teleomorph Mycosphaerella gracilis Crous & Alfenas) 159, 164, 167 Pseudocercospora heimii Crous (teleomorph Mycosphaerella heimii Crous) 160, 167, 172 Pseudocercospora heimioides Crous & M.J.Wingf. (teleomorph Mycosphaerella heimioides Crous & M.J.Wingf.) 160, 164, 167 Pseudocercospora irregulariramosa Crous & M.J.Wingf. (teleomorph Mycosphaerella irregulariramosa Crous & M.J.Wingf.) 160, 164, 167 Pseudocercospora irregularis Crous 167 Pseudocercospora natalensis Crous & T.A.Cout. 167, 200 Pseudocercospora paraguayensis (Tak.Kobay.) Crous 167, 207 Pseudocercospora robusta Crous & M.J.Wingf. 167 Pseudocercosporella endophytica Crous & H.Sm.ter (teleomorph Mycosphaerella endophytica Crous & H.Sm.ter) 159, 164 Pseudomonas solanacearum (Smith 1896) Smith 1914 [this is Ralstonia solanacearum (Smith 1896) Yabuuchi, Kosako, Yano, Hotta & Nishiuchi 1995] (Bacterium) 343, 431, 524 Pseudopeziza eucalypti Hansf. [this is Ascocoma eucalypti (Hansf.) H.J.Swart] 176 Pseudophaeolus 293, 300, 434 Pseudophaeolus baudonii (Pat.) Ryvarden 300, 301, 431, Plates 12.13, 12.14 Puccinia psidii G.Winter 27, 119, 137, 143, 154, 191, 192, 193, 227, 229, 427, 431, 432, 436, 440, 499, 509, 520, 523, 524, 526, 527, Plates 9.14–9.18 Pulcherricium caeruleum (Schrad.:Fr.) Parmasto 315 Pulvinaria typica Rodway [this is Waydora typica (Rodway) B.Sutton] 106 Pulvinula tetraspora (Hansf.) Rifai 82 Punctularia strigoso-zonata (Schwein.) P.H.B.Talbot 316 Pythium (Oomycota) 103, 112, 119, 121, 122, 123, 126, 134, 135, 260, 261, 262, 263, 264, 268, 270, 276, 278, 279, 490, 495, 504, 507, 508 Pythium acanthicum Drechsler (Oomycota) 260, 268 Pythium acanthophoron Sideris (Oomycota) 260, 268 Pythium afertile Kanouse & T.Humphrey (Oomycota) 135 Pythium anandrum Drechsler (Oomycota) 135, 499, 508 Pythium aphanidermatum (Edson) Fitzp. (Oomycota) 502 Pythium aquatile Höhnk (Oomycota) 135 Pythium debaryanum R.Hesse (Oomycota) 135, 268 Pythium deliense Meurs (Oomycota) 123, 260, 268 Pythium intermedium de Bary (Oomycota) 123, 260, 268 Pythium irregulare Buisman (Oomycota) 123, 135, 260, 268 Pythium mamillatum Meurs (Oomycota) 123, 260, 268 Pythium middletonii Sparrow (Oomycota) 260 Pythium myriotylum Drechsler (Oomycota) 123, 268 Pythium oedochilum Drechsler (Oomycota) 260 Pythium paroecandrum Drechsler (Oomycota) 123, 260, 268 Pythium perplexum H.Kouyeas & Theoh. (Oomycota) 123, 260, 268

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Pythium spinosum Sawada (Oomycota) 123, 135 Pythium splendens Hans Braun (Oomycota) 135, 260, 261, 268 Pythium ultimum Trow (Oomycota) 123, 135, 260, 268, 508 Pythium ultimum Trow var. sporangiferum Drechsler (Oomycota) 260 Pythium vexans de Bary (Oomycota) 268 Ralstonia solanacearum (Smith 1896) Yabuuchi, Kosako, Yano, Hotta & Nishiuchi 1995 (Bacterium) 339, 343, 344, 345, 348, 431, 436, 524, Plates 14.6–14.10 Ramaria 80, 85, 89 Ramaria formosa (Pers.:Fr.) Quél. 81 Ramaria ochraceo-salmonicolor (Cleland) Corner 81 Ramaria sinapicolor (Cleland) Corner 81 Ramularia 103, 104, 112 Ramularia pitereka J.Walker & Bertus [this is Sporothrix pitereka (J.Walker & Bertus) U.Braun & Crous] 137, 206, 208, 509 Readeriella mirabilis Syd. & P.Syd. 154, 187, 226, 227 Reddellomyces westraliensis (G.W.Beaton & Malajczuk) Trappe, Castellano & Malajczuk 82 Rehmiodothis 189 Rehmiodothis eucalypti (Cooke & Massee) H.J.Swart 177, 189 Rehmiodothis inaequalis (Cooke) H.J.Swart 177, 189 Rhizoctonia 121, 126, 504, 505 Rhizoctonia bataticola (Taubenh.) E.J.Butler [mycelial form of Macrophomina phaseolina (Tassi) Goid.] 133 Rhizoctonia solani J.G.Kühn [teleomorph Thanatephorus cucumeris (A.B.Frank) Donk] 119, 121, 122, 123, 131, 138, 139, 143, 490, 491, 493, 495, 500, 501, 504, 509, 510 Rhizomorpha subcorticicalis Pers. [teleomorph Armillaria mellea (Vahl: Fr.) P.Kumm.] Rhizopogon 492 Rhizopogon luteolus Fr. 84, 502 Rhizopogon roseolus (Corda) Th.Fr. 84 Rhizopus 112, 114 Rhizopus arrhizus A.Fisch. (this is Rhizopus oryzae Went & Prins. Geerl.) 112 Rhizopus oryzae Went & Prins. Geerl. 112 Rhizopus stolonifer (Ehrenb.:Fr.) Vuill. 112 Rigidoporus 434 Rigidoporus laetus (Cooke) P.K.Buchanan & Ryvarden 316, 323 Rigidoporus lineatus (Pers.) Ryvarden 302 Rigidoporus vinctus (Berk.) Ryvarden [this is Junghuhnia vincta (Berk.) Hood & M.Dick] 302 Rosellinia necatrix Prill. (anamorph Dematophora necatrix R.Hartig) 302 Rosellinia radiciperda Massee 302 Rozites 85 Rozites roseolilacina Bougher, Fuhrer & E.Horak 81 Rozites symeae Bougher, Fuhrer & E.Horak 81 Ruhlandiella berolinensis Henn. emen. Dissing & Korf 82 Russula 83, 86, 89 Russula clelandii O.K.Mill. & R.N.Hilton 81 Russula cyanoxantha (Schaeff.) Fr. 81 Russula delica (Paulet) Fr. 81

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Russula emetica (Schaeff.:Fr.) Gray 81 Russula flocktoniae Cleland & Cheel 81 Russula mariae Peck 81 Russula purpureoflava Cleland 81 Ryvardenia campyla (Berk.) Rajchenb. 316, 319 Ryvardenia cretacea (Lloyd) Rajchenb. 316 Sarcostroma 200, 203, 204 Sarcostroma brevilatum (H.J.Swart & D.A.Griffiths) Nag Raj 200, 201, 203 Schizoparme straminea Shear [anamorph Coniella castaneicola (Ellis & Everh.) B.Sutton] 183, 220 Schizoparme versoniana (Sacc. & Penz.) Nag Raj & Lowen [anamorph Coniella granati (Sacc.) Petr. & Syd.] Schizopora carneolutea (Rodway & Cleland) Kotl. & Pouzar [this is Schizopora flavipora (Cooke) Ryvarden] 319 Schizopora flavipora (Cooke) Ryvarden 319 Schizothyrium Desm. 181 Scleroderma 81, 83, 85, 86, 89 Scleroderma albidum Pat. & Trab. 81 Scleroderma areolatum Ehrenb. 81 Scleroderma aurantium Pers. (this is Scleroderma citrinum Pers.) 81, 91 Scleroderma bovista Fr. 81 Scleroderma cepa Pers. 72, 81, 85, 91 Scleroderma citrinum Pers. 81, 91 Scleroderma flavidum Ellis & Everh. 72, 81 Scleroderma geaster Fr. 81 Scleroderma laeve Lloyd 81 Scleroderma paradoxum G.W.Beaton 81 Scleroderma texense Berk. 81, 91 Scleroderma verrucosum (Bull.) Pers. 81, 85, 91 Sclerogone eucalypti Warcup 82 Sclerotinia fuckeliana (de Bary) Fuckel [this is Botryotinia fuckeliana (de Bary) Whetzel] 123, 207 Sclerotiopsis australasica Speg. [this is Pilidium concavum (Desm.) Höhn.] 225 Sclerotium rolfsii Sacc. [teleomorph Athelia rolfsii (Curzi) C.C.Tu & Kimbr.] 119, 139, 140, 509 Secotium 83, 85 Secotium tenuipes Setch. [this is Setchelliogaster tenuipes (Setch.) Pouzar] 81, 85 Seimatosporium 200, 203, 215 Seimatosporium brevilatum H.J.Swart & D.A.Griffiths [this is Sarcostroma brevilatum (H.J.Swart & D.A.Griffiths) Nag Raj] 201, 203 Seimatosporium cylindrosporum H.J.Swart [this is Vermisporium cylindrosporum (H.J.Swart) Nag Raj] 202, 203 Seimatosporium eucalypti (McAlpine) H.J.Swart [this is Vermisporium eucalypti (McAlpine) Nag Raj] 202, 203 Seimatosporium falcatum (B.Sutton) Shoemaker [this is Vermisporium falcatum (B.Sutton) Nag Raj] 154, 203 Seimatosporium fusisporum H.J.Swart & D.A.Griffiths [this is Sarcostroma brevilatum (H.J.Swart & D.A.Griffiths) Nag Raj] 201, 203 Seimatosporium lichenicola (Corda) Shoemaker & E.Müll. [teleomorph Discostroma corticola (Fuckel) Brockmann] 215

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Seimatosporium samuelii (Hansf.) J.Walker & H.J.Swart [this is Vermisporium samuelii (Hansf.) J.A.Simpson & Grgur.] 203 Seiridium 252 Seiridium eucalypti Nag Raj 252 Selenophoma eucalypti Crous, C.L.Lennox & B.Sutton 187, 215 Septoria normae Heather, nom. nud. [this is Phaeophleospora eucalypti (Cooke & Massee) Crous, F.A.Ferreira & B.Sutton] 133, 197 Septoria pulcherrima Gadgil & M.Dick [this is Phaeophleospora eucalypti (Cooke & Massee) Crous, F.A.Ferreira & B.Sutton] 133, 171, 197 Setchelliogaster 81, 83, 91 Setchelliogaster tenuipes (Setch.) Pouzar 81, 85 Setosphaeria rostrata K.J.Leonard [anamorph Exserohilum rostratum (Drechsler) K.J.Leonard & Suggs, emen. K.J.Leonard] 142 Seynesia microthyrioides (G.Winter) Theiss. [this is Phaeothyriolum microthyrioides (G.Winter) H.J.Swart] 179 Sonderhenia 176, 215 Sonderhenia eucalypticola (A.R.Davis) H.J.Swart & J.Walker (teleomorph Mycosphaerella walkeri R.F.Park & Keane) 162, 165, 187, 214, 215, 217, Plates 9.23, 9.24 Sonderhenia eucalyptorum (Hansf.) H.J.Swart & J.Walker (teleomorph Mycosphaerella swartii R.F.Park & Keane) 134, 162, 165, 187, 215, 216, 217, Plate 9.22 Sphaceloma sp. (teleomorph Elsinoë eucalypti Hansf.) 158, 176 Sphaerella cryptica Cooke [this is Mycosphaerella cryptica (Cooke) Hansf.] 168 Sphaerella molleriana Thüm. [this is Mycosphaerella molleriana (Thüm.) Lindau] 173 Sphaerella nubilosa Cooke [this is Mycosphaerella nubilosa (Cooke) Hansf.] 173 Sphaeria mediterranea De Not. [this is Biscogniauxia mediterranea (De Not.) Kuntze] 251 Sphaeropsis eucalypti Berk. & Broome [this is Dothiorella eucalypti (Berk. & Broome) Sacc.] 104 Sphaeropsis sapinea (Fr.) Dyko & B.Sutton 245 Sphaeropsis stictoides Earle [this is Harknessia uromycoides (Speg.) Speg.] 105 Sphaerosoma mucidum (Rodway) Hansf. (this is Ruhlandiella berolinensis Henn. emen. Dissing & Korf) 82 Sphaerosoma trispora McLennan & Cookson 82 Sphaerotheca alchemillae (Grev.) L.Junell [this is Sphaerotheca aphanis (Wallr.) U.Braun] 136, 137, 191 Sphaerotheca aphanis (Wallr.) U.Braun (anamorph Oidium ruborum Rabenh.) 136, 137, 191 Sphaerotheca fuliginea (Schltdl.:Fr.) Pollacci 136, 191 Sphaerotheca macularis (Wallr.:Fr.) Lind 136, 191 Sphaerotheca pannosa (Wallr.:Fr.) Lév. (anamorph Oidium leucoconium Desm.) 136, 137, 191 Spicaria 112 Spiroplasma citri Saglio, L’hospital, Laflèche, Dupont, Bové, Tully & Freundt 1973 (Bacterium) 342 Sporothrix 206

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Sporothrix eucalypti M.J.Wingf., Crous & W.J.Swart 206, 208 Sporothrix pitereka (J.Walker & Bertus) U.Braun & Crous 24, 104, 137, 138, 206, 208, 228, 229, 509 Sporothrix pusilla U.Braun & Crous 206, 209 Sporotrichum destructor Pittman nom. nud. 206 Stachybotrys 112 Stachybotrys atra Corda 112 Stagonospora 171 Stagonospora delegatensis R.F.Park & Keane [this is Phaeophleospora delegatensis (R.F.Park & Keane) Crous] 171 Stagonospora orbicularis Cooke [this is Vermisporium orbiculare (Cooke) H.J.Swart & M.A.Will.] 203, 204 Stagonospora pulcherrima (Gadgil & M.Dick) H.J.Swart [this is Phaeophleospora eucalypti (Cooke & Massee) Crous, F.A.Ferreira & B.Sutton] 133, 197 Staninwardia breviuscula B.Sutton 202, 217 Stemphylium 326 Stenella parkii Crous & Alfenas (teleomorph Mycosphaerella parkii Crous, M.J.Wingf., F.A.Ferreira & Alfenas) 161, 174 Stereum 307, 319, 325 Stereum hirsutum (Willd.:Fr.) Gray 309, 316, 319, 322, 330, 332 Stereum radiato-fissum Berk. & Broome [this is Xylobolus spectabilis (Klotzsch) Boidin] 316 Stictis emarginata Cooke & Massee [this is Propolis emarginata (Cooke & Massee) Sherwood] 226 Stigmina 189 Stigmina eucalypti Alcorn 189, 209 Stigmina eucalypticola B.Sutton & Pascoe 189, 209 Stigmina hansfordii B.Sutton & Pascoe 189, 209 Stigmina robbenensis Crous, C.L.Lennox & B.Sutton 191, 209 Stilbospora foliorum Cooke 202, 217, 218 Streptomyces (Actinomycete) 507 Suillus 492 Suillus granulatus (L.:Fr.) Roussel 84 Suillus luteus (L.:Fr.) Roussel 84 Syncephalastrum racemosum Cohn 112, 114 Talaromyces wortmannii (Klöcker) C.R.Benj. (anamorph Penicillium kloeckeri Pitt) Thamnostylum lucknowense (J.N.Rai, J.P.Tewari & Mukerji) Arx & H.P.Upadhyay 112 Thanatephorus 121 Thanatephorus cucumeris (A.B.Frank) Donk (mycelial state Rhizoctonia solani J.G.Kühn) 119, 121, 126, 138, 139, 143, 495, 500, 509 Thaxterogaster 81, 83 Thelephora terrestris Ehrh.:Fr. 84 Thyrinula eucalypti (Cooke & Massee) H.J.Swart [teleomorph Aulographina eucalypti (Cooke & Massee) Arx & E.Müll.] 156, 158 Thyrinula eucalyptina Petr. & Syd. [this is Thyrinula eucalypti (Cooke & Massee) H.J.Swart] 156 Thyriopsis sphaerospora Marasas 182 Torula 104, 112 Trabutia eucalypti Cooke & Massee [this is Plectosphaera eucalypti (Cooke & Massee) H.J.Swart] 182

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Tracylla aristata (Cooke) Tassi 227 Trametes cubensis (Mont.) Sacc. 322 Trametes feei (Fr.) Pat. [this is Fomitopsis feei (Fr.) Kreisel] 320 Trametes scabrosa (Pers.) G.Cunn. 322 Trechispora mollusca (Pers.:Fr.) Liberta 316 Trichoderma 297, 465, 466, 504 Trichoderma harzianum Rifai 503, 507 Trichoderma viride Pers. 113, 493, 503, 507 Tricholoma 83, 88 Tricholoma coarctatum (Cooke & Massee) Sacc. [this is Hebeloma coarctatum (Cooke & Massee) Pegler] 79 Tricholoma eucalyptorum A.Pearson 81 Tricholoma pessundatum (Fr.:Fr.) Quél. 81 Tricholoma saponaceum (Fr.) P.Kumm. 81 Tricholoma terreum (Schaeff.:Fr.) P.Kumm. 84 Tricholoma tigrinum (Schaeff.) P.Kumm. 81 Trichothecium roseum (Pers.) Link 113 Trimmatostroma 217 Trimmatostroma bifarium Gadgil & M.Dick 209, 217 Trimmatostroma excentricum B.Sutton & Ganap. 205, 209, 217 Tyromyces merulinus (Berk.) G.Cunn. 316 Tyromyces pelliculosus (Berk.) G.Cunn. [this is Postia pelliculosa (Berk.) Rajchenb.] 315 Tyromyces pulcherrimus (Rodway) G.Cunn. [this is Aurantioporus pulcherrimus (Rodway) P.K.Buchanan & Hood] 310 Ulocladium atrum Preuss 113 Uwebraunia 172 Uwebraunia ellipsoidea Crous & M.J.Wingf. (teleomorph Mycosphaerella ellipsoidea Crous & M.J.Wingf.) 159, 164 Uwebraunia juvenis Crous & M.J.Wingf. (teleomorph Mycosphaerella juvenis Crous & M.J.Wingf.) 160, 172 Uwebraunia lateralis Crous & M.J.Wingf. (teleomorph Mycosphaerella lateralis Crous & M.J.Wingf.) 160, 164 Valsa 251, 252 Valsa ceratosperma (Tode:Fr.) Maire (anamorph Cytospora eucalypticola Van der Westh.) 250, 251 Valsa eucalypti Cooke & Harkn. 251 Valsa eucalypticola J.K.Sharma, C.N.Mohanan & Florence 251 Vararia 319 Vermisporium 154, 200, 203, 204 Vermisporium acutum H.J.Swart & M.A.Will. 202, 204, 205

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Vermisporium biseptatum H.J.Swart & M.A.Will. 202, 204, 205 Vermisporium brevicentrum H.J.Swart & M.A.Will. 202, 204, 205 Vermisporium cylindrosporum (H.J.Swart) Nag Raj 202, 203, 204, 205 Vermisporium eucalypti (McAlpine) Nag Raj 202, 203, 205 Vermisporium falcatum (B.Sutton) Nag Raj 202, 203, 205, 206, 228 Vermisporium obtusum H.J.Swart & M.A.Will. 203, 204, 205, 206 Vermisporium orbiculare (Cooke) H.J.Swart & M.A.Will. 203, 204, 205 Vermisporium samuelii (Hansf.) J.A.Simpson & Grgur. 203, 204 Vermisporium verrucisporum Nag Raj 203 Vermisporium walkeri H.J.Swart & M.A.Will. 203, 204, 205 Verticillium 113, 114, 115, 122, 248, 496 Verticillium albo-atrum Reinke & Berthold 103, 113, 114 Waydora typica (Rodway) B.Sutton 105, 106 Wuestneia eucalyptorum Crous, M.J.Wingf. & Nag Raj (anamorph Harknessia eucalyptorum Crous, M.J.Wingf. & Nag Raj) Xanthomonas campestris (Pammel 1895) Dowson 1939 pv. eucalypti (Truman 1974) Dye 1978 (Bacterium) 343, 346 Xanthomonas eucalypti Truman 1974 [this is Xanthomonas campestris (Pammel 1895) Dowson 1939 pv. eucalypti (Truman 1974) Dye 1978] (Bacterium) 346 Xenogliocladiopsis eucalyptorum Crous & W.B.Kendr. (teleomorph Arnaudiella eucalyptorum Crous & W.B.Kendr.) 182 Xerocomus chrysenteron (Bull.) Quél. 81, 85 Xylaria 113 Xylobolus 319 Xylobolus spectabilis (Klotzsch) Boidin 316 Zelleromyces 83 Zelleromyces australiensis (Berk. & Broome) Pegler & T.W.K.Young 81 Zelleromyces daucinus G.W.Beaton, Pegler & T.W.K.Young 81 Zelleromyces malaiensis (Corner & Hawker) A.H.Sm. 81

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Plant Index Eucalypt (Angophora, Corymbia, Eucalyptus) Scientific Names Angophora Cav. 2, 11, 12, 14, 15, 17, 18, 19, 20, 24, 179, 206, 229, 355 Angophora costata (Gaertn.) Britten 24, 106, 138, 156, 222 Angophora floribunda (Sm.) Sweet 356, 462 Corymbia K.D.Hill & L.A.S.Johnson 2, 3, 11, 14, 15, 17, 18, 19, 20, 22, 24, 48, 50, 72, 83, 91, 103, 105, 123, 126, 127, 137, 138, 155, 192, 206, 243, 261, 262, 295, 299, 309, 341, 354, 355, 386, 389, 399, 456, 464 Corymbia bleeseri (Blakely) K.D.Hill & L.A.S.Johnson 49 Corymbia calophylla (Lindl.) K.D.Hill & L.A.S.Johnson 20, 21, 24, 57, 65, 91, 206, 262, 267, 279, 281, 282, 295, 296, 310, 312, 313, 315, 316, 319, 341, 398, 450, 451, 462 Corymbia calophylla (Lindl.) K.D.Hill & L.A.S.Johnson var. rosea Guilf. 462 Corymbia citriodora (Hook.) K.D.Hill & L.A.S.Johnson 1 5, 6, 107, 108, 109, 110, 111, 112, 113, 127, 128, 129, 130, 132, 134, 136, 137, 138, 141, 189, 191, 192, 212, 217, 223, 224, 246, 248, 249, 295, 298, 299, 300, 301, 302, 310, 311, 312, 320, 321, 322, 340, 341, 342, 343, 344, 345, 346, 347, 357, 389, 398, 437, 464, 509, 525 Corymbia confertiflora (F.Muell.) K.D.Hill & L.A.S.Johnson 12, 321 Corymbia dichromophloia (F.Muell.) K.D.Hill & L.A.S.Johnson 355 Corymbia disjuncta K.D.Hill & L.A.S.Johnson 18 Corymbia eximia (Schauer) K.D.Hill & L.A.S.Johnson 138, 187, 198, 206 1.

Corymbia ficifolia (F.Muell.) K.D.Hill & L.A.S.Johnson 20, 24, 134, 138, 180, 206, 295, 299, 341 Corymbia gummifera (Gaertn.) K.D.Hill & L.A.S.Johnson 50, 55, 295, 341, 355, Plate 14.2 Corymbia intermedia (R.T.Baker) K.D.Hill & L.A.S.Johnson 57, 318 Corymbia jacobsiana (Blakely) K.D.Hill & L.A.S.Johnson 49, 53 Corymbia latifolia (F.Muell.) K.D.Hill & L.A.S.Johnson 18 Corymbia maculata (Hook.) K.D.Hill & L.A.S.Johnson1 20, 24, 25, 65, 66, 67, 68, 130, 133, 138, 165, 195, 206, 223, 248, 267, 301, 310, 311, 312, 313, 318, 321, 325, 331, 340, 346, 348, 366, 388, 389, 390, 392, 393, 394, 397, 399, 437, 462, 464, 522 Corymbia novoguinensis (D.J.Carr & S.G.M.Carr) K.D.Hill & L.A.S.Johnson 18 Corymbia papuana (F.Muell.) K.D.Hill & L.A.S.Johnson 18, 19, 321, 355 Corymbia paracolpica K.D.Hill & L.A.S.Johnson 18 Corymbia porrecta (S.T.Blake) K.D.Hill & L.A.S.Johnson 49, 53, Plate 4.2 Corymbia ptychocarpa (F.Muell.) K.D.Hill & L.A.S.Johnson 312 Corymbia tessellaris (F.Muell.) K.D.Hill & L.A.S.Johnson 18, 130, 138, 302, 311, 341, 398 Corymbia torelliana (F.Muell.) K.D.Hill & L.A.S.Johnson 19, 104, 129, 130, 223, 225, 246, 250, 301, 316, 345, 391, 421, 525 Corymbia variegata (F.Muell.) K.D.Hill & L.A.S.Johnson 1 [see Corymbia citriodora (Hook.) K.D.Hill & L.A.S.Johnson] Corymbia xanthope (A.R.Bean & Brooker) K.D.Hill & L.A.S.Johnson 395 Eucalyptus L’Her. 2, 3, 11, 12, 14, 15, 17, 18, 19, 20, 42, 43, 48, 50, 72, 83, 91, 103, 104, 105, 106, 107, 108,

Spotted gums Chippendale (1988) [Chippendale, G.M. (1988) Eucalyptus, Angophora (Myrtaceae). Flora of Australia. Vol. 19 (Australian Government Publishing Service: Canberra.)] listed only three species in the Series Maculatae, that is, the spotted gums. These occurred in Queensland, New South Wales and north-east Victoria and were Eucalyptus citriodora Hook. (syn. E. variegata F.Muell.), E. maculata Hook. and E. henryi S.T.Blake. The distribution of E. citriodora was given as several disjunct areas in Queensland, one including the Atherton Tableland and another from Mackay to Maryborough and extending inland. A characteristic of the species was the strong lemon scent when the leaves are crushed; hence the name lemon-scented gum. Eucalyptus maculata (spotted gum) was listed as being widespread from south-east Queensland through coastal New South Wales and just into Victoria. Eucalyptus henryi (large-leaved spotted gum) was listed as occurring around Brisbane, Qld, and southwards to near Grafton, NSW. Hill and Johnson (1995) [Hill, K.D. and Johnson, L.A.S. (1995). Systematic studies in the eucalypts 7. A revision of the bloodwoods, genus Corymbia (Myrtaceae). Telopea 6, 185–504.] recognised four species of spotted gum which they placed into Section Politaria of the new genus Corymbia, with two interzonal intergrading populations. The four species that they recognised were C. citriodora (Hook.) K.D.Hill & L.A.S.Johnson (distributed in Queensland, with some disjunctions from south-west of Cooktown to south of Gladstone and west to the Great Dividing Range west of Springsure; they called this ‘lemon-scented gum’), C. variegata (F.Muell.) K.D.Hill & L.A.S.Johnson (this was described as being similar to C. citriodora and more or less intermediate between that species and C. maculata; with its distribution widely ranging, from the Carnarvon Range and north of Monto, Qld, contracting southward to subcoastal regions as far south as the Upper Nymboida River and north-west of Coffs Harbour, NSW), C. maculata (Hook.) K.D.Hill & L.A.S.Johnson (occurring in the coast division of New South Wales from the Manning River valley south to near Bega; also near Nowa Nowa, Vic., and at the head of the Goulburn River, NSW) and C. henryi (S.T.Blake) K.D.Hill & L.A.S.Johnson (Brisbane area, Qld, to south of Grafton, NSW). The Queensland Herbarium (BRI) considers that C. variegata is a synonym of C. citriodora with distribution in Queensland south to mid coastal New South Wales and that C. maculata is a southern species, occurring from mid New South Wales into Victoria. The name Corymbia henryi (syn. E. henryi) was not used at all in this book and the entries as C. citriodora (syn. E. citriodora) undoubtedly refer to the ‘lemon-scented’ form which is found naturally only in Queensland, from the north to about Gladstone. However, the name C. maculata (syn. E. maculata) as used in this book would include not only C. maculata in the strict sense (i.e. the species that occurs in New South Wales from the Manning River valley southwards and in Victoria) but also the non-scented spotted gum which occurs from mid New South Wales into southern Queensland (i.e.C. variegata or the non-scented form of C. citriodora depending on the taxonomic view that is followed). Thus, the actual identity of the spotted gum trees named in this book as C. maculata would have to be resolved by taxonomic study, or by referring to the locality of occurrence for naturally growing trees, or to the provenance of the seed used for planted trees either in Australia or in other countries. These trees could actually be C. citriodora (the non-scented form), C. maculata or C. variegata.

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109, 110, 111, 112, 113, 120, 123, 126, 127, 131, 134, 135, 136, 137, 138, 141, 142, 155, 156, 164, 166, 167, 174, 175, 181, 192, 194, 195, 197, 206, 217, 220, 243, 245, 250, 251, 261, 262, 268, 294, 295, 299, 300, 302, 308, 309, 317, 320, 321, 322, 341, 344, 346, 347, 348, 354, 355, 356, 357, 373, 386, 389, 400, 456, 463, 493, 502, 504, 507, 508, 510, 522, 527, Plates 9.14–9.18, 10.10, 14.9 Eucalyptus acmenoides Schauer 130, 360 Eucalyptus agglomerata Maiden 123, 154, 395 Eucalyptus alba Blume 18, 107, 108, 109, 111, 112, 127, 128, 130, 223, 250, 299, 321, 347, Plate 4.4 Eucalyptus alba Blume (‘Rio Claro hybrid’) 525 Eucalyptus albens Benth. 136, 137, 191, 356 Eucalyptus amplifolia Naudin 112, 314, 341, 462 Eucalyptus amygdalina Labill. 142, 264, 295, 316, 318, 319, 320 Eucalyptus andrewsii Maiden 347 Eucalyptus angulosa Schauer 112, 299 Eucalyptus aromaphloia L.D.Pryor & J.H.Willis 262 Eucalyptus bancroftii (Maiden) Maiden 324, 325, 326, 4691 Eucalyptus baxteri (Benth.) J.M.Black 53, 211, 227, 261, 314, 315, 316, 317, 387, 389, 391, 393, 462, Plates 9.21, 16.4 Eucalyptus behriana F.Muell. 53, 66, 202, 203 Eucalyptus bicostata Maiden, Blakely & Simmonds [this is Eucalyptus globulus Labill. ssp. bicostata (Maiden, Blakely & Simmonds) J.B.Kirkp.] 168 Eucalyptus blakelyi Maiden 106, 197, 314, 356, 359, 361, 362, 365, 366, 371, 372, 415, 419, Plates 10.3, 15.2, 15.4, 17.2 Eucalyptus blaxlandii Maiden & Cambage 315 Eucalyptus bleeseri Blakely [this is Corymbia bleeseri (Blakely) K.D.Hill & L.A.S.Johnson] Eucalyptus bosistoana F.Muell. 318, 319 Eucalyptus botryoides Sm. 50, 55, 123, 140, 165, 200, 249, 302, 314, 318, 319, 344, 389, 393, 397, 437, 462, 524 Eucalyptus botryoides Sm. x E. camaldulensis Dehnh. 140 Eucalyptus brachyandra F.Muell. 14 Eucalyptus brassiana S.T.Blake 18, Plate 16.17 Eucalyptus brevifolia F.Muell. 398 Eucalyptus bridgesiana R.T.Baker 24, 173, 311, 319, 356, 373 Eucalyptus caliginosa Blakely & McKie 356, 362 Eucalyptus calophylla Lindl. [this is Corymbia. calophylla (Lindl.) K.D.Hill & L.A.S.Johnson] Eucalyptus camaldulensis Dehnh. 4, 5, 13, 16, 19, 20, 23, 37, 49, 54, 55, 91, 104, 106, 107, 108, 109, 110, 111, 112, 113, 114, 124, 129, 131, 132, 133, 134, 142, 166, 173, 179, 195, 197, 199, 200, 202, 203, 206, 210, 219, 220, 221, 222, 223, 226, 246, 248, 250, 295, 298, 299, 310, 313, 314, 317, 318, 319, 320, 340, 344, 345, 346, 347, 357, 366, 373, 377, 389, 391, 393, 401, 419, 421, 422, 437, 462, 463, 464, 521, 522, 525, 527, Plates 4.5, 4.6, 9.10, 9.19, 9.20, 9.25, 9.26, 10.9, 14.4, 14.5, 19.3 Eucalyptus camaldulensis Dehnh. x E. grandis W.Hill 521 Eucalyptus camphora R.T.Baker 49, 180 Eucalyptus capitellata Sm. 226

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Eucalyptus cephalocarpa Blakely 180, 197 Eucalyptus cinerea Benth. 12, 135, 299, 314 Eucalyptus citriodora Hook.1 [this is Corymbia citriodora (Hook.) K.D.Hill & L.A.S.Johnson] Eucalyptus cladocalyx F.Muell. 123, 131, 164, 211, 219, 295, 398, 462 Eucalyptus cloeziana F.Muell. 5, 16, 130, 133, 137, 191, 192, 223, 321, 341, 345, 398, 501, 509, 523, 524, 525, 526, Plate 14.1 Eucalyptus cloeziana F.Muell. x E. acmenoides Schauer 22 Eucalyptus coccifera Hook.f. 112 Eucalyptus conferruminata D.J.Carr & S.G.M.Carr 462 Eucalyptus confertiflora F.Muell. [this is Corymbia confertiflora (F.Muell.) K.D.Hill & L.A.S.Johnson] Eucalyptus consideniana Maiden 261, 315, Plate 11.2 Eucalyptus cornuta Labill. 250 Eucalyptus crebra F.Muell. 104, 112, 136, 137, 138, 191, 299, 312, 313, 318, 347, 398, 462 Eucalyptus crebra F.Muell. x E. melanophloia F.Muell. 104, 112, 138 Eucalyptus crenulata Blakely & Beuzev. 191 Eucalyptus crucis Maiden 19 Eucalyptus curtisii Blakely & C.T.White 16 Eucalyptus cypellocarpa L.A.S.Johnson 21, 24, 173, 174, 179, 191, 197, 249, 295, 310, 311, 314, 318, 319, 389, Plates 12.3, 12.6 Eucalyptus dalrympleana Maiden 176, 180, 197, 299, 313, 314, 318, 356, 393, 435 Eucalyptus dealbata Schauer 313, 324, 325, 328, 356 Eucalyptus deanei Maiden 345 Eucalyptus deglupta Blume 4, 12, 14, 17, 18, 19, 107, 108, 109, 110, 111, 112, 122, 129, 130, 131, 138, 166, 220, 223, 246, 250, 302, 320, 321, 322, 329, 340, 341, 344, 345, 348, 413, 416, 490 Eucalyptus delegatensis R.T.Baker 16, 21, 25, 37, 49, 56, 57, 123, 154, 168, 169, 171, 176, 179, 181, 200, 214, 217, 219, 225, 245, 249, 252, 264, 294, 295, 298, 299, 302, 310, 313, 314, 316, 317, 319, 320, 326, 329, 395, 400, 413, 416, 435, 446, 461, 467, 468, 522, Plates 4.12, 9.9, 9.13, 12.12 Eucalyptus delegatensis R.T.Baker ssp. tasmaniensis Boland 113 Eucalyptus dendromorpha (Blakely) L.A.S.Johnson & Blaxell 168 Eucalyptus denticulata I.O.Cook & Ladiges 156, 466 Eucalyptus dichromophloia F.Muell. [this is Corymbia dichromophloia (F.Muell.) K.D.Hill & L.A.S.Johnson] Eucalyptus disjuncta K.D.Hill & L.A.S.Johnson [this is Corymbia disjuncta K.D.Hill & L.A.S.Johnson] Eucalyptus diversicolor F.Muell. 12, 16, 19, 20, 21, 37, 39, 41, 57, 90, 91, 133, 246, 262, 279, 295, 296, 298, 309, 311, 312, 314, 315, 316, 317, 319, 322, 332, 389, 391, 438, 464, 465, 468, Plates 4.13, 13.10, 19.1 Eucalyptus diversifolia Bonpl. 16, 179, 393, 462 Eucalyptus dives Schauer 50, 55, 72, 112, 179, 180, 215, 295, 315, 317, 373 Eucalyptus drepanophylla Benth. 65, 112, 130, 138, 295, 302, 311, 313, 318 Eucalyptus dumosa J.Oxley 76, 91, 318, Plate 13.5 Eucalyptus dunnii Maiden 174, 346, 521 Eucalyptus elata Dehnh. 174, 179, 315

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Eucalyptus erythrocorys F.Muell. 295 Eucalyptus eugenioides Spreng. 311, 343 Eucalyptus eximia Schauer [this is Corymbia eximia (Schauer) K.D.Hill & L.A.S.Johnson] Eucalyptus exserta F.Muell. 6, 130, 143, 345 Eucalyptus fasciculosa F.Muell. 212, 313, 347, 364, 462, 463 Eucalyptus fastigata H.Deane & Maiden 16, 76, 112, 133, 134, 156, 168, 180, 200, 298, 302, 314, 503, 521, 524 Eucalyptus fibrosa F.Muell. 398 Eucalyptus fibrosa F.Muell. ssp. ‘Q1’ 395 (unnamed subspecies) Eucalyptus ficifolia F.Muell. [this is Corymbia ficifolia (F.Muell.) K.D.Hill & L.A.S.Johnson] Eucalyptus foecunda Schauer 462 Eucalyptus forrestiana Diels 295 Eucalyptus fraxinoides H.Deane & Maiden 133, 156, 168, 302, 523 Eucalyptus fruticetorum Miq. (this is Eucalyptus odorata Behr) 301 Eucalyptus fruticosa Brooker 12 Eucalyptus globoidea Blakely 26, 55, 215, 251, 261, 310, 314, 315, 317, Plate 9.22 Eucalyptus globulus Labill. 3, 4, 6, 7, 14, 16, 21, 22, 24, 25, 26, 37, 38, 43, 63, 67, 68, 91, 104, 105, 106, 107, 108, 110, 111, 112, 123, 131, 133, 139, 140, 141, 142, 154, 155, 156, 159, 160, 164, 165, 167, 168, 169, 170, 171, 172, 173, 174, 175, 180, 181, 182, 187, 189, 191, 194, 195, 197, 200, 202, 203, 205, 206, 210, 212, 213, 215, 217, 219, 220, 225, 226, 227, 228, 246, 249, 250, 251, 252, 299, 301, 302, 318, 320, 322, 327, 329, 342, 343, 347, 357, 373, 388, 389, 391, 392, 393, 394, 395, 398, 400, 421, 422, 429, 433, 435, 436, 437, 438, 462, 466, 467, 507, 520, 521, 522, 523, 527, Plates 9.6, 9.8, 9.11, 9.23, 9.24, 9.29, 13.11, 16.1, 16.7, 16.8, 16.10, 16.20 Eucalyptus globulus Labill. ssp. bicostata (Maiden, Blakely & Simmonds) J.B.Kirkp. 64, 123, 140, 164, 165, 166, 168, 196, 197, 295, 296, 297, 299, 313, 318, 320, 340, 396, 465, Plates 12.1, 12.4 Eucalyptus globulus Labill. ssp. globulus 12, 13, 14, 64, 165, 313 Eucalyptus globulus Labill. ssp. maidenii (F.Muell.) J.B.Kirkp. 64, 107, 109, 110, 111, 112, 113, 123, 140, 142, 165, 168, 172, 299, 319, 322 Eucalyptus globulus Labill. ssp. pseudoglobulus (Maiden) J.B.Kirkp. 165, 173 Eucalyptus gomphocephala DC. 106, 131, 132, 262, 295, 299, 311, 315, 319, 389, 390, 391, 392, 398 Eucalyptus goniocalyx Miq. 178, 179, 182, 262, 314, 373, Plate 9.12 Eucalyptus gracilis F.Muell. 298, 299 Eucalyptus grandis W.Hill 4, 5, 6, 16, 24, 25, 37, 49, 57, 63, 64, 91, 106, 107, 108, 109, 110, 111, 112, 113, 114, 121, 122, 127, 129, 130, 131, 133, 137, 138, 139, 140, 141, 142, 143, 160, 164, 165, 166, 171, 172, 174, 175, 182, 183, 186, 187, 192, 195, 197, 198, 206, 210, 218, 219, 220, 221, 222, 223, 224, 226, 245, 246, 247, 248, 249, 250, 252, 261, 299, 301, 313, 315, 317, 319, 320, 321, 329, 330, 342, 343, 344, 345, 346, 347, 348, 388, 389, 391, 393, 394, 395, 402, 421, 422, 436, 467,

550

488, 504, 510, 521, 522, 525, 527, Plates 10.7, 10.8, 14.3, 16.2, 16.5, 16.15, 16.21, 16.23 Eucalyptus grandis W.Hill x E. camaldulensis Dehnh. 164, 166, 347 Eucalyptus grandis W.Hill x E. saligna Sm. 164, 166 Eucalyptus grandis W.Hill x E. urophylla S.T.Blake 133, Plates 9.27, 9.28 Eucalyptus guilfoylei Maiden 14, 57, 310, 311, 319 Eucalyptus gummifera (Gaertn.) Hochr. [this is Corymbia gummifera (Gaertn.) K.D.Hill & L.A.S.Johnson] Eucalyptus gunnii Hook.f. 24, 136, 168, 173, 197, 346, 347, 521 Eucalyptus haemastoma Sm. 346 Eucalyptus howittiana F.Muell. 14, 341 Eucalyptus hybrid 6, 107, 108, 109, 110, 111, 112, 113, 114, 115, 128, 129, 130, 134, 140, 141, 301, 342, 490, 506, 508 Eucalyptus incrassata Labill. 49, 462, 463 Eucalyptus intermedia R.T.Baker [this is Corymbia intermedia (R.T.Baker) K.D.Hill & L.A.S.Johnson] Eucalyptus jacksonii Maiden 57, 310, 311, Plate 4.13 Eucalyptus jacobsiana Blakely [this is Corymbia jacobsiana (Blakely) K.D.Hill & L.A.S.Johnson] Eucalyptus johnstonii Maiden 20, 168, 302 Eucalyptus kirtoniana F.Muell. (this is Eucalyptus robusta Sm. x E. tereticornis Sm.) 246 Eucalyptus kybeanensis Maiden & Cambage 112 Eucalyptus laevopinea R.T.Baker 109, 112, 346, 356, 364, 366 Eucalyptus largiflorens F.Muell. 54, 462 Eucalyptus latifolia F.Muell. [this is Corymbia latifolia (F.Muell.) K.D.Hill & L.A.S.Johnson] Eucalyptus lehmannii (Schauer) Benth. 134, 211 Eucalyptus leizhou No. 1 (a cultivated line of uncertain parentage) 6 Eucalyptus leptophleba F.Muell. 299 Eucalyptus leptophylla Miq. 462, 463 Eucalyptus leucoxylon F.Muell. 135, 182, 295, 299, 314, 366, 368, 462, 463 Eucalyptus macarthurii H.Deane & Maiden 133, 195, 224, 522, 524 Eucalyptus macrorhyncha Benth. 49, 55, 72, 261, 295, 311, 312, 314, 315, 317, 324, 325, 326, 340, 348, 373, 395, 399, 413, 415, Plate 4.8 Eucalyptus maculata Hook.1 [this is Corymbia maculata (Hook.) K.D.Hill & L.A.S.Johnson] Eucalyptus maidenii F.Muell. [this is Eucalyptus globulus Labill. ssp. maidenii (F.Muell.) J.B.Kirkp.] 142, 168 Eucalyptus major (Maiden) Blakely 347 Eucalyptus mannifera Mudie 250, 310, 314, Plate 10.1 Eucalyptus mannifera Mudie ssp. maculosa (R.T.Baker) L.A.S.Johnson 462 Eucalyptus marginata Sm. 21, 24, 26, 41, 55, 62, 65, 68, 88, 168, 169, 175, 184, 211, 219, 228, 242, 243, 245, 248, 251, 260, 261, 262, 263, 265, 266, 267, 268, 269, 270, 271, 272, 273, 274, 275, 276, 277, 278, 279, 280, 282, 283, 284, 295, 296, 310, 311, 312, 315, 325, 327, 328, 329, 331, 332, 389, 393, 398, 400, 429, 431, 433, 437, 445, 446, 450, 451, 452, 453, 454, 455, 456, 457, 458, 459, 462, 466, 467, 468, 469, 477, 478, 479, 480, 484, 485, 508, Plates 4.7, 11.1, 19.1, 19.2

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Eucalyptus megacarpa F.Muell. 295 Eucalyptus melanophloia F.Muell. 104, 112, 132, 138, 318 Eucalyptus melanophloia F.Muell. x E. crebra F.Muell. 104, 112 Eucalyptus melliodora Schauer 133, 182, 295, 318, 319, 356, 359, 360, 361, 362, 365, 366, 371, 372, 373, 395, 415, 419, 464 Eucalyptus microcarpa (Maiden) Maiden 66, 311, 314, 318, 366, 377, 462 Eucalyptus microcorys F.Muell. 14, 49, 65, 112, 130, 133, 137, 191, 192, 197, 211, 222, 223, 248, 301, 311, 315, 316, 325, 326, 347, 366, 398 Eucalyptus microtheca F.Muell. 19, 342, 343 Eucalyptus miniata Schauer 49 Eucalyptus moluccana Roxb. 136, 137, 174, 191, 311, 318 Eucalyptus morrisii R.T.Baker 200 Eucalyptus muelleriana A.W.Howitt 26, 319 Eucalyptus multiflora Poiret (this is Eucalyptus robusta Sm.) 300 Eucalyptus naudinia (incorrect spelling for Eucalyptus naudiniana F.Muell.) 131 Eucalyptus naudiniana F.Muell. (this is Eucalyptus deglupta Blume) 131 Eucalyptus nicholii Maiden & Blakely 130, 295, 310, 313 Eucalyptus nidularis (unknown taxon) 112 Eucalyptus nigra R.T.Baker 137, 223 Eucalyptus niphophila Maiden & Blakely [this is Eucalyptus pauciflora Spreng. ssp. niphophila (Maiden & Blakely) L.A.S.Johnson & Blaxell] 250 Eucalyptus nitens (H.Deane & Maiden) Maiden 3, 16, 22, 24, 25, 62, 64, 68, 105, 107, 109, 112, 114, 133, 136, 142, 154, 156, 160, 164, 165, 166, 167, 168, 172, 174, 179, 180, 181, 193, 194, 195, 197, 198, 199, 200, 202, 205, 206, 211, 212, 215, 219, 221, 227, 245, 249, 250, 251, 264, 295, 299, 302, 329, 346, 392, 394, 400, 421, 433, 436, 466, 491, 521, 522, 524, 526, 527, Plates 10.11, 16.11, 16.24 Eucalyptus nitida Hook.f. 395 Eucalyptus nova-anglica H.Deane & Maiden 112, 313, 356 Eucalyptus novoguinensis D.J.Carr & S.G.M.Carr [this is Corymbia novoguinensis (D.J.Carr & S.G.M.Carr) K.D.Hill & L.A.S.Johnson] Eucalyptus obliqua L’Her. 16, 19, 21, 26, 38, 49, 53, 55, 91, 114, 123, 134, 135, 154, 156, 168, 169, 170, 171, 172, 179, 180, 182, 189, 194, 206, 211, 214, 215, 227, 261, 262, 264, 270, 271, 274, 295, 296, 297, 302, 310, 311, 312, 313, 314, 315, 316, 317, 318, 319, 325, 326, 342, 347, 389, 391, 393, 395, 413, 414, 415, 460, 461, 462, 465, 466, 490, 508, Plates 4.8, 9.1, 9.3–9.5, 9.7, 12.7, 12.8, 12.10, 16.3 Eucalyptus obtusiflora DC. 347 Eucalyptus occidentalis Endl. 299, Plate 16.16 Eucalyptus ochrophloia F.Muell. 299 Eucalyptus odorata Behr 110, 179, 301, 311, 313, 462 Eucalyptus oleosa Miq. 49, 313 Eucalyptus oreades R.T.Baker 133, 174, 314 Eucalyptus orophila L.D.Pryor 18, 19

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Eucalyptus ovata Labill. 49, 168, 179, 197, 262, 295, 299, 302, 311, 313, 314, 315, 318, 373, 393, Plate 4.11 Eucalyptus paniculata Sm. 5, 132, 136, 191, 248, 299, 301, 417, 462, Plate 13.8 Eucalyptus papuana F.Muell. [this is Corymbia papuana (F.Muell.) K.D.Hill & L.A.S.Johnson] Eucalyptus parramattensis E.C.Hall 314 Eucalyptus patens Benth. 168, 295, 315, 389, 393, 466 Eucalyptus pauciflora Spreng. 20, 41, 49, 53, 72, 112, 123, 140, 141, 176, 179, 180, 181, 182, 225, 227, 310, 314, 319, 366, 393, 400, Plates 4.1, 4.11 Eucalyptus pauciflora Spreng. ssp. niphophila (Maiden & Blakely) L.A.S.Johnson & Blaxell 20, 250 Eucalyptus pellita F.Muell. 4, 19, 107, 108, 109, 110, 111, 112, 113, 114, 130, 137, 166, 191, 192, 219, 223, 344, 345, 388, 389, 393, 421, 525 Eucalyptus perriniana Rodway 12, 21, 136, 217 Eucalyptus phaeotricha Blakely & McKie (this is Eucalyptus nigra R.T.Baker) 137 Eucalyptus phoenicea F.Muell. 128 Eucalyptus pilligaensis Maiden 313 Eucalyptus pilularis Sm. 36, 37, 38, 43, 49, 57, 66, 67, 68, 75, 76, 91, 134, 137, 154, 191, 197, 222, 223, 295, 300, 301, 310, 312, 317, 321, 329, 389, 390, 392, 393, 398, 417, 430, 462, 521, Plates 16.6, 16.9, 16.12–16.14 Eucalyptus piperita Sm. 312 Eucalyptus platypus Hook. 462 Eucalyptus polyanthemos Schauer 66, 179, 203, 225, 298, 300, 314, 315, 318, 319, 365, 366, 373, 415 Eucalyptus populifolia Desf. (this is Eucalyptus tereticornis Sm.) 141 Eucalyptus populifolia Hook. (this is Eucalyptus populnea F.Muell.) 141 Eucalyptus populnea F.Muell. 104, 112, 141, 313, 318, 360 Eucalyptus populnea F.Muell. x E. crebra F.Muell. 104, 112 Eucalyptus porosa Miq. 462 Eucalyptus porrecta S.T.Blake [this is Corymbia porrecta (S.T.Blake) K.D.Hill & L.A.S.Johnson] Eucalyptus propinqua H.Deane & Maiden 130, 248, 295, 314, 319, 340, 522 Eucalyptus ptychocarpa F.Muell. [this is Corymbia ptychocarpa (F.Muell.) K.D.Hill & L.A.S.Johnson] Eucalyptus pulchella Desf. 302 Eucalyptus pulverulenta Sims 112, 298, 300 Eucalyptus punctata DC. 295, 301, 347, 421 Eucalyptus pyrocarpa L.A.S.Johnson & Blaxell 222, 524 Eucalyptus quadrangulata H.Deane & Maiden 173 Eucalyptus radiata DC. 49, 55, 114, 123, 215, 249, 261, 295, 312, 314, 317, 318, 319, 373, 413, 467 Eucalyptus radiata DC. ssp. robertsonii (Blakely) L.A.S.Johnson & Blaxell 112 Eucalyptus rameliana F.Muell. 19 Eucalyptus raveretiana F.Muell. 14, 129 Eucalyptus regnans F.Muell. 12, 16, 19, 20, 21, 23, 25, 26, 37, 38, 41, 49, 51, 56, 57, 58, 64, 91, 134, 140, 141, 154, 156, 168, 169, 170, 171, 178, 179, 182, 183, 187, 200, 203, 206, 210, 213, 214, 217, 219, 225, 226,

551

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245, 249, 262, 264, 294, 295, 297, 298, 302, 310, 311, 312, 313, 314, 315, 316, 317, 318, 319, 325, 326, 327, 328, 329, 330, 347, 389, 413, 414, 430, 438, 460, 461, 466, 467, 468, 469, 521, 522, 524, Plates 4.9, 4.10, 12.2, 12.10, 12.11, 17.1 Eucalyptus regnans F.Muell. x E. delegatensis R.T.Baker 25 Eucalyptus resinifera Sm. 65, 130, 223, 300, 311, 313, 318, 321, 345, 421 Eucalyptus risdonii Hook.f. 12, 13 Eucalyptus robusta Sm. 104, 106, 108, 109, 127, 132, 167, 223, 225, 248, 300, 302, 311, 314, 320, 342, 346, 347, 357 Eucalyptus robusta Sm. x E. tereticornis Sm. 246 Eucalyptus rodwayi R.T.Baker & H.G.Sm. 112 Eucalyptus rossii R.T.Baker & H.G.Sm. 399, 413, 415, Plate 10.5 Eucalyptus rostrata Schltdl. (this is Eucalyptus camaldulensis Dehnh.) 340 Eucalyptus rubida H.Deane & Maiden 180, 197, 295, 317 Eucalyptus rudis Endl. 19, 23, 106, 132, 295, 298, 300, 315, 342 Eucalyptus rugosa Blakely 462 Eucalyptus rupestris Brooker & Done 355 Eucalyptus saligna Sm. 16, 25, 65, 106, 109, 112, 127, 129, 130, 142, 164, 165, 167, 168, 192, 193, 195, 197, 200, 223, 224, 225, 246, 247, 248, 249, 298, 300, 302, 310, 311, 312, 313, 320, 321, 322, 329, 332, 340, 344, 345, 346, 347, 357, 389, 413, 417, 421, 462, 521, 522, 525 Eucalyptus salmonophloia F.Muell. 370 Eucalyptus sclerophylla (Blakely) L.A.S.Johnson & Blaxell 462 Eucalyptus serpentinicola L.A.S.Johnson & Blaxell 395 Eucalyptus shirleyi Maiden 355 Eucalyptus siderophloia Benth. 49 Eucalyptus sideroxylon Woolls 195, 262, 298, 300, 318, 319, 324, 325, 328, 347, 366, 373, 377, 469 Eucalyptus sideroxylon Woolls var. rosea Rehder (this is Eucalyptus sideroxylon Woolls) 298 Eucalyptus sieberi L.A.S.Johnson 24, 37, 55, 65, 66, 67, 68, 123, 135, 168, 170, 180, 217, 251, 262, 264, 266, 267, 270, 284, 312, 314, 315, 330, 389, 395, 433, 437, 438, 456, 457, 468, 508 Eucalyptus signata F.Muell. 223, 295 Eucalyptus smithii R.T.Baker 133, 314 Eucalyptus sphaerocarpa L.A.S.Johnson & Blaxell 130 Eucalyptus staeri (Maiden) Kessell & C.A.Gardner 311 Eucalyptus staigerana F.M.Bailey 301 Eucalyptus steedmanii C.A.Gardner 462 Eucalyptus stellulata DC. 49, 123, 140, 141 Eucalyptus stricta Spreng. 112 Eucalyptus subcrenulata Maiden & Blakely 20 Eucalyptus tasmanica Blakely (identity uncertain, either E. delegatensis R.T.Baker ssp. tasmaniensis Boland or E. tenuiramis Miq.) 112, 113 Eucalyptus tenuipes (Maiden & Blakely) Blakely & C.T.White 16, 341 Eucalyptus tenuiramis Miq. 113, 168 Eucalyptus tereticornis Sm. 6, 16, 18, 20, 23, 91, 106, 107, 108, 109, 110, 111, 112, 129, 130, 131, 132, 133,

552

134, 136, 137, 138, 139, 140, 141, 142, 143, 191, 197, 218, 221, 223, 224, 242, 246, 248, 250, 301, 312, 314, 317, 319, 322, 340, 342, 343, 345, 346, 366, 372, 389, 392, 393, 394, 462, 502, 504, 521, 522, 524, 525, 526 Eucalyptus tessellaris F.Muell. [this is Corymbia tessellaris (F.Muell.) K.D.Hill & L.A.S.Johnson] Eucalyptus tetragona (R. Br.) F.Muell. 341 Eucalyptus tetraptera Turcz. 194, 397 Eucalyptus tetrodonta F.Muell. 49, 54, 180, 263, Plate 4.3 Eucalyptus thozetiana R.T.Baker 318 Eucalyptus todtiana F.Muell. 462, Plate 19.4 Eucalyptus torelliana F.Muell. [this is Corymbia torelliana (F.Muell.) K.D.Hill & L.A.S.Johnson] Eucalyptus trabutii A.Vilm. ex Trab. (this is Eucalyptus botryoides Sm. x E. camaldulensis Dehnh.) 140, 344 Eucalyptus urnigera Hook.f. 22, 23, 397 Eucalyptus urophylla S.T.Blake 4, 6, 16, 18, 19, 25, 91, 137, 143, 164, 166, 167, 172, 191, 211, 219, 220, 221, 223, 225, 226, 248, 249, 309, 344, 388, 389, 391, 393, 436, 504, 521, 525, Plates 14.6, 14.7, 14.9, 14.10 Eucalyptus urophylla S.T.Blake hybrid 91 Eucalyptus urophylla S.T.Blake x E. grandis W.Hill ex Maiden 521 Eucalyptus variegata F.Muell.1 [this is Corymbia variegata (F.Muell.) K.D.Hill & L.A.S.Johnson but see Corymbia citriodora (Hook.) K.D.Hill & L.A.S.Johnson] Eucalyptus vernicosa Hook.f. 12, 20 Eucalyptus viminalis Labill. 12, 16, 49, 67, 104, 131, 140, 141, 142, 173, 175, 179, 180, 194, 197, 262, 295, 300, 311, 313, 314, 316, 317, 318, 319, 327, 356, 366, 389, 393, 400, 415, 521, 522, 524, Plates 4.11, 15.1 Eucalyptus viminalis Labill. ssp. viminalis 214 Eucalyptus wandoo Blakely 65, 262, 295, 296, 313, 318, 319, 366 Eucalyptus wetarensis L.D.Pryor 18, 19 Eucalyptus xanthope A.R.Bean & Brooker [this is Corymbia xanthope (A.R.Bean & Brooker) K.D.Hill & L.A.S.Johnson]

Eucalypt (Angophora, Corymbia, Eucalyptus) Common Names Please refer to the index of scientific names to obtain the corresponding page numbers. Albany blackbutt Eucalyptus staeri (Maiden) Kessell & C.A.Gardner Alpine ash Eucalyptus delegatensis R.T.Baker Ampupu Eucalyptus urophylla S.T.Blake Apple Eucalyptus bridgesiana R.T.Baker Apple Eucalyptus goniocalyx Miq. Apple box Eucalyptus bridgesiana R.T.Baker Apple gum Eucalyptus bridgesiana R.T.Baker Argyle apple Eucalyptus cinerea Benth. Bald Island marlock Eucalyptus conferruminata D.J.Carr & S.G.M.Carr Bancroft’s red gum Eucalyptus bancroftii (Maiden) Maiden Bangalay Eucalyptus botryoides Sm. Bimble box Eucalyptus populnea F.Muell.

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Black box Eucalyptus largiflorens F.Muell. Black gum Eucalyptus ovata Labill. Black ironbox Eucalyptus raveretiana F.Muell. Black peppermint Eucalyptus amygdalina Labill., Eucalyptus nova-anglica H.Deane & Maiden Black sallee Eucalyptus stellulata DC. Blackbutt Eucalyptus patens Benth., Eucalyptus pilularis Sm., Eucalyptus todtiana F.Muell. Blackbutt peppermint Eucalyptus smithii R.T.Baker Blackdown stringybark Eucalyptus sphaerocarpa L.A.S.Johnson & Blaxell Blakeley’s red gum Eucalyptus blakelyi Maiden Blaxland’s stringybark Eucalyptus blaxlandii Maiden & Cambage Blue gum Eucalyptus leucoxylon F.Muell., Eucalyptus saligna Sm., Eucalyptus tereticornis Sm. Blue Mountains ash Eucalyptus oreades R.T.Baker Blue Mountains mallee Eucalyptus stricta Spreng. Blue Mountains mallee ash Eucalyptus stricta Spreng. Blue peppermint Eucalyptus dives Schauer Blue-leaved stringybark Eucalyptus agglomerata Maiden Bosisto’s box Eucalyptus bosistoana F.Muell. Brittle gum Eucalyptus mannifera Mudie, Eucalyptus mannifera Mudie ssp. maculosa (R.T.Baker) L.A.S.Johnson Broad-leaved box Eucalyptus behriana F.Muell. Broad-leaved carbeen Corymbia confertiflora (F.Muell.) K.D.Hill & L.A.S.Johnson [syn. Eucalyptus confertiflora F.Muell.] Broad-leaved ironbark Eucalyptus fibrosa F.Muell. Broad-leaved peppermint Eucalyptus dives Schauer Broad-leaved red ironbark Eucalyptus fibrosa F.Muell. Broad-leaved ribbon gum Eucalyptus dalrympleana Maiden Broad-leaved sally Eucalyptus camphora R.T.Baker Broad-leaved stringybark Eucalyptus caliginosa Blakely & McKie Brown barrel Eucalyptus fastigata H.Deane & Maiden Brown stringybark Eucalyptus baxteri (Benth.) J.M.Black, Eucalyptus capitellata Sm. Budawang ash Eucalyptus dendromorpha (Blakely) L.A.S.Johnson & Blaxell Bull mallee Eucalyptus behriana F.Muell. Bullich Eucalyptus megacarpa F.Muell. Bundy Eucalyptus goniocalyx Miq. Bushy yate Eucalyptus lehmannii (Schauer) Benth. Buxton gum Eucalyptus crenulata Blakely & Beuzev. Cabbage gum Corymbia papuana (F.Muell.) K.D.Hill & L.A.S.Johnson [syn. Eucalyptus papuana F.Muell.], Eucalyptus amplifolia Naudin, Eucalyptus pauciflora Spreng. Cadaga (Cadaghi) Corymbia torelliana (F.Muell.) K.D.Hill & L.A.S.Johnson [syn. Eucalyptus torelliana F.Muell.] Camden woollybutt Eucalyptus macarthurii H.Deane & Maiden Candlebark Eucalyptus rubida H.Deane & Maiden, Eucalyptus rubida H.Deane & Maiden Cape York ghost gum Corymbia papuana (F.Muell.) K.D.Hill & L.A.S.Johnson [syn. Eucalyptus papuana F.Muell.]

I N D E X

Cape York red gum Eucalyptus brassiana S.T.Blake Carbeen Corymbia papuana (F.Muell.) K.D.Hill & L.A.S.Johnson [syn. Eucalyptus papuana F.Muell.], Corymbia tessellaris (F.Muell.) K.D.Hill & L.A.S.Johnson [syn. Eucalyptus tessellaris F.Muell.] Carbeen gum Corymbia confertiflora (F.Muell.) K.D.Hill & L.A.S.Johnson [syn. Eucalyptus confertiflora F.Muell.] Cider gum Eucalyptus gunnii Hook.f. Coast ash Eucalyptus sieberi L.A.S.Johnson Coast grey box Eucalyptus bosistoana F.Muell. Coastal dune mallee Eucalyptus foecunda Schauer Coastal white mallee Eucalyptus diversifolia Bonpl. Congoo mallee Eucalyptus dumosa J.Oxley Coolibah Eucalyptus microtheca F.Muell. Creswick apple-box Eucalyptus aromaphloia L.D.Pryor & J.H.Willis Cut-tail Eucalyptus fastigata H.Deane & Maiden Darwin stringybark Eucalyptus tetrodonta F.Muell. Darwin woollybutt Eucalyptus miniata Schauer Deane’s gum Eucalyptus deanei Maiden Desert gum Corymbia papuana (F.Muell.) K.D.Hill & L.A.S.Johnson [syn. Eucalyptus papuana F.Muell.] Dongara mallee Eucalyptus obtusiflora DC. Drooping red gum Eucalyptus parramattensis E.C.Hall Dunn’s white gum Eucalyptus dunnii Maiden Eurabbie Eucalyptus globulus Labill. ssp. bicostata (Maiden, Blakely & Simmonds) J.B.Kirkp. Flat-topped yate Eucalyptus occidentalis Endl. Flooded gum Eucalyptus grandis W.Hill, Eucalyptus rudis Endl. Forest red gum Eucalyptus tereticornis Sm. Fremantle mallee Eucalyptus foecunda Schauer Fuschia gum Eucalyptus forrestiana Diels Fuschia mallee Eucalyptus forrestiana Diels Ghost gum Corymbia papuana (F.Muell.) K.D.Hill & L.A.S.Johnson [syn. Eucalyptus papuana F.Muell.] Giant mallee Eucalyptus oleosa Miq. Giles’s mallee Eucalyptus rameliana F.Muell. Gippsland grey box Eucalyptus bosistoana F.Muell. Glen Geddes bloodwood Corymbia xanthope (A.R.Bean & Brooker) K.D.Hill & L.A.S.Johnson Glossy-leaved red mallee Eucalyptus oleosa Miq. Gnaingar Eucalyptus phoenicea F.Muell. Grey bloodwood Corymbia porrecta (S.T.Blake) K.D.Hill & L.A.S.Johnson Grey box Eucalyptus microcarpa (Maiden) Maiden, Eucalyptus moluccana Roxb. Grey gum Eucalyptus major (Maiden) Blakely, Eucalyptus propinqua H.Deane & Maiden, Eucalyptus punctata DC. Grey ironbark Eucalyptus paniculata Sm. Grey mallee Eucalyptus morrisii R.T.Baker Gully gum Eucalyptus smithii R.T.Baker Gully peppermint Eucalyptus smithii R.T.Baker Gum-topped bloodwood Corymbia dichromophloia (F.Muell.) K.D.Hill & L.A.S.Johnson [syn. Eucalyptus

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dichromophloia F.Muell.], Corymbia dichromophloia (F.Muell.) K.D.Hill & L.A.S.Johnson [syn. Eucalyptus dichromophloia F.Muell.] Gum-topped box Eucalyptus moluccana Roxb. Gum-topped peppermint Eucalyptus brassiana S.T.Blake Gum-topped stringybark Eucalyptus delegatensis R.T.Baker Gympie messmate Eucalyptus cloeziana F.Muell.

Mountain grey gum Eucalyptus cypellocarpa L.A.S.Johnson Mountain gum Eucalyptus cypellocarpa L.A.S.Johnson, Eucalyptus dalrympleana Maiden Mountain swamp gum Eucalyptus camphora R.T.Baker Mountain white gum Eucalyptus dalrympleana Maiden Mugga (Mugga ironbark) Eucalyptus sideroxylon Woolls Murray red gum Eucalyptus camaldulensis Dehnh.

Hard-leaved scribbly gum Eucalyptus sclerophylla (Blakely) L.A.S.Johnson & Blaxell Honey box Eucalyptus melliodora Schauer Howitt’s box Eucalyptus howittiana F.Muell.

Napunyah Eucalyptus thozetiana R.T.Baker Narrow-leaved black peppermint Eucalyptus nicholii Maiden & Blakely Narrow-leaved box Eucalyptus microcarpa (Maiden) Maiden, Eucalyptus pilligaensis Maiden Narrow-leaved grey box Eucalyptus pilligaensis Maiden Narrow-leaved ironbark Eucalyptus crebra F.Muell. Narrow-leaved peppermint Eucalyptus nicholii Maiden & Blakely, Eucalyptus pulchella Desf., Eucalyptus radiata DC., Eucalyptus radiata DC. ssp. robertsonii (Blakely) L.A.S.Johnson & Blaxell Narrow-leaved red ironbark Eucalyptus crebra F.Muell. Narrow-leaved red mallee Eucalyptus leptophylla Miq. Narrow-leaved white mahogany Eucalyptus tenuipes (Maiden & Blakely) Blakely & C.T.White New England blackbutt Eucalyptus andrewsii Maiden New England peppermint Eucalyptus nova-anglica H.Deane & Maiden New England stringybark Eucalyptus caliginosa Blakely & McKie Northern grey ironbark Eucalyptus siderophloia Benth. Northern white gum Eucalyptus brevifolia F.Muell.

Illyarrie Eucalyptus erythrocorys F.Muell. Inland grey box Eucalyptus microcarpa (Maiden) Maiden Ironbark Eucalyptus siderophloia Benth. Jacob’s bloodwood Corymbia jacobsiana (Blakely) K.D.Hill & L.A.S.Johnson [syn. Eucalyptus jacobsiana Blakely] Jarrah Eucalyptus marginata Sm. Kamarere (Kumurere) Eucalyptus deglupta Blume Karo Eucalyptus brassiana S.T.Blake Karri Eucalyptus diversicolor F.Muell. Kingscote mallee Eucalyptus rugosa Blakely Kybean mallee ash Eucalyptus kybeanensis Maiden & Cambage Large-fruited blackbutt Eucalyptus pyrocarpa L.A.S.Johnson & Blaxell Large-fruited red mahogany Eucalyptus pellita F.Muell. Lemon-scented gum Corymbia citriodora (Hook.) K.D.Hill & L.A.S.Johnson [syn. Eucalyptus citriodora Hook.] Lemon-scented ironbark Eucalyptus staigerana F.M.Bailey Lerp mallee Eucalyptus incrassata Labill. Long-leaved box Eucalyptus goniocalyx Miq. Maiden’s gum Eucalyptus globulus Labill. ssp. maidenii (F.Muell.) J.B.Kirkp. Mallee box Eucalyptus porosa Miq. Manna gum Eucalyptus viminalis Labill., Eucalyptus viminalis Labill. ssp. viminalis Marri Corymbia calophylla (Lindl.) K.D.Hill & L.A.S.Johnson [syn. Eucalyptus calophylla Lindl.] Mealy stringybark Eucalyptus cephalocarpa Blakely, Eucalyptus cinerea Benth. Messmate Eucalyptus obliqua L’Her. Messmate stringybark Eucalyptus obliqua L’Her. Mindanao gum Eucalyptus deglupta Blume Molloy red box Eucalyptus leptophleba F.Muell. Monkey gum Eucalyptus cypellocarpa L.A.S.Johnson Moort Eucalyptus platypus Hook. Moreton Bay ash Corymbia tessellaris (F.Muell.) K.D.Hill & L.A.S.Johnson [syn. Eucalyptus tessellaris F.Muell.] Mottled gum Eucalyptus mannifera Mudie Mountain ash Eucalyptus regnans F.Muell. Mountain blue gum Eucalyptus deanei Maiden

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Olive-barked box Eucalyptus goniocalyx Miq. Orange gum Eucalyptus bancroftii (Maiden) Maiden Paddy’s River box Eucalyptus macarthurii H.Deane & Maiden Paramatta red gum Eucalyptus parramattensis E.C.Hall Peppermint box Eucalyptus odorata Behr Pilliga box Eucalyptus pilligaensis Maiden Pink bloodwood Corymbia intermedia (R.T.Baker) K.D.Hill & L.A.S.Johnson [syn. Eucalyptus intermedia R.T.Baker] Pink gum Eucalyptus fasciculosa F.Muell. Plunkett mallee Eucalyptus curtisii Blakely & C.T.White Poplar box Eucalyptus populnea F.Muell. Port Jackson mallee Eucalyptus obtusiflora DC. Pricklybark Eucalyptus todtiana F.Muell. Queensland grey ironbark Eucalyptus drepanophylla Benth. Queensland peppermint Eucalyptus exserta F.Muell. Queensland white stringybark Eucalyptus nigra R.T.Baker Red bloodwood Corymbia gummifera (Gaertn.) K.D.Hill & L.A.S.Johnson [syn. Eucalyptus gummifera Gaertn.] Red box Eucalyptus polyanthemos Schauer Red gum Eucalyptus camaldulensis Dehnh. Red ironbark Eucalyptus fibrosa F.Muell., Eucalyptus sideroxylon Woolls Red irongum Eucalyptus tereticornis Sm.

P L A N T

Red mahogany Eucalyptus resinifera Sm. Red mallee Eucalyptus gracilis F.Muell., Eucalyptus oleosa Miq. Red messmate Eucalyptus resinifera Sm. Red stringybark Eucalyptus macrorhyncha Benth. Red tingle Eucalyptus jacksonii Maiden Red-flowering gum Corymbia ficifolia (F.Muell.) K.D.Hill & L.A.S.Johnson [syn. Eucalyptus ficifolia F.Muell.] Red-spotted gum Eucalyptus mannifera Mudie Ribbon gum Eucalyptus viminalis Labill., Eucalyptus viminalis Labill. ssp. viminalis Ridge-fruited mallee Eucalyptus angulosa Schauer, Eucalyptus incrassata Labill. Risdon peppermint Eucalyptus risdonii Hook.f. River peppermint Eucalyptus elata Dehnh. River red gum Eucalyptus camaldulensis Dehnh. River white gum Eucalyptus elata Dehnh. Rose gum Eucalyptus grandis W.Hill Rose-flowered bloodwood Corymbia calophylla (Lindl.) K.D.Hill & L.A.S.Johnson var. rosea Guilf. Rough-barked apple Angophora floribunda (Sm.) Sweet Round-leaved bloodwood Corymbia latifolia (F.Muell.) K.D.Hill & L.A.S.Johnson [syn. Eucalyptus latifolia F.Muell.] Round-leaved gum Eucalyptus deanei Maiden Salmon gum Eucalyptus salmonophloia F.Muell. Scarlet gum Eucalyptus phoenicea F.Muell. Scent bark (Scented bark) Eucalyptus aromaphloia L.D.Pryor & J.H.Willis Scribbly gum Eucalyptus haemastoma Sm., Eucalyptus rossii R.T.Baker & H.G.Sm., Eucalyptus sclerophylla (Blakely) L.A.S.Johnson & Blaxell, Eucalyptus signata F.Muell. Shining gum Eucalyptus denticulata I.O.Cook & Ladiges, Eucalyptus nitens (H.Deane & Maiden) Maiden Shirley’s silver-leaved ironbark Eucalyptus shirleyi Maiden Silver gum Eucalyptus crenulata Blakely & Beuzev. Silver mallee Eucalyptus crucis Maiden Silver peppermint Eucalyptus tenuiramis Miq. Silver stringybark Eucalyptus cephalocarpa Blakely Silver top Eucalyptus nitens (H.Deane & Maiden) Maiden Silver-leaved ironbark Eucalyptus melanophloia F.Muell., Eucalyptus shirleyi Maiden Silver-leaved mountain gum Eucalyptus pulverulenta Sims Silvertop ash Eucalyptus sieberi L.A.S.Johnson Silvertop stringybark Eucalyptus laevopinea R.T.Baker Small-fruited bloodwood Corymbia dichromophloia (F.Muell.) K.D.Hill & L.A.S.Johnson [syn. Eucalyptus dichromophloia F.Muell.] Small-fruited grey gum Eucalyptus propinqua H.Deane & Maiden Smithton peppermint Eucalyptus nitida Hook.f. Smooth-barked apple Angophora costata (Gaertn.) Britten Smooth-barked mountain ash Eucalyptus oreades R.T.Baker Smooth-stemmed bloodwood Corymbia bleeseri (Blakely) K.D.Hill & L.A.S.Johnson [syn. Eucalyptus bleeseri Blakely] Snap-and-rattle Eucalyptus gracilis F.Muell. Snappy gum Eucalyptus brevifolia F.Muell.

I N D E X

Snow gum Eucalyptus pauciflora Spreng., Eucalyptus pauciflora Spreng. ssp. niphophila (Maiden & Blakely) L.A.S.Johnson & Blaxell Soap mallee Eucalyptus diversifolia Bonpl. South Australian mallee box Eucalyptus porosa Miq. Southern blue gum Eucalyptus globulus Labill., Eucalyptus globulus Labill. ssp. bicostata (Maiden, Blakely & Simmonds) J.B.Kirkp., Eucalyptus globulus Labill. ssp. globulus Southern mahogany Eucalyptus botryoides Sm. Spinning gum Eucalyptus perriniana Rodway Spotted gum Corymbia maculata (Hook.) K.D.Hill & L.A.S.Johnson [syn. Eucalyptus maculata Hook.], Corymbia variegata (F.Muell.) K.D.Hill & L.A.S.Johnson Spotted iron gum Corymbia maculata (Hook.) K.D.Hill & L.A.S.Johnson [syn. Eucalyptus maculata Hook.] Spotted mountain grey gum Eucalyptus cypellocarpa L.A.S.Johnson Spring bloodwood Corymbia ptychocarpa (F.Muell.) K.D.Hill & L.A.S.Johnson [syn. Eucalyptus ptychocarpa F.Muell.] Square-fruited Mallee Eucalyptus tetraptera Turcz. Steedman’s gum Eucalyptus steedmanii C.A.Gardner Steedman’s mallet Eucalyptus steedmanii C.A.Gardner Stringy gum Eucalyptus regnans F.Muell. Stringy-barked bloodwood Corymbia jacobsiana (Blakely) K.D.Hill & L.A.S.Johnson [syn. Eucalyptus jacobsiana Blakely] Sugar gum Eucalyptus cladocalyx F.Muell. Swamp gum Eucalyptus ovata Labill., Eucalyptus regnans F.Muell. Swamp mahogany Eucalyptus robusta Sm. Swamp messmate Eucalyptus robusta Sm. Swamp peppermint Eucalyptus rodwayi R.T.Baker & H.G.Sm. Swamp yate Eucalyptus occidentalis Endl. Sydney blue gum Eucalyptus saligna Sm. Sydney peppermint Eucalyptus piperita Sm. Tallerack Eucalyptus tetragona (R. Br.) F.Muell. Tallow-wood Eucalyptus microcorys F.Muell. Tasmanan alpine yellow gum Eucalyptus subcrenulata Maiden & Blakely Tasmanan yellow gum Eucalyptus johnstonii Maiden Tasmanian blue gum Eucalyptus globulus Labill., Eucalyptus globulus Labill. ssp. globulus Tasmanian snow gum Eucalyptus coccifera Hook.f. Thin-leaved stringybark Eucalyptus eugenioides Spreng. Thozet’s box Eucalyptus thozetiana R.T.Baker Tropical red box Eucalyptus brachyandra F.Muell. Tuart Eucalyptus gomphocephala DC. Tumbledown gum (Tumbledown red gum) Eucalyptus dealbata Schauer Urn gum Eucalyptus urnigera Hook.f. Varnished gum (Varnished-leaved gum) Eucalyptus vernicosa Hook.f. Victorian blue gum Eucalyptus globulus Labill. ssp. bicostata (Maiden, Blakely & Simmonds) J.B.Kirkp.

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Victorian eurabbie Eucalyptus globulus Labill. ssp. pseudoglobulus (Maiden) J.B.Kirkp. Victorian silver gum Eucalyptus crenulata Blakely & Beuzev. Wandoo Eucalyptus wandoo Blakely Western coolibah Eucalyptus microtheca F.Muell. White ash Eucalyptus fraxinoides H.Deane & Maiden, Eucalyptus oreades R.T.Baker White box Eucalyptus albens Benth. White gum Eucalyptus alba Blume, Eucalyptus dalrympleana Maiden, Eucalyptus rubida H.Deane & Maiden, Eucalyptus viminalis Labill., Eucalyptus viminalis Labill. ssp. viminalis White ironbark Eucalyptus leucoxylon F.Muell. White mahogany Eucalyptus acmenoides Schauer White mallee Eucalyptus dumosa J.Oxley, Eucalyptus gracilis F.Muell. White mountain ash Eucalyptus fraxinoides H.Deane & Maiden White peppermint Eucalyptus pulchella Desf. White sally Eucalyptus pauciflora Spreng. White stringybark Eucalyptus eugenioides Spreng., Eucalyptus globoidea Blakely White-top Eucalyptus delegatensis R.T.Baker White-topped box Eucalyptus quadrangulata H.Deane & Maiden Yapunyah Eucalyptus ochrophloia F.Muell., Eucalyptus thozetiana R.T.Baker Yarri Eucalyptus patens Benth. Yate Eucalyptus cornuta Labill. Yellow bloodwood Corymbia eximia (Schauer) K.D.Hill & L.A.S.Johnson [syn. Eucalyptus eximia Schauer] Yellow box Eucalyptus melliodora Schauer Yellow gum Eucalyptus leucoxylon F.Muell. Yellow ironbark Eucalyptus melliodora Schauer Yellow ironbox Eucalyptus melliodora Schauer Yellow messmate Eucalyptus exserta F.Muell. Yellow stringybark Eucalyptus muelleriana A.W.Howitt Yellow tingle Eucalyptus guilfoylei Maiden Yertchuk Eucalyptus consideniana Maiden Yorrell Eucalyptus gracilis F.Muell.

Other Plants Acacia 18, 41, 48, 106, 355, 366, 372, 397, 455, 457, 464 Acacia acuminata Benth. 366 Acacia melanoxylon R.Br. 57, 367 Acacia papyrocarpa Benth. 357, 359, 367 Acacia pulchella R.Br. 41, 277 Acacia terminalis (Salisb.) J.F.Macbr. 366 Acacia verniciflua A.Cunn. 330 Acacia victoriae Benth. 366 Agonis 229 Agonis flexuosa (Willd.) Sweet 156, 222 Allocasuarina 48 Allocasuarina decussata (Benth.) L.A.S.Johnson 57 Allocasuarina pusilla (Macklin) L.A.S.Johnson 53 Amyema 355, 356, 358, 361, 372, 377 Amyema bifurcata (Benth.) Tiegh. 355

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Amyema bifurcata (Benth.) Tiegh. var. eburnea Barlow 355 Amyema biniflora Barlow 355 Amyema cambagei (Blakely) Danser 368 Amyema congener (Sieber ex Schult. & Schult.f.) Tiegh. 366 Amyema linophylla (Fenzl) Tiegh. 358 Amyema maidenii (Blakely) Barlow 364 Amyema miquelii (Miq.) Tiegh. 353, 354, 355, 356, 359, 360, 361, 362, 363, 364, 365, 366, 367, 368, 369, 370, 371, 372, 373, 374, Plates 15.2–15.4 Amyema pendula (Spreng.) Tiegh. 353, 354, 355, 356, 359, 361, 362, 363, 364, 365, 367, 368, 369, 372, 373, Plate 15.1 Amyema pendula (Spreng.) Tiegh. ssp. longifolia (Hook.) Barlow 360 Amyema pendula (Spreng.) Tiegh. ssp. pendula 365, 366 Amyema preissii (Miq.) Tiegh. 359, 361, 365, 366 Amyema pyriformis Barlow 355 Amyema quandang (Lindl.) Tiegh. 357, 358, 361, 363, 364, 366, 367 Amyema sanguinea (F.Muell.) Danser 355 Amylotheca dictyophleba (F.Muell.) Tiegh. 367 Arceuthobium 357 Arceuthobium americanum Nutt. ex Engelm. in A.Gray 358 Arillastrum 12, 14, 17 Atkinsonia ligustrina (Lindl.) F.Muell. 357 Azolla 55 Banksia 194, 377, 450, 454, 456 Banksia grandis Willd. 266, 276, 277, 278, 279, 450, 451, 454, 455 Barringtonia 355 Betula platyphylla Sukaczev 360 Brachychiton 48, 355, 372 Brachychiton populneus (Schott & Endl.) R.Br. 367 Callitris 48, 367, 397 Carica papaya L. 137 Cassytha 353, 354, 377 Cassytha ciliolata Nees 377 Cassytha filiformis L. 377 Cassytha melantha R.Br. 377 Casuarina 18, 344, 367, 377, 397 Casuarina glauca Spreng. 368 Casuarina obesa Miq. 358 Catharanthus roseus (L.) G.Don 342 Chenopodium amaranticolor (H.J.Coste & A.Reyn.) H.J.Coste & A.Reyn. 340 Codonocarpus 48 Dahlia 137 Decaisnina 357 Decaisnina petiolata (Barlow) Barlow ssp. angustata Barlow 354 Dendrophthoe 357 Dendrophthoe falcata (L.f.) Ettingsh. 357 Dendrophthoe glabrescens (Blakely) Barlow 355, 367 Dendrophthoe homoplastica (Blakely) Danser 355 Dendrophthoe nilgherrensis (Wright & Arn.) Tiegh. 357

P L A N T

Dendrophthoe odontocalyx (Benth.) Tiegh. 355 Dendrophthoe vitellina (F.Muell.) Tiegh. 355 Diplatia 355 Diplatia grandibractea (F.Muell.) Tiegh. 355 Dryandra sessilis (Knight) Domin 451 Exocarpos 353, 354, 375, 376, 377 Exocarpos aphyllus R.Br. 375, 377 Exocarpos bidwillii Hook.f. 375, 376 Exocarpos cupressiformis Labill. 375, 377 Exocarpos latifolius R.Br. 375 Exocarpos sparteus R.Br. 375 Exocarpos strictus R.Br. 375, 377 Exocarpos syrticolus (Miq.) Stauffer 375 Fragaria 137 Geijera parviflora Lindl. 367 Gmelina arborea Roxb. 344 Godetia amoena G.Don 341 Gossypium hirsutum L. 341 Grevillea 355 Henslowia 354 Hibbertia 377 Imperata cylindrica (L.) P.Beauv. 57 Korthalsella lindsayi (Oliv. ex Hook.f.) Engl. 358 Korthalsella rubra (Tiegh.) Endl. ssp. geijericola Barlow 367 Lambertia 194 Lemna 55 Leptospermum myrsinoides Schldtl. 53 Liquidambar formosana Hance 251 Lophostemon 48, 355 Lysiana 357 Lysiana exocarpi (Behr) Tiegh. 367, 371 Mangifera indica L. 245 Manihot esculenta Crantz (syn. Manihot utilissima Pohl) Manihot utilissima Pohl 524 Melaleuca 355, 397 Muellerina 355 Muellerina bidwillii (Benth.) Barlow 367 Muellerina eucalyptoides (DC.) Barlow 354, 355, 356, 360, 361, 362, 364, 367, 371 Nothofagus 85 Nothofagus cunninghamii (Hook.) Oerst. 416, 461, Plates 4.10, 4.12 Notothixos subaureus Oliv. 368 Nuytsia floribunda (Labill.) R.Br. 354, 357, 376

I N D E X

Olearia argophylla (Labill.) Benth. 57 Persoonia 450 Phacellaria 354 Phaseolus aureus Roxb. 341 Phaseolus vulgaris L. 340 Phoradendron juniperinum Engelm. ex Gray 358 Phoradendron macrophyllum (Engelm.) Cockerell 402 Pinus 2, 5, 43, 135, 245, 456, 491, 492 Pinus contorta Douglas ex Loud. 365 Pinus radiata D.Don 84, 85, 297, 298, 431, 436, 454, 465, 507 Poa hiemata Vickery 53 Pomaderris aspera A.Cunn. ex DC. 57 Prunus armeniaca L. 137 Psidium 191, 192 Psidium guajava L. 137, 191 Psittacanthus calyculatus (DC.) G.Don 356, 357 Punica granatum L. 137 Quercus 251, 331 Quercus alba L. 243 Quercus rubra L. 245 Quercus suber L. 251 Rosa 137 Rosa multiflora Thunb. ex Murray 137 Santalum album L. 343, 348 Scurrula cordifolia (Wall.) G.Don 371 Scurrula parasitica L. 357 Shorea robusta Gaertner.f. 251 Sorghum 54 Struthanthus polystachys (Ruiz & Pav.) Eichler 357 Syncarpia 48 Syzygium 195, 355 Syzygium aromaticum (L.) Merr. & L.M.Perry 25, 247 Syzygium cordatum Hochst. 182 Syzygium jambos (L.) Alston 192 Tapinanthus bangwensis (Engl. & K.Krause) Danser 358 Tapinanthus erianthus (Sprague) Danser 357 Tapinanthus oleifolius (J.C.Wendl.) Danser 358 Themeda triandra Forssk. 57 Tripodanthus acutifolius (Ruiz & Pav.) Tiegh. 357 Tristania 355 Vinca rosea L. [this is Catharanthus roseus (L.) G.Don] 342 Viscum loranthi Elmer 371 Vitis 507 Xanthorrhoea australis R.Br. 266, 450, 457

557

S U B J E C T

I N D E X

Subject Index Abiotic disease 120, 385, 412, 422, 487, 520 Adnataria 16, 19, 138, 206, 386, 399 Advance growth 39, 40, 42, 48, 55 Aerial photography 451, 452 Agrobacterium 50, 140, 343, 345, Air pollution 385, 396, 403 Alcoa of Australia 478 Allozymes 23 Algeria 105 Alternaria leaf spot 218 Anthracnose 114, 130, 143, 421, 505 Antibiotics 342 Appressoria 173, 181, 193 Aracruz Celulose S.A. 4, 525 Argentina 85, 105, 140, 193, 222, 249, 250, 301, 340 Armillaria Diseases of complex etiology 412, 413, 414, 415, 416, 460, 521 Longevity of trees 48 Management 432, 433, 438, 449, 452, 464, 465, 469 Physiology of disease 65 Resistance 437 Victoria 42 Ashy stem blight 506 Assessment of disease 228, 246 Aulographina leaf spot 56, 154, 155, 158, 176, 227, 228, 229, 428, 466, 522 Australian Capital Territory 54, 413, 414, 415, 418, 421 Avoidance of disease 488 Bacteria 326, 339, 343 Bacterial wilt 343, 431, 519, 524 Bark 50, 242, 526 Bauxite mining 477 Barron Road syndrome 522, 526 Bell miner dieback 413, 416 Biological control Armillaria root rot 297, 438, 465 Cryphonectria canker 527 Insect pests 522, 527 Mistletoe 370 Mycorrhizas 77, 506 Nursery diseases 491, 493, 503, 504, 507, 508 Phytophthora cinnamomi 455 Root rot 297, 438 Wood decay 326 Biotrophic parasitism 155, 163, 169, 176, 178, 179, 182, 195, 198, 215 Bisectaria 16, 19, 386, 399 Black straw rot 325 Blakella 14, 15, 22, 399 Blister diseases 178 Bolivia 105 Boron 387, 389, 390, 394, 395, 400, 402, 403 Botryodiplodia stem canker 248, 522 Botryosphaeria canker 241, 245, 248, 252, 419, 422, 467, 526 Botrytis 56, 120, 121, 123, 210, 219, 489, 491, 493, 496, 502, 506, 510

558

Branch shedding 12, 323, 330, 468 Brazil Abiotic disease 520 Aracruz Celulose S.A. 5 Bacterial diseases 339, 343, 344, 346, 348, 431, 436, 524 Canker diseases 246, 247, 248, 249, 250, 252 Cryphonectria canker 25, 27, 435, 519, 522, 524, 527 Cylindrocladium diseases 221, 222, 223, 224, 225, 436, 491, 525 Diseases of cuttings 132, 143 Eucalypt productivity 63 Foliar diseases 154, 156, 176, 182, 189, 194, 195, 200, 217, 219, 220, 226 Insect pests 415 Leaf litter 141 Mal do Rio Dôcé 421, 423, 436 Management of nursery diseases 488, 489, 491, 492, 493, 504, 505, 509, 510, 511 Mycorrhizas 85 Mycosphaerella leaf diseases 163, 173, 174 Nematodes 347 Nursery diseases 119, 121, 123, 127, 128, 133, 140, 142, 506 Nutrient disorders 394 Plantations 3 Powdery mildew 136 Resistance 130, 436, 519, 522 Rust 27, 137, 191, 192, 519, 523 Seed technology 115 Selection and breeding 1, 25, 436, 522, 524, 525 Smallholders 7 Wood decay 329, 330 Breeding for disease resistance 436, 439, 464, 467, 523, 524, 527 Cryphonectria canker 25, 436 Cylindrocladium leaf disease 223 Foliar diseases 24, 25 Root rot 301 Wood decay 329 Britain 105 Brown rot 325 Brown wood 332 Burma 220 Butt scars 48, 323 Butt rot 301 Cable thinning 468 Cadmium 395 Calcium 77, 387, 389, 392, 395, 403 California Armillaria sp. 298 Bacterial disease 346 Canker disease 251 Foliar diseases 182, 189, 193 Fungi on fruit capsules 105, 212 Fungi on wood 106 Insect pests 415 Leaf litter 215 Mycosphaerella sp. 173 Nursery diseases 131

S U B J E C T

Sudden death 422 Wood decay 302 Canada 220, 465 Canker 104, 105, 114, 155, 169, 206, 218, 219, 241, 413, 419, 421, 435, 440, 445, 465 Canker rot 332 Capsule infection 104, 206 Caribbean 191 Casuarinaceae 18, 372 Cercospora 198 Charcoal rot 506 Chemical defences 50 Chile 4, 85, 163, 168, 195, 212, 346, 520 China Bacterial diseases 343, 344, 345 Eucalypt plantings 4, 6 Foliar diseases 220, 225 Nursery diseases 121, 123, 139, 142 Nutritional disorders 391, 395 Plantation diseases 132, 225 Phanerogamic parasites 377 Phytoplasmas 342 Chlorine 387, 396, 491, 493, 494, 501, 505, 510 Clonal forestry 436 Clonal propagation 27, 429 Clonal selection 5, 522, 525, 527 Cobalt 387 Cohort senescence 413 Collar rot 120, 139 Colombia 174, 395, 422 Competition 37 Complex etiology 411, 421, 422, 432, 445, 460, 469, Coniella leaf blight 143, 220 Coniothyrium canker 249, 252, 521, 522, 525, 527 Conservation 3, 36, 42, 43, 284, 374, 430, 447, 449, 469 Copper 77, 387, 389, 390, 394, 395, 403, 495, 500 Costa Rica 130, 222, 223, 246 Crown gall 140, 343, 345 Cryphonectria canker Biological control 527 Drought stress 244, 252 Economic importance 247 Epidemiology 246 Exotic pathogen 27, 241 Management 248, 519, 522, 524, 525, 526, 527 Plantations 435 Quarantine 431, 523 Resistance 25, 245, 436, 467, 522, 524, 525, 526, 527 Sapwood invasion 243 Symptoms 246 Taxonomy 249 Cryptococcus 106 Cuba 220, 247 Cupressaceae 252 Cuttings 131, 139, 141, 143, 501, 510 Cylindrocladium diseases Biological control 491, 493, 504 Disease of cuttings 143 Foliar diseases 154, 207, 221, 229 Infection process 65

I N D E X

Management 396, 436, 496, 497, 503, 510, 519, 520, 524, 525 Nursery diseases 119, 120, 121, 122, 123, 124, 138 Plantations 4, 520, 525, 527 Quarantine 523 Resistance 436, 522, 524 Damping-off Causal fungi 119 Cylindrocladium spp. 127, 221, 224 Management 488, 490, 493, 495 Native forests 50, 56 Nursery diseases 120, 121, 488 Pythium spp. 121, 123, 260, 261, 262, 268 Rhizoctonia sp. 139 Seedborne fungi 114 Defence response 84 Defoliation 63, 64, 221, 223, 418, 419, 420, 421, 464, 467, 522, 525 Diagnosis 155, 386, 388, 402, 403, 412, 432, 445, 447, 449, 450, 480 Dieback Cause 42, 218 Complex etiology 412, 413, 414, 415, 420, 421, 422 Cylindrocladium spp. 128 Management 435, 439, 445, 446, 449, 469 Phytophthora cinnamomi 259 Salinity 396 Dieback Review Panel 460 Dilleniaceae 272 Disease risk 5, 26, 453, 458, 524 Diversity 42 Dodder-laurel 354, 377 Drought Damage 385, 398, 403 Diseases of complex etiology 411, 412, 413, 414, 418, 419, 446, 460, 463 Effect on mistletoe 368, 369 Effect on regeneration 52, 53, 56, 120, 121 Management 439, 460, 519, 520, 521 Predisposition to disease 154, 244, 252, 283, 284, 298, 465, 466, 467 Symptoms 266 Tolerance 43, 77, 394, 521 Dumaria 16, 19, 386, 399 Ecological sustainability 36, 40, 44, 429, 430, 439 Economic effect 246, 248, 308, 329, 348 Egypt 114 Elaphomycetales 83 Endemic disease 469 Electron microscopy 342, 343, 414 Endogonales 83 Endophyte 105, 182, 189, 194, 215, 219, 220, 225, 227, 245, 249, 250 Endothia canker 25, 241, 245, 247, 250, 251, 419, 526 England 72, 154, 245, 249, 250, 346 Epacridaceae 266, 272 Epicormic growth 48, 368, Epidemics 93, 229, 266, Epidemiology

559

S U B J E C T

I N D E X

Armillaria root rot 296, 450 Cylindrocladium spp. 129 Foliar diseases 154, 156, 165, 170, 173, 195, 197, 210, 219 Mycorrhizas 93 Phytophthora cinnamomi 272 Rhizoctonia sp. 139 Rust 192 Equador 85 Eradication 431, 453, Eremolepidaceae 354 Ethiopia 6 Etiology 412, 415, 421 Eucalypts Adaptation in native forests 40 Adaptation to the tropics 4, 18, 23 Breeding 23, 24, 120, 223 Competition 37 Distribution 1, 17, 18, 48, 49 Economic benefit for smallholders 6 Exploitation of native forest 2, 36 Genetic variation 11, 23 Growth habits 12, 36, 48, 50, 52, 52, 63, 64, 428, 525 Growth rates 37, 90 Growth increments 38, 62 Hybridisation 21 Juvenile foliage 12, 55, 64, 168, 172, 173, 435, 466, Morphology 12 Origin 2, 16 Phylogeny 14 Physiology- 61, 267, 386, Productivity 62, 63 Regeneration 36, 39, 48, 51, 53, 54, 55 Scale of planting 2, 3 Seed 50, 54, 55, 103 Uses 3, 5, 6 Water relations 66, 89, 244, 398 Eucalypt crown decline 413 Eudesmia 14, 15, 17, 20, 399 Exsertaria 16, 19, 399 Fergusoninidae 348 Fire 13, 36, 48, 50, 53, 55, 57, 323, 329, 368, 373, 434, 466, 468 Effect on forest health 40, 41, 58, 412, 454, 461, 465 Effects on seedling growth 36, 41, 56, 58 Slash-disposal burns 36, 39, 40, 43, 329, 331, 458 Fire scars 435, 468 Flooding 51, 54, 283, 385, 412 Florida 104, 106, 127, 219, 225, 247, 249, 250, 298, 347 Fluoride 397, 403 Foliar diseases 50, 153, 427, 431, 435, 440, 445, 465 Forest conservation 40 Forest structure 40 Frost 51, 52, 53, 56, 120, 121, 124, 250, 385, 394, 400, 403, 519, 520, 522 France 85, 298, 521 Fumigation 490, 492, 493, 494, 507, 509 Fungicides Canker diseases 246 Disease management 427, 438, 439, 440, 524, 526

560

Foliar diseases 171, 191, 193, 197, 222 Management of nursery diseases 487, 489, 491, 493, 494, 495, 496, 497, 498, 499, 500, 501, 502, 503, 504, 505, 506, 507, 508, 509, 510 Protection of seed 115 Phytotoxicity 396 Root-infecting pathogens 270, 456 Fusarium 109, 114, 115, 121, 123, 131, 143, 489, 490, 491, 496, 505 Galls 50, 347, 348, 401 Ganoderma root rot 301 Gaubaea 14, 15, 16, 17, 19 Genetic diversity 12, 23, 27, 42, 261, Genetic vulnerability 27, 252, 520, 527 Germany 85 Glomales 86 Greasy spot 189 Gully dieback 413, 415, 433, 460 Gummosis 421 Hail damage 120, 121 Hainesia blight 119, 132, 225, 228, 503, 506 Haiti 490 Haustorium 178, 358, 376, Hawaii 105, 106, 142, 156, 212, 247, 354, 490 Heart rot 307, 309, 310, 317, 323, 430, 469 Heat scorch 521 Heavy metals 395 Herbicides 396 Heritability of resistance 457, 525 High altitude dieback 413, 416, 446, 461 Hong Kong 247 Host specificity 20, 83, 129, 196, 197, 205, 206, 217, 228, 261, 355 Human pathogen 106 Humidity 401 Hybridisation 22 Hybrids 521, 522, 525, 527 Hygiene 457, 458, 459, 481, 482, 487, 489, 490, 492, 502, 519 Hypovirulence 527 Idiogenes 14, 15, 16, 17, 19, 22, 398 India Bacterial disease 346 Canker diseases 246, 247, 248, 249, 250 Capsule and flower infection 104, 106 Cylindrocladium diseases 122, 124, 126, 127, 129, 130, 222, 223, 224, 225, 503, 526 Dodder-laurel 377 Eucalypt plantings 4, 5, 6, 7, 521, 522 Foliar diseases 154, 189, 195, 219, 220, 226 Management of disease 488, 490, 496, 500, 503, 506, 509, 510, 526 Mistletoe 371 Mycorrhizas 72, 85 Nursery diseases 120, 121, 131, 133, 134, 138, 139, 142, 488, 490, 496, 500 Phylloplane fungi 140 Phytoplasmas 342, 348

S U B J E C T

Pink disease 246, 247, 524 Powdery mildew 136 Resistance 525 Root rot 301 Rust 191 Seedborne disease 114, 141 Virus 340 Inoculum potential 464 Indonesia 2, 19, 25, 114, 132, 163, 172, 174, 175, 195, 198, 200, 220, 246, 247, 261 Insects Canker diseases 248, 252 Damage caused by 228 Diseases of complex etiology 411, 412, 413, 414, 415, 416, 417, 418, 419, 420, 422, 423, 461, 464 Foliar diseases 155, 175, 226, 227, 466 Mistletoe 370 Nematodes 339, 348 Resistance to insects 23, 42, 522 Seed predation 50, 51, 55 Stem and butt rots 323, 434, 468 Insecticides 396 Integrated Pest Management 428 International conventions 439 Iran 173 Iron 77, 387, 389, 392, 395, 403 Israel 72 Italy 72, 85, 135, 140, 195, 199, 218, 342 Japan 122, 220, 246, 249, 250, 251 Jarrah dieback 260, 262, 270 Kenya 377 Kino 12, 133, 241, 243, 244, 249, 300, 301, 324, 386, 399, 421 Koch’s postulates 309, 343 Latent infections 245 Lauraceae 353, 354, 377 Lead 395 Leaf blight 124, 133, 134, 163, 219, 221, 222 Leaf litter 37, 41, 48, 50, 58, 77, 87, 88, 123, 141, 182, 189, 194, 210, 227, 272, 455 Leaf scab 176 Leaf shed 64 Legislation 438 Lerps 56 Light 402 Lignotuber 13, 37, 48, 50, 52, 53, 57, 58, 345, 368 Lime induced chlorosis 403 Little leaf disease 342 Loranthaceae 354, 361, 366 Lycaenidae 364 Lygaeid 50 Macrophomina disease 507 Madagascar 172, 300, 346 Malaysia 200, 261 Magnesium 77, 387, 389, 391, 395, 396, 403 Maidenaria 16, 19, 399 Mal do Rio Dôcé 421, 423, 436

I N D E X

Malawi 195, 197, 249 Management of disease 427, 445, 519 Armillaria root rot 297, 464 Bacterial wilt 344 Bauxite mines 477 Biological control 438, 527 Canker diseases 246, 248, 249, 252 Chemical control 438, 526 Diseases of complex etiology 460 Foliar and canker diseases 466 Native forests 445 Nurseries 487 Phytophthora cinnamomi 284, 449 Plantations 519 Resistance 24, 436, 524 Seed fungi 114 Silviculture 433, 523 Stem and butt rots 330, 332, 467 Manganese 387, 389, 392, 395, 403 Mapping disease 451, 459, 480 Mauritius 217 Mexico 356 Microclimate 435 Misodendraceae 354 Mistletoe 48, 324, 353, 402, 433, 437, 461, 464 Mites 402 Mixed species forests 40, 330 Molecular techniques 452 Molybdenum 387, 389, 394 Monocalyptus Adaptation 48, 398 Distribution 19, 20 Establishment 93 Frost tolerance 401 Hybrids 22 Morphology 50 Phylogeny 14, 15, 16, 17, 18 Resistance to disease 24, 42, 156, 168, 170, 197, 202, 203, 205, 217, 228, 229, 261, 262, 264, 266, 268, 279, 280, 282, 456 Response to infection 243 Salinity tolerance 395 Tolerance to alkaline conditions 393 Tolerance to waterlogging 283, 400 Morocco 4, 5, 391 Mount Toorong dieback 413 Mundulla Yellows 343, 447, 462, 463 Multiple use 36, 42, 44 Mycoplasma-like organisms 341 Mycorrhizas 37, 58, 71, 456, 492, 502 Mycosphaerella leaf diseases Association with insects 175 Chemical control 438, 498, 501 Effect on growth 62 Host specificity 229 Infection 65 Juvenile foliage 50, 64, 466, 525 Management 466, 467, 507, 511, 519, 521, 525, 526, 527 Nursery diseases 134, 498, 507, 511 Occurrence on cuttings 143

561

S U B J E C T

I N D E X

Pathogens and their occurrence 154, 158, 163, 431, 520, 521 Plantations 165, 435, 522 Quarantine 523 Resistance 12, 22, 24, 25, 26, 467, 522, 526, 527 Specialised pathogens 153, 227 Myrtaceae 12, 13, 16, 192, 272, 355 Mysore gum 6 Mysore hybrid 140, 301 Native cherries 354, 375 Nematodes 339, 346 Nepal 395 New Caledonia 16 New encounter diseases 25, 27, 154, 227, 348 New England dieback 417, 461 New South Wales Bacterial disease 346 Canker diseases 245, 246 Capsule fungi 106 Diseases of complex etiology 413, 414 Distribution of eucalypts 19 Eucalypt fossils 18 Foliar diseases 154, 156, 172, 197, 198, 206, 222, 225, 226, 228 Heart rot 329 Mistletoe 356, 360, 372, 377 Mundulla Yellows 462 Mycorrhizas 93 Nutrient disorders 395 Resistance 464, 526, 527 Rural dieback 47, 65, 418, 419, 461, 463 Silviculture 38, 39 Stem and butt rot 469 Woody root rot 302 New Zealand Armillaria root rot 298 Canker diseases 246, 249, 250 Chemical control 526 Eucalypt fossils 16, 18 Exocarpos sp. 375 Foliar diseases 154, 156, 176, 179, 180, 193, 195, 197, 200, 204, 211, 212, 214, 217, 219, 225, 226 Frost tolerance 521, 522 Mycorrhizas 84 Mycosphaerella spp. 154, 163, 165, 168, 169, 170, 171, 173, 229, 507, 519, 520 Nursery diseases 133, 134, 135, 136, 142, 191 Nutrient disorders 395 Powdery mildew 136, 191 Quarantine 431, 523 Resistance 25, 522 Wood decay 329, 330, 524 Woody root rot 302 Nickel 395 Nigeria 302, 395 Nitrogen 41, 77, 89, 283, 358, 369, 387, 389, 390, 395, 403, 419, 461, 493 Nitrogen fixation 41 Nitrogen oxides 398 Nutrients 41, 77, 89

562

Northern Territory 23, 128, 129, 223, 263, 490 Nursery diseases 115, 119, 206, 222, 225, 260, 393, 429, 439, 487, 525, 526 Nutrients 41, 385, 420, 488, 506 see also specific nutrients Nutritional disorders 385 Nutrient deficiency 84, 385 Obligate parasite 358, 371 Olethreutinae 364 Ozone 397, 403 Pakistan 131, 211, 347 Papilionaceae 266, 272 Papua New Guinea Armillaria sp. 294 Crown decline 413, 416 Distribution of eucalypts 2, 16, 18, 19, 20 Flower bud galls 348 Nutrient disorders 395 Phytophthora cinnamomi 261 Plantations 131 Saprophytic fungi 220 Seedling diseases 122, 129, 131 Root rot 302 Wood decay 329 Pathogenicity 206, 221, 222, 242, 250, 252, 267, 295, 346, 523 Pencilling 331 Peru 6, 85, 105 Petauridae 364 Pezizales 83 Phaeophleospora (Kirramyces) 64, 120, 133, 143, 171, 175, 176, 179, 195, 227, 229, 498, 506, 522 Phalageridae 364 Philippines 2, 6, 7, 122, 131, 246, 340, 341, 348, 391, 393, 395 Phosphorus 58, 76, 89, 283, 369, 387, 389, 390, 391, 395, 403, 461 Phosphonate 456, 469 Phylloplane 123, 131, 140, 141, 142, 218 Physical control methods 490, 505, 507 Phytophthora cinnamomi Bauxite mining 477 Biological control 455 Chemical treatments 456 Diagnosis 450 Effect of fire 41 Effect of mycorrhizas 77 Effect on forests 269, 433 Effect on trees 48, 62, 65, 68, 267, 429, 523 Epidemiology 272, 282, 450 Hazard and risk rating 453 Host range 261 Infection processes 242, 243, 264 Interaction with foliar diseases 157 Management 428, 432, 433, 438, 439, 445, 449, 490, 491, 498, 499, 507 Mapping 451 Native forests 259, 260, 412, 446 Nursery diseases 123, 134, 490, 491, 498, 499, 507

S U B J E C T

Origin 261 Plantations 519, 523 Quarantine 427, 431, 457 Resistance 24, 26, 280, 456 Waterlogging 400 Phytoplasmas 339, 341, 463 Phytotoxiciy 396, 505 Pieridae 364 Pink disease 245, 519, 521, 524, 525, 526, 527 Plantations Area 3 Australia 43, 93 Canker diseases 244, 245, 246, 248, 252 Diseases of complex etiology 413, 421, 422 Disease risk 26 Management of diseases 427, 429, 433, 435, 436, 438, 439, 440, 467, 519 Mycorrhizas 93 Nematodes 347 Occurrence of diseases 141, 154, 155, 173, 180, 192, 205, 206, 210, 213, 218, 228, 229, 348 Root diseases 298, 300, 302 Seed supplies 115 South Africa 195 Stem and butt rots 308, 329 Tropical 221, 222, 245, 246 Virus 340, 341 Yields 63 Platyceridae 364 Portugal 4, 5, 85, 104, 105, 163, 172, 173, 182, 189, 195, 215, 225, 252, 302 Potassium 77, 387, 389, 390, 391, 395, 403 Powdery mildew 135, 176, 191, 491, 499, 508 Predisposition to disease 129, 132, 197, 247, 252, 283, 412 Proteaceae 266, 272 Pruning 246, 251, 434, 523, 524, 526 Pseudocercospora 198, 522 Psyllids 55, 56, 447 Pythium 112, 121, 122, 123, 134, 259, 260, 264, 267, 268, 270, 280, 490, 495, 499, 507 Puerto Rico 247 Quantitative trait loci 27 Quarantine 191, 229, 431, 439, 457, 459, 489, 492, 519, 523 Queensland Bacterial diseases 344 Diseases of complex etiology 416, 447 Eucalypt fossils 18 Foliar diseases 156, 175, 195, 206, 211, 220, 223 Forest types 57 Management of disease 490, 492, 511 Management of forests 38 Mistletoe 364, 368, 372 Nematodes 347 Nursery diseases 133, 134, 135, 136 Nutrient disorders 395 Occurrence of diseases 104, 132 Resistance 23, 25

I N D E X

Rainforest 416 Ramularia (Sporothrix) 24, 104, 137, 228, 229, 509 Regeneration 13, 47, 451 Regrowth dieback 42, 413, 414, 433, 446, 460 Rehabilitation 457, 459, 479, 484 Resistance (susceptibility) to disease Armillaria root rot 296, 298, 437, 465 Bacterial diseases 345 Canker diseases 242, 244, 246, 249, 251, 252, 526 Changes with plant development 12 Cryphonectria canker 25, 247, 248, 435, 436, 467, 522, 524, 527 Cylindrocladium diseases 128, 129, 223, 224, 525, 527 Differences between subgenera 24, 156 Diseases of complex etiology 41, 421, 423 Foliar diseases 197, 206, 221 Genetic variation 24, 25, 26, 229, 524 Host specificity 229, 356 Hybrids 22 Insect pests 22, 42, 43, 55, 419, 522 Management of disease 421, 430, 436, 439, 445, 456, 464, 465, 467, 469, 519, 522, 524, 525, 526, 527 Mechanisms 64, 65, 122, 242, 280 Mistletoe 356, 374, 464 Mycosphaerella leaf diseases 24, 25, 64, 165, 168, 169, 171, 172, 173, 174, 435, 437, 526, 527 Natural forests 40, 41, 42 Nematodes 347 Phytophthora cinnamomi 26, 68, 262, 263, 264, 266, 272, 279, 280, 284, 437, 450, 453, 456, 467, 480, 484, 523, 526 Phytoplasmas 343 Powdery mildew 137, 191 Quantitative trait loci 27 Rural dieback 419, 437 Rust 137, 192 Seedling diseases 122, 123, 126, 132, 139, 140 Selection 436, 521 Stem and butt rots 325, 326, 327, 437, 469 Woody root rots 301, 302 Rhizoctonia 120, 121, 122, 123, 126, 133, 138, 143, 490, 491, 493, 495, 500, 501, 509, 510 Rhizoplane 57 Ribosomal DNA 136 Ring infections 17 Risk prediction 432, 453 Root rot 122, 127, 131, 134, 139, 140, 221, 264, 294, 434, 507 Rufaria 14, 20 Rural dieback 65, 412, 413, 417, 420, 429, 433, 446, 463 Rust Biotrophic parasite 176 Infection process 192 Management 427, 431, 432, 499, 509, 519, 520, 523, 524, 525, 526, 527 New encounter disease 27, 154, 191, 227, 229 Nursery disease 137, 143 Occurrence 191 Quarantine 229, 440 Rwanda 63

563

S U B J E C T

I N D E X

Salinity 272, 283, 284, 385, 395, 403, 413, 464, 491 Santalaceae 354 Santales 353 Sardinia 340 Scotland 72, 106 Secondary invader 172 Seed 50, 54, 55, 103, 467, 479, 502 Seed fungi 103, 106, 107, 142 Seed harvest by ants 55, 56 Seed infection 104, 227 Seed orchard 26, 27, 104, 429, 438 Seed trees 39, 42 Seedbed 36, 37, 39, 41, 43, 51, 488, 489 Seedlings Inhibition of growth in native forests 36, 57 Development of 50, 51 Seedling blight 488 Senegal 347 Silicon 387 Silviculture 35, 38, 42, 246, 329, 430, 433, 457, 469, 470, 519, 523 Clearfelling 39, 41, 92, 297, 433, 457, 465 Selection methods 38, 433, 464, 465 Shelterwood method 39 Sodium 387, 396 Soft rot 325 Soils 48 Soil fertility 419 Soil microflora 41, 51, 277 Soil mycoflora 71, 86 Soilborne disease 120, 133, 222, 259, 293, 343, 346, 489 Solarisation – 490, 506, 508 Solomon Islands 249, 250, 422 Sooty blotch 179 Sooty mould 195 South Africa Canker diseases 245, 246, 249, 250, 251 Cryphonectria canker 247, 248, 519, 522, 525, 527 Cylindrocladium diseases 127, 154, 222, 224 Foliar diseases 154, 156, 182, 189, 194, 200, 203, 206, 210, 211, 212, 213, 215, 219, 220, 225 Fungi of reproductive structures 105 Management of diseases 436, 488, 506, 525, 526, 527 Mycosphaerella leaf diseases 62, 64, 154, 163, 165, 172, 229, 431, 435, 519, 522, 526, 527 Nematodes 347 Nursery diseases 131, 132, 133, 134, 141, 142, 488, 503, 506 Occurrence of eucalypts 3, 4 Phaeophleospora spp. 195, 196, 197, 198 Phytophthora cinnamomi 134, 260, 261, 523 Plantations 520, 521 Resistance 436, 526, 527 Rust 193 Seed infections 115 Tree breeding 5 Woody root rots 300, 302 South Australia Capsule infections 106 Foliar diseases 176, 179, 189 Management of diseases 449, 450, 452, 459

564

Mistletoe 357, 361, 364, 368, 371, 372, 373 Mundulla Yellows 343, 462, 463 Nematodes 347 Phytophthora cinnamomi 263, 449, 450, 452, 459 Southern regrowth dieback 42 Spain 4, 5, 6, 104, 106, 154, 173, 193, 219, 302 Species mixtures 20, 55, 57 Sphaerulariidae 348 Stem and butt rot 37, 48, 52, 307, 434, 435, 437, 439, 445, 446, 449, 467, 523, 524 Stem canker 62, 126, 127, 128, 522, 524, 525, 526, 527 Stomata 64, 65 Storage fungi 103, 114 Succession 41, 413, 416, 446 Sudan 342 Sudden death 422 Sulphur 77, 387, 389, 390, 403 Sulphur dioxide 397, 403 Sun scald 120 Surinam 247 Surveillance 432 Survey 452 Symphyomyrtus Adaptation 48, 398 Distribution 19, 20 Frost tolerance 401 Growth rate 43 Morphology 50, 386 Phylogeny 14, 15, 16, 17, 18 Resistance to disease 24, 156, 168, 170, 173, 196, 197, 202, 205, 206, 217, 228, 261, 264, 279, 280, 282, 415, 456, 523 Response to infection 243 Salinity tolerance 395 Tolerance to alkaline conditions 393 Tolerance to waterlogging 283, 400 Taiwan 137, 191, 195, 261, 342 Tanzania 131, 377 Tasmania Armillaria root rot 296, 297, 464 Canker diseases 251, 252 Diseases of complex etiology 416, 421, 433, 446, 460, 461, 463 Distribution of eucalypts 12, 19, 20, 21, 23 Dodder-laurel 377 Drought 433 Effects of fire 48, 56 Foliar diseases 180, 194, 197, 199, 205, 210, 211, 213, 215, 227, 466 Frost tolerance 521 Heart rot 309 Leaf litter 106, 210 Management of diseases 449, 459, 465, 520, 523, 526 Management of nursery diseases 503 Mycorrhizas 85 Mycosphaerella leaf diseases 154, 168, 171, 522 Nursery diseases 135 Nutrient disorders 394, 395 Phytophthora cinnamomi 263, 264, 268, 450, 452 Powdery mildew 136

S U B J E C T

Regrowth dieback 342, 412, 413, 414 Resistance 22 Root rot 221 Rural dieback 417 Seedling diseases 37 Silviculture 39, 40 Variation in eucalypts 23, 386 Wood decay 469, 524 Telocalyptus 14, 15, 17 Tephritidae 364 Termites 54, 430, 435 Thailand 4, 114, 142, 206, 220, 247 Tissue culture 439 Toxicities 395 Transversaria 16, 19, 399 Tree surgery 371 Trinidad 247 Tunisia 182, 298 Tylenchida 348 Uganda 422 United Kingdom 85, 220, 226 United States of America 85, 105, 154, 193, 220, 298, 308, 374, 465, 505 Upper Volta 395 Uruguay 172, 189, 194, 215, 220 Venezuela 247 Vesicular-arbuscular mycorrhizas 74, 86, 87 Victoria Adaptation of eucalypts 23 Armillaria root rot 42, 295, 296, 297, 298, 464 Diseases of complex etiology 413, 447 Distribution of eucalypts 12, 19, 20 Dodder-laurel 354, 377 Drought 416 Effects of fire 48, 53, 56 Foliar diseases 104, 154, 155, 156, 179, 189, 194, 195, 204, 210, 211, 212, 215, 226, 227 Fossil eucalypts 18 Hybrids 22 Management of diseases 437, 449, 453, 455, 457, 458, 465, 467, 470, 526, 527 Mistletoe 361, 364, 367, 368, 372 Mycosphaerella leaf diseases 154, 165, 168, 171, 172, 173, 174, 175 Nematodes 347 Nursery diseases 135 Nutrient disorders 393 Phytophthora cinnamomi 134, 135, 263, 264, 266, 277, 428, 450, 452, 467 Regeneration of forests 52, 55, 56 Resistance 25 Silviculture 39, 40 Variation in eucalypts 23 Winter leaf spot 206, 466

I N D E X

Vietnam Canker diseases 246, 248, 250 Cylindrocladium leaf diseases 154, 222, 223, 522, 525, 527 Eucalypt plantings 4, 6 Foliar diseases 156, 195, 199, 211, 220, 221, 226 Management of diseases 525, 527 Mycosphaerella leaf diseases 163, 172, 173 Viminales 173 Virus 339, 340, 463 Viscaceae 354, 358, 366 Vulnerability to disease 429, 452 Wallace’s line 17 Water stress 398 Water treatment 491 Waterlogging 400, 403, 413 Web blight 121, 138, 143, 488, 500 Western Australia Armillaria root rot 295, 297, 298, 438 Bauxite mining 477, 478 Canker diseases 24, 219, 249, 251, 467 Cryphonectria canker 248 Distribution of eucalypts 18, 19, 23 Drought 400 Foliar diseases 206, 211, 466 Management of diseases 427, 438, 449, 453, 454, 456, 457, 458, 459, 460, 465, 469 Mistletoe 368, 370, 372 Mundulla Yellows 462 Mycosphaerella leaf diseases 163, 169, 172, 174 Nursery diseases 134, 503 Nutrient disorders 391, 392, 394, 395 Phytophthora cinnamomi 262, 264, 268, 429, 447, 448, 450, 452 Regeneration of forests 55, 57 Silviculture 39 Variation in eucalypts 23 Western Samoa 247 White pocket rot 325, 332 White rot 325, 332 Wilt 128, 131, 138, 139, 140, 422, 450 Witches’ broom 342, 414 Wood, durability of 326, 328 Wood decay 323, 430, 435, 437, 460, 465, 467 Woodland dieback 413 Woody root rot 293, 439, 445 Winter leaf spot 51, 56, 206, 208 Xanthomonas 343, 346 Xanthorrhoeaceae 266, 272 Zambia 212, 246, 250, 329 Zimbabwe 200, 249, 301, 395, 421 Zinc 77, 387, 389, 393, 395, 403 Zygomycota 82, 83

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