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THE FAMILIES AND GENERA OF VASCULAR PLANTS

Edited by K. Kubitzki

Volumes published in this series Volume I

Pteridophytes and Gymnosperms Edited by K.U. Kramer and P.S. Green (1990) Date of publication: 28.9.1990

Volume II

Flowering Plants. Dicotyledons. Magnoliid, Hamamelid and Caryophyllid Families Edited by K. Kubitzki, J.G. Rohwer, and V. Bittrich (1993) Date of publication: 28.7.1993

Volume III

Flowering Plants. Monocotyledons: Lilianae (except Orchidaceae) Edited by K. Kubitzki (1998) Date of publication: 27.8.1998

Volume IV

Flowering Plants. Monocotyledons: Alismatanae and Commelinanae (except Gramineae) Edited by K. Kubitzki (1998) Date of publication: 27.8.1998

Volume V

Flowering Plants. Dicotyledons: Malvales, Capparales and Non-betalain Caryophyllales Edited by K. Kubitzki and C. Bayer (2003) Date of publication: 12.9.2002

Volume VI

Flowering Plants. Dicotyledons: Celastrales, Oxalidales, Rosales, Cornales, Ericales Edited by K. Kubitzki (2004) Date of publication: 21.1.2004

Volume VII

Flowering Plants. Dicotyledons: Lamiales (except Acanthaceae including Avicenniaceae) Edited by J.W. Kadereit (2004) Date of publication: 13.4.2004

Volume VIII Flowering Plants. Eudicots: Asterales Edited by J.W. Kadereit and C. Jeffrey (2007) Volume IX

Flowering Plants. Eudicots: Berberidopsidales, Buxales, Crossosomatales, Fabales p.p., Geraniales, Gunnerales, Myrtales p.p., Proteales, Saxifragales, Vitales, Zygophyllales, Clusiaceae Alliance, Passiﬂoraceae Alliance, Dilleniaceae, Huaceae, Picramniaceae, Sabiaceae Edited by K. Kubitzki (2007)

The Families and Genera of Vascular Plants Edited by K. Kubitzki

IX

Flowering Plants · Eudicots Berberidopsidales, Buxales, Crossosomatales, Fabales p.p., Geraniales, Gunnerales, Myrtales p.p., Proteales, Saxifragales, Vitales, Zygophyllales, Clusiaceae Alliance, Passiﬂoraceae Alliance, Dilleniaceae, Huaceae, Picramniaceae, Sabiaceae

Volume Editor: K. Kubitzki in Collaboration with C. Bayer and P. F. Stevens

With 174 Figures

123

Professor Dr. Klaus Kubitzki Universität Hamburg Biozentrum Klein-Flottbek und Botanischer Garten Ohnhorststraße 18 22609 Hamburg Germany

Library of Congress Control Number: 2006928744

ISBN-10 3-540-32214-0 Springer Berlin Heidelberg New York ISBN-13 978-3-540-32214-6 Springer Berlin Heidelberg New York This work is subject to copyright. All rights are reserved, whether the whole or part of the material is concerned, speciﬁcally the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microﬁlm or in any other way, and storage in data banks. Duplication of this publication or parts thereof is permitted only under the provisions of the German Copyright Law of September 9, 1965, in its current version, and permissions for use must always be obtained from Springer-Verlag. Violations are liable for prosecution under the German Copyright Law. Springer is a part of Springer Science+Business Media springer.com © Springer-Verlag Berlin Heidelberg 2007 The use of general descriptive names, registered names, trademarks, etc. in this publication does not imply, even in the absence of a speciﬁc statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. Cover design: WMXDesign, Heidelberg, Germany Typesetting and production: LE-TEX Jelonek, Schmidt & Vöckler GbR, Leipzig, Germany Printed on acid-free paper

31/3150/YL – 5 4 3 2 1 0

Preface

The present volume contains treatments of various eudicot orders which all are strongly supported in molecular analyses. A ﬁrst group comprises Proteales, Buxales and the enigmatic Sabiaceae which, together with Ranunculales and Trochodendrales, treated earlier in Vol. II of this series, represent the basal grade of early-diverging eudicots. Although all of them have clearly tri-orate pollen, making them eudicots, they otherwise lack the strict eudicot ﬂoral organisation, particularly with regard to ﬂower merosity, phyllotaxis and perianth structure. The same is true for the order Gunnerales which, however, according to ﬁndings of molecular systematics, forms part of the strongly supported core eudicots. All these orders to some extent bridge the morphological gap between basal angiosperms and typical core eudicots. Plesiomorphic ﬂoral traits, although less pronounced, are also found among the isolated but clearly core eudicotyledonous Saxifragales, treated in this volume, and particularly in the early-diverging woody families of this order. Some of these latter families were included in Vol. II, which followed a classiﬁcation used prior to the discovery of the modern concept of Saxifragales. The exact interrelationships among the early-diverging eudicot orders still remain largely unresolved. This is even more true for many of the core eudicot orders included in the present volume, i.e. Vitales, Crossosomatales, Geraniales, Zygophyllales and Myrtales, and also for two of the families not assigned to order, i.e. Huaceae and Picramniaceae. A possible relationship between Dilleniaceae and woody Caryophyllales, as suggested by recent studies, opens an interesting new perspective on the evolution of this family. Included in this volume are two subclades of the vast Malpighiales. These are Passiﬂoraceae with two satellite families, and Clusiaceae/Hypericaceae with Podostemaceae, which recently have been identiﬁed as very close relatives. My deep thanks go to all authors of this volume, who have provided such highly interesting and scholarly contributions, and to all those who have freely shared additional information and/or have commented on earlier drafts of the contributions. These include B.G. Briggs, T. Clifford, G. Jordan, B. Makinson, P. Olde, R. Barker, J.A. Doyle, P.J. Rudall and C.A. Furness (Proteaceae); H. Manitz (Aphanopetalaceae); A.E. Orchard (Haloragaceae); P.H. Linder and M. Weigend (Geraniales); A. Bernhard and W.J.J.O. de Wilde (Passiﬂoraceae); the late M. Ricardi S. (Malesherbiaceae); I. Jäger-Zürn and T. Philbrick (Podostemaceae); and S. Renner, P.G. Wilson and J. Schönenberger (Myrtales). I am also grateful to M.L. Matthews and P.K. Endress for showing me their papers prior to publication elsewhere. Mark C. Chase is thanked for always making available the newest results of his pathbreaking studies. The copyright holders of the illustrations included in this volume are thanked for their generous permission to use their valuable material. As always, it is a pleasure to acknowledge the agreeable collaboration with the staff of Springer-Verlag, who kindly responded to all requests I had in connection with the production of this volume, and to thank Monique T. Delafontaine for her meticulous copy editing of the manuscript. Hamburg, September 2006

K. Kubitzki

Contents

Introduction to the Groups Treated in this Volume K. Kubitzki . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Introduction to Berberidopsidales . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Introduction to Buxales . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Introduction to the Clusiaceae Alliance (Malpighiales) . . . . . . . . . . . . . . . . . Introduction to Crossosomatales . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Introduction to Fabales . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Introduction to Geraniales . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Introduction to Gunnerales . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Introduction to Myrtales . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Introduction to the Passiﬂoraceae Alliance (“Passiﬂorales” = Malpighiales) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Introduction to Proteales . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Introduction to Saxifragales . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Introduction to Vitales . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Introduction to Zygophyllales . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Families Unassigned to Order . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . General References

1 1 2 3 3 5 5 7 7 12 12 15 18 19 20

............................................

21

Aextoxicaceae

K. Kubitzki . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

23

Alzateaceae

S.A. Graham . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

26

Aphanopetalaceae

K. Kubitzki . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

29

Aphloiaceae

K. Kubitzki . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

31

Berberidopsidaceae

K. Kubitzki . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

33

Bonnetiaceae

A.L. Weitzman, K. Kubitzki and P.F.Stevens . . . . .

36

Buxaceae

E. Köhler . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

40

Clusiaceae-Guttiferae

P.F. Stevens . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

48

Combretaceae

C.A. Stace . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

67

Crassulaceae

J. Thiede and U. Eggli . . . . . . . . . . . . . . . . . . . . . . . .

83

Crossosomataceae

V. Sosa . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 119

Crypteroniaceae

S.S. Renner . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 123

Daphniphyllaceae

K. Kubitzki . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 127

VIII

Contents

Didymelaceae

E. Köhler . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 129

Dilleniaceae

J.W. Horn . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 132

Geissolomataceae

F. Forest . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 155

Geraniaceae

F. Albers and J.J.A. Van der Walt . . . . . . . . . . . . . . 157

Grossulariaceae

M. Weigend . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 168

Gunneraceae

H.P. Wilkinson and L. Wanntorp . . . . . . . . . . . . . . 177

Haloragaceae

K. Kubitzki . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 184

Huaceae

C. Bayer . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 191

Hypericaceae

P.F. Stevens . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 194

Iteaceae

K. Kubitzki . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 202

Ixerbaceae

J.V. Schneider . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 205

Krameriaceae

B.B. Simpson . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 208

Ledocarpaceae

M. Weigend . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 213

Leeaceae

J. Wen . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 221

Lythraceae

S.A. Graham . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 226

Malesherbiaceae

K. Kubitzki . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 247

Melianthaceae

H.P. Linder . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 250

Oliniaceae

M. von Balthazar and J. Schönenberger . . . . . . 260

Paeoniaceae

M. Tamura . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 265

Passiﬂoraceae

C. Feuillet and J.M. MacDougal . . . . . . . . . . . . . . 270

Penaeaceae

J. Schönenberger, E. Conti and F. Rutschmann . 282

Penthoraceae

J. Thiede . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 292

Peridiscaceae

C. Bayer . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 297

Picramniaceae

K. Kubitzki . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 301

Podostemaceae

C.D.K. Cook and R. Rutishauser . . . . . . . . . . . . . . . 304

Polygalaceae

B. Eriksen and C. Persson . . . . . . . . . . . . . . . . . . . . 345

Proteaceae

P.H. Weston . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 364

Pterostemonaceae

K. Kubitzki . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 405

Quillajaceae

K. Kubitzki . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 407

Rhynchocalycaceae

J. Schönenberger . . . . . . . . . . . . . . . . . . . . . . . . . . . 409

Sabiaceae

K. Kubitzki . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 413

Saxifragaceae

D.E. Soltis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 418

Stachyuraceae

J.V. Schneider . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 436

Staphyleaceae

S.L. Simmons . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 440

Strasburgeriaceae

W.C. Dickison . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 446

Contents

IX

Surianaceae

J.V. Schneider . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 449

Tetracarpaeaceae

K. Kubitzki . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 456

Turneraceae

M.M. Arbo . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 458

Vitaceae

J. Wen . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 467

Vochysiaceae

M.L. Kawasaki . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 480

Zygophyllaceae

M.C. Sheahan . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 488

Additions and Corrections to Volumes II–VI . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 501 Index to Scientiﬁc Names . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 503

List of Contributors

Albers, Focke

Botanischer Garten, Universität Münster, Schlossgarten 3, 48149 Münster, Germany

Arbo, María M.

Instituto de Botánica del Nordeste, Casilla de Correo 209, 3400 Corrientes, Rep. Argentina

Balthazar, Maria von

Swedish Museum of Natural History, Division of Palaeobotany, P.O. Box 50007, 10405 Stockholm, Sweden

Bayer, Clemens

Palmengarten der Stadt Frankfurt, Siesmayerstr. 61, 60323 Frankfurt/Main, Germany

Conti, Elena

Institut für Systematische Botanik und Botanischer Garten, Universität Zürich, Zollikerstr. 107, 8008 Zürich, Switzerland Institut für Systematische Botanik und Botanischer Garten, Universität Zürich, Zollikerstr. 107, 8008 Zürich, Switzerland (deceased)

Cook, Christopher D.K. Dickison, W.C. Eggli, Urs Eriksen, Bente

Sukkulenten-Sammlung, Mythenquai 88, 8002 Zürich, Switzerland Department of Botany, University of Göteborg, P.O. Box 461, 40530 Göteborg, Sweden

Feuillet, Christian

Department of Botany, Smithsonian Institution, P.O. Box 37012, Washington, DC 20013-7012, USA

Forest, Felix L.

School of Biological Sciences, Plant Sciences Laboratories, The University of Reading, Reading RG6 6AS, UK

Graham, Shirley A.

Missouri Botanical Garden, P.O. Box 299, St. Louis, MO 63166-0299, USA

Horn, James W.

Department of Biology, Duke University, P.O. Box 90338, Durham, NC 27708-0338, USA. Present address: Fairchild Tropical Botanic Garden, 11935 Old Cutler Road, Miami, FL 33156-4242, USA

Kawasaki, M. Lúcia

Department of Botany, Field Museum, 1400 S. Lake Shore Drive, Chicago, IL 60605-2496, USA

Köhler, Egon

Spezielle Botanik und Arboretum, Humboldt-Universität, Späthstr. 80/81, 12437 Berlin, Germany

Kubitzki, Klaus

Biozentrum Klein-Flottbek und Botanischer Garten, Universität Hamburg, 22609 Hamburg, Germany

XII

Linder, H. Peter

MacDougal, John M.

List of Contributors

Institut für Systematische Botanik und Botanischer Garten, Universität Zürich, Zollikerstr. 107, 8008 Zürich, Switzerland Missouri Botanical Garden, P.O. Box 299, St. Louis, MO 63166-0299, USA

Persson, Claes

Department of Botany, University of Göteborg, P.O. Box 461, 40530 Göteborg, Sweden

Renner, Susanne S.

Botanische Staatssammlung, Menzinger Str. 67, 80638 München, Germany

Rutishauser, Rolf

Institut für Systematische Botanik und Botanischer Garten, Universität Zürich, Zollikerstr. 107, 8008 Zürich, Switzerland Institut für Systematische Botanik und Botanischer Garten, Universität Zürich, Zollikerstr. 107, 8008 Zürich, Switzerland Spezielle Botanik, Universität Leipzig, Johannisallee 21–23, 04103 Leipzig, Germany

Rutschmann, Frank

Schneider, Julio V. Schönenberger, Jürg

Department of Botany, University of Stockholm, Lilla Frescativägen 5, 10691 Stockholm, Sweden

Sheahan, Mary C.

Jodrell Laboratory, Royal Botanic Gardens Kew, Richmond SRY TW9 3DS, UK

Simmons, Sara L.

Department of Integrative Biology, University of Texas, Austin, TX 78712, USA

Simpson, Beryl B.

University of Texas, Section of Integrative Biology, 1 University Station A 6700, Austin, TX 78712, USA

Soltis, Douglas E.

Department of Botany, University of Florida, Gainesville, FL 32611-7800, USA

Sosa, Victoria

Instituto de Ecología, A.C., Apartado Postal 63, 91000 Xalapa, Veracruz, México

Stace, Clive A.

Department of Botany, University of Leicester, University Road, Leicester LE1 7RH, UK

Stevens, Peter F.

Missouri Botanical Garden, P.O. Box 299, St. Louis, MO 63166-0299, USA

Tamura, Michio

4-25-7 Ao-gein, Mino, Osaka 562-0025, Japan

Thiede, Joachim

Schenefelder Holt 3, 22589 Hamburg, Germany

Van der Walt, J.J.A.

(deceased)

Wanntorp, Livia

Department of Botany, University of Stockholm, Lilla Frescativägen 5, 10691 Stockholm, Sweden

Weigend, Maximilian

Institut für Biologie/Systematische Botanik, Freie Universität Berlin, Altensteinstr. 6, 14195 Berlin, Germany

Weitzman, Anna L.

Department of Botany, Smithsonian Institution, P.O. Box 37012, Washington, DC 20013-7012, USA

List of Contributors

Wen, Jun

Department of Botany, Smithsonian Institution, P.O. Box 37012, Washington, DC 20013-7012, USA

Weston, Peter

Royal Botanic Gardens, Mrs Macquaries Road, Sydney, NSW 2000, Australia

Wilkinson, Hazel P.

Jodrell Laboratory, Royal Botanic Gardens Kew, Richmond SRY TW9 3DS, UK

XIII

Introduction to the Groups Treated in this Volume K. Kubitzki

Introduction to Berberidopsidales 1. Dioecious tree, young parts covered with ferrugineous scales; leaves conduplicate, entire; ﬂowers 5(6)merous, enveloped in bud by ﬁrm calyptrate bract; stamens 5, alternating with nectary glands; gynoecium 1-carpellate; ovules 2, pendulous from apex of locule; style apically biﬁd; fruit dry, indehiscent; seed with ruminate endosperm and embryo of about half the length of seed. 1/1, S Chile and adjacent Argentina Aextoxicaceae – Scandent shrubs, largely glabrous; leaves involute (Berberidopsis), spiny-toothed or entire; ﬂowers hermaphrodite, acyclic and with disk, or cyclic, pentamerous and without disk; gynoecium 3–5-carpellate; ovules several to many, each on 3–5 placentas; style not biﬁd; fruit berry-like; embryo small. 2/3, S Chile and SE Australia Berberidopsidaceae

A close relationship between Berberidopsidaceae and Aextoxicaceae has never been considered until gene sequence studies provided strong support for a relationship between them (see family treatments). In the four-gene analysis of eudicots (Soltis et al. 2003), Gunnerales and subsequently Berberidopsidales are sister to all other core eudicots, the latter being strongly supported by molecular data and isolated from all other clades (Fig. 1). Aextoxicum has long been known for its peculiar wood anatomy, particularly the high number of bars of the vessel element perforations. A recent study by Carlquist (2003) has revealed many important similarities in the wood anatomy of the two families, although these are plesiomorphic. Pollen grains are relatively small and tricolpate to indistinctly colporate. The two families share encyclocytic stomata (Soltis et al. 2005), a rare character in angiosperms, stout ﬁlaments, and a ring of vascular bundles in the petiole (Judd and Olmstead 2004). Unfortunately, many important characters are not known for both taxa but available information shows that Berberidopsidales are very plastic in their ﬂoral structure, combining (even within the same family, Berberidospidaceae) both spiral and whorled patterns, and 1-, 3- and 5-merous

gynoecia. The spiral sequence of initiation of ﬂoral organs in Berberidopsis, with a tendency of arrangement in alternating groups of ﬁve, may represent an incipient case of pentamery (Ronse DeCraene 2004) but this is problematic, in view of the ﬁrmly established pentamerous ﬂoral structure characteristic for core eudicots which exists in parts of Berberidopsidaceae and in the closely related Aextoxicum (see Berberidopsidaceae and Aextoxicaceae, this volume).

Fig. 1. A phylogenetic hypothesis of eudicot relationships, based on a four-gene dataset (Soltis et al. 2003)

2

K. Kubitzki

Morphologically, basal eudicots exhibit considerable structural disjunctions, which underlines their relict nature. This is also corroborated by the remarkable angiospermous fossil from the Early Cretaceous, Teixeira lusitanica, which shows afﬁnities to members of Ranunculales, and to Berberidopsidaceae, Hamamelidaceae and Daphniphyllaceae (von Balthazar et al. 2005). Characters such as the dimerous ﬂoral structure, known from Gunnera, and presumably plesiomorphic traits (decurrent stigmas, antepetalous stamens, etc.), known from other basal eudicot families such as Proteaceae and Sabiaceae, are not found in Berberidopsidales.

References Balthazar, M. von, Pedersen, K.R., Friis, M.E. 2005. Teixeira lusitanica, a new fossil ﬂower from the Early Cretaceous of Portugal with afﬁnities to Ranunculales. Pl. Syst. Evol. 255:55–75. Carlquist, S. 2003. Wood anatomy of Aextoxicaceae and Berberidopsidaceae is compatible with their inclusion in Berberidopsidales. Syst. Bot. 28:317–325. Judd, W.S., Olmstead, R.G. 2004. A survey of tricolpate (eudicot) phylogenetic relationships. Amer. J. Bot. 91:1627–1644. Ronse DeCraene, L.P. 2004. Floral development of Berberidopsis corallina: a crucial link in the evolution of ﬂowers in the core eudicots. Ann. Bot. 94:741–751. Soltis, D.E. et al. 2003. See general references. Soltis, D.E. et al. 2005. See general references.

Introduction to Buxales 1. Dioecious trees; ﬂowers apetalous, male with one stamen pair, female often paired, a single carpel; pollen grains tricolpo-di-orate; seeds exalbuminous. 1/2, Madagascar Didymelaceae – Monoecious, rarely dioecious shrubs or herbs; ﬂowers with weakly differentiated perianth, male with decussate tepals and 4, 6 or more stamens, female with spiral tepals and a 2–4-carpellate, syncarpous gynoecium; pollen grains 3–7-colporate with 3–6 pores per colpus, or pantoporate; seeds albuminous. 5/c. 100, all continents, except Australia Buxaceae

Buxales comprise Buxaceae and Didymelaceae, grouped together by traits such as cyclocytic stomata, leaf venation pattern, wood anatomical peculiarities including many sclereids, racemose inﬂorescences, small, imperfect, often dimerous ﬂowers with decurrent stigmas extending the entire length of the stylodia, stamens with more or less basiﬁxed anthers and conspicuous connective anther protrusions, and the occurrence of very

peculiar steroidal pregnan alkaloids. The most obvious trait of Buxales is the plasticity and simplicity of perianth organisation. In some of their members (Didymeles, male Styloceras), a perianth is completely lacking and, in Buxaceae, the tepals hardly differ from vegetative bracts below the ﬂower (von Balthazar and Endress 2002a) and in female ﬂowers they are spirally arranged, making the delimitation of ﬂowers difﬁcult. The stamens are always antesepalous and the stamen-sepalum complex of Buxaceae is similar to that of Proteaceae, also in the supply of the sepals by a single trace. Stamens, when occurring in low number, are arranged in dimerous whorls but, for higher numbers (in Notobuxus 6, 8, and up to more than 40), less regular arrangements prevail. Palynologically, Buxales are highly diverse (Bessedik 1983; Doyle 1999). An early fossil attributable to Buxales (Doyle 1999) is a pollen from the Aptian/Albian of northern Gondwana, which has simple colpate apertures and a striate(-reticulate) sculpture and has been related to the buxaceous megafossil Spanomera (Drinnan et al. 1991). In the late Albian of Gabon and Brazil, the tricolpodiorate pollen Hexaporotricolpites (Boltenhagen 1967) appears. This pollen type may be related to extant Didymeles from Madagascar (cf. Fig. 36), which has left a fossil record in the southern Indian Ocean, Australia, New Zealand and New Caledonia. Similar pollen grains with an increasing number of pores and meridional colpi, later in pantocolporate and eventually pantoporate conﬁguration, the latter combined with a crotonoid exine pattern (cf. Fig. 11D), appear both in the fossil record and in extant Buxus (Köhler 1981; Köhler and Brückner 1982; Bessedik 1983). Buxales form part of the grade of earlydiverging tricolpate(-derived) dicots or eudicots, which also comprises Ranunculales, Sabiaceae, Proteales and Trochodendraceae (cf. Fig. 1). With several early-diverging eudicots, and partly also with some basal core eudicots (Gunneraceae, Myrothamnaceae and some basal families of Saxifragales), Buxales share characters which are known also from the eumagnoliids. Particularly remarkable are the dimerous ﬂowers, the supply of the sepals by a single trace, and the stamensepalum complex, in which Buxaceae agree with Proteaceae. Conspicuous connective protrusions are known from other early-diverging eudicots and some basal core eudicots, including Proteaceae, Platanaceae, Trochodendraceae, Myrothamnaceae; basiﬁxed anthers are widespread in early-diverging

Introduction to the Groups Treated in this Volume

eudicots. Elongate stigmas decurrent in two crests are shared with Platanaceae, Myrothamnaceae and Trochodendraceae but are also found in some Saxifragales. Nectary disks are rare in early-diverging eudicots and, apart from the intrastylodial nectariferous structures in Buxaceae, are known only from Proteaceae and Sabiaceae.

References Doyle, J.A. 1999. The rise of angiosperms as seen in the African Cretaceous pollen record. In: Heine, K. (ed.) Palaeoecology of Africa and the surrounding islands. Rotterdam: Balkema, pp. 3–29. For other references, see the selected bibliographies of Buxaceae and Didymelaceae, and the General References (this volume).

3

now well established (Soltis et al. 2000; Savolainen, Fay et al. 2000), and Podostemaceae appear sister to Hypericaceae or perhaps nested inside this family (Gustafsson et al. 2002). As the sinking of Podostemaceae in the broadly delimited Clusiaceae would lead to a highly heterogeneous unit, it appears preferable to “save” an independent family Podostemaceae by segregating Hypericaceae from Clusiaceae s.l., following the approach of many earlier authors such as Takhtajan (1997), although the separation in terms of contrasting characters between the latter two is not very strong. Characters common to the three families include resin cells and secretory ducts, containing xanthones, and bitegmic and tenuinucellate ovules.

References Introduction to the Clusiaceae Alliance (Malpighiales) 1. Annual cataract-dwellers with unclear differentiation of stems, roots and leaves (roots often crustaceous, ribbon-like; leaves sometimes terminal and doublesheathed); fertile pollen and fertilisable embryo sacs developed underwater; [pollination autogamous or cleistogamous, rarely allogamous; female gametophyte reduced Allium type; no double fertilisation and no endosperm; seed set high]. 49/c. 280, worldwide, tropical and warm-temperate regions Podostemaceae – Woody or herbaceous land plants 2 2. Leaves alternate, serrulate, initially setulose, convolute; latex 0; stamen connective glands 0; capsule with persistent column. 3/40, northern South America, West Indies, and SE Asia to New Guinea Bonnetiaceae – Leaves opposite or alternate, entire, not setulose, not convolute; latex often present in glands or secretory canals; stamen connectives often with glands producing oil or resin; fruit, if capsular, then rarely with persistent column 3 3. Stylodia free, at least distally; ﬂowers perfect; sepals and petals 3–5; aril 0; trichomes, if multicellular, then stellate; woody or herbaceous. 9/540, worldwide Hypericaceae – Stylodia free or fused to form a simple style; ﬂowers perfect or unisexual; sepals 2–20, petals 0–8; aril sometimes present; stellate hairs very rare (Caraipa, Marila); woody. 27/1090, pantropical Clusiaceae

Although these families have been intensely studied by generations of botanists, recent work has considerably modiﬁed our understanding of their phylogenetic relationships and details of their family and tribal delimitation. Molecular studies have revealed one enigma of long standing – the systematic position of Podostemaceae. Their close relationship with Clusiaceae s.l. (i.e. including Hypericaceae) is

For references, see the Selected Bibliography of ClusiaceaeGuttiferae and the General References (this volume).

Introduction to Crossosomatales 1. Perianth biseriate 2 – Perianth uniseriate; [ﬂowers solitary] 6 2. Leaves opposite, pinnately compound, rarely unifoliolate; embryo green; [ovary syncarpous or apocarpous; ovules anatropous]. 2/40–50, temperate to tropical regions, mainly of the northern hemisphere Staphyleaceae – Leaves alternate, simple (if opposite and simple to slightly trilobate and gynoecium apocarpous, see Apacheria in Crossosomataceae); embryo achlorophyllous 3 3. Flowers solitary 4 – Flowers in panicles, racemes or spikes 5 4. Sepals 4–10; stamens 5 + 5; anthers dorsiﬁxed; pistil 4–7-carpellate; style simple; ovules 1 per locule, anatropous; fruit indehiscent, ﬁbrous; seed with rudimentary aril; embryo straight; vessel element perforation scalariform; T-shaped unicellular trichomes present. 1/1, New Caledonia Strasburgeriaceae – Sepals (3)4–5(6); stamens 4–50 (ﬂower haplostemonous, diplostemonous or polystemonous); anthers basiﬁxed; gynoecium apocarpous, 1–5(–9)-carpellate; ovules 1–many per carpel, campylotropous; fruit follicular; seed arillate; embryo curved; vessel element perforation mostly simple; T-shaped trichomes 0. 4/10, North America, with Mexico Crossosomataceae 5. Flowers strictly 5-merous; ovules 2 per locule; pollen 4(5)-colporate; fruit capsular; aril rudimentary; vessel element perforation scalariform; T-shaped unicellular trichomes present. 1/1, New Zealand Ixerbaceae – Flowers strictly 4-merous; ovules many per locule; pollen 3-colporate; fruit berry-like; seed with soft

4

K. Kubitzki funicular aril; vessel element perforation simple; T-shaped trichomes 0. 1/c. 16, E Asia Stachyuraceae 6. Leaves decussate, entire; tepals 4; stamens 4 + 4; anthers dorsiﬁxed; ovary 4-locular, with 4 twisted stylodia; ovules anatropous; fruit capsular; seeds with swollen funicle; embryo straight; T-shaped unicellular trichomes present. 1/1, South Africa Geissolomataceae – Leaves alternate, serrate; tepals 4–5(6); stamens many; anthers basiﬁxed; ovary unilocular; style simple; ovules campylotropous; fruit a berry; seeds arillate, incurved with hippocrepiform embryo. 1/1, E and southern Africa, islands of Indian Ocean Aphloiaceae

Until very recently, these apparently disparate families had been placed in different rosid orders and some had been “dumped” in larger families such as the broadly construed Saxifragaceae (Ixerba) or Flacourtiaceae (Aphloia). The taxonomic history of the individual families is brieﬂy described in the family treatments, and has been treated in more depth by Matthews and Endress (2005). Although Takhtajan (1987) for the ﬁrst time used the name of the order Crossosomatales which, in his approach, comprised only the name-giving family, a broader concept of the order was not achievable in the pre-molecular era largely because the characters traditionally used in higher-level classiﬁcation are very variable in these seven families (see Conspectus). During recent years, several molecular studies have contributed to the recognition of the relationships in the entourage of Crossosomataceae. In their rbcL and combined morphological and rbcL studies, Nandi et al. (1998) found a clade of {[(Crossosoma + Stachyurus) Staphylea] Geissoloma}, albeit without signiﬁcant support. Strong support for [(Crossosoma + Stachyurus) Staphylea] was adduced by further rbcL studies (Savolainen, Fay et al. 2000; Sosa and Chase 2003) and multigene analyses (Soltis et al. 2000; Cameron 2003), and for Ixerba + Strasburgeria by rbcL (Savolainen, Fay et al. 2000; Sosa and Chase 2003) and multigene studies (Cameron 2003). When included in the analysis, Ixerba + Strasburgeria, Aphloia and Geissoloma usually appeared in the same clade as Crossosoma, Stachyurus and Staphylea, although statistical support for this was low. The concept of Crossosomatales proposed by Savolainen, Fay et al. (2000) and Soltis et al. (2000), comprising Crossosomataceae, Stachyuraceae and Staphyleaceae, has later been extended to include all seven aforementioned families (see also Stevens 2005). This concept is now conﬁrmed by the broad-based comparative study of Matthews and Endress (2005), which has revealed structural traits, particularly previ-

ously neglected ﬂoral characters, which are shared in different constellations by groups of two, three or more families of the whole alliance. The group as a whole is only weakly characterised. Stomata are usually anomocytic. Leaf margins are usually toothed. Stipules are lacking only in Ixerbaxceae and some Crossosomataceae. Vessel elements have scalariform perforation, Crossosomataceae and Stachyuraceae excepted. Sepal and petal aestivation is imbricate throughout, and stamens are always incurved in bud; anthers are tetrasporangiate; nectary disks are present. Ovules are bitegmic and crassinucellar, mostly anatropous; Aphloiaceae and Crossosomataceae have campylotropous ovules. Pollen grains are colporate and usually have lalongate endoapertures; the gynoecium is often stalked; the carpel tips are often postgenitally united to form a compitum. The seed coat is testal. Sieve element plastids are S type throughout. Ellagitannins and gallotannins, but no proanthocyanidins, are known from Crossosomataceae. More restricted are the following traits. Ixerbaceae and Strasburgeriaceae have large ﬂowers with petals forming a tight, pointed cone in bud, stamens with sagittate anthers, and a rudimentary aril. These families share with Geissolomataceae T-shaped unicellular trichomes and a punctiform stigma on postgenitally united and twisted carpel tips, and only one or two ovules per carpel. Aphloiaceae, Geissolomataceae, Ixerbaceae and Strasburgeriaceae share pollen grains with pronounced protruding endoapertures (“pollen buds”). Crossosomataceae, Stachyuraceae and Staphyleaceae have polygamous or functionally unisexual ﬂowers, and Crossosomataceae and Aphloiaceae (although not resolved as sisters in molecular studies) share polyandrous ﬂowers, basiﬁxed anthers, a stigma with two or more decurrent crests, campylotropous ovules and reniform seeds (data from Matthews and Endress 2005). Crossosomatales are core eudicots but otherwise their relationships are still unclear: they appear at the base of eurosids II (Savolainen, Fay et al. 2000; Soltis et al. 2000) or eurosids I (Hilu et al. 2003), or in a polytomy with Geraniales, Myrtales, eurosids I and eurosids II (APG II 2003), but always with low statistical support.

References For references, see the General References (this volume).

Introduction to the Groups Treated in this Volume

Introduction to Fabales 1. Stylodia gynobasic; [woody; ﬂowers regular; gynoecium apocarpous, 1–5-carpellate; ovule unitegmic (only Suriana known); endosperm 0 or sparse; nectary only rarely present; vestured pits in Recchia]. 5/8, in warm-temperate and tropical regions, widely distributed Surianaceae – Style or stylodia not gynobasic 2 2. Gynoecium syncarpous, 2–8-carpellate (sometimes 1locular); pollen grains 7–28-colporate; seeds mainly endotestal; leaves estipulate; [woody or herbaceous; nodes unilacunar with a single trace; vessel element perforations usually simple; vestured pits sometimes present; ﬂowers actinomorphic to zygomorphic; nectary a disk, a gland, or 0; seeds often arillate]. n = 6–23. 21/800–1,000, widely distributed in tropical, subtropical and temperate regions Polygalaceae – Gynoecium (nearly) apocarpous; pollen grains mostly 3-aperturate; seeds exotestal; leaves stipulate; [nectariferous disk usually present] 3 3. Flowers strictly actinomorphic; carpels 5, only basally connate; pollen grains in monads; seeds exarillate; endosperm thin; cotyledons convolute; stipules small; nodes unilacunar; vessel elements with simple and scalariform perforation; vestured pits 0; [woody; bark strongly saponiferous]. n = 14. 1/2, warm-temperate southern South America Quillajaceae – Flowers actinomorphic to zygomorphic; carpel usually 1 or very rarely more (and then each carpel with a terminal stylodium); pollen grains in monads, tetrads or polyads; seeds arillate or not; endosperm usually 0, rarely sparse or even copious; stipules sometimes modiﬁed into prickles or spines; nodes tri-(penta-)lacunar; vessel elements with simple perforations, the lateral pits often vestured; [roots very often with N-ﬁxing root nodules]. 640/1800, widely distributed throughout the world Leguminosae–Fabaceae s.l. (not treated in this volume)

A clade comprising these four families was resolved as belonging to eurosids I by early molecular studies (Chase et al. 1993; Fernando et al. 1993; Morgan et al. 1994) and is strongly supported in several multigene analyses (e.g. Soltis et al. 1999, 2000). Morphologically, the four families have little in common, apart from the basically core eudicot ﬂoral organisation. Stevens (2005) notes green embryos and often ﬂuorescent wood, and absence of ellagitannins (which are, however, present in Leguminosae) as common traits.

References Chase, M.W. et al. 1993. See general references. Fernando, E.S. et al. 1993. See selected bibliography of Surianaceae. Morgan, D.R. et al. 1994. See selected bibliography of Quillajaceae.

5

Soltis, P.S., Soltis, D.E., Chase, M.W. 1999. Angiosperm phylogeny inferred from multiple genes as a tool for comparative biology. Nature 402:402–404. Soltis, D.E. et al. 2000. See general references. Stevens, P.F. 2005. See general references.

