Horticultural Reviews, Volume 32

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HORTICULTURAL REVIEWS Volume 32

Horticultural Reviews is sponsored by: American Society for Horticultural Science International Society for Horticultural Science

Editorial Board, Volume 32 Jianjun Chen Thomas L. Davenport Elias Fereres

HORTICULTURAL REVIEWS Volume 32

edited by

Jules Janick Purdue University

John Wiley & Sons, Inc.

This book is printed on acid-free paper. Copyright © 2006 by John Wiley & Sons. All rights reserved. Published by John Wiley & Sons, Inc., Hoboken, New Jersey Published simultaneously in Canada 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, scanning, or otherwise, except as permitted under Section 107 or 108 of the 1976 United States Copyright Act, without either the prior written permission of the Publisher, or authorization through payment of the appropriate per-copy fee to the Copyright Clearance Center, Inc., 222 Rosewood Drive, Danvers, MA 01923, (978) 750-8400, fax (978) 750-4470, or on the web at www.copyright.com. Requests to the Publisher for permission should be addressed to the Permissions Department, John Wiley & Sons, Inc., 111 River Street, Hoboken, NJ 07030, (201) 748-6011, fax (201) 748-6008, e-mail: [email protected]. Limit of Liability/Disclaimer of Warranty: While the publisher and author have used their best efforts in preparing this book, they make no representations or warranties with respect to the accuracy or completeness of the contents of this book and specifically disclaim any implied warranties of merchantability or fitness for a particular purpose. No warranty may be created or extended by sales representatives or written sales materials. The advice and strategies contained herein may not be suitable for your situation. You should consult with a professional where appropriate. Neither the publisher nor author shall be liable for any loss of profit or any other commercial damages, including but not limited to special, incidental, consequential, or other damages. For general information on our other products and services or for technical support, please contact our Customer Care Department within the United States at (800) 7622974, outside the United States at (317) 572-3993 or fax (317) 572-4002. Wiley also publishes its books in a variety of electronic formats. Some content that appears in print may not be available in electronic books. For more information about Wiley products, visit our web site at www.wiley.com. Library of Congress Cataloging-in-Publication Data: ISBN-10: 0-471-73216-8 ISBN-13: 978-0-471-73216-7 ISSN: 0163-7851 Printed in the United States of America 10

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Contents Contributors Dedication: Margaret Sedgley

viii xi

Bryan Coombs

l.

Analyzing Fruit Tree Architecture: Implications for Tree Management and Fruit Production

1

E. Costes, P. E. Lauri, and J. L. Regnard I. II. III. IV. V.

Introduction Architectural Analysis Consequences of Tree Architecture for Tree Training, Orchard Management, and Fruit Production Conclusions Glossary Literature Cited

2. Peach Orchard Systems

2 3 29 43 45 47

63

Richard P. Marini and Luca Corelli-Grappadelli I. II. III. IV. V. VI. VII.

Introduction Crop Physiology Light Management Peach Orchard Systems Vigor-Controlling Methods for Peach Trees Limitations to High Peach Yields Future Trends and Direction Literature Cited

64 67 71 73 90 95 99 102

3. Irrigation Scheduling and Evaluation of Tree Water Status in Deciduous Orchards

111

Amos Naor v

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CONTENTS

I. II. III. IV. V.

Introduction The Modern Irrigation Scheduling Concept Deficit Irrigation Water Stress Assessment and Timing of Irrigation Concluding Remarks Literature Cited

4. Leucadendron: A Major Proteaceous Floricultural Crop

112 113 115 129 152 154

167

Jaacov Ben-Jaacov and Avner Silber I. II. III. IV. V.

Introduction Botany of the Genus Leucadendron World Industry and Economics Horticulture Crop Potential and Research Needs Literature Cited

5. Chinese Jujube: Botany and Horticulture

168 169 173 176 214 216

229

Mengjun Liu I. II. III. IV. V.

Introduction Botany Physiology Environmental Requirements Horticulture Literature Cited

6. Taxus spp.: Botany, Horticulture, and Source of Anti-Cancer Compounds

230 234 250 262 265 288

299

John M. DeLong and Robert K. Prange I. II. III. IV. V. VI.

Introduction Historical Botany Horticulture Pharmacology of Anti-Cancer Compounds from Taxus Conclusions Literature Cited

300 301 303 306 310 321 322

CONTENTS

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7. The Genus Allium: A Developmental and Horticultural Analysis

329

Rina Kamenetsky and Haim D. Rabinowitch I. II. III. IV. V. VI. VII. VIII.

Introduction Taxonomy and Geographical Distribution Genetic Resources and Possible Use of Wild Allium Species Morphological Structures and Comparisons Between Biomorphological Groups Plant Development Propagation Chemical Composition Concluding Remarks Literature Cited

8. The Invasive Plant Debate: A Horticultural Perspective

330 333 335 340 347 361 363 364 366

379

Alex X. Niemiera and Guy Phillips I. II. III. IV. V.

Introduction Perspectives Ecology of Invasive Species Regulatory Matters Conclusion Literature Cited Appendix A

380 393 406 418 430 436 443

Subject Index

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Cumulative Subject Index

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Cumulative Contributor Index

473

Contributors Jaacov Ben-Jaacov, Department of Ornamental Horticulture and Floriculture, Agricultural Research Organization, the Volcani Center, P.O. Box 6, Bet Dagan, Israel, 50-250, [email protected] Bryan Coombe, The University of Adelaide, Australia Luca Corelli-Grappadelli, Dipartimento di Colture Arboree, University of Bologna, 40127 Bologna, Italy E. Costes, UMR 1098—Biologie du développement des Espèces Pérennes Cultivées, Equipe INRA-Agro.M “Architecture et Fonctionnement des Espèces Fruitières”, INRA, 2 Place Viala, 34000 Montpellier Cedex 1, France, [email protected] John M. DeLong, Agriculture and Agri-Food Canada, 32 Main St., Kentville, Nova Scotia, B4N 1J5, Canada Rina Kamenetsky, Department of Ornamental Horticulture, The Volcani Center, Bet Dagan, 50250, Israel, [email protected] P. E. Lauri, UMR 1098—Biologie du développement des Espèces Pérennes Cultivées, Equipe INRA-Agro.M “Architecture et Fonctionnement des Espèces Fruitières”, INRA, 2 Place Viala, 34000 Montpellier Cedex 1, France Mengjun Liu, Research Center of Chinese Jujube, Agricultural University of Hebei, Baoding, 071001, P. R. China, [email protected] Richard P. Marini, Department of Horticulture, Pennsylvania State University, University Park, Pennsylvania, USA 16802-4200, [email protected] Amos Naor, Golan Research Institute, University of Haifa, P.O. Box 97 Kazrin 12900, Israel, [email protected] Alex X. Niemiera, Department of Horticulture, Virginia Polytechnic Institute and State University, Blacksburg, Virginia 24061, USA, [email protected] Guy Phillips, Department of Forestry, Virginia Polytechnic Institute and State University, Blacksburg, Virginia 24061, USA

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CONTRIBUTORS

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Robert K. Prange, Agriculture and Agri-Food Canada, 32 Main St., Kentville, Nova Scotia, B4N 1J5, Canada, [email protected] Haim D. Rabinowitch, Institute of Plant Science and Genetics in Agriculture, The Hebrew University of Jerusalem, Faculty of Agricultural, Food, and Environmental Quality Sciences, Rehovot, 76100, Israel, [email protected] J. L. Regnard, UMR 1098—Biologie du développement des Espèces Pérennes Cultivées, Equipe INRA-Agro.M “Architecture et Fonctionnement des Espèces Fruitières”, INRA, 2 Place Viala, 34000 Montpellier Cedex 1, France Avner Silber, Institute of Soil, Water and Environmental Sciences, Agricultural Research Organization, the Volcani Center, P.O. Box 6, Bet Dagan, Israel, 50-250, [email protected]

Margaret Sedgley

Dedication: Margaret Sedgley This volume of Horticultural Reviews is dedicated to Professor Margaret Sedgley in recognition of her outstanding contributions to horticultural science and to the work of the University of Adelaide. Margaret was born in Oldham, Lancashire, UK and in her late teens was attracted to horticultural science because of the wide range of crops and problems available for study and the promise of applying new and innovative techniques, including microanalysis and molecular biology. Margaret’s university training was at Leeds where she received a B.Sc. (Hons.) in 1970, and in 1974 received her Ph.D. from University of St. Andrews with her work conducted at the Scottish Horticultural Research Institute, Dundee. The rest of her scientific career, from 1974 to the present, has been based in Adelaide. Initially Margaret joined the CSIRO Division of Horticultural Research, attaining the level of Principal Research Scientist in 1985. She then crossed the road to the Department of Plant Physiology of the Waite Agricultural Research Institute, The University of Adelaide, where she became Reader in Horticultural Science. This department was melded with grape and wine researchers from Roseworthy Agricultural College to form the Department of Horticulture, Viticulture and Oenology, of which she was appointed Deputy Head in 1993 and became Head of the Department and Professor of Horticultural Science in 1995. The new arrangements coincided with the mushrooming of undergraduate and graduate student numbers, and an expansion of facilities bringing a heavy administrative load. The scarcity of female professors in the university meant an additional load when sex balancing of committee membership was introduced. Professor Sedgley managed such matters with competence and flair and at the same time handled a huge research program. Summarising her scientific work is a humbling exercise because of its breadth, depth, and sheer volume. This is despite the fact that horticultural industries have been parsimonious in the funding of research. The number of publications that include her name now stands at 528 and is made up of 174 papers in refereed journals, 187 publications and articles, 146 presentations to scientific meetings, 19 chapters, symposia and reviews, and 2 books. She was senior author of a significant proportion of these. In 1981 her work was recognised by the P.L. Goldacre xi

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DEDICATION: MARGARET SEDGLEY

award for distinguished research in plant physiology and, in 1983, the Regents Lectureship of the University of California. A scan of Margaret’s publication list reveals a central theme of the reproductive biology of higher plants comprising the pistil-pollen interaction, outcrossing mechanisms, and breeding methodology. But opportunistic topics are evident such as “Anatomical characteristics affecting the musical performance of clarinet reeds made from Arundo donax L.” The number of her publications increased with each successive five-year period; indeed, 323 (61% of the total) were published in the last ten years. In addition, during that same period she received 41 research grants totalling 7.7 million Australian dollars. She has close ties with a large number of industry bodies and also with the Australian Research Council. Margaret considers her major achievements to be elucidation of outcrossing mechanisms of horticultural plants; matching avocado cultivar to climate, based on flowering biology; domestication of Australian native plants, including quandong (Santalum), Banksia, Acacia, Eucalyptus, bush tomato (Solanum centrale); development of the first three cultivars of Banksia for cut stem production; use of Australian native bees for crop pollination; establishment of the first Australian almond breeding programme; and survey of Australian feral olive germplasm for superior genotype; establishment of the first breeding programme in the world of eucalypts for cut flower production; application of molecular techniques to horticultural plant breeding in Australia, including meiotic maps, molecular marker development, and PCR-based virus testing; and investigation of a new and unique bacterial disease of pistachio. One of Margaret’s major strengths is her ability to successfully put together projects involving the coordination of large numbers of research staff. She has a policy of keeping people informed through regular, productive meetings that include all levels of project staff members. They are invariably good-humoured and passers-by of the meeting rooms often hear Margaret’s hearty laughter, a trademark of her relaxed but efficient style of administration. Another quality is her skill in addressing visiting groups or making introductions; no matter how complicated the occasion Margaret conveys, without notes, all points appropriate for the audience. Margaret’s love of horticulture naturally extends to her own garden, a large area in the Adelaide Hills, full of plants representing many horticultural genera. It has often been the site of many a social gathering. Altogether, Professor Sedgley is an inspiring leader and a very productive scientist and we are grateful that she chose to work with us. Bryan Coombe The University of Adelaide

1 Analyzing Fruit Tree Architecture: Implications for Tree Management and Fruit Production E. Costes, P. É. Lauri, and J. L. Regnard UMR 1098—Biologie du développement des Espèces Pérennes Cultivées Equipe INRA-Agro.M “Architecture et Fonctionnement des Espèces Fruitières” INRA, 2 Place Viala, 34000 Montpellier Cedex 1, France

I. INTRODUCTION II. ARCHITECTURAL ANALYSIS A. General Concepts B. Defining Architectural Models of Fruit Tree Species 1. Identifying Shoot Types 2. Analyzing Branching 3. Examples of Architectural Analysis in Fruit Trees 4. Describing the Intra-Species Variability of Tree Architecture C. Quantitative Studies of Fruit Tree Topology 1. Primary Growth 2. Branching Patterns 3. Location of Flowering 4. Meristem and Shoot Mortality D. Describing Fruit Tree Form 1. Measuring a 3D Form 2. Models for Representing Whole Tree or Row Form 3. Modeling Axis Form Changes 4. Models for Representing the Organ Distributions within Canopy III. CONSEQUENCES OF TREE ARCHITECTURE FOR TREE TRAINING, ORCHARD MANAGEMENT, AND FRUIT PRODUCTION A. Initial Choices of the Grower and Young Tree Training 1. Rootstock Effects 2. Tree Development and Initial Fruit Production

Horticultural Reviews, Volume 32, Edited by Jules Janick ISBN 0-471-73216-8 © 2006 John Wiley & Sons 1

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B. Adult Tree Training 1. Fruit Load Effects on Tree Growth, Architecture, and Ecophysiology 2. Consequences for Fruit Thinning 3. Implementation of Adult Tree Training Procedures IV. CONCLUSIONS V. GLOSSARY LITERATURE CITED

I. INTRODUCTION High yield performance of fruit crops results from the integration of various components, which, pieced together, constitute the “orchard system puzzle” (Barritt 1992). They are implemented at two different time scales: a set of initial choices determines the basic components of the orchard during its life-span (support system, tree arrangement and quality, density, rootstock and cultivar), and a set of annual procedures that is closely related to the training system but evolves from one year to the next (pruning, training, and thinning practices). These components are strongly related to each other and they need to be assembled properly to ensure good economic results (Hoying and Robinson 2000). Provided that techniques are compatible, a large range of combinations is possible. In all cases, however, the training system should integrate the following objectives: (1) light capture needs to be optimized at the orchard scale, in order to obtain a high biomass production (e.g., Jackson 1980); (2) canopy porosity to light (Lakso 1994) should be as high as possible to improve light distribution between fruiting structures (Lakso and Corelli-Grappadelli 1992; Wünsche and Lakso 2000) and to lower the variability in fruit quality; (3) biomass must be partitioned to fruiting shoots, as demonstrated in apple (Lespinasse and Delort 1993) or avocado (Thorp and Stowell 2001); and (4) competition with vegetative sinks by inappropriate heading cuts, which stimulates tree growth and vigor as shown in kiwi (Miller et al. 2001), should be avoided. It is therefore of major importance to develop training concepts that optimally combine training and management systems at the orchard scale and training methods at the tree scale (pruning, bending). At both levels, an accurate knowledge of growth, branching, and flowering processes within the tree canopy, i.e., tree architecture, is thus required to optimize tree manipulation adapted to the plant material. In the first section, we will present the main concepts that are used in architectural analysis and illustrate how they have been introduced and applied to fruit species, from both a qualitative and quantitative point of view. The

1. ANALYZING FRUIT TREE ARCHITECTURE

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second section will present the consequences of fruit tree architectural analysis for tree and orchard management, especially regarding the manipulation of both vegetative and floral organs at the tree level.

II. ARCHITECTURAL ANALYSIS In the last 20 years, architectural analysis of plants has led to the development of new approaches to horticulture from the acquisition of knowledge about tree development to the study of intra-species variations of related characters and, in more applied aspects, to the improvement of fruit tree management at the orchard level. Architectural analysis was introduced in a botanical and forestry context by Hallé and co-workers (Hallé and Oldeman 1970; Hallé et al. 1978) by observing the whole tree with a particular focus on the dynamics of development. From these studies, a general comprehensive framework of the invariant features and rules that are responsible for a tree’s architecture has been extracted. This procedure has been shown to apply to all plant species (Hallé et al. 1978), while the rules are defined at the species scale. Applications developed in horticulture have focused mainly on two within-tree scales: (1) organ arrangement, including both vegetative and floral organs, and their relative equilibrium, and (2) fruiting branches and whole tree behavior. These two scales constitute a basic framework that is then used to interpret the effect of agronomical practices at the tree and orchard scales. A. General Concepts For many years, the diversity of plant morphology has been fascinating scientists and has been extensively studied from both a scientific and philosophic point of view, e.g., Goethe (1790) and Arber (1950). Plant form diversity results from differences in organ morphology and from differences in constructional organization (Bell 1991). The constructional organization of trees, also called architecture, results from the activity of the meristems. All plant organs are made of cells and tissues, which initially organize within a meristematic zone. Thus, a tree, whatever its final size, is initially constructed by the activity of at least two primary meristems (one for the aerial part, one for the root system) or possibly more, and to a lesser extent, by the activity of secondary meristems, which are responsible for the diameter increment of woody axes (Hallé et al. 1978). After observation of the aerial meristem activity in many species, Hallé and co-workers proposed a classification of the aerial organization

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E. COSTES, P. É. LAURI, AND J. L. REGNARD

of trees into four main categories. The first two categories separate trees constructed by a single aerial meristem (monoaxial trees) or several meristems (polyaxial trees) (Fig. 1.1). Polyaxial trees are thus split into three subcategories based on the differentiation state of axes produced by meristems: (1) all meristems have a similar activity and produce equivalent non-differentiated axes, (2) different meristems have different potentialities and produce different axis types (i.e., differentiated axes), and (3) a given meristem changes its activity with time and produces mixed axes, i.e., axes whose basal and top parts have different organization. Within these four main categories, finer classes are considered that are named “architectural models” and are dedicated to famous botanists. The model definitions are based on the concept of “axis differentiation,” which combines five main morphological criteria all related to the meristem activity: (1) the growth direction associated with phyllotaxy makes it possible to distinguish plagiotropic from orthotropic axes. Plagiotropic axes are characterized by a horizontal to oblique growth direction with alternate or distic phyllotaxy and a plane symmetry, while orthotropic axes combine vertical growth with a spiral phyllotaxy and axial symmetry; (2) the growth rhythm can be either continuous or rhythmic. In case of rhythmic growth, the portion of axis developed during the same growing period is called a growth unit (GU); (3) the branching mode (monopodial versus sympodial), position (acrotonic versus basitonic, i.e., long shoots located respectively in the top or basal part of the bearer shoot), and dynamics (immediate or sylleptic vs. delayed or proleptic); (4) the sexual differentiation of meristems; and (5) the polymorphism of axes that allows distinguishing between short (brachyblasts), medium (mesoblasts), and long (auxiblasts) shoots. The proposed classification, composed of 23 models, provided a framework for analyzing plant architecture and led to observations of the

(a)

(b)

Fig. 1.1. Example of monoaxial (a) and polyaxial trees (b) belonging, respectively, to Holtum and Troll models (Source: Hallé, Oldman, and Tomlinson. Tropical Trees and Forests, p. 84, 97. With permission of Springer Science and Business Media.)

1. ANALYZING FRUIT TREE ARCHITECTURE

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developmental dynamics of trees, at the whole tree scale, and the identification of phenomena that are invariant with respect to the environment (Hallé et al. 1978). This approach showed that it was possible to account for the variability of all higher plants by defining a limited number of developmental patterns, defined at the whole tree and axis scales (Edelin 1981; Remphrey and Powell 1987; Caraglio and Edelin 1990; Thorp and Sedgley 1993). In parallel, other concepts emerged from the analysis of plants at both more detailed and more global scales than axes, and from the observation of the repetitive nature of tree construction that results from repetitions of similar organs or sets of organs. At a more detailed scale, a particular focus has been put on metamer or phytomer repetition (White 1979; Barlow 1989) since this entity is composed of a node and its leaf(ves) and axillary bud(s) plus the subtending internode, thereby constituting the basic element of plant construction. However, the repeated entities are not exactly similar and their development was shown to change with their position within the tree structure and during plant development. Different concepts have been proposed to account for the existence of different metamer states and bud fates: “morphogenetic program” and internal correlation (Nozeran 1984), “age state” (Gatsuk et al. 1980), or “physiological age” of the meristems (Barthélémy et al. 1997). Even though the changes in bud fate and entity states are specific to each species and lead to the differentiation of axes (e.g., orthotropic versus plagiotropic axes; short versus long axes, etc.), general rules established for a Rauh architectural tree model are as follows (Barthélémy et al. 1997; Fig. 1.2): (1) an increase in shoot length and in axillary shoot development during an initial period (observed in seedlings and called “establishment growth”); (2) a period of stability during which specific branching gradients can be observed (such as acrotony); and (3) a progressive decrease in shoot length growth and in axillary shoot development towards the final development stage or aging. At the whole-tree scale, two concepts have been introduced in order to define the branching system. First, the concept of “organization plan” has been proposed to account for the hierarchic level between the constitutive axes of a tree (Edelin 1991). The terms hierarchic versus polyarchic were introduced to indicate a hierarchy between main shoots and their laterals, respectively, or conversely the absence of hierarchy. In forest trees, one easily can observe trees that develop in a hierarchic way for a few years before developing a fork and becoming polyarchic. Second, the concept of excurrent versus decurrent trees has been introduced, in relation to apical dominance, in forest trees (Brown et al. 1967). These terms, which refer to a definitive main stem producing lateral

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Fig. 1.2. Schematic representation of architectural gradients in a tree belonging to the Rauh model (Source: Barthélémy et al. 1997).

branches (excurrent) or a main stem that spreads and becomes indistinguishable from the uppermost branches (decurrent), have probably been among the most commonly used in classifications of forest and fruit trees. We will present how these concepts, whether applied at the tree, branching system, axis, or metamer scales, have been used in fruit tree species. First, qualitative concepts will be considered to define the architectural models of several fruit species. Second, quantitative studies will be described to highlight architectural edification rules as well as morphological gradients in fruit species. The following section will thus develop how the architecture of fruit trees has been or can be analyzed. The last section will present how these results were integrated to improve tree training and led to the proposal of new training systems.

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B. Defining Architectural Models of Fruit Tree Species 1. Identifying Shoot Types. The identification of architectural models in a given species first requires identifying the categories of shoots that are observed within the tree structure, on the basis of morphological criteria. As with many other species, fruit trees exhibit a polymorphic development of axes (Fig. 1.3). Usually, two main shoot categories, i.e., short and long shoots, are distinguished by a simple visual observation (Champagnat 1965; Zimmerman and Brown 1971). Champagnat (1965) used three criteria to define short shoots (or brachyblasts): a limited length,

(c) Long shoots

(a) Spurs

(b) Medium shoots Fig. 1.3. Heteroblastic development of shoots in fruit tree: Example of shoot types in an apple branch. (a) Spurs, (b) medium shoots, and (c) long shoots (Original drawing from J. M. Lespinasse reprinted by his courtesy).

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a limited number of organs, and possibly a limited life span. An equivalent definition, based on morphological characters at the metamer level and on shoot growth dynamics, has been proposed (Rivals 1965, 1966, 1967): short shoots are made of organs contained in the resting bud (also called preformed organs), which do not elongate after bud burst. In the horticultural context, different terms have been used for short shoots, according to the species and to their floral or vegetative fate (Champagnat 1954b; Forshey et al. 1992). In pome fruit species, short shoots have been named “dards” when they are strictly vegetative or “spurs” when they are usually floral. In stone fruits they have been named “bouquets de mai” or “clusters” with respect to their early cessation of growth after bud burst. By contrast, long shoots are possibly made of (1) preformed organs solely, whose internodes elongate, or (2) preformed organs followed by neoformed organs resulting from apical growth (Rivals 1965, 1966, 1967). In the first case, the final length is limited and the corresponding shoots often have been considered to be an intermediate category, that of mesoblasts. In a horticultural context, other terms have been used for intermediate shoots according to the fruit species, such as “brindles” in apple or pear, and “chiffonnes” or “mixed shoot” in stone fruit species (Boyes 1922; Champagnat 1954a). In the second case, shoots result from both internodal growth of the preformed shoot and apical growth, which produces a neoformed part, and generally form long shoots. These shoots have been named auxiblasts but occasionally are called “water shoots” in horticulture when growth is extended and/or rate is high. The term “extension shoots” is also widely used for long shoots in both stone and pome fruits. However, most of the horticultural terms have the disadvantage of not strictly fitting with a clearly defined biological phenomenon such as internodal growth and apical growth, or with shoots composed of preformed or neoformed organs. In addition, horticultural terms are often ambiguous with respect to the perennial development of shoots. Indeed, terms can refer either to the result of annual growth or the total growth occurring over several years. For instance, a “spur” can simply be a oneyear-old short shoot or consist of a perennial set of branched shoots, which have all remained short. As a consequence, there is no adequate term in horticulture that can be used to speak of a short annual shoot occurring in the second, third, or fourth year of growth on a long axis. Considering more detailed levels of organization such as growth units (GU) and metamers, even though there are no equivalent horticultural terms, is thus necessary to describe precisely the development of fruit trees over successive years.

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2. Analyzing Branching. In addition to the identification of shoot types, architectural analysis of a tree requires studying whole tree development, analyzing the relative position of the shoots one to another, i.e., tree topology, all over the tree ontogeny. Architectural analysis is made difficult for fruit trees because training systems generally alter tree architecture, often by pruning. Pruning cuts promote local re-growth, which interacts with the natural growth and branching patterns. Thus it appears more convenient, at least as a first step of investigation, to analyze the architectural development of trees grown with minimal training, in particular without severe pruning over several years. The interactions between tree architecture and the agronomic practices then can constitute a second step in the investigations, based on the knowledge of the tree developmental rules. Section III will detail how this second step can be carried out. In temperate climates, investigations of the branching process of fruit trees have focused on one-year-old shoots and on the winter period, because key events, such as apical dominance and bud dormancy, occur at this level of organization and during this period of time. These two main events lead to correlative relationships between buds and dictate the organization of the one-year-old shoot. According to Cline (1997, 2000), apical dominance is defined as the control exerted by the shoot apex on the outgrowth of axillary buds. Its morphological consequence is the inhibition of axillary buds during the growing season when they are formed, often described under the term “bud dormancy.” Research on tree morphogenesis (Crabbé 1980; Champagnat 1989) has initiated the reappraisal of this generic term and led to the differentiation of three different physiological states of the bud—ecodormancy, paradormancy, and endodormancy (Lang et al. 1987)—depending on whether bud inhibition is conditioned on environmental causes or on a correlation with other tree parts, or lies within the bud itself, respectively. Apical dominance involves different correlative mechanisms mediated by auxin and cytokinins (Cline 2000; Sussex and Kerk 2001) and the nutritional status of the axillary buds (Champagnat 1989). However, there are exceptions to the general pattern of apical dominance since some lateral buds can develop during the growing season in which they are formed, producing sylleptic shoots (Champagnat 1954b) (Fig. 1.4). For a review of terms used for branching, see Caraglio and Barthélémy (1997). The capability of axillary buds to develop into sylleptic shoots depends on the parent shoot relative growth rate (Génard et al. 1994; Lauri and Costes 1995) and on the stage of tree maturity. In fruit trees, sylleptic shoots mainly develop during the early developmental years (Crabbé 1987), such as “feathers” in the nursery,

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E. COSTES, P. É. LAURI, AND J. L. REGNARD -1-

-2-

(a)

(b)

(a)

(b)

-3-

(a)

(b)

(c)

Fig. 1.4. Axillary shoot positions and associated terminology regarding branching: 1 (a) monopodial, (b) sympodial; 2 (a) sylleptic, (b) proleptic; 3 (a) acrotonic, (b) mesotonic, (c) basitonic (Source: Caraglio and Barthélémy 1997).

and these branches are considered to be advantageous for young tree establishment (Maggs 1960; van Oosten 1984). Naturally occurring sylleptic shoots have been shown to be naturally located in a median position along the bearing shoot in apple (Costes and Lauri 1995; Costes and Guédon 1997) and peach trees (Lauri 1991; Fournier 1994). This distribution makes it possible to select among these shoots, retaining some of them and pruning those located in the lower part of the trunk or possibly including other criteria for further tree training. Except in the case of sylleptic development, axillary buds develop along the one-year-old shoot, after having passed the three stages of dormancy previously described. In this case, they are called proleptic or delayed shoots (Crabbé 1987), and the axillary shoot development strongly depends on the bud position along the bearer shoot (see Fig. 1.4). In temperate fruit trees, the distribution of laterals most commonly corresponds to an acrotonic distribution, i.e., the longest laterals are located near (just below) the apical (distal) end of the one-year-old shoot (Champagnat 1965; Champagnat et al. 1971). Such a distribution has been described in many species, like apple (Crabbé 1987; Cook et al. 1998b), apricot (Costes et al. 1992), plum (Cook et al. 1998a), and walnut (Solar and Stampar 2003). Quantitative investigations and modeling of lateral distribution are described in section II.C.2 (Branching Patterns).

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3. Examples of Architectural Analysis in Fruit Trees. In the following paragraphs suppress applications of architectural analysis will be illustrated for two main fruit species with contrasting architecture, apple and cherry tree. Complementary elements will also be provided regarding two other Prunus species, apricot and peach tree. For the apple tree, numerous studies in the literature must be compiled to obtain a complete description of its architectural development. Primary growth is usually rhythmic (Zanette 1981; Abbott 1984) and the successive leaves spread along an axis with a spiral phyllotaxy whose angle varies from 3/8 to 2/5 (Abbott 1984; Pratt 1990). Branching remains monopodial before the occurrence of flowering and lateral branches are displayed according to acrotony (Crabbé 1987). Thus, during the juvenile phase, which can be defined in a young seedling tree as a state characterized by the inability to flower (Miller 1988), or during the vegetative state of a non-flowering scion, the apple tree develops according to a Rauh model (Lauri and Térouanne 1995). The different shoot categories that can be identified within an apple tree are often classified into two or three types, based on their length and on their constitutive growth unit types (see Fig. 1.3). Short axes (or spurs) are composed only of short GUs whose constitutive metamers elongate slightly or not at all. As a rule of thumb, the length of each constitutive GU is less than 5 cm. Two types of short GU can be distinguished according to whether the apical meristem is differentiated into an inflorescence (flowering GU) or not (vegetative GU). In the case of floral GU, a leafy basal part is followed by a floral distal part (Fulford 1966a, b; Abbott 1984). This GU, whose diameter is often increased by the presence of an inflorescence and fruit development, is usually named a “bourse.” “Brindle” or medium shoots are constituted of GUs whose lengths reach 6 to 20 cm (Lespinasse and Delort 1993). Long GUs, also called extension shoots, correspond to GUs whose apical meristem has a prolonged activity, leading to the development of neoformed metamers. Floral differentiation, which occurs in the terminal position of axes, ends the monopodial phase. Branching on the floral GUs is immediate and sympodial ( Crabbé and Escobedo 1991). Because of the change in branching mode, from monopodial to sympodial, the architectural model of apple tree evolves from the Rauh to the Scaronne model (Lauri and Térouanne 1995). In addition, adult trees usually exhibit a polyarchic organization resulting from both their sympodial branching and gravimorphic reactions. Indeed, long shoots begin to bend usually after fruiting has begun with long re-growth developing in the upper part of curved axes (Crabbé and Lakhoua 1978). However, this tendency varies greatly among genotypes (Lauri et al. 1995).

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It is worth noting that at least two other fruit species have a roughly similar architectural development to that of apple tree: pear tree, which also belongs to the Rosaceae family, and walnut tree from the Juglandaceae family. Indeed, walnut trees have a rhythmic growth, and a monopodial and acrotonic branching until flowering occurs (Sabatier et al. 1998; Sabatier and Barthélémy 1999; Solar and Stampar 2003). Terminal flowering is a discriminant feature between apple as opposed to Prunus species, since in these latter species flowers differentiate in lateral positions along one-year-old shoots, while the apical bud remains vegetative. Two cases can be distinguished that correspond to cherry or to apricot and peach trees, respectively (Fig. 1.5). In cherry trees, flowers differentiate in lateral buds located on the preformed zone of the oneyear-old shoots. Thus, after bud burst, flowers are located on the basal part of short and long shoots and are clearly separate from vegetative buds. In both apricot and peach trees, floral bud differentiation can occur in meristems located along the one-year-old shoots either directly in an axillary position or on prophylls (i.e., the first two foliar organs of a shoot) of axillary buds (see Fig. 1.6a).

1-year-old shoot

Short shoots

2-year-old shoot

(a)

(b) Flower or inflorescence Vegetative bud

Fig. 1.5. Location of floral differentiation with respect to vegetative buds and shoot organization in two Prunus species: (a) cherry tree—complete separation between floral and vegetative zones; (b) apricot or peach tree—flowers and vegetative buds associated at same nodes.

1. ANALYZING FRUIT TREE ARCHITECTURE

13

Flowering position, combined with the terminal meristem behavior, defines different tree architectures. In cherry and peach trees, the terminal meristem remains alive, leading to a monopodial branching system, while in apricot (or plum) trees the terminal meristem usually dies after each growth period, leading to sympodial branching. Thus, cherry and peach trees both correspond to the Rauh model. In particular, the cherry tree corresponds very strictly to the Rauh model definition, since it is constituted of clearly defined short and long shoots and exhibits a pronounced hierarchic structure. Moreover, the acrotonic gradient is particularly abrupt, leading to long shoots located solely on the uppermost nodes of the annual shoots and thus to a rhythmic distribution of long branches along the main axis. By contrast, in the peach tree, Lauri (1991) observed a more polyarchic organization resulting from the development of basitonic reiterated complexes. The apricot tree also exhibits a polyarchic architecture based on entirely sympodial branching and including a continuum of shoot types between short and long shoots (Costes 1993). The apricot tree provides an example of the Champagnat model, with a definite and rhythmic primary growth, sympodial branching, and long shoots that naturally bend. Shoot bending leads to the development of re-growth from short shoots or latent buds located on the upper side of the curved axes. This pattern has been shown to repeat with tree aging, leading to the formation of successive reiterated complexes whose size decreases from the center to the periphery of the trees (Fig. 1.6). Thus, the polyarchic organization can be exhibited very early in the apricot tree ontogeny. However, this whole tree organization depends on the cultivar, for some apricot cultivars, such as ‘Stark Early Orange’, exhibit a dominant central trunk throughout the life of the tree (Costes et al. 2001a) (Fig. 1.7). 4. Describing the Intra-Species Variability of Tree Architecture. While the aim of architectural studies is to extract invariant features that may adequately define the architecture of a given species, the variability that exists among cultivars in growth, branching, and flowering location must also be explored to propose optimized training methods, adapted to the different behaviors observed within a given species. Different criteria have been used to qualitatively classify cultivars within the different fruit tree species. A pioneer study in this domain was proposed by Bernhard (1961), who first attempted to type apple trees according to both the overall tree growth pattern—i.e., direction of growth of scaffold branches, from upright to weeping—and their fruiting types (types I to IV) (Fig. 1.8). Type I apple cultivars mostly bear fruits on spurs that are branched on “old wood,” whereas type IV cultivars mostly

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E. COSTES, P. É. LAURI, AND J. L. REGNARD

Second growth unit: GU2 axillary bud with two flowers on its prophylls

annual shoot n+1

First growth unit: GU1

axillary bud alone

Short twigs (spurs)

(a)

annual shoot n

carrier shoot (annual shoot n) flowering shoots (annual shoots n+1 and axillary short twigs)

(b) Fig. 1.6. Apricot tree architecture. (a) Organization of annual shoots showing the sympodial branching and the location of floral buds; (b) schematic representation of apricot tree at adult stage showing the progressive decrease in size of the successive branching systems with tree aging (Source: Costes 1993).

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15

Erect Stark Early Orange

Sortilège

Fantasme

Bergeron

Harcot

Comédie

Slender

Shoot slenderness

Goldrich

Shoot bending

Lambertin

Orange Red

Palsteyn

Weeping

Thick

Fig. 1.7. Qualitative classification of apricot varieties observed in France, based on two main criteria represented respectively in X and Y axes: (i) the shoot slenderness, (ii) shoot bending.

ideotype 1

ideotype 2

ideotype 3

ideotype 4

Fig. 1.8. Apple ideotypes from spur (type I) to weeping trees (type IV), as defined by Lespinasse (1992) based on previous studies on “fruiting types” from Bernhard (1961) and Lespinasse (1977).

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E. COSTES, P. É. LAURI, AND J. L. REGNARD

bear fruit at the terminal positions on brindle-type shoots. Lespinasse and colleagues (Lespinasse 1977; Lespinasse and Delort 1986) later included a third parameter, the position of the scaffold branches along the trunk from basitonic to acrotonic. Lespinasse (1992) subsequently proposed including all spur-type cultivars in type II, restricting type I to cultivars that exhibit a typical columnar habit (mainly produced by English breeding selection programs; Tobutt 1985, 1994). Thus all spurtype apple cultivars will hereafter be considered to belong to type I/II. These spur-type cultivars are characterized by a temporal and spatial disjunction between vegetative growth and fruiting since they usually have strong, erect shoots with no or little terminal fruiting. By contrast, type IV (tip bearing type) cultivars develop fruit in terminal positions on all types of shoots, including water-shoots. These architectural features are related to fruiting pattern, with alternate vs. regular fruiting patterns, respectively (Lauri et al. 1995, 1997a, b). Between these two extremes, types II and III (standard type) have an intermediate growth and fruiting pattern. Classifications based upon similar criteria, i.e., branch orientation, position of flowering and lateral branches, have been proposed in other fruit species, such as walnut by Germain (1990, 1992). Qualitative classifications also have been proposed on the basis of shoot types or mixing shoot type with branching density, as the phenotypic classes of peach cultivars proposed by Scorza (1984) and further studied by Bassi et al. (1994) or in pear trees by Sansavini and Musacchi (1994). C. Quantitative Studies of Fruit Tree Topology The existence of generic rules and the repetitive nature of plant construction led different scientists to introduce mathematics into plant architectural studies. Different formalisms were proposed to simulate plant growth processes (Borchert and Honda 1984; Fisher and Weeks 1985; Prusinkiewicz and Lindenmayer 1990; Fisher 1992; Prusinkiewicz et al. 1997; Barczi et al. 1997). On the other hand, tree structure was explored in order to quantify the general rules of tree architecture development that were first highlighted from a qualitative and conceptual point of view. Pioneer research in this area was performed on coffee trees by introducing stochastic modeling of meristem activity (de Reffye 1981a, b, c). Four processes were considered: (1) primary growth, i.e., the dynamics of metamer emergence; (2) branching, i.e., the probability of a given axillary meristem to elongate into a shoot; (3) flowering, i.e., the probability of a given terminal or axillary meristem to develop into a flower; and (4) the probability of meristem mortality.

1. ANALYZING FRUIT TREE ARCHITECTURE

17

According to Godin et al. (1999), the measurements made to characterize plant structure and the different organs plants are composed of can be organized into two categories: (1) those dealing with the form or the spatial location of organs and therefore defining the organ geometry and (2) those that enumerate the organs and determine their relative connections, therefore defining tree topology. Topological descriptions have been designed to simultaneously integrate several organization levels using Multi-scale Tree Graph (MTG) as an underlying model (Godin and Caraglio 1998). Specific softwares, such as 3A (Adam et al. 1999) and AMAPmod (Godin et al. 1997), are currently freely available to collect data for plant architectural databases, and explore them with appropriate statistical tools, respectively. 1. Primary Growth. The number of metamers per axis has been modeled by binomial distributions on both orthotropic and plagiotropic axes of coffee trees (de Reffye 1981c). In this approach, the two parameters of a binomial distribution, p and n, represented respectively the probability that a new metamer emerged from the terminal meristem and the total number of leaves that potentially could be developed by a given axis type. This stochastic approach was adapted to fruit trees with rhythmic growth, such as litchi (Costes 1988) and apricot (Costes et al. 1992). In the case of rhythmic growth, the number of metamers developed per growth unit was modeled either by a Poisson distribution, in the case of entirely preformed organs, or by a mixture of two distributions, in the case of growth units composed of both preformed and neoformed organs (de Reffye et al. 1991). For apricot, the mixture included a binomial distribution for preformed organs and a negative binomial distribution for the neoformed part of the shoot. This formalism made it possible to demonstrate that the progressive decrease in annual shoot length over time resulted from a decrease in the number of neoformed organs, while the number of preformed organs remained almost invariant (Costes et al. 1992, Fig. 1.9). This result was consistent with the observations of Rivals (1965), who assumed a constant number of preformed primordia in resting vegetative buds, this number being at the first order specific to the species. However, within a given species, the number of preformed organs was shown to depend on bud location within branching systems (Costes 2003). Similarly, the acrotonic distribution of axillary shoots was shown to correspond to a decrease in the neoformation development of these shoots according to their position from the distal end of the initial shoot. These concepts were useful for explaining the different shoot types in Actinidia (Seleznyova et al. 2002) or the progressive decrease of successive GUs along axes in apple trees (Costes et al. 2003b).

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E. COSTES, P. É. LAURI, AND J. L. REGNARD

Number of GUs

Number of GUs 1st GU 1987

2nd GU 1987

1st GU 1988

2nd GU 1988

1st GU 1989

2nd GU 1989

1st GU 1990

2nd GU 1990

1st GU 1991

2nd GU 1991

Number of metamers

Number of metamers

Fig. 1.9. Distributions of the number of metamers per growth unit (GU) during the successive years of growth (from 1987 to 1991) and for two successive GUs. The 1st GUs are represented by a set of histograms on the left and the 2nd GUs by a set of histograms on the right of the figure. For each histogram, the total number of metamers per GU was modeled as a mixture of binomial distribution representing the number of preformed organs of the shoot and a negative binomial distribution for the number of neoformed organs. The number of neoformed metamers decreased progressively with years in both 1st and 2nd GUs (Source: Costes et al. 1992).

2. Branching Patterns. In temperate fruit trees, axillary buds develop during two main periods (during the current growing season producing a sylleptic shoot, or during the following growing period producing a proleptic—or delayed—shoot) and at different locations along the original shoot. The median distribution of sylleptic shoots organizes the branching pattern along the main shoot in three successive zones that are observed from the base to the top: (1) not branched, (2) branched, and (3) not branched zones. In addition, axillary shoots can be divided into three types according to their length (short, medium, and long). Thus, the class of Markovian models was selected, since it emerged as a reference

1. ANALYZING FRUIT TREE ARCHITECTURE

19

for analyzing successions of homogeneous zones in discrete sequences, in both computational molecular biology and plant architecture domains (Guédon et al. 2001). More precisely, hidden semi-Markov chains (Durbin et al. 1998) were used to represent both the succession of zones and the proportion of shoot types within the branched zone. At the first level, a semi-Markov chain represents the succession of zones and the length of each zone, the successive zones being connected by transition probabilities. The second level consists in associating each zone with a discrete distribution representing the different probabilities of different types of axillary shoots. The resulting organization of axillary shoots according to specific zones along parent shoots has been demonstrated and modeled in several fruit species, including apple (Costes and Guédon 1997; Costes et al. 1999; Costes and Guédon 2002), peach (Fournier et al. 1998), and Actinidia (Seleznyova et al. 2002). This modeling approach also has been applied to the distribution of both sylleptic and proleptic axillary shoots in one-year-old apple trees, comparing a set of cultivars belonging to contrasting architectural types according to the classification of Lespinasse (1992). All were shown to present a similar organization in successive branching zones that differed one from the other by their composition of axillary shoot types (Costes and Guédon 2002). Roughly, all the cultivars exhibited six successive zones that could be described from the distal end of the shoot as follows: in the most distal zone, long proleptic shoots were observed mixed with latent buds and short shoots; the second zone was occupied mainly by lateral bourses mixed with latent buds; the third zone corresponded exclusively to sylleptic shoots. These first three zones spread over the upper half of the bearer shoot. The basal half of the shoot comprised the three remaining zones: two unbranched zones flanking a large branched zone where long proleptic shoots and spurs were mixed with latent buds (Fig. 1.10). The different cultivars were shown to differ by the length of each zone and the relative proportion of the axillary shoot types within each zone. The long lateral shoots, which can appear in the nursery, were observed in three zones: the most distal, the median zone (corresponding to the sylleptic zone), and the basal branched zone. Thus, the total number of long shoots as well as their relative position along the trunk differed according to cultivar. On average, all cultivars developed more than ten long laterals, except ‘Wijcik’. Most of the long shoots were located in the proximal zone in ‘Reinette Blanche du Canada’ and in ‘Fuji’. In ‘Belrène’, the long proleptic shoots were located equally in the distal and proximal zones. A high number of long shoots in the distal zone were observed in ‘Granny Smith’, reflecting an acrotonic behavior. ‘Imperial

Fuji (III) 20

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symbols

(73.00)

symbols

(57.26)

0123 symbols

(75.06) Most probable axillary shoot in the state Latent bud (symbol 0) Spur (symbol 1) Long delayed shoot (symbol 2)

Axillary floral shoot (symbol 3) Sylleptic shoots (symbol 4) Diffuse mixture of spurs and long delayed shoots

Transition probability

Fig. 1.10. Simplified representation of the branching patterns along one-year-old trunks in four apple cultivars: ‘Fuji’ (type III), Granny Smith (type IV), and Reinette Blanche du Canada (type II), and ‘Wijcik’ (type I, compact). Branching patterns are modeled by hidden semi-Markov chains represented as follows: each branching zone is represented as a state and its length is represented by its mean number of nodes; transitions between states are represented by arrows, with transition probability noted nearby; the proportion of latent buds (symbol 0), short (1), long (2), floral (3), and sylleptic (4) axillary shoots within each zone is represented by a histogram attached at the right of the considered zone. The total mean number of nodes per shoot is noted between brackets at the bottom of the diagram (Source: Costes and Guédon. 2002. Annals of Botany, Modeling Branching Patterns on 1-Year-Old Trunks of Six Apple Cultivars, Vol. 89, p. 520, Figure 6. With permission of Oxford University Press.)

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Gala’, ‘Granny Smith’, and ‘Elstar’ exhibited the highest mean values of long shoots in the median zone. In ‘Granny Smith’, however, the zones were densely branched and separated by latent buds, while in ‘Imperial Gala’, the long shoots were more equally distributed and mixed with latent buds (Costes and Guédon 1997, 2002). The branching pattern of ‘Imperial Gala’ along two-year-old trunks seemed more adapted to the further branching organization of the adult tree. 3. Location of Flowering. Plant architectural descriptions previously showed that flowering is often linked to the branching process. In most temperate fruit species, flowers or inflorescences differentiate on leafy shoots a few weeks after metamer expansion (Foster et al. 2003). Thus, flower organogenesis occurs when and where sylleptic shoots can grow (Crabbé 1987). However, they bloom the following year and finally fruits that are currently borne on one-year-old shoots develop at the same time as proleptic shoots. Therefore, flowering distribution along shoots has been modeled according to the same philosophy as branching, exploring the number of flowers associated at each node rank, either with sylleptic shoots (on current year shoots) or with proleptic shoots (on one-year-old shoots). In both peach and apricot trees, because of the axillary position of flowers and the possible vegetative or floral fate of the main axillary bud, two variables must be simultaneously considered in order to represent, respectively, the main axillary bud fate and the number of associated flowers. In the peach tree, long, medium, and short one-year-old shoots were compared by analyzing the number of lateral flowers relative to the central bud fate, as either a sylleptic shoot or as a flower (Fournier 1994, Fournier et al. 1998, Fig. 1.11). Whatever their type, peach tree shoots were highly structured from the base to the top, and this organization was described as a succession of zones. The proximal and distal zones, which contained latent buds and no flowers, were present in all shoot types. Similarly, the zone that contained central buds, which had differentiated into flowers, was always located in the upper half of the shoot. Two median zones contained one associated flower with short sylleptic shoots or vegetative buds. An additional zone, which contained two or more lateral flowers, was observed in the median part of the longest shoots only. This floral zone also contained long sylleptic shoots. Thus, the number of zones that contained associated flowers, as well as the number of flowers per node and the number of sylleptic shoots, increased with shoot vigor. However, the number of flowers also can be affected by rootstocks since an intermediate growth rhythm has been shown to promote

22 X1

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(a)

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Zone with latent buds and no flower Zone with vegetative buds and 0 to 1 lateral flower per node Zone with sylleptic shoots and 0 to 2 lateral flowers per node Zone with vegetative buds and 1 central flower per node Fig. 1.11. Branching patterns of (a) long, (b) medium, and (c) short mixed shoots of peach tree, modeled by hidden semi-Markov chains that associate the number of lateral flowers (X2 variable) to the axillary bud fate (X1 variable). The length of each zone is represented by the mean number of nodes (Source: Fournier, D., Costes, E. and Guédon, Y. 1998. A Comparison of Different Fruiting Shoots of Peach Tree. Acta Hort. (ISHS) 465:557–566 http://www.actahort.org/books/465/465_69.htm).

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more floral differentiation in peach trees grafted on St Julien rootstock than on those grafted on more vigorous rootstocks (Edin 1982). In apricot, the association between flowers and axillary proleptic shoots was only studied on long annual shoots (Costes and Guédon 1996; Costes et al. 1999). As previously, two variables were considered: the number of flowers associated with each node and the type of proleptic axillary shoot that developed at this node. Along these long shoots, only the basal part did not bear any flowers. Two-thirds of the upper part of the shoots were potentially floral. However, the transitions between the number of flowers per node were gradual: they increased progressively from one to three or more flowers, from the base to the top of the shoot, and then decreased symmetrically from three flowers to two and then one flower per node. As previously described in the peach tree, sylleptic shoots were observed more frequently in the zone that contained three flowers or more. Such an increasing gradient was also observed in annual shoots composed of several GUs in apricot trees, with the second and third GUs bearing more flowers than the first GU within annual shoots (Clanet and Salles 1974). 4. Meristem and Shoot Mortality. In all trees, different shoot categories usually exhibit different life spans. Shoot death is a general phenomenon that may occur in large branches in forest trees or, more usually in short shoots, from the year of bud burst to several or many years later (Bell 1991). Meristem mortality has been modeled by an exponential distribution, considering death probability as a constant (de Reffye 1981b). In temperate fruit trees, among the different shoot categories, short shoots usually have the shortest life span. Thus they have been the most studied organs with respect to mortality. These studies were mainly focused on apple by Lauri et al. (1995, 1997a, b), who demonstrated that spur death, also called “extinction,” is a precocious phenomenon in lateral development and depends upon the cultivar. Moreover, spur death was shown to be correlated positively to the capability of each cultivar to bear fruits regularly in the remaining branchlets through the “bourseover-bourse” phenomenon, which is defined as the proportion of fruitful laterals that give rise to a fruitful lateral the following year. This phenomenon was first described in apple (Lauri et al. 1997a; Fig. 1.12) and, more recently, demonstrated in pear (Lauri et al. 2002). Spur extinction was also shown to occur at a constant rate over years and to be higher for spurs on medium shoots than on long shoots in both ‘Fuji’ and ‘Braeburn’ (Costes et al. 2003b). Thus, it appears that spur extinction is an interesting horticultural trait, specific of cultivar.

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E. COSTES, P. É. LAURI, AND J. L. REGNARD 0.35

Granny Smith

0.30

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0.00 0

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bourse-over-bourse Fig. 1.12. Relationship between bourse-over-bourse and extinction for the various cultivars. Each point represents the mean value for the couples of years 1-2 and 2-3. Bourseover-bourse is defined as the proportion of fruitful laterals that give rise to a fruitful lateral the following year. Extinction is defined as the proportion of laterals that abort (Source: Lauri et al. 1997a. Reproduced with permission of the Journal of Horticultural Science of Biotechnology.)

D. Describing Fruit Tree Form Tree form is another criterion that defines tree architecture, even though little information about plant geometry has been initially included in architectural model definitions. The variability of tree forms within a given species has been described as a continuous phenomenon, from upright to weeping (Bernhard 1961; Lespinasse 1977; Scorza 1984; Sansavini and Musacchi 1994). However, tree and shoot form remains a quite vague concept, and is quite difficult to measure and formally describe, especially when the considered trees do not exhibit an extreme behavior. At the whole tree scale, tree form can be defined according to canopy volume and to the branching organization. It can be evaluated through the overall tree hierarchic organization using the concepts of hierarchy vs. polyarchy introduced by Edelin (1991) and used, for instance, to describe two-year-old apple trees (De Wit et al. 2002). It also can be evaluated through the concepts of excurrent vs. decurrent trees (Brown et al. 1967). At more detailed scales, tree form relies on that of its constitutive organs: for instance, a weeping tree can be viewed as a set of weeping long axes, while an erected tree is a set of erected axes. Stem form and orientation are important components of intra-specific fruit tree architectural diversity and have a qualitative and quantitative impact on fruit production: bending or tilting stems increase flowering, reduce vigor, and modify the branching pattern of the stems (Wareing and Nasr 1958).

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Moreover, taking into account stem form and orientation allows one to tackle problems related to the within tree heterogeneity: (1) when leaves or fruits are considered, spatial position and aggregation are input variables with which to estimate light interception within the canopy; (2) when shoots are considered, it becomes possible to study the geometry of axes and its changes with time. In the following paragraphs, we introduce briefly the techniques that are presently available to collect 3D coordinates of plant organs and we describe the different models of forms that have been proposed to represent either the whole tree, the axes, or the tree organs at more detailed scales. According to the scale considered, applications dealing with light interception or shoot bending prediction are mentioned. 1. Measuring a 3D Form. Different digitizing techniques have been developed involving articulated arms and sonic and magnetic methods to measure the 3D coordinates of plant constituents (Sinoquet et al. 1997). Depending on the study goals, a method based on digital 3D measurements can be applied either to leaves or to axis segments (Fig. 1.13). A further step, which consists of coupling plant topological description to that of constituent geometry, was achieved by coupling a one-scale description of plant topology to sonic digitizing (Hanan and Room 1997)

(a)

(b)

Fig. 1.13. Example of three-dimensional representation of digitized apple trees acquired using a BD magnetic Polhemus digitizer (Adam et al 2001). (a) Branch digitized at leaf scale and visualized with VegeStar software (Source: Massonnet et al. 2004); (b) Whole tree digitized at woody segment scale, and reconstructed by AMAPmod software (Unpublished data from Costes and Sinoquet).

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or by coupling a multi-scale tree graph representation of plant topology to magnetic digitizing (Godin et al. 1999). In both methods, the following softwares are available for data acquisition: 3A (Adam et al. 1999) and Floradig (Hanan and Wang 2004). Despite these software developments, the acquisition of organ 3D coordinates remains time consuming, and simplification procedures are currently under investigation. Casella and Sinoquet (2003) proposed the use of allometric relationships between shoot length, number of leaves, and leaf area to reconstruct 3D architecture from sampling of 3D coordinates. Another solution could be to reconstruct 3D coordinates from stereoscopic photographs coupled to automatic processing that allows an automatic extraction of morphological parameters (Kaminuma et al. 2004). A good correlation between direct 3D measurements of tree canopies and 3D reconstruction has also been recently proposed, which relied upon the calculation of gap fractions from series or peripheral pictures (Phattaralerphong and Sinoquet 2005). 2. Models for Representing Whole Tree or Row Form. The question of whole canopy representation has been developed mainly in the context of physical exchanges between canopy and the environment, especially light interception. In these approaches, canopy structure has been considered at the whole tree, row, or orchard scales, and simple geometrical models are sometimes considered as sufficient (e.g., Li et al. 2002). Jackson and Palmer (1972), who pioneered the calculation of light interception in orchards, first considered solid, non-transmitting, and nonreflecting hedgerows of different forms, latitudes, and times within the year. The hedgerows were considered either as triangular, truncated triangular, or rectangular in cross-section. Palmer and Jackson further refined this modeling approach by considering the tree canopies to be transmitting turbid media according to the law of Beer-Lambert (Palmer and Jackson 1977; Jackson and Palmer 1979; Jackson 1980). Both simpler and more complex models have also been proposed to represent the whole tree canopies. For instance, a two-dimensional (2D) model for representing orchard rows in light interception estimations for different fruit tree species has been proposed by Annandale et al. (2004) (Fig. 1.14). Refinements also have been introduced by considering each tree individually, with tree shape being approximated as conic, parabolic, cylindrical, or as intermediate between a cone and a cylinder (Wagenmakers 1991). Excellent estimations of light interception have been obtained for symmetrical and elliptical canopies, but discrepancies occur with asymmetric canopies or when the assumption of a uniform leaf area distribution was not valid. This drawback can be overcome by a three-dimensional (3D) model that makes it possible to account for

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Fig. 1.14. Simplified ellipsoidal representation of whole tree form and hedgerow used in a 2D solar radiation interception model (Source: Annandale, J. G., N. Z. Jovanovic, G. S. Campbell, N. D. Santoy, and P. Lobit, 2004. Two-dimensional Solar Radiation Interception Model of Hedgerow Fruit Trees, 207-225. With permission of Elsevier.)

canopy asymmetry, such as the model proposed by Cescatti (1997) in a forest context. However, this approach has not yet been applied in a horticultural context. 3. Modeling Axis Form Changes. Except for mutants, in which bending was described during the first year of growth (Monet et al. 1988), main changes in axis form occur in one-year-old shoots when the thin and long to medium shoots are fruiting for the first time. Thus, a weeping habit can be assumed to result from the individual shoot propensity to bend under its own weight and the fruit load. The elaboration of stem form was first studied in a forest context, and is the purpose of tree biomechanics (Castera and Morlier 1991; Fournier et al. 1991a, b; 1994). Stem form depends on several factors related to its growth habit. The first factor is the primary direction of elongation of the apex, which can be modified by subsequent re-orientations of the stem. The weight of wood, axillary shoots, leaves, and fruits causes bending of the stem. The intensity of this bending depends on the amount and location of loads, dimensions of the stem, and mechanical properties of wood. Secondary growth creates an increase in stem rigidity, and the relative dynamics of loading and diameter growth plays an important role in the final shoot form (Fournier et al. 1994). Another effect of diameter growth is active re-orientation of the stem, due to the maturation of new wood layers and more specifically to the action of tension wood (Archer 1986).

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A modeling approach carried out in three contrasting varieties of apricot trees showed that the main factors involved in final shoot form were: (1) its initial geometry (in particular its slenderness and inclination), and (2) the distribution of loads along the shoot (Alméras 2001; Alméras et al. 2002) (Fig. 1.15). The dynamics of cambial growth also impacts reorientation, which corresponds to an up-righting movement after harvest, since lignification stiffens the shoot during the period of maximal curvature due to fruit development. By contrast, the mechanical properties of the wood (i.e., its modulus of elasticity and the presence of tension wood) have a small impact on the final shoot form (Alméras et al. 2004). These results suggest that the variables related to shoot morphology are the first targets to evaluate the propensity of a shoot to bend among different genotypes. Diameter and shoot length constitute elementary variables for characterizing the shoot form, and are putative descriptors of the genetic variability (Kervella et al. 1994), despite the fact that they may be plastic under various environmental conditions (Fournier et al. 2003). Other variables, such as the variation in shoot curvature over two years, shoot slenderness, or branching angles, could also be relevant but need to be confirmed by further studies.

Measured

Measured

Simulated

Simulated

1

1

T0 T0 T0 T0 0.5

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Fig. 1.15. Observed and simulated dynamics of long shoot form during the second growth season, from blooming time (T0) to physiological fruit drop (T1) and a few days before harvest (T2). Example of a shoot belonging to (a) ‘Lambertin’ and (b) ‘Modesto’ cultivars (Source: Alméras, 2001).

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4. Models for Representing the Organ Distributions within Canopy. In horticulture, there is a major interest in quantifying the heterogeneity of organ environment within the canopy, especially considering the heterogeneity of leaves and fruits during their development. Indeed, the organs of the same plant may be subject to contrasting environmental conditions, especially for light distribution, and this may result in differential responses, e.g., in terms of carbon assimilation potential of the leaves and fruit coloring. Two main types of plant representations that account for the organ distribution within the canopy have been proposed. Firstly, individual trees can be split into voxels resulting from a spatial discretization of the space occupied by the tree. Leaf area density (LAD) in a voxel is then assumed to be uniformly and randomly distributed and spatial variation of leaf area density is therefore accounted for by the inter-voxel differences in LAD. This approach has been used for modeling light capture with a turbid medium analogy and has been used to compute radiation balance at canopy, plant, and shoot scale (Sinoquet et al. 1991). Secondly, organs can be explicitly described, with their shape, size, orientation, and spatial co-ordinates being taken into account in 3D plant mock-ups. These mock-ups may be provided by either digitizing methods or simulation softwares. Thus, methods based on polygon projection or on Monte Carlo ray-tracing can be used for modeling light capture at the organ scale. These approaches have been recently reviewed by Godin et al. (2005). Finally, the numerous studies that have been carried out on fruit tree architecture provide nowadays a large set of concepts, methods, and techniques to quantify both the tree topology and geometry, with the possibility to choose between different scales according to specific goals. This overall knowledge constitutes a framework that also benefits orchard and tree training systems, since growth, branching, and flowering processes can be explicitly taken into account in their conception.

III. CONSEQUENCES OF TREE ARCHITECTURE FOR TREE TRAINING, ORCHARD MANAGEMENT, AND FRUIT PRODUCTION Training systems have drawn considerable attention over the past 40 years since they must combine different purposes. Those have been revealed to be more or less conflicting, since economic conditions have varied over time. The main purposes, especially in intensive orchards, are the following: (1) a rapid achievement of a developed canopy structure to reach orchard maturity and maximum fruit production within a

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few years; (2) an optimal capture of light to optimize carbon gain and fruit yield per hectare; (3) a fair distribution of intercepted light within the aerial system of the tree to minimize the spatial heterogeneity of local vegetative growth and fruit quality; and (4) management of tree shape and fruit load with minimal pruning, to take advantage of the natural trends of the cultivar and reduce the economic cost of this manual operation. This last point is of major importance since training systems initially conceived to improve light interception by the tree overall may stimulate growth of vigorous water-shoots, i.e., reiterated complexes, on the upper side of scaffold branches. If not removed, these shoots acting mainly as assimilate sinks may also thwart the benefits of high illumination within the tree by decreasing light interception by fruiting shoots. On the other hand, an unpruned tree, in which vigor is well-distributed to fruiting shoots, quickly begins production but, in most cases, results in an overcrowded canopy after some years and eventually fruit size and quality are reduced. Training methods have then been particularly developed at the tree scale to manipulate both the vegetative and the fruiting components. Pruning vegetative shoots at different positions in the tree or/and at different phenological stages is used both for the building of the tree structure, according to a specific tree shape, and to optimize light distribution within the canopy as in cherry (Flore et al. 1996) or in apple (Barritt 1992). Bending or tying down branches is often used with two objectives. One is to maintain the tree in the allotted space in relation with the tree management system. It is preferred to heading cuts for the control of tree growth and shape and is currently used in particular training procedures, as described for Solaxe (see section III B 3). A second objective of bending is to reduce vegetative growth of the branch and promote flowering. However, the effects of bending on flowering and fruiting remain controversial and, depending on the experiment, orienting entire trees or individual branches horizontally or downward either increases (Tromp 1970; Wareing 1970) or does not have a consistent effect (Longman et al. 1965; Mullins 1965) on flower bud formation and fruiting. It has been shown in apple that both the time and genotype influence the branch response to bending (Fig. 1.16) (Lauri and Lespinasse 2001). A. Initial Choices of the Grower and Young Tree Training Reducing the amount of vegetative growth discarded by pruning should be a main objective of training procedures, as shown in both apple and pear (Forshey et al. 1992). Especially during the early stages of tree

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Logarithmic mean of length (cm)

A X.3318 1-year-old wood

B X.3318 2-year-old wood

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Relative position Fig. 1.16. Effects of time of bending and age of wood on logarithmic mean of the length of laterals (vegetative and bourse-shoots) relative to the position on the shoot (0 = basal to 1 = subapical) for genotypes (A, B) X.3318 and (C, D) ‘Chantecler’. Only positions with at least 15 laterals were considered. Vertical bars represent ±1 SE when larger than symbol size (Source: Lauri and Lespinasse 2001).

development, training a tree to obtain a shape different from its natural growth habit may delay initial fruit production and requires considerable care. Attention may also be needed to maintain the framework of the new allotted shape (Preston 1974). Training the tree with less pruning and taking into account the natural growth and fruiting habit of the tree (Lespinasse 1977, 1980; Forshey et al. 1992) or vine (Possingham 1994) is of major importance and may lead to higher yield performance. The consequences of initial management choices on the young tree

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construction is discussed through two examples dealing with the choice of the rootstock and training system. 1. Rootstock Effects. Among the numerous initial decisions faced by growers when establishing an orchard, that of rootstock is crucial. The grafting of scion cultivars on various selected rootstocks allows the grower to increase orchard density and tree productivity (for historical points of view see Fallahi et al. 2002). Indeed, dwarfing rootstocks reduce the whole tree volume and promote earlier flowering (Lockard and Schneider 1981; Larsen et al. 1992; Barritt et al. 1995). A wide range of rootstocks that promote various tree volumes is available in many fruit species, though not in all (Webster 1997). Important efforts have been devoted to comparing rootstock/scion performance in different climatic areas. From the 1980s, several national programs involving evaluation of different apple rootstocks, cultivars, training systems, and planting sites have been established in the USA, such as NC-140 (www.nc140.org; Fernandez et al. 1991; Perry and Fernandez 1993; Barritt et al. 1995; Marini et al. 2001; Robinson 2003), as well as in northern Europe (Callesen 1997), and in New Zealand (White and Tustin 2000). Detailed interpretations of dwarfing rootstock effects on the development of the aerial part of the trees have been made. They addressed two main questions: (1) is the reduction of aerial growth due to a delay of leaf emergence rate or to a shorter period of growth? and (2) what variables are involved in the reduction of shoot length and in the structural changes of branching systems? The first question has been addressed in apple (Costes and Lauri 1995) and peach cultivars (Weibel et al. 2003) grafted on different rootstocks. In both studies, the length of the growing period was shown to be reduced by dwarfing rootstocks. It also has been demonstrated that rootstocks reduce the internode length (Seleznyova et al. 2003; Weibel et al. 2003). However, different results have been obtained regarding the effect of dwarfing rootstocks on the mean number of nodes per shoot. In peach, Weibel et al. (2003) indicated that differences in shoot length were related primarily to internode length rather than to the number of nodes, whereas Seleznyova et al. (2003) attributed the difference in apple branch size to a reduction in both the length of internodes and the number of nodes that are neoformed within long growth units. Average internode length per extension unit depends on unit node number, with internodes being shorter for units with fewer nodes. Rootstock not only affects shoot length and number of nodes but also branching density and location, and branch characteristics. On cherry, Schaumberg and Gruppe (1985) showed that rootstocks from the Giessen series altered the number of flowers per bud but not the number of buds

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per spur of ‘Hedelfinger’ sweet cherry cultivar. More recently Maguylo et al. (2004) showed that the effects of the rootstock on growth and flowering of ‘Hedelfinger’ may be split into two components, vigor and genotype, with an increase in the number of spurs and the number of flowers per spur as vigor increases in the Giessen series, and a decrease in both variables as vigor increases in the other rootstocks. The effect of rootstock on branching pattern was also studied in apple relative to different axis types, with annual shoots sampled on four- to nine-year-old trees (Hirst and Ferree 1995a), three-year-old fruiting branches (Seleznyova et al. 2003), and along six-year-old trunks (Costes et al. 2001b). In all these situations, the percentage of budbreak of axillary buds on extension growth units was unaffected, regardless of the rootstock. Thus, differences in the number of axillary annual shoots per branch were shown to result mainly from that of the number of nodes developed during the previous year (Costes et al. 2001b). This led to the interpretation that the effect of rootstock on aerial growth is cumulative and superimposed year after year. The changes induced in branching patterns, including both the floral and vegetative development of the axillary shoots, are currently being analyzed, such as applying Hidden-Semi Markov chain models to assess the structural differences induced by a range of rootstock/interstock combinations (Seleznyova et al. 2004). Despite the interest in using dwarfing rootstocks to control tree volume and height, counterproductive effects have also been noticed in the case of excessive dwarfing effects, for instance in cherry (Webster and Lucas 1997; Moreno et al. 2001), peach (Layne et al. 1976; Bussi et al. 1995; Bussi et al. 2002), and apple (Marini et al. 2002). Due to cultivarrootstock interactions, the highest yields at the tree scale are usually not obtained in the most dwarfed trees but in larger trees. A positive relationship between rootstock vigor and cumulative yield has been observed (Warrington et al. 1990). Evidence of a positive correlation between shoot growth and flower bud formation has also been provided in apple, at least under specific conditions of water and nutrient supply (Decker and Hansen 1990). Thus, the choice of the growth level, through the use of rootstocks of various vigor, has to be considered with other variables, such as the intrinsic flowering pattern of the scion, to obtain long-term tree efficiency. The possibility of reducing initial orchard investment through less expensive plant material has been explored through the use of micropropagated, own-rooted trees in Malus (Webster et al. 1985; Quamme and Brownlee 1993) and Prunus (Quamme and Brownlee 1993). In Pyrus, it has been argued that this procedure would be interesting to avoid “pear decline,” often related to grafting, or more generally to the

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graft incompatibility phenomenon (Thibault and Hermann 1982), even though this last argument is no longer applicable to OH × F rootstock selections. As a general trend, self-rooted trees are similar in size to trees grafted on a semi-vigorous or vigorous rootstock, with similar delays for beginning fruit production (Hirst and Ferree 1995b). However, great differences exist among scion genotypes. Some own-rooted apple cultivars such as ‘Greensleeves’ have precocious cropping efficiency higher than that of ‘Greensleeves’ on MM.106, although not as high as that of ‘Greensleeves’ on M9 (Webster et al. 1985). For other cultivars (e.g., ‘Cox’s Orange Pippin’), growing own-rooted trees was much less satisfactory (Webster et al. 1985). It is likely that the branching and flowering patterns have to be taken into consideration when evaluating the potential for growing trees on their own roots. A recent study (Maguylo and Lauri 2004) showed that own-rooted apple genotypes belonging to fruiting type IV with downward-oriented branches and a high frequency of bourse-over-bourse may reach similar or higher cumulated yields than grafted trees in the fourth year of growth. For these genotypes, strong vegetative growth before the first crop significantly reduces branch breakage due to overloading and wind, as compared to trees grafted on M9. It thus makes it possible to grow self-supporting trees needing only a minimal support, with a large root system that ensures good anchorage and possibly enhances water and mineral uptake. 2. Tree Development and Initial Fruit Production. The choice of the training system usually is made at the early stage of orchard planting and, in some cases, has early implications in the nursery, in particular through the selection or pruning of long shoots along the trunk. The manipulations to be carried out usually are described step by step via training schemes (Fig. 1.17). Major changes in training systems were introduced in the 1970s when physiological and architectural rules of tree development were integrated progressively to training concepts. Indeed, the training systems proposed at that time strongly differed from older ones that were mainly influenced by esthetic considerations (Loreti and Pisani 1990). Due to the high number of systems proposed, many studies and discussions have been devoted to the comparison of their relative benefits. According to Robinson et al. (1991b), training systems can be roughly divided into two categories according to whether they (1) apply the natural shape of the trees, such as multiple and central leader (Barritt and Dilley 1989), vertical axes (Lespinasse and Delort 1986), and slender spindle forms (Wertheim 1985), or (2) restrict the canopy in a geometric form such as the A, V, or T forms (van den Ende and Kenez 1985; Lakso et al. 1989). Some of these tree training systems have been conceived as

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Fig. 1.17. The Solaxe apple training system during the first four years (Source: Lauri, P. E. and Lespinasse, J. M. 1998. The Vertical Axis and Solaxe Systems in France, Acta Hort. (ISHS) 513:287–296.) http://www.actahort.org/books/513/513_34.htm.

technical strategies to ease harvest or pruning mechanization, e.g., Tatura or MIA. The early development of the canopy, the initial fruit production and the resulting yield efficiency have been compared for many training systems and fruit crops, including apple (Robinson et al. 1991a; Barden and Marini 1998), cherry (Kappel and Quamme 1993), plum (Wustenberg and Keulemans 1997), and peach (Myers 1994). However, it is difficult to make unbiased comparisons because climatic and horticultural conditions usually differ from one experimental site to another (Tustin et al. 1997). It is also difficult to take into account the economic efficiency of these systems (DeJong et al. 1999) without simulating the weight of different inputs (cost of trees, labor) or outputs (fruit prices). Moreover, the genotypic variability of tree habit makes comparisons between training systems difficult, since genotypes may react differently (Bassi et al. 1994; Lauri and Lespinasse 2000). An important goal of young tree manipulations is to reduce the length of the unproductive period for obvious economic reasons. The counterproductive effect of heading the central leader on the early production of the trees has been emphasized by different authors (Lespinasse 1977, 1980; Barden and Marini 1998; Lauri and Lespinasse 2000). By contrast, taking advantage of the natural branching habit and promoting feathering has been demonstrated to be a possible strategy to reduce the duration of the unproductive period. This arose from studies that were

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carried out either during the juvenile period of seedlings, in the context of breeding programs, especially in apple and pear trees (Visser 1965; Visser and De Vries 1970; Zimmerman 1972; Zimmerman 1977), or in young grafted trees (Maggs 1960). As mentioned previously, in the context of commercial fruit production, the development of sylleptic shoots, or feathering, can be promoted by the application of different chemicals (Preston 1968; Quinlan 1978; Wertheim 1978; Miller 1988). The evidence of a relationship between feathering and earlier initial cropping led to the development of “preformed” nursery trees. In pear (Costes et al. 2004), the number of long sylleptic shoots has been correlated with the number of inflorescences developed per tree in the third year of growth, based on a set of cultivars with different habits and durations of the unproductive period. The most accurate predictive variable of initial flower formation was the difference in the number of sylleptic laterals during the first two years of growth. This suggests that management of young trees should take advantage of the genotypic differences in sylleptic laterals during the first years of growth in order to reduce the length of the unproductive period. The combination of a supported central leader having a selection of long sylleptic shoots along the trunk represents a key step towards training systems with early efficiency and low labor cost. B. Adult Tree Training Once the tree structure is established, the main focus of all training systems is to annually balance the fruit number and weight with vegetative growth. In many perennial crops, an excess of fruit at the expense of vegetative growth may lead to irregular cropping, alternating between large and small crops in consecutive years. Thus, training methods at the tree scale (pruning, bending) aim at directing vegetative growth towards fruiting sinks through precocious growth cessation that optimizes the carbon budget of the tree with regard to fruiting (Sansavini and CorelliGrappadelli 1992; Lauri and Kelner 2001) and reduces heterogeneity between shoots (Lespinasse 1996). The balance between the vegetative growth and the flowering/fruiting components also refers to the concept of crop load, which has been recently reviewed by Bound (2001) and Wünsche and Ferguson (2005). Since there is not a unique definition of crop load, various expressions have been proposed: ratio of fruit buds to vegetative buds or number of buds per meter of frame-wood in pear (Helsen and Deckers 1984), number of leaves per fruit in peach (Ben Mimoun et al. 1998), or number of fruit per canopy volume in citrus (Bound 2001). An easy-to-use method for expressing crop load is to consider it the ratio of the number of fruits (or alternatively weight of

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fruits) per trunk cross-sectional area (TCSA) (Abbott and Adam 1978) or even branch cross-sectional area (BCSA) (Abbott and Adam 1978; Lauri et al. 2004b). Wünsche and Ferguson (2005) here prefer the term of “yield efficiency,” and discuss its validity in the context of tree aging. Nevertheless, large variations may be observed in the relationships between the intensity of alternate bearing and values of TCSA, as shown in apple (Goldschmidtreischel 1996), suggesting that TCSA alone is not sufficient and other parameters should be considered, such as canopy spur leaf area (Sansavini and Corelli-Grappadelli 1992; Wünsche et al. 1996; Lakso et al. 1999). 1. Fruit Load Effects on Tree Growth, Architecture, and Ecophysiology. In what follows, fruiting will be considered through its strong effects on individual tree growth and architecture: (1) fruit load modifies the partitioning of available carbohydrates and water economy in a short term, i.e., during annual cycle, and (2) heavy yields affect tree vigor in a longer term by reducing cumulated growth over years (Regnard et al. 2002) and the fruiting potential possibly inducing an alternate bearing. Reaching an equilibrium between both growth and fruiting is thus one of the main objectives of the fruit grower, as noted by Forshey and Elfving (1989). When trees are young, newly formed biomass is allocated preferentially to growth and directed towards the scaffold establishment and the development of the root system. Biomass investment in fruit progressively increases as the tree ages (Cannell 1985). When the orchard reaches its adult phase, and provided that environmental and cultural practices are at the optimum, the fruit yield compared to total annual biomass increment—namely the harvest index—can reach seventy per cent or more in peach (Cannell 1985) or apple (Lakso 1994). In any case, biomass acquisition and utilization should be considered at the whole plant level in terms of functional balance, which requires modeling approaches (e.g., Cannell and Dewar 1994; DeJong and Grossman 1994). Considering the large numbers of flowers or inflorescences that a fruit tree usually bears, regulation of fruit load is needed. This implies: (1) knowledge of the normal rates of fruit set that are compatible with vegetative growth equilibrium, (2) assessment of the fruit set ratio after bloom, (3) a comparison of fruit/leaf ratios, and (4) use of efficient and low-cost practices to thin excess fruitlets. Branch pruning combined with thinning are, in fact, the one key control strategy for regulating fruit load. When trees are overloaded, fruits act as major sinks for carbohydrates (Ho 1988) and divert a major proportion of photoassimilates. This can be detrimental to primary and secondary vegetative growth of the aerial system, and can starve the root system (Lenz 2001). Numerous

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studies have demonstrated that altering growth can result in modifications of tree architecture. In peach, a reduction of primary shoot growth is observed in stems with subtending fruit compared to shoots with no fruit (Berman and DeJong 1997). Furthermore, shoot length and weight decrease exponentially as the crop load increases, while the relative gain in trunk girth decreases linearly (Blanco et al. 1995). In apricot, high fruit loads were shown to affect primary growth rhythmicity and growth resumption during the growing season, and to enhance the acrotonic pattern of branching (Costes et al. 2000). However the long-term effects of the spatial distribution of fruits within the canopy on tree architecture have not specifically been investigated. In three- and four-year-old apple trees, heavy fruit loads led to higher allocation of biomass to fruit, and lower allocation to new shoot growth, which resulted in reduced thickening of branches and less root growth (Palmer 1992). Experimental defruiting of young apple trees can result in higher leaf weight on area basis, longer shoots, and greater increases in TCSA compared to normal fruiting (Erf and Proctor 1987), while the presence of fruits conversely reduces leaf and root dry weight up to 45% (Buwalda and Lenz 1992). In sweet cherry, current-season growth appears to be a greater sink for photosynthates than fruits, but fruiting is recognized as a factor that reduces shoot growth (Kappel 1991). In highbush blueberry, Maust et al. (1999b) demonstrated that high flower bud density decreased vegetative budbreak, new shoot dry weight, leaf area, and leaf area to fruit ratios. Excessive crops can lead to biennial bearing. A classic study carried out in seeded vs. seedless apples by Chan and Cain (1967) demonstrated the specific role played by seeds in inhibiting floral initiation. The effect of seeds, which peaks from 6 to 10 weeks after full bloom, is generally attributed to gibberellin synthesis, which is assumed to counteract the floral process within apical buds of brachyblasts (Crabbé 1987; Crabbé and Escobedo-Alvarez 1991). Excessive fruit load during “on” years also lowers the amount of vegetative growth and consequently potential photosynthesis and C-assimilate supply by sources to sinks, ultimately resulting in decreased floral initiation during the growing season. Moreover, it has been frequently noticed that during the following year, when the return bloom is low (“off year”), the quality of flower buds and the effective pollination period (Williams 1965) are often reduced. Combination of both phenomenons strongly reduces fruit yield. The biennial cycle is then auto-reproducible, high yield and poor growth alternating with low yield and vigorous growth. The propensity for biennial bearing is particularly important in apple (type I and II), pear, plum, olive, and citrus, although there are important differences among cultivars. A thorough analysis of the strong alternate bearing of types I and II apple cultivars was developed by Lauri et al. (1995, 1997a).

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Source-sink relationships and particularly carbon budgets have received considerable attention in fruit trees (Blanke and Notton 1992; Wibbe et al. 1993; Wibbe and Blanke 1995), leading to the development of carbon balance models, e.g., in apple (Johnson and Lakso 1986a; 1986b) and peach (Grossman and DeJong 1994). Distribution of Cassimilates is subject to complex mechanisms involving many aspects, including the distance between sources and sinks as described in both kiwifruit (Lai et al. 1989) and apple (Palmer et al. 1991), the capacity of the translocation system as noted in peach (DeJong and Grossman 1995) and more generally sink strength variations (Ho 1988). Moreover, the stimulation of the assimilation process by the fruit itself has been demonstrated, e.g., in peach (DeJong 1986; Bruchou and Génard 1999) and apple (Gucci et al. 1995; Giuliani et al. 1997; Palmer et al. 1997; Wünsche et al. 2000; Untiedt and Blanke 2001). Relations between crop load and water economy of the tree also must be considered, for it has frequently been shown that high fruit load results in modifying the trade-off between carbon assimilation and transpiration, as the tree meets the increasing sink demand by increasing the assimilation rates and concomitantly transpiring water at a higher rate. Conversely, defruiting or harvesting trees produce a decrease in sink demand that suddenly results in lower assimilation rates and secondarily higher water use efficiency (Chen and Lenz 1997; Pretorius and Wand 2003). Although fruit nitrogen demand is not generally large, except in nut crops, high fruit loads can deplete nitrogen availability during early shoot growth. This in turn can limit the vegetative growth extension rate (Forshey 1982; Sadowski et al. 1995). High crop loads also result in competition between fruits, which affects their development and final size (Denne 1960; Goffinet et al. 1995; Maust et al. 1999a) and generally lowers their quality (Kelner et al. 2000; Link 2000; Wünsche et al. 2000; Bound 2001; Wünsche and Ferguson 2005). Comparing severely thinned vs. unthinned peach trees, Grossman and DeJong (1995) suggested that heavy flower suppression could give a fair estimate of the potential relative growth rate of the remaining fruits, while fruit growth was source-limited on unthinned trees. A similar approach led Lakso et al. (1995) to develop an expolinear model for apple fruit potential growth under non resource-limited conditions. 2. Consequences for Fruit Thinning. In response to the necessity for fruit load regulation, biennial bearing avoidance, and fruit quality improvement, thinning methods have received considerable attention in recent years, as attested by successive reviews (Williams 1979; Miller 1988; Dennis 2000; Bangerth et al. 2000). In apple, where chemical thinning

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has been commonly applied since the 1950s, the suppression of excess fruitlets is performed up to 30 days after full bloom. Thinning effects are optimal during this period because fruit-to-fruit competition for photoassimilates is limited and excess fruits abscise before the detrimental effect of fruit on floral initiation for the next year can be observed. Chemical thinning often operates by anticipating the June drop. Considering the differential genotypic sensitivity of different apple cultivars to thinning agents and also the numerous factors that can affect tree responses, the ultimate choice of a thinning program includes several parameters that must be adjusted by the fruit grower: active ingredient(s), concentration, wetting agents, spray volume per ha, and time of application. Some specific objectives have to be kept in mind and achieved. For example, lateral fruits borne on one-year-old shoots are generally undesirable (and are thinned by chemicals) because their potential growth is much lower than that of fruits borne in terminal positions either on mesoblasts or auxiblasts (Jackson 1970; Lespinasse 1970; Marguery and Sangwan 1993). As chemical thinning procedures to date have not produced totally predictable results, the grower also must decide whether additional manual fruit thinning must be performed. In apple, the strategy of fruiting shoot removal, also called artificial extinction, has proven to be effective in reducing biennial bearing and frequently in improving fruit color and size, and will probably receive increasing attention in the future (see section III B.3). 3. Implementation of Adult Tree Training Procedures. There is interest in developing a better knowledge of tree architecture, i.e., growth and fruiting patterns, to develop training procedures adapted to commercial tree fruit species and cultivars. Over the last four decades, the evolution of cultivation of apple is a good example of how the knowledge of tree architecture can be used to improve tree training. Indeed, pioneering work of Bernhard (1961) and Lespinasse and co-workers (Lespinasse 1977, 1980; Lespinasse and Delort 1986) ranked apple cultivars more or less linearly according to their fruiting type, from type I to IV. In relation to this classification, three fruiting zones have been defined, each corresponding to the successive stages of branch development over time (Lespinasse 1977; Lauri and Lespinasse 2000). Moreover, in the apple tree, terminal flowering greatly varied depending on the cultivar (Lespinasse 1977) and this trait has great consequences on branch bending and consequently on the distribution of vegetative growth on parent branches. The morphological expression of the apple tree architecture is then highly dependent on the cultivar. Similarly, although acrotonic branching is a common trait of all cultivars, the density of branches, espe-

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cially short laterals in median and possibly proximal positions, is related to regularity of bearing (Lauri et al. 1995). The aim of training is therefore to use the variability existing among cultivars in growth, branching, and flowering location to optimize training methods. These studies have led to the introduction of two main improvements in apple tree training in France in the last decades. They involve the regulation of both branch growth and crop load by controlling fruiting lateral density. From Renewal Pruning to the Free Growing Fruiting Branch. Renewal pruning was a cornerstone of the Vertical Axis training system proposed by Lespinasse (1980). However, observations in commercial orchards showed that regular heading back of the branch to develop new shoots may lead to an imbalance between vegetative growth and fruiting, especially under vigorous conditions, and also to an increase in the proportion of fruit on one-year-old wood (Lauri and Lespinasse 2000). An opposing concept has been proposed, involving the removal of competing shoots on the upper-proximal part of the branch to invigorate distal fruiting organs. This new concept was integrated into the Solaxe training system, without any heading of the trunk, and minimal pruning and shoot bending of lateral branches (if necessary) to better control branch growth and tree shape (Lespinasse 1996; Lespinasse and Lauri 1996; Lauri and Lespinasse 2000). Crop Regulation via Artificial Extinction and Centrifugal Training. The positive relationship between natural extinction of some laterals and the increase of bourse-over-bourse trend of other laterals observed in regular bearing cultivars suggested that lateral density in a branch is in some way physiologically related to the development of the other laterals (growth and flowering frequency). From this result, it has been hypothesized that “artificial extinction” practices, i.e., thinning out of young fruiting laterals (Lauri et al. 1997b; Lauri and Lespinasse 2000; Lauri 2002; Lauri et al. 2004b), implemented in alternate bearing, usually spur-bound, cultivars would improve sustainability of the remaining fruiting laterals over the years (Lauri et al. 2004a). Artificial extinction is carried out more specifically on the underside as well as the proximal part of the fruiting branch, and around the vertical trunk where shaded laterals have poor vegetative development and low fruit set and size, color, and soluble solids (Tustin et al. 1988; Rom 1992). This procedure, called centrifugal training (Fig. 1.18), favors fruiting in the peripheral zone of the canopy and significantly improves light interception by fruiting shoots as well as canopy porosity (Willaume et al. 2004). From a biological point of view, centrifugal training does not

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Light well brought about by centrifugal training: extinction is carried out along the trunk and on the proximal part of branches to improve light penetration within the canopy

Fruiting zone in the upper three-quarters of tree canopy

Extinction on the underside of branches to increase light penetration through the canopy

No branching below 1-1.2 m to permit development of the fruiting branches

Fig. 1.18. Centrifugal training concept to improve light distribution (gray arrows) in the tree (Source: Lauri 2002).

act only as a fruit load-regulating technique, since some photosynthate sources (leaves) and sinks (fruits) are removed at the same time. It is therefore not fully comparable to chemical thinning, or hand thinning, of flowers and fruitlets during which only generative organs are removed, while all the leaves are kept. Results on cultivars ‘Gala’ and ‘Braeburn’ showed that centrifugal training improved and homogenized fruit size and return bloom as compared to Vertical Axis or Solaxe systems (Larrive et al. 2000, 2001; Crété

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et al. 2002; Ferré et al. 2002; Lauri et al. 2004a). A possible interpretation of these effects would be the moderate length increase of bourseshoots that are brought about by the decrease of branching density (Lauri et al. 2004b). From a physiological point of view, this manipulation would improve the autonomy of the fruiting shoot with regard to carbohydrate acquisition and allocation, leading to a higher return-bloom potential (Lespinasse and Delort 1993). Implementation of centrifugal training in commercial orchards is now under development and evaluation in various places in France and in other countries (e.g., Italy, Diemoz et al. 2002, Neri and Sansavini 2004; Argentina, Rodriguez 2003) through the impetus of the Mafcot network (Lauri et al. 1999). Artificial extinction and its development as a training procedure through the setting up of centrifugal training is one among several manipulations (artificial bending, pruning methods, etc.) that the grower may use in the orchard. It has been shown that the relevance of centrifugal training depends on the cultivar. Although the “light well” (see Fig. 1.18) is not necessary for ‘Granny Smith’ training, it is recommended for colored cultivars such as ‘Pink Lady®’ (Hucbourg et al. 2004a, 2004b). These changes in training concepts already have practical consequences on the desired nursery tree structure: it is now recommended to plant trees that are unbranched up to 100–120 cm from the ground (Fig. 1.18) in order to keep the branches growing downwards as perennial structures (Lauri 2002). Specific studies are now carried out to end up in an overall “LITE planting system” (Lauri et al. 2004b) that optimally combines rootstock/cultivar material, planting distances, and tree height. This concept of crop regulation through detailed pruning of fruiting shoots, minimizing pruning of structural wood, is now under development in other species, in particular cherry (Claverie and Lauri 2005; Lang et al. 2004a; Lauri and Claverie 2005).

IV. CONCLUSIONS In order to constitute its own “orchard puzzle system,” each grower must consider numerous possible choices. Other criteria than those detailed above will of course be considered, particularly the socio-economic context that is specific to each species and production area. Even though these criteria were not addressed in this review, they may be of major importance and complementary to those related to tree architecture. Similarly, we did not detail all the agronomic practices that can be performed in an orchard or at the tree scale. Our primary aim was to

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demonstrate that any manipulation could be analyzed from an “architectural” point of view. This approach integrates the tree architectural development, the desired equilibrium between vegetative and reproductive organs, and their changes in these relationships over time. This has been demonstrated through specific examples, but this approach could be extended to other agronomic practices or tree manipulations such as mineral and water supply, pest management, etc. This is made possible by the perennial behavior of trees that allows one to “read” their history over time. The approaches presented here also open new perspectives for integrating traits related to morphology and architecture into breeding and selection schemes. Recently, this integration has become a goal in different countries, including France, as a complement to disease resistance and fruit quality, which remain the main selection targets in fruit tree breeding (Laurens et al. 2000). A first step consists of studying the inheritance of morphological traits, and relies on an estimation of the respective effects of the genotype and the environment and their possible interactions. Because the comparison of successive years integrates both different climatic conditions and the evolution of traits with plant development, these effects cannot be easily separated in perennial woody plants. Tree architectural analysis could thus provide a methodological framework for genetic studies in the future, to develop new strategies for the phenotypic description of progenies (Costes et al. 2003a). Quantitative studies that have concentrated on different processes involved in tree architecture development are opening new perspectives in modeling approaches. During the last few decades, strategies have focused on modeling either the tree’s structure—mainly considering each developmental unit separately—or its physiological functions, such as carbon acquisition and partitioning. In the last five years, a new trend has emerged that aims at modeling both structure and function in so-called “functional structural models” (Sievänen et al. 2000) in several species. Results have been presented recently for peach, by integrating the sink-driven PEACH model (Grossman and DeJong 1994) into 3D structure simulations using Lindenmayer L-system formalism (LPEACH, Allen et al. 2004). This new approach allows the simulated distribution of carbon acquisition and partitioning among the individual organs of the tree, while the previous model (Grossman and DeJong 1994) represented all the organs of the tree as belonging to the same component with a single function, for each given function. Research is currently under way to develop different modeling strategies for cherry (Lang et al. 2004b) and apple (Renton et al. 2004). In the latter case, the focus is on the integration of the branching and biomechanical models

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presented above to end up in a full tree simulation. This approach would make it possible to address the issue of model validation by comparing simulated trees to architectural databases on both topological and geometrical characters. In the future, 3D simulations obtained by these different projects could open new perspectives for the use of virtual (computer-based) orchards and to test new assumptions in silico regarding the interactions between tree development and agronomic practices. V. GLOSSARY Acrotonic/mesotonic/basitonic branching. Terms related to the location of long lateral shoots along a one-year-old, or even older, bearer shoot. They correspond to long laterals located in the top, medium, and basal part of the bearer shoot, respectively. Notice that these definitions can be used either at the whole tree or at finer scales, such as annual shoot scale. While acrotony is usually considered to be a consequence of the “apical control,” the physiological bases of basitony are not fully elucidated (Barnola and Crabbé 1991). Apical dominance. Control exerted by the shoot apex on the outgrowth of axillary buds during the first year of growth (Cline 1997). Brachyblast/mesoblast/auxiblast. Short, medium, and long shoots, respectively (Chadefaud and Emberger 1960). Delayed (or proleptic) branching. Discontinuous development of a lateral from a terminal meristem to establish a branch, with some intervening period of rest of the lateral meristem. Proleptic branches have one or more basal bud-scales and usually a series of transitional forms towards the adult leaf (Hallé et al. 1978). Excurrent/decurrent. Form of woody plant determined by the differential elongation of branches. Columnar and cone-shaped trees with a strong apical dominance are termed excurrent, while trees with a weak apical dominance are decurrent (Brown et al. 1967). Gravimorphism. Effects of shoot position, in relation to the gravity, on its growth, branching, and flowering (Wareing and Nasr 1958). Growth unit/annual shoot. Growth units (GU) can be distinguished in plants characterized by their rhythmic growth. A growth unit is the part of an axis that develops during a non-interrupted phase of lengthening (Hallé and Martin 1968; Hallé et al. 1978). Each growth unit comprises a basal part that bears basal cataphylls (ultimately leaving scars) followed by a set of true leaves. In temperate climates, annual growth is the sum of growth units that are produced during a growing season.

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Hierarchic/polyarchic organization. Existence of differentiation between axes with dominance of an axis or absence of a main dominant axis, all the axes being equivalent. These terms apply at the whole tree scale (Edelin 1991). Immediate (or sylleptic) branching. Continuous development of a lateral from a terminal meristem to establish a branch, without an evident intervening period of rest of the lateral meristem. Sylleptic branches lack basal bud scales and generally have an extended basal internode (hypopodium) below the first leaf(ves) (Hallé et al. 1978). Meristematic zone (apical and root meristems). Cellular territories, located at the axis end, which are major sites of cell divisions and provide a source of cells for primary shoot and root growth. In higher plants, one to three layers of meristematic cells are usually observed (named L1, L2, and L3) but other terms and organization have been considered (in particular a tunica-corpus organization) (see Lyndon (1998) and Nougarède (2001) for reviews). Metamer/phytomer. Basic module in plants resulting from the shoot apical activity and composed of a node, its axillary production, leaf(ves), and axillary bud(s), and subtending internode (White 1979). Monaxial/polyaxial. Trees whose aerial part is made of a single axis (derived from a single meristem) or several axes respectively (Hallé et al. 1978). Monopodial branching. The outgrowth of axillary buds occurs as the terminal meristem grows and remains dominant (Bell 1991). Orthotropy. An orthotropic axis is erect with essentially radial symmetry, phyllotaxis spiral or decussate, branching 3-dimensional, often non-flowering. The orthotropy of axis implies self-sustaining of the axis, involving secondary growth process. (Both definitions from Hallé et al. 1978). Phyllotaxy. Overall arrangement of leaves along an axis, frequently expressed as the radial angle between two successive leaves or by an index corresponding to a fraction of 360° between two successive leaves (Jean 1995). For detailed explanations on different phyllotaxy in plants see Bell (1991). Plagiotropy. A plagiotropic axis is more or less horizontal with dorsiventral symmetry, leaves either distichous or secondarily arranged in a plan, branching 2-dimensional, often flowering. Different forms of plagiotropism can be observed: plagiotropism by apposition or by substitution.

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Preformed/neoformed organs. Preformed organs correspond to primordia that were formed but not elongated before the meristem enters into a resting period; neoformed organs correspond to primordia that elongate just after their formation from a meristem, without a resting period (Rivals 1965, 1966, 1967). Rhythmic/continuous growth. Terms related to the rhythm of emission of new leaves from an apical meristem. An axis with a constant delay between the successive leaves during all the year has a continuous growth (can be observed in tropical zones), while an axis with clear periods of rest of the apical meristem has a rhythmic growth (Hallé and Martin 1968). Secondary meristem or vascular cambium. Secondary meristem that derives from the procambium and is responsible of the diametral growth of plants and trees. It is composed of a layer of cells (usually considered as uniseriate) that produces phloem and xylem mother cells (phloem being formed in the outer side and xylem in the inner side of the stem) (Lachaud et al. 1999). Sympodial branching. A new axis develops from an axillary bud situated on the previous axis, which dies or grows very slowly. The resulting series of axes is termed a sympodium, or a sympode; each member of the series is termed a sympodial unit (Bell 1991).

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2 Peach Orchard Systems Richard P. Marini Department of Horticulture The Pennsylvania State University University Park, Pennsylvania, USA 16802-4200 Luca Corelli-Grappadelli Dipartimento di Colture Arboree University of Bologna 40127 Bologna, Italy

I. INTRODUCTION II. CROP PHYSIOLOGY A. Cycles of Growth 1. Tree 2. Flowering 3. Fruit III. LIGHT MANAGEMENT IV. PEACH ORCHARD SYSTEMS A. Tree Forms B. Tree Form Effect on Yield C. Tree Density Effect on Yield D. Effect of Tree Density Plus Tree Form on Yield E. Meadow Type Systems F. Protected Peach Culture G. Economics of Peach Orchard Systems V. VIGOR-CONTROLLING METHODS FOR PEACH TREES A. Root Restriction B. Deficit Irrigation C. Summer Pruning D. Plant Growth Regulators E. Tree Growth Habit VI. LIMITATIONS TO HIGH PEACH YIELDS A. Rootstocks Affect Partitioning B. Scion Affects Partitioning

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C. Tree Spacing Affects Partitioning D. Training System Affects Partitioning VII. FUTURE TRENDS AND DIRECTION LITERATURE CITED

I. INTRODUCTION Peach is one of the most important deciduous tree fruits, second only to apple, and the annual worldwide production is about 10 million tons (Fideghelli et al. 1998), but annual production is increasing exponentially as land devoted to peach production is increasing at the rate of about 77,000 ha/year (Fig. 2.1) (FAOSTAT 2003). Much of this growth has occurred in China, where peach plantings increased about 426,000 ha from 1995 to 2002. Profit margins for commercial peach orchards have declined, partly because prices have increased less than production costs. Profits may be improved by increasing yield per unit of land area or by reducing labor costs. Orchard system modification may influence both of these factors. Worldwide, peach yield/ha has declined during the past decade (Fig. 2.1), probably because young orchards have not yet reached full production and because a higher percentage of world production is from China, where yields are low. Yield/ha varies greatly from one country to another. During the past 50 years, yield/ha has improved in developed, but not developing countries (Fig. 2.2). The lack of improvement in developing countries is likely due to the lack of research leading to new orchard practices, but even in developed countries average yield/ha has improved little since 1980. Researchers and commercial producers have evaluated a number of stone fruit orchard systems, but the majority of commercial peach orchards have changed little during the past 150 years. For more than a century, the Open-Vase system, with about 250 to 350 trees per hectare, has been the predominant peach tree form, but hedgerow systems have also been grown for many years (Cole 1849; Fitz 1872; Hedrick 1917). In contrast, during the last 40 years, dramatic changes in apple orchard systems have resulted in greatly improved yields. Dwarf rootstocks and spur-type scion cultivars have allowed apple producers to plant highdensity orchards with 700 to 1400 trees per hectare. Combining these genotypes with cultural practices such as shallow planting, slender spindle and North-Holland Spindle systems, very limited pruning in the early years, and cropping as a tool to reduce vegetative vigor in the early years allowed establishment of plantings with 4000 or more trees per ha (Jackson 1989; Sansavini and Corelli-Grappadelli 1997). The benefits of

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Hectares (millions)

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Year Fig. 2.1. Trends in worldwide peach production from 1960 to 2000: Hectares of peaches planted (Top), average annual production of peaches (Middle), average peach yield per ha (Bottom) (Source: Food and Agriculture Organization Statistics Database, 2003).

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Year Fig. 2.2. Yield (t/ha) for different peach-producing regions from 1960 to 2000. Southern Europe includes France, Greece, Italy, and Spain. To avoid large yearly fluctuations, values are actually 3-year means: for example, values for 1980 are the means for 1979, 1980, and 1981 (Source: Food and Agriculture Organization Statistics Database, 2003).

high-density plantings include precocity of bearing, higher early yields, and earlier returns in the critical first years from planting (Goedegebure 1989). Training systems, such as the Vertical Axis (Lespinasse 1980), were also developed to take advantage of the precocity, the variation in disease and insect resistance, and the vigor-controlling characteristics of these rootstocks and cultivars. With such systems, relatively tall trees (3.1 to 4 m tall) produced high yields of quality fruit within 5 years of planting and productivity was maintained for a number of years (Marini et al. 2001a). However, these plantings with tall trees were expensive to prune and harvest due to the need for ladders or expensive picking platforms, an alternative to ladders in intensive South-European orchards. Peach trees may easily reach a similar height because of the species’ intrinsic vigor and lack of vigor-controlling rootstocks. Tall peach trees tend to be more expensive to maintain because more hand labor is required for pruning, and to manage the crop load with hand thinning. Additionally, most peach cultivars ripen non-uniformly and require several spot-pickings. In Spain and France, where emphasis is being placed on harvesting ripe fruit, commercial peach orchards are being harvested as many as 5 to 8 times. Some of the most intensive (i.e., highest tree densities) peach orchard systems, such as the Meadow Orchard (Erez 1978), were designed for mechanical harvest, but they have not yet been successful because of many limitations, primarily mechanization; they may become more economical as harvesting technology improves.

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Researchers and commercial producers have few tools to alter the balance of vegetative and reproductive growth of peach trees. Thus, the primary benefit of intensive peach orchards is the high production of young orchards associated with rapid development of the fruiting canopy. Intensive orchards are sophisticated production units, which require very careful management to retain their performance. Very often, as these orchards mature, yields may decline as shade reduces the productivity of the lower and inner canopy, pushing the productive zone out and upward. The primary challenge with these systems is to maintain high productivity over the life of the orchard. Lacking vigorcontrolling rootstocks or suitable compact/spur cultivars, some researchers have successfully used water stress, root restriction, and root competition to control tree vigor. This review is intended to provide a critical evaluation of peach orchard systems research, and to identify potential areas of future research.

II. CROP PHYSIOLOGY A. Cycles of Growth Before discussing various components of peach orchard systems and techniques employed to manage various systems, it seems appropriate to discuss seasonal growth of the tree and fruit. 1. Tree. Like all deciduous trees, peach trees undergo a dormant period during the winter. During dormancy root growth may continue if soil temperatures are appropriate and buds develop slowly. In late winter the buds develop at an accelerated rate, in response to higher temperatures. Flower buds and vegetative buds break at about the same time, so there are no fully expanded leaves on the tree during bloom. Early-season growth of roots, shoots, fruit, and cambium depend on stored carbon reserves within the woody tissues of the tree. All of these “sinks” compete for a limited supply of reserves. Growing leaves and shoots are sinks until enough leaf area develops on a shoot for the shoot to become a net exporter of carbohydrates; in apple this occurs about 15 to 19 days after bud break (Johnson and Lakso 1986). Fruit growth competes with shoot growth because defruited trees produce more primary stems, more long primary stems, and more and longer secondary shoots than trees with a crop (Grossman and DeJong 1995c). Fruit also compete with trunk growth because trunk growth of an early-season and a late-season cultivar was reduced by the presence of fruit, but trunk growth was reduced more for the late-season cultivar. The sink strength of vegetative organs

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is sufficient to compete with the high sink strength of growing fruit because vegetative growth continued during periods of resource-limited fruit growth (Grossman and DeJong 1995c). Early-maturing cultivars partition a greater amount of dry weight to vegetative growth because there was a shorter period of competition between vegetative growth and reproductive growth (Grossman and DeJong 1995a). Maximum root growth for fruiting and non-fruiting trees occurred after shoot extension ceased and before leaf drop (Williamson and Coston 1989). Root growth apparently is a relatively weak sink, because root growth was low during times of rapid shoot growth. Cropping resulted in a temporary (about 4 weeks) decline in root growth during the last 3 to 4 weeks before harvest and for a short period after harvest (Williamson and Coston 1989). 2. Flowering. Flower bud initiation for the subsequent season commences about 60 days after bloom and continues for up to two months, depending on latitude. Flower bud differentiation begins at the lower nodes and progresses up the shoot as shoots increase in length. Dorsey (1935) reported that flower bud differentiation was first detected about four nodes from the shoot apex. Removing flowers or young fruit reduced the competition between vegetative shoots and fruit and increased the number of flower buds at the basal five nodes of the current season’s shoots (Byers et al. 1990). Not only did early fruit thinning enhance flower bud formation, but also the percentage of flower buds surviving a spring frost was increased and flower bud survival was negatively related to crop load the previous year (Byers and Marini 1994). Three weeks of shade during the period of 10 to 16 weeks after bloom also inhibited flower bud formation (Marini and Sowers 1990). 3. Fruit. Peach fruit growth, measured as fruit diameter, is traditionally divided into three stages (Tukey 1933; Chalmers and van den Ende 1975). The first stage is a period of rapid fruit growth from bloom to about 50 days after bloom, when the pits harden. Fruit growth during this stage is primarily due to cell division, although cell expansion and intercellular space formation begin about 24 days after bloom (Masia et al. 1992). The second stage varies in length depending on the maturity date of the cultivar, being very short (just a few days) in early cultivars, and much longer (up to two months) in late-season cultivars. This stage is characterized by slow diameter increase. Fruit dry weight continues to increase during the second stage due to endocarp development. Because the components of the endocarp have a high construction cost (Corelli-Grappadelli et al. unpublished), this is a time when the tree has a high demand for resources for the growing fruit. The third stage is a period of rapid fruit diameter increase as the mesocarp cells expand.

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This final stage is often called the “final swell” and lasts several weeks before harvest, depending on the time of ripening. Water stress during the final swell reduces fruit growth, regardless of crop load. Dry weight increase was reduced by water stress only on heavy-cropped trees, indicating that late-season water stress affects fruit hydration rather than resource availability when trees are adequately thinned (DeJong 1998). In a series of papers, Grossman and DeJong (1995a; 1995b; 1995c) identified periods of resource-limited fruit and vegetative growth in fruiting peach trees. For an early-maturing cultivar there was one period beginning during stage I, at about 3.5 weeks after bloom, and continuing through harvest (about 12 weeks after bloom). For the late-maturing cultivar, the first period also occurred from about 3.5 to about 12 weeks after bloom, and a second period occurred during the last 4 weeks of the final swell (18 to 22 weeks after bloom). Fruit exposed to resource limitations grew normally when resources became available, indicating that fruit growth caused by resource limitations was only temporary. The patterns of contribution of different leaves to the growth of the fruit during the season have been studied with 14carbon techniques (Corelli-Grappadelli et al. 1996). The extension shoot growing from the tip of a 1-year-old shoot was a very strong sink in the first four weeks after full bloom (WAFB), a time when fruit growth largely depended on reserves and, to a small extent, on carbohydrates produced by the axillary shoot (the lateral shoot growing off the same node bearing a fruit). The axillary shoots without fruit partitioned carbon only to the growing extension shoot tip. By four WAFB, the extension shoot began exporting to the fruits on lower nodes, while the axillary shoot continued to support fruit growth, but the axillary shoot without fruit did not support this growth. Only much later in the season (well after pit hardening) did this shoot contribute to the growth of the fruit. These findings underscore the importance of the axillary shoot for the growth of the fruit, which had been indicated by Manaresi and Draghetti (1915) and by Marini and Sowers (1994). This role of the axillary shoot was confirmed in specific fruit growth studies (Fig. 2.3). Fruits growing on the same node as an axillary shoot were 17% heavier at 60 DAFB than fruits growing on nodes without the lateral shoot. Carbon partitioning to growing fruit was also affected by crop load: active export of fixed carbon from the leaves to the fruit (CorelliGrappadelli and Ravaglia unpublished) was found during stage three of fruit development. In shoots with high crop load, more than 50% of the fixed carbon was translocated out of the labeled leaf within 24 hours. This amount decreased with decreasing crop load (Fig. 2.4). The carbon uptake in the fruits of the high crop load mirrored the export pattern of the leaves: most carbon was imported within 24 hours of labeling (Fig.

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Fruit weight (g)

30

With axillary shoot

20

10

Without axillary shoot

0 20

30

40

50

60

70

Days after full bloom Fig. 2.3. Growth of peach fruits, cv. Elegant Lady, as a function of the presence or absence of an axillary shoot on the same node bearing the fruit, during the first stage of fruit growth. Each point is the mean of a least 30 fruit. Treatment means differ at the 5% level of significance on each of the last three measurement dates.

14C remaining in the labelled leaves (%)

100 High Intermediate Low Average

80 60 40 20 0

0

2

4

0

2

4

6

8

10

12

6

8

10

12

14C Translocation to the fruit (DPM/g dm)

40 30 20 10 0

Days after labelling Fig. 2.4. Patterns of 14C label export from exposed peach leaves, cv. Elegant Lady, as a function of the crop load of the branch to which the exposed shoot was attached. Labeling occurred at the onset of the final swell of fruit development.

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2.4). An understanding of resource allocation throughout the season is critical to the development of techniques to suppress tree vigor, without reducing yield or fruit size. From about 12 to 18 weeks after bloom, resources, even on non-thinned trees, do not limit fruit growth. It seems that this may be the optimum time to suppress vegetative growth. Major increases in yield will probably require development of cultivars that partition a greater portion of resources into fruit rather than wood.

III. LIGHT MANAGEMENT Energy required for the growth of all green plants comes from sunlight and, like most C3 plants, the carbon exchange rate (CER) of peach leaves saturated at about 800 µmol·s–1·m–2 of photosynthetically active radiation (400 to 700 nm) (DeJong and Doyle 1985; Marini and Marini 1983). Whole-tree CER is saturated at about 1600 µmol·s–1·m–2 of photosynthetically active radiation (Giuliani et al. 1998). Specific leaf weight (the ratio of leaf dry weight to leaf area) was lower for shaded than for non-shaded leaves and can be used as a biological integrator of cumulative light exposure for a leaf until mid-season (Marini and Barden 1981). After leaves were exposed to a range of light levels for 18 days, specific leaf weight was linearly related to light level and CER was related to specific leaf weight, even when CER was measured under light-saturating conditions. The CER and specific leaf weight of leaves that were shaded for 18 days and then exposed to full sun for 26 and 4 days, respectively, were similar to non-shaded leaves (Marini and Sowers 1990). DeJong and Doyle (1985) found that leaf nitrogen content was related to the light environment of a leaf, and leaf nitrogen was reallocated from shaded leaves to more exposed leaves of the tree canopy. Their data indicate that the redistribution of leaf nitrogen is a means for maximizing whole-tree carbon gain. Apple yield per unit land area was linearly related to light interception (Lakso 1994; Robinson 1997), so it is critical for young orchards to fill their space quickly to capture light, but in mature orchards light penetration throughout the canopy must be adequate to maintain fruiting wood and to produce quality fruit. In the absence of similar data relating yield to light interception in peach orchards, but considering the reports by Grossman and DeJong (1998) and Giuliani et al. (1998), it seems reasonable to assume that peach yields are also related to the amount of light energy intercepted per unit of land area. Peach fruit quality is influenced by the amount of light intercepted by the fruit and the leaves near the fruit, which is influenced by the

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position of the fruit in the canopy. Critical light levels were identified for various aspects of peach fruit quality by shading portions of trees during the final six weeks before harvest (Marini et al. 1991; Marini and Sowers 1990) and by measuring light interception by fruit during the final swell (Lewallen 2000). Flore and Kesner (1982) also described critical light levels for various aspects of peach tree growth and fruit quality. These critical light levels are presented in Table 2.1. To obtain high yields, fruit orchards must intercept a high proportion of light, but light must also be distributed throughout the canopy at levels adequate to maintain fruiting wood and fruit quality. Levels of interception greater than 70% of available light have been reported for apple, but at such levels light distribution may be inadequate for continued high yields of quality fruit (Jackson 1980). Spurs of pome fruits require a certain level of light to remain fruitful, but leafy peach shoots must be exposed to adequate light to remain alive. Heavily shaded portions of peach canopies are devoid of fruiting shoots because they die during the late summer. Flower bud density was also positively related to light levels from about 50 to 100 days after bloom (Marini and Sowers 1990). Therefore, to maintain high production, light distribution in peach orchards is more important than in apple orchards. Light distribution patterns were reported for various fruit tree forms. In general, when light was measured through a horizontal cross-section of the canopy, light was distributed in a U-shaped pattern for Central

Table 2.1. A summary of critical light levels (% full sun) for various aspects of peach leaf function and fruit quality. Light threshold (% full sun) Parameter

Response to light

Flore and Kesner 1982

Marini et al. 1990 & 1991

Leaf size Leaf thickness Sp. leaf weight Max. CER Cold hardiness Fruit size Fruit color Soluble solids Flesh firmness Flower densityz

negative positive positive positive positive positive positive positive none positive

36 36 36 36 21 — 36 — — —

40 40 40 35 — 10 30 50 No response 23

z

Flower bud formation was most affected by shade during the period 50 to 100 days after bloom.

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Leader trees (Porpiglia and Barden 1980; Marini and Barden 1982), but light was distributed in a W-shaped pattern in Open-Vase type trees (Marini and Marini 1983). Regardless of tree shape, light penetration declined rapidly from the tree periphery towards the tree center and adequate light for high fruit quality was limited to a zone of about 1.5 m thick around the outside of the tree (Marini and Barden 1982; Kappel et al. 1983). Light levels were relatively high in the center of trees (Marini and Marini 1983) and following pruning or shearing of hedgerow systems in the summer (Kappel et al. 1983; Marini 1985a). Génard and Baret (1994) measured the spatial and temporal variation of light transmitted to shoots in peach trees. Some shoots were exposed to light almost all day, while other shoots were in sunlight very little. Well-exposed shoots were mostly located at the top of the tree and were relatively erect. Shoots located in the outer parts of the canopy were slightly but significantly more sunlit than others. About 30% of the shoots received < 30% of the incoming light. Light transmitted to the shoots did not depend on shoot compass direction. Drooping shoots were preferentially shaded by horizontal and erect shoots above and next to their position on the branch. Grossman and DeJong (1998) measured daily patterns of intercepted photosynthetic photon flux (PPF) for peach trees in four training systems in California. The intercepted PPF was relatively constant from 0900 to 1500 hrs for all training systems. The KAC-V (1196 trees/ha) was the highest density system and the Cordon system (919 trees/ha) had the most horizontal canopy, and both intercepted more light than the KACV (919 trees/ha), whereas the open vase (299 trees/ha) system intercepted the least light. The high-density KAC-V and Cordon systems intercepted nearly twice as much light as the Open-Vase system, but no system intercepted much more than 50% of the available light. Robinson and Lakso (1991) also found that Y-shaped apple trees intercepted more light than conical-shaped trees. More information is needed to determine the relationship between light interception and peach yield per ha over a wide range of light levels. Only then can orchard systems be developed that capture the optimum amount of light.

IV. PEACH ORCHARD SYSTEMS An orchard system is the combination of cultivar, rootstock, tree training system, and tree spacing. Because so many factors are involved, evaluating the impact of the individual components of a system is difficult. Training systems and spacing, for example, are tightly interwoven. It is

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impossible to compare an open vase to a Y-trellis at a common tree density because the size of the canopy for these two forms is very different. Tree spacing must be adjusted for the training system to fully exploit the potential profitability of a system. Therefore, comparisons are usually made with reference to orchard area, regardless of the training system/tree density involved. Another consequence of the interplay between the different factors involved in orchard design is that the environmental conditions (climate, soil, length of season), as well as economics, often limit the options available, leaving little room for experimentation. This is also true from a scientific point of view and may explain why there have been relatively few studies dealing with peach orchard design. In addition to the duration and expense of these trials, it is often difficult to train, manage and crop different systems with the same proficiency. The same applies to multi-location studies, particularly when the selected cultivars are unequally suited to the environmental conditions of the different locations. Experiences with international apple trials in Europe have shown this very clearly. Multiple-row layouts, for example, used in northern Europe or south Tyrol in Italy are not suited for vigorous sites where managing multiple rows are difficult (Palmer et al. 1989). Similarly, the vigorous triploid cultivar ‘Jonagold’ was poorly adapted to the high vigor, high light levels in Bologna, Italy where bearing was delayed and fruit quality was poor compared to many apple-growing districts in the world (Tustin et al. 1997). Cooperators in the NC-140 multi-location rootstock trials in North America also learned to adjust tree spacing to site vigor (Marini et al. 2000). Because of these considerations, it is difficult to evaluate orchard systems in a single analysis that is comprehensive of all the factors involved. It is therefore preferable to review the single main factors separately. A. Tree Forms Peach trees have been trained to four basic forms, but there are modifications of each. These modifications have in general been prompted by advancements in growing techniques, or the need to reduce costs in order to maintain profitability. For example, the widespread adoption of the so called “Potatura A Tutta Cima” (no-heading-cuts pruning), reported by Sansavini (1980) and Fideghelli (1990), was one of the turning points for the shift in Italy from the traditional to the more intensive and better producing Palmette. Extension specialists and researchers found that avoiding heading cuts during the training phase induced

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peach trees to start bearing one or two years sooner (Baldassari 1950; 1967). Earlier bearing also shortened the productive life of an orchard. In the intensive peach industries of southern European countries (Italy, Spain, France, and Greece), this is not considered a disadvantage because it is desirable to renew orchards with cultivars with improved fruit quality and that expand the harvest season. In Spain, for example, the introduction of new cultivars expanded the harvest season from May through June in the 1970s and mid 1980s to April through October at the beginning of the 21st century (Table 2.2, Borras Escriba 2001). Open-Vase or Open-Center trees have been most common in commercial orchards for more than 150 years (Cole 1849), but variations of the system evolved differently in different regions. Open-Vase trees in California, USA usually have three primary scaffold branches, each with two secondary scaffolds; mature trees are fairly upright and are about 4 to 5 m tall (Rizzi 1975). In eastern North America, Open-Vase and modified leader trees have three to six primary scaffold branches and bench cuts are used to develop low (2.2 to 3.2 m tall) spreading trees with tree densities of 220 to 550 trees per hectare. The Open-Vase, with about 500 trees per hectare, is the most important training system in Spain (Royo Diaz and Martinez Lopez 1992), France (Hugard 1986), and Greece (Tsipouridis 2003). In Spain, the variants of the Open-Vase include the “Vaso Italiano,” “Vaso de Plataformas,” and “Vaso Californiano.” The main difference is in the angle of the branches and the hierarchy of the secondary branches. Trees of the Italian vase are spaced more widely because the branches are trained less vertical and more horizontal. The “Vaso de Plataformas” has more

Table 2.2. Changes in cultivar composition of the Spanish peach and nectarine industry over the last three decades, expressed as a percentage of harvested fruit per month (adapted from Borras Escriba 2001). 1973–84 Month April May June July August September October

1985–90

1991–95

1997–99

Peach Nectarine Peach Nectarine Peach Nectarine Peach Nectarine — 43.4 54.5 1.0 0.3 0.2 0.6

— 13.4 69.9 16.4 0.3 — —

— 63.3 29.3 0.6 1.1 2.2 3.5

— 32.1 62.3 5.2 0.3 0.1 —

0.9 45.8 29.8 9.6 7.8 4.6 1.5

0.3 28.7 35.0 15.9 10.0 7.5 2.6

2.5 41.0 20.2 15.8 9.2 7.1 4.2

1.5 27.3 30.5 18.8 11.8 7.3 2.9

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upright scaffold branches (35 to 40° from the vertical) and each carries three tiers of secondary branches, up to four in the first tier and descending to two in the top tier. The height of the tree is about 3.0 m. The “Vaso Californiano” features three fairly upright scaffold branches (15 to 20° from vertical), each with two secondary scaffolds (Royo Diaz and Martinez Lopez 1992). In Italy, the Open-Vase has long been one of the most popular training systems, and even today it is second only to the Palmette (Sansavini et al. 2000). The most common vase is called “Delayed” because this tree is trained without heading cuts to stimulate the formation of the whorl of primary branches; only the top of the tree is headed above a high lateral in the winter after the first season. The goal is to weaken the leader, thus stimulating the lowest laterals to take over and naturally spread out and form the main whorl of branches. The leader is removed only after the third season, thus the name, “Delayed.” The number of branches retained may vary, but normally it is 5 to 6, arranged in two whirls. Tree density is about 550 trees per hectare. The vase is rather difficult to maintain low, within 2.2 to 2.5 m from the ground, and it is recommended mostly for low-vigor cultivar/rootstock combinations, or in low-vigor environments. Summer pruning is required during the whole life of the orchard to avoid excessive shading that pushes the vegetative zone out and up, in a doughnut shape. A variant of the vase that is sometimes used in Italy and Spain is the socalled “Forma Libera” or free-shape (Sansavini 1980; Royo Diaz and Martinez Lopez 1992). The tree is left totally unpruned in the first 3 to 4 years, which makes it very productive early on, but in severe need of reform pruning after this initial period. Because the tree develops a bushy appearance, very often it is pruned back to form a vase, which reduces yield. This is the main reason for its limited adoption. Y-shaped trees of several species have been grown for many years. In this training system, the leader is removed and only two primary scaffold branches are retained; they are trained to grow perpendicular to the row axis. Sometimes branches are oriented within the row to form narrow hedgerows referred to as the Parallel-V. The Y-system is suited to high densities. Reports of densities up to 2000 trees/ha exist in the literature, but most common densities range between 900 and 1500 trees/ha (Corelli-Grappadelli et al. 1986; Chalmers et al. 1978; Caruso et al. 1997; Caruso et al. 2003). Although Y-shaped trees had been grown for many years (Baldassari 1950), interest was rekindled by the potential for very high light interception (above 70%, Nuzzo et al. 2000; Corelli-Grappadelli, unpublished). A variant of this system is the socalled V, where trees are planted at an angle from the horizontal and alternated along the row to form a V-shaped canopy perpendicular to the

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row axis (Costa et al. 1989). Tree densities for this system can be quite high, reaching 2000 trees/ha (4 × 1.25 m). The Tatura Trellis (Chalmers et al. 1978) was developed for mechanical harvest of cling peaches, and scaffold limbs are supported with a wire trellis. The Kearney Agricultural Center Perpendicular-V (KAC-V), developed for hand harvest, is not supported (DeJong et al. 1994). Typical tree densities are 900 to 1200 trees/ha and trees are about 5.5 m tall. The M.I.A. trellis is a modification of the V-shaped tree. The A-shaped canopy is developed by orienting the leaders at 60° from vertical and leaning trees in adjacent rows towards each other. The Y-trellis has been adopted in Southern Italy with some modifications, including a wider angle between branches (45°, compared to 35° for the Tatura Trellis), which are allowed to converge and touch each other in the middle of the alley row (Caruso et al. 2003). This system has very high light interception, up to 70% at orchard maturity (Nuzzo et al. 2000), and has very high productivity. Full production yields reported by Caruso et al. (2003) average 67 t/ha per year from the third to the eighth year for “Venus”, a late-season cultivar grafted on the vigorous stock GF677. Plantings of Y-trellis are becoming more widespread in the peach-growing districts of southern Italy, where they are replacing Open-Center trees and Palmettes (Caruso et al. 2003). A version of the Y-trellis, proposed by Caruso et al. (1997) for low-chill early-season cultivars, is a variant of the meadow orchard concept proposed by Erez (1978), but for greenhouse cultivation. The goal was to restrict growth and retain productivity on small non-supported trees. This free-standing Tatura was dubbed the fsTatura by the authors, who adopted a pruning technique involving heading of all the one-year-old wood, above the most proximal lateral shoot. Trees were pruned immediately after harvest, early enough in the season to allow flower bud differentiation on the newly formed shoots, which bloomed and fruited the following season. By using vigorous rootstocks, such as GF 677, this cycle could be maintained. Yields in this system were high, because of the high tree density of 2000 tree/ha. The average for the first three harvest seasons was 18 t/ha, but the yield in the first fruiting season (the third year from planting) was 14 t/ha (Caruso et al. 1997). The Y-trellis is the system used in protected cultivation in southern Italy because this shape fits very well the structure of the tunnels used. In these tunnels, the support arches are set along the row, where there is no vegetation, and the dome of the tunnel is placed above the row-middle where the branches extend. Because tree spacings are reduced (4.5 × 1.5 m), tree densities are fairly high (about 1500 trees/ha), which favors precocity and higher yields. For ‘Armking’ nectarine on seedling rootstock in the Basilicata region of southern Italy, Fideghelli et al. (1988) reported

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yields of 5.0 t/ha in the second season, and up to about 30 t/ha at full production. Hedgerow systems are developed by planting trees fairly closely in the row, and trees can be trained to various forms to develop a solid wall of foliage. The most widespread hedgerow system is the Palmette, which was developed in Italy (Baldassari 1967). This system was more productive and less expensive than the traditional vase (Fideghelli 1969), and was ideally suited to the use of platforms for pruning, thinning, and picking, which greatly improved labor efficiency over the use of ladders needed for the vase. The Palmette is still the most widespread system in the Italian peach industry by a wide margin (Sansavini et al. 2000), although it is quite different than the original concept. Today’s Palmettes (“Free” or “Sprint” Palmette) are planted closer, with typical densities of 600 to 900 trees per ha, and trees are trained with summer pruning. The structure of the tree is rather “free”, meaning the best branches are retained irrespective of their position along the trunk. The angle of branch insertion is reduced, to allow closer spacing in the row. The number of branches is reduced, sometimes to one tier, which is grown out and up to occupy the space between adjacent trees. With the exception of Italy, the desired height, spread, and shape of hedgerows are often maintained with mechanical shearing during the summer (Hayden and Emerson 1988), but the resulting dense layer of foliage at the tops and sides of the hedge must be removed by selective dormant pruning to improve light penetration into the hedge. Central Leader. As the advantages of high-density plantings were being demonstrated with apple, a move towards higher densities occurred in peach as well, with the adaptation of the “Axis Central” to this species in France (Hugard 1981; Belluau and Lemaire 1986), and the introduction of ‘Fusetto”, or Free Spindle, in Italy (Bargioni et al. 1983). Both systems are suited for densities above 1000 to 2000 trees per ha. However, both systems tend to suffer from excessive shading and loss of bearing wood in the lower part of the canopy, particularly after 4 to 5 years from planting, and at the higher densities (Belluau and Lemaire 1986; Loreti et al. 1989). The trees have a single vertical leader and are conical in shape, and are about 3.0 to 3.5 m tall (Bargioni et al. 1983). The trees create a hedgerow, well suited to picking platforms. Both systems feature a leader, with no permanent branches. Fruiting wood is retained on short branches, which are renewed every few years. Since Central Leader trees are closer to the natural growth habit of peach than the Palmette, these training systems require less pruning during training, and their training is much easier. As a result, early yields are normally fairly high, which is their greatest advantage.

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B. Tree Form Effect on Yield Several researchers have compared yield for trees planted at the same spacing but trained to different shapes to evaluate tree performance. It is important to evaluate the inherent bearing potential of a training system, and especially its capacity for early fruit production. In the highly intensive orchards of the south European peach industries, precocity is considered very important. Often the training systems requiring the least initial pruning are most precocious and tend to have higher cumulative yields over the first 4 to 6 seasons. Many trials have demonstrated this advantage for more “natural” systems. The Free Shape, which is nearly nonpruned initially, the Fusetto and sometimes the Delayed Vasette all require less early pruning and are more precocious than systems such as the Palmette or the Y-Trellis (Bargioni et al. 1985; Bassi et al. 1985; Blay Coll 1988; Corelli-Grappadelli et al. 1986; Sansavini et al. 1980; Sansavini et al. 1985; Toribio Mancebo 1993). Many orchard systems trials demonstrated that the initial high yields of the aforementioned systems are temporary and as orchards age the yields are similar to other systems. Bassi et al. (1985) reported yields from an 8-year comparison of six training systems where, despite frost damage in two seasons, after the initial advantage of the Free Shape, yields tended to become equivalent across all the systems. Yields per tree, averaged over the six growing seasons, were highest for the Free Shape and lowest for the Regular and Free Palmette; yields for the three vase-derived systems were intermediate between the Free Shape and the Palmette. These results illustrate that training the tree into a given form can influence yield. The nearly nonpruned Free Shape was most productive early in the life of the orchard, whereas the Vase types or the Palmettes had relatively low early yields due to the pruning required for tree training. Later, as the trees occupied their allotted space, the Free Shape had to be contain-pruned to either a Hedgerow system or to a Vase, and the loss of a large portion of its canopy caused decreased yield. A similar situation exists with Fusetto, which is pruned very little initially, and is capable of high early yields, but excessive growth may cause shading, which reduces wood quality and productivity. In other studies, when trees were planted at the same density, the KAC-V and the Cordon systems produced similar yields per hectare (Grossman and DeJong 1998). When planted at low densities, Open-Vase trees had higher yields per tree, but lower yield per unit of land area under the canopy or per unit of canopy volume than did Central Leader trees (Marini et al. 1995). In another experiment, Central Leader and Open-Vase forms were compared at low density (370 trees per hectare)

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and at moderate density (740 trees per hectare) (Marini and Sowers 2000). The interaction between tree form and tree density was not significant, and tree form had little effect on cumulative yield. Allison and Overcash (1987) compared Central Leader trees to a Palmette Trellis system planted at 1292 trees/ha. Training system did not influence cumulative yield during the first four years. Menzies (1988) compared a Palmette Hedgerow to the Lincoln Canopy, both at 1000 trees/ha: after six years cumulative yield was about 25% greater for the Palmette system. Taylor (1988) compared six different training systems, all with 1680 trees/ha. Low temperatures eliminated the crop in the third year. Yields/ha in the fourth year, ranked highest to lowest, were: Open Vase > Modified Belgian Fence > Tatura Trellis > Perpendicular Fan > Parallel Fan > Central Leader. Results from a number of experiments generally indicate that training system has little impact on peach yield. In apple, Y-shaped trees were 11% and 18% more productive than trees trained as Slender Spindles and Palmette, respectively, and differences in yield were related to light interception, because yield per unit of light energy was similar (Robinson 1997). In agreement with this, Giuliani et al. (1998) found that whole-canopy photosynthesis of peach trees was linearly related to the amount of light intercepted by the tree, irrespective of the training system (Y-trellis, Sprint Palmette, and delayed Vase). The Y-Trellis intercepted more light, it also had the highest photosynthetic rates and, in this trial, it also had the highest yields over nine cropping seasons (Corelli-Grappadelli unpublished). Therefore, when training systems planted at the same density do not show much difference in yield, this should not be surprising if they efficiently fill the allotted space and intercept similar amounts of light. C. Tree Density Effect on Yield Conventional orchards are planned to fit the dimensions of mature bearing trees. As a result, trees require two or more years to fill their allotted space and for the orchard to attain maximum yields, even if the trees are not pruned to hasten their development. Several experiments were performed in which tree density, but not tree form, was varied. After five years for the KAC-V system, increasing the tree density from 919 to 1196 trees/ha (23%), increased cumulative yield/ha and cumulative number of fruit harvested per ha only 14% and 17%, respectively (DeJong et al. 1999). After nine years, when Central Leader or Open Vase tree densities were increased from 370 to 740 trees/ha (100%), cumulative yield and cumulative number of fruit harvested/ha increased only

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40% and 57%, respectively (Marini and Sowers 2000). Giulivo et al. (1984) grew peach and nectarine trees as free spindles at densities ranging from 1250 to 2000 trees/ha and found that yield/ha increased less than proportional to tree density. Hutton et al. (1987) compared three training systems, each at three tree densities and reported cumulative yield after eight years. The effect of tree density on yield varied with the training system. For the Palmette Hedgerow at 865 trees/ha, increasing the tree density by 40% or 100% resulted in increased yields of 38% and 84%, respectively. For Tatura Trellis, increasing the tree density by 45% or 95% resulted in yields 4% greater and 5% less than when trees were planted at 853 trees/ha. For M.I.A. Trellis at 1110 trees/ha, increasing the tree density by 48% or 100% reduced yields by 12% and 5%, respectively. In Texas, yields for Y-shape trees were positively related to tree density from 350 to 700 trees/ha (Reeder et al. 1980). In Ontario, Canada Central Leader (Fusetto) trees were compared at three tree densities (504, 775, and 1291 trees/ha) (Miles et al. 1999). Cumulative yield per ha for the first three years was slightly more than double for the highest-density trees than for the lowest-density trees. While testing the Fusetto at varying tree densities (1250, 1665, and 2500 trees/ha) in Italy, Bargioni et al. (1985) concluded that the density best suited for the environmental conditions (soil type and climate) of the Verona area in Northern Italy was 1665 trees/ha. The 2500 trees/ha had slightly higher yield, but only marginally, and was not economically justified. Since maximum orchard productivity cannot be attained until trees fill their allotted space, the larger that trees are allowed to grow, the farther apart they must be planted, and the longer it will take to reach full production. Tree training can also influence the length of time required to reach full production. With today’s Palmette, for example, trees are seldom headed back to stimulate branch formation, which is completely opposite to the guidelines of 30 years ago. The goal of planting higher tree densities, combined with minimal pruning, is to reap earlier and more abundant yields. Once trees fill the allotted space, the capacity for yield will be limited by the amount of light that can be intercepted. That is why in virtually all the trials there is a poor relationship between the cumulative yield increase and tree density increase, after the first few seasons. Results with apples are similar. In the international training systems trial, involving five European locations during the 1980s, Palmer et al. (1989) compared systems with densities ranging from 2667 to 8889 trees/ha, trained as single-, double-, and triple-row spindles and 6-row beds of full field minitrees. After six cropping seasons, the highest-density system, with 233% more trees/ha, produced only 38% more fruit.

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However, in the first cropping season (the year after planting), the highest-density trees yielded 14 to 20 t/ha, compared to 5 to 11 t/ha for the other systems. From the fourth season on, when the orchards were at full bearing, there were no differences in yield/year across all training systems. Training systems utilizing small trees are more conducive to high densities, and generally tend to have high early yields. Later on this advantage is lost and the risk of losing production due to excessive tree competition becomes a factor to be carefully evaluated. Because of the interaction between tree behavior with site environmental conditions, the ideal tree density will vary with site and training system. Regardless of training system, in most of the studies reported increases in yield were usually relatively small as tree densities increased above 1000 trees/ha. D. Effect of Tree Density Plus Tree Form on Yield As discussed above, the choice of training system dictates the spacing that can be used, and often it also defines the training strategy, i.e., the sequence of summer and winter pruning events that will lead to a fully developed tree. As a result, yield may be dramatically affected by the combination of these two factors. A number of studies have demonstrated this. Hayden and Emerson (1988) conducted one of the first high-density peach trials in North America. In 1969, they compared seven systems with tree densities ranging from 717 to 2392 trees/ha. Frost problems complicated their data, but yields in the third and fifth years were high as long as trees were grown in a hedge form and were maintained by summer pruning. Yields were highest for high-density Pillar (2392 trees/ha) and Belgian Fence (1794 trees/ha) and lowest for low-density Pillar (798 trees/ha); the other four systems had intermediate yields and were high-density Open Vase (717 trees/ha), 2-Scaffold Vase Fan (717 trees/ha), Modified Leader Fan (717 trees/ha), and Pillar (1196 trees/ha). Based on results from three trials, they felt that the ideal system was the flat fan tree wall, with a tree density of 500 to 750 trees/ha, 3.1 m tall, 1.2 m wide at the top, and 1.8 m wide at the bottom, maintained with summer shearing and dormant pruning (Hayden and Emerson 1988). Phillips and Weaver (1975) compared three systems for 9 years. During the first five years compared to Modified Leader (397 trees/ha), cumulative yield was more than double for Palmette trees (1157 trees/ha), and 67% higher for hedgerow trees (868 trees/ha). In the sixth year, yield was similar for all systems, and the Modified Leader trees were most productive in the seventh and eighth years. After nine years,

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cumulative yield was 100, 102, and 113 t/ha for Modified Leader, Hedgerow, and Palmette trees, respectively. Leuty and Pree (1980) continued this trial for another four years, and found that cumulative yields were related to tree density only during the first three fruiting years. After nine years, increasing the tree population from 397 to 1157 trees/ha (290%) resulted in only a 12% increase in cumulative yield/ha. Pruning and thinning costs were also related to tree density, and they concluded that the benefit of high density was mostly in the early years, but high density offered little economic advantage over the life of the orchard. Layne et al. (1981) compared three tree densities at three levels of irrigation for trees trained as Open-Vases. After seven years, cumulative yield increased as tree density increased from 266 to 536 trees/ha. Irrigation improved cumulative yield at high, but not low tree densities. Doubling the tree density increased yield by 75% for non-irrigated trees and 96% for irrigated trees. When four hedgerow systems were compared over a 10-year period, cumulative yields were 125, 111, 104, and 92 t/ha for Oblique Fan (567 trees/ha), Modified Central Leader (606 trees/ha), Canted Oblique Fan (969 trees/ha), and Open Center (381 trees/ha) (Kappel et al. 1983). After six years, Grossman and DeJong (1998) reported that annual clingstone yields of 75.5 t/ha for high-density KAC-V (1196 trees/ha), 56.5 t/ha for KAC-V (919 trees/ha), 53.7 t/ha for Cordon (919 trees/ha), and 41.2 t/ha for Open Vase (299 trees/ha). Menzies (1988) compared five orchard systems, and cumulative yields for six years were highest for Palmette Hedgerow (1000 trees/ha) and Tatura Trellis (2500 trees/ha), yields were lowest for Open Vase (500 trees/ha), and yields were intermediate for Lincoln Canopy (1000 trees/ha) and Central Leader (666 trees/ha). Hutton et al. (1987) compared three tree forms, each at three tree densities. Cumulative yields for the first eight years were highest for the M.I.A. Trellis (1110 trees/ha and 1646 trees/ha) and the Palmette Hedgerow (1732 trees/ha); yields were lowest for Palmette Hedgerow (865 trees/ha); the other combinations had intermediate yields. The optimum tree density appeared to vary with tree form and was 1732 trees/ha for Palmette Hedgerow, 1234 trees/ha for Tatura Trellis, and 1110 trees/ha for M.I.A. Trellis. Four orchard systems were compared for eight years in California (DeJong et al. 1992). The systems included the standard Open Vase with 298 trees/ha, Parallel V with 598 trees/ha, KAC-V with 909 trees/ha, and Central Leader with 909 trees/ha. During the first 2 cropping years the higher density systems had higher yields per ha, but yield was similar for all systems after the third growing season. They concluded that the

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Open Vase system has a physiological yield capacity similar to the Perpendicular V system at orchard maturity, but the two systems differ in their physical ability to support the crop. Open Vase trees required more support than the V-shaped trees and more limb breakage was still observed on Open Vase trees. They concluded that the practical advantages and disadvantages of the high-density systems are probably less related to crop yield than to orchard management considerations such as: tree structural strength, uniformity, access to ladder work, and simplicity of cultural operations. Light interception by Hedgerows can be fairly low because hedge width should be limited to 1.5 to 2.0 m to allow adequate light distribution throughout the canopy (Marini and Barden 1982; Marini and Marini 1983). As a result, more than half the orchard floor is devoid of trees. Stembridge (1977) tried to increase the amount of orchard floor covered with canopy by planting short Hedgerows arranged in a bed system. Compared to traditional Hedgerows, this increased coverage of ground by 50%. The individual Hedgerow had 5 trees oriented diagonally across the 2.3 m-wide beds to provide a row length of 3.7 m. Beds were separated by 3.05 m-wide drive middles to provide 1210 trees/ha. At planting, trees were inclined 45 degrees and oriented down the row to fill the space quickly. Yield the year after planting was 6.5 to 8.6 t/ha and 33.2 t/ha in the third year, compared to only 9.7 t/ha for the traditional orchard. Weed control was difficult in the Hedgerow system. The primary advantage of Hedgerow systems is that the orchard space is filled quickly and yields of young orchards are improved. DeJong et al. (1994) compared the KAC-V (909 trees/ha) with the traditional Open Vase system (298 trees/ha). Cumulative yields for the first three years were about 44 t/ha for the KAC-V and 24 t/ha for the Open Vase, but after eight years yields were 224 and 190 t/ha, respectively. Therefore, the increased yield due to high tree populations is temporary and the economic feasibility of such systems may depend on the cost of trees and the value of new cultivars where supply has not satisfied demand. The training strategy can have a large impact on productivity, especially in the critical early years. The move away from heading cuts demonstrates this. When Vase trees are trained with heading cuts, their initial yields are generally very low, but in the case of the Delayed Vasette, where the tree is left nearly intact initially, early yields are improved. In a comparison of five systems, Delayed Vasette planted at 727 trees/ha was compared to Fusetto and Y-Trellis trees each planted at 727 and 1454 trees/ha. The yield per tree in the second season was similar for the Delayed Vasette and Fusetto at 727 trees/ha, but all other systems had lower yields. The study was terminated after four years, due

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to tree mortality following a winter freeze, but through the third cropping season the Delayed Vasette still had high yields per tree. However, because of the planting density, this form had one of the lowest cumulative yields/ha for the three seasons. Cumulative yields per ha were 52.9, 64.4, and 50.1 t/ha for the Delayed Vasette, Fusetto, and Y-Trellis with 727 trees/ha, respectively. The Fusetto and Y-trellis at 1454 trees/ha had 96.1 and 77.3 t/ha, respectively (Corelli-Grappadelli et al. 1986). For most studies, the high yields associated with high tree density appear to result from early production, which most intensive systems stimulate, and higher number of trees per ha. This advantage may be lost over the life of the orchard, particularly if the orchard is maintained for more than 20 years. For this reason, the choice of training system may have less to do with tree performance than with the equipment on the farm, labor availability, proficiency in training the tree into a given form, the costs of establishing and maintaining various systems, and their impact on fruit size and quality. From this survey it is clear that, although early yields are of utmost interest, the overall performance of the orchard is of equal importance. Therefore, future trials involving training systems and tree spacing should be long-term studies, intended to provide information well past the 10th growing season of the orchard. E. Meadow Type Systems Trees in conventional orchards are spaced to accommodate mature trees. Yields are relatively low until the trees fill their space. As conventional orchards mature, the lower limbs often become less productive and produce low-quality fruit due to within-tree shading. Another shortcoming of traditional trees is that mature orchards are expensive to manage as the fruiting zone moves toward the top of the tree. The “meadow orchard” was conceived to produce vigorous shoot growth, with adequate light exposure, on short trees. The meadow orchard, originally developed by Hudson (1971), was an ultra-high-density orchard for apples intended for mechanical harvest by mowing the trees with their fruit as grass in a meadow. There were about 100,000 trees/ha, on dwarfing rootstocks, and full field cover was obtained with no alleyways for machinery. The tree was allowed to grow and induced to fruit on 1-year-old wood. The following year, the tree set fruit that ripened in fall. At harvest, the tree was cut back to a short stump. A new biennial cycle started in the next year, with a new vegetative flush. Theoretically, the two primary advantages for the meadow orchard are that the yields of young orchards would be high

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because the orchard space is filled quickly, and the fruiting zone would remain near the ground because the tree top would be periodically removed. The apple meadow orchard was not economical because apple trees cropped only every other year. Peaches seem better suited to a meadow orchard system for two reasons: (1) establishment costs are relatively low because peach trees can be produced from rooted cuttings (Couvillon and Erez 1980), and (2) peaches fruit on 1-year-old wood and may crop annually. Erez (1988) evaluated two variations of the meadow orchard in Israel. The “mechanized system” was developed for mechanized harvesting (Erez 1976; 1978). This system involved planting cuttings in winter and a single shoot was allowed to develop the following summer. When shoots were about 60 cm long, they were headed to induce thicker laterals. By the end of the season, tree height was about 1.3 to 2.0 m with many laterals. The second year trees may produce crops similar to mature orchards, especially for early-maturing cultivars. At harvest, the stem was detached to leave a short stump from which regrowth occurred and shoots were thinned to only one per tree. In areas with long growing seasons (4 to 5 months of growing conditions after harvest), early-maturing cultivars regenerated enough shoots with flower buds to crop annually and produce 3 to 4 kg/tree/year (13,333 trees/ha). Orchard longevity is not known, but one orchard cropped for 9 years. The 2 factors related to tree mortality seemed to be desiccation of the stump following tree harvest and nutrient deficiency. Mulching the trees with the shredded tree tops reduced heat stress, and nutritional problems were alleviated with continuous fertigation. Results with prototype machinery for harvesting trees and separating fruit from the trees were encouraging, but are probably too expensive for small-scale orchards (Couvillon and Erez 1980). A modified-mechanized system was tested in Georgia, USA (Couvillon and Erez 1982) with 9810 or 3924 trees/ha. Early-maturing, but not latematuring, cultivars regenerated enough flower buds for annual production. They also noticed that trees became deficient in several elements and constant fertigation was needed to alleviate the problem. Although yields were high for a young orchard, fruit size was too small for today’s markets; the percentage of fruit > 5.7 cm in diameter was only 12%, 46%, and 7% for ‘Redhaven’, ‘Loring’, and ‘Blake’, respectively. The second type of meadow orchard was called the “Intensive System” (Erez 1988). In this system, the tree was trained to 2 main shoots and each winter one of the two shoots was headed back to a short stump to allow regeneration of new growth and flower bud formation during the growing season. Therefore, each side of the tree fruited every second year. Compared to the mechanized system, the intensive system had bet-

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ter flower bud differentiation, fruit set, and yield per tree, especially for late-season cultivars. Although both systems should lend themselves to mechanization, commercial success with the meadow orchard will require new cultivars that are moderately vigorous, have an upright growth habit, have moderate flower density, and have fruit that ripen uniformly. Both systems require some type of summer pruning before harvest to improve fruit color. Optimum tree spacing for the mechanized system is probably about 1.5 to 1.8 m between rows and 0.6 m between trees within the row. For the intensive system, trees should be spaced about 1.5 m × 0.5 m. Although meadow orchard systems have been tested for nearly 30 years, for economic reasons, they have not been commercially adopted. Modifications of the meadow orchard were tested in Florida, USA with 3333 trees/ha, where trees were topped after harvest at 0.75 m above ground to leave the basal portion of scaffold branches (Young and Crocker 1982). This system allowed annual cropping and yields in young orchards were considerably higher than for traditional peach orchards (Crocker et al. 1988). Another alternative to encourage annual cropping was to cut alternate trees in the row after harvest (Evert 1988). In Sicily, a study was conducted on a commercial farm where Meadow Orchard trees were grown under greenhouse cultivation (Bellini et al. 2000). Tree densities were 5000 trees/ha for the Small Vase trees and 3300 trees/ha for Y-Trellis with ‘Maravilha’, a low-chill cultivar. Trees were highly productive: average annual yields during the first four seasons were 25 and 33 t/ha for trees trained as Y-trellis and Small Vase, respectively. The authors indicated that trees could be successfully grown at these very high densities, although maintaining a productive canopy required summer pruning several times per season, particularly with the more densely planted Small Vase. F. Protected Peach Culture During the Renaissance, exotic fruit, especially citrus, were grown in containers in European courts. One of the most famous was the citrus collection maintained over the centuries by the Medici family in Florence (Baldini 2001). The trees were grown outside during the summer, and moved into glass houses to avoid cold damage in the winter and spring frost (Brace 1904). Growing peach trees in containers allows fruit production on land that is otherwise unsuitable for fruit culture. Container-grown trees are also mobile and can be transferred to environmental conditions that are favorable for growth and fruiting in regions that would otherwise be unsuitable for peach production.

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Today, the goals of protected peach cultivation are to reap economic benefits associated with advanced ripening, or to extend the cultivation of peaches to areas of the world where it would be impossible to grow this species outdoors. Protected peach culture prevents winter injury and spring frosts, eliminates Cytospora canker disease associated with cold injury, allows marketing fresh fruit earlier in the summer than normal, allows production of cold-tender cultivars, and increases productivity per ha in regions where peach production is usually not profitable. Peach production in Ontario, Canada is limited to areas close to lake Ontario. Miles and Leuty (1988) attempted to expand the area suitable for peach culture by evaluating the feasibility of growing peach trees planted in the soil in a greenhouse. The house was maintained at about –5 to 7°C during dormancy. The house was cooled with ventilation during the spring, and then the walls of the house were removed to provide ambient climatic conditions. Three training systems were evaluated for four years, and the Tatura Trellis had the highest yields. Compared to similar trees in the field, yields were 40 to 80% higher in the greenhouse. Establishment costs were more than three times higher for protected culture, but due to higher yields and higher prices for early-season fruit, the protected culture system was more profitable than the standard system. Peach culture in Nova Scotia, Canada is marginally profitable due to low winter temperatures and short tree life associated with winter injury, and the growing season is short and cool. To evaluate the commercial feasibility of growing peaches, early-season peach cultivars were grown in large containers and were over-wintered in heated poly-covered houses (Crowe et al. 1987). Average annual yield was about 16 to 19 kg/tree from the third to the seventh year after planting. Although these yields are less than 30% of what would be expected of field-grown trees in traditional peach-growing regions, the system was considered to be profitable in regions where traditionally-grown peaches are normally not profitable. In southern Italy, commercial protected peach production began in the early 1970s (Sansavini 1974), and at that time the first research trials were established (Bellini et al. 1997). Today in southern Italy, apricot, peach, and table grape are grown in greenhouses. The greenhouses used for peach and apricot are normally plastic tunnels with the support arches placed in the row, and trees are trained to the Y-Trellis with tree densities of about 1500 trees/ha (Fideghelli et al. 1988). This training system lends itself quite well to the structure of the tunnel because the supporting arches are placed within the tree rows and the inter-row is free for equipment. The tunnels are covered after completion of the chill requirement, which is normally during January in southern Italy. Following closure of the tunnel, flowering occurs in early February and,

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depending on the cultivar, harvest commences in mid to late April. Thus, fruit can be harvested about a month earlier than in traditional orchards. Yields are satisfactory, especially considering the premium prices received for early fruit. Fideghelli et al. (1988) reported an average yield of 20.9 t/ha over the first four years for 'Armking.' In some areas of Israel, natural chilling is inadequate to grow most commercial peach cultivars (Erez et al. 1998). Erez et al. (1989) planted rooted cuttings in 25-L pots and trained the trees as trees in a meadow orchard. They demonstrated that container-grown trees could be placed in refrigerated rooms or transferred to cooler regions for a period of time to satisfy the chilling requirement. Upon attaining adequate chilling, trees could also be placed in greenhouses to advance maturity and take advantage of high prices for early-season fruit. Yields in this system were 20 to 30 t/ha. Although these systems are feasible, they have not been commercially accepted for economic reasons. In southern Italy, low-cost non-heated PVC-covered tunnels are used because the environmental conditions allow for sufficient natural heating of the greenhouses. If this were not the case, the cost of heating would totally offset the economics of this type of cultivation. In areas where heating is required, the economic feasibility of protected peach culture may depend on the price of fuel to maintain trees at appropriate temperatures. Interest rates on the capital required to build protective structures and the price and availability of imported fruit from other regions may also impact the profitability of these systems. G. Economics of Peach Orchard Systems The success of high-density apple plantings has prompted researchers to evaluate various high-density peach systems. It is difficult to find good data for mature high-density peach plantings and few researchers have reported data from which the profitability of various systems can be compared. Due to the scarcity of data, the discussion of this crucial subject is very brief. Marini et al. (1995) first published the economic impact of different tree forms in Virginia, USA. When planted at low densities, Open-Vase trees had higher yield and crop value per tree, but lower yield and crop value per unit of land area under the canopy or per unit of canopy volume than did Central Leader trees. In another study, Central Leader and Open-Vase trees were compared at two densities (Marini and Sowers 2000). After nine years, cumulative yield was highest for highdensity trees (700 vs. 350 trees/ha), but cumulative yield was not affected by tree form. Income minus costs for the nine years was about $4,200/ha higher, and net present value was about $2,200/ha higher, for

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Open-Vase than for Central Leader trees. Cumulative net present value for the nine years was about $2,660/ha higher for high- than for low-density trees. In California, four spacing/training-systems were compared with a clingstone peach for five years (DeJong et al. 1999). The four systems were: high-density KAC-V (1196 trees/ha), KAC-V (919 trees/ha), Cordon (919 trees/ha), and Open Vase (299 trees/ha). The Cordon system had the highest yield in the second year, but the V systems had the highest returns after five years. Mitchell and Chalmers (1983) did not perform an economic analysis of their study comparing Central Leader trees planted 2.0 × 1.0 m, 4.0 × 1.0 m, and 2.0 × 1.0 m with removal of alternate rows after five years to give a final spacing of 4.0 × 2.0 m. Canning yield/ha was highest in years 2, 3, and 4 for 2.0 × 1.0 m; yields were similar for all densities in the fifth year; and yield was higher for the 4.0 × 1.0 m plots in the sixth year. Cumulative yield for the six years was 21 t/ha more for the higher-density system. If one assumes a wholesale price of $234.58/t and a wholesale price for trees of $5.00/tree, the cumulative crop value minus the cost of trees is $2,426/ha higher for the high-density system. However, if additional costs for pruning and fruit thinning, and the time value of money were taken into account, the differences in net profit would likely be less. Although high-density peach orchards produce high yields, more conclusive economic data are needed before intensive orchard systems can be recommended over traditional Open-Vase systems.

V. VIGOR-CONTROLLING METHODS FOR PEACH TREES Through the years, a number of rootstocks less vigorous than seedling, such as Damas 1869, Saint Julien, GF 665-2, MRS2/5, PSA5, and PSA6, have been tested, but none has provided the same type of vigor control as dwarf apple rootstocks. Because of this, peach orchard intensification is challenging. As peach trees age, fruiting in the lower portion of the canopy is limited by shade and intensive tree management is required to prevent the fruiting zone from moving higher above ground. Several orchard practices have been used, with varying degrees of success, to suppress tree vigor in intensive peach orchards. Below is a brief description of some of these techniques. A. Root Restriction Peach trees exhibit a functional equilibrium between the roots and shoots (Richards 1977, 1986; Richards and Rowe 1977). Vegetative growth was directly proportional to the soil volume of the roots (Tan and Buttery

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1986), whereas fruiting was inversely proportional to the soil volume (Richards 1986). Williamson et al. (1992) evaluated two methods of restricting tree growth in a high-density peach planting (5000 trees/ha). Planting in fabric-lined trenches or narrow herbicide strips reduced shoot diameter and length, and flowering was increased in fabric-lined trenches, but not narrow herbicide strips. Trees in fabric-lined trenches quickly filled their space and developed many of the desirable characteristics of trees on dwarfing rootstocks. Although this method of controlling vegetative growth by restricting root growth appeared promising, the experiment was terminated after only four years, and the evaluation of this approach should be evaluated until the orchard is mature. B. Deficit Irrigation Researchers have been able to partially control assimilate partitioning with judicial irrigation. Chalmers et al. (1981) and Mitchell and Chalmers (1983) developed the concept of regulated deficit irrigation (RDI) for peaches and pears. By applying less water than the plant used at certain times of the season, plant water stress was temporarily induced, which suppressed vegetative growth without reducing fruit growth and yield. They identified an interaction between tree density and irrigation. Depending on the year, when trees were planted 2 × 1 m, partial irrigation during stage I suppressed trunk growth 11% to 18% and partial irrigation during stages I plus II suppressed trunk growth 1% to 11% without adversely affecting average fruit size or yield. When trees were spaced 4 × 1 m, trunk growth was reduced 8% to 30%, and yield was reduced by 6% one year and it was increased by 30% the other year. Proebsting et al. (1989) also found that the effect of restricted irrigated soil volume for apple was similar to that of deficit irrigation. When deficit irrigation was terminated, shoot growth resumed at rates above those of trees with non-deficit irrigation. Deficit irrigation probably has little potential in humid regions where soil moisture cannot be easily controlled. Deficit irrigation has not been widely adapted commercially because the results have usually been disappointing. C. Summer Pruning The world literature on summer pruning of apple and peach trees was summarized in a review by Marini and Barden (1987), so this discussion is a synopsis of how summer pruning affects peach tree growth and fruiting and how summer pruning might be used in intensive peach orchards. Summer pruning has traditionally been thought to induce fruiting, while dormant pruning induces vegetative growth (Saunders 1863; Tukey

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1964), but there are few research data to support these beliefs. Unfortunately, many summer pruning experiments included a non-pruned control rather than a dormant-pruned control, so there are few direct comparisons of pruning trees in the same manner but at different times of the year. Summer pruning removes foliage during the summer, and theoretically reduces the amount of reserve carbohydrate available for earlyseason growth the following year. Although summer pruning reduced late-season root and trunk growth, and reduced the concentration of nonstructural carbohydrates in the bark, shoot extension the following season was as great or sometimes greater than when trees were dormant pruned (Marini and Barden 1987). Since shoot extension, and not trunk enlargement, causes tree crowding and shading in intensive plantings, summer pruning cannot be used to restrict shoot growth. Early-season summer pruning or shearing, before shoot extension ceased, temporarily improved light penetration into the tree canopy. Late-season summer pruning, after shoots had ceased growing, improved light penetration into the canopy for the remainder of the season (Kappel et al. 1983). Summer pruning peach trees during the final swell sometimes improved red color development, but also reduced fruit size and fruit soluble solids concentration. The influence of summer pruning or shearing on yield and fruit quality seems to vary with cultivar and time of treatment. Published data do not conclusively indicate that summer shearing is preferable to winter shearing in various orchard systems. Summer shearing was originally considered by some as a component of peach Hedgerow and meadow orchard systems management to eliminate vigorous, nonproductive, upright shoots and to allow adequate light penetration for the production of high-quality fruit (Chalmers et al. 1978; Young and Crocker 1982; Erez 1982; Hayden and Emerson 1979, 1988; Horton 1985). Some type of summer pruning is generally required for intensive peach orchards to avoid losing fruiting wood in the lower portions of the canopy. Walsh et al. (1989) suggested that shearing at the onset of pit hardening plus reduced irrigation following harvest might be used to suppress vegetative vigor of early-maturing cultivars. This strategy has merit because flower bud formation on peach shoots requires light from about 50 to 100 days after bloom (Marini and Sowers 1990) and this timing would coincide with a time of non-resource limited fruit growth (Grossman and DeJong 1995b). Summer pruning within 3 or 4 weeks before harvest sometimes improves fruit red color development (Marini 2002b). Therefore, summer pruning for color improvement would be too late to improve flower bud development, except for early-maturing cultivars. Summer removal of vigorous upright shoots that shade the tree center should be a standard practice for all vig-

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orously growing peach trees, regardless of tree spacing, to maintain fruiting wood in the lower portion of the canopy (Marini 2002a). Summer pruning is widely used in intensive commercial orchards in Italy, particularly while training the trees, when trees are normally summer pruned more than once per year. Corelli-Grappadelli et al. (1986) reported times required for winter and summer pruning for five training systems at two tree densities. In all cases, summer pruning required more time (up to 5 times as much) than winter pruning in the second year, when most of the tree training was accomplished. Only from the third year, and not for all forms, did winter pruning take more time. For systems such as Fusetto and Delayed Vasette, summer pruning is a recommended practice. Summer pruning becomes increasingly important as the trees age, to avoid losing bearing wood in the lower parts of the tree. Normally pruning is performed after the cessation of shoot growth in late June. For reasons already mentioned, it may have controversial effects on tree performance. D. Plant Growth Regulators For several decades, pomologists have been searching for plant growth regulators to suppress shoot extension and increase cropping or fruit size. Paclobutrazol and flurprimidol are two gibberellin biosynthesis inhibitors that showed great promise for suppressing shoot extension and enhancing peach fruit size (Marini 1986, 1987), but the materials were not registered for edible crops in the United States. There are currently no plant growth retardants registered for commercial peach production in North America. E. Tree Growth Habit One of the challenges with developing new training systems for peach is that the same standard vigorous tree type on a vigorous rootstock must be adapted to all systems. In high-density systems, severe pruning is required to allow adequate light penetration throughout the canopy to maintain a relatively low fruiting zone. Severe pruning induces vigorous growth, and the resulting shade can adversely affect fruit quality and subsequent flower bud formation. Summer pruning can temporarily help alleviate the shade problem, but it does not suppress vegetative vigor and there may not be an economic benefit. Until dwarfing rootstocks or cultivars with different growth and fruiting characteristics are available, researchers and producers will continue to “fight” the natural growth habit of the tree while trying to make it fit a desirable system. There is a great diversity of growth habits within peach, and breeders

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in the United States and Italy have been cooperating to develop new cultivars with a range of tree growth habits that may be suitable for different training systems. There are six distinct naturally occurring growth habits and these can be hybridized to develop intermediate types (Scorza 1984). Peach breeders are attempting to develop different tree forms that produce fruit with commercial quality. Before these different tree forms become commercially important, breeders will have to work with pomologists to develop appropriate training and pruning systems for each form. The six growth forms can be grouped into three horticultural classes (Bassi et al. 1994). The “standard” class consists of standard, dwarf, semidwarf, and spur-type, which are similar in shape with only small differences in height and overall architecture. The second class includes upright and columnar because both have upright canopies. The third class contains the weeping growth habit. A brief description of the tree forms follows. Standard—Commercial peach production relies solely on standard trees with 1-yr-old fruiting branches, moderately strong apical dominance, and vigorous acropetal growth. Dwarf—There are two types of dwarf trees, which usually are less than 2.5 m tall. The “brachytic” dwarf has very short internodes, long leaves, and a dense canopy. High fruit quality brachytic dwarf cultivars were released (Hansche 1989), but the dense canopy presents problems and may not be suitable for commercial production (DeJong and Doyle 1984). Another type of dwarf (A72) was reported by Monet and Salesses (1975) in France, but has received little attention. At this time the fruit quality is poor, but the canopies are more open than the brachytic dwarfs. Compact—Compact trees have relatively short internodes, wide branch angles, and more and longer laterals than standard trees. The trees are smaller than standard, but the canopy is dense. ‘Com-Pact Redhaven’ is an example of a compact cultivar. Spur-type—Peaches with spur-type growth habit have been imported into the U.S. and some are apparently peach-almond hybrids. These trees are not dwarf or compact and there are no commercial cultivars available. Weeping—Weeping peaches have been released as ornamentals. Two breeding programs in Europe are developing commercial fruit quality weeping peach cultivars and this growth habit may be suitable for new training systems. Columnar—The columnar or pillar peach was first developed in Japan as an ornamental. Non-pruned trees grow about 4.5 m tall and about 1.7 m in diameter. Trees have very narrow branch angles and breeders are rapidly improving the fruit quality. Spacing trees about 2 m in the row can rapidly form a tall narrow Hedgerow.

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Mixed growth trees—Hybridizing the naturally occurring growth habits produces new tree types. The “upright” tree is a combination of the columnar and standard forms and is similar to the standard form, but branches tend to grow more upright; this form may have potential in high-density production systems.

VI. LIMITATIONS TO HIGH PEACH YIELDS Yields of mature peach orchards were generally lower than yields of mature apple orchards. Currently, the average yields in the U.S. are only 9 to 10 t/ha for freestone peach, whereas average yields for apple in the U.S. were 18 to 22 t/ha (Scorza et al. 1999). The 10-year average yield (1992–2002) in the more intensive southern European peach-producing countries, was 14 to 18 t/ha (FAOSTAT 2003). In high-density orchards, apple yields of 46 t/ha were not unusual, whereas peach yields rarely exceeded 33 t/ha with quality fruit. One reason for low peach yields in some regions is because yields are reduced by low temperature injury. Another reason for low freestone peach yields is the requirement for aggressive crop load management to obtain large fruit, but clingstone yields of 70 t/ha have been reported in California (DeJong et al. 1999). Yet another reason for low peach yields may be that peach trees partition a relatively low proportion of resources into fruit. Trunk crosssectional area (TCA) is related linearly to aboveground dry weight and fresh weight of apple trees regardless of rootstock (Barden and Marini 2001; Westwood and Roberts 1970). Pomologists use several indices to express carbon partitioning by trees. The most common index of partitioning is “yield efficiency” (YE) and is expressed as yield (kg/tree) per cm2 of TCA or cumulative YE (cumulative kg/cm2 TCA). YE is useful for comparing treatments within an experiment, but not for comparing trees of different ages or different orchards. When trees have filled their allotted space, annual pruning is used to limit canopy size, but trunks continue to enlarge. Values for YE decline each year in mature orchards because yield (the numerator) is fairly constant each year, whereas TCA (the denominator) increases each year. Most likely the reason that YE is so commonly reported is because it is easy to measure, but values for YE must be interpreted cautiously. The amount of fruit produced per land area covered by canopy or yield per unit of light intercepted may also be calculated. “Harvest Index” (HI) is the yield divided by the above- or above- plus below-ground portion of the tree (kg/kg) on a dry weight basis. Other times crop/scion ratio (C/S) is reported and it is calculated as the cumulative yield/tree divided by weight of the scion (kg/kg) on a

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fresh weight basis (Barden pers. comm.). Unless the weights of wood removed by pruning are reported, HI and C/S ratio may have similar limitations as YE in mature orchards. A. Rootstocks Affect Partitioning Although YE is not ideal for comparing partitioning in different studies, YE is the only index of partitioning that is widely available in the literature. For mature freestone peach trees in the eastern U.S., YEs of 0.3 to 0.8 kg/cm2 are typical (Marini 1985b; Marini 2002b), whereas values of 0.4 to 1.4 are common for mature apple trees on vigorous rootstocks (Elfving and Schechter 1993; Marini et al. 1994; Forshey et al. 1983). In a multi-location rootstock trial, cumulative yield efficiencies ranged from 0.19 to 2.12 kg/cm2 for 7-yr-old own-rooted freestone peach trees (Perry et al. 2000). In that trial, Citation, GH 655-2, and Damas-1869 produced small trees and GF- 677 and Halford produced the largest trees. Average cumulative YEs for 7-yr-old trees were 0.88, 0.87, 1.01, 1.05, and 1.13 kg/cm2, respectively, for Citation, GH 655-2, Damas-1869, GF-677, and Halford. In a similar multi-location apple rootstock trial, average cumulative YEs for 10-year-old apple trees were 1.34, 2.73, and 3.34 for trees on seedling, the semi-dwarf M.26, and the dwarf B.9 rootstocks, respectively (NC-140, 1996). YE for 10-yr-old trees on seedling rootstock ranged from 0.49 to 2.55 kg/cm2 (NC-140, 1996). Although location greatly influenced YE, cumulative YEs for 10-yr-old ‘Gala’ apple trees, averaged over 6 locations, was 1.0 for the relatively nonproductive semi-dwarf P.1 and 3.3 for the very dwarfing M.27, respectively (Marini et al. 2001b). In summary, cumulative YEs for peach and apple on vigorous rootstocks seem similar. However, dwarfing rootstocks tend to partition resources into fruit rather than wood for apple, but not for the peach rootstocks that have been evaluated. For apple, cumulative YE tended to be negatively related to TCA, but for peach cumulative YE tended to be positively related to TCA. Reasons for this discrepancy are unknown, but this could be an important area for future research. Based on experiences with apples, many pomologists have assumed that dwarfing peach rootstocks would have higher YEs. Apparently, this assumption may not be valid. B. Scion Affects Partitioning A second factor that could affect partitioning is the scion cultivar. There are few published reports for peach where YE is reported for more than one cultivar in an experiment. Marini (1985b) reported YEs of 0.2, 0.4,

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0.5, and 0.3 kg/cm2 for 5-yr-old ‘Redhaven’, 7-yr-old ‘Cresthaven’, 9-yrold ‘Loring’, and 15-yr-old ‘Sunqueen’ trees, respectively. Grossman and DeJong (1995c) reported the ratio of the dry weight of fruit per tree and the trunk radial increment for the season. Based on these data, the ratio of fruit dry weight (kg/tree) to mm of trunk growth was 0.43 and 2.76 for the early-maturing ‘Spring Lady’ and the late-maturing ‘Cal Red’, respectively. YEs of apple have drastically improved by growing spur-type strains on dwarfing rootstocks. The cumulative YEs for 18-yrold apple trees was influenced by both scion growth habit and rootstock (Barden and Marini 1999). Non-spur ‘Red Prince Delicious’ had YEs only 88% as high as the ‘Redchief’ spur-type strain; trees on the vigorous MM.111 rootstock had YEs 60% as high as trees on the dwarfing M.9. The cumulative YE for ‘Redchief’/M.9 was 6.4, whereas the cumulative YE for ‘Red Prince’/MM.111 was only 3.4. The data of Grossman and DeJong (1995c) indicate that a major reason for the relatively low YEs for peach may be the length of time from bloom to harvest. TCA is typically measured after leaf fall, and trunk growth rate increases after peach harvest, so peach might be expected to have low YEs. To obtain large fruit, early-season peaches must be thinned to low crop loads. However, compared to apple on dwarfing rootstocks, even the YEs reported for the late-season peach cultivars are relatively low. C. Tree Spacing Affects Partitioning Trees planted close together compete for water and nutrients and tended to have smaller trunks than trees in low-density plantings. The effect of tree density on YE was inconsistent. Cumulative YEs were 0.38 and 0.61 kg/cm2 for 9-yr-old ‘Norman’ trees planted at 370 and 740 trees/ha, respectively (Marini and Sowers 2000). Grossman and DeJong (1998) reported that YE (dry weight of fruit) for ‘Ross’ cling-stone peaches was not influenced by spacing V-shaped trees at 919 vs. 1196 trees/ha. The 30% difference in tree density may have been too small to influence YE. YE of 6-yr-old ‘Suncrest’ peach and ‘Redgold’ nectarine declined linearly as density of spindle trees increased from 1250 to 2000 trees/ha (Giulivo et al. 1984). However, Chalmers et al. (1981) reported that YE of 4-yr-old peach trees planted at 4166 trees/ha was 0.43 and YE of trees planted at 2500 trees/ha was 0.34. The effect of tree spacing on partitioning may be influenced by cultivar, climate, or tree age. YE in the experiment performed by Chalmers et al. (1981) showed an interaction between season, irrigation, and tree spacing. During the third year, YE was higher for highdensity trees when trees received deficit irrigation during Stage I or during Stages I & II. However, during the fourth year, YE was significantly

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higher for high-density trees only when trees received deficit irrigation during Stages I & II of fruit growth. More data, from experiments designed to compare tree spacing without differences in tree training, are needed before we will understand how tree spacing influences partitioning. D. Training System Affects Partitioning Training system did not influence YE of peach (Grossman and DeJong 1998; Marini and Sowers 2000). Although tree density varied with system, apple YEs were 2.9 and 3.9, respectively, for 10-yr-old ‘Empire’/M.9 trees when trained to the Slender Spindle or Vertical Axe system, respectively (Marini et al. 2001a). Cumulative YEs for ‘Empire’/Mark were 3.42 (2460 trees/ha), 3.93 (1561 trees/ha), and 4.33 (1111 trees/ha) for Slender Spindle, Vertical Axe, and Central Leader trees, respectively. Robinson and Lakso (1991) and Robinson et al. (1991) compared YTrellis, Slender Spindle, and Central Leader systems for apple. They reported that cumulative yields were correlated to the amount of light intercepted (Y-Trellis > Slender Spindle > Central Leader). When light interception was used as a covariate, the ranking for yield was unchanged, but differences between systems were no longer significant at the 5% level. The Y-Trellis had the highest YE and was the best system for converting light energy into fruit. The differences in yield between orchard systems were largely the result of differences in light interception. Besides differences in light interception, apple orchard management systems could differ in the use of intercepted light energy. Further research is needed to determine if the same is true for peach and to elucidate the physiological bases for these differences. Another way to evaluate partitioning is by calculating the harvest index, which is the ratio of crop weight to tree weight, and is usually reported on a dry weight basis. Apple trees with a light (60% of the previous season’s crop) crop produced 0.22 kg of fruit per kg of wood on a dry weight basis (Forshey et al. 1983) and nonthinned apple trees produced 0.33 to 0.48 kg of fruit per kg of wood, depending on rootstock (Strong and Azarenko 2000). Values of 0.34 and 0.11 were reported for peach trees that were not thinned or thinned to a commercial crop, respectively (Miller and Walsh 1988). Barden and Marini (2001) reported that the cumulative crop-weight-to-final-scion-weight ratio (C/S) of 17yr-old apple trees varied widely with rootstock, but much less with cultivar and strain. Trees on the dwarfing M.9 rootstock had a C/S ratio of about 15, indicating that the average annual production of fruit for each of the 14 fruiting years was equal to the final scion weight. For the more vigorous M.7 and MM.111 rootstocks, the annual yields of fruit were equal to about 50% of the final scion weights. Based on these types of

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data, the partitioning of nonthinned peach trees is similar to apple trees on relatively nonproductive rootstocks; but when trees are thinned to a commercial crop load, peach trees partition less resources into fruit than apple trees. Based on the data of Grossman and DeJong (1995a), where an early-season cultivar had less fruit/wood than the latematuring cultivar, it may be unrealistic to expect peach trees to have harvest indices similar to apple because peaches mature earlier than most apple cultivars. Following harvest, most peach cultivars have more time before leaf fall to produce wood than most apple cultivars. Resource partitioning is influenced by location, scion cultivar, rootstock, cultural practices, crop load, and training system. The most efficient cultural practices and training systems for peach at various locations have probably been identified, but partitioning efficiency for peach remains relatively low, compared to apple. Partitioning efficiency and yields per unit land area in peach seem to be limited by genetic factors. Dramatic increases in apple yields have resulted from growing efficient cultivars on efficient dwarfing rootstocks, and training systems have been developed to take advantage of these characteristics. Major improvements in peach yield will probably not occur until new genotypes for scions and rootstocks are developed that result in more efficient partitioning of resources into fruit. Scorza et al. (1986) compared the dry matter distribution in 3-yr-old limbs of peach trees with four growth habits. The percentages of dry weight partitioned into fruit were 56%, 53%, 38%, and 45%, respectively, for standard, semi-dwarf, compact, and dwarf trees. Although none of these tree types were more efficient than the standard, these data indicate that partitioning can be influenced by growth habit and peach breeders should continue to search for growth habits with efficient partitioning characteristics.

VII. FUTURE TRENDS AND DIRECTION Researchers and commercial producers have extensively evaluated peach orchard systems. Unless new cultivars, rootstocks, or plant growth regulators become available for controlling tree vegetative growth, future orchards will consist of low or moderate tree densities. The two most common tree training systems are the Open-Center in the western hemisphere and the Palmette in some European countries. These training systems will continue to dominate commercial orchards because alternative systems have not proven consistently more profitable. The choice of training system will be determined by factors such as the cost and availability of land and skilled labor, and ownership of previously purchased materials and equipment. In developing countries

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and North America, where land is available and relatively inexpensive, simply planting more land can enhance farm income. In Europe, where new orchard land is largely unavailable, increasing the farm income requires increased returns per unit of land area or per unit of input. In the future, peach orchard systems will likely evolve differently in different parts of the world and economic pressures will drive technical solutions to production problems. Most developing countries with peach industries are located in the southern hemisphere and farmers obtain high wholesale prices for fresh fruit exported to developed countries during their off-season. Both land and labor are widely available and inexpensive, but labor is unskilled. Tree uniformity within an orchard will facilitate standardizing orchard operations performed by nonskilled labor. Orchard systems will evolve slowly unless economic conditions change. Peach trees are easily trained to the Open-Center system and this system will continue to predominate because there is little incentive to obtain high early yields or to make more efficient use of land or labor. More vigorous rootstocks, such as GF667, may become more common as old orchard sites are replanted. Small orchards dominate the peach industry in most of Europe and orchard owners do much of the routine work; in the larger operations, highly skilled resident immigrants and experienced migrant labor are increasingly employed. Farmers must perform most of the orchard operations because labor is very expensive. Land and labor are already being used efficiently, but there will be increasing economic pressure to further improve efficiencies. Intensive orchard practices, performed by highly skilled labor, will be required to improve early bearing and yields per unit of land area. Minimally pruning young trees is but one example of the modern techniques employed to obtain early production. Summer pruning will be used to obtain high-quality fruit and maintain fruiting wood in the lower canopy, as well as to spread out the pruning labor by performing some of the pruning during the growing season. In France, this quest for efficiency can be represented by the concept of “supervised productivism” (productivisme raisonné, Giauque, 2001): devising a system of evaluation of the performance of an individual orchard (in terms of labor used per unit of sellable product) against the best orchard’s and the average values for a given production district. Interestingly, these studies reveal that high yields and high quality can coexist and are not antithetic. Early bearing, high yields over the life of the orchard, and frequent orchard renovation to take advantage of new high-quality cultivars will be necessary, in an economic scenario that is already characterized by high costs and diminishing returns. One of the consequences is that, in many cases, to a large extent the choice of a training system can be

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influenced by the equipment that is on the farm. In the main peach district of Italy, the Romagna region, many farmers have purchased expensive platforms to reduce the cost of orchard operations, such as pruning, fruit thinning, and harvest. Very often these farmers maintain their orchards as Palmettes, to extend the returns on the investment in the platform (these will easily exceed 25 years of operation with normal maintenance). Trees in Palmette systems are typically supported with three or four wires attached to concrete posts, and these posts can be reused as orchards are renovated. Therefore, in Europe, barring new breakthroughs in habitus, pruning, or training techniques, the future trend appears more likely to be one of improving efficiency of existing orchard systems by tweaking the management practices, more than adopting radically different orchard designs (unlikely from current developments in other crops, such as apple). Peach growers in western North America grow mostly fairly upright trees that are 4.0 to 5.0 m tall, and planted at about 300 trees per ha. North American orchards are relatively large and workers are unskilled. Therefore, trees within an orchard will have to be uniform to facilitate orchard worker training. The cost of labor is increasing rapidly and California growers are starting to lower their trees. As land and labor become increasingly scarce and expensive, peach orchard systems likely will evolve towards those found in Europe. Some type of Hedgerow system that allows use of platforms may dominate the peach industry, and where platforms are not used, tree height will be limited to less than 3.0 m. At higher latitudes, where trees grow slowly and winter injury results in early tree mortality, tree densities will increase to allow rapid filling of orchard space. Clingstone orchards have low profit margins because the prices received for raw product and finished goods have not kept pace with inflation. Although yields for processing fruit are high, because large fruit size is not required, processing orchards may become nonprofitable in developed countries. Since the mid 1980s, when subsidization started, Greece has exported increasing amounts of clingstone peaches to European countries and to the United States. The United States is now a net importer of canned peaches. The high cost of production, unfavorable exchange rates, subsidized Greek over-production and low cost Chinese production is a challenge for U.S. exporters of canned fruit (Anonymous 2001). Interest in mechanization will increase in North America as labor costs continue to increase. Many European orchards are too small to justify the cost of expensive equipment and they will rely on skilled labor. It is difficult for researchers to have much impact on commercial growers because growers are locked into systems similar to those currently being used. Large growers in North America and in developing countries

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are reluctant to purchase the smaller orchard equipment required for more intensive orchards. European growers who already own platforms used for several orchard operations and reusable cement posts will likely stick with the trellised Palmettes: after making these investments it would be difficult to change to an entirely new system. Orchard systems being used will certainly continue to be modified to local conditions and to the equipment and labor situations for each orchard. Modifications of existing orchard systems and development of new systems will require research breakthroughs. Rootstocks that provide a range of tree vigor and enhance carbon partitioning, such as those available for apple, may allow development of novel orchard systems. Plant growth regulators to control flowering and vegetative growth, crop load, or fruit ripening could be utilized in new orchard systems. Growers need trees that produce high yields of uniformly high-quality fruit that can be harvested tree ripe. Improvements in other aspects of fruit quality such as fruit size, color, soluble solids concentration, flesh firmness, and high concentrations of health-promoting compounds may improve peach consumption and lead to increased prices. There is a need for long-term studies to determine profitability of various orchard practices and orchard systems. More information on fundamental relationships in peach tree physiology is needed to develop new systems or to modify existing systems. The relationship between light interception and yield per unit land area has yet to be described. Currently peach growers do not have fruit thinning strategies based on sound scientific data, nor practical methods for assessing in real time the progress of the crop and the performance of the orchard. A better understanding of partitioning is needed to develop better strategies for hand-thinning and pruning that may alter carbon partitioning. LITERATURE CITED Allison, M. L., and J. P. Overcash. 1987. Factors affecting hedgerow peach orchard establishment. J. Amer. Soc. Hort. Sci. 112:62–66. Anonymous. 2001. Canned peach industry situation: A history of EU subsidies and their effect on production and trade. www.fas.usda.gov/htp/highlights/2001/IATR/canftr.pdf. Baldassari, T. 1950. La potatura dei fruttiferi. Proc. II Convegno Provinciale Frutticolo, Ferrara, 16 January 1950:71–76. Baldassari, T. 1967. Frutticoltura industriale con la nuova palmetta. Edizioni Agricole, Bologna. pp. 119. Baldini, E. 2001. Agrumi, frutti e uve alla corte dei Granduchi di Toscana. p. 20–32. In: D. Savoia and M. L. Strocchi (eds.), Le belle forme della natura: la pittura di Bartolomeo Bimbi (1648–1730) tra scienzae “maraviglia”. Bologna, Abacus.

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Barden, J. A., and R. P. Marini. 1999. Rootstock effects on growth and fruiting of a spurtype and a standard strain of ‘Delicious’ over eighteen years. Fruit Var. J. 53:115–125. Barden, J. A., and R. P. Marini. 2001. Comparison of methods to express growth, size, and productivity of apple trees. J. Amer. Pomol. Soc. 55:251–256. Bargioni, G., F. Loreti, and P. L. Pisani. 1983. Performance of peach and nectarine in a high density system in Italy. HortScience 18:143–146. Bargioni, G., P. L. Pisani, and F. Loreti. 1985. Ten years of research on peach and nectarine in a high density system in the Verona area. Acta Hort. 173:299–310. Bassi, D., G. Brighenti, and V. Nardi. 1985. Training systems of Klamt cling peach: performance after 8 years—IV Contribution. Acta Hort. 173:339–348. Bassi, D., A. Dina, and R. Scorza. 1994. Tree structure and pruning response of six peach growth forms. J. Amer. Soc. Hort. Sci. 119:378–382. Bellini, E., D. Falqui, and O. Musso. 1997. La coltura protetta del pesco. Inf. Agrario (31): 41–50. Bellini, E., D. Falqui, and O. Musso. 2000. Comparison between two training systems in peach protected culture in Sicily. Acta Hort. 513:427–433. Belluau, E., and A. Lemaire. 1986. Bilan de neuf annees d’experimentation sur la conduite du pecher en axe a haute densite dans le sud est de la France. Acta Hort. 160:327–340. Blay Coll, J. 1988. Formación del melocotonero en un solo eje principal (fuseto). Fruticultura Profesional, 15—Mayo/Junio:3–17. Borras Escriba, F. 2001. La peschicoltura spagnola nel mercato globale. Proc. Xxiv Convegno Peschicolo, Cesena, 24–25 February 2000:31–34. Brace, J. 1904. The culture of fruit trees in pots. William Clowes and Son, London and Beccles. 109 pp. Byers, R. E., D. H. Carbaugh, and C. N. Presley. 1990. The influence of bloom thinning and GA3 sprays on flower bud numbers and distribution in peach trees. J. Hort. Sci. 65: 143–150. Byers, R. E., and R. P. Marini. 1994. Influence of blossom and fruit thinning on peach flower bud tolerance to an early spring freeze. HortScience 29:146–148. Caruso, T., D. Giovannini, F. P. Marra, and F. Sottile. 1997. Two new planting systems for early ripening peaches (Prunus persica L. Batsch): yield and fruit quality in four lowchill cultivars. J. Hort. Sci. 72:873–883. Caruso, T., C. Di Vaio, F. Guarino, A. Motisi, and V. Nuzzo. 2003. Le tipologie d’impianto per la peschicoltura intensiva nell’Italia meridionale. Proc. IV Convegno Nazionale sulla Peschicoltura Meridionale, Agrigento, 11–12 September 2003:44–51. Chalmers, D. J., G. Burge, P. H. Jerie, and P. D. Mitchell. 1986. The mechanism of regulation of ‘Bartlett’ pear fruit and vegetative growth by irrigation withholding and regulated deficit irrigation. J. Amer. Soc. Hort. Sci. 111:904–907. Chalmers, D. J., P. D. Mitchell, and L. van Heek. 1981. Control of peach tree growth and productivity by regulated water supply, tree density, and summer pruning. J. Amer. Soc. Hort. Sci. 106:307–312. Chalmers, D. J., and B. van den Ende. 1975. A reappraisal of the growth and development of peach fruit. Austral. J. Plant Physiol. 2:623–634. Chalmers, D. J., B. van den Ende, and L. van Heek. 1978. Productivity and mechanization of the Tatura trellis orchard. HortScience 13:517–521. Cole, S. W. 1849. The American fruit book. John P. Jewett, New York, NY. 288 pp. Corelli-Grappadelli, L., G. Brighenti, U. Palara, F. Ravaioli, and S. Sansavini. 1986. Esperienze su forme di allevamento del pesco per medie ed alte densità di impianto. Frutticoltura 12:55–60.

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Corelli-Grappadelli, L., G. Ravaglia, and A. Asirelli. 1996. Shoot type and light exposure influence carbon partitioning in peach (Prunus persica L. (Batsch)) cv ‘Elegant Lady’. J. Hort. Sci. 71:533–543. Costa, G., S. Musacchi, F. Succi, and S. Martelli. 1989. Forme di allevamento del pesco per impianti ad elevata densità di piantagione. Riv. Frutticoltura (1):111–119. Couvillon, G. A., and A. Erez. 1980. Rooting, survival, and development of several peach cultivars propagated from semi hardwood cuttings. HortScience 15:41–43. Couvillon, G. A., and A. Erez. 1982. Production potential and tree regeneration in a peach meadow orchard in southeastern United States. Compact Fruit Tree 15:166–169. Crocker, T. E., W. B. Sherman, M. J. Young, and L. G. McDermont. 1988. An experimental high-density system for low-chill peaches and nectarines. p. 432–434. In: Childers and Sherman (eds.), The peach. Horticultural Publ., Gainesville, FL. Crowe, A. D., D. R. Henniger, W. E. Craig, and R. T. O’Regan. 1987. Containerized peach orchards are profitable and avoid winter injury. Compact Fruit Tree 20:90–94. DeJong, T. M. 1998. Using organ growth potentials to identify physiological and horticultural limitations to yield. Acta Hort. 465:293–302. DeJong, T. M., K. R. Day, and J. F. Doyle. 1992. Evaluation of training/pruning systems for peach, plum and nectarine trees in California. Acta Hort. 322:99–105. DeJong, T. M., K. R. Day, J. F. Doyle, and R. S. Johnson. 1994. The Kearney Agricultural Center perpendicular “V” (KAC-V) orchard system for peaches and nectarines. HortTechnology 4:362–367. DeJong, T. M., and J. F. Doyle. 1984. Cropping efficiency, dry matter and nitrogen distribution in mature genetic dwarf and standard peach trees. Acta Hort. 146:89– 95. DeJong, T. M., and J. F. Doyle. 1985. Seasonal relationships between leaf nitrogen content (photosynthetic capacity) and leaf canopy light exposure in peach (Prunus persica). Plant, Cell and Environment 8:701–706. DeJong, T. M., W. Tsuji, J. F. Doyle, and Y. L. Grossman. 1999. Comparative economic efficiency of four peach production systems in California. HortScience 34:73–78. Dorsey, M. J. 1935. Nodal development of the peach shoot as related to fruit bud formation. Proc. Amer. Soc. Hort. Sci. 33:245–257. Elfving, D. C., and I. Schecter. 1993. Fruit count, fruit weight, and yield relationships in ‘Delicious’ apple trees on nine rootstocks. HortScience 28:793–795. Erez, A. 1976. Meadow orchard for the peach. Scientia Hort. 5:43–48. Erez, A. 1978. Adaptation of the peach to the meadow orchard system. Acta Hort. 65:245–250. Erez, A. 1982. Peach meadow orchard: two feasible systems. HortScience 17:138–142. Erez, A. 1988. Peach meadow orchard: two feasible systems. p. 424–431. In: Childers and Sherman (eds.), The peach. Horticultural Publ., Gainesville, FL. Erez, A., Z. Yablowitz, and G. Nir. 1989. Container-grown peach orchard. Compact Fruit Tree 22:96–98. Erez, A., Z. Yablowitz, and P. Korcinski. 1998. Greenhouse peach growing. Acta Hort. 465:593–600. Evert, D. R. 1988. A modified meadow system. p. 434. In: Childers and Sherman (eds.), The peach. Horticultural Publ., Gainesville, FL. FAOSTAT, data. 2003. http://apps.fao.org/faostat/form?collection=Production.Crops .Primary&Domain =Production&servlet=1&hasbulk=0&version=ext&language=EN Fideghelli, C. 1969. Confronto tra i sistemi di allevamento a vaso ed a palmetta del pesco. Proc. Symposium “Giornate di studio sulla potatura degli alberi da frutto. Florence, 24–27 February 1969:133–147.

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Fideghelli, C. 1990. La potatura e le forme di allevamento del pesco e delle nettarine. Proc. Symposium “La potatura degli alberi da frutto negli anni 90”. Verona, 27 April 1990: 167–194. Fideghelli, C., F. Monastra, and R. F. De Salvador. 1988. Evoluzione delle forme d’allevamento e delle densità d’impianto in peschicoltura. Proc. XVIII Convegno Peschicolo, Cesena, 3 May 1986:63–81. Fideghelli, C., G. Della Strada, F. Grassi, and G. Monica. 1998. The peach industry in the world; present situation and trends. Acta Hort. 465:29–40. Fitz, J. 1872. The southern apple and peach culturist. J. W. Randolf and English, Richmond, VA. 336 pp. Flore, J. A., and C. Kesner. 1982. Orchard design for stone fruit based on light interception. Compact Fruit Tree 5:159–165. Forshey, C. G., R. W. Weires, B. H. Stanley, and R. C. Sem. 1983. Dry weight portioning of ‘MacIntosh’ apple trees. J. Amer. Soc. Hort. Sci. 108:149–154. Génard, M., and Frédéric Baret. 1994. Spatial and temporal variation of light inside peach trees. J. Amer. Soc. Hort. Sci. 119:669–677. Giauque, P. 2001. L’ère du productivisme raisonné. Infos-Ctifl/septembre 2001:37–40. Giuliani, R., E. Magnanini, and L. Corelli-Grappadelli. 1998. Whole canopy gas exchange and light interception of three peach training systems. Acta Hort. 465:309–317. Giulivo, C., A. Ramina, and G. Costa. 1984. Effects of planting density on peach and nectarine productivity. J. Amer. Soc. Hort. Sci. 109:287–290. Goedegebure, J. 1989. Economic aspects of HDP-developments in The Netherlands. Acta Hort. 243:389–397. Grossman, Y. L., and T. M. DeJong. 1995a. Maximum fruit growth potential and seasonal patterns of resource dynamics during peach growth. Annals Bot. 75:553–560. Grossman, Y. L., and T. M. DeJong. 1995b. Maximum fruit growth potential following resource limitation during peach growth. Annals Bot. 75:561–567. Grossman, Y. L., and T. M. DeJong. 1995c. Maximum vegetative growth potential and seasonal patterns of resource dynamics during peach growth. Annals Bot. 76:473–482. Grossman, Y. L., and T. M. DeJong. 1998. Training and pruning system effects on vegetative growth potential, light interception, and cropping efficiency in peach trees. J. Amer. Soc. Hort. Sci. 123:1058–1064. Hansche, P. E. 1989. Three brachytic dwarf peach cultivars: Valley Gem, Valley Red, and Valley Sun. HortScience 24:707–709. Hayden, R. A., and F. H. Emerson. 1979. Pruning high density peach hedge plantings. Compact Fruit Tree 12:76–78. Hayden, R. A., and F. H. Emerson. 1988. High density plantings for peaches. p. 404–411. In: Childers and Sherman (eds.), The peach. Horticultural Publ., Gainesville, FL. Hedrick, U. P. 1917. The peaches of New York. Rept. New York Agric. Expt. Stat. J.B. Company, Albany, NY. 541 pp. Horton, B. D. 1985. Effects of tree density on mortality of peaches on a short life site. HortScience 20:950–951. Hudson, J. P. 1971. Meadow orchards. Agriculture 78:157–160. Hugard, J. 1980. High density plantings in French orchards: development and current achievements. Acta Hort. 114:300–308. Hugard, J. 1981. Caracteristiques principales des productions fruitieres de la zone Mediterraneenne Francaise. Acta Hort. 160:15–22. Hutton, R. J., L. M. McFadyen, and J. L. Warwick. 1987. Relative productivity and yield efficiency of canning peach trees in three intensive growing systems. HortScience 22:552–560.

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Jackson, J. E. 1980. Light interception and utilization by orchards. Hort. Rev. 2:208–267. Jackson, J. E. 1989. World-wide development of high density planting in research and practice. Acta Hort. 243:17–27. Johnson, R. S., and A. N. Lakso. 1986. Carbon model of a growing apple shoot: I. Development of the model. J. Amer. Soc. Hort. Sci. 111:160–164. Kappel, F., J. A. Flore, and R. E. C. Layne. 1983. Characterization of the light microclimate in four peach hedgerow canopies. J. Amer. Soc. Hort. Sci. 108:102–105. Lakso, A. N. 1994. Apple. p. 3–42. In: Schaffer and Anderson (eds.), Handbook of environmental physiology of fruit crops—Vol. I Temperate crops. CRC Press, Boca Raton, FL. Layne, R. E. C., C. S. Tan, and J. M. Fulton. 1981. Effect of irrigation and tree density on peach production. J. Amer. Soc. Hort. Sci. 106:151–156. Lespinasse, J. M. 1980. La conduite du pommier. Liaxe vertical la renovation des vergers (2e partie). Center Technique interprofessionel des Fruits et Legumes, Paris. Leuty, S. J., and D. J. Pree. 1980. The influence of tree population and summer pruning on productivity, growth, and quality of peaches. J. Amer. Soc. Hort. Sci. 105:702–705. Lewallen, K. 2000. Effects of light availability and canopy position on peach fruit quality. M.S. Thesis, Dept. of Horticulture, Virginia Polytechnic Institute and State University, Blacksburg. (http://scholar.lib.vt.edu/thesis/available/etd-04262000-13090002/) Loreti, F., R. Massai, and S. Morini. 1989. Further observations on high-density nectarine plantings. Acta Hort. 243:353–360. Manaresi, A., and A. Draghetti. 1915. Influenza del germoglio ascellare sullo sviluppo e sulla composizione del frutto del pesco. Boll. Ass. Orticola Professionale Italiana (1):1–4. Marini, R. P. 1985a. Vegetative growth, yield, and fruit quality of peach as influenced by dormant pruning, summer pruning, and summer topping. J. Amer. Soc. Hort. Sci. 110:133–139. Marini, R. P. 1985b. Sample size estimates for peach tree growth and yield experiments. J. Amer. Soc. Hort. Sci. 110:604–608. Marini, R. P. 1986. Growth and cropping of ‘Redhaven’ peach trees following foliar applications of flurprimidol and paclobutrazol. J. Amer. Soc. Hort. Sci. 111:849–853. Marini, R. P. 1987. Growth and cropping of ‘Redhaven’ peach trees following soil application of paclobutrazol. J. Amer. Soc. Hort. Sci. 112:18–21. Marini, R. P. 2002a. Pruning peach trees. VA Coop. Ext. Pub. 422-020. Marini, R. P. 2002b. Heading fruiting shoots before bloom is equally effective as blossom removal in peach crop load management. HortScience 37:642–646. Marini, R. P., J. L. Anderson, W. R. Autio, B. H. Barritt, J. A. Cline, W. P. Cowgill, Jr., R. M. Crassweller, P. A. Domoto, D. C. Ferree, J. Garner, A. Gaus, G. M. Greene, C. Hampson, P. Hirst, M. M. Kushad, E. Mielke, C. A. Mullins, M. Parker, R. L. Perry, J. P. Privé, G. L. Reighard, T. Robinson, C. R. Rom, T. R. Roper, J. R. Schupp, E. Stover, and R. Unrath. 2000. Performance of ‘Gala’ apple on 18 dwarf rootstocks: Five-year Summary of the 1994 NC-140 Dwarf Rootstock Trial. J. Amer. Pomol. Soc. 54:92–107. Marini, R. P., and J. A. Barden. 1981. Seasonal correlations of specific leaf weight to net photosynthesis and dark respiration of apple leaves. Photosynthetic Res. 2:251–258. Marini, R. P., and J. A. Barden. 1982. Light penetration on overcast and clear days, and specific leaf weight in apple trees as affected by summer or dormant pruning. J. Amer. Soc. Hort. Sci. 107:39–43. Marini, R. P., and J. A. Barden. 1987. Summer pruning of apple and peach trees. Hort. Rev. 9:351–375. Marini, R. P., B. H. Barritt, J. A. Barden, J. Cline, E. E. Hoover, R. L. Granger, M. M. Kushad, M. Parker, R. L. Perry, T. Robinson, S. Khanizaheh, and C. R. Unrath. 2001a. Performance of ten apple orchard systems: ten-year summary of the 1990 NC-140 systems trial. J. Amer. Pomol. Soc. 55:222–238.

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3 Irrigation Scheduling and Evaluation of Tree Water Status in Deciduous Orchards Amos Naor Golan Research Institute University of Haifa P.O. Box 97 Kazrin 12900 Israel

I. INTRODUCTION II. THE MODERN IRRIGATION SCHEDULING CONCEPT III. DEFICIT IRRIGATION A. Reproductive Cell Division Stage B. Pit Hardening Stage (Stone Fruits) C. Final Fruit Growth Stage (Stone Fruits) D. Preharvest Deficit Irrigation in Almonds E. Post Reproductive Cell Division Stage (Pip Fruits) F. Flower Bud Differentiation and Development Stage G. Deficit Irrigation and Fruit Quality in Deciduous Fruit Trees H. Partial Root Drying 1. Physiological Basis 2. Field Examination IV. WATER STRESS ASSESSMENT AND TIMING OF IRRIGATION A. Factors Affecting Transpiration and Irrigation Level 1. Intercepted Radiation and Canopy Size 2. Crop Yield 3. Potential Fruit Size 4. Application Efficiency B. The Grower’s Dilemma C. The Use of Water Stress Indicators 1. General Requirements for a Water Stress Indicator

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2. Types of Water Stress Indicators Available for Commercial Use 3. The Relevance of Plant Water Stress Indicators D. Response to Moisture and Irrigation Regimes E. Sensitivity of Water Stress Indicators F. Early Detection of Water Stress G. Representing Water Status on an Orchard Basis 1. Within Tree and Root Zone Variability 2. Spatial Variability H. Considerations in Setting Thresholds 1. Minimum Stress Conditions 2. Setting Thresholds for Daily Trunk Shrinkage 3. Setting Thresholds Under Deficit Irrigation Conditions I. Conditions of Limited Response to Irrigation 1. Soil-root Zone Limitations 2. Fruit Pedicle Limitations V. CONCLUDING REMARKS LITERATURE CITED

I. INTRODUCTION Irrigation is a major horticultural activity and is the most intensively practiced operation throughout the season. Its importance depends on the climate, and increases with progress from temperate to drier and to arid zones. Dryland orchards can survive and be productive in temperate zones without irrigation, whereas the survival of deciduous orchards in semi-arid zones depends on the availability of water for irrigation throughout most of the growing season. The performance of deciduous trees, i.e., crop yield, fruit size, fruit quality, storability, and long-term productivity are highly dependent on irrigation, and different species respond differently to irrigation. Worldwide, the amount of fresh water available for agricultural use is decreasing and, since shortages of fresh water are to be expected, there is a need to increase water use efficiency, either by improving genetic performance and horticultural practices, or by improving irrigation scheduling. The level of irrigation of deciduous orchards depends on environmental factors that drive evaporative demand and transpiration, salinity, and electrolyte composition in the soil solution, the resistance of the soil to root penetration and moisture transport, soil aeration, tree hydraulic architecture, and crop load. Irrigation interacts indirectly with the susceptibility of deciduous orchards to diseases and pests, and through the effects of soil moisture on pests. The above-mentioned interactions are beyond the scope of the present review. Irrigation affects the performance of deciduous trees through two major mechanisms: its effects on stomatal conductance and assimilation

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rate; and its effects on turgor and expansive growth. This emphasizes the important role of tree-water relations in irrigation, and the reader may refer to a few reviews on that topic (Landsberg and Jones 1982; Jones et al. 1985; Flore and Lakso 1989; Lakso 2003). Whereas earlier reviews covered older studies (Behboudian and Mills 1997; Fereres and Goldhamer 1990), the present review will focus mainly on recent publications. It is divided into two major topics: (1) The effects of deficit irrigation at different phenological stages on productivity and fruit quality and (2) factors affecting irrigation level, water stress assessment, and timing of irrigation.

II. THE MODERN IRRIGATION SCHEDULING CONCEPT Minimum water stress may be the optimal tree water status in certain phenological stages, where a certain degree of stress would be optimal in other phenological stages. Irrigation is applied mainly to maintain optimal availability of assimilates, which is achieved through the control of stomatal aperture, and maintenance of an adequate turgor potential when expansive growth of either the canopy and/or the fruit is expected. The irrigation level used is intended to return to the soil profile the amount of water transpired by the tree and the cover crop (T) in addition to the amount evaporated from the soil surface (E). The sum of these components is called evapotranspiration (ET). Transpiration is a two-step process that starts with conversion of the water from the liquid to the gas phase, a process that requires a significant amount of energy (2.54 MJ kg–1 at 20°C). After the water is vaporized in the stomatal cavities, it diffuses into the free air at a rate controlled by vapor pressure deficit—the difference between saturated vapor pressure at the leaf temperature and the actual vapor pressure at the atmospheric temperature—which is determined by air and leaf temperatures and air humidity. The resistance to this transport process is the sum (in series) of stomatal resistance and the boundary layer resistance, the latter being determined by wind speed, leaf size and shape, and canopy structure. Day-to-day variations in ET are expected because of the significant role of changing weather conditions in transpiration. The modern irrigation-scheduling concept (Allen et al. 1999) assumes: 1. ET of non-stressed crops, reference crop and evaporation from a free-water surface respond similarly to atmospheric evaporative demand.

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2. ET increases linearly with intercepted radiation by the crop. 3. Further differences in ET between crops are due to differences in canopy conductance and canopy roughness. Based on these assumptions, the ET of a specific crop under maximum moisture availability (ETa) is defined as ET0·KC, where ET0 is the evapotranspiration of a reference crop that covers the whole surface area, and which can be replaced by the evaporation from a free water surface in a standard pan, and KC (crop coefficient) is a proportion factor that depends on the fraction of the soil surface covered by the crop, the canopy conductance, and the canopy roughness. There are many models of calculating ET0, from empirical to more mechanistic ones where the effect of wind speed on ET is based on empirical relationships. Pan evaporation rates are highly correlated with ET0, but the slopes of these relationships are not unique and may change between types of evaporation pans and between operational standards. Detailed analysis of the methods of calculating ET0, their correlation with data collected in lysimeters, and the relationships between ET0 and pan evaporation rates can be found elsewhere (Jensen et al. 1990). Canopy conductance of deciduous trees during the dormant season is zero and they are not irrigated in spite the fact that the soil evaporation term of ETa is not zero. KC of deciduous trees increases with increasing foliage coverage, and varies according to seasonal changes in canopy conductance that result from changes in tree-water relations and according to crop level (as will be discussed in detail below). Sets of seasonal crop coefficients are available for various crops; they are based on lysimeter or soil water balance measurements (Allen et al. 1999). Irrigation for maximum biomass production requires no stress, while in other crops, including trees, stress may not affect economic yields. In many cases, tree water status attains its optimal value from the horticultural point of view under a certain stress, and ETa must be multiplied by a stress factor (KS), which is expected to change in the course of the season in accordance with the optimal tree water status. The actual irrigation level assuming no water depletion below the root zone (I) is the product of ET0, KC and KS: I = ET0·KC·KS. In cases where there is a risk of high salinity build up during the growing season, a leaching fraction is added. Two major aspects will be covered in the following: the response of deciduous trees to irrigation at different phenological stages, and issues related to timing of irrigation in relation to the degree of water stress. Also addressed will be the proper representation of water status in commercial orchards.

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III. DEFICIT IRRIGATION Growers have practiced deficit irrigation for decades. In the past, deficit irrigation was restricted to the postharvest period based on the belief that water stress introduces no problems during phenological stages when no fruit exist on the tree and additional vegetative growth is undesirable; an exception is early cultivars in which the desired shoot growth is not completed by harvest. The effect of severe postharvest water stress on the productivity of stone fruits was studied mainly in early-maturing species such as apricot. Deficit irrigation at phenological stages other than postharvest was proposed in the early 1980s (Chalmers et al. 1981, 1986) as a beneficial irrigation strategy, and since then has been studied extensively. Several different processes are sensitive to water stress, and the times of occurrence of those processes may influence the sensitivity to deficit irrigation: 1. Reproductive cell division—lasts 30–40 days post anthesis. 2. Fruit drop—occurs usually during the first 40 days post anthesis. 3. Canopy growth—occurs mainly at the beginning of the season, but may continue longer if sufficient moisture is available and the crop load is low. 4. Flower bud differentiation and development—starts in midsummer and continues throughout the rest of the growing season. The above-mentioned processes are expected to respond differently to moisture availability. Therefore, the effects of deficit irrigation at each phenological stage will be discussed separately. In the cited reports, different water stress indicators were used, the intensity and duration of deficit irrigation varied, and several different cultivars were studied. These differences among others may result sometimes in inconsistent and contradictory findings. Therefore, the interpretation of the results is not always straightforward and the discussion on the effects of water stress, in most cases, is restricted to general terms such as low, moderate, and severe water stress. The post reproductive-cell division fruit growth stage in stone fruits can be divided into two parts, the pit-hardening stage and the final fruit growth stage, where in pip fruits there is practically a single post reproductive-cell division stage. Therefore, the post reproductivecell division stage of stone fruits and pip fruits will be discussed separately.

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A. Reproductive Cell Division Stage Reproductive cell division lasts 30–40 days after full bloom (Westwood 1993) and is accompanied by initial fruit growth. Water stress in the reproductive cell division stage did not affect the number of cells in the fruits (Marsal et al. 2000) but at harvest the cells in the fruits of the stressed trees were smaller, which indicates that water stress during the reproductive cell division stage affects the potential cell size. The proportion of fruit drop in apple increased in response to early water stress (Powell 1974; A. Naor, unpubl.). Water stress in the reproductive cell division stage decreased tree vegetative growth in pear (Mitchell et al. 1984, 1986, 1989; Chalmers et al. 1986; Marsal et al. 2000, 2002a), in which vegetative growth decreased with decreasing irrigation level (Mitchell et al. 1984, 1986, 1989), and decreasing midday leaf water potential (Chalmers et al. 1986) or midday stem water potential (Marsal et al. 2002a). Early water stress led to smaller apple (Failla et al. 1992) and pear (Marsal et al. 2000, 2002a; Naor et al. 2000) fruits; fruit size decreased with decreasing midday stem water potential during the reproductive cell division stage (Marsal et al. 2000, 2002a), and the smaller fruit size persisted until harvest in apple and pear (Marsal et al. 2000; Naor et al. 2000). Early water stress decreased the fruit sizes attained in peach by the end of the reproductive cell division stage (Fig. 3.1) and at harvest (Girona et al. 2002, 2004; Goldhamer et al. 2002). Deficit irrigation during both the reproductive cell division and the pit hardening stages in apricot decreased fruit size at the end of the pit hardening stage, but a significant fruit size recovery was apparent after the water stress was relieved during the final fruit growth stage (Ruiz-Sanchez et al. 2000a; Torrecillas et al. 2000). However, the statistical analysis of final fruit size in these studies is insufficient to conclude that the decrease in fruit size in response to early stages water stress is fully reversible. Contradicting results of increasing final fruit size in response to early water stress was reported for high-density pear (Mitchell et al. 1984; Chalmers et al. 1986), and it could be related to the higher midday leaf water potential in the pre-stressed treatment than in the control after resumption of irrigation (Chalmers et al. 1986). It seems that larger canopies in the control of high-density pear orchard, because of a significant increase in vegetative growth (Mitchell et al. 1984, 1986, 1989; Chalmers et al. 1986), may have increased water consumption and therefore decreased water potential. It may well be that in high-density orchards, the vegetative part invokes a significant competition for assim-

3. IRRIGATION SCHEDULING OF DECIDUOUS ORCHARDS

100

a

a

a

ab

Fruit weight (% of control)

b 90

b

b

80

Control WI Stage I WI Stage II WI Stage III

a

a a

117

c c

70

60

End of Stage I

End of Stage II

End of Stage III

Date of fruit weight measurements Fig. 3.1. Effects of withholding irrigation (WI) in the reproductive cell division (Stage I), pit hardening (Stage II), and final fruit growth (Stage III) stages on peach fruit fresh weight relative to unstressed trees (control). Fruit weights of the control were 41.2, 68.5, and 215 g at the end of stages I, II, and III, respectively (Source: Girona et al. 2002).

ilates, explaining the contradicting results of increased fruit size in early-stressed trees in high-density trees. A multiseason test of the effects of early water stress resulted in increased numbers of pears per tree (Mitchell et al. 1989), similar to the effect of moderate postharvest water stress (Fig. 3.2). This may indicate that moderate water stress improves the completion of flower bud development, resulting in higher flower intensity and fruit set in subsequent seasons. B. Pit Hardening Stage (Stone Fruits) The duration of the pit hardening stage changes with harvest date: the later the harvest the longer the duration of this stage (Westwood 1993). In early-maturing cultivars, the fruits continue to grow during the pit hardening stage, but slightly more slowly, making it hard to distinguish among the different fruit growth stages. The extent of fruit growth in the pit hardening stage decreases with increasing its duration. In practice,

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Total crop yield (t/ha)

40

a

30 b b

20

10

0 High

Med.

Low

Post-harvest irrigation level Fig. 3.2. Effects of postharvest irrigation levels in 2001 and 2002 on next-season pear crop yield (cumulative for 2002 and 2003). Midday stem water potentials were –2.8 MPa, –2.4 MPa, and –1.5 MPa in the Low, Med. and High irrigation levels, respectively (A. Naor et al. unpubl.).

the duration of the pit hardening stage in early-maturing cultivars is too short for deficit irrigation to be considered. Water stress during the pit hardening stage reduced fruit size at the end of the stage in peach (Girona et al. 2002) and nectarine (A. Naor, unpubl.), and water stress during both reproductive cell division and pit hardening stages also caused reductions in fruit size by the end of the latter stage in peach (Mitchell and Chalmers 1982) and apricot (RuizSanchez et al. 2000a; Torrecillas et al. 2000). In the above studies, fruit size recovered when irrigation was applied at a minimal-stressing level in the final fruit growth stage. An increase in fruit size in response to water stress in the pit hardening stage was reported in the third year, in a high-density peach orchard (Chalmers et al. 1981); this contradictory response could be a result of higher competition of the dense-shaded canopy for assimilates in minimum-stressed trees compared with stressed trees at that particular high-density orchard. Water stress dur-

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ing the pit hardening stage in peach led to a lower percentage of large fruits (Goldhamer et al. 2002), in a study in which there was a 10-mm increase in fruit diameter during the stress period, which could have increased the sensitivity to water stress at this stage. If the designated end of the pit hardening stage in that study had been too late, that could also account for the smaller fruit size. Fruit expansive growth is affected by water stress, and the relative insensitivity of fruit size to water stress in the pit hardening stage is related to the limited fruit expansive growth that is usually apparent in this stage. The start of the pit hardening stage is easy to determine, whereas the end of this stage is not clear and in most cases it can be determined only post factum, on the basis of continuous measurements of fruit weight in the course of the season. In addition, the duration of the pit hardening stage and the date of its end change markedly from one season to another (Girona et al. 2003; A. Naor, unpubl.), therefore the use of a predetermined duration of deficit irrigation during this stage might be risky. In shallow soils both the build-up and the relief of water stress are rapid (Goldhamer et al. 2002), but in a deep heavy soil profile the relief of water stress at the end of pit hardening may take a few weeks, unless a significant extra amount of irrigation water is provided, to fill the soil profile (Naor, unpubl.); this may reduce the amount of annual applied water that can be saved through deficit irrigation at that stage. Shoot growth in grown apricot is almost completed by the end of the reproductive cell division stage (Torrecillas et al. 2000), therefore using deficit irrigation in the pit hardening stage is not beneficial for vegetative control. In peach, on the other hand, active shoot growth continues into the pit hardening stage (Fig. 3.3), therefore water stress in that stage might be beneficial for canopy size control. Improved color in peach that resulted from deficit irrigation in the pit hardening stage was attributed to reduced shoot growth and an improved light regime around the fruit (Gelly et al. 2003, 2004). C. Final Fruit Growth Stage (Stone Fruits) Fruit growth in the final fruit growth stage is highly responsive to irrigation, as a significant proportion of dry and fresh weight is accumulated in the fruit (Pavel and DeJong 1993; Grossman and DeJong 1995a,b; Girona et al. 2004). Water stress in the final fruit growth stage significantly decreased the final fruit size in peach (Besset et al. 2001; Girona et al. 2002), nectarine (Naor et al. 1999, 2001), apricot (Torrecillas et al. 2000), and Japanese plum (Naor et al. 2004). Under water stress, reductions in average fruit weight and yield were found to increase with increasing numbers of fruits per tree in both nectarine (Naor et al. 1999,

120

A. NAOR 60

Shoot extension length (cm)

50

Control NI-SI NI-SII NI-SIII

a a b

40 c

30

20

10 May

Stage-I

Stage II

Stage III

Jun

Jul

Aug

Sep

Oct

Date (1996)

Fig. 3.3. Effects of withholding irrigation at stage I (NI-SI), stage II (NI-SII), and stage III (NI-SIII) of peach fruit growth on shoot extension compared with unstressed trees (control) (Source: Girona et al. 2004. This figure is reproduced with permission from the JHSB.).

2001) and Japanese plum (Naor et al. 2004). Under minimum water stress conditions, the nectarine fruit size distribution was shifted towards smaller fruits as the number of fruit per tree increased (Naor et al. 1999), indicating the magnitude of crop the canopy can support is limited and the crop level should not exceed this limit if large fruits are to be achieved. In Japanese plum under minimum stress conditions (Naor et al. 2004), the fruit size distribution was unaffected by the number of fruit per tree, probably because of lower crop yield, which did not introduce significant limitation of assimilates. D. Preharvest Deficit Irrigation in Almonds Preharvest deficit irrigation is a common practice in almond, for technical reasons: to reduce damage to the trunk caused by the shaker, and to simplify collection of the fruit. Withholding irrigation prior to harvest slightly decreased the shaker damage to the trunk (Gurusinghe and Shackel 1995; Goldhamer and Viveros 2000) but, on the other hand, severe water stress increased the proportion of the fruits that remained on the tree, delayed the opening of the hull, and increased the proportion of unopened hulls at harvest (Goldhamer et al. 2004).

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Water stress in the final fruit growth stage of almond decreased (Goldhamer and Viveros 2000; Goldhamer et al. 2004; Romero et al. 2004) or did not affect kernel weight (Esparza et al. 2001a; Girona et al. 2005). The kernel size in almond decreased by <20% (Goldhamer and Viveros 2000; Goldhamer et al. 2004) in response to preharvest water stress, compared with reductions of up to 40% in fruit sizes (in peach, nectarine, plum, and apricot) (Naor et al. 1999, 2001, 2004; Besset et al. 2001). Most of the reduction in almond fruit size was restricted to the hull shell (Goldhamer et al. 2004), which is of no economic value. Preharvest water stress in almond slightly increased the number of fruit per tree in subsequent years (Goldhamer and Viveros 2000; Goldhamer et al. 2004); the increase was probably caused by an increased proportion of not fully developed flower buds in well irrigated trees (Forshey and Elfving 1989), similar to the case of pear (Mitchell et al. 1989; Fig. 3.2). The longer the duration of withholding irrigation prior to harvest (or the higher the degree of water stress) the lower the fruit set in the following season, provided postharvest water stress was applied (Goldhamer and Viveros 2000). This may indicate that the functioning of the flowers was damaged, which could also be related to a decrease in non-structural carbohydrate accumulation caused by water stress (Esparza et al. 2001b). Productivity of almond is highly correlated with canopy size in both young (Castel and Fereres 1982; Torrecillas et al. 1989; Girona et al. 1993a; Hutmacher et al. 1994) and grown trees (Esparza et al. 2001a; Romero et al. 2004). Productivity of almond is dependent on shoot growth, since some of the fruits are carried on 1-year-old shoots, and because of the high mortality rate of spurs (60% in three years), irrespective of irrigation level (Esparza et al. 2001a). Preharvest water stress in almond did not affect subsequent season productivity (Goldhamer and Viveros 2000), since most of the shoot growth occurs in earlier stages in the course of the season. On the other hand, preharvest water stress caused the productivity of a young orchard to decrease from year 4 to 7 (Fereres et al. 1981; Girona et al. 2005), because productivity is more dependent on canopy growth in young, not fully developed orchards. E. Post Reproductive Cell Division Stage (Pip Fruits) The fruit growth patterns of apple (Lakso et al. 1995) and pear (Naor et al. 2000) are expolinear—exponential increase during reproductive cell division stage followed by a linear growth pattern thereafter. In many studies the post-cell-division stage, which extends up to harvest, was arbitrarily divided into two sub-stages (early deficit and late deficit), so

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only general information was obtained about the sensitivity to water stress in the course of that stage. Moderate water stress up to 102 days after full bloom reduced canopy growth in apple (Behboudian et al. 1998), whereas water stress applied after this period had no effect. This indicates that shoot growth ends within 3 months after bloom (Irving and Drost 1987; Forshey and Elfving 1989). An early deficit created moderate water stress and resulted in a lower return bloom, whereas no reduction in return bloom was apparent in a late-deficit treatment (Kilili et al. 1996a; Behboudian et al. 1998). In another study, deficit irrigation throughout the season did not affect return bloom (Mills et al. 1994), but, in that particular case, water stress did not develop up to 100 days after bloom. Non-stress conditions decreased subsequent season productivity in pear (Mitchell et al. 1989; Fig. 3.2) and stone fruits (Larson et al. 1988; Johnson et al. 1992), probably by delaying flower bud development. Reductions in return bloom and productivity under severe water stress were found in pear (A. Naor et al. unpubl.) and apple (Ebel 1991), as well as in stone fruits (Brown 1953; Uriu 1964; Johnson et al. 1994; Ruiz-Sanchez et al. 1999; Goldhamer and Viveros 2000; Torrrecillas et al. 2000; Girona et al. 2003; Naor et al. 2005); the above-mentioned apple studies that showed lower return bloom did not involve such a high level of water stress (Kilili et al. 1996a; Behboudian et al. 1998). The reduction in the proportion of return bloom in apple trees moderately stressed early in the season can be explained as follows: A vegetative bud (bourse shoot) emerges from apple flower buds, and the longer the bourse shoot the higher the probability for its terminal bud to flower the following year (Lauri et al. 1996; Lauri and Trottier 2004). There is a possibility that water stress in the early-deficit treatments reduced the length of the bourse shoots, which resulted in a lower proportion of return bloom, whereas the bourse shoots had already reached their final size by the time the latedeficit treatments were started. Early water deficit (for about 2 months post reproductive cell division) reduced apple fruit size (Kilili et al. 1996a; Mpelasoka et al. 2000, 2001a), similar to the effect when late deficit was imposed on pear (Ramos et al. 1994; Naor et al. 1999; Marsal et al. 2000) or apple (Failla et al. 1992; Naor et al. 1995, 1997a,b; Mpelasoka et al. 2000, 2001a; Ebel et al. 2001). In a few studies, post-cell-division water deficit did not reduce fruit size (Behboudian et al. 1998; Mpelasoka et al. 2001a). Caspari et al. (1994) found that the average fruit weight of Asian pear at harvest was unaffected by either early or late water deficit, whereas fruit growth (measured on selected fruit) under the late-deficit treatment was smaller.

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123

The effect of late deficit on fruit size interacted with the number of fruit per tree with both apple (Naor et al. 1997a) and pear (Naor et al. 2000), as well as with stone fruits (Naor et al. 1999, 2001, 2004): the more fruit per tree, the greater the water-stress-induced reduction in fruit size (Fig. 3.4), but when there were few fruits per tree their size was unaffected by water stress. It may suggest that the reduction in assimilation rate in response to tree water stress does not invoke limitation of assimilates at low crop yields. F. Flower Bud Differentiation and Development Stage In many cases the initial stages of bud development are noted before harvest (Tufts and Morrow 1925; Westwood 1993), and the development continues throughout the rest of the season. Water stress is known to affect flower bud development, but past research on this topic was restricted to the postharvest period because of the high sensitivity of expansive fruit growth to preharvest water stress. Application of preharvest water stress is now considered normal for almond and processing prunes, therefore study of the effect of water stress on bud development in deciduous trees is no longer restricted to the postharvest stage.

Crop yield >70 mm in diameter (ton/ha)

100 Pan evap. coefficient 0.42 0.58 0.75 0.90 1.06

80

60

40

20

0 0

100

200

300

400

500

Fruit per tree Fig. 3.4. Effect of the number of fruits per tree on apple crop yield >70 mm at five irrigation levels prior to harvest (Naor et al. 1997a).

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The occurrence of twin fruits in peach and nectarine is related to postharvest water stress (Larson et al. 1988; Johnson et al. 1992; Handley and Johnson 2000; Naor et al. 2005). Both twin fruits and those with deep sutures result from postharvest water stress (Handley and Johnson 2000; Naor et al. 2005). The percentage of twins in nectarine increased with decreasing average midday stem water potential in August (Fig. 3.5), and a lower limit of –2.0 MPa can be set for postharvest irrigation scheduling, as lower values cause a significant increase in fruit twinning. In nectarine, more twin fruit were formed in response to severe postharvest water stress that occurred before Sept. 1, than to that which occurred later (Naor et al. 2005), and this is consistent with the finding of a significant decrease in the occurrence of twin fruits in peach when postharvest water stress was relieved at the end of August (Handley and Johnson 2000). Severe postharvest water stress at 25°C did not cause fruit twinning in cherry (Beppu and Kataoka 1999), which suggests the responses of cherry

80

Percent twins

60

40

20

0 –3.0

–2.5

–2.0

–1.5

–1.0

Midday stem water potential (MPa) in August 2002 Fig. 3.5. The relationship between average midday stem water potential in August and next-season occurrence of double fruits (30 days after full bloom) in Snow Queen nectarine (Naor et al. 2005).

3. IRRIGATION SCHEDULING OF DECIDUOUS ORCHARDS

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and peach to postharvest water stress are different; the difference could be related to cherry fruit carried on spurs and nectarines on one-year-old shoots, which may alter the timing and dynamics of flower bud development. This hypothesis might be supported by the fact that no twins were reported to result from severe postharvest water stress in spur-type Japanese plum cultivars (Johnson et al. 1994; Naor et al. 2004). The percentage of twin fruit in cherry increased with increasing temperature above 30°C (Beppu and Kataoka 1999; Beppu et al. 2001) in a controlled environment, and it decreased in field-grown trees under shade netting that reduced the air temperature (Beppu and Kataoka 2000). These findings are in agreement with those for peach (Johnson et al. 1992; Naor et al. 2005), in which the percentages of twin fruit were much higher when high postharvest temperatures were apparent in a former season. Both temperature (Beppu and Kataoka 1999; Beppu et al. 2001; Johnson et al. 1992; Naor et al. in press) and postharvest water stress (Larson et al. 1988; Johnson et al. 1992; Handley and Johnson 2000; Naor et al. in press) are responsible for the occurrence of double fruits. It seems that flower buds exposed to high temperature during the bud development stage acquire the potential to form twin fruits, but that the proportion of buds that realized this potential was strongly affected by postharvest water stress. Beppu et al. (2001) suggested the sensitivity to double pistil formation occurs during the transition from sepal to petal differentiation. Severe postharvest water stress decreased the productivity in the subsequent year, in apricot (Brown 1953; Uriu 1964; Ruiz-Sanchez et al. 1999; Torrecillas et al. 2000), peach (Girona et al. 2003; Naor et al. 2005), Japanese plum (Johnson et al. 1994), almond (Goldhamer and Viveros 2000), and pear (Fig. 3.2), and contrary findings of increased productivity in the season following postharvest water stress (Larson et al. 1988; Johnson et al. 1992) were related to a lower level of stress and to pre-winter irrigation that had shortened the duration of the postharvest water stress. A moderate level of postharvest water stress resulted in the highest pear crop yield in the following season (Fig. 3.2) due to increased number of fruits per tree, which appears to indicate that minimal water stress conditions slow flower bud development so that some of the buds are not fully matured in time for the subsequent season bud break. The decrease in productivity caused by severe postharvest water stress was due to reduced flowering intensity (Brown 1953; Girona et al. 2003) and lower fruit set (Ruiz-Sanchez et al. 1999; Goldhamer and Viveros 2000; Torrecillas et al. 2000; Girona et al. 2003). The lower fruit set in apricot was attributed to reduced pollen vitality (Ruiz-Sanchez et al. 1999). Severe postharvest water stress delayed flower bud development (Brown 1953; Naor et al. 2005), and the resulting buds had smaller

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leaves surrounding the fruit, and smaller stones, and their harvest was delayed (Brown 1953). Sporadic flowering of terminal buds occurs in pear after harvest. A significant autumn flowering (including spurs) occurred in pears as a consequence of severe postharvest water stress that was relieved at the beginning of October (60 mm irrigation in 6 days) (A. Naor et al. unpubl.); unstressed and moderately stressed trees had higher midday stem water potentials and they did not flower in response to 60 mm of irrigation at the beginning of October (Fig. 3.6). This raises the possibility that severely stressed pears may respond to heavy autumn rains by massive flowering. G. Deficit Irrigation and Fruit Quality in Deciduous Fruit Trees In general, deficit irrigation advances maturity, increases total soluble solids content and firmness, improves red color, and decreases the background color. It also affects volatile aroma compounds. Many past studies found higher firmness as a result of deficit irrigation. However, it was argued (Behboudian and Mills 1997) that the

Number of flowers per tree

2000

1500

1000

500

0 –3.4

–3.2

–3.0

–2.8

–2.6

–2.4

–2.2

–2.0

–1.8

Midday stem water potential (MPa) Fig. 3.6. Effect of midday stem water potential at the end of September (prior to the application of 60 mm of irrigation in ten days) on the cumulative number of Spadona pear flowers counted up to mid-November (A. Naor et al. unpubl.).

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increased fruit firmness in stressed trees could be an artifact because fruit size decreases as a direct result of deficit irrigation, and the firmness of apples increases with decreasing fruit weight (Ebel et al. 1993). In different studies, post-cell-division water stress increased (Mpelasoka et al. 2000, 2001a,b), did not affect (Ebel et al. 1993; Behboudian et al. 1998), or decreased (Mills et al. 1994) apple firmness at harvest. Pear firmness was unaffected by tree water status (Ramos et al. 1994), and deficit irrigation did not affect fruit firmness in peach (Gelly et al. 2003). In another apple study, fruit firmness increased by the end of the earlydeficit treatment, but the differences had disappeared by harvest time (Kilili et al. 1996a). The dynamics of fruit firmness in cold storage were examined in two studies in apple (Kilili et al. 1996b; Mpelasoka et al. 2001a). The differences in firmness between fruits from different waterstress treatments remained the same during 12 weeks (Kilili et al. 1996b) and 10 weeks (Mpelasoka et al. 2001a) in cold storage; they diminished after 10 weeks and reached similar levels by 17 weeks (Mpelasoka et al. 2001a). During a shelf life study (Mpelasoka et al. 2001a), the higher firmness imparted by a deficit irrigation treatment was retained for 6 days, after which the differences diminished and disappeared. Data collected in the past decade suggest firmness increases in response to postcell-division water stress, but that the increase is often temporary. Many studies found that deficit irrigation increased ethylene concentrations in apple, at harvest or during storage (Ebel et al. 1993; Kilili et al. 1996b; Behboudian et al. 1998; Mpelasoka et al. 2000, 2001a, 2002); a similar response was reported for peach (Gelly et al. 2003, 2004); deficit irrigation increased also the proportion of mature fruits in Asian pear (Caspari et al. 1996) and apple (Mpelasoka et al. 2002) at harvest. Background color is an indicator of maturity in apple and it was reported to either decrease (Kilili et al. 1996a,b) or to remain unchanged (Mpelasoka et al. 2001b) in response to deficit irrigation. These findings indicate deficit irrigation advances maturity in most cases. Studies on the effect of deficit irrigation on aroma volatiles yielded inconsistent results (Behboudian et al. 1998; Mpelasoka et al. 2002) probably because of the dramatic rise of those compounds at a certain point, together with the fact that there is not a distinct definition of maturation and the advancement of maturity in response to deficit irrigation. Water deficit was reported to increase emissions of volatile compounds from other tree organs in apple (Ebel et al. 1995), therefore, in spite of the inconsistent findings, a direct effect of deficit irrigation on volatile compounds in the fruit cannot be ruled out. Deficit irrigation increased total soluble solids in apple at harvest (Ebel et al. 1993; Behboudian et al. 1994, 1998; Mills et al. 1994; Kilili

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et al. 1996a,b; Mpelasoka and Behboudian 2000, 2001a,b, 2002), and the differences were retained during storage (Ebel et al. 1993; Kilili et al. 1996b; Behboudian et al. 1998; Mpelasoka et al. 2000, 2001a, 2002). Deficit irrigation increased total soluble solids at harvest in peach (Crisosto et al. 1994; Gelly et al. 2003) but not in apricot (Torrecillas et al. 2000) or Asian pear (Behboudian et al. 1994). The increased total soluble solids content was accompanied by an increased percentage of dry matter (Mills et al. 1994; Kilili et al. 1996a; Mpelasoka et al. 2001a), suggesting part of the increase in soluble solids was due to water losses from the fruit. However, deficit irrigation elicited specific metabolic effects that were manifested in changed proportions of specific sugars— increased fructose (Mpelasoka et al. 2000) or sorbitol content (Mills et al. 1994)—under deficit irrigation compared with unstressed treatments. Deficit irrigation increased the color intensity in apricot (Torrecillas et al. 2000) and peach (Gelly et al. 2003, 2004), but different researchers found it increased the red color (Mills et al. 1994; Kilili et al. 1996a,b) or did not affect it in apple (Mpelasoka et al. 2001) and European pear (Caspari et al. 1996). Enhancement of the red color could be an indirect effect of deficit irrigation, via a reduction in vegetative growth, which affects light regime within the canopy. Irrigation of previously water-stressed prune has been found to induce fruit-end cracking (Uriu et al. 1962); the formation of cracks was accompanied by increased osmotic potential gradients along the fruit in rewatered trees (Milad and Shackel 1992), which probably was accompanied by a gradient in turgor potential. H. Partial Root Drying The use of both high and low soil moisture regimes within the root zone of a single tree was proposed to manipulate tree water relations and tree performance (Loveys et al. 2000). This technique was tested in both winegrapes and deciduous fruit trees. 1. Physiological Basis. It is now well established that the control of the stomatal opening under light saturation conditions is influenced by root water status (e.g., Gollan et al. 1986; Davis and Zhang 1991) through root signals, and that ABA seems to be involved in this process. Stomatal conductance was found to respond both to root signals and to leaf water potential, and the responsiveness of stomatal conductance to ABA decreased with decreasing leaf water potential (Tardieu and Davies 1993; Tardieu et al. 1993). Root signals also decreased shoot growth in apple under non-stressed conditions (Gowing et al. 1990).

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In light of the above-mentioned responses, the possible use of partial root drying was examined. Stomatal conductance of container-grown wine-grapes decreased in response to withholding of irrigation in half of the root zone, but after 8 days it started to recover (Loveys et al. 2000; Stoll et al. 2000). Shoot growth of container-grown wine-grapes was reduced under partial root zone drying (Loveys et al. 2000). In a partial root zone drying experiment with container-grown apple (Gowing et al. 1990), shoot growth recovered in response to both re-watering and to elimination of the dried part of the root zone. Partial root zone drying has the potential to manipulate tree-water relations so as to combine high turgor with low stomatal conductance and low shoot growth. However, the ability of partial root zone drying to manipulate fruit growth was not examined in details. 2. Field Examination. Partial root zone drying did not affect stomatal conductance in pear (O’Connell and Goodwin, 2004) and apple (Caspari et al. 2004a; Einhorn and Caspari, 2004). Similar crop yields and fruit sizes were measured in apple both under regular deficit irrigation and with partial root zone drying at the same irrigation levels (Caspari et al. 2004b; Einhorn and Caspari 2004; Leib et al. in press), but in one study there were larger fruit in the partial root zone drying treatment in one of two seasons (Caspari et al. 2004). Similar crop yields, fruit sizes, and fruit color were obtained in peach under both regular deficit irrigation and partial root zone drying at the same irrigation levels (Goldhamer et al. 2002). In summary, the physiological responses to partial root drying were obtained in container-grown wine-grapes (Stoll et al. 2000) and apple (Gowing et al. 1990) and in semi-controlled conditions in wine-grapes (Loveys et al. 2000). However, no responses were obtained to partial root zone drying under commercial-scale conditions. It seems as if the size of the root zone in commercial plots and the non-uniformity of moisture content created different dynamics of root water status development in the drying side compare to the experiments that were performed in containers; this was probably responsible for the failure to reproduce the effects found in a controlled root zone under commercial field scale conditions.

IV. WATER STRESS ASSESSMENT AND TIMING OF IRRIGATION Commercial orchards consist of numerous combinations of many factors that may require adjustment of the published KC and KS values to suit the actual conditions. These factors include rootstock, training system,

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row spacing, cultivar, the number of fruit per tree, crop load (the ability of the canopy to support the crop), and potential fruit size. In addition, the irrigation level is calculated on the assumption that application efficiency is 1, which is not the case in commercial orchards: it may vary with the combination of soil depth and soil hydraulic properties, irrigation equipment and spacing of emitters, irrigation level, and irrigation intervals, and therefore may require site-specific corrections. There are also some concerns about the assumption that fruit trees and the reference crop respond similarly to evaporative demand under all weather conditions (Johnson et al. 2004). The above-mentioned limitations leave growers with uncertainty about optimal day-to-day decisions on irrigation scheduling. Those uncertainties and ways to minimize them are discussed below. A. Factors Affecting Transpiration and Irrigation Level Irrigation level is affected by the amount of intercepted radiation by the canopy and the presence of crop, which directly affect tree transpiration rate. The demand for assimilates increases with increasing the expected crop yield and it may affect irrigation level as well. Potential fruit size may affect the optimal tree water status needed to achieve the target fruit size and therefore it affects irrigation level. These aspects and the attention that should be paid to application efficiency of the irrigation water will be discussed in the following. 1. Intercepted Radiation and Canopy Size. The transpiration rate is proportional to leaf area (Angelocci and Valancogne 1993) and it dictates the amount of light intercepted by the canopy (Johnson et al. 2000; Ayars et al. 2003) to supply latent heat flux that drives the evaporation of water from the canopy (Green et al. 2003). Canopy size and light interception varied with the training system in apple (Robinson and Lakso 1991; Wunsche et al. 1995) and peach (Giuliani et al. 1998), and with cultivars in apple (Robinson and Lakso 1991). These findings suggest that the effects of canopy size on transpiration and, therefore, on irrigation level should be evaluated for each specific plot. Light interception can be measured quite accurately, but most procedures are not suitable for use by growers (Pearcy 1989; Wunsche et al. 1995; Welles and Cohen 1996). High correlations were found between percentage shade at midday (whose measurement requires a simple procedure that growers could perform) and KC for young almonds (Fig. 33-4 in Fereres and Goldhamer 1990) and peach (Ayars et al. 2003; Goodwin and Connor, in press). However, there is no unique relationship between midday light

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interception and daily light interception that is valid for every combination of training system and row orientation (Palmer 1993). There is a need for modeling the relationships between midday and daily light interception for combinations of training systems, rootstocks, cultivars and row orientation; and such a model might reduce the uncertainty in evaluating the effect of canopy size on the crop coefficient in each particular plot. Tree size is correlated with trunk cross-section area and light interception in the first years, before significant pruning is performed, and growers can then utilize this measurement to adjust KC for orchards of different ages. However, care should be taken as the slope of this relationship may vary with rootstock and training system and cultivars. 2. Crop Yield. Two aspects of the effect of crop yield on irrigation level should be considered: the direct effect of cropping on stomatal conductance and hence on transpiration and water consumption; and the increasing demand for assimilates as crop yield increases. Direct Effect of Cropping on Transpiration. Leaf photosynthesis and stomatal conductance of deciduous trees have been found to increase with the presence of a crop (Hansen 1971; Fuji and Kennedy 1985; DeJong 1986; Erf and Proctor 1989; Gucci et al. 1991, 1994; Wibbe and Blanke 1995; Giuliani et al. 1997; Wunsche et al. 2000; Marsal et al. 2005), although in a few cases no effect (Palmer 1986, 1992; McFayden et al. 1996) or the opposite effect (Fuji and Kennedy 1985; Schechter et al. 1991; Mpelasoka et al. 2001b) was apparent. The effect of cropping on assimilation rate was found to change in the course of the season (Fuji and Kennedy 1985; Palmer 1992; Wibbe et al. 1993; Gucci et al. 1994; Giuliani et al. 1997; Wunsche and Palmer 1997; Wunsche et al. 2000), with the maximum effect occurring at midsummer and diminishing after harvest. In general, the contradictory results have been attributed to changing responses in the course of the season, changes in the response after fruit thinning (Gucci et al. 1991), differing morning and afternoon responses (Gucci et al. 1991), or the existence of sinks other than fruit. Cropping in plum increased leaf water use efficiency (Gucci et al. 1991), but did not affect it in apple (Wunsche et al. 2000). Assimilation rate increases with increasing crop load and it starts to level off at daily demand of ~15 mg carbon per leaf in peach (Ben Mimoun et al. 1996) or up to about 15 fruits per square meter of leaf area in apple (Palmer et al. 1997). In the latter case, the crop load was equivalent to ~30 ton/ha, whereas the whole-tree assimilation rate has been found to respond to crop loads as high as 45 ton/ha (Wunsche et al. 2000). In another study (Giuliani et al. 1997), all crop loads were in

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the range in which leaf assimilation rate does not respond any more to crop load. Studies with containerized (Lenz 1986) and lysimeter trees (Buwalda and Lenz 1992; Buwalda and Lenz 1995; Mpelasoka et al. 2001), and with whole-tree gas-exchange systems (Wibbe et al. 1993; Wunsche et al. 2000) demonstrated that cropping trees use more water. A 36% increase in transpiration in high crop loaded relative to defruited field grown apple trees in whole-tree gas-exchange system (Wunsche et al. 2000) is the closest available estimate to commercial field conditions. Cropping also decreased water potential (Erf and Proctor 1989; Berman and DeJong 1996; Naor et al. 1997b, 2001, 2004; Mpelasoka et al. 2001b), and thus indirectly supports increased transpiration in cropping trees. The data collected in the past two decades generally show a direct effect of increased transpiration caused by cropping, and irrigation levels should be adjusted to account for this effect. Annual Irrigation Level Adjustment According to Crop Yield Estimates. The higher the yield the higher the demand for assimilates, and, since the assimilation rate is affected by water stress and therefore by the irrigation rate, there is a need for a quantitative evaluation of the effect of crop yield on irrigation level. Naschitz and Naor (2005) proposed an operative model that may enable the adjustment of the annual irrigation level according to crop yield predictions, and the evaluation of relative water use efficiency on the orchard scale. Fruit diameter increases with increasing specific reproductive water use, i.e., annual irrigation rate – annual vegetative water use —————–––––––––––––––––––––———————total crop yield until it reaches a maximum (Fig. 3.7) and the maximum fruit diameter changes from year to year because of changes in the potential fruit size. The “vegetative water use” is estimated by extrapolating the model to zero fruit diameter. The cost in terms of water use for the production of 1 tonne (fresh weight) of apple fruits would be approximately 47 m3 (Naschitz and Naor 2005), which might differ between climatic regions because of the effect of humidity on the water use efficiency (Jones 1992) and the effect of air temperature on respiration. Consistent application of specific reproductive use levels either higher or lower than 47 m3 t–1 for a few years would result in the adjustment of the tree structure (increase or decrease) so as to change vegetative water use until the

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actual specific reproductive use approaches 47 m3 t–1 in a new steadystate condition. The cost in terms of water use for the production of 1 t (fresh weight) should be determined for each species on a regional basis, as it is affected by climatic conditions, and the resulting value could then serve for planning irrigation levels once good estimates of crop yield are available. Water use efficiency on an orchard scale could be evaluated once a regional response curve (as in Fig. 3.7) was constructed. Commercial plots whose data lie on the model curve (Fig. 3.7) are considered efficient plots, whereas if the data of a specific plot lie below the model line it indicates that the specific plot is inefficient. 3. Potential Fruit Size. The number of cells in the flesh determines the potential fruit size, and the fulfillment of that potential is dependent on irrigation and the crop load, and different potential fruit sizes may require different irrigation levels to reach the target fruit size (Fig. 3.7). Therefore, early predictions of potential fruit size are essential to enable growers to optimize fruit size by either fruit thinning or irrigation. 80

Fruit diameter (mm)

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70

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60 1995; r 2=0.58 1996; r 2=0.56 55 0

50

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Specific reproductive water use (m3 ⋅ t–1)

Fig. 3.7. The effects of irrigation rate per tonne of fresh weight (in addition to a constant irrigation level for the maintenance of the canopy structure and foliage) on ‘Golden Delicious’ apple fruit diameter in 1995 (n = 79) and in 1996 (n = 92) (Source: Naschitz and Naor 2005).

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The reproductive cell division lasts up to 40 days post bloom (Westwood 1993). Temperatures lower than 25°C during the reproductive cell division phase reduced apple fruit size (Tromp 1997; Warrington et al. 1999), but, on the other hand, the number of cells in apples decreased when the trees were grown at 35/15°C (day/night) rather than 25/15°C (M. Flaishman and A. Naor, unpubl.). It suggests that there is an optimum temperature for reproductive cell division, and limitations in potential fruit size are expected in both cold and hot climates. The previous-year crop yield (Bergh 1985) affects the initial cell number in the pedicle of the apple at bloom time: the greater the previous yield, the smaller the number of cells in the receptacle in the current year. The current-year crop level affects the number of cells, and the timing of fruit thinning affects the number of cells and the potential fruit size in apple (Quinlan and Preston 1968; Goffinet et al. 1995). Thus, potential fruit size is expected to vary from year to year according to the temperature regime during the reproductive cell division phase, the previous- and current-year crop levels, and the timing of fruit thinning. Models based on the effect of temperature on reproductive cell division were proposed as a tool for predicting final fruit size in apple (Austin et al. 1999; Stanley et al. 2000, 2001); such models might enable the grower to adjust his irrigation level and thinning strategy early in the season. Other models, which assume a given seasonal pattern of fruit growth (Assaf et al. 1982; Lakso et al. 1995) can also be utilized for that purpose, but the first relevant predictions can be expected only two or three weeks into the main fruit growth phase. 4. Application Efficiency. Application efficiency is the fraction of the irrigation water that remains in the main root zone and is available for the plant use, and is rarely close to 1. Its accurate evaluation requires intensive measurement of the soil moisture distribution in the soil profile, and the less uniform the soil, the greater the number of measurements required for proper assessment. Spatial variability of soil depth and of soil hydraulic properties may cause non-uniform application efficiency, with the lowest value expected at the shallowest levels. Maximum application efficiency can be attained through appropriate choices of emitter density and of recharge and irrigation intervals. Further increases in application efficiency can be achieved by combining blocks of uniform soil depth and soil hydraulic properties for a given irrigation operation. The irrigation should be increased by the proportion of inefficiency, but under commercial field conditions there is always uncertainty about the actual value of application efficiency.

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B. The Grower’s Dilemma In commercial orchards, there is a wide diversity of combinations of cultivars, rootstocks, training systems, crop loads, potential fruit sizes, and irrigation efficiencies, and, since each combination can affect irrigation requirements differently, there is a need to adjust the general set of crop coefficients for each particular plot. The growers have limited possibilities to quantitatively estimate the effect of each of the above-mentioned factors on the crop coefficient, and they are left with uncertainty about how to determine the irrigation amount for each specific plot. In order to visualize the grower’s dilemma, consider the response of marketable yield to irrigation level, as depicted in Fig. 3.8. A reasonable grower would choose irrigation level A and expect it to elicit a marketable yield level B. However, if the canopy size and crop level in a particular orchard were greater, and application efficiency lower than the experimental site where the response curve was determined, the actual response curve might shift to the right (dashed line), so the choice of irrigation level A would lead to a significantly lower marketable yield (C). The response of a reasonable grower would be to apply a safety factor and increase irrigation in order to get high marketable yield (D) and would hope not to reach E, which could happen if fruit development were in phenological stages in which deficit irrigation was beneficial.

D

B

Marketable yield

E

C

A Irrigation level Fig. 3.8.

Hypothetical response of marketable crop yield to irrigation level.

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C. The Use of Water Stress Indicators A curve that depicts the response of marketable yield to plant water status (e.g., Fig. 3.9A, B), rather than to irrigation level (Fig. 3.8), might provide a partial solution to the grower’s irrigation dilemma. A threshold value of water status could be determined from the response curves (e.g., Fig. 3.9) and the product of crop and stress coefficients would be adjusted by trial and error until the threshold water status was reached. Setting a threshold is composed of physiological and horticultural response to the water stress indicator reading and economical considerations such as the amount of water that can be saved and the costs of water stress monitoring—the closer the threshold to the point where a damage can occur the more frequent and intensive water stress assessment should be performed. The use of a water status threshold based on the response curves (e.g., Fig. 3.9A, B) eliminates the uncertainties related to application efficiency, canopy size, and, to a certain extent, crop level. However, thresholds may change from year to year according to potential fruit size (Fig. 3.7); they may also differ in plots where the crop load is extremely high. The response curves (e.g., Fig. 3.9) might also differ among cultivars according to their tendency to produce large fruit, and among rootstocks, which could affect tree hydraulic architecture. Different thresholds might be needed for different climatic regions, because of differences in light intensity and temperature, which could alter the relationships between tree water status and the amount of assimilates available for the accumulation of dry matter. However, the

Relative yield (% of total)

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Fig. 3.9. Relative yield of nectarine (A) (Naor et al. 2001) and apple (B) (A. Naor, unpubl.) as a function of midday stem water potential. Bars denote SE.

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question of the transferability of thresholds for irrigation scheduling has not yet been addressed experimentally in any water stress indicator. In the following sections, the relevance and applicability of water stress indicators, as well as their limitations, are discussed in detail. The discussion includes issues such as responses to moisture availability and variability, and correlation with yield and quality attributes. 1. General Requirements for a Water Stress Indicator. The choice of a good water stress indicator for irrigation scheduling involves the following requirements: 1. Readings of water stress indicator should be correlated and consistent with horticultural parameters of economic importance: crop yield, fruit size, fruit growth rate, fruit quality, etc. In light of these relationships, a threshold for irrigation scheduling can be set, taking into account economical aspects. Water stress indicator readings should be correlated with assimilation rate or stomatal conductance, since optimizing the availability of assimilates is a major goal of irrigation. High correlation of the water stress indicator with horticultural parameters of economic importance is a prerequisite, and once it has been met the following requirements should be examined. 2. Response to moisture and irrigation regime—water stress indicator values should respond to the irrigation regime, especially near optimal conditions. 3. General applicability—thresholds for irrigation scheduling are usually based on controlled irrigation experiments. The transferability of thresholds to each commercial plot and the procedure for adjusting thresholds need to be straightforward. 4. Variability of the readings—this is an important issue since it determines how many measurements should be taken in order to properly represent the water status of a commercial plot. The number of measurements and the ease of operation and interpretation, as well as cost, may determine (on an economic basis) the efforts that should be invested in water status assessment in commercial orchards. 5. Early detection of water stress may allow the grower to respond by adjusting the irrigation regime before a significant irreversible damage occurs. There are many good water stress indicators, such as stomatal conductance and assimilation rate, or tree transpiration rate, that are useful for research but are not applicable for irrigation scheduling because

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of cost, and the complexity of operation and/or interpretation of the data. Therefore, only water stress indicators that have been proposed for or have potential for use in irrigation scheduling in commercial orchards are reviewed. 2. Types of Water Stress Indicators Available for Commercial Use. There are three major groups of water stress indicators in terms of the practical meaning of the measurement. (1) Those that estimate moisture availability—the ability of the soil to supply the water at an adequate rate —where the desired rate is dictated by the changing evaporative demand. Soil water stress indicators and predawn leaf water potential belong to this group. (2) Those that estimate peak daily water stress, including midday stem water potential, midday leaf water potential, and daily trunk shrinkage. (3) Those that provide information related to average daily water stress—daily transpiration, daily growth of fruit or trunk or other plant tissues. 3. The Relevance of Plant Water Stress Indicators. The relevance of a water stress indicator is determined by either direct correlation with horticultural attributes having an economical value, such as crop yield, fruit size, and fruit quality, or correlation with physiological parameters that are indirectly related to horticultural attributes having an economical value, such as stomatal conductance, assimilation rate, or shoot growth. Direct Correlation. Midday stem water potential prior to harvest was highly correlated with fruit size in apple (Naor et al. 1995, 1997b; Ebel et al. 2001; Fig. 3.8), nectarine (Naor et al. 1999, 2001), pear (Ramos et al. 1994; Naor et al. 2000; Naor 2001), and Japanese plum (Intrigliolo and Castel 2005; Naor 2004), whereas practically no correlation was apparent between midday leaf water potential and fruit size in one experiment in apple (Naor et al. 1995). Fruit growth rate was correlated with daily trunk shrinkage, predawn leaf water potential, and midday stem water potential in apple (Bonany et al. 2000); and the highest, medium and lowest correlations were exhibited by the daily trunk shrinkage, the predawn leaf water potential, and the midday stem water potential, respectively. Midday stem water potential was highly correlated with pear fruit growth rate (Marsal et al. 2002a), and the faster the growth rate the higher the correlation. The postharvest midday stem water potential was correlated with the following season’s crop yields of nectarine (Naor et al. 2005) and Japanese plum (Johnson et al. 1994), and postharvest midday leaf water potential was correlated with the following season’s fruit set in peach (Girona et al. 2003). Postharvest midday stem water

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potential was highly correlated with subsequent season proportion of twin fruit (Fig. 3.5). Indirect Correlation. Stem water potential was highly correlated with stomatal conductance or assimilation rate in apple (Naor et al. 1995; Naor 1998), nectarine (Naor 1998), pear (Naor 2001; Marsal et al. 2002a), plum (Naor 2004), and prune (Lampinen et al. 2004). Leaf water potential was correlated with stomatal conductance or assimilation rate in apple (Naor 1998), pear (Naor 2001), nectarine (Naor 1998), peach (Garnier and Berger 1987; Escobar-Guttirez et al. 1998), and plum (Naor 2004). The correlation of midday stem water potential with stomatal conductance was better than that of midday leaf water potential with stomatal conductance in apple, pear, nectarine, and plum (Naor 1998, 2001, 2004), and this applied whether the leaves were covered before or after excision (Naor 2004), a finding that eliminates the possibility that the better correlation of stem water potential with stomatal conductance was due to measurement error (Williams and Araujo 2002). The response of stomatal conductance to water potential changed in the course of the season (Marsal and Girona 1997; Marsal et al. 2002a), which may affect thresholds for irrigation scheduling. D. Response to Moisture and Irrigation Regimes Most studies have compared extreme water regimes and there are very few that enable the construction of curves that describe the response of plant water status to irrigation levels (Lampinen et al. 1995; Naor et al. 1997b, 1999, 2000, 2001, 2004; Goldhamer and Viveros 2000; Shackel et al. 2000b). Predawn leaf water potential was highly correlated with the preharvest irrigation level (Goldhamer and Viveros 2000) in almond (Fig. 3.10); midday stem water potential was highly correlated with the irrigation level during the main fruit growth phase (Naor et al. 2000) in pear (Fig. 3.10). In prune, the seasonal average of midday stem water potential was highly correlated with annual irrigation level (Lampinen et al. 1995) when different irrigation regimes were applied at different phenological stages, which may indicate that plant water status responds similarly to irrigation level at all phenological stages. Significant reductions in soil moisture content have been observed before the occurrence of reductions in predawn leaf water potential (Garnier and Berger 1987; Girona et al. 1993b; Ruiz-Sanchez et al. 2004), midday stem water potential (Shackel et al. 2000a; Ebel et al. 2001; Romero et al. 2004), and relative transpiration (Ferreira et al. 1997). It may suggest that a significant reduction in moisture content should occur before soil moisture availability starts to decrease.

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Cumulative irrigation level (mm) Fig. 3.10. Effects of cumulative irrigation level on predawn leaf water potential in Nonpareli almond (closed triangle), and on midday stem water potential in French prune (open triangle), and in Spadona pear (open circle).

Relative transpiration was highly correlated with predawn leaf water potential in a drying cycle in peach (Ferreira et al. 1997; Valancogne et al. 1997), plum, apple, and walnut (Valancogne et al. 1997). However, the relationships between relative transpiration and predawn leaf water potential changed in the course of the season (Valancogne et al. 1997), suggesting that thresholds for irrigation scheduling might change along the season as well. In spite of the high responsiveness of predawn leaf water potential to the irrigation regime and to soil moisture content in the range within which it affects transpiration, setting a threshold might be a problem under nonhomogenous soil conditions, which are commonly found in commercial orchards. It was argued that predawn leaf water potential equilibrates with the wettest parts of the root zone (Dirksen and Raats

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1985; Garnier and Berger 1987; Breda et al. 1995; Ameglio et al. 1999), whereas the opposite was apparent for cotton (Jordan and Ritchie 1971). Ameglio et al. (1999) demonstrated that relative transpiration was highly correlated with predawn leaf water potential in homogenous soils but not in heterogeneous soil profiles. This suggests that the predawn leaf water potential in heterogeneous soils does not correlate with average soil moisture content in the entire root zone, and therefore does not properly represent the soil moisture availability—the ability of the soil to meet the peak demand for water by the trees. The predawn leaf water potential of soybean grown in compartmented nutrition solutions of differing osmotic potential was equal to the average of the water potentials of the two compartments (Maertens and Blanchet 1981; Cited by Ameglio et al. 1999); as nutrition solutions introduce no hydraulic limitations in the growing medium, this suggests the responses of transpiration to predawn leaf water potential is dependent on the soil hydraulic properties. Therefore, different thresholds would be needed for different soil hydraulic properties and it may limit the transferability of predawn leaf water potential thresholds for irrigation scheduling from one site to another. There is a possibility that under extremely heterogenous soil hydraulic properties conditions, predawn leaf water potential will not represent properly the average soil moisture availability (Ameglio et al. 1999). E. Sensitivity of Water Stress Indicators The sensitivity of a water stress indicator relates to the degree of change in water status that can be detected statistically, i.e., the least significant difference for a given number of measurements. The sensitivity of a water stress indicator is expected to increase with the level of response of the sensor to changes in water status, and to decrease with increasing variability between sensors/readings. Goldhamer et al. (2000) employed the following terminology to compare sensitivity of different water stress indicators: “signal”—is the extent of response of the water stress indicator to changes in water status or water availability; “noise”— is the variability between readings of different sensors; and “sensitivity” is the signal/noise ratio. Midday stem water potential was more sensitive than midday leaf water potential in many deciduous trees (Garnier and Berger 1985; Higgs and Jones 1991; McCutchan and Shackel 1992; Behboudian et al. 1994; Naor et al. 1995; Naor 1998; Marsal et al. 2000; Girona et al. 2004). This suggests midday leaf water potential is inferior to midday stem water potential as a water stress indicator (Fig. 3.11).

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Israel saving time (h) Fig. 3.11. Effects of low (triangle-dotted line) and high (circle-solid line) irrigation levels on diurnal leaf (closed symbols) and stem (open symbol) water potentials in apple on Aug. 4, 2003 (Naor et al. 1995).

Daily trunk shrinkage gave a stronger signal than midday stem water potential (Goldhamer et al. 2000; Goldhamer and Fereres 2001; Fereres and Goldhamer 2003; Naor and Cohen 2003; Intrigliolo and Castel 2004), but the noise (variability ) of the daily trunk shrinkage was higher than that of midday stem water potential (Goldhamer et al. 2000; Goldhamer and Fereres 2001; Fereres and Goldhamer 2003; Naor and Cohen 2003; Intrigliolo and Castel 2004; Fig. 3.12). The sensitivity (signal/noise ratio) of daily trunk shrinkage was found to be higher than that of midday stem water potential in some studies (Goldhamer and Fereres 2001; Goldhamer et al. 1999), but the opposite was found in other studies (Naor and Cohen 2003; Intrigliolo and Castel 2004).

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Relative differences between stressed and control trees (% of control)

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Fig. 3.12. The responses of midday stem water potential (SWP) and daily trunk shrinkage (DTS) to withholding of irrigation for 17 days (bold horizontal bar) in apple. Bars denote SE (Source: Naor and Cohen 2003).

F. Early Detection of Water Stress Use of predawn leaf water potential, midday stem water potential, and cumulative transpiration rate enabled the detection of water stress earlier than the use of midday leaf water potential and canopy temperature (Remorini and Massai 2003). Water stress was detected earlier by using midday stem water potential than by using midday leaf water potential (Selles and Berger 1990), daily trunk shrinkage (Goldhamer et al. 2000; Naor and Cohen 2003), and daily transpiration (Naor and Cohen 2003). In other studies, water stress was detected earlier by using daily trunk shrinkage than by using midday stem water potential (Intrigliolo and Castel 2004), predawn leaf water potential, midday leaf water potential, or midday stem water potential (Goldhamer et al. 1999). Use of predawn leaf water potential enabled the detection of water stress earlier than the use of midday leaf water potential (Girona et al. 1993b; Goldhamer and Viveros 2000; Ruiz-Sanchez et al. 2000b). It can be concluded that midday leaf water potential and canopy temperature were inferior to other parameters as indicators of water stress. However, the relative merits of daily trunk shrinkage, midday stem water potential, and predawn leaf water potential in early water stress detection are not clear. G. Representing Water Status on an Orchard Basis This section deals with the efforts in terms of the number of measurements that are required for representing tree water status on an orchard

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basis within acceptable uncertainty; this topic covers the within-tree and root-zone variability and the orchard-wide spatial variability. An acceptable variability depends on how close the threshold is to a point at which damage can occur and the probability of the actual tree water status to be beyond that point. 1. Within Tree and Root Zone Variability. The thresholds of soil water stress indicators are intended for evaluating the ability of the soil to meet the peak demand for water by the tree. Moisture availability is dependent on: the distribution of the sink strength of the water-absorbing roots; the soil moisture distribution; and the distribution of soil hydraulic properties, including those in close proximity to the roots. The average soil moisture availability within the root zone can be evaluated by using three-dimensional water transport models, assuming those distributions are available. However, the root-zones of perennial trees are irregular and usually occupy a non-uniform soil volume that is larger than the irrigated volume. Therefore, modeling moisture availability is not practical, and the choice of locations to monitor the soil water status remains problematic, and the ability to determine thresholds for soil water stress indicators is limited. Soil water stress indicators were reported to have greater variability than daily trunk shrinkage and midday stem water potential (Naor et al. 1995, 1999, 2000, 2005; Goldhamer and Fereres 2001; Intrigliolo and Castel 2004; Fig. 3.13). The tree responds to average soil moisture availability and the tree water status indicators readings reflect the response to the average soil moisture conditions in terms of tree water status, thus avoiding the within root zone variability; this may account for the consistently greater variability of soil-based water stress indicators than of plant-based ones. In spite of the above-mentioned limitations, soil water status sensors are the most popular water stress indicators for irrigation scheduling (Phene et al. 1990; Howell 1996), including that of perennial trees. In general, these indicators are easy to use and most of them provide analog outputs that enable continuous on-line monitoring. Thus, growers need to apply only empirical, site-specific calibration when they rely on soil water stress indicators to guide the decision on when to irrigate. Within-tree variability should be taken into account for proper representation of tree water status: the stem water potential decreases along the transport pathway, and the gradient increases with increasing transpiration rate. Gradients of stem water potential of 0.08–0.09 MPa.m–1 (Olien and Lakso 1986) and of 0.2 MPa.m–1 (Jones et al. 1991) were reported for apple, and of 0.15 MPa.m–1 for peach (Garnier and Berger

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8 6

90 cm

10

60 cm

LWP SWP TS SWT 30 cm

Population standard error (% of the population mean)

12

4 2 0 Apple

Nectarine

Pear

Fig. 3.13. Standard error of midday leaf (LWP) and stem (SWP) water potential, daily trunk shrinkage (TS), and soil water tension at 30, 60, and 90 cm depth, in apple, nectarine, and pear (Naor et al. in press). A set of 27, 27, and 30 trees in close vicinity were selected in apple, nectarine, and pear, respectively, and a single measurement of each of the water stress indicators was taken in each tree.

1986). In semi-arid zones, where transpiration rates are higher, these gradients are expected to be greater. These findings suggest that, in order to represent the average tree water status properly and to minimize variability, measurements should be taken in the middle of the canopy close to the trunk. Inconsistent procedures such as the duration needed for covered leaves to reach equilibrium with stem water potential (Fulton et al. 2001) or the pressure increase rate (Naor and Peres 2001) may affect variability. 2. Spatial Variability. Soil water content is spatially variable within an orchard; therefore, one would need dozens of measurements in order to represent the soil water status properly on an orchard scale (e.g., Warrick and Nielsen 1980; Russo and Bresler 1982). A test case—Midday stem water potential as measured by growers using five-leaf samples in a few commercial apple orchards were compared with those obtained by using randomly selected 25-leaf samples in each of the commercial orchards under study (Naor et al. in press); the differences between the two sets of measurements ranged from 0.03 to 0.21 MPa (Table 3.1). The minimum sample size for each plot for different acceptable deviations was calculated from the variability of the

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Table 3.1. The differences between apple midday stem water potential on a five-leaf sample selected by the grower and a 25-leaf sample randomly selected in a commercial orchard. Sample size for differences in SWP (MPa) lower than: Orchard El-1 El-2 If-1 If-2 Me-1 MG-1 MG2 EZ-1 EZ-2

0.075

0.1

0.15

Absolute difference in SWP (MPa) between experimental sets and commercial sets

27 27 18 15 28 8 10 7 7

15 15 11 8 16 5 6 4 4

7 7 5 4 7 2 3 2 2

0.14 0.21 0.21 0.21 0.04 0.05 0.15 0.11 0.03

Source: Naor et al. in press.

25-leaf samples, and it ranged from four to 15 leaves, depending on the specific variability of each plot. This indicates that growers could evaluate the variability of each plot to determine the sample size needed for water stress assessment. Soil hydraulic properties have a statistical structure, i.e., the correlation between measurements increases as the distance between them decreases (Warrick and Nielsen 1980). The number of measurements a grower can take in a single plot is economically limited, and the statistical structure of the hydraulic properties may serve to determine the minimum distance between neighboring measurement locations (Or 1995; Plana et al. 2002). Mapping relative tree water stress by using remote sensing of canopy temperature (e.g., Meron et al. 2003) might provide the growers with a means of selecting representative sites within an orchard; such a tool could help reduce sample size and the cost of water stress monitoring. In addition, the pattern of canopy temperature distribution might provide the grower with information about extreme conditions related to malfunctioning of the irrigation system, variable irrigation efficiencies, or other factors. H. Considerations in Setting Thresholds The effects of irrigation on horticultural yields and quality are complex: the dominant effect is on the availability of assimilates, which is known

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to limit production (Grossman and DeJong 1995a,b), whereas other factors, such as canopy temperature, nutritional status, and plant growth regulators may interact with the availability of assimilates and the vegetative-to-reproductive growth ratio. Water stress indicators do not evaluate the above-mentioned processes directly, but do so only through variables that correlate with them. Therefore, thresholds for irrigation scheduling might change from one site to another because of factors such as cultivars, rootstocks, crop loads, and climatic conditions that may influence the availability of assimilates. The factors to be considered in setting thresholds for minimum stress conditions, which is the simplest situation, as well as for deficit conditions, are discussed below. 1. Minimum Stress Conditions Account for Evaporative Demand. The midday stem water potential of well irrigated trees decreases with increasing evaporative demand, because of the high resistance to water flow from the bulk soil to the tree xylem vessels. As a result, the water balance (the amount of water absorbed minus the amount of water transpired) becomes more negative with increasing evaporative demand, leading to a lowering of the midday stem water potential. McCutchan and Shackel (1992) developed relationships between midday stem water potential of well irrigated prune trees and daily maximum vapor pressure deficit, whereby the threshold of midday stem water potential should be adjusted by 0.12 MPa for each change of 1 kPa in maximum vapor pressure deficit. A similar response of midday stem water potential to maximum vapor pressure deficit was found for almond (Shackel et al. 1997, 1998), but a slightly lower response (Fereres and Goldhamer 2003); no correlation was found between midday stem water potential and maximum vapor pressure deficit (Goldhamer et al. 2000) probably because all the treatments were under stress conditions. A change of midday stem water potential by 0.1 MPa per 1-kPa change in maximum vapor pressure deficit was found for apple (A. Naor, unpubl.). The above-mentioned response of midday stem water potential to maximum vapor pressure deficit can be utilized to adjust the thresholds and thus avoid unnecessary irrigations on days of high evaporative demand. Daily trunk shrinkage was found to be highly responsive to maximum daily vapor pressure deficit in almond (Goldhamer et al. 2000; Fereres and Goldhamer 2003; Goldhamer and Fereres 2004) and apple (A. Naor, unpubl.), for which the correlation with vapor pressure deficit was higher than that of midday stem water potential with vapor pressure

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deficit. Changes of 0.03 to 0.08 mm in daily trunk shrinkage per unit change in maximum vapor pressure deficit were reported for almond (Goldhamer et al. 2000; Fereres and Goldhamer 2003; Goldhamer and Fereres 2004). Corrections for the response of daily trunk shrinkage to maximum daily vapor pressure deficit were used in scheduling irrigation of almonds (Goldhamer and Fereres 2004) where quite stable midday stem water potentials were apparent for each of the two daily shrinkage thresholds that were examined. In diurnal measurements, leaf water potential had lower correlation with whole trunk contraction than with trunk xylem contraction (excluding the bark) (Ueda and Shibata 2001). Similar responses of the trunk xylem contraction to leaf water potential were apparent for four consecutive days (Ueda and Shibata 2001), whereas the response of the contraction of the whole trunk varied from one day to another. The high resistance to water transport from bark to xylem, which is exhibited as a lag of trunk diameter changes behind stem water potential (Cohen et al. 2001), may explain the day-to-day variability in the relationships between trunk diameter changes and leaf water potential. It may also account for the higher dependence of daily trunk shrinkage on maximum daily vapor pressure deficit than midday stem water potential (Goldhamer et al. 2000; Fereres and Goldhamer 2003; Goldhamer and Fereres 2004). Diurnal changes in leaf thickness in apple did not lag at all behind the changes in stem water potential, unlike trunk contraction (A. Naor, unpubl.) and it was highly correlated with leaf water potential (Syvertsen and Levy 1982), indicating that it might offer an advantage over trunk contraction measurements. However, the response of leaf thickness to water status varies between leaves (McBurney 1992), and calibration of the threshold would be required. It should be emphasized that consideration of trunk xylem contraction and leaf thickness contraction for irrigation scheduling are in the very early stages of examination. In addition, based on the small daily trunk xylem contraction, errors from a significant thermal contraction may arise (Irvine and Grace 1997). Seasonal Drift in Tree Water Status. There are a few examples of seasonal decrease in tree water status when minimum water stress was expected, irrespective of the effect of evaporative demand (Lampinen et al. 1995; Shackel et al. 1998; Goldhamer and Fereres 2001; Intrigliolo and Castel 2004). It could be that a higher value of KC should be used, to take into account different seasonal dynamics of canopy size, greater

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crop load, and lower application efficiency in the above-mentioned reports than in the experiments used for the determination of KC values, raising a possibility of insufficient irrigation. At the beginning of the season, the soil profile retains enough moisture from winter precipitation to compensate for unsatisfactory irrigation, but as the season progresses the initial reservoir is exhausted, which may result in a decrease in midday stem water potential. The root volume at the beginning of the season is larger than the irrigated volume as roots are absorbing moisture that remained from winter precipitation, but as the season progresses the effective root volume decreases and converges to the irrigated soil volume; this may decrease the water absorption capacity (Naor et al. 2000) due to increased root resistance to water transport, which, in turn, may affect the midday stem water potential. 2. Setting Thresholds for Daily Trunk Shrinkage. The seasonal pattern of daily trunk shrinkage was found to be less stable than that of midday stem water potential (Goldhammer and Fereres 2001; Intrigliolo and Castel 2004; J. Marsal et al. unpubl.; A. Naor, unpubl.), and the high correlation between daily trunk shrinkage and the daily maximum vapor pressure deficit (Goldhamer et al. 1999, 2000, 2001) only partially accounts for this instability. To account for such instability Genard and Huguet (1999) used well-irrigated peach trees as an internal reference to calculate relative daily trunk shrinkage, which provided good predictions of the effects of water stress on fruit growth. Goldhamer and Fereres (2001, 2004) proposed the use of internal references of well-irrigated trees for irrigation scheduling to correct for the response of daily trunk shrinkage to vapor pressure deficit, and they discussed a few considerations relating to the internal reference. The number of dendrometers to be installed in the well-irrigated reference plot must be considered, because of the variability of daily trunk shrinkage. Possible changes in tree size and therefore in water consumption and daily trunk shrinkage caused by long-term excessive irrigation of the reference plot should also be taken into account—it may create a situation in which the reference trees and the orchard trees are not similar anymore, thus a change of the reference trees might be required along the season. Combined Use of Midday Stem Water Potential and Daily Trunk Shrinkage. Midday stem water potential has been found to be a relevant and reliable water stress indicator, but its use is labor intensive, and measurements are limited to about two hours a day around midday. In addition, the measurements do not yield an analog output, and therefore are

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not amenable to automatic data acquisition. Daily trunk shrinkage, on the other hand, is highly responsive, easy to use, and yields an analog output, but setting a threshold is problematic. Therefore, calibration of daily trunk shrinkage against stem water potential may provide thresholds for the use of daily trunk shrinkage for irrigation scheduling. Daily trunk shrinkage is highly correlated with stem water potential (Goldhamer et al. 1999, 2000, 2003; Bonany et al. 2000), but the relationships change during the season (Marsal et al. 2002b; Fereres and Goldhamer 2003; Intrigliolo and Castel 2004). This may necessitate periodical recalibration of the relationships, but the necessary frequency of recalibration against stem water potential is yet to be determined experimentally. The above-mentioned combined use of midday stem water potential and daily trunk shrinkage could be adapted to other easy-touse water stress indicators that have difficulties in setting thresholds for irrigation. 3. Setting Thresholds Under Deficit Irrigation Conditions. Deficit irrigation is a common irrigation practice during some phenological stages, and it introduces some major difficulties in the use of several water stress indicators. Thresholds for irrigation scheduling in stressed conditions may be determined in regional experiments that produce response curves. For example, in the case of postharvest irrigation of nectarines the optimal midday stem water potential would be about –2.0 MPa (Fig. 3.5), which is a value that allows water saving without risking the occurrence of twin fruits. Except for one study (Goldhamer et al. 2000), the variability of all water stress indicators increases with increasing water stress (Johnson et al. 1994; Naor et al. 1995, 2000, 2004; Ruiz-Sanchez et al. 2000b; Naor and Cohen 2003) and therefore more measurements will be needed for water stress assessment under deficit irrigation. The use of reference trees for setting thresholds for irrigation scheduling according to daily trunk shrinkage does not apply under deficit (stressed) conditions. The response of daily trunk shrinkage to midday stem water potential decreases under high water stress conditions (Bonany et al. 2000; Goldhamer et al. 2000), probably as a result of a significant decrease in the morning readings (maximum values). For the same reason, the daily trunk shrinkage under severe water stress might be less than that under less severe stress (Besset et al. 2001), and this could result in a misleading interpretation. Both predawn leaf water potential and midday stem water potential provided clear distinctions between different stress

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conditions (Fig. 3.10), including severe water stress (Johnson et al. 1994; Naor et al., 2005; Ruiz-Sanchez et al. 2000b). I. Conditions of Limited Response to Irrigation There are significant resistances along the flow path of the water from the soil into the tree and also in specific places within the tree (Jones 1992). Therefore, diurnal water transport in the tree is under non-steadystate conditions, and when there is high evaporative demand and conductance is low, the response to irrigation might be limited. 1. Soil-root Zone Limitations. Midday stem water potential under high soil-moisture availability decreases with increasing vapor pressure deficit (McCutchan and Shackel 1992), because of the high resistance to water flow in the soil-root zone. In soils with high clay contents, the midday stem water potential is lower than in soils with low clay content (Naor et al. 2000; O’Connell and Goodwin 2004), even under full irrigation; this indicates that there may be some limitation to the water absorption capacity of the root system in these soils. Such a limitation could be related to lower oxygen fluxes into the root zone, or to mechanical resistance to root growth (Taylor 1983) or low soil hydraulic conductivity. The choice of an appropriate rootstock could improve water absorption capacity (Atkinson 1980): for instance, a higher midday stem water potential was found in pear grafted on Betulifolia than on Quince C (R. A. Stern and A. Naor, unpubl.). 2. Fruit Pedicle Limitations Early Season Limitation. Water stress affects fruit set and abscission of fruitlets in apple (A. Naor, unpubl.; Powell 1974). The pedicle water conductance in apple is low for the first two weeks after bloom (Drazeta et al. 2004a), but a dramatic increase occurs at the end of the second week after bloom, and a further slight increase a couple of weeks later. The diameter of the xylem vessels and, therefore, their conductance decreases towards the end of the pedicle adjacent to the abscission zone. Under conditions of high evaporative demand and, therefore, of high fruit transpiration rate, pedicle conductance could impose a limitation that would limit the possibility of relieving fruit water stress by increasing the irrigation rate. Preharvest Limitation. The conductance of the peach fruit surface was found to increase in the course of the season, and in most cultivars the

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increase occurred close to harvest (Lescourret et al. 2001), therefore fruit transpiration is expected to increase along the season. In contrast, in apples fruit transpiration decreased during the season (Tromp 1984). Fruit surface conductance was found to be much higher in peach, nectarine (Lescourret et al. 2001), and pepper (Aloni et al. 1998) than in apple (Lang 1990), grape (Lang and Thorpe 1989), or tomato (Lee 1990); and in peach and pepper (Aloni et al. 1998; Lescourret et al. 2001) its increase towards harvest was attributed to the increased size of microcracks with increasing fruit surface area. Maguire et al. (1999) showed that the proportion of Braeburn apples showing microcracks increased with increasing fruit surface conductance. Lescourret et al. (2001) showed by means of a model simulation (Fishman and Genard 1998) that towards harvest fruit growth decreases as surface conductance increases, because the high tree water status could not compensate for the increased fruit water loss through the highly permeable fruit surfaces. The growth rate of Japanese plum fruits decreased dramatically under high evaporative demand (Naor et al. 2004), and the decrease was greater than could be accounted for by the parallel decrease in stem water potential. A decrease in net water transport through the xylem vessels to the fruits was reported for apples (Lang 1990); it was accounted for by a reduction in the conductance of the xylem vessels in the course of the season (Lang 1990; Lang and Ryan 1994; Drazeta et al. 2004b). It seems that partial blockage of xylem vessels may reduce the capability of high irrigation rates to compensate for the increased water losses through the fruit surface that are caused by high surface conductance, especially under conditions of high vapor pressure deficit. Therefore, high evaporative demand close to harvest is expected to decrease fruit size in conditions of high fruit surface conductance.

V. CONCLUDING REMARKS Research in the past two decades has clearly shown that growers may benefit from deficit irrigation in certain phenological stages. This may be accomplished both by saving water and by improving productivity and fruit quality. Stone fruits in the pit hardening stage are not sensitive to moderate water stress, however, the duration of the pit hardening stage varies with harvest date and there is a risk of missing the end of this stage and then decreasing fruit size by extending the water stress well into the final fruit growth stage; therefore it seems that in many cases the potential bene-

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fit will not justify the risk. In early-maturing cultivars, the duration of the pit hardening stage is too short for deficit irrigation to be considered. Excessive canopy growth due to high irrigation levels decreases subsequent season productivity both early in the season and post harvest; severe water stress decreased subsequent season productivity as well. Thus, moderate water stress, which controls canopy growth and avoids damage to the developing reproductive buds, seems to be optimal in terms of subsequent season productivity. Deficit irrigation in the reproductive cell division stage and in the final fruit growth stage decreases fruit size at harvest. Therefore, water stress should be avoided during the main fruit growth stages unless extreme conditions of high vigorous trees are apparent or in high-density orchards. In order to avoid the risk of decreasing fruit size in those extreme situations, other practices of controlling shoot growth such as shoot bending or the use of plant growth retardant should be considered. Water stress during fruit growth accelerates maturation and improves fruit firmness, total soluble solids content, and fruit color, but it decreases fruit size, which is a major attribute of fruit quality. It seems that one would be able to benefit from deficit irrigation during the fruit growth stage only when potential fruit size is higher than the optimal marketable size; thus, both optimal fruit size and improved fruit quality can be gained in such conditions. Evidence for any effects of deficit irrigation on aroma compounds is inconclusive. Severe water stress in the bud development stage increases the proportions of twin fruits and of fruits with deep sutures in peach and nectarine. The present review indicates that the process of making decisions on irrigation is complex because it involves many factors (physiological, phenological, agronomical, meteorological, and economic). Unfortunately, each of these factors is subject to uncertainty; therefore, the grower has to monitor the response of each specific orchard to a given irrigation regime and to adjust the latter accordingly. The use of water stress indicators may enable the grower to adjust irrigation and to compensate for the effects of canopy size, application efficiency, and (partly) of crop load on irrigation level. Data collected in the past decade suggest that soil water stress indicators are more variable than plant water stress indicators; midday leaf water potential was found to be inferior as an indicator to midday stem water potential, predawn leaf water potential, and daily trunk shrinkage. Setting thresholds is more complicated for soil water stress indicators and for daily trunk shrinkage in general, especially under deficit irrigation conditions, and for predawn leaf water potential in heterogeneous soils.

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The issue of transferability of threshold of water stress indicators for irrigation scheduling from one region to another is an extremely important issue that was not addressed experimentally yet for all the water stress indicators. The use of an unstressed internal reference might avoid the need to set thresholds for daily trunk shrinkage in some cases when no deficit irrigation is applied. There is room for decision support systems that would handle the decision-making process and simplify it for the grower. The development of a decision support system would not involve new research, but would necessitate the manipulation of existing physiological and horticultural knowledge, together with cumulative regional experience and the experience of the specific grower who is to use the decision support system. The use of the cumulative experience could reduce the uncertainty and compensate for the gaps in scientific knowledge for specific orchard conditions. The input to a decision support system could include meteorological data from which ET0 and vapor pressure deficit could be calculated, water meter data from which actual irrigation levels and actual irrigation coefficients could be calculated, seasonal dynamics of fruit size from which the expected fruit size at harvest could be calculated, tree water status and soil water status. A decision support system would be able to compare the performance of each particular plot with that of neighboring plots. In addition, the use of historical information could facilitate comparisons between the actual, present-day performance with that under similar conditions (e.g., meteorological, crop load) in the past. Commercial orchards are spatially variable with respect to soil hydraulic properties, soil depth, irrigation application and crop load, all which may affect the optimal irrigation level for each specific tree or subplot. Remote sensing of canopy temperature already enables the grower to produce maps of relative water stress, and further developments might enable him to map canopy size and crop load. Based on such maps, growers might be able to produce high-resolution maps of irrigation level. The limit to the resolution of such maps would be the ability to adjust the irrigation level at high spatial resolution in commercial orchards; and this introduces a challenge to the irrigation equipment industry.

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Shackel, K. A., B. Lampinen, S. Sibbett, and W. Olson. 2000a. The relation of midday stem water potential to the growth and physiology of fruit trees under water limited conditions. Acta Hort. 537:425–430. Shackel, K. A., B. Lampinen, S. Southwick, W. Krueger, J. Yeager, and D. Goldhamer. 2000b. Deficit irrigation in prunes: Maintaining productivity with less water. HortScience 35:30–33. Stanley, C. J., D. S. Austin, G. B. Lupton, S. McArtney, W. M. Cashmore, and H. N. de-Silva. 2000. Towards understanding the role of temperature in apple fruit growth responses in three geographical regions within New Zealand. J. Hort. Sci. Biotech. 75:413–422. Stanley, C. J., J. R. Stokes, and D. S. Tustin. 2001. Early prediction of apple fruit size using environmental indicators. Acta Hort. 557:441–446. Stoll, M., B. Loveys, and P. Dry. 2000. Hormonal changes induced by partial rootzone drying of irrigated grapevine. J. Expt. Bot. 51:1627–1634. Syvertsen, J. P., and Y. Levy. 1982. Diurnal changes in citrus leaf thickness, leaf water potential and leaf to air temperature difference. J. Exp. Bot. 33:783–789. Tardieu, F., and W. J. Davies. 1993. Integration of hydraulic and chemical signalling in control of stomatal conductance and water status of droughted plants. Plant Cell Environ. 16:341–349. Tardieu, F., J. Zhang, and D. J. G. Gowing. 1993. Stomatal control by both [ABA] in the xylem sap and leaf water status: a test of a model for droughted or ABA-fed field grown maize. Plant Cell Environ. 16:413–420. Taylor, H. M. 1983. Managing root systems for efficient water use: an overview. p. 87–113. In: H. M. Taylor, P. S. Nobel, and T. R. Sinclair (eds.), Limitations to efficient water use in crop production. Am. Soc. Agron. Inc., Madison, WI. Torrecillas, A., M. C. Ruiz-Sanchez, A. Leon, and F. Del Amor. 1989. The response of young almond trees to different drip irrigation conditions. Development and yield. J. Hort. Sci. 64:1–7. Torrecillas, A., A. Domingo, R. Galego, and M. C. Ruiz-Sanchez. 2000. Apricot tree response to withholding irrigation at different phenological periods. Scientia Hort. 85:201–215. Tromp, J. 1984. Diurnal fruit shrinkage in apple as affected by leaf water potential and vapour pressure deficit of the air. Scientia Hort. 22:81–87. Tromp, J. 1997. Maturity of apple cv Elstar as affected by temperature during a six-week period following bloom. J. Hort. Sci. 72:811–819. Tufts, W. P., and E. B. Morrow. 1925. Fruit bud differentiation in deciduous fruits. Hilgardia 1:3–14. Ueda, M., and E. Shibata. 2001. Diurnal changes in branch diameter as indicator of water status of Hinoki cypress Chamaecyparis obtuse. Trees 15:315–318. Uriu, K. 1964. Effect of postharvest soil moisture depletion on subsequent yield of apricot. Proc. Am. Soc. Hort. Sci. 84:93–97. Uriu, K., C. J. Hansen, and J. J. Smith. 1962. The cracking of prunes in relation to irrigation. Proc. Soc. Hort. Sci. 80:211–219. Valancogne, C., S. Dayau, M. I. Ferreira Gama, T. Ameglio, P. Archer, F. A. Daudet, and M. Cohen. 1997. Relations between relative transpiration and predawn leaf water potential in different fruit tree species. Acta Hort. 449:423–429. Warrick, A. W., and D. R. Nielsen. 1980. Spatial variability of soil physical properties in the field. p. 319–344. In: D. Hillel (ed.), Applications of soil physics. Academic Press, New York. Warrington, I. J., T. A. Fulton, E. A. Halligan, and H. N. de Silva. 1999. Apple fruit growth and maturity are affected by early season temperatures. J. Am. Hort. Sci. 124:468–477.

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Welles, J. M., and S. Cohen. 1996. Canopy structure measurement by gap fractional analysis using commercial instrumentation. J. Expt. Bot. 47:1335–1342. Westwood, M. N. 1993. Temperate-zone pomology. Timber Press, Inc. Wibbe, M. L., and M. M. Blanke. 1995. Effects of defruiting on source-sink relationship, carbon budget, leaf carbohydrate content and water use efficiency of apple trees. Physiol. Plant. 94:529–533. Wibbe, M. L., M. M. Blanke, and F. Lenz. 1993. Effect of fruiting on carbon budgets of apple tree canopies. Trees 8:56–60. Williams, L. E., and F. J. Araujo. 2002. Correlations between predawn leaf, midday leaf, and midday stem water potential and their correlations with other measures of soil and plant water status in Vitis vinifera. J. Am. Soc. Hort. Sci. 127:448–454. Wunsche, J. N., and J. W. Palmer. 1997. Effects of fruiting on seasonal leaf and whole canopy carbon dioxide exchange of apple. Acta Hort. 451:295–301. Wunsche, J. N., A. N. Lakso, and T. Robinson. 1995. Comparison of four methods for estimating total light interception by apple trees of varying forms. HortScience 30:272–276. Wunsche, J. N., J. W. Palmer, and D. H. Greer. 2000. Effect of crop load on fruiting and gas exchange characteristics of ‘Braeburn’/M.26 apple trees at full canopy. J. Am. Soc. Hort. Sci. 125:93–99.

4 Leucadendron: A Major Proteaceous Floricultural Crop* Jaacov Ben-Jaacov and Avner Silber Department of Ornamental Horticulture and Floriculture and Institute of Soil, Water and Environmental Sciences, Agricultural Research Organization, the Volcani Center P.O. Box 6, Bet Dagan Israel, 50-250

I. INTRODUCTION II. BOTANY OF THE GENUS LEUCADENDRON A. Taxonomy B. Distribution and Ecology III. WORLD INDUSTRY AND ECONOMICS A. Types of Leucadendron Cut Branches B. Yield IV. HORTICULTURE A. Genetic Improvement B. Propagation 1. Seeds 2. Cuttings 3. Grafting 4. Tissue Culture C. Site Selection and Environmental Responses D. Cultural Practices 1. Specific Requirements of Species and Cultivars 2. Spacing 3. Nutrition of Leucadendron 4. Response of L. ‘Safari Sunset’ to Irrigation Regime 5. Overcoming Soil Problems in Cultivating L. ‘Safari Sunset’ in Israel 6. Control of Growth and Flowering—Pruning and Pinching *The authors thank the many protea specialists—botanists, horticulturists, nurserymen, and farmers—for sharing with us their personal knowledge and experience in the preparation of this review. Horticultural Reviews, Volume 32, Edited by Jules Janick ISBN 0-471-73216-8 © 2006 John Wiley & Sons 167

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E. Plant Protection 1. Diseases 2. Physiological Disorders 3. Insects 4. Nematodes 5. Weeds F. Post Harvest Studies 1. Handling and Storage 2. Insect Eradication G. Leucadendron as a Pot Plant V. CROP POTENTIAL AND RESEARCH NEEDS LITERATURE CITED

I. INTRODUCTION Many members of the Proteaceae are being used as fresh and dry cut flowers (Plate I and II). Some of these crops have been reviewed recently: Leucospermum (Criley 1998), Protea (Coetzee and Littlejohn 2001), and Banksia (Sedgley 1998). Recent publication on cultivation and diseases of Proteaceae are reviewed by Crous et al. (2004). The total number of Proteaceous cut stems around the world is about 100 million (Littlejohn 2001), and leucadendrons probably account for at least half of this total. Israel alone produces more than 35 million branches annually—about 25% of all the cut foliage exported from this country (Gazit 2002). All leucadendrons provide good cut foliage, but one of them, L. ‘Safari Sunset’, a Leucadendron hybrid developed some 40 years ago in New Zealand, is the most popular (Matthews 2002). This single cultivar accounts for about 90% of the proteas produced in Israel. Most of the scientific research on Leucadendron in Israel, especially with regard to commercial cultural practices, has addressed this cultivar. Proteas, including leucadendrons, have been investigated and cultivated for over 250 years (Knight 1809; Linnaeus 1753) and still there are many myths regarding their uniqueness and thus their very special methods of cultivation. In fact, there is still relatively little solid, scientifically based information available on these plants. Three types of information have been consulted for this review: (1) scientific and technical publications; (2) books about proteas, some written for amateur botanists and nature lovers (Vogts 1982; Eliovson 1983; Rebelo 2001; Matthews and Carter 1983) and other books for commercial growers (Parvin and Criley 1991; Matthews 1993; McLennan 1993; Harre 1988, 1991; Salinger 1985; Matthews 2002); and (3) published and unpublished accounts of practical experience, provided mainly by Israeli farmers, extension specialists, and researchers. In general, for simplification,

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the name “protea” will be used, in this review, for all plants belonging to the Proteaceae. Growers of Proteas, including Leucadendron, on a worldwide basis cooperate and exchange information via the International Protea Association (IPA) (Brits 1984; Criley 1998).

II. BOTANY OF THE GENUS LEUCADENDRON A. Taxonomy About 100 years passed between the discovery of South Africa and the beginning of scientific description of the proteas. In 1737, Linnaeus described the first two species of Leucadendron (L. argenteum and L. coniferum), but it took a long time to understand and to classify the South African proteas. With the introduction of the binomial system of nomenclature by Linnaeus in his Species Plantarum (1753), only six species of plants were listed under the name protea. In the case of L. argenteum, Linnaeus became lyrical in his description and stated that “This tree is the most shining and splendid of all plants,” but he then continued and wrote about the Silver Tree that: “yes, (it is) like Proteus himself extremely variable and different” (Williams 1972). The difficulties and misunderstanding were probably partly due to the fact that the genus Leucadendron is dioecious, and the male and the female plants are very different in appearance (Williams 1972). A general introduction to the origin of the protea family can be found in Criley’s review on Leucospermum (Criley 1998), and the systematics and phylogeny of the African Proteaceae were reviewed recently by Rourke (1998). The taxonomy of the genus Leucadendron was revised about 30 years ago (Williams 1972). Recent studies, based on gene-sequencing data, have contributed to the understanding of the genetics, systematics, and phylogeny of the African Proteaceae, including Leucadendron (Barker et al. 1995; Hoot and Douglas 1998; Tansley and Brown 2000). The genus Leucadendron is easily identified as having plants of separate sexes: the pistillate plants (known as female plants in the leucadendron literature) produce woody conical, fruit-bearing flower heads, called “cones” (Rebelo 2001). The flower heads of the staminate plants (known as male plants in the leucadendron literature) do not form those conical flower heads. The conspicuous cones of the female plants consist of spirally arranged floral bracts, each of which covers a small flower (floret), and the bracts become hard and woody, forming the conical structures (Rebelo 2001). There are also morphological differences between the male and the

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female plants: the males are usually more branched and often slightly larger than the females, with smaller leaves and flower heads (Rebelo 2001). Bond and Midgley (1988) reported great differences in stem diameter, leaf area, number of inflorescences and mass of each individual inflorescence between the sexes of L. rubrum, and some differences in these characters in L. tinctum also. There are other extreme phenomena of dimorphism that distinguish between the sexes in L. rubrum (De Kock et al. 1994). Williams (1972) reviewed the taxonomic history of the main South African genera of Protea. Because emphasis had been placed on different features, the family had been divided into different genera in several different ways, and each genus into different groups of species. Williams (1972) adopted R. Brown’s (1810) approach and based his classification of Leucadendron on division into sections and sub-sections, mainly according to fruit and floral characters (Table 4.1). Rebelo (2001) is continuing his research on the taxonomy and distribution of the genus Leucadendron, and much of the more recent information can be found in his Protea Atlas Project (Rebelo 2004). Thorough knowledge of the generic relationships among the Leucadendrons is contributing greatly to their horticulture and breeding. Rebelo (2001) simplified the use of Williams’ (1972) classification of the Leucadendrons by adding the English common name “conebush” to the genus Leucadendron as well as common names to the subsections (Table 4.1); he described each of the sections, subsections and species. Species belonging to the section Leucadendron have round nuts or nutlets (fruits) and those belonging to the section Alatosperma have flat, winged fruits. B. Distribution and Ecology The distribution range of the genus Leucadendron is limited to the Cape geological series in the southern Cape Province (Cape Floral Kingdom), with a small outlier on the Cape geological series near the coast in Natal (Williams 1972). All leucadendrons, except 3, are found in the Cape Floral Kingdom (Rebelo 2001) and all of them are well adapted to the fynbos vegetation type (Cowling and Richardson 1995). The fynbos is the most common vegetative type of the Cape Floral Kingdom, contributing more than 80% of its species, including the leucadendrons (Goldblatt and Manning 2000). Rourke (1980) defined fynbos as the sclerophyllous vegetation of the southwestern Cape, composed mainly of plants having fine, hard, heath-like leaves, or stems. The exact distribution of the

4. LEUCADENDRON: A MAJOR PROTEACEOUS FLORICULTURAL CROP Table 4.1.

171

Classification of the genus Leucadendron (modified from Rebelo 2001). Subsection name

Section Leucadendron

Alatospermum

Scientific

Sandveld

Membranacea Carinata Uniflora Aliena Cuneata Nervosa Leucadendron Nucifera

Arid Ridge-seed Pauciflor Kouga Fuse-bract Jonaskop Silver Silver Sun

Ventricosa

Crown

Trigona

Delta-seed

conicum, floridum, loeriense, macowanii, pondoense, roukei, radiatum, salicifolium, uliginosum

Oilbract Sunshine& Clay

microcephalum coniferum, cryptocephalum, diemontianum, discolor, eucalyptifolium, flexuosum, foedum, gandogeri, lanigerum, laureolum, meridianum, modestum, procerum, salignum, spissifolium, strobilinum, stelligerum, xanthoconus comosum, immordoratum, muirii, nobile, osbornei, platyspermum, spirale, teretifolium

Compressa

Cone bush

Species

Villosa

Brunneobracteata Alata

z

Commonz

Needle-leaf

brunioides, cinereum, concavum, coriaceum, dubium, galpinii, levisanus, linifolium, stellare, thymifolium arcuatum, bonum, remotum, pubescens nitidum, sericeum ericifolium, olens singulare, sorocephalodes corymbosum, laxum, verticillatum nervosum album, argenteum, dregei, rubrum barkerae, burchellii, cordatum, cadens, daphnoides, glaberrinum, gydoense, loranthifolium, meyerianum, orientale, pubibracteolatum, rodii, sessile, sheilae, tinctum, tradouwense chamelaea, elimense, globosum, grandiflorum

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individual Leucadendron species was described by Goldblatt and Manning (2000), and distribution maps were presented by Williams (1972) and Rebelo (2001). The survival risk for leucadendrons species in nature is: 2 extinct, 16 endangered, 8 vulnerable, 17 naturally rare, and 1 uncertain (Hilton-Taylor 1996). Additional information is available at www.nbi.ac.za/protea. This situation is even more prevalent with regard to some of the local types and subspecies (Rebelo 2001). The South African Agricultural Research Council—Fynbos Unit has directed great efforts into the ex situ conservation of horticulturally important proteas, including leucadendrons (Littlejohn et al. 2000). The diversity, endemism, and distribution of leucadendrons and also of other Fynbos plants in the Cape Floristic Region are extensive. The rugged and dissected nature of the Cape landscape is a significant factor in the understanding of this diversity and endemism (Goldblatt and Manning 2000), as is the fact that after more than 250 years of Leucadendron research (Linnaeus 1753; Knight 1809) new species belonging to this genus are still being discovered (A. E. Van-Wyk 1990; Rourke 1997). Many studies and publications address various ecological and distribution aspects of the place of the Leucadendron species in the natural vegetation (Midgley 1998). Fires are an important factor in the life cycle of leucadendrons and affect the germination of its serotinous species, as well as some of the myrmecochorous and therophilous species (T. Rebelo, pers. commun., 2004). The fire causes the releases of the seeds from the cones to the ground, making the germination possible (Bond 1985; Le-Maitre 1988, 1989; Le-Maitre et al. 1992; Midgley 2000). Flower harvesting methods, seed dispersibility, and seed size affect the distribution and ecology of leucadendrons (Stock et al. 1990; Mustart and Cowling 1993a,b; Midgley 1998). The type of soil, its nutrient levels, its pH and hence its nutrient availability, as well as plant competition and tillage of the heathland soil are also important determinants of the distribution of Leucadendron in its natural habitat (Davis and Midgley 1990; Davis 1992; Mustart and Cowling 1993a,b; Mustart et al. 1994; Richards et al. 1997a,b; Laurie et al. 1997). Data regarding the climate of the Cape Region reveal average daily maximum temperatures of 28°C and 17°C in midsummer and midwinter, respectively. Extreme maxima reach 43°C in the summer and 30°C in the winter, and extreme minima reach 4°C in midsummer and –5°C in midwinter. Temperatures, especially leaf temperatures, are greatly affected by ocean breezes and overcast skies. Annual rainfall ranges from 3000 mm on some mountain peaks to less than 250 mm in some inland valleys (Schulze 1984; Goldblatt and Manning 2000). The soils of the Cape region have various geological origins, including sandstone,

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granite, and limestone (Goldblatt and Manning 2000), and accordingly, in nature, different species of Leucadendron grow in sandy or heavy, boggy soils, and in soils with high or low pH (Williams 1972; Eliovson 1983; Laurie et al. 1997).

III. WORLD INDUSTRY AND ECONOMICS World trade in the three most widely used genera among the South African Proteaceae is estimated at 100 million stems annually, with the greatest volume involving a single Leucadendron cultivar ‘Safari Sunset’ (Littlejohn 2001). Littlejohn (2001) estimated the annual market volume of L. ‘Safari Sunset’ to be about 25 million stems; today, however, we know that the current volume is probably more than 40 million. A large proportion of the Leucadendron branches produced for the world market are of seed-propagated species and not of cutting-propagated cultivars (Table 4.2). This is especially true in the South African production of Leucadendron. Except for some hybrids, most of the seedpropagated plants and those propagated vegetatively from unidentified clones are sold under the species name or under trade names. In many cases, the “old” synonymous species name is used as the trade/commercial name. In other cases, the species name is followed by an indication of whether the flower is male or female. The SAPPEX (South African Protea Producers and Exporters Association, undated) Catalogue includes 24 species and six cultivars of Leucadendron that are currently exported from South Africa. The main leucadendrons sold on the Sydney market are: L. ‘Silvan Red’, L. ‘Safari Sunset’, L. salignum red, L. salignum yellow, L. gandogeri green and yellow, L. laureolum green and yellow, L. ‘Tall Red’, L. ‘Inca Gold’ yellow, L. ‘Maui Sunset’, L. salicifolium, L . floridum ‘Pisa’, L. ‘Harvest’; leucadendrons with “cones” (“Christmas-nuts” as it is called on the Sydney market in the mid-summer, Christmas season) include: L. galpinii and L. ‘Jubilee Crown’. More exotic Leucadendrons are: L. ‘Katies Blush’, L. ‘Sundance’, L. tinctum, L. orientale, L. strobilinium, L. discolor female (white), L. discolor male (yellow with red center), L. argenteum, and L. elemense (with “nuts” at Christmas; Scott 2000). A. Types of Leucadendron Cut Branches In analyzing the different types of Leucadendron cut products on the market, one may classify them into four main groups, more than one of which may be produced by a given species or cultivar during different

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Table 4.2. The main species and cultivars of Leucadendron in the international floricultural trade and their methods of propagation. (Sources: Cape Flora—South Africa, SAPPEX (Catalogue). Types of Plantation Seedlings

Botanical

Trade of cultivar name

Clones

All types of seedlings x

L. argenteum

Silver tree

x

L. coniferum L. coniferum × floridum L. discolor L. discolor L. discolor L. floridum L. galpinii L. laureolum L. laureolum L. laureolum × L. salignum L. linifolium L. linifolium L. laxum L. laxum L. meridianum L. muirii L. nervosum L. nervosum L. platyspermum L. platyspermum L. rubrum L. rubrum L. salicifolium L. salignum L. salignum L. salignum × L. eucalyptifolium L. teretifolium L. xanthoconus L. laureolum × L. salignum

Sabulosum Pisa

x

Green Discolor Red Discolor Yellow Discolor Florida

x x x x

Special types

Sex separated at harvest

x

x x x x x

Decorum Star Laureolum male Safari Sunset Tortum female Tortum male Smartrose Jubilee Crown

x x x x x x x x x

Nervosum male Platy male Platystar Rubrum female Rubrum male Strictum Blush Red adscendens Chameleon Cumosum Salignum Gold Strike

x x x x x x

x x x x x x x x x x x

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175

seasons. The four main groups according to SAPPEX (undated) and L. J. Matthews (2002) include: (1) Foliage—cut branches are sold for their attractive foliage, which is relatively uniform along the whole length of the branch. The color of foliage varies among species and between specific clones: silver in silver tree (L. argenteum), green in ‘green discolor’ (L. discolor) and ‘Pisa’ (L. coniferum × L. floridum), and light green in male L. platyspermum. The product is available almost throughout the year, except when new growth is too soft. (2) Attractive colorful “heads”—in these branches, when vegetative growth is stopped or slowed down and flowering commences, the larger terminal leaves become colorful. These involucre leaves commonly mistakenly known as “bracts” (Rebelo 2001, 2004) change their color during the marketing season. The main colors are various shades of red and yellow. Particular examples are: L. ‘Safari Sunset’, L. ‘Yaeli’, L. ‘Inca Gold’, and L. ‘Gold Strike’. Depending on the cultivar, the product may be available for long or short periods, though its shape and color may change in the course of the marketing season. (3) Male colorful “heads”—inflorescence and surrounding involucre leaves as in red and yellow discolors (L. discolor). The marketing season is extremely short (two to three weeks). (4) Branches terminating in attractive female cones—the main examples are females of: L. teretifolium, L. linifolium, L. galpinii, L. coniferum, L. salicifolium, L. platyspermum, and the cultivar ‘Jubilee Crown’ (L. laureolum × L. salignum). Some species or cultivars may be sold with attractive colorful involucral leaves and cones (e.g., L. ‘Safari Sunset’). This type of product has a long marketing period. B. Yield It is difficult to assess the potential and the actual yields of leucadendrons. Yield may be counted in terms of production per plant or per hectare. In commercial plantations of L. ‘Silvan Red’, Barth et al. (1996) counted average annual yields of 314 and 219 marketable stems per plant on highly fertile and infertile sites, respectively. They indicated that the plants were 1.0 to 1.5 m wide, but they did not indicate the distances between plants. However, in Australia, the planting density is generally 2600 plants per hectare (Cecil et al. 1995), so that the average annual yield is almost 700,000 stems per hectare. Leucadendron ‘Safari Sunset’ is planted in Israel at spacings of 2 m between rows and at 0.8 m within the row, i.e., 6250 plants per hectare (Shtaynmetz 1998; Shtaynmetz et al. 2004a). When planting is done in the spring, the average

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annual yields are 60,000, 150,000, 240,000, and about 400,000 marketable stems per hectare in the first, second, third, and fourth year onwards, respectively (Shtaynmetz et al. 2004a). The discrepancies between the Australian and Israeli figures may be related to the different cultivars and/or to the fact that in Israel the figure is solely for quality exportable stems.

IV. HORTICULTURE A. Genetic Improvement In the early days of the protea industry, flowers were harvested from natural plant stands. Even now, many of the Leucadendron branches, especially those produced in South Africa, are harvested from natural fynbos or produced on seed-propagated species, rather than on cuttingpropagated, selectively bred cultivars. The first dedicated, scientific breeding of proteas—which included Leucadendron as an important component—was started in South Africa in 1973 (Brits 1983; Brits et al. 1983). The breeding of Leucadendron was initially based on the extensive collections that Marie Vogts had made, from nature, of so-called “commercial variants” (botanical ecotypes) of the best variations of species, and which she subsequently established in cultivation (Brits et al. 1983). However, the trend towards production of high-quality cultivars of Leucadendron started in other countries, rather than South Africa (Littlejohn et al. 1995). Leucadendrons are easily reproduced by cuttings, therefore the improvement process has to produce only a single superior plant; the new cultivar can then be developed simply by multiplying this plant by means of cuttings. There are several ways to select the superior single plant from which to develop a new cultivar: taking cuttings from superior plants grown in the natural fynbos or in seedpropagated plantations, or developing superior variations by controlled or uncontrolled hybridization (Brits 1983). Hybrid seeds may be produced from crossing variants of the same species (intraspecific), or from crosses between species (interspecific). Hybrid plants may be produced by planting the parent plants in the same field and waiting for crosspollination to take place naturally (open pollination) and then collecting hybrid seeds, or by artificial, controlled pollination (van den Berg and Brits 1995). In Leucadendron, the genetic variations available are vast and as yet largely untapped (Brits 1983; Littlejohn et al. 1995; van den Berg and Brits 1995). In 1995, Littlejohn et al. (1995) stated that the techniques to

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successfully hybridize any Proteas at will were not yet available, and that there was a need to overcome difficulties of low seed set and crossincompatibility between species. The natural pollination modes in Leucadendron differ among species; some species are wind pollinated and others depend on specific insects (Hattingh and Giliomee 1989). In their review, Collins and Rebelo (1987) indicated that the pollination biology and breeding systems of Australian and southern African Proteaceae resemble one another. Proteas exhibit low seed set relative to the number of flowers available, and functional abandromonoecy (overcrowded, functional and non-functional flowers on the same receptacle) seems to be the main cause of poor seed set (Hattingh and Giliomee 1989). Originally, leucadendrons were marketed mainly as green/foliagetype flowers. Van den Berg and Brits (1995) were the first to recognize the potentially high market demand for superior quality Leucadendron single-stem cut flowers as a separate product. They pointed out that it was almost impossible to find all the desirable cut flower combinations of attractive large flower heads, long flowering branches and a high yield, within a single species, and argued that interspecific crosses must be used to combine the desirable qualities from different species. It was, however, much earlier, in the early 1960s, that the first excellent, singlestem cut flower cultivar ‘Safari Sunset’ was originated; it served as the role model for Brits’ and van den Berg’s 1986 research project (Bell 1988; Matthews and Carter 1983; van den Berg and Brits 1995; Matthews 2002). Heterosis (hybrid vigor) is often found in proteaceous hybrids (Brits 1983). In 1986 van den Berg and Brits (1995) started an extensive and systematic interspecies hybridization program with Leucadendron, intended partly to study both interspecific compatibility and heterosis in this genus. They found, surprisingly, a relatively high incidence of successful crosses, as well as high seed set, in the crosses, especially among the Alatosperma. Furthermore, among over 3000 hybrid seedlings produced from 36 interspecific crossing combinations, with average seed set approaching 50% of the pollinated florets, the majority showed strong hybrid vigor. This demonstrated the unusual potential for systematic interspecific breeding in Leucadendron. In The International Proteaceae Registrar (including the register and the checklist, Sadie 2002) are listed over 110 names of Leucadendron cultivars; of these 38 are interspecific hybrids (Table 4.3, Sadie 2002). Most of the successful crosses are among species of the Section Alatosperma, Subsection Sunshine (Alata) con bushes, mainly between L. laureolum × L. salignum. However, there are reported hybrids between species belonging to different Subsections (L. discolor × L. lanigerum)

178 Table 4.3. Species/ Species conicum coniferum daphnoides discolor elimense eucalyptifolium gandogeri lanigerum laureolum salignum

Number of successful interspecific hybrid combinations as reported in “the International Protea Registrar” (Sadie 2002).

discolor

elimense

eucalyptifolium

gandogeri

lanigerum

laureolum

salignum

spissifolium

tinctum

uliginosum

1 1 1 1

1

2 1

3

2

2 1 14

1 1

xanthoconus 1 1 1

1 1 1

Total 2 2 3 8 1 4 1 2 14 1

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and even between species belonging to different Sections (L. elimense × L. laureolum). The main species used for successful, interspecific hybridization are listed in Tables 4.3 and 4.4 (Sadie 2002). The first four cultivars of Leucadendron were developed in New Zealand during the 1960s. Sadie’s Registrar lists eight cultivars developed in the 1970s, 42 during the 1980s, and 51 during the 1990s. The first intentional breeding of Leucadendron was done in New Zealand, in the early 1960s. The original breeding was done by Jean Stevens of Wanganui and was continued by her son-in-law Ian Bell (Bell 1988; Matthews and Carter 1983; Matthews 2002); they crossed Leucadendron laureolum with a red form of L. salignum, which was probably native to Langkloof, South Africa (FFTRI 1972; G. Brits, pers. commun., 2001). From this original cross emerged several selections, the best and most famous ones being L. ‘Safari Sunset’ and L. ‘Red Gem’. The registrar (Sadie 2002) lists 14 additional cultivars based on the same cross combination; the most famous of these is L. ‘Silvan Red’, which was bred in Australia in 1992 (Sadie 2002). It is difficult to select sufficiently superior cultivars just by selection within a species; therefore, crosses must be used to combine favorable qualities from different species. In the wild there are many “natural hybrids” between related species (for more information see www .nbi.ac.za/protea (protea information>protea ecology>hybrid relationships within proteas). It is more difficult to obtain viable crosses between taxonomically distant Leucadendron species (van den Berg and Brits 1995; Littlejohn 2001; Robyn and Littlejohn 2001). Genetic and breeding research has been accelerated in the last 5 to 10 years, especially by the very active programs at the ARC in South Africa (van den Berg and Brits 1995; Littlejohn 2001; Robyn and Littlejohn 2001) and more recently in Western Australia (Sedgley et al. 2001; Yan et al. 2001; Croxford et al. 2003).

Table 4.4. Classification of the main species used for interspecific hybridization in Leucadendron (Sadie 2002). Section

Subsection

Species

Leucadendron

Sun Crown Delta-seeds Clay Sunshine

daphnoides, tinctum elimense conicum, uliginosum lanigerum coniferum, discolor, eucalyptifolium, gandogeri, laureolum, salignum, spissifolium, xanthoconus

Alatosperma

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The current range of Leucadendron cultivars includes: (1) clonal selections from within species, such as L. salignum cultivars ‘Blush’ or ‘Yaeli’ (Ackerman et al. 1997a); (2) interspecific hybrids of speculative parentage, such as the L. laxum hybrid cultivar ‘Jubilee Crown’; and (3) interspecific hybrids of known parentage such as the L. salignum × L. eucalyptifolium cultivar ‘Chameleon’ or the L. laureolum × L. elimense cultivar ‘Rosette’ (Littlejohn et al. 1998; Littlejohn and Robyn 2000; Sadie 2002). Controlled pollination in Leucadendron is relatively simple, because of dioecy (Brits 1983). A. Robyn (pers. commun., 2000) recognized three main steps in achieving controlled hybridization among Leucadendrons: (1) covering the female inflorescence to prevent uncontrolled pollination—a cone of the selected female parent is covered for two to four days with a greaseproof bag to prevent wind or insect pollination while the stigmas ripen; (2) pollination—ripe pollen from the selected male parent is applied to the ripe stigmas of the female florets, with a fine brush, and the pollinated cones are again covered with the greaseproof bags; and (3) seed maturation—the seeds in the successfully pollinated florets must ripen to full maturity on the plant during the following four to six months, before harvesting. The following are the main aspects of a breeding program: (1) Pollen collection, storage, and viability assessment—since interspecific hybridization is a necessary approach to the development of superior new cultivars of Leucadendron (van den Berg and Brits 1995), and since different species flower at different times of the year, it is important to develop methods for storing pollen. Both investigating teams, in South Africa and in Western Australia, studied pollen storage and assessment. Sedgley et al. (2001) recommended collecting male flower heads at anthesis: the cut stems, bearing many flower heads, are held at room temperature, and pollen can be separated from the flowering heads by removing the entire heads and sieving the pollen through a fine mesh sieve onto clean paper. The pollen is placed in open tubes within a sealed jar containing freshly dried silica gel at 4°C for 48 hr. The tubes should then be kept at either –20°C for short-term storage or at –80°C for long-term storage (Sedgley et al. 2001).Viability may be assessed by counting percentage pollen germination and pollen tube growth or by use of a fluorescent dye (Sedgley et al. 2001). (2) Hybridization compatibility—the main successful interspecific crosses in the genus Leucadendron are those between closely related species. Hybridization compatibility may be evaluated by scoring pollen-pistil interactions (Yan et al. 2001), or by estimating the percentage seed set (van den Berg and Brits 1995; Robyn and Littlejohn 2003). (3) Inheritance of important traits—relatively little is known

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about the genetics of Leucadendron and how important traits are inherited in these plants. Croxford et al. (2003) analyzed the inheritance of some important traits. (4) Survival at different trial sites—survival of hybrids was related to genotype, site, and the interaction between these two factors. Hybrid seedlings sometimes died because of incompatibility and delayed genetic incompatibility. The various sites had differing soil types and thus differed in the severity of infection from soil-borne pathogens, including Phytophthora cinnamomi. It has been observed that hybrids between pairs of parents chosen from L. strobilinum, L. loureolum. L. gandogeri, L. eucalyptifolium, L. xanthoconus, L. uliginosum, L. salicifolium, and L. muirii survived well in unfavorable sites, whereas when one of the above was crossed with L. procerum the tolerance of the resulting hybrids to those adverse sites was lost. (5) Juvenility—the length of the juvenile period was related to the parental combinations. Crosses having L. muirii, L. discolor L. procerum, L. salignum, L. spissifolium, L. strobilinum, or L. gandogeri as at least one parent produced hybrids with long juvenile periods, whereas crosses with species of the trigona subsection usually produced hybrids with shorter juvenile periods. (6) Flowering time—in general, the flowering time of hybrids is closely related to that of the parental species. Van den Berg and Brits (1995) found a wide variation of flowering times in their hybrid leucadendrons, ranging from June to September (Southern hemisphere). (7) Color of male flower heads—most male flower heads are yellow; however, two species, L. discolor and L. procerum can produce bright red male flower heads. When female plants from these species were crossed with other species, all the male offspring produced red flower heads. On the other hand, when a red L. discolor male was crossed with other species, only 70% of the male offspring were red. These results should be viewed as preliminary observations, indicating the beginning of understanding color inheritance in Leucadendron. (8) Bract (or more correctly “Involucre leaves”) color—most Leucadendron species have yellow or green bracts, but some genotypes of L. salignum have red bracts or combinations of these colors. Some species have their own unique bract colors. Crosses between red-bract L. salignum and yellow-bract species often produced hybrids with red bracts. When the red-bract hybrid ‘Red Gem’ (an F1 hybrid between red L. salignum and yellow L. laureolum) was crossed with L. laureolum (yellow bracts), 50% of the offspring had yellow bracts and 50% red ones, indicating a simple single-gene inheritance of the red color. Hybridization with the ‘Langkloof’ forms of L. salignum seems to offer special potential, since these plants effectively have two distinct flowering seasons: in winter-spring, when flowering proper occurs, and in midsummer at the termination of

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elongation growth, when the fully expanded terminal bracts (‘flower’) turn bright red (usually). This latter stage may be the most lucrative for marketing the plant—as in the case of ‘Safari Sunset’ (van den Berg and Brits 1995). (9) Plant form—the leucadendrons most suitable for use as cut flower varieties have an upright form and an annual vegetative flush of long, straight stems, which may be single-head or multi-head. It has been observed that, in some species, the flowering stems of female plants tend to be single-head and those of male plants multi-head. In general, hybrids tended to combine form traits from both parents. (10) Regeneration from epicormic buds of the lignotuber—the ability to regenerate new shoots from the base of the plant is an important quality for a good cut-flower cultivar. It seems that all the hybrids that result from a cross between a species with and one without a lignotuber have functional lignotubers, even though these may not be morphologically prominent (Brits et al. 1986). Second generation crosses of the above with a species with no epicormic trait produced hybrids that lacked this important trait. (11) Chromosome number—Croxford et al. (2003) counted the chromosomes of 25 genotypes from 15 different species and found that in all of them 2n = 26. These counts agree with the findings of de Vos (1943). Croxford et al. (2003) found neither aneuploidy nor euploidy in their counts. Littlejohn (1996c, 1997) evaluated Leucadendron selections according to the following traits: characteristics of the bush, the leaves, and the flower heads, flowering time, the ability to recover after harvesting of the flowers, and the yield. In many of these traits, she found great differences between closely related cultivars. For example, the average single-stem yields of various L. salignum clones ranged from eight per plant for the least productive to as high as 65 per plant for the most productive (at the third harvest). B. Propagation Malan (1992, 1995) reviewed the various propagation methods used for proteas. Here we outline some of these methods and add some accounts of practical experience reported by commercial propagators in Israel. 1. Seeds. Seeds are used for propagating Leucadendron for two reasons. Firstly, many of the Leucadendron branches sold on the world market are still harvested from seed-propagated species. This is especially true in South Africa, where most of the production is based on broadcasting seeds on ripped ground (M. Middelmann, pers. commun., 2002) and not on vegetatively propagated cultivars. The second reason is that propagating from seeds is part of the process of breeding new cultivars.

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In general, proteas do not set abundant seeds, especially when they are grown outside their natural habitat, out of reach of their unique pollinators. In Leucadendron, cross pollination is obligatory since they are dioecious plants and is accomplished by insects, mainly beetles, or/and by the wind. The 10 most common wind-pollinated Proteas in southern Africa are all Leucadendron species (Rebelo 2001). Among southern African Proteaceae, the average percentage of florets that set seeds ranged from 77% in Leucadendron and 100% Aulax, to 8% in Protea and 15% in Leucospermum (Rebelo and Rourke 1986). Leucadendrons have two major types of seeds (strictly speaking, achenes): nut-like (6 being myrmecochorous—ant dispersed, and over 25 species are rodent dispersed) and serotinous (Bond 1985; Brits 1986b; Rebelo 2001). This biological dichotomy is common among the seeds of SA Proteaceae at the generic level with Aulax and Protea serotinous and the remaining genera being myrmecochorous. Rodent-dispersed seeds are only known in Leucadendron. The unique feature of Leucadendron to contain more than one seed type prompted Salisbury (in Knight 1809) to split the genus into several genera based on seed morphology—his groupings are now recognized at the subgeneric level. These seeds are rounded, nut or nutlet-like, and are relatively hard-shelled (Williams 1972; Brits 1986b). Myrmecochorous nutlets are covered with a fleshy skin—called the elaiosome—that attracts ants, which carry them away and store them in their nests. Serotinous seeds have a flattened, winged shape and are retained on the plant for long periods, in live (turgid) protective woody cones or seedheads that protect them from fire and predators. They are released and dispersed by a hygroscopic mechanism that is activated by dessication when the water supply to the seedheads stops as a result of fire or the death of the plant (Brits 1987; Rebelo 2001). The seeds are ripe for harvesting 6–7 months after flowering, when the young flower heads on the tips of the new growth are already developing (Vogts et al. 1976). Serotinous seeds are common in species of the Section Alatosperma (Table 4.1). With regard to dormancy and germinability, it is important to distinguish between two main types of seeds: the hard-coat nuts and the flat seeds (Brits 1986b). The first type is more difficult to germinate and should be handled similarly to other hard-coated proteaceous seeds; it includes Leucospermum (Van Staden and Brown 1977; Brits 1986b,c). Dormancy of hard-coated seeds can be overcome by mechanical or acid scarification, by hydrogen peroxide treatment (Brits 1986a,b; McLennan 1993; Brits et al. 1995), or by soaking the seeds in hot water (Harre 1988), although the last method may be an indirect form of scarification, which occurs when desiccated seeds are wetted (Brits et al. 1993).

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Rourke (1994) stated that John Herschel studied the effect of heat on germination of Leucadendron argenteum as early as 1836. Herschel wrote: “The seeds of protea argentea will be several years in the ground without germinating—but if the seeds be sown half an inch deep and then the ground burnt they come up at once.” This reaction may in fact be induced indirectly by the desiccating effect of heat on the buried seeds, followed by watering (Brits et al. 1993): treating any welldesiccated fynbos nut-fruited Proteaceae seeds with free water may result in cracking of the seed coat, which amounts to mechanical scarification, and subsequent dormancy breaking, i.e., germination. However, scarification may also mechanically assist the embryo to emerge, which is probably a much lesser effect than that of oxygenation (van Staden and Brown 1977). Van Staden and Brown (1973) and Brown and van Staden (1973b) in studies of the effects of oxygen on endogenous cytokinins levels and on germination of Leucadendron daphnoides, which has hard-coated seeds, found that scarification treatments and incubation of seeds in oxygen improved germination under alternating temperatures. The effect of high oxygen appears to be mediated by increased levels of endogenous cytokinins, since the latter condition is closely correlated with enhanced germination. Brits (1986b) showed that soaking in 1% H2O2 solution for 24 hr could be a practical way of oxygenating non-scarified, hard-coated proteaceous seeds. In Leucadendron, flat or winged seeds (alatosperma) appear not to need additional (artificial) oxygenation. The stimulating effect of elevated oxygen partial pressure within intact hard-coated seeds is consistent with the stimulating effect of scarification, which acts by breaking the impermeability of the intact seed coat to atmospheric oxygen, so that seeds are subsequently naturally oxygenated from the air (Brits et al. 1993). The effect of daily alternating temperature on germination of the hard, nut-like seeds of Cape Proteas has been studied thoroughly by Brits (1986c). It appears that all nut-like proteaceous seeds, including Leucadendron, require daily temperature variations between about 8°C–10°C night (16 hr) and 20°C day (8 hr) for optimal germination. There are also indications that some aqueous germination inhibitors may be present in seeds of L. daphnoides (Brown and van Staden 1971). There are many publications on dormancy and germination in proteas (Brown 1975; Brown and van Staden 1973a,b,c; van Staden and Brown 1977; Brown and Dix 1985), and recently Criley (1988) summarized all the methods being used for overcoming seed dormancy in hard-coated proteaceous seeds. In summary, all highquality Leucadendron seeds primarily need low temperature, preferably 10°C, with daily fluctuations to 20°C for successful germination; and

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non-scarified (intact) hard-coated seeds also need oxygenation (Brits 1986b; Brits et al. 1993). After overcoming dormancy, the main cause for failure in propagating leucadendrons by seeds is death caused by fungi, and these deaths can occur both pre- and post-emergence. The development of dampingoff diseases is always accelerated by the presence of high levels of inocula in the germinating medium, and by excessive watering, insufficient aeration, and excessively high temperature (Harre 1988). Recently, Brown and Botha (2002) reported that seeds of L. rubrum and L. tinctum increased germination in response to smoke. The germination percentage also depends a great deal on the source of the seed and the species, i.e., on seed quality (Robyn and Littlejohn 2001). There are several ways to sow the seeds: (1) broadcasting, is used mainly in South Africa. The mature cones are shredded and, without separating seeds from other components, the shredded material is broadcast onto ripped fields; (2) inserting brunches with the matured cones in the ground. This is done with L. platyspermum, whose winged seeds may germinate before they emerge from the cones (Rourke 1998); (3) sowing in open beds; (4) sowing in shallow flats, which can be placed in the open or in a shade house and irrigated when necessary, or irrigated once and then stacked for 17–26 days at controlled temperatures (see recommended temperature regime above). When germination begins, the flats are removed from the stack and placed in an exposed location. Temperature fluctuations between 10°C (night) and 20°C (day) are essential for optimal germination (Brits 1986c); (5) seeds are spread between two layers of canvas and placed under mist in an unheated shade house, in autumn or mild winter. Seeds that are starting to germinate are collected every few days and placed in small pots; and (6) seeds are sown in individual plugs and a few days after germination the plugs with the germinated seeds are moved to a different location with a suitable irrigation regime. Publications that address the seed ecology of Proteaceae include Bond (1988), Bond et al. (1995), and Bond and Maze (1999). Publications concerning seed germination under natural conditions were written by Brits (1987), Mustart and Cowling (1991), Lamont and Milberg (1997), and Musil et al. (1998). 2. Cuttings. Most cultivars of Leucadendron are no longer considered difficult to root by means of standard techniques (Malan 1995). Jacobs (1981) indicated that the fall (March, April in the Southern hemisphere) is the best time for rooting leucadendrons. Nurserymen in Israel and New Zealand (Harre 1988) root leucadendrons all year round, provided

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that suitable wood is available and that there are proper facilities for rooting the cuttings. Terminal and sub-terminal cuttings can be used, which should not be “too soft” nor “too hard”; if too soft they will rot in the propagation bed, and if too hard they will root only after several months or not at all. It is best to use wood not more than 6 months old (R. Arlevsky, pers. commun., 2002). The cuttings, measuring 12 cm long by 8 mm diameter, should be taken from good healthy plants, grown under full sunlight, washed well, disinfected, e.g., with active chlorine solution, and kept under refrigeration until being inserted in the propagation bench. Cuttings should be treated with rooting hormones; Malan (1995) gave a general recommendation of 4000 ppm IBA for proteas. Harre (1988) indicated an optimal level of 2000 ppm for Leucadendron, and recommended reducing this concentration to 1000 ppm for ‘hairy-leaf’ varieties. A 1-cm length at the base of the cuttings should be placed in the hormone solution for 10 seconds. The cuttings should be inserted in well drained and sterilized growth medium. Malan (1995) recommended sand: peat: polystyrene (1:1:1 v/v/v). In Israel it is common to use a mixture of finely ground polystyrene: medium-size peat (7:3 v/v) packed in “Ellepot” propagating plugs (Ellegard, Denmark). The cuttings should be kept under a mist system in a protected and well-aerated greenhouse, with a light intensity of about 300 lux. Under Israeli conditions, in the summer the plastic cover of the propagation house is whitewashed and a 30% shade net is placed inside the house; in winter the whitewash is washed off by the rain and the 30% net is kept in position. In New Zealand, Harre (1988) recommended allowing full light intensity during the morning and evening, and cutting the 900-lux full light intensity at midday by 50%; higher light intensity could be maintained if it is possible to do so without elevating the temperature. The temperature at the base of the cuttings should be kept at a minimum of 18°C, and the air temperature should not exceed 26°C. The pad and fan cooling system is recommended. However, the highhumidity/high-temperature environment is excellent for the spread of diseases, against which a high level of phytosanitary conditions should be maintained. The house should be well aerated and the plants should be sprayed regularly against foliar diseases. To prevent root rots, the medium should be drained against Pythium and similar diseases with materials such as Dynon (propamocarb) or Rizolex (tolclofos-methyl). When all the recommendations are followed, good propagators achieve 85–95% well-rooted plants. There have been several detailed studies that provide some additional information on propagation by cuttings of leucadendrons: Rodriguez-

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Perez (1992) examined the possibility of using leaf-bud cuttings of L. ‘Safari Sunset’, and achieved a maximum rooting of 20%. The use of leafbud cuttings may be advantageous when the quantity of propagating wood is limited, but the low rate of rooting makes this method impracticable. Rodriguez-Perez et al. (1993) showed that wounding the base of the cuttings significantly improved the rooting percentage of L. ‘Safari Sunset’. Perez-Frances et al. (2001a) studied the anatomy of adventitious root formation on wounded and unwounded cuttings of L. ‘Safari Sunset’ and L. discolor, and were able to show that adventitious root formation was initiated mainly in the wounded area, and at the basal cut surface of the cuttings. They also found that root primordia were present in the wounded areas as soon as 2 weeks from the time of inserting the cuttings. Perez-Frances et al. (2001a) cited MacKenzie et al. (1986) as claiming that wounding the bases of cuttings improved their rooting. Epstein et al. (1993) studied the metabolism of IBA in two cultivars of L. discolor—one early flowering and the other late flowering. He demonstrated that the early flowering rooted well, whereas the late flowering was difficult to root; ‘early’ also responded better to a 4000ppm IBA treatment. Five weeks after inserting the cuttings, the rooting results were as follows: untreated ‘early’, 17%; hormone-treated ‘early’, 77%; untreated ‘late’, 0%; and hormone-treated ‘late’, 10%. Epstein et al. (1993) showed that these differences in rootability were related to IBA transport and metabolism in the cuttings. There were higher levels of IBA accumulation at the base of the ‘early’ rooting cultivar than in the ‘late’, difficult-to-root one. Ben-Jaacov et al. (1995) studied the rooting of L. linifolium cuttings, produced outdoors in vitro conditions, found that NAA, CO2 enrichment, and sucrose all affected rooting. NAA had the greatest effect among the factors tested, but photosynthesis and sugar levels were also important. When the cuttings were treated with NAA, without adding either CO2 or sucrose, rooting was only 25%. When the atmosphere in the test tubes was enriched with CO2, rooting was increased to 41%, probably because of enhanced photosynthesis. When sugar was included in the medium, without CO2 enrichment, rooting was at a similar level of 43%. However, it is most interesting to note that when both sucrose and CO2 were used, rooting was increased to 70%. These results may have some important implications, both for rooting of cuttings and for propagation of Leucadendron in tissue culture. 3. Grafting. The aim of plant breeding is to make genetic improvements, especially those that lead to better quality and higher yield. It is, however, a long and expensive process. To make breeding more efficient, it

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is possible to breed the scion and the rootstock separately. Grafting is a common technique that is practiced in fruit trees, ornamentals, and vegetables (Gardner 1958; Elliot and Jones 1982; Hartmann et al. 1990; Lee and Oda 2003), and its use had already been suggested in the early days of protea cultivation (Rousseau 1966; Anonymous 1971; Vogts et al. 1976). Many of the Australian proteaceous plants are often grafted (Elliot and Jones 1982; Barth and Benell 1986; Crossen 1991). A comprehensive study of grafting of Leucospermum was carried out from 1976 to 1980 by Brits (1979; 1990a,b). Moffatt and Turnbull (1994) carried out a wideranging study on grafting, which covered many Protea, Leucospermum, and Leucadendron species, and presented the following reasons for grafting proteas: to overcome soil-borne diseases, especially phytophthora and nematodes; to enhance soil adaptability; to propagate hard-toroot clones; to achieve rapid increase of genetic stock; and to preserve endangered selections. However, their studies, and those of Brits, were mainly intended to enable the cultivation of proteas in phytophthorainfested areas of Eastern Australia (Turnbull 1991; Moffatt and Turnbull 1994) and South Africa (Brits 1990a, 1990b). At about the same time, Ben-Jaacov et al. (1989a, 1991a, 1991b) and Ackerman et al. (1997b) demonstrated the beneficial effect of using L. ‘Orot’ (a local selection of L. coniferum) rootstock on the growth of L. ‘Safari Sunset’ and L. discolor in extremely high pH soils in Israel. This demonstration and publications in the local trade journals stimulated local nurseries to produce commercial quantities of grafted Leucadendron plants that were planted in all parts of the country, in all types of soils, and in artificial growth media (Ben-Jaacov et al. 1991b; Ackerman et al. 1997b). Grafting efficiency was greatly improved with the development of the “cutting-graft” method (Burke 1989; Gibian and Gibian 1989; Ackerman et al. 1997b). This simultaneous rooting-grafting method, designated as “stenting” by Van de Pol et al. (1986), is frequently used for propagating roses. Most of the commercial Leucadendron grafting in Israel is done by “cutting-grafts”. Wedge-grafting is used and tying is done with Parafilm strips (Ackerman et al. 1997b). The nurseryman R. Arlevsky (pers. commun., 2002), recognized that L. galpinii might serve as a good rootstock for Leucadendron. Field observations of L. ‘Safari Sunset’ plants grafted on L. galpinii and on L. ‘Orot’ showed differing behavior of these rootstocks in different soils. It is well known that different species of Leucadendron have differing degrees of adaptability to different soil conditions (Eliovson 1983); also, different cultivars respond differently to differing phosphorus regimes (Silber et al. 2000b). Recent studies of water requirements of grafted and non-grafted L. ‘Safari Sunset’ indicated that there were interactions between the rootstock and the water requirements: grafted L. ‘Safari Sunset’ on L. ‘Orot’ pro-

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duced higher yields of flowers under lower levels of irrigation than L. ‘Safari Sunset’ on its own roots. On the other hand, the grafted plants were more sensitive to soil-borne diseases under a high-watering regime (Silber et al. 2003). All the information reported above suggests that further studies are needed of the suitability of rootstocks to specific cultivars, specific soils, and specific cultivation technologies. Grafting compatibility has never been studied methodically: Van der Merwe (1985) tried to understand the intergeneric relationships among the Proteaceae by comparing grafting compatibility between the genera. In general, it seems that grafting compatibility between species in Leucadendron is wider than their hybridization compatibility (Ben-Jaacov et al. 1991b; Moffatt and Turnbull 1994; R. Arlevsky, pers. commun., 2002). Table 4.5 (modified from Moffatt and Turnbull 1994) summarizes leucadendrons grafting. The rootstocks used all belonged to the section Alatosperma. Of the scions used, six were species belonging to the section Leucadendron, and nine to Alatosperma. When the first group (Leucadendron on Alatosperma) was used, 37% of the grafting combinations were 100% successful and 37% gave a success rate below 50%. When the second group (Alatosperma on Alatosperma) was used, 32% of the grafting combinations were 100% successful and 12% gave a success rate below 50%. The conclusion from these data is that there was no correlation in grafting compatibility within the sections or between the sections. The same conclusion may be drawn, regarding grafting compatibility between or within the sub-sections. Two species predominate as rootstocks in Israel: L. galpinii and L. ‘Orot’ (a local selection of L. coniferum). Successful (i.e., the plants stayed alive for at least 5 years) grafting of the following species and cultivars on these rootstocks has been achieved: L. discolor, L. ‘Safari Sunset’, L. ‘Yaeli’, and L. argenteum (R. Arlevsky, pers. commun., 2002). 4. Tissue Culture. Success rates (in vitro multiplication) varied greatly among members of the Proteaceae (Perez-Frances et al. 2001b). Research on in vitro propagation has been done with most of the commerciallygrown proteas (Ben-Jaacov and Jacobs 1986), but at present, commercially grown cultures are available only of some Grevilleas, and a few cultivars of Telopea. Since Leucadendron can be easily propagated by cuttings, there has been little effort to propagate them in vitro. PerezFrances et al. (2001b) reported successful establishment of L. discolor in vitro; they used spring-grown nodal and shoot-tip explants, and treated them with polyvinyl-pyrrolidone to prevent oxidation. Shoots grew and proliferated on half-strength MS medium containing 3% sucrose, 0.7% agar, and benzyl adenine at 0.5 mg L–1. The multiplication rate was low, and it declined with sub-culturing. Earlier attempts to propagate L.

190 Table 4.5.

Grafting compatibility among leucadendrons belonging to various subsections (Source: Moffatt and Turnbull 1994). Delta-seeds CB (Alatosperma)

Scion/Rootstock Leucadendron galpinii (Sandveld)z arcuatum (Arid) nervosum (Jonaskop silver) album (Silver) orientale (Sun) elimense (Crown) Alatosperma floridum (Delta-Seed) macowanii (Delta-Seed) uliginosum (Delta-Seed) stelligerum (Clay) discolor (Sunshine) gandogeri (Sunshine) laureolum (Sunshine) procerum (Sunshine) ‘Safari Sunset’ (Sunshine) z y

Sunshine CB (Alatosperma)

eucalyptifolium

gandogeri

Safari Sunset

salicifolium

—

— — — — 16 (10) —

66 (26) 100 (26) 100 (8) 100 (13) 50 (27) 28 (12)

33 (28) — — — 0 —

— — — — — —

100 (27) 100 (20) — 90 (8) 100 (47) 100 (27)

— — — 57 (7) 57 (18) 16 (5)

— — — — — — — —

— — 83 (27) — 100 (27) — — — 100 (27)

100 (15) — 66 (30) 0 83 (27) 77 (26) 83 (14) 100 (29) 66 (21)

— 33 (28) — — — — — — —

— — — — — — — 91 (41) —

— 100 (28) 37 (17) — 66 (33) 100 (27) 90 (27) 66 (27) 100 (33)

— — — — 77 (29) 71 (19) 83 (12) 100 (29) 66 (15)

floridum

— 33 (20)y — 0

macowanii

Cone bush Successful grafts (%), in brackets: age of oldest grafts (months).

xanthoconus

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‘Safari Sunset’ in vitro failed because of the very low multiplication rate (Perez-Frances et al. 1995). Recently, Ferreira et al. (2003) reported an efficient method for in vitro propagation of L. ‘Safari Sunset’: a modified MS medium containing ascorbic acid (15 mg L–1) and 2% sucrose, amended with BAP at 2 mg L–1 and GA3 at 2 mg L–1, and obtained seven 19-mm-long shoots from each explant. They cut off these shoots, dipped their basal ends in auxin solution (IBA 1 g L–1) for 5 min and for rooting placed them on solid medium or Sorbarods plugs saturated with basal liquid medium, without growth regulators. In both cases, 83% of the shoots showed root formation. The small rooted plantlets exhibited cytological and morphological modifications that might be responsible for their incapacity to survive ex vitro. C. Site Selection and Environmental Responses Leucadendrons and other Proteas are commercially cultivated, very successfully in many places, under very different environmental conditions from those found in their natural habitats (Veld and Flora 1984). Ben-Jaacov (1986) used revised versions of the Climatic Diagrams of Walter and Helmut (1976) to illustrate the climates of the main protea production areas around the world. All books about Proteas emphasize the importance of proper site selection for their cultivation, including that of leucadendrons. Most of these recommendations, however, are based on the various authors’ experience and the environments and soils found in their own areas, and are therefore not always relevant to other places. Matthews (2002) describes 32 species and cultivars of Leucadendron, 28 of which are suitable for use as cut flowers or/and cut foliage. He discussed the hardiness of each, and indicated that most of them are hardy and sustain midwinter frosts of –3°C to –6°C. The plants can probably sustain these temperatures, but flowers of at least some of these species and cultivars (e.g., L. discolor) can be damaged even in lighter frosts. Eliovson (1983) indicated that L. album, L. arcuatum, and L. rubrum grow above the snowline or at high altitudes in the Cape mountains, and should tolerate cold conditions. Leucadendrons are evergreen, but the degree of their activity depends on the location of their cultivation. Vegetative growth of L. ‘Silvan Red’ in South Australia commenced between October and November (spring) and ceased by March (fall). During the summer peak growth season, the average elongation was about 12 cm per month and the average increase in diameter was 0.63 mm (Barth et al. 1996). At high elevation in Ecuador (0 degrees latitude), growth and flowering of L. ‘Safari Sunset’ continues year round (S. Pollack, pers. commun., 2004).

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D. Cultural Practices 1. Specific Requirements of Species and Cultivars. Methods of cultivation vary among species planted as seedlings and vegetatively propagated plants as well as among the cultivars themselves, and specialized publications supply information on the cultivation and post-harvest treatment of specific cultivars, e.g., L. ‘Rosette’, L. ‘Chameleon’, L. ‘Flash’, and L. ‘Asteroid’ (Littlejohn 1994a, 1994b, 1996a, 1996b). In Israel, most of the publications intended to inform farmers are specific for L. ‘Safari Sunset’, the main protea produced in Israel (Shtaynmetz 1998; Shtaynmetz et al. 2002, 2004a), but there are also publications that deal specifically with other cultivars (Shtaynmetz et al. 2000). 2. Spacing. Distances between plants and between rows vary according to the cultivar, methods of production, and traditions around the world: Barth et al. (1996), reporting the yield of fully producing, 6-year-old L. ‘Silvan Red’, indicated that the bushes were 1.0–1.5 m wide and 1.5–2.0 m tall; Cecil et al. (1995) indicated that in Australia, the planting density is generally 2600 plants per hectare. In Israel, L. ‘Safari Sunset’ is planted with spacings of 2 m between rows and 0.8 m within rows, i.e., 6250 plants per hectare, and some growers plant even more densely (Shtaynmetz et al. 2004a). It is recommended to leave a wider space between rows every 50 m, to allow the passage of harvesting vehicles (Shtaynmetz et al. 2004a). With smaller cultivars, such as L. ‘Yaeli’, the distance between rows can be reduced to 1.8 m (Shtaynmetz 1998; Shtaynmetz et al. 2000). 3. Nutrition of Leucadendron The Effect of P Application. Proteaceae originated in Australia and South Africa, where most species grow on leached soils, which are poor in available minerals (Handreck 1997; Richards et al. 1997a). Purnell (1960) described proteoid roots as “clusters of rootlets of limited growth which form lateral root”, are widespread in the Proteaceae. Similar root structures have been described in several other families, and Lamont (1982) described them as “root clusters”. Dinkelaker and Marschner (1995) divided the root clusters into: (1) proteoid-like root clusters, including (1a) proteoid roots of the Proteaceae, and (1b) other non-root clusters of the genera: Casaurina, Acacia, Lupinus, Kennedia, Viminaria, Myrica, and Ficus; and (2) non-proteoid-like root clusters, including dauciform, capilarroid, and stalagmiform roots of the Cyperaceae and Restionaceae, and of the genus Eucalyptus. The function of proteoid roots has been

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investigated since the early 1960s, but their specific role in uptake of nutritional elements, especially phosphorus P, was poorly understood. Jeffrey (1967) observed that the proteoid roots of Banksia ornata were very efficient in adsorbing P, and related this beneficial property to their high surface area rather than to a metabolic factor. Lamont (1983) and Lamont et al. (1984) too attributed the higher P uptake of proteoid roots to the greater soil volume they exploited, and found that, compared with non-proteoid roots, proteoid roots in Leucadendron laureolum had a 15× greater specific surface area (mm2 mg–1) and exploited a 33× greater specific soil volume (mm3 mg–1). Jeffrey (1967) suggested that low P status in a plant induces the formation of proteoid roots and Lamont (1972) extended this idea to include deficiency levels of other nutrients, especially N. Several investigations demonstrated that a proper nutrient regime induced decreased formation of proteoid roots, and at the same time improved shoot growth (Lamont 1972; Groves and Keraitis 1976; Thomas 1981). Idealized relationships between soil nutrient availability and proteoid roots, non-proteoid roots, and shoot production are presented in Fig. 4.1. However, despite the clear evidences that adequate nutrition may be beneficial to shoot growth even in the absence of proteoid roots, Lamont (1986) stated that “There can be no denying that the presence of abundant proteoid roots is a sign of a healthy plant”.

Mass

Shoots

Other roots

Root clusters

Nutrient availability Fig. 4.1. Idealized relationships between nutrients availability and production of root clusters, other roots and shoots (copied from Lamont 2003, adapted from Lamont 1982).

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Nutritional problems gave the impression of being the greatest single cause of difficulties in the nursery culture of proteaceous plants (Thomas 1974). During the 1970s and the 1980s, studies conducted in Australia, Hawaii, New Zealand, and South Africa focused on the nutritional demands of pot-grown Proteaceae (Specht and Groves 1966; Thomas 1974; Groves and Keraitis 1976; Nichols et al. 1979; Thomas 1980, 1981; Nichols and Beardsell 1981a,b; Goodwin 1983; Dennis 1985; Dennis and Prasad 1986; Claassens 1986; Heinsohn and Pammenter 1986; Parvin 1986; Prasad and Dennis 1986; Grose 1989; Buining and Cresswell 1993). It was found that P application to pot-grown plants induced growth impairment, leaf chlorosis and necrosis, and abscission of mature leaves (Thomas 1974; Groves and Keraitis 1976; Nichols et al. 1979; Thomas 1980, 1981; Nichols and Beardsell 1981a,b; Goodwin 1983), therefore, P levels that generally applied for agricultural crops were regarded as toxic for the Proteaceae (Grose 1989). The problem introduced by Nichols et al. (1979), of why P levels that are essential for most other plants are toxic to the Proteaceae, remained unsolved. Elucidation of the problem posed by Nichols et al. (1979), regarding the effect of P nutrition on the development of Proteaceae, gained a breakthrough as a result of the excellent research conducted by Gardner on the legume white lupin (Lupinus albus L.). Gardner et al. (1982a,b, 1983) demonstrated that the availability of P and metal ions in the root environment of white lupin was improved as a result of excretion of citrate and protons from the proteoid roots. Furthermore, the activity of proteoid roots was primarily influenced by the P status in the plant, and their formation was depressed at high rhizosphere-P levels. High P levels and low proteoid root activity in turn reduced manganese uptake (Gardner et al. 1982b). Subsequently, numerous investigations using Lupinus albus as a plant model established a comprehensive knowledge on the interactions between P status in the plant and the formation and functions of proteoid roots (Dinkelaker et al. 1989; Dinkelaker and Marschner 1992; Gerke et al. 1994; Dinkelaker and Marschner 1995; Johnson et al. 1994, 1996a,b; Keerthisinghe et al. 1998; Watt and Evans 1999; Neumann et al. 2000). Recent and up-to-date reviews on these topics have been collected by Lambers and Poot (2003). It is generally accepted that the primary role of proteoid roots is associated with modification of the root environment, i.e., by exudation of organic acids (mainly citric) that enhance P mobilization towards the plant root. It seems that under intensive cultivation conditions, when all nutrient elements are supplied according to plant needs, the specific role of the proteoid roots is limited. In light of the recently accumulated knowledge, it is suggested that high rates of P application to proteaceous plants could reduce the avail-

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ability of micronutrients, especially Fe, Mn, and Zn, because of: (1) precipitation of metal-P compounds; (2) enhancement of specific adsorption of metal ions on the charged surfaces of oxides and hydroxides in the soil following increases in negative charges; and (3) a decrease in solubilization of metal ions following the decrease in excretion of organic acids. It is possible, therefore, that the symptoms of growth impairment, leaf chlorosis, necrosis, and abscission of mature leaves that characteristically affect proteaceous plants following P application, and which in the past were attributed to P toxicity, actually derive from deficiency of metal ions. Thus, it may be correct to extend the term “P-induced zinc deficiency” introduced by Cakmak and Marschner (1986, 1987), to Fe, Mn, and/or any other metal micro-nutrient. This suggestion is supported by Handreck’s (1991) observations that iron deficiency was the main visible effect of P excess on the shoot of Banksia ericifolia, that its severity increased as the P supply increased, and that classic symptoms of P toxicity appeared in plants exposed to high levels of P and low Fe supplementation. Nutritional Demand of Leucadendron. The nutritional demands of Leucadendron ‘Safari Sunset’, the most important cultivar in the protea industry, have been extensively investigated during the last two decades (Silber et al. 1998, 2000a,b,c, 2003). The objective of the research was to assess the response of L. ‘Safari Sunset’ to nutritional management, especially that of phosphate, and all their findings showed that adding fertilizer to the irrigation water resulted in increased biomass production compared with that of tap-water-irrigated plants. The nutritional treatments affected the development of proteoid roots, and root clusters were present mostly in tap-water-irrigated plants. Some proteoid roots developed on plants irrigated with nutrient solution when P was omitted, but none developed in any of the other treatments. Increasing the P concentration up to 20 mg L–1 significantly improved L. ‘Safari Sunset’ growth and there was no indication of toxic symptoms that could be attributed to an excess of P. These results are consistent with the conclusions of Prasad and Dennis (1986) that realistic levels of soil-P concentration (below 40 mg kg–1 as assessed by bicarbonate extraction) are not toxic to L. ‘Safari Sunset’. A significant quadratic regression was obtained between the number of marketable branches and leaf-P concentration of L. ‘Safari Sunset’ plants exposed to various nutrient application rates (Silber et al. 2000a), and similar relationships were obtained for the fresh and dry weights of shoots (not presented). According to the quadratic equation presented in Fig. 4.2, the maximum number of marketable branches was achieved when leaf-P concentration approached 3.4 g kg–1 DW, similar to what has

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Market. branches/plant

20

15

10

5

0

2

4

6

–1

Leaf -P (g kg DW) Fig. 4.2. Number of marketable branches of L. ‘Safari Sunset’ at the end of the 2nd year as a function of leaf-P concentration. The solid line was calculated from the data (open circles) of L. ‘Safari Sunset’ grown in Bet Dagan, Israel, during 1994–1995 and exposed to different nutrient rates in the irrigation water (detailed in Silber et al. 2000a). The solid symbols represent data from a different experiment in which L. ‘Safari Sunset’ plants were grown during 1999–2000 under an identical nutritional regime but were planted in four soils that differed in their buffer capacity and the native pH, which induced differing P availability in the root environment (Silber et al. 2003).

been reported for many plants (Marschner 1995). These results indicate that L. ‘Safari Sunset’ plants are not susceptible to P toxicity at normal P application rates. Fig. 4.2 also includes added data from a further experiment, carried out 5 years later, in which L. ‘Safari Sunset’ plants were grown in several different soils (Silber et al. 2003). The plants in the later experiment were grown under the same nutritional regime but were planted in four soils that differed in their buffering capacity and their native pH, and so induced differing P availability in the root environment. The effect of plant-P status on L. ‘Safari Sunset’ growth is highlighted by the similarity between results attained under two different growth conditions: (1) plants grown in 40-cm deep holes, dug in sandy soil and filled with volcanic material, which were exposed to various nutrient application rates (Silber et al. 2000a); and (2) plants grown

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under an equivalent nutritional regime in soils that differed in their chemical properties (Silber et al. 2003). Furthermore, these findings indicate that leaf-P concentration may be used to monitor the P nutritional regime. The response of two other Leucadendron cultivars (clonal selections of L. coniferum and L. muirii) to different P level was also tested by Silber et al. (2000b). The development of L. coniferum (L. ‘Orot’) plants under P deficiency (no P added in the irrigation water) was significantly superior to that of L. ‘Safari Sunset’ and L. muirii cultivars, but as P application increased to 20 mg L–1, the growth of L. ‘Safari Sunset’ became quite similar to that of L. coniferum. No symptoms of P toxicity were observed even at the highest P level (20 mg L–1) in any of the cultivars tested. Shoot dry weight of L. coniferum plants irrigated with tap water was almost three times that of L. ‘Safari Sunset’ under the same conditions. Nevertheless, the response of L. coniferum to nutrient addition was lower and less significant than that of L. ‘Safari Sunset’. Thus, the dry weight (shoots and roots) production of L. ‘Safari Sunset’ fed with an adequate P level (20 mg L–1) was quite similar to that of L. coniferum plants under the same conditions. The dry weight production (shoots plus roots) of L. muirii plants and their response to the fertilization treatments were the lowest (Silber et al. 2000b). Higher water-N and -P concentrations led to enhanced leaf nutrient status and associated increased photosynthesis rates and stomatal conductance in four Leucadendron species: L. xanthoconus, L. laureolum, L. coniferum, and L. meridianum (Midgley et al. 1999). Increased nitrogen application up to 100 mg L–1 progressively increased the yield of L. ‘Safari Sunset’ but further nitrogen increases reduced it (Silber et al. 1998; 2000a). The NH4-N:NO3-N ratio in the irrigation water is an important factor in ‘Safari Sunset’ growth: the yield of NO3-fed plants was low, their leaves were small and their stem elongation was inhibited, with a “little-leaf” appearance, compared with those of NH4-fed plants (Silber et al. 2000a). These results are consistent with the data of Heinsohn and Pammenter (1986) for L. salignum grown in water culture. However, in an aero-hydroponic system at two fixed pHs (5.5 and 7.5) L. ‘Safari Sunset’ growth was not inhibited at a low NH4-N:NO3-N ratio (Silber et al. 2000c). The results obtained at fixed pH may indicate that the main detrimental effect of a low NH4:NO3 ratio is indirect, e.g., via the pH in the root environment (Silber et al. 2000a). The potassium concentration in the leaves of L. ‘Safari Sunset’ was found to be very low (Cecil et al. 1995; Silber et al. 1998, 2000a,b,c) and below the values considered necessary for other ornamental plants (Jones et al. 1991). Sodium concentrations were high and exceeded on

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a molar basis those of K (Silber et al. 1998). The low K requirement of the Proteaceae may be attributed to an adaptation to the low-K soils on which they originated (Parks et al. 1996; Walters et al. 1991) and that Na may partially substitute for K as suggested by Walters et al. (1991). Effect of pH on L. ‘Safari Sunset’ Growth. The pH in the rhizosphere is an important factor affecting the growth of L. ‘Safari Sunset’ (GanmoreNeumann et al. 1997; Silber et al. 1998, 2000a,c). Silber et al. (2000a) achieved the maximum number of marketable branches when the rhizosphere pH was approximately 6.0; below this value, release of toxic Mn and Al from soil constituents (Silber et al. 1999) impaired plant development, and above it the availability of micro-nutrients was probably too low to provide adequate nutrition. Despite the use of chelates, Fe, Zn, and Mn concentrations in the leaves of plants grown in high pHs were lower than those in plants grown in acidic pHs, and the incidence of “little leaf” attributed to Zn deficiency increased (Silber et al. 2000a,c). Whether pH affects the plants directly through physiological mechanisms or indirectly through its effects on nutrient availability is not clear. Effects of Various Nutritional Regimes on the Growth of Leucadendron Species and on Leaf-Nutrient Concentrations. The optimal nutritional regime for a Leucadendron plant depends on the nutrient availability in the soil, on the one hand, and on the desired or expected yield (number and quality of marketable stems, and the amount of nutrients removed by the crop), on the other hand. Most Leucadendron species are not grown in commercial fields and data are scarce, but information is available for two cultivars of L. salignum × L. laureolum: ‘Safari Sunset’ in South Australia (Cecil et al. 1995) and in Israel (Silber et al. 2003; Shtaynmetz et al. 2004a), and ‘Silvan Red’ in South Australia (Barth et al. 1994, 1996; Cecil et al. 1995). Leucadendron is grown in South Australia on various soil types, including clay, sandy loam and highly leached sands, with pH values between 4.8 and 7.0 (Barth et al. 1996; Cecil et al. 1995). Leucadendron is grown in Israel on sandy soils in the coastal plain or in volcanic clayey soils in the north of the country (Silber et al. 2003; Shtaynmetz et al. 2004a). The climates of both countries are Mediterranean, with cool, wet winters and dry, warm summers. Planting in Australia is at a stand of 2600 plants ha–1, whereas in Israel a much higher stand is used: 6000–6500 plants ha–1. Yields and nutrient removal rates by the crops in the two countries are summarized in Table 4.6. Monitoring nutrient concentrations in plant organs, especially in the leaves, may be a useful means of surveying plant growth and optimizing the nutritional regime. However, caution is advised when trying to

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Table 4.6. Accumulation of dry weight and annual nutrient removal per plant or ha basis for Leucadendron ‘Safari Sunset’ and ‘Silvan Red’ in South Australia and in Israel. Nutrient Cultivar

Silvan Redz Safari Sunsetz Safari Sunsety Silvan Redz Safari Sunsetz Safari Sunsety

DW

N

kg plant–1 5 19 5 28 2.2 19 1300 1300 1360

4.9 7.3 11.8

P

2.8 2.8 5 0.7 0.7 3.1

K

Na

Ca

Mg

Fe

g plant–1 10 25 14 19 10 9

19 26 6

11 9 2

mg plant–1 450 50 450 220 100 500 82 10 380

kg ha–1 2.6 6.5 3.6 4.9 6.2 5.6

4.9 6.8 3.7

2.9 2.3 1.2

117 57 51

Zn

g ha–1 13 26 6

Mn

117 130 99

z

Cecil et al. (1995). Silber et al. (2003).

y

translate analysis data from leaves (or any other organ) into agricultural recommendations, because of seasonal variations in the chemical composition of leaves (Cecil et al. 1995) and in growth conditions. Two groups of published data are available for nutrient values in leaves of Leucadendron plants (Table 4.7): (1) data from commercial fields in Australia (Barth et al. 1994, 1996; Cecil et al. 1995); and (2) data from nutritional experiments in Israel (Silber et al. 1998, 2000a, 2000b, 2000c, 2003), Australia (Parks et al. 1996), and South Africa (Heinsohn and Pammenter 1986). In addition, the recommendations of the Israeli Extension Service (Shtaynmetz et al. 2004a) are included in Table 4.7. Data obtained from commercial fields provide useful information on nutrient contents of field-grown plants, but the growth conditions are rarely well defined or controlled; therefore, the interpretations and the comparison with other data obtained under different conditions may be problematic. On the other hand, data obtained from nutritional experiments representing only small numbers of plants may provide valuable information on nutrient status under well-controlled conditions in which only a single parameter is varied. Leaf-nutrient concentration data from several sources under wide ranges of nutritional regimes and growth conditions, including plant ages, are presented in Table 4.7. 4. Response of L. ‘Safari Sunset’ to Irrigation Regime. The effect of irrigation regime on the growth of Leucadendron species has been examined solely for L. ‘Safari Sunset’ in Israel, where there is a Mediterranean climate, with cool, wet winters and dry, warm summers. The harvest

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Table 4.7. Nutrient concentrations in leaves (Young = youngest leaves on the top of the stem; YFEL = youngest fully expanded leaves; Mature = leaves at the bottom of the stem; All = all the leaves of several Leucadendron species). Macronutrient removal (g kg–1 DW) Leaf

K

Na

Ca

Mg

Safari Sunset Youngz 9–12 1.2–1.5 Youngy 10–12 1.0–1.3 YFELx 4–12 0.3–1.3 Mature1 12–15 0.5–3.5 Allz 10–11 2.2–3.5 Allx 6 0.6 15 3.5 Allw

5–7 3–5 1–4 6–10 5–6 3 6

5–7 nd 2–7 7–11 6–7 4 nd

5–6 7–10 2–5 7–10 7–8 5 14

2–3 70–100 30–90 3–10 60–100 17–25 2–3 26–59 11–61 1–2 100–350 10–90 2–3 80–200 15–70 2 42 19 7 250 120

Silvan Red YFELx Allx L. coniferum (‘Orot’) Allv

N

P

Micronutrient removal (µg g–1 DW) Fe

Zn

Mn

150–350 150–250 105–313 300–400 150–500 95 280

3–7 3

0.3–1.3 0.3

1–3 1–2

3–7 4–5

3–6 3–4

2–3 1–2

22–46 50–199

7–34 8–11

60–146 65–75

18

9.1

7

nd

10

5

nd

nd

nd

Sundance Matureu

10–22 0.5–1.1

6–10

nd

nd

nd

nd

nd

nd

L. salignum Allt

20–30

7–12

nd

nd

nd

nd

nd

nd

0.6

z

Silber et al. (2003) Shtaynmetz et al. (2004a) x Cecil et al. (1995) w Silber et al. (2000a) v Silber et al. (2000b) u Parks et al. (1996) t Heinsohn and Pammenter (1986) y

period of L. ‘Safari Sunset’ in Israel extends from the middle of September (autumn) to the end of April (spring), but usually the majority of the yield (80%) is harvested between early October and the end of December. The plants are pruned during the winter, and the new vegetation appears as the weather becomes warmer around the end of March. Water doses should be adjusted according to weather conditions and plant growth; therefore, the recommendations to the Israeli growers regarding water application are based on pan evaporation data and plant

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conditions (Shtaynmetz et al. 2004a). The pan coefficient (Kp) for the class A pan according to Shtaynmetz et al. (2004a) for adult L. ‘Safari Sunset’ plants is 0.3 (i.e., 2–4 litres per plant per day) in early April (spring), and it increases progressively to 0.9 (12–14 litres per plant per day) at the end of July (summer), and then decreases to 0.6–0.8 (6–10 litres per plant per day) in September–October (fall). Usually, water supply via precipitation during the winter (November–February) provides sufficient water for plant demands and irrigation ceases. Silber et al. (2003) examined the effect of irrigation dose and frequency on L. ‘Safari Sunset’ grown in clayey soil of volcanic origin in the Golan Heights. The daily global irradiance and pan evaporation data (calculated per plant) from the experimental site are presented in Fig. 4.3. The maximum water application rate (100%) was defined as the water dose required to fulfill plant demands without any stress, and was monitored with tensiometers located around the plants at various distances and with phytomonitors. It was found that young plants (1–3 years after planting) responded positively to increased irrigation doses, and significant linear regressions were obtained between the biomass production of the shoots, on the one hand, and the water dose applied and the soil water content, on the other hand (Fig. 4.4). The positive effect of increased water amount on biomass production of L. xanthoconus was reported by Davis, Flynn, and Midgley (1992). However, in the fourth year, after the space between plants had been covered entirely (6200 plants ha–1), the irradiation became the limiting factor for shoot growth, and the yield was no better under the highest water doses (100%) than under a lower rate (70%). Irrigation dose did not affect the number of marketable stems but significantly affected their quality. The diameter of the “flower heads” of plants exposed to low irrigation doses was small, and it increased progressively as the irrigation dose increased (Fig. 4.5). From the marketing point of view, this effect is extremely important in light of the dominant role of the ‘flower head’ dimension on the price of L. ‘Safari Sunset’ stems in the cut flower markets. 5. Overcoming Soil Problems in Cultivating L. ‘Safari Sunset’ in Israel. The two parents of Leucadendron ‘Safari Sunset’ are native to South African soils that have low pH. However, in Israel, despite the suitable climate, growers of proteas have encountered problems because of unfavorable soil characteristics, such as high pH and high free-lime content. Two agro-technical methods are feasible for overcoming these soil limitations (Silber and Ben-Jaacov 2001): (1) improvement of the rhizosphere conditions; and (2) grafting sensitive cultivars onto resistant rootstocks.

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2001 2002

Irradiance (MJ m–2 d–1)

30

2003

25

20

15 1 April 30 July 10

0

50

100

18 October 150

200

250

20 2001 2002 2003

Pan (L pl–1 d–1)

15

10

5 1 April 30 July 0

0

50

100

18 October 150

200

250

Days Fig. 4.3. Meteorological data of three years from the experimental site in the Golan Heights: (top) global irradiation, and (bottom) pan evaporation calculated for single plant (6200 plants ha–1).

4. LEUCADENDRON: A MAJOR PROTEACEOUS FLORICULTURAL CROP

2002 R2 = 0.95 FW = 0.003 * Wat + 1.44

FW (kg/plant)

6

6

4

203

2002 R2 = 0.99 FW = 0.46 * Wat – 8.0

4

2 500

900

1300

1700

2 24

26

Annual water application (L /plant)

28

30

Soil water content (%)

Fig. 4.4. Total fresh weight production (not including roots) of ‘Safari Sunset’ plants (3 years after planting) as a function of: (left) annual water application (L/plant), and (right) soil water content (mL g–1 soil) * 100.

I1

20

Marketable branches per plant

I2 I3 15

10

5

0

4

6

8

10

Head diameter (cm) Fig. 4.5. Effect of water application doses on the “head” diameter of ‘Safari Sunset’ plants (3 years after planting). I1: irrigation doses that fulfill all plant demands during the season, without any stress; I2: 70% of I1; and I3: 40% of I1 (from Silber et al. 2003).

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Improvement of the Rhizosphere Conditions. The common horticultural practice in Israel is to improve the rhizosphere conditions in a restricted volume of the root zone by using a small volume (30–50 litres) of artificial substrate and/or by employing nutritional management that reduces the pH. Leucadendron ‘Safari Sunset’ is often planted in tuff (volcanic material), which is placed in holes dug in the native soil, or on the soil as a small pile. Usually, there are no barriers to the free extension of roots from the tuff into the native soil, and the roots develop under two different environments: (1) a predetermined volume (usually 30–50 L) in the vicinity of the plant, where the tuff properties ensure suitable drainage and pH conditions for plant growth; and (2) the surrounding native soil, where air deficiency or high pH may restrict plant development. Examination of roots at the end of the second year of L. ‘Safari Sunset’ growth demonstrated that at least 80% of the root system was located in the tuff (Silber et al. 2000a). The root system in the tuff was healthy and white with good branching, whereas that in the soil was restricted and brown with poor branching. The use of artificial substrates and of modern irrigation and fertilization equipment enables the appropriate conditions to be provided for plant growth and facilitates control of the rhizosphere pH. Reducing the soil pH through addition of acids via the irrigating solution is almost ineffective and is not recommended, whereas an indirect approach, such as modifying the rhizosphere pH by choice of the N source is more likely to succeed. The nitrogen source affects the rhizosphere pH via three mechanisms (Marschner 1995; Marschner and Romheld 1996): (1) displacement of H+/OH– adsorbed on the solid phase; (2) nitrification/denitrification reactions; and (3) release/uptake of H+ by roots in response to NH4/NO3 uptake. Mechanisms 1 and 2 are not associated with any plant activity, and affect the whole volume of the fertigated soil, but mechanism 3 is directly related to the uptake of nutritional elements and may be very effective because it affects a limited volume of soil in the immediate vicinity of the roots. Obviously, in addition to the above indirect effect, the nature and concentration of the irrigation-N source may have direct effects on plant growth, on chlorophyll content in leaves, and on chlorosis incidence (Mengel and Kirkby 1987; Marschner 1995). Use of a high NH4:NO3 ratio and appropriate nutritional management are common means for achieving desirable pH and ion concentrations in the tuff medium (Fig. 4.6), and hence for improving L. ‘Safari Sunset’ growth (Silber et al. 1998). Grafting Sensitive Cultivars onto Resistant Rootstocks. The use of rootstocks in cultivating Proteaceae was suggested as early as 1966 by Rousseau (1966), but has been commercially adopted only during the

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Total N = 100 mg L–1 NH4:NO3 – N = 1:2

pH

7

6

NH4:NO3 – N = 2:1

5

4

0

50

100

150

200

Days Fig. 4.6. The effect of NH4-N:NO3-N ratio on pH in leachates from growth containers with ‘Safari Sunset’ plants (adapted from Silber et al. 2000a).

last two decades (Ben-Jaacov et al. 1992). Some species, native to highpH soils in South Africa, were studied as potential rootstocks in Israel in the late 1980s. As a result of these studies, several clones and species were selected and the best results were achieved by using a clonal selection of L. coniferum, which was named ‘Orot’, and by propagating L. galpinii. The possibility of improving plant production by using the two alternatives simultaneously, i.e., growing L. ‘Safari Sunset’ grafted on a resistant rootstock in a tuff medium under optimal nutritional management, was proposed as the most promising method. Several studies have shown that the growth of grafted plants was significantly superior to that of ungrafted plants, and that this advantage was more significant under conditions of nutrient deficiency and non-optimal pH. 6. Control of Growth and Flowering—Pruning and Pinching. Efficient pruning to maximize yield is essential, and is a specialized operation in Leucadendron. Brits et al. (1986) first attempted to give systematic, general guidelines for commercial pruning of proteas, including Leucadendron. The growth cycle of leucadendrons depends on the season. They sprout in the spring, slow down their growth through the summer, and then initiate flowers. The reason for the cessation of growth, for flower induction, and for the development of the colorful involucre leaves is unknown. Pruning in done mainly by picking the flowers at harvesting time (Mathews 1982; Brits et al. 1986). Leucadendrons will

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take heavy pruning; therefore, the shrubs can be kept tidy and shaped to any particular need. Ben-Jaacov and Kadman-Zahavi (1988) showed that the imposition of long days at the end of the summer delayed flower development in Leucadendron discolors. At high elevation in Ecuador (latitude 0°), growth and flowering of L. ‘Safari Sunset’ continue year round (S. Pollack, pers. commun., 2004). Like other proteas, leucadendrons may be divided into two groups; sprouters and seeders. The sprouters, which have a lignotuber, will recover easily after heavy pruning, whereas seeders, if pruned heavily, i.e., down to heavy wood that has already lost its leaves, will not sprout (Brits et al. 1986). Most leucadendrons are shrubs, but the silver tree (L. argenteum) is a tree and if allowed to grow straight up it will reach a height of 10 m. It can, however, be restricted to a height of 4–6 m if tip pruned in the first, second, or third year, and it will then cover a diameter of 4–5 m (Mathews 1982). However, if this tree is pruned down to old branches that lack foliage, it will not sprout. The yield and seasonal growth flushing of Leucadendron ‘Silvan Red’, in South Australia, were studied by Barth et al. (1996). They indicated that in South Australia L. ‘Silvan Red’ produces two types of products: in fall stems that terminate in red “flower heads” are harvested, but stems can remain on the bush to be harvested in the winter with tricolor (yellow-red-green) “flower heads.” The use of soft pinch in the springtime doubled or even tripled production, by the growth of two to four more branches on each pinched stem. It is important to pinch only stems that are at least 10 mm in diameter at the base (Wolfson et al. 2001). When pinching is done later in the summer, some of the branches develop into good-quality multi-headed stems, but most of the stems originating in the middle of the summer are of poor quality, many of them of the “little leaf” type (see E2, Wallerstein et al. 1989; Wolfson et al. 2001). Lahav et al. (1997) indicated that the last date for soft pinch of L. ‘Safari Sunset’ grown in the coastal region of Israel is at the end of May or beginning of June. The current recommendation for L. ‘Safari Sunset’ in Israel is to prune heavily in the first two years in order to branch the young plants. Later the commercial pruning is done by harvesting and corrective pruning in the early spring (Shtaynmetz et al. 2004a). E. Plant Protection 1. Diseases. In the recent book by Crous et al (2004) there is excellent information regarding Leucadendron diseases. In addition there are 2 booklets devoted entirely to protea diseases (von Broembsen 1989; Forsberg 1993). In addition, Swart (undated) of the Fynbos Unit in South

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Africa compiled information on the main Protea diseases in South Africa, including the following diseases that attack Leucadendron: Phytophthora cinnamomi (Pc) commonly called “root rot”, “crown rot” or “collar rot”, Fusarium oxysporum commonly called “wilt”, Elisinoe spp. commonly called, “scab” or “corky bark”, Botryts cinerea commonly called “flower head blight”, Coleroa senniana commonly called “coleroa leaf spot”, Batcheloromyces proteae and B. leucadendri commonly called “batcheloromyces leaf spot”, Cerostigmina protearum var. protearum, and C. protearum var. leucadendri commonly called “stigmina leaf spot”, and Vizella interrupta commonly called “five o’clock shadow disease”. In much of the literature, leucadendron diseases are addressed together with diseases of other genera of proteas. Leucadendrons are often infected with fungal diseases of the stems and roots as well as several post-harvest diseases, which are generally caused by widespread fungi with little host specificity. On the other hand, diseases of the leaves are generally caused by Leucadendron-specific pathogens, many of which originated in South Africa. Protea pathogens in South Africa are fairly well documented (Knox-Davies et al. 1986, 1987, 1988) but little is known about pathogens of South African Proteas cultivated elsewhere in the world. Taylor (2001) has recently surveyed all such pathogens in Australia, South Africa, U.S.A., and Zimbabwe, in light of the recent changes in the phytosanitary regulations, ratified by the World Trade Organization (World Trade Organization 1994). Taylor concluded that many of the pathogens that originated in South Africa are already widespread and have varying degrees of importance in other countries. However, other pathogens have been recorded only in South Africa, and measures must be taken to prevent their spread. Different pathogens assume greater or smaller importance in some countries or regions than in others. South African proteas and especially leucadendrons originated in areas of winter rainfall, and when planted in wet and humid parts of the world, where summer rainfall prevails, they are very susceptible to many fungal diseases. Phytophthora root and collar disease, caused by the fungus Phytophthora cinnamomi (Pc), is probably the most serious soil-borne disease of Leucadendron (Von Broembsen and Brits 1985). Pc has an extremely wide host range and has a worldwide distribution (Von Broembsen and Kruger 1985) but, nevertheless, the economic pressure of this fungus on the commercial production of Leucadendron as cut flowers varies greatly with the location. For instance, Forsberg (1993) pointed out that Proteas grown in Queensland are more susceptible to this fungus than those grown in southern states of Australia. This variability may occur because the pressure of this disease is greater in summer rainfall areas (Zentmyer et al. 1994; Zentmyer 1980), or because the

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type of Phytophthora (A2 type) that is dominant in Australia is more virulent than the type (A1) that affects proteas in South Africa (Forsberg 1993). A survey of wild flower farms in the south-west of Western Australia identified two other species of Phytophthora that attack Leucadendrons: P. citricola and P. cactorum (Boersma et al. 2000). Phytophthora cinnamomi has been rarely identified on Leucadendron-infected plants in Israel. Several other soil-borne fungi: Fusarium solani and Pythium Sp. were identified as causing death of Leucadendron plants (Ben-Yephet et al. 1999). The difficulties in identifying the exact cause of a sudden death of mature Leucadendron plants can be seen in a report from New Zealand: Soteros and Dennis (undated) described two wilt disorders that caused concern to leucadendron growers in some areas of the southern parts of New Zealand’s North Island; both are commonly called “wiri wiri” wilt by growers. One disorder was indeed root rot disease, caused by Pc; it was reported to be active mainly when soil conditions were warm and moist. The other disease, which they called “waitara” wilt, initially displayed similar leaf symptoms to the root rot disease caused by Pc, but as Soteros and Dennis (undated) indicated, it is a different disease, which affected only the cultivars ‘Safari Sunset’, ‘Red Gem’, and L. laureolum; it does not affect the root system and is evident mainly during production of the bracts, from autumn to winter. Although chemical spray reduced the spread of the disease, the cause of the disorder has not been identified. Phytophthora dieback, or as it called in Western Australia “protea sudden death”, is still a major problem and is, therefore, currently being investigated in many places (Dieback Working Group 2000; Duncan and Dunne 2000). The occurrence of Pc on silver trees was reported as early as 1973 (Van-Wyk 1973).The occurrence of Pc on indigenous (Von Broembsen and Kruger 1985) and exotic hosts in South Africa has been reported by Von Broembsen (1984). There are four main ways to avoid or overcome sudden death (Pc) of Leucadendron (Brits and von Broembsen 1978; von Broembsen and Brits 1986): (1) plant only on well-drained soil and avoiding over-watering; (2) sanitation: prevent the presence of the fungi in the nursery, in the soil of the plantation, and in the water used for irrigation; (3) use of chemical (Turnbull and Crees 1995; Marks and Smith 1990, 1992), biological (Turnbull et al. 1989), and biofumigant (Duncan and Dunne 2000) methods to control the disease; and (4) use of resistant plant material and/or grafting the desired cultivar on a resistant rootstock. Von Broembsen and Brits (1985) found that L. argenteum and L. salignum were very sensitive to Pc, whereas L. nervosum and L. uliginosum were resistant. Turnbull (1991) and Moffatt and Turnbull (1994) found that L. eucalyptifolium and L. xanthoconus were resistant,

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whereas L. procerum and L. ‘Silvan Red’ were very sensitive. Cultivars and rootstocks can be evaluated for resistance to Pc by several methods, such as stem inoculation techniques (Denman and Sadie 2001). In irrigation experiments conducted in Israel, Silber et al. (2003) observed that under intensive watering treatments more L. ‘Safari Sunset’ grafted on L. ‘Orot’ died from soil-borne diseases than those grown on their own roots. Although Pc, when present, is the main killer of Leucadendron, many other fungi are often found on dying plants, on rooting cuttings, and on young seedlings in the nursery. Among these are: Armillaria (Forsberg 1993), Fusarium solani, and Pythium spp. (Ben-Yephet et al. 1999), and Fusarium oxysporum (Benic 1986). Anthracnose, caused by Colletotrichum gloesporioides, is known in Protea and Leucospermum, but Leucadendron was recorded as being resistant to this disease (KnoxDavies et al. 1986). Moura and Rodrigues (2001) reported that Rosellinea necatrix was the “most frequent” soil fungus found on roots of Leucadendron in the Madeira Islands and indicated that the cultivars ‘Safari Sunset’, ‘Long Tom’, ‘Inca Gold’, and ‘Wilson Wonder’ are very susceptible to the disease, whereas ‘Pisa’, ‘Silvan Red’, and ‘Rising Sun’ seem to be more tolerant. They also identified Fusarium solani and Rhizoctonia solani among the root diseases present in Leucadendron in Madeira Island. Dunne et al. (2003) surveyed 28 protea plantations in southwest parts of Western Australia and were able to isolate Pc in 11 of them. In other plantations, Protea death and decline were attributed to other fungal pathogens, including Fusarium, Botryosphaeria, and Pestalotiopsis, as well as to nutritional disorders and physical factors. Leaf and shoot diseases are very common on proteas (Doidge and Bottomley 1931) and are less common on Leucadendron (Doidge 1950). Schizophyllum commune has been reported to cause “trunk rot” in Leucadendron argenteum (Doidge 1950), and Van-Wyk (1973) reported that Botrryosphaeria ribis caused branch die-back on L. argenteum. The scab disease caused by Elsinoe is a very serious disease of Leucospermum (Forsberg 1993), however it has been reported also on several Leucadendron species (Forsberg 1993). In 1985 Van-Wyk et al. (1985a) reported the identification of Helicosingula as a new genus of fungi that attacks Leucadendron tinctum, and they found Batcheloromyces leucadendri on other Leucadendron spp. (Van-Wyk et al. 1985b) in South Africa. In humid climates, Botrytis blight (B. cinerea) has been reported to damage leucadendrons (Serfontein and Knox-Davies 1990; Forsberg 1993; Moura and Rodrigues 2001). Silver leaf caused by the fungus Chondrostereum purpureum has been reported from New Zealand but has not been detected on Leucadendron in Australia (Forsberg 1993).

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Lasidiplodia, Botyodiplodia, Phomopsis, and Botryosphaeria may cause rotting, mainly of wounded or weak branches (Forsberg 1993). Moura and Rodrigues (2001) isolated Pestalotia guepini, Phoma glomerata, and Stemphylium botryosum from Leucadendron in Madeira. The only fungi that were reported to cause leaf and stem diseases on L. ‘Safari Sunset’ in Israel are Lasidodiplodia (known in Israel as diplodia), which mainly attacks wounded and weak stems, and Alternaria, which has been reported as a storage disease (Shtaynmetz et al. 2004b). In Australia, several leaf and shoot diseases have been reported to attack leucadendrons (Crous and Palm 1999; Crous et al. 2000). Elsinoe scab causes substantial economic losses to proteas including leucadendrons in Australia; a survey showed the most severely affected species and cultivars to be (in descending order): Leucadendron ‘Silvan Red’, L. ‘Safari Sunset’, Leucospermum cordifolium, Leucadendron laureolum, Leucospermum tottum ‘Firewheel’, Leucadendron ‘Inca Gold’, Leucadendron ‘Red Gem’, and Serruria florida (Pascoe et al. 1995) 2. Physiological Disorders. The “little-leaves” phenomenon in L. ‘Safari Sunset’ is well known in Israel (Lahav et al. 1997; Wallerstein et al. 1989; Wolfson et al. 2001; Silber et al. 2003), although this physiological disorder has not been described in the international literature. The leaves along the shoot are small, most of the buds situated at the axes of these leaves are somewhat elongated, and in the autumn the ends of the stems terminate in small involucre leaves without real flower heads. The exact cause of this phenomenon is not well known, but it is enhanced by one or several stress conditions: pruning or pinching in the middle of the summer (Lahav et al. 1997; Wolfson et al. 2001), high soil pH (Silber et al. 2000a), insufficient irrigation (Silber et al. 2003), and insufficient light (Wallerstein et al. 1989). This phenomenon could have been a result of Zn deficiency as hypothesize by Silber et al (2000a), however direct evidence is missing. 3. Insects. Insects are a relatively minor problem in Leucadendron cultivation. Most publications related to insects as pests of Proteaceae address the subject in general and are not specific for Leucadendron (Coetzee et al. 1997; Zachariades and Midgley 1999; Leandro et al. 2003; Wright 2003). Wright (2003) reviewed pests that attack Proteaceae around the world (Table 4.8). It is clear that the greatest problems with insects are in South Africa, so it is very important to try to prevent the entry of these insect into other Protea-producing countries. Leandro et al. (2003) were more specific, and indicated the insects they found on leucadendrons grown in southwest Portugal: Helicoverpa armigera and

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Table 4.8. Major pest groups found on South African proteaceous species, grown in different countries.

Pest group Bud borers Stem borers Root borers Leaf minors Leaf chewers Scale insects Mealybugs Thrips

S. Africa

Australia

New Zealand

x

x

x

x x x

USA (Calif.)

USA (Hawaii)

z

xx xx x xx x xx xx x

x

Zimbabwe x x x

x

x

x x x x

x

z

xx = severe pest, x = occasional/moderate pest (Revised from Wright 2003).

Cacoecimorpha pronubana were found on shoots and flowers; Sesamia nonagrioides attacked the stems of young plants; scales and mealybugs damaged stems and leaves; and aphids attacked shoots of leucadendrons. Wright (undated) described the following insects that attack leucadendrons in South Africa: Epichoristodes acerbella (Lepidoptera: Tortricidae), commonly known as “Carnation worm” and Phyllocnistis spp. (Lepidoptera: Phyllocnistidae), commonly known as “Channel leaf miner”. 4. Nematodes. Root knot nematodes can be a major problem with some proteas under certain climatic and soil conditions (Cho and Apt 1977). These works screened several species of proteas, leucospermums, and leucadendrons for resistance to the nematode Meloidogyne incognita, and found that, in general, Leucadendron is more resistant than the other two genera. Among leucadendrons, L. argenteum and L. discolor were resistant to the nematode, whereas L. laureolum and L. uliginosum were more susceptible. 5. Weeds. Uncontrolled weeds in Leucadendron plantations are harmful. Weed control is important, since Leucadendrons have shallow roots that can be easily damaged by hand-hoeing. Therefore, it is recommended to install woven ground cover in the planting rows. Between the rows, mechanical weed control may be applied, whether the ground is tilled or untilled. If it is untilled, the weeds may be mowed (a common practice in New Zealand), or they can be controlled chemically (DeFrank and Easton-Smith 1990). It is recommended for L. ‘Safari Sunset’ in Israel to spray in the fall, using Goal (oxyfluorfen) at 1000 g/ha +

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Simazine at 2000 g/ha, against winter weeds, and to use nonselective weed killers in the summer (Shtaynmetz 1998). F. Post Harvest Studies 1. Handling and Storage. In general, Leucadendrons have very long shelf lives. Storage, if done properly, can be continued for long periods without any reduction in the shelf life of the flowers. For these reasons, there have been relatively few attempts to improve their storage or vase life. With the increased importance of sea transport, several studies were done, in attempts to improve vase life after long periods of dry storage. Jones and Faragher (1991) and Jones (1991) reported that L. ‘Silvan Red’ maintained a commercially acceptable vase life of 19 days even after 49 days of storage. Pulsing L. ‘Silvan Red’ stems with sucrose solutions at a concentration of 200 g L–1 (20%) or higher for 24 h at 1°C prevented leaf desiccation during 42 days of dry storage at 1°C (Jones 1995). Street and Sedgley (1990) showed that water stress was the main factor that reduced the vase life of L. ‘Silvan Red’. In the last few years, the Israeli growers have been sending about 75% of their yearly 30 million L. ‘Safari Sunset’ stems to Europe by sea (Gazit 2002). The duration of the transport is 10 days, from the producers’ packing house to the Aalsmeer Auction floor. Meir et al. (2000) were able to store L. ‘Safari Sunset’ successfully even for 6.5 weeks. The post harvest procedure for sea transport, as recommended by the Israeli Research and Extension Service (S. Philosoph-Hadas and S. Meir, pers. commun., 2002; Shtaynmetz et al. 2002, 2004b), includes the following steps and precautions: (1) harvest and ship only ripe and lignified, healthy and undamaged stems; (2) place the stems in water containing organic chlorine or simply hydrochlorite; (3) cool the stems at 2–5°C for 24 hr; (4) after sorting the stems, pulse them with 0.5% TOG 4 (containing 8-HQC, citric acid and surfactants) or 0.1% TOG 3 (containing 8-HQC, TBZ, glycolic acid and surfactants); (5) cool the stems in the above solution for 12–24 hr; and (6) dry the foliage and the stems well before placing them in the shipping boxes. However, even when the above procedure is used, problems have occurred from time to time (un-predicted and irregular), involving dry or rotting stems (sometimes only a few in a bunch). The main causes for these problems were identified as diseases, mainly Alternaria but sometimes Clodosporium, Fusarium, or Diplodia; physiological stresses; and physical injuries that stimulate the diseases. After a humid summer, the damage caused by Alternaria was the most serious. To overcome the above fungal diseases, it was recommended to apply preventive sprays

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in the plantations and/or in the packing house, to fumigate the cut stems in the cold rooms, and to remove all physically damaged tissues. Physiological stresses may be caused by freezing and/or by overheating if stems are not cooled down sufficiently before putting them in the shipping boxes or in case of a failure in the cooling chain. The main conclusion was that careful observance of the above recommendation would eliminate the arrival of damaged stems to the markets (Shtaynmetz et al. 2002, 2004a,b). Prolonged storage may be needed not only for sea shipping, but also to regulate the market and to ensure uniformity of the product over a long time. The involucral leaves of the Israeli L. salignum selection ‘Yaeli’ turn yellow about one month before Easter, and in order to be able to market the yellow flowering stems during Easter, (S. Meir pers. commun., 2002) stored the yellow flowering stems for one month. At the end of the storage period, the stored stems bore nice yellow involucral leaves, whereas the stems harvested during Easter carried less attractive, green involucral leaves (Shtaynmetz et al. 2000; S. Meir, pers. commun., 2002). 2. Insect Eradication. Leucadendrons are produced in open field plantations, therefore it is difficult to achieve 100% control of insects, especially if the production is under wild or semi-wild conditions, so that it is sometimes necessary to eradicate insects from the harvested cut branches after harvesting and before marketing. This can be done by chemical treatments or by hot-air disinfestation. In a recent study, it was found possible to achieve control of quarantine pests, including thrips and armored scales, with a hot-air treatment (Hara et al. 2003). The following protocol was recommended for cut branches of Leucadendron ‘Safari Sunset’: increasing the temperature gradually, starting at 39°C for 15 min and at 41°C for 15 min, both at RH of 60–75%, then the eradication treatment at 44°C and RH 60% for 1 hr. This treatment controlled the insects, did not damage the foliage, and did not impair shelf life (Hara et al. 2003). G. Leucadendron as a Pot Plant Woody flowering plants have potential for use as flowering pot plants (Ben-Jaacov et al. 1989b). There is a continuous introduction and development of new woody flowering pot plants (Tal et al. 1994). There is no problem in being able to produce large flowering plants in large pots or tubs, but transport and marketing considerations make the production of such plants uneconomical, and the production and marketing of small (in pots up to 15 cm in diameter) woody flowering pot plants present a

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challenge. Of all the proteas, plants from only three genera are currently being marketed as small flowering pot plants; they are Serruria (Brits 1995), Leucospermum (Criley 1998), and Grevillea (Tal and Ben-Jaacov 1988). There have been only a few attempts to study and produce small flowering pot plants of Leucadendron. To overcome the difficulties in inducing flowers on young Leucadendron plants in small pots, BenJaacov et al. (1986) attempted to use the “Rapid Production System”, which involves the rooting of induced, large, and branched cuttings. This system, which had been suggested several years earlier by Jacobs, Brits and others, was finally developed for Leucospermum by Ackerman and Brits (1991), and Ackerman et al. (1995), who found it possible to root large, branched, and induced cuttings of Leucadendron discolor. The best flowering occurred on cuttings taken between Nov. 21 and Dec. 25 (in the Northern hemisphere). In cuttings taken earlier, the percentage of flowering terminals was low; some did not initiate flowers and many of the flowers that were initiated aborted or reverted to vegetative growth. The stress placed on the plants during the rooting period resulted in the production of low-quality potted plants (Ben-Jaacov et al. 1986). Tal and Ben-Jaacov (1988) attempted to produce L. discolor and L. ‘Safari Sunset’ as flowering pot plants in small (10 cm diameter) pots by using conventional methods of production. They planted 3-month-old rooted cuttings in 10-cm pots, and studied the effects of the growth retardants paclobutrazol and diaminozide in retarding shoot elongation. Two weeks after planting, all the shoots were cut back to two-bud branches. After a further two weeks, when the new growth had reached about 1 cm, the young plants were sprayed or drenched with the growth retardants. Both chemicals and methods of application were effective in dwarfing the plants. However, since the plants never flowered in the small pots, the project was terminated.

V. CROP POTENTIAL AND RESEARCH NEEDS Leucadendron is probably one of the best decorative foliage plants available in the flower market. Its product characteristics (Coetzee and Littlejohn 2001) are excellent, branches have a very long shelf life, measured in weeks; it can be easily shipped by sea and can travel for at least 10 days; and its stems are straight, making it very easy to pack efficiently. Many of the species and cultivars are sold as foliage and can be marketed almost the year round. The color of the foliage ranges from bronze-red through yellow to various shades of green and silvery gray.

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Some of the species and cultivars present greater difficulties than others in marketing, especially male cultivars that are marketed at their flowering time, for example, male L. discolor, characterized by rapid flower senescence leading to very short shelf life. However, the selection of early, mid-season, and late cultivars could extend the production and marketing period of this beautiful flower. The production characteristics of Leucadendron (Coetzee and Littlejohn 2001) are also almost perfect: the yield is much higher than that of any other protea; most species and cultivars have very vigorous growth; production starts from a young age, and the plantations can have a fairly long life. Most species and cultivars are tolerant of low and high temperatures, and if planted under suitable conditions the plants are relatively resistant to diseases and pests. Nevertheless, growers and researchers can do much to further the prosperity and continued expansion of the leucadendron industry. Aspects worthy of attention include: genetic improvement; diversification of leucadendrons; continuous development and improvement of the agro-technology; and increased public awareness of this wonderful flower. We should conserve all the available genetic variability to ensure the possibility of future improvement (Littlejohn et al. 2000). Genetic improvement may be achieved through advances in breeding technology and through the use of a wider range of interspecific hybrids, and also by mutation breeding. Sub-clonal selections have already led to the development of some excellent cultivars, e.g., the variegated L. ‘Safari Sunset’ named ‘Jester’ (Sadie 2002), and the Israeli improved L. ‘Safari Sunset’ named ‘Petra’ (S. Kadosh, pers. commun., 2003). Increasing the selection of leucadendrons available in the market is an important way to increase the total sales volume. There is a need to develop cultivars specifically suited for the production of potted plants, and research is needed for the development of the appropriate technology. There is very little knowledge of the mechanisms of flower induction and development, and greater knowledge of how to control growth and flowering is needed for many reasons. In modern intensive production of L. ‘Safari Sunset’, an excess of shoot length is produced, which is wasted. This is because the achievement of high-quality, large flower heads in this cultivar demands a high level of irrigation, which also leads to excessively long shoots (Silber et al. 2003). Thus, the question is how to produce the large flower heads without producing excessively long stems. For better and more profitable marketing, it is important to improve selling standards. There is an attempt in Israel to sort and market L. ‘Safari Sunset’ according to the size of the “flower head”. Growers and machinery manufacturers are now working on the development

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of a sorting machine based on photographic image processing (S. Kadosh, pers. commun., 2004). It is hoped that this machine will help to ensure the marketing of more uniformly high-quality flowers in an efficient way. There is a need to increase leucadendron production efficiency, and there is now a joint effort in Israel to develop a pruningharvesting machine (Lev et al. 2004). Production and marketing technology of L. ‘Safari Sunset’ is already advanced, and it is important to extend this production technology to other Leucadendron cultivars.

ACKNOWLEDGMENT This paper is contribution No. 617/04 of the Agricultural Research Organization, the Volcani Center, Israel.

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5 Chinese Jujube: Botany and Horticulture* Mengjun Liu Research Center of Chinese Jujube Agricultural University of Hebei Baoding, 071001, P. R. China I. INTRODUCTION A. Origin and History B. Distribution and Production 1. Distribution and Production in China 2. Distribution and Production outside China II. BOTANY A. Taxonomy 1. Botanical Description of Ziziphus 2. Subdivision of Genus Ziziphus 3. Classification of Ziziphus taxa 4. Botanical Description of Important Ziziphus Species 5. Geographical Distribution of Ziziphus B. Morphology and Anatomy 1. Roots 2. Buds and Shoots 3. Flowers and Fruits III. PHYSIOLOGY A. Phenological Phase and Life Cycle B. Flowering and Fruit Set 1. Flowering Time 2. Flower Order 3. Dehiscence of Anther and Stigma Receptivity 4. Pollination and Pollen Germination 5. Fruit Set and Fruit Drop C. Fruit Development *This review was supported by the National Natural Science Foundation of China (30170652), Hebei Natural Science Foundation (302300), and Agricultural University of Hebei (9816-02). The author thanks Mrs. Jia Chunxiang for drawings and Dr. Zhao Jin, Dr. Zhao Zhihui, and Master Qi Yefeng for their help in literature collection. Horticultural Reviews, Volume 32, Edited by Jules Janick ISBN 0-471-73216-8 © 2006 John Wiley & Sons 229

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D. Chemical Composition 1. Fruit 2. Seed 3. Stem Bark 4. Leaf and Root IV. ENVIRONMENTAL REQUIREMENTS A. Temperature B. Water C. Soils D. Wind E. Light, Elevation, and Exposure V. HORTICULTURE A. Crop Improvement 1. Genetic Diversity and Important Cultivars 2. Selection 3. Hybridization 4. Ploidy Manipulation 5. Biotechnology and Mutation B. Propagation 1. Grafting 2. Tissue Culture 3. Seedling Standard C. Field Cultivation 1. Orchard Establishment 2. Training and Pruning 3. Water, Soil and Fertilizer Management 4. Techniques for Improving Fruit Set D. Pests and Diseases E. Harvesting and Handling 1. Harvesting Maturity 2. Proper Harvesting Time 3. Harvesting Methods F. Storage 1. Storage of Fresh Fruits 2. Storage of Dry Fruits G. Processing LITERATURE CITED

I. INTRODUCTION Chinese jujube or Chinese date (Zao or Hongzao in Chinese), Ziziphus jujuba Mill. (Z. sativa Gaetn., Z. vulgaris Lam.), belongs to the Rhamnaceae, Order Rhamnales, which is often confused with ber or Indian jujube (Z. mauritiana Lam. syn. Z. jujuba Lam. non Mill.) but is a distinctly different species (Pareek 2001). It is a native fruit and medicinal plant of China with a very distinct characteristic of producing deciduous bearing branches. It is now commercially produced in China and

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South Korea but grown mainly for ornamental or research purposes in many other counties (Liu 1999, 2000). Chinese jujube is a deciduous fruit tree that blooms in early summer and ripens its fruit in autumn. It is grown in the temperate and subtropical areas of the Northern Hemisphere, especially the drier parts of north China (Liu and Cheng 1995; Liu 2000). The fruits are rich in nutritive substances and have high medicinal value. They are mainly consumed fresh, dehydrated, or processed into candy, jam, juice, wine, syrup, canned food and vinegar (Liu 2004). Because it is widely adapted, early bearing, long lived, rich in nutrition, easy to manage and has multiple uses and fits into long-term intercropping systems, Chinese jujube is becoming increasingly popular in many parts of China, especially in the dry northern parts (Liu 2003, 2004). With appropriate cultivars, commercial cultivation of Chinese jujube can be carried out where the annual average temperature is 5.5–22°C, annual rainfall is 87–2000 mm, and soil pH is 4.5–8.4 (Liu 2003). Chinese jujube is considered to be an ideal economic crop for arid and semiarid areas of the temperate zone where common fruit trees do not grow well. There have been publications and reviews in several languages on various aspects of Chinese jujube (Zeng et al. 1959; Qu 1963; Sin’ko 1976; Tagiev 1976; Guo Y.X. 1982; Cireasa et al. 1984; Chen Z.Y. et al. 1986; Qu et al. 1987; Sivakov et al. 1988; Kim and Kim 1988; Bertolami 1997; Mao 1997; Yang and Liu 1990; Walker et al. 1990; Chen Y.J. 1991; Liu 1992, 1999, 2000, 2002, 2004; Wang 1992; Wang et al. 1992; Qu and Wang 1993; Pareek 2001; Zhang Z.S. 2003; Zhou and Jiang 2003). Most of the research on Chinese jujube has so far been restricted to China and South Korea. The objective of this chapter is to review the botany and horticulture of Chinese jujube, and to summarize recent research, with emphasis on Chinese and Korean investigations. A. Origin and History 1. Origin. Chinese jujube is believed to be a native of China (Qu 1963; Qu et al. 1987, 1989). Its original cultivation center is in the middle and lower reaches of the Yellow River of China and its direct ancestor is sour jujube, Z. acidojujuba C.Y.Cheng et M.J.Liu (syn. Z. jujuba var. spinosa, Z. sativa var. spinosa, Z. vulgaris var. spinosa) (Qu 1963). The fossil record of sour jujube, which still exists in wild, goes back more than 12–14 million years (Qu et al. 1987, 1989). 2. History. Chinese jujube is one of the oldest fruit trees in China. Because of their importance in ancient China, Chinese jujube, peach,

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apricot, plum, and chestnut were called “The Five Fruits” (Liu 2000). Chinese jujube has been in cultivation in China for at least 3000 years based on records in The Book of Songs, a famous Chinese poem book written 3000 years ago (Qu 1963). According to studies of fossils and archaeological finds, the utilization of Chinese jujube is estimated to be more than 7000 years (5290±80 BCE) (Qu et al. 1989). B. Distribution and Production 1. Distribution and Production in China. Chinese jujube is now found within almost all the provinces of China except the northernmost province, Heilongjiang, and the highest and most southwest province, Tibet, from 76° to 124°E longitude, and 19° to 43°N latitude (Liu 2000). It grows at elevations to 1300–1800 m in northern China, and up to 2000 m on the southwest Yun-Gui Plateau (Liu 2000). This distribution is similar to that of walnut in China, except that Chinese jujube can withstand lower temperatures and poorer soil. Because jujubes are widely adapted and their cultivation can be quite profitable, the Chinese jujube cultivator has been increasing dramatically during the past 10 years. Young trees amount to up to half of the total trees in most areas. According to the Yearbook of Chinese Agriculture, the production of Chinese jujube in China increased more than 3fold from 1980 to 2000, i.e., from 376,000 tonnes (t) to 1,306,000 t (see Fig. 5.1).

1400000

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19 94

19 92

19 90

19 88

19 86

19 84

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0

Year Fig. 5.1.

Changes of annual total production of Chinese jujube in China (From Liu 2004).

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The cultivated area in 2003 was estimated to be over 1,000,000 ha with production about 1,500,000 t of fresh weight. Jujube ranks eighth for fresh fruit and first for dry fruit production. The major commercial production is concentrated in the semi-arid and arid areas of North China. The five leading provinces, Hebei, Shandong, Henan, Shanxi, and Shannxi, account for 89% of the total production (see Table 5.1). 2. Distribution and Production outside China. All Chinese jujube growing outside China was directly or indirectly introduced from China (Qu et al. 1987). It was first introduced to countries bordering China, such as Korea, Japan, Afghanistan, Russia, India, Burma, Pakistan, Malaysia, and Thailand (Qu et al. 1987). About the beginning of the Christian era, the Chinese jujube was introduced into Europe through the famous “Silk Road” and is now widely distributed throughout Persia, Armenia, Syria, and the Mediterranean region, especially in Spain and France (Lyrene 1979; Qu et al. 1987). Chinese jujube was first introduced into the USA from Europe by Robert Chisholm and planted in Beaufort, South Carolina in 1837 (Rixford 1917). They were introduced to California and neighbouring states from southern France by Rixford in 1876. By 1901, jujubes had escaped from cultivation in Alabama and are now naturalized along the Gulf Coast from Alabama to Louisiana (Pareek 2001). In places, they have become problematic weeds. During the period 1908 to 1914, several superior Chinese cultivars were introduced

Table 5.1. Leading provinces of Chinese jujube production in China in 2000.

Province

Production (1000 t)

Hebei Shandong Henan Shanxi Shannxi Gansu Guangxi Hubei Liaoning Hunan Total

442 354 178 113 79 31 17 17 14 13 1306

Data from The Yearbook of Chinese Agriculture, 2001.

234 Table 5.2.

M. LIU The distribution of Chinese jujube in the world.

Continent

Country

Asia

Afghanistan, Armenia, Azerbaijan, Bengal, Burma, China, Cyprus, India, Iraq, Iran, Israel, Japan, Kyrgyzstan, Lebanon, Malaysia, Mongolia, Pakistan, Palestine, South Korea, Syria, Thailand, Turkey, Turkmenistan, Uzbekistan

Europe

Bulgaria, Croatia, England, France, German, Greece, Italy, Macedonia, Portugal, Romania, Spain, Russia, Yugoslavia, Slovenia

Africa

Egypt, Tanzania

North America

Canada, USA

Oceania

Australia

Data from Pareek 2001; Liu 2004.

into the USA and tested primarily in California, Texas, Oklahoma, and other southwestern states (Lyrene 1979). Up to now, Chinese jujube has been distributed to more than 30 countries (Liu 2000, 2004) (see Table 5.2). Outside China, the crop is grown commercially mainly in South Korea, with a growing area of 4676 ha and annual production of about 20,000 t, which does not satisfy the local demand (Liu 1999a). There are also smaller production areas in the drier parts of Thailand, Azerbaijan, France, Italy, and the USA (Pareek 2001). In other countries, Chinese jujube trees are used mainly for germplasm research or ornamental purposes (Liu 2000). At present, China is the center of jujube production and trade. Over 98% of the world’s Chinese jujube trees are concentrated in China and almost 100% of Chinese jujube products in the international market are from China (Liu 2000, 2004).

II. BOTANY A. Taxonomy Ziziphus was established as an independent genus by Phillip Miller in 1754 (Liu and Cheng 1995). The generic name was believed to have been derived from Zizouf, the Arabic name of Z. lotus (Bailey 1947). However, some authors prefer Zizyphus as the spelling for the genus name (Paclt 1999). Ziziphus is widespread in tropical, subtropical, and temperate areas of both hemispheres (Liu 1995,1999). It includes many famous medical and fruit species such as Chinese jujube, wild jujube, and Indian jujube (Liu 1995), and is the most concentrated natural source of cyclic

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peptide alkaloid (Zeng 1986), making it one of the most important genera of the Rhamnaceae. 1. Botanical Description of Ziziphus. Pareek (2001) described the genus as erect trees or shrubs, having stipules modified into straight or curved spines. Spines are solitary or in pairs, usually one straight, the other curved. Leaves alternate or subopposite with stipules, coriaceous, strongly 3- to 5-nerved from the base. Branchlets with stipular spines. Inflorescences fascicled or cymose. Calyx 5, with triangular acute lobes, keeled inside. Petals 5, small, cucullate, deflexed, or absent. Stamens 5, slightly adnate to the base of petals, usually longer than the petals. Ovary inferior, 2- to 4-celled, sunk in flat or pitted disk; disk 5- or 10-lobed with a free margin and confluent at base; styles 2 to 4, distinct, or more or less connate, stigma small, papillose. Fruits subglobose, drupaceous and 1to 4-seeded; embryo large or absent. A continuous sclerenchymatous pericycle is present in the axis of the Ziziphus tree (Mitra 1974). The basic chromosome number of the genus is x = 12. Most species, such as Z. acidojujuba C.Y. Cheng et M.J.Liu, Z. incurva Roxb., Z. lotus Lam., Z. nummularia Walk., Z. oxyphylla Edgew, Z. pubescens Oliv., Z. rugosa Lam., and Z. xylopyrus Willd. are mainly diploid (2n = 24), while Z. jujuba Mill. is both diploid and triploid, Z. oenoplia is both diploid and tetraploid, Z. rotundifolia is both tetraploid and hexaploid, and Z. mauritiana contains an array of forms ranging from diploid to tetraploid, pentaploid, hexaploid, and octaploid types, of which tetraploid is predominant (Liu 1993; Pareek 2001). 2. Subdivision of Genus Ziziphus. Based on material available to him, Don (1832) divided the 39 species of Ziziphus into two groups: (1) leaves smooth on both surfaces, (2) leaves downy (pubescent) beneath. Hooker (1872) separated 18 Indian species into three groups on the basis of the type of inflorescence and length of peduncle: (1) flowers in sessile cymes or fascicled in the axils of leaves, (2) flowers in pedunculated axillary cymes, (3) flowers in pedunculated cymes, which are disposed in leafless (rarely leafy) simple or compound spikes. Brandis (1911) classified 14 Indian species into two groups: (1) cymes axillary, sessile or shortly pedunculate, (2) cymes pedunculate, arranged in terminal or lateral panicles. Sussenguth (1953) divided Ziziphus into four groups: (1) cymes simple, axillary, (2) cymes big, disposed in terminal or lateral large panicles, spine short, (3) inflorescence disposed in leafy panicles, (4) cymes in leafy spur. The above-mentioned cannot be regarded as valid subdivisions since they do not point out the status and scientific name of each group and

236

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the characters used are quite unstable (Liu and Cheng 1995). After comparative studies of morphology, growth habit, and geographical distribution, Liu and Cheng (1995) gave the following subdivision of Ziziphus: Section 1. Ziziphus M.J.Liu et C.Y.Cheng Plants glabrous with deciduous fruiting branches and mainly distributed in temperate zones, including: Z. jujuba Mill. and Z. acidqjujuba C.Y.Cheng et M.J.Liu. Section 2. Perdurans M.J.Liu et C.Y.Cheng Plants having at least two kinds of pilose organ, without deciduous fruiting branchlets, and distributed in tropical and subtropical regions. This section contains the following two series. Series Cymosiflorae M.J.Liu et C.Y.Cheng Axillary cymes, glabrous ovary and fruit, thick and hard endocarp, widely distributed in tropical and subtropical areas, including: Z. mauritiana Lam., Z. oenoplia Mill., Z. cambodiana Pierre, Z. spina-christi (L.)Willd., Z. nummularia (Burm.f.) Wight &Arn., Z. horrida Roth., Z. incurva Roxb., Z. lenticellaria Merr., Z. lotus Lam., Z. apetala Hook., Z. glabrata Heyne ex Roth, Z. abyssinica Hochst.ex A.Rich., Z. mucronata Willd., Z. truncata Blatt.et Hall., Z. guatemalensis Hemsl., Z. xiangchengensis Y.L.Chen et P.K.Chou, Z. mairei Dod., Z. montana W.W.Smith, Z. publinervis Rehd., and Z. laui Merr. Series Thyrsiflorae M.J.Liu et C.Y.Cheng Terminal or axillary thyrse, pilose young fruit and (or) ovary, thin and fragile endocarp, concentrated in South and South East Asia, including: Z. rugosa Lam., Z. calophylla Will., Z. attopensis Pierre, Z. hoaensis Pierre, Z. kunatleri King, Z. borneensis E.D.Merrill, Z. javanensis Bl., and Z. fungii Merr. Liu and Cheng (1995) indicated that there are only two species in Sect. Ziziphus and most species belong to Sect. Perdurans, of which about 30% belong to Ser. Cymosiflorae and 70% to Ser. Thyrsiflorae. There are 14 native species in China, two belong to Sect. Ziziphus, eight to Ser. Cymosiflorae, and four to Ser. Thyrsiflorae (Liu and Cheng 1995). 3. Classification of Ziziphus taxa. The number of species of Ziziphus varies according to authors (Pareek 2001). Don (1832) recorded 39 species, Rendle (1959) 40 species, Evreinoff (1964) 80 species, and Johnston (1972) 86 species. Bhansali (1975) reported that the genus contains as many as 135 species, of which nearly 90 are found in the Old World

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and 45 in the New World. Chen and Chou (1982) recognized about 100 species. Liu and Cheng (1995) stated that the number of Ziziphus species is about 170. A precise and comprehensive key needs to be developed after proper characterization of the species. Pareek (2001), based on the available botanical descriptions, developed a tentative key to the classification of Ziziphus taxa under the structure of Liu and Cheng’s subdivision system of Ziziphus. Plants glabrous, fruiting branchlets deciduous

Z. jujuba Mill.

Plants having pilose organs, fruiting branchlets are not deciduous: Axillary cymes, glabrous ovary and fruit, hard endocarp: Trees: Leaves glabrous on both sides: Leaves broadly ovate, many flowered cymes Z. joazerio Mart. Leaves elliptic or ovate elliptic, armed trees Z. spina-christi(L.)Desf. Leaves elliptic, unarmed trees Z. trinervia Roxb. Leaves glabrous above, tornentose beneath: Leaves oblong-ovate or orbicular, obtuse or acute, base rounded oblique, nearly asymmetric Z. mauritiana Lam. Leaves ovate, acuminate, base very asymmetric Z. abyssinica Hochst. ex Rich. Leaves tomentose on both sides, oval, minutely serrulate Z. mistol Griseb. Shrubs: Leaves smaller than 2 cm: Leaves oblong, sharp shining spines, cyme 2–4 flowered Z. hamur Engl. Leaves sub-orbicular or elliptic to ovate, tomentose beneath and

238

M. LIU

less above, flower solitary or 2–3 Leaves ovate, tomentose on both sides, long spines pilose when young, cyme 10–20 flowered Leaves elliptic to obovate, glabrous, sessile cyme Leaves larger than 2 cm: Leaves glabrous on both sides: Leaves oval, acuminate, woolly branchlets Leaves ovate-oblong, prickly shrub Leaves truncate, downy branchlets, two prickles Glabrous branchlets, solitary spines or unarmed Leaves glabrous above and tomentose beneath: Elliptic or ovate-elliptic, sub-entire, several flowered cyme Oval-oblong, entire or slightly denticulate Semi-scandent shrub: Leaves glabrous above and tomentose beneath: Leaves lanceolate-oval, unequal sided, only one spine developed

Z. lotus L.subsp. saharae Maire

Z. nummularia Wight & Arn. Z. parryi Weberb.

Z. napeca Willd. Z. lotus Lam.

Z. truncata Blatt.& Hall.

Z. glabra Roxb.

Z. sipna-christi var. microphylla Hochst. ex A.Rich. Z. mauritiana var. orthacantha (DC.) Chevalier

Z. oenoplia Mill.

Plants having terminal or axillary thyrse, pilose young fruit and (or) ovary, thin and fragile endocarp: Fruit woody, inedible, trees

Z. xylopyra Willd.

5. CHINESE JUJUBE: BOTANY AND HORTICULTURE

Fruit edible: Shrubs, leaves smaller than 2 cm, long petioles Climbing shrubs: Petals 0 Leaves glabrous above, dense fulvous tornentose to glabrous beneath Petals 5 Leaves elliptic oblong, glabrous except on nerves tomentose beneath Leaves ovate acuminate, glabrous above, branches and cyme pubescent Climbers: Glabrous branchlets and cyme, vigorous climber Cyme densely tomentose, vigorous climber Branchlets and cyme pubescent, slender climber Branchlets and cyme sparingly pubescent, slender liane Scattered hair on branchlets, leaves smaller than 2 cm, slender woody creeper

239

Z. oxyphylla Edgew.

Z. rugosa Lam.

Z. kunstleri King.

Z. elegans Wall.

Z. affinis Hemsl. Z. calophylla Wall.

Z. elegans Wall.

Z. horsfieldii Miq.

Z. pernettyoides Ridl.

4. Botanical Description of Important Ziziphus Species. Z. jujuba Mill. and Z. mauritiana Lam. are the two most important cultivated species. The former is deciduous with glabrous leaves, less tropical, and mainly distributed in the temperate zone of China and South Korea. The fruit is used mainly after dehydration and referred to as Chinese jujube or Chinese date. The other major cultivated species, ber or Indian jujube, is evergreen with pubescent leaves and is mainly distributed in the tropical zone of India, Pakistan, Bangladesh, and south China. It produces larger fruit, usually not as sweet as Chinese jujube, and is mainly used fresh rather than dehydrated. Other important species of genus Ziziphus

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M. LIU

include Z. acidojujuba C.Y.Cheng et M.J.Liu, Z. spina-Christi Wild, Z. nummularia Burm., Z. oenoplia Mill., Z. xylopyrus Wild., Z. fumiculose Buch-Ham, Z. glabrata Hyne., Z. oxyphylla Edgew, and Z. rugosa Lam. Chinese jujube (zao in Chinese), [Z. jujuba Mill. non Lam. = Z. jujuba Mill.var. inermis (Bunge) Rhed., Z. vulgaris Lam., Z. vulgaris Lam. var. inermis Bunge, Z. sativa Gaertn., Z. sativa Gaertn. var. inermis (Bunge) Schneid., Z. officinarum Medic., Z. sinensis Lam., Z. chinensis Lam., Z. ziziphus (L.) Karsten, Z. natsme Sieb., Z. flexuosa Wall., Z. nitida Roxb., Z. soprifera Rhom. et Schult., Z. mairei Dode, Rhamnus ziziphus L., and R. lucidus Salisb.] (Qu and Wang 1993; Liu and Cheng 1994; Pareek 2001). A deciduous tree, cultivated in the drier parts of China and South Korea, and to a limited extent in Japan, Thailand, Armenia, Azerbaijan, Turkmenistan, Uzbekistan, Kyrgyzstan, Syria, Spain, France, Yugoslavia, and the southwestern USA. It is 5–10 (30) m high, with glabrous leaves. The bark of young trees is smooth and red-brown, while that of old trees is dark grey with cracks. The branches are zigzagged, usually with paired spines in young plants, one straight, 2.5 cm or so long, the other much shorter, recurved and the older trees usually with no spines. Flowering shoots (bearing shoot) are about 15 cm long, thin, soft and deciduous, fascicled on extremely dwarf branches (mother bearing shoot), and drooping under their weight of fruit. Leaves are alternate and simple, 2.5–5.5 cm long, 2–4 cm wide, broad ovate to lanceolate, glabrous, crenate-serrate, oblique, three nerved; petiole short; the upper lustrous and dark green and the lower light green. Flower is yellow, axillary, single or cymose, 3.5–10 mm in diameter; petals clawed, tips truncate; disk obscurely lobed; styles two, united to the middle. Fruit is a drupe and consists of a thin epicarp and thick, sweet, fleshy mesocarp and a hard endocarp with none to two seeds, red to dark red, round, oblong, ellipsoid or ovate, 1.5–6 cm long, 1.4–4 cm in diameter, short stalked. Stone is spindly, acuate, and tuberculate. Flowers bloom May to July and fruits ripen August to October in northern China. Spineless Chinese jujube has been reported, regarded as a variety of Chinese jujube (Z. jujuba Mill.var. inermis Rhed., Z. vulgaris Lam. var. inermis Bunge, Z. sativa Gaertn. var. inermis Schneid.). Liu and Cheng (1994) found that the extent of spininess varies continuously among cultivars and depends greatly on the age of tree, type of shoot, growing season and habitat; many branches lose their spines gradually and there is no absolutely spineless type of Chinese jujube. In view of this, Liu and Cheng (1994) indicated that the variety (var. inermis) is untenable and should be merged into Chinese jujube.

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241

A number of forms under Z. jujuba Mill. have been reported (Liu and Cheng 1994; Chen and Chou 1982), e.g., Z. jujuba Mill. f. tortuosa C.Y.Cheng et M.J.Liu (Z. jujuba Mill. var. tortuosa Hort., Z. jujuba Mill. cv. Tortuosa), Z. jujuba Mill. f. lageniformis (Nakai) Kitag. (Z. sativa Gatern. var. lageniformis Nakai, Z. jujuba Mill.var. lageniformis Hort.), Z. jujuba Mill. f. carnosicalycis (Wang) C.Y.Cheng et M.J.Liu (Z. jujuba Mill. var. carnosicalycis Wang), Z. jujuba Mill. f. allochroa C.Y.Cheng et M.J.Liu, Z. jujuba Mill. f. heteroformis C.Y.Cheng et M.J.Liu (Z. jujuba Mill. cv. Heteroformis Hort., Z. jujuba Mill. var. quinequeflora Hort.), and Z. jujuba Mill. f. apyrena C.Y.Cheng et M.J.Liu (Z. jujuba Mill.var. anucleatus Y. G. Chen, no latin description). Sour jujube, (wild jujube, acid jujube or suanzao in Chinese), [Z. acidojujuba C.Y.Cheng et M.J.Liu = Z. jujuba Mill. var. spinosa Hu ex H.F.Chow., Z. vulgaris Lam. var. spinosa Bunge, Z. sativa Gaertn. var. spinosa (Bunge) Schneid., Z. spinosa Hu ex Chen non St. Lag., Z. jujuba non Mill.] (Wang and Sun 1986; Qu and Wang 1993; Liu and Cheng 1994). It is deciduous, usually a bush but sometimes a vigorous tree, widely distributed in North China. It grows 2–6 m high, with glabrous leaves. Branches are quite zigzagged with strong paired spines, one straight and 2–5 cm long, the other recurved and shorter; bearing shoots thin, soft and deciduous, fascicled on extremely dwarf branches, drooping after fruit enlarge. Leaves are alternate and simple, 2–5 cm long, 0.7–3 cm wide, ovate to lanceolate, glabrous, crenate-serrate, oblique, three nerved; petiole short; the upper leaf surfaces are lustrous and dark green and the lower surfaces are light green. Flowers are yellow, axillary, single or in cyme, 4–6.4 mm in diameter; petals clawed, tips truncate; disk obscurely lobed, styles two, united to the middle. Fruit is a small drupe, red to dark red, round to ellipsoid, 0.8–2.5 cm long, 0.7–2 cm in diameter, with thick epicarp and thin, sour mesocarp that forms big cavum after dried, short stalked. Stone is tuberculate, round to ellipsoid, obtuse, with two, seldom one, plumpy seed. Flowers bloom during May to July and fruits ripen during August to October in northern China. The taxonomic status of Chinese jujube and sour jujube has been quite disputed, as can be seen from Latin names that have been used for them. Liu and Cheng (1994) treated them as two independent species based on their obvious differences in morphology (fruit size, dried epicarp and mesocarp, and stone shape), habitat, anatomy, utilization, chemical composition, and palynology. Under Z. acidojujuba C.Y. Cheng et M.J.Liu, Liu and Cheng (1994) established three forms: f. granulata, f. trachysperma, and f. infecunda.

242

M. LIU

Ber (Indian jujube), [Z. mauritiana Lam. = Z. jujuba Lam. non Mill., Z. insularis Smith, Z. sororia Schult., Rhamnus jujuba L.] (Pareek 2001). Distributed, either wild or naturalized, in the warmer parts of India, Pakistan, Bangladesh, Sri Lanka, China, Central to Southern Africa, and in the northern parts of Australia (Pareek 2001). It is morphologically diverse, and botanical descriptions of it vary according to authors. Brandis (1874) described ber as a moderate-sized tree, ends of branches decurved or drooping, and in some cultivars erect or spreading, tomentose, rarely glabrous; two-year-old branches slightly flexuose, either dull brown or grey; branches armed with two short stipular spines, one straight, the other bent, or one wanting, or entirely unarmed. Leaves sessile, short-petiolate or on petioles one-fourth the length of leaf, oblongovate, or nearly orbicular, obtuse or acute, 2.5–7.5 cm long, entire or serrulate, often mucronate, occasionally with a few large irregular teeth near the apex, with three main basal nerves or more or less prominent lateral nerves; leaves generally bright tawny or nearly white tomentose beneath, dark green and glabrous above, or more or less glabrous on both sides. Flowers greenish yellow, on short stalk or sub-sessile, or in short pedunculate cymes; pedicels longer than peduncles; calyx lobes keeled to the middle; petals unguiculate, with an oblong-ovate or hood-shaped lamina; anther cells parallel; disk fleshy, 10-lobed, 10-sulcate; styles two, thick, conical, connate to middle. Drupes varying in size, generally about 1.25–1.90 cm long, on a stalk about half its length, globose, oblong, or ovoid, dark brown, orange or red when ripe; kernel irregularly furrowed, mostly two-celled with a hard, thick, bony shell. Trimen (1893) has described ber as a small, much-branched tree or large shrub with a dense spreading crown; bark dark grey, with deep, longitudinal fissures; branchlets elongated, flexuose, woolly-pubescent. Spines paired, short, very sharp, one usually curved, the other straight, often absent. Leaves, 2.5–3.75 cm, broadly oblong-oval or rotundate, rounded at both ends, faintly and irregularly denticulate, base oblique and three-nerved, nerves depressed on the glabrous shining upper surface, densely covered beneath with whitish or buff colored tomentum, petiole short, woolly. Flower in small axillary clusters or very shortly pedunculate, paniculate cymes, greenish-white; pedicel hairy; calyx woolly outside, segments very acute; petals very small, spathulate, recurved; disk 10-lobed, 10-grooved; styles two, connate for half the length, trifid. Drupe about 1.25 cm, globose, fleshy, smooth, yellow; stone two-celled, brown, excavated on surface. The fruit of the cultivated types (Portuguese name ‘Masau’) is larger and more elongated and stone generally one-celled. Troup (1921) reported that the tree sometimes reaches large dimensions (24 m high and 7 m girth). Bailey (1947) gave a similar account and

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stated that the trees may reach 9–15 m in height, flowering in March–June and berries ripening in November–December. Kirtikar and Basu (1975) stated that ber is a sub-deciduous tree, the juice turning purplish-black on the blade of a knife; leaves 3–6.3 × 2.5 × 5 cm; petiole 2.5 to 10 mm long. Johnston (1972) described the species as follows: branchlets dense and minutely pubescent; leaf blades elliptic to ovate to nearly orbicular, 3–8 cm long, 1.5–5 cm broad with rounded symmetrical or nearly symmetrical base, obtuse, densely tomentose beneath, petioles 5–10 cm long; few to many flowered cymes, peduncles 1–4 mm long, tomentose; pedicels 2–4 mm long in flower, 3–6 mm in fruit, tomentose; sepals 1.5–2.0 mm long, dorsally tomentulose; petals 1–1.5 mm long; ovary cells and seeds two; drupes globose to ellipsoidal, 1–2 cm wide. Pareek (2001) mentioned two varieties under Z. mauritiana Lam., i.e., Z. mauritiana Lam. var. jujuba (L.) Lam. (Z. mauritiana Lam. var. orthacantha Chevalier, Z. orthacantha DC.) and Z. mauritiana var. deserticola Chevalier. 5. Geographical Distribution of Ziziphus (Liu 1995). Ziziphus is distributed horizontally from 34° south latitude (Z. mucronata Willd.) to 51° north latitude (Z. jujuba Mill.), and up to 2800 m vertically (Z. xiangchengensis Y. L. Chen et P. K. Chou). Most of the species are distributed in tropical and subtropical regions. Very few species are distributed in the temperate zone. More than 50% of the total species are concentrated in Asia but only 2.9% in Europe and 5.3% in Oceania (see Table 5.3). Most species are very localized, limited to one continent, one country, or even one small island. However, a few species are dispersed over vast areas. Z. jujuba is distributed in temperate to subtropical areas in the Northern Hemisphere; Table 5.3.

Distribution of Ziziphus species in the world. Distinct species

Continent Asia Africa North America South America Oceania Europe Data from Liu 1995.

Species No.

Continent/world (%)

No.

(%)

88 28 31 28 9 5

51.8 16.5 18.2 16.5 5.3 2.9

82 19 28 27 2 3

93.2 67.9 90.3 94.4 22.2 60.0

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M. LIU

Z. mauritiana in tropical and subtropical areas of Asia, Africa, and Australia; Z. spina-christi in north Africa and southwest Asia; Z. oenoplia in South and Southeast Asia and North Australia; Z. lotus in the littoral countries of the Mediterranean. Ziziphus is distributed in all of the six regions, seven of the eight subregions, and 23 of the 34 districts of Takhtajan’s system on the subdivision of world flora put forward in 1978. The Indo-Malaysia subregion, i.e., South and Southeast Asia, includes 92.5% of the Asian Ziziphus species and 47.7% of the world species. It also includes all the sections and series of Ziziphus. In addition, almost all species of Ser. Thyrsiflorae are concentrated in this area. In view of these facts, the Indo-Malaysia subregion should be considered the center of both distribution and evolution of genus Ziziphus. China has abundant Ziziphus resources. Its 14 species are distributed throughout the country, with the exception of the northern Heilongjiang province. In China, Sect. Ziziphus is concentrated in the middle and lower parts of the Huanghe River valley. This is also the evolutionary center of Sect. Ziziphus. Sect. Perdurans and Ser. Cymosiflorae are distributed in Taiwan, Yunnan, Hainan, the southeast of Tibet, the southwest of Sichuan and Guizhou, and the south of Guangdong and Fujian provinces. Ser. Thyrsiflorae is distributed only in Hainan, the south of Yunnan, and the southwest of Guangxi province, which is also the evolutionary center of Ziziphus in China. B. Morphology and Anatomy 1. Roots. The root systems of Chinese jujube are of two types according to propagation methods (Qu and Wang 1957; Liu 2004): seedling root (propagated by seed) and stem-originated root (propagated by dividing suckers or offshoots, cuttings, or tissue culture). A seedling root system has both vertical (main) and horizontal (lateral) roots, of which the former is more developed (see Fig. 5.2). In young seedlings, the length of the vertical root is usually twice that of the aerial part of the plant. However, a stem-originated root system has much longer horizontal roots, which often run more than twice the spread of the canopy. Compared with common fruit trees such as apple and peach, Chinese jujube has a sparser root system, usually occupying the top 15 to 100 cm of the soil. Prolific offshoot or sucker is a predominant characteristic of Chinese jujube. The offshoots mainly occur from horizontal roots with diameter of 5–10 mm. The formation of offshoots is related to cultivar, propagation method, and tree vigor. Using offshoots is a common method of traditional reproduction of Chinese jujube. There is a natural Vesicular arbuseular mycorrhiza (VAM) often asso-

5. CHINESE JUJUBE: BOTANY AND HORTICULTURE

Fig. 5.2.

245

Germinating process of seed of Chinese jujube.

ciated with the root system of Chinese jujube. Lu et al. (2003) reported that VAM could increase plant height, leaf area, fresh and dry mass, leaf relative water content, photosynthetic rate, transpiration rate, and stomatal conductance, and improve plant drought tolerance when the relative water content of the soil was less than 60%. Mycorrhizal plants consumed 16.5%–29.8% less water than non-mycorrhizal plants in producing. 2. Buds and Shoots. Chinese jujube has three kinds of buds: main bud (primary bud), secondary bud, and dormant bud, and four types of shoots: (primary) extension shoot, secondary shoot, mother bearing shoot, and bearing shoot (see Figs. 5.3–5.7).

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Each node has one main bud (upper) and one secondary bud (lower). The main bud exists on the tip and at each node of the primary extension shoot and at the apex of the mother bearing shoot. The main bud on the tip of the primary extension shoot develops a new primary extension shoot every year, and the lateral main bud (beneath the nodes of primary extension shoot or the base of secondary shoot) does not sprout new ES* TMB MS

MB

NS* LMB

ES

MS ES SS

SB

MS* TM MB

ES

MB

NS LMB

MS

Shoot *

MS ES

SB

BS

Bud TMB

DA MS*

MB LMB SB

ES

SS SB

BS*

ES DB MS * Main type at beginning, but becoming secondary gradually as age increases; = forming; = including. Fig. 5.3.

The interrelation between buds and shoots (from Liu 2002, 2004).

MB = main bud; SB = secondary bud; DB = dormant bud; ES = primary extension shoot; SS = secondary shoot; MS = mother bearing shoot; BS = bearing shoot; TMB = top main bud; LMB = lateral main bud; NS = not sprouting; DA = die away.

5. CHINESE JUJUBE: BOTANY AND HORTICULTURE

Fig. 5.4.

247

Morphology of structure of 1-year-old shoot of Chinese jujube.

1. Shoot system in dormant season. 2. Shoot system in growing season. 3. Extension shoot. 4. Secondary shoot. 5. Top main bud. 6. Lateral main bud. 7. Stipulary spine. 8. Bearing shoot. 9. Deciduous secondary shoot. 10. Leaf.

Fig. 5.5.

Morphology of structure of perennial shoot of Chinese jujube.

1. Perennial shoot system in dormant season. 2. Perennial shoot system in growing season. 3. Mother bearing shoot. 4. Bearing shoot.

248

Fig. 5.6.

M. LIU

Mother bearing shoot (MBS) of Chinese jujube.

1. Young MBS. 2. Middle-aged MBS. 3. Old MBS. 4. Very old branching MBS. 5. The top main bud of MBS forming extension shoot system.

Fig. 5.7.

Shoots from dormant buds of Chinese jujube.

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shoot except when given strong stimulation. On the other hand, the secondary bud is an early-maturing bud, existing on each node of the extension shoot and the mother bearing shoot, producing a secondary shoot or a fruit-bearing shoot in the current year, respectively. The main buds on each node of the secondary shoot sprout mother bearing shoots. With strong young trees, fertile soil, good irrigation, or severe pruning, the main buds on the tip of the mother bearing shoot and the lateral main buds may also develop extension shoots. The primary extension shoot (zaotou in Chinese) elongates every year, usually by more than 50 cm. Secondary shoots, usually shorter than 40 cm, do not elongate and wither back year by year from the second year on. The mother bearing shoot (zaogu in Chinese) is an extremely condensed spur that grows only about 1 mm a year, producing 3–5 bearing shoots each year. Bearing shoots (zaodiao in Chinese), usually shorter than 20 cm, are very thin, soft, and deciduous. They form in spring and drop in late autumn. The primary extension shoot, secondary shoot, and bearing shoot are zig-zagged and spiny. 3. Flowers and Fruits. The inflorescence is a cyme borne in the axils of the leaves on the current-season bearing shoots. The flowers are shortstalked, light greenish-yellow, and 2.9 to 10 mm in diameter. The flower buds appear singly or in clusters up to 10 in the axil of each leaf (Ackerman 1961) (see Figs. 5.8 and 5.9). Flower buds complete differentiation and development to mature fruit within a single growing season (Qu et al. 1963, 1981).

Fig. 5.8.

Morphology of inflorescence and opening order of flower in Chinese jujube.

a, Single flower cyme. b and c, Common cyme. 1–4, Opening order of flower.

250

Fig. 5.9.

M. LIU

Opening process of single flower of Chinese jujube.

The fruit of Chinese jujube develops from two parts of the flower, the disk and the ovary (see Fig. 5.10). The shape of the fruit may be round, oblong, oval, ovate, obovate, oblate, red pepper-like, apple-like, and also some abnormal shapes (see Fig. 5.11). More than half of the cultivars have either no seed or shriveled kernels, while others have one or two plump seeds per fruit.

III. PHYSIOLOGY A. Phenological Phase and Life Cycle 1. Phenological Phase. The phenological phase of Chinese jujube (see Fig. 5.12) varies with year, location, and cultivar. Compared with common fruit trees, it begins growth later in the spring and completes leaf fall earlier in the autumn, with a growing season of only 160–185 days. ‘Pozao’, a leading cultivar, illustrates this annual pattern. In Baoding, Hebei, China, the buds sprout in middle April, the leaves expand in middle to late April, flowering starts in middle to late May and finishes around the end of July, fruits ripen around the end of October, and leaf fall begins in late October.

5. CHINESE JUJUBE: BOTANY AND HORTICULTURE

Fig. 5.10.

251

Fruit, stone and seed of Chinese jujube.

1. Lignified bearing shoot. 2. Common bearing shoot. 3. Fruit formation: 3a from ovary, 3b from disk. 4. Straight-cut of fruit. 5. Stone. 6. Two seed stone. 7. One seed stone. 8. Seedless stone.

Fig. 5.11.

Fruit shape diversity of Chinese jujube.

252

Fig. 5.12.

M. LIU

Phenological phase of Chinese jujube.

2. Life Cycle. The life cycle of a natural-growing Chinese jujube can be divided into five phases (Qu and Wang 1993; Liu 2002): juvenile phase (lasting 3–8 years), growing and fruiting phase (some 5–10 years), fruiting phase (over 50 years), fruiting and renewing phase (some 30 years), senescence phase (some 20 years). Under proper soil and climate conditions, the tree can enter another cycle. Chinese jujube is outstanding for its long life as a productive tree. Trees can continue to bear fruit for up to 1000 years and even more. B. Flowering and Fruit Set 1. Flowering Time. Flowering time in Chinese jujube varies at different locations and depends on cultivar and climate. In northern China, flowers emerge during the summer (mid May–late July), with peak flowering occurring around mid June (Qu and Wang 1957; Zeng et al. 1959). The flowering season ranges from June 10 to July 25 in Korea (Cheong and Kim 1984; Kim and Kim 1984). In Chico, California, USA, flowering begins in the middle of May, reaching a peak two or three weeks later, followed by sporadic flowering until the end of August (Ackerman

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1961). Flowering can be prolonged by supplementary light in the autumn (Lyrene 1983). Within an inflorescence, the central bud is the first to open, while those around the outer edge may open as much as two weeks later (see Fig. 5.8). About 17 to 20 days pass between first appearance of a flower bud and anthesis. A slit at the top of the flower bud indicates initiation of its opening (see Fig. 5.9). A cultivar-specific anthesis pattern has been observed in Chinese jujube and other Ziziphus species such as ber and sour jujube (Qu et al. 1989; Wang et al. 1989; Pareek 2001). Anthesis in one group of cultivars takes place at night and in the other group occurs during the daytime. However, the petal stamen separation time (time of anther dehiscence) of both groups is in daytime (Qu et al. 1989). The time of anthesis can be significantly influenced by low temperature, and cloudy and rainy weather (Qu et al. 1989; Wang et al. 1989). Kim and Kim (1984) observed that some Chinese jujube cultivars, including ‘Moodeung’, ‘Geumsung’, ‘Jj-3’, ‘Ja-2’, ‘Jb-21’, ‘Jc-3l’, and ‘Jk4’, opened their flowers in the afternoon and ten other cultivars had anthesis in the morning. Some Chinese jujube cultivars grown in Florida (USA) opened their flowers each day between 7.00 and l0.00, while in other cultivars, the flowers opened between 14.00 and 17.00 (Lyrene 1983). Kim and Kim (1984) observed that the cultivars that opened their flowers in the afternoon required a photoperiod of 12 hr, while those having anthesis in the morning did not require a definite dark period for induction of flowering. On completion of anthesis, the sepals slowly turn outwards, leaving the anthers and petals leaning over the ovary. Thereafter, the petals also move outward, close to the sepals, and finally the anthers follow the same pattern (Qu et al. 1989). 2. Flower Order. The flowering habit of Chinese jujube is distinctive (Pareek 2001). Bearing shoots develop leaves and flowers simultaneously. Flower emergence was more abundant on the middle part of the bearing shoot than on the basal or upper part. The flowers near the middle of the bearing shoots are usually the first to mature. Later blossoms develop along the branchlet towards both the apex and base (Qu et al. 1989). 3. Dehiscence of Anther and Stigma Receptivity. When anthers dehisce, a longitudinal slit is formed on the lobes. The epidermal layer then dries and rolls back, exposing the yellow sticky pollen. Dehiscence usually begins soon after the petals open, but it may begin even before the anthers emerge from the sheaths (Ackerman 1961). Pollen dehiscence takes place during the first day of flower opening (Thomas 1924).

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The dark orange flower disk begins to exude nectar shortly after the petals open and remains sticky for 16 to 22 hours. Ackerman (1961) found that maximum fruit set occurred when pollination took place on the day of anthesis. 4. Pollination and Pollen Germination. To the naked eye, fresh pollen appears as a sticky mass of fine, yellowish powder. A number of pollen anomalies have been observed in Chinese jujube cultivars. These include very large or very small grain size, two pores (versus the normal 3 pores), polyporous, sterile or with vegetative cells having coarsely granulated cytoplasm (Romanova et al. 1985). The pollen of Chinese jujube is sticky and ineffective for wind pollination. The nectariferous disk attracts considerable insect activity. Ackerman (1961) observed large numbers of honeybees, houseflies, and ladybirds (Coccinella novemnotata) in Chinese jujube flowers in Chico (California). The housefly and the honeybee were most active at noon. The housefly was active over a longer period than the honeybee and its frequency of visits was higher. Maximum insect activity during the day was between 11.00 hr and 15.00 hr. It is reported that insects such as the honeybee (Apis sp.), housefly (Musca domestica), and yellow wasp (Polistes herbaracus) are the main pollinating agents for ber (Teaotia and Chauhan 1964; Dhaliwal 1975). A degree of pollen sterility has been observed. Pollen viability is low in most Chinese jujube cultivars (50% to less than 10%, Liu and Peng 1992; Wang 2004) compared with ber (over 68%, Prasad 1964; Hulwale et al. 1995). ‘Kitalskil 86’ has completely inviable pollen, ‘Ya-tszav’ has only 15% viable pollen, but ‘Yubilelnyl’ has 96%, ‘Vakhshskil 41-91’ and ‘Kitalskil 52’ 100% viable pollen (Romanova et al. 1985). The percentage of empty pollen varied in cultivars from 30.2% in ‘Moodeung’ to 29.2% in ‘Geumsung’, 11.75% in ‘Wolchul’ and 5.1% in ‘Sanjo’, a sour jujube (Yun et al. 1989). Pollen was observed to lose viability when stored at –18°C (Yang et al. 1994). After pollination, success in fertilization depends not only upon viability of the pollen but also the stigma receptivity. Yun et al. (1994) observed only 1.5 pollen grains per stigma in the Chinese jujube ‘Moodeung’. It is difficult for the pollen grains to adhere to the characteristically dry stigma; pollen tube growth is also slow in the style. Pollen can germinate in sucrose culture medium. Pollen germination and pollen tube elongation increased with increasing sucrose concentration up to 10% in 1% agar medium and then decreased at higher concentrations in ‘Moodeung’ and ‘Bokjo’ (Park and Yun 1989). Addition of 35 ppm boric acid to the culture medium increased pollen tube growth (Yun et al. 1989). Yun et al. (1989) obtained maximum pollen ger-

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mination of 37–39% by 24h culture at 25–30°C in 1% agar medium containing 15% sucrose if the pollen was obtained immediately after anthesis. Percentage germination decreased thereafter with no germination 24 hr after flowering. 5. Fruit Set and Fruit Drop. There is an old saying in China: “three years for peach, four years for apricot, five years for pear, while only one year for Chinese jujube to get repayment.” Under proper management, Chinese jujube begins to blossom and set fruits in the year of planting or the next. In northern China, some Chinese jujube trees are more than 1,000 years old and are still fruitful. Chinese jujube can complete the whole process from flower bud differentiation to fruit ripening in one growing season (Qu et al. 1981). With abundant flowering and a long flowering season (1–2 months), it has great potential for high yield (see Table 5.4). Fertilization was observed 10 days after pollination, proembryo formation after 20 days, the globular embryo stage appeared after 30 days, and the embryo could be distinguished after 40 days. The embryo grew rapidly between 45 and 50 days post anthesis. Chinese jujube has abundant flowering but very low fruit set. Less than 2% of the flowers normally develop into mature fruits (Qu and Wang 1993). A heavy drop occurs soon after fruit set, which is caused by lack of fertilization or degeneration of the ovule. Fruit drop also occurs due to soil moisture stress, low relative humidity, lack of sunlight, and strong wind during the fruit maturity period (Liu et al. 1997). Diseases and pests can also cause fruit drop. The extent of fruit drop varies among cultivars and times of fruit set. In Chinese jujube ‘Geumsung’, fruit drop was lower (30%) and the proportion of seeded endocarps was higher (90%) in the fruits that set between June 21 and 25 compared to those set earlier (Kim and Kim 1983a). C. Fruit Development The time required for fruit maturation varies among early-, mid-, and late-maturing cultivars and climatic conditions, ranging from 60 days to Table 5.4. The yield of ‘Linyilizao’ under a superintensive planting system (15,000 plants/ha). Year after planting Planting year Second year Third year Fourth year

Yield (t/ha) 1.8 11.3 19.1 26.1

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145 days (Liu 2003). The fruit development period is slightly longer in the warmer climate and slightly shorter in the cooler climate. Cheong and Kim (1984) reported that fruits took 40–50 days for pit hardening and 100 to 120 days for maturity after full bloom. The testa became dark brown 100–110 days after full bloom (Kim and Kim 1983b). The period before pit hardening was characterized by rapid growth of the seed and fruit and the appearance and growth of endosperm. During pit hardening, there was a temporary cessation in fruit growth when the seed and endosperm reached full size. After pit hardening, slow growth of the fruit, growth and maturation of the embryo, and deterioration of the endosperm occurred. The average percentage of fruits with seeds and normal embryos was 20 and 17%, respectively. It is not known for certain whether or not Chinese jujube is a climacteric fruit. Lu et al. (1993) regarded Chinese jujube as non-climacteric. Slicing the fruit of ‘Gansu’ evoked a typical wound-induced respiration, with a peak at about 12 hours (Lu et al. 1993). The maximum ethylene production lagged behind the respiration peak. Exposure to abscisic acid significantly increased both ethylene production and respiration, whereas IAA decreased both. Application of GA increased but delayed the respiration rise and repressed ethylene production. Development of the wound-induced respiration and abscisic acid- or GA-stimulated respiration were blocked by chloramphenicol, but were not inhibited by cycloheximide or actinomycin D. Potassium cyanide inhibited both wound-induced and abscisic acid- or GA-stimulated respiration. In the ripening fruit, abscisic acid content increased rapidly during the early stages but declined toward the end (Kuliev and Akhundov 1975). A close correlation has been observed between abscisic acid and catechin contents during the ripening period. Catechin content declined to 10 to 20% of the original content during the second half of the fruit ripening period. Total carbohydrates, starch, total sugars, and reducing sugars increased both in the fruit and seed during fruit development, while non-reducing sugars and moisture content in the seed decreased with seed development. Lipid content in the seed increased 42 days after full bloom (Pareek 2001). D. Chemical Composition 1. Fruit. Chinese jujube fruit is a well-known nourishing food and traditional medicine in China and many other countries of East and Southeast Asia. It is richer than most other fruits in sugar, vitamin C, cAMP, edible cellulose, and minerals (Qu et al. 1987; Liu and Wang 1991; Liu

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2003). The composition of fruits has been widely reported (Tasmatov 1963; Baratov et al. 1974; Ristevski et al. 1982; Ivanova 1982; Cireasa et al. 1984; Ming and Sun 1986; Liu 2003). Wang et al. (2002) reported the chemical composition of the fruit of nine representative cultivars of Chinese jujube, and most compounds varied among cultivars (see Table 5.5). Chinese jujube fruits were found to be generally much richer in calories, carbohydrates, minerals (calcium, iron), vitamin C, and cAMP than other fruits (Liu 2004) (see Table 5.6). Chinese jujube fruits are very rich in vitamin C and vitamin B-complex (Troyan and Kruglyakov 1972; Kuliev and Guseinova 1974). In some fruits, Baratov et al. (1974) reported 188 to 544 mg vitamin C and 354 to 888 mg vitamin P per 100 g pulp. Ahmedov and Halmatov (1969) and Troyan and Kruglyakov (1972) have reported even higher contents of vitamin C (up to 881 mg/100 g) and vitamin P (up to 1230 mg/100 g) in jujube fruits. Fresh fruits of sour jujube contain 800 mg/100 g vitamin C (Wang et al. 1992). Bi et al. (1990) and Kuliev and Akhundov (1975) reported very high contents of vitamin C in Chinese jujube cultivars at the early ripening stage. The peak vitamin C content occurs at the whitegreen ripening stage (Kuliev and Akhundov 1975; Bi et al. 1990; Peng 2003). The contents decline during the later stages, reaching levels two to 10 times lower than that of the early ripening stage. Catechin content is 10 to 20 times lower in fully mature jujubes (Kuliev and Akhundov 1975). Bi et al. (1990) observed that the vitamin C content declined from 1096 to 411 mg/100 g during ‘Hamazao’ ripening. More vitamin C was found in the fruit flesh at the centre than near the skin and more in the upper part than at the styler end (Krivencov et al. 1970). In addition, the contents of vitamin C decreased sharply by 8–10 times within one to three months after harvest, while vitamin P declined only slightly (Baratov et al. 1974). Even one fruit of Chinese jujube per day in the daily diet of an adult person would meet the requirements of vitamin C and vitamin B-complex recommended by FAO/WHO (Anon. 1974). Cyong and Hanabusa (1980) and Cyong and Takahashi (1982) first isolated cyclic adenosine monophosphate (cAMP) and cyclic guanosine monophosphate (cGMP) from the fruits of Chinese jujube. Dried fruit contained 100 to 600 nmol/g cAMP and fresh fruit from 100 to 150 nmol/g. Hanabusa et al. (1981) observed that the contents were about ten times higher than in any other fruit. Qu et al. (1987) reported that the contents of cAMP and cGMP as well as cAMP/cGMP in flesh varied greatly during fruit development; cAMP and cGMP contents increased sharply during fruit ripening and peaked in fully mature fruit; the value of cAMP/cGMP varied between 0.6–3.53. Liu and Wang (1991) analysed cAMP contents in mature fruits of 14 horticultural plants, 44 Chinese jujube cultivars, and

258 Table 5.5.

Nutritional constituents in pulp of dry mature fruit of 9 Chinese jujube cultivars.

Cultivar Jianzao Junzao Longzao Yazao Popozao Linglingzao Sanbianhongzao Jinsixiaozao Qingjianmuzao

Total sugars (%)

Reducing sugars (%)

Fructose (%)

Acidity (%)

Vit C (mg/ 100g)

Cellulose (%)

Pectin (%)

Lipid (%)

Protein (%)

Moisture (%)

Total ash (%)

CaO (μg/g)

P2O5 (μg/g)

Fe2O3 (μg/g)

72.1 67.3 70.4 67.1 53.3 70.3 70.2 68.6 67.6

66.2 48.1 46.9 50.0 50.6 48.4 55.2 48.4 62.5

34.7 17.5 14.3 15.3 18.4 16.5 19.2 15.8 25.5

1.35 1.34 1.74 1.75 2.03 1.29 1.56 1.15 1.38

14.4 15.8 17.7 14.1 18.6 14.7 14.5 16.9 9.3

4.45 4.78 6.26 5.96 10.30 5.65 4.56 5.13 5.75

1.28 0.88 0.89 1.21 2.09 0.42 0.47 1.92 0.61

0.33 0.58 0.56 0.85 0.79 0.36 0.53 0.31 0.92

4.04 5.27 5.56 5.69 6.84 4.56 5.41 5.47 5.45

14.77 18.03 16.59 17.42 18.81 11.76 18.47 15.95 13.39

2.04 2.46 2.33 2.31 2.98 2.58 2.10 1.90 1.53

210 862 521 576 491 475 455 373 456

683 930 1085 476 1095 664 878 676 441

53.8 65.1 99.7 56.8 62.1 93.0 63.3 39.4 26.9

Data from Wang et al. 2002.

Table 5.6.

Comparison of nutritional constituents between apple and different products of Chinese jujube.

Type Fresh mature jujube Dry mature jujube Candied jujube Fresh mature apple Data from Liu 2004.

Moisture (%)

Calorific value (Them/100g)

Protein (%)

Lipid (%)

Carbohydrate (%)

Cellulose (%)

Total ash (%)

CaO (mg/100g)

Vit C (mg/100g)

cAMP (nmol/g)

73.4 19.0 18.6 84.6

99 308 315 58

1.2 3.3 1.3 0.4

0.2 0.4 0.1 0.5

23.2 72.8 77.2 13.0

1.6 3.1 2.1 1.2

0.4 1.4 0.7 0.3

14 61 43 11

540 12

10–200 20–500

2–4

<0.01

259

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59 sour jujube genotypes. The highest content was 303 nmol/g FW (756 nmol/g DW), found in Chinese jujube cultivar ‘Muzao’, which was also the highest among higher plants. During storage for 24 days at 10°C and –24°C, the cAMP content in fresh mature Chinese jujube increased, while cGMP content decreased slightly (Liu et al. 1996). Dried fruit of jujube contains several volatile substances, which have significance in imparting the typical flavour to the fruit. Seventy-eight such kinds of compounds were identified. Aliphatic acids and carbonyl compounds accounted for 62.97% and 29.56% of the total volatiles, respectively (Wong et al. 1996). The major components were decanoic acid (20.0%) and dodecanoic acid (15.6%). Succinic and malic acids have also been identified (Ahmedov and Halmatov 1969). Ziziphus-pectin A has been isolated from the fruits of Chinese jujube. This pectin contains 2,3,6,tri-o-acetyl D-galactose units in the side chain (Tomoda et al. 1985). It binds bile acid, lowers plasma cholesterol, and has anti-diarrhoeal properties. Mature jujube fruits also contain polyphenols and rutin (Kriventsov and Karakhanova 1970). Isoquinoline alkaloids, isolated from the fruits of Chinese jujube, have been identified as steppharin, N-nor-nuciferine, and asimilokine (Khokhar 1978). A pyrrolidine alkaloid obtained from the dried fruits of Chinese jujube showed sedative activity in laboratory trials with mice (Han et al. 1987). Both the pericarp and the seeds of Chinese jujube ‘Ta-yan-tszao’ contained phospholipids of two main classes, phosphatidylcholines and phosphatidylglycerols. Oleic acid was present in the fatty oil of the seed. The neutral lipid of the pericarp was palmitoleic (Goncharova et al. 1990). 2. Seed. Chinese jujube seeds contain a number of medicinal saponins including jujubogenin and ebelin lactone (Shibata et al. 1970; Kawai et al. 1974; Ogihara et al. 1976). Jujubosides A and B have also been isolated from the seeds of Chinese jujube (Otsuka et al. 1978; Zhou et al. 1994). Tanaka and Sanada (1991) identified spinosin, swertisin, 6”’-feruloylspinosin, 6”’-sinapoylspinosin, 6”’-p-coumaroylspinosin, 2”-O-glucosylisowertisin, vicenin-2 and a flavonoid, apigenin 6-C-[(6O-p-hydroxybenzoyl) beta-D-glucopyranosyl (1 fwdarw 2)] beta-Dglucopyranoside from water extracts of seeds. These extracts possess a mild sedative activity and are used to treat insomnia. Goncharova et al. (1990) reported oleic acid in the fatty oil of the seeds of Chinese jujube ‘Ta-yan-tszao’ (Goncharova et al. 1990). The seeds showed a diversity of phospholipids with a lower proportion of saturated phospholipids.

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Woo et al. (1979, 1980) and Kuk et al. (1982) reported spinosin compounds such as 2”-O-β-glucosyl swertisin, 6”’-feruloylspinosin and 6”’sinapoylspinosin, 6”’-p-coumaroylspinosin in the seeds of sour jujube. The seeds of sour jujube used in Chinese medicine as a sedative also contain cyclic peptide alkaloids, sanjoinenine, franguploine and amphibineD, and four peptide alkaloids, sanjoinine-B,-D,-F and -G2 (Han et al. 1990). Matsuda et al. (1999) isolated protojujubosides A, B and B1 from seeds of sour jujube, of which protojujuboside A and jujubosides A, B and C exhibited potent immunological adjuvant activity. 3. Stem Bark. Stem bark of Chinese jujube contains a number of cyclopeptide alkaloids including mauritine-A mucronine-D, amphibine-H, nummularine-A and -B, jubanine-A and -B (Tschesche et al. 1976), sativanine-A and -B, frangulanine, nummularine-B, mucronine-D (Tschesche et al. 1979), sativanine-C (Shah et al. 1984a), sativanine-G (Shah et al. 1984b), sativanine-E (Shah et al. 1985c), sativanine-H (Shah et al. 1986b), sativanine-F (Shah et al. 1985a), sativanine-D (Shah et al. 1985b), and sativanine-K (Shah et al. 1987). Devi et al. (1987) identified β-sitosterol, betulinic acid, betulin, kaempferol, myrecetin and β-sitosterol glucoside and Tripathi et al. (1989) isolated nummularine-P, sativanine-H and rugosarnine-B from the stem bark. 4. Leaf and Root. The leaves of Chinese jujube contain a neolignan, which increases the release of endogenous prostaglandin I2 (Fukuyama et al. 1986). From fresh and dried leaves, a sweetness-inhibiting saponin, ziziphin, which has a structure, 3-O-α-L-rhamnopyranosyl (1.2)-α-Larabinopyranosyl-20-O- (2,3-di-O- acetyl-α-L-rhamnopyranosyl jujubogenin was extracted (Kurihara et al. 1988; Yoshikawa et al. 1991). This ziziphin inhibited the sweet taste receptor in humans but does not suppress taste sensations of saltiness, sourness, and bitterness (Kurihara et al. 1988). Ikram et al. (1981) isolated a saponin from Z. jujuba leaves and stems and assigned the structure 3-O-[(2-O-α-D-furopyranosyl-3-O-β-Dglucopyranosyl)-α-L-arabinopyranosyl] jujubogenin. Cyclopeptide alkaloids are also present in Z. jujuba leaves (Ziyaev et al. 1977; Chughtai et al. 1978). Ziyaev et al. (1977) isolated coclaurine, isoboldine, norisoboldine, asimilobine, insiphine, and insirine from jujube leaves. The leaves were found to contain 1,020 mg per 100 g vitamin C (Ahmedov and Halmatov 1969). Root bark of Ziziphus species is rich in alkaloids. Otsuka et al. (1974) reported coclaurine, a benzylisoquinoline in the root bark of Z. jujuba Mill.

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IV. ENVIRONMENTAL REQUIREMENTS A. Temperature Chinese jujube can grow well under various climatic conditions (Qu and Wang 1993) from sea level up to an elevation of 2000 m, at average temperatures of 5.5–28°C (see Table 5.7). Commercial plantations are found growing in areas having an average annual temperature of 8 to 22°C and occasionally reaching as low as 5.5°C for some special cultivars. The trees can tolerate winter temperatures as low as –30 to –38°C. In the USA, Chinese jujube has withstood temperatures of –22°C without injury (Thomas 1924) and has tolerated –30 in Azerbaijan (Troyan and Kruglyakov 1972). Tolerance to low temperatures depends greatly on cultivar and age of the tree. However, being covered by snow for a long period and alternation of freezing and melting may damage young trees. The 2002 cold winter in northern China resulted in considerable death of trees 1–3 years old of most cultivars, but a few cultivars did not show obvious injury, and most old trees survived and recovered the following spring. Fruit set of Chinese jujube requires average daily temperatures above 20°C. Fruit development requires average daily temperatures over 24–25°C (see Fig. 5.13). Maturation date is 2 weeks earlier in the warmer areas of Azerbaijan where summer temperatures rise to 36°C (Tagiev 1992). Chinese jujube trees shed leaves and enter dormancy after average daily temperatures fall below 15°C. In northern China, leaf senescence and leaf fall begins from late October, which is much earlier than common fruit trees. This appears to be an adaptive mechanism to escape damage through desiccation during cold weather.

Table 5.7. Natural climatic conditions of the production areas of Chinese jujube in China. Items Annual average temperature (°C) Average temperature of flower season (°C) Minimum temperature (°C) Frost-free period (d) Annual rainfall (mm) Annual sunshine (hr) Data from Qu and Wang 1993; Liu 2003, 2004.

Value 5.5–22 ≥22–24 ≥ –38.2°C ≥ 100 87–2000 ≥ 1100

5. CHINESE JUJUBE: BOTANY AND HORTICULTURE >7.2°C

22–25°C

O

Root

263

I

<21°C

R

D <15°C

13–15°C > 17°C Leaf

O

LF

R 18–19°C O

B-shoot

R

D

18–19°C O

E-shoot

>25°C R

D

>19°C 20°C 22°C B

Flower

E

F

L

>25°C 25–30°C C

Fruit March

April

May

June

R

18–25°C S

July

P

August

September

October

Fig. 5.13. Relationship between temperature and phenological phase of Ziziphus jujuba Mill. cv. Jinsixiaozao Hort. (from Yang and Liu 1990). B-shoot: bearing shoot; E-shoot: extension shoot; O: occurring; I: increasing; R: rapid growing; D: decreasing; LF: Leaf fall; B: bud stage; E: early bloom stage; F: full bloom stage; L: late bloom stage; C: rapid cell division; S: slow growing; P: pre-mature growing.

B. Water The vertical root system reaches a depth of 13 m (Ming and Sun 1986) and well-developed horizontal roots (Liu 2004) enable Chinese jujube to survive under extended moisture stress. Reduced loss of water through leaf transpiration makes it adaptable to arid microclimates. Drought-stressed Ziziphus trees control water loss by stomatal closure and even by reduction in leaf area, which results in a higher intrinsic water use efficiency and assimilation/leaf conductance ratio than in unstressed trees (Jones 1992). Chinese jujube can withstand extreme drought conditions (Lanham 1926; Locke 1948; Sin’ko 1971). It cannot only survive but also obtain reasonable yield under severe drought. Many famous cultivars of Chinese jujube are grown in northwest China, well known for its aridity, including arid areas with annual rainfall below 200 mm (see Table 5.8),

264 Table 5.8. China.

M. LIU Climatic conditions of the north border of distribution of Chinese jujube in

Latitude

Average

Minimum

Annual rainfall (mm)

41°33′ 40°49′ 38°06′ 39°23′ 44°10′

8.3 5.5 9.1 8.1 5.7

–31.1 –32.8 –28.0 –26.4 –38.2

474.2 437.2 219.8 87.4 203.2

Temperature (°C) District Chaoyang, Liaoning Huhehaote, Neimeng Lingwu, Ningxia Gaotai, Gansu Changji, Xinjiang

Sunshine duration (hr) 2893.9 2960.7 2894.4 3049.3 2828.0

Data from Qu and Wang 1993; Liu 2003, 2004.

semi-arid areas with 200 to 450 mm rainfall, and sub-humid areas with 450 to 650 mm rainfall (Ming and Sun 1986; Qu and Wang 1993). Fruit set and fruit expansion require higher atmospheric humidity and soil water. Higher fruit yields can be expected during higher rainfall years. On the other hand, overcast and rainy weather during ripening usually causes severe fruit-splitting and fruit diseases, and results in great loss. According to statistics of Liu et al. (1992) based on 30-year (1958–1987) records of Chinese jujube yield and rainfall in Fuping county of China, days of continual rain in September were inversely correlated with yield. C. Soils Chinese jujube can grow and set fruit well on a variety of soils ranging from shallow to deep, barren to fertile, gravelly and sandy to clay, and from alkaline to acidic. It can be cultivated on marginal lands unfit for growing other fruit crops. Many famous cultivars of Chinese jujube, including ‘Jinsixiaozao’, ‘Zanhuangdazao’, ‘Pozao’, ‘Muzao’, and ‘Huizao’, are grown in well-known drought areas such as the sandy old course of the Yellow River, the barren Taihang Mountain, and the alkaline zone around the Bohai Sea. However, for high yield and high-quality cultivation of Chinese jujube, well-drained, slightly acidic to slightly alkaline (pH 5.5–8.5) soils with the following additional characteristics are required: NaCl content less than 0.1%, total salt content below 0.3%, sandy or loamy texture, good depth (over 50 cm), and an ample quantity of organic matter (Liu 2002, 2004) (see Table 5.9).

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Table 5.9. Natural soil conditions of the production areas of Chinese jujube in China. Soil condition Depth (cm) pH NaCl (%) Na2CO3 (%) Na2SO4 (%)

Value ≥30 4.5–8.4 ≤0.15 ≤0.3 ≤0.5

Data from Qu and Wang 1993; Liu 2003, 2004.

D. Wind According to the investigations in ‘Fupingdazao’ of Liu and Geng (1992 and Liu et al. (1997), the resistance to wind is highest in the dormant period and the susceptibility to wind damage increases thereafter until fruit maturation; during the day, wind resistance was highest at noon and lowest at sunrise; among various organs, the order of wind-resistance from high to low was bearing shoot and leaf, young fruit, flower, mature fruit, and abortive flower and fruit; wind speed less than 6 m.s–1 was not harmful to any organs of Chinese jujube during the growing season. The wind-resistance of Chinese jujube also varied with cultivar, age, prunning, density of plantation, fruit capacity, and geographic environment. E. Light, Elevation, and Exposure Chinese jujube is a light-demanding plant. Liu et al. (1992) observed that better yield and fruit quality could be obtained at sites with elevation less than 400 m, and slope open to the south in the Taihang mountain area, north China. As elevation goes beyond 550 m in northern China, both yield and fruit quality decreased significantly and the stone of fruit did not develop normally. V. HORTICULTURE A. Crop Improvement 1. Genetic Diversity and Important Cultivars. Chinese jujube has very high diversity in distribution, climate and soil adaptation, chemical

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M. LIU

composition, morphological character, disease resistance, chromosome number, pollen characteristics, and genomic DNA (Liu 2003). Botanical Characteristics. During the long history of evolution, a great amount of differentiation occurred in Chinese jujube. Liu (2003) reported that the coefficient of variation in leaf length (39.4%) was much higher than for ratio of edible to inedible matter of fruit (only 2.7%) (see Table 5.10); high diversity was also found in fruit shape (round, flat round, oblong, columned, ovate, inverse ovate, olive like, red pepper like, etc.), fruit taste (very sweet, sweet, acid, sweet-acid, acidsweet, etc.), seed (plump, shriveled, seedless), stipular spine (strong, weak, absent), and open time of flower bud (morning, afternoon, night). There are some special variations that manifest in a single or very few cultivars, such as tortuous branch in ‘Longzao’, persistent calyx in ‘Shitizao’, purple flower and young fruit in ‘Tailihongzao’, tea-pot shape fruit in ‘Chahuzao’, calabash shape fruit in ‘Huluzao’ and stone-less in ‘Wuhexiaozao’ (Liu 2003). These cultivars are usually of ornamental or commercial importance. Nutrient Composition and Resistance. Chemical composition content (see Table 5.11), and disease and pest resistance depend greatly on cultivars. Reaction to witches’ broom disease varies from almost immune to highly sensitive; fruit splitting varies from less than 5% to over 95% (Liu 2003, Liu et al. 2003). Chromosome Number and Pollen. The diversity in chromosome number of Chinese jujube is low. Among the 117 cultivars investigated, one is triploid (Qu et al. 1986) and all the others are diploid. The pollen of Chinese jujube is flat-ball-like in equator (rarely ball-like) and obtuse triangle in polar. It has 3 (rarely 2, 4, or even more) germination holes. BasTable 5.10.

The variation of botanical characters of Chinese jujube.

Items Bearing branch (cm) Leaf length (cm) Flower diameter (mm) Fruit weight (g) Fruit edible rate (%) Fresh fruit/dry fruit (%) Fruit growth period (d) Data from Liu 2003.

Minimum

Maximum

Average

9.0 2.3 2.9 2.0 81.0 23.0 60.0

32.0 10.1 10.0 46.0 99.0 70.0 145.0

17.6 5.4 6.1 10.8 94.8 45.5 98.3

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Table 5.11. The variation of some nutrient components of dried Chinese jujube. Items Vc (mg/100g)* cAMP (nmol/g)* Soluble solid (%)* Sugar (%) Reducing sugar (%) Fructose (%) Cellulose (%) Pectic (%) Protein (%) Acidity (%) Ash content (%) Ca (μg/g) P (μg/g) Fe (μg/g)

Minimum

Maximum

Average

61.0 3.8 17.2 53.3 46.9 14.3 4.5 0.4 4.0 1.2 1.5 127.0 410.0 26.9

1174.0 302.5 45.0 72.1 66.2 34.7 10.3 2.2 6.8 2.0 3.0 862.0 1095.0 99.7

408.4 38.1 29.4 66.8 54.7 21.0 6.1 1.2 5.3 1.6 2.2 453.2 711.5 61.3

Data from Liu 2003. Note: *Fresh fruit.

ing on G.. Erdtman’s standard, the pollen of Chinese jujube is a medium to small type (18.98 × 22.10 μm ~ 20.22 × 26.39 μm). Some 70% of the cultivars tested have large pollen grains (2–3 times the size of common pollen), but the percentage of large grains varied among cultivars. Diversity within Cultivars. Most cultivars of Chinese jujube have a long history, and most show obvious morphological variations within the cultivar (Liu and Zhao 2003). RAPD analysis showed that most cultivars have more than one genotype. For example, at least 11 genotypes have been identified in ‘Zanhuangdazao’ (Zhao and Liu 2003). Important Cultivars. There are about 700 cultivars of Chinese jujube grown in China. These can be classified into five groups based on their major purpose, i.e., table, dried, candied, multipurpose, and ornamental (see Table 5.12). Isozyme, pollen, DNA characteristics, as well as fruit shape and size, have been employed in cultivar classification (Liu 1999). ‘Jinsxiaozao’, ‘Pozao’ (‘Fupingdazao’), ‘Yuanlingzao’, ‘Changhongzao’, ‘Muzao’, ‘Bianhesuan’, ‘Zanhuangdazao’, and ‘Huizao’ are the leading cultivars in China (see Table 5.13). Each is concentrated in several to a dozen counties, with production of 20,000 to 200,000 t of fresh fruit per year. These cultivars account for at least 60% of the total production in China. Cultivars for dry fruit are traditionally dominant, but fresh-fruit

268

M. LIU Table 5.12. in China.

Diversity in the utilization of Chinese jujube cultivars

Cultivar type

No. cultivars

Relative production (%)

Distribution

224 261 56 159 ~10

~80 <5 5–8 ~10 <1

North North & South South North & South North

Dry Fresh Candied Multi-purpose Ornamental

data from Qu and Wang 1993; Liu 2003.

Table 5.13.

The leading cultivars of Chinese jujube.

Cultivar Jinsxiaozao Pozao (Fupingdazao) Changhongzao Yuanlingzao Muzao Bianhesuanzao Zanhuangdazao Huizao

Purpose

Producing area

Dry Dry Dry Dry Dry Dry Multi-purpose Multi-purpose

Hebei, Shandong Hebei Shandong Shandong Shanxi, Shannxi Henan Hebei Henan

cultivars are becoming more and more important. The recommended cultivars are listed in Tables 5.14–5.17. 2. Selection. Because cross breeding is very difficult in Chinese jujube, most crop improvement work, up to now, has been focused on local selections (Kim et al. 1981; Liu and Wang 1991; Zhu et al. 1998). In view of the wide variation within traditional leading cultivars, selection within cultivars is still very active (Krestnikov 1981; Massover and Buryakov 1982; Luo et al. 1997). Newly released cultivars from local selection include ‘Wolchul’ (Kim et al. 1988), ‘Sihongdazao’ (Wan 1994), ‘Daguazao’ (Wang et al. 1999), ‘Tianshuiyuanzao’ (Yang et al. 1999), and ‘Dabailing’ (Gao et al. 2002). New cultivars from within-cultivar selection include ‘Jinsixin 4’ (Guo 1999) and ‘Yuanling 1’ (Wang et al. 2001). 3. Hybridization. Chinese jujube has very small flower buds (3 mm in diameter) and it is hard to emasculate the flowers without damaging

Table 5.14.

Recommended fresh fruit cultivars.

Shape

Weight (g)

Edible rate (%)

Quality

Yield

Dongzao Linyilizao

Apple-like Obovate

10.7 30.0

96.9 97.3

E G

G E

Chengwudongzao Dabailing

Oblong Elliptic

25.8 25.6

97.8 95.0

G G

Binxiansuzao Dachengpingguozao Hamazao Xiangfenyuanzao

Ovate Apple-like Oblong Ovate

12–13 23.3 34.0 15.4

96.2 95.8 96.5

E G G E

Cultivar

E = Excellent; G = Good; M = Middle.

Harvest period

Storability

Fruit split

Oct. 1–20, Sept. 20–30

E M

Very low High

M G

Oct. 1–20 Sept. 1–20

M

Low Low

G G M G

Oct. 1–10 Late Aug. Mid–Late Sept. Early Oct.

Remarks Best quality Bearing early & very productive Bearing early & very productive

High Fruit very beautiful E E

High Low

269

270 Table 5.15.

Recommended dry cultivars.

Cultivar

Shape

Weight (g)

Edible portion (%)

Dry/Fresh (%)

Qualityz

Yield

Harvest period

Storability

Fruit split

Jinsixiaozaoy

Oblong

5.0

95–97

55–58

E

G

Late Sept.

E

Middle

Yuanlingzao

Round

12.5

97.0

60–62

G

G

Mid Sept.

E

Very low

Xiangzao

Apple-like

22.9

97.6

53

G

M

Late Sept.

E

Very low

Huizao

Long ovate

12.3

97.3

50

G

G

Mid Sept.

E

High

Pozao

Obovate

11.5

95.4

53

G

G

Early Oct.

M

High

Jixinzao

Elliptic

4.9

92.0

50

G

G

Late Sept.

E

Low

96.5

G

M

Mid–Late Sept.

E

High

E

G

Early Oct.

E

Low

Hamazao

Oblong

34.0

Xiangfenyuanzao

Ovate

15.4

z

E = Excellent; G = Good; M = Middle. Adapted to alkaline soil.

y

Table 5.16.

Recommended multi-purpose cultivars.

Shape

Weight (g)

Edible portion (%)

Dry/Fresh (%)

Qualityz

Yield

Round or Cylindric

17.5

96.0

48

E

E

E

G

Mid–Late Sept.

Very high

E

G

Early Oct.

Middle High

Cultivar Zanhuangdazaoy

Harvest period Late Sept.

Fruit split High

Junzao

Obovate

22.9

96.3

Jinzao

Long ovate

21.6

97.8

40

Banzao

Obovate

11.2

96.3

57

E

G

Mid–Late Sept.

Mingshandazao

Cylindric

23.9

95.4

52

G

G

Early Sept.

Tongbaidazao

Round

30.0

97.2

G

E

Early–Mid Sept.

High

Hunanjidanzao

Ovate

19.4

94–96

G

E

Mid Aug.

Low

Sihongdazao

Elliptic

G

G

Mid–Late Sept.

Low

z

E = Excellent; G = Good; M = Middle. Triploid.

y

30–50

271

272 Table 5.17.

Recommended candied cultivars and ornamental cultivars.

Cultivar

Shape

Weight (g)

Edible portion (%)

Qualityz

Yield

Harvest period

Fruit split

Remarks

Xuanchengjianzao

Ovate

22.5

97.0

E

G

Late Aug.

Low

Candied cultivar

Fanchangchangzao

Cylindric

14.3

98.3

G

E

Early Aug.

Very low

Candied cultivar

Chunandazao

Cylindric

18.0

96.8

E

G

Early Sept.

Low

Candied cultivar

Guanyangchangzao

Cylindric

14.3

96.9

E

G

Early Aug.

Low

Candied cultivar

Dalilongzao

Elliptic

10.3

96.2

M

G

Early–Mid Sept.

Sanbianhong

Oblong

18.5

95.6

G

G

Mid Sept.

Middle

Fruit color

z

E = Excellent; G = Good; M = Middle.

Dwarf, winding branch

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them. In addition, most excellent cultivars that might serve as parents have serious embryo abortion. Thus, crossing in Chinese jujube is extremely difficult. In 2002 and 2004, seven jujube researchers and graduate students, including the author, took two weeks to cross 2000 flowers and obtained only 10 fruit, all of which had no well-developed embryos and dropped prior to maturity (unpublished data). Up to now, no cultivars have been bred through controlled crossing. To successfully cross in Chinese jujube, the two obstacles, emasculation and embryo abortion, must be overcome. Embryo Abortion and Embryo Culture. Embryo abortion rates vary widely among cultivars. Within one tree, large fruits show less embryo abortion than small fruits. Qi (2002) and Qi and Liu (2004) studied the mechanism of embryo abortion and embryo culture of ‘Dongzao’, ‘Jisifeng’, ‘Wudeng’, and ‘Fuzao’, Chinese jujube with middle to high embryo abortion. An optimized two-step culture model was established, i.e., initially cultured in germination medium: MS + BA 0.1~0.5 mg/L + IBA 0.5~1.0 mg/L + NAA 0.1 mg/L + sucrose 50 g/L + agar 7 g/L + LH (lactalbumin hydrolysate) 500 mg/L, then transferred to growing medium: MS + sucrose 30g/L + agar 5g/L. There are three strategies for obtaining plants using embryo culture: direct development from immature embryos, callus formation from younger immature embryos, and keeping on with embryo development from very young embryos (less than 30 days old). Many factors are involved in embryo culture (Qi and Liu 2004). The quality and age of the embryos are key factors. The survival rate of 55-day embryos is 87–90% and that of 20-day embryos is only 3.7%. Low levels of BA, high levels of IBA, and the proper quantity of LH favor germination and plantlet induction from embryoid and adventious buds. Low temperature treatment (2–4°C, 44 days) favors plantlet formation from poor-quality plantlets. Seven- to ten-day dark treatment favors rooting of embryos. Practices that improve embryo culture include selecting earlier set fruit with normal embryos, adopting a two-step-culture method, and cutting the tip of the main root to stimulate lateral root formation. Embryo abortion of Chinese jujube is related to hormones and nutrients (Qi 2002; Wang 2004). Qi (2002) observed that the flesh of seedless cultivars contains higher GA3 and IAA levels than cultivars with seeds, and within high embryo abortion cultivars, the flesh of seedless fruits contain higher GA3 and IAA levels than the flesh of fruit with seed. Wang (2004) indicated that high levels of hormones and nutrients in the flesh probably lead to low nutrient levels in the ovules, which consequently causes embryo abortion at the stone hardening stage. The high

274

M. LIU

zeatin (Z) content and ratios of Z/GA probably caused seeds to shrink at the late stages of embryo development. Male Sterility. Wang (2004) studied variation in male sterility among cultivars and its cytological, physiological, and biochemical mechanisms. Pollen fertility varies significantly with cultivar. Based on pollen fertility estimated by I2 – IK (iodine – potassium iodide) staining, cultivars were divided into 5 groups, i.e., high fertility (VPR, i.e., viable pollen rate ≥ 54%), medium-high fertility (43% ≤ VPR < 54%), medium fertility (28% ≤ VPR < 43%), medium sterility (17% ≤ VPR < 28%), and high male sterility (VPR < 17%). Two types of male sterility have been found in Chinese jujube (Wang 2004), i.e., functional pollen sterility and empty anther sacs. Anthers of the first type contain highly sterile pollen (e.g., ‘Dongzao’) with pollen germination less than 3%, and anthers of the second type become empty at the yellow bud stage (e.g., male sterile No1 and male sterile No2). Hormones, nutrients, and enzymes in flower buds were significantly different among cultivars with different pollen fertility (Wang 2004). High levels of ethylene and GA and Z at low levels during the earlier stages of single flower opening were related to low pollen germination in ‘Dongzao’. Marker-Assisted Cross Breeding. Along with conventional cross breeding aided by embryo rescue, marker-assisted cross breeding has been carried out in the author’s institute. Two parent cultivars are planted or moved together or grafted in the same tree. These are covered with a white net to keep away outside pollinators. A box of honeybees is placed inside the net and they act as pollinators. Molecular markers such as RAPDs and AFLPs are used to identify whether the seeds obtained are from hybridization or self-pollination. This method has increased crossing efficiency considerably. 4. Ploidy Manipulation. Some of the leading cultivars have obvious faults. For instance, the leading dry cultivar ‘Jinsixiaozao’ has small fruit, and the two top leading fresh cultivars, ‘Dongzao’ and ‘Linyilizao’, have weak tolerance to cold and disease. In view of the difficulties of cross breeding, polyploid breeding is regarded as a possible fast way to breed for large fruit and high resistance. Jiang (2003) treated shoot tips in the field with colchicine and produced tetroploids from three famous Chinese jujube cultivars ‘Dongzao’ (0.15%/18hr), “Linyilizao’ (0.1%/30hr), and ‘Lajiaozao’ (0.15%/18hr). Under the best treatment combinations, ‘Linyilizao’, ‘Dongzao’, and

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‘Lajiaozao’ showed induction rates of 50%, 43.3%, and 43.3%, respectively. Jiang (2003) also observed cells with chromosome number of 2n = 26 and 48 in inducted tissue (normal diploid number is 2n = 24). Plant parts with induced tetroploidy showed double chromosome number (2n = 48), larger cells, larger and longer guard cells, more chloroplasts in the guard cells, and lower density of the stomata. Pollen grains were larger, rounder, more often deformed, and more frequently had 4 germination pores. Leaves were rounder and thicker, flower buds were larger and rounder, and internodes were shorter. There were fewer lenticels per unit area on the shoot (Jiang 2003). Wang (2004) obtained two tetraploid plants of sour jujube and one tetraploid plant of Chinese jujube ‘Dongzao’ by treating shoot segments and cluster buds with colchicine under tissue culture conditions. For cluster buds, the optimum concentrations and treatment periods of colchicine for sour jujube and ‘Dongzao’ were MS medium plus 50 mg/L colchicine for 40 days, with doubling rates of 36.7% and 26.3%, respectively. Pre-culture for 4 days, dark treatment for 15 days, and adding 0.5% DMSO and 1.5 mg/L activated carbon to the medium can improve the doubling effect. Tetraploid plants produced in vitro showed similar changes to those induced in the field, but the leaf index and internode length became smaller at the beginning of induction and recovered to normal (Jiang 2003; Wang 2004). Cells in different layers of the tetraploid shoots were significantly larger than those of the diploids. Diploid and tetraploid chimeras can be separated in vitro by continuously transplanting aided by appearance and ploidy inspection. The tetraploid parts can be efficiently purified after 3 or 4 times (at most 8 times) of transplanting. Wang et al. (1998) reported anther culture in vitro. The ploidy levels of plants derived from the same callus tissue varied from n to 4n. 5. Biotechnology and Mutation. Gene transformation has not been carried out in Chinese jujube, but some relevant research has been accomplished. Zhou (2004) studied the factors affecting in vitro regeneration of adventitious shoots from leaves of Chinese jujube ‘Dongzao’ and ‘Lajiaozao’, and established a highly efficient regeneration system. The suitable medium for ‘Dongzao’ was MS + TDZ 1.0mg/L + IBA 1.0~0.5mg/L (pH 5.8~6.4) during the first 4 weeks followed by medium with no CTK (MS + IBA 0.1mg/L + GA3 0.05mg/L). The regeneration rate was 91.3%. For ‘Lajiaozao’, the suitable medium was WPM + TDZ 0.5mg/L + IBA 0.1mg/L (pH 5.8~6.4) and MS + IBA 0.1mg/L + GA3 0.05mg/L, respectively, with a regeneration rate of 78.9%.

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Leaves of 30 to 40 days from tube-plants subcultured more than six times were suitable for regeneration. Dark treatment for 14 days increased the regeneration rate. Supplementation of 0.1 mg/L AgNO3 to the medium was also beneficial (Zhou 2004). Adding kanamycin to the medium influenced leaf regeneration and shoot growth. For ‘Dongzao’, the critical concentration for leaf generation was 50 mg/L, and for shoot growth was 100 mg/L (Zhou 2004). Sin’ko and Chemarin (1979, 1982) tried gamma radiation in Chinese jujube breeding and revealed the effect of irradiation on the growth and development of seedlings. Some mutants were obtained (Sin’ko and Karakhanova 1982). B. Propagation Vegetative propagation of improved or selected cultivars is important to make Chinese jujube cultivation economically viable. Softwood cuttings, grafting, and root offshoot reproduction are quite common and successful (Tarasenko and Shaumarov 1977; Kim et al. 1982; Dong and Song 1988; Shen et al. 1992). Propagation by tissue culture has also been tried with success. The recent trend in propagation of Chinese jujube is using grafting (Liu 2004). 1. Grafting Rootstocks. The rootstocks used in northern China include Chinese jujube and its direct ancestor, sour jujube (Z. acidojujuba). Paliurus hemsleyanus Rehd. may be used as well in southern China. Among the three, sour jujube is most commonly used. Both fully matured stones and kernels can be used to grow plants from seed. The stones must be stratified in moist sand for 3–4 months at 2–5°C before sowing. The kernels (removed from the stones) need to be soaked in water for 24–48 hr. Use of kernels is becoming increasingly popular because germination is early and even and growth is rapid. Treated seeds are sown at a distance of 10–15 cm in rows and 40–50 cm apart during early spring. In general, 75–150 kg of stones or 20–30 kg of kernels are needed per hectare. Seedbeds are covered with plastic film to promote germination. Grafting. After 1 year, the suitably sized seedlings are used for grafting. Among the various grafting methods, cleft grafting is preferred. The 5–6 weeks around bud sprouting is the best grafting time. Scions from 1- to 2-year old extension shoots have been shown to be very successful. Those from secondary shoots seldom develop new shoots in the current

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year of grafting except in a few cultivars such as ‘Liyilizao’. To prevent water loss, scions should be dipped briefly in 100–110°C paraffin. 2. Tissue Culture Reproduction. Several tissue culture systems have been published, which vary among cultivars and explants (Lee et al. 1986; Kim and Lee 1988; Ooishi and Yazaki 1990; Mitrofanova et al. 1994; Du et al. 1997; Chai et al. 1998). A relatively common system is described below (Dai 2003). Explant Selection. Stem tips and stem segments are suitable explants. Shoots from water-cultured branches during winter are best. Sterilization of Explants. The optimum methods for sterilization of explants vary with season, i.e., 70% C2H5OH + 0.1% HgCl2 for 6 min during the dormant period, 70% C2H5OH + 0.1% HgCl2 for 8 min during the initial growth period, two-step sterilization (0.1% HgCl2 for 4 min + 4 min) in the growth period. Tissue Culture System. The best basic medium is MS with sucrose 3%, agar 0.4% (pH 5.8). Culture conditions include light period 16hr/8hr, light intensity 2500Lx, temperature 25 – 28°C and air humidity 40% – 60%. The optimum initial medium is MS + 6-BA 1.0mg/L + NAA 0.1mg/L. The optimum proliferating medium is MS + 6-BA 2.0mg/L or MS + 6-BA 3.0mg/L. The optimum rooting medium is 1/2 MS + IBA 0.5mg/L. To increase the survival rate of seedlings, transitional soil, temperature, humidity, and light intensity are important. 3. Seedling Standard. Generally, 2 year old seedlings (1 year after grafting) are used for commercial plantation. The seedlings to be planted should be at least 80cm high and 0.8cm in ground diameter. The national seedling standard of China for Chinese jujube is listed in Table 5.18. The qualified seedlings should be dug out after leaf fall, or before bud bursting. Those Table 5.18. Specialized standard of the People’s Republic of China (ZBB64008-89)— Chinese jujube (Grading standard of seedling). Height (m)

Ground diameter (cm)

1

1.2–1.15

>1.5

2

1.0–1.2

>1.0

Grades

Root system At least 6 lateral roots over 2 mm in diameter and 20cm in lenth At least 6 lateral roots over 2 mm in diameter and 15cm in lenth

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that cannot be transported away or planted in time should be temporarily planted and watered sufficiently. C. Field Cultivation 1. Orchard Establishment Selection of Orchard Site. Chinese jujube can grow and fruit on a wide variety of soils and climatic conditions. However, high yield and high quality require plenty of sunshine, annual average temperatures over 8°C, and well-drained, approximately neutral, sandy or loamy soils with good depth and rich organic matter (Liu 2002, 2004). Because the storability of fresh fruit of Chinese jujube is very poor, table cultivars should be grown near cities. Good conditions of irrigation, storage, and transportation are needed for table fruit production (Chen et al. 1986). To prevent witches’ broom, a destructive phytoplasma disease, establishment of Chinese jujube orchards near pine and cypress forests should be avoided (Zhou et al. 1998; Liu 2002). Before planting, sloping fields should be terraced and excessively barren, acidic, and salty fields must be improved for commercial cultivation (Wang et al. 1992; Liu 2002). Density and Planting Patterns. There are three kinds of practical orchard patterns for commercial cultivation of Chinese jujube: (1) the traditional common orchards, 4–5 m × 5–6 m; (2) high-density orchards, 0.5–3 m × 1–4 m (Tian et al. 1983; Xie and Xie 1991; Zhang et al. 1998); (3) intercropping (Liu 2002). As tree size of Chinese jujube is quite easy to control, intensive planting is becoming increasingly popular in China. Density is usually 2–3 m × 3–4 m in common plantings, 1 m × 2 m in planned intensive plantings, and 0.5–0.7 m × 1 m in super-intensive plantings and protected plantings in greenhouses (Liu 2002). Chinese jujube is very suitable for long-term intercropping because it has relatively sparse roots and leaves that expand late and fall early (Kumar 1987; Yang and Liu 1990; Liu and Wang 1992; Liu 2002) (see Fig. 5.14). Its major phenological phases seldom coincide with those of the principal cereal and oil crops such as wheat, maize, peanut, and beans (Yang and Liu 1990). The yield of cereal/oil crop under this kind of intercropping is almost the same as that without Chinese jujube, sometimes even higher. Intercropping Chinese jujube and cereal/oil crops can produce both good economical, ecological, and social profits, and has been considered to be a model of agroforesty management all over China (Liu 2002). There are two major intercropping types: (1) the trees are planted

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----------------------+++++++++++---------------

Peanut

-----------------+++++++++------------Sesame Summer corn --------------+++++++++--------------Summer cereal -------+++++++--------+++++++--------------++++++++++---------Soyabean -------------Wheat -------------+++++++++++-----------------+++++++++++++--------------------------J-root -----------------------------------------J-shoot /leaf ---------------++++++++++---------------------J-flower ----+++++-----J-fruit -------++++++++--------------++++++++-----March

April

May

June

July

August

September October

Fig. 5.14. Comparison of peak time of fertilizer demand between Chinese jujube and some kinds of crops (from Yang and Liu 1990). J = Chinese jujube; +++ = fertilizer demanding period; ----: non-fertilizer demanding period

7–10 m in a row and 3–4 m apart, with wheat, peanut, beans, fodder, and medicinal crops as the intercrop fillers; (2) popular in plain areas, Chinese jujube spaced 3–4 m × 15–20 m are intercropped with cereal or oil crops. Planting. Prior to planting, pits of 0.6–1 m × 0.6–1 m × 0.6–1 m are dug at proper distances (Liu 2002). The pits are filled with original soil mixed with 50 kg of farmyard manure, and some superphosphate and urea. Transplanting to the field in April (around bud bursting) is most favorable for maximum success. In windy and droughty regions, the plants should be headed back after planting to a height around 30 cm above ground to reduce water evaporation and increase survival rate. It is better to plant local cultivars or to use local cultivars or sour jujube as rootstock for in-situ grafting with improved cultivars. This favors better growth and adaptation to environmental conditions than transplanting the grafted plants to the field. 2. Training and Pruning Training. Training is done during the first 2–5 years of tree growth (Liu 2002). The traditional forms of Chinese jujube trees include central leader and open center or modified central leader systems. With the introduction of the intensive planting systems, several new systems of training trees, such as cordon, dwarf pyramid, pillar, espailer, hedgerow, and spindle have been tested with success (Zhang et al. 1998; Liu 2004). In general, about 6 to 8 primary branches are kept within a height

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of 3–5 m, well spaced in all directions. The proper headed height for the central leader is usually 60 to 100 cm but varies with planting density, intercropping pattern, training form, and soil. To obtain the desired sprouting of lateral main buds, the secondary shoots beneath the heading cut must be removed because the lateral main bud does not sprout new shoots without strong stimulation. This is the so-called “one scissors stop, two scissors sprout” in Chinese jujube. In order to develop a good framework of the tree, the fruit are usually removed during the first 2 years. Pruning. Chinese jujube is light demanding. Pruning affects vigor, productivity, fruit quality, and susceptibility to diseases and pests (Liu 2002). Even after proper training, regular annual pruning is necessary. The yearly pruning of bearing trees is important to enable the tree to bear a full crop during subsequent bearing periods. Improper pruning leads to hormonal and nutritional imbalances and may reduce the yield of subsequent crops. Pruning can be done in both dormant and growing seasons. Summer pruning has been proven very effective and applicable to trees from young to adult. Dormant-season pruning should be done late winter or early spring to protect plants from winter injury. Dormant pruning is done mainly to remove shoots that are incapable of producing fruit of satisfactory size and quality, including weak, diseased, pest-damaged, and crowded shoots; heading back of old branches, drooping branches, excessively long branches and high-leaders is also done. After dormant pruning, the number of buds on current year shoots should be one eighth to one sixth of the total, and the number of mother bearing branches should be around 120/m3. Summer pruning includes removing useless or crowded sprouted buds and new shoots, and diseased and pest-damaged shoots; it includes heading back the current-year shoots that are expected to set fruits and changing the direction of branches so that they receive more sunshine and space. Summer pruning is also used to reduce plant vigor, which improves fruit set (Wang and Huang 1982). 3. Water, Soil and Fertilizer Management Soil Management. Soil management of a Chinese jujube orchard includes improvement of acidic, alkaline, salty, and sandy soils, building and fixing terraces and fish-scale pits, removing useless root offshoots, deep digging of the soil, tillage, and weeding. Deep digging of the soil is important to expand the growing space of the root system. It is usually carried out after harvest, together with the application of base manuring. In stony

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land with only a thin soil layer, deep digging can be done with the aid of explosives made from ammonium nitrate (Wang et al. 1992). Manuring, Fertilization, and Irrigation. Chinese jujube has strong tolerance to drought. However, proper irrigation in severe drought years can improve fruit set, reduce fruit drop, and markedly improve fruit size, yield, and quality. In general, irrigation is done together with fertilizing for mutual benefits. The key times of irrigation and fertilizing are immediately after fruit harvest (October), before bud break (April), early in the flowering season (June), and during the rapid growth stage of young fruit (July). Farmyard manure should be applied during the dormant period (late autumn or early spring). It was estimated that 1.5kg N2, 1.0kg P2O5, and 1.3kg K2O are needed to obtain 100 kg of high-quality fresh fruits. The water management of non-irrigated orchards includes mulching, tilling, weeding, establishing a water cellar, and repairing water and soil conservation engineerings such as fish-scale pits and terraces. Fertilization in non-irrigated orchards can be carried out through manuring, together with deep digging of the soil in late autumn, fertilizing during or after rain, planting green manure, mulching, weeding, etc. Storing fertilizer and water in the holes surrounding the tree is successfully practiced (Wang et al. 1999; Liu 2004). Crop straw or weeds that have high water holding capacity are used to make bundles 35 cm in diameter and 50 cm in length after harvest. Four to six such bundles, each mixed with 100–150 g urea and 100–150 g KH2PO3, are buried along the outline of the tree’s vertical shadow where there are abundant absorbing roots. Snow is piled up on them in winter. After the snow melts, the bundles are covered with 1 m2 plastic film. By this method, the effects of water and fertilizer can be maintained from June to July. Another proved and practical way of fertilizing is to rest sheep flocks in the montane orchard of Chinese jujube at least three nights and mix their excrement and urine with the soil (Liu 2004). The beneficial effects can continue 2–3 years. Foliar spraying is an efficient way to fertilize Chinese jujube. Fertilizer can be applied 5–6 times a year along with sprays of fungicides, pesticides, and growth regulators. In general, sprays of urea (0.3–0.5%) are carried out from leaf expansion to the early period of fruit development, and sprays of 0.1–0.3% KH2PO3 or superphosphate are made in the middle and late stages of fruit development. 4. Techniques for Improving Fruit Set. Chinese jujube trees usually flower abundantly, but fruit set is low, usually less than 1% under natural conditions. It is very important to improve the fruit set in Chinese jujube production.

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Adjusting the Distribution of Photosynthates. Trunk girdling is commonly practiced in strong trees and in orchards that are on fertile soils. It is usually carried out during full-bloom. The stronger the tree, the earlier the girdling is done. The first girdle is made 20–30 cm above ground, with subsequent girdles moving up 3–5 cm every year. The correct width of girdling is such that the opened area can heal within 30 days (usually being 3–8 mm wide). If healing does not occur fast enough, the girdled place should be covered with plastic film to speed healing. During the growing season, heading back the shoots that are not used as extension leaders and have space to branch can significantly increase fruit set and quality. The method is to remove the shoot tip when it has more than 3–4 secondary branches. Creating Appropriate Pollination Conditions. Better fruit set and fruit evenness are improved by keeping bees in the orchard during flowering. High-quality honey can also be obtained. Jujube pollen does not germinate normally when the relative humidity is below 60%. Continuously high temperatures and drought cause severe flower drop. So, spraying water is very helpful in such conditions. Spraying Growth Regulators and Rare Elements. Progress has been made in regulating fruit setting and preventing pre-harvest fruit drop. Fruit set of Chinese jujube can be improved significantly by spraying 10–20 ppm GA3 3–4 times starting at full-bloom at an interval of 5–6 days, or by twice spraying 0.2% borate during full-bloom and the rapid growth period of young fruit, respectively (Wang 1992; Meng et al. 1993; Liu 2004). Fruit set of 10.4–12.2% and seed set of 22.1–28.8% were obtained by pollination in the morning after anthesis, followed by application of boric acid at 100 or 200 ppm in the afternoon (Yun et al. 1995). However, pollination in the evening immediately after anthesis followed by application of boric acid at 200 ppm together with 1 ppm NAA gave a fruit set of only 2% and seed set of 11.8%. On the other hand, pre-harvest fruit drop can be prevented by application of 10–20 ppm NAA before the expected fruit drop or 4 weeks before harvest (Yang and Liu 1990). D. Pests and Diseases Some 86 pests and 10 diseases have been reported to be harmful to Chinese jujube (Qu and Wang 1993) (see Tables 5.19 and 5.20). 1. Pests. Of the pests, the peach fruit moth is the most common and serious. The adult fly makes a hole and lays eggs inside the immature fruits.

5. CHINESE JUJUBE: BOTANY AND HORTICULTURE Table 5.19.

283

The major diseases of Chinese jujube.

Pathogeny

English name

Chinese name

Typical symptom

Phytoplasma

Witches’ broom

Zaofengbing

Shoot: witches’ broom; Flower: metamorphosis; Tree: dies early

Alternaria tenuis, A. alternata,

Fruitshrink/ brown cortex

Zaosuoguobing/ Zaotiepibing

Unconfirmed physiological disease

Fruit split

Zaolieguobing

Fruit: split, rot, early drop

Phakopsora zizyphivulgaris (P. Henn.) Diet.

Rust

Zaoxiubing

Leaf: rusty, drops early

Colletotrichum gloeosporides Penz.

Anthracnose

Zaotanzubing

Fruit rot, drop early

Phytophthora citricola

Phytophthora rot

Phoma destructive Fusicoccum sp.

Fruit rot, drop early

Data from Qu and Wang 1993; Jee et al. 1998; Liu 2004.

After hatching, the maggots feed on the pulp around the stone. The adults emerge from the fruit and fall to the ground. Infected fruits subsequently drop, causing huge losses. This pest can be controlled by spraying pesticide at the proper time. The fallen infected fruits should be gathered and destroyed. 2. Diseases. Among diseases, jujube witches’ broom (JWB) is the most serious and widely distributed in China, South Korea, Japan, and India (Pandey et al. 1976; Wang et al. 1981; Zhou et al. 1998). Trees die 1–5 years after infection (Zhou et al 1998). The pathogen has been identified as a phytoplasma, formerly called a mycoplasma-like organism (MLO) (Yi and La 1973; Nakamura et al. 1977). The pathogen can be detected by fluorescence microscopic diagnosis, electron microscope, and polymerase chain reaction (PCR) using phytoplasma ribosomal (16Sr) general and specific primer pairs (Xu 1980; Zhu et al. 1988; Bak et al. 1991; Qiu et al. 1998; Wang et al. 1999; Tian et al. 2000; Zhao 2003). It is proposed that CLY (cherry lethal yellows disease) and JWB phytoplasmas represent a new taxon distinct at the rank of subspecies from other members of the 16S rRNA group V (Zhu et al. 1998). The pathogen exists and propagates inside the xylem causing witches’ broom and metamorphosis of flowers (La and Lee 1984; Shi et al. 1984; Zhou et al.

284 Table 5.20.

M. LIU The major pests of Chinese jujube.

Scientific name

English name

Chinese name

Typical symptom

Carpasina niponensis Wals.

Peach fruit moth

Taoxiaoshixinchong

Eating pulp around stone, causing fruit drop

Chihuo zao Yang

Jujube looper

Zaochhihu

Eating opened bud and young leaves

Ancylis sativa Liu

Armyworm

Zaonianchong

Sticking/eating leaf and fruit

Cnidocampa flavescens Walkor.

Huangciee

Eating leaves

Zeuzera sp.

Zaobaoduee

Eating the pith of stem or shoot

Ceroplastes japonicus Gr.

Zaoguilajie

Sucking sap from shoot and leaf

Lygus pratensis Linn.

Mucaochunxiang

Causing irregular holes in leaf and falling

Scythropus y asumatsu Kone et Mor.

Zaoshiyaxiangjia

Eating opened bud and young leaf

Contarinia sp.

Zaiyingwen

Causing wither of young leaf

1998). JWB is transmitted mainly by grafting and by insect vectors such as Hishimonides chinensis Anufriev (Wang et al. 1981; Chen et al. 1984; Zhou et al. 1998). The disease can be controlled temporarily by trunk girdling after bud break through obstructing the transportation of pathogen from root to canopy (Feng, J.H. and H. C. Xue 1989), timely removal of infected branches, gravity flow trunk injection of oxytetracycline and other antibiotics (La et al. 1976; Yong 1976; Wang et al. 1980; Yun et al. 1990; Yeo et al. 1991) as well as by reconstructing the canopy by grafting new cultivars with extremely high resistance to the disease (Liu 2004, unpublished data). Resistance to JWB varies greatly among cultivars (Yun et al. 1990; Liu et al. 2003). Jujube fruit shrink or Chinese jujube brown cortex, which shrinks the head, middle, or base of the fruit, is another destructive disease of Chinese jujube. It often reduces yield by 50–60%, sometimes over 90%, and results in poor-quality, bitter fruits. The causal organism is not yet fully understood. Zheng et al. (1998) isolated and identified the pathogen as Alternaria tenuis (A. alternata) and observed jujube fruits being infected throughout the growing period. Kang et al. (1998) identified

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three fungi (Alternaria alternata, Phoma destructiva, and Fusicoccum sp.) that could infect the Chinese jujube fruit individually or in combination. Up to now, no reliable control methods have been established. Fruit split, beginning at the white-ripe stage, is one of the main problems in Chinese jujube production. Susceptibility to fruit split is related to the direction and degree of slope in the field, cultivar, fruit maturity, epidermis characteristics, and rainfall during fruit ripening (Gao et al. 1998; Liu 2004). The extent of split is greater on the south slope of a hill compared to the north slope, and greater on flat, wet ground than on sloping sandy ground; resistance to split differs significantly among cultivars, being greater in dry cultivars than in fresh ones and greater in latematuring than in medium-maturing ones. The thicker the cuticle of the fruit, the stronger the resistance. The size, shape, sugar content, and thickness of the cuticle do not show obvious correlations with split resistance. Li and Gao (1990) observed that susceptibility to split increased with maturity. This appears to be due to accumulation of soluble sugar. Cultivar ‘Hupingzao’ was more susceptible than ‘Heiyezao’ and ‘Langzao’. Elasticity and plasticity of the flesh were the main factors affecting cultivar susceptibility. Adequate control of fruit split still has a long way to go. Anthracnose is becoming more and more serious in some places. Mu (1999) reported that constant cleaning of the diseased fruit and leaves and applying straw mulching in late May (to a thickness of 5 cm) reduced disease damage by 15–20%. Spraying lime-sulfur before bud break and spraying 75% chlorothalonil or 50% carbendazim diluted 700× with water every 10–15 days in the rain season also gave good disease control. For more effective and more environment-friendly control of diseases and pests, careful field scouting and integrated pest management strategies are needed. E. Harvesting and Handling 1. Harvesting Maturity. The ripening process of Chinese jujube can be divided into three phases based largely on color (external and internal), flesh firmness, and composition (starch, sugar, acid, water). White Mature. The fruit is near full size and shape; the skin or epicarp of the fruit is thin and light or white green color; flesh or endocarp becomes milky white and loose with less juice and sugar and more starch. Crisp Mature. The fruit is half to fully red; the skin becomes thicker, harder, and easily separated from the flesh after boiling; the flesh becomes crisp, juicy, and sweet and contains more sugar and acid.

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Fully Mature. The sugar content of the flesh increases rapidly and water content begins to decrease. The flesh near the stone and fruit stalk becomes yellow and soft. 2. Proper Harvesting Time. The fruits of Chinese jujube usually set from late May to July and are ready for harvest from August to late October in northern China. The proper harvesting date depends on the proposed use of the fruit. In general, fruits to be candied should be harvested in the whitemature period. The best harvesting maturity for table and smoked jujube is crisp mature, of which fruits for long-term storage should be harvested at half-red stage. Late picking can lead to storage disorders and shorten storage life. Fruits for drying should be picked when fully matured. 3. Harvesting Methods. The ultimate use of the Chinese jujube fruits determines the harvesting method (Liu 2004). The most commonly used harvesting method for fresh-market and processed smoked jujube is by hand, which requires careful handling at every step to prevent bruising. Fruits to be dried or candied are usually harvested by shaking the tree or beating branches. For a chemically-assisted harvest, 200–300 ppm of ethephon is sprayed 5–7 days before harvest, and this is recommended for dried fruit. This method can increase harvest efficiency by 10 times and is harmless to the tree. In addition, it increases the output and quality of dried fruit. A shaker-harvester suitable for Chinese jujube has been developed, which was reported to reduce working hours by 35% and costs by 41% compared with conventional methods (RNAM Newsletter. 1993, No. 47, 13). After harvest, fruits should be graded according to the degree of ripening and fruit size, and then stored at low temperature, dried, or processed. F. Storage 1. Storage of Fresh Fruits. The storability of fresh fruits of Chinese jujube is very poor. Under ambient temperature its shelf life is usually only 2–3 days. However, storage life is significantly longer at low temperature (Chen et al. 1986; Wang et al. 1992). Currently, semi-red fresh fruits of some selected Chinese jujube cultivars can be kept crisp for more than 100 days if packed in 0.04–0.07 mm vented polyethylene bags and stored around 0 ± 1°C. Inside the bag, the relative humidity and CO2 concentration should be kept at 90–95% and 5%, respectively. During storage, the vitamin C content remains high until fruits become soft but decreases rapidly thereafter. Xue et al. (2003) reported the effects of hypobaric storage on physiological and biochemical changes in fruit of ‘Dongzao’. Hypobaric stor-

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age significantly delayed the decrease in firmness, maintained ascorbic acid levels, reduced respiration and accumulation of ethanol and acetaldehyde in the pulp, inhibited activities of ascorbic acid oxidase and alcohol dehydrogenase, and slowed the rate of ethylene production. Hypobaric storage had little effect on flesh browning. Over-maturing at the postharvest stage usually results in a dramatic decline in quality of Chinese jujube fruit. Jiang et al. (2004) reported that the rates of respiration and ethylene production of the fruit could be reduced by 1-methylcyclopropene (1-MCP). Treatment with 1-MCP or GA delayed decreases in firmness and vitamin C and reduced the level of ethanol. GA + 1-MCP had synergistic beneficial effects on ripening inhibition of the fruit. 2. Storage of Dry Fruits. Dry fruit of Chinese jujube is easy to store. It can be stored in jars, bins, or rooms at room temperature. A cool, sheltered storage environment is required (Liu 2004). Proper control of pests and mice is necessary, especially during the rainy summer season. Lee et al. (2000) studied the lipid and color changes in dried jujube fruits during storage at 25 or 0°C for 16 weeks. Dried jujube fruits stored in the dark showed little fatty acid (mainly palmitoleic and palmitic acids) decomposition, but those stored at 25°C under light showed higher lipid oxidation. Linolenic acid decreased significantly with storage time. Ratio of unsaturated fats to saturated fats decreased when stored at 25°C under light. Color difference was affected by the presence of light and storage temperature. The effect of storage temperature was higher than that of light at the later period of storage, while the reverse was true for the earlier period. The results strongly suggest that low temperature and darkness extend the shelf life of dried jujube fruits. G. Processing Chinese jujube fruit is a well-known nourishing food and traditional Chinese medicine. It can be consumed as a table fruit or a dry fruit and also be processed into candied fruit, smoked fruit, canned fruit, jam, wine, beverage, powder, tea, flavoring pigment, and cigarette essence, etc. In addition, the flower of Chinese jujube produces a high-quality honey. Fully ripe fruits can be dehydrated through exposing them to sunlight for 2–3 weeks. Improved methods to prepare good-quality dehydrated products have been developed both in Korea and China (Kim et al. 1981; Yang and Liu 1990), i.e., dehydrated in a cabinet drier around 60°C for 36–48 hr until the moisture content of the product was reduced to less than 25%. Dehydrated jujubes are exported, usually under the name “Chinese dates.” The demand is expected to rise because dehydrated

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fruit without added sugar are preferred. Dried fruit can be consumed directly or further processed into other products such as juice, wine, and powder. Dzheneeva and Chernogorod (1989) studied the effects of freezing temperatures (–10°C to –70°C) on the biochemical composition and cellular structure of ‘Ta-yan-tszao’ fruits and concluded that a temperature between –20 and –40°C is best for deep-freezing Chinese jujube fruits.

LITERATURE CITED Ackerman, W. L. 1961. Flowering, pollination, self-sterility and seed development of Chinese jujube. Proc. Am. Soc. of Hort. Sci. 77:265–269. Ahmedov, V. A., and H. H. Halmatov. 1969. Pharmacognostic studies on Ziziphus jujuba growing in Uzbekistan (in Russian). Rastitel’nye Resursy 5:579–581. Anonymous. 1974. Handbook on human nutritional requirements. FAO studies No. 28. FAO. Rome. Bailey, L. H. 1947. The standard cyclopaedia of horticulture. Macmillan Co., New York. Bak, W. C., W. H. Yeo, J. H. Lee, Y. J. La, and C. K. Yi. 1991. Studies on fluorescence microscopic diagnosis of mycoplasmal infections in trees (in Korean). Research Reports of the Forestry Research Institute, Seoul 42:172–180. Baratov, K. B., L. V. Shipkova, I. I. Babaev, and B. L. Massover. 1974. The contents of vitamin C and P and total sugars in some Zizyphus jujuba forms cultivated in Tadznik SSR (in Russian). In: Nauchnye Osnovy Pitaniya Zdorovogo i Bol’ nogo cheloveka T.1. Alma Ata, Kazakh SSR. Kazakhstan 158–160, from Referativnyi Zhurnal (1975) 4.55.810. Bertolami, G. 1997. Chinese jujube with large fruits: prospects for extending cultivation (in Italian). Riv. Frutticoltura Ortofloricoltura 59(2):51–53. Bhansali, A. K. 1975. Monographic study of the family Rhamnaceae of India. Ph.D. thesis, Univ. Jodhpur, India. Bi, P., Z. Y. Kang, F. M. Lai, and X. Y. Lu. 1990. Study on the changes in vitamin C content of fruits of Chinese date cultivars (in Chinese). Shanxi Guoshu 4:24–25. Brandis, D. 1874. The forest flora of northwest and central India. Herbarium of the Royal Botanic Gardens, Kew. Reprinted by Bishen Singh Mahendra Pal Singh, Dehra Dun, 1972. p. 84–90. Brandis, D. 1911. Indian trees. Constable and Company L. London. p. 169–172. Chai, C. J., B. S. Ning and G. L. Chen. 1998. Effect of transplantation method on the survival rate of in vitro jujube tube plantlets (in Chinese). China Fruits 4:53–54. Chen, Y. J. (editor in chief). 1991. General introduction of Chinese jujube (in Chinese). China Science and Technology Publ. House, Beijing. Chen, Y. L., and P. K. Chou. 1982. Flora Reipublicae (in Chinese). Popularis Sinicae 48(1) Science Press. Beijing. p. 133–147. Chen, Z. W., F. W. Zhang, X. D. Tian, J. Q. Zhang, Q. K. Wang, C. L. Shi, and J. C. Ma. 1984. On the transmission of jujube witches’ broom disease (in Chinese). Acta Phytopathologica Sinica 14(3):141–146. Chen, Z. Y., C. Liu, and Z. X. Liu. 1986. Storage and processing of Chinese jujube (in Chinese). Shanxi Science and Technology Publ. House, Taiyuan. Cheong, S. T., and J. S. Kim. 1984. Characteristics of the fruit as affected by the developmental stage, embryo germination and in vitro propagation of seedling Ziziphus jujuba Mill. (in Korean). J. Korean Soc. Hort. Sci. 25(3):241–249.

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6 Taxus spp.: Botany, Horticulture, and Source of Anti-Cancer Compounds John M. DeLong and Robert K. Prange* Agriculture and Agri-Food Canada 32 Main St., Kentville, Nova Scotia, Canada, B4N 1J5

I. II. III. IV.

INTRODUCTION HISTORY BOTANY HORTICULTURE A. Ornamental Taxus B. Taxus Cultivation C. Harvesting and Storing Taxus Tissue V. PHARMACOLOGY OF ANTI-CANCER COMPOUNDS FROM TAXUS A. The Discovery of Taxol® B. Taxane Biosynthesis C. Up-regulation of Taxanes D. Pharmacology E. Taxus Toxicity F. Taxane Analogues and Mimics VI. CONCLUSIONS LITERATURE CITED

*Agriculture and Agri-Food Canada Contribution no. 2293. The authors thank Ms. Conny Bishop for computer graphic assistance and Drs. P.G. Braun and W. Kalt for reviewing this manuscript.

Horticultural Reviews, Volume 32, Edited by Jules Janick ISBN 0-471-73216-8 © 2006 John Wiley & Sons 299

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I. INTRODUCTION Taxol® is likely the most well known chemotherapeutic agent in medical history, which is an ironic distinction because Taxus spp. have garnered little other modern interest except within the ornamental industry of North America and Europe. Up until the 1980s, Taxus brevifolia (Pacific yew) and Taxus canadensis (Canadian yew) were viewed as weedy forest species with no economic value as lumber or pulp, and were either overlooked or left to rot in forest clear-cut operations. This changed in the 1960s and 1970s with the discovery of the potent anticancer activity of the taxane family of compounds found ubiquitously in yew plants. The obscure Pacific yew eventually became the focal point for the inevitable conflict between those wanting to exploit its tremendous medical potential and those wanting to keep it from becoming scarce or worse. Staggering amounts of research monies have been poured into efforts to unlock Taxol®’s unique anti-cancer mode of action and then to patent processes and technologies that have eventually made Taxol® and related compounds a pharmaceutical reality. A recent estimate that 28% of all FDA-registered clinical cancer trials involve Taxol® or its relatives (Bioxel Pharma 2003) underscores the hope that the taxanes will prove to be the silver bullet of cancer medicines, i.e., very effective and widely applicable. With such attention being paid to compounds contained within Taxus plant cells, it is ironic that modern horticultural science adds little to the cultural knowledge of yew our ancestors possessed. Yew was a highly prized wood for many purposes in medieval Europe, and was recognized as the best material for bow making. It was so valued that all importation of Spanish wine to England was to be accompanied by staves of yew wood (likely Taxus baccata), which were used by the English for longbow construction. Hence, Europeans were familiar with the details of yew culture, i.e., how to plant, grow, and harvest it and then use it for many domestic, medical, and military purposes. The highly toxic nature of all parts of the yew (with the exception of the red aril fruit; the seeds, however, are toxic) also added to the veneration and fear the ancients afforded this family of plants. A Greek botanist once reported that sleeping in the shade of the yew could induce sickness or even death. For many people, yew held deep spiritual significance: for the pagan, it was the portal to the underworld—an entrance to Hades; for the Christian, its evergreen nature came to be associated with eternal themes. Thus, Taxus spp. were prominently stationed within the cultures of many ancient peoples whose knowledge

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of its diverse attributes permitted it to be grown and harvested for multiusage, or honored as having special symbolic significance. During the last 20 years, most research published on Taxus spp. describes attempts to either up-regulate the medically important taxanes or advance knowledge on taxane anti-cancer biochemistry. Along with pharmacological data on the taxane family of compounds, this review incorporates historical, botanical, and horticultural information to provide a more comprehensive perspective for horticulturalists, plant scientists, and those interested in learning about a broader past and present yew culture than merely the biochemistry of some of its cellular constituents.

II. HISTORY The yew tree commonly appears in the historical, sacred, mythic, and folklore literature of the peoples of western Europe in particular. Not only was yew wood prized for its utility, but the tree was symbolically associated with both pre-Christian and then Christian religious belief. Pre-Christian pagans often venerated the yew tree, ascribing to it magical powers of protection against fairies and witches. The yew tree was viewed as the most powerful sacred tree of Ireland and the Druids made their wands of divination from its wood. The Roman poet Ovid stated that the yew tree marked the entrance to Hades and the underworld. The ancient Greek botanists Dioscorides, Theophrastus, and Nicander as well as Pliny the Elder recorded the botanical and toxic attributes of yew; some claimed that even sleeping under a yew tree caused sickness and sometimes death (Gerard 1633; Gunther 1968). According to Nicander, the yew was reckoned to be among the venomous plants: Shun the poysnous Yew, the which on Oeta growes, Like to the Firre, it causes bitter death, Unlesse besides they use pure wine that flows, From empty’d cups, thou drinke, when as thy breath Begins to faile, and passage of thy life Growes straight. (Gerard 1633). As Europe became increasingly Christian, the symbolism of the yew tree took on different meaning: the tree’s longevity and evergreen nature came to be associated with themes of immortality, resurrection, and new life (Hartzell 1991). One of the most impressive ancient testimonies

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to the value of yew wood was discovered in 1991 when Ötzi, the frozen 5,300-year-old Bronze Age corpse uncovered in the Austrian Alps, possessed a perfectly preserved 1.82 m bow stave made from yew wood at the time of his death (Iceman 2004). Many ancient yews thrive still and can be viewed in English churchyards where they were planted at the founding of the church, or even pre-date its establishment. For example, in a churchyard in Fortingall, Perthshire, Scotland, a magnificent specimen, split in two since the middle 1700s, is believed to be 3,000 years old, which would make it the oldest living tree in Europe. Legend has it that Pontius Pilate was born at Dun Gael, an escarpment fortress at Fortingall. If true, the Fortingall yew would have been a venerable 1,000 years old at the time of Pilate’s birth. King John signed the Magna Carta at Runnymede in June of 1215, allegedly near or in the shade of the Ankerwyke yew, which is still flourishing and is thought to be at least 1,400 years old. Also, ancient yews in England were meeting places for the “Court of the Hundreds”—a form of local government based upon land-holdings of one hundred hides (approx. 50 ha) (Bevan-Jones 2002). From the 12th to the 16th century, the yew wood longbow gained an eminent place in English history in particular, as the strength, elasticity, and light weight of the wood produced bows of superior quality. The 13th or 14th-century English folk hero Robin Hood was supposedly armed with a mighty yew bow (Hartzell 1991). At the battle of Agincourt (France) in 1415, the English army was vastly outnumbered by the French forces. As the French horsemen advanced on the English lines, Sir Thomas Erpingham (King Henry V’s archery master) gave the sign for the longbowmen to fire. When the battle ended, 5,000–10,000 French soldiers were dead, while the English lost 200–500. The victory was decided by the English army’s use of the yew wood longbow, while the French relied on a larger army, heavier armor, and horses (Hartzell 1991). In North America, indigenous peoples have used the bark, foliage, and fruit of the yew for tool and weapon-making and for ceremonial and medicinal purposes for generations. The hard, decay-resistant, yet springy wood has been prized for making canoe paddles, fish hooks, archery bows, spears, digging sticks, and ceremonial items, and more recently, for gunstocks, boat decking, furniture, snowshoe frames, and musical instruments (Small and Catling 1999). Though all parts of the yew are poisonous (except the flesh of the aril fruit), indigenous peoples used crushed yew leaves or bark to treat rheumatism, fever, pain, blood clots, scurvy, colds, bowel ailments, stomachache, venereal disease, lung ailments, and to induce healthful sweating (Voliotis 1986; Hartzell 1991; Small and Catling 1999). One

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wonders how much trial and error was necessary to come to the right ingredient mixture for these native medicines as ingested yew juice has often proven fatal!

III. BOTANY The origin of the genus name Taxus is uncertain—some believe it is derived from the Latin texere (to weave) due to the arrangement of the distichous (2-ranked) leaves, while others suggest that the name Taxus is derived from the Greek toxus or toxon, meaning a bow, or from the Greek toxikon (toxicon, toxicum), meaning poison. Whatever its origin, the genus name Taxus was first proposed by Tournefort in 1717 and was subsequently adopted by Linnaeus in his Species Planatarum in 1753 (Chadwick and Keen 1974). Modern delimitation of Taxus species has been difficult due to lack of adherence in applying universal taxonomic standards, the morphological similarities among species, and the vast number of varieties within species (Patel 1998; Spjut 2003). Taxus spp. are widespread and native to moist, temperate forests of the world, particularly the Pacific and Atlantic coasts, the mid-Atlantic and Great Lakes regions of North America, western, northern and southern Europe, Algeria, southeastern Russia, eastern China, Nepal, Burma, Laos, Thailand, Vietnam, Iran, and as far south as Sumatra and Celebes (Voliotis 1986; Hartzell 1991; Patel 1998). Depending on the authority, six to 20 Taxus species have been recognized (Small and Catling 1999), although eight or nine species, indigenous to the northern hemisphere, appear in most taxonomic descriptions. These include: Taxus brevifolia (Pacific yew), T. baccata (English yew), T. canadensis (Canadian yew, ground hemlock), T. cuspidata (Japanese yew), T. chinensis (Chinese yew), T. floridana (Florida yew), T. wallichiana (Himalayan yew), and T. globosa (Mesoamerican yew) (Bailey and Bailey 1976; Spjut 2003). Although the Taxus genus is distinguished by its cone (aril) and leaf morphology (Spjut 2003), differentiating Taxus species in cultivation can be very difficult; however, morphological features such as growth and branching habit, leaf shape, color, and arrangement may be helpful (Cope 1998; Spjut 2003). According to Dirr (1990), generic morphological characteristics of Taxus spp. include: Evergreen trees and shrubs with reddish to brown bark and spreading and ascending branches with green branchlets. Leaves are glossy or dull-dark above and lighter green below and are flat and needle-like, abruptly pointed

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or tapering and acute. Leaves are arranged radially or lie in a flat plane. Winter buds are small and scaly. Plants are mainly dioecious with globose male flowers and female flowers appearing as small stalked conical buds in the leaf axils. Seeds are brown and nut-like and are covered with a red fleshy aril, ripening in the first year (Fig. 6.1).

Chadwick and Keen (1974) report that both dioecious and monoecious plants are found in the species and cultivars of Taxus; interestingly, yews have been known to change sex as they mature (e.g., a plant changes from producing female to male flowers) (Hatfield 1929), likely due to environmental signals/stresses. In North and South America, four native species are recognized by their geographic location: (1) the Pacific yew (T. brevifolia), distributed in western Canada and the U.S.; (2) the Mexican yew (T. globosa), native to Mexico, El Salvador, Honduras, and Guatemala; (3) the Florida yew (T. floridana), native to northern Florida; and (4) the Canadian yew (T. canadensis), which grows from Newfoundland to Manitoba and southward to Iowa and North Carolina. The English yew (T. baccata) flourishes in Europe and north Africa (Patel 1998). The Japanese yew (T. cuspidata) is endemic to eastern Asia (China, Japan, Korea, and Russia), while the Himalayan yew (T. wallichiana) grows from eastern Afghanistan to Tibet and China (Patel 1998). Taxus spp. can also be differentiated on the basis of the morphological attributes of the leaves, resulting in three main groupings: the Baccata group—including T. canadensis and some of the cultivated species, e.g., T. baccata and T. cuspidata; the Wallichiana group—including T. brevifolia, T. floridana, and T. globosa; and the Sumatrana group. The Baccata and Wallichiana groups are native to North America, while the Sumatrana group is largely represented by southeast Asian species (Spjut 2003). Attempts have been made to classify Taxus spp. on the basis of the levels of anti-cancer taxane compounds (e.g., baccatin III, 10-deacetyl baccatin III; paclitaxel, in particular) present in the needles (van Rozendaal et al. 2000; Parc et al. 2002). Although cultivars of a species or hybrid (e.g., Taxus × media) have differing leaf taxane content, it is not possible presently to create consistent high-to-low taxane categories due to the inherent variation encountered when needle taxane levels are measured (Poupat et al. 2000; van Rozendaal et al. 2000). Interestingly, species like T. canadensis show unique taxane profiles that may be potentially exploited for the pharmaceutical industry (Parmar et al. 1999; Zamir et al. 1992; Nikolakakis et al. 2004). Thus, segregating Taxus species, hybrids, or cultivars on the basis of commonly shared taxane compounds may be more useful than delineation

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Fig. 6.1. Taxus baccata leaves, flowers, and fruiting structures. (1A) Immature female flowers. (1B) Mature female flower following fertilization. The red cup-like covering (aril) surrounding the seed is forming. (2A) Immature fruit. (2B) Mature aril fruit with fleshy outer aril and a single seed at the center. (2C) Mature fruit (aril and seed) cut longitudinally. (3A & 3B) Male flowers. (4) Leaf spray with male flowers in the axils. (5) Leaf spray with mature aril fruit. Permission for use granted by Kurt Stüber of the Max Planck Institute for Plant Breeding Research, Cologne, Germany. www.biolib.de

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based on leaf taxane content or leaf morphology (van Rozendaal et al. 1999). Also, genome analysis would aid in understanding the genetic relationships among the many species and cultivars of the Taxus genera.

IV. HORTICULTURE A. Ornamental Taxus In 1862, Japanese yews were imported into the United States when Dr. George Hall brought them back from Japan during a plant collection trip. Dr. Hall made the plants available to the nursery trade through Parson’s Nursery, Flushing, Long Island, New York. Around 1866, H.H. Hunnewell (Wellesley, Mass.) received specimens of T. cuspidata and T. cuspidata var. nana from the Parson’s Nursery and planted them on his estate because he had a keen interest in evergreen species not previously available in the U.S. In 1886, Theopolius D. Hatfield (1855–1929) began working for the Hunnewell family and was a major influence in introducing and developing ornamental Taxus in the U.S. Hatfield began to propagate yews from seeds and identified a hybrid from a cross of T. baccata var fastigiata (Irish yew) and T. cuspidata. Although Hatfield makes no mention of an intentional cross, the new hybrid plants may have been the first specimens of the Taxus × media hybrid (Anglojap yew). Eventually, the varied forms that he selected from his seedling experiments were introduced in the American nursery trade (Hatfield 1921, 1929; Cochran 1999). Hatfield studied the imported species of Japanese yew (T. cuspidata) growing at the Hunnewell Estate and reported that the spreading varieties ‘nana’ and ‘brevifolia’ (later given the name ‘Densa’) were the first to become popular in the nursery industry (Cochran 1999). Also growing at Hunnewell was the English yew (T. baccata), which possessed a fine appearance for a few years, but was susceptible to winter injury resulting in foliage browning and a disfigured appearance, traits that led Hatfield to conclude that the Japanese yew was a superior ornamental plant (Cochran 1999). In 1902, the Hicks yew (T. × media ‘Hicksii’) became available from the Hicks nursery of Long Island, New York. It was a seedling selection collected from the Dana Arboretum (Long Island, NY) and has since become the standard yew of the nursery trade in North America (Cochran 1999). The taxonomist, Alfred Rehder, first proposed the name T. × media for the hybrids of T. baccata and T. cuspidata and recognized that a wide variety of forms was possible (Chadwick and Keen 1974).

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Taxus × media is the hybrid designation for most of the cultivars that have been introduced since Hicks and Hatfield; however, the definitive genetic basis for Taxus × media needs to be determined through gene analysis (Cochran 2001). Approximately 190 ornamental cultivars of yew have been identified to date (Cope 1998). Yews have become the most popular narrow-leaved evergreen ornamental plants in the 2nd half of the 20th century in North America and will likely retain their popularity well into the 21st century (Cochran 1999). The handsome, lustrous, dark, evergreen foliage and the varied physical forms of the commercially available cultivars, which range from low-profile, compact, and dense types to the taller columnar and pyramidal forms, have played an indispensable role in establishing the yew’s landscape popularity (Chadwick and Keen 1974; Dirr 1990; Cochran 1999). B. Taxus Cultivation In general, Taxus spp. can grow in a wide range of cultural conditions but thrive best on loamy soils of a slightly acidic or neutral pH having adequate moisture. According to Dirr (1990), good soil drainage is critical for yews and anything less than excellent drainage results in marked reductions in growth or eventual death of the plants. In poorly drained soils, root rot can be a problem (Taylor et al. 1996). Yews will flourish in open sun or partial shade, but should be kept out of sweeping, desiccating winds, and generally do not tolerate extreme cold or heat well. Depending on the species, yews grow in most hardiness zones, ranging from USDA zone 2 (T. canadensis) to zone 8 (T. floridana) (Dirr 1990; Gilman and Watson 1993; Taylor et al. 1996). Since many of the cultivars have a compact and symmetrical form, little corrective pruning is required. Dirr (1990) recommends pruning rather than shearing to retain the natural shape and habit of the particular yew cultivar. Nonetheless, Taxus spp. can be sheared or pruned severely into topiary forms; for example, the Levens Hall estate in Cumbria, England has a famous topiary garden dating back to the late 1600s that presently contains many finely clipped yew specimens (Levens Hall 2004). The size and shape of the ornamental Taxus spp. varies greatly—ranging from the upright tree form of T. baccata ‘Fastigiata’ (Irish yew) to the low spreading cultivars of T. × media (‘Densiformis’, ‘Chadwickii’)—attributes that have led to the wide use of Taxus in the landscape (Dirr 1990). Although woody ornamental or Christmas tree fertilizer guidelines can be used for Taxus spp., annual fertilizer practices should be based on foliar and soil analyses. Generally, the application of fertilizers with

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N, P, K having elemental ratios of 4:0.4:0.8, 3:0.4:0.8, or 3:0.4:1.6 are recommended and can be top-dressed around the base of the shrub’s drip line in the early Spring for established plants. A sole N fertilizer can be applied if the soil analyses indicate adequate levels of P and K; otherwise, slow release fertilizers may be used. Organic materials such as compost and manure can be utilized and will improve soil structure; however, nutrient levels are often variable and should be determined through analyses. Compost guidelines for northeast North America indicate application of no more than 3 m3 per 0.1 m2 of surface area [about 2 cm deep]. During site preparation just prior to planting, incorporate P and K if tests show deficiency, and leave N application for the next year, or use compost or well-rotted manure to avoid root burning. Split applications of N fertilizer during the growing season will reduce the likelihood of root burn and will lessen the potential for ground water contamination. Lime applied at the time of planting will help correct low soil pH and should be thoroughly mixed with the soil in the root zone area (Kujawski and Ryan 2000). Yews are resistant to many pests and diseases and are relatively trouble-free. However, the Taxus mealybug (Dysmicoccus wistariae), the Taxus scale (Pulvinaria floccifera), the yew-gall midge (Taxomyia taxi), the black vine weevil (Otiorhynchus sulcatus), and nematodes (Pratylenchus spp.) have been known to cause plant damage (Gilman and Watson 1993; Taylor et al. 1996). C. Harvesting and Storing Taxus Tissue Several studies have shown that in T. brevifolia, the taxane content of needles is comparable to that of bark (Witherup et al. 1990; Mattina and Paiva 1992; Wheeler et al. 1992). These findings have aided development of a more sustainable system of procuring taxanes from Taxus tissue in which yew needles rather than bark are harvested because the latter process results in tree destruction. More recent efforts to ascertain which Taxus species (and even cultivars) possess the highest natural level of needle taxanes show that concentrations of these metabolites can so vary among individual shrubs/trees of the same species that consistent average quantities are very difficult or impossible to establish (Wheeler et al. 1992; Poupat et al. 2000; van Rozendaal et al. 2000). For example, Mattina and Paiva (1992) report that the paclitaxel concentrations in needles of T. × media ‘Nigra’ are higher than in 13 other species/cultivar; however, marked variation was present in the data from the 2 nurseries that supplied the yew plants. Variation in cellular taxane levels is affected by the same factors that influence other crops, such as inherent genetic

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differences, the presence or absence of water stress, soil pH, temperatures, and insect pressure (Wheeler et al. 1992; Hoffman et al. 1999). To maximize the taxane yield from yew needles, it is necessary to harvest the tissue when cellular taxane levels are at their highest concentration. Griffin and Hook (1996) and Németh-Kiss et al. (1996) have shown that the highest content of paclitaxel is present in the dormant winter/early spring months, while tissue sampled in May and June during the period of rapid new growth exhibit some of the lowest paclitaxel content. Griffin and Hook (1996) also showed that the “golden leaf” Irish yew cultivar has significantly less paclitaxel than the common green leaf types. Interestingly, ElSohly et al. (1997) conducted a similar study on Taxus × media ‘Dark Green Spreader’ and concluded that the best time to harvest Taxus clippings for the production of taxanes is approximately one month after the beginning of new growth, i.e., June. As each of these 3 studies used divergent Taxus species, the differences in taxane content were likely due to inherent genetic differences. Geographic/climatic dissimilarities at the experimental sites were less likely to have caused the differences since Dublin, Ireland (53°N latitude) (Griffin and Hook 1996), Budapest, Hungary (47°N latitude) (Németh-Kiss et al. 1996), and Oxford, Mississippi (35°N latitude) (ElSohly et al. 1997) are all temperate regions with mild winters and little snow. The goal in harvesting Taxus spp. shoots is to collect adequate plant biomass without jeopardizing regrowth potential. T. canadensis handharvest guidelines published by the Canadian Forest Service (CFS) attempts to arrive at this concession by emphasizing cutting of no more than 3 years growth (20–25 cm) per harvest and not harvesting the same plant for at least 4 years (number of years growth removed + 1) (NRCan 2002). The CFS recommendations suggest that the ideal harvest time is in the dormant months when taxane levels in the tissue tend to be the greatest. The same recommendations are appropriate for commercial harvest of other types of Taxus spp., although 5–10 cm of terminal shoot tissue is a common harvest length reported in scientific research (Schutzki et al. 1994; Hoffman et al. 1999). Mechanization of Taxus shoot harvest has been developed and is particularly well suited for uniform nursery plantations on flat land (Holmes and Wuertz 1999); however, hand harvest is necessary for collecting wild Taxus biomass due to the types of terrain on which it flourishes. Following the harvest of yew sprigs, the fresh clippings are often stored for a period of time before the needles are processed for taxane extraction. Schutzki et al. (1994) found that storage of intact Taxus × media clippings for 27 days results in a paclitaxel increase in the needle tissue from harvest until day 9, followed by a gradual decline to

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slightly below harvest levels at day 27. They also show that storing the clippings at 22 versus 4°C during the first 9 days resulted in an increase in paclitaxel concentration of 40 and 26%, respectively, compared with ‘at harvest’ levels. Their study did not, however, specifically address the issue of the influence of tissue moisture loss on taxane measurements. The goal in drying fresh Taxus biomass is to find the temperature/time combination that adequately dries the tissue without causing loss of taxane content. DeLong et al. (2003, 2004; unpublished data) have shown that: (1) tissue moisture content can strongly influence taxane measurements, particularly those made over an extended storage duration (e.g., 4–8 weeks) during which gradual drying of the needles occurs; and (2) when tissue moisture is accounted for, taxanes can increase in stored Taxus clippings with needles and stems intact. Hansen et al. (1993) dried intact Taxus × media ‘Hicksii’ clippings at 30, 40, 50, and 60°C for 4, 3, 1, and 0.7 days, respectively, and found that tissue dried at 60°C yielded the highest needle taxane content. It may be that drying Taxus needles for a short time at 60°C inactivates or slows degradative pathways without causing taxane loss. Irrespective of the optimal drying process, Taxus biomass requires dehydration, particularly if the intent is to store it for lengthy periods; drying is also necessary for precise taxane measurement, as varying tissue moisture levels can influence the results.

V. PHARMACOLOGY OF ANTI-CANCER COMPOUNDS FROM TAXUS A. The Discovery of Taxol® The modern discovery of Taxol® [paclitaxel (generic name)] as a unique, natural, anti-cancer agent is traced back to an early 1960s United States Department of Agriculture (USDA) screening program initiated by the National Cancer Institute (NCI), which emphasized discovery of new plant-based, anti-tumor agents (Stephenson 2002). In 1962, Arthur Barclay and three student assistants collected 650 plant samples in California, Washington, and Oregon, which included the bark, twigs, leaves, and fruit of the Pacific yew tree (T. brevifolia) collected from the Gifford Pinchot National Forest in Washington state (Wall and Wani 1995; Patel 1998). These yew samples, initially tested by the phytochemists Monroe Wall and Mansukh Wani from the Research Triangle Institute in Durham, North Carolina, demonstrated only modest activity against the bioassay standards used in the 1960s. Tests in the 1970s showed much

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better activity against newly developed assay models; consequently, paclitaxel was selected as a candidate for further development. Nonetheless, there were formidable obstacles ahead as the raw resource underwent development as a potential drug, including: paclitaxel being highly insoluble in water, which presented difficult formulation challenges; paclitaxel being present in minute concentrations in the bark of the slow-growing and uncommon Pacific yew; and, harvesting the yew bark was done at the cost of destroying the tree. In addition, the potential devastation to the species sparked off a controversial and highly influential chapter in the Taxol® story as conservation groups took action to stop the seemingly relentless destructive harvest of the Pacific yew (Hartzell 1991; Kingston 2000). Currently, the Pacific yew harvest has greatly diminished as the source of taxanes has switched from non-renewable bark to renewable needles in either native stands or yew plantations (Mark Savage, Washington State Department of Natural Resources, pers. commun.). As an example, native stands of T. canadensis (ground hemlock) are presently being harvested in eastern Canada as a renewable source of taxanes for the pharmaceutical industry (Atlantis Bioactives 2004). Thus, by shifting to a more sustainable system of taxane supply, the ecological and political controversies that surrounded the Pacific yew saga can be avoided. B. Taxane Biosynthesis Paclitaxel is comprised of a complex and unusual diterpene carbon skeleton (C20) with eight oxy-functional groups and several acyl side chains resulting in 11 chiral carbons (Sankawa and Itokawa 2003; Fig. 6.2A). Earlier studies suggest that paclitaxel is synthesized via the mevalonic acid pathway; however, exogenous, radio-labelled acetate and mevalonate are incorporated into the taxane ring system at rates of only 0.02–0.12% (Lansing et al. 1991; Zamir et al. 1992). More recent research has demonstrated that the unique taxane ring is formed from the mevalonate-independent, 2-C-methyl-D-erythritol phosophate (MEP) [also called the glyceraldehyde 3-phosphate/pyruvate pathway or the 1deoxy-D-xylulose-5-phosphate pathway] plastidic pathway, which supplies the fundamental isoprenoid precursor molecules—isopentenyl diphosphate (IPP) and dimethylallyl diphosphate (DMAPP)—for subsequent taxane (and other terpenoid) biosynthesis (Schwender et al. 1996; Eisenreich et al. 1996, 2001; Croteau et al. 2000; Jennewein et al. 2004). Although the non-mevalonate plastid pathway(s) appears to be the major contributor of IPP for taxane synthesis, some studies suggest there may be “crosstalk” with the cytoplasmic mevalonic acid route to

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A

B Figs. 6.2A&B.

Chemical structures of: (A) paclitaxel (Taxol®) and (B) docetaxel (Taxotere®).

provide IPP or other metabolites for taxane anabolism (Srinivasan et al. 1996; Cusidó et al. 2002; Palazón et al. 2003). The complex taxol biosynthesis pathway is proposed to be a series of 19 or 20 enzyme-mediated reactions in which the diterpenoid precursor geranylgeranyl diphosphate (GGPP) (C-20) is cyclized by taxadiene synthase to form taxadiene, the core taxane ring structure. This is followed by a series of oxygenation and acetylation reactions with the final anabolic chemistry resulting in addition of the benzoylphenylisoserine acyl group at carbon 13. Paclitaxel synthesis is catalyzed by eight cytochrome P450 oxygenases (hydroxylases) that incorporate oxygen

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groups into the ring structure at C-5, then at C-10, C-2, C-9, C-13, C-7, and C-1; the two acetate and benzoate groups are added by acyl and aroyl CoA-dependent transferases (Fig. 6.3; Walker and Croteau 2001; Sankawa and Itokawa 2003; Jennewein et al. 2004). The potent antimitotic activity of the taxanes like paclitaxel is contingent upon molecular structure, and requires: (1) the presence of the N-benzoyl-3-phenylisoserine side chain (or an appropriate substitution as with docetaxel) at C-13; (2) the oxetane ring structure involving C-20, C-4, and C-5; and (3) the benzoyl group at C-2 (Fig. 6.2A.; Jennewein and Croteau 2001; Kingston 2001). If any of these 3 structural components are missing, paclitaxel in particular will either have no activity or a markedly reduced microtubule stabilization/cell cytotoxicity function (He et al. 2001; Kingston 2000, 2001). Although complete chemical synthesis of Taxol® is currently possible (Kingston 2001), it is a costly, non-feasible process as a means of commercial supply. Taxol® and its analog Taxotere® [Fig. 6.2B.; docetaxel (generic name)] are semi-synthesized more efficiently from the natural precursor molecules baccatin III and 10-deacetyl baccatin III (10-DAB) (Patel 1998; Jennewein and Croteau 2001), which are often found in higher cellular concentrations than is paclitaxel and are also ubiquitous in Taxus tissue (Kikuchi and Yatagai 2003; van Rozendaal et al. 2000). Harvest of Taxus needles for extraction of these precursor taxanes (and of paclitaxel) has become a common and renewable practice that circumvents the destructive harvest of bark tissue. Hence, the routes from baccatin III and 10-DAB to Taxol® and its analog Taxotere® are presently the major pathways of semi-synthesis, involving insertion of the Nbenzoyl-3-phenylisoserine side chain to the C-13 hydroxy group of 10DAB and acetylation of the 10β-hydroxyl position for Taxol® formation, or addition of an N-t-butoxylcarbonyl-3-isophenylserine side chain to the 13α-position of 10-DAB for Taxotere® synthesis. The use of cell cultures to supply the taxane precursors for semi-synthesis is a promising approach, but is currently not commercially viable due to low and unstable production yields (Jennewein and Croteau 2001). It appears that the semi-synthetic route for Taxol® and Taxotere® production from taxane precursors extracted from needles, in particular, will remain the principal means of commercial supply for the foreseeable future. C. Up-regulation of Taxanes Since the discovery that the taxanes have a unique mode-of-action and are effective against certain cancers, researchers have grappled with how to increase the minute concentrations of naturally produced taxanes

314 Fig. 6.3. Taxol biosynthesis steps: (a) cyclization of geranylgeranyl diphosphate by taxadiene synthase to yield taxa-4(5), 11(12)-diene; (b) hydroxylation at C-5 by taxadine 5α-hydroxylase (a cytochrome P450 oxygenase) to form taxa-4(20), 11(12)-dien-5α-ol; (c) acetylation at C-5 by taxa-4(20), 11(12)-dien-5α-O-acetyltransferase to form taxa-4(20), 11(12)-dien-5α-yl acetate; (d) hydroxylation at C-10 by cytochrome P450 taxane 10βhydroxylase to form taxa-4(20), 11(12)-dien-5α-acetoxy-10β-ol; (e) formation of 2-debenzoyltaxane via hydroxylation reactions and the synthesis of the functional oxetane ring involving C-5, C-4 and C-20; (f) 10-deacetylbaccatin III (10-DAB) formation from 2-debenzoyltaxane by taxane 2αO-debenzoyltransferase; (g) conversion of 10-DAB to baccatin III by 10-deacetylbaccatin III 10-O-acetyltransferase; and (h) benzoylphenylisoserine side-chain synthesis and attachment to C-13 of baccatin III involves aminomutase-, hydroxylase- and transferase-mediated reactions (Jennewein and Croteau 2001; Schoendorf et al. 2001; Walker and Croteau 2001; Walker et al. 2002; Sankawa and Itokawa 2003; Jennewein et al. 2004).

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in yew tissue. Basically, two approaches have been taken: (1) a focus on Taxus cell cultures (Mirjalili and Linden 1996; Linden et al. 2001; Cusidó et al. 2002; Zhang and Wu 2003); or (2) manipulation of the intact Taxus plant followed by sprig or whole plant harvest (Hoffman et al. 1999; Kikuchi and Yatagai 2003). Much more research emphasis has been placed on the former due to the ease of manipulation of the cell culture system, and cell cultures have shown a marked ability to increase taxane content under the appropriate conditions. The methods of this “up-regulation research” largely center on introducing an elicitor(s) or imposing an external condition/environmental stress on the system (intact tissue or cell culture) as a trigger for up-regulation of the terpenoid synthesis pathway(s), which results in greater taxane accumulation (Srinivasan et al. 1996; Wu et al. 2001; Chen et al. 2003). Significant research effort has focused on taxane elicitation induced by methyl jasmonate (MJ) and ethylene, singly or in combination, in Taxus cell suspension cultures. Phisalaphong and Linden (1999) and Linden et al. (2001) theorize that taxane biosynthesis is controlled by MJmediated allosteric regulation of ethylene binding; MJ thus acts as an “ethylene sensitivity factor” modulating ethylene binding, which then initiates the signal cascade that results in accumulation of secondary metabolites. Differing MJ concentrations appear to strongly influence taxane promotion. For example, in the presence of constant headspace ethylene (5–8 ppm), low exogenous MJ concentrations (0–20 μM; unmodulated ethylene binding) applied to T. canadensis cell suspensions, block induction of enzymes that synthesize or add the phenylisoserine side chain to baccatin III. At mid-high levels (up to 200 μM), MJ stimulates paclitaxel production, while at higher concentrations (> 200 μM), the modulation protein site is saturated, resulting in declining taxanepromoting effects (Phisalaphong and Linden 1999). Methyl jasmonate has been shown to induce GGPP synthase activity, which stimulates significant taxane accumulation in cell cultures of T. baccata (Laskaris et al. 1999), presumably through an increase in the synthesis of the primary C20 diterpene molecule (GGPP) that forms the taxane skeleton. Yukimune et al. (1996) demonstrate that the structure of MJ can affect the production of taxanes: an acetic acid substitution or its ester at C-1 and a keto group at C-3 are important for taxane enhancement. Their work also indicates that MJ stimulates paclitaxel production from GGPP to baccatin III, and from baccatin III to paclitaxel. More recently, Yukimune et al. (2000) show that the 3R,7R stereoisomer configuration of MJ promotes the highest production of paclitaxel and baccatin III in T. × media cell cultures (it also inhibited cell growth), although the biochemical mechanism is unknown.

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Ethylene concentration between 5 and 8 ppm and 100–200 μM MJ in the headspace above the growth media are apparently optimal for taxane up-regulation in Taxus cell cultures (Mirjalili and Linden 1995; Yukimune et al. 1996; Ketchum et al. 1999). At lower and higher ethylene and MJ levels, taxane elicitation either does not occur or is significantly reduced (Mirjalili and Linden 1996; Phisalaphong and Linden 1999; Linden and Phisalaphong 2000; Linden et al. 2001). Interestingly, ethylene inhibitors (e.g., α-amino isobutyric acid, CoCl2, NiCl2, Ag+) applied with a fungal (Aspergillus niger) elicitor, increase paclitaxel production while application of ethrel (ethylene generator) along with the fungal elicitor, decrease taxane accumulation in cell cultures of several Taxus species (Zhang and Wu 2003). Other elicitors exogenously applied have been shown to up-regulate taxanes. A chitosan-derived oligosaccharide (N-acetylchitohexaose) stimulates an increase in paclitaxel production when applied with 50 or 100 μM MJ (Linden and Phisalaphong 2000)—results similar to that generated when MJ and ethylene are concomitantly applied (Mirjalili and Linden 1996; Phisalaphong and Linden 1999). Linden and Phisalaphong (2000) conclude that MJ-induced ethylene production may heighten the tissue sensitivity to low levels of the oligosaccharide elicitor. Interestingly, ethylene generation by the Taxus cell suspension cultures was markedly inhibited by the elicitor. Hence, there appears to be complex “crosstalk” between the putative elicitors of taxane upregulation and the intra- and intercellular signals induced by hormone molecules like MJ and ethylene that regulate fundamental cellular biochemistry in response to environmental stress. Other elicitors/promotors of taxane up-regulation in Taxus cell suspensions include: the rare earth element lanthanum (Wu et al. 2001), nitrate and ammonium (Chen et al. 2003), UV-C irradiance (Hajnos et al. 2001), temperature elevation from 24 to 29°C (Choi et al. 2000), water deprivation (Hoffman et al. 1999) and increased osmotic pressure, which increases exogenous cellular sugar concentrations (Kim et al. 2001). It may be that these elicitors eventually induce an ethylene and/or MJ response that consequently alters the production of cellular diterpene compounds. Elicitor-induced biochemical mechanism(s) responsible for the increase in cellular taxanes have not been identified to date. The oxygen and carbon dioxide concentrations surrounding Taxus cell cultures have been shown to influence the production of paclitaxel. Mirjalili and Linden (1995) found that 10% (v/v) oxygen and 0.5% (v/v) carbon dioxide, accompanied with 5 ppm (v/v) ethylene, was the most effective gas composition for eliciting the highest paclitaxel production. The authors suggest that this particular gas composition favorably

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altered the partitioning of nutrients facilitating high cellular growth rates as well as paclitaxel production. In another report, Linden et al. (2001) state that the optimum gas composition for paclitaxel elicitation in Taxus cell culture was 17% (v/v) oxygen and 1.5 % (v/v) carbon dioxide in the presence of 5 ppm (v/v) ethylene. Although little has been published on taxane up-regulation in wholeplants, Hoffman et al. (1999) report that severely water-stressed ‘Hicks’ yew produce significantly greater amounts of needle taxanes compared with minimally or moderately stressed shrubs. For arid areas in particular, controlled water stress appears to be a potential tool for boosting taxane content in the field. However, the application of cell culture upregulation methods for increasing taxanes may not be successful with intact sprigs or whole yew plants. DeLong and Prange (2004; unpublished data) found that altering the storage CO2 and O2 environments from 0.3–10% (v/v) and 10–21% (v/v), respectively, or the application of 100–400 μM MJ, 1–5 ppm (v/v) ethylene or 0.5 mM salicylic acid, or a continuous irradiance of 300–400 μmol m–2 s–1 to harvested T. × media sprigs, had no effect on cellular taxane levels. D. Pharmacology Paclitaxel has demonstrated significant antineoplastic (anti-cancer) activity against a broad spectrum of human tumors, including: ovarian, breast, head, neck, small-cell, and non-small-cell lung (Parekh and Simpkins 1997; Gautam and Koshkina 2003), gastric (Roth and Ajani 2003) and prostate cancers (Beer et al. 2003). It is presently approved for the treatment of breast, ovarian and non-small-cell lung cancers, and AIDSrelated Kaposi’s sarcoma (BMS 2004). The unique anti-tumor properties of Taxol® (Fig. 6.2A) and the semisynthetic Taxotere® (Fig. 6.2B) are based upon their ability to promote the assembly and then the stabilization of mitotic spindle microtubules during the late G2/early M phases of the mitotic cell cycle. By the late G2 phase of the cell cycle, DNA has replicated and the cell is preparing for mitosis. During prophase, the replicated chromosomes condense, the nuclear membrane disintegrates, and the mitotic spindle forms. The mitotic spindle is composed of microtubules—contractile fibers of αβ-tubulin protein—that pull apart chromosome pairs to the poles of the cell in preparation for cytokinesis. In the later mitotic phases, the spindle disappears just prior to cell division. During prophase, taxanes promote microtubule stability by binding to the hydrophobic Nterminus region of the β-tubulin protein, which mimics the binding of the GTP nucleotide during normal cell mitosis. Taxane binding alters the

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conformation of the protein subunit, which then disables the disassociation or depolymerization of the tubulin dimer (Fig. 6.4) Cell division in the later mitotic phases is thus blocked and the cell subsequently dies (Parekh and Simpkins 1997; Patel 1998; Rao et al. 1999). In contrast to the taxanes, other plant-based anti-mitotic agents such as vinblastine and vincristine (from Catharanthus roseus), colchicine (from Colchicum spp.), and podophyllotoxin (from Podophyllum hexandrum) promote microtubule depolymerization or destabilization that prevents the mitotic spindle from fully forming, thus microtubule dynamics are suppressed (Desbene and Giorgi-Renault 2002; Gordaliza et al. 2004; Jordan and Wilson 2004). Paclitaxel may also cause cell cytotoxicity by promoting an exit from mitosis to a G1 state of the cell cycle that is marked by abnormal chromosomal segregation, the appearance of multiple cellular micronuclei, and finally apoptosis (Abal et al. 2003). Recent research has also shown that paclitaxel impairs the normal function of the centrosome, resulting in abnormal mitotic spindle formation and eventually cell death (Abal Initiation

Heterodimer Formation Nucleation Center α-Tubulin

MAPS, Mg 2+ GTP Ca 2+, 0 °C

Polymerization/ Elongation Normal polymerization

Normal microtubule 13 protofilaments 24 nm diameter

(α β) β-Tubulin

Taxol-promoted polymerization Taxol

Taxol-promoted polymerization

Stabilized microtubule 12 protofilaments 22 nm diameter

Fig. 6.4. Normal (upper) and Taxol®-promoted (below) microtubule assembly. Once polymerization occurs, microtubules cannot de-polymerize, resulting in mitotic arrest and eventually, cell death. MAPS: microtubule associated proteins; GTP: guanosine triphosphate (from Kingston 2001).

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et al. 2001). Paclitaxel also binds to the Bcl-2 apoptic protein facilitating dose-dependent hyperphosphorylation of that protein, which is linked to tubulin assembly, Raf-1 protein activity, and then to cellular apoptosis (Kingston 2001). The microtubule stabilizing activity of the taxanes is being presently exploited for non-chemotherapeutic applications. Likely the most promising is a paclitaxel-coated stent used in balloon angioplasty surgery, which greatly reduces the degree of post-operative tissue regrowth (restenosis) in the region of the artery where the stent is placed. The paclitaxel eluting from the stent causes mitotic arrest in the cells of the arterial wall, which effectively halts any tissue proliferation. The result is a clean, open artery through which blood flows without restriction (Angiotech 2004; Cooper Woods and Marks 2004). The taxanes are also being tested for treatment of urethral cancer and kidney disease (Woo et al. 1997; Vaughn et al. 2002; Gitlitz et al. 2003), severe psorarisis (Ehrlick et al. 2004), and rheumatoid arthritis (Angiotech 2004). E. Taxus Toxicity All parts of the yew plant are poisonous, with the exception of the outer flesh of the aril fruit; however, the seed within the flesh is highly toxic (Kingsbury 1964). Leaves of Taxus spp. are toxic whether they are green and healthy on the plant or dry and desiccated following senescence. Taxus is poisonous to many animals, although white-tailed deer and certain seed-eating birds seem to be less affected than horses or cattle. The green foliage is toxic to both monogastric (e.g., horses) and polygastric ruminant animals (e.g., cattle) at about 0.1% and 0.5%, respectively, of body weight (Kingsbury 1964). Following ingestion of yew leaves, animals are frequently found dead within 1–3 hours. Symptoms of yew ingestion may include: diarrhea, vomiting, tremors and convulsions, dilated pupils, respiratory difficulty, weakness, collapse, slowed heart rate, circulatory failure, coma, and death. The onset of acute symptoms is often rapid; usually an animal appears healthy, then unexpectedly gasps several times and dies. Hence, it is important to keep grazing animals away from yew plants and to ensure that yew trimmings are not accidentally combined with grass clippings fed to stock. The taxine alkaloids, in particular, are thought to be responsible for the severe toxicity of the yew (Wilson et al. 2001). These alkaloids act as cardio-depressants, inhibit sodium and calcium currents that block myocardial conduction, and cause the heart to stop in the diastole (expansion) phase; the usual cause of death is cardiac arrhythmia. Presently, there is no known antidote to taxine poisoning, although

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induction of vomiting, gastric lavage, activated charcoal, and atropine injections may have some effect if performed soon after ingestion occurs (Kingsbury 1964; Wilson et al. 2001). F. Taxane Analogues and Mimics Taxane analogues have been developed that possess paclitaxel-like activity but do not have its deleterious side effects, which are partially attributed to the carrier(s) necessary to solubilize hydrophobic Taxol® into the bloodstream. Presently, Taxol® is intravenously administered with Cremophor® EL, a polyoxyethylated castor oil surfactant, which markedly improves its solubility (Taberelli et al. 2003). However, Cremophor® EL side effects may include: anaphylactic hypersensitivity (Mounier et al. 1995), and degeneration, demylineation, and swelling of axons, as well as peripheral neuropathy (Arthier et al. 2000; Windebank et al. 1994). Although hypersensitive reactions are controlled by pretreatment with antihistamines or corticosteriods, the development of antineoplastic agents having Taxol®-like activity, but are less hydrophobic, has been the focus of much recent research. As a result, docetaxel (Taxotere®)—a 2nd generation, semi-synthetic taxane derived from Taxus spp. needles—is presently marketed by Aventis Pharmaceuticals Inc. and shows greater cytotoxicity to some tumor assays than does Taxol®. It is currently prescribed as a mono- or combination therapy for breast, non-small cell lung, and prostate cancers (Taxotere 2004). While its mode of activity is similar to Taxol®’s, docetaxel’s higher tumour cell potency is due partly to longer intracellular retention. Glycosylated analogues of docetaxel show increased water solubility, which affects cellular retention and thus antineoplastic activity (Nikolakakis et al. 2004). Docetaxel is primarily active in the S-phase of mitosis, whereas paclitaxel is mainly active in the G2/M phase (Crown and O’Leary 2000). Besides microtubule stabilization, docetaxel has also demonstrated proapoptotic activity via down-regulation of the apoptosis signal transduction Bcl-2 gene family, and inhibition of angiogenesis (process of tumors developing new capillary blood vessels), resulting in suppression of metastases (Herbst and Khuri 2003). Paclitaxel and docetaxel also show immunomodulatory effects that indicate their cancer cell suppression action may be attributable to several mechanisms and not solely to disruption of cell division (Fitzpatrick and Wheeler 2003). Several other natural compounds have been discovered that mimic the mitotic disruption activity of the taxanes. The epothilones (A and B), derived from the myxobacterium, Sorangium cellulosum strain 90, show antifungal and cytotoxic effects through microtubule stabilization (Bol-

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lag et al. 1995; Kowalski et al. 1997; He et al. 2001). Discodermolide, originally isolated from a deep-sea marine sponge (Discordermia dissoluta) promotes microtubule stabilization in a way similar to that of Taxol®, but also initiates tubulin assembly instantaneously, resulting in microtubules that are shorter than those treated with paclitaxel (He et al. 2001). Discodermolide binds to microtubules and then stabilizes them against disassembly more potently than does paclitaxel and is effective even at 4°C (ter Haar et al. 1996; Martello et al. 2001; Kar et al. 2003). Clinical formulations of the epothilones and discodermolide (and their analogues) are presently being developed and clinically tested at the Phase I & II levels (Lin et al. 2003; Goodin et al. 2004; Honore et al. 2004; Kolman 2004; Mani et al. 2004) and will likely be available within a few years as valued additions in the arsenal of compounds that disrupt the mitotic cycle of cancer cells by de-stabilizing microtubule assembly.

VI. CONCLUSIONS Since antiquity, few plants have had the yew’s double distinction of being both feared due to its toxicity, and yet honored for the unsurpassed qualities of the bows, staves, and tools crafted from its wood. A plausible argument can be made that the English victory at Agincourt in 1415, made possible by the use of the yew-wood longbow, helped lay important foundations for modern European states; if the armies of Charles VI had been victorious, this report could well have been written in French. In English churchyards in particular, the yews stand as the most ancient living sentinels, recording in growth rings the slow accumulation of decades, generations, and millennia. Some U.K. specimens that continue to thrive are purported to be a venerable 3,000 years old. Although ancient peoples used the yew for medicines and tool- and weapon-making, it was not until the latter part of the 20th century that a compound in Taxus spp. became a household word: Taxol® entered the marketplace as one of the most effective treatment options for breast and ovarian cancers. Today, research continues to achieve the most effective drug delivery and combination drug therapy protocols, and to find new applications in the fight to conquer as many cancers as the taxanes can kill. Presently, the antitumour activity of the taxanes is being tested against head, neck, smallcell lung (Parekh and Simpkins 1997; Gautam and Koshkina 2003), and gastric (Roth and Ajani 2003; Yoshida et al. 2004) cancers. From a horticultural standpoint, much of the historic research on Taxus spp. has been centered on those attributes valuable to the landscape industry, a focus justified by the fact that cultivars of the hybrid T. ×

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media alone dominate the North American landscape as foundation plantings. Nonetheless, in recent years the marked increase in the volume of research detailing efforts to up-regulate taxane concentration in cell suspension culture of Taxus spp. is indicative of the determined effort to get more precious chemical into the pharmaceutical pipeline. Interestingly, little work has been done with the whole yew-plant system to achieve heightened cellular taxane content; it is in this area that plant scientists can push the present limits of knowledge for the sake of their own discipline, and perhaps for those who now or later will suffer in the clutches of one of humanity’s greatest scourges.

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7 The Genus Allium: A Developmental and Horticultural Analysis Rina Kamenetsky Department of Ornamental Horticulture The Volcani Center Bet Dagan, 50250, Israel Haim D. Rabinowitch Institute of Plant Science and Genetics in Agriculture The Hebrew University of Jerusalem Faculty of Agricultural, Food, and Environmental Quality Sciences Rehovot, 76100, Israel

I. II. III. IV.

INTRODUCTION TAXONOMY AND GEOGRAPHICAL DISTRIBUTION GENETIC RESOURCES AND POSSIBLE USE OF WILD ALLIUM SPECIES MORPHOLOGICAL STRUCTURES AND COMPARISONS BETWEEN BIOMORPHOLOGICAL GROUPS A. Bulbous Group B. Rhizomatous Group C. Edible Allium Species V. PLANT DEVELOPMENT A. Seed Germination B. Juvenile Period and Transition to Reproductive State C. Annual Developmental Programs 1. Bulbous Species 2. Rhizomatous Species 3. Edible Allium Crops

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VI. PROPAGATION A. Seed Propagation B. Vegetative Propagation VII. CHEMICAL COMPOSITION VIII. CONCLUDING REMARKS LITERATURE CITED

I. INTRODUCTION The large and heterogeneous genus Allium L. (Alliaceae, Takhtajan 1997) includes a great number of perennial plants with underground storage organs consisting of bulbs or rhizomes. Many plants of this genus are of a high economic significance, including vegetables [A. cepa (bulb onion and shallot), A. sativum (garlic), A. fistulosum (Japanese bunching onion), A. ampeloprasum (leek, kurrat, great-headed garlic, and pearl onion), A. schoenoprasum (chives), A. tuberosum (Chinese chives)], ornamentals [A. aflatunense, A. giganteum, A. karataviense], and numerous species with medicinal traits, e.g., onion, garlic, chives, A. victorialis, A. tricoccum, and more (Table 7.1). The main center of evolution of the genus stretches along the IranoTuranian bio-geographical region. Secondary centers of diversity are found in the Mediterranean basin and western North America (Hanelt 1990; Fritsch and Friesen 2002). From these centers, Allium plants have widely spread all over the northern hemisphere. A. dregeanum is the only exception; it grows wild in South Africa (De Wilde-Duyfjes 1976). Alliums are common from the dry subtropics to the boreal zone, and a few species grow wild even in the sub-arctic belt (Hanelt 1990). Adaptation to diverse habitats promoted different evolutionary routes with a wide range of developmental pathways. We hereby review the morphology and physiology of a number of Allium species, including vegetative growth, flowering, and summer or winter dormancy. Detailed knowledge of developmental features of diverse biomorphological types in conjunction with their geographical distribution and evolution should facilitate the use of a wider range of Allium species as edible, ornamental, and neutraceutical plants. Recent advances in Allium science were reviewed by several experts (Rabinowitch and Brewster 1990a,b; Brewster and Rabinowitch 1990; Rabinowitch and Currah 2002). However, the information on the biomorphological features and interactions between environment and life cycles of Allium species is scattered in the literature, and to the best of our knowledge a comprehensive overview of these processes has not been published in recent years.

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Table 7.1. List of Allium species cited in the text. Species names according to Gregory et al. (1998). Species name

Common Name

Origin

A. aflatunense B. Fedtsch. A. altaicum Pall. A. altissimum Regel A. ampeloprasum L.

Persian onion Altai onion

Central Asia Asia Central Asia Mediterranean

A. atroviolaceum Boiss. A. aschersonianum W. Barbey. A. caeruleum Pall. A. caespitosum Siev.ex Bong.et Mey A. canadense L. A. cepa L. A. cernuum Roth A. chinense G.Don A. cristophii Trautv. A. delicatulum Siev.ex Schult. et Schult fil. A. dictyoprasum C.A. Mey A. dregeanum Kunth A. galanthum Kar.et Kir A. giganteum Regel A. fibrosum Regel A. fistulosum L. A. jodanthum Vved. A. jesdianum Vved. A. hollandicum R.M. Fritsch A. incrustatum Vved. A. karataviense Regel A. komarovianum Vved. A. macleanii Baker A. macrostemon Bunge A. moly L. A. motor Kamelin and Levichev

Leek, kurrat, greatheaded garlic, and pearl onion

Blue Globe Onion

Canada garlic, meadow leek Bulb onion and Shallot Nodding Onion Rakkyo Star of Persia

Wildeui [Afrikaans] Giant allium Japanese bunching onion, Welsh onion

Chinese or Japanese garlic Golden garlic

Asia Mediterranean Asia Asia North America Unknown, possibly Asia North America Asia Asia Asia Asia South Africa Central Asia Central Asia Asia Unknown, possibly Asia Asia Asia Known only in culture Asia Asia Asia Asia Asia Mediterranean

(continues)

332 Table 7.1.

R. KAMENETSKY AND H. RABINOWITCH (continued)

Species name

Common Name

Origin

A. neapolitanum Cirillo

Naples onion, daffodil onion

Mediterranean

A. nutans L.

Asia

A. obliquum L.

Oblique onion

A. oschaninii O. Fedtsch.

French shallot

Asia Asia

A. oreophilum C. Mey

Central Asia

A. oreoprasum Schrenk

Asia

A. phanerantherum Boiss. et Hausskn.

Asia

A. platyspathum

Asia

A. proliferum

Egyptian tree onion

Possibly Central Asia

A. pskemense B. Fedtsch.

Pskem onion

Central Asia

A. rosenbachianum Regel A. ramosum L. (=A. odorum L.)

Central Asia Chinese chive

A. regelii Trautv. A. rothii Zucc

Asia Asia

Desert onion

A. roylei Stearn

Mediterranean Asia

A. rubens Schrad. ex Willd.

Asia

A. sativum L.

Garlic

A. scorodoprasum L.

Rocambole, Sand leek

Europe

A. schoenoprasum L.

Chive

Europe

A. schoenoprasoides Regel

Unknown, possibly Central Asia

Asia

A. senescens L.

Europe, Asia

A. sergii Vved.

Central Asia

A. sikkimense Baker A. sphaerocephalon L.

Himalaya Round-headed leek

Europe

A. stipitatum Regel

Asia

A. strictum Schrad.

Asia

A. subtilissimum Ledeb.

Asia

A. suworowii Regel

Asia

A. tel-avivense Eig.

Mediterranean

A. trachyscordum Vved. A. tricoccum Solander

Asia Ramps

North America

Long-rooted garlic

Asia

Ramsons, wood garlic

Europe

A. vavilovii M. Pop. et Vved. A. victorialis L.

Asia

A. unifolium Kell. A. ursinum L.

North America

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II. TAXONOMY AND GEOGRAPHICAL DISTRIBUTION The genus Allium includes more that 700 species that grow wild throughout the temperate, semi-arid, and arid regions of the Northern hemisphere (Hanelt et al. 1992; Stearn 1980). Their adaptation to the wide array of geo-climatic conditions resulted in a remarkable polymorphism (Hanelt et al. 1992), and therefore taxonomic analysis within the genus is rather complicated. Early monographers divided the genus into six subgroups (Don 1832; Regel 1875). In the second half of the 20th century, taxonomists revised the classification, and proposed a division of the genus into three subgenera and 12 sections (Stearn 1980), six subgenera and 30 sections (Kamelin 1973), or five subgenera and 16 sections (Hanelt 1990). Modern studies of morphology, anatomy, and cytology of Alliums in both living plants and herbarium specimens revealed even higher diversity within the taxon. Thus, a long-term research of the genus Allium in Gatersleben, Germany, yielded a new taxonomical categorization of Allium, named “Gatersleben infragereneric classification” (Hanelt et al. 1992), and the genus was subdivided into six subgenera and 57 sections and subsections. According to this classification, the four main subgenera are: 1. Allium: the largest subgenus. It consists of species with true ovoid or subglobose bulbs. Members of this subgenus are commonly found in the Mediterranean area, Asia Minor, and Central Asia, and include a number of cultivated species, e.g., A. sativum (garlic) and A. ampeloprasum (leek, kurrat, pearl onion, and great-headed garlic) and ornamentals, e.g., A. atroviolaceum and A. sphaerocephalon. 2. Rhizirideum: the rhizomatous species were grouped into one subgenus. They grow wild in all altitude belts of Europe, Asia, and North America, and include many economically important plants, e.g., A. cepa (onion, shallot), A. fistulosum (Japanese bunching onion), and A. schoenoprasum (chives). 3. Melanocrommyum: consists of species with true tunicated bulbs. The plants are spread from the Canary Islands to Kazakhstan, China, and Pakistan, with the centre of diversity in the eastern parts of the Mediterranean area, South-West and Central Asia. Most of the popular ornamental species belong to this subgenus, e.g., A. aflatunense, A. giganteum, and A. aschersonianum.

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4. Amerallium: members of this subgenus are spread over a wide range of ecological conditions, from hot dry deserts to the very humid dense forests in the Mediterranean basin and in North America. The species of this taxon differ markedly in morphology, some produce mainly rhizomes and poorly developed bulbs (e.g., A. cernuum), others form distinct bulbs and broad leaves similar to those common in the subgenus Melanocrommyum (e.g., A. moly), or very narrow leaves as in the subgenus Allium (e.g., A. unifolium). In addition to the above, the Gatersleben classification recognizes two small subgenera, Bromatorriza and Anguinum (Hanelt et al. 1992). Based on morphological studies, Cheremushkina (1992) proposed that rhizomes were ancestral and primitive traits of Allium species, whereas bulb formation represents an advanced evolutionary stage. However, the phylogenetic connections between the various Allium taxonomic groups remained unclear. Recent molecular studies (Havey 1992a,b; Bradeen et al. 1994; Maaß and Klaas 1995; Mes et al. 1997, 1999; Xingjin et al. 2000; van Raamsdonk et al. 2003) contributed to our understanding of the evolutionary processes and taxonomic relations within the genus, and thus Allium classification was revised to include 14 subgenera with about 60 taxonomic groups at subgeneric, sectional, and subsectional ranks (Fritsch 2001; Fritsch and Friesen 2002). Contrary to previous views (e.g., Hanelt et al. 1992; Cheremushkina 1992; Kamenetsky 1996), Fritsch and Friesen (2002), argue that rhizomatous Allium species do not belong to a single monophyletic group, and regard the presence of elongated rhizome and false bulbs as an advanced evolutionary stage, independently developed in several evolutionary lines. Concomitantly, bulbs are not considered the most advanced product of evolution, but one of the ancestral characteristics in Allium development (Fritsch 2001; Fritsch and Friesen 2002). They suggest therefore that Allium evolution proceeded in three separate lines, which may currently include distinct representatives of both ancient and advanced groups (Fig. 7.1). The most ancient line consists of only bulbous plants from subgenera Amerallium, Nectaroscordum, and Microscordum, which rarely produce a notable rhizome. The other two evolutionary lines contain both rhizomatous and bulbous taxa (Fig. 7.1).

7. ALLIUM: A DEVELOPMENTAL AND HORTICULTURAL ANALYSIS

Evolutionary lines of genus Allium

advanced

3

335

subg. Cepa (split tunics) (retic. tunics) (short spathe) (long spathe)

subg. Reticulatobulbosa

subg. Allium

subg. Rhizirideum s. str. subg. Cyathophora subg. Butomissa subg. Anguinum

2

subg. Melanocrommyum subg. Porphyroprasum subg. Caloscordum subg. Microscordum

1

(Old World) (New World)

subg. Amerallium

subg. Nectaroscordum

basal

Nothoscordum, Ipheion, Tulbaghia, etc. other genera

Fig. 7.1.

Phylogenetic classification of Alliums (Source: Fritsch 2001, with permission).

III. GENETIC RESOURCES AND POSSIBLE USE OF WILD ALLIUM SPECIES Domestication of wild Alliums started millennia ago, and was followed by a wide distribution of the flavoring condiments all over Asia and Europe (Hanelt 1990; Engeland 1991). Similar to many other plant crops, being farther away from the center of evolution significantly reduced the possibilities of genes introgressions from both parental species and close relatives. Additionally, since the initial domestication, many of the immediate ancestors have either been lost or changed beyond recognition. Genetic shifts and drastic, unbalanced selection pressure by growers and breeders resulted in the loss of many traits important for modern agriculture, and therefore genes of potentially useful characteristics were lost or not readily available for crop improvement. Modern biology provides tools for introgression of genes (Eady 2002; Sher 1980; Zheng et al. 2004) from one species to another. Thus, close and

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distant relatives are of paramount importance for crop improvement and introduction of new crops (Jones and Mann 1963; Astley et al. 1982; Astley 1990; Currah et al. 1984; De Ponti and Inggamer 1984; Schweisguth 1984; Van der Meer 1984; Peters et al. 1984; Dowker 1990; Rabinowitch 1997; Havey 1999; Rouamba et al. 2001; Kik 2002; García Lampasona et al. 2003) and should be collected, evaluated, and conserved. The general awareness of genetic resources has risen ever since N.I. Vavilov (1926) discovered the geographical centers of genetic diversity. However, only a few and irregular collection missions and conservation activities of Allium plants took place until the early 1970s. Since then, collection of seeds and storage organs and conservation activities of land races and wild relatives of the edible cultivated species were initiated by various agencies, gene-banks and researches (Astley 1990, 1994; Etoh and Simon 2002; Maggioni 2004). The main seed collections are located in Wellesbourne, UK; Wageningen, The Netherlands; Fort Collins, Colorado, USA; St. Petersburg, Russia; and Gatersleben, Germany. The main field gene banks were established in Rehovot and Bet Dagan, Israel; Olomouc, Czech Republic; Almaty, Kazakhstan; Skierniewice, Poland; Gatersleben, Germany; and Pullman, Washington, USA. Lesser efforts were invested in systematic collection and preservation of non-edible wild Allium species, including sources for novel ornamentals, and for plants rich in natural compounds with therapeutic qualities. Moreover, only small efforts were invested in evaluating the conserved germplasm (Pooler and Simon 1993; Baitulin et al. 2000; Van Raamsdonk et al. 2003; Kamenetsky et al. 2004b, 2005). When such efforts were made, the benefits have immediately become evident. One good example is the case of A. roylei, a member of the section Cepa, from the Himalayas. A single specimen was collected in the 1950s, conserved for a number of years, and evaluated only in the 1980s (Kofoet at al. 1990; Kofoet and Zinkernagel 1990). It was then found to be the only source for complete resistance to downy mildew (Perenospora destructor) and a good source for resistance to Botrytis diseases (Kofoet et al. 1990; Kofoet and Zinkernagel 1990; van der Meer and de Vries 1990; de Vries et al. 1992a,b,c). The two fungi infect bulb onions and cause severe economic losses due to reduced yields and quality (Maude 1990). Offspring of crosses between this individual plant and bulb onion are being used in a number of breeding programs in the Netherlands, USA, and Israel. In addition to living collections of vegetatively propagated Alliums, in vitro conservation offers an alternative means of conserving valuable germplasm. It can also be used to revive small collections and maintain the material under disease-free conditions. Numerous works were pub-

7. ALLIUM: A DEVELOPMENTAL AND HORTICULTURAL ANALYSIS

337

lished on the in vitro production of planting materials and conservation of Alliums (e.g., Novak 1990; Nagakubo et al. 1993; Keller et al. 1995; Keller and Lesemann 1997; Pateña et al. 1998; Senula et al. 2000), but these techniques are still not adopted by curators of Allium field collections. Cryopreservation for long-term maintenance of various tissues and organs was also developed (Keller 2002), but the costs of such operations limited their use to a small number of clones and prohibit its wide application in the conservation of vegetatively propagated Alliums. Centers of diversity of crops and their wild relatives are restricted to specific geographical regions, and have become priority areas for collections and preservation. The diversity of Alliums in the Irano-Turanian floristic region, and especially Central Asia, is uniquely rich (Khassanov 1997; Fritsch and Friesen 2002). About 300 species of the genus grow wild in this region, and over a hundred of them are endemic to the area (Vvedensky 1968). This genepool is of highest importance for introduction of useful genes to the current cultivated Alliums, as well as for immediate, intermediate, and long-term domestication of new cultivated crops. Domestication of species with ornamental potential depends on the acquaintance with their physiological responses to the environment; new species can be domesticated as condiment vegetables and spices, and many species and local landraces can serve as resources for quality traits, such as dry matter content, pungency, and sweetness, colors, yield, resistance to pests and/or to environmental stresses, and for raw materials for the pharmaceutical and neutraceutical industries (Kamenetsky et al. 1999; Kik et al. 2001; Keusgen 2002). Initial evaluation of about 40 Allium species (ca. 60 clones) preserved in our collection (Bet Dagan and Rehovot, Israel) was carried out in 1997–1998. Bulbs stored under ambient conditions were analyzed for dry matter and pyruvate content. A number of species exhibited a great homogeneity in dry matter content. Hence, A. ampeloprasum 43.9–46.0%, A. fibrosum 42.0–43.6%, A. incrustatum 39.7–40.0%, A. regelii 34.9–35.5% and more, whereas dry matter content within A. longicuspis (=A. sativum) ranged between 46.8 and 62.8%, and similarly a range of 46.4 to 62.8% was measured in A. schoenoprasoides. Coefficient of variation was less than 15% for each clone. Similar variation was recorded within and between the assayed species for pyruvic acid. For both traits, some wild species exhibited levels considerably higher than those measured in the domesticated species. Therefore, in addition to being a unique source for introduction of new crops, the rich genepool within the genus may well be considered an invaluable reservoir for the improvement and introduction of new economic traits in Alliums (Kamenetsky et al. 1999).

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At present, many wild Allium species with characteristic onion- or garlic-like odor and flavor are used as spices and green vegetables by different communities, in addition to the known crops. These include Chinese or Japanese garlic A. macrostemon, Naples garlic A. neapolitanum, Ramsons A. ursinum, long-rooted garlic A. victorialis, Canada garlic A. canadense, Ramp A. tricoccum, Altai onion A. altaicum (Table 7.1). Domestication of wild edible Allium species is still continuing (Fritsch and Friesen 2002). For instance, A. komarovianum is cultivated commercially in North Korea, A. canadense in Cuba (Hanelt 2001), A. tricoccum in Canada and the USA (Davis and Greenfield 2002), and A. ramosum in East and Central Asia (Fritsch and Friesen 2002). Others are collected from natural populations for commercial or semi-commercial purposes (e.g., A. pskemense, A. obliquum, A. altaicum, A. nutans). Wild Alliums are also used in folk medicine, e.g., A. ramosum is prescribed for a heart condition, as a cure for snakes’, insects’ and dogs’ bites, and for accelerating blood clotting. A. ursinum and A. victorialis are used as an antimicrobial remedy for stomach infections (Sklyarevsky 1975). During and after the Second World War, wild Allium species were studied in the former USSR in order to identify new vegetables and sources of vitamins (Zizina 1955; Baitulin et al. 1986; Khassanov and Umarov 1989). Locally grown wild Allium species from Central Asia were divided into the following five groups: (1) edible species, e.g., A. altaicum, A. vavilovii, A. caesium, A. odorum, A. galanthum, A. pskemense, A. nutans, A. obliquum; (2) species with strong antimicrobial activity and high vitamin content, e.g., A. altissimum, A. altaicum,, A. schoenoprasum, A. ursinum, A. nutans; (3) melliferous species rich in nectar and bee-bread, e.g., A. fistulosum, A. altaicum, A. obliquum; (4) species containing natural dyes and glues, e.g., A. aflatunense, A. suworowii, A. altissimum, A. karataviense; (5) ornamental species with colorful inflorescences and a long period of flowering, e.g., A. giganteum, A. aflatunense, A. odorum, and A. karataviense (Zizina 1955). Recent collection missions to Central Asia (Khassanov and Umarov 1989; Kamenetsky et al. 2004b) expanded ethnobotanical knowledge about use of indigenous Alliums, and consequently 18 wild Allium species were listed as condiments and for medicinal purposes (Table 7.2). In rural areas, plants of subgenus Melanocrommyum are collected for the orange juice extracts from bulbs and stems; wild Alliums, such as A. motor, A. caesium, and A. pskemense are consumed in the winter as sources of vitamins and for their medicinal properties, and flowers of A. jodanthum stored in alcohol are used as an antiseptic.

Table 7.2. Ethnobotanical data on wild Alliums used by local population in Central Asia. Data were collected in 2001–2004, during collection mission in Uzbekistan and neighboring countries (Kamenetsky et al. 2004b). Species names according to Gregory et al. (1998). Species name

Purpose of use

Plant parts used

A. jodanthum Vved. A. motor Kamelin and Levichev A. pskemense B. Fedtsch. A. filidens Regel A. severtztovioides R.M. Fritsch A. karataviense Regel A. suworowii Regel A. stipitatum Regel A. oschaninii O. Fedtsch. A. longicuspis Regel A. caesium Schrenk A. brevidentiforme Vved. A. komarowii Lipsky A. rosenorum R.M. Fritsch A. crystallinum Vved. A. majus Vved. A. giganteum Regel A. praemixtum Vved.

Stored in alcohol as antiseptic In food in April–May after winter period as tonic In food against stomach problems Against toothache and mumps In food against stomachache Added in food as tonic Added in food as tonic Used marinated as tonic Used as common onion A. cepa Used as common garlic Used as common garlic Used as common garlic Used in food against heartache Used in food as tonic Used as common garlic Used in food as tonic Used in food as tonic Used as common onion A. cepa

Leaves and stems in unfolded bud Leaves with orange juice Bulbs, leaves and stems with milky juice Leaves and bulbs (garlic-taste and smell) Leaves (without orange juice) Leaves and bulbs Bulbs Bulbs Bulbs, leaves and stems Bulbs, leaves and stems Bulbs and leaves Bulbs and leaves Bulbs Leaves Bulbs and leaves Bulbs with orange juice Bulbs with orange juice Bulbs, leaves and stems

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IV. MORPHOLOGICAL STRUCTURES AND COMPARISONS BETWEEN BIOMORPHOLOGICAL GROUPS Allium species display a remarkable polymorphism, and consequently their taxonomic analysis is rather complicated. Moreover, the structure of the generative organs, usually used by taxonomists for Allium classification, cannot serve as a single and sufficient criterion of the taxon identity because of the lability of the Allium reproductive system. The phylogenetic system of the genus could therefore be completed through biomorphological analysis and identification of connections between plant development traits and environmental conditions in their natural habitats (Khokhryakov 1975). In addition to Allium taxonomy, larger categorization of “biomorphological types” can be used to understand correlations between annual developmental programs of various species with their geographical distribution and environment (Pastor and Valdes 1985; Hanelt et al. 1992; Kamenetsky 1992, 1996; Kamenetsky and Fritsch 2002; Kamenetsky and Rabinowitch 2002). Biomorphological types incorporate different Allium taxa and serve for both theoretical knowledge and practical implications, such as use in horticulture and further domestication and utilization of valuable wild Allium species. The environment prevailing in the geographical and ecological niches and the nature of the plants’ habitats are important parameters for the biomorphological typing of Allium species (Kamenetsky 1996). Life form classification (Raunkiaer 1934) reveals that Allium species belong to the geophyte and hemicriptophyte group and that the metamorphosis of their underground shoots is highly variable. Evolution of Alliums and their diversification were strongly affected by the ecological conditions in their natural habitats of mainly open terrain, sunny and rather dry regions. Some species, however, adapted to different ecological niches, including forests (e.g., A. scorodoprasum, A. ursinum, A. victorialis), alpine grasslands of the Himalaya (e.g., A. sikkimense), and Central Asian high mountains (e.g., A. oreophilum). In the following, we discuss the morphological and physiological traits typical of the three main biomorphological types: bulbous, rhizomatous, and domesticated edible species. The long history of breeding and cultivation of edible species resulted in a partial or complete change of the original morphological and physiological traits, hence, their separated biomorphological grouping. The three groups are distinguished by the morphology of their root system, presence and development of the storage organ(s), type of seed germination, vegetative development, branching, annual life cycle, dormancy, and florogenesis.

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341

A. Bulbous Group Members of this group inhabit mainly steppes, semi-desert and desert areas (Kollmann 1986; Kamenetsky 1996; Hanelt et al. 1992, Fig. 7.2). The bulbs consist of concentric storage scales located on top of a compressed flattened stem disc (basal plate) (De Mason 1990; Brewster 1994; Kamenetsky 1996). When bulbing is complete, the plants usually enter a dormancy period that lasts a few weeks to a number of months, followed by sprouting either in the autumn or in the spring (Brewster 1990; Pistrick 1992). Partially or completely subterranean bulbs enable the plants to survive the harsh winter and summer environmental conditions prevailing in the center of evolution. Depending on species, the juvenile phase lasts 1–5 years, and post-juvenile plants flower in the spring (Kamenetsky 1992, 1996). These plant species are clustered into two distinct subgroups: 1. Bulbs consist of a condensed basal plate with a number of true and false scales (thick leaf sheaths) (Fig. 7.3); the annual root system is diffused or semi-diffused, and branches only to the first order. Members of this subgroup include: A. ampeloprasum, A. caeruleum, A. delicatulum, A. dictyoprasum, A. phanerantherum, and more.

Fig. 7.2. Scheme of geographical distribution of bulbous Allium species, based on floristic literature from several different regions (De Wilde-Duyfjes 1976; Friesen 1987; Goloskokov 1984; Gregory and al. 1998; Hanelt 1985, 1990; Kollmann 1986; Pavlov and Polyakov 1958; Vvedensky 1968; Wendelbo 1971; Xu et al. 1990).

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Next year

A

Present year B

Last year C

cover leaf (tunic)

vegetative apex

storage leaf (scale)

inflorescence

foliage leaf Fig. 7.3. Morphological structure of underground organs in A. caesium, subgenus Allium. Lateral shoots may develop secondary inflorescences. (A) Longitude section of postjuvenile bulb, (B) Cross-section of post-juvenile bulb, (C) Diagrammatic representation of morphological structure.

2. Bulbs are formed only of basal plate and fleshy, thick specialized scales (Fig. 7.4). At the end of the growing season, leaf sheaths dry out and form the enveloping dry skins, which do not contain storage materials. The root system is diffused and consists of numerous annual, non-branching roots. Roots are frequently ephemeroidal and allow fast and efficient water absorption during

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343

Next year Lateral bud

Renewal bud

A

Present year

B Last year

C

cover leaf (tunic)

vegetative apex

storage leaf (scale)

inflorescence

foliage leaf Fig. 7.4. Morphological structure of underground organs in A. altissimum, subgenus Melanocrommyum. (A) Longitude section of post-juvenile bulb, (B) Cross-section of postjuvenile bulb, (C) Diagrammatic representation of morphological structure.

the short vegetation period common in the desert regions (Baitulin et al. 1986; Kamenetsky 1996). Most species of this subgroup belong to the subgenus Melanocrommyum, which has undergone an evolutionary process under the arid conditions of Central Asia and the Middle East (Fritsch 2001). ‘Melanoallium’ type (Pastor and Valdes 1985) or ‘Extreme Geoephemeroid’ (Kamenetsky 1992) are also used in reference to this subgroup, which includes plant species such as A. altissimum, A. karataviense, A. oreophilum, A. rothii, A. sergii, A. tel-avivense, and more.

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B. Rhizomatous Group Allium species with rhizomatous underground organs are common mainly in the temperate zone, mostly in mesoxerophytic habitats, such as meadows, forests, and the high mountains of Siberia; northern Europe and Canada; and also in arid areas of the sub-alpine and alpine mountainous zones (Hanelt et al. 1992; Fritsch and Friesen 2002, Fig. 7.5). The plants produce false bulbs made of leaf sheaths of different thickness, and underground rhizomes that function primarily as storage organs (Fig. 7.6). The fleshy rhizomes consist of successive concrescence of the basal plates developing over several seasons, and grow in a horizontal, oblique, or vertical direction (Cheremushkina 1985, 1992; Baitulin et al. 1986; Kamenetsky 1992, 1996). Plant species of the rhizomatous group are clustered in three distinct subgroups: 1. Hemicryptophytes with horizontal rhizomes and false bulbs, composed of slightly thickened leaf sheaths, as in A. senescens, A. nutans, A. odorum, and A. subtilissimum. The root system is perennial, adventitious, and generally has a second order branch-

Fig. 7.5. Scheme of geographical distribution of rhizomatous Allium species, based on floristic literature from several different regions (Friesen 1987; Goloskokov 1984; Gregory and al. 1998; Hanelt 1985, 1990; Kollmann 1986; Pavlov and Polyakov 1958; Vvedensky 1968; Wendelbo 1971; Xu et al. 1990).

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345

Next year

A Present year

B

Last years

C

rhizome

vegetative apex

foliage leaf

inflorescence

Fig. 7.6. Morphological structure of underground organs in A. nutans subgenus Rhizerideum. (A) Longitude section of post-juvenile bulb, (B) Cross-section of post-juvenile bulb, (C) Diagrammatic representation of morphological structure.

ing. Some species (e.g., the endemic species A. caespitosum from Kazakhstan and China) underwent a very strong specialization to the point that it resembles sedge (Carex) rather than a bulbous plant. It produces long twine-like and highly branched rhizomes that anchor the plant into the shifting sands. The plants produce

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long-branched roots and thin shoots composed of two or three leaves that develop in the rhizome’s nodes. 2. Geophytes with oblique and oblique-vertical rhizomes. The root system is usually perennial, branched to the first order, and the false bulbs are enveloped by numerous tunics, the remnants of leaf sheaths from the previous years’ vegetation. Members of this subgroup include A. oreoprasum, A. rubens, A. strictum, and more. 3. The intermediate type between rhizomatous and bulbous species possesses short vertical rhizomes, an annual root system with first order branching, and large false bulbs. The latter consist of true scales and thick leaf sheaths. This large subgroup includes many wild relatives of the bulb onion (A. cepa), including A. altaicum, A. galanthum, and A. pskemense. C. Edible Allium Species Domestication of Allium spp. started over 10 millennia ago. Since then growers and breeders have selected plants with specific economically important traits, thus significantly affecting the morphology and physiology of these species. For example, onion and shallot (A. cepa) are close relatives of the rhizomatous species A. vavilovii and A. oschaninii of the subgenus Cepa (Hanelt 1990; Havey 1992b; Fritsch et al. 2001; Van Raamsdonk et al. 2003). However, the morphology of A. cepa resembles that of a true bulbous plant: the bulb is enveloped by a few skins and consists of a condensed basal plate with a number of true and false scales. (For a detailed description, see: Brewster 1990, 1994; De Mason 1990; Krontal et al. 1998.) Selection by breeders of leek and kurrat from the bulbous A. ampeloprasum resulted in the development of storage organs made of a successive concrescence of leaf sheaths, which form long fleshy false stems (Van der Meer and Hanelt 1990; De Clercq and Van Bockstaele 2002). Originally a bulbous species, garlic bulbs consist of a number of lateral buds transformed into storage organs (cloves). The clustered bulb, enveloped by layers of dry thick leaf bases, consists of one or more whorls of cloves; each one is made of a vegetative bud embedded inside a thick storage leaf enveloped by an external dry, protective cylindrical leaf sheath (Mann 1952; De Mason 1990). The biennial rakkyo (A. chinense), common in the central eastern region of China, have rhizomes and false bulbs formed by leaf sheaths. During growth, plants subdivide continuously and form a dense clump of shoots (Toyama and Wakamiya 1990).

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V. PLANT DEVELOPMENT A. Seed Germination On maturation, seed of most Alliums become dormant, and their germination depends on environmental factors, mainly moisture and temperature (Dalezkaya and Nikiforova 1984; Specht and Keller 1997; Kamenetsky and Gutterman 2000). For instance, optimum conditions for seed germination of A. rothii (subgenus Melanocrommyum, a native plant in the Negev Desert, Israel, where winter is mild), are 14–28 days under wet conditions at 15°C (Gutterman et al. 1995). In comparison, seed germination of A. rosenbachianum (= A. rosenorum), which grows wild in the continental climate of Central Asia, occurs at 5–25°C, but cotyledon elongation is faster at 20–25°C than at 5°C (Aoba 1968). Epigeal development is common in Allium species, namely emergence of the cotyledon is followed by growth of the embryonic rootlet, and both ends of the crooked upper part of the cotyledon (loop; knee) elongate simultaneously, thus heading the way up. When exposed to light, the cotyledon turns green, and the distal part straightens up (Jones and Mann 1963; De Mason 1990). A few species, however, exhibit hypogeal germination, especially those adapted to humid conditions (e.g., A. ursinum and A. victorialis) (Druselmann 1992). Based on seedlings’ morphology, Allium species were classified into two distinct morphological groups: 1. The dominant growth habit includes the formation of the first foliage leaf within the cotyledonal sheath, and the following leaves emerge from within their predecessors through a side pore (De Mason 1990). Juvenile plants are thus made of a number of opposite cylindrical leaves connected at the basal plate, and a number of adventitious roots (De Mason 1990; Druselmann 1992; Brewster 1994). This mode was named Allium cepa-type (Druselmann 1992), and is common in the bulb onion and in many other Allium species from a number of bulbous and rhizomatous subgenera. 2. The specific Allium karataviense-type is restricted to the members of the bulbous subgenus Melanocrommyum. Upon germination, the epigeal part of the cotyledon extends considerably, reaching more than 10 cm in length. It remains green for several weeks and serves as the sole assimilating organ throughout the first growing season. During this period, water and nutrient supply are absorbed by the primary root solely, since neither adventitious nor lateral roots are formed (Druselmann 1992). At the end of the growing season,

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a single storage leaf develops at the underground growing point, and forms a small subterranean bulb (Glimcher 1951; Kamenetsky 1994a). The first true leaf forms in the second growing season. During the 3–5 years of the juvenile period, leaf number and bulb size increase. The juvenile plant is monopodial and forms only adventitious roots (Kamenetsky 1994a) B. Juvenile Period and Transition to Reproductive State When propagated from seed, all Allium plants undergo an obligatory time-limited juvenile phase before they can respond to environmental induction and bloom. This period ranges from a few months (e.g., bulb onion: Rabinowitch 1985, 1990a; Brewster 1994; chives: Poulsen 1990; Japanese bunching onion: Inden and Asahira 1990; leek: Van der Meer and Hanelt 1990; De Clercq and Van Bockstaele 2002; shallot: Messiaen et al. 1993; Krontal et al. 1998), to 5–6 years (e.g., A. giganteum and A. karataviense: De Hertogh and Zimmer 1993, A. rothii: Kamenetsky 1994a), and ends when the plant reaches a certain physiological age and/or a critical mass. Then, the plant is ready to shift to the reproductive stage (Brewster 1990, 1994). The length of the juvenile phase depends on the genetic make-up of the plant and on the specific environmental conditions. Both regulate and affect the rate of photosynthesis, accumulation of assimilates, and the amount of stored reserves available for successful blooming and seed production. During the vegetative stage, the shoot apical meristem (SAM) initiates leaf primordia only. At the post-juvenile phase, and upon exposure to appropriate environmental conditions, SAM becomes generative. At this stage, the plant changes from the characteristic monopodial development to sympodial growth habit. Thereafter, Allium plants flower and produce renewal bulbs every year (Kamenetsky and Fritsch 2002). Horticulturists, and especially floriculturalists, consider bulb circumference a reliable measure of the bulb’s readiness to flower. Namely, the plants have reached the required critical mass and the appropriate physiological age, which enables them to support the development of the flower and seeds upon induction. The minimum circumference, however, varies from a few mm to tens of cm with species and cultivar, as in the following examples: A. caeruleum, A. neapolitanum, A. unifolium—3 to 5 cm; A. aflatunense (=A. hollandicum), A. cristophii, A. karataviense—12 to 14 cm; and A. giganteum—20 to 22 cm (De Hertogh and Zimmer 1993). In general, the time required from seed emergence to the post-juvenile phase correlates with bulb size. Ornamental Alliums

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with small bulbs may bloom already at the end of the second growing season after emergence (e.g., A. neapolitanum, A. caeruleum; Kamenetsky and Fritsch 2002), whereas plants with large bulbs (e.g., members of the subgenus Melanocrommyum, such as A. rothii, A. aflatunense, A. giganteum) require 3–5 years of growth to reach the same state of development (De Hertogh and Zimmer 1993; Kamenetsky 1994a). However, in A. aschersonianum (subgenus Melanocrommyum) the transition of apical meristem from vegetative to reproductive state was observed in the second year of development from seeds, but the insufficient critical mass could not support the development of the inflorescence. Hence, young floral buds abort inside the bulb. Normal flowering occurs in 3rd or 4th years in more developed plants (Hovav 2001). Seedlings of wild rhizomatous species (e.g., A. senescens) branch after emergence to form a primary clump. Growth and branching continue through one to five years, until the vegetative shoots reach the required physiological age (or critical mass) for blooming. At that point, all vegetative shoots become reproductive simultaneously and form a cluster of flower stalks (Cheremushkina 1985). In edible Allium crops, meristem transition to the reproductive stage occurs at the first or second year of development from seed. The number of leaves and leaf primordia serves as a reliable, time independent measure of plant physiological state and readiness to flower (Table 7.3).

Table 7.3 Minimum physiological age required for transition from vegetative to reproductive state in a number of edible alliaceous crops.

Allium spp.

Crop

A. cepa

Bulb onion

A. cepa Aggregatum group A. fistulosum

Shallot

A. sativum

Japanese bunching onion Garlic

A. ampeloprasum

Leek

Minimum leaf number prior to transition to reproductive stage

Source

10–14 (3–4 in extreme cases) 6–7

Rabinowitch 1985; 1990 Krontal et al. 1998

10–14

Inden and Asahira 1990

6–30, genotype dependent 6–7

E. Shemesh, Israel, pers. commun., 2003 Van der Meer and Hanelt 1990; De Clercq and Van Bockstaele 2002

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C. Annual Developmental Programs Allium species vary significantly in their annual life cycle and morphogenetic processes, as in the following examples. 1. Bulbous Species. During bulbing, and following flowering and seed maturation, bulbous species lose their roots and the aboveground parts. On maturation, the renewal bulbs enter a dormancy period,1 during which they maintain slow life activities, including low respiration rate, and both slow cell division and shoot elongation (Abdalla and Mann 1963; Komochi 1990). Dormancy period ranges from a few weeks to a number of months, and allows survival through seasons with unfavourable environmental conditions. During this period there is a gradual breakdown of endogenous growth retardants and changes in the profile of growth promoting substances (Thomas 1969; Isenberg and Thomas 1970; Isenberg et al. 1974, 1987). Sprouting occurs when the concentration of growth retardants is reduced below a certain critical level and the internal hormonal balance favours re-growth. In post-juvenile bulbous Alliums, the transition from vegetative to reproductive state and the following florogenesis occur either after growth renewal, during the active growth phase, at the end of the growth period, or during dormancy (Kamenetsky and Rabinowitch 2002). Bulbous Species of Mediterranean Origin. Most plants of this group belong to the subgenera Amerallium and Nectaroscordum, and some are members of the subgenus Allium. They have evolved in the Mediterranean basin and in California, where summer is hot and dry, but winter conditions are mild and favourable for plant growth and development (McNeal and Ownbey 1973; Hanelt 1990). Therefore, sprouting begins in the fall, leaf development continues through the winter and spring, floral scape elongation occurs in the spring, and summer dormancy is common (Kamenetsky 1994a; Kamenetsky et al. 2000; Kamenetsky and Rabinowitch 2002) (Fig. 7.7). In these regions, the drop in temperatures in the autumn is followed by a transition of the shoot apical meristem (SAM) from the vegetative to the reproductive state (Fig. 7.7). Optimum temperature for floral initiation in members of the subgenus Amerallium (e.g., A. unifolium, A. neapolitanum, and A. roseum) ranges between 9 and 17°C (Leeuwen and 1

Dormancy is defined as a complex and dynamic physiological, morphological, and biochemical state of the plant, during which there are no apparent external morphological changes. This state is also referred in literature as rest, quiescence, or intrabulb developmental period (Rees 1972; Halevy 1990; Le Nard and De Hertogh 1993; Kamenetsky 1996).

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Winter

Leaf growth

Reproductive SAM

Differentiated inflorescence

Fall

Spring Flowering

Vegetative SAM Dormancy

Summer Fig. 7.7. Annual life cycle of A. triquetrum, subgenus Amerallium, which originated from South France. A transition of the shoot apical meristem (SAM) from the vegetative to the reproductive state occurs with temperature decrease in the autumn, and inflorescences is formed during the active growth. Summer dormancy is initiated after flowering and seed formation.

Weijden 1994; Maeda et al. 1994; Kodaira et al. 1996). Scape emergence and blooming are promoted by low storage temperatures of 2 to 9°C; however, exposure of plants to these conditions resulted in a lower percentage of flowering and in shorter scapes (Leeuwen and Weijden 1994; Maeda et al. 1994; Kodaira et al. 1991a,b; 1996). Long photoperiod promotes scape elongation and flowering of A. moly and A. roseum (De Hertogh and Zimmer 1993; Maeda et al. 1994). Species of subgenus Allium form inflorescences during the active growth and development stage, following the differentiation of several leaf primordia (Kamenetsky and Rabinowitch 2002). Autumn storage at 2, 5, or 9°C resulted in both reduced percentage of flowering plants and in inferior flower quality (e.g., A. caeruleum: Leeuwen and Weijden

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1994), whereas intermediate temperatures of 17 to 20°C during growth and development promote blooming (Berghoef and Zevenbergen 1992; Leeuwen and Weijden 1994). Long photoperiod is essential for flower initiation in A. sphaerocephalon (Berghoef and Zevenbergen 1992) and accelerates floral development of A. ampeloprasum (De Hertogh and Zimmer 1993). Bulbous Species of the Irano-Turanian Origin. Most plant species of this group belong to the subgenus Melanocrommyum. They inhabit regions where winters are cold and summers are hot and dry, such as Central Asia, Iran, and Afghanistan. Avoidance of the harsh conditions is achieved by reduced above-ground growth rate in both winter and summer (Pistrick 1992), and by focusing the main developmental efforts in the fall and spring. Spring blooming of these bulbous plants is followed by seed production (Fig. 7.8). High air and soil temperatures and low moisture cause root and foliage death, and termination of the above-ground development. Concomitantly, intensive morphogenetic processes proceed inside the bulbs throughout dormancy. The duration of this period of intrabulb development depends on the genetic makeup of the plants and the degree of adaptation to ambient conditions (Kamenetsky 1996). Thus, A. karataviense from Central Asian semi-deserts and A. rothii from the Israeli desert remain dormant for four and six months, respectively (Kamenetsky 1996). Dormancy ends in the fall, following the drop in temperatures, and thereafter sprouting and elongation of both root and shoot commence. Growth rate and development, however, are slow in the winter, and increases again in the spring (Fig. 7.8). In the spring, leaf primordia are initiated in the renewal bulbs concomitantly with the flowering of the mother plant. Following differentiation of five to seven leaf primordia, the apical meristem either undergoes transition from vegetative to reproductive state already at the end of the growing period, immediately after the cessation of leaf initiation (e.g., A. aflatunense (=A. hollandicum): Zemah et al. 2001), or becomes dormant for 3–10 weeks before the transition takes place (e.g., A. altissimum and A. karataviense: Kamenetsky and Japarova 1997). In both cases, leaf initiation at the apical meristem ceases, and the flat SAM swells upwards and forms a dome shape with a concomitant development of a spathe at the apex periphery (for a detailed description, see: Kamenetsky and Rabinowitch 2002). The microscopic floral primordia in the transitioned apex become visible, while the bulb is dormant (Kamenetsky 1996; Kamenetsky and Japarova 1997). At the same time,

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Winter

Leaf growth Flowering

Fall

Differentiated inflorescence

Vegetative SAM

Spring

Reproductive SAM

Dormancy

Summer Fig. 7.8. Annual life cycle of A. rothii, subgenus Melanocrommyum, which originated from the Negev desert in Israel. Flowering and seed production occur in early spring and are following by termination of the aboveground development. Dormancy period is prolonged and ends in the fall, when sprouting and root elongation commence. Leaf primordia are initiated in the renewal bulbs concomitantly with the flowering of the mother plant. Apical meristem undergoes transition from vegetative to reproductive state during summer dormancy stage.

the reserves stored in the bulb scales are used to support cell division, differentiation, cell growth, and floral stalk elongation (Aoba 1970; Baitulin et al. 1986). Floral initiation and differentiation of the bulbous species of the IranoTuranian origin proceed inside the bulbs through the hot summer. Similar to other geophytes from the Irano-Turanian region (e.g., Tulipa: Le Nard and De Hertogh 1993), a long pre-planting exposure of the bulbs to low temperatures is required following intrabulb florogenesis for the initiation of renewal bud(s), scape elongation, and normal flowering (Dosser 1980; De Hertogh and Zimmer 1993; Zemah et al. 2001). In

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nature, these cold requirements are satisfied by winter conditions. Cultivated species of this group, however, require six to 12 weeks of chilling to induce scape elongation and achieve proper bloom (De Hertogh and Zimmer 1993; Zemah et al. 2001; Kamenetsky and Fritsch 2002). When active growth is resumed, moderate temperatures (17–23°C and 9–15°C day and night, respectively) are required for proper continuation and conclusion of the flowering processes (Dosser 1980; De Hertogh and Zimmer 1993; Zemah et al. 2001). In this group, photoperiod has no effect on scape elongation, as demonstrated in A. aflatunense (=A. hollandicum) (Zemah et al. 2001). Melanocrommyum species, native to Israel (A. rothii, A. aschersonianum, and A. nigrum), are adapted to the harsh conditions of the long and hot summer. During the 12- to 15-week exposure to high temperatures, SAM remains inactive and turns into the generative phase only in October–November, when temperatures drop. Flowering occurs after the mild Mediterranean winter in February–March, and low temperatures are not required. The length of the dormancy period can be modulated by summer storage temperatures. When stored at 20–25°C, dormancy is drastically shortened, floral initiation occurs already in August, and plants are ready to flower in November–December, two to three months earlier compared to plants stored at higher temperatures prior to planting (Kamenetsky et al. 2000; Gilad et al. 2001). 2. Rhizomatous Species. Most rhizomatous Allium species remain active, produce new leaves, and form renewal bulbs all year round (Cheremushkina 1992; Pistrick 1992; Kamenetsky 1996). The winter slows growth, and development accelerates in the spring by the favourable environmental conditions (Fig. 7.9). SAM remains vegetative almost year round, and becomes reproductive in the spring in response to the long photoperiod. Flower differentiation and stalk elongation are fast, and flowering occurs in the summer. Hence, A. nutans and A. senescense, two typical species of this group, form 20–22 leaves annually (Baitulin et al. 1986; Kamenetsky et al. 2004c), and flower in the summer, between June and August. Some members of the rhizomatous group undergo two to three flowering cycles per summer, and form one to several complete sets of leaves and a few prophylls per flower scape per cycle (Cheremushkina 1985; Kruse 1992). Only a little experimental data is available on the effect of environment on florogenesis of rhizomatous species from the subgenus Rhizirideum. Flower initiation and development in A. nutans, A. senescens, and A. tuberosum does not require strong cold induction, and the tran-

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Winter Slow leaf growth under snow

Vegetative SAM

Fall

Axillary bud and new leaf formation

Spring

Reproductive SAM

Differentiated inflorescence

Summer Fig. 7.9. Annual life cycle of A. nutans, subgenus Rhizirideum, which originated from Siberia. The plant remains active and produces new leaves all year round. The winter slows down leaf growth, which accelerates again in the spring due to the favourable environmental conditions. SAM remains vegetative almost year round, and becomes reproductive in the spring in response to the long photoperiod. Flower differentiation and stalk elongation are fast, and flowering occurs in the summer.

sition of the apical meristem from vegetative to reproductive state is rather fast. SAM differentiation begins late in the spring, and is followed by floral stalk elongation and summer flowering (Cheremushkina 1985; Baitulin et al. 1986; Kamenetsky 2000). Absence of cold requirements was demonstrated by the easy blooming of some introductions of rhizomatous species from Siberia and Kazakhstan to Israel (e.g., A. trachyscordum, A. petraeum, A. platyspathum, and A. nutans). These species were grown as perennial plants and flower in the Mediterranean climate in the summer, between May and August, without additional cold treatment (Kamenetsky 2000).

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An intermediate group of rhizomatous-bulbous plants consists of several species from the section Cepa, including some wild relatives of the bulb onion, such as A. altaicum, A. pskemense, A. galanthum, and A. vavilovii. In their natural habitats, these plants undergo short summer dormancy, and sprouting resumes in the autumn. Flowering is initiated by the intermediate-low temperatures and the short photoperiod in the autumn. However, winter temperatures slow down or completely inhibit plant development, and thus leaf and scape elongation occur in the spring. Flowering occurs in May–June following formation of six to eight leaves per axillary shoot (Pistrick 1992; Cheremushkina 1985). 3. Edible Allium Crops. In Allium crops, long-term cultivation and selection by farmers, and breeding pressure for both adaptation to various environmental conditions and improved economical traits strongly affected their developmental processes and quality traits. These include: reduced bolting in all edible alliums; long shafts in leek; fast leaf growth in chives, in Chinese chives, and in Japanese bunching onion; single heart in the bulb onion and maximum doubling in shallot. In the bulb onion, selection was made also for big and medium bulbs, for skins adhesion and colors and for a variety of shapes; for high and low pungency, and for high and low dry matter content for the processing and fresh markets, respectively, and more. Recent advances in the biology of Allium crops were reviewed in detail (Rabinowitch and Brewster 1990a,b; Brewster and Rabinowitch 1990; Rabinowitch and Currah 2002), and thus we shall limit the discussion to the main points related to the annual development of major edible alliaceous crops. With the exception of garlic, great-headed garlic (A. ampeloprasum), and all the traditional shallot clones, edible Alliums are cultivated as annual or biennial crops, and are propagated by seed. Climatic conditions, soils, and pre- and post-harvest technologies affect plant growth and development, as well as plant chemistry and morphology, e.g., bolting (Rabinowitch 1985, 1990a), single heartedness or doubling (Rabinowitch 1979), pungency and sweetness (Randle et al. 1995; Randle and Lancaster 2002), length of dormancy and storage ability (Komochi 1990; Gubb and MacTavish 2002). In general, florogenesis of this group is promoted by low temperatures (e.g., bulb onion: Rabinowitch 1985, 1990a; chives: Poulsen 1990; Japanese bunching onion: Inden and Asahira 1990; shallot: Rabinowitch and Kamenetsky 2002) and by long photoperiod (e.g., bulb onion: Rabinowitch 1985, 1990a; Chinese chives: Saito 1990; garlic: Kamenetsky et al. 2004a; rakkyo: Toyama and Wakamiya 1990). In most onion cultivars,

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only seedlings with 10–12 leaves respond to cold induction (Rabinowitch 1985, 1990a), with optimum temperature ranging between 7 and 12°C (Brewster 1987). A similar response is evident in shallot (A. cepa Aggregatum group), except for the minimum physiological age of 6–7 leaves required by shallot seedlings for flowering (Krontal et al. 2000). The following two examples on the effect of selection pressure by man on plant physiology are the exception to the above rule: optimum temperature for floral induction in the West African onion cv. ‘Bawku’ is 15–21°C, while in some North Russia landraces florogenesis is promoted at 3–4°C (for reviews, see Rabinowitch 1985, 1990a). High storage temperatures adversely affect Allium blooming. In the bulb onion, temperatures of 28 to 30°C inhibited inflorescence initiation and delayed flowering (Heath and Mathur 1944; Aoba 1960). It resulted also in marked reduction in flowering (Jones and Emsweller 1936; Kampen 1970). The further the inflorescence had progressed, the longer was the required warm treatment to cause reversion from floral to vegetative phase (Heath and Mathur 1944; Sinnadurai 1970). Following floral initiation, lateral meristems become dormant in the bulb onion, but not in shallot. In the latter, axillary meristems remain active and generate new leaves concomitantly with the development of the inflorescence in the apex (Rabinowitch and Kamenetsky 2002, Fig. 7.10B). However, some shallot genotypes (and especially clones from Central and Northern Europe, Nepal, and other temperate regions) seem to require a very large number of cold units to induce flowering, possibly due to a long history of selection for quality yields, as quality of flowering shallot are lower in bolting plants than those which remain vegetative (Messiaen et al. 1993; Y. Krontal, pers. commun.). Floral initiation of Japanese bunching onion (A. fistulosum) requires low temperatures and short photoperiod (Nakamura 1985b). Genotypes markedly differ, however, in the number of leaves developed before reaching the post-juvenile age, in cold requirement for floral induction, and in the interactions between temperature and photoperiod with regard to scape elongation (Nakamura 1985b; Inden and Asahira 1990; Yamasaki et al. 2000a,b). Hence, some mid-season cultivars require a similar amount of cold units for flower initiation, but their scape elongation response to photoperiod is considerably different (Yamasaki et al. 2000b). Chives (A. schoenoprasum) (Poulsen 1990) and leek (A. ampeloprasum) (van der Meer and Hanelt 1990; De Clercq and Van Bockstaele 2002) are biennials. The physiological age of leek cultivars, which are ready to bloom, varies with both growth conditions and genotype

358

A

cover leaf (tunic)

vegetative apex

storage leaf (scale)

inflorescence

B

foliage leaf Fig. 7.10. Vegetative propagation of Allium species. (A) Cross-section and diagram of A. aschersonianum. Formation of the terminal inflorescence is followed by differentiation of the single axillary renewal bulb (adapted from Hovav 2001). (B) Cross-section and diagram of shallot A. cepa Aggregatum group. Plants develop several axillary shoots, some of which may flower in parallel with terminal inflorescence (adapted from Shiftan 2005).

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(Dragland 1972; van der Meer and Hanelt 1990). Cold induction promotes blooming in both leek and chives. Flowering of chives can actually be eliminated by maintaining growth temperatures above 18°C (Poulsen 1990). In leek, however, flower initials and bolting occurred in plants grown at a constant 21°C, thus indicating the quantitative effect of cold treatment on bolting in leek (Dragland 1972). Short photoperiod promotes florogenesis and scape elongation in chives (Poulsen 1990; Brewster 1994). In leek, a long photoperiod is required for this process; however, flower initiation and visible bolting occur in vernalized leek even in short photoperiods (van der Meer and Hanelt 1990; De Clercq and Van Bockstaele 2002; Brewster 1994). In rakkyo (A. chinense), and Chinese chives (A. tuberosum), vegetative plants subdivide continuously to form a dense clump of shoots, and flowering occurs in the late summer. The differentiation and growth of the inflorescence are promoted by long photoperiod, and inhibited by short days (Toyama and Wakamiya 1990; Nakamura 1985a,c; Saito 1990) and drought (Mann and Stearn 1960). All modern commercial garlic (A. sativum) clones are completely sterile and thus propagated only vegetatively (Simon and Jenderek 2004). In the absence of sexual reproduction, increase in genetic variation is limited to random or induced mutations (Burba 1993), somaclonal variation (Novak 1990), or genetic transformation (Kondo et al. 2000; Sawahel 2002; Zheng et al. 2004a,b). The recent discovery of fertile clones in Central Asia (Etoh et al. 1988; Kamenetsky et al. 2004b), combined with the application of physiological means to restore fertility (Kamenetsky et al. 2004a), are expected to facilitate the exploitation of the vast genetic diversity existing within and between clones, currently inaccessible for both genetic studies and crop improvement. In garlic, inflorescence development and bulbing compete for limited resources. Long-term selection pressure applied by man for earliness and for large bulbs thus modified the hormonal balance in favor of the storage organs. Consequently, many garlic clones do not bolt or bolt and produce scapes without flower heads (Takagi 1990). The latter usually produce scapes crowned by topsets (inflorescence bulbils) only, yet some produce a variable mix of flower buds and topsets. During their development, the fast-growing topsets squeeze and strangulate flower buds, thus causing their degeneration and complete sterility (Kamenetsky and Rabinowitch 2001). Fertile flowers were obtained, however, when topsets were frequently removed (Konvicka 1984; Pooler and Simon 1994; Etoh et al. 1988; Jenderek 1998).

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During the vegetative stage in both young seedlings and sprouting cloves, garlic SAM initiates only leaf primordia. Thereafter, when plants reach a critical mass and in response to environmental effects (Kamenetsky and Rabinowitch 2001; Kamenetsky et al. 2004a), the apical meristem turns into one of the following alternative routes: (1) degeneration of the apex and cessation of growth; (2) formation of a clove in the center of the bulb; (3) initiation of a spathe (prophyll), followed by the formation of reproductive meristem, scape elongation, and differentiation of an inflorescence (Takagi 1990). Bolting ability was used as a means of garlic classification (Takagi 1990), as follows: (1) Nonbolting—plants do not normally form a flower stalk, but only produce cloves inside an incomplete scape; (2) Incomplete bolting—plants produce a thin, short flower stalk, bear only a few large topsets, and usually form no flowers; (3) Complete bolting—plants produce a long, thick flower stalk, with many flowers and topsets. Florogenetic studies of the complete bolters revealed four phases of development, including: (1) transition of the apical meristem; (2) scape elongation; (3) inflorescence differentiation; and (4) completion of floral development. Meristem transition occurs in growing plants under a variety of storage and growth conditions, but long photoperiod is essential for the initial elongation of the scape (Kamenetsky and Rabinowitch 2001; Kamenetsky et al. 2004a). Under a continuous, long photoperiod, differentiation of flower buds in the developing inflorescence is followed by formation of topsets, and the consequent flower buds’ degeneration. A short photoperiod is not conductive to topsets’ development. Hence, a short interruption of a long photoperiod was sufficient to induce scape elongation, but insufficient for topset development, and resulted in blooming of fertile flowers (Kamenetsky et al. 2004a). Temperature and photoperiod effects on both garlic development and florogenesis are quantitative: under long photoperiod, low temperatures promote scape elongation, while warm temperatures enhance translocation of reserves to the cloves and the topsets, with the consequent degeneration of the developing floral buds. Short photoperiod promotes foliage growth and sprouting axillary bud (cloves). Hence, introductions from high latitudes to regions with somewhat shorter photoperiods may result in initial formation of cloves and bulbs in the late spring. The bulbs, however, do not reach maturation and when photoperiod re-shortens, sprouting begins (e.g., introductions from China and Southern Europe to Israel: H.D. Rabinowitch, personal observations).

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VI. PROPAGATION A. Seed Propagation Most Allium species produce viable seeds (for a detailed review on seed development in cultivated Alliums, see: Rabinowitch 1990b). Temperature appears to be the dominant factor affecting seed germination, with species specific response. Specht and Keller (1997) recommended a standard temperature germination test at 16°C for species of subgenus Allium, 16 or 26°C for species of subgenus Rhiziridium, and 5°C for species of subgenus Melanocrommyum. Optimal seed germination of rhizomatous species (mainly from moderate climatic zones) occurs after 4 days of wetting at 20°C, and in bulbous species of subgenus Melanocrommyum (from the semi-desert conditions of Central Asia) after 4–7 months of wetting at 0–3°C (Aoba 1967; Dalezkaya and Nikiforova 1984). In Europe, bulbous ornamentals are sown in the autumn, germination occurs in the spring, and vegetative growth lasts 6–8 weeks in the first year, followed by bulbing and dormancy. In the fall, juvenile sets are replanted for a second cycle. The process is repeated 2–3 or 3–5 times (years) in species with small or large bulbs, respectively (Kamenetsky and Fritsch 2002). Seeds of rhizomatous species have no dormancy and thus are ready for sowing in the late spring. They germinate quickly and grow throughout the summer to produce plants of marketable size in the autumn. A few plant species manage to produce flowers already in the first season, but mostly, blooming occurs in the second year of development (Kamenetsky and Fritsch 2002). In most of the edible species, selection by man eliminated seed dormancy and, when moisture is available, germination occurs under a wide range of temperatures. For bulb onion, the upper and lower limits are 5 to 35°C, with the optimum between 25 and 30°C (Rabinowitch 1990b). In cultivated Alliums, deterioration of seed vigour begins immediately after ripening, and under ambient conditions viability is lost very quickly. Cold storage and low moisture conditions enable long storage with minimal reduction in vigour (Roberts 1972). Fertile flowers and viable seeds of garlic were produced in Kagoshima, Japan from the plants collected in Central Asia and Kazakhstan (Etoh et al. 1988; Etoh and Simon 2002). Seed set was improved by scape decapitation and removal of topsets, but germination rates were low (Pooler and Simon 1994). Inaba et al. (1995) and Jenderek (1998) selected some fertile genotypes and obtained 50,000 and 1.2 million garlic seeds,

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respectively. Later, 36 fertile accessions were identified in two garlic collections in the USA (Jenderek and Hannan 2000). During 1995–2001, more than 300 garlic landraces and specimens from natural populations were collected in Kazakhstan and Central Asia (Baitulin et al. 2000; Kamenetsky et al. 2004b), and true garlic seeds were obtained from 30 accessions. Seven accessions produced some 400–500 viable seeds/umbel, without the removal of topsets. Normal seedlings development was evident, and the young plants formed two to five leaves, prior to bulbing and ripening. Plants varied in bulbing ability, but many produced a single-clove bulb covered with white, purple, gray and brown skins. Bulb diameter varied between 0.5 and 2 cm (Kamenetsky et al. 2004b). Massive garlic seed propagation seems to be a feasible option (Etoh and Simon 2002; Jenderek 2004; Kamenetsky et al. 2004a,b; Simon and Jenderek 2004), and in the future sexual reproduction can be exploited in plant breeding for improvements of yield and quality, for tolerance to biotic and abiotic stresses, and for adaptation to given ecological niches. In addition, seed production of established cultivars may be used for production of virus-free propagules, and to reduce the costs of propagation material. B. Vegetative Propagation Some Allium species, e.g., garlic, shallot, and most ornamentals, are propagated vegetatively from axillary bulbs, bulblets on stolons, division of rhizomes, and topsets (Kamenetsky 1994b). The rate of natural vegetative propagation, however, is generally low; thus, some horticultural techniques are employed for increased efficiency. The intrabulb ramification in bulbous species ranges from one or two sets (e.g., A. aflatunense, A. macleanii, A. flavum) to tens of axillary daughter bulbs (e.g., A. moly, A. oreophilum, A. ampeloprasum, A. scorodoprasum) (Fig. 7.10). The process can, however, be enhanced by growth conditions (optimal fertigation, optimal growing temperatures of 20–30°C, strict plant protection, and more [Fritsch R., Germany, pers. commun.]). Some species from subgenus Melanocrommyum (e.g. A. aschersonianum and A. rothii) form a single renewal bulb (Kamenetsky 1994a,b; Kamenetsky et al. 2000). The latter cases prohibit standard clonal propagation of selected genotypes, and require special means for reproduction enhancement, such as autumn scaling (e.g., A. cristophii and A. giganteum: Alkema 1976; A. aschersonianum: Gilad et al. 2001). Rhizomatous species exhibit a differential productivity with age. Thus, juvenile plants of A. senescens produce one or two laterals, as

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compared with annual production of 6–12 daughter bulbs in postjuvenile plants (Cheremushkina 1985). Further increase in vegetative propagation is achieved by rhizome division (Davies 1992). Topsets (inflorescence bulbils) are used for propagation of vegetatively propagated edible alliums, e.g., garlic, rocambole (A. scorodoprasum), Egyptian tree onion (A. proliferum) (Popova 1975; Brewster and Rabinowitch 1990). In the first year, garlic grown from topsets produce only small bulbs; hence, economic yields are obtained only in the second growing season. Similar to cloves, however, topsets are infected with viruses (Salomon, R., Israel, pers. commun.), and thus yield and quality are lower than those obtained from virus-free propagules. The inherent contamination of vegetative propagules with viruses and other pathogens result in up to 70% yield and quality losses (Davis 1995; Nagakubo et al. 1993). Pathogen-free garlic (and other Allium spp., e.g., shallot) plants were obtained by meristem-tip culture combined with thermotherapy and chemotherapy, followed by in vitro multiplication (Walkey et al. 1987; Moriconi et al. 1990; Ucman et al. 1998; for a recent review, see: Salomon 2002). Protocols for massive propagation via tissue culture are available for garlic and shallot (Walkey et al. 1987; Novak 1990; Robledo-Paz et al. 2000; Salomon 2002; Zheng et al. 2003); A. aflatunense, A. ampeloprasum, and A. aschersonianum (Evenor et al. 1997; Ziv et al. 1983). Recent improvements also include in vitro propagation from callus (Barandiaran et al. 1999a,b,c), from inflorescence meristem (Xu et al. 2001), and by embryogenesis (Haque et al. 1998; Fereol et al. 2002; Fereol et al. 2005).

VII. CHEMICAL COMPOSITION Carbohydrates are the most abundant class of chemical compounds in Allium species and include glucose, fructose, and sucrose, together with a series of oligosaccharides, the fructans (Darbyshire and Steer 1990). Allium plants also contain proteins, pectin, minerals, and polyamines (Fenwick and Hanley 1990; Parolo et al. 1997). A distinguishing trait of all Allium spp. is the metabolic chain of sulfur compounds (Block et al. 1986, 2001; Randle and Lancaster 2002). Most of the sulphur-containing compounds are in the form of non-protein amino acids, some of which serve as precursors of the volatile flavor (Randle and Lancaster 2002) and of neutraceutical compounds (Augusti 1990, 1996; Dorsch 1996; Koch and Lawson 1996; Craig 1999; Griffiths et al. 2001; Kik et al. 2001; Keusgen 2002; Jones et al. 2004). The precursors are odorless, stable, nonvolatile amino acids of the general name S-alk(en)yl cysteine sulfoxides

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(ACSOs). Four different ACSOs have been recognized in Allium species (Freeman and Whenham 1975; Hashimoto et al. 1984). Differences between species and cultivars in flavour characteristics probably arise from variability in sulfur uptake and in its metabolism through the flavour biosynthetic pathway. Some Allium species exhibit a characteristic pattern of cystein sulfoxide considerably different from that of garlic or onion, and their total amount may be higher that 1% of the bulb fresh weight (Fritsch 2001). For instance, the Siberian species A. obliquum contains high levels of alliin, isoalliin, and methiin. A high level of alliin and isoalliin was also found in A. ampeloprasum, while methinin was reported for a number of species from Central Asia, including A. stipitatum and A. jestianum. Chemotaxonomy of more than 40 Allium species from various subgenera revealed at least seven different chemo-types of the aroma profiles, and showed specific arrays of volatile sulphur compounds in the rhizomatous species (Schulz et al. 2000; Storsberg et al. 2003). This classification can contribute to a better selection of wild species for breeding experiments, aiming at a purposeful improvement in aroma, taste, and also pharmacological properties of interspecific Allium hydrids. However, the proposed classification into chemo-types does not agree with taxonomical or biomorphological division within the genus.

VIII. CONCLUDING REMARKS For generations, tens of Allium species have been consumed by man worldwide (Van Deven 1992; van der Meer 1997). In addition to their role as flavoring condiments, there has been an increasing awareness of both consumers and researchers to the health benefits of Alliums, as well as of their potential as ornamentals (Keusgen 2002; Kamenetsky and Fritsch 2002). Therefore, great efforts have been made in breeding locally adapted Allium cultivars, from the tropics to the sub-arctic regions (Brewster 1990, 1994; Dowker 1990; Rabinowitch 1985, 1990a). However, the intensive breeding pressures and the increasing distance away from co-evolutionary processes with pests, diseases, and environmental stress resulted in drastic reduction in the respective variability within the genepool of the domesticated species. Hence, resources for tolerance to biotic and a-biotic stress are scarce, if not lacking, in the bulb onion, shallot, chives, and leek. Millennia of human selections and spontaneous mutations of the vegetatively propagated garlic resulted only in a limited selection of clones in any given locality and worldwide. Most

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of these clones are susceptible to pests, diseases, and environmental stress. On the other hand, more than 700 Allium species grow in the wild, where co-evolution with biotic and abiotic stress continued for generations. These plants may include genes for desired traits, as in A. roylei (De Vries et al. 1992c), and may thus serve as invaluable sources for Allium improvement. In addition to the major crops, such as onion, garlic, Japanese bunching onion, shallot, chives, and leek, many edible wild species are used by specific populations (e.g., A. tricoccum in North America, A. motor in Central Asia, A. altaicum in Siberia). Allium plants are rich in neutraceutics (Ip et al. 1992; Sampson et al. 2002; Keusgen 2002) including flavonoids (e.g., A. altaicum, A. ampeloprasum, A. galanthum, A. proliferum, and A. vavilovii: Patil and Pike 1995; Horbowicz and Kotlinska 2000), sulfur (Keusgen 2002; Randle and Lancaster 2002), and selenium-containing compounds (Havey 1999; Randle and Lancaster 2002). Hence, in addition to their potential reservoir for improvement of edible alliums (Kik 2002) as a source for novel ornamentals (Kamenetsky and Fritch 2002) and new condiments, wild alliums may also become a unique source for health compounds (Havey 1999). When compared to other major crops, molecular studies of Allium spp. commenced rather late (Rabinowitch 1988) and molecular knowledge and applied modern technologies are still far behind those common in other important vegetables (e.g., tomato: Martineau 2001). However, initial steps to employ state-of-the-art molecular techniques are being taken (Havey 2002). Hence, vector-mediated and direct gene-transfer systems have been applied to Alliums (Eady et al. 2000; Eady 2002; Zheng 2004; Zheng et al. 2004a,b; X. Barandiaran, pers. commun.). RAPD and AFLP methods and DNA fingerprinting are used for diversity studies (Al-Zahim et al. 1997; Bradley et al. 1996; Hong et al. 1997; Klaas and Friesen 2002; Jenderek and Hannan 2004; Ipek et al. 2003; Volk et al. 2004; Kamenetsky et al. 2005). In Allium spp., the genetics of most important traits is unknown. With regard to flowering, only the genes for male sterility (ms, T: Havey 2002) and for dwarfed scape (dw) (Rabinowitch et al. 1984, 1991; Horobin 1986) are known in bulb onion. There is no information on genetic regulation of flower color, length of blooming period, and odor in any Allium spp., nor do we have any knowledge of the genetic control of the stages of flower development, or of the genetic and environment interactions on these and other traits. Progress in Allium improvement depends on the availability of genetic variation. Therefore, the fast-dwindling genetic resources may jeopardize

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future attempts for improvement and the immediate endeavor of systematic collections and evaluation of the genetic reserves. In comparison to the limited diversity of the Lycopersicon (the genus comprises of nine species, Warnock 1988), the Allium genepool is exceedingly rich (Hanelt 1990) and has a great potential for utilization (Havey 1999). Adoption of both classical and novel (Havey 2002; Kik 2002) tools, including molecular markers for yield and quality traits (Cramer and Havey 1999; Galmarini et al. 2001; McCallum et al. 2001), for malesterility (Gokce and Havey 2000, 2002; Gokce et al. 2002), and for crossing inert-specific barriers; deeper genetics and physiological (Kik 2002; Bohanec 2002; Etoh and Simon 2002; Kamenetsky and Rabinowitch 2001; Kamenetsky et al. 2004a) knowledge and that of inherent control mechanisms of vital processes such as florogenesis (N. Rotem, Israel pers. commun.) and dormancy of Allium spp. are therefore expected to facilitate a quantum leap in the improvement of these important plants. Consequently, it is expected to provide humans with a greater variety of quality functional produce, raw material for the food processing and the neutraceutical industries, and new ornamentals that are environmentally adapted and need less protection from pests and diseases. LITERATURE CITED Abdalla, A. A., and L. K. Mann. 1963. Bulb development in the onion (Allium cepa L.) and the effects of storage temperature on bulb rest. Hilgardia 35:85–112. Alkema, H. Y. 1976. Vegetatieve vermeerdering van Allium species. (In Dutch). Weekblad voor Bloembollencultuur. 86:981–982. Al-Zahim, M., H. J. Newbury, and B. V. Ford-Lloyd. 1997. Classification of genetic variation in garlic (Allium sativum L.) revealed by RAPD. HortScience 32:1102–1104. Aoba, T. 1960. The influence of the storage temperature for onion bulbs on their seed production. (In Japanese with English summary). J. Japanese Soc. Hort. Sci. 29:135–141. Aoba, T. 1967. Effects of different temperatures on seed germination of garden ornamentals in Allium. (In Japanese with English summary). J. Japanese Soc. Hort. Sci. 36:333–338. Aoba, T. 1968. Studies on propagation of Allium rosenbachianum Regel. II. Process of bulb formation in seedling. (In Japanese with English summary). J. Japanese Soc. Hort. Sci. 37:166–171. Aoba, T. 1970. Effect of low temperature on the bulb or corm formation in some ornamental plants. (In Japanese with English summary). J. Japanese Soc. Hort. Sci. 39:369–374. Astley, D., N. L. Innes, and Q. P. van der Meer. 1982. Genetic resources of Allium species: a global report. IBPGR, Rome. Astley, D. 1990. Conservation of genetic resources. p. 177–198. In: H. D. Rabinowitch and J. L. Brewster (eds.), Onions and allied crops. Vol. I. CRC Press, Boca Raton, FL. Astley, D. 1994. A network approach to the conservation of Allium genetic resources. Acta Horticulturae, 358:135–142. Augusti, K. T. 1990. Therapeutic and medicinal values of onion and garlic. p. 94–108. In: H. D. Rabinowitch and J. L. Brewster (eds.), Onions and allied crops. Vol. III. CRC Press, Boca Raton, FL.

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Rabinowitch, H. D., B. Friedlander, and R. J. Peters. 1991. Dwarf flower stalk in onion (Allium cepa L.): characterization, genetic control and physiological response to ethephon and to gibberellic acid. J. Am. Soc. Hort. Sci. 116:574–579. Randle, W. M., and J. E. Lancaster. 2002. Sulphur compounds in alliums in relation to flavour quality. p. 329–356. In: H. D. Rabinowitch and L. Currah (eds.), Allium crop science: recent advances. CAB Int., Wallingford, UK. Randle, W. M., J. E. Lancaster, M. L. Shaw, K. H. Sutton, R. L. Hay, and M. L. Bussard. 1995. Quantifying onion flavor compounds responding to sulfur fertility: sulfur increases levels of alk(en)yl cysteine sulfoxides and biosynthetic intermediates. J. Am. Soc. Hort. Sci. 120:1075–1081. Raunkiaer, C. 1934. Life forms of plants and statistical plant geography. Clarendon Press, Oxford. Rees, A. R. 1972. The growth of bulbs. Academic Press, London and New York. Regel, E. 1875. Alliorum adhuc cognitorum monographia. Acta Horti Petropolitani 3:1–266. Roberts, E. H. 1972. Viability in seeds. Chapman and Hall, London. Robledo-Paz, A., V. M. Villalobos-Arámbula, and A. E. Jofre-Garfias. 2000. Efficient plant regeneration of garlic (Allium sativum L.) by root-tip culture. In Vitro Cell. Develop. Biol.—Plant 36:416–419. Rouamba, A., M. Sandmeyer, A. Sarr, and A. Ricroch. 2001. Allozyme variation within and among populations of onion (Allium cepa L.) from West Africa. Theor. Appl. Genet. 103:855–861. Saito, S. 1990. Chinese chives Allium tuberosum Rottl. p. 219–230. In: J. L. Brewster and H. D. Rabinowitch (eds.), Onions and allied crops. Vol. III. CRC Press, Boca Raton, FL. Salomon, R. 2002. Virus diseases in garlic and propagation of virus-free plants. p. 311–328. In: H. D. Rabinowitch and L. Currah (eds.), Allium crop science: recent advances. CAB Int., Wallingford, UK. Sampson, L., E. Rimm, P. C. H. Hollman, and M. B. Katan. 2002. Flavonol and flavone intakes in US health professionals. Res. J. Am. Dietetic Ass. http://www.findarticles .com/p/articles/mi_m0822/is_10_102/ai_103994080 Sawahel, W. A. 2002. Stable genetic transformation of garlic plants using particle bombardment. Cell. Mol. Biol. Let. 7:49–59. Schulz, H., H. Krueger, N. Herchert, and R. R. J. Keller. 2000. Occurrence of volatile secondary metabolites in selected Allium wild types. J. App. Bot. 74(3-4):119–121. Schweisguth, B. 1984. The use of exotic germplasm in breeding onions for temperate climates. 3rd Eucarpia Allium Symp. Sept. 4–6, 1984, Wageningen, The Netherlands. p. 44–48. Senula, A., E. R. J. Keller, and D. E. Lesemann. 2000. Elimination of viruses through meristem culture and thermotherapy for the establishment of an in vitro collection of garlic (Allium sativum). Acta Hort. 550:21–128. Sher, N. 1980. Hybrid protoplast formation by fusion of enucleated protoplasts, “cytoplasts”, and nucleated protoplasts, “miniplasts”. (in Hebrew). M.Sc. Thesis. Hebrew Univ., Jerusalem. Shiftan, A. 2005. Morphology and physiology of branching in shallot (Allium cepa L. Aggregatum group) (in Hebrew). M.Sc. Thesis. Hebrew Univ., Jerusalem. Simon, P. W., and M. M. Jenderek. 2004. Flowering, seed production and the genesis of garlic breeding. Plant Breeding Review 23:211–244 Sinnadurai, S. 1970. The effect of light and temperature on onions. Ghana J. Agr. Sci. 3:13–15.

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8 The Invasive Plant Debate: A Horticultural Perspective Alex X. Niemiera and Guy Phillips Department of Horticulture and Department of Forestry Virginia Polytechnic Institute and State University Blacksburg, Virginia 24061

I. INTRODUCTION A. The Invasive Plant B. Definitions C. Historical Sketch II. PERSPECTIVES A. Economic B. Human C. Ornamental Horticulture D. Predicting Invasive Potential III. ECOLOGY OF INVASIVE SPECIES A. Lag Time B. Environment C. Ecosystem Transformations Due to Invasive Species 1. Purple Loosestrife 2. Spartina 3. Elodea 4. Prickly Pear 5. Ailanthus 6. Multiflora Rose IV. REGULATORY MATTERS A. International Aspects B. APHIS C. State and Self-Regulation V. CONCLUSION A. Research B. Regulation LITERATURE CITED APPENDIX A

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I. INTRODUCTION The invasive plant topic is complex, controversial, and multifaceted. There is a tremendous amount of literature on this topic, yet scientists of varied disciplines acknowledge that there is much to be discovered and understood regarding the biology of invasive plants and the ecological ramifications of their invasions. Invasive plants, defined in an ecological context (Richardson et al. 2000), are naturalized plants that produce reproductive offspring, often in very large numbers, at considerable distances from parent plants, and thus, have the potential for considerable spread. Davis and Thompson (2001), proponents of a more broad definition, make a convincing case for including “impact” in the definition of species considered as an invader because this term is more consistent with the audience outside the field of ecology. They take issue with the narrow definition, generally accepted by ecologists, that an invader is a plant that spreads into a new area. The term “impact” carries a certain ambiguity and a debate exists on the inclusion and interpretation of this word (Daehler 2001). The World Conservation Union (IUCN) defines invasive alien species as an alien species whose establishment and spread threaten ecosystems, habitats, or species with economic or environmental harm (McNeely 2001a). We are in favor of the definition(s) that have a reference to impact because the audience of invasive plant information is very large and inclusion of the impact concept has direct relevance to the commerce and regulation of invasive species. Aspects of the current controversial debate regarding the definition of invasive species are discussed by Davis and Thompson (2000), Heger and Trepl (2003), and Kowarik (2003). The U.S. government, which has both economic and environmental interests, defined invasive species in the Invasive Species Executive Order 13112 (Federal Register, Presidential Documents 1999, Appendix A) as “an alien species whose introduction does or is likely to cause economic or environmental harm or harm to human health.” Alien is defined as “with respect to a particular ecosystem, including its seeds, eggs, spores, or other biological material capable of propagating that species, that is not native to that ecosystem.” The interpretation of native and nonnative (or alien) seems evident but a “true” meaning of these terms is dependent on the context in which they are used. There are many terms used in the literature defining the various aspects of invasive species. A definition or an explanation of a biological process often differs depending on the author or the context of the issue in question. For example, a scientist’s or policy maker’s definition

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of “invasive species” often depends on their background and approach to the issue. “Invasive species” as well many other terms used in the invasive plant forum can have multiple interpretations. Such ambiguity is one of the reasons for the confusion amongst vested interests in the invasive plant debate. On the subject of the appropriate use of language to address invasive plant issues, Hattingh (2001) makes a convincing and detailed call for “an ethic of conceptual responsibility—that is, an ethic in which we take responsibility for the conceptual distinctions we choose to make and the values we allow to inform these choices.” This ethic requires us to (1) articulate the reasons for our conceptual distinctions and the narrative frameworks, and the codes and rules in terms of which we utilize them; (2) acknowledge that these narrative frameworks in terms of decision making have histories, are imbued with ideological bias, and have significant real-life consequences; and (3) avoid final answers in our thinking as well as in our actions and acknowledge that we cannot realize absolute truths or final certainties. Acknowledging the limitations of the definitions of any one author, definitions for other terms are presented in Section IB. The complexity of the invasive plant debate, while certainly exacerbated by a lack of scientific understanding, stems from multiple, often conflicting perspectives. Facets of the invasive plant debate include a long list of vested individuals, organizations, business and academic entities, and government agencies. Major stakeholders involved include the industries of agronomy, nursery, landscape, forestry, ranching, and recreation (and all the people whose lives in some way intersect with these entities). Added to this mix are the perspectives of environmental scientists and numerous organizations involved with land management issues, land conservation, and land preservation. Such a convergence of divergent perspectives gives rise to a continual, sometimes contentious, debate between vested interests. This mix, which contrasts economic versus environmental issues, makes the construction of compromises and regulations concerning invasive plants quite difficult. A simple principle of invasion ecology correlates the probability of invasion success with a species’ initial population size and the geographic spread of introduction attempts (Rejmanek 2000). This principle alone highlights the role of horticulture in the invasive plant problem. A commonly cited statistic shows 85% of 235 known invasive woody plants in the U.S. owe their introduction to the nursery trade and widespread use as landscape material (Reichard and White 2001). Given the scale of today’s U.S. nursery industry, the steady prominence of the urban and suburban landscape contractor market, the role of landscape

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architects, and the popularity of home gardening, the horticultural world has been increasingly called on to scrutinize and revise some of its own practices. When applicable, aspects of the plant debate will be presented in the context of ornamental plants and the nursery industry that produces them since this industry is largely responsible for importing a significant portion of the introduced invasive plant species. Of course, many so-called ornamental plants such as trees, shrubs, and groundcovers often provide other functions such as windbreaks, controlling soil erosion, providing shade, acting as a privacy barrier, and serving as a wildlife habitat. We will also point out that the nursery industry is not the only indictable party importing invasive and potentially invasive species. For an understanding of the role that the horticulture industry plays in the invasive plant debate, one must view the debate in the context of the various biological, economic, horticultural, and regulatory aspects. These aspects are sufficiently diverse, often intricate and interactive, and contentious enough to pose a substantial barrier to a debate resolution. We will endeavor to cover these aspects and show how they constitute the overall, and specifically the horticultural portion, of the debate. All species discussed within this review are presented in Table 8.1. Referenced websites are presented in Appendix A. A. The Invasive Plant Difficulty in identifying specific traits of invasive plants that remain statistically significant when analyzed across a wide range of environments and other chance phenomena (e.g., climate trends, land disturbance coincidental with propagule source, and pathogen spread debilitating a competitor) has led to some cynicism regarding the feasibility of predicting invaders based on biological traits alone (Crawley 1989; Roy 1990; Pysek et al. 1995). The invasive process itself can be interpreted in various ways (Kowarik 2003; Myers and Bazely 2003). Despite the crucial relevance of environment and timing (chance) in plant invasions, invasive plants have been shown to possess many characteristics in common. However, biological traits of successful invaders differ between herbaceous and woody plants. A number of characteristics are generalized traits potentially shared by woody and herbaceous species. Traits are segregated into physiological, general biological, reproductive, and genetic characteristics. Physiological characteristics are: (1) Baker’s (1974) “general purpose genotype,” the ability of a species (or a population of the species) to remain fit and viable over a range of differing environments, allows a species to successfully compete seemingly wherever it is introduced and therefore be potentially

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Plants discussed in this chapter.

Common name

Scientific name

Ailanthus, tree-of-heaven Alfalfa American chestnut Apple Asian privet Autumn olive Barley Bean Black locust Black raspberry Blueberry Boxelder Bradford pear Burning bush Candleberry myrtle Cattail Cherry Chick pea Chinafir Common plantain Cranberry Currant Date Dawn redwood Eastern hemlock Eastern redcedar Elodea, canadian pondweed English ivy Fig Filbert flax Flowering dogwood Garlic mustard Ginger Ginkgo, maidenhair tree Grape Hemp Herb robert Honeysuckle Hop Hydrilla Japanese barberry Japanese rose Japanese zelkova Katsura tree Kudzu

Ailanthus altissima (Mill.) Swingle. Medicago sativa L. Castanea dentata (Marshall) Borkh. Malus spp. Mill. Ligustrum spp. L. Elaeagnus umbellata Thunb. Hordeum spp. L. Phaseolus spp. L. Robinia pseudoacacia L. Rubus occidentalis L. Vaccinium corymbosum L. Acer negundo L. Pyrus calleryana Decne. ‘Bradford’ Euonymus alatus (Thunb.) Sieb. Myrica faya Ait. Typha spp. L. Prunus spp. L. Cicer arietinum L. Cunninghamia lanceolata (Lamb.) Hook. Platago major L. Vaccinium macrocarpon Ait. Ribes spp. L. Phoenix spp. L. Metasequoia glyptostroboides Hu & Cheng. Tsuga canadensis (L.) Carr. Juniperus virginiana L. Elodea canadensis Michx. Hedera helix L. Ficus spp. L. Corylus maxima Mill. Linum spp. L. Cornus florida L. Alliaria petiolata (M. Bieb.) Cavara & Grande Zingiber spp. Boehm. Ginkgo biloba L. Vitis spp. L. Cannabis sativa L. Geranium robertianum L. Lonicera spp. L. Humulus lupulus L. Hydrilla verticillata (L.f.) Royle Berberis thunbergii D.C. Rosa rugosa Thunb. Zelkova serrata (Thunb.) Mak. Cercidiphyllum japonicum Sieb. & Zucc. Pueraria montana var. lobata (Willd.) Onwi. (continues)

384 Table 8.1.

A. NIEMIERA AND G. PHILLIPS (continued)

Common name

Scientific name

Laurel fig Lemon Lettuce Licorice Madder Maize (corn) Melaleuca Melon Mexican weeping pine Mimosa Monterey pine Multiflora rose Norway maple Oat Olive Onion Opuntia, prickly pear

Ficus microcarpa L. Citrus limon (L.) Burm. Lactuca sativa L. Glycyrrhiza glabra L. Rubia tinctoria L. Zea mays L. Melaleuca spp. L. Cucumis melo L. Pinus patula Schiede ex Schldl. & Cham. Albizia julibrissin Durazz. Pinus radiata D. Don. Rosa multiflora Thunb. ex Murray. Acer platanoides L. Avena spp. L. Olea europaea L. Allium cepa L. Opuntia spp. Mill. Opuntia stricta Haw. Citrus spp. L. Celastrus orbiculatus Thunb. Asimina triloba (L.) Dunal Pisum sativum L. Prunus persica (L.) Batsch Pyrus spp. L. Prunus spp. L. Punica granatum L. Solanum tuberosum L. Lythrum salicaria L. Cydonia oblonga Mill. Rhododendron ponticum L. Oryza sativa L. Paulownia tomentosa (Thunb.) Steud. Lolium perenne L. Crocus sativa L. Tamarix spp. L. Glycine max (L.) Merrill. Spartina anglica C. E. Hubbard Spartina maritima (M.A. Curtis) Fern. Spartina alterniflora Loisel. Hypericum perforatum L. Fragaria spp. L. Saccharum officinarum L. Helianthus annuus L. Rosa × odorata (Andrews) Sweet. Nicotiana spp. L. Acer circinatum Pursh. Triticum aestivum L. Isatis tinctoria L.

Orange Oriental bittersweet Pawpaw Pea Peach Pear Plum Pomegranate Potato Purple loosestrife Quince Rhododendron Rice Royal paulownia Rye Saffron Salt cedar Soybean Spartina, common cordgrass small cordgrass smooth cordgrass St. John’s wort Strawberry Sugar cane Sunflower Tea rose Tobacco Vine maple Wheat Woad

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invasive (Rejmanek 2000). (2) Root exudates (allelopathic activity) have been observed to increase species competitiveness by altering root/resource interactions of competitors and therefore aid in potential invasiveness (Roy 1990; Callaway and Aschehoug 2000). (3) High growth rate, relative to competing neighbors, especially of seedlings (high photosynthetic, respiration, and transpiration rates) and high leaf area ratio (leaf area/total dry weight; i.e., leafiness) increase competitiveness and therefore invasive capability (Roy 1990; Rejmanek and Richardson 1996). General biological characteristics are: (1) The potential for invasiveness increases as the size of a species’ native range increases. The “general purpose genotype” and seed dispersal strategies are linked to this increased range as well. The activities of humans also play a great part in this factor: the more widespread a plant species, the more likely it is to have its propagules moved around (Goodwin et al. 1999; Rejmanek 2000). (2) Species with population bases spread over relatively distant areas will achieve greater numbers than will those species with a single, though perhaps even larger, population base (Reichard and Campbell 1996). This difference may be the difference, at least initially, between naturalized and invasive status. (3) Alien species without native cogeners (allied species of the same genus typically possessing many similar traits) tend to be successful invaders due to a lack of resident herbivores and pathogens capable of switching to hosts of strange and unaccustomed lineage. Alien species with native congeners are less likely to have this advantage (Rejmanek 2000). (4) Plant species that do not depend on specific mutualistic relationships such as root symbionts (e.g., mycorrhizae), pollinators, and seed dispersers are less likely to be thwarted by the abiotic and biotic challenges of their new environments. In other words, species with generalist mutualistic relationships have greater potential for invasion success (Rejmanek 2000; Richardson et al. 2000). (5) Free-floating aquatic plants, either surface-dwelling or submerged, are often potentially invasive (Panetta 1993). Reproductive characteristics are: (1) Reproductive characteristics such as selffertilization (with wind or generalist pollinators), perfect flowers, longer flowering and fruiting periods, and high reproductive energy allocation in general, have been correlated with invasiveness (Roy 1990; Reichard and Hamilton 1997). (2) Vegetative reproduction is an advantageous trait that increases habitat compatibility, and therefore establishment and spread. Vegetative reproduction is especially advantageous for dispersal of invasive plants in aquatic environments (Rejmanek 2000). (3) Seed attributes that favor invasiveness include: germination requirements fulfilled in many environments (perhaps no requirements), secondary (induced) dormancy, prolific seed production, small intervals between large seed crops, long seed viability, small seed size, long seed

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dispersal in time and space (i.e., long fruiting period and wide-ranging seed dispersal strategies), and seed production over a wide variety of environmental conditions (Roy 1990; Rejmanek and Richardson 1996). (4) A short minimum generation time (i.e., those species that are capable of reproducing at a relatively young age) has been associated with invasiveness (Grotkopp et al. 1998; Rejmanek 2000). Genetic characteristics include a small genome size, which has been correlated with short minimum generation time, small seed size, high leaf area ratio, and high relative growth rate (especially of seedlings), and therefore invasiveness (Rejmanek and Richardson 1996). Other genetic traits believed to increase invasive potential include: polyploidy, which is thought to confer wide ecological tolerance given by gene duplication and subsequent diversification, fixed heterozygosity and buffering against inbreeding depression in founder populations (Levin 1983), high genetic variation, and non-obligatory self-pollination (Roy 1990). Specific characteristics indicative of invasive potential of woody plants can differ from those specific to herbaceous plants. One of the most significant factors for potential invasiveness of herbaceous species relates to the size of a species’ native (primary) range (Rejmanek 2000). Herbaceous species with greater primary ranges are more likely to be adaptable to diverse environmental conditions and therefore have greater potential to be invasive. Herbaceous species with more than one reproductive method (e.g., by seed and vegetative structures) and those species with more than one kind of seed dispersal mechanism (e.g., by animals and by abiotic factors such as wind or water) have greater invasive potential than species without those features (Panetta 1993). In undisturbed mesic (a moisture regime somewhere between wet and dry) herbaceous plant communities, taller plants are more capable of invasion than shorter plants. In forest situations, short herbaceous species tend to invade. In undisturbed semi-arid habitats, species with rapidly developed deep root systems are potential invaders (Rejmanek 2000). There are a number of specific characteristics indicative of invasive potential of woody plants. Early leaf emergence (and to a lesser degree delayed senescence) enables some woody species in light-competitive environments to significantly increase annual carbon gains and therefore overall persistence and vigor (Harrington et al. 1989; Morris et al. 2002). In disturbed habitats, as well as habitats thought to be undisturbed, woody plants with seed dispersal by vertebrates can also lead to invasion success (Rejmanek 2000), especially when bird-dispersed (Mack 1996). Plants that have a climbing habit (vines) and low light compensation points (light level needed to balance carbon used in “main-

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tenance” respiration with carbon gained by photosynthesis), and protracted immature stages (rapid growth for an extended period) are attributes for woody plants that naturalize in forests (Mack 1996). Similar to herbaceous plants, the native range of woody plants can be related to potential adaptability to a new area but this factor is not as reliable with woody species as it is with herbaceous species. Some woody species of limited range have proven to be very invasive, such as monterey pine and mexican weeping pine in the Southern Hemisphere (Rejmanek 1995). Panetta and Mitchell (1991) call this “cryptic climatic adaptation,” the uncommon potential of a species to be tolerant of a wider amplitude of climatic factors than what is suggested by its primary (native), or even secondary (introduced) range. Despite the commonality between many invasive species and the factors (or suite of factors) just outlined, the advantages of a new environment devoid of coevolved parasites, pathogens, herbivores, and competitors may often be the most significant (Mack 1996). For example, Mitchell and Power (2003) found that nonnative species had an average of 84% fewer fungi species and 24% fewer virus species to defend themselves against in their new, introduced ranges, compared to their native ranges. In addition to this lack of coevolved pathogens, Klironomos (2002) found that some species seem to resist the accumulation of pathogens even at very high population densities. This uncommon ability leads to an increased competitiveness and sometimes increased invasiveness. The absence of coevolved population inhibitors is a fundamental advantage that brings into question the validity of compiling lists of other plant traits shown to be statistically common in known invaders (Mack 1996). To further complicate the reliability of relating specific traits to invasive potential, the significance of genotype × environment interaction cannot be underestimated. In different environments, a single genotype will often display different phenotypic responses; this phenomenon is called phenotypic plasticity (Sultan 2004). Traits associated with invasive potential such as high reproductive performance and wide geographical range are not often displayed by species in their native ranges but are manifested in foreign ecological settings. Here, again, environment and chance play a prominent role in the complexity of the invasive plant dilemma. B. Definitions To set the stage, invasive species terminology as according to the World Conservation Union (McNeely 2001a) is presented as follows:

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Alien species: (synonyms = non-native, foreign, exotic); a species, subspecies, or lower taxon introduced outside of its normal past or present distribution; includes any part, gametes, seeds, eggs, or propagules of such species that might survive and subsequently reproduce. Introduction: the movement, by human agency, of a species, subspecies, or lower taxon (including any part, gametes, seeds, eggs, or propagule that might survive and subsequently reproduce) outside its natural range (past or present). This movement can be either within a country or between countries. Native species: (synonym = indigenous species); a species, subspecies, or lower taxon living within its natural range (past or present), including the area which it can reach and occupy using its own legs, wings, wind/water-borne or other dispersal systems, even if it is seldom found there. Naturalized species: alien species that reproduce consistently and sustain populations over more than one life cycle without direct intervention by humans (or in spite of human intervention); they often reproduce freely, and do not necessarily invade natural, semi-natural or human-made ecosystems. Weeds: (synonyms = plant pests, harmful species; problem plants); plants (not necessarily alien) that grow in sites where they are not wanted and have detectable economic or environmental effects; alien weeds are invasive alien species. C. Historical Sketch Humans have a very long history of expanding and testing the ranges of the earth’s flora. Humans, in their first travels around the earth, carried familiar plants as food, medicine, or technology (Fritz 1994). Much has been written on this interesting subject. The following is a cursory account intended to illustrate the history and legacy of plant introductions in North America, beginning with the exploration of the New World. Crosby (2004) presents a comprehensive account of the spread of plants from Europe to other areas of the world in Ecological Imperialism—The Biological Expansion of Europe, 900–1900. The first great exchange of New World and Old World plants was a result of the second voyage of Columbus, which left Spain in 1493. Wheat, grape, chick peas, melons, olives, onions, lettuce, and sugarcane were taken to the New World. Although Columbus remained in the New World until 1496, most of the fleet returned to Spain in 1494 carrying back many seeds, including maize (Deagan and Cruxent 2002).

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In Klose’s America’s Crop Heritage (1950), many examples of alien plant introduction are presented. Plant introduction began simultaneously with the age of ocean exploration and colonization. A letter written in 1578 by an English fisherman living in the area of modern-day Newfoundland stated, “I have in sundry places sowen Wheate, Barlie, Rie, Oates, Beanes, Pease and seeds of herbs, kernels, Plumstones, nuts, all of which prospered as in England.” Farther south on the eastern seaboard, tobacco users in colonial Virginia circa 1610 lamented the fact that native Virginia tobacco seemed inferior to those cultivars hailing from the West Indies. Sir Walter Raleigh had imported more appealing cultivars from Trinidad via England in 1595 to make such a comparison possible. In 1628, the Endicott expedition for the Massachusetts Bay Colony reportedly carried alien species such as peach, cherry, filbert, pear, apple, quince, pomegranate, woad, saffron, licorice, madder, potato, hop, hemp, flax, and currant. Similar introductions were made everywhere else European colonization took place. For example, on the western colonial front, Spaniards introduced and cultivated plants such as figs, dates, grapes, olives, alfalfa, lemons, oranges, and ginger. Mack (2003) offers a comprehensive description of alien plant introduction into the United States between the early 17th and mid 19th centuries. The introduced species that ultimately became invasive were primarily plant species that human immigrants imported for their agricultural uses or species that were accidentally introduced as seed contaminating desirable seed lots. The Founding Fathers of the United States were interested in nonnative plants for all kinds of potential uses. Benjamin Franklin, and especially Thomas Jefferson, took advantage of their diplomatic sojourns abroad, and actively sought useful plants to test in the New World. President John Quincy Adams encouraged the procurement of useful plants unknown to North American cultivation. In 1827, a U.S. consulate circular stated: “The President is desirous of causing to be introduced into the United States all such trees and plants from other countries not heretofore known in the United States, as may give promise, under proper cultivation, of flourishing and becoming useful. Forest trees useful for timber; grain of any description; fruit trees; vegetables for the table; esculent roots; and, in short, plants of whatever nature whether useful as food for man or the domestic animals, or for purposes connected with manufactures of any of the useful arts, fall within the scope of the plan proposed” (Hodge 1956). This utilitarian spirit has led to many introductions, some of which have proven indispensable, some of which have disappeared, and some that have irreparably affected our ecosystems.

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Wide-scale seed distribution of exotic useful plants began in 1836 under the initiative of then Commissioner of Patents, Henry L. Ellsworth, funded by appropriations from Congress. This informal “Congressional Seed Distribution” program sent out as many as 30,000 seed packets a year to U.S. farmers. Distribution of seeds in this manner continued until 1925. In 1862, during President Lincoln’s administration, the United States Department of Agriculture (USDA) was formed, beginning an era of increased organization and zeal for novel seed and plant introductions and breeding improvements. Such introductions were fueled by the fact that North America is poor in terms of native species serving as crop plants. In general, species diversity increases with proximity to the equator, in areas with a moister climate compared to those of a drier climate, and in areas with a greater topographic or environmental variability compared to more uniform areas (Withers et al. 1998, Appendix A). With the exception of sunflower, cranberry, and blueberry (and a few other minor crops), the U.S. has depended on exotic species for its plantbased food supply. The 20th century saw many new plant introductions and developments, some very successful and some just short of disastrous. The ecological impacts of nonnative plants are ever-dynamic and predictions about future implications are difficult, to say the least. Like all promising plant introductions and innovations of any kind, there is the risk of unforeseen and unintended consequences. A very brief list of fortuitous introductions of the 20th century include: winter wheat, rice, improved cultivars of barley, numerous forage grasses and cover crops, soybeans, and many unsung cultivars of grains, fruits, vegetables, and other useful plants valuable for breeding and improvement programs. At present, more than 98% of our country’s food production, accounting for $800 billion per year, comes from introduced plant and animal species (Pimental et al. 2000). However, a number of alien introductions, intended as ornamentals or serving other functions, have turned out to be short-sighted and have, over time, significantly disrupted various environments including farm land, wetlands, and forests. Japanese barberry, native to Japan, was introduced into the U.S. about 1875 by way of seeds sent from St. Petersburg, Russia to the Arnold Arboretum in Massachusetts (Invasive Plant Atlas of New England, Appendix A). This widely used landscape plant escaped from cultivation and is regarded as an invasive species (Plant Conservation Alliance, Alien Plant Working Group—Japanese Barberry, Appendix A). Japanese barberry, whose fruit are readily spread by birds, is a very serious threat to New England habitats ranging from open fields to closed-canopy forests to wetlands. This plant has been described as “probably one of the most destructive

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invasive plants in Connecticut” (Connecticut Botanical Society, Appendix A). The traits that enable Japanese barberry to be a serious invader of natural habitats are the ability to tolerate very low light levels and a wide range of soil moisture levels, to leaf out early in the spring, and to suppress the growth of co-occurring species (Silander and Klepeis 1999). Melaleuca, also called Australian paperbark tree, was brought to southern Florida in the early 1900s as an ornamental and later to dry swamps for development (Introduced Species Summary Project – Australian Paperbark, Appendix A). This subtropical species spreads extremely rapidly and threatens to fundamentally change the ecosystem of the Florida Everglades system, which is colonized by as much as an estimated one million ha. Kudzu, an Asian vine that is ubiquitous in the forests and roadsides in the southern U.S., was introduced into the U.S. in 1876 at the Centennial Exposition in Philadelphia, Pennsylvania as an ornamental and forage crop plant (Plant Invaders of Mid-Atlantic Natural Areas, Vines, Kudzu, Appendix A). The Soil Conservation Service, a federal agency (now known as the Natural Resource Conservation Service, NRCS), distributed 85 million kudzu cuttings to southern landowners beginning in the 1930s, and paid $18 per ha ($8 per acre) as an incentive to plant kudzu to reduce soil erosion (Reichard and White 2001). Multiflora rose, also actively promoted by the Soil Conservation Service, was intended for use as wildlife food and cover and ornamental/utilitarian livestock hedges and is now a major pest of farm lands (Blossey 1999). Other examples of introduced invasive species are oriental bittersweet, Asian privet, and a number of nonnative honeysuckle species that were introduced for ornamental purposes and sometimes wildlife purposes. Autumn olive was imported for wildlife food and strip-mine reclamation (Miller 2003). Thus, the U.S. is beset by exotic, noxious weeds as a result of horticultural as well as utilitarian endeavors. The role of the federal government in disseminating nonnative species was not without some degree of caution and forethought. The Plant Quarantine Act was first passed by Congress in 1912, and demonstrated a comprehension of the scope of potential pest problems stemming from hasty introductions (Reichard and White 2001). An example of patience and prudence on the government’s part comes from a report issued in 1953 by the USDA. That report indicated a 40-year evaluation of a collection of several dozen hardy trees and shrubs for distribution and cultivation throughout the Northern Great Plains (Hodge 1956). Perhaps the price we pay for the benefits provided by the vast majority of alien plants is the unwelcome presence of the relative few that compromise our native ecology. With our current understanding of invasive species,

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a model to predict whether a species will be invasive in a particular area is needed and this approach will be discussed later in Section II D. Rapid introduction of useful plants led to rapid introduction of undesired incidentals. By 1672, approximately 50 years after the arrival of the first European settlers, 22 European weed species had already become common around the Massachusetts area (Mack and Lonsdale 2001). The presence of common plantain, currently a ubiquitous garden and landscape weed, was so prevalent and concurrent with the arrival of European colonists that Native Americans named it “Englishman’s foot” (Mack and Lonsdale 2001). Introduced plant species and their associated, unintended ramifications continue to plague North America. Native populations of eastern hemlock (McClure 1996) and flowering dogwood (Redlin 1991), both common landscape species in the eastern U.S., are currently being decimated by alien pests and pathogens that were inadvertently introduced. Perhaps the most well known and greatest impact on a prized timber and food species caused by an incidental, accidental introduction was the arrival in the U.S. of the chestnut blight caused by Cryphonectria parasitica, via Asian ornamental nursery stock in the late 1890s. American chestnut, a species estimated to compose up to 25% of southeastern U.S. forests, and highly valued for its wood and important mast production, and as a wildlife and rural subsistence food supply, was effectively extirpated throughout its natural range in less than 50 years (Von Broembsen 1989). The “unknown” element in plant introductions can have, and has had, grave consequences. What is clear in this historical perspective is that cultivation of alien species is the driving force for the naturalization of alien species. Mack and Erneberg (2002) state that cultivation affords alien species protection from environmental hazards (including those associated with stochastic expression) and as a result this protection allows naturalization to occur. In a historical review of seed importation in five United States geographical areas during the last 400 years, these authors found that at least 57% of the naturalized species arrived as deliberate introductions. They crystallize their views on the impact of deliberate introductions and subsequent naturalization as “Thus, cultivation emerges as a potential counter-force to environmental stochasticity and may well facilitate naturalization.” With all this said about the historical aspects of human transport of plants, plants were invading territories as long as they have been in existence (Labandeira 2005). Plant invasion is a natural process, and in fact, humans are part of the natural process as is their intentional and unintentional relocation of plants. Lodge and Shrader-Frechette (2003) dis-

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cuss the naturalness of species invasion but contend that such naturalness is not to be used as rationale for a permissive public policy regarding alien species importation.

II. PERSPECTIVES A. Economic Alien plant species impose significant economic costs to countries around the globe. The costs of crop production losses as well as the quarantine, control, and eradication of alien species are formidable. Costs associated with the impact of alien species on environments are also significant but often difficult to quantify. Approximately 73% of agricultural weeds in the U.S. are introduced nonnatives and cause annual economic losses (based on crop loss and herbicide expenditures) estimated at $26 billion (Pimental et al. 2000) and estimates as high as $35 billion have been reported (Reichard and White 2001). Weeds decrease yields and decrease profits due to impurities in harvests and herbicide expenditures (Westbrooks 1998). Nonnative weeds also seriously impact the quality of pasture for animal forage crops, forestry plantations, golf courses, lawns, and gardens. In addition, approximately 500 non-indigenous insect and mite species plague U.S. crops. Many of these pests accompanied alien plants at the time of their introduction. Pathogenic fungi and microbes have been accidentally introduced by contaminated seeds and other parts of host plants. Pimental (1993) estimated that the cost of control for such non-indigenous pests is approximately $13.5 billion per year. Nonindigenous pests established in U.S. forests cause approximately $2.1 billion in losses per year. Conservative estimates of introduced plant pathogen related losses are estimated at $23.5 billion per year. Considering impacts other than these large dollar amounts, ecological losses and changes brought about by invasive plants are less quantifiable but perhaps even more profound. Plant introductions in the U.S., whether they are intended for agronomic, horticultural, or other functional purposes, are generally not subjected to a cost-benefit analysis (McNeely 2001b, Appendix A). The lack of such analysis is most likely due to introducers being unaware of the advantages of such a tool, or they purposely ignore the deleterious effects of an introduction because they would be liable for the ensuing damages. In either case, the general public pays for the negative impacts of invasive species because “the line of responsibility is insufficiently

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clear to bring about the necessary change in behaviour . . .” (McNeely 2001b, Appendix A). The justification for a cost-benefit analysis is not initially apparent to importers of potentially invasive exotic plants because of the lag time for a species to pose an environmental problem. The efforts and costs of monitoring, early detection, and containment of a potentially invasive species are unlikely to be deemed necessary because the efforts and costs are in the present while the payoffs (future control costs) occur in the future, if at all (McNeely 2001a). McNeely (2001b) presented several examples that illustrate the sizable costs of unintended consequences from invasive species. One of those examples is a case of an invasive alien species affecting the water resources in the mountain regions of Western Cape Province, South Africa (research of Wilgen et al. 1996). Native shrubland vegetation, termed fynbos, in water catchment areas prevents soil erosion and plays an important role in supplying two-thirds of the Western Cape’s water needs. The fynbos vegetation yields cut flowers and thatch grass that generated a combined value of about $19 million in 1993 and provided a livelihood for about 25,000 people. Alien woody species, introduced into South Africa for timber, soil erosion control, and ornamental functions, invaded the fynbos vegetation and displaced the native flora. There was a 50% to 100% increase in biomass in the fynbos area due to the alien species. As a result of the invasion, the area was prone to increased fire intensities that led to severe soil erosion. Wilgen et al. (1996) calculated that the cost of managing the alien plants, to a point where they would no longer be a part of the ecosystem, would increase the net unit cost of water by 16%. If plant introduction history is repeated, the number of exotic weeds that enter our environment will inevitably increase and the economic, agricultural, and environmental challenges to society will be greater than ever. Based on the approximately 260,000 vascular plant species known to exist on earth, a predicted 22,000 potential weed species have not yet been distributed outside of their native ranges (Reichard and White 2001). In view of the 500 nonnative plants already considered to be serious weedy impediments to U.S. agriculture (Pimental et al. 2000), the potential for further plant invasion is great. Such invasions have the power to inflict high economic losses and serious environmental impacts. For example, Florida spends $14.5 million per year to fight the waterbody-clogging hydrilla and $3 million to $6 million per year to fight the Everglades invader melaleuca (Pimental et al. 2000). The economic damage that alien species cause on native environments is generally not available (Pimentel 2000). The impacts of alien species on environment function (e.g., nutrient cycling, pollution filtration, water filtration), biodiversity, as well as outdoor recreation are

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difficult are difficult to monetize. In a February 25, 2005 letter from the Director of Natural Resources and Environment, R. Nazzaro, to the Chairman of the Committee on Resources, U.S. House of Representatives, R. Pombo, the impact of alien species on the environment was characterized as such: “But invasive species are not limited to just agricultural lands, and there is growing awareness that they also cause harm to other types of ecosystems and natural resources such as forests, rangelands, and urban areas by, for example, crowding out native species, and affecting the frequency of wildfires. The spread of invasive weeds in these nonagricultural areas is said to resemble an explosion in slow motion, and weeds now cover an estimated 133 million acres in the United States” (United States Government Accountability Office Appendix A). The Environmental Protection Agency (EPA) is in the process of developing methodologies to identify, quantify, and value ecological benefits so that EPA regulations are justified by cost-benefit analysis (National Center for Environmental Economics Appendix A). At present, the EPA has produced a draft form (Nov. 3, 2004) entitled Ecological Benefits Assessment Strategic Plan. In terms of funding to support resource conservation including weed control, the U.S. Department of the Interior and USDA provided over $36 million for weed funding in 2004 to other federal agencies, state and local governments, nongovernmental organizations, and private landowners (United States Government Accounting Office, Appendix A). The U.S. Congress recently enacted the Noxious Weed Control Act of 2004, which called for the establishment of a new source of funds for weed management including education, inventories and mapping, management, monitoring, methods development, and other control activities. The law authorizes $15 million for each of five years beginning in fiscal year 2005 and, if fully funded, the authorized amount is approximately 40% of all federal grants dedicated to nonagricultural invasive weed management in fiscal year 2004 (United States General Accounting Office, Appendix A). B. Human Humans have long had an anthropocentric view of the world. We often consider our requirements and our comforts without their connection to or impact on the natural world and, as a result, humans often modify the environment in a way that pleases us in the short run. The satisfaction of dietary, economic, and social needs and desires is met by importing exotic plants that, sometimes unwittingly, cause significant environmental and economic damage. The motives for transporting plants to new areas are (1) secure food sources that are familiar and thus safe;

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(2) a desire for the familiar (a psychological a link to “home”), and (3) a desire to have what is new and different in the case of ornamentals (Mack 2001). A quick glance at most plant catalogs or Internet nursery sites indicates the tremendous popularity of new plant introductions, many of which are exotic. Thus, most invasive species emerge from introduced ornamental plants (Mack 2001), although forestry and agronomic industries, botanical gardens, and the scientific community have also contributed their share (Binggeli 2001; Reichard and White 2001). Unfortunately, an intentionally introduced species yielding economic benefits that becomes invasive results in costs that are not borne by the importers but by the general public (McNeely 2001b). Inadvertent introductions occur via human travel, international trade, and military operations (McNeely 2001a, 2001b). The itinerant nature of humans also plays a role in the spread of plants. Global travel and trade are everincreasing vectors of plant transfer. Human impact on the environment via enthusiastic and cavalier plant introduction can unequivocally be judged as short sighted. Ehrlich (1990) stated: “Ecosystems maintain what may be thought of as a giant genetic library. Humanity has already drawn from that library the very basis of its civilization: the ancestors of all domestic plants and animals and thousands of medicines and industrial products . . . the potential of that library has barely been scratched.” A greater diversity of plant life correlates with more diverse communities of microbes, insects, herbivores, predators, and greater diversity on all trophic levels, from the soil up into the atmosphere (Knops et al. 1999). Since any use of natural resources by humans has some “cost” to biodiversity (Redford and Richter 1999), enhancing our understanding of natural processes will bring us closer to a just compromise (environment versus economics) when faced with the difficult decisions regarding altering the web of life. In the pursuit of human desires and needs, we often disregard biodiversity. Plant diversity and ecosystems can be negatively affected by an introduced plant species depending on the aggressiveness of the species. An introduced alien species (of any phylum) is one of the causes of human-induced species extinction (Myers and Bazely 2003). The juxtaposition of the personal freedom to import what we like versus acknowledging the impacts of importing a potentially invasive species can be viewed as an ethical debate (McNeely 2001a). The impact of an invasive species on the environment, and ultimately a society, is generally unanticipated (intentionally or unintentionally) by the importer. In view of an importer’s self-assumed right to introduce potentially invasive species (in many cases implicitly endorsed by the lack of regulations), the ethics of obligations and responsibility are not understood or recognized.

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Humans are certainly not the only agent of plant spread. Plants and animals have migrated over large distances in the northern temperate regions in the last 10,000 years (Thompson et al. 1995). Most seeds travel short distances (a few meters); however, there are many examples of long distance seed dispersal (> 100 m) via vertebrate, wind, and water distribution with some dispersal distances in the 650 to 1540 km range (Cain et al. 2000). Modern-day invasive species have been introduced by human intervention and the lack of specialized predators, herbivores, and pathogens exacerbates the problem. Elton (1972), in his seminal book The Ecology of Invasions by Animals and Plants, associates the ethics of conservation with the maintenance of diversity, regardless of native or alien status. The following statement suggests an acceptance of inevitable invasions, past and future: “. . . provided the native species have their place, I see no reason why the reconstitution of communities to make them rich and interesting and stable should not include a careful selection of exotic forms, especially as many of these are in any case going to arrive in due course and occupy some niche.” Not everyone is willing to see the intrinsic value of biological entities and the environments in which they exist, independent of their apparent usefulness to humans. The same holds true even when the value applies not just to singular species, but to entire ecosystems, the complex and intertwined “web of life” that has come to be called biodiversity (Redford and Richter 1999). Redford and Richter (1999) aptly stated: “Any human activity that results in substantial natural resource extraction or modification will always entail significant, often unknown, and almost always unappreciated consequences for one or more biodiversity components, primarily by redirecting matter and energy flows.” In this framework, it is a given that agriculture, by its nature, replaces native flora and fauna with a very few crop plants and domestic animals, and thus reduces genetic diversity. It is extraordinary that only 30 crops produce 90% of human calories and proteins, and half of our food derives from only four plant species: rice, maize, wheat, and potato (Janick 2001). The one exception is ornamental horticulture, which greatly increased the number of exotic species in our landscapes. The loss of native biodiversity by invasion of alien species can result in a population that is less genetically diverse than the pre-existing population (Barrett and Kohn 1991). The reduced genetic diversity can cause inbreeding depression which may limit population growth and decrease the probability that a population will persist. However, loss of native biodiversity by invasion of alien species can result in a population that is less genetically diverse than the pre-existing population (Barrett and Kohn 1991).

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C. Ornamental Horticulture The modern ornamental horticulture industry remains largely predicated on the introduction, propagation, and distribution of plants from faraway places. As an example, sorting plants according to their origin in the catalog of a representative large wholesale nursery in Virginia (Lancaster Farms, Suffolk) showed that 65% of the 306 plant species (excluding hybrids) listed in the broadleaf, conifer, and tree categories are not native to North America. This fascination with and desire for exotic plants is not a U.S. phenomenon. Myers and Bazely (2003) show that the exotic flora of Nottingham in the UK and of Spain are primarily from Europe but also from North America, South America, Asia, and Africa. Perrings et al. (2005) cite figures showing that only 2% of garden plants in the UK are native. The appetite for ornamental plants in the U.S. is nearly insatiable and the ornamental plant industry is thriving. The American Nursery and Landscape Association (ANLA, Appendix A ) cites USDA statistics stating that the U.S. is the largest producer and market for nursery and greenhouse crops in the world (American Nursery & Landscape Association). Furthermore, the nursery and greenhouse industry is the fastestgrowing segment of U.S. agriculture. During peak season, the U.S. nursery and landscape industries employ over 600,000 workers (American Nursery & Landscape Association). The USDA Economics, Statistics, and Market Information System reported that the 2003 (estimated) cash receipts for greenhouse and nursery plants in the U.S. were $14.3 billion, which represents a 39% increase in sales in 10 years (USDA Economics and Statistics System, Appendix A). In the U.S., as in the other affluent countries of the world, gardening is a very popular hobby and plant trade is lucrative business (Reichard and White 2001). There is, however, a contradiction between the ornamental horticulture industry and the regulators who oversee their activities. Both entities promote, either explicitly or implicitly, the importation of alien species and take part in the financial gains either by profits or by tax revenue. In contrast, regulators spend a huge amount of money on control of alien plant species, many of which were imported by the ornamental plant industry. Well-publicized nonnative and highly invasive plants such as purple loosestrife are frequently referenced in the invasive plant debate. In the invasive plant debate, the reputations of these oft-cited exotics generally supersede the vast majority of introduced and widely used exotic noninvasive plants. The invasive plant problem cannot be reduced to a simple dichotomy: those plants that are thought to be indigenous and are therefore given the honorable tag “native” versus alien plants, tagged

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“nonnative” or “exotic.” Does a plant native to the U.S. Pacific Northwest (e.g., vine maple) but growing in eastern Maryland retain its status as “native”? Does a pawpaw tree, derived from wild stock in North Carolina, bred for superior fruit in West Virginia, and grown in Massachusetts, remain a “native”? The answer depends on one’s interpretation of the meaning of “native.” In The World Conservation Union definition (McNeely 2001a), a native species lives within its natural range (past or present) and thus the vine maple and pawpaw would not be considered native in their displaced environs. “Native” has been defined in the 1999 Invasive Species Executive Order (Federal Register, Presidential Documents 1999, Appendix A) as: “native species means, with respect to a particular ecosystem, a species that, other than a result of introduction, historically or currently occurs in that ecosystem.” In the widest sense, and often the most commonly used by horticulturists, native refers to a plant within a continental boundary. To demonstrate the ambiguity in the interpretation of nativity, Flora of North America (1993) notes that currently Asian genera (e.g., Metasequoia, Cercidiphyllum, Cunninghamia, Ginkgo, Paulownia, Zelkova, and even Ailanthus, among others) are known to have been indigenous to North America millions of years ago, before losing competitiveness and fading out. Distinguishing native species from nonindigenous species is seemingly apparent, however, recent debate in the biological invasion realm indicates that this distinction is not as apparent as it appears (Lodge and Shrader-Frechette 2003; Donlan and Martin 2004; Lodge and Shrader-Frechette 2004). However, semantics regarding the basis for a plant’s native status do little to devalue the fact that flora presently existing in North America have coevolved over millennia with an almost infinite array of biological checks (e.g., pathogens, parasites, predators) that serve to keep our ecosystems in balance (Mack 1996). Introduced alien species lack such checks, at least in the early stages of invasion. While interest and concern for native species is a worthy horticultural and ecological endeavor, the heart of the invasive plant issue is more pertinently focused on distinguishing between plants that are invasive and those that are noninvasive. There are invasive species that are native, typically termed colonizers by ecologists, and these species tend to share many common attributes with those invasive species that are nonnative or “exotic” (Thompson et al. 1995). An example of one such colonizing native is black locust. Black locust also provides an example of a species that has had its native range somewhat obscured over the course of time, a process begun by Native Americans and continued into the present due to the species’ ability to grow quickly on poor sites and yield useful wood (Little 1980). Other examples of native colonizers, or

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pioneers—plants suited for quick establishment on altered, disturbed grounds—include black raspberry, eastern redcedar, and boxelder. Some alien species “invade” areas without any detectable negative impact on the ecology of that area and are generally considered “naturalized species.” Of course, this distinction depends on one’s interpretation of the definition of “invasive.” Again, the semantics of the debate have a significant impact on how we perceive the “facts” of the debate. The fact that the nursery industry is responsible for a significant portion of invasive species (Reichard and White 2001) is not a coincidence. The industry has imported hundreds of alien plant taxa; some of the same important biological traits that are valuable to gardeners and landscapers are also those that favor invasiveness. Ideal ornamental plant traits such as quick growth, resilience to adverse environmental conditions, and abundance of fruit are also characteristics that make a species economically viable for nursery growers and potentially invasive outside of cultivation (Li et al. 2004). Together with the landscape industry, alien plants travel throughout the country. Thus, attempts to predict the spread of these plants (discussed in the next section) is complicated by the unpredictable nature of human activity. Plant sales via the wholesale and retail markets are essentially vectors of alien plants. The mail order plant business, now made extremely popular with Internet sales, is greatly increasing the spread of alien plants. Thus, beyond the initial introduction of these plants, these market vectors are promoting the opportunities for alien taxa to invade areas previously unexposed to these taxa. Kowarik (2003) shows that “secondary releases” of alien species, i.e., sale and movement of plants through nursery and landscape markets, enhances the invasive potential of plants. Pemberton (2000), in a study of Florida nursery industry sales (1886–1930), found that alien plant species that sold for a longer period of time were more likely to naturalize than those sold for a shorter period of time. If species were sold for one, 10 or more, or 30 or more years, then the percentage of the 1884 alien species that naturalized were 2, 31, and 69, respectively. Should the nursery industry be portrayed, at least in part, as purveyors of potentially invasive species? Or, as the nursery industry justly contends (Barnes 1996), is the industry providing plant material to satisfy customer demand? Putting aside the invasive plant issue, the U.S. nursery industry has grown and distributed millions of plants (since the late 1700s) with environmental benefits such as carbon sequestration, soil erosion control, noise and air pollution amelioration, and the maintenance of wildlife habitat. In terms of economics, the nursery and landscape industry is the fastest growing sector of U.S. agriculture (American

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Nursery & Landscape Association). One of the reasons the nursery industry is flourishing is the public’s desire for novel plant introductions. One can interpret the scenario as the nursery industry fueling consumer demand for potentially invasive species by providing new and interesting plants, and promoting these and other fashionable plants via media such as plant catalogs and magazines. However one views the dissemination of potentially problematic plants, information regarding species having shown invasive tendencies or potential, either elsewhere in the world or here in the U.S., must be shared freely. Professionals responsible for choosing landscape materials should reconsider some of their traditionally used taxa known be invasive, at least in some areas, and keep themselves abreast of the latest information relative to invasive plants. All invasive plant information that is relevant must also reach the consumer public. Since gardeners are generally environmentally-minded, the consumer public will likely influence nursery industry practices concerning invasive plant material. Organizations such as state native plant societies, the Nature Conservancy, and state departments of natural resources and agriculture, as well as federal agencies have developed lists of known invasive species. Many of these lists have been aggregated (see Appendix A for: “Links of Interest” in the Virginia Native Plant Society website (Virginia Native Plant Society); the Plants—National Database Reports and Topics—USDA Natural Resources Conservation Service website (USDA Natural Resources Conservation Service—National Database Reports and Topics): National Park Service (National Park Service—Weeds Gone Wild—Alien Plant Invaders of Natural Areas: More Info; and Environment. A comprehensive listing of international and national invasive plant Internet sites occurs in Plant Talk Resource Page (Plant Talk Resource Page, Appendix A). These published invasive species lists serve valuable functions in informing and bringing about regulatory responses. In addition, invasive plant working groups developing these lists often bring together diverse parties who would otherwise not interact. However, there are two main shortcomings of these published invasive species lists relative to their impact on controlling the sale and use of invasive species and the educational value of these lists. First, since these organizations have independently developed lists, there is a lack of consistency in the information presented by the various states, agencies, departments, and societies. In many cases, criteria to rank species differ among states/organizations, or in some cases invasive species are not ranked or not listed. Also, no information exists on the USDA hardiness zone(s) or regions in which a species will likely flourish. This is a cogent factor, since a

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state such as Virginia encompasses USDA hardiness zones from 5b to 8a. Thus, the difference in minimum winter temperature, for example, can be as great as 16.6°C (30°F) within the borders of a single state and the survivability of a relatively tender invasive species would be much greater in zone 8a than in zone 5b. Heffernan et al. (2001), who conducted the in-depth study Ranking Invasive Exotic Species in Virginia and reviewed the corresponding literature, emphasized the discrepancy among organizations and agencies reporting and ranking invasive species. The second significant problem with the current state of published invasive species lists is that there is no link between the invasive species information generated by the environmentally concerned organizations and the nursery and landscape industries. In general, the nursery industry has not embraced the voluntary responsibility of integrating invasive information in their plant sales literature. An exception to this occurs with Heronswood Nursery (Kingston Washington; to be discussed in Section IVC) and a few other plant vendors. The nursery and landscape industries must make a concerted effort to regulate the introduction and sale of potentially invasive species to demonstrate to the public and regulatory groups their intent to be responsible stewards of our environment. D. Predicting Invasive Potential In comparing the number of alien species that become naturalized to the total number of alien species that have been introduced, Mack (2002) notes a conclusion that has a general consensus among the scientific community: “few immigrant species ever become naturalized.” Mack’s definition of naturalized is a species that produces a permanent population (Mack and Erneberg 2002). Biologists have a keen interest in understanding the reasons why so few immigrant species succeed in naturalizing because such an understanding would increase our ability to predict which alien species are apt to establish permanent populations. In recent years, methods have been devised to predict the invasive potential of introduced species. The accurate prediction of a species’ potential to be invasive is an extremely useful tool for governments, scientists, and land managers. The most commonly used tool has been expert judgment to assess species invasiveness (Predicting Invasions of Nonindigenous Plants and Plant Pests 2002). An example of such an effort is Randall et al. (2001), who used members of an expert network to rank weeds using a list of invasive categories. Heger and Trepl (2003) categorized biological prediction schemes into four approaches: (1) focusing on the characteristics of invading

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species, (2) focusing on the ecosystems invaded, (3) investigating the relationship between the invading species and the environment to be invaded, and (4) differentiating the invasion process in time. They find the invasion process in time approach to be most elucidative since each invasion is unique and is determined by a contingency of events. They also note that the impact of humans is not taken into account by methods of natural science and this component must be taken into consideration to increase the power of prediction. Kowarik (2003), noting the lack of anthropogenic factors in invasive prediction, states “This may also lead to the paradox of acknowledging a broad-scale human mediation of invasion processes in the light of empirical evidence, but virtually excluding it from explanatory or predictive models.” Predictive models have also been categorized by Radosevich et al. (2003) in terms of parameters, advantages, and limitations. Reichard and Hamilton’s (1997) “decision tree,” based on statistical models, is a relatively simple way by which new plant introductions can be screened for potential invasiveness. Such traits as a species’ history of invading elsewhere, vegetative reproduction, perfect flowers (as opposed to dioecious or monoecious), and long fruiting time are highly correlated with invasive potential. Testing (post priori) the models with known invasive and non-invasive taxa yielded 97% accuracy when testing known invasive taxa, and 71% accuracy when predicting noninvasive taxa (Reichard 1996). Widrlechner et al. (2004) found Reichard and Hamilton’s (1997) method to be only 65% effective when employed in Iowa. Widrlechner et al. (2004) modified the “decision tree” and tested alternative methods. Their work ultimately led to a compromise between a method’s ability to successfully classify a species as invasive or noninvasive, and a method’s simplicity and practicality. Widrlechner et al. (2004) incorporated a correlation between the climate of a species’ native range and the climate of Iowa, as well as a non-quantified “quick maturity” variable, and a fleshy, bird-dispersed fruit variable, and achieved 81% correct classification. Their methods also reduced the likelihood of incorrectly predicting an alien species as invasive to 4%. Models, such as those proposed by Widrlechner et al. (2004), will need to be tested in other regions and fine-tuned on a regional basis before they will be able to be used as an a priori tool. Other methods have also been created. Rejmanek and Richardson (1996) created what they believe is a less region-dependent screening procedure based on species biology and some environmental interactions. Peterson et al. (2003), using ecological niche modeling, predicted the geographical distributions of four alien invasive species in North America with a high degree of accuracy. In ecological niche modeling,

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a species’ native ecological niches and native geographical distributions are used to predict the distribution of that species in another area. Panetta (1993) developed a screening system for use in Australia that may be particularly suited for herbaceous plant screening. A weed risk assessment system (Pheloung et al. 1999) serves as a basis for exotic plant introduction regulation in Australia (discussed in Section IV A). This assessment system model rejected species or deemed species as requiring further evaluation that were already classified as serious weeds, while only rejecting 7% of non-weeds. The screening systems of Pheloung et al. (1999), Reichard and Hamilton developed for North America (1997), and Tucker and Richardson (1995) developed for the South African fynbos, were tested on non-indigenous plant species of Hawaii (Daehler and Carino 2000). The North American and Australian systems were most reliable and rejected 82% and 90% of known invasive species, respectively. The Australian system has the advantage of assessing herbaceous as well as woody species (the North American system is designed for woody plants), and can assess risk when the answers to some of the risk assessment questions are unknown (Daehler and Carino 2000). However, the North American and Australian systems rejected 10% and 14% of species known as non-invaders, respectively, and recommended 10% and 32% of non-invaders for further study. While some are concerned with the rejection of species falsely identified as potential invaders (Smith et al. 1999), erring on the side of caution seems defensible on many levels. A disadvantage of risk assessment systems is that they use subjective, qualitative determinations of characteristics of non-indigenous plants, which ultimately reduces the opportunity for results to be replicated (Predicting Invasions of Nonindigenous Plants and Plant Pests 2002). Risk assessment methods that incorporate a quantitative analysis are an improvement “despite the lingering subjectivity in the probability distribution attached to events.” Another method to help curb further spread of already invasive plant species and limit the potential for invasiveness of future plant introductions may come from plant biotechnology. Li et al. (2004) foresee the use of “molecular tools” to develop sterile cultivars of invasive or potentially invasive ornamental plants. For those ornamental plants in which male or female sterility will interfere with the production of attractive and desirable fruits, Li et al. (2004) “believe that a combined use of male sterility, female sterility, and parthenocarpic technologies may lead to the development of “super-sterile” cultivars that are both male and female sterile but that also bear normal-sized fruits (seedless).” They noted that ornamental cultivars advertised as “sterile” are often not sterile but more accurately self-incompatible. Self-incompatible plants

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remain capable of producing abundant seed when functioning as either male or female parents in crosses with nearby, closely related plants (a likely scenario in suburban settings). Li et al. (2004) have recently created a “super-sterile gene cassette” and are currently testing its effectiveness in modifying several invasive ornamental plant species. Whether the use of such technologies will ultimately prove to have practical applications, and whether the public will accept plant materials that have been “genetically modified,” remains to be seen. The ‘Bradford’ pear is an interesting example of a species that was originally thought to be sterile (Sierra Club—Washington, D.C. Chapter, Appendix A). This clone, a result of USDA’s screening of thousands of seedlings for fireblight resistance, is virtually ubiquitous in most of the East and Midwest U.S. landscapes because of its showy flowers, fall foliage color, and tolerance of adverse conditions. New clones of the species (Pyrus calleryana) are serving as cross pollinators and producing heavy fruit set. The fruit are bird-dispersed and the seedling-grown trees are showing up in many areas in the eastern U.S. Clones of the species have been put on several invasive plant lists (see Appendix A: Control of Invasive Non-Native Plants; Plant Invaders of Mid-Atlantic Natural Areas, Trees, Bradford Pear; Tennessee Exotic Plant Pest Council’s Invasive Exotic Plant Pests in Tennessee 2004). Some reduce invasion potential to statistical simplicity and reject the contention that particular invasions are predictable (Gilpin 1990; Williamson 1993; Williamson and Fitter 1996). The “10:10 rule” (Williamson 1993) maintains that approximately 10% of all imported species (brought into the country) will be introduced (found in the wild; feral; casual), and 10% of the introduced only 10% will ultimately become “pests” (with a negative economic effect). Of course, the 10% figure is an approximation and the author considers 10% as statistically similar to values that occur in the range of 5% and 20% of species moving from one stage to the next. Williamson and Fitter (1996) revised the 10:10 rule by inserting the level “established” between the introduced and pest levels, established meaning a self-sustaining population; naturalized. Thus, the new scheme was the 10:10:10 rule. In the former scheme there is a 1% chance of a species becoming a pest, whereas in the latter scheme, there is a 0.1% chance of becoming a pest. These authors noted significant exceptions to the rule with imported crop plant species having a much greater tendency for being in the introduction, establishment, and pest levels than predicted by their scheme. Lockwood et al. (2001) tested the 10:10 rule for invasive plant species in California, Florida, and Tennessee. They found that the proportions of established alien species in these states that invaded natural areas were

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5.8%, 9.7%, and 13.4%, respectively, and the 10:10 rule was validated since these values fall within the expanded 5% to 20% limits of the rule. Kowarik’s (1995) research also supported the 10:10 rule. Smith et al. (1999) use the generalized proportion (10:10 rule) to contradict predictive models such as those proposed by Reichard and Hamilton (1996) and Pheloung (1995). However, Rejmanek (2000) and Kowarik (1995), refute the 10:10 rule. Their contention is that the proportion of invasive introduced plants is not constant. They contend that the ratios are very much confounded by several factors: a phenomenon called lag time (discussed in the next section), the number of individuals of a species introduced or present at any one time, and other factors such as climate change and disturbance. Kowarik (1995) based his skepticism regarding the 10:10 rule on observations made in North America, Europe, and eastern Asia. A review on the subject of the ecology of introduced plants is given by Myers and Bazely (2003).

III. ECOLOGY OF INVASIVE SPECIES Ecology studies the distribution and abundance of living organisms and the interactions between organisms and their environment. All biological entities exist with dynamic relevance to their surrounding entities, and every change within a system affects the entire system to some degree. In McIntosh’s (1985) review of ecological philosophies, Lewontin crystallizes the essence of ecology: “It is not that a whole is more than the sum of its parts but that the parts themselves are re-defined and recreated in the process of their interaction.” Regardless of where one’s bias originates concerning the invasive plant debate, there is much to be gained by attempting to understand the world from an ecological perspective. Within the broad field of ecology, a subfield has evolved with many scientists grappling to understand the dynamics of invasive species, especially nonnative species (a phenomenon most ominously termed “bioinvasion”). The field of invasion biology emerged in the early 1980s as a result of the increased scientific interest in invasion biology and the realization that world trade and world travel increase the frequency of invasion (Reichard and White 2003). There is a vast literature on the ecological aspects of invasive plants; the intent of the following paragraphs is to describe the fundamental aspects of plant invasion ecology. The negative impacts on environments are well documented. Macdonald et al. (1989) described the effects of alien invasive species at the ecosystem level and at the community and population levels. At the ecosystem level, alien invasive species alter 1) geomorphological processes

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(e.g., erosion rate, sedimentation rate, water channels), 2) hydrological channeling (e.g., water-holding capacity, water-table depth, surfaceflow patterns), 3) biogeochemical cycling (e.g., nutrient mineralization and immobilization rate, soil or water chemistry), and 4) disturbance regime (e.g., type, frequency, intensity, duration). At the community and population levels, alien invasive species alter 1) stand structure (e.g., new life form, vertical structure), 2) recruitment of natives (i.e., allelopathy, microclimate shift, physical barrier), and 3) resource competition (e.g., light absorption, water and nutrient uptake, space preemption). For example, some species are known to be atmospheric nitrogen fixers, and they could be expected to enrich the soil where they grow, gradually changing the growing conditions for other species already growing there, or for species that could potentially grow there (Rejmanek 2000). In Hawaii, candleberry myrtle is an invasive nitrogen-fixing shrub observed to quadruple nitrogen fixation on sites (example of ecosystem level soil chemistry alteration) and thereby ultimately change the sites’ vegetational composition (Vitousek et al. 1987). Other invaders are known to have high transpiration rates. Monospecific stands of these kinds of plants can lead to drastic changes in an area’s hydrology (Rejmanek 2000). An example of this ecosystem alteration is the effect of salt cedar on sensitive desert riparian systems in the arid U.S. Southwest (Howe and Knopf 1991). A third example comes from several places in Ireland and the UK where invasive rhododendron has caused a drastic decline in diversity as a result of acidification of the soil. The leaves of rhododendron form a dense mat, rapidly acidifying the soil and altering nutrient dynamics (ecosystem alteration via soil chemistry change) and therefore community diversity (Gritten 1995). All three examples describe changes in fundamental site characteristics that ultimately lead to overall changes in ecosystem activity and functioning. Gordon (1998) reviews several examples of ecosystem and community level alterations using ornamental species that escaped cultivation in Florida. As with all biological events, numerous and often complex interactions occur in invasion biology. As an example, the laurel fig, native to Asia and introduced into Florida in the early 1900s, served as a street tree in south Florida for decades without being invasive (Center for Aquatic and Invasive Plants, Appendix A). However, laurel fig began spreading by bird-dispersed seed in the 1970s as a result of the apparently accidental introduction of a species-specific pollinating wasp (McKey and Kaufmann 1991; Nader et al. 1992). Simberloff and Von Holle (1999) and Lambrinos (2004) emphasize the need for elucidation of these interactions, which can have serious impacts on the environment. Invasive alien species also have a significant effect on the composition and function of soil biota. As an example, research by

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Klironomos (2002) showed that an alien species introduced into a new environment will be free from attack by its indigenous pathogens and benefit from mycorrhizal fungi that tend to have a more broad host range than pathogenic fungi. Thus, even a plant that is rare in its native environment is a potential invader in a new environment (Van der Puten 2002). Wolfe and Klironomos (2005) note that our current understanding of plant invasion and soil biota interactions is “weak,” and that there is a need “for elucidating basic principles of community ecology and for the successful management and restoration of invaded communities.” Interactions involving global change processes such as nitrogen deposition, enhanced CO2 levels, and climate change will undoubtedly affect the pool of invading species, potential invasion pathways, and the vulnerability of native habitats to invasion (Chornesky and Randall 2003). A. Lag Time The centuries of eager and optimistic plant introductions previously described have likely created a kind of invasive plant inertia. Even without a single new (deliberate) plant introduction, invasive species, as of yet unrecognized, will continue to emerge. The concept of lag time or lag phase refers to the amount of time following initial introduction for a species to establish enough of a population base so that it can begin to invade, or expand its population exponentially. Radosevich et al. (2003) characterized lag time as “the early phase of an exponential population increase during colonization or the existence of a threshold constraining the establishment of a metapopulation of the new species.” Initial studies in Germany found average lag phases of trees to be 170 years, and, for shrubs, 131 years (Kowarik 1995). However, citing the time of settlement by Europeans, and the advent of invasive species in the U.S. Pacific Northwest, Reichard and White (2001) believe lag times to be less, especially for herbaceous species. This is to say nothing of those plants without significant lag times typically called “weeds,” generally colonizers with fast resource acquisition rates (high photosynthetic, respiration, and transpiration rates), broad adaptability of seeds (early reproductive maturity, germination requirements fulfilled in many environments, secondary, environmentally induced dormancy with great longevity of seeds afterward), and a host of potential other traits that assist in speedy and aggressive colonization of disturbed areas (Roy 1990). The concept of lag time implies that the screening of potentially invasive nonnative plants by way of controlled field-testing is impractical, especially for woody shrubs and trees. Reichard and White (2001) suggest that delayed introduction and field-test screening may still be useful with some herbaceous

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species. Other time-related difficulties for prediction or anticipation of invasive species include latent invasions by a species due to changes in the environment (e.g., climate trends), genetic changes within plants themselves, or the advent of new pollinators or seed dispersers (Reichard and White 2001). Lag time and an unstable array of stochastic forces combine to account for much of the difficulty in predicting and anticipating invasive species. Egler and Niering (1976) expressed the difficulties inherent in the prediction of vegetation succession this way: “. . . both environment and species are unstable changing phenomena, with both gradual and catastrophic alterations in both time and space that can only be referred to as chance and coincidence . . . we must face the unpleasant scientific fact that to a large extent vegetation is unpredictable—ecological dogma not withstanding.” B. Environment The potential of a particular area to be invaded varies between communities. Stohlgren et al. (2003) refute the long-held contention that low plant diversity habitats are more vulnerable to invasion than high diversity habitats. These authors present a case that areas of high plant diversity are more vulnerable to invasion than areas of low plant diversity. A common misperception is that invasive plants only succeed in disturbed areas (i.e., highways, vacant lots, abandoned agricultural lands, clearcuts). Rejmanek (1989) points out that “. . . there seems to be no community without some degree of natural disturbance” and relates an area’s potential to be invaded to three factors: succession stage, moisture gradient, and natural disturbance. Garlic mustard, english ivy, and herb robert are examples of invasive plants that are known to succeed in natural areas of no significant disturbance. Roy (1990) points out that disturbances occur in all communities, regardless of ecological succession stage, and that while disturbed communities are more prone to invasion, all communities are subject to invasion. MacDougall and Turkington (2005) investigated whether dominant invasive species drive community change (driver model) or are “along for the environmental ride” (passenger model) in a disturbed ecosystem. In the driver model, community structure is altered by competition due to a highly interactive community and dominant species out compete subordinate species. In the passenger model, community structure is affected by non-interactive factors (environmental change, dispersal limitation); dominant species are less constrained, and therefore dominate the subordinate species. These authors concluded that the passenger model was the “underlying cause of exotic dominance, although their combined effects (suppressive and facilitative) on community structure are substantial.”

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Pertaining to succession, those plant species adapted to colonizing pioneer communities are often the very same species (or class of species, e.g., ruderals—those species tolerant of harsh conditions that mature quickly and spread profusely) that demonstrate invasive behavior. Therefore, areas in an early stage of succession are bound to be populated with species of an invasive nature, which leads to their characterization as “more apt to be invaded” (Rejmanek 1989). Certainly, plants exhibiting pioneer traits are indeed valuable and necessary in natural settings. As succession stages mature, the proportion of species in a given environment with invasive potential declines; thus, a system’s potential to be invaded is said to decline as it matures in successional stage (Rejmanek 1989). Invasive species are most abundant in early succession mesic environments. As for the extremes of the moisture gradient, hydric and xeric environments at any stage of succession tend to be less apt to be invaded. If a list of all plants considered to be invasive were tallied, the majority of them would be characterized by their preference for mesic environments in early stages of succession (Rejmanek 1989). The apparent resistance of xeric and hydric communities to invasion is thought to relate to the poor environmental conditions for seed germination and seedling survival in xeric communities, and the high level of native plant competition in hydric communities (Rejmanek 1989). Disturbance—in simple terms, a loss to some degree of biomass or “plant cover”—is the window of opportunity for invasion. Disturbance does not necessarily lead to an invasion unless there is a source or an already existing supply of propagules, some of which may be those of potentially invasive species (Rejmanek 1989). Propagule pressure, synonymous with introduction effort (Blackburn and Duncan 2001), irrespective of disturbance, has been shown to be a positively correlated and one of the primary predictors of invasion success (Kolar and Lodge 2001; Lockwood et al. 2005). The impact of human activity cannot be excluded from the success of an alien species to become invasive. Plant cultivation increases the chance that an alien population will grow to a threshold size and become established (Mack et al. 2000). Not requiring cultivation to persist, such a population is said to be “naturalized” and may eventually become invasive. Thus, humans serve as dispersal agents and guardians for species that otherwise would not overcome the natural barriers to invasion (Veltman et al. 1996). C. Ecosystem Transformations Due to Invasive Species There are numerous invasive plant articles in trade journals and the popular media. Topics range from an entirely “pro-native plant” stance to a “pro-exotic” stance. Many authors of these articles make generaliza-

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tions from specific cases. Such inductive reasoning may be faulty, since the invasive plant issue is quite complex and often very specific to stochastic factors dependent on place and time. Review of the literature has shown many contradictory studies, conclusions, and opinions. 1. Purple Loosestrife. Purple loosestrife is a case in point of opposing scientific conclusions regarding an invasive species. Purple loosestrife is a case in point of opposing scientific conclusions regarding an invasive species. One of the most well-known invasive plants in the U.S., dubbed by some the purple plague, purple loosestrife is thought to have been first introduced to North America from Northern Europe in the early 1800s via ship ballast, soil dug from marshy ports in Europe and carried across in hulls to improve ship stability and draft, then dumped to accommodate the increased cargo loads on the return trip back to Europe (Thompson et al. 1987). Colonist also may have deliberately brought seeds to North America because they valued the plant as a medicinal herb. Expansion of purple loosestrife was facilitated by the era of canal construction and the associated disturbances of the riparian and marshy wetland areas. Completion of the Erie Canal in 1825 led to construction of more than 4,800 km of canals in New England, New York, Pennsylvania, New Jersey, and Ohio. Today, purple loosestrife is a common sight in wetlands from New England to Minnesota and from Delaware to Indiana. This invasive species is also known to occur in western North America from British Columbia to northern California, and in arid regions such as Utah, Wyoming, and Colorado, as well as sporadically across the Northern Plains Prairie Pothole region of the U.S. and Canada. Many other states have spot infestations. The more recent infestations of purple loosestrife in the alkaline watersheds of the semiarid and arid western U.S. are an unpleasant surprise to scientists and land managers. The spread and dominance of purple loosestrife is widely accepted to be detrimental to wetland ecosystems. Dense stands of purple loosestrife are said to be a serious threat to species diversity of both wetland flora and fauna. “Although we need quantitative measurements of the effects of various stages of Lythrum salicaria [purple loosestrife] invasion on the structure, function, and productivity of North American wetland habitats, the replacement of a native wetland plant community by a monospecific stand of an exotic weed does not need a refined assessment to demonstrate that a local ecological disaster has occurred” (Thompson et al. 1987). Many studies have substantiated this view. Purple loosestrife has been shown: (1) to be a superlative competitor (Keddy et al. 1994; Weihe and Neely 1997; Weiher et al. 1996), (2) to reduce the population of cattail species (Mal et al. 1997), and (3) to alter the composition of wetland

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bird and insect communities (Blossey 1999). Other reports attribute declines in water fowl and muskrat habitat suitability to purple loosestrife dominance (Thompson et al. 1987). However, generally unmentioned in the purple loosestrife dialog are the several studies that have failed to find conclusive quantitative evidence backing the allegations that purple loosestrife negatively impacts plant species diversity in wetlands (Anderson 1995; Hager and McCoy 1998; Farnsworth and Ellis 2001). Treberg and Husband (1999) in Ontario, Canada, found no relationship between the density of purple loosestrife stem area and the diversity of other associated wetland plant species. Farnsworth and Ellis (2001), using multiple and diverse sites and greater numbers of quadrats per site than had previously been used in other studies, found a weak correlation between increasing biomass of purple loosestrife and lower biomass of other species. However, like Treberg and Husband (1999), they did not find a correlation between density of purple loosestrife and diminished diversity of other plant species. Farnsworth and Ellis (2001) suggest the discrepancies regarding the impact of purple loosestrife relate to the size of the study area and the fact that many studies are small-scale and short-term. Within the scientific community, no one denies or debates the competitive superiority of purple loosestrife or its ability to spread far and wide. Rather, the question remains whether the spread and dominance of purple loosestrife constitutes an “ecological disaster.” 2. Spartina. Invasive populations are subject to impermanence and instability. Whether countered by natural occurrences or by humaninfluenced occurrences, large populations of invasive plant species display a natural vulnerability to pathogens, plant-feeding invertebrates and other debilitating organisms, or sometimes yet to be understood forces. Elton (1972) terms this natural return to some semblance of equilibrium as “ecological resistance.” Spartina and the following plants are examples of invasive species that have succumbed to natural forces. Alien plant species, as well as alien fauna, that show utter dominance in their new environments, achieving dense, monospecific stands, have been known to experience a spontaneous population collapse. Such collapses are a “minor phenomenon in invasive biology” which may be related to pathogens but often the cause is unknown (Simberloff and Gibbons 2004). The case of spartina, an intertidal salt-marsh cordgrass colonizing the coastline of Great Britain for the last century, is an example of a spontaneous population collapse (Thompson 1991). Spartina is a perennial grass that spreads by rhizomatous vegetative (clonal) growth. Interestingly, spartina (Spartina anglica) is the result of a natural

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hybridization between Spartina alterniflora (N. American origin) and Spartina maritima (European origin). The hybrid was initially sterile, but chromosomal doubling occurred and a new species (S. anglica) was created possessing the genetic complements of both parent species (polyploidal) (Thompson 1991). This new spartina was able to fill a vacant niche, the frequently inundated low-lying intertidal mudflats. The grass’s ability to collect tidal sediment (10 cm per year) and its rapid clonal growth transformed a virtually barren mudflat into a monospecific meadow-like sward in just a couple years (Thompson 1991). However, observations since the late 1980s have witnessed spartina tidal meadows dying back. The cause of this population decline is an ergot fungus (Claviceps purpurea) that infects inflorescences and prevents the formation of viable seed (Thompson 1991). A less definitive cause of decline is thought to be soft-rotting of rhizomes in over-mature populations due to prolonged anaerobic toxicity (Thompson 1991). Thompson stated that vegetative reproduction, “. . . may represent an Achilles’ heel for long-term persistence. If genetic variation is low, S. anglica may yet succumb, like other monocultures, to parasite or pathogen infestation.” 3. Elodea. Elton (1972) gives another interesting account of an invasive species’ rise to dominance and subsequent decline. Elodea (also known as Canadian pondweed) is a submerged aquatic plant from North America, inadvertently imported to Great Britain in the 1800s via American timber logs. From the time elodea was first observed in a pond on the Scottish border, several decades of population explosion followed, resulting in the clogging of rivers, canals, lochs, ponds, and ditches across Great Britain. At its peak, throughout the 1860s, elodea rendered parts of the Thames River impassable. At Cambridge, along the River Cam, elodea interfered with rowing and caused the necessity of extra teams of horses to haul barges through thick mats of vegetation. Following the 1860s, the elodea population drastically, mysteriously, declined. Elton (1972) concluded, “The plant is still quite easy to find living in moderate and permanent occupation of many waters. The reasons for its decline are quite unknown. They could be genetic, or indicate the exhaustion of some rare food element. In some places control was helped by cattle and waterfowl eating it. But one thing is quite certain: man did not directly control this weed.” 4. Prickly Pear. The preceding two examples involved population declines uninfluenced by human interference. In contrast, the story of prickly-pear (Opuntia spp.) in Australia is one of the most dramatic cases

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in the history of invasion ecology. The rise and fall of opuntia is also a major event in the modern history of human-induced biological control campaigns against weedy species (Zimmerman et al. 2000). Opuntia is a large genus native to the Americas with a myriad of traditional, culturally important uses (Dodd 1940). Introduction of opuntia to Australia, as well as other places such as South Africa, India, Madagascar, and the Mediterranean region, can be originally attributed to opuntia’s traditional use in the cochineal industry, in which certain species are used as host plants in the rearing of the scale (mealy-bug) insect Dactylopius coccus, which in turn is used to produce a reddish “carmine” dye. As modern dye techniques developed and the use of cochineal insects diminished in importance, the continued introduction of American opuntia is thought to be largely attributable to the ornamental lure of the prickly-pear, which displays many phenotypic varieties. A third, less significant reason for introduction may occasionally have been for the use of opuntia fruits as a food source (Dodd 1940). First introduced to Australia in 1787, opuntia achieved its peak population during the 1920s, with a rate of spread considered by many observers to be no less than a “botanical wonder” (Dodd 1940). At its peak, opuntia covered 24 million ha (60 million acres) of Queensland and New South Wales; 12 million ha (30 million acres) were said to be so densely covered with opuntia that they were rendered completely useless from a production standpoint (Dodd 1940). Aspects of opuntia’s biology partly account for its ability to establish, persist, and thrive in Australia (and elsewhere), yet the case of opuntia in Australia also provides another example of an invasive plant demonstrating cryptic climatic adaptation. Detached opuntia segments (cladodes) remain alive and capable of producing roots and new growth for months without favorable conditions and this makes importation and dissemination a simple exercise. Opuntia also puts forth abundant fruits that are highly palatable to many birds and other animals and these fruits contain seeds that can remain viable for as long as 15 years. Opuntia is also very tolerant of drought, and though often considered a desert species, generally thrives in areas of moderate rainfall (Dodd 1940). Native to coastal Texas and Florida, Opuntia stricta, the species that most plagued Australia, thrived in its new range in areas much farther removed from the coast, at much higher elevations, and with considerably less annual precipitation (Dodd 1940). The spread of opuntia went largely unchecked for two main reasons. The vastness of land holdings characteristic of post-colonial Australia allowed populations of opuntia to go virtually unnoticed by landowners. The second reason for the unimpeded opuntia spread was due to the low value of the land it often occupied; practical economics rendered

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chemical or manual control efforts unfeasible given the unimproved nature of the land. The cost of fighting the spread of opuntia was many times that of the value of the land. Efforts including engineering water catchments, removing scrub trees, and building homesteads, other shelters and fences needed to be done before the land could be inhabited and considered valuable, i.e., useful for grazing and farming purposes (Dodd 1940). Also, as is often the case with invasive plants, the problem with opuntia was steadily exacerbated by continuous human introduction. At the same time opuntia was establishing strong population bases in remote areas, many Australians continued to plant opuntia for hedges around their homesteads (Dodd 1940). From approximately 1918 through the mid-1930s, Australian scientists conducted research on opuntias and their native enemies in many foreign locations, from the U.S. southwest, throughout Mexico, into Central America and the Caribbean, and southward to Argentina and Brazil. In 1925, a moth native to South America, Cactoblastis cactorum, was released in Australia as a biological control agent against the invasive opuntia. The moth functioned as an enemy by feeding gregariously while in larval stage on the internal tissue of opuntia cladodes, ultimately causing host plants to collapse into pulpy piles of decay (Zimmerman et al. 2000). Massive rearing and dispersing efforts helped C. cactorum become established, and the moth’s subsequent proliferation and impact on opuntia populations was successful far beyond Australia’s hope and expectations. Over the course of one decade, 1925–1935, the opuntia infestation problem was completely under control (Dodd 1940). But the story of opuntia and Cactoblastis cactorum did not end in Australia in 1940. Based on the success of C. cactorum in Australia, the moth was introduced for similar measures in many other locations around the world. The introduction of C. cactorum in 1957 to the Caribbean Islands was not considered controversial at the time. However, C. cactorum was observed in Florida in 1989, and the wisdom of the 1957 Caribbean introduction came into question. Great anxieties about the fate of native opuntia species throughout the U. S. and Mexico began to arise (Zimmerman et al. 2000). The very same nonspecific (oligophagous) host habit that made C. cactorum so useful in Australia now suggests its potential to be extremely harmful in the U.S. and Mexico where at least 79 species of opuntia between the two countries will be vulnerable (Zimmerman et al. 2000). Investigations as to how C. cactorum arrived in Florida are inconclusive, though recent studies suggest there is strong evidence the moth arrived not by natural dispersal, but via horticultural shipments originating from any number of Caribbean islands. For instance, between 1981 and 1986, 13 interceptions of C. cactorum

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infected opuntia were made at Miami area ports. The cultivation of opuntia species in places such as the Dominican Republic for horticultural purposes is commonplace. Throughout the 1980s, over 300,000 opuntia plants were imported annually into the U.S through Miami. The number of opuntia plants imported unofficially by cactus collectors and black marketers may have also played a significant role in the entry of C. cactorum into Florida (Zimmerman et al. 2000). C. cactorum is a serious threat to native opuntia in Florida as well as Mexico. Opuntia fruit infested with C. cactorum was intercepted at an airport in Texas in 1995 (Stiling 2002); thus, the movement of this moth to the U.S. southwest and Mexico seems inevitable. The rate at which C. cactorum has spread through Florida is alarmingly swift when compared to observations made from past introductions in Australia, South Africa, and the Caribbean. The possibility exists that the relatively low densities of opuntia in Florida have encouraged increased natural dispersal of C. cactorum in search of suitable hosts. This natural dispersal combined with frequent human-mediated transport of larvae-infected horticultural material has helped the moth travel as far north as Sapelo Island, Georgia (Zimmerman et al. 2000). The impact of the spread of this moth is significant. Traditional uses of various opuntia species include both cultivated and wild sources of animal fodder, fruit and other food items for human consumption, pharmaceuticals, cosmetics, and carmine dye. The Opuntia genus is important to the Mexican culture; both the national flag and modern-day Mexican coat-of-arms include portrayals of opuntia plants (Zimmerman et al. 2000). Rare and endangered opuntia species in the U.S. and Mexico are in danger and the potential of extinction exists (Stiling 2002). 5. Ailanthus. As demonstrated by the still-unfolding story of opuntia and C. cactorum, the future of human-mediated biological control efforts will likely be guided by a philosophy that willingly compromises degree of effectiveness in exchange for greater conservativeness. Effectiveness will not necessarily be compromised, but vague concerns regarding future possibilities of impacts on non-target organisms will likely bear greater weight in decision-making processes than they once did. For instance, augmentation of biological control agents already present in an area (whether these agents are truly indigenous or of unknown origin, a difficult distinction, as is often the case with fungal pathogens) would seem to be more conservative in nature than the introduction of biological control agents wholly unknown to a region. For example, ailanthus (tree-of-heaven) is an introduced tree species that is regarded as an invasive species (Plant Conservation Alliance, Alien Plant Working Group—Tree of Heaven, Appendix A). Stipes (2003) observed declining

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populations of ailanthus along major roadways in Virginia and isolated numerous fungi, including the vascular pathogen Fusarium oxysporum f. perniciosum, the wilt-inducing pathogen also known to be responsible for the decline of the attractive but invasive mimosa tree. F. oxysporum f. perniciosum was first observed around 1930 in North Carolina, and its status as indigenous or exotic is uncertain (Sinclair et al. 1987). Stipes (2003) proposed the use of F. oxysporum. f. perniciosum as a mycoherbicide, an alternative approach to traditional herbicidal management of pervasive, difficult to eradicate, ailanthus colonies. Interestingly, landscape and naturalized populations of the alien invasive mimosa (silk tree) (Plant Conservation Alliance, Alien Plant Working Group—Silk Tree, Appendix A) are also subject to the lethal F. oxysporum. f. perniciosum (Florida Division of Forestry, Conservation and Management, Appendix A) and provides another example of a nonnative and widely naturalized species facing “ecological resistance.” See Culliney (2005) for a thorough review of classical biological control as a tool for managing invasive plants. 6. Multiflora Rose. Another example of a nonnative invasive species experiencing population decline involves multiflora rose, the hardy Asian ornamental and soil stabilization species long introduced and promoted in the United States (Plant Conservation Alliance, Alien Plant Working Group—Multiflora Rose, Appendix A). As a result of such a long history of importation and zealous government encouragement, over 45 million acres of land, primarily in midwestern and eastern parts of the U.S., have been impacted, and in terms of grazing and recreational uses, degraded. However, Epstein and Hill (1999) report rising incidence of an endemic, eriophyid mite-transmitted disease, rose rosette disease (RRD) that is lethal to muliflora rose. Rose rosette disease is caused by what remains to be an uncharacterized etiologic agent, and has shown a host range restricted to the genus Rosa, within which many native species show strong resistance. Several ornamental rose hybrids show mild susceptibility to RRD (e.g., R. rugosa × R. odorata cultivars), while many important rose-related (Rosaceae) species have demonstrated a high level of resistance (e.g., species and their cultivars from the genera Malus, Pyrus, Prunus, Rubus, and Fragaria) (Epstein and Hill 1999). Rose rosette disease is widely distributed in the area from Kansas east to West Virginia and Pennsylvania, and Iowa south to Tennessee, and is slowly and steadily helping diminish the obnoxious presence of the thorny, often impenetrable multiflora rose (Epstein and Hill 1999). In Iowa, augmentation of RRD-infected populations of multiflora rose by human endeavors has resulted in reclamation of highly infested pastures within 5 to 6 years (Epstein and Hill 1999). Peck et al. (2003) have

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observed RRD as far east as Maryland, Virginia, North Carolina, South Carolina, and Georgia. The examples of spartina, elodea, opuntia, ailanthus, mimosa, and multiflora rose serve to demonstrate the tendency of natural systems, in varying degrees, to reassume a state of ecological equilibrium following periods of unnatural influence exerted by introduced alien species. Of course, the case of opuntia and the introduction of Cactoblastis cactorum represents an extreme scenario, a paradoxically unnatural solution to an unnatural problem: the massive-scale introduction of an oligophagous moth native to South America to combat unruly populations of cacti native to North America growing out of control on a third continent, Australia. The story of opuntia and C. cactorum is certainly a very impressive example of both human ignorance and human cleverness and the occasional result of both to effect great changes upon the natural world. Arguably, the story of ailanthus is one of the more exaggerated examples of bioinvasion; while its prolificness in the eastern U.S. is undeniable, it has not established monotypic populations approaching the magnitude of spartina, elodea, or multiflora rose, to name just a few. Examples of spartina, elodea, and multiflora rose represent an optimistic view of the effects of bioinvasion. They serve to remind us that ecological resistance is a force to be reckoned with, regardless of human meddling and human understanding of such processes.

IV. REGULATORY MATTERS All the preceding ideas and information collectively demonstrate the complexity of devising and implementing fair, comprehensive, and effective regulations to protect the environment but at the same time allow the nursery industry to thrive. Before the 1900s, the decision to introduce exotic species into the U.S. was primarily made by private individuals with minor, if any, government involvement (Office of Technology Assessment—Harmful Non-Indigenous Species in the United States 1993). At present, federal and state governments have some degree of authority regarding the importation of non-indigenous species. Money is a central issue to any regulation concerning potentially invasive species. For horticulture species, regulation will limit (or prevent) the introduction of potentially invasive species, and reduce sales, profit and employment. However, a lack of regulation will inevitably allow the floodgates controlling alien species to remain open, resulting in taxpayer dollars spent on controlling alien weed species. Regulation itself repre-

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sents a cost to taxpayers. We discuss next the regulation of invasive species in terms of international, federal, state, and self-regulation perspectives. A. International Aspects Since the invasive plant problem is international in nature, the prominent role of the World Trade Organization (WTO) in invasive plantrelated matters further exemplifies the complexity and bias that so often surrounds the debate. With the advent of the WTO in 1994 also came an Agreement on the Application of Sanitary and Phytosanitary Measures (SPS agreement), and the revision of the International Plant Protection Convention (IPPC, in place since 1951) to bring it into accordance with WTO goals. The IPPC is one of two main international agreements regarding alien species; the other is the Convention on Biological Diversity (CBD). The United States has signed and ratified the IPPC treaty but only signed and not ratified the CBD treaty. The SPS agreement explicitly promotes international trade while restricting phytosanitary safeguards and underestimating the ramifications of biological invasion. Under SPS/IPPC agreements, a country that is part of the WTO is not free to establish phytosanitary safeguards without scientifically-based, species-specific risk assessment. The multilateral North American Free Trade Agreement also requires risk assessment for limiting movement of goods based on SPS reasons (Simberloff 2005). This pro-trade position disregards the immense variety and number of unstudied species that have the potential to be problem plants, and associated plant pests and pathogens. For example, fewer than 5% of the Earth’s fungi have yet to be named, and fewer still have been comprehensively studied (Campbell 2001). Also disregarded are the real-life challenges to scientific endeavors such as funding, and logistics related to ecological scope and international scale (Campbell 2001). In essence, the paucity of scientifically-based information regarding the great majority of potentially harmful organisms makes species-specific risk assessment next to impossible. Relative to the WTO’s requirement for scientifically-based, speciesspecific risk assessment, governments and the scientific community are challenged to devise systems that encourage the collection of information relative to invasive species. However, the economic costs of research to assess a particular risk can be prohibitively expensive. For example, in 1991 a risk assessment for the importation of larch logs into the U.S. cost the USDA approximately $500,000 (Jenkins 1996). To generate funds for the assessment and control of invasive species, Jenkins

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(2001) suggests the implementation of fees and taxes. He proposes three categories of individuals who should pay fees: (1) receivers of an intercontinental imported plant or seed, (2) international travelers (by plane or ship), and (3) owners of a cargo plane or ship that makes an intercontinental arrival with cargo in it. Perrings et al. (2005) propose an ‘invasion risk-related tarrif,’ imbedded in trade agreements, to impart the cost an importer’s action to the importer. To support their proposal, they cite Costello and McAusland (2003) whose model shows that import tariffs reduce import volumes of risky species. To avoid the financial imposition that a tariff would potentially impose on poor countries, Perrings et al. (2005) suggest that tariffs be used in conjunction with international aid to countries who cannot afford to monitor and control the flow of potentially invasive species. In view of the current international trade scenario, the likelihood of international agreements and cooperation to implement such fees and taxes seems unlikely. Simberloff (2005) questions the value of risk assessment to determine the net impact of the introduction of an alien species. He points out that risk assessment procedures “are narrowly focused, subjective, often arbitrary and unquantified, and subject to political interference.” He contends that risk assessments rely on inexact quantification and prediction, and are perfunctory exercises that generally do not result in denying the introduction of an alien species. Simberloff also questions the value of cost-benefit analysis since benefits are generally conferred to an industry and costs are shared by the public. As an alternative to conventional risk assessment, he proposes the adoption of a more conservative method termed alternative assessment developed by O’Brien (2000). The three key components of alternative assessment are (1) precaution, (2) focusing on the goals of the introduction, and (3) examining an array of alternatives to fulfilling the goal. The Committee on the Scientific Basis for Predicting the Invasive Potential of Nonindigenous Plants and Plant Pests in the United States, composed of renowned invasive species experts and convened by the National Research Council, assessed the current scientific status of harmful non-indigenous species and presented recommendations for action in dealing with the future introduction of harmful non-indigenous species (Predicting Invasions of Nonindigenous Plants and Plant Pests 2002). The committee found that the “the current basis for evaluating the potential risks by newly introduced species is not adequate to address the problem of biological invasions—a problem that is certain to continue growing the coming decades.” The committee’s recommendations were directed toward (1) the regulatory activities of APHIS (Animal and Plant Health Inspection Service; a branch of the USDA), (2) the

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documentation and standardization required to better understand invasions, (3) needed research, and (4) organizational infrastructure and scientific expertise required to increase the multidisciplinary understanding and predictive accuracy of invasive species. These recommendations were delivered with urgency in view of the increasing volume of trade and the growing number of countries that are linked via trade to the U.S. Such trade will inevitably result in an ever-increasing amount of non-indigenous species delivered to U.S. ports. Another avenue of importation is Internet-based sales and seed exchanges. Discovering that vendors were selling banned plants on the Internet, an APHIS official, L. Fowler, collaborated with researchers from North Carolina State University’s Center for Integrated Pest Management and the Fast Search & Transfer Company to develop a high-tech enforcement tool, called the Agricultural Internet Monitoring System (AIMS) for use in early 2005 (North Carolina State University News Release. 2004 Appendix A; Water Conserve—A Water Conservation Portal [citing Christian Science Monitor article] Appendix A). In a pilot test, the AIMS system detected over 4,700 distinct pages on websites of U.S. suppliers that were potentially selling banned plants. Western Australia has recognized the threat that Internet seed sales pose to the environment and agriculture and has a program for citizens to determine whether their desired species is acceptable for importation (Department of Agriculture, Government of Western Australia, Appendix A). Citizens are warned that anyone who deliberately violates Western Australia’s Quarantine Laws is subject to severe penalties ranging from fines to jail terms. To control illegal plant propagule imports, Western Australia Quarantine Authorities screen mail with sophisticated x-ray devices and highly trained detector dogs. The recent popularity of medicinal plants and herbs has also resulted in invasive plant problems in some areas of the U.S. (Predicting Invasions of Nonindigenous Plants and Plant Pests 2002). Australia has implemented a model Import Risk Analysis (IRA) system (AQIS Import Risk Analysis Handbook, Appendix A) to regulate exotic species imports. The IRA system is based on six assessment principles that are to be: (1) conducted in a consultative framework; (2) a scientific process and therefore politically independent; (3) transparent and open process; (4) consistent with both Government policy and Australian international obligations (under the SPS agreement); (5) harmonized, through taking account of international standards and guidelines; and (6) subject to the appeal process. Within the IRA system, the Australian Weed Risk Assessment (WRA) system is a model methodology for determining whether to import a non-indigenous species into Australia (Biosecurity Australia, Appendix A). In this system, an importer

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answers up to 49 questions on the species in question, including the species’ climatic preferences, biological attributes, and reproductive and dispersal methods. Answers from these questions generate a numerical score which is then used to accept, reject, or further evaluate the species. A prediction is also made on the potential for the species to be a weed of agriculture or the environment. The person who oversees the WRA in Australia, R. Randall, doubts that any screening system would work without regulation (Environment Hawaii 2002, Appendix A). Randall supports his contention by citing New Zealand’s attempt to halt the distribution of weedy plants by nurseries via a voluntary system. A minority of nurseries did not adopt the voluntary system and New Zealand therefore instituted a regulatory system. With regard to the U.S., Randall stated “I doubt the situation would be any different in the U.S. and would probably be worse, considering the market size and economic forces in operation. Money first, environment second.” In view of the need for a better scientific understanding regarding invasive plants and bioinvasion, in general, a more conservative attitude towards introducing the “unknown” seems prudent. Biological invasions are generally irreversible and limited funding might be better spent preventing invasions rather than combating them (Campbell 2001; Fay 2002, Appendix A). Prominent invasion ecologist Marcel Rejmanek (2000) states: “Early detection of an invasive organism can make the difference between being able to employ feasible offensive strategies (eradication) and the necessity of retreating to defensive strategies with their long-term financial commitments.” Mack and Lonsdale (2001) state: “Individuals and their governments around the world observe a curious ambivalence about the potential spread of plant species. By no rational practice would the parasites of humans or their domesticated animals be freely dispersed.” Considering the risks associated with plant importations, and policies that expressly favor international trade and disregard the risks of bioinvasion in general, Hughes (1994) succinctly characterizes the potential risk as the biotic equivalent of “playing with fire.” B. APHIS The U.S. federal agency chiefly responsible for minimizing the threat of potentially devastating introductions, APHIS (a branch of the USDA), has an almost impossible role to perform. Until recently, the Federal Noxious Weed Act (FNWA), enacted in 1975, was the primary legislation used by APHIS to restrict entry and spread of noxious weeds (Office of Technology Assessment—Harmful Non-Indigenous Species in the United States 1993). The FNWA was relatively weak and criticized by

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environmental groups, scientists (including the Weed Science Society of America), and state representatives. Because the FNWA was an inadequate tool to control the spread of noxious weeds, in 2000 Congress passed the Plant Protection Act (PPA) (Pest Protection and Management Programs, Appendix A). According to APHIS (aphis.usda.gov—Plant Protection Act, Appendix A), “The PPA consolidates all or part of 10 existing USDA plant health laws into one comprehensive law, including the authority to regulate plants, plant products, certain biological control organisms, noxious weeds, and plant pests. . . . The PPA gives the Secretary of Agriculture, and through delegated authority, USDA’s Animal and Plant Health Inspection Service (APHIS), the ability to prohibit or restrict the importation, exportation, and the interstate movement of plants, plant products, certain biological control organisms, noxious weeds, and plant pests. Under the PPA, violators face harsher civil penalties than ever before for smuggling illegal plants or produce that could harbor plant pests or diseases.” To shed darkness on the regulatory scenario, the PPA does not consider the plants being imported by the nursery industry whose invasive potential is unknown. USDA officials have had little choice but to ostensibly “balance” two disparate goals: domestic protection and the continuation of procedures conducive to international trade. Simberloff (2005) characterizes this mission as “profoundly schizophrenic” and suggests that the Secretary of Agriculture should not have the ultimate authority to determine introduction risk because the Secretary’s position is political, closely aligned to the current risk assessment methodology, and represents a single stakeholder viewpoint. To shed darkness on the regulatory scenario, the PPA does not consider the plants being imported by the nursery industry whose invasive potential is unknown. The precautionary “if in doubt, keep it out” stance is incompatible with trade promotion (Campbell 2001). Campbell (2001) states: “Although USDA policy that proves ineffective can be changed through domestic political channels, pro-trade policies now have the force of international law through U.S. adherence to global trade rules enforced by the World Trade Organization (WTO). Thus, if these policies do result in too high a risk of introduction of pests, international treaties adopted by 135 countries must be changed—a daunting challenge.” Personal communications with several representatives of APHIS were generally in accord with the preceding notions of domestic protection and caution ostensibly balanced with trade expedition and logistic complexities due to volume. APHIS has the capability to inspect less than 2% of the cars, trucks, ships, and planes that transport imported products and people (Predicting Invasions of Nonindigenous Plants and Plant Pests 2002). D’Antonio et al. (2004) further illustrate the inspection

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challenge to APHIS by showing that the rate of increase for U.S. horticultural imports exceeds that of total merchandise (1979 to 1999), and the APHIS budget as a function of volume of importation in the U.S. (1970–2000) is decreasing. In terms of current procedures affecting the importation of horticultural material, APHIS recognizes an imminent need to modernize its procedures. Phytosanitary certification, a longstanding rule not quite stringently observed, is now more comprehensively enforced (A.V. Tasker, APHIS, National Noxious Weed Program Coordinator, pers. commun., 2004). The previously mentioned Plant Protection Act of 2000, an act designed to help consolidate and streamline government activities against invasive plant problems, also enabled APHIS to levy more serious fines, which should lead to increasing observance of plant importation protocol (N. Lemon, APHIS, Legislative and Public Affairs, Public Affairs Specialist, pers. commun., 2004). Former President Clinton’s invasive species Executive Order 13112 (Feb. 1999) led to the creation of the National Invasive Species Council and the development of a National Management Plan (NMP) (Federal Register, Presidential Documents 1999, Appendix A). The NMP, in turn, calls for the National Invasive Species Council “. . . to develop and test a fair, feasible and risk-based comprehensive invasive species screening system” (Williams 2001). The National Invasive Species Council relies on the Federal Interagency Committee for the Management of Noxious and Exotic Weeds (FICMNEW) for implementation of Executive Order 13112 and coordination of the 17 federal agencies (Federal Interagency Committee for the Management of Noxious and Exotic Weeds, Appendix A). Goals of the FICMNEW are to (1) develop biologically sound techniques to manage invasive species on federal and private lands; (2) promote weed programs of individual agencies; (3) promote weed programs of individual agencies as well as interagency projects that emphasize weed prevention, timely control, and restoration of degraded lands; and (4) form partnerships with state and local agencies and non-governmental organizations to identify new ways to deal with invasive plants (Westbrooks, 1998). FICMNEW has published Pulling Together: A National Strategy for Management of Invasive Plants to set goals for the control of and protection against alien plants in the U.S. (Westbrooks 1998). At present (June 2005), there is no screening process or risk assessment for horticultural imports, as there is for fruits and vegetables. This is related to historical policies created in an era when fruit and vegetable imports far outweighed ornamental plant imports, in terms of volume and potential risks. In addition, traditional food crops are derived from far fewer genera, about which considerably more scientific knowledge has been accumulated, than is the case with ornamental plant imports (A. Tschanz, APHIS, Director, National Plant Germplasm Quarantine

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Center and Coordinator of the Quarantine 37 Revision Effort, pers. commun., 2004). Different sets of procedures and quarantines have been developed over time that reflect the relatively greater significance of fruit and vegetable imports, compared to ornamental plant intended imports. A substantial increase in the volume of horticultural imports, while not unrelated to World Trade Organization agreements of 1994, is perhaps more the outcome of rapidly increasing consumer demand for such plant material (most likely off-season fruits from tropical and Southern Hemisphere countries) and hand-in-hand industry expansion (P. Henstridge, APHIS Special Assistant to the Deputy Administrator, pers. commun., 2004). Currently, APHIS is working on updating the quarantine procedures pertaining to horticultural imports. Representatives from APHIS foresee in the near future a screening system for horticultural imports, with some of the financial burden placed on the importer (P. Henstridge, pers. commun., 2004). The Australian weed screening system, WRA (previously mentioned in Section IV A), will likely be used as a model, but will have to be modified so as to not impede or conflict with existing international trade agreements observed by the U.S. government as a whole (P. Henstridge, pers. commun., 2004). When asked to estimate how many years from now such a screening system might come to pass, none of the contacted APHIS representatives were inclined to speculate. One serious hindrance to the development of a reasonable screening system and its enforcement is APHIS’ uncertain future operating budget. The recent 2003 Homeland Security Act resulted in the transfer of 2,500 APHIS employees (along with their proportional funding) to the Bureau of Customs and Border Protection (P. Henstridge, pers. commun., 2004). Acknowledging an increased amount of alarm about domestic security against terrorism of all kinds, there is an obvious need to adequately fund the U.S. Department of Homeland Security programs. Simberloff et al. (2005) ascribe the failure of the U.S. to effectively manage invasive species to “insufficient policy, inadequate research and management funding, and gaps in scientific knowledge.” For effective management, these authors point to the need of a comparative policy analysis because the predominant shortcoming is the lack of a coherent set of policies to address the entire invasive issue rather than policies aimed at individual invasive species. They also contend that policy makers are unaware of the “true magnitude of the problem.” C. State and Self-Regulation Despite slow progress in federal programs concerning invasive plants, stakeholders involved in the horticultural realm have shown some signs

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of self-governance and self-regulation The threat of regulation of the introduction and trade of nonnative plants has elicited reaction mainly in the form of meetings and conventions, copious articles, and company and organization position statements. State legislators are gaining momentum in the assertion to ban the sale of some potentially invasive plants. The Governor of Connecticut signed an invasive plant bill that bans the sale, distribution, and cultivation of more than 80 plants (Weekly NMPRO e-mail, June 1, 2004, Appendix A). This ban will cause an estimated $18.7 million loss to Connecticut’s nursery and landscape industries (Weekly NMPRO e-mail, March 16, 2004, Appendix A). Other states, such as New Hampshire and Idaho, have similar legislation pending. In Texas, a person possessing any one of 12 prohibited aquatic plant species commits a Class B Parks and Wildlife Code misdemeanor and is subject to a fine, jail term, or both for each plant possessed (North Texas Water Garden Society, Appendix A). Hawaii, which spends more on the control of invasive plants than any other pest, has adopted a version of Australia’s Weed Risk Assessment system (Weed Risk Assessment for Hawaii and the Pacific Islands, Appendix A). Unlike Australia, the WRA system is not legally binding but is meant to assist in the decision process on introducing an exotic species. A ban on specific species may be justified and necessary; however, due to the complexities described in this chapter, a statewide ban on numerous species may not be appropriate. The impacts of these regulatory actions on the environment and the industry are yet to be assessed but the invasive species regulation on the state level is clearly gaining momentum. The American Seed Trade Association (ASTA) supports environmental consciousness, but opposes efforts to label a species as “invasive” unless “a full and careful consideration of all relevant scientific and economic factors is carried out” (American Seed Trade Association 2000, Appendix A). Another example of a situation seemingly in conflict with itself involves the cultivation of St. John’s wort in Washington State for use as an herbal antidepressant. Changes in state regulation downgraded the herb from a restricted noxious weed (noxious to livestock) to an unregulated noxious weed to facilitate its growth as a commercial crop (Reichard and White 2001). Examples of a proactive behavior by those affected by the potential legal and regulatory actions also exist. The 2004 Heronswood Nursery catalog (Kingston, Washington) explains the company’s efforts to stem the tide of invasive plants. Voluntary stoppage of all shipments to Hawaii and Florida (two states where impacts of bioinvasion have been severe), voluntary restrictions on shipments of known invasive species to other parts of the U.S. where proliferation of such species has been

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documented, and the voluntary tagging of plants as “potentially invasive” concerning species in doubt are some of Heronswood’s selfimposed efforts. As laudable as these efforts are, the catalog continues with a statement characteristic of many in the nursery industry: “. . . by no means should these steps be interpreted by anyone as an apology for what we do. Exotic plants are not the only problem. Thousands of square miles of scarred landscape, urban sprawl, polluted rivers and clearcut forests should elicit that conclusion to anyone who desires to make plants culpable for waning biodiversity, in this country as well as abroad. With a growing governmental interest in regulating what we grow in our gardens, it is my hope that we as a community of gardeners, environmentalists and legislators can cultivate a common wisdom and mutual respect on this subject.” In December of 2001, internationally renowned experts met at the Missouri Botanical Garden in St. Louis to explore and develop feasible voluntary strategies to reduce the introduction and spread of nonnative invasive plants that threaten biodiversity and ecosystems. This meeting resulted in the St. Louis declaration, a concise two-part treaty outlining Findings and Proceedings and establishing Voluntary Codes of Conduct for government agencies, the gardening public, landscape architects, and botanic gardens and arboreta, which can ameliorate the invasive plant problem (Fay 2002, Appendix A). The Voluntary Codes of Conduct stressed six points: (1) assessment of invasive potential prior to introduction or marketing of plant species new to North America; (2) regional focus concerning presently or potentially invasive plant species and identification of comparable alternative species; (3) development and promotion of alternative plant material through selection and breeding; (4) phase-out of existing stocks of unilaterally agreed upon invasive species; (5) strict adherence to importation and quarantine laws; and (6) active encouragement of noninvasive plant use to customers and the general public. The Voluntary Codes of Conduct were endorsed by various organizations including the American Nursery and Landscape Association (ANLA, Appendix A), Florida Nurserymen and Growers Association, as well as The Garden Club of America, The Missouri Botanical Garden, The Chicago Botanic Garden, and the North Carolina Botanical Garden (the latter has both endorsed and adopted the codes). A follow-up workshop to the fruitful 2001 Missouri Botanical Garden meeting was held in October of 2002 at the Chicago Botanic Garden. By the time of this second workshop, the American Society of Landscape Architects (ASLA) was willing to endorse the St. Louis Voluntary Codes of Conduct, as well as the American Association of Botanic Gardens and Arboreta, the Perennial Plant Association, and several other organizations (Fay 2003, Appendix A). Despite the positive measures taken by the aforementioned organizations, with

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the exception of plant sales in Florida (to be discussed), there has been no evidence that these measures have affected sales of invasive or apparently invasive species by the nursery industry. Another example of proactive behavior occurred in Florida. The state of Florida and its particularly severe problems with invasive species of all kinds (as with Hawaii and California) serves as a good example of cooperation amongst professionals of multiple disciplines. Beginning in 1999, the Florida Exotic Pest Plant Council (FLEPPC), a professional society comprised of resource managers and researchers established in 1984, has been meeting with officers of the Florida Nurserymen and Growers Association and the Tampa Bay Wholesale Growers. These groups have collectively agreed upon the problems associated with certain species and have decided to voluntarily cease their propagation, sale, and use (Fox et al. 2003). As of 2002, 45 species had been removed from commerce in Florida as a result of these cooperative efforts. However, some species remain in commerce despite their classification as invasive and ecosystem-altering due to their more significant commercial value (Baskin 2002). Wirth et al. (2004) conducted a study of 14 species (Table 8.2) produced by Florida nurseries, widely considered invasive yet still in commerce due to high demand and commercial significance. The study concluded that a phase-out of the 14 species would reflect a loss of approximately $59 million and 800 jobs; note that $59 million is approximately 3% of total nursery revenue in Florida. Wirth et al. (2004) believe that this number alone should not be the sole basis for decision making. They suggest that the cost of controlling these species in natural environments and on private property, as well as the Table 8.2.

Florida’s 14 invasive species remaining in commerce.

Common name

Scientific name

Asparagus fern Beach naupaka Camphor tree Chinese privet Coral ardisia Japanese honeysuckle Lantana Laurel fig Mexican petunia Nandina, heavenly bamboo Schefflera, umbrella tree Strawberry guava Surinam cherry Taro

Asparagus densiflorus Kunth (Jessop) Scaevola sericea Vahl. Cinnamomum camphora (L.) J. Presl Ligustrum sinense Lour. Ardisia crenata Sims Lonicera japonica Thunb. Lantana camara L. Ficus microcarpa L. Ruellia brittoniana Leonard ex Fernald Nandina domestica Thunb. Schefflera actinophylla (Endl.) Harms Psidium cattleianum Sabine. Eugenia uniflora L. Colocasia esculenta (L.) Schott

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costs of implementation and enforcement of regulatory actions, should be considered in policy-making. Despite these lingering issues and debates, the interaction of these Florida entities represents a model of interdisciplinary cooperation and compromise between opposed interest groups. Reichard and White (2001) examined the concerns of nursery industry personnel and noted that restricting the sales or importation of known invasive species, and potentially invasive species, does not mean that “exotic” species will no longer be used in trade. Addressing whether anti-invasive policies would harm the nursery industry, Reichard and White (2001) suggest several points to the contrary. They feel increased interest and understanding of the invasive plant issue by the consumer public will likely lead to increased pressure to be informed regarding which plants are thought to be invasive. However, nurseries will have to respond to environmental awareness pressures and help consumers make environmentally conscious choices. They also suggest that known invasive plants are only a small portion of overall sales. Therefore, removing them from trade will not result in disproportionate financial hardship and may stimulate sales of other species. English ivy, invasive in the Pacific Northwest and other areas of the country, is an example of a species that warrants removal (Plant Conservation Alliance, Alien Plant Working Group—English Ivy, Appendix A). They also believe that nurseries can use a proactive stance against invasive material as a marketing tool. As public interest in environmental topics continues to grow, businesses that advertise themselves as environmentally friendly are likely to benefit. However, the former president of the American Nursery & Landscape Association (2002–2003), and third-generation nurseryman (Weston Nurseries, Hopkinton, Massachusetts), Wayne Mezitt, disagrees with the suggestion that known invasive plants comprise only a small portion of industry revenues (Mezitt and Churchill 2002). Species such as burning bush, Japanese barberry, and norway maple, three species on invasive plant lists in the eastern U.S., account for a significant amount of revenue (Mezitt and Churchill 2002). Mezitt supports multi-disciplined cooperation to establish science-based criteria for invasive plants, together with cost/benefit analyses. He doubts whether bans on sales of already established invasive species would do much to curb the proliferation of such taxa. He suggests that if the nursery industry agrees to eliminate certain invasive species from commerce, then environmental groups and land-managers should agree to take on the responsibility of attempting to eradicate these species in the wild. This suggestion is not likely to be enacted under any agreement because widespread eradication of invasive species in the wild would incur prohibitively high costs.

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The position of the nursery and landscape industries is put forth by Regelbrugge et al. (2001). Regelbrugge, senior director of government relations for the ANLA, states: “However, industry is also well aware that new plants, including some plants viewed by some people as “invasive” plants, drive the nursery market. In view of this, ANLA prefers that solutions recognize the benefits of plant introductions and that the potential of one plant to be invasive may be different than another, depending on what the plant is and where it is being introduced. ANLA also acknowledges that some nursery practices need to change, while solutions must be realistic, prioritized and market-based.” Despite industry acknowledgment of the invasive plant problem and the various agreements, these industries have not yet made a noticeable effort to change any of its practices. However, the Horticultural Research Institute (HRI), the research arm of the ANLA, has funded research on invasive horticultural species. In 2003, 2004, and 2005, HRI has funded invasive plant research in the amounts of $12,500, $15,500, and $34,000, respectively (American Nursery and Landscape Association, Horticultural Research Institute, Appendix A). The yearly HRI research budget (from 2003 to 2005) has ranged from $200,000 to $220,000. Individual states vary in their approach to controlling invasive plants. Various approaches include state noxious weed laws, exotic species laws, and a variety of other legal measures (Klein 2004). Odell (2004) of the Environmental Law Institute has fashioned a model state law to manage the threat of invasive species (plant and animal) that is based on 17 state legal and policy tools proposed by Filbey et al. (2002). The model state law encompasses prevention, regulation, control and management, enforcement and implementation, and coordination.

V. CONCLUSION The invasive plant topic is indeed complex, controversial, and multifaceted. In essence, the topic is beset by scientific and regulatory challenges. Positioned within these challenges are: (1) the diversity of stakeholders involved and their respective interests; (2) the international nature of the issue and the difficulties inherent in balancing trade and phytosanitary caution; (3) the tremendous economic aspect: commercial revenues at the cost of less quantifiable environmental impacts, and the need for funding to sustain progress for science, education, implementation of programs, and eradication of already existing inva-

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sive species; and (4) the complicated human aspects that are embedded in decision making. The ornamental plant industry is particularly immersed in the debate because it has introduced and continues to introduce large numbers of alien species, some of which may be invasive. Empirically based estimates show that less than 1% of alien species become “pests” (Williamson and Fitter 1996). However, two key aspects directly related to the ornamental plant industry may render this very low probability of an alien species becoming a pest an unreliable estimate: (1) propagule pressure (i.e., introduction effort) is apt to be a key predictor of invasion success (Lockwood et al. 2005), and (2) the fact that widespread transport and sale of alien species increases the chance for naturalization, the population stage immediately prior to becoming a pest (Mack 2000; Kowarik 2003). By definition, an invasive status implies a negative impact on the environment and not all invaders have a negative effect on the environment (Farnsworth 2004). Determination of negative impact requires documentation and the requisite documentation funds. Where will these funds come from? The debate can be distilled to scientific and regulatory aspects. We next discuss the scientific and regulatory issues and challenges in the context of resolving the debate. A. Research Our understanding of plant invasion, even in view of the bountiful research already amassed, is in a nascent stage. Despite our current understanding of plant invasions, the challenge remains how to separate a species’ biological traits, its evolution in a foreign environment, the characteristics of its new environment, and the role of timing and chance when attempting to understand its invasion success or make predictions. Or as Roy (1990) noted: “. . . due to the many biological components of plant performance as well as to the many parameters that characterize habitats, it may be that invasion is case-specific.” Roy attended seven major symposia on biological invasions (North America 1984, South Africa 1985, Australia 1985, the Netherlands 1986, Great Britain 1986, France 1986, and Hawaii 1986), and returned home still feeling scientifically unsatisfied. Now, nearly two decades later, many scientists in the field of invasion ecology still remain uncomfortable with their collective understanding. Research is needed to further elucidate the complex dynamic systems of plant invasion. The great number of species and the immense scope of the ecological interactions in need of being studied and understood

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pose daunting challenges. At the heart of the plant invasion issue is the challenge to develop reliable and feasible models to predict plant invasion. Current models, and risk assessment systems, are relatively reliable. However, models to accurately predict an invasive potential for the thousands of plant species and numerous ecosystems and to incorporate anthropogenic factors are still on the horizon. Such models would not only be extremely useful tools to screen plants for potential introduction, but will satisfy requirements of regulations such as those described for the WTO. Whether these models would satisfy the skepticism of nursery industry personnel and groups remains to be seen. In a nursery survey with 76 respondents (Hall 2000, Appendix A), only 58% of respondents said they would be willing to stop selling a species that was scientifically documented to be invasive. This obvious lack of unanimity foretells that regulation may be the only reliable measure to control alien plant introduction and distribution. So, what scientific directions do we take to solve the problem of invasive species knowing that these directions will inevitably intersect with the regulatory realm? The Committee on the Scientific Basis for Predicting the Invasive Potential of Nonindigenous Plants and Pests in the U.S. (Predicting Invasions of Nonindigenous Plants and Plant Pests 2002) has addressed this question. After reviewing the history of invasions in the U.S., the scientific literature regarding invasive species factors, and the efforts to predict the potential of species to invade, they found that the current scientific foundation for the risk evaluation of non-indigenous species is inadequate to handle the continuing problem of plant invasions. Specifically, they reached the following four conclusions: (1) The record of a plant’s invasiveness in other geographical areas is currently the most reliable predictor of its ability to establish and invade in the U.S.; (2) There are currently no known broad scientific principles or reliable procedures for identifying the invasive potential of plants, plant pests, or biological control agents in new geographical ranges, but a conceptual basis exists for understanding invasions that could be developed into predictive principles; (3) The inability to predict accurately which non-indigenous species will become invasive stems from a lack of comprehensive knowledge of the events that dictate species’ immigration (arrival), persistence (survival), and invasion (proliferation and spread) in new environments; (4) Some data on the natural history of plant pests exist, but they often reside in grey literature and in datasets that are not easily accessible. As a result of their review, the Committee put forth a set of recommendations, proffered with urgency, to fortify the scientific foundation of invasive plant prediction. The recommendations relative to invasive plant species, in an

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abridged form, are as follows: (1) determine and quantify the pathways of plant invasion; (2) improve risk assessment systems and methods to evaluate imported plants; (3) assemble, update, and make available information on worldwide plant invasions, immigrant species, and scientific literature; (4) document information on the structure and composition of natural ecosystems in North America and analyze these ecosystems’ vulnerability to biotic invasion; (5) develop standardized procedures to measure the impact of invasive species for the scientific and regulatory communities; and (6) encourage multidisciplinary collaboration among scientists with taxonomic expertise and those who specialize in population biology, community ecology, epidemiology, and simulation modeling. The Global Invasive Species Programme (GISP), a consortium of scientific groups, advocates four main management approaches that are similar to the recommendations described above but also include the improvement of management techniques to eradicate or control invasive alien species once prevention has failed or has become impractical (McNeely 2001a). We endorse these recommendations. Many of these recommendations will require funding, thus federal and state governments, as well as the commercial parties responsible for importing potentially invasive species, must put forth the funds to turn these recommendations into action items. B. Regulation Regulators at the international, national, and state levels are faced with the dilemma of protecting the environment from non-indigenous native plant species while at the same time fostering commerce. With an increase in the volume of international commerce in biological commodities and changes in international trade relationships, the number of new species entering the U.S. will inevitably increase (Office of Technology Assessment—Harmful Non-Indigenous Species in the United States 1993). The popularity of ornamental plant taxa and gardening as a hobby in the U.S. are factors that will only encourage plant exploration and plant introduction. Tax revenues and lobbying efforts of the lucrative nursery and landscape organizations represent a persuasive force to minimize regulations, while vocal and influential environmental groups represent a persuasive force to enact regulations. Future invasive plant legislation, or the lack thereof, will depend on which faction succeeds in convincing regulators that their cause most benefits society. The pace of change towards regulation will certainly be affected by the fact that the responsibilities of the U.S. government and all relevant agencies are overwhelming, while at the same time under-funded and under-staffed.

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An impediment to developing and implementing invasive species regulations is that the complex and multi-tiered problems of nonindigenous invasive species do not easily mesh with the numerous and varied agencies of a government bureaucracy (Staples 2001). With exotic plants streaming into the U.S., the best case scenario to protect our environment and to establish a uniform system that will satisfy environmental and commercial stakeholders is to implement a national weed risk assessment screening system similar to that of Australia (Pheloung et al. 1999). However, a risk assessment program may not be sufficient. In addition to regulating new introductions into a country, Kowarik (2003) endorses “regulating the varying pathways of secondary releases within an already existing range of alien species may be most effective even decades and centuries after its initial introduction.” This suggestion is noteworthy, but regulating the pathways of the very large number of exotic plant introductions in the U.S. seems beyond the scope of feasibility. The lack of a general consensus on regulation between all stakeholders, including the international trade in alien species, has proved especially problematic to develop a solution that satisfies the environmental as well as commercial factions. Sociological factors are certainly embedded in the regulatory challenge. Miller and Gunderson (2004) succinctly describe the lack of a unified regulatory policy with the statement “The morass of human and social dimensions swirling around the issue of invasive species makes the lack of coherent and comprehensive laws easier to understand. . . .” Legislation at the state level is where most of the regulatory action is occurring. The banning or proposed banning of non-indigenous invasive plants in Connecticut and New Hampshire (Section IVC) is indicative of a trend towards individual states enacting regulation before the federal government. However, the difference in regulatory zeal and political philosophies between states is apt to create nursery industry “friendly” and “unfriendly” states. Such state-by-state regulatory differences exist in the hog production industry. One can legitimately question the effectiveness of state regulations in the absence of a national program to regulate the introduction of potentially invasive species. In the absence of regulation, will a voluntary invasive plant screening system or a set of best management practices effectively prevent the importation of potentially invasive species based on voluntary compliance? Since effective prevention is contingent on a 100% compliance, the answer is most likely no. There is evidence that a significant portion of the nursery and landscape industries would heed a voluntary system. The Voluntary Codes of Conduct (Fay 2002, 2003, Appendix A) endorsed

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by some industry groups and the voluntary action taken in Florida to ban the sale of 45 species due to industry and natural resource interactions (Section IVC) are evidence that an effective voluntary, non-regulatory system has a chance of success. A significant part of the problem is that the nursery industry is composed of thousands of businesses of varying sizes and dispositions on the subject of invasive plants. In a survey of the nursery industry, Hall (2000, Appendix A) found a wide range of responses in terms of whether private or government groups should regulate invasive species entering the U.S. and prevent the spread of invasive plants already sold in the U.S. Thus, getting all facets and personnel in the nursery and landscape industries to collectively comply with a voluntary system to regulate the introduction and sales of invasive and potentially invasive species is a formidable task. Total compliance may only be accomplished with regulation. There are various scenarios in which voluntary compliance to a set of best management practices may, at least in part, stem the tide of potentially invasive species into the U.S. The National Invasive Species Council may provide leadership in the development of a web-based information network, one that is regionally specific, and useful in acknowledging problem plant species and coordinating eradication efforts along with elimination from commerce. Regardless of impending regulation, the horticultural industry now has its back against the wall with nowhere to turn but to adopt a “best management practices” (BMP) approach to potentially invasive species. BMP manuals offer methods to carry out operations in an environmentally sound manner. There is evidence that BMPs could be adopted and effective in the nursery industry. The Southern Nursery Association (SNA), an affiliation of approximately 1,800 businesses, funded and published Best Management Practices—Guide for Growing Container-grown Plants (Yeager et al. 1994), which details numerous plant producing strategies that minimize the environmental impact of production practices. Over 3,000 copies of the manual have been sold, and the manual is now in its second printing. Specific invasive plant BMP measure are: (1) labeling of plants to indicate the degree of potential invasiveness on a regional basis; (2) developing and conducting education programs for nursery personnel and the public; and (3) promoting dialogs with environmental, regulatory, industry, and academic groups to establish collaborative efforts. Of these three measures, the greatest need is for education of nursery and landscape personnel and the public. Since the invasive species problem is often area-specific, a region-by-region approach to educate industry personnel and the public on the species that are invasive and the disruptive nature of each species. This educational effort will entail collaboration of academics and regional nursery and

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landscape representatives. Brewer (2002) endorses outreach (connecting science with a lay audience in a unidirectional manner) and partnership (multidirectional sharing of information and perspectives) programs to stimulate cooperation and conservation action in local communities through school and informal citizen science programs. The benefits of a well-designed program can promote the understanding of local ecosystem ecology and encourage participants to be involved in local conservation efforts. Educating the public will potentially garner the political support required to put into action coherent policies, laws, and regulations to effectively address the problem of non-indigenous invasive species (McNeely 2001a). A significant impediment in persuading people to adopt a more cautious approach to importing exotic species is that, due to the lag factor, a particular species may take years or decades to show itself as an invasive species. Nonetheless, adoption of BMPs would demonstrate to the public and regulatory groups that the horticultural industry is making a sincere and diligent effort to maintain its role as a steward of the land. Whether such a BMP approach will work will depend on the level of resolve, collaboration, and compromise between vested interests.

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APPENDIX A. WEBSITE CITATIONS American Nursery & Landscape Association. http://anla.org/industry/index.htm American Nursery and Landscape Association, Horticultural Research Institute. http:// www.anla.org/research/grants/index.htm American Seed Trade Association. 2000. http://www.amseed.com/govt_statementsDetail .asp?id=54 aphis.usda.gov.—Plant Protection Act. http://www.aphis.usda.gov/lpa/pubs/fsheet_faq_ notice/fs_phproact.html AQIS Import Risk Analysis Handbook. http://www.affa.gov.au/corporate_docs/publications/ pdf/market_access/biosecurity/risk.pdf Biosecurity Australia. http://www.affa.gov.au/content/output.cfm?ObjectID=D2C48F86BA1A-11A1-A2200060B0A04014

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Center for Aquatic and Invasive Plants, University of Florida (information cited from Langeland/Burks book: Identification & biology of non-native plants in Florida’s natural areas) http://plants.ifas.ufl.edu/ficmic.pdfe Connecticut Botanical Society. Japanese barberry. http://www.ct-botanical-society.org/ galleries/berberisthun.html Department of Agriculture, Government of Western Australia. Western Australia Quarantine Service—Garden Seed Dangers on the Internet. http://www.agric.wa.gov.au/ servlet/page?_pageid=449&_dad=portal30&_schema=PORTAL30&p_reference_path=7 98_IKMP_NAVIGATION_PORTLET_260&p_start_url=&p_home_url=&p_show_menu= &p_login_url=&p_topic_id=20030&p_topic_name=0PW0&p_no_summpage=N Environment. http://www.envirotech-list.com/Top_Science_Environment_Biodiversity_ Invasive_Species_Terrestrial_Plants.html Environment Hawaii. 2002. vol. 13, no. 6. http://www.environment-hawaii.org/1202 assessing.htm Fay, K. 2002. Linking ecology and horticulture to prevent plant invasions. Workshop at the Missouri Botanical Garden, St. Louis. http://www.centerforplantconservation.org/ invasives/Download%20PDF/Proceedings_FINAL.pdf Fay, K. 2003. Linking Ecology and Horticulture to Prevent Plant Invasions II. Workshop at the Chicago Botanic Garden. http://www.centerforplantconservation.org/invasives/ Download%20PDF/CBG_Proceedings.pdf Federal Interagency Committee for the Management of Noxious and Exotic Weeds. http://ficmnew.fws.gov/page2.html Federal Register, Presidential Documents. 1999. Vol. 64 no. 25. http://www.invasivespecies .gov/laws/eo13112.pdf Florida Division of Forestry, Conservation and Management—Hardwood Root Diseases: Mimosa Wilt. http://www.fl-dof.com/Pubs/Insects_and_Diseases/td_hrd_mimosa_wilt .htm Global Invasive Species Information Network. http://www.gisinetwork.org/index.html Hall, M. 2000. IPlants: Invasive plants and the Nursery Industry. Undergraduate senior thesis in environmental studies, Brown University. http://www.old-scholls.com/iplants/ Home.html Introduced Species Summary Project—Australian Paperbark. http://www.columbia .edu/itc/cerc/danoff-burg/invasion_bio/inv_spp_summ/Melaleuca_quinquenervia .html Invasive Plant Atlas of New England. Berberis thunbergii http://webapps.lib.uconn .edu/ipane/browsing.cfm?descriptionid=26 Maryland Native Plant Society, Control of Invasive Non-Native Plants. http://www.mdflora.org/ publications/invasives.htm McNeely, J.A. 2001b. The great reshuffling: How alien species help feed the global economy. IUCN, The World Conservation Union. http://www.iucn.org/biodiversityday/ mcneelyreshuffling.html National Center for Environmental Economics. http://yosemite.epa.gov/ee/epa/eed.nsf/ Webpages/SABReview.html National Park Service. Weeds Gone Wild—Alien Plant Invaders of Natural Areas: More Info. http://www.nps.gov/plants/alien/moreinfo.htm North Carolina State University News Release. 2004. Researchers aim to halt sales of noxious weeds on the internet. http://www.ncsu.edu/news/press_releases/03_07/196.htm North Texas Water Garden Society. http://www.ntwgs.org/articles/illegalAquatics.html#the% 20list Pest Protection and Management Programs. Noxious Weeds. http://www.aphis.usda.gov/ ppq/weeds/nwpolicy2001.html#intro

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Plant Conservation Alliance, Alien Plant Working Group—English Ivy. http://www.nps.gov/ plants/alien/fact/hehe1.htm Plant Conservation Alliance, Alien Plant Working Group—Japanese Barberry. http:// www.nps.gov/plants/alien/fact/beth1.htm Plant Conservation Alliance, Alien Plant Working Group—Multiflora Rose. http://www .nps.gov/plants/alien/fact/romu1.htm Plant Conservation Alliance, Alien Plant Working Group—Silk Tree. http://www.nps .gov/plants/alien/fact/alju1.htm Plant Conservation Alliance, Alien Plant Working Group—Tree of Heaven. http://www .nps.gov/plants/alien/fact/aial1.htm Plant Invaders of Mid-Atlantic Natural > Areas > Vines > Kudzu. National Park Service and U.S. Fish & Wildlife Service, Washington, D.C. http://www.nps.gov/plants/alien/ pubs/midatlantic/pumo.htm Plant Invaders of Mid-Atlantic Natural > Areas > Trees > Bradford Pear. National Park Service and U.S. Fish & Wildlife Service, Washington, D.C. http://www.nps.gov/plants/ alien/pubs/midatlantic/pyca.htm Plant Talk Resource Page. http://www.plant-talk.org/resource/invasive.html Sierra Club—Washington, D.C. Chapter. Trees for Washington, D.C.—The ten least wanted. http://www.dc.sierraclub.org/articles/nativetrees.htm Tennessee Exotic Plant Pest Council’s Invasive Exotic Plant Pests in Tennessee—2004. http://www.tneppc.org/TNEPPC2004PlantList-8x11.pdf United States Government Accountability Office. http://www.gao.gov/new.items/d05185.pdf USDA Economics and Statistics System. Floriculture and Nursery Crops; a link within: Specialty Agriculture—Floriculture, Horticulture and Nursery http://usda.mannlib .cornell.edu/ USDA Natural Resources Conservation Service. Plants—National Database Reports and Topics. http://plants.usda.gov/cgi_bin/topics.cgi?earl=noxious.cgi Virginia Native Plant Society. http://vnps.org/links.htm#invasive Water Conserve—A Water Conservation Portal. http://www.waterconserve.info/articles/ reader.asp?linkid=35927 Weed Risk Assessment for Hawaii and the Pacific Islands. http://www.botany.hawaii .edu/faculty/daehler/WRA/default2.htm Weekly NMPRO e-mail. March 16, 2004. Connecticut demands plant bans. T. Davis, (ed.) www.greenbeam.com. Weekly NMPRO e-mail. June 1, 2004. Governor signs Connecticut invasives bill. T. Davis, (ed.) www.greenbeam.com. Withers, M. A., M. W. Palmer, G. L. Wade, P. S. White, and P. R. Neal. 1998. Changing patterns in the number of species in North American floras. Chapter 4. In: T. D. Sisk (ed.), Perspectives on the land-use history of North America: a context for understanding our changing environment. U.S. Geological Survey, Biological Resources Division, Biological Science Report USGS/BRD/BSR 1998-0003 (Revised September 1999). http:// biology.usgs.gov/luhna/chap4.html

Subject Index Volume 32 A Allium development, 329–378 Anatomy & morphology: Allium development, 329–378 plant architecture, 1–61 Architecture, plant, 1–61 D Dedication, Sedgely, M., x–xii Deficit irrigation, 111–165 F Fruit, jujube, 229–298 Fruit crops: architecture, 1–61 jujube, 229–298 peach orchard systems, 63–109 water stress, 111–165 I Invasive plants, 379–437 Irrigation: deficit, 111–165 scheduling, 111–165 J Jujube, 229–298 L Leucadendron, 167–228 M Medicinal crops, Taxus, 299–327

O Ornamental plants: Leucadendon, 167–228 Taxus, 299–327 P Peach, orchard systems, 63–109 Physiology, Allium development, 329–378 Plant architecture, 1–63 Protaceous flower crops, Leucadendron, 167–228 Pruning, plant architecture, 1–63 S Stress, irrigation scheduling, 111–165 T Taxus, 299–327 V Vegetable crops, Allium development, 329–378 W Weeds, invasive, 379–437 Y Yew, see Taxus Z Zizipus, see Jujube

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Cumulative Subject Index (Volumes 1–32) A Abscisic acid: chilling injury, 15:78–79 cold hardiness, 11:65 dormancy, 7:275–277 genetic regulation, 16:9–14; 20–21 lychee, 28:437–443 mango fruit drop, 31:124–125 mechanical stress, 17:20 rose senescence, 9:66 stress, 4:249–250 Abscission: anatomy and histochemistry, 1:172–203 citrus, 15:145–182 flower and petals, 3:104–107 mango fruit drop, 31:113–155 regulation, 7:415–416 rose, 9:63–64 Acclimatization: foliage plants, 6:119–154 herbaceous plants, 6:379–395 micropropagation, 9:278–281, 316–317 Actinidia, 6:4–12 Adzuki bean, genetics, 2:373 Agapanthus, 25:56–57 Agaricus, 6:85–118 Agrobacterium tumefaciens, 3:34 Air pollution, 8:1–42 Alkaloids, steroidal, 25:171–196 Allium: development, 32:329–378 phytonutrients, 28:156–159 Almond: bloom delay, 15:100–101

in vitro culture, 9:313 postharvest technology and utilization, 20:267–311 wild of Kazakhstan, 29:262–265 Alocasia, 8:46, 57, see also Aroids Alternate bearing: chemical thinning, 1:285–289 fruit crops, 4:128–173 pistachio, 3:387–388 Aluminum: deficiency and toxicity symptoms in fruits and nuts, 2:154 Ericaceae, 10:195–196 Amarcrinum, 25: 57 Amaryllidaceae, growth, development, flowering, 25:1–70 Amaryllis, 25:4–15 Amorphophallus, 8:46, 57, see also Aroids Anatomy and morphology: Allium development, 32:329–378 apple flower and fruit, 10:273–308 apple tree, 12:265–305 asparagus, 12:71 cassava, 13:106–112 citrus, abscission, 15:147–156 embryogenesis, 1:4–21, 35–40 fig, 12:420–424 fruit abscission, 1:172–203 fruit storage, 1:314 ginseng, 9:198–201 grape flower, 13:315–337 grape seedlessness, 11:160–164 heliconia, 14:5–13 kiwifruit, 6:13–50

Horticultural Reviews, Volume 32, Edited by Jules Janick ISBN 0-471-73216-8 © 2005 John Wiley & Sons, Inc. 449

450 Anatomy and morphology (cont.) magnetic resonance imaging, 20:78–86, 225–266 orchid, 5:281–283 navel orange, 8:132–133 pecan flower, 8:217–255 plant architecture, 32:1–61 pollution injury, 8:15 red bayberry, 20:92–96 waxes, 23:1–68 androgenesis, woody species, 10:171–173 Angiosperms, embryogenesis, 1:1–78 Anthurium, see also Aroids, ornamental fertilization, 5:334–335 Antitranspirants, 7:334 cold hardiness, 11:65 Apical meristem, cryopreservation, 6:357–372 Apple: alternate bearing, 4:136–137 anatomy and morphology of flower and fruit, 10:273–309 bioregulation, 10:309–401 bitter pit, 11:289–355 bloom delay, 15:102–104 CA storage, 1:303–306 crop load, 31:233–292 chemical thinning, 1:270–300 fertilization, 1:105 fire blight control, 1:423–474 flavor, 16:197–234 flower induction, 4:174–203 fruiting, 11:229–287 fruit cracking and splitting, 19:217–262 functional phytonutrients, 27:304 germplasm acquisition and resources, 29:1–61 in vitro, 5:241–243; 9:319–321 light, 2:240–248 maturity indices, 13:407–432 mealiness, 20:200 nitrogen metabolism, 4:204–246 replant disease, 2:3 root distribution, 2:453–456 scald, 27:227–267 stock-scion relationships, 3:315–375 summer pruning, 9:351–375 tree morphology and anatomy, 12:265–305 vegetative growth, 11:229–287 watercore, 6:189–251 weight loss, 25:197–234

CUMULATIVE SUBJECT INDEX wild of Kazakhstan, 29:63–303, 305–315 yield, 1:397–424 Apricot: bloom delay, 15:101–102 CA storage, 1:309 origin and dissemination, 22:225–266 wild of Kazakhstan, 29:325–326 Arabidopsis: molecular biology of flowering, 27:1–39, 41–77 Architecture, plant, 32:1–61 Aroids: edible, 8:43–99; 12:166–170 ornamental, 10:1–33 Arsenic, deficiency and toxicity symptoms in fruits and nuts, 2:154 Artemisia, 19:319–371 Artemisinin, 19:346–359 Artichoke, CA storage, 1:349–350 Asexual embryogenesis, 1:1–78; 2:268–310; 3:214–314; 7:163–168, 171–173, 176–177, 184–188, 189; 10:153–181; 14:258–259, 337–339; 24:6–7; 26:105–110 Asparagus: CA storage, 1:350–351 fluid drilling of seed, 3:21 postharvest biology, 12:69–155 Auxin: abscission, citrus, 15:161, 168–176 bloom delay, 15:114–115 citrus abscission, 15:161, 168–176 dormancy, 7:273–274 flowering, 15:290–291, 315 genetic regulation, 16:5–6, 14, 21–22 geotropism, 15:246–267 mango fruit drop, 31:118–120 mechanical stress, 17:18–19 petal senescence, 11:31 Avocado: CA and MA, 22:135–141 flowering, 8:257–289 fruit development, 10:230–238 fruit ripening, 10:238–259 rootstocks, 17:381–429 Azalea, fertilization, 5:335–337 B Babaco, in vitro culture, 7:178 Bacteria: diseases of fig, 12:447–451

CUMULATIVE SUBJECT INDEX ice nucleating, 7:210–212; 11:69–71 pathogens of bean, 3:28–58 tree short life, 2:46–47 wilt of bean, 3:46–47 Bacteriocides, fire blight, 1:450–459 Bacteriophage, fire blight control, 1:449–450 Banana: CA and MA, 22:141–146 CA storage, 1:311–312 fertilization, 1:105 in vitro culture, 7:178–180 Banksia, 22:1–25 Barberry, wild of Kazakhstan, 29:332–336 Bean: CA storage, 1:352–353 fluid drilling of seed, 3:21 resistance to bacterial pathogens, 3:28–58 Bedding plants, fertilization, 1:99–100; 5:337–341 Beet: CA storage, 1:353 fluid drilling of seed, 3:18–19 Begonia (Rieger), fertilization, 1:104 Biennial bearing. See Alternate bearing Bilberry, wild of Kazakhstan, 29:347–348 Biochemistry, petal senescence, 11:15–43 Bioreactor technology, 24:1–30 Bioregulation, see also Growth substances apple and pear, 10:309–401 Bird damage, 6:277–278 Bitter pit in apple, 11:289–355 Blackberry: harvesting, 16:282–298 wild of Kazakhstan, 29:345 Black currant, bloom delay, 15:104 Bloom delay, deciduous fruits, 15:97 Blueberry: developmental physiology, 13:339–405 harvesting, 16:257–282 nutrition, 10:183–227 Boron: deficiency and toxicity symptoms in fruits and nuts, 2:151–152 foliar application, 6:328 nutrition, 5:327–328 pine bark media, 9:119–122 Botanic gardens, 15:1–62 Bramble, harvesting, 16:282–298

451 Branching, lateral: apple, 10:328–330 pear, 10:328–330 Brassica classification, 28:27–28 Brassicaceae, in vitro, 5:232–235 Breeding, see Genetics and breeding Broccoli, CA storage, 1:354–355 Brussels sprouts, CA storage, 1:355 Bulb crops, see also Tulip development, 25:1–70 flowering, 25:1–70 genetics and breeding, 18:119–123 growth, 25: 1–70 in vitro, 18:87–169 micropropagation, 18:89–113 root physiology, 14:57–88 virus elimination, 18:113–123 C CA storage. see Controlled-atmosphere storage Cabbage: CA storage, 1:355–359 fertilization, 1:117–118 Cactus: crops, 18:291–320 grafting, 28:106–109 reproductive biology, 18:321–346 Caladium, see Aroids, ornamental Calciole, nutrition, 10:183–227 Calcifuge, nutrition, 10:183–227 Calcium: bitter pit, 11:289–355 cell wall, 5:203–205 container growing, 9:84–85 deficiency and toxicity symptoms in fruits and nuts, 2:148–149 Ericaceae nutrition, 10:196–197 foliar application, 6:328–329 fruit softening, 10:107–152 nutrition, 5:322–323 pine bark media, 9:116–117 tipburn, disorder, 4:50–57 Calmodulin, 10:132–134, 137–138 Caparis, see Caper bush Caper bush, 27:125–188 Carbohydrate: fig, 12:436–437 kiwifruit partitioning, 12:318–324 metabolism, 7:69–108 partitioning, 7:69–108 petal senescence, 11:19–20

452 Carbohydrate (cont.): reserves in deciduous fruit trees, 10:403–430 Carbon dioxide, enrichment, 7:345–398, 544–545 Carnation, fertilization, 1:100; 5:341–345 Carrot: CA storage, 1:362–366 fluid drilling of seed, 3:13–14 postharvest physiology, 30:284–288 Caryophyllaceae, in vitro, 5:237–239 Cassava: crop physiology, 13:105–129 molecular biology, 26:85–159 multiple cropping, 30:355–50 postharvest physiology, 30:288–295 root crop, 12:158–166 Cauliflower, CA storage, 1:359–362 Celeriac, CA storage, 1:366–367 Celery: CA storage, 1:366–367 fluid drilling of seed, 3:14 Cell culture, 3:214–314 woody legumes, 14:265–332 Cell membrane: calcium, 10:126–140 petal senescence, 11:20–26 Cellular mechanisms, salt tolerance, 16:33–69 Cell wall: calcium, 10:109–122 hydrolases, 5:169–219 ice spread, 13:245–246 tomato, 13:70–71 Chelates, 9:169–171 Cherimoya, CA and MA, 22:146–147 Cherry: bloom delay, 15:105 CA storage, 1:308 origin, 19:263–317 wild of Kazakhstan, 29:326–330 Chestnut: blight, 8:281–336 botany and horticulture, 31:293–349 in vitro culture, 9:311–312 Chicory, CA storage, 1:379 Chilling: injury, 4:260–261; 15:63–95 injury, chlorophyll fluorescence, 23:79–84 pistachio, 3:388–389

CUMULATIVE SUBJECT INDEX China, protected cultivation, 30:37–82 Chlorine: deficiency and toxicity symptoms in fruits and nuts, 2:153 nutrition, 5:239 Chlorophyll fluorescence, 23:69–107 Chlorosis, iron deficiency induced, 9:133–186 Chrysanthemum fertilization, 1:100–101; 5:345–352 Citrus: abscission, 15:145–182 alternate bearing, 4:141–144 asexual embryogenesis, 7:163–168 CA storage, 1:312–313 chlorosis, 9:166–168 cold hardiness, 7:201–238 fertilization, 1:105 flowering, 12:349–408 functional phytochemicals, fruit, 27:269–315 honey bee pollination, 9:247–248 in vitro culture, 7:161–170 irrigation, 30:37–82 juice loss, 20:200–201 navel orange, 8:129–179 nitrogen metabolism, 8:181 practices for young trees, 24:319–372 rootstock, 1:237–269 viroid dwarfing, 24:277–317 Classification: Brassica, 28:27–28 lettuce, 28:25–27 potato, 28:23–26 tomato, 28:21–23 Clivia, 25:57 Cloche (tunnel), 7:356–357 Coconut palm: asexual embryogenesis, 7:184 in vitro culture, 7:183–185 Cold hardiness, 2:33–34 apple and pear bioregulation, 10:374–375 citrus, 7:201–238 factors affecting, 11:55–56 herbaceous plants, 6:373–417 injury, 2:26–27 nutrition, 3:144–171 pruning, 8:356–357 Colocasia, 8:45, 55–56, see also Aroids

CUMULATIVE SUBJECT INDEX Common blight of bean, 3:45–46 Compositae, in vitro, 5:235–237 Container production, nursery crops, 9:75–101 Controlled-atmosphere (CA) storage: asparagus, 12:76–77, 127–130 chilling injury, 15:74–77 flowers, 3:98; 10:52–55 fruit quality, 8:101–127 fruits, 1:301–336; 4:259–260 pathogens, 3:412–461 seeds, 2:134–135 tropical fruit, 22:123–183 tulip, 5:105 vegetable quality, 8:101–127 vegetables, 1:337–394; 4:259–260 Controlled environment agriculture, 7:534–545, see also Greenhouse greenhouse crops; hydroponic culture; protected culture Copper: deficiency and toxicity symptoms in fruits and nuts, 2:153 foliar application, 6:329–330 nutrition, 5:326–327 pine bark media, 9:122–123 Corynebacterium flaccumfaciens, 3:33, 46 Cotoneaster, wild of Kazakhstan, 29:316–317 Cowpea: genetics, 2:317–348 U.S. production, 12:197–222 Cranberry: botany and horticulture, 21:215–249 fertilization, 1:106 harvesting, 16:298–311 wild of Kazakhstan, 29:349 Crinum, 25:58 Crucifers phytochemicals, 28:150–156 Cryopreservation: apical meristems, 6:357–372 cold hardiness, 11:65–66 Cryphonectria parasitica. See Endothia parasitica Crytosperma, 8:47, 58, see also Aroids Cucumber: CA storage, 1:367–368 grafting, 28:91–96 Cucurbita pepo, cultivar groups history, 25:71–170

453 Currant: harvesting, 16:311–327 wild of Kazakhstan, 29:341 Custard apple, CA and MA, 22:164 Cyrtanthus, 25:15–19 Cytokinin: cold hardiness, 11:65 dormancy, 7:272–273 floral promoter, 4:112–113 flowering, 15:294–295, 318 genetic regulation, 16:4–5, 14, 22–23 grape root, 5:150, 153–156 lettuce tipburn, 4:57–58 mango fruit drop, 31:118–120 petal senescence, 11:30–31 rose senescence, 9:66 D Date palm: asexual embryogenesis, 7:185–187 in vitro culture, 7:185–187 Daylength, see Photoperiod Dedication: Bailey, L.H., 1:v–viii Beach, S.A., 1:v–viii Bukovac, M.J., 6:x–xii Campbell, C.W., 19:xiii Cummins, J.N., 15:xii–xv Dennis, F.G., 22:xi–xii De Hertogh, A.A., 26:xi–xii Faust, Miklos, 5:vi–x Hackett, W.P., 12:x–xiii Halevy, A.H., 8:x–xii Hess, C.E., 13:x–xii Kader, A.A., 16:xii–xv Kamemoto, H., 24:x–xiii Kester, D.E., 30:xiii–xvii Looney, N.E., 18:xii–xv Magness, J.R., 2:vi–viii Moore, J.N., 14:xii–xv Possingham, J.V., 27:xi–xiii Pratt, C., 20:ix–xi Proebsting, Jr., E.L., 9:x–xiv Rick, Jr., C.M., 4:vi–ix Ryugo, K., 25:x–xii Sansavini, S., 17:xii–xiv Sedgely, M., 32:x–xii Sherman, W.B., 21:xi–xiii Smock, R.M., 7:x–xiii Sperling, C.E., 29:ix–x Stevens, M.A., 28:xi–xiii

454 Dedication (cont.): Warrington, L.J. 31:xi–xii Weiser, C.J., 11:x–xiii Whitaker, T.W., 3:vi–x Wittwer, S.H., 10:x–xiii Yang, S.F., 23:xi Deficit irrigation, 21:105–131; 32:111–165 Deficiency symptoms, in fruit and nut crops, 2:145–154 Defoliation, apple and pear bioregulation, 10:326–328 ‘Delicious’ apple, 1:397–424 Desiccation tolerance, 18:171–213 Dieffenbachia, see Aroids, ornamental Dioscorea, see Yam Disease: air pollution, 8:25 aroids, 8:67–69; 10:18; 12:168–169 bacterial, of bean, 3:28–58 cassava, 12:163–164 control by virus, 3:399–403 controlled-atmosphere storage, 3:412–461 cowpea, 12:210–213 fig, 12:447–479 flooding, 13:288–299 hydroponic crops, 7:530–534 lettuce, 2:187–197 mycorrhizal fungi, 3:182–185 ornamental aroids, 10:18 resistance, acquired, 18:247–289 root, 5:29–31 stress, 4:261–262 sweet potato, 12:173–175 tulip, 5:63, 92 turnip moasic virus, 14:199–238 waxes, 23:1–68 yam (Dioscorea), 12:181–183 Disorder, see also Postharvest physiology: bitterpit, 11:289–355 fig, 12:477–479 pear fruit, 11:357–411 watercore, 6:189–251; 11:385–387 Dormancy, 2:27–30 blueberry, 13:362–370 fruit trees, 7:239–300 tulip, 5:93 Drip irrigation, 4:1–48 Drought resistance, 4:250–251 cassava, 13:114–115

CUMULATIVE SUBJECT INDEX Durian, CA and MA, 22:147–148 Dwarfing: apple, 3:315–375 apple mutants, 12:297–298 by virus, 3:404–405 E Easter lily, fertilization, 5:352–355 Eggplant: grafting, 28:103–104 phytochemicals, 28:162–163 Elderberry, wild of Kazakhstan, 29:349–350 Embryogenesis. See Asexual embryogenesis Endothia parasitica, 8:291–336 Energy efficiency, in greenhouses, 1:141–171; 9:1–52 Environment: air pollution, 8:20–22 controlled for agriculture, 7:534–545 controlled for energy efficiency, 1:141–171; 9:1–52 embryogenesis, 1:22, 43–44 fruit set, 1:411–412 ginseng, 9:211–226 greenhouse management, 9:32–38 navel orange, 8:138–140 nutrient film technique, 5:13–26 Epipremnum, see Aroids, ornamental Eriobotrya japonica. see Loquat Erwinia: amylovora, 1:423–474 lathyri, 3:34 Essential elements: foliar nutrition, 6:287–355 pine bark media, 9:103–131 plant nutrition, 5:318–330 soil testing, 7:1–68 Ethylene: abscission, citrus, 15:158–161, 168–176 apple bioregulation, 10:366–369 avocado, 10:239–241 bloom delay, 15:107–111 CA storage, 1:317–319, 348 chilling injury, 15:80 citrus abscission, 15:158–161, 168–176 cut flower storage, 10:44–46 dormancy, 7:277–279 flowering, 15:295–296, 319 flower longevity, 3:66–75

CUMULATIVE SUBJECT INDEX genetic regulation, 16:6–7, 14–15, 19–20 kiwifruit respiration, 6:47–48 mango fruit crop, 31:120–122 mechanical stress, 17:16–17 petal senescence, 11:16–19, 27–30 rose senescence, 9:65–66 Eucharis, 25:19–22 Eucrosia, 25:58 F Feed crops, cactus, 18:298–300 Feijoa, CA and MA, 22:148 Fertilization and fertilizer: anthurium, 5:334–335 azalea, 5:335–337 bedding plants, 5:337–341 blueberry, 10:183–227 carnation, 5:341–345 chrysanthemum, 5:345–352 controlled release, 1:79–139; 5:347–348 Easter lily, 5:352–355 Ericaceae, 10:183–227 foliage plants, 5:367–380 foliar, 6:287–355 geranium, 5:355–357 greenhouse crops, 5:317–403 lettuce, 2:175 nitrogen, 2:401–404 orchid, 5:357–358 poinsettia, 5:358–360 rose, 5:361–363 snapdragon, 5:363–364 soil testing, 7:1–68 trickle irrigation, 4:28–31 tulip, 5:364–366 Vaccinium, 10:183–227 zinc nutrition, 23:109–128 Fig: industry, 12:409–490 ripening, 4:258–259 Filbert, in vitro culture, 9:313–314 Fire blight, 1:423–474 Flooding, fruit crops, 13:257–313 Floral scents, 24:31–53 Floricultural crops, see also individual crops: Amaryllidaceae, 25:1–70 Banksia, 22:1–25 China, protected culture, 30:141–148 fertilization, 1:98–104 growth regulation, 7:399–481

455 heliconia, 14:1–55 Leucospermum, 22:27–90 postharvest physiology and senescence, 1:204–236; 3:59–143; 10:35–62; 11:15–43 Protea, 26:1–48 Florigen, 4:94–98 Flower and flowering: Amaryllidaceae, 25:1–70 apple anatomy and morphology, 10:277–283 apple bioregulation, 10:344–348 Arabidopsis, 27:1–39, 41–77 aroids, ornamental, 10:19–24 avocado, 8:257–289 Banksia, 22:1–25 blueberry development, 13:354–378 cactus, 18:325–335 citrus, 12:349–408 control, 4:159–160; 15:279–334 development (postpollination), 19:1–58 fig, 12:424–429 girdling, 20:1–26 grape anatomy and morphology, 13:354–378 homeotic gene regulation, 27:41–77 honey bee pollination, 9:239–243 induction, 4:174–203, 254–256 initiation, 4:152–153 in vitro, 4:106–127 kiwifruit, 6:21–35; 12:316–318 Leucospermum, 22:27–90 lychee, 28:397–421 orchid, 5:297–300 pear bioregulation, 10:344–348 pecan, 8:217–255 perennial fruit crops, 12:223–264 phase change, 7:109–155 photoperiod, 4:66–105 pistachio, 3:378–387 postharvest physiology, 1:204–236; 3:59–143; 10:35–62; 11:15–43 postpollination development, 19:1–58 protea leaf blackening, 17:173–201 pruning, 8:359–362 raspberry, 11:187–188 regulation in floriculture, 7:416–424 rhododendron, 12:1–42 rose, 9:60–66 scents, 24:31–53 senescence, 1:204–236; 3:59–143; 10:35–62; 11:15–43;18:1–85

456 Flower and flowering (cont.): strawberry, 28:325–349 sugars, 4:114 thin cell layer morphogenesis, 14:239–256 tulip, 5:57–59 water relations, 18:1–85 Fluid drilling, 3:1–58 Foliage plants: acclimatization, 6:119–154 fertilization, 1:102–103; 5:367–380 industry, 31:47–112 Foliar nutrition, 6:287–355 Freeze protection, see Frost protection Frost: apple fruit set, 1:407–408 citrus, 7:201–238 protection, 11:45–109 Fruit: abscission, 1:172–203 abscission, citrus, 15:145–182 apple anatomy and morphology, 10:283–297 apple bioregulation, 10:348–374 apple bitter pit, 11:289–355 apple crop load, 31:233–292 apple flavor, 16:197–234 apple maturity indices, 13:407–432 apple ripening and quality, 10:361–374 apple scald, 27:227–267 apple weight loss, 25:197–234 avocado development and ripening, 10:229–271 bloom delay, 15:97–144 blueberry development, 13:378–390 cactus physiology, 18:335–341 CA storage and quality, 8:101–127 chilling injury, 15:63–95 coating physiology, 26:161–238 cracking, 19:217–262; 30:163–184 diseases in CA storage, 3:412–461 fresh cut, 30:185–251 functional phytochemicals, 27:269–315 growth measurement, 24:373–431 jujube, 32:229–298 kiwifruit, 6:35–48; 12:316–318 loquat, 23:233–276 lychee, 28:433–444 mango fruit drop, 31:113–155 maturity indices, 13:407–432 navel orange, 8:129–179

CUMULATIVE SUBJECT INDEX nectarine, postharvest, 11:413–452 nondestructive postharvest quality evaluation, 20:1–119 olive physiology, 31:157–231 olive processing, 25:235–260 pawpaw, 31:351–384 peach, postharvest, 11:413–452 pear, bioregulation, 10:348–374 pear, fruit disorders, 11:357–411 pear maturity indices, 13:407–432 pear ripening and quality, 10:361–374 pear scald, 27:227–267 pear volatiles, 28:237–324 pistachio, 3:382–391 phytochemicals, 28:125–185 plum, 23:179–231 quality and pruning, 8:365–367 red bayberry, 30: 83–113 ripening, 5:190–205 set, 1:397–424; 4:153–154 set in navel oranges, 8:140–142 size and thinning, 1:293–294; 4:161 softening, 5:109–219; 10:107–152 splitting, 19:217–262 strawberry growth and ripening, 17:267–297 texture, 20:121–224 thinning, apple and pear, 10:353–359 tomato cracking, 30:163–184 tomato parthenocarpy, 6:65–84 tomato ripening, 13:67–103 volatiles, pear, 28:237–324 Fruit crops, see also Individual crop apple, wild of Kazakhstan, 29:63–303, 305–315 alternate bearing, 4:128–173 apple bitter pit, 11:289–355 apple crop load, 31233–292 apple flavor, 16:197–234 apple fruit splitting and cracking, 19:217–262 apple germplasm, 29:1–61, 63–303 apple growth, 11:229–287 apple maturity indices, 13:407–432 apple scald, 27:227–267 apricot, origin and dissemination, 22:225–266 apricot, wild of Kazakhstan, 29:325–326 architecture, 32:1–61 avocado flowering, 8:257–289

CUMULATIVE SUBJECT INDEX avocado rootstocks, 17:381–429 barberry, wild of Kazakhstan, 29:332–336 berry crop harvesting, 16:255–382 bilberry, wild of Kazakhstan, 29:347–348 blackberry, wild of Kazakhstan, 29:345 bloom delay, 15:97–144 blueberry developmental physiology, 13:339–405 blueberry harvesting, 16:257–282 blueberry nutrition, 10:183–227 bramble harvesting, 16:282–298 cactus, 18:302–309 carbohydrate reserves, 10:403–430 CA and MA for tropicals, 22:123–183 CA storage, 1:301–336 CA storage diseases, 3:412–461 cherry, wild of Kazakhstan, 29:326–330 cherry origin, 19:263–317 chilling injury, 15:145–182 chlorosis, 9:161–165 citrus abscission, 15:145–182 citrus cold hardiness, 7:201–238 citrus, culture of young trees, 24:319–372 citrus dwarfing by viroids, 24:277–317 citrus flowering, 12:349–408 citrus irrigation, 30:37–82 cotoneaster, wild of Kazakhstan, 29:316–317 cranberry, 21:215–249 cranberry, wild of Kazakhstan, 29:349 cranberry harvesting, 16:298–311 currant, wild of Kazakhstan, 29:341 currant harvesting, 16:311–327 deficit irrigation, 21:105–131 dormancy release, 7:239–300 elderberry, wild of Kazakhstan, 29:349–350 Ericaceae nutrition, 10:183–227 fertilization, 1:104–106 fig, industry, 12:409–490 fireblight, 11:423–474 flowering, 12:223–264 foliar nutrition, 6:287–355 frost control, 11:45–109 gooseberry, wild of Kazakhstan, 29:341–342 grape, wild of Kazakhstan, 29:342–343

457 grape flower anatomy and morphology, 13:315–337 grape harvesting, 16:327–348 grape irrigation, 27:189–225 grape nitrogen metabolism, 14:407–452 grape pruning, 16:235–254, 336–340 grape root, 5:127–168 grape seedlessness, 11:164–176 grapevine pruning, 16:235–254, 336–340 greenhouse, China, 30:149–158 honey bee pollination, 9:244–250, 254–256 jojoba, 17:233–266 jujube, 32:229–298 in vitro culture, 7:157–200; 9:273–349 irrigation, deficit, 21:105–131 kiwifruit, 6:1–64; 12:307–347 lingonberry, 27:79–123 lingonberry, wild of Kazakhstan, 29:348–349 longan, 16:143–196 loquat, 23:233–276 lychee, 16:143–196, 28:393–453 mango fruit drop, 31:113–155 mountain ash, wild of Kazakhstan, 29:322–324 mulberry, wild of Kazakhstan, 29:350–351 muscadine grape breeding, 14:357–405 navel orange, 8:129–179 nectarine postharvest, 11:413–452 nondestructive postharvest quality evaluation, 20:1–119 nutritional ranges, 2:143–164 oleaster, wild of Kazakhstan, 29:351–353 olive physiology, 31:157–231 olive salinity tolerance, 21:177–214 orange, navel, 8:129–179 orchard floor management, 9:377–430 pawpaw, 31:351–384 peach origin, 17:331–379 peach orchard systems, 32:63–109 peach postharvest, 11:413–452 peach thinning, 28:351–392 pear, wild of Kazakhstan, 29:315–316 pear fruit disorders, 11:357–411; 27:227–267 pear maturity indices, 13:407–432

458 Fruit crops (cont.) pear scald, 27:227–267 pear volatiles, 28:237–324 pecan flowering, 8:217–255 photosynthesis, 11:111–157 Phytophthora control, 17:299–330 plum, wild of Kazakhstan, 29:330–332 plum origin, 23:179–231 pruning, 8:339–380 rambutan, 16:143–196 raspberry, 11:185–228 raspberry, wild of Kazakhstan, 29:343–345 roots, 2:453–457 rose, wild of Kazakhstan, 29:353–360 sapindaceous fruits, 16:143–196 sea buckthorn, wild of Kazakhstan, 29:361 short life and replant problem, 2:1–116 strawberry, wild of Kazakhstan, 29:347 strawberry fruit growth, 17:267–297 strawberry harvesting, 16:348–365 summer pruning, 9:351–375 Vaccinium nutrition, 10:183–227 vacciniums, wild of Kazakhstan, 29:347–349 viburnam, wild of Kazakhstan, 29:361–362 virus elimination, 28:187–236 water status, 7:301–344 water stress, 32:111–165 Functional phytochemicals, fruit, 27:269–315 Fungi: fig, 12:451–474 mushroom, 6:85–118 mycorrhiza, 3:172–213; 10:211–212 pathogens in postharvest storage, 3:412–461 truffle cultivation, 16:71–107 Fungicide, and apple fruit set, 1:416 G Galanthus, 25:22–25 Garlic, CA storage, 1:375 Genetic variation: alternate bearing, 4:146–150 photoperiodic response, 4:82 pollution injury, 8:16–19 temperature-photoperiod interaction, 17:73–123 wild apple, 29:63–303

CUMULATIVE SUBJECT INDEX Genetics and breeding: aroids (edible), 8:72–75; 12:169 aroids (ornamental), 10:18–25 bean, bacterial resistance, 3:28–58 bloom delay in fruits, 15:98–107 bulbs, flowering, 18:119–123 cassava, 12:164 chestnut blight resistance, 8:313–321 citrus cold hardiness, 7:221–223 cranberry, 21:236–239 embryogenesis, 1:23 fig, 12:432–433 fire blight resistance, 1:435–436 flowering, 15:287–290, 303–305, 306–309, 314–315; 27:1–39, 41–77 flower longevity, 1:208–209 ginseng, 9:197–198 grafting use, 28:109–115 in vitro techniques, 9:318–324; 18:119–123 lettuce, 2:185–187 lingonberry, 27:108–111 loquat, 23:252–257 muscadine grapes, 14:357–405 mushroom, 6:100–111 navel orange, 8:150–156 nitrogen nutrition, 2:410–411 pineapple, 21:138–164 plant regeneration, 3:278–283 pollution insensitivity, 8:18–19 potato tuberization, 14:121–124 rhododendron, 12:54–59 sweet potato, 12:175 sweet sorghum, 21:87–90 tomato parthenocarpy, 6:69–70 tomato ripening, 13:77–98 tree short life, 2:66–70 Vigna, 2:311–394 waxes, 23:50–53 woody legume tissue and cell culture, 14:311–314 yam (Dioscorea), 12:183 Geophyte, see Bulb, Tuber Geranium, fertilization, 5:355–357 Germination, seed, 2:117–141, 173–174; 24:229–275 Germplasm: acquisition, apple, 29:1–61 characterization, apple, 29:45–56 cryopreservation, 6:357–372 in vitro, 5:261–264; 9:324–325 pineapple, 21:133–175

CUMULATIVE SUBJECT INDEX resources, apple, 29:1–61 Gibberellin: abscission, citrus, 15:166–167 bloom delay, 15:111–114 citrus, abscission, 15:166–167 cold hardiness, 11:63 dormancy, 7:270–271 floral promoter, 4:114 flowering, 15:219–293, 315–318 genetic regulation, 16:15 grape root, 5:150–151 mango fruit drop, 31:113–155 mechanical stress, 17:19–20 Ginger postharvest physiology, 30:297–299 Ginseng, 9:187–236 Girdling, 1:416–417; 4:251–252, 30:1–26 Glucosinolates, 19:99–215 Gooseberry, wild of Kazakhstan, 29:341–342 Gourd, history, 25:71–171 Graft and grafting: herbaceous, 28:61–124 incompatibility, 15:183–232 phase change, 7:136–137, 141–142 rose, 9:56–57 Grape: CA storage, 1:308 chlorosis, 9:165–166 flower anatomy and morphology, 13:315–337 functional phytochemicals, 27:291–298 irrigation, 27:189–225 harvesting, 16:327–348 muscadine breeding, 14:357–405 nitrogen metabolism, 14:407–452 pollen morphology, 13:331–332 pruning, 16:235–254, 336–340 root, 5:127–168 seedlessness, 11:159–187 sex determination, 13:329–33 wild of Kazakhstan, 29:342–343 Gravitropism, 15:233–278 Greenhouse and greenhouse crops: carbon dioxide, 7:357–360, 544–545 China protected cultivation, 30:115–162 energy efficiency, 1:141–171; 9:1–52 growth substances, 7:399–481 nutrition and fertilization, 5:317–403 pest management, 13:1–66 vegetables, 21:1–39

459 Growth regulators, see Growth substances Growth substances, 2:60–66; 24:55–138, see also Abscisic acid, Auxin, Cytokinins, Ethylene, Gibberellins abscission, citrus, 15:157–176 apple bioregulation, 10:309–401 apple dwarfing, 3:315–375 apple fruit set, 1:417 apple thinning, 1:270–300 aroids, ornamental, 10:14–18 avocado fruit development, 10:229–243 bloom delay, 15:107–119 CA storage in vegetables, 1:346–348 cell cultures, 3:214–314 chilling injury, 15:77–83 citrus abscission, 15:157–176 cold hardiness, 7:223–225; 11:58–66 dormancy, 7:270–279 embryogenesis, 1:41–43; 2:277–281 floriculture, 7:399–481 flower induction, 4:190–195 flowering, 15:290–296 flower storage, 10:46–51 genetic regulation, 16:1–32 ginseng, 9:226 girdling, 20:1–26 grape seedlessness, 11:177–180 hormone reception, 26:49–84 in vitro flowering, 4:112–115 mango fruit drop, 31:113–155 mechanical stress, 17:16–21 meristem and shoot-tip culture, 5:221–227 navel oranges, 8:146–147 pear bioregulation, 10:309–401 petal senescence, 3:76–78 phase change, 7:137–138, 142–143 raspberry, 11:196–197 regulation, 11:1–14 rose, 9:53–73 seedlessness in grape, 11:177–180 triazole, 10:63–105 H Haemanthus, 25:25–28 Halo blight of beans, 3:44–45 Hardiness, 4:250–251 Harvest: flower stage, 1:211–212 index, 7:72–74

460 Harvest (cont.): lettuce, 2:176–181 mechanical of berry crops, 16:255–382 Hawthorne, wild of Kazakhstan, 29:317–322 Hazelnut. See Filbert wild of Kazakhstan, 29:365–366 Health phytochemicals: fruit, 27:269–315 vegetables, 28:125–185 Heat treatment (postharvest), 22:91–121 Heliconia, 14:1–55 Herbaceous plants, subzero stress, 6:373–417 Hippeastrum, 25:29–34 Histochemistry: flower induction, 4:177–179 fruit abscission, 1:172–203 Histology, flower induction, 4:179–184, see also Anatomy and morphology Honey bee, 9:237–272 Honeysuckle, wild of Kazakhstan, 29:350 Horseradish, CA storage, 1:368 Hydrolases, 5:169–219 Hydroponic culture, 5:1–44; 7:483–558 Hymenocallis, 25:59 Hypovirulence, in Endothia parasitica, 8:299–310 I Invasive plants, 32:379–437 Ismene, 25:59 Ice, formation and spread in tissues, 13:215–255 Ice-nucleating bacteria, 7:210–212; 13:230–235 Industrial crops, cactus, 18:309–312 Insects and mites: aroids, 8:65–66 avocado pollination, 8:275–277 fig, 12:442–447 hydroponic crops, 7:530–534 integrated pest management, 13:1–66 lettuce, 2:197–198 ornamental aroids, 10:18 particle film control, 31:1–45 tree short life, 2:52 tulip, 5:63, 92 waxes, 23:1–68 Integrated pest management, greenhouse crops, 13:1–66

CUMULATIVE SUBJECT INDEX In vitro: abscission, 15:156–157 apple propagation, 10:325–326 aroids, ornamental, 10:13–14 artemisia, 19:342–345 bioreactor technology, 24:1–30 bulbs, flowering, 18:87–169 cassava propagation, 13:121–123; 26:99–119 cellular salinity tolerance, 16:33–69 cold acclimation, 6:382 cryopreservation, 6:357–372 embryogenesis, 1:1–78; 2:268–310; 7:157–200; 10:153–181 environmental control, 17:123–170 flowering, 4:106–127 flowering bulbs, 18:87–169 pear propagation, 10:325–326 phase change, 7:144–145 propagation, 3:214–314; 5:221–277; 7:157–200; 9:57–58, 273–349; 17:125–172 thin cell layer morphogenesis, 14:239–264 woody legume culture, 14:265–332 Iron: deficiency and toxicity symptoms in fruits and nuts, 2:150 deficiency chlorosis, 9:133–186 Ericaceae nutrition, 10:193–195 foliar application, 6:330 nutrition, 5:324–325 pine bark media, 9:123 Irrigation: citrus, 30:37–82 deficit, deciduous orchards, 21:105–131; 32:111–165 drip or trickle, 4:1–48 frost control, 11:76–82 fruit trees, 7:331–332 grape, 27:189–225 grape root growth, 5:140–141 lettuce industry, 2:175 navel orange, 8:161–162 root growth, 2:464–465 scheduling, 32:111–165 J Jojoba, 17:233–266 Jujube, 32:229–298 Juvenility, 4:111–112

CUMULATIVE SUBJECT INDEX pecan, 8:245–247 tulip, 5:62–63 woody plants, 7:109–155 K Kale, fluid drilling of seed, 3:21 Kazakhstan, see Wild fruits and nuts Kiwifruit: botany, 6:1–64 vine growth, 12:307–347 L Lamps, for plant growth, 2:514–531 Lanzon, CA and MA, 22:149 Leaves: apple morphology, 12:283–288 flower induction, 4:188–189 Leek: CA storage, 1:375 fertilization, 1:118 Leguminosae, in vitro, 5:227–229; 14:265–332 Lemon, rootstock, 1:244–246, see also Citrus Lettuce: CA storage, 1:369–371 classification, 28:25–27 fertilization, 1:118 fluid drilling of seed, 3:14–17 industry, 2:164–207 seed germination, 24:229–275 tipburn, 4:49–65 Leucadendron, 32:167–228 Leucojum, 25:34–39 Leucospermum, 22:27–90 Light: fertilization, greenhouse crops, 5:330–331 flowering, 15:282–287, 310–312 fruit set, 1:412–413 lamps, 2:514–531 nitrogen nutrition, 2:406–407 orchards, 2:208–267 ornamental aroids, 10:4–6 photoperiod, 4:66–105 photosynthesis, 11:117–121 plant growth, 2:491–537 tolerance, 18:215–246 Lingonberry, 27:79–123 wild of Kazakhstan, 29:348–349 Longan, see also Sapindaceous fruits CA and MA, 22:150

461 Loquat: botany and horticulture, 23:233–276 CA and MA, 22:149–150 Lychee, see also Sapindaceous fruits CA and MA, 22:150 flowering, 28:397–421 fruit abscission, 28:437–443 fruit development, 28:433–436 pollination, 28:422–428 reproductive biology, 28:393–453 Lycoris, 25:39–43 M Magnesium: container growing, 9:84–85 deficiency and toxicity symptoms in fruits and nuts, 2:148 Ericaceae nutrition, 10:196–198 foliar application, 6:331 nutrition, 5:323 pine bark media, 9:117–119 Magnetic resonance imaging, 20:78–86, 225–266 Male sterility, temperature-photoperiod induction, 17:103–106 Mandarin, rootstock, 1:250–252 Manganese: deficiency and toxicity symptoms in fruits and nuts, 2:150–151 Ericaceae nutrition, 10:189–193 foliar application, 6:331 nutrition, 5:235–326 pine bark media, 9:123–124 Mango: alternate bearing, 4:145–146 asexual embryogenesis, 7:171–173 CA and MA, 22:151–157 CA storage, 1:313 fruit drop, 31:113–155 in vitro culture, 7:171–173 Mangosteen, CA and MA, 22:157 Mechanical harvest, berry crops, 16:255–382 Mechanical stress regulation, 17:1–42 Media: fertilization, greenhouse crops, 5:333 pine bark, 9:103–131 Medicinal crops: Artemisia, 19:319–371 poppy, 19:373–408 Taxus, 32:299–327

462 Melon grafting, 28:96–98 Meristem culture, 5:221–277 Metabolism: flower, 1:219–223 nitrogen in citrus, 8:181–215 seed, 2:117–141 Micronutrients: container growing, 9:85–87 pine bark media, 9:119–124 Micropropagation, see also In vitro; propagation: bulbs, flowering, 18:89–113 environmental control, 17:125–172 nuts, 9:273–349 rose, 9:57–58 temperate fruits, 9:273–349 tropical fruits and palms, 7:157–200 Microtu, see Vole Modified atmosphere (MA) for tropical fruits, 22:123–183 Moistureand seed storage, 2:125–132 Molecular biology: cassava, 26:85–159 floral induction, 27:3–20 flowering, 27:1–39;41–77 hormone reception, 26:49–84 Molybdenum nutrition, 5:328–329 Monocot, in vitro, 5:253–257 Monstera, see Aroids, ornamental Morphology: navel orange, 8:132–133 orchid, 5:283–286 pecan flowering, 8:217–243 red bayberry, 30: 92–96 Moth bean, genetics, 2:373–374 Mountain ash, wild of Kazakhstan, 29:322–324 Mulberry, wild of Kazakhstan, 29:350–351 Multiple cropping, 30:355–500 Mung bean, genetics, 2:348–364 Mushroom: CA storage, 1:371–372 cultivation, 19:59–97 spawn, 6:85–118 Muskmelon, fertilization, 1:118–119 Mycoplasma-like organisms, tree short life, 2:50–51 Mycorrhizae: container growing, 9:93 Ericaceae, 10:211–212

CUMULATIVE SUBJECT INDEX fungi, 3:172–213 grape root, 5:145–146 Myrica, see Red baybery N Narcissus, 25:43–48 Navel orange, 8:129–179 Nectarine: bloom delay, 15:105–106 CA storage, 1:309–310 postharvest physiology, 11:413–452 Nematodes: aroids, 8:66 fig, 12:475–477 lettuce, 2:197–198 tree short life, 2:49–50 Nerine, 25:48–56 NFT (nutrient film technique), 5:1–44 Nitrogen: CA storage, 8:116–117 container growing, 9:80–82 deficiency and toxicity symptoms in fruits and nuts, 2:146 Ericaceae nutrition, 10:198–202 fixation in woody legumes, 14:322–323 foliar application, 6:332 in embryogenesis, 2:273–275 metabolism in apple, 4:204–246 metabolism in citrus, 8:181–215 metabolism in grapevine, 14:407–452 nutrition, 2:395, 423; 5:319–320 pine bark media, 9:108–112 trickle irrigation, 4:29–30 vegetable crops, 22:185–223 Nomenclature, 28:1–60 Nondestructive quality evaluation of fruits and vegetables, 20:1–119 Nursery crops: fertilization, 1:106–112 nutrition, 9:75–101 Nut crops, see also Individual crop almond, wild of Kazakhstan, 29:262–265 almond postharvest technology and utilization, 20:267–311 chestnut, botany and horticulture, 31:293–349 chestnut blight, 8:291–336 fertilization, 1:106 hazelnut, wild of Kazakhstan, 29:365–366

CUMULATIVE SUBJECT INDEX honey bee pollination, 9:250–251 in vitro culture, 9:273–349 nutritional ranges, 2:143–164 pine, wild of Kazakhstan, 29:368–369 pistachio, wild of Kazakhstan, 29:366–368 pistachio culture, 3:376–396 walnut, wild of Kazakhstan, 29:369–370 Nutrient: concentration in fruit and nut crops, 2:154–162 film technique, 5:1–44 foliar-applied, 6:287–355 media, for asexual embryogenesis, 2:273–281 media, for organogenesis, 3:214–314 plant and tissue analysis, 7:30–56 solutions, 7:524–530 uptake, in trickle irrigation, 4:30–31 Nutrition (human): aroids, 8:79–84 CA storage, 8:101–127 phytochemicals in fruit, 27:269–315 phytochemicals in vegetables, 28:125–185 steroidal alkaloids, 25:171–196 Nutrition (plant): air pollution, 8:22–23, 26 blueberry, 10:183–227 calcifuge, 10:183–227 cold hardiness, 3:144–171 container nursery crops, 9:75–101 cranberry, 21:234–235 ecologically based, 24:156–172 embryogenesis, 1:40–41 Ericaceae, 10:183–227 fire blight, 1:438–441 foliar, 6:287–355 fruit and nut crops, 2:143–164 ginseng, 9:209–211 greenhouse crops, 5:317–403 kiwifruit, 12:325–332 mycorrhizal fungi, 3:185–191 navel orange, 8:162–166 nitrogen in apple, 4:204–246 nitrogen in vegetable crops, 22:185–223 nutrient film techniques, 5:18–21, 31–53 ornamental aroids, 10:7–14 pine bark media, 9:103–131

463 raspberry, 11:194–195 slow-release fertilizers, 1:79–139 O Oil palm: asexual embryogenesis, 7:187–188 in vitro culture, 7:187–188 Okra: botany and horticulture, 21:41–72 CA storage, 1:372–373 Oleaster, wild of Kazakhstan, 29:351–353 Olive: alternate bearing, 4:140–141 olive physiology, 31:147–231 salinity tolerance, 21:177–214 processing technology, 25:235–260 Onion: CA storage, 1:373–375 fluid drilling of seed, 3:17–18 Opium poppy, 19:373–408 Orange, see also Citrus alternate bearing, 4:143–144 sour, rootstock, 1:242–244 sweet, rootstock, 1:252–253 trifoliate, rootstock, 1:247–250 Orchard and orchard systems: floor management, 9:377–430 light, 2:208–267 root growth, 2:469–470 water, 7:301–344 Orchid: fertilization, 5:357–358 pollination regulation of flower development, 19:28–38 physiology, 5:279–315 Organogenesis, 3:214–314, see also In vitro; tissue culture Ornamental plants, see also individual plant Amaryllidaceae Banksia, 22:1–25 cactus grafting, 28:106–109 chlorosis, 9:168–169 cotoneaster, wild of Kazakhstan, 29:316–317 fertilization, 1:98–104, 106–116 flowering bulb roots, 14:57–88 flowering bulbs in vitro, 18:87–169 foliage acclimatization, 6:119–154 foliage industry, 31:47–112 heliconia, 14:1–55

464 Ornamental plants (cont.) honeysuckle, wild of Kazakhstan, 29:350 Leucadendron, 32:167–228 Leucospermum, 22:27–90 oleaster, wild of Kazakhstan, 29:351–353 orchid pollination regulation, 19:28–38 poppy, 19:373–408 protea leaf blackening, 17:173–201 rhododendron, 12:1–42 rose, wild of Kazakhstan, 29:353–360 viburnam, wild of Kazakhstan, 29:361–362 P Paclobutrazol, see Triazole Papaya: asexual embryogenesis, 7:176–177 CA and MA, 22:157–160 CA storage, 1:314 in vitro culture, 7:175–178 Parsley: CA storage, 1:375 drilling of seed, 3:13–14 Parsnip, fluid drilling of seed, 3:13–14 Parthenocarpy, tomato, 6:65–84 Particle films, 31:1–45 Passion fruit: in vitro culture, 7:180–181 CA and MA, 22:160–161 Pathogen elimination, in vitro, 5:257–261 Pawpaw, 31:351–384 Peach: bloom delay, 15:105–106 CA storage, 1:309–310 orchard systems, 32:63–109 origin, 17:333–379 postharvest physiology, 11:413–452 short life, 2:4 summer pruning, 9:351–375 thinning, 28:351–392 wooliness, 20:198–199 Peach palm (Pejibaye): in vitro culture, 7:187–188 Pear: bioregulation, 10:309–401 bloom delay, 15:106–107 CA storage, 1:306–308 decline, 2:11 fire blight control, 1:423–474

CUMULATIVE SUBJECT INDEX fruit disorders, 11:357–411; 27:227–267 fruit volatiles, 28:237–324 in vitro, 9:321 maturity indices, 13:407–432 root distribution, 2:456 scald, 27:227–267 short life, 2:6 wild of Kazakhstan, 29:315–316 Pecan: alternate bearing, 4:139–140 fertilization, 1:106 flowering, 8:217–255 in vitro culture, 9:314–315 Pejibaye, in vitro culture, 7:189 Pepper (Capsicum): CA storage, 1:375–376 fertilization, 1:119 fluid drilling in seed, 3:20 grafting, 28:104–105 phytochemicals, 28:161–162 Persimmon: CA storage, 1:314 quality, 4:259 Pest control: aroids (edible), 12:168–169 aroids (ornamental), 10:18 cassava, 12:163–164 cowpea, 12:210–213 ecologically based, 24:172–201 fig, 12:442–477 fire blight, 1:423–474 ginseng, 9:227–229 greenhouse management, 13:1–66 hydroponics, 7:530–534 particle films, 31:1–45 sweet potato, 12:173–175 vertebrate, 6:253–285 yam (Dioscorea), 12:181–183 Petal senescence, 11:15–43 pH: container growing, 9:87–88 fertilization greenhouse crops, 5:332–333 pine bark media, 9:114–117 soil testing, 7:8–12, 19–23 Phase change, 7:109–155 Phenology: apple, 11:231–237 raspberry, 11:186–190 Philodendron, see Aroids, ornamental

CUMULATIVE SUBJECT INDEX Phosphonates, Phytophthora control, 17:299–330 Phosphorus: container growing, 9:82–84 deficiency and toxicity symptoms in fruits and nuts, 2:146–147 nutrition, 5:320–321 pine bark media, 9:112–113 trickle irrigation, 4:30 Photoautotrophic micropropagation, 17:125–172 Photoperiod, 4:66–105, 116–117; 17:73–123 flowering, 15:282–284, 310–312 Photosynthesis: cassava, 13:112–114 efficiency, 7:71–72; 10:378 fruit crops, 11:111–157 ginseng, 9:223–226 light, 2:237–238 Physiology, see also Postharvest physiology Allium development, 32:329–378 apple crop load, 31:233–292 bitter pit, 11:289–355 blueberry development, 13:339–405 cactus reproductive biology, 18:321–346 calcium, 10:107–152 carbohydrate metabolism, 7:69–108 cassava, 13:105–129 citrus cold hardiness, 7:201–238 citrus irrigation, 30:55–67 conditioning 13:131–181 cut flower, 1:204–236; 3:59–143; 10:35–62 desiccation tolerance, 18:171–213 disease resistance, 18:247–289 dormancy, 7:239–300 embryogenesis, 1:21–23; 2:268–310 floral scents, 24:31–53 flower development, 19:1–58 flowering, 4:106–127 fruit ripening, 13:67–103 fruit softening, 10:107–152 ginseng, 9:211–213 girdling, 30: 1–26 glucosinolates, 19:99–215 grafting, 28:78–84 heliconia, 14:5–13 hormone reception, 26:49–84

465 juvenility, 7:109–155 lettuce seed germination, 24:229–275 light tolerance, 18:215–246 loquat, 23:242–252 lychee reproduction, 28:393–453 male sterility, 17:103–106 mango fruit drop, 31:113–155 mechanical stress, 17:1–42 nitrogen metabolism in grapevine, 14:407–452 nutritional quality and CA storage, 8:118–120 olive, 31:157–231 olive salinity tolerance, 21:177–214 orchid, 5:279–315 particle films, 31:1–45 petal senescence, 11:15–43 photoperiodism, 17:73–123 pollution injury, 8:12–16 polyamines, 14:333–356 potato tuberization, 14:89–188 pruning, 8:339–380 raspberry, 11:190–199 red bayberry, 30:96–99 regulation, 11:1–14 root pruning, 6:158–171 roots of flowering bulbs, 14:57–88 rose, 9:3–53 salinity hormone action, 16:1–32 salinity tolerance, 16:33–69 seed, 2:117–141 seed priming, 16:109–141 strawberry flowering, 28:325–349 subzero stress, 6:373–417 summer pruning, 9:351–375 sweet potato, 23:277–338 thin cell layer morphogenesis, 14:239–264 tomato fruit ripening, 13:67–103 tomato parthenocarpy, 6:71–74 triazoles, 10:63–105; 24:55–138 tulip, 5:45–125 vernalization, 17:73–123 volatiles, 17:43–72 water relations cut flowers, 18:1–85 watercore, 6:189–251 waxes, 23:1–68 Phytochemicals, functional: fruits, 27:269–315 vegetables, 28:125–185 Phytohormones. see Growth substances

466 Phytophthora control, 17:299–330 Phytotoxins, 2:53–56 Pigmentation: flower, 1:216–219 rose, 9:64–65 Pinching, by chemicals, 7:453–461 Pine, wild of Kazakhstan, 29:368–369 Pineapple: CA and MA, 22:161–162 CA storage, 1:314 genetic resources, 21:138–141 in vitro culture, 7:181–182 Pine bark, potting media, 9:103–131 Pistachio: alternate bearing, 4:137–139 culture, 3:376–393 in vitro culture, 9:315 wild of Kazakhstan, 29:366–368 Plantain: CA and MA, 22:141–146 in vitro culture, 7:178–180 Plant: architecture, 32:1–63 classification, 28:1–60 protection, short life, 2:79–84 systematics, 28:1–60 Plastic cover, sod production, 27:317–351 Plum: CA storage, 1:309 origin, 23:179–231 wild of Kazakhstan, 29:330–332 Poinsettia, fertilization, 1:103–104; 5:358–360 Pollen, desiccation tolerance, 18:195 Pollination: apple, 1:402–404 avocado, 8:272–283 cactus, 18:331–335 embryogenesis, 1:21–22 fig, 12:426–429 floral scents, 24:31–53 flower regulation, 19:1–58 fruit crops, 12:223–264 fruit set, 4:153–154 ginseng, 9:201–202 grape, 13:331–332 heliconia, 14:13–15 honey bee, 9:237–272 kiwifruit, 6:32–35 lychee, 28:422–428

CUMULATIVE SUBJECT INDEX navel orange, 8:145–146 orchid, 5:300–302 petal senescence, 11:33–35 protection, 7:463–464 rhododendron, 12:1–67 Pollution, 8:1–42 Polyamines: chilling injury, 15:80 in horticulture, 14:333–356 mango fruit drop, 31:125–127 Polygalacturonase, 13:67–103 Poppy, opium, 19:373–408 Postharvest physiology: almond, 20:267–311 apple bitter pit, 11:289–355 apple maturity indices, 13:407–432 apple scald, 27:227–257 apple weight loss, 25:197–234 aroids, 8:84–86 asparagus, 12:69–155 CA for tropical fruit, 22:123–183 CA for storage and quality, 8:101–127 carrot storage: 30:284–288 cassava storage, 30:288–295 chlorophyll fluorescence, 23:69–107 coated fruits and vegetables, 26:161–238 cut flower, 1:204–236; 3:59–143; 10:35–62 foliage plants, 6:119–154 fresh-cut fruits and vegetables, 30:85–255 fruit, 1:301–336 fruit softening, 10:107–152 ginger storage, 30:297–299 Jerusalem artichoke storage, 30:271–276 heat treatment, 22:91–121 lettuce, 2:181–185 low-temperature sweetening, 17:203–231, 30:317–355 MA for tropical fruit, 22:123–183 navel orange, 8:166–172 nectarine, 11:413–452 nondestructive quality evaluation, 20:1–119 pathogens, 3:412–461 peach, 11:413–452 pear disorders, 11:357–411; 27:227–267 pear maturity indices, 13:407–432 pear scald, 27:227–257

CUMULATIVE SUBJECT INDEX petal senescence, 11:15–43 potato low temperature sweetening, 30:317–355 potato storage, 30:259–271 protea leaf blackening, 17:173–201 quality evaluation, 20:1–119 scald, 27:227–267 seed, 2:117–141 sweet potato storage, 30:276–284 texture in fresh fruit, 20:121–244 taro storage, 30:295–297 tomato fruit ripening, 13:67–103 vegetables, 1:337–394 watercore, 6:189–251; 11:385–387 Potassium: container growing, 9:84 deficiency and toxicity symptoms in fruits and nuts, 2:147–148 foliar application, 6:331–332 nutrition, 5:321–322 pine bark media, 9:113–114 trickle irrigation, 4:29 Potato: CA storage, 1:376–378 classification, 28:23–26 fertilization, 1:120–121 low temperature sweetening, 17:203–231; 30:317–353 phytochemicals, 28:160–161 postharvest physiology and storage, 259–271 tuberization, 14:89–198 Processing, table olives, 25:235–260 Propagation, see also In vitro apple, 10:324–326; 12:288–295 aroids, ornamental, 10:12–13 bioreactor technology, 24:1–30 cassava, 13:120–123 floricultural crops, 7:461–462 foliage plants, 31:47–112 ginseng, 9:206–209 orchid, 5:291–297 pear, 10:324–326 rose, 9:54–58 tropical fruit, palms 7:157–200 woody legumes in vitro, 14:265–332 Protaceous flower crop: Banksia, 22:1–25 Leukcadendron, 32:167–228 Leucospermum, 22:27–90 Protea, 17:173–201; 26:1–48

467 Protea floricultural crop, 26:1–48 leaf blackening, 17:173–201 Protected crops, carbon dioxide, 7:345–398 Protoplast culture, woody species, 10:173–201 Pruning: alternate bearing, 4:161 apple, 9:351–375 apple training, 1:414 chemical, 7:453–461 cold hardiness, 11:56 fire blight, 1:441–442 grapevines, 16:235–254 light interception, 2:250–251 peach, 9:351–375 phase change, 7:143–144 physiology, 8:339–380 plant architecture, 32:1–63 root, 6:155–188 Prunus, see also Almond; Cherry; Nectarine; Peach; Plum in vitro, 5:243–244; 9:322 root distribution, 2:456 Pseudomonas: phaseolicola, 3:32–33, 39, 44–45 solanacearum, 3:33 syringae, 3:33, 40; 7:210–212 Pumpkin, history, 25:71–170 Q Quality evaluation: fruits and vegetables, 20:1–119, 121–224 nondestructive, 20:1–119 texture in fresh fruit, 20:121–224 R Rabbit, 6:275–276 Radish, fertilization, 1:121 Rambutan. see Sapindaceous fruits CA and MA, 22:163 Raspberry: harvesting, 16:282–298 productivity, 11:185–228 wild of Kazakhstan, 29:343–345 Red bayberry, 30:83–113 Rejuvenation: rose, 9:59–60 woody plants, 7:109–155

468 Replant problem, deciduous fruit trees, 2:1–116 Respiration: asparagus postharvest, 12:72–77 fruit in CA storage, 1:315–316 kiwifruit, 6:47–48 vegetables in CA storage, 1:341–346 Rhizobium, 3:34, 41 Rhododendron, 12:1–67 Rice bean, genetics, 2:375–376 Root: apple, 12:269–272 cactus, 18:297–298 diseases, 5:29–31 environment, nutrient film technique, 5:13–26 Ericaceae, 10:202–209 grape, 5:127–168 kiwifruit, 12:310–313 physiology of bulbs, 14:57–88 pruning, 6:155–188 raspberry, 11:190 rose, 9:57 tree crops, 2:424–490 Root and tuber crops: Amaryllidaceae, 25:1–79 aroids, 8:43–99; 12:166–170 carrot postharvest physiology, 30:284–288 cassava crop physiology, 13:105–129 cassava molecular biology, 26:85–159 cassava multiple cropping, 30:355–50 cassava postharvest physiology, 30:288–295 cassava root crop, 12:158–166 low-temperature sweetening, 17:203–231, 30:317 -355 minor crops, 12:184–188 potato low temperature sweetening, 30:317–355 potato tuberization, 14:89–188 sweet potato, 12:170–176 sweet potato physiology, 23:277–338 sweet potato postharvest physiology, 30:276–284 taro postharvest physiology, 30:295–297 yam (Dioscorea), 12:177–184 Rootstocks: alternate bearing, 4:148 apple, 1:405–407; 12:295–297

CUMULATIVE SUBJECT INDEX avocado, 17:381–429 citrus, 1:237–269 cold hardiness, 11:57–58 fire blight, 1:432–435 light interception, 2:249–250 navel orange, 8:156–161 root systems, 2:471–474 stress, 4:253–254 tree short life, 2:70–75 Rosaceae, in vitro, 5:239–248 Rose: fertilization, 1:104; 5:361–363 growth substances, 9:3–53 in vitro, 5:244–248 wild of Kazakhstan, 29:353–360 S Salinity: air pollution, 8:25–26 citrus irrigation, 30:37–83 olive, 21:177–214 soils, 4:22–27 tolerance, 16:33–69 Sapindaceous fruits, 16:143–196 Sapodilla, CA and MA, 22:164 Scadoxus, 25:25–28 Scald, apple and pear, 27:227–265 Scoring and fruit set, 1:416–417 Sea buckthorn, wild of Kazakhstan, 29:361 Seed: abortion, 1:293–294 apple anatomy and morphology, 10:285–286 conditioning, 13:131–181 desiccation tolerance, 18:196–203 environmental influences on size and composition, 13:183–213 flower induction, 4:190–195 fluid drilling, 3:1–58 grape seedlessness, 11:159–184 kiwifruit, 6:48–50 lettuce, 2:166–174 lettuce germination, 24:229–275 priming, 16:109–141 rose propagation, 9:54–55 vegetable, 3:1–58 viability and storage, 2:117–141 Secondary metabolites, woody legumes, 14:314–322 Senescence: chlorophyll senescence, 23:88–93

CUMULATIVE SUBJECT INDEX cut flower, 1:204–236; 3:59–143; 10:35–62; 18:1–85 petal, 11:15–43 pollination-induced, 19:4–25 rose, 9:65–66 whole plant, 15:335–370 Sensory quality: CA storage, 8:101–127 Shoot-tip culture, 5:221–277, see also Micropropagation Short life problem, fruit crops, 2:1–116 Signal transduction, 26:49–84 Small fruit, CA storage, 1:308 Snapdragon fertilization, 5:363–364 Sod production, 27:317–351 Sodium, deficiency and toxicity symptoms in fruits and nuts, 2:153–154 Soil: grape root growth, 5:141–144 management and root growth, 2:465–469 orchard floor management, 9:377–430 plant relations, trickle irrigation, 4:18–21 stress, 4:151–152 testing, 7:1–68; 9:88–90 zinc, 23:109–178 Soilless culture, 5:1–44 Solanaceae: in vitro, 5:229–232 steroidal alkaloids, 25:171–196 Somatic embryogenesis. See Asexual embryogenesis Sorghum, sweet, 21:73–104 Spathiphyllum, see Aroids, ornamental Squash, history, 25:71–170 Stem, apple morphology, 12:272–283 Sternbergia, 25:59 Steroidal alkaloids, solanaceous, 25:171–196 Storage, see also Postharvest physiology, Controlled-atmosphere (CA) storage carrot postharvest physiology, 30:284–288 cassava postharvest physiology, 30: 288–295 cut flower, 3:96–100; 10:35–62 ginger postharvest physiology, 30:297–299 Jerusalem artichoke postharvest physiology, 30:259–271

469 low temperature sweetening, 17:203–231; 30:317–353 potato low temperature sweetening, 30:317–353 potato postharvedst physiology, 30:259–271 root and tuber crops, 30:253–316 rose plants, 9:58–59 seed, 2:117–141 sweetpotato postharvest physiology, 30:295–297 taro postharvest physiology, 30:295–297 Strawberry: fertilization, 1:106 flowering, 28:325–349 fruit growth and ripening, 17:267–297 functional phytonutrients, 27: 303–304 harvesting, 16:348–365 in vitro, 5:239–241 wild of Kazakhstan, 29:347 Stress: benefits of, 4:247–271 chlorophyll fluorescence, 23:69–107 climatic, 4:150–151 flooding, 13:257–313 irrigation scheduling, 32:11–165 mechanical, 17:1–42 olive, 31:2207–217 petal, 11:32–33 plant, 2:34–37 protectants (triazoles), 24:55–138 protection, 7:463–466 salinity tolerance in olive, 21:177–214 subzero temperature, 6:373–417 waxes, 23:1–68 Sugar, see also Carbohydrate allocation, 7:74–94 flowering, 4:114 Sugar apple, CA and MA, 22:164 Sugar beet, fluid drilling of seed, 3:18–19 Sulfur: deficiency and toxicity symptoms in fruits and nuts, 2:154 nutrition, 5:323–324 Sweet potato: culture, 12:170–176 fertilization, 1:121 physiology, 23:277–338 postharvest physiology and storage, 30:276–284

470 Sweet sop, CA and MA, 22:164 Symptoms, deficiency and toxicity symptoms in fruits and nuts, 2:145–154 Syngonium, see Aroids, ornamental Systematics, 28:1–60 T Taro, see Aroids, edible postharvest physiology and storage, 30:276–284 Taxus, 32:299–327 Taxonomy, 28:1–60 Tea, botany and horticulture, 22:267–295 Temperature: apple fruit set, 1:408–411 bloom delay, 15:119–128 CA storage of vegetables, 1:340–341 chilling injury, 15:67–74 cryopreservation, 6:357–372 cut flower storage, 10:40–43 fertilization, greenhouse crops, 5:331–332 fire blight forecasting, 1:456–459 flowering, 15:284–287, 312–313 interaction with photoperiod, 4:80–81 low temperature sweetening, 17:203–231 navel orange, 8:142 nutrient film technique, 5:21–24 photoperiod interaction, 17:73–123 photosynthesis, 11:121–124 plant growth, 2:36–37 seed storage, 2:132–133 subzero stress, 6:373–417 Texture in fresh fruit, 20:121–224 Thinning: apple, 1:270–300 peach and Prunus, 28:351–392 Tipburn, in lettuce, 4:49–65 Tissue: see also In vitro culture 1:1–78; 2:268–310; 3:214–314; 4:106–127; 5:221–277; 6:357–372; 7:157–200; 8:75–78; 9:273–349; 10:153–181; 24:1–30 cassava, 26:85–159 dwarfing, 3:347–348 nutrient analysis, 7:52–56; 9:90 Tomato: CA storage, 1:380–386 classification, 28:21–23

CUMULATIVE SUBJECT INDEX chilling injury, 20:199–200 fruit cracking, 30:163–184 fertilization, 1:121–123 fluid drilling of seed, 3:19–20 fruit ripening, 13:67–103 galacturonase, 13:67–103 grafting, 28:98–103 greenhouse quality, 26:239 parthenocarpy, 6:65–84 phytochemicals, 28:160 Toxicity symptoms in fruit and nut crops, 2:145–154 Transport, cut flowers, 3:100–104 Tree decline, 2:1–116 Triazoles, 10:63–105; 24:55–138 chilling injury, 15:79–80 Trickle irrigation, 4:1–48 Truffle cultivation, 16:71–107 Tuber, potato, 14:89–188 Tuber and root crops. See Root and tuber crops Tulip, see also Bulb fertilization, 5:364–366 in vitro, 18:144–145 physiology, 5:45–125 Tunnel (cloche), 7:356–357 Turfgrass, fertilization, 1:112–117 Turnip, fertilization, 1:123–124 Turnip Mosaic Virus, 14:199–238 U Urd bean, genetics, 2:364–373 Urea, foliar application, 6:332 V Vaccinium, 10:185–187, see also Blueberry; Cranberry; Lingonberry functional phytonutrients, 27:303 wild of Kazakhstan, 29:347–349 Vase solutions, 3:82–95; 10:46–51 Vegetable crops, see also Specific crop Allium development, 329–378 Allium phytochemicals, 28:156–159 aroids, 8:43–99; 12:166–170 asparagus postharvest, 12:69–155 cactus, 18:300–302 carrot postharvest physiology and storage, 30:284–288 cassava: cassava molecular biology, 26:85–159

CUMULATIVE SUBJECT INDEX cassava multiple cropping, 30:355–450 cassava postharvest physiology and storage, 30:288–295 cassava root crop, 12:158–166 crop physiology, 13:105–129 CA storage, 1:337–394 CA storage and quality, 8:101–127 CA storage diseases, 3:412–461 caper bush, 27:125–188 chilling injury, 15:63–95 coating physiology, 26:161–238 crucifer phytochemicals, 28:150–156 cucumber grafting, 28:91–96 ecologically based, 24:139–228 eggplant grafting, 28:103–104 eggplant phytochemicals, 28:162–163 fertilization, 1:117–124 fluid drilling of seeds, 3:1–58 fresh cut, 30:185–255 ginger postharvest physiology and storage, 30:297–299 gourd history, 25:71–170 grafting, 28:61–124 greenhouse management, 21:1–39 greenhouse pest management, 13:1–66 greenhouses in China, 30:126–141 honey bee pollination, 9:251–254 hydroponics, 7:483–558 Jerusalem artichoke postharvest physiology and; storage, 30:271–276 lettuce seed germination, 24:229–275 low-temperature sweetening, 17:203–231 melon grafting, 28:96–98 minor root and tubers, 12:184–188 mushroom cultivation, 19:59–97 mushroom spawn, 6:85–118 N nutrition, 22:185–223 nondestructive postharvest quality evaluation, 20:1–119 okra, 21:41–72 pepper phytochemicals, 28:161–162 phytochemicals, 28:125–185 potato low temperature sweetening, 30:317–353 potato postharvest physiology and storage, 30:271–276 potato phytochemicals, 28:160–161 potato tuberization, 14:89–188 pumpkin history, 25:71–170

471 root and tuber postharvest and storage, 30: 295–297 seed conditioing, 13:131–181 seed priming, 16:109–141 squash history, 25:71–170 steroidal alkaloids, Solanaceae, 25:171–196 sweet potato, 12:170–176 sweet potato physiology, 23:277–338 tomato (greenhouse) fruit cracking, 30:163–184 tomato fruit ripening, 13:67–103 tomato (greenhouse) quality: 26:239–319 tomato parthenocarpy, 6:65–84 tomato phytochemicals, 28:160 tropical production, 24:139–228 truffle cultivation, 16:71–107 watermelon grafting, 28:86–91 yam (Dioscorea), 12:177–184 Vegetative tissue, desiccation tolerance, 18:176–195 Vernalization, 4:117; 15:284–287; 17:73–123 Vertebrate pests, 6:253–285 Viburnam, wild of Kazakhstan, 29:361–362 Vigna, see also Cowpea genetics, 2:311–394 U.S. production, 12:197–222 Viroid, dwarfing for citrus, 24:277–317 Virus: benefits in horticulture, 3:394–411 dwarfing for citrus, 24:277–317 elimination, 7:157–200; 9:318; 18:113–123; 28:187–236 fig, 12:474–475 tree short life, 2:50–51 turnip mosaic, 14:199–238 Volatiles, 17:43–72; 24:31–53; 28:237–324 Vole, 6:254–274 W Walnut: in vitro culture, 9:312 wild of Kazakhstan, 29:369–370 Water relations: cut flower, 3:61–66; 18:1–85 citrus, 30:37–83 deciduous orchards, 21:105–131

472 Water relations (cont.) desiccation tolerance, 18:171–213 fertilization, grape and grapevine, 27:189–225 kiwifruit, 12:332–339 light in orchards, 2:248–249 Water relations (cont.): photosynthesis, 11:124–131 trickle irrigation, 4:1–48 Watercore, 6:189–251 apple, 6:189–251 pear, 11:385–387 Watermelon: fertilization, 1:124 grafting, 28:86–91 Wax apple, CA and MA, 22:164 Waxes, 23:1–68 Weed control, ginseng, 9:228–229 Weeds: invasive, 32:379–437 lettuce research, 2:198 virus, 3:403 Wild fruit and nuts of Kazakhstan, 29:305–371 almond, 29:262–265 apple, 29:63–303, 305–315 apricot, 29:325–326 barberry, 29:332–336 bilberry, 29:347–348 blackberry, 29:345 cherry, 29:326–330 cotoneaster, 29:316–317 cranberry, 29:349 currant, 29:341 elderberry, 29:349–350 gooseberry, 29:341–342 grape, 29:342–343 hazelnut, 29:365–366 lingonberry, 29:348–349 mountain ash, 29:322–324

CUMULATIVE SUBJECT INDEX mulberry, 29:350–351 oleaster, 29:351–353 pear, 29:315–316 pine, 29:368–369 pistachio, 29:366–368 plum, 29:330–332 raspberry, 29:343–345 rose, 29:353–360 sea buckthorn, 29:361 strawberry, 29:347 vacciniums, 29:347–349 viburnam, 29:361–362 walnut, 29:369–370 Woodchuck, 6:276–277 Woody species, somatic embryogenesis, 10:153–181 X Xanthomonas phaseoli, 3:29–32, 41, 45–46 Xanthophyll cycle, 18:226–239 Xanthosoma, 8:45–46, 56–57, see also Aroids Y Yam (Dioscorea), 12:177–184 Yield: determinants, 7:70–74; 97–99 limiting factors, 15:413–452 Z Zantedeschi, see Aroids, ornamental Zephyranthes, 25:60–61 Zinc: deficiency and toxicity symptoms in fruits and nuts, 2:151 foliar application, 6:332, 336 nutrition, 5:326; 23:109–178 pine bark media, 9:124 Zizipus, see Jujube

Cumulative Contributor Index (Volumes 1–32)

Abbott, J.A., 20:1 Adams III, W.W., 18:215 Afek, U., 30:253 Aldwinckle, H.S., 1:423; 15:xiii, 29:1 Amarante, C., 28:161 Anderson, I.C., 21:73 Anderson, J.L., 15:97 Anderson, P.C., 13:257 Andrews, P.K., 15:183 Ashworth, E.N., 13:215; 23:1 Asokan, M.P., 8:43 Atkinson, D., 2:424 Aung, L.H., 5:45 Bailey, W.G., 9:187 Baird, L.A.M., 1:172 Banks, N.H., 19:217; 25:197; 26:161 Barden, J.A., 9:351 Barker, A.V., 2:411 Bartz, J.A., 30:185 Bass, L.N., 2:117 Bassett, C. L., 26:49 Becker, J.S., 18:247 Beer, S.V., 1:423 Behboudian, M.H., 21:105; 27:189 Ben-Jaacov, J., 32:167 Bennett, A.B., 13:67 Benschop, M., 5:45 Ben-Ya’acov, A., 17:381 Benzioni, A., 17:233 Bevington, K.B., 24:277 Bewley, J.D., 18:171 Binzel, M.L., 16:33 Blanpied, G.D., 7:xi

Blenkinsop, R.W., 30:317 Bliss, F.A., 16:xiii; 28:xi Boardman, K. 27 xi Borochov, A., 11:15 Bounous, G.; 31:293 Bower, J.P., 10:229 Bradley, G.A., 14:xiii Brandenburg, W., 28:1 Brecht, J.K., 30:185 Brennan, R., 16:255 Broadbent, P., 24:277 Broschat, T.K., 14:1 Brown, S. 15:xiii Buban, T., 4:174 Bukovac, M.J., 11:1 Burke, M.J., 11:xiii Buwalda, J.G., 12:307 Byers, R.E., 6:253; 28:351 Caldas, L.S., 2:568 Campbell, L.E., 2:524 Cantliffe, D.J., 16:109; 17:43; 24:229; 28:325 Carter, G., 20:121 Carter, J.V., 3:144 Cathey, H.M., 2:524 Chambers, R.J., 13:1 Chandler, C.K. 28:325 Charron, C.S., 17:43 Chen, J., 31:47 Chen, K., 30:83 Chen, Z., 25:171 Chin, C.K., 5:221 Clarke, N.D., 21:1

Horticultural Reviews, Volume 32, Edited by Jules Janick ISBN 0-471-73216-8 © 2005 John Wiley & Sons, Inc. 473

474 Coetzee, J.H., 26:1 Cohen, M., 3:394 Collier, G.F., 4:49 Collins, G., 25:235 Collins, W.L., 7:483 Colmagro, S., 25:235 Compton, M.E., 14:239 Conover, C.A., 5:317; 6:119 Connor, D.J., 31:157 Coombs, B., 32:xi Coppens d’Eeckenbrugge, G., 21:133 Corelli-Grappadelli, L., 32:63 Costa, G. 28:351 Costes, E., 32:1 Coyne, D.P., 3:28 Crane, J.C., 3:376 Criley, R.A., 14:1; 22:27; 24:x Crowly, W., 15:1 Cutting, J.G., 10:229 Daie, J., 7:69 Dale, A., 11:185; 16:255 Darnell, R.L., 13:339, 28:325 Davenport, T.L., 8:257; 12:349; 31:113 Davies, F.S., 8:129; 24:319 Davies, P.J., 15:335 Davis, T.D., 10:63; 24:55 Decker, H.F., 27:317 DeEll, J.R., 23:69 DeGrandi-Hoffman, G., 9:237 De Hertogh, A.A., 5:45; 14:57; 18:87; 25:1 Deikman, J., 16:1 DellaPenna, D., 13:67 DeLong, J.M., 32:299 Demers, D.-A., 30:163 Demmig-Adams, B., 18:215 Dennis, F.G., Jr., 1:395 Dickson, E.E., 29:1 Dorais, M., 26:239; 30:163 Doud, S.L., 2:1 Dudareva, N., 24:31 Duke, S.O., 15:371 Dunavent, M.G., 9:103 Duval, M.-F., 21:133 Düzyaman, E., 21:41 Dyer, W.E., 15:371 Dzhangaliev, A.D., 29:63, 305 Early, J.D., 13:339 Eastman, K., 28:125 Elfving, D.C., 4:1; 11:229

CUMULATIVE CONTRIBUTOR INDEX El-Goorani, M.A., 3:412 Esan, E.B., 1:1 Evans, D.A., 3:214 Ewing, E.E., 14:89 Faust, M., 2:vii, 142; 4:174; 6:287; 14:333; 17:331; 19:263; 22:225; 23:179 Felkey, K., 30:185 Fenner, M., 13:183 Fenwick, G.R., 19:99 Fereres, E., 31:157 Ferguson, A.R., 6:1 Ferguson, I.B., 11:289; 30:83; 31:233 Ferguson, J.J., 24:277 Ferguson, L., 12:409 Ferree, D.C., 6:155; 31:xi Ferreira, J.F.S., 19:319 Fery, R.L., 2:311; 12:157 Fischer, R.L., 13:67 Fletcher, R.A., 24:53 Flick, C.E., 3:214 Flore, J.A., 11:111 Forshey, C.G., 11:229 Forsline, P.L., 29:ix; 1 Franks, R. G., 27:41 Fujiwara, K., 17:125 Gazit, S., 28:393 Geisler, D., 6:155 Geneve, R.L., 14:265 George, W.L., Jr., 6:25 Gerrath, J.M., 13:315 Gilley, A., 24:55 Giovannetti, G., 16:71 Giovannoni, J.J., 13:67 Glenn, G.M., 10:107; 31:1 Goffinet, M.C., 20:ix Goldschmidt, E.E., 4:128; 30:1 Goldy, R.G., 14:357 Goren, R., 15:145; 30:1 Gosselin, A., 26:239 Goszczynska, D.M., 10:35 Grace, S.C., 18:215 Gradziel, T.M., 30: xiii Graves, C.J., 5:1 Gray, D., 3:1 Grierson, W., 4:247 Griffen, G.J., 8:291 Grodzinski, B., 7:345 Gucci, R., 21:177 Guest, D.I., 17:299 Guiltinan, M.J., 16:1

CUMULATIVE CONTRIBUTOR INDEX Hackett, W.P., 7:109 Halevy, A.H., 1:204; 3:59 Hallett, I.C., 20:121 Hammerschmidt, R., 18:247 Hanson, E.J., 16:255 Harker, F.R., 20:121 Heaney, R.K., 19:99 Heath, R.R., 17:43 Helzer, N.L., 13:1 Hendrix, J.W., 3:172 Henny, R.J., 10:1; 31:47 Hergert, G.B., 16:255 Hess, F.D., 15:371 Hetterscheid, W.L.A., 28:1 Heywood, V., 15:1 Hjalmarsson, I., 27:79–123 Hogue, E.J., 9:377 Hokanson, S.C. 29:1 Holt, J.S., 15:371 Huber, D.J., 5:169 Huberman, M., 30:1 Hunter, E.L., 21:73 Hutchinson, J.F., 9:273 Hutton, R.J., 24:277 Indira, P., 23:277 Ingle, M. 27:227 Isenberg, F.M.R., 1:337 Iwakiri, B.T., 3:376 Jackson, J.E., 2:208 Janick, J., 1:ix; 8:xi; 17:xiii; 19:319; 21:xi; 23:233 Jarvis, W.R., 21:1 Jenks, M.A., 23:1 Jensen, M.H., 7:483 Jeong, B.R., 17:125 Jewett, T.J., 21:1 Jiang, W., 30:115 Joiner, J.N., 5:317 Jones, H.G., 7:301 Jones, J.B., Jr., 7:1 Jones, R.B., 17:173 Kagan-Zur, V., 16:71 Kalt, W. 27:269; 28:125 Kamenetsky, R., 32:329 Kang, S.-M., 4:204 Kato, T., 8:181 Kawa, L., 14:57 Kawada, K., 4:247 Kays, S.J., 30:253

475 Kelly, J.F., 10:ix; 22:xi Kester, D.E., 25:xii Khan, A.A., 13:131 Kierman, J., 3:172 Kim, K.-W., 18:87 Kinet, J.-M., 15:279 King, G.A., 11:413 Kingston, C.M., 13:407–432 Kirschbaum, D.S. 28:325 Kliewer, W.M., 14:407 Knight, R.J., 19:xiii Knox, R.B., 12:1 Kofranek, A.M., 8:xi Korcak, R.F., 9:133; 10:183 Kozai, T., 17:125 Krezdorn, A.H., 1:vii Kushad, M.M., 28:125 Lakso, A.N., 7:301; 11:111 Laimer, M., 28:187 Lamb, R.C., 15:xiii Lang, G.A., 13:339 Larsen, R.P., 9:xi Larson, R.A., 7:399 Lauri, P.E. 32:1 Layne, D.R., 31:351 Leal, F., 21:133 Ledbetter, C.A., 11:159 Lee, J.-M., 28:61 Levy, Y., 30:37 Li, P.H., 6:373 Liu, M., 32: 229 Lill, R.E., 11:413 Lin, S., 23:233 Liu, Z., 27:41 Lipton, W.J., 12:69 Littlejohn, G.M., 26:1 Litz, R.E., 7:157 Lockard, R.G., 3:315 Loescher, W.H., 6:198 Lorenz, O.A., 1:79 Lu, R., 20:1 Luby, J.J., 29:1 Lurie, S., 22:91–121 Lyrene, P., 21:xi Maguire, K.M., 25:197 Malik, A.U., 31:113 Manivel, L., 22:267 Maraffa, S.B., 2:268 Marangoni, A.G., 17:203; 30:317 Marini, R.P., 9:351; 32:63

476 Marinoni, D.T., 31:293 Marlow, G.C., 6:189 Maronek, D.M., 3:172 Martin, G.G., 13:339 Masiunas, J., 28:125 Mayak, S., 1:204; 3:59 Maynard, D.N., 1:79 McConchie, R., 17:173 McConnell, D.B., 31:47 McNicol, R.J., 16:255 Merkle, S.A., 14:265 Michailides, T.J., 12:409 Michelson, E., 17:381 Mika, A., 8:339 Miller, A.R., 25:171 Miller, S.S., 10:309 Mills, H.A., 2:411; 9:103 Mills, T.M., 21:105 Mitchell, C.A., 17:1 Mizrahi, Y., 18:291, 321 Mohankumar, C.R., 30:355 Molnar, J.M., 9:1 Monk, G.J., 9:1 Monselise, S.P., 4:128 Moore, G.A., 7:157 Mor, Y., 9:53 Morris, J.R., 16:255 Mu, D., 30:115 Murashige, T., 1:1 Murr, D.P., 23:69 Murray, S.H., 20:121 Myers, P.N., 17:1 Nadeau, J.A., 19:1 Naor, A., 32:111 Nascimento, W.M., 24:229 Neilsen, G.H., 9:377 Nelson, P.V., 26:xi Nerd, A., 18:291, 321 Niemiera, A.X., 9:75; 32:379 Nobel, P.S., 18:291 Norman, D.J., 31:47 Nyujtò, F., 22:225 Oda, M., 28:61 O’Donoghue, E.M., 11:413 Ogden, R.J., 9:103 O’Hair, S.K., 8:43; 12:157 Oliveira, C.M., 10:403 Oliver, M.J., 18:171 O’Neill, S.D., 19:1 Opara, L.U., 19:217; 24:373; 25:197

CUMULATIVE CONTRIBUTOR INDEX Ormrod, D.P., 8:1 Ortiz, R., 27:79 Palser, B.F., 12:1 Papadopoulos, A.P., 21:1; 26:239; 30:163 Pararajasingham, S., 21:1 Parera, C.A., 16:109 Paris, H.S., 25:71 Pegg, K.G., 17:299 Pellett, H.M., 3:144 Perkins-Veazil, P., 17:267 Phillips, G., 32:379 Pichersky, E., 24:31 Piechulla, B., 24:31 Ploetz, R.C., 13:257 Pokorny, F.A., 9:103 Pomper, K.W., 31:351 Poole, R.T., 5:317; 6:119 Poovaiah, B.W., 10:107 Portas, C.A.M., 19:99 Porter, M.A., 7:345 Possingham, J.V., 16:235 Prange, R.K., 23:69; 32:299 Pratt, C., 10:273; 12:265 Predieri, S., 28:237 Preece, J.E., 14:265 Priestley, C.A., 10:403 Proctor, J.T.A., 9:187 Puonti-Kaerlas, J., 26:85 Puterka, G.J., 31:1 Qu, D., 30:115 Quamme, H., 18:xiii Rabinowitch, H.D., 32:329 Raese, J.T., 11:357 Ramming, D.W., 11:159 Rapparini, F., 28:237 Ravi, V., 23:277; 30:355 Reddy, A.S.N., 10:107 Redgwell, R.J., 20:121 Regnard, J.L., 32:1 Reid, M., 12:xiii; 17:123 Reuveni, M., 16:33 Richards, D., 5:127 Rieger, M., 11:45 Roper, T.R., 21:215 Rosa, E.A.S., 19:99 Roth-Bejerano, N., 16:71 Roubelakis-Angelakis, K.A., 14:407 Rouse, J.L., 12:1 Royse, D.J., 19:59

CUMULATIVE CONTRIBUTOR INDEX Rudnicki, R.M., 10:35 Ryder, E.J., 2:164; 3:vii Sachs, R., 12:xiii Sakai, A., 6:357 Salisbury, F.B., 4:66; 15:233 Salova, T. H., 29:305 Saltveit, M.E., 23:x; 23:185 San Antonio, J.P., 6:85 Sankhla, N., 10:63; 24:55 Saure, M.C., 7:239 Schaffer, B., 13:257 Schenk, M.K., 22:185 Schneider, G.W., 3:315 Schneider, K.R., 30:185 Schuster, M.L., 3:28 Scorza, R., 4:106 Scott, J.W., 6:25 Sedgley, M., 12:223; 22:1; 25:235 Seeley, S.S., 15:97 Serrano Marquez, C., 15:183 Sharp, W.R., 2:268; 3:214 Sharpe, R.H., 23:233 Shattuck, V.I., 14:199 Shear, C.B., 2:142 Sheehan, T.J., 5:279 Shipp, J.L., 21:1 Shirra, M., 20:267 Shorey, H.H., 12:409 Silber, A., 32:167 Simon, J.E., 19:319 Singh, Z. 27:189; 31:113 Sklensky, D.E., 15:335 Smith, A.H., Jr., 28:351 Smith, G.S., 12:307 Smith, M.A.L., 28:125 Smock, R.M., 1:301 Sommer, N.F., 3:412 Sondahl, M.R., 2:268 Sopp, P.I., 13:1 Soule, J., 4:247 Sozzi, G. O., 27:125 Sparks, D., 8:217 Splittstoesser, W.E., 6:25; 13:105 Spooner, D.M., 28:1 Srinivasan, C., 7:157 Stang, E.J., 16:255 Steffens, G.L., 10:63 Stern, R.A., 28:393 Stevens, M.A., 4:vii Stroshine, R.L., 20:1 Struik, P.C., 14:89

477 Studman, C.J., 19:217 Stutte, G.W., 13:339 Styer, D.J., 5:221 Sunderland, K.D., 13:1 Sung, Y., 24:229 Surányi, D., 19:263; 22:225; 23:179 Swanson, B., 12:xiii Swietlik, D., 6:287; 23:109 Syvertsen, J.P., 7:301, 30:37 Talcott, S.T., 30:185 Tattini, M., 21:177 Tétényi, P., 19:373 Theron, K.I., 25:1 Tibbitts, T.W., 4:49 Timon, B., 17:331 Tindall, H.D., 16:143 Tisserat, B., 1:1 Titus, J.S., 4:204 Trigiano, R.N., 14:265 Tunya, G.O., 13:105 Turekhanova, P.M., 29:305 Upchurch, B.L., 20:1 Valenzuela, H.R., 24:139 van den Berg, W.L.A., 28:1 van Doorn, W.G., 17:173; 18:1 Van Iepersen. W., 30: 163 van Kooten, O., 23:69 van Nocker, S. 27:1 Veilleux, R.E., 14:239 Vorsa, N., 21:215 Vizzotto, G., 28: 351 Wallace, A., 15:413 Wallace, D.H., 17:73 Wallace, G.A., 15:413 Wang, C.Y., 15:63 Wang, L., 30:115 Wang, S.Y., 14:333 Wann, S.R., 10:153 Watkins, C.B., 11:289 Watson, G.W., 15:1 Webster, B.D., 1:172; 13:xi Weichmann, J., 8:101 Wetzstein, H.Y., 8:217 Whiley, A.W., 17:299 Whitaker, T.W., 2:164 White, J.W., 1:141 Williams, E.G., 12:1 Williams, M.W., 1:270

478 Wismer, W.V., 17:203 Wittwer, S.H., 6:xi Woodson, W.R., 11:15 Wright, R.D., 9:75 W_nsche, J.N., 31:233 Wutscher, H.K., 1:237 Xu, C., 30:83. Yada, R.Y., 17:203; 30:317 Yadava, U.L., 2:1

CUMULATIVE CONTRIBUTOR INDEX Yahia, E.M., 16:197; 22:123 Yan, W., 17:73 Yarborough, D.E., 16:255 Yelenosky, G., 7:201 Zanini, E., 16:71 Zhang, B., 30:83 Zieslin, N., 9:53 Zimmerman, R.H., 5:vii; 9:273 Ziv, M., 24:1 Zucconi, F., 11:1

1a

2a

3a

1b

2b

3b

4

5

6

Plate 4.1 1. ‘Safari Sunset’ (Leucodendron salignum × L. laureolum): (a) flower head; (b) typical commercial branches (Photograph courtesy of S. Kadosh). 2. ‘Yaeli’ (selection of L. salignum): (a) flower head; (b) typical commercial branches (Photograph courtesy of S. Kadosh). 3. ‘Jester’, a variegated mutant of ‘Safari Sunset’: (a) flower head; (b) typical commercial branches (Photograph courtesy of S. Kadosh). 4. Spray branches of L. ‘Gold Strike’ (L. salignum × L. laureolum) (Photograph courtesy of S. Kadosh). 5. Spray branches of L. procerum (Photograph courtesy of S. Kadosh). 6. Spray branches of ‘Inca Gold’ (L. salignum × L. laureolum) (Photograph courtesy of S. Kadosh).

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Plate 4.2 1. ‘Safari Sunset’ field before harvest (Photograph courtesy of Y. Shtaynmetz). 2. Pot plant of L. album (Photograph courtesy of J. Ben-Jaacov). 3. Male flower head of L. discolor ‘Red Discolor’. 4. Foliage of L. discolor ‘Green Discolor’.