Introduction to Geraniales 1. Embryo small, straight, achlorophyllous; endosperm copious; secondary xylem always with rays; [either (sub)shrubs or small trees with mostly 5-merous ﬂowers and simple leaves and regular ﬂowers (Greyia), or with pinnate leaves and ± zygomorphic ﬂowers (Melianthus, Bersama), or herbs with mostly 4-merous ﬂowers and commissural stigmas (Francoa, Tetilla)]. 5/19, subsaharan Africa, southern South America Melianthaceae – Embryo large, circinate, twisted, or cochlear, rarely (Rhynchotheca) straight, chlorophyllous; endosperm usually scant; secondary xylem often rayless 2 2. Pollen grains tricolp(or)ate; style elongate, with 5 style branches or (Hypseocharis) unbranched with capitate stigma; fruits schizocarpic with 1-seeded awned mericarps or (Hypseocharis) loculicidal capsules; seed coat with crystalliferous endotesta and thickened but not ligniﬁed exotegmen. 5/c. 835, nearly worldwide Geraniaceae – Pollen grains pantoporate or inaperturate; style very short, with 5–3 elongate stigmatic branches; fruits septicidal or septifragous capsules with 1–many-seeded locules; seed coat usually lacking mechanical layers (Viviania, exotegmic); Balbisia with mucilaginous exotesta. 4/c. 18, South America, mostly Andean Ledocarpaceae

The former, broadly construed concept of the order Geraniales (e.g. Engler 1892) comprised 15–20 families including disparate groups such as Oxalidaceae, Tropaeolaceae, Zygophyllaceae, Rutaceae and Euphorbiaceae. Based on the work of many authors, notably Takhtajan (e.g. 1959, 1987) and Dahlgren (e.g. 1980), Geraniales were stepwise restricted by the exclusion of orders such as Rutales, Polygalales and Malpighiales. Yet, in a still more recent survey of dicotyledon families, Thorne (2001) merged Geraniales with Linales (= Malpighiales), mainly on account of these sharing a tendency for obdiplostemonous ﬂowers with 10–15 stamens and a 5-partite gynoecium. It is difﬁcult to understand why Oxalidaceae, for instance, were for so long considered to belong to Geraniales, although the former differ in possessing traits such as free stylodia, abundant endosperm, and capsular fruits (see treatment of Oxalidales in Vol. VI of this series). In the pioneering molecular studies of Price and Palmer (1993), Morgan and Soltis (1993) and

6

K. Kubitzki

Chase et al. (1993), the ﬁve genera of Geraniaceae s.str. grouped with Hypseocharis and, in some analyses, also with Viviania, Greyia and Francoa, and often also with Crossosoma, whereas other families of the erstwhile Geraniales were clearly excluded. More recent molecular work (Soltis et al. 2000; Savolainen, Fay et al. 2000; Sosa and Chase 2003) has resolved Geraniales and Crossosomatales (see treatment in this volume) as sister groups placed at the base of eurosid II orders, but the statistical support is tenuous and the Angiosperm Phylogeny Group (APG II 2003) lists both orders among the unresolved rosids. Evidence for a sister group relationship of Melianthaceae and Ledocarpaceae and, in turn, of both of these with Geraniaceae is provided by the rbcL analyses of Savolainen, Fay et al. (2000) and Sosa and Chase (2003). This is notable, as morphologically Ledocarpaceae and Geraniaceae seem to have more in common than any of them have with Melianthaceae (see below). Support is also strong for recognising Melanthiaceae and Geraniaceae in the circumscription adopted in this volume but it is less strong for the morphologically more diverse Ledocarpaceae. Biebersteinia, a Eurasian monotype which often had been related to Geraniaceae (e.g. Knuth 1931), agreeing with this family in some details of fruit and seed morphology (Boesewinkel 1988), in molecular studies is resolved as sapindalean (APG II 2003). A morphological characterisation of Geraniales is difﬁcult because the genera of Melianthaceae and, less so, of Ledocarpaceae are diverse. It is true that all Geraniales have anomocytic stomata, vessels with simple perforation, 5- or 4-merous hypogynous ﬂowers with a persistent calyx, and either haplostemonous or more often obdiplostemonous androecia with paired antepetalous stamens, 5(–3)-carpellate syncarpous gynoecia with simple styles (extremely short in Balbisia) terminating in 3–5 stigmatic lobes or branches, axile or rarely basal placentation, anatropous to campylotropous bitegmic and crassinucellar ovules and, where known, a Polygonum type embryo sac and Nuclear endosperm. All Melianthaceae have copious endosperm, and Melianthus, Bersama and Greyia share multilacunar nodes. Francoa and Tetilla, formerly included in Saxifragaceae, differ from this family in the commissural stigma, the 4-merous ﬂowers, Nuclear endosperm and the lack of myricetin. Otherwise, multilacunar nodes are not known in Geraniales, and the endosperm is absent or scanty in Geraniaceae. Ledocarpaceae and

Geraniaceae agree, however, in numerous traits, such as rayless wood, acuminate to awned sepals, broadened ﬁlaments and sometimes basal nectariferous appendages, tanniniferous seed coats, green embryos and (Rhynchotheca excepted) curved or cochlear embryos. Differences between the two families exist in growth habit, pollen morphology and seed coat anatomy (Boesewinkel 1997). Anthecologically, Geraniales families are diversiﬁed. Nectaries are present in all families, and Geraniaceae depend on a broad variety of insect groups as pollinators and only occasionally on bird, whereas Melianthaceae rely strongly on bird pollination. In Ledocarpaceae, Viviania produces copious nectar as reward for insect and other pollinators whereas the remaining genera, Balbisia and Rhynchotheca, lack nectaries. Balbisia has pollen ﬂowers, and its showy corolla indicates that it is also zoophilous; one species, B. gracilis, may be anemophilous. Rhynchotheca has apetalous ﬂowers with large, pendulous anthers and shows synchronous mass-ﬂowering, all indicative of anomophily (Weigend 2005). Thus, the morphological disparity of Ledocarpaceae appears to be related to their range of pollination syndromes, which may explain the difﬁculties morphological workers had in recognising the circumscription and afﬁnities of the family. Phytochemically, Geraniales are characterised by the typical presence of ellagitannins; ellagic acid has been recorded from all genera (Tetilla not studied); gallotannins are also present in Geranicaeae, and geraniin, an ellagitannin based on dehydroxyhexahydroxydiphenic acid, is a prominent compound in Geranium. Proanthocyanidins are uniformly lacking from aerial parts but occur in seed coats and are recorded also from the rootstocks of Geraniaceae. Other biodynamic compounds include the bufodienolides and pentacyclic triterpenoids in Melianthaceae (Hegnauer 1969, 1989).

References APG II 2003. See general references. Boesewinkel, F.D. 1988. The seed structure and taxonomic relationships of Hypseocharis Remy. Acta Bot. Neerl. 37:111–120. Boesewinkel, F.D. 1997. Seed structure and phylogenetic relationships of the Geraniales. Bot. Jahrb. Syst. 119:277– 291. Chase, M.W. et al. 1993. See general references. Dahlgren, R. 1980. A revised system of classiﬁcation of the angiosperms. Bot. J. Linn. Soc. 80:91–124.

Introduction to the Groups Treated in this Volume Engler, A. 1892. Syllabus der Vorlesungen über spezielle und medizinisch-pharmazeutische Botanik. Berlin: Gebr. Borntraeger. Hegnauer, R. 1969, 1989. See general references. Knuth, R. 1931. Geraniaceae. In: Engler, A., Harms, H. (eds) Die natürlichen Pﬂanzenfamilien, ed. 2, 19a. Leipzig: W. Engelmann. Kubitzki, K. (ed.) 2004. Flowering plants. Dicotyledons. Celastrales, Oxalidales, Rosales, Cornales, Ericales. The Families and Genera of Flowering Plants, VI. Berlin Heidelberg New York: Springer. Morgan, D.R., Soltis, D.E. 1993. See general references. Price, R.A., Palmer, J.D. 1993. See general references. Savolainen, V., Fay, M.F. et al. 2000. See general references. Soltis, D.E. et al. 2000. See general references. Sosa, V., Chase, M.W. 2003. See general references. Takhtajan, A.L. 1959. Die Evolution der Angiospermen. Stuttgart: G. Fischer. Takhtajan, A. 1987. See general references. Thorne, R.F. 2001. See general references. Weigend, M. 2005. Notes on the ﬂoral morphology in Vivianiaceae (Geraniales). Pl. Syst. Evol. 253:125–131.

Introduction to Gunnerales 1. Poikilohydric shrubs; nodes trilacunar; axial parenchyma 0; rays uniseriate; leaves opposite; ﬂowers unisexual, hypogynous; perianth of up to 4 scales; stamens 3–8; ovary 3–4-locular; stylodia 3–4, broad, recurved, with ventrally decurrent stigma; pollen in tetrads; embryo sac Allium type (bisporic, 8-celled); fruit a septicidal capsule; sieve-element plastids S type. 1/2, E and South Africa, Madagascar Myrothamnaceae (see Vol. II) – Perennial herbs, often giant and nearly acaulescent, with endosymbiontic Nostoc cells; nodes multilacunar; vascular system nearly always polystelic; leaves alternate; ﬂowers epigynous, 2-merous; ovary 1-locular; stylodia subulate; pollen in monads; embryo sac Peperomia type (tetrasporic, 16-celled); stylodia 2; fruit a drupe; ellagitannins present; sieve-element plastids Pcf type. 1/c. 60, mainly in southern hemisphere Gunneraceae

Traditionally, Gunneraceae were included in Haloragaceae; Takhtajan (1997) placed them in Saxifraganae. Numerous molecular studies recovered the family in close association with the desert shrub Myrothamnus at the base of core eudicots, where they form a strongly supported clade. There is also evidence for the position of this clade as sister to all remaining core eudicots (cf. Fig. 1), a grouping indicated in various analyses and strongly supported particularly by Soltis et al. (2000, 2003) and Hilu et al. (2003). Gunnera very probably has dimerous ﬂowers and the same may apply to Myrothamnus (see Conspectus). Dimery is not only widespread in early-diverging eudicots such as Proteaceae and

7

many Ranunculaceae but usually also co-occurs with trimery in basal angiosperms (Kubitzki 1987) or even with pentamery in early-diverging eudicots (Soltis et al. 2003). This is not seen in character reconstructions if only a single exemplar per family is included in a tree, as in the reconstruction of perianth merosity in Fig. 3 of Soltis et al. (2003). Indeed, both in basal angiosperms and early-diverging eudicots, there is pronounced variation in ﬂoral merosity, and the stereotyped pentamerous ﬂoral structure with diplostemony or haplostemony occurs only above the node to Gunnerales. Thus, in Ranunculaceae, pentamery, where it occurs, is restricted to the perianth and, in pentamerous Sabia (Sabiaceae), the sepals, petals and stamens stand on the same radius, a clear violation of Hofmeister’s rule but quite common in “basal” eudicots, as in Gunnera itself (see also Doust and Stevens 2005). Yet, following the node to Gunnerales, the typical pentamerous eudicot pattern is strictly conserved, and further variation is limited to processes such as fusion, reduction and multiplication of stamens and/or carpels and of perianth parts. Gunnerales, although forming part of the core eudicot clade, have not achieved (or have lost?) the pentamerous pattern, but agree with many core eudicots in possessing potent allelochemicals based on ellagic acid.

References Doust, A.W., Stevens, P.F. 2005. A reinterpretation of the staminate ﬂowers of Haptanthus. Syst. Bot. 30:779–785. Hilu, K.W. et al. 2003. See general references. Kubitzki, K. 1987. Origin and signiﬁcance of trimerous ﬂowers. Taxon 36:21–28. Kubitzki, K., Rohwer, J.G., Bittrich, V. (eds) Flowering plants. Dicotyledons. Magnoliid, Hamamelid and Caryophyllid families. The Families and Genera of Vascular Plants, II. Berlin Heidelberg New York: Springer. Soltis, P.S., Soltis, D.E. 2004. The origin and diversiﬁcation of angiosperms. Amer. J. Bot. 91:1614–1626. Soltis, D.E. et al. 2000. See general references. Soltis, D.E. et al. 2003. See general references. Takhtajan, A. 1997. See general references.

Introduction to Myrtales 1. Ovary unilocular with apical placentation, inferior (half-inferior in Strephonema); indumentum almost always of slender, unicellular, thick-walled, pointed hairs with a distinctive basal compartment; inﬂorescences indeterminate; [stamen whorls 1 or 2, the

8

K. Kubitzki

–

2.

– 3.

–

4.

– 5.

– 6. – 7.

–

1

outer sometimes with 2 or 3 times the normal number of stamens; pseudocolpi + (0 in Strephonema); intrastaminal disk often +; fruit 1-seeded, a drupe, usually ﬂattened, ridged and/or winged; cotyledons twisted (massive and hemispheric in Strephonema)]. 14/500, pantropical Combretaceae Ovary usually multilocular with axile placentation, more or less inferior; fruit 1–many-seeded, usually a capsule or berry; indumentum various but not as above 2 Leaves with secretory cavities usually containing essential oils (0 in Psiloxylon), spirally arranged or opposite; pollen oblate, brevi- to longicolpate, lacking pseudocolpi; style base often sunken in apex of gynoecium 3 Leaves lacking secretory cavities, not aromatic; pollen often with pseudocolpi; style base generally not sunken (sunken in some Vochysiaceae) 4 Dioecious; leaves spiral; stamens ≥ 10, erect in bud; anthers tetralocular at anthesis, dehiscing by slits; embryo sac bisporic. 2/4, south-eastern Africa, Mascarenes Myrtaceae–Psiloxyloideae∗1 Flowers bisexual, rarely andromonoecious; leaves spiral or opposite; stamens (few–)usually many, inﬂexed in bud; anthers bilocular at anthesis, dehiscing with longitudinal or apical slits or pores; embryo sac monosporic; [ovary (nearly superior–)inferior, (1)2– 4(–18)-locular; fruits capsular, indehiscent, or ﬂeshy]. c. 140/over 5,500, tropical to warm-temperate regions mainly of southern hemisphere, with greatest diversity in the Australasian region Myrtaceae–Myrtoideae∗ Flowers strongly mono- or asymmetric; fertile stamen 1, staminodes 0–several; pollen without pseudocolpi; [petals (0)1–3(5); style base ± sunken in apex of gynoecium; fruit a loculicidal capsule or samaroid]. 8/200, most neotropical, 2/5 of them in West Africa Vochysiaceae Flowers usually not strongly zygomorphic; stamens > than 1; pollen often with peudocolpi 5 Pollen with viscin threads on proximal surface and unique paracrystalline beaded exine, the central body of the grain circular to triangular with (2)3(–6) protruding apertures, pseudocolpi 0; embryo sac monosporic, 4-nucleate; endosperm diploid; [ﬂowers (2)4(5, 7)-merous; stamens usually arising from rim of the well-developed hypanthium; fruit a capsule, or dry and indehiscent; interxylary phloem often present; vegetative parts rich in oxalate raphides; exotegmen ﬁbrous]. 17–24/675, widely distributed from tropics to arctic-alpine regions Onagraceae∗ Viscin threads 0, exine different; pollen apertures usually not protruding but pseudocolpi often present; embryo sac 8-nucleate, endosperm triploid 6 Pollen grains 3-porate, lacking pseudocolpi; [ovary superior to partly inferior; branched foliar sclereids +] 7 Pollen grains (2)3-colporate; pseudocolpi present or not 8 Gynoecium 4–8-carpellate and -locular; petals shortly clawed; stamens 12 or numerous; tall trees with drooping, 4-angled ultimate branches. x = 10. 1/2, Southeast Asia, New Guinea Lythraceae p.p. (Duabanga) Gynoecium 10–20-carpellate and -locular; petals linear(-lanceolate) or 0; stamens numerous; swamp

The asterisk denotes taxa not treated in this volume.

8.

– 9.

– 10. – 11.

– 12.

–

13.

–

and mangrove trees with pneumatophores. x = 12. 1/5, coastal Africa to Paciﬁc islands Lythraceae p.p. (Sonneratia) Annual aquatic with ﬂoating leaves and submerged ﬁliform-dissected stipules; ﬂowers emergent, 4merous; sepals basally connate into a tube, 2 or 4 of them accrescent in fruit as hornlike or spine-like projections; stamens 4, alternipetalous; gynoecium 2-carpellate, ovary partly inferior; fruits 1-seeded; endosperm 0 but one cotyledon starchy, very large, retained within the fruit. 1/3 (or 15?), temperate to tropical regions of Old World, except Australia Lythraceae p.p. (Trapa) Terrestrial 9 Endothelium present (at least, in Axinandra); [glabrous trees, often with quadrangular twigs; inﬂorescences indeterminate; ﬂowers hypogynous to perigynous, 4–5-merous, obhaplostemonous or rarely diplostemonous; anther endothecium ephemeral; pollen tricolporate-pseudocolpate or (Crypteronia) bisyncolporate; petals 0 or (Axinandra) small and connate apically, falling off as a cup when the ﬂower opens; ovary ± inferior, 2–6-locular; capsule woody or chartaceous]. 3/10, South and Southeast Asia, Malaysia Crypteroniaceae Endothelium 0 10 Flowers strictly obhaplostemonous; [plants woody; anther endothecium ephemeral] 11 Flowers usually diplostemonous or multistaminate; Melastomataceae and Lythraceae rarely (ob)haplostemonous 14 Hypanthium rim ending with some blunt teeth (“epicalyx”); ovary inferior, 3–5-locular; pollen heteropolar with unequal colpi and “half pseudocolpi” restricted to one polar face; sepals conspicuous, white or pinkish, inserted on margin of hypanthium; petals scale-like, minute, closing the hypanthium in bud; [stamens inserted on inner rim of tube below petals; fruit drupaceous]. x = 10. 1/c. 8, southern and eastern Africa, from Ethiopia to South Africa Oliniaceae Epicalyx 0; ovary superior; pollen isopolar; petals, if present, not closing the hypanthium 12 Flowers (5)6(7)-merous; hypanthium stellate; petals minute, hood-like, lobate and unguiculate, arising from hypanthial rim; septum between the two microsporangia of each theca persistent; pollen 3-colporate with pseudocolpi; gynoecium 2(3)carpellate, ovary 1-locular/partly bilocular; embryo sac monosporic/8-nuclear; fruit capsular. n = 10. 1/1 Rhynchocalycaceae Flowers 4–5(6)-merous; hypanthium tubular; petals strongly reduced or 0; septum between the two microsporangia not persistent; embryo sac bisporic or tetrasporic 13 Flowers 4-merous; nodes unilacunar; foliar sclereids 0; hypanthium large, often conspicuously coloured; ovary 4-locular; pollen with pseudocolpi isomerous with apertures; embryo sac tetrasporic, 16-nucleate. n = 10. 7/23, Cape Province of South Africa Penaeaceae Flowers 5(6)-merous; nodes trilacunar; branched foliar sclereids +; pollen without pseudocolpi; hypanthium green to yellow, 4–6 mm long; ovary 2-locular; embryo sac bisporic. 1/1, Costa Rica to Bolivia Alzateaceae

Introduction to the Groups Treated in this Volume 14. Stamen connectives dorsally enlarged and often massive; anther dehiscence often ± poricidal; [pollen with pseudocolpi; leaves opposite; crystal druses and/or styloids +] 15 – Stamen connectives dorsally not enlarged; anther dehiscence by longitudinal slits 16 15. Leaf venation pinnate or brochidodromous (very rarely, acrodromous); plants woody; ﬂowers strictly epigynous, diplostemonous; stamen connectives generally provided with depressed elliptic terpenoidproducing dorsal glands; anthers with ﬁbrous endothecium, dehiscing by slits (sometimes short and functioning as pores); terminal leaf sclereids +; stomata paracytic; secondary xylem with axially included phloem islands; fruit baccate; seed coat with ﬁbrous exotegmen; seeds 1–few, generally with welldeveloped storage cotyledons. x =? 6/440, pantropical Memecylaceae∗ – Leaf venation acrodromous (very rarely, pinnate); plants woody or herbaceous; ﬂowers actino- to zygomorphic, wholly or partly epigynous, diplostemonous or (ob)haplostemonous; stamen connectives without dorsal glands; anthers mostly poricidal, endothecium 0; terminal leaf sclereids 0; stomata anemocytic, polycytic or encyclocytic; secondary xylem generally without included phloem islands; fruit capsular or baccate; seed coat without ﬁbrous exotegmen; seeds many, with small cotyledons; [indumentum very diverse, trichomes multicellular, scale-like]. x = 17. 185/4,500, mainly in tropical and subtropical regions of the world, with greatest diversity in South America Melastomataceae∗ 16. Herbaceous or woody; ovary superior (to inferior); ﬂowers usually diplostemonous or ﬂowers (ob)haplostemonous; petals crumpled in bud; stamens inserted at the base of ﬂoral tube or above, whorls of unequal length; heterostyly widespread; pollen grains tricolporate, pseudocolpi 0 or isomerous with or double the number of apertures; fruit capsular or baccate. 30/c. 600, worldwide, mainly in subtropical and tropical regions Lythraceae p.m.p. – Woody; ovary inferior; stamens many, covering the inner ﬂoral tube surface from the rim to the ovary; homostylous; pollen tricolporate, with indistinct pseudocolpi; ovary 7–9(–15)-loculate, carpels in 1 whorl or in 2–3 superposed layers; fruit a leathery berry; seeds many, with translucent sarcotesta. 1/2, from Balkan Peninsula to Himalayas and on Soqotra Lythraceae p.p. (Punica)

Earlier hypotheses on the composition of the order Myrtales are partly congruent with modern concepts. A.P. de Candolle, for instance, in 1828 in the third volume of his Prodromus, combined all major myrtalean families, such as Combretaceae, Onagraceae, Memecylaceae, Melastomataceae, Myrtaceae and, surprisingly, also Vochysiaceae into Myrtales. In addition, he included Alangiaceae, Rhizophoraceae and Lecythidaceae. This and similar circumscriptions of Myrtales persisted in most classiﬁcations up to the second half of the 20th century. Mainly due to the work of Briggs

9

and Johnson (1979) and Dahlgren and Thorne (1984), heterogeneous elements were subsequently excluded. Since then, the circumscription of the order has remained unchanged, the only exception being the reinsertion of Vochysiaceae which, based on their unique ﬂoral morphology, had not been included by most authors. Rather, they had associated it with families such as Polygalaceae and Euphroniaceae. However, phylogenetic analyses of molecular data as well as morphological evidence strongly supports the inclusion of Vochysiaceae into the order (Conti et al. 1996). In the present circumscription, the order comprises 12 families (see Fig. 2 for a phylogenetic hypothesis) and more than 9,000 species, representing about 6% of core eudicot diversity. Myrtales

Fig. 2. A phylogenetic hypothesis of relationships of Myrtales families, mainly based on Clausing and Renner (2001), Sytsma et al. (2004) and Wilson et al. (2005)

10

K. Kubitzki

are characterised by the combination of vestured pits and bicollateral vascular bundles in the primary xylem, resulting in the appearance of phloem included within the secondary xylem (van Vliet and Baas 1984), and also by several embryological features (Tobe and Raven 1983). Additional characters found in part throughout the order include opposite leaves with undivided laminas, even in the aquatic members; small or rudimentary stipules; short to elongate hypanthia; stamens incurved in bud; vessel elements with simple perforations, paratracheal axial parenchyma and usually nonseptate ﬁbres; secondary phloem stratiﬁed in young twigs; unilacunar nodes; simple styles; pollen with subsidiary “colpi” (“pseudocolpi”, i.e. meridional invaginations in the intercolpial regions, apparently with a harmomegathic function); 2-celled pollen; a crystalliferous endotesta; scarce or no endosperm; and copious amounts of galloand ellagitannins, the latter often methylated. Morphological studies signiﬁcantly contributed to our knowledge of Myrtales in the 1970s and 1980s, and many of these appear in the Myrtales symposium volume published in the Annals of the Missouri Botanic Garden (vol. 71, 1984). Following the comparative analysis of inﬂorescence structure by Briggs and Johnson (1979), Weberling (1988) analysed the inﬂorescences from a typological point of view. Monotelic thyrsopaniculate inﬂorescences, postulated to be basic in the order, predominate in Myrtaceae, Melastomataceae, Oliniaceae and other smaller families whereas Combretaceae and Onagraceae are polytelic throughout. Nevertheless, the aspect of character polarity of inﬂorescences is yet not completely settled, and recent work shows that within Lythraceae alone the monotelic condition is derived at least four times from the polytelic (Graham et al. 2005). The so-called pseudocolpi are a peculiar character of the pollen grains of many Myrtales, and the distribution and different expressions of these structures are problematic. The absence of pseudocolpi from part of Lythraceae is striking, as is the occurrence of “double” pseudocolpi in another part (Patel et al. 1984). Their complete absence from Onagraceae and the Myrtaceae clade have led earlier authors (Dahlgren and Thorne 1984; see also Johnson and Briggs 1984) to postulate the origin of the pseudocolpi after the branching off of these two families. In view of recent phylogenetic hypotheses (Fig. 2), however, it seems more parsimonious to consider pseudocolpi as ancestral for the order as a whole.

Modern phylogenetic studies in Myrtales started with the seminal work of Johnson and Briggs (1984), and many of their ﬁndings have later been conﬁrmed by molecular studies (Conti et al. 1996, 1997, 2002; Clausing and Renner 2001; Sytsma et al. 2004; Wilson et al. 2005). Molecular analyses generally provided strong support for the monophyly of individual families, and also interfamilial relationships have been greatly clariﬁed. The morphological circumscription of families and larger clades turned out to be more difﬁcult (see Conspectus of families). The exact position of the order within the eudicots is not clear and, together with Crossosomatales and Geraniales, Myrtales are left unplaced within the rosids (APG II 2003; see also the angiosperm-wide analysis of matK sequences by Hilu et al. 2003). Combretaceae often appear to be sister to the rest of the order but statistical support for this is still tenuous. Onagraceae and Lythraceae are sister taxa, the former possessing raphides, the latter alkaloids. Onagraceae are highly autapomorphic (see Conspectus). Among the remaining families, Melastomataceae, Memecylaceae and their sister group, the CAROP families (Crypteroniaceae, Alzateaceae, Rhynchocalycaceae, Oliniaceae and Peneaeaceae), are characterised by dorsally massive anther connectives. Renner (1993) and Clausing and Renner (2001) determined the acrodromous leaf venation and lack of a ﬁbrous anther endothecium as being synapomorphic for Melastomataceae, and the terpenoid-producing connective glands as synapomorphic for Memecylaceae. The few genera of Melastomataceae which lack the peculiar, arching leaf venation are nested within the family and thus are clearly derived, and the occurrence of an anther endothecium in the basal melastom genus Pternandra is interpreted as a plesiomorphy (Clausing and Renner 2001). Interestingly, Pternandra also has the interxylary phloem islands (included phloem) which generally occur in Memecylaceae. This trait is interpreted as parallelism, and not as plesiomorphy, because Pternandra agrees with Melastomataceae in most other wood characters. The CAROP families share the loss of an anther endothecium (probably evolved independently from Melastomataceae) with obhaplostemonous ﬂowers (Schönenberger and Conti 2003) and the presence of stipules (Johnson and Briggs 1984). Apart from these features, the four families are strongly diversiﬁed. Particularly Crypteroniaceae, with their variable androecium and gynoecium

Introduction to the Groups Treated in this Volume

structure, defy any attempt for a sound morphological family characterisation; the circumscription of this family follows largely molecular ﬁndings. The melastom/CAROP clade is sister to the Myrtaceae/Vochysiaceae clade. Myrtaceae represent the largest, most diverse family of the order, for which a detailed classiﬁcation has recently been established (Wilson et al. 2005). The inclusion of the somewhat aberrant genera Psiloxylon and Heteropyxis in Myrtaceae increases the support for the monophyly of the family, compared to a separate treatment of these two taxa as monogeneric families. The great size of Myrtaceae encompasses much variation in inﬂorescence, ﬂoral and fruit structure, which has been explored by numerous studies subsequent to the seminal contributions by Briggs and Johnson (1979) and Johnson and Briggs (1984). Until the advent of molecular systematics, the close relationship of Vochysiaceae and Myrtaceae had been camouﬂaged by the distinct ﬂoral organisation of the former family but Vochysiaceae have many myrtalean traits, and share the plesiomorphic (see the hypothetic “Protomyrtalis” of Johnson and Briggs 1984) sunken styles and 1–2-celled hairs with many Myrtaceae (Stevens 2005). Much work has been dedicated to the elucidation of the biogeographic history of Myrtales. This task is complicated due to the ancient origin of the order and its poor fossil record (see Sytsma et al. 2004). Recent dating analyses have estimated the crown group of Myrtales to be 107 (Wikström et al. 2001) or 110 million years old (Sytsma et al. 2004), corresponding to the Albian of the Lower Cretaceous. The split between the Myrtaceae/Vochysiaceae clade and the Melastom/CAROP clade may also have occurred in the Albian. This implies that Gondwanan vicariance was an important factor in the biogeographic history of this lineage, as seems reﬂected by, for instance, the disjunct distribution of the CAROP families and the out-of-India dispersal of Crypteroniaceae (Rutschmann et al. 2004). As for Myrtaceae, Sytsma et al. (2004) could not unambiguously determine the place of their initial diversiﬁcation, although the extant members of the family are clearly Australasian in origin and a more recent move to South America occurred in the early Eocene, possibly using the temperate Antarctic land bridge. Vochysiaceae are clearly neotropical; the African representatives of the family are nested within a South American clade and may have reached Africa by long-distance

11

dispersal in the Neogene, when the Atlantic had already rifted c. 80 million years ago in the equatorial region (Sytsma et al. 2004). The initial radiation of Melastomataceae is hypothesised to have occurred during the Palaeocene/Eocene along the northern shore of the Sea of Tethys (Renner et al. 2001). From there, the family may have dispersed to North America and throughout Eurasia, later also to South America and from there with repeated long-distance dispersal events to Africa, Madagascar, India and Indochina.

References APG II 2003. See general references. Briggs, B.G., Johnson, L.A.S. 1979. Evolution in the Myrtaceae – evidence from inﬂorescence structure. Proc. Linn. Soc. New South Wales 102:157–256. Candolle, A.P. de 1828. Prodromus systematis naturalis regni vegetabilis. Pars III. Paris: Treuttel & Würtz. Clausing, G., Renner, S.S. 2001. Molecular phylogenetics of Melastomataceae and Memcylaceae: implications for character evolution. Amer. J. Bot. 88:486–498. Conti, E. et al. 1996. See general references. Conti, E. et al. 1997. See general references. Conti, E. et al. 2002. See general references. Dahlgren, R., Thorne, R.F. 1984. The order Myrtales: circumscription, variation, and relationships. Ann. Missouri Bot. Gard. 71:633–699. Graham, S.A. et al. 2005. See general references. Hilu, K.W. et al. 2003. See general references. Johnson, L.A.S., Briggs, B.G. 1984. Myrtales and Myrtaceae – a phylogenetic analysis. Ann. Missouri Bot. Gard. 71:700–756. Patel, V.C., Skvarla, J.J., Raven, P.H. 1984. Pollen characters in relation to the delimitation of Myrtales. Ann. Missouri Bot. Gard. 71:858–969. Renner, S.S. 1993. Phylogeny and classiﬁcation of the Melastomataceae and Memecylaceae. Nordic J. Bot. 13:519– 540. Renner, S.S., Clausing, G., Meyer, K. 2001. Historical biogeography of Melatomataceae: the roles of Tertiary migration and long-distance dispersal. Amer. J. Bot. 88:1290–1300. Rutschmann, F., Eriksson, T., Schönenberger, J., Conti, E. 2004. Did Crypteroniaceae disperse out of India? Molecular dating evidence from rbcL, ndhF, and rpl16 intron sequences. Intl J. Pl. Sci. 165, suppl. 4:S69–S83. Schmid, R. 1980. Comparative anatomy and morphology of Psiloxylon and Heteropyxis, and the subfamilial and tribal classiﬁcation of Myrtaceae. Taxon 29:559–595. Schönenberger, J., Conti, E. 2003. Molecular phylogeny and ﬂoral evolution of Penaeaceae, Oliniaceae, Rhynchocalycaceae, and Alzateaceae (Myrtales). Amer. J. Bot. 90:293–309. Stevens, P.F. 2005. See general references. Sytsma, K.J. et al. 2004. See general references. Tobe, H., Raven, P.H. 1983. An embryological analysis of the Myrtales: its deﬁnition and characteristics. Ann. Missouri Bot. Gard. 70:71–94.

12

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Vliet, G.J.C.M. van, Baas, P. 1984. Wood anatomy and classiﬁcation of the Myrtales. Ann. Missouri Bot. Gard. 71:783–800. Weberling, F. 1988. The architecture of inﬂorescences in the Myrtales. Ann. Missouri Bot. Gard. 75:226–310. Wikström, N. et al. 2001. See general references. Wilson, P.G., O’Brien, M.M., Heslewood, M.M., Quinn, C.J. 2005. Relationships within Myrtaceae sensu lato based on matK phylogeny. Pl. Syst. Evol. 251:3–19.

Introduction to the Passiﬂoraceae Alliance (“Passiﬂorales” = Malpighiales) 1. (Andro)gynophore 0; petal aestivation contorted; corona rarely present and then weakly developed; calyx and corolla separating from developing fruit and falling together; seeds arillate, pitted. 10/+200, Africa, America Turneraceae – (Andro)gynophore usually present; petal aestivation cochlear; corona often present and strikingly coloured 2 2. Stylodia inserted beneath the top of ovary; stamens 5; pollen grains 3-colporate; seeds exarillate; calyx persistent in fruit; tendrils 0. 1/24, Chile, Peru Malesherbiaceae – Stylodia inserted on top of ovary; stamens 4, 5, or many; pollen grains 3–12-colporate or -foraminate; seeds arillate; tendrils often present. 17/700–750, pantropical Passiﬂoraceae

These three families are closely related and also could be merged into one, as suggested as an option by the Angiosperm Phylogeny Group (APG II 2003); here, they are treated separately because their authors prefer the traditional family circumscription. Whereas the molecular data of Chase et al. (2002) conﬁrm that these families form a clade, at the time of writing of these accounts and this introduction (Sept. 2005), it still remains unclear whether the separation of these families involves paraphyly. They share important characters such as an extrastaminal corona, exotestal seeds, cyclopentenoid cyanogenic glucosides and/or cyclopentenyl fatty acids, and biparental or paternal transmission of plastids (the latter not observed in Malesherbiaceae). Whereas seed structure and chemical make-up appear quite constant in the group, a corona is not always present and its expression is quite diverse. It is developed in its full-ﬂedged form in Passiﬂoraceae, mainly Passiﬂora, but is only weakly in the possibly basal Adenias and also in Turneraceae and Malesherbiaceae; it is difﬁcult to decide whether this represents an anagenetic or reductional transformation. Accessory or superposed buds, as in Passiﬂoraceae, are found also in various

members of Salicaceae and Achariaceae (de Wilde 1971b, at that time included in Flacourtiaceae) where, however, no cyanogens are present; still, a corona is known from Abatia, which led earlier researchers to include the genus in Passiﬂoraceae. Its placement in Salicaceae on the basis of molecular evidence (Chase et al. 2002) is corroborated by morphological evidence. Thus, in contrast to Passiﬂoraceae, Abatia has opposite leaves, valvate calyx aestivation and extrorse anthers, and both the coronal threads and stamens are irregularly arranged whereas in Passiﬂoraceae the corona elements are in distinct whorls and the stamens in the polystemononous genera of this family are in a single whorl (Bernhard 1999); the corona may not be homologous in both groups.

References For references, see the Selected Bibliography of Passiﬂoraceae and the General References (this volume).

Introduction to Proteales 1. Herbaceous, cambial activity 0; sepals 2, stamens numerous, spirally arranged; carpel closure by secretion; ovule 1 per carpel, anatropous; pollen grains variously furrowed or rarely sulcate or tricolpate; simple benzylisoquinoline alkaloids (aporphines) present; myricetin and condensed tannins 0; carpel closure by secretion; ﬂowers thermogenic]. 1/1 or 2, North America, Asia, Australia Nelumbonaceae (see Vol. II) – Woody; sepals or tepals > 2, stamens whorled; carpels postgenitally fused; ovules 1 or 2, rarely more per carpel, usually orthotropous; pollen grains triaperturate(-derived); benzylisoquinoline alkaloids 0; myricetin and condensed tannins present but gallate 0; [seeds lacking starch but containing fat oil and protein] 2 2. Stipules 2, often fused; ﬂowers small, unisexual, in globular heads; perianth 3–4(–7)-merous, the petals vestigial; carpels 3–8, distinct, ovules 1(2); pollen grains tricolpate; triterpenes +. 1/c. 7, North America and Asia Minor to East Asia Platanaceae (see Vol. II) – Stipules 0; ﬂowers usually bisexual, in racemes, panicles, or condensed, often paired; perianth of 4 (very rarely 3 or 5) valvate tepals; stamens antetepalous, often adnate to tepals, alternating with hypogynous nectar secreting glands; carpel 1; ovules 1–2(–many); pollen grains triporate, rarely tricolporoidate or diporate; triterpenes 0. 80/1,700, mainly southern hemisphere, best developed in Australia Proteaceae

The three families united in this order form an unexpected alliance, which was discovered by early molecular work and since has received support in

Introduction to the Groups Treated in this Volume

various multigene analyses. Sabiaceae, here left unplaced as to ordinal allocation (see family treatment), are also often found together with Proteales (cf. Fig. 1). As is evident from the characters given in the Conspectus, Nelumbonaceae appear quite out of place in this alliance. Their ranunculalean chemistry (see Gottlieb et al. 1993) is accompanied by completely ascidiate carpels without any postgenital fusion, which Nelumbo shares only with Berberidaceae; the ovules are anatropous (Igersheim and Endress 1998). Nelumbo has a dimerous calyx (Hayes et al. 2000; in contrast to information given erroneously by Kubitzki 1993), but dimerous whorls are widespread in basal eudicots (Drinnan et al. 1994; Doyle and Endress 2000; Soltis et al. 2003) and are by no means exclusive for earlydiverging eudicots. Nelumbonaceae are remarkable with regard to pollen development. Whereas in basal angiosperms (monosulcates) there is much variation between the simultaneous and successive type of microsporogenesis, almost all eudicots (triaperturates) have simultaneous microsporogenesis, with the notable exception of Nelumbonaceae (Kreunen and Osborn 1999) and Proteaceae (Furness et al. 2002; including the diporate proteaceous pollen: Blackmore and Barnes 1995). The co-occurrence of putatively monosulcate and triaperturate pollen in Nelumbo (Kuprianova 1979; Blackmore et al. 1995) raised great phylogenetic interest but later (Borsch and Wilde 2000) was found to be part of an extensive, regular variation pattern inﬂuenced by factors such as a delay in aperture ontogeny (Kreunen and Osborn 1999). Platanaceae and Proteaceae, which are resolved as sister taxa in most molecular analyses, have much in common morphologically, including the presence of ﬁve carpellary bundles (rather than three in most Ranunculales and in the early-branching Proteacea Bellendena), ample tanniniferous tissue in the carpels, mostly one or two large, orthotropous ovules of which the upper is pendent, and ﬂoral organs which may be arranged in dimerous whorls. Traditionally, Proteaceae had been interpreted as tetramerous but the ontogenetic work of Douglas and Tucker (1996a) supports the interpretation of their perianth and androecium as dimerous. Possibly, Proteaceae are primarily apetalous; the nectarial hypogynous scales, which alternate with the tepals, are positioned inside the stamen whorl and their initiation takes places after that of all other ﬂoral organs (Douglas and Tucker 1996),

13

which is inconsistent with their interpretation as erstwhile petals. Both extant and fossil Platanaceae show considerable variability in the number of ﬂoral parts. Some of their mid-Cretaceous and early Tertiary representatives had strictly pentamerous perianths with ﬁve stamens and ﬁve carpels respectively (Friis and Crane 1989), but clear tetramery existed, for instance, in the Late Cretaceous Quadriplatanus (Magallón et al. 1997), in which the female ﬂowers had two perianth whorls and eight carpels. Proteaceae pollen is known for differing from the widespread developmental pattern in eudicots, in which apertures are formed in pairs at six points in the developing tetrad, following Fischer’s Rule. In Proteaceae, the apertures are formed in groups of three at four points in the tetrad (Garside 1946). Furness and Rudall (2004), who quoted Illiciales, Proteaceae and Olacaceae as the only examples in angiosperms for pore orientation according to Garside’s Rule, argued for origins of this developmental mode of triaperturate pollen independent from the developmental pattern following Fischer’s Rule which characterises the majority of the eudicots. Illiciales are, however, irrelevant in this context because their “tricolpate” condition is an extension of the trichotomosulcate arrangement, which is often found among monosulcates in which Illiciales are embedded (Huynh 1976; Doyle et al. 1990). The pollen grains of some Olacaceae, which are formed according to Garside’s Rule, appear autapomorphic because this family is deeply embedded within the triaperturate group. Also for Proteaceae, it is difﬁcult to envisage a completely independent origin of the triaperturate condition from a monosulcate/trichotomosulcate ancestor: even if Proteales were basal in eudicots, Proteaceae are nested within Proteales, in which Platanaceae and Nelumbonaceae produce “normal” triaperturates. Any hypothesis of an independent origin within this order would then require one or two additional origins of the normal Fischer’s Rule tricolpate type, a non-parsimonious assumption. Rather, these considerations all favour an origin of the proteaceous condition from normal tricolpates, much as concluded for Olacaceae. This view is shared by Blackmore and Crane (1998) who tend to view the Garside’s Rule arrangement in Proteaceae as derived. A triporate fossil pollen from the Cenomanian (mid-Cretaceous) of the Northern Gondwana Province, Triorites africaensis, has often been related to Proteaceae. The ultrastructural analysis of

14

K. Kubitzki

Triorites by Ward and Doyle (1994) suggests that Triorites pollen is not tricolporate-derived, as usually is the case with triporates, but perhaps directly from tricolpate. Ward and Doyle (1994) considered this as an additional piece of evidence against a derivation of the family from a rosid ancestor – of course, amply conﬁrmed by molecular data. A number of Late Cretaceous (Late Santonian-Early Campanian) follicular fruits from southern Sweden (Leng et al. 2005) exhibit several similarities with Proteaceae, particularly with the ﬁrst branching lineages in the family. These include a plicate carpel structure with a vascular system of three bundles, several anatropous, probably bitegmic ovules, and a more or less sessile stigmatic area which is located at the distal-most part of the ventral slit and extends over the topological apex to the abaxial side of the follicle. Although these fossils differ from extant Proteaceae in having unisexual and obviously perianth-free ﬂowers and several ovules, they represent an extinct lineage of basal eudicots which probably was close to modern Proteaceae. Johnson and Briggs (1975), with admirable intuition, anticipated that Proteaceae are not only an “isolated” but also a fairly basal family, rather than belonging somewhere in the rosids, this having been fully conﬁrmed by the evidence available 30 years later.

References Blackmore, S., Barnes, S.H. 1995. Garside’s rule and the microspore tetrads of Grevillea rosmarinifolia A. Cunningham and Dryandra polycephala Bentham (Proteaceae). Rev. Palaeobot. Palynol. 85:111–121. Blackmore, S., Crane, P.R. 1998. The evolution of apertures in the spores and pollen grains of embryophytes. In: Owens, S.J., Rudall, P.J. (eds) Reproductive biology. Royal Botanic Gardens, Kew, pp. 159–182. Blackmore, S., Stafford, P., Persson, V. 1995. Palynology and systematics of Ranunculiﬂorae. Pl. Syst. Evol. suppl. 9:71–82. Borsch, T., Wilde, V. 2000. Pollen variability within species, populations, and individuals, with particular reference to Nelumbo. In: Harley, M.M., Morton, C.M., Blackmore, S. (eds) Pollen and spores: morphology and biology. Royal Botanic Gardens, Kew, pp. 285–299. Douglas, A.W., Tucker, S.C. 1996. Comparative ﬂoral ontogenies among Persoonioideae including Bellendena (Proteaceae). Amer. J. Bot. 83:1528–1555. Doyle, J.A., Endress, P.K. 2000. Morphological phylogenetic analysis of basal angiosperms: comparisons and combination with molecular data. Intl J. Pl. Sci. 161, suppl. 6:S121–S153. Doyle, J.A., Hotton, C.L., Ward, J.V. 1990. Early Cretaceous tetrads, zonasulculate pollen, and Winteraceae. II.

Cladistic analysis and implications. Amer. J. Bot. 77:1558–1568. Drinnan, A.N., Crane, P.R., Hoot, S.B. 1994. Patterns of ﬂoral evolution in the early diversiﬁcation of non-magnoliid dicotyledons (eudicots). Pl. Syst. Evol. suppl. 8:93–122. Endress, P.K., Igersheim, A. 1999. Gynoecium diversity and systematics of the basal eudicots. Bot. J. Linn. Soc. 130:305–393. Friis, E.M., Crane, P.R. 1989. Reproductive structures of Cretaceous Hamamelidae. In: Crane, P.R., Blackmore, S. (eds) Evolution, systematics and fossil history of the Hamamelidae, 1. Oxford: Clarendon Press, pp. 155– 174. Furness, C.A., Rudall, P.J. 2004. Pollen aperture evolution – a crucial factor for eudicot success? Trends Pl. Sci. 9:154–158. Furness, C.A., Rudall, P.J., Sampson, F.B. 2002. Evolution of microsporogenesis in angiosperms. Intl J. Pl. Sci. 163:235–260. Garside, S. 1946. The developmental morphology of the pollen of Proteaceae. J. S. African Bot. 12:27–34. Gottlieb, O.R., Kaplan, M.A.C., Zocher, D.H.T. 1993. A chemosystematic overview of Magnoliidae, Ranunculidae, Caryophyllidae and Hamamelidae. In: Kubitzki, K. (ed.) The Families and Genera of Vascular Plants, 2. Berlin Heidelberg New York: Springer, pp. 20–31. Hayes, V., Schneider, E.L., Carlquist, S. 2000. Floral development of Nelumbo nucifera (Nelumbonaceae). Intl J. Pl. Sci. 161, suppl. 6:S183–S191. Hoot, S.B., Magallón, S., Crane, P.R. 1999. Phylogeny of basal eudicots based on three molecular data sets: atpB, rbcL, and 18S nuclear ribosomal DNA sequences. Ann. Missouri Bot. Gard. 86:1–32. Huynh, K.-L. 1976. L’arrangement du pollen du genre Schisandra (Schisandraceae) et sa signiﬁcation phylogénique chez les Angiospermes. Beitr. Biol. Pﬂanzen 52:227–253. Igersheim, A., Endress, P.K. 1998. Gynoecium diversity and systematics of the paleoherbs. Bot. J. Linn. Soc. 127:289–370. Johnson, L.A.S., Briggs, B. 1975. See general references. Kreunen, S.S., Osborn, J.M. 1999. Pollen and anther development in Nelumbo (Nelumbonaceae). Amer. J. Bot. 86:1662–1676. Kubitzki, K. 1993. Platanaceae. In: Kubitzki, K., Rohwer, J.G., Bittrich, V. (eds) Flowering plants. Dicotyledons. Magnoliid, Hamamelid and Caryophyllid families. The Families and Genera of Vascular Plants, II. Berlin Heidelberg New York: Springer, pp. 521–522. Kubitzki, K., Rohwer, J.G., Bittrich, V. (eds) Flowering plants. Dicotyledons. Magnoliid, Hamamelid and Caryophyllid families. The Families and Genera of Vascular Plants, II. Berlin Heidelberg New York: Springer. Kuprianova, L.A. 1979. On the possibility of the development of tricolpate pollen from monosulcate. Grana 18:1–4. Leng, Q., Schönenberger, J., Friis, E.M. 2005. Late Cretaceous follicular fruits from southern Sweden with systematic afﬁnities to early diverging dicots. Bot. J. Linn. Soc. 148:377–407. Magallón, S., Herendeen, P.S., Crane, P.R. 1997. Quadriplatanus georgianus gen. et sp. nov.: staminate and pis-

Introduction to the Groups Treated in this Volume tillate platanaceous ﬂowers from the Late Cretaceous (Coniacian-Santonian) of Georgia, U.S.A. Intl J. Pl. Sci. 158:373–394. Ressayre, A., Dreyer, L., Triki-Teurtroy, S., Forchioni, A., Nadot, S. 2005. Post-meiotic cytokinesis and pollen aperture pattern ontogeny: comparison of development in four species differing in aperture pattern. Amer. J. Bot. 92:576–583. Soltis, D.E. et al. 2003. See general references. Ward, J.V., Doyle, J.A. 1994. Ultrastructure and relationships of mid-Cretaceous polyforate and triporate pollen from northern Gondwana. In: Kurmann, M.H., Doyle, J.A. (eds) Ultrastructure of fossil spores and pollen. Royal Botanic Gardens, Kew, pp. 161–172.

– 9.

–

Introduction to Saxifragales 10. 1. Trees; stigmas decurrent; pollen colpate or pantoporate; [anthers with protruding connectives] 2 – Trees or herbs; stigmas subulate, capitate or spatulate; pollen colpor(oid)ate, rarely porate 5 2. Flowers mostly hermaphroditic; anthers mostly dehiscing with valves; [trichomes mostly stellate or tufted; ﬂowers (2–)4–5(–7)-merous, calyx rarely 0, petals often adaxially circinate; ovary inferior to superior, 2-carpellate with straight stylodia; iridoids 0]. n = 8, 12, 18. 27/82, tropical to temperate, C and E North America, SE Europe through S, E and SE Asia to New Guinea and NE Australia Hamamelidaceae (see Vol. II) – Dioecious; anthers dehiscing with slits or rudimentary valves 3 3. Ovary unicarpellate with abaxial suture [but the solitary carpels (= female ﬂowers) united into pseudanthia]; iridoids 0; [fruit a samara; seed with large embryo]. n = 19. 1/2, China and Japan Cercidiphyllaceae (see Vol. II) – Ovary bicarpellate; no pronounced shoot dimorphism; iridoids present 4 4. Female ﬂowers in globose heads, male in terminal globose racemes; stipules present; pollen pantoporate; embryo > half the length of the seed; secretory ducts in all vegetative tissues. n = 8. 1/13, C America, E Mediterranean, E Asia to Malesia Altingiaceae (see Vol. II under Hamamelidaceae) – Flowers in elongate racemes; stipules 0; pollen tricolpate; embryo minute; secretory ducts 0. n = 8. 1/10, E Asia, Malesia Daphniphyllaceae 5. Flowers polyandrous 6 – Flowers haplostemonous or diplostemonous. Core Saxifragales 7 6. Apocarpous; stamens in 5 fascicles; seeds with shining sarcotesta; perennial herbs or (half)shrubs. 1/40, northern hemisphere Paeoniaceae – Syncarpous, ovary unilocular; stamens not distinctly fasciculate; seeds with black crustaceous coat; trees. 3/11, South America, Africa Peridiscaceae 7. Flowers essentially 4-merous; [leaves estipulate; nodes unilacunar] 8 – Flowers essentially 5 >-merous 10 8. Ovary superior, nearly apocarpous; anther wall without ﬁbrous endothecium; [pollen tricolporate; fruit fol-

– 11.

– 12.

–

13.

– 14.

–

15

licular; seeds very small, winged; low glabrous shrub]. 1/1, Tasmania Tetracarpaeaceae Ovary inferior or semi-inferior, the carpels at least basally connate; anther wall with ﬁbrous endothecium 9 Leaves alternate, opposite, or verticillate; ovary inferior, 4(–2)-carpellate; stylodia free with penicillate stigmas; vessel elements with simple perforation; pollen 4– 6(–20)-colpate or -porate, often aspidiate; [tanniniferous terrestrial or aquatic herbs, shrubs or small trees]. n = 7 (6, 9, 21, 29). 8/150, worldwide but mainly Australia Haloragaceae Leaves opposite; ovary semi-inferior, 4-carpellate; style shortly 4-lobed; stigmas papillate; vessel elements with scalariform perforation; pollen tricolporate; [petals small or 0; climbing shrubs]. 1/2, Australia Aphanopetalaceae Shrubs; [leaves alternate; vessel element perforation mainly scalariform; ovary syncarpous] 11 Herbs; [seeds exotestal] (but see Crassulaceae) 13 Gynoecium 5-carpellate; style shortly 5-lobed; [ovary largely inferior with 4–6 ascending ovules/locule; stigmas radiate; stipules minute; pollen 3-colporate; vessel elements also with simple perforations]. 1/3, Mexico Pterostemonaceae Gynoecium 2-carpellate; style cleft or not 12 Ovary inferior, 1-locular; fruit a berry; seeds usually numerous, small, mucilaginous; embryo small; pollen 8-zonocolporate, pentacolpo-di-orate, or pantoporate; erect, arching, trailing or prostrate shrubs often with 3- or 2-forked or simple nodal spines and smaller internodal bristles, and long-petiolate, basally 2-veined leaves; [seed coat with exotestal mucilaginous palisade, endotesta crystalliferous]. n = 8. 1/150–200 Grossulariaceae Ovary nearly superior to 3/4 inferior, 2-locular; fruit a capsule; seeds few to many, dry; embryo large, curved; pollen bilateral, 2-porate; unarmed shrubs or small trees with short-petiolate, pinnately veined leaves; [anthers with globular protrusion of the connective; stylodia separate to fused but apically coherent with globular stigmas]. n = 11. 1/c. 27, E and SE Asia, one sp. in Africa, one in North America Iteaceae Fruit a 5–7-carpellate and -beaked stellate capsule, the beak of each carpel circumscissile above the syncarpous region; nodes unilacunar; vessel element perforation scalariform; [rhizomatous perennials; petals 0 or very small]. n = 8, 9. 1/2, E North America, E and SE Asia Penthoraceae Fruiting carpels not dehiscing along a circumscissile suture; nodes uni-, tri- or multilacunar; vessel element perforation simple 14 Succulent herbs, subshrubs or rarely shrubs; stipules 0; nodes trilacunar or unilacunar; leaves usually simple and entire; gynoecium isomerous with perianth; nectariferous scale near base of each carpel (petaloid in Monanthes and some Sedum). n = 4–22+. 33/1,410, widely distributed mostly in arid temperate or warm regions, and centred in Mexico and South Africa Crassulaceae Not succulent, perennial and annual herbs; stipules present or leaf basis sheathing; nodes trilacunar or multilacunar; leaves simple or pinnately or

16

K. Kubitzki palmately compound or decompound; gynoecium 2(– 5)-carpellate; nectariferous disk mostly present. n = (5, 6)7(11, 12, 15, 17, 18). 33/1,410, nearly cosmopolitan but mainly in northern temperate zone and centred in North America Saxifragaceae

Saxifragales, in the circumscription followed in this volume, are the result of a series of molecular analyses carried out over the past 15 years or so (Chase

Fig. 3. A phylogenetic hypothesis of relationships of Saxifragales families, based on Fishbein et al. (2001), Fishbein and Soltis (2004) and, for Peridiscaceae, on Davis and Chase (2004). Note that resolution among the basal woody families is weekly supported. Hamamelidaceae, Altingiaceae and Cercidiphyllaceae were treated in Vol. II (Kubitzki et al. 1993) of this series

et al. 1993; Morgan and Soltis 1993; Soltis and Soltis 1997; Fishbein et al. 2001; APG II 2003; Davis and Chase 2004; Fishbein and Soltis 2004, among others). The monophyly of this clade is strongly supported. Moreover, there is a 1 bp insertion common to all members of the order (Soltis and Soltis 1997). In addition to the Core Saxifragales traditionally considered to belong to this order (see Fig. 3), it comprises also Haloragaceae, the controversial Paeoniaceae, some woody “hamamelidid” families (Cercidiphyllaceae, Hamamelidaceae, Altingiaceae, Daphniphyllaceae), and the enigmatic Peridiscaceae. Outgroup relationships of Saxifragales are weakly supported (Savolainen, Chase et al. 2000; Soltis et al. 2000) but the group is often found together with Vitaceae at the base of the large eurosid clade. A group comprising the families now constituting the order Saxifragales has never before been recognised in traditional systematic studies. In comparison with older concepts such as of those of Bentham (1865), Engler (1891, 1930) and Cronquist (1981), and partly also with the more recent but essentially morphologically based classiﬁcations by Huber (1991), Takhtajan (1997) and Thorne (2001), the present circumscription differs in three major points, ﬁrst, in the exclusion of the lineages having tenuinucellate ovules and containing iridoids; second, in the inclusion of Haloragaceae, Peridiscaceae and Paeoniaceae (included in Saxifragales by Huber 1991); and third, in the addition of several woody families showing presumably plesiomorphic characters such as valvate anther dehiscence, apiculate connective protrusions and tricolpate pollen, some of which persist here and there in the Core Saxifragales. ad 1. The ﬁrst to recognise the systematic signiﬁcance of ovules was Warming (1878), and the bitegmic ovules of Itea led van Tieghem (1898) to propose the transfer of Itea from Escalloniaceae to Saxifragaceae. He later (van Tieghem 1901) used the distinction between bitegmic and unitegmic ovules as a rigorous criterion in the classiﬁcation of the whole plant kingdom, which resulted in a system containing inconsistent and unnatural groupings, discrediting the use of this character. Consequently, his views were wholly rejected by other botanists and Engler (1930), when commenting on Hydrangioideae and Escalloniodeae which he included in his Saxifragaceae, argued that the number of integuments had little systematic signiﬁcance because, among otherwise clearly related genera of Ranunculaceae, their number

Introduction to the Groups Treated in this Volume

can be variable. However, Mauritzon (1933), in his embryological studies of Saxifragales, found ovule characters to be useful, and Philipson (1974) suggested that a distinction be made between families in which the ovular characters are constant, as opposed to those in which some variation in this respect occurs sporadically. Taxa such as Escalloniaceae, Hydrangeaceae, Phyllonoma, Montinia and Eremosyne, transferred to the asterids by Soltis and Soltis (1997) on the basis of molecular evidence, are all unitegmic and iridoid-positive. Some unitegmic genera (Darmera, Micranthes) persist in Saxifragaceae but these are embedded in broader bitegmic lineages and lack iridoids, whereas the few iridoid-positive Saxifragales are bitegmic. ad 2. Haloragaceae traditionally have been related with Myrtales but Takhtajan (1997) demonstrated that they have more characters in common with Saxifragales. Peridiscaceae have often been related to Flacourtiaceae but the three-gene analysis of Davis and Chase (2004) adds the family, with the inclusion of Soyauxia, to the Saxifragales where they come out with Daphniphyllaceae and the other woody groups at the base of the Saxifragales clade, albeit with low support (M.W. Chase, pers. comm. Nov. 2003). A close relationship between these three taxa is not reﬂected by morphological traits, although the anther ﬂaps of Soyauxia are found in some basal Saxifragales families as well. Paeoniaceae, large-ﬂowered, apocarpous, with striking seed-presentation and strongly autapomorphic2 , in the analysis of Fishbein and Soltis (2004) are basal to Core Saxifragales. ad 3. Within the Saxifragales, but outside the Core Saxifragales, iridoids occur in two families, Altingiaceae and Daphniphyllaceae, where they are poorly diversiﬁed chemically (Kaplan and Gottlieb 1982), perhaps due to the small size of these families. These are the only reports of iridoids outside the asterids. The tricolpate pollen predominating in Cercidiphyllaceae, Hamamelidaceae and Daphniphyllaceae is likely to be a plesiomorphic trait; in fact, the apertures of Cercidiphyllum appear quite archaic, and are intermediate between the poroidate and colpoidate condition (Praglowski 1975); however, there are transitions to compound (colporoidate or colporate) apertures known from within Daphniphyllum. In the Core Saxifragales, elabo2 The record of iridoids sometimes indicated for Paeonia (e.g. in Stevens 2005) may be based on Nekratova et al. (1988, in Rast. Resur. 24:392–399), who may have mistaken monoterpene glucosides of the Paeoniﬂorin type for iridoids (Hegnauer 1990).

17

rate compound apertures (with well-differentiated exo- and endoapertures) are the rule but sometimes (Saxifragaceae) they are not fully developed. On the whole, the woody basal families of (“nonCore”) Saxifragales appear as isolated remnants of formerly more richly developed, archaic lineages, as is particularly well documented for Cercidiphyllaceae. Resolution within the Core Saxifragales is better supported, mainly due to the efforts of Fishbein et al. (2001), and even a cursory glance at the topology reproduced in Fig. 3 reveals that a broader concept of Saxifragaceae (with the inclusion of Tetracarpaea and Penthorum) is untenable, unless Crassulaceae and Haloragaceae were to be incorporated, too. The topology of Fig. 3 is also useful for a comparison with character transformations which can be recognised in the Core Saxifragales. The transition from woody to herbaceous growth, usually accompanied by the loss of scalariform perforation plates of the vessel elements, has taken place some ﬁve times within Saxifragales – in Paeoniaceae, Saxifragaceae, Crassulaceae (the few woody members of which are deﬁnitely secondarily woody; see Crassulaceae, this volume), Penthoraceae and the woody/herbaceous Haloragaceae. Penthoraceae are remarkable for having “retained” scalariform perforation in spite of being herbaceous. Grossulariaceae are strictly woody whereas their sister group Saxifragaceae is largely herbaceous – a remarkable difference, although both agree in details of shoot morphology and growth dynamics, as is well described by Weigend under “Afﬁnities” of Grossulariaceae (this volume). Anthers in Saxifragales are remarkably uniformly basiﬁxed but gynoecium structure, particularly in Core Saxifragales, is labile. Pterostemonaceae stand out with an isomerous and apocarpous gynoecium within an otherwise 2–3-carpellate Saxifragaceae alliance; the gynoecia of Crassulaceae and Tetracarpaeaceae are also (nearly) apocarpous. Free stylodia are widespread, and most groups with this character seem to lack a compitum. The functionally advantageous fusion of stylodia into a common style is uncommon (Grossulariaceae, Iteaceae, Aphanopetalaceae). Although there is no indication that apocarpy here, or in the (other) eurosids where it also occurs, is due to a reversal, it is difﬁcult to imagine that this character expression should be plesiomorphic in these groups. Minute embryos characterise Peridiscaceae, Daphniphyllaceae, Paeoniaceae, Grossulariaceae and Tetracarpaeaceae; all other groups have medium-sized or large embryos.

18

K. Kubitzki

References APG II 2003. See general references. Bentham, G. 1865. Ordo LIX. Saxifrageae. In: Bentham, G., Hooker, J.D., Genera Plantarum, I, ii. London: Reeve, pp. 629–655. Chase, M.W. et al. 1993. See general references. Cronquist, A. 1981. See general references. Cutler, D.F., Gregory, M. (eds) 2000. Anatomy of the Dicotyledons, 2nd edn. Vol. 4, Saxifragales. Oxford: Clarendon Press. Davis, C.C., Chase, M.W. 2004. Elatinaceae are sister to Malpighiaceae; Peridiscaceae belong to Saxifragales. Amer. J. Bot. 91:262–273. Engler, A. 1891. Saxifragaceae. In: Engler, A., Prantl, K., Die natürlichen Pﬂanzenfamilien III, 2a. Leipzig: W. Engelmann, pp. 41–93. Engler, A. 1930. Saxifragaceae. In: Engler, A., Prantl, K., Die natürlichen Pﬂanzenfamilien, ed. 2, 18a. Leipzig, W. Engelmannn, pp. 74–226. Fishbein, M., Soltis, D.E. 2004. Further resolution of the rapid radiation of Saxifragales (Angiospetrms, Eudicots) supported by mixed-model Bayesian analysis. Syst. Bot. 29:883–891. Fishbein, M. et al. 2001. See general references. Hegnauer, R. 1990. See general references. Huber, H. 1991. Angiospermen. Leitfaden durch die Ordnungen und Familien der Bedecktsamer. Stuttgart: G. Fischer. Kaplan, M.A.C., Gottlieb, O.R. 1982. Iridoids as systematic markers in dicotyledons. Biochem. Syst. Ecol. 10:329– 347. Kubitzki, K., Rohwer, J.G., Bittrich, V. (eds) Flowering plants. Dicotyledons. Magnoliid, Hamamelid and Caryophyllid families. The Families and Genera of Vascular Plants, II. Berlin Heidelberg New York: Springer. Mauritzon, J. 1933. Studien über die Embryologie der Familien Crassulaceae und Saxifragaceae. Ph.D. Thesis, Lund University. Morgan, D.R., Soltis, D.E. 1993. Phylogenetic relationships among members of Saxifragaceae sensu lato based on rbcL sequence data. Amer. J. Bot. 80:631–660. Nemirovich-Danchenko, E.N. 1994. Morphology and anatomy of the seeds of Iteaceae (in Russian). Bot. Zhurn. (Moscow & Leningrad) 79:83–87. Philipson, W.R. 1974. Ovular morphology and the major classiﬁcation of the dicotyledons. Bot. J. Linn. Soc. 68:89–108. Praglowski, J. 1975. Pollen morphology of the Trochodendraceae, Tetracentraceae, Cercidiphyllaceae and Eupteleaceae with reference to taxonomy. Pollen Spores 16:449–467. Savolainen, V., Chase, M.W. et al. 2000. See general references. Soltis, D.E., Soltis, P.S. 1997. Phylogenetic relationships in Saxifragaceae sensu lato: a comparison of topologies based on 18S rDNA and rbcL sequences. Amer. J. Bot. 84:504–522. Soltis, D.E. et al. 2000. See general references. Stevens, P.F. 2005. See general references. Takhtajan, A. 1997. See general references. Thorne, R.F. 2001. See general references.

Tieghem, Ph. van 1898. Structures de quelques ovules et parti qu’on en peut tirer pour améliorer la classiﬁcation. J. Bot. (Paris) 12:197–220. Tieghem, Ph. van 1901. L’œuf des plantes considéré comme base de leur classiﬁcation. Ann. Sci. Nat., Bot. VIII, 14:213–390. Walker, J.W. 1974. Aperture evolution in the pollen grains of primitive angiosperms. Amer. J. Bot. 61:1112–1136. Warming, E. 1878. De l’ovule. Ann. Sci. Nat. VI, 5:177–266.

Introduction to Vitales 1. Small trees, shrubs, or herbs; tendrils 0; stipular wings conspicuous, sheathing; inﬂorescences terminal; ﬂoral disk tubular, not producing nectar; due to secondary septation, ovary 4–6(–8)-locular, ovule 1 per locule. 1/34, mainly southern Asia, extending to Africa/Madagascar and Australia Leeaceae – Woody lianas usually with leaf-opposite tendrils, rarely succulent small trees or erect herbs; stipules not sheathing the petiole margins; inﬂorescences often leaf-opposed; ﬂoral disk intrastaminal, ring-shaped, cupular, or gland-shaped, usually nectariferous; ovary 2-locular, ovules 2 per locule. 14/c. 750, pantropical Vitaceae

Traditionally, Vitales were included in Rhamnales – both have antepetalous stamens – but Takhtajan (1997) dismembered this association because Vitaceae and Leeaceae differ from Rhamnaceae in their berry-like fruits and seed structure, and in having raphide sacs in the parenchymatous tissue; he placed them as “Vitalanae” close to his Proteanae at the end of his Rosidae. Corner (1976) was much impressed by the thick, ligniﬁed endotesta and small embryo of the seeds of Vitaceae, which he found “scarcely improved on that of Magnolia and. . . even more primitive”. Vitales also have a tracheidal exotegmen, which is a rare feature in angiosperm seeds – apart from Dilleniaceae; it is listed only for Cunoniaceae by Nandi et al. (1998). Vitaceae, Leeaceae and Dilleniaceae are the only angiosperm families which share the ligniﬁed endotesta and tracheidal exotegmen. The ﬁrst to ﬁnd an association between Vitaceae and Dilleniaceae were Nandi et al. (1998) in a combined rbcL/morphological analysis. In an rbcL analysis (Savolainen, Fay et al. 2000), Vitales and Dilleniaceae appear in a sister position to Caryophyllales. The two-gene analysis of Savolainen, Chase et al. (2000) and the three-gene analysis of Soltis et al. (2000) place Vitales at the base of the rosid clade. In the matK analysis of Hilu et al. (2003), the rosids are sister to Vitis and Tetracera (in turn, sister taxa) and to other taxa

Introduction to the Groups Treated in this Volume

including Berberopsidales, Santalales (relative positions were uncertain), and Caryophyllales plus asterids. In the four-gene study of Soltis et al. (2003), Vitales occupy a position at the base of a Caryophyllales/Saxifragales clade. None of these associations is strongly supported. Thus, a closer relationship between Vitaceae/Leeaceae and Dilleniaceae can not be ruled out. Perhaps both families branched off at the base of the core eudicot tree and both, but Dilleniaceae more probably than Vitaceae/Leeaceae, may be related to Caryophyllales. Evidence for placing Vitales in rosids is tenuous because the molecular data are not convincing. Note, however, that Stevens (2005), citing Oxelman et al. (2004), mentions that the RPB2 gene may not be duplicated in Vitales, perhaps suggesting a position outside core eudicots. Summarising, one may agree with Stevens (2005, on Vitales) that Vitales have no ﬁrm position as yet, although a more strongly supported association with Dillenaceae and Caryophyllales would not come as a surprise.

References Corner, E.J.H. 1976. See general references. Hilu, K.W. 2003. See general references. Nandi, O.I. et al. 1998. See general references. Oxelman, B., Yoshikawa, N., McConaughy, B.L., Luo, J., Denton, A.L., Hill, B.D. 2004. RPB2 gene phylogeny in ﬂowering plants, with particular emphasis on asterids. Mol. Phylog. Evol. 32:462–479. Savolainen, V., Chase, M.W. et al. 2000. See general references. Savolainen, V., Fay, M.F. et al. 2000. See general references. Soltis, D.E. et al. 2000. See general references. Soltis, D.E. et al. 2003. See general references. Stevens, P.F. 2005. See general references. Takhtajan, A. 1997. See general references.

Introduction to Zygophyllales 1. Hemiparasitic; stipules 0; ﬂowers solitary or in botryoid panicles, zygomorphic; the two abaxial petals lipid-secreting, the three adaxial ones forming a ﬂag; stamens ± as many as petals; ovary 1-locular; pollen 3-porate; vessels with non-vestured pits; axial parenchyma usually with one cell per strand; storying absent or nearly so; crystals many per cell, mostly in axial phloem parenchyma; n = 6. 1/18, New World Krameriaceae – Autotrophic; stipules +; ﬂowers solitary, paired or in few-ﬂowered cymes, regular or rarely slightly zygomorphic; nectar-secreting disk often +; stamens 1 or

19

2 times as many as petals; ovary (2–)5(–12)-locular; vessels with vestured pits; axial parenchyma usually with 2–4 cells per strand; storying present in axial parenchyma, sometimes in rays; crystals one per cell or septate portion of cell in wood or secondary phloem; x = 6–15. 22/230–240, in hot dry regions all over the world Zygophyllaceae

Previously, Krameriaceae and Zygophyllaceae were placed in different orders, and no close relationship between them had been recognised. Molecular studies, particularly the multigene analyses of Soltis et al. (2000) and Savolainen, Chase et al. (2000), revealed a strongly supported clade consisting of the two families within eurosids I. Ordinal status for this clade, which appears not to ﬁt in any other rosid order, was suggested by Soltis et al. (2000). Zygophyllaceae and Krameriaceae are quite diverse but have more or less pentamerous and (ob-)diplostemonous(-derived) ﬂowers, bitegmic/crassinucellate ovules, and simple styles, and thus conform to a generalised rosid pattern. They agree in various wood characters such as simple perforation plates in vessels, and the presence of tracheids (vasicentric, in the case of Zygophyllaceae), which are considered as plesiomorphous within eurosids whereas other characters, listed by Carlquist (2005) and partly included in the Conspectus above, are autapomorphous; the paedomorphic rays of Krameria are probably related to its hemiparasitism. The presence of anthraquinones may indicate their relationship to the nitrogen-ﬁxing clade (Cucurbitales, Fagales, Fabales, Rosales) where these compounds are more often found (Savolainen, Chase et al. 2000), and to which they appear close in some analyses, although with low support. Apart from the presence of harman alkaloids in both families, the remarkable diversiﬁcation of lignans and neolignans is a strong link between them (see “Phytochemistry” in family treatments) although, according to our present knowledge, these compounds in Krameriaceae are localised in the roots but in Zygophyllaceae on the leaf surface and in the wood.

References Carlquist, S. 2005. Wood anatomy of Krameriaceae with comparisons with Zygophyllaceae: phylesis, ecology and systematics. Bot. J. Linn. Soc. 149:257–270. Savolainen, V., Chase, M.W. et al. 2000. See general references. Soltis, D.E. et al. 2000. See general references. Stevens, P.F. 2005. See general references.

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Families Unassigned to Order Four families are treated in this volume which are not assigned to order: Dilleniaceae, Huaceae, Picramniaceae and Sabiaceae. By and large, they do appear related to groups contained in this volume but, currently, evidence is not sufﬁcient for including them into a speciﬁc order, and elevating them to monotypic orders does not seem appropriate because it would not convey any phylogenetic information. Apart from the following brief comments, a fuller discussion of the relationships of these families is found in the family treatments. Dilleniaceae. In the past, this family was considered a central group from which others radiated. This has not been conﬁrmed by recent phylogenetic studies. Dilleniaceae have resisted attempts of molecular studies to determine their closest relative but it seems that they have some afﬁnity with Caryophyllales. In his treatment of the family (this volume), J.W. Horn describes several important characters uniting Dilleniaceae and (woody) Caryophyllales such as Rhabdodendraceae. In the light of the internal topology of Dilleniaceae, with the genera showing anomalous secondary growth at the base of the family tree, this connection between Dilleniaceae and Caryophyllales gains weight. Molecular support for this relationship is, however, still weak (see also Introduction to Vitales, this volume).

Huaceae. This family has rare features, including the sepaline glands, cristarque cells, odour of garlic, and folds in the polar areas of the peroblate pollen grains. All existing morphology-based hypotheses for the placement of Huaceae are untenable (see family treatment, this volume), and the results of molecular studies, pointing to an association with Oxalidales/Malpighiales, have no strong support. The afﬁnity of the family remains obscure. Picramniaceae. The two genera forming this pinnate-leaved family do not show particularly striking morphological features and traditionally have been considered an aberrant element of Simaroubaceae, from which they differ in structural and chemical traits (see family treatment, this volume). Molecular data point, albeit with low support, to a position of the family either sister to all rosids or sister to Zygophyllales. Sabiaceae. This family, formerly included either in Sapindales or in Ranunculales, is now clearly placed in the early-diverging eudicots. In molecular analyses it diverges after, before, or with Proteales but the support uniting these two groups is nearly always low. The pentamerous ﬂoral structure is quite different from the stereotyped pentamerous pattern of core eudicots; it is unique within eudicots. Available molecular evidence is not sufﬁcient for an inclusion of Sabiaceae in Proteales, apart from the limited anatomical similarities between them. For further details, see treatment of Sabiaceae and Introduction to Gunnerales (this volume).

General References

Morphology, Anatomy, Embryology, Chromosomes and Palynology Behnke, H.-D. 1991. Distribution and evolution of forms and types of sieve-element plastids in the dicotyledons. Aliso 13:167–182. Carlquist, S. 2003. Wood anatomy of Aextoxicaceae and Berberidopsidaceae is compatible with their inclusion in Berberidopsidales. Syst. Bot. 28:317–325. Corner, E.J.H. 1976. The seeds of dicotyledons, 2 vols. Cambridge: Cambridge University Press. Davis, G.L. 1966. Systematic embryology of the angiosperms. New York: Wiley. Eichler, A.W. 1875–1878. Blüthendiagramme, 2 vols. Leipzig: W. Engelmann. Erdtman, G. 1952. Pollen morphology and plant taxonomy. Stockholm: Almquist & Wiksell. Fedorov, A.A. (ed.) 1969. Chromosome numbers of ﬂowering plants (in Russian). Leningrad: Nauka. Hideux, M.J., Ferguson, I.K. 1976. The stereostructure of the exine and its evolutionary signiﬁcance in Saxifragaceae sensu lato. In Ferguson, I.K., Muller, J. (eds) The evolutionary signiﬁcance of the exine. Linnean Society Symposium Series no. 1:327–378. London: Academic Press. Johri, B.M., Ambegoakar, K.B., Srivastava, P.S. 1992. Comparative embryology of angiosperms, 2 vols. Berlin Heidelberg New York: Springer. Matthews, M.L., Endress, P.K. 2005. Comparative ﬂoral structure and systematics in Crossosomatales (Crossosomataceae, Stachyuraceae, Staphyleaceae, Aphloiaceae, Geissolomataceae, Ixerbaceae, Strasburgeriaceae). Bot. J. Linn. Soc. 147:1–46. Metcalfe, C.R., Chalk, L. 1950. Anatomy of the dicotyledons, 2 vols. Oxford: Clarendon Press (2nd edn 1979 onwards). Netolitzky, F. 1926. Anatomie der Angiospermen– Samen. In: Linsbauer, K. (ed.) Handbuch der Pﬂanzenanatomie, 2. Abt., 2. Teil, vol. 10. Berlin: Borntraeger. Takhtajan, A. (ed.) 1991–2000. Anatomia seminum comparative (in Russian). Leningrad St. Petersburg: Nauka/Mir et Semja (Vol. 3: CaryophyllidaeDilleniidae; Vol. 4: Dicotyledons Dilleniidae; Vol. 5: Rosidae I; Vol. 6: Rosidae II).

Systematics and Classiﬁcation APG (Angiosperm Phylogeny Group) 1998. An ordinal classiﬁcation for the families of ﬂowering plants. Ann. Missouri Bot. Gard. 85:531–553.

APG (Angiosperm Phylogeny Group) II 2003. An update of the Angiosperm Phylogeny Group classiﬁcation for the orders and families of ﬂowering plants. Bot. J. Linn. Soc. 141:399–436. Cronquist, A. 1981. An integrated system of classiﬁcation of ﬂowering plants. New York: Columbia University Press. Cronquist, A. 1988. The evolution and classiﬁcation of ﬂowering plants, 2nd edn. Bronx, NY: New York Botanical Garden. Johnson, L.A.S., Briggs, B. 1975. On the Proteaceae – the evolution and classiﬁcation of a southern family. Bot. J. Linn. Soc. 70:83–182. Johnson, L.A.S., Briggs, B.G. 1984. Myrtales and Myrtaceae – a phylogenetic analysis. Ann. Missouri Bot. Gard. 71:700–756. Stevens, P.F. 2005. Angiosperm Phylogeny website, version 5. http://www.mobot.org/MOBOT/research/ APweb/welcome.html Takhtajan, A. 1980. Plant life, vol. 5, 1. Leningrad: Nauka. Takhtajan, A. (ed.) 1981. Plant life, vol. 5, 2. Leningrad: Nauka. Takhtajan, A. 1987. Systema Magnoliophytorum. Leningrad: Nauka. Takhtajan, A.L. (ed.) 1996. Anatomia seminum comparativa, vol. 5 (in Russian). St. Petersburg: Mir et Semja. Takhtajan, A. 1997. Diversity and classiﬁcation of ﬂowering plants. New York: Columbia University Press. Thorne, R.F. 2001. The classiﬁcation and geography of the ﬂowering plants: dicotyledons of the class Angiospermae. Bot. Rev. 66:441–647. Thorne, R.F. 2004. An updated classiﬁcation of the class Angiospermae (8/9/2004). Xeroxed and privately distributed.

Phytochemistry Bate-Smith, E.C. 1962. The phenolic constituents of plants and their taxonomic signiﬁcance. I. Dicotyledons. J. Linn. Soc. Bot. 58:95–173. Gibbs, R.D. 1974. Chemotaxonomy of ﬂowering plants, 4 vols. Montreal: McGill-Queen’s University Press. Hegnauer, R. 1962–1992. Chemotaxonomie der Pﬂanzen. Basel: Birkhaeuser (Vol. 1: 1962; Vol. 2: 1963; Vol. 3: 1964; Vol. 4: 1966; Vol. 5: 1969; Vol. 6: 1973; Vol. 7: 1986; Vol. 8: 1989; Vol. 9: 1990; Vol. 10: 1992). Nandi, O.I., Chase, M.W., Endress, P.K. 1998. A combined cladistic analysis of angiosperms using rbcL and non-molecular data. Ann. Missouri Bot. Gard. 85:137–212.

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Palaeobotany Knobloch, E., Mai, D. 1986. Monographie der Früchte und Samen in der Kreide Mitteleuropas. Rozpravy ústredního ústavu geologického svazek 47. Praha: Czechoslovachian Academy. Krutzsch, W. 1989. Paleogeography and historical phytogeography (paleochorology) in the Neophyticum. Pl. Syst. Evol. 162:5–61. Muller, J. 1981. Fossil pollen records of extant angiosperms. Bot. Rev. 47:1–142.

Molecular Systematics Albach, D.C., Soltis, P.S., Soltis, D.E., Olmstead, R.G. 2001. Phylogenetic analysis of asterids based on sequences of four genes. Ann. Missouri Bot. Gard. 88:163–212. Anderberg, A.A., Rydin, C., Källersjö, M. 2002. Phylogenetic relationships in the order Ericales s.l.: analyses of molecular data from ﬁve genes from the plastid and mitochondrial genomes. Amer. J. Bot. 89:677–687. Anderson, C.L., Bremer, K., Friis, E.M. 2005. Dating phylogenetically basal eudicots unsing rbcL sequences and multiple fossil reference points. Amer. J. Bot. 92:1737– 1748. Cameron, K.M. 2003. On the phylogenetic position of the New Caledonian endemic families Paracryphiaceae, Oncothecaceae, and Strasburgeriaceae: a comparison of molecules and morphology. Bot. Rev. 68:428–443. Chase, M.W., Soltis, D.E., Olmstead, R.G., Morgan, D., Les, D.H. and 37 others 1993. Phylogenetics of seed plants: an analysis of nucleotide sequences from the plastid gene rbcL. Ann. Missouri Bot. Gard. 80:528–580. Chase, M.W., Zmarzty, S., Lledo, M.D., Wurdack, K.J., Swensen, S.M., Fay, M.F. 2002. When in doubt, put it in Flacourtiaceae: a molecular phylogenetic analysis based on plastid rbcL DNA sequences. Kew Bull. 57:141–181. Conti, E., Litt, A., Sytsma, K.J. 1996. Circumscription of Myrtales and their relationships to other rosids: evidence from rbcL sequence data. Amer. J. Bot. 83:221–233. Conti, E., Litt, A., Wilson, P.G., Graham, S.A., Briggs, B.G., Johnson, L.A.S., Sytsma, K.J. 1997. Interfamilial relationships in Myrtales: molecular phylogeny and patterns of morphological evolution. Syst. Bot. 22:629– 647. Conti, E., Eriksson, T., Schönenberger, J., Sytsma, K.J., Baum, D.A. 2002. Early Tertiary out-of-India dispersal of Crypteroniaceae: evidence from phylogeny and molecular dating. Evolution 56:1931–1942. Davis, C.C., Webb, C.O., Wurdack, K.J., Jaramillo, C.A., Donoghue, M.J. 2005. Explosive radiation of Malpighiales supports a Mid-Cretaceous origin of modern tropical rain forests. Amer. Naturalist 165: E36–E65. Fishbein, M., Hibsch-Jetter, C., Soltis, D.E., Hufford, L. 2001. Phylogeny of Saxifragales (angiosperms, eudicots): analysis of a rapid, ancient radiation. Syst. Biol. 50:817–847.

Graham, S.A., Hall, J., Sytsma, K., Shi, S.-H. 2005. Phylogenetic analysis of the Lythraceae based on four gene regions and morphology. Intl J. Pl. Sci. 166:995– 1017. Hilu, K.W., Borsch, T., Müller, K., Soltis, D.E., Soltis, P.S., Savolainen, V. and 10 others 2003. Angiosperm phylogeny based on matK sequence information. Amer. J. Bot. 90:1758–1776. Morgan, D.R., Soltis, D.E. 1993. Phylogenetic relationships among members of Saxifragaceae sensu lato based on rbcL sequence data. Ann. Missouri Bot. Gard. 80:631–660. Price, R.A., Palmer, J.D. 1993. Phylogenetic relationships of the Geraniaceae and Geraniales from rbcL sequence comparisons. Ann. Missouri Bot. Gard. 80:661–671. Savolainen, V., Chase, M.W., Hoot, S.B., Morton, C.M., Soltis, D.E., Bayer, C., Fay, M.F., de Bruijn, A.Y., Sullivan, S., Qiu, Y.-L. 2000. Phylogenetics of ﬂowering plants based on combined analysis of plastid atpB gene sequences. Syst. Biol. 49:306–362. Savolainen, V., Fay, M.F., Albach, D.C., Backlund, A., van der Bank, M., Cameron, K.M., Johnson, S.A., Lledó, M.D., Pintaud, J.C., Powell, M., Sheahan, M.C., Soltis, D.E., Soltis, P.S., Weston, P., Whitten, W.M., Wurdack, K.J., Chase, M.W. 2000. Phylogeny of the eudicots: a nearly complete familial analysis based on rbcL gene sequences. Kew Bull. 55:257–309. Soltis, S.E., Soltis, P.S., Nickrent, D.L., Johnson, L.A., Hahn, W.J., Hoot, S.B., Sweere, J.A., Kuzoff, R.K., Kron, K.A., Chase, M.W., Swensen, S.M., Zimmer, E.A., Chaw, S.M., Gillespie, L.J., Kress, W.J., Sytsma, K.J. 1997. Angiosperm phylogeny inferred from 18S ribosomal DNA sequences. Ann. Missouri Bot. Gard. 84:1–49. Soltis, D.E., Soltis, P.S., Chase, M.W., Mort, M.E., Albach, D.C., Zanis, M., Savolainen, V., Hahn, W.H., Hoot, S.B., Fay, M.F., Axtell, M., Swensen, S.M., Prince, L.M., Kress, W.J., Nixon, K.C., Farris, J.S. 2000. Angiosperm phylogeny inferred from 18S rDNA, rbcL, and atpB sequences. Bot. J. Linn. Soc. 133:381–461. Soltis, D.E., Senters, A.E., Zanis, M.J., Kim, S., Thompson, J.D., Soltis, P.S., Ronse deCraene, L.P., Endress, P.K., Farris, J.S. 2003. Gunnerales are sister to other core eudicots: implications for the evolution of pentamery. Amer. J. Bot. 90:461–470. Soltis, D.E., Soltis, P.S., Endress, P.K., Chase, M.W. 2005. Angiosperm phylogeny, classiﬁcation, and evolution. Washington, DC: Smithsonian Institution Press. Sosa, V., Chase, M.W. 2003. Phylogenetics of Crossosomataceae based on rbcL sequence data. Syst. Bot. 28:96–105. Sytsma, K.J., Litt, A., Zjhra, M.L., Pires, C., Nepokroeff, M., Conti, E., Walker, J., Wilson, P.G. 2004. Clades, clocks and continents: historical and biogeographical analysis of Myrtaceae, Vochysiaceae and relatives in the southern hemisphere. Intl J. Pl. Sci. 165 suppl.:85– 105. Wikström, N., Savolainen, V., Chase, M.W. 2001. Evolution of the angiosperms: calibrating the family tree. Proc. Roy. Soc. London B, 268:2211–2220.

Aextoxicaceae1 Aextoxicaceae Engler & Gilg in Engler, Syllabus, ed. 8:250 (1920), nom. cons.

K. Kubitzki

Dioecious trees; twigs, the lower side of leaves, inﬂorescences and ﬂowers including the ovary covered with ferrugineous scales. Leaves alternate to subopposite, simple, entire, conduplicate and sometimes minutely peltate, pinnately veined, estipulate. Inﬂorescences racemes or botryoids usually in groups of 3 or more, branching from axils of basal prophylls, the male ones longer and more abundant than the female ones; bracts very small, rounded. Flowers (4)5(6)-merous, hypogynous, regular, enveloped in bud by a ﬁrm calyptrate bract; sepals orbicular, free, thin, strongly imbricate, caducous; petals broadly clawed, incurved in bud, oblong, with thick midrib, imbricate, persistent; male ﬂowers: stamens 5, antesepalous, alternating with well-developed ﬂeshy, reniform nectary glands; anthers dorsiﬁxed, introrse, opening by short slits towards the apex, with persistent septum between pollen sacs; gynoecium vestigial; female ﬂowers: staminodia ﬂeshy, alternating with the nectary glands; gynoecium 1-carpellate, style short, strongly deﬂexed to one side and appressed to the ovary, apically biﬁd; ovary with 2 pendulous ovules; ovules anatropous, with a long extended endostome. Fruits dry, indehiscent, oneseeded; endosperm ruminate, oily-proteinaceous; embryo well-developed, cotyledons ﬂattened, cordate-orbicular. n = 16. Monotypic, Aextoxicon punctatum Ruiz & Pav., a tree of the coastal and lake region of southern Chile and adjacent Argentina. Morphology and Anatomy. On young shoots, the far-advanced conduplicate leaf primordia appear the year before they unfold (Fig. 4). They are densely covered by stellate scales and overwinter without being enclosed in a bud. Such “naked buds” are characteristic of several trees of the humid-temperate Valdivian rainforest and are also well-developed in young shoots of Proteaceae such 1

Including personal observations by P.F. Stevens and W. Stuppy.

Fig. 4. Aextoxicaceae. Aextioxicon punctatum, “naked bud” in February (early fall), the conduplicate leaf primordia densely covered by stellate scales; note also the minute peltation. (Photograph B. Fiebig)

as Gevuina avellana (pers. obs.). In the unfolded leaves, the cover of stellate scales is restricted to the lower leaf surface. Between the scales, short glands are interspersed. The plants are strongly tanniniferous but lack ethereal oil cells. The leaves are sometimes minutely peltate; on the adaxial side, the mesophyll tissue is uninterrupted at the base. Phellogen is superﬁcial, and there are cortical sclereids, pericyclic ﬁbres, and a strikingly heterogeneous pith. Nodes are trilacunar, and the peti-

24

K. Kubitzki

ole bundle is annular, although slightly ﬂatter on the adaxial surface. Stomata are actinocyclic with 5–7 accessory cells. There are two layers of palisade tissue. Prismatic crystals, but no druses, are present in the stem, petiole and lamina, as are sclereids; in the lamina, they are quite spectacular, being as tall as about half the thickness of the blade. The wood of Aextoxicon is remarkable for its long vessel elements and tracheids (mean length 1,357 and 1,528 µm respectively), the former with perforation plates showing various degrees of pit membrane remnants and 49–84 bars per plate. Axial parenchyma is diffuse; rays are multiseriate and uniseriate, the uniseriate rays and uniseriate portions of multiseriate rays composed of upright cells, the central portion of multiseriate rays composed of markedly procumbent cells (Carlquist 2003). The morphological interpretation of the ﬁrm cover enclosing the ﬂower buds has always been contentious. Some authors thought that it might represent the fused prophylls or a transformed sepal. The latter view was favoured by Pax and Hoffmann (1917), who found cross sections of the ﬂower cover to consist of a single leaf organ. In contrast to all earlier descriptions, the ovary is 1-carpellate, not 2-carpellate. Embryology. The ovules are bitegmic and crassinucellate; the outer integument 2–3 cells thick, the inner 5–7. The endostome projects beyond the exostome. The ovules have a massive nucellar beak and numerous parietal layers (Mauritzon 1936). Several authors characterised the ovule as apotropous, which is inappropriate by deﬁnition, as the monomerous ovary has no central axis. Pollen Morphology. Pollen grains are spheroidal, tricolporate, with lalongate ora, 17 × 18 µm (Erdtman 1952). Fruit and Seed. The drupes have a coriaceous pericarp, and the endocarp cracks along two lines. The solitary seed is campylotropous, the seed coat is undifferentiated, about 6 cells thick, and tanniniferous, the endosperm is ruminate, and the embryo is slightly curved and seems to be horizontaloblique in the seed. Phytochemistry. Aextoxicon is strongly tanniniferous.

Fig. 5. Aextoxicaceae. Aextoxicon punctatum. A Flowering and fruiting branch. B Two leaves with axillary raceme. C Stellate scale. D Flower bud. E Same, calyptrate bract removed. F Male ﬂower, one petal removed. G Female ﬂower showing disk, staminodes, scaly gynoecium and deﬂexed style, petals removed. H Fruit with seed. (Drawn by M. Raspini; Dimitri 1972)

Aextoxicaceae

Afﬁnities. The position of Aextoxicon has been disputed by many authors (see, e.g. Pax and Hoffmann 1917; Takhtajan 1997), and placements in or close to Euphorbiaceae, Celastrales, Sapindales and Icacinaceae have been proposed. More recently, gene sequence analyses established a sister relationship with Berberidopsidaceae at the basis of the core eudicots (Angiosperm Phylogeny Group, APG II 2003). This is supported also by anatomical data, although these refer mostly to plesiomorphies, as emphasised by Carlquist (2003). Distribution and Habitat. Aextoxicon is member of the temperate Valdivian rainforest in Chile and adjacent border with Argentina, growing preferentially at localities with high air humidity. In coastal habitats, it is a small tree and wind-shorn shrub on dunes and rocks and, further inland in the lake region, a medium-sized tree. Aextoxicon extends from 36 to 44◦ S and, further north at about 30◦ S, has a relic occurrence in the Chilean Coastal Cordillera.

25

One monotypic genus: 1. Aextoxicon Ruiz & Pav.

Figs. 4, 5

Aextoxicon Ruiz & Pav., Prodr.: 131, t. 29 (1794).

Selected Bibliography APG II (2003). See general references. Carlquist, S. 2003. Wood anatomy of Aextoxicaceae and Berberidopsidaceae is compatible with their inclusion in Berberidopsidales. Syst. Bot. 28:317–325. Dimitri, M.J. (ed.) 1972. La región de los bosques andinopatagónicos. Buenos Aires: INTA. Erdtman, G. 1952. See general references. Mauritzon, J. 1936. Die Embryologie und systematische Abgrenzung der Reihen Terebinthales und Celastrales. Bot. Notiser 1936:161–212. Pax, F., Hoffmann, K. 1917. Systematische Stellung der Gattung Aextoxicon. Jahresber. Schles. Gesell. für vaterländ. Cultur 1916, II. Abt., Zool.-bot. Sekt.: 17–21. Radcliffe-Smith, A. 1987. Segregate families from the Euphorbiaceae. Bot. J. Linn. Soc. 94:47–66. Takhtajan, A. 1997. See general references.

Alzateaceae Alzateaceae S.A. Graham, Ann. Missouri Bot. Gard. 71:775 (1985).

S.A. Graham

Small evergreen trees or shrubs, sometimes hemiepiphytic; young stems and axes of the inﬂorescence quadrangulate. Leaves opposite or whorled, simple, entire; blades oblong-obovate or elliptical, coriaceous, glabrous, venation brochidodromous; stipules 2–a few. Inﬂorescences thyrsoidal, axillary at the ends of branches, 10–30-ﬂowered; ﬂowers actinomorphic, bisexual, barely hemi-epigynous, 5(6)-merous, apetalous or possibly petals rudimentary; ﬂoral tube campanulate; sepals valvate, thick, irregularly ﬂeshy on the adaxial surface; stamens 5, ﬂeshy, inserted below the sinus of adjacent sepals at the margin of a broad lobed nectary, ﬁlaments short with large cordate connective, the anthers dorsiﬁxed, introrse, the sporangia terminal; ovary superior, bilaterally compressed, bilocular; placentation parietal; ovules 40–60, horizontally imbricate in staggered vertical rows. Fruits bilaterally compressed dry capsules dehiscing loculicidally. Seeds ﬂattened, oblong to lunate, thin, encircled by a fragile membranous wing; embryo central, straight; endosperm 0. n = 14. A single species, Alzatea verticillata Ruiz & Pav. with two narrowly separated subspecies from Central and South America. Vegetative Anatomy. Anatomy agrees with generalized characteristics of the Myrtales but does not indicate close afﬁnities to any one family. Leaves include sclereids of the same shape as the spongy mesophyll cells; stomates are anomocytic and cyclocytic (Keating 1984). Uniquely, among the families to which Alzatea has been previously related, Alzatea has trilacunar three-trace nodes, rather than unilacunar one-trace nodes (Graham 1984). Wood anatomy (Baas 1979; Baas and Zweypfenning 1979) is characterized by diffuse vessels, solitary or in radial multiples of 2–4 with inter-vessel pits vestured and end walls oblique with simple perforations; septate ﬁbers with thin walls; very scanty paratracheal parenchyma; rays of type heterogeneous I-II, 1–3-seriate; crystals

absent. Internal phloem forms a continuous ring, and druses are abundant in chambered phloem parenchyma. Flower Structure. The ﬂeshy ﬂowers are small, 4–6 mm long. They are obhaplostemonous, a synapomorphy that unites members of the clade Alzatea + Rhynchocalycaceae + Oliniaceae + Penaeaceae (Schönenberger and Conti 2003). van Beusekom-Osinga and van Beusekom (1975) report rudimentary petals that are scarcely visible and already mucilaginous in bud, although even these are not always present (Graham, pers. obs.). The stamens are easily mistaken for petals, due to enlarged heart-shaped, pinkish connectives that are conspicuously exserted between the sepals at anthesis. Embryology. Tobe and Raven (1984) investigated the embryological development of Alzatea and compared it to that of related families. The anthers are tetrasporangiate; the endothecium and the middle layers of the anther wall degenerate early; dehiscence is accomplished by rupture of thin-walled epidermal cells. Ovules are anatropous, crassinucellate, and bitegmic. Embryo sac formation is of the bisporic Allium type, a type unknown elsewhere in the order. The archesporium is multicelled. The inner integument remains two-layered, and ultimately elongates beyond the outer integument to form the micropyle. Endosperm is probably of the Nuclear type and cotyledons are planar. Embryology of Alzatea is most similar to that of Rhynchocalycaceae, and in general agreement with other Myrtales (Tobe and Raven 1984, 1987). Pollen Morphology. Pollen grains are circular in outline, tricolporate; the ektexine bridges over a circular pore; the exine is psilate bordering the colpi, thinner and verrucate-aerolate in the mesocolpal regions, thus suggesting faint sub-

Alzateaceae

sidiary colpi; diameter 18–22 µm (Graham 1984; Patel et al. 1984; Graham et al. 1985). The external morphology of the exine is relatively generalized whereas the internal structure shares a zigzag columellar layer with Dactylocladus and Axinandra in the Crypteroniaceae (Patel et al. 1984).

27

and South America. Considered restricted to Peru and Bolivia until it was discovered in Costa Rica in 1936, subsequent discoveries in Panama in 1978 and Colombia in 1986 revealed a more continuous distribution than previously known (Silverstone-Sopkin and Graham 1986). Increased

Karyology. A haploid chromosome number of n = 14 has been counted from A. verticillata subsp. amplifolia (Almeda 1997). Given a basic number for the order Myrtales of x = 12 (Raven 1975), the basic number of Alzateaceae may have arisen from x = 12 as an ascending dysploid or alternatively, it may represent a tetraploid from an ancestral base of 7 (Almeda 1997). Clariﬁcation may come when chromosome numbers of Crypteroniaceae, considered ancestral to Alzateaceae (Schönenberger and Conti 2003), become known. Phytochemistry. Ellagic acid and ﬂavonoid mono- and di-glycosides, including quercetin 3-Oglucoside and quercetin 3-O-diglucoside, have been detected in leaves of Alzatea (Graham 1984; Graham and Averett 1984). The proﬁle is in keeping with that of the order, which is rich in ellagic acid and tannins (Hegnauer 1969). It differs from the common pattern by the absence of myricetin and C-glycoﬂavones (Graham and Averett 1984). Afﬁnities. In the past, Alzatea has been aligned with eight families in ﬁve orders, among them, Lythraceae and Crypteroniaceae in Myrtales (Lourteig 1965; van Beusekom-Osinga and van Beusekom 1975). Graham (1984) elevated Alzatea to family status after comparison of extensive non-molecular data that determined that Alzatea was distinctly separated from its nearest living relative, Rhynchocalyx. Phylogenetic analyses of cpDNA sequences from several genes and chloroplast spacer regions now afﬁrm the monophyly of Alzateaceae as a member of Myrtales in a lineage with the Southeast Asian Crypteroniaceae sister to Alzateaceae + the African families Rhynchocalycaceae, Oliniaceae, and Penaeaceae. Alzateaceae, in turn, are sister to Rhynchocalycaceae–Oliniaceae + Penaeaceae, a position supported by bootstrap values varying from ≤ 50 to 92%, depending on the analysis (Conti et al. 1997, 2002; Clausing and Renner 2001; Schönenberger and Conti 2003). Distribution and Habitats. Alzatea grows in mid- to low-montane forests along the eastern slopes of the Andes and mountains of Central

Fig. 6. Alzateaceae. Alzatea verticillata. A Flowering twig. B Flower bud. C Flower. D Disk. E Three stamens. F Transversal section of ovary. G Fruit. H Transversal section of fruit. I Seed. (Lourteig 1965)

28

S.A. Graham

collections have diminished the morphological differences between subspecies (Graham 1995). Only one genus: Alzatea Ruiz & Pav.

Fig. 6

Alzatea Ruiz & Pav., Prodr.: 40 (1794).

Description as for family.

Selected Bibliography Almeda, F. 1997. Chromosomal observations on the Alzateaceae (Myrtales). Ann. Missouri Bot. Gard. 84:305– 308. Baas, P. 1979. The anatomy of Alzatea Ruiz & Pav. (Myrtales). Acta Bot. Neerl. 28:156–158. Baas, P., Zweypfenning, R.C.V.J. 1979. Wood anatomy of the Lythraceae. Acta Bot. Neerl. 28:117–155. Clausing, G., Renner, S.S. 2001. Molecular phylogenetics of Melastomataceae and Memecylaceae: implications for character evolution. Amer. J. Bot. 88:486–498. Conti, E. et al. 1997. See general references. Conti, E. et al. 2002. See general references. Graham, S.A. 1984. Alzateaceae, a new family of Myrtales in the American Tropics. Ann. Missouri Bot. Gard. 71:757–779. Graham, S.A. 1995. Two new species in Cuphea (Lythraceae), and a note on Alzateaceae. Novon 5:272–277.

Graham, S.A., Averett, J.E. 1984. Flavonoids of Alzateaceae (Myrtales). Ann. Missouri Bot. Gard. 71:855–857. Graham, A., Nowicke, J., Skvarla, J.J., Graham, S.A., Patel, V., Lee, S. 1985. Palynology and systematics of the Lythraceae. I. Introduction and genera Adenaria through Ginoria. Amer. J. Bot. 72:1012–1031. Hegnauer, R. 1969. See general references. Keating, R.C. 1984. Leaf histology and its contribution to relationships in the Myrtales. Ann. Missouri Bot. Gard. 71:801–823. Lourteig, A. 1965. On the systematic position of Alzatea verticillata R. & P. Ann. Missouri Bot. Gard. 52:371– 378. Patel, V.C., Skvarla, J.J., Raven, P.H. 1984. Pollen characters in relation to the delimitation of Myrtales. Ann. Missouri Bot. Gard. 71:858–969. Raven, P.H. 1975. The bases of angiosperm phylogeny: cytology. Ann. Missouri Bot. Gard. 62:724–764. Schönenberger, J., Conti, E. 2003. Molecular phylogeny and ﬂoral evolution of Penaeaceae, Oliniaceae, Rhynchocalycaceae, and Alzateaceae (Myrtales). Amer. J. Bot. 90:293–309. Silverstone-Sopkin, P.A., Graham, S.A. 1986. Alzateaceae, a plant family new to Colombia. Brittonia 38:340–343. Tobe, H., Raven, P.H. 1984. The embryology and relationships of Alzatea Ruiz & Pav. (Alzateaceae, Myrtales). Ann. Missouri Bot. Gard. 71:844–852. Tobe, H., Raven, P.H. 1987. The embryology and relationships of Dactylocladus (Crypteroniaceae) and a discussion of the family. Bot. Gaz. 148:103–111. van Beusekom-Osinga, R.J., van Beusekom, C.F. 1975. Delimitation and subdivision of the Crypteroniaceae (Myrtales). Blumea 22:255–266.

Aphanopetalaceae Aphanopetalaceae Doweld, Prosyllabus tracheophytorum: XXVII (2001).

K. Kubitzki

Scrambling or viny shrubs, glabrous throughout; nodes unilacunar, 1(+ 2) trace; stems with conspicuous raised lenticels. Leaves opposite, simple, serrate to mostly entire, shortly petiolate; stipules 0 but with minute colleters at each side of the nodes. Inﬂorescences lax axillary panicles, or ﬂowers solitary; pedicels at the mid with 2 prophylls. Flowers regular, hermaphrodite, tetramerous, half-inferior; sepals largely separate, imbricate at lower level, greatly enlarged in fruit and persistent, borne in pairs at slightly different levels, their basal parts coalescing with basal portions of petals (when present) and stamens into a short ﬂoral tube which is adnate to the lower half of the ovary wall; petals minute with reduced blade or completely absent (even within the same individual); stamens 8; anthers oblong, 2-lobed at base, almost basiﬁxed, tetrasporangiate, with connective protrusion, dehiscing with longitudinal slits, latrorse-introrse; gynoecium of 4 laterally concrescent carpels; ovary one quarter- to half-inferior, 4-locular, deeply 4-furrowed, gradually tapering into a 4grooved, apically 4-lobed style with 4 canals; stigmas terminal, highly papillate; ovules 1 per locule, descending, suspended on axile placenta with long, thick funiculus, bitegmic, anatropous. Fruit nut-like, hard, 1-locular and 1-seeded, with the sepals persistent; seed hippocrepiform or reniform; embryo curved; endosperm ﬂeshy. A family comprising a single genus with two species in Australia. Anatomy and Morphology. (All data from Dickison 1980b, Dickison et al. 1994, and Dickison and Rutishauser 1990). Between the opposite leaves, small non-vascular colleters are present, which perhaps are reduced stipules. The innermost layer of the cortex is formed by a well-deﬁned endodermis. Nodes are unilacunar and the single large trace diverges to produce dorsally or laterally situated petiolar bundles. Stomata are anomocytic. The leaves are bifacial; the epidermis is uniseriate.

Dark deposits have been found in the mesophyll of both species. Leaf teeth are weakly vascularized and non-glandular. In mature stems, prominent lenticels develop on the cortex. Cork is surﬁcial. Vessels are solitary or rarely in radial multiples; vessel elements with scalariform perforation plates with 2–6 thick, fully bordered bars; ﬁbre-tracheids non-septate, thick-walled, pitted, rays homocellular, uniseriate and heterocellular, multiseriate, the latter 2–4 cells wide and composed of procumbent and upright cells. Axial parenchyma is scarce and apotrachealdiffuse. Floral Structure. Apart from the details given in the family description, information on the vascular anatomy of Aphanopetalum can be found in Dickison (1975) and Dickison et al. (1994). Pollen Morphology. Pollen of Aphanopetalum is tricolporate, prolate, fully tectate; the endoaperture is simple-diffuse; the rugulate-stellate sculpture is unique in Saxifragaceae/Cunoniaceae (Hideux and Ferguson 1976). Embryology. The anther has a ﬁbrous endothecium and a tapetum of 2–3 cells. The ovules have a long, thick funiculus, and are bitegmic and anatropous. Afﬁnities and Phylogeny. Until recently, the systematic relationships of Aphanopetalum were unclear. Hoogland (1960) and Dickison (1980b) noted that this genus was out of place in Cunoniaceae. It differs from Cunoniaceae in having unilacunar nodes and lacking stipules, and from Saxifragaceae in having opposite leaves and lacking foliar trichomes, and is unique in possessing a pronounced endodermis. However, tetramerous ﬂowers and single (or 2) ovules per carpel are known elsewhere in woody Saxifragales. This is consistent with the results of molecular studies, particularly with the topology of Fishbein et al. (2001), in which

30

K. Kubitzki

Fig. 7. Aphanopetalaceae. Aphanopetalum resinosum. A Habit. B, C Flower. D Androecium and gynoecium.

E Stamen. F Pistil. G Carpel, vertical section. (Drawing F. Bauer; Endlicher 1841)

Aphanopetalum is part of the “Haloragis clade”, which is sister to the “Saxifragaceae clade”.

Dickison, W.C. 1975. Studies on the ﬂoral anatomy of the Cunoniaceae. Amer. J. Bot. 62:433–447. Dickison, W.C. 1980a. Diverse nodal anatomy of the Cunoniaceae. Amer. J. Bot. 67:975–981. Dickison, W.C. 1980b. Comparative wood anatomy and evolution of the Cunoniaceae. Allertonia 2:281–321. Dickison, W.C., Rutishauser, R. 1990. Developmental morphology of stipules and systematics of the Cunoniaceae and presumed allies. II. Taxa without interpetiolar stipules and conclusions. Bot. Helv. 100:75–95. Dickison, W.C., Hils, H.M., Lugansky, T.W., Stern, W.L. 1994. Comparative anatomy and systematics of woody Saxifragaceae. Aphanopetalum Endl. Bot. J. Linn. Soc. 114:167–182. Endlicher, S. 1841. Iconographia generum plantarum, II, tabula 39. Wien: F. Beck. Fishbein, M. et al. 2001. See general references. Hideux, M.J., Ferguson, I.K. 1976. See general references. Hoogland, R.D. 1960. Studies in the Cunoniaceae. I. The genera Ceratopetalum, Gillbeea, Aistopetalum, and Calycomis. Austral. J. Bot. 8:318–341.

Only one genus: Aphanopetalum Endl.

Fig. 7

Aphanopetalum Endl., Gen. Pl.: 818 (1839), and Iconogr. t. 96 (1839); Bentham, Fl. Austral. 2:441–442 (1864).

Description as for family. Two species in Australia, A. resinosum Endl. in river scrubs of temperate southern Queensland and New South Wales, and A. clematideum Domin in crevices of limestone rocks in south-western Australia.

Selected Bibliography Bailey, F.M. 1990. The Queensland ﬂora. Queensland: H.J. Diddams.

Aphloiaceae Aphloiaceae Takht., Bot. Zhurn. (Moscow & Leningrad) 70:1691 (1985).

K. Kubitzki

Evergreen shrubs or slender trees, entirely glabrous. Leaves persistent, alternate, serrate or serrulate, rarely subentire, penninerved, petiolate; stipules minute, caducous. Flowers hermaphrodite, axillary, solitary or in few-ﬂowered racemes or fascicles, sweet-scented; bracts scale-like, minute; pedicels with 1–3 scaly bracteoles in the lower half; perianth uniseriate; sepals 4–5(6), white, turning yellowish, free except at the base, imbricate, orbicular, the inner 3 more membranous and petaloid; petals 0; stamens very numerous, free, inserted towards the outer edge of a glandular disk; ﬁlaments ﬁliform; anthers small, orbicular, introrse, basiﬁxed near the base; gynoecium monomerous; ovary superior, ellipsoid, sessile or shortly stipitate, 1-locular; placentation lateral with 6–8 alternating ovules in 2 rows; ovules campylotropous; stigma sessile, large, capitate-bilobed and somewhat decurrent on ventral side. Fruit a ﬂeshy, white berry with persistent perianth and about 6 obovate seeds; testa crustaceous, smooth, whitish, glossy; embryo incurved; endosperm sparse. A monogeneric family with a single polymorphic (or 8?) species in eastern and South Africa, Madagascar including the Comores, and the Mascarenes and Seychelles. Vegetative Morphology and Anatomy. Aphloia theiformis is a shrub or slender tree; the branchlets are drooping and longitudinally striate with a stronger line decurrent from a stipulate cushion. Leaves are distichous. Friedmann and Cadet (1976) observed that juvenile plants growing in xeric habitats on Réunion have pinnatisect leaves, whereas these are undivided in adult specimens. The cork is pericyclic; stomata are anisocytic; nodes are 3-lacunar (Stevens 2005). In the wood, growth rings are poorly deﬁned. The vessel elements are mostly very long (1,051–2,416 µm) and have scalariform perforation plates. Rays are unicellular with upright cells, and multiseriate heterocellular with long uniseriate extensions. Fibre-

tracheids are present, and the axial parenchyma is vasicentric and apotracheal-diffuse (Miller 1975). Reproductive Structures. van Tieghem (1899) found the vascular supply of the stamens originating from ﬁve antesepalous trunk bundles. A detailed analysis of the ﬂoral morphology and anatomy was given by Matthews and Endress (2005). The bitegmic, crassinucellate and campylotropous ovule develops into an incurved seed with a hippocrepiform embryo. The seeds are exotestal. In the mature seeds, the testa is multiplicative with several outer, strongly thickened ligniﬁed layers and the tegmen crushed (Trifonova 1992).

Fig. 8. Aphloiaceae. Aphloia theiformis. A Flowering branch. B Flower bud. C Flower. D Stamen. E Pistil, vertical section. F Same, transversal section. G Fruit. H, I Seed. (Engler 1910)

32

K. Kubitzki

Pollen Morphology. The pollen grains are spheroidal, 20–25 µm long and wide, striate, tricolporate with large, elliptical, lalongate endoapertures, the colpi diffuse, weakly costate; the exine is 1.5–2 µm thick (Keating 1973). Phytochemistry. Bate-Smith (1965) recorded mangiferin from Aphloia. Afﬁnities. Takhtajan (1987) placed Aphloiaceae in his Violales, along with Berberidopsidaceae and Flacourtiaceae. Since then, various molecular studies have recovered Aphloia together with Ixerba in association with the Crossosomatales clade (see Soltis et al. 2000; Savolainen, Fay et al. 2000; Cameron 2003). Distribution and Habitats. In submontane forest, mist forest and riverine forest, and in upland riverine bushland, 1,300–2,900 m. A single genus: Aphloia (DC.) Benn.

Fig. 8

Aphloia (DC.) Benn. in Benn. & Br., Pl. Jav. Rar. 2:192 (1838). Neumannia A. Rich. (1845).

A problematic, polymorphic species, Aphloia theiformis (Vahl) Benn., see above.

Selected Bibliography Bate-Smith, E.C. 1965. Recent progress in the chemical taxonomy of some phenolic constituents of plants. Mém. Soc. Bot. France 1965:16–28. Cameron, K.M. 2003. See general references. Engler, A. 1910. Die Pﬂanzenwelt Afrikas, 1. Leipzig: W. Engelmann. Friedmann, F., Cadet, T. 1976. Observation sur l’hétérophyllie dans les îles Mascareignes. Adansonia II, 15:423– 440. Keating, R.C. 1973. Pollen morphology and relationships of the Flacourtiaceae. Ann. Missouri Bot. Gard. 60:273– 305. Krishnan, N. 1981. Pollen morphology of some Flacourtiaceae. Proc. Ind. Acad. Sci., Pl. Sci. 90:163–168. Matthews, M.L., Endress, P.K. 2005. See general references. Miller, R.B. 1975. Systematic anatomy of the xylem and comments on the relationships of Flacourtiaceae. J. Arnold Arb. 56:20–102. Savolainen, V., Fay, M.F. et al. 2000. See general references. Soltis, D.E. et al. 2000. See general references. Stevens, P.F. 2005. See general references. Takhtajan, A. 1987. See general references. Tieghem, P. van 1899. Sur le genre Neumannia considéré comme type d’une famille nouvelle, les Neumanniacées. J. Bot. (Morot) 13:361–367. Trifonova, W.I. 1992. Aphloiaceae. In: Takhtajan, A. (ed.) Anatomia seminum comparativa, 4. St. Petersburg: Nauka, p. 80. Wild, H. 1960. Flacourtiaceae. In: Exell, A.W., Wild, H. (eds) Flora Zambesiaca 1, 1:261–298. London: Crown Agents.

Berberidopsidaceae Berberidopsidaceae A.L. Takhtajan, Bot. Zhurn. (Moscow & Leningrad) 70:1691 (1985).

K. Kubitzki

Scandent shrubs with sympodial branching and collateral axillary buds. Leaves spiral, simple, sub-3–5-pli-nerved, entire to coarsely dentate, estipulate, petioles pulvinate or not. Flowers in racemes or solitary, hypogynous, hermaphrodite (always?); pedicels with prophylls; petals welldeveloped, either distinct from sepals, or outer sepaloid tepals grading into inner petaloid ones; disk extra-staminal, persistent in fruit, or 0; stamens either in a single whorl of 6–13, or numerous and densely packed on torus; anthers (sub)basiﬁxed, dehiscing longitudinally laterointrorse; ovary 1-locular, placentas parietal, 3 or 5, ovules epitropous, 2 or more per placenta. Fruit berry-like, indehiscent, with persistent style; seeds with ﬂeshy or leathery exotesta, with chalazal arilloid (only Streptothamnus); endosperm copious, oily-proteinaceous; embryo minute. Two genera, one monotypic in Australia, the other with one species in Australia, another in Chile. Vegetative Anatomy. The leaves are hypostomatic, and the stomata are cyclocytic and surrounded by one or two rings of subsidiary cells. Other leaf anatomical features are restricted to the two species of Berberidopsis, such as the possession of 1–3-celled uniseriate hairs, druses and solitary crystals in the petiole, and sclerenchyma accompanying major leaf veins. In the c. 4 mm thick twigs of both genera, cork is not developed; growth rings are present; rays in secondary xylem are 1–multi-seriate, composed of procumbent cells, the uniseriate portions composed of upright cells; vessels are exclusively solitary and have scalariform perforations with 18–41 bars; a faint spiral thickening is present only in vessels of Berberidopsis corallina; ﬁbres have distinctly bordered pits in radial and tangential walls and are non-septate (ﬁbre-tracheids); axial parenchyma is mostly diffuse (Miller 1975; Baas 1984; Carlquist 2003).

Floral Morphology. Whereas Streptothamnus (and the closely related Aextoxicum) have cyclic pentamerous ﬂowers with persistent calyx lobes and ﬁve caducous petals, the ﬂowers of Berberidopsis are acyclic and fully spiral, with all ﬂoral organs following a regular sequence in a 2/5 pattern (Ronse De Craene 2004) and tending to appear in alternating groups of ﬁve. Pollen Morphology. Pollen grains are spheroidal to prolate and tricolpate to tricolporate, and tectate-columellate with an imperforate to microperforate tectum the sculpture of which varies from foveolate to rugulate and striate; those of Berberidopsis are 20–30 µm and of Streptothamnus smaller than 15 µm (Keating 1973, 1975; van Heel 1984). Seed. The seeds of Berberidopsidaceae have a peculiar protruding, “sausage-shaped” raphe. They are endotestal; the inner epidermis of the testa has strongly ligniﬁed pitted cells each containing a crystal. There are also indications of a less pronounced ﬁbrous exotegmen. The embryo is very small. All these features distinguish Berberidopsidaceae from Flacourtiaceae (= Salicacaceae plus Achariaceae), in which they formerly were included and the seeds of which are exotegmic and have a sarcotesta formed by the outer integument (van Heel 1979, 1984); the embryo in those families is also larger. Afﬁnities. The recognition of a second species of Berberidopsis (formerly included in Streptothamnus) by Veldkamp (1984) has prompted the anatomical studies of van Heel (1984) and Baas (1984), which have provided evidence for the restriction of the formerly more broadly circumscribed tribe Berberidopsideae to Berberidopsis and Streptothamnus. Takhtajan (1985) elevated this tribe to family rank but retained the narrowly circumscribed Berberidopsidaceae

34

K. Kubitzki

in Violales, along with Flacourtiaceae (Takhtajan 1987, 1997). Nandi et al. (1998), on the basis of a combined morphological/rbcL analysis, were the ﬁrst to suggest a relationship between Berberidospsidaceae and Aextoxicaceae – never even considered in pre-molecular times – and Carlquist (2003) pointed to the great similarities in the wood anatomy of the two families, all of which, however, are plesiomorphic. The association of Berberidospidaceae with Aextoxicaceare has received such strong molecular support that Soltis et al. (2000) and Savolainen, Fay et al. (2000) suggested that the two families be placed in the same order. A four-gene analysis of eudicots (Soltis et al. 2003) has provided a resolution of the major core eudicot lineages, in which Gunnerales and subsequently Berberidopsidales are sister to all major core eudicot lineages. However, the relation of Berberidopsidales to other core eudicots is unclear.

Ronse DeCraene (2004) analysed the spiral sequence of initiation of perianth members and stamens in Berberidopsis corallina, and found a tendency of these organs to occur in alternating groups of ﬁve which, according to him, may represent an incipient case of pentamery. At ﬁrst glance, this might appear convincing, particularly in view of the position of Berberidopsidaceae at the basis of the core eudicots above the node leading to (dimerous) Gunnerales, but it is problematic with regard to various structural aspects of the relatives of Berberidopsis, and of Berberidopsis itself. Berberidopsis has a tepaline perianth of 13–17 members whereas in Streptothamnus, which has ﬁve sepals and ﬁve petals, the androecium consists of numerous stamens which are densely packed but do not show any particular arrangement – evidently a derived condition. The paracarpous gynoecium in both genera of Berberidopsidaceae is also probably derived. These traits would hardly be expected in a group in which the transition from the spiral to the whorled condition took place quasi before our eyes, because then a less derived gynoecium structure would be expected, too. Even more pertinent seems the fact that the ﬂowers of closely related Aextoxicon, with their ﬁxed pentamery and haplostemony, are quite typically core eudicot. For these reasons, the spiral arrangement in Berberidopsis is probably a derived, rather than the original condition. Uses. Berberidospsis corallina has very showy, coral red or scarlet ﬂowers, and has been introduced into gardens in Chile and Great Britain. Key to the Genera 1. Flowers acyclic; tepals 13–17, spirally set, caducous; disk present, persistent; stamens 6–13, ﬁlaments short, connective broad, muriculate, anthers muriculate 1. Berberidopsis – Flowers cyclic; sepals 5, persistent, petals 5, caducous; disk 0; stamens numerous, ﬁlaments longer than anthers, ﬁliform, connective inconspicuous except for terminal lobe, anthers smooth 2. Streptothamnus

1. Berberidopsis Hook. f.

Fig. 9

Berberidopsis Hook. f. in Curtis, Bot. Mag. III, 18: t. 5343 (1862); Gunckel, Bol. Univ. Chile 46: 24:24–27, ﬁg. (1964); Veldkamp, Blumea 30:24–28 (1984). Fig. 9. Berberidospidaceae. Berberidopsis corallina. A Flowering branch. B Flower buds. C Androecium. D Pistil with nectary disk. E Pistil, vertically cut. (Schneider 1912)

Leaf blades ovate to hastiform, entire to coarsely dentate. Flowers solitary or in many-ﬂowered racemes; disk with as many lobes as stamens; style

Berberidopsidaceae

club-shaped with inconspicuous stigma; ovary with 3 or 5 placentae. Fruit with thin pericarp; seeds numerous; raphe a narrow, sausage-shaped lateral wing. Two species, B. beckleri (F. Muell.) Veldk., in montane rainforest of Queensland and New South Wales, Australia, and B. corallina Hook. f., in gorges by streams in the Coastal Cordillera of southern Chile from Prov. Talca to Osorno. 2. Streptothamnus F. Muell. Streptothamnus F. Muell., Fragm. Phyt. Austral. 3:27 (1862); Jessup in Fl. Australia 8:76 (1982).

Leaf blades ovate to elliptic, entire; ﬂowers solitary or in a ± leafy raceme; disk 0; anthers basiﬁxed; stigma mushroom-shaped; ovary 1-locular, placentas indistinct, probably 3. Fruit with thickish pericarp; seeds up to 25 per fruit, with median-lateral chalazal aril. One species, S. moorei F. Muell., in montane rainforest of Queensland and New South Wales, Australia, sometimes together with Berberidopsis beckleri F. Muell.

Selected Bibliography Baas, P. 1984. Vegetative anatomy and taxonomy of Berberidopsis and Streptothamnus (Flacourtiaceae). Blumea 30:39–44.

35

Carlquist, S. 2003. Wood anatomy of Aextoxicaceae and Berberidopsidaceae is compatible with their inclusion in Berberidopsidales. Syst. Bot. 28:317–325. Heel, W.A. van 1979. Flowers and fruits in Flacourtiaceae. IV. Hydnocarpus spp., Kiggelaria africana L., Casearia spp., Berberidopsis corallina Hook. f. Blumea 25:513–529. Heel, W.A. van 1984. Flowers and fruits in Flacourtiaceae. V. The seed anatomy and pollen morphology of Berberidopsis and Streptothamnus. Blumea 30:31–37. Keating, R.C. 1973. Pollen morphology and relationships of the Flacourtiaceae. Ann. Missouri Bot. Gard. 60:273–305. Keating, R.C. 1975. Trends in specialization in pollen of Flacourtiaceae with comparative observations of Cochlospermaceae and Bixaceae. Grana 15:29–49. Miller, R.B. 1975. Systematic anatomy of the xylem and comments on the relationships of the Flacourtiaceae. J. Arnold Arb. 56:20–102. Nandi, O.I. et al. 1998. See general references. Ronse DeCraene, L.P. 2004. Floral development of Berberidopsis corallina: a crucial link in the evolution of ﬂowers in the core eudicots. Ann. Bot. 94:741–751. Savolainen, V., Fay, M.F. et al. 2000. See general references. Schneider, C.K. 1912. Illustriertes Handbuch der Laubholzkunde, 2. Jena: G. Fischer. Soltis, D.E. et al. 2000. See general references. Soltis, D.E. et al. 2003. See general references. Takhtajan, A. 1987. See general references. Takhtajan, A. 1997. See general references. Veldkamp, J.F. 1984. Berberidopsis (Flacourtiaceae) in Australia. Blumea 30:21–29. Warburg, O. 1894. Flacourtiaceae. In: Engler, A., Prantl, K., Die natürlichen Pﬂanzenfamilien III, 6a. Leipzig: W. Engelmann. pp. 1–56.

Bonnetiaceae Bonnetiaceae (Bartl.) L. Beauvis. ex Nakai in Bull. Tokyo Sci. Mus. 22:25 (1948).

A.L. Weitzman, K. Kubitzki, and P.F. Stevens

More or less subpachycaulous small to mediumsized trees and shrubs. Leaves convolute, spiral, crowded towards apex of branches, with close, ascending lateral veins, margins serrulate, initially setulose, estipulate; petiole short or 0. Flowers single, or more or less cymose inﬂorescences; pedicels with 2 prophylls or several bracts; ﬂowers bisexual, cyclic; sepals 5, unequal, free, quincuncial; petals 5, contorted, free; stamens numerous; ﬁlaments slender, free, or basally connate into 5 antepetalous bundles; anthers short, basiﬁxed; fasciclode + or 0; ovary 3(–5)-locular, with numerous orderly arranged ovules on biseriate axile placentae; stylodia free or united into a branched or simple style; stigmas papillate. Fruits septicidal capsules with a persistent central column; seeds with scanty endosperm; embryo straight. Three genera and about 40 species, northern South America, West Indies, Southeast Asia, West Malesia, Moluccas and New Guinea. Vegetative Morphology and Anatomy. Bonnetiaceae are stout-stemmed shrubs or usually small trees with few branches. The smallest species, Bonnetia ahogadoi, is notable for its trailing and rooting inﬂorescence axis which also acts as a stolon (Fig. 10), whereas Ploiarium alterniﬂorum, a small, stilt-rooted tree, may grow up to 25 m high on swampy peat soil in Johore (Corner 1978). The terminal bud usually lacks scales, axillary buds are small, and branching appears to be sylleptic, although in B. ahogadoi growth of the main axis appears to be rhythmic (Steyermark 1984) and there are scales at the base of ﬂagelliform inﬂorescence shoots. The leaves remain rolled up as the bud elongates, and are more or less sessile and usually have a distinct but not very prominent midrib. The plants are completely glabrous, except for tiny colleters found in the leaf axils. The leaf margin is usually minutely serrulate and only rarely entire but, in the juvenile stage, it is always provided with minute setae which fall off during leaf expansion

but persist in the tiny, revolute leaves of Bonnetia roraimae. Archytaea and Ploiarium have vascularised, disciform structures borne immediately inside the margin and on the lower surface of the blade and in its upper one-third. Venation is often eucamptodromous, sometimes more or less brochidodromous or parallelodromous. The phellogen in the stem is surﬁcial in origin, that in the root is initiated 3 or 4 layers deep in the cortex. There are brachysclereids in the stem cortex, a sheath of ﬁbres in the pericyclic position, and groups of ﬁbres in the secondary phloem (see also van Tieghem 1885). The heartwood is dark reddish brown and heavy. Vessel elements are solitary, of medium length, and their perforations are simple/transverse; uniseriate rays are of upright cells, and multiseriates (2–4 cells wide) consist of procumbent cells with uniseriate extensions of upright cells; axial parenchyma is scanty paratracheal, and ﬁbres are mostly thick-walled. Xylem parenchyma forms an adaxial cap on the vessels. Nodes are trilacunar in Bonnetia, unilacunar in Archytaea and Ploiarium. The separate traces are visible in leaf scars although, in taxa such as Bonnetia ahogadai, traces are more or less conﬂuent in the outer part of the cortex. Ploiarium has an arcuate midrib bundle, that of other taxa is more complex, the tissue on the adaxial side in particular being irregularly arranged. Vascular bundles are embedded, and the marginal setae of Archytaea and Ploiarium, but not those of Bonnetia, are associated with vascular tissue. Stomata are anomocytic and an adaxial hypodermis is sometimes present. The leaf anatomy of Bonnetia is remarkable: the epidermis is often mucilaginous and its cells bulge and intrude between the mesophyll cells; foliar sclereids are widespread in the mesophyll; and the leaf midrib and all veins including the terminal veinlets are surrounded by an endodermis of thin-walled cells provided with Casparian strips (Maguire 1972; Dickison and Weitzman 1996; Weitzman and Stevens 1997).

Bonnetiaceae

Inﬂorescence and Flowers. Inﬂorescences are lateral, and several species appear to have axillary ﬂowers. However, these are probably reduced inﬂorescences, and the “pedicels” bear 2–several bracts along their length, sometimes very close to the calyx. The sepals of Bonnetia, and perhaps also Ploiarium, are terminated by setae very like those found on the leaf margins. The petals are predominantly white or pink. Whether or not the androecium of Bonnetia is fasciculate needs study; fascicles have been reported (e.g. Steyermark 1984) but their existence – at least, as evident in later bud or ﬂower – has been questioned (Kobuski 1948; PFS, pers. obs.). It is not known if the fasciclodes of Ploiarium secrete nectar; otherwise, there are no reports of nectar from the family (Dickison and Weitzman 1998). Pollen Morphology. Pollen is 28 to almost 60 µm long, oblate-spheroidal, tricolporate with wide colpi and circular ora. Sometimes, as in B. lancifolia, the colpi are fused at the poles, leaving a triangular polar space. There are costal colpi in Archytaea and Ploiarium, and all taxa have costal pori. The nexine, 0.5–4 µm thick, is thicker than the sexine, which is ﬁnely reticulate (Erdtman 1952; Maguire 1972; Steyermark 1984; Salgado-Laboriau and Villar de Seoane 1992). Seed. The seeds are quite small, and Corner (1976) suggested that the seed coat of Ploiarium is probably endotestal, although its development has not been studied. Exotestal cells are thin-walled and polygonal, endotestal cells are usually isodiametric, low, and with sinuous anticlinal walls, ligniﬁcation is extensive and there are numerous narrow plasmodesmata. Ploiarium alternifolium has rather elongated endotestal cells, and the anticlinal walls of those of Archytaea are almost straight. There is a thin, persistent layer of endoperm surrounding the straight embryo. Although the cotyledons are generally small, those of Bonnetia range from 1/2–1/6 the length of the embryo. Germination is epigeal (Ploiarium). Phytochemistry. Bonnetiaceae are rich in xanthones with various substitution patterns, and bixanthones and anthraquinone xanthones have been reported from Ploiarium (Kubitzki et al. 1978; Bennett et al. 1990). Xanthones are also richly diversiﬁed in Clusiaceae and Hypericaceae (Bennett and Lee 1989).

37

Family Circumscription and Afﬁnities. When the exudate-producing genus Neotatea and the anther gland-bearing genera around Kielmeyera and Caraipa are removed from Bonnetiaceae, as suggested by Weitzman and Stevens (1997), the family becomes very homogeneous. Although in the past members of the family have been included in the “intermediate” zone between Theaceae and Clusiaceae/Hypericaceae, the former are now in Ericales, and possession of xanthones, ﬂoral morphology, testa anatomy, etc., all link Bonnetiaceae with Clusiaceae/Hypericaceae. The combination of characters of wood anatomical characters presented above sets Bonnetiaceae apart from Theaceae, with which Baretta-Kuipers (1976) compared them, and also Guttiferae and Hypericaceae. Gene sequence analyses by Savolainen, Fay et al. (2000) and Gustafsson et al. (2002) conﬁrm the close relationship of Bonnetiaceae with Clusiaceae/Hypericaceae. The inclusion of Ploiarium in Malvales (Savolainen, Fay et al. 2000) was probably due to a mistaken identiﬁcation, since i.a. the distinctive seed coat anatomy of Archytaea is quite unlike that of Malvales. Elatinaceae have also often been considered as possibly related to Bonnetiaceae, agreeing in testa anatomy and a number of other features, but molecular data place them sister to Malpighiaceae (Davis and Chase 2004); whether or not that family is close to Bonnetiaceae, etc., is unclear. Distribution and Habitats. The two closely related, small genera Archytaea and Ploiarium are disjunct between Southeast Asia/Malesia and northern South America, whereas Bonnetia is restricted to continental South America, with one species on Cuba. Archytaea prefers open habitats, often by creeks, always on nutrient-poor soil, ranging from lowland to mid-altitudes. Bonnetia is most speciose in the Guayana Highland and its surroundings, where 27 species are found, all but one (B. paniculata) of which are endemic to this region. Most of them have only a limited altitudinal range, with the majority preferring the mesothermic/submicrothermic belt (1,200–2,700 m; Huber 1988), but Bonnetia crassa spans a belt of 2,000 m. With increasing altitude, the bonnetias tend to be of lower stature. Bonnetia ahogadoi is a low shrublet growing at localized sites on peat in rock depressions of the Chimatá Massif in Venezuela

38

A.L. Weitzman, K. Kubitzki, and P.F. Stevens

Fig. 10. Bonnetiaceae. Bonnetia ahogadoi. A Habit. B Leaf. C Flower. D Androecium and gynoecium. E Anther. F Ovary, transversal section. G Capsule at beginning of dehiscence.

H Two valves of dehiscent capsule with adherent seeds and persistent columella. I Seeds, various positions. (Drawing by B. Manara; Steyermark 1984)

at an altitude of about 2,100 m (Huber 1992). Ploiarium grows in the lowland, often close to the sea, and on swampy peaty soil (Corner 1978) or on nutrient-poor white sand in the heath forests of Borneo.

Genera of Bonnetiaceae

Uses. The wood is durable and in Asia/Malesia locally used for constructions, but is not a commercial timber.

Key to the Genera 1. Androecium not fasciculate; ovary 3(4)-locular 3. Bonnetia – Androecium 5-fasciculate; ovary 5-locular 2 2. Flowers in 3–many-ﬂowered inﬂorescences; sepals and stamens caducous; style simple 2. Archytaea – Flowers solitary; sepals and stamens persistent; stylodia 5, free to base 1. Ploiarium

1. Ploiarium Korthals Ploiarium Korthals, Verh. Nat. Gesch. Bot., ed. Temminck: 135 (1840); Kobuski, J. Arnold Arb. 31:196–207 (1950), rev.

Trees, sometimes vast, or shrubs. Flowers solitary; pedicels ancipitous, increasing in diameter towards apex; sepals caducous; nectary glands 5, alternating with petals; stamens numerous, caducous, in 5 antesepalous fascicles; ovary 5-locular; stylodia 5, free to base, persistent. Capsule dehiscing from the base; seeds linear; endosperm ﬂeshy. Three species, from Cambodia through Malay Peninsula to Sumatra, Borneo and Halmahera. 2. Archytaea Mart. Archytaea Mart. in Mart. & Zucc., Nov. Gen. Sp. Pl. 1:116 (1826); Weitzman & Stevens, BioLlania Esp. 6:556–557 (1997); Weitzman, Fl. Venez. Guayana 9:310–313 (2005).

Bonnetiaceae

Small trees or shrubs. Inﬂorescences axillary, 3– many-ﬂowered; peduncles ancipitous, increasing in diameter towards apex; pedicels midway with prophylls; sepals persistent; nectary glands 5, alternate with petals; stamens numerous, persistent, in 5 antesepalous fascicles; ovary 5-locular; style simple, persistent. Seeds numerous, linear, imbricate, exalbuminous. Two species, in the Guayana sandstone region and adjacent lowlands of northern South America. 3. Bonnetia Mart.

Fig. 10

Bonnetia Mart. in Mart. & Zucc., Nov. Gen. Sp. Pl. 1:114 (1826), nom. cons.; Kobuski, J. Arnold Arb. 29:393–413 (1948), rev.; Weitzman, Fl. Venez. Guayana 9:313–324 (2005). Neblinaria Maguire (1972). Neogleasonia Maguire (1972) except N. duidae (Kobuski & Steyerm.) Maguire Acopanea Steyerm. (1984).

Trees or shrubs. Flowers solitary or up to three on axillary peduncles or occasionally arranged in loose panicles with ancipitous or terete peduncles; sepals persistent; stamens very numerous, persistent, the ﬁlaments adnate to the base of the ovary and otherwise free; anthers dehiscing longitudinally or by two pores at the base; ovary 3(4)-celled; stylodia 3, or style simple and then sometimes apically branched. Seeds linear, elongated above and below into a small membranous wing. About 29 species, mainly in the Guayana highland and adjacent regions, with B. paniculata Spr. ex Benth. extending along the Andes to Peru, B. stricta (Nees) Nees & Mart. along the Atlantic coast southwards to Rio de Janeiro, and B. cubensis (Britton) Howard in Cuba.

Selected Bibliography Baretta-Kuipers, T. 1976. Comparative wood anatomy of Bonnetiaceae, Theaceae and Guttiferae. In: Baas, P., Bolton, A.M., Catling, D.M. (eds) Wood structure in biological and technological research. Leiden Botanical Series 3, pp. 76–101.

39

Bennett, G.J., Lee, H.-H. 1989. Xanthones from Guttiferae. Phytochemistry 28:967–998. Bennett, G.J., Lee, H.-H., Lowrey, T.K. 1990. Novel metabolites from Ploiarium alternifolium: a bixanthone and two anthraquinolyxanthones. Tetrahedron Lett. 31:751–754. Corner, E.J.H. 1976. See general references. Corner, E.J.H. 1978. The freshwater swamp-forest of South Johore and Singapore. Gard. Bull. suppl. 1. Singapore: Government Printers. Davis, C.C., Chase, M.W. 2004. Elatinaceae are sister to Malpighiaceae, and Peridiscaceae are members of Saxifragales. Amer. J. Bot. 91:262–273. Dickison, W.C., Weitzman, A.L. 1996. Comparative anatomy of the young stem, node and leaf of Bonnetiaceae, including observations on a foliar endodermis. Amer. J. Bot. 83:405–418. Dickison, W.C., Weitzman, A.L. 1998. Floral morphology and anatomy of Bonnetiaceae. J. Torrey Bot. Soc. 125:268–286. Erdtman, G. 1952. See general references. Gustafsson, M.H.G., Bittrich, V., Stevens, P.F. 2002. Phylogeny of Clusiaceae based on rbcL sequences. Intl J. Pl. Sci. 163:1045–1054. Huber, O. 1988. Guayana highlands versus Guayana lowlands, a reappraisal. Taxon 37:595–614. Huber, O. 1992. La vegetación. In: Huber, O. (ed.) El macizo de Chimatá. Caracas: Todtmann, pp. 161–177. Kobuski, C.E. 1948. Studies in the Theaceae, XVII. A review of the genus Bonnetia. J. Arnold Arb. 29:393–413. Kubitzki, K., Mesquita, A.A.L., Gottlieb, O.R. 1978. Chemosystematic implications of xanthones in Bonnetia and Archytaea. Biochem. Syst. Ecol. 6:185–187. Maguire, B. 1972. Bonnetiaceae. In: The Botany of the Guyana Highland. Part IX. Mem. New York Bot. Gard. 23:131–165. Prakash, N., Lau, Y.Y. 1976. Morphology of Ploiarium alternifolium and the taxonomic position of Ploiarium. Bot. Notiser 129:279–285. Salgado-Laboriau, M.L., Villar de Seoane, L. 1992. Contribución a la ﬂora polínica de los tepuyes. In: Huber, O. (ed.) El macizo de Chimatá. Caracas: Todtmann, pp. 219–236. Savolainen, V., Fay, M.F. et al. 2000. See general references. Steyermark, J.A., 1984. Theaceae (Bonnetiaceae), pp. 323– 330. In: Flora of the Venezuelan Guayana, I. Ann. Missouri Bot. Gard. 71:297–340. van Tieghem, Ph. 1885. Second mémoire sur les canaux sécréteurs des plantes. Ann. Sci. Nat. VII, Bot. 1:5–96; see particularly Ternstroemiacées, pp. 43–46. Weitzman, A.L., Stevens, P.F. 1997. Notes on the circumscription of Bonnetiaceae and Clusiaceae, with taxa and new combinations. BioLlania Edic. Esp. 6:661– 564.

Buxaceae Buxaceae Dumort., Comment. Bot.: 54 (1822), nom. cons.

E. Köhler

Evergreen shrubs or trees, rarely subshrubs or rhizomatous perennial herbs, glabrous, sometimes with uni- or multicellular hairs, monoecious, rarely dioecious. Leaves alternate or decussate, petiolate, rarely sessile, entire, rarely dentate, pinnately veined, less often tripliveined, estipulate. Flowers in axillary or terminal botryoids or spikes, the male above the female ones, or one female above the male, subtended by decurrent bracts, the female with prophylls. Flowers actinomorphic, hypogynous; male: tepals 4, decussate, rarely wanting; stamens free, 4, 6 or 8, antetepalous, or rarely up to 45 in a more complex arrangement, if 6, then two pairs opposite the inner tepals, often inserted around a pistillode; anthers dorsiﬁxed, dithecal, tetrasporangiate, longitudinally dehiscent, borne on long ﬁlaments, rarely sessile; pistillode present or wanting; female: often larger than the male, fewer or solitary; tepals 4–6; ovary syncarpous with free stylodia, (2)3(4)-carpellate, sometimes with false septa; placentation axile; stylodia subulate, divergent, rarely connate at the base, stigmatic area decurrent along the ventral fold; ovules usually 2 per locule, anatropous. Fruit a dry capsule with persistent stylodia, loculicidally dehiscent into 2-horned valves, or indehiscent, subdrupaceous or berry-like. Seeds black or dark, frequently carunculate; endosperm copious, ﬂeshy, oily; embryo straight, cotyledons ﬂat. A family comprising 5 genera with c. 100 species, distributed in the Northern Hemisphere of the Old and New World, extending to Andean South America and its Caribbean coast, to South Africa and Madagascar, and to peninsular Malaysia. Vegetative Morphology. Most Buxaceae are evergreen shrubs or trees up to 15 m tall. Only Pachysandra comprises erect or prostrate subshrubs and perennial herbs. Its sympodial rhizomes have adventitious roots and develop simple or sympodially branched stems with alternate, apically clustered leaves. The leaves are alternate in

Styloceras, Sarcococca and Pachysandra, decussate in Buxus and Notobuxus, where decurrent leaf bases form lateral internodal folds (Fig. 12A). In some Cuban Buxus, distichous leaves are interspersed with decussate pairs of very small ones inserted on short shoots. The leaves are usually entire but toothed in Pachysandra. Brochidodromous venation, occurring in Sarcococca, Notobuxus and Buxus, and variously modiﬁed in the latter, is regarded as basic. Styloceras and Asian Buxus species possess eucamptodromous venation. Cladodromous patterns are found in South African and Malagasy Buxus; Pachysandra has craspedodromous venation. Whereas the brochidodromous type prevails in the tropics, the derived patterns occur in subtropical and temperate regions of both hemispheres (Köhler 1993). Species of Buxus possess a grey, deeply ﬁssured bark. Vegetative Anatomy. Old World Buxus and Notobuxus species have a cortical vascular bundle in each angle of the branchlets, accompanied by ﬁbre strands in the Eurasian taxa. Both are wanting in New World Buxus and the remaining genera (van Tieghem 1897; Mathou 1940). Elongated ﬁbres and large stone cells are frequent in the primary cortex. Chains of small, irregularly thickened sclereids with oxalate crystals, surrounding a larger ﬁbre (‘Kristallkammerfasern’), occur in Pachysandra, Sarcococca and Styloceras. Secretory cells, often arranged in longitudinal rows, are frequent in Buxus, Pachysandra and Sarcococca, less prominent in Styloceras (Metcalfe and Chalk 1950). Vessels are mostly solitary and of small diameter, rather wide in Styloceras. They are of medium length in Buxus and Notobuxus but exceptionally long in Sarcococca and Styloceras, reﬂecting a continuous occupation of mesic sites (Carlquist 1982). They have scalariform perforations with a great range of numbers of bars (Köhler, unpubl. data). The ﬁbrous elements are tracheids with bordered

Buxaceae

pits similar to vessels. The axial parenchyma is diffuse apotracheal throughout the family. Uniseriate rays are as frequent as multiseriate ones. The heterogeneous rays of Styloceras, which are up to four cells wide, are most primitive. Styloceras is an unspecialized, highly mesic type, followed by Sarcococca, whereas Notobuxus and especially Buxus are more specialized in adaptation to xeric conditions. The sieve element plastids represent a speciﬁc subtype, PVIc, with a globose protein crystal (Behnke 1982). Leaf epidermis cells are thin to strongly cutinized in Buxus, and covered with epicuticular waxes. Their anticlinal walls are sometimes extremely thickened, conﬁning lumina to a central canal or basal rests in Cuban Buxus (Köhler and Schirarend 1989). The indumentum comprises thick-walled hairs of one to several cells. Stomata are usually abaxial and are laterocytic, occasionally cyclocytic (Baranova 1980); they have prominent outer ledges which sometimes bear a peristomal rim. A hypodermis is present only in Styloceras. The mesophyll contains prominent secretory cells, which sometimes form a continuous hypodermal layer and may be interspersed with brachy- , osteoor astrosclereids. Druses and solitary oxalate crystals are frequent; cells with coarse crystal sand are rarer. The vascular bundles are accompanied by arc-shaped or ring-like sclerenchymatous sheaths. The petiole is supplied by a median and two lateral bundles, the latter being replaced by ﬁbre strands in Eurasian Buxus. The nodes are unilocular with one trace. Inﬂorescence Structure. Inﬂorescences are axillary or terminal, rarely borne at the base of the stem (Pachysandra procumbens), and shortly pedunculate or sessile. In Buxus, Notobuxus and Styloceras kunthianum, they are usually botryoids with lateral male ﬂowers and a terminal female ﬂower. Pachysandra and some Sarcococca have open spikes with lateral male ﬂowers in the upper part of the inﬂorescence and female ﬂowers below. In the dioecious species of Styloceras, male ﬂowers form long spikes sometimes terminated by a peloric ﬂower; female ﬂowers are solitary or in thyrses (von Balthazar and Endress 2002b). Flower Structure. The bracts preceding the reproductive organs of male ﬂowers are always arranged in a decussate pattern whereas the uppermost four, bract-like phyllomes are tepal-like and inconspicuous or whitish (Sarcococca) and creamy

41

petaloid (Buxus). There are typically four stamens, in Notobuxus six or up to ten; in Styloceras, they are numerous. Filaments are long-exserted, stout, sometimes clavate. Anthers are introrse, dorsiﬁxed with a protruding, ± coloured connective tip. The stamens are frequently inserted around a pistillode, which is quadrangular to 4-lobed, sometimes truncate in Buxus and Pachysandra or urceolate in Sarcococca, but very reduced in Notobuxus and absent in Styloceras. It possesses a nectariferous structure (Daumann 1974; Vogel 1998). In the female ﬂowers the carpels are usually preceded by a pair of prophylls and several spirally arranged bracts which are only weakly differentiated towards tepals (von Balthazar and Endress 2002b). The locules of the ovary contain two collateral ovules and are separated by spurious septa in Pachysandra and Styloceras. The stylodia are rather long, slender and recurved in Styloceras, erectsubulate in Pachysandra, more stout in Sarcococca, and short-divergent in Notobuxus and Buxus. Protuberances between the bases of the stylodia function as nectaries and are considered to be of androecial derivation (Daumann 1974). Embryology. The anther wall has a 1-layered ﬁbrous endothecium. The tapetum is secretory and its cells become binucleate. Pollen meiosis is simultaneous, resulting in tetrahedral or isobilateral tetrads. Pollen is 2-celled when shed (Davis 1966). The ovules are anatropous, pendulous, with the micropyle towards the axis in Buxus and Notobuxus or averted in Sarcococca. They are bitegmic, crassinucellate with a pronounced nucellar cap; the micropyle is made up by the inner integument (Wunderlich 1967; Corner 1976). Protuberances of the placenta form an obturator in Pachysandra. A proliferation of the outer integument, forming a hood over the nucellus, develops a prominent caruncle in the latter (Channel and Wood 1987). The megaspores are arranged in linear (Sarcococca, Pachysandra) or T-shaped tetrads (Buxus and Notobuxus), the chalazal one developing into a Polygonum type embryo sac. The synergids have a ﬁliform apparatus. The antipodes persist into postfertilization stages and a small degree of secondary multiplication has been reported. Endosperm formation is cellular, but nuclear in Sarcococca (Wiger 1935). Embryogeny follows the Onagrad type. Occasionally, parthenocarpy has been reported for Buxus, and some Sarcococca species seem to be obligate apomicts (Naumova 1980). Nucellar polyembryogeny is recorded for S. humilis.

42

E. Köhler

Pollen Morphology. Pollen grains are ± spheroidal and vary in the size range 20–50 µm. Apertures range from 3-colporate in Notobuxus to 3–7-colporate, 5–12-pantocolporate and 12–40pantoporate in Buxus (Fig. 11A–C), whereas only pantoporate grains occur in Sarcococca, Pachysandra and Styloceras (Köhler 1981; Köhler and Brückner 1982). The colpi of Buxus pollen contain 3–6 circular ora, the number of ora decreasing in pantocolporate forms (Fig. 11B), eventually giving

rise to pantoporate grains (Fig. 11C). The pores are roundish with sculptured membranes (Brückner 1993), which also occur in Styloceras. The exine sculpture, providing taxonomically signiﬁcant characters in Buxus and Notobuxus, comprises comparatively free, interlaced ridges and a coarse or ﬁne reticulum, which sometimes bears small spinulae. Others have supratectal pilate-verrucate elements. The exine of Styloceras is ﬁnely reticulate with pointed spinulae and, in Sarcococca and

Fig. 11. Buxaceae, pollen grains. A Buxus arborea, tricolpo4-orate grain showing one colpus, ×3,500. B Buxus benguellensis, pantocolpo-2-orate grain, ×2,700. C Buxus

cochinchinensis, pantoporate grain, ×2,600. D Sarcococca wallichii, pantoporate grain with crotonoid exine pattern, ×1,800. (Orig. Köhler)

Buxaceae

Pachysandra, a ‘crotonoid’ pattern is observed with reticulately arranged triangular and linear units based on a ledge, which is supported by bacula (Fig. 11D). Karyology. Chromosome numbers of the family are mainly multiples of x = 7 (Hans 1973). With the exception of a tetraploid record for Buxus sinica (Huang et al. 1986), the Eurasian and New World species of Buxus share 2n = 28 (Köhler, unpubl. data). For Sarcococca, diploids with 2n = 28 (less frequently, tetraploids) are recorded. An aberrant number of n = 12 is given by Singh et al. (1982). In Pachysandra, a wider range with n = 12, 13, 24, 27 is found (Raven 1975; Kurosawa 1981). Notobuxus diverges with 2n = 20. Pollination and Reproductive System. (See also the summary by von Balthazar and Endress 2002a). In male ﬂowers of Buxus, Sarcococca and Pachysandra and, perhaps, also of Notobuxus, rudiments of a pistil are present but the ﬂowers are functionally unisexual. In female ﬂowers, no rudiments of stamens are found. The mixed inﬂorescences of Buxus, Sarcococca and Pachysandra are protogynous. Self-fertility is reported for Pachysandra procumbens by Robbins (1962). Since the tepals are commonly inconspicuous, pollinator attraction is by other ﬂoral parts. Sarcococca and Pachysandra have showy tepals with white ﬁlaments and red or yellow anthers; the ﬁlaments emit a strong, sweet scent. In the centre of the male ﬂowers of Sarcococca and Pachysandra, a nectary is present but, in their female ﬂowers, attractants are lacking. Pollination depends on the strict foraging behaviour of insect visitors, which always move from the base to the apex of the inﬂorescence and thereby inadvertently touch the female ﬂowers (Vogel 1998). The ﬂowers in many Buxus attract bees and ﬂies by a faint scent, and nectar is produced by the pistillode in male ﬂowers or on nectariferous structures between the carpels in the female ﬂowers (Fig. 12C). In African Buxus and the closely related Notobuxus, no nectariferous pistillodes nor pistils are found, and wind pollination was suggested for these species (Vogel 1998), which would be compatible with their increased number of stamens, although the pollen is well-sculptured and does not suggest wind pollination (Köhler and Brückner 1982). Fruit and Seed. The fruit of Buxus and Notobuxus is a dry, loculicidal capsule with leathery exocarp and persistent stylodia, dehiscing basipetally

43

into three spreading, 2-horned valves. The detached cartilaginous endocarp partly encloses both seeds and ejects them forcibly. In Pachysandra, transitions from indehiscent capsules to subdrupaceous white and pulpy fruits occur. In Sarcococca and Styloceras, the fruit is sub- to fully drupaceous, with a pulpy mesocarp and a thin crustaceous endocarp in the former, and a cartilaginous endocarp divided in 4–6 pyrenes in the latter. The seeds are oblong, trigonal, with a smooth, shining black, brown or blue coat. The raphe is scarcely discernible, showing a slight postchalazal ramiﬁcation of bundles in Buxus. There is a caruncle, rather prominent in Pachysandra, and reduced to two small, white lobes on either side of the micropyle in Buxus. Seeds of Sarcococca and Styloceras are ecarunculate. The family has an exomesotestal seed coat, with a multiplicative testa in Sarcococca and Pachysandra but not in Buxus. These genera share a palisade of thick-walled, prismatic cells in the outer epidermis, followed by crushed parenchymatous cells (Melikian 1968). In Buxus, the inner epidermis is shortly palisadic and ligniﬁed at the micropyle, forming a false endostome (Corner 1976). The embryo is slightly curved with a long radicle in Buxus, but straight with a short radicle in Sarcococca. The cotyledons are thin and ﬂat and the endosperm is ﬂeshy and oily. Dispersal. The ejection mechanism of Buxus and Notobuxus may sufﬁce for localized seed dispersal; abiotic agents such as rain or ﬂowing water may account for dispersal over larger distances. The caruncle is related to ant dispersal, which has been observed in B. sempervirens and is likely to act also in Pachysandra procumbens, where the carunculate seeds are released on the ground. The drupaceous fruits of Sarcococca and Pachysandra terminalis are indicative of endozoochory, probably by birds. This seems to be true also for Styloceras, where the tardily dehiscing fruit exposes a gelatinous pulp surrounding the blue seeds (Gentry and Foster 1981). Phytochemistry. Buxus, Sarcococca and Pachysandra contain a series of highly elaborated steroidal alkaloids of the aminopregnan type, which are derived from triterpenoids (Hegnauer 1964, 1989) and are shared with Didymelaceae. More than 150 alkaloids, mainly pregnan and irehdiamine derivatives, have been isolated from Buxus, Sarcococca and Pachysandra, whereas those of Styloceras are unknown. Condensed tannins

44

E. Köhler

have been found in some Buxus but are not prominent. Seventeen Cuban Buxus species have been recognized as nickel-hyperaccumulators, reaching nickel contents of 1,000 to 25,000 µg g−1 dry weight (Reeves et al. 1996), which might be of taxonomic interest. Relationships Within the Family. Two major clades can be recognized within the family (von Balthazar and Endress 2000, 2002a), one comprising Pachysandra, Sarcococcus and Styloceras, and another of Buxus with Notobuxus. Pachysandra and Sarcococcus are strongly supported as monophyletic groups in a sister relationship to Styloceras. American and Eurasian Buxus each represent a strongly supported clade, with Notobuxus embedded among the African members of Buxus. von Balthazar and Endress (2002a) suggest either to sink Notobuxus in Buxus, or to keep Notobuxus at generic level and integrate all African Buxus in this genus. Shared characters among Sarcococcus, Pachysandra and Styloceras include the occurrence of two (rarely three) carpels, the lack of interstylar nectaries, a micropyle formed by both integuments, attractive stamens in male ﬂowers, and ﬂeshy fruits. In addition, Styloceras and Pachysandra share a secondary partition of the ovary. Notobuxus shares with Buxus a similar inﬂorescence and perianth structure, 3-carpellate female ﬂowers, interstylodial nectaries, micropyles formed by the inner integument, rudimentary arils, and capsular fruits; in male ﬂowers, stamens are sessile and the pistillode is lacking in some species (von Balthazar and Endress 2002a). Afﬁnities. Until very recently, the phylogenetic position of Buxaceae has remained problematic (see Webster 1987 and Jarvis 1989 for reviews). The family has frequently been associated with Euphorbiaceae and also Celastrales, but Hamamelidales and Pittosporales have also been considered. Recent morphological, molecular and combined data analyses (Nandi et al. 1998; Soltis et al. 2000, 2003; The Angiosperm Phylogeny Group, APG II 2003) place Buxaceae as sister to Didymelaceae (Buxales) together with Ranunculales, Sabiaceae, Proteales and Trochodendraceae in a grade at the base of the eudicots. Palaeobotany. Early fossil records (Spanomera) from the Albian/Cenomanian of the Potomac

Group are closely related to Buxaceae (Drinnan et al. 1991). Among fossil pollen attributable to Buxaceae, the ‘crotonoid’ Pachysandra-Sarcococca type appeared initially in the Upper Cretaceous of central Europe and, in the Palaeogene, subsequently extended westwards and then eastwards along the north-Tethyan warm-temperate vegetation belt; by the Miocene, it had arrived in East Asia (Krutzsch 1989). Macrofossils of Pachysandra are known from the Upper Eocene and of Sarcococca from the Upper Oligocene/Miocene of central Europe (Mai and Walther 1985). Colporate Buxus pollen is known from the Lower Eocene (Kedves 1962), followed by a succession of types (Bessedik 1983) which document the coherence with pantoporate Buxus pollen of the Lower Miocene (Krutzsch 1966). Fruits and leaf remains of Buxus with Eurasian-type venation have been found in the Miocene of Bohemia (Kvacek et al. 1982) and the Oligocene of East Asia (Uemura 1979). Styloceras pollen is recorded from the Eocene of Argentina and the Pliocene of Colombia (van der Hammen 1974). Distribution and Habitats. The genus Buxus has a disjunct intercontinental distribution with a centre of diversity in tropical to temperate East Asia and another in the Caribbean, whereas only few species, including the most primitive taxa, occur in Africa from Ethiopia to the eastern Cape in South Africa and in Madagascar. The genus has a wide ecological range and grows in dry scrub forests, on limestone cliffs, in the understorey of montane rainforests, occasionally in cloud forests, sometimes above 3,000 m; it frequently grows on ultramaﬁc soils. Notobuxus has a scattered distribution in coastal forests between Kenya and the eastern Cape, and in equatorial forests from Sierra Leone to Nigeria. Sarcococca is widely distributed in tropical and subtropical Asia from Afghanistan to China, Indonesia and the Philippines, growing in the understorey of montane forests, often at higher altitudes. A single New World species occurs in Guatemala. Three species of Pachysandra are native to China, Japan and Taiwan, and one to south-eastern North America, growing in rich mesophytic forests in mountain regions. Species of Styloceras are conﬁned to the Andes of South America from Venezuela to Bolivia, growing in forests between 2,500 and 3,800 m. A recently discovered species from Amazonian Peru suggests that the genus may be an old lowland forest element (Gentry and Foster 1981).

Buxaceae

45

3. Male ﬂowers with 4 stamens opposite the tepals, longexserted; pistillode present 1. Buxus – Male ﬂowers with 6(–10) stamens, two pairs opposite the inner tepals; anthers sessile; pistillode as a ﬂat disk, or absent 2. Notobuxus 4. Woody shrubs or small trees with entire leaves; fruit ± drupaceous 3. Sarcococca – Perennial herbs with procumbent stems, leaves ± coarsely toothed; ﬂowers borne at the base of the stem or terminal; fruit an indehiscent capsule or subdrupaceous 4. Pachysandra

Genera of Buxaceae 1. Buxus L.

Fig. 12

Buxus L., Sp. Pl. 2:983 (1753); Hatusima, J. Dept. Agric. Kyusyu Imp. Univ. 6:261–342 (1942), Asiatic spp.; Friis, Kew Bull. 44:293–299 (1988), African spp.; Schatz & Lowry II, Adansonia III, 24:179–196 (2002), Malagasy spp.

Fig. 12. Buxaceae. Buxus moctezumae. A Portion of branch with decurrent leaf bases. B Inﬂorescence with a terminal female ﬂower and lateral male ﬂowers. C Nectaries of female ﬂower, surrounded by stylodia. D Dehisced fruit. (Köhler et al. 1993)

Economic Importance. The family is economically important for its horticultural value. The genus Buxus has yielded more than 150 registered cultivars, mainly of B. sempervirens and B. microphylla (Batdorf 1995), which are used for edging, as hedges suitable for pruning and topiary work. The hard, closely grained wood is employed for turning, engraving and manufacturing instruments. Pachysandra terminalis is widely grown as ornamental ground cover. Styloceras provides ﬁrstclass timber for joinery.

Key to the Genera 1. Tepals absent in male ﬂowers, stamens numerous; rudiment of ovary wanting; ovary 2(3)-carpellate 5. Styloceras – Tepals present; stamens usually 4, rarely 6–10 2 2. Leaves decussate; female ﬂowers terminal in racemes or clusters; fruit a 3-valved capsule 3 – Leaves alternate; female ﬂowers at base of racemes or spikes; fruit ± drupaceous 4

Shrubs or trees with tetragonal branchlets, leaves decussate. Inﬂorescences lax to glomerate botryoids of male ﬂowers with a terminal female. Male ﬂowers 4-merous, tepals decussate, stamens antetepalous, inserted around a pistillode. Female ﬂowers with 4–6 tepals, ovary 3-carpellate, with divergent stylodia, stigmas 2-lobed, decurrent along the ventral fold. Fruit a 3-horned capsule, loculicidally dehiscing into 2-horned valves, ejecting trigonal black seeds. 2n = 28, (56). About 90 species in Central America, West Indies, northern and southern Africa, Madagascar, East Asia. For the relationship between the African Buxus and Notobuxus, see below. 2. Notobuxus Oliv. Notobuxus Oliv. in Hook, Ic. Pl. 14:78, t. 1400 (1882); Friis, Kew Bull. 44:293–299 (1989); Phillips, J. S African Bot. 9:138– 140 (1943).

Shrubs or small trees; leaves decussate. Inﬂorescences subfasciculate botryoids with few male and a terminal female ﬂower. Male ﬂowers tepals 4, stamens 6(–10), two pairs opposite the inner tepals; anthers sessile, pistillode minute or wanting. Female ﬂowers tepals 4–6, ovary 3-carpellate with short, recurved stylodia; stigmas decurring. Fruit a greenish-brown, red or black, loculicidal capsule with persistent stylodia. Seeds oblong-ovoid to trigonal, black, 2n = 40. Five species, equatorial West and Central Africa, east to South Africa. This genus is close to Buxus, of which it is treated as a subgenus by Friis, but it differs in the number of stamens, chromosome number and traits of the exine.

46

E. Köhler

3. Sarcococca Lindl. Sarcococca Lindl., Bot. Reg.: t. 1012 (1826); Sealy, Bot. J. Linn. Soc. 92:117–159 (1986), rev.

Small trees or shrubs; leaves alternate, ± triplinerved. Inﬂorescences androgynous botryoids or spikes, sometimes unisexual. Male ﬂowers above, 4merous, with pale or white tepals, whitish stamens and an urceolate pistillode. Females bracteolate, 4– 6 tepals, ovary 3–2-carpellate, with stout recurved stylodia, stigma sulcate, ventrally decurrent. Fruit purplish red or black, indehiscent, subdrupaceous or with dry mesocarp, stylodia persistent. Seeds often solitary, hemispherical to subglobose, brownish black. 2n = 28, less frequent 2n = 56. Eleven species, Southeast Asia. The afﬁliation of S. conzattii (Standley) I.M. Johnst. from Guatemala is doubtful. 4. Pachysandra Mich. Pachysandra Mich., Fl. Bor. Amer. 2:177 (1803); Robbins, Sida 3:211–248 (1968), rev.

Procumbent rhizomatous subshrubs or perennial herbs, branches ascending, leaves alternate, coarsely dentate to nearly entire. Inﬂorescences axillary or terminal spikes, male ﬂowers above, few females below, male 4-merous, with pale tepals, whitish stamens, attached around a rectangular to truncate pistillode; female subtended by prophylls, with 4–6 tepals, ovary 2–3-carpellate, with spurious septa, stylodia erect to recurved, stigma sulcate, decurrent. Fruit reddish brown to black, indehiscent 3-horned capsules or subdrupaceous, white and pulpy. Seeds trigonal, dark brown or black. 2n = 24, 26, 48, 54. Five species, Atlantic North America, China, Taiwan. 5. Styloceras Adr. Juss. Styloceras Adr. Juss., Euph. Tent. 53: t. 17 (1824).

Trees or shrubs, dioecious, rarely monoecious, leaves alternate. Male inﬂorescences short, pendent spikes, sometimes bisexual, tepals wanting, numerous subsessile stamens inserted in a triangular bract, pistillode absent. Female ﬂowers solitary, tepals 3–5, bract-like, ovary 2–3-carpellate, divided by secondary septae, with long, basally distant stylodia, recurved at the tip, and long, decurrent stigmas. Fruit yellow, globose, drupaceous, ± ﬂeshy, indehiscent or tardily dehiscent, stylodia persisting as subapical horns. Seeds oblong, dark blue. Five species, Andean South America.

Selected Bibliography APG II 2003. See general references. Balthazar, M. von, Endress, P.K. 2002a. Reproductive structures and systematics of Buxaceae. Bot. J. Linn. Soc. 140:193–228. Balthazar, M. von, Endress, P.K. 2002b. Development of inﬂorescences and ﬂowers in Buxaceae and the problem of perianth interpretation. Intl J. Pl. Sci. 163:847–876. Balthazar, M. von, Endress, P.K., Qiu, Y.-L. 2000. Phylogenetic relationships in Buxaceae based on nuclear internal transcribed spacers and plastid ndhF sequences. Intl J. Pl. Sci. 161:785–792. Baranova, M.A. 1980. Comparative stomatographic studies in the family Buxaceae and Simmondsiaceae (in Russian). In: Zhilin, S.G. (ed.) Systematics and evolution of higher plants. Leningrad: Nauka, pp. 68–75. Batdorf, L.R. 1995. Boxwood handbook. Boyce: American Boxwood Society. Behnke, H.-D. 1982. Sieve-element plastids, exine sculpturing and the systematic afﬁnities of the Buxaceae. Pl. Syst. Evol. 139:257–266. Bessedik, M. 1983. Le genre Buxus L. (Nagyipollis Kedves 1962) au Tertiaire en Europe occidentale: évolution et implications paléogéographiques. Pollen Spores 25:461–486. Brückner, P. 1993. Pollen morphology and taxonomy of Eurasiatic species of the genus Buxus (Buxaceae). Grana 32:65–78. Carlquist, S. 1982. Wood anatomy of Buxaceae: correlations with ecology and phylogeny. Flora 172:463–491. Channell, R.B., Wood, C.E. 1987. The Buxaceae in the southeastern United States. J. Arnold Arb. 68:241–257. Corner, E.J.H. 1976. See general references. Daumann, E. 1974. Zur Frage nach dem Vorkommen eines Septalnektariums bei Dikotyledonen. Zugleich ein Beitrag zur Blütenmorphologie und Bestäubungsökologie von Buxus L. und Cneorum L. Preslia 46:97–109. Davis, G.L. 1966. See general references. Drinnan, A.N., Crane, P.R., Friis, E.M., Raunsgaard Pedersen, K. 1991. Angiosperm ﬂowers and tricolpate pollen of Buxaceous afﬁnity from the Potomac group (MidCretaceous) of Eastern North America. Amer. J. Bot. 78:153–176. Gentry, A.H., Foster, R. 1981. A new Peruvian Styloceras (Buxaceae): discovery of a phytogeographical missing link. Ann. Missouri Bot. Gard. 68:122–124. Gibbs, R.D. 1974. Chemotaxonomy of ﬂowering plants, 2. Montreal: McGill-Queen’s University Press. Hans, A.S. 1973. Chromosomal conspectus of the Euphorbiaceae. Taxon 22:591–636. Hardman, R. 1987. Recent developments in our knowledge of steroids. Pl. Medica 53:233–238. Hegnauer, R. 1964, 1989. See general references. Huang, S.F., Chen, S.J., Shi, X.H. 1986. Plant chromosome count (2). Subtrop. For. Sci. Tech. 3:41–47. Jarvis, Ch.E. 1989. A review of the family Buxaceae Dumortier. In: Crane, P.R., Blackmore, S. (eds) Evolution, systematics, and fossil history of the Hamamelidae, 1. Oxford: Clarendon Press, pp. 273–278. Kedves, M. 1962. Nagyipollis, a new pollen fgen. from the Hungarian Lower Eocene. Szeged: Acta Biol. 8:83–84.

Buxaceae Köhler, E. 1981. Pollen morphology of the West IndianCentral American species of the genus Buxus L. (Buxaceae) with reference to taxonomy. Pollen Spores 23:37–91. Köhler, E. 1993. Blattnervatur-Muster der Buxaceae Dumortier und Simmondsiaceae van Tieghem. Feddes Repert. 104:145–167. Köhler, E., Brückner, P. 1982. Die Pollenmorphologie der afrikanischen Buxus- und Notobuxus-Arten (Buxaceae) und ihre systematische Bedeutung. Grana 21:71– 82. Köhler, E., Brückner, P. 1990. Considerations on the evolution and chorogenesis of the genus Buxus (Buxaceae). Mem. New York Bot. Gard. 55:153–168. Köhler, E., Schirarend, C. 1989. Zur Blattanatomie der neotropischen Buxus-Arten und ihre Bedeutung für die Systematik. Flora 183:1–38. Köhler, E., Fernández, R., Zamudio, S. 1993. Buxus moctezmae Köhler, Fernández et Zamudio (Buxaceae) una especie nova de Estado de Querétaro, México. Feddes Repert. 104:295–305. Krutzsch, W. 1966. Zur Kenntnis der präquartären periporaten Pollenformen. Geologie 15:16–71. Krutzsch, W. 1989. Palaeogeography and historical phytogeography (palaeochorology) in the Neophyticum. Pl. Syst. Evol. 162:5–61. Kurosawa, S. 1981. Notes on chromosome numbers of Spermatophytes. J. Jap. Bot. 56:245–251. Kvacek, Z., Buzek, C., Holý, F. 1982. Review of Buxusfossils and a new large-leaved species from the Miocene of Central Europe. Rev. Palaeobot. Palynol. 37:361–394. Mai, D.H., Walther, H. 1985. Die obereozänen Floren des Weißelster-Beckens und seiner Randgebiete. Abh. Staatl. Mus. Mineral. Geol. Dresden 33:1–260. Martin-Sans, E., Ponchet, J. 1930. Sur l’appareil sécréteur des Buxus. Bull. Soc. Hist. Nat. Toulouse 60:231–232. Mathou, Th. 1940. Recherches sur la famille des Buxacées. Toulouse: Douladoure. Melikian, A.P. 1968. On the position of the families Buxaceae and Simmondsiaceae in the system (in Russian). Bot. Zhurn. (Moscow & Leningrad) 53:1043–1047. Metcalfe, C.R., Chalk, L. 1957. See general references. Nandi, O.I. et al. 1998. See general references.

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Naumova, T.N. 1980. Nucellar polyembryony in the genus Sarcococca (Buxaceae) (in Russian). Bot. Zhurn. (Moscow & Leningrad) 65:230–240. Pax, F. 1896. Buxaceae. In: Engler, A., Prantl, K., Die natürlichen Pﬂanzenfamilien III, 5. Leipzig: W. Engelmann, pp. 7–23. Raven, P.H. 1975. The bases of angiosperm phylogeny: cytology. Ann. Missouri Bot. Gard. 62:724–764. Reeves, R.D., Baker, A.J.M., Borhidi, A., Berazaín, R. 1996. Nickel-accumulating plants from the ancient serpentine soils of Cuba. New Phytol. 133:217–224. Robbins, H.C. 1962. A monographic study of the genus Pachysandra (Buxaceae). Ph.D. Thesis, Vanderbilt University, Nashville, TN. Sealy, J.R. 1986. A revision of the genus Sarcococca (Buxaceae). Bot. J. Linn. Soc. 92: 117-159. Singh, G., Bir, S.S., Gill, B.S. 1982. In: Löve, A. (ed.) IOPB Chromosome number reports LXXVII. Taxon 31:761– 777. Smets, E. 1988. La présence des ‘nectaria persistentia’ chez les Magnoliophytina (Angiospermes). Candollea 43:709–716. Soltis, D.E. et al. 2000. See general references. Soltis, D.E. et al. 2003. See general references. Uemura, K. 1979. Leaf compressions of Buxus from the upper Miocene of Japan. Bull. Nat. Sci. Mus. Tokyo, C, 5:1–8. van der Hammen, T. 1974. The Pleistocene changes of vegetation and climate in tropical South America. J. Biogeogr. 1:3–26. van Tieghem, P. 1897. Sur les Buxacées. Ann. Sci. Nat. Bot. VIII, 5:289–338. Vogel, S. 1998. Remarkable nectaries: structure, ecology, organophyletic perspectives, IV. Miscellaneous cases. Flora 193:225–248. Webster, G.L. 1987. The saga of the spurges: a review of the classiﬁcation and relationships in the Euphorbiales. Bot. J. Linn. Soc. 94:3–46. Wiger, J. 1935. Embryological studies on the families Buxaceae, Meliaceae, Simaroubaceae and Burseraceae. Thesis, Lund University. Wunderlich, R. 1967. Some remarks on the taxonomic signiﬁcance of the seed coat. Phytomorphology 17:301– 311.

Clusiaceae-Guttiferae Guttiferae Jussieu, Gen. Pl.: 255 (1789), nom. cons. Clusiaceae Lindl., Nat. Syst. Bot., ed. 2: 74 (1836), nom. cons., nom. alt.

P.F. Stevens

Evergreen shrubs or trees, epiphytic or not, glands and/or canals in most parts of the plant; xanthones widespread; plants glabrous or with uni- or multicellular hairs, colleters common; terminal bud scaly or naked. Leaves opposite, sometimes whorled or alternate, entire, estipulate, but paired ‘glands’ sometimes found at base. Inﬂorescences terminal or axillary, rarely ﬂowers single, often modiﬁed cymose. Flowers perfect or unisexual, actinomorphic, usually with prophylls, sepals free, occasionally fused, 2(3)4, or 5(–20); petals (0, 3)4–5(–8), free; stamens (4–)∞, free or variously fasciculate, phalangiate, or otherwise connate, fascicles or phalanges opposite the petals, anthers dithecate, extrose to introrse, opening by slits, rarely pores, connective often with glands of various types; receptacular nectary absent; ovary superior, 1–5(–20)-locular, placentation axile or parietal, apical or basal, ovules (1)2–∞/carpel, anatropous, sometimes amphitropous, bitegmic, tenuinucellate; free stylodia or simple style long to short or 0, stigmas more or less expanded, smooth and sticky or minutely porate, rarely papillose or ± punctate; fruit a berry or septicidal or -fragal capsule, seeds small to large, winged or arillate or not, testa with epidermis and exotegmen alone, the latter ligniﬁed and with sinuous anticlinal walls, or more complex and with vascular bundles permeating a many-layered testa, distinctive exotegmen then often absent; embryo large to small, cotyledons massive to almost absent; endosperm initially free nuclear, often absent at maturity; germination epigeal or hypogeal, if latter, then radicle may die early, replaced by adventitious roots. A family of 27 genera and 1,090 species; largely restricted to lowland tropics. Characters of Rare Occurrence. Exudate black (surrounding embryo of Chrysochlamys, ﬂoral resin of Clusia scrobiculata); leaves lacking free glands or canals (some Kielmeyera, Kayea);

bracts enveloping partial inﬂorescences and falling off like a calyptra (Tovomita calodictyos); ﬂowers zygomorphic by abortion of fascicles (Marila sp.); petals and sepals 3 (some Garcinia); abaxial glands on prophylls and calyx (Clusiella); corolla tubular (Clusia gundlachii) or absent (Calophyllum); anthers with porose dehiscence (Poeciloneuron, some Marila, Clusia, and Garcinia); staminodes of the pistillate ﬂower more strongly adnate to the corolla than phalanges of the staminate ﬂower (Garcinia hollrungii) or staminodes opposite the sepals; pollen in tetrads (Kielmeyera spp.); fruits drupaceous (some Garcinia); seeds papillate (Neotatea); testa soft, with disorganized xylem (Kayea kunstleri, Symphonia); cotyledons fused (Mammea spp.). Vegetative Morphology. Clusiaceae are all woody plants. The trunk may be buttressed (some Calophyllum), or there may be knee (some Symphonia) or prop (Dystovomita) roots; the latter are strongly diageotropic initially. Clusia and its relatives are often epiphytes that only secondarily establish contact with the ground; adventitious roots commonly develop along the stem, and in epiphytic species of Clusia they may encircle and even strangle the host. Kielmeyera, a plant of rather drier areas, may develop a lignotuber, from which it resprouts after ﬁre or drought; root suckering occurs in Mammea acuminata and Garcinia grifﬁthii and layering in Chrysochlamys. Some species of Kielmeyera, Neotatea and Mammea have relatively stout, little- or unbranched stems and large leaves, although the three genera grow in very different habitats. Growth of most taxa is initially monopodial, the lateral branches being orthotropic to plagiotropic (in Garcinia and Symphonia, these may be rigidly plagiotropic). The terminal bud may lack scales, and then the ﬂush may have only one (frequent in Garcinia, Clusia, and Calophyllum) or more pairs of leaves; branches develop from the axils of the uppermost

Clusiaceae-Guttiferae

pair of leaves of the last ﬂush as the terminal bud grows out. Symphonieae, Mammea, some species of Calophyllum, etc., have terminal buds with two or more pairs of scales (Garcinia may approach this condition); branches here usually arise in the axils of the uppermost scales (Mammea) or the lowest pair of expanded leaves (Symphonia). In Mesua, the apical bud aborts at the seedling stage (at least, in M. ferrea), and all growth is by axillary branches; apical buds also abort in some Calophyllum, Lebrunia, etc. In several (?all) species of Kayea, the apical bud of each orthotropic innovation grows on as a plagiotropic lateral shoot, and an axillary bud produces the next orthotropic leader. Tovomita has lateral branches that are plagiotropic by substitution; axillary shoots there may be truly sylleptic. Clusiaceae are often glabrous (Mammea, many Clusioideae); taxa with unicellular hairs are scattered throughout the family. Stellate hairs characterize Caraipa, and branched or stellate hairs occur in Marila; Calophyllum has irregular multicellular hairs. Colleters are common. Buds in taxa that lack perulae are sometimes covered with dense indumentum, as in Calophyllum (it lacks colleters). Terminal and axillary buds in Garcinia, Dystovomita, Poeciloneuron, and elsewhere are often enclosed in deep excavations of the petiole bases; colleters are usually present as well. In Mesua, axillary buds are immersed in stem tissue, and in Mammea they are small and lie almost ﬂush with the stem; they are usually more prominent. There are no stipules, but paired ‘glands’ on either side of the leaf base are quite common. In Mahurea exstipulata, these occur immediately above the insertion of the leaf and appear to be modiﬁed colleters. Garcinia commonly has small, glandular or eglandular stipuliform structures immediately below the leaf insertion, while in Endodesmieae and Symphonieae similar structures are lateral and more delicate; they may even be peltate. In Montrouziera, Garcinia, and Mahurea (the only taxa examined), they lack a vascular supply. The lamina is usually petiolate and the midrib is nearly always obvious. Venation is commonly eucamptodromous or brochidodromous, rarely acrodromous, and is more or less reticulodromous in Kayea, Mammea, and Caraipa in particular. The secondary veins are often rather close together and are joined by a submarginal vein; in Calophyllum, the marginal vein is embedded in marginal thickening and usually cannot be seen, while in

49

Garcinieae, Symphonieae and Endodesmieae the submarginal vein is within 2 mm of the margin. Tertiary venation is notably scalariform in many species of Mahurea, Caraipa, and Marila; in Calophyllum and Neotatea in particular, tertiary venation is apparently absent. Seedlings of Calophyllum and Mammea can show substantial variation in leaf arrangement and rate of growth that is not evident in adults, in Calophyllum some species even having alternate leaves (all adults have opposite leaves; Stevens 1980). Vegetative Anatomy. Vesque (1889, 1892) provides a general survey of leaf anatomy that has still not been surpassed; Metcalfe and Chalk (1950) summarize other early literature; more recent studies include those of Schoﬁeld (1968), and Paula (1976 and references therein). A distinctive feature of Clusiaceae is the exudate-containing glands and canals found throughout the plant (hence the alternative name, Guttiferae), although this has not been surveyed at even a gross level. Canals are associated with the vascular tissue and are also found in both the cortex and pith. Systematically important variation is found in the secretory tissues of the appendicular organs of the plant. These are commonly more or less independent of the vascular tissue, and are probably schizogenous glands or canals. All cotyledons that I have seen possess canals, whatever the condition in the foliage leaves. Clusiella has both glands and canals in its leaves, a combination found in some species of Mammea, Garcinia (probably independently derived in sections Tagmanthera and Daedalanthera), and perhaps also in Symphonieae (particularly poorly known). However, a genus usually has either glands or canals. Glands are notably elongated in Endodesmia and some species of Mammea and Marila. Black glands, perhaps containing hypericin, occur in Mammea, Marila, etc. (these can be confused with spots caused by fungal infections). Most Clusieae and Garcinieae have two or more series of canals in the mesophyll, one near the adaxial side of the lamina and the other near the abaxial; they pursue a more admedial course than the secondary veins (and are more admedial on the adaxial side of the lamina than on the abaxial). Canals are dendritic in Clusia (Pilosperma), and branched canals occur in some species of Garcinia, Clusia, and possibly in Symphonieae such as Pentadesma. Calophyllum has distinctive leaves with closely set secondary veins alternating with canals; the latter are interpreted as being modiﬁed veins

50

P.F. Stevens

(Ramji 1967). Neotatea is similar, and there are tendencies toward this condition in Kayea. Canals commonly occur in petals and ﬁlaments (not all genera have been surveyed); in Clusia, for example, the stout ﬁlaments may consist very largely of resin-containing glands and canals. Nodes are single trace from a single gap. In Montrouziera, the single trace divides in the bottom of the petiole into several, normally oriented bundles. In some species of Mammea, too, the trace divides, but the additional petiole bundles are inverted. The petiole bundle is usually simple, either arcuate (Calophyllum) or more or less circular, or more complex (Marila). The midrib bundle is arcuate when the petiole bundle is arcuate, or more or less circular, with phloem toward the outside. However, in Mammea, Mesua, and some species of Marila, the adaxial layer of vascular tissue is inverted, the adaxial tissue being xylem, while in many genera there are three or more layers of xylem and phloem (the phloem of the adaxial layer is itself adaxial). In Endodesmieae, xylem and phloem of the midrib bundle do not form large blocks of tissues. The vascular bundles of even the higherorder veinlets are often transcurrent, being joined to at least one surface of the lamina by echlorophyllous and often ligniﬁed tissue, but in Clusioideae in particular the vascular bundles – sometimes even the midrib, too – are embedded. Hypodermes are common, although their presence is rarely entirely consistent within genera of any size. The abaxial or near-abaxial layers of spongy mesophyll may become thick-walled and ligniﬁed; again, this is usually not completely consistent in a genus. Isolated mesophyllar sclereids are rare, but most species of Mammea have ﬁbers, either in a subepidermal sheet, as vertically elongated bundles in the palisade mesophyll, or, less frequently, isolated and wandering through the mesophyll (Dunthorn 2002). Epidermal cells have straight to sinuous anticlinal walls (the latter especially on the abaxial surface). Leaves are overwhelmingly hypostomatic; stomata are paracytic. Ligniﬁcation of the echlorophyllous tissue in the lamina margin is common in Kielmeyeroideae. The position of initiation of the phellogen in the root is taxonomically very important; it may be superﬁcial, (sub)epidermal, or deep-seated, interior to the pericycle. The phellogen in the stem is superﬁcial. There are fairly extensive data on wood anatomy, but inconsistencies in the use of descriptive terms and a number of contradictions in the literature present problems. Vessels are

either single or in multiples, being in oblique lines in large-seeded Kielmeyeroideae. Perforation plates are usually simple, although they are sometimes scalariform. Vasicentric tracheids have been recorded from a number of taxa. Wood parenchyma usually occurs; it is paratracheal (in a variety of conﬁgurations) or apotracheal, diffuse or banded. Fiber tracheids and libriform ﬁbers have both been recorded; both may occur within the one genus (Kayea, Marila). Septate ﬁbers occur, but their distribution is very sporadic; septate and non-septate ﬁbers can be found in the same individual (Baretta-Kuipers 1976). A variety of ray types have been reported and there may be variation of systematic interest – thus, the rays of Mesua are largely uniseriate, those of Kayea largely multiseriate. Silica may occur in the rays. Inﬂorescence Structure. Inﬂorescences are terminal or axillary, rarely ramiﬂorous. In Clusiella, the terminal inﬂorescence is evicted by the vigorous growth of an axillary shoot from immediately below the inﬂorescence, and hence appears axillary. The inﬂorescence is usually modiﬁed cymose or thyrsiform, and a terminal ﬂower is nearly always present. Single, terminal ﬂowers are common in Symphonieae. In Mesua ferrea there are single, axillary ﬂowers, perhaps the terminal ﬂowers of a reduced inﬂorescence, but in other species of the genus the few-ﬂowered inﬂorescences lack terminal ﬂowers. Marila has racemiform inﬂorescences in which the often numerous ﬂowers open more or less simultaneously; again, there is no obvious terminal ﬂower. Fasciculate inﬂorescences are common (e.g., Garcinia, Symphonia, Mammea); they are usually modiﬁed cymes. Flowers normally have both bracts and prophylls, but the latter are absent in Calophyllum, Lebrunia, and Kayea lepidota. Bracts, prophylls and sepals intergrade in some Clusieae (see also Gustaffsson 2000), and the lowermost pair of sepals in genera such as Tovomitopsis may in fact be prophyllar. Floral Structure. Sepals and petals are nearly always present and are usually free; they can be difﬁcult to distinguish (Gustafsson 2000). Sepals are commonly ﬁve in number and quincuncial in aestivation, four and decussate, or two and valvate or even connate. When there are ﬁve petals, they are often contorted, when four, then decussate aestivation is common; petal numbers in Mammea increase by the division of the innermost petals. Clusia gundlachii has a remarkable, undivided tube

Clusiaceae-Guttiferae

surrounding the androecium; it shows no evidence of being a composite structure, even when very young (Gustafsson 2000). Pubescence of the calyx and corolla is uncommon. The androecium may be basically fasciculate or phalangiate, the numerous stamens found in most species representing the products of ﬁve, antepetalous primordia (Figs. 14, 16, 17, 19). In pistillate ﬂowers, structures that are usually in the antepetalous position may represent these fascicles. Kielmeyeroideae have slender, free (rarely fused – some species of Mammea) stamens with no evidence of fasciculation, although in the monosymmetric ﬂowers of an undescribed species of Marila there are no stamens opposite two petals, suggesting that two fascicles are missing. Anther glands are common and diverse: they may be absent (Calophyllum, Poeciloneuron); barely perceptible, sometimes paired and apical (Mammea); single and more prominent (Mammea, Marila, Kayea); strongly crateriform, presumably after the contents are removed (Marila; in Caraipa, they contain a highly aromatic oil and the covering ruptures during anthesis); or relatively long and apparently tubular (Marila). Clusioideae show extreme androecial variation, although our knowledge is based almost entirely on general surveys from over a century ago (e.g., Pierre 1883–1885; Engler 1888, 1925; Vesque 1889, 1892, 1893, but see Gustafsson and Bittrich 2002 for Clusia). The ﬁlaments are stout, the anthers even being embedded in them. Garcinieae and Symphonieae often have clearly phalangiate androecia; in the latter, they occur at the end of a long tube. Decaphalangium (= Clusia) was described as having ten phalanges; it is best interpreted as having ten locellate anthers; some other Clusia, Kielmeyera, and Poeciloneuron also have locellate anthers. In both Garcinia and Clusia, androecial fusion may obscure the limits of individual stamens (see below), although epidermides delimiting the stamens can at least sometimes be seen in transverse section. Although an exudate may cover the whole androecium in Clusia and its relatives, or the whole ﬁlaments may consist of massive glands, distinct anther glands are rare in Clusioideae. There is no nectary at the base of the ovary. In Symphonia, however, there is a nectariferous disc surrounding the staminal tube that may represent the antesepalous whorl of the androecium (Fig. 19C); nectar is also secreted by other Symphonieae. Nectar may be secreted at the base of the androecium, as in some species of Clusia.

51

Some species of Garcinia produce an almost mucilaginous secretion from the center of the ﬂower (P. Sweeney, pers. comm.). There are usually 2–5 carpels; when equal in number to the perianth whorls, they are opposite the sepals. Calophyllum has several vascular bundles in the style, the stigma is often deﬁnitely 2or more-lobed, and the single-ovulate gynoecium is multicarpellary. However, how many carpels make up the gynoecium in Endodesmia and Lebrunia, with its single, apical ovule and punctate stigma, is not clear. There is an apparent increase in carpel number within Garcinia, Clusia, and Mammea (Paramammea); in the latter, there may also be twice as many ovary loculi as stigmatic lobes. Placentation is basically axile, although the placentae may fail to meet in the middle, as in Mesua and Mammea; Clusiella has laminar placentation (Notis 2004), and Allanblackia has parietal placentation. Basal ovules occur in Kayea and Calophyllum, apical ovules in Endodesmieae. Ovules are anatropous, bitegmic, bistomal and tenuinucellate, although Mammea americana apparently has a single, massive integument some 26 cells across (Mourão and Beltrati 2000), while the micropyle of Garcinia mangostana is described as being exostomal (Lim 1984). Embryo sac development is of Polygonum type. However, little is known of ovule morphology and embryo sac development. Most Clusioideae have short stylodia representing the separate tips of carpels; the stigmas are usually distinct. The sessile stigmas of Garcinia are more nearly connate; Kielmeyeroideae often have long, simple styles, whether free or fused. The stigma is often more or less expanded, and the surface is smooth or variously sculptured (the latter especially in Garcinia). However, in Kayea, Poeciloneuron, and Endodesmieae it is punctate, while the expanded stigmas of Clusia section Cordylandra have stout, pointed hairs and those of C. section Criuva are papillate. There is a small aperture at the apex of the style branches in Symphonieae through which the pollen enters, but no exposed stigmatic surface at all. Floral Anatomy and Development. Little is known about ﬂoral anatomy and development. Stamen initiation is centrifugal in those few taxa in which this feature has been observed (e.g., Kubitzki 1978). Androecial development in Garcinia and Clusia shows extreme variability, in some species of the latter the normal parts of the stamen be-

52

P.F. Stevens

ing unrecognizable (Bittrich and Amaral 1996). The two antesepalous phalanges in species of Garcinia section Tagmanthera (Exell and Robson 1960) may result from fusion of phalanges in pairs (cf. Hypericaceae, this volume). The vascular tissue of the stamen phalanges of Lorostemon and its relatives is siphonostelic (Kawano 1965); siphonosteles, or close approximations to them, are found in the stout ﬁlaments of some species of Clusia (pers. obs.). Pollen Morphology. Seetharam (1985) surveyed the pollen of the family using a light microscope (see also Yi 1979; Barth 1980; Jones 1980; Seetharam and Maheshwari 1986; GonçalvesEsteves and Mendonça 2001). Extensive pollen variation in Madagascan species of Mammea (Presting et al. 1983) is caused by cryptic dioecy (Dunthorn 2004, see below). Pollen is usually in monads, although Kielmeyera may have tetrads. The grains are usually tricolporate, sometimes triporate; Garcinieae and Symphonieae often have more than three apertures. Costae colpi are usually present, and there is considerable variation in endaperture type and orientation. The pollen surface may be reticulate, rugulose, fossulate, foveolate, psilate or scabrate; supratectal elements occur in some genera, notably Chrysochlamys, and some species of Garcinia are densely spinulate. In most taxa, the nexine is < 1 µm thick, but in many Symphonieae it is > 1.5 µm thick. Karyology. There is extensive infraspeciﬁc variation within Garcinia xanthochymus (Chennaveeraiah and Radzan 1980). However, there may be little cytological variation within Clusia, gametic numbers of 30 having been recorded for several unrelated taxa (da Cruz et al. 1990). The few counts known from Clusioideae show high base numbers of 28–48, and comparable numbers for Kielmeyeroideae are 16–21 (Carr and McPherson 1986). Pollination and Reproductive Systems. Dioecy is common in Clusieae and Garcinieae, but is only sporadic elsewhere. The breeding system of Mammea, often described as being androdioecious, is cryptically dioecious (Dunthorn 2004) – hence the bizarre pollen morphology of some species, usually reported from ‘perfect’ ﬂowers (see above). A few Calophyllum are dioecious; andromonoecy is common in Kielmeyera (Saddi 1989). Garcinia and Clusia need more study. Ag-

amospermy is known from Clusia rosea, C. minor, and Garcinia mangostana; in the latter, adventive embryony in particular occurs (Maguire 1976; Lim 1984; Richards 1990a, b, c). Furthermore, in some species of Clusia there are three ﬂower types – staminate, pistillate, and perfect (Bittrich and Amaral 1997; Lopes and Machado 1998) – while C. minor has perfect ﬂowers (B. Hammel, pers. comm.); in neither Garcinia nor Clusia is dioecy strict. Apomixis is sporadic elsewhere in Clusiaceae, possibly occurring in Calophyllum (Stevens 1980); polyembryony is known from a few species in Calophyllum, Kayea, and Garcinia, including G. magostana. There is little information about hybridization in Clusiaceae (for Calophyllum, see Stevens 1980); fairly extensive artiﬁcial crosses have been made in Clusia (V. Bittrich, pers. comm.). The predominant petal color in the family is white or yellow; pink, purple or red being less common. Many Clusiaceae from the New World tropics produce resins – in particular, polyisoprenylated benzophenones mixed with fatty acids – or other exudates from distinctive anther glands, secretions by the whole staminal mass, the stigmatic surface, or the staminode or pistillode (Ramirez B. and Gomez 1978; Armbruster 1984; Rodrigues C. et al. 1999; Mesquita and Franciscon 1995; Bittrich and Amaral 1996, 1997; Oliveira et al. 1996; Porto et al. 2000; Carmo and Franceschinelli 2002). In Clusia in particular, the secretions are collected by megachilid and other resin-collecting bees, and such pollination mechanisms have evolved more than once (including in Clusiella, see especially Gustafsson and Bittrich 2002). The aromatic oils in the ﬁlaments of Tovomita are collected by euglossine bees, and different fragrances may be involved in species barriers (Noguiera et al. 1998). Some Clusia are night-ﬂowering and pollinated by beetles (including the banana-scented C. ﬂava; B. Hammel, pers. comm.), with pistillate ﬂowers perhaps mimicking staminate ﬂowers (Correia et al. 1993); Clusia growing at higher elevations tends to produce nectar, rather than resin (Armbruster 1984). Little is known about what the various anther glands produce, although resins and/or hypericin and similar substances are likely candidates. Pollen may be a major reward, e.g., Calophyllum; buzz pollination is reported from Kielmeyera (Oliveira and Sazima 1990) and some Clusia, Mahurea, and Caraipa (Bittrich and Amaral 1996). Symphonia and its relatives have large, often red ﬂowers and produce nectar; birds, butterﬂies, monkeys, and in Madagascar,

Clusiaceae-Guttiferae

also lemurs are reported to visit the ﬂowers (e.g., Perrier de la Bâthie 1951; Croat 1978; Pascarella 1992). Platonia insignis is bird-pollinated (Maués and Venturieri 1996), Moronobea coccinea was observed to be pollinated exclusively by parrots (Vicentini and Fischer 1999), while Pentadesma butyracea is bat-pollinated (Petterson et al. 2004). Fruit and Seed. Fruits are commonly capsular, dehiscence being septicidal or septifragal (Mesua, Clusieae). In Kayea, the calyx is often massively accrescent, in some species quite surrounding the capsule; the fruits are then indehiscent. Berries with a single seed and a woody testa occur in Mammea and Calophyllum; similar fruits of Endodesmieae have a thinner testa and the pedicels may be swollen. In Mammea americana, the inner part of the endocarp often becomes ﬁrmly attached to the seed coat (Mourão and Beltrati 2000; pers. obs.), and there is a well-developed periderm. Garcinieae and Symphonieae have several-seeded berries, while in Clusiella the berries may contain thousands of minute seeds. In Platonia insignis, the ﬂeshy inner part of the pericarp becomes attached to the testa and covers it when the seeds are released after dehiscence of the fruit (Mourão and Beltrati 1996a). The endocarp is notably massive and scleriﬁed in some species of Garcinia (largely east Malesian), the surface being strongly ridged. Clusiaceae with seeds less than 4 mm long usually have a testa with an epidermis, as well as a low, ligniﬁed exotegmen with sinuous anticlinal walls developing from the outer epidermis of the inner integument (see also Corner 1976). There is a single, chalazal vascular bundle. In many larger-seeded taxa, the testa is thicker and the vascular bundle proliferates (in Dystovomita it is braided, but restricted to the chalazal position); the exotegmen is then often absent. The exotegmen in large-seeded taxa such as Allanblackia is tall (Delay and Mangenot 1960), although it is difﬁcult to equate the massive ligniﬁed layer in the seed coat of genera such as Lorostemon with an exotegmen. Platonia insignis has a testa of unthickened cells and a few brachysclereids in the tegmen (Mourão and Beltrati 1996b). The seed coat of Symphonia consists of a mass of almost cottony and unligniﬁed ﬁbers, while there is a layer of cells with scalariform thickenings in that of Kielmeyera. In Clusieae, the seed is more or less surrounded by a red or white aril, the latter in some Chrysochlamys, and in Tovomita the fruits are also red inside (V. Bittrich, pers. comm.). In Tovomita, the aril appears to be vascularized.

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The endosperm may persist in small-seeded taxa as a thin layer around the embryo; it has largely disappeared by maturity in larger-seeded taxa. The proportions of cotyledon, hypocotyl and radicle vary greatly. Kielmeyeroideae such as Marila and Clusiella have small embryos less than 3 mm long and with cotyledons 30–60% of their lengths, but most genera have seeds over 6 mm long that are made up largely of cotyledons; in Caraipa, Haploclathra, and Kielmeyera, the cotyledons are strongly cordate whereas in Kayea they are more or less peltate. In Clusioideae, on the other hand, the cotyledons are minute (e.g., Clusia) or almost invisible (many species of Garcinia, Symphonieae), the often large embryo being made up of a grossly swollen hypocotylar region, the tigellus (e.g., Brandza 1908). Axes of such embryos are usually straight, but are S-shaped in Platonia insignis (Mourão and Beltrati 1996b) and some species of Garcinia. The embryo is usually white, but in Caraipa, Kielmeyera, and Clusieae it is often green, while in Calophyllum suberosum it is a rather violent purple. There is much variation in germination (La Mensbruge 1966 provides some information). Species with seeds under 10 mm long are usually epigeal and phanerocotylar, even when the cotyledons are relatively minute, c. 1/10 the seed in length, as in Clusia. Larger seeds over 10 mm long and consisting of proportionally huge cotyledons are either hypogeal and cryptocotylar (Calophyllum, Mammea), or epigeal and phanerocotylar (Caraipa, Kielmeyera); there is infrageneric variation in Poeciloneuron. Larger seeds consisting mostly of tigellus often develop adventitious roots in the epicotylar region, the hypocotyl does not elongate, the cotyledons do not develop further, and the radicle eventually dies, or at least becomes inconspicuous (Garcinia-type germination – see Brandza 1908; also in Symphonia, Tovomita, etc.). However, in other taxa with such seeds, the hypocotyl elongates, the tigellus becomes erect, and the cotyledons expand (Garcinia section Macrostigma, Chrysochlamys), while germination in Platonia is hypogeal, but adventitious roots do not develop. Dispersal. Mammea odorata, with its thick, woody, but not notably dense seed coat, and Calophyllum inophyllum, with a spongy layer immediately surrounding the seed, are strand plants that are water-dispersed. Fruits of the latter species may also be eaten by bats, as are some other

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species of the genus; the many blue-fruited species of Calophyllum (primarily from east of Wallace’s Line) may be dispersed by birds (Stevens 1980). The large, ﬂeshy fruits of Mammea seem to be attractive to mammals, being eaten by a variety of lemurs in Madagascar, and seeds of the arillate New World Clusieae are dispersed by birds (e.g., Spruce 1855), although ants subsequently affect the distribution and germination of seeds of the primarily bird-dispersed Clusia criuva (Passos and Oliveira 2002). Taxa with small, dry seeds, and those with winged seeds, are probably wind-dispersed, although seeds of Haploclathra and Caraipa, with their proportionally very small wings, may be water-dispersed (Kubitzki 1989: the seeds certainly ﬂoat well). Symphonia, whose fruits are eaten by animals, has dispersed across water to achieve its present-day distribution (Dick et al. 2003). Phytochemistry. Clusiaceae are noted for producing a wide array of isoprenylated xanthones, biﬂavonoids and anthraquinones (e.g., Xu et al. 2001 and references therein), 80 new xanthone structures having been reported in the years 1980–1988 alone (Bennett and Lee 1989). Most xanthones have a restricted distribution, although macluroxanthone and in particular mangiferin are more widespread. Interestingly, few xanthones are known from Clusieae, although benzophenones, their precursors, have been isolated from them. Prenylated benzophenones are known from Clusia, Tovomita, Tovomitopsis, and Moronobea (Delle Monache et al. 1991; A. Marsaioli, pers. comm.). 1,3,5,6-tetraoxygenated xanthones are known only from African species of Garcinia and from species of Rheedia (= Garcinia), but not in Asian species of Garcinia (Bennett and Lee 1989). Biﬂavonoids with 3-8 , 3 -8 and 8-8 linkages also show distributions of potential systematic interest (Owen and Scheinmann 1974; Waterman and Husain 1983), while there are distinctive coumarin derivates substituted at position 4 in Kielmeyeroideae (Taylor and Brooker 1969). Tocotrienolic acids and terpenes are also found in Clusia exudates (A. Marsaioli, pers. comm.). Relationships Within the Family. Planchon and Triana (1860, 1862 and references therein) laid the foundation of our knowledge of the family, while Vesque (1893) was its last monographer; he also made extensive anatomical observations. Mahurea, Kielmeyera, Marila, and their relatives are here included in Clusiaceae, although usually

placed in Bonnetiaceae or Theaceae, often having been considered to be ‘linking’ genera (e.g., Maguire 1972; Baretta-Kuipers 1976; Field 1978; Cronquist 1981). Hypericaceae are here excluded from Clusiaceae (Stevens, this volume). Within Clusiaceae, Kielmeyeroideae (as Calophylloideae – Robson 1978) form one major clade. Phylogenetic relationships between genera are unclear, taxa with cordate cotyledons apparently forming a paraphyletic group in some family-level morphological analyses (own unpubl. data), although monophyletic in a three-gene molecular study (Notis 2004). Although Clusiella is sister to Clusioideae in morphological analyses, molecular data place it ﬁrmly within Kielmeyeroideae, where it is a fascinating example of general ecological convergence with Clusia (Gustafsson et al. 2002); it may be associated with other small-seeded Kielmeyeroideae, especially when morphological data are included (Notis 2004). Within Kielmeyeroideae, Endodesmia may be sister to all other taxa, with Mammea sister to the remaining taxa; within the latter, Calophyllum + Mesua and Kayea + Poeciloneuron are two pairs of sister taxa (Notis 2004). (Endodesmieae are vegetatively like Clusioideae, they have fruits like Calophyllum (Kielmeyeroideae), and a unique gynoecium; their germination, chromosome number, root anatomy, etc., are all unknown.) Clusioideae, also monophyletic, are made up of Clusieae, Symphonieae, and Garcinieae. Evidence from both the androecium and gynoecium (the stigma) suggests that Symphonieae are monophyletic, but most genera are poorly known; Montrouziera and Moronobea in particular are very similar. Molecular data do not ﬁnd a strongly supported Symphonieae (Gustafsson et al. 2002). Tovomita (Clusieae) has Garciniatype germination, while some species of Garcinia section Macrostigma germinate like Clusia, as well as apparently having seeds with an exotegmen. Garcinieae and Clusieae are clearly distinguished, and Garcinia germination type may have evolved twice. Clusia includes Decaphalangium and Renggeria, which with Clusia section Cordylandra make a clade (Gustafsson and Bittrich 2002) characterized i.a. by their stigmas, which have stout hairs. Other genera have been synonymized under Clusia (Gustafsson and Bittrich 2002); they were based on slight differences in the androecium, e.g., generally having few anthers (and also ovules). Pilosperma has distinctive branching canals in the leaf; it, too, is best included in Clusia. Tovomitopsis is poorly known, but it may be sister to

Clusiaceae-Guttiferae

Chrysochlamys (Gustafsson and Bittrich 2002), and so it is recognized here (cf. Gustafsson et al. 2002). Afﬁnities. In the past, Clusiaceae have been linked to the heterogeneous Theaceae by ‘intermediate’ genera such as Kielmeyera (e.g., Baretta-Kuipers 1976). Although both have numerous, centrifugally developing stamens and bitegmic, tenuinucellate ovules (e.g., Erbar 1986), Sladeniaceae, Theaceae, and Pentaphylacaceae, into which Theaceae are currently divided (Stevens and Weitzman 2004; Stevens et al. 2004; Weitzman et al. 2004 [as Ternstroemiaceae]), are now all well established as members of the asterid Ericales (e.g., Anderberg et al. 2002). Clusiaceae are part of Malpighiales (e.g., Chase et al. 1993; Davis and Chase 2004). Within Malpighiales, the immediate relatives of Clusiaceae seem well established. Clusiaceae are close to Bonnetiaceae (e.g., Gustaffson et al. 2002) and in particular Hypericaceae (see also Crepet and Nixon 1998). At least some members of all three families have distinctive xanthones (Kubitzki et al. 1978), similar, exotegmic seeds, and antepetalous staminal fascicles or phalanges. However, Bonnetiaceae have long, terminal buds, trilacunar nodes (most taxa), and minutely serrate leaves, although the polarities of these characters are unclear. A rather low base number of n = 11 from Ploiarium is most like numbers in Hypericaceae; Hypericaceae-Hypericeae and Bonnetiaceae also both have papillate stigmas, although Bonnetiaceae apparently lack glands or canals. It has caused something of a stir to ﬁnd that Podostemaceae are also part of this group, and they, too, have tenuinucellate ovules and at least some xanthones; for further details, see Hypericaceae (this volume). The relationships of the Clusiaceae group of families are unclear. Elatinaceae have often been associated with them, but they are probably sister to Malpighiaceae (Davis and Chase 2004). Although Elatinaceae have exotegmic seeds rather like those of Clusiaceae, xanthones have not been detected in them (Hegnauer 1966), and there are a number of similarities between them and Malpighiaceae (Davis and Chase 2004; Stevens 2005). The Clusiaceae group may be close to families such as Ochnaceae (Davis and Chase 2004); interestingly, Malpighiaceae + Elatinaceae may in turn be close to that group. Distribution and Habitats. Clusiaceae are mostly plants of moist, tropical, lowland or

55

lower montane forests. Most genera occur in primary forest, where they may be rheophytes (e.g., Calophyllum rupicola) or grow in peat swamps (C. sundaicum) or black-water ﬂoodplains (Caraipa, Haploclathra spp.). Kielmeyera in South America grows in more open and drier vegetation. Epiphytic or lianescent taxa are found almost exclusively in Clusieae and Clusiella, both tropical American. Crassulacean acid metabolism occurs in Clusia, which shows considerable ﬂexibility in carbon metabolism (Lüttge 1999, 2002). Pending a more detailed phylogeny, little can be said about the biogeography of the family. Bonnetiaceae, close to Clusiaceae, includes the New World Bonnetia and the Malesian-American Ploiarium and Archytaea. Within Clusiaceae, Kielmeyeroideae have many neotropical taxa, e.g., Marila, Caraipa, Neotatea, and Mahurea; Endodesmia and Lebrunia are from the African mainland. Other genera are primarily IndoMalesian, although Mammea is notably diverse in Madagascar; it and Calophyllum are also poorly represented in America. The African and American species of Mammea are notably more similar to each other than to other species in the genus. Within Clusioideae, Symphonieae occur in Africa-Madagascar, America, and New Caledonia (Montrouziera). Symphonia has an amphi-Atlantic distribution, and shows strong molecular differentiation within S. globulifera s.l. (Dick et al. 2003); at least three dispersal events across marine barriers seem necessary, given the age of the genus and its current geographic distribution. Clusieae are restricted to America, while Garcinieae are largely Old World (Garcinia in America is not at all diverse). The diversiﬁcation of both Clusia and Garcinia may be linked to the extreme variation of their androecium. Fossil Record. The fossil record of Clusiaceae is poor. Fossil pollen such as Kielmeyeropollenites eoceni is known from the Eocene of India, and pollen ascribed to genera such as Symphonia, Pentadesma, and Calophyllum is known from the middle Eocene onward in the regions the genera currently inhabit (Muller 1981). Pachydermites diederexii, fossil pollen of Symphonia, is used for stratigraphic dating by the oil industry (R.J. Morley, in Dick et al. 2003). Some fossil woods have been identiﬁed as Clusiaceae, including Symphonioxylon from the lower Miocene in Egypt, the Middle Tertiary of India, and Cretaceous rocks of Somalia; woods similar to those of Calophyllum,

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Kayea, and Mesua have less-startling distributions (Müller-Stoll and Mädel-Angeliewa 1986). Flowers of Paleoclusia, recently described from the Turonian (c. 90 Ma b.p.) in New Jersey, USA, show signs of producing resins and being pollinated by meliponine or similar bees (see above); note, however, that unlike at least some Clusia, the outer anticlinal walls of the exotesta are well developed and there are hairs on the ﬂower (Crepet and Nixon 1998). A few Pleistocene fossils are also known, e.g., of Garcinia in the New Hebrides (Fosberg 1977). Economic Importance. Garcinia mangostana, the mangosteen, is one of the ﬁnest tropical fruits; the inner part of the pericarp (the ‘aril’ of some) is eaten. Other species of the genus also produce tasty fruits, often more acid than those of the mangosteen, and the young leaves of some are edible. The pericarp of Mammea americana (the mammey apple) is another tropical delicacy, and fruits of Moronobea coccinea and in particular Platonia insignis (‘bacuri’; Maués and Venturieri 1996) are also esteemed. The ﬂowers of Mammea siamensis yield a scent. Garcinia twigs are commonly used as chew sticks in West Africa (M. Cheek, pers. comm.). The wood of Mesua ferrea, the ironwood, is very hard; the plant has very ornamental ﬂowers and foliage, and has long been cultivated in India and Java in particular. Species of Symphonia are also spectacular when in ﬂower; the stiff leaves of Clusia rosea have been sent as postcards through the U.S. mail (C.E. Wood Jr., pers. comm.). Many of the larger trees in the family provide useful timber. Thus, Calophyllum is logged through much of Malesia (as ‘bintangor’ or Calophyllum); the wood of C. inophyllum was formerly much valued for the building of canoes and boats. Oils and fats, valuable as medicines and for household activities such as lighting, cooking and making soap, can be obtained from the seeds of species of Calophyllum, Pentadesma, and Garcinia. Moronobea can be weedy. Gamboge (the name is derived from ‘Cambodia’) is extracted from the resin of species of Garcinia; it is a pigment giving a bright yellow color, and also a potent purgative. Several species are important in local pharmacopeias, while in western medicine anti-tumor activity has been detected in xanthones and benzophenones (Bennett and Lee 1989); Calophyllum show some promise as a source of anti-AIDS drugs (McKee et al. 1996). A methanolic extract of Clusia exudate is active against bacteria and fungi (A. Marsaioli, pers. comm.).

Classiﬁcation of Clusiaceae I. Subfamily Kielmeyeroideae Engler (1888). 1. Tribe Calophylleae Choisy (1824). Genera 1–12 2. Tribe Endodesmieae Engler (1921). Genera 13–14 II. Subfamily Clusioideae Engler (1888). 1. Tribe Clusieae Choisy (1824). Genera 15–18 2. Tribe Garcinieae Choisy (1824). Genera 19–20 3. Tribe Symphonieae Choisy (1824). Genera 21–27

Key to the Genera 1. Leaves alternate; androecium not obviously fasciculate or phalangiate; fruit capsular 2 – Leaves opposite, if alternate, then androecium fasciculate and fruit a berry 5 2. Secondary veins closely parallel, tertiary veins not evident 1. Neotatea – Secondary veins not closely parallel, tertiary veins well developed 3 3. Anthers lacking obviously crateriform glands; seeds with wing > 2 mm wide 5. Kielmeyera – Anthers usually with crateriform glands; seeds with wing < 2 mm wide 4 4. Plants lacking stellate hairs; capsules longer than wide, seeds numerous 3. Mahurea – Plants with (minute) stellate hairs; capsules about as long as wide, seeds < 3 6. Caraipa 5. Styles simple, often longer than the ovary (Poeciloneuron with free stylodia), ﬁlaments long, much more slender than the anthers; stigma papillate or smooth; plants rarely dioecious 6 – Free stylodia or simple styles usually shorter than the ovary; ﬁlaments none, or at least half the width of the anthers; stigmas not papillate; plants often dioecious 14 6. Lamina with prominent, close secondary veins almost at right angles to midrib; fruit baccate, seed single, large 7 – Lamina with often inconspicuous secondary veins leaving midrib at acute angle; fruit usually capsular, with few to many seeds 9 7. Stipuliform structures absent; indumentum well developed, at least on buds; stamens free 12. Calophyllum – Stipuliform structures present; indumentum none or slight; stamens fused and/or fasciculate 8 8. Lamina with glands and short canals; inﬂorescences terminal; sepals 5, quincuncial 13. Endodesmia – Lamina with canals, but not crossing secondary veins; inﬂorescences axillary; sepals 4, decussate 14. Lebrunia 9. Terminal bud aborting; axillary buds immersed in stem 9. Mesua – Terminal bud functional; axillary buds more or less evident 10 10. Inﬂorescences racemose, ﬂowers opening simultaneously; capsules with ∞ seeds < 3 mm long 2. Marila – Inﬂorescences not racemose, ﬂowers usually opening successively; capsules with < 4(–8) seeds > 8 mm long 11

Clusiaceae-Guttiferae 11. Terminal buds without perulae; hairs multicellular; cotyledons cordate 7. Haploclathra – Terminal buds perulate; hairs unicellular or plant glabrous; cotyledons not cordate 12 12. Anthers porose; stylodia long, free 8. Poeciloneuron – Anthers dehiscing by slits; style very short to long, more or less fused 13 13. Inﬂorescence usually with axis; style long; fruit capsular, and/or calyx massively accrescent 10. Kayea – Inﬂorescence fasciculate; style short; fruit a ﬁbrous berry; calyx deciduous 11. Mammea 14. Lamina clearly with glands and canals; large gland on abaxial surface of prophylls and often sepals; fruit a many-seeded berry; cotyledons 1/2 length of embryo 4. Clusiella – Lamina rarely with both glands and canals; prophylls and calyx lacking surface glands; fruit capsular, or if baccate, then seeds few; cotyledons < 1|10 length of embryo 15 15. Terminal bud perulate; ﬂowers perfect; anthers 1.7– 40 mm long; stigmas minute, porose 16 – Terminal bud usually not perulate; ﬂowers rarely perfect; anthers usually < 2 mm long; stigmas much expanded 22 16. Filaments connate into a tube; seed with hairyappearing testa 28. Symphonia – Filaments not connate into a tube; seeds lacking hairy testa 17 17. Stamens 15+/phalange; anthers more or less locellate 18 – Stamens 3–13/phalange, anthers rarely locellate 19 18. Inﬂorescences with single ﬂowers; ﬁlaments well fused 24. Platonia – Inﬂorescences with 3–15 ﬂowers; ﬁlaments barely fused 22. Pentadesma 19. Petals ligulate, usually spreading at anthesis 20 – Petals usually broadly elliptic and erect at anthesis 21 20. Anthers 10–40 mm long; ovules 12–∞/carpel; tall, ligniﬁed exotegmen usually present 26. Lorostemon – Anthers 8–9 mm long; ovules c. 4/carpel; exotegmen absent 27. Thysanostemon 21. Style usually shorter than ovary; stamens twisted; ovules 3–10/carpel 23. Moronobea – Style as long as or longer than ovary; stamens straight; ovules 12–∞/carpel 25. Montrouziera 22. Stipuliform structures present or not; androecium often fasciculate; fruit nearly always baccate (capsular, drupaceous) 23 – Stipuliform structures absent; androecium not obviously fasciculate; fruit capsular 24 23. Placentation parietal; ovules 12–∞/carpel 21. Allanblackia – Placentation axile; ovule 1/carpel 20. Garcinia 24. Ovules 1–2(–4)/loculus; aril vascularized 25 – Ovules (1–)4–∞/loculus; aril not vascularized 27 25. Petiole base only slightly if at all excavated; axillary branches lacking long basal internode; stylodia none 19. Chrysochlamys – Petiole base often strongly excavated; axillary branches with a distinctively long basal internode; stylodia often distinct 26 26. Stylodia distinct; outer sepals enveloping bud 17. Tovomita – Stylodia none; outer sepals not enveloping bud 18. Tovomitopsis

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27. Leaf base deeply excavated; inﬂorescences axillary 16. Dystovomita – Leaf base not or slightly excavated; inﬂorescences usually terminal 15. Clusia

Genera of Clusiaceae Basic Characters Plant woody; leaves opposite, ± coriaceous, entire, stipules 0; inﬂorescence ± cymose; stamens free, anthers extrorse, ovary superior, placentation axile, stigma wet; fruit dehiscing down septal radius; seed exarillate. I. Subfam. Kielmeyeroideae Engler (1888). Leaves with ± spherical glands, veins usually transcurrent; ﬂowers perfect; ﬁlaments much narrower than the anthers; style simple; cotyledons > 1/3 length of seed; phellogen in root deep-seated. I.1. Tribe Calophylleae [No characters for the tribe.] 1. Neotatea Maguire Neotatea Maguire, Mem. New York Bot. Gard. 23:161 (1972).

Sparsely branched small trees; hairs unicellular; terminal bud not perulate, no colleters; leaves spiral, secondary veins closely parallel, alternating with canals; inﬂorescences terminal, 1–5-ﬂowered; sepals 5, quincuncial; petals 5, contorted; anthers 5–6 mm long, glands large, spherical; carpels 3, ∞ ovules/carpel, style short, stigma expanded; fruit septicidal; seed papillate, testa simple, exotegmen present; embryo c. 2.5 mm long, cotyledons 1/3– 1/2 its length, endosperm present; germination unknown. Four species, northern South America; colline. 2. Marila Swartz Marila Swartz, Prodr. veg. ind. occ.: 84 (1788).

Trees; hairs stellate or branched, also often uniseriate; terminal bud not perulate, no colleters; secondary veins distant, tertiaries often scalariform, glands sometimes elongated; inﬂorescences with (2–)∞ ﬂowers, racemiform, terminal, branched, or axillary, branched or unbranched, ﬂowers opening simultaneously; sepals 5, quincuncial; petals 5, aestivation various,

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anthers 1–5.5 mm long, porose or not, glands large, spherical, or becoming strongly crateriform, or tubular; carpels 3–6, ∞ ovules/carpel, style short, stigma moderately expanded; fruit septicidal, seeds often with a tuft of hairs at one end, testa simple, exotegmen present, embryo < 1 mm long, cotyledons 1/2–2/3 its length; germination epigeal. Circa 40 species, many undescribed, Central America, the Caribbean, and northwestern South America; usually below 1,000 m. 3. Mahurea Aublet Mahurea Aublet, Hist. Pl. Guiane 1:558 (1775); Kubitzki, Mem. New York Bot. Gard. 29:131–138 (1978).

Trees; hairs unicellular; terminal bud perulate, colleters present; leaves spiral, secondary veins distant, tertiaries often scalariform; inﬂorescences terminal, with ∞ ﬂowers; sepals 5, quincuncial; petals 5, contorted; anthers 1.2–2 mm long, gland large, becoming deeply crateriform; carpels 3(4), ∞ ovules/carpel, stigma moderately expanded; fruit septicidal, seeds winged, testa simple, exotegmen present, embryo c. 1.5 mm long, cotyledons 1/2–2/3 its length; germination unknown. Two species, the Guyanas, Venezuela and northern Brazil; low to moderate alt. 4. Clusiella Planchon & Triana Clusiella Planchon & Triana, Ann. Sci. Nat. Bot. IV, 14:253 (1860); Hammel, Novon 9:349 (1999), rev.

Trees, epiphytes or lianes; glabrous; terminal bud perulate, single interpetiolar stipuliform structure; secondary veins rather close, tertiaries obscure, also canals; plant dioecious; inﬂorescences pseudo-axillary, with 1–15 ﬂowers, prophylls and all or some sepals with a prominent abaxial gland; sepals 5, quincuncial; petals 5, contorted; anthers < 1 mm long, gland 0; carpels 5–15, placentation laminar, ∞ ovules/loculus, funicles long, style 0, stigmas expanded, ± separate; fruit a many-seeded berry, testa simple, exotegmen present, embryo < 2 mm long, cotyledons ± 2/3 its length; germination unknown. Seven species, Central America and tropical South America; low alt. 5. Kielmeyera Mart. Kielmeyera Mart. & Zucch., Flora 8:30 (1825); Saddi, Comp. ext. morph. studies genus Kielmeyera (1989); Saddi, O genero Kielmeyera na ﬂora de Mato Grosso (1996).

Small trees, sometimes little branched, or sprouting from a enlarged rootstock; glabrous, or hairs unicellular, sometimes fasciculate or uniseriate; terminal bud perulate, colleters present; leaves spiral, secondary veins distant, ﬁne venation reticulate; inﬂorescences terminal, 3–∞ ﬂowers; sepals 5, quincuncial; petals 5, contorted; anthers 1–2.5 mm long, locellate or not, gland sometimes subcrateriform, present or not; carpels (2)3, ∞ ovules/carpel, stigma expanded; fruit septicidal; seeds winged, testa with scalariform layer, exotegmen absent, embryo 10–25 mm long, ﬂattened, cotyledons huge, cordate; germination epigeal (?always). Forty-seven species, overwhelmingly Brazilian; low alt. 6. Caraipa Aublet Caraipa Aublet, Hist. Pl. Guiane 1:561 (1775); Kubitzki, Mem. New York Bot. Gard. 29:82–131 (1978).

Trees; hairs stellate, sometimes unicellular or uniseriate; terminal bud perulate or not, colleters present; leaves spiral or distichous, secondary veins distant, tertiaries often scalariform. Inﬂorescences terminal and axillary, with 3–∞ ﬂowers; sepals 5, quincuncial; petals 5, contorted; anthers < 2.5 mm long, gland large, becoming crateriform, rarely absent; carpels 3, 1–4 ovules/carpel, style long, stigma expanded; fruit septifragal; seeds narrowly winged or not, embryo > 6 mm long, ﬂattened, exotegmen 0, cotyledons huge, cordate; germination epigeal. Circa 28 species, from Brazil (most) to Peru, Colombia, Venezuela and the Guianas; low to moderate alt. One undescribed species lacks glands on the anthers. 7. Haploclathra Bentham Haploclathra Bentham, J. Proc. Linn. Soc., Bot. 5:58 & 64 (1860); Lleras, Mem. New York Bot. Gard. 22:129–136 (1972).

Trees; hairs unicellular, branched or multicellular, uniseriate; terminal bud not perulate, colleters present; secondary veins distant, tertiaries scalariform; inﬂorescences terminal, with ∞ ﬂowers; sepals 5, quincuncial; petals 5, contorted; anthers 1.5–5 mm long, locellate, eglandular; carpels 3, 1–2 ovules/carpel, style short, stigma expanded; fruit septifragal; seeds narrowly winged, testa complex, exotegmen absent, embryo > 9 mm long, ﬂattened, cotyledons huge, cordate. Four species, Brazilian Amazonas and Peru; low alt.

Clusiaceae-Guttiferae

8. Poeciloneuron Beddome Poeciloneuron Beddome, J. Linn. Soc., Bot. 8:267, pl. 17 (1865).

Trees; hairs unicellular; stipuliform structures present; terminal bud perulate, colleters present or not; petiole base excavated; secondary veins distant, ﬁne venation reticulate; inﬂorescences axillary or terminal, with 1–∞ ﬂowers; sepals 4, decussate, or 5, imbricate; petals 6, ± imbricate, or 5, contorted; anthers 2.5–6 mm long, porose, locellate or not, eglandular; carpels 2, 2 ovules/carpel, stylodia free, long, stigma punctiform; fruit septicidal (?septifragal); testa complex, exotegmen absent, embryo 1–3 cm long, cotyledons huge, germination hypogeal or epigeal. Three species, Western Ghats of India; medium alt. P. pauciﬂorum Beddome very distinct, but poorly known. 9. Mesua L. Mesua L., Sp. Pl.: 515 (1753).

Trees; plant glabrous or hairs unicellular; terminal bud aborting, axillary buds immersed, colleters not obvious; secondary veins rather close, ﬁne venation closely reticulate. Flowers single, axillary, or in 2–6-ﬂowered axillary inﬂorescences; sepals 4, decussate, or 5, quincuncial; petals 4 or 5; anthers 1.5–4 mm long, with obscure glands in connective or not; carpels 2, 2 ovules/carpel, style long, stigma peltate; fruit septifragal, septae woody, persistent; testa complex, exotegmen absent, embryo 1.2–2.5 cm long, cotyledons huge, germination hypogeal. Five species, Sri Lanka and the Western Ghats of India (4 spp. only from there) to Sumatra; usually low alt. M. ferrea L. throughout the range, long introduced (and problematic taxonomically) in Java, widely cultivated elsewhere. 10. Kayea Wall. Kayea Wall., Pl. Asiat. Rar. 3:5, t. 10 (1832).

Tree; plant glabrous, but stem often papillate; terminal bud perulate, colleters present; secondary veins usually distant, ﬁne venation closely reticulate. Inﬂorescences terminal and axillary, (1–)5–∞ ﬂowers; sepals 4, decussate, outer pair connate or not; petals 4, aestivation various; anthers < 1 mm long, gland large or absent; carpels (3)4, 1–3 ovules/carpel, basal, septae not developed, style long, usually shortly divided at the apex, stigmas

59

punctate; fruit capsular, usually surrounded by massively accrescent calyx; testa complex, exotegmen absent, embryo > 5 mm long, cotyledons huge, (sub)peltate, germination hypogeal. Circa 75 species, many undescribed, one species in Sri Lanka, the rest northeast India to Australia; low (moderate) alt. Most diverse in western Malesia.

11. Mammea L. Mammea L., Sp. Pl.: 512 (1753). Paramammea Leroy (1977).

Trees, sometimes unbranched and schopfbaum; plant glabrous; terminal bud perulate; colleters present; leaves rarely spiral, secondary veins distant, ﬁne venation reticulate, resin canals also rarely present; plant dioecious, inﬂorescences axillary, fasciculate; sepals 2, connate; petals 4–6, aestivation various; anthers 0.6–4 mm long, glands large and single, to small or absent; carpels 2(4), 2(4) ovules/carpel (ovary 8-locular), style short, stigma peltate; fruit a ﬁbrous berry, rarely a septifragal capsule; testa complex, exotegmen absent, embryo ≤ 1.2 cm long, cotyledons massive, sometimes connate, germination hypogeal. Circa 75 species, many undescribed, 2 species in Central America, 3 species in Africa, the others from Madagascar (the center of diversity) to the Paciﬁc and New Caledonia; low to medium alt. The plants appear to be andromonoecious.

12. Calophyllum L.

Fig. 13

Calophyllum L., Sp. Pl.: 513 (1753); Stevens, J. Arnold Arb. 61:117–699 (1980), rev.

Trees; hairs multicellular; terminal bud perulate or not, colleters absent; secondary veins closely parallel, alternating with canals, glands 0; inﬂorescences axillary, rarely terminal, (1–)3–∞ ﬂowers, prophylls absent; sepals 4, decussate; petals like sepals, 0–8, aestivation various; anthers 0.4–2.5 mm long, gland absent; carpels ?2–?4, ovule single, basal, septae absent, style usually long, stigma moderately expanded to peltate; fruit a ﬁbrous one-seeded berry; testa complex, exotegmen absent, embryo (3–)6 mm long, cotyledons massive; germination hypogeal. Circa 186 species, c. 10 species in the American tropics, the rest from Madagascar to the Paciﬁc; low (moderate) alt.

60

P.F. Stevens

sate; petals 4, contorted; stamens 9–12/fascicle, ﬁlaments free; embryo ?1.5–2.2 cm long. One species, L. bushaie Staner, western tropical Africa; low alt. II. Subfam. Clusioideae Engler (1888). Plant usually glabrous; lamina with canals (glands), veins usually embedded; plant dioecious (ﬂowers perfect); anthers usually lacking glands; ﬁlaments usually stout; style or stylodia short or none; cotyledons <1/10 length of embryo; phellogen in root superﬁcial. II.1. Tribe Clusieae Choisy (1824).

Fig. 13. Clusiaceae. Calophyllum trachycaule. A Flowering branch. B Flower. C Stamen. D Pistil. E Fruit. (Lauterbach 1922)

I.2. Tribe Endodesmieae Engler (1921). Indumentum sparse, hairs unicellular; terminal bud not functional; stipuliform structures present; veins more or less embedded; androecium fasciculate, anthers < 1.1 mm long, lacking glands; ovary apparently 1-carpellate, ovule 1, apical, style long, slender, punctate; fruit a 1-seeded berry, pedicel more or less swollen; testa complex, exotegmen absent; embryo large, cotyledons massive (germination and position of root phellogen unknown). 13. Endodesmia Bentham Endodesmia Bentham in Bentham & Hooker f., Gen. Pl. 1:166 (1862).

Tree; lamina with elongated glands or short canals; inﬂorescences terminal, 5–∞ ﬂowers, prophylls present; sepals 5, quincuncial; petals 5, contorted; stamens ∞/phalange, ﬁlaments connate; embryo 1–1.4 cm long. One species, E. calophylloidea Bentham, western tropical Africa; low alt.

Terminal bud eperulate; stipuliform structures absent; plants usually dioecious; androecium not obviously fasciculate or phalangiate; stylodia ± free, stigmas expanded, smooth; fruit septifragal; seeds arillate, exotegmen present (absent). 15. Clusia L.

Fig. 14

Clusia L., Sp. Pl.: 509 (1753); Vesque in C. DC., Monogr. Phanerog. 8:27–144 (1893); Engler in Nat. Pﬂanzenfam. ed. 2, 21:198–204 (1925). Quapoya Aublet (1775); Maguire, Mem. New York Bot. Gard. 23:192–193 (1972). Havetia Kunth (1821). Renggeria Meisn. (1837); Maguire, Mem. New York. Bot. Gard. 23:193–197 (1972). Havetiopsis Planchon & Triana (1860). Oedomatopus Planchon & Triana (1860). Pilosperma Planchon & Triana (1860). Decaphalangium Melchior (1930).

Trees, shrubs, epiphytes or lianes; petiole bases at most very slightly excavated; stamens sometimes connate, anthers also introrse, variable in morphology; 1–∞ ovules/carpel, sometimes stylodia +, or stigma with sharp or rounded papillae; exotegmen present, aril evascular; embryo green, less often white, 2–8 mm long; germination epigeal. Circa 300 species, Mexico to South America, the Caribbean; low (moderate) alt. The genus is poorly known; Vesque recognized 4 genera, and within Clusia, 4 subgenera and 9 sections; Engler placed all taxa in Clusia in 2 subgenera and 16 sections.

14. Lebrunia Staner

16. Dystovomita D’Arcy

Lebrunia Staner, Bull. Jard. Bot. Brux. 13:105 (1934).

Dystovomita (Engl.) D’Arcy, Ann. Missouri Bot. Gard. 65:694 (1979).

Tree; lamina with canals crossing ﬁne veins but parallel to the secondary veins; inﬂorescences axillary, c. 10-ﬂowered, prophylls 0; sepals 4, decus-

Trees; petiole bases very deeply excavated; inﬂorescence axillary; sepals not enclosing bud;

Clusiaceae-Guttiferae

61

garcinioid. Circa 25 species, Central and South America; low (moderate) alt. The genus needs revision. 18. Tovomitopsis Planchon & Triana Tovomitopsis Planchon & Triana, Ann. Sci. Nat. IV, Bot. 14: 261 (1860).

Tree; petiole bases not excavated; sepals 2, free; one ovule/carpel; stylodia free; seeds unknown. Circa 3 species, South America; low alt. The genus is very poorly known. 19. Chrysochlamys Poepp. Chrysochlamys Poepp. in Poepp. & Endl., Nov. Gen. Sp. 3: 13, t. 211 (1840). Balboa Planchon & Triana (1860).

Trees; petiole bases slightly to not excavated; inﬂorescences sometimes axillary; 1 ovule/carpel; testa

Fig. 14. Clusiaceae. Clusia (Decaphalangium peruvianum). A Flowering branch. B Flower seen from above. C Flower seen from beneath. D Anther, ventral view. E Vertical section of ﬂower with rudimentary ovary and anther. (Melchior 1930)

1–2 ovules/carpel; aril evascular, testa sometimes moderately complex, exotegmen present; embryo c. 10 mm long; germination not known. Four species, Central and South America; low alt. 17. Tovomita Aublet

Fig. 15

Tovomita Aublet, Hist. Pl. Guiane 2:956, t. 364 (1775). Tovomitidium Ducke (1935).

Trees; basal internode of branches long; petiole bases moderately excavated or rarely not; sepals 2, connate or rarely free, enveloping bud; 1 ovule/carpel, stylodia sometimes as long as ovary; testa complex, exotegmen absent, aril vascularized; embryo 10–30 mm long; germination

Fig. 15. Clusiaceae. Tovomita brasiliensis. A Flowering branch. B Partial male inﬂorescence with one open ﬂower. C Stamens and pistillode. D Part of infructescence, enlarged the coherent stylodia. E Dehisced fruit. F Seed. (Drawn by B. Angel; Mori 2002)

62

P.F. Stevens

complex or not, exotegmen absent, vascularized; embryo 8–20 mm long; germination epigeal. Circa 55 species, Central and South America, Caribbean (St. Lucia); low (moderate) alt. The genus needs revision. II.2. Tribe Garcinieae Choisy (1824). Terminal bud usually eperulate; stipuliform structures present or not, stout; plants usually dioecious; androecium in staminate ﬂowers phalangiate; style simple, short or 0, stigma expanded, free or ± fused; fruit baccate; testa complex, exotegmen usually absent; embryo (0.4–)1 cm long, cotyledons < 1|10 its length. 20. Garcinia L.

Fig. 16

Garcinia L., Sp. Pl.: 443 (1753). Rheedia L. (1753). Ochrocarpos Noronha ex Du Petit-Thouars (1806). Tripetalum K. Schum. (1889). Pentaphalangium Warb. (1891). Septogarcinia Kostermans (1962).

Terminal bud eperulate, occasionally with perulae; glands sometimes also present, petiole bases usually strongly excavated; androecium sometimes not phalangiate, stamens connate or not, staminodia frequently present in pistillate ﬂowers;

carpels 2–7(–c. 20), 1 ovule/carpel; fruit sometimes septifragal; exotegmen absent or rarely present and then the cells low; germination garcinioid (epigeal). Circa 260 species, pantropic, least diverse in America; low to medium alt. The anthers may sometimes be introrse, and the surface of the style varies considerably. 21. Allanblackia Oliver Allanblackia Oliver in Bentham & Hooker, Gen. Pl. 1:980 (1867); Bamps, Bull. Jard. Bot. Natl Belg. 39:347–357 (1969), rev.

Terminal bud perulate (?); petiole bases with slight excavations; stamens connate, anthers with small ‘glands’, staminodia present; carpels 5, placentation parietal, ovules 12–∞/carpel; exotegmen present, the cells tall; germination hypogeal. Nine species, Africa, Guinea and Zaire east to Tanzania; low alt. II.3. Tribe Symphonieae Choisy (1824). Terminal bud perulate, colleters usually absent; ± peltate stipuliform structures present; inﬂorescence terminal; ﬂowers large, with short androgynophore; sepals 5, quincuncial, petals 5, contorted; androecium phalangiate, phalanges usually free, anthers introrse, staminodia common, usually free; carpels 5, 4–8 ovules/carpel, style simple, usually with 5 distal branches, stigma small, with apical aperture; fruit ± baccate; testa complex, exotegmen with tall cells, or 0; embryo > 1 cm long, cotyledons < 1|20 its length. 22. Pentadesma Sabine Pentadesma Sabine, Trans. Hort. Soc. 4:457 (1824); van Meer, Bull. Jard. Bot. Etat Brux. 35:411–433 (1965).

Inﬂorescence with 3–15 ﬂowers; petals broad; ∞ stamens/fascicle, ﬁlaments smooth, only slightly connate, anthers 7–16 mm long, locellate; ∞ ovules/carpel; exotegmen absent; germination garcinioid. Five species, Mali to Zaire and Ruanda; low alt. 23. Moronobea Aublet Fig. 16. Clusiaceae. Garcinia hunsteinii. A Flowering branch. B Flower. C Male ﬂower, perianth removed. D Two stamen fascicles. E Anther. F Pistil of female ﬂower. G Stigma, seen from above. H Ovary, transversally sectioned. I Branchlet with two fruits, one of which vertically sectioned. J Seed. (Lauterbach 1922)

Moronobea Aublet, Hist. Pl. Guiane 2:788, t. 313 (1775).

Flowers single; petals usually broad, erect; 3–4 stamens/fascicle, spiral, ﬁlaments papillate, anthers 18–25 mm long, locellate; 3–10 ovules/carpel, style medium; exotegmen present; germination

Clusiaceae-Guttiferae

hypogeal. Seven species, Brazil, the Guyanas, Venezuela, Colombia; low to medium alt. 24. Platonia Mart.

63

papillate or not, anthers 4–20 mm long; 12–∞ ovules/carpel; exotegmen present; germination unknown. Five species, New Caledonia; low alt.

Fig. 17

Platonia Mart., Nov. Gen. Sp. 3:168, t. 289 (1829).

26. Lorostemon Ducke

Fig. 18

Flowers single; petals broad; ∞ stamens/fascicle, ﬁlaments papillate, anthers 8–11 mm long, ± locellate; ∞ ovules/carpel, style long; exotegmen absent, germination hypogeal. One species, P. insignis Mart., Guyanas, Brazil; low alt.

Lorostemon Ducke, Arq. Int. Biol. Veg. Rio de Janeiro 1:210 (1935).

Montrouziera Planchon & Triana, Ann. Sci. Nat. IV, Bot. 14:292 (1860).

Flowers single; petals narrow; 3–13 stamens/fascicle, ﬁlaments papillate or not, anthers 10–40 mm long; ovary long-stipitate or not, 12–∞ ovules/carpel; style not branched; exotegmen usually present; germination not known. Five species, South America; low (moderate) alt. Poorly known.

Inﬂorescence with 1–5 ﬂowers, sometimes axillary; petals broad; 3–10 stamens/fascicle, ﬁlaments

27. Thysanostemon Maguire

25. Montrouziera Planchon & Triana

Thysanostemon Maguire, Mem. New York Bot. Gard. 10:132 (1964).

Fig. 17. Clusiaceae. Platonia insignis. A Flower buds. B Flower in anthesis. C Flower with perianth removed, showing phalanges and style with style branches. D Vegetative branch tip. E Two fruits, in one the pericarp partly removed. F Seed. (Cavalcante 1972)

Fig. 18. Clusiaceae. Lorostemon bombaciﬂorum. A Flowering branch. B Flower. C Stamen fascicle, ventral and dorsal view. D Pistil. E Ovary, transversally sectioned. F Fruit. G Seed. (Ducke 1935)

64

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Stipuliform stuctures not seen; ﬂowers single; petals narrow; 4–6 stamens/fascicle, ﬁlaments papillate, anthers 8–9 mm long; c. 4 ovules/carpel; exotegmen absent; germination not known. Two species, Venezuela; low to moderate alt. Poorly known.

ovules/carpel; testa ﬁbrous, exotegmen absent; germination garcinioid. Circa 23 species, tropical America, Africa, most diverse in Madagascar, S. globulifera L. f. widespread and variable; low to medium alt.

28. Symphonia L. f.

Selected Bibliography

Fig. 19

Symphonia L. f., Suppl.: 49 & 303 (1781); H. Perrier, Fl. Madag. Comores 135e & 136e fam.: 13–31 (1951).

Inﬂorescences with 3–9 ﬂowers (axillary); petals broad; androgynophore absent; fascicles connate, 3–6 stamens/fascicle, ﬁlaments smooth, anthers 1.7–5 mm long, extrorse, connective with glands, a low annular nectary outside androecium; 4–8

Fig. 19. Clusiaceae. Symphonia globulifera. A Flowering branch. B Flower. C Flower with petals removed. D Same with perianth and most of staminal tube removed. E As D, but showing ovary in transversal section. F Fruit. G Seed. (Robson 1961)

Anderberg, A.A., Rydin, C., Källersjö, M. 2002. Phylogenetic relationships in the order Ericales s.l.: analyses of molecular data from ﬁve genes from the plastid and mitochondrial genomes. Amer. J. Bot. 89:677–687. Armbruster, W.S. 1984. The role of resin in angiosperm pollination: ecological and chemical considerations. Amer. J. Bot. 71:1149–1160. Baretta-Kuipers, T. 1976. Comparative wood anatomy of Bonnetiaceae, Theaceae and Guttiferae. In: Baas, P., Bolton, A.M., Catling, D.M. (eds), Wood structure in biological and technological research. Leiden Botanical Series 3, pp. 76–101. Barth, O.M. 1980. Morfologia do pólen e palinotaxinomia do género Kielmeyera (Guttiferae). Rodriguesia 32, 55:105–133. Bennett, G.J., Lee, H.-H. 1989. Xanthones from Guttiferae. Phytochemistry 28:967–998. Bittrich, V., Amaral, M. do C.E. 1996. Flower morphology and pollination biology of some Clusia species from the Gran Sabana (Venezuela). Kew Bull. 51:681–694. Bittrich, V., Amaral, M. do C.E. 1997. Flower biology of some Clusia species from Central Amazonia. Kew Bull. 52:617–635. Brandza, G. 1908. Recherches anatomiques sur la germination des Hypéricacées et des Guttifères. Ann. Sci. Nat. IX, Bot. 8:221–300, pls 5–15. Carmo, R.M., Franceschinelli, E.V. 2002. Pollinação e biologia ﬂoral de Clusia arrudea Planchon & Triana (Clusiaceae) na Serra da Calçada, município de Brumadinho, MG. Revista Brasil. Bot. 25:351–360. Carr, G.D., McPherson, G. 1986. Chromosome numbers of New Caledonian plants. Ann. Missouri Bot. Gard. 73:486–489. Cavalcante, P.B. 1972. Frutas comestiveis da Amazônia, I. Belém, Pará: Museu Paraense Museu Goeldi. Chase, M.W. et al. 2003. See general references. Chennaveeraiah, M.S., Radzan, M.K. 1980. Karyomorphological and phytochemical studies in evaluating species relationships in Garcinia L. and systematic position of the G. xanthochymus complex. J. Indian Bot. Soc. 59:251–262. Corner, E.J.H. 1976. See general references. Correia, M.C.R., Ormond, W.T., Pinheiro, M.C.B., De Lima, H.A. 1993. Estudo de biologia ﬂoral de Clusia criuva Camb. Um caso de mimetismo. Bradea 6:209–219. Crepet, W.L., Nixon, K.C. 1998. Fossil Clusiaceae from the Late Cretaceous (Turonian) of New Jersey and implications regarding the history of bee pollination. Amer. J. Bot. 85:1122–1133. Croat, T.B. 1978. Flora of Barro Colorado Island. Stanford: Stanford University Press. Cronquist, A. 1981. See general references.

Clusiaceae-Guttiferae da Cruz, N.D., Sellito Boaventura, V.M., Sellito, Y.M. 1990. Cytological studies on some species of the genus Clusia L. (Guttiferae). Revista Brasil. Genet. 13:335–345. Davis, C.R., Chase, M.C. 2004. Elatinaceae are sister to Malpighiaceae; Peridiscaceae belong to Saxifragales. Amer. J. Bot. 91:262–274. Delay, C., Mangenot, G. 1960. Le développement de la graine chez Allanblackia ﬂoribunda Oliv. Ann. Sci. Nat. XII, Bot. 1:387–440. Delle Monache, F., Delle Monache, G., Gáes-Baitz, E. 1991. Chemistry of the Clusia genus. Part 6. Prenylated benzophenones from Clusia sandiensis. Phytochemistry 30:2003–2005. Dick, C.W., Abdul-Salim, K., Bermingham, E. 2003. Molecular systematic analysis reveals cryptic Tertiary diversiﬁcation of a widespread tropical rain forest tree. Amer. Naturalist 162:691–703. Ducke, A. 1935. Plantes nouvelles ou peu connues de la région amazonienne (VIIème série). Arq. Inst. Biol. Veg. Rio de Janeiro 1:205–212. Dunthorn, M.S. 2002. Anatomy and palynology of Mammea L. (Clusiaceae). M.Sc. Thesis, University of Missouri, St. Louis. Dunthorn, M.S. 2004. Cryptic dioecy in Mammea (Clusiaceae). Pl. Syst. Evol. 249:191–196. Engler, A. 1888. Guttiferae and Quiinaceae. In: Urban, I. (ed.) Flora Brasiliensis, vol. 12, 1. Leipzig: Fleischer, pp. 382–486, pls 79–110. Engler, A. 1925. Guttiferae. In: Engler, A., Prantl, K., Die natürlichen Pﬂanzenfamilien, ed. 2, vol. 21. Leipzig: W. Engelmann, pp. 154–237. Erbar, C. 1986. Untersuchungen zur Entwicklung der spiraligen Blüte von Stewartia pseudocamellia (Theaceae). Bot. Jahrb. Syst. 106:391–407. Exell, A.W., Robson, N.K.B. 1960. New species of Polygala and Garcinia from tropical Africa. Bol. Soc. Brot. II, 34:93–97. Field, B.S. 1978. Theaceae. In: Heywood, V.H. (ed.) Flowering plants of the world. New York: Mayﬂower Press, pp. 82–83. Fosberg, F.R. 1977. A fossil Garcinia fruit from the New Hebrides, Melanesia. Paciﬁc Sci. 31:293–297. Gonçalves-Esteves, V., Mendonça, C.B.F. 2001. Estudo polínico em plantas de restinga do Estado do Rio de Janeiro – Clusiaceae Lindl. Revista Brasil. Bot. 24:527–536. Gustafsson, M.H.G. 2000. Floral morphology and relationships of Clusia gundlachii with a discussion of ﬂoral organ identity and diversity on the genus Clusia. Intl J. Pl. Sci. 161:43–53. Gustafsson, M.H.G., Bittrich, V. 2002. Evolution of morphological diversity and resin secretion in ﬂowers of Clusia (Clusiaceae): insights from ITS sequence variation. Nordic J. Bot. 22:183–203. Gustafsson, M.H.G., Bittrich, V., Stevens, P.F. 2002. Phylogeny of Clusiaceae based on rbcL sequences. Intl J. Pl. Sci. 163:1045–1054. Hegnauer, R. 1966. See general references. Jones, S.J. 1980. Morphology and major taxonomy of Garcinia (Guttiferae). Ph.D. Thesis, University of Leicester. Kawano, S. 1965. Anatomical studies on the androecia of some members of the Guttiferae – Moronoboideae. Bot. Mag. Tokyo 78:97–108.

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Kubitzki, K. 1978. Caraipa and Mahurea (Bonnetiaceae). In: Maguire, B. and Collaborators, The botany of the Guyana Highlands, part X, pp. 82–138. Mem. New York Bot. Gard. 29:1–832. Kubitzki, K. 1989. The ecogeographical differentiation of Amazonian inundation-forests. Pl. Syst. Evol. 162:285– 304. Kubitzki, K., Mesquita, A.A.L., Gottlieb, O.R. 1978. Chemosystematic implications of xanthones in Bonnetia and Archytaea. Biochem. Syst. Ecol. 6:185–187. La Mensbruge, G. de 1966. La germination et les plantules des essences arborées de la fôret dense humide de la Côte d’Ivoire. Nogent-sur-Marne: Centre Technique Forestier Tropical. Lauterbach, C. 1922. Beiträge zur Flora von Papuasien. IX. Die Guttiferen Papuasiens. Bot. Jahrb. Syst. 58:1–49. Lim, A.L. 1984. The embryology of Garcinia mangostana L. (Clusiaceae). Gard. Bull. Singapore 37:93–103. Lopes, A.V., Machado, I.C. 1998. Floral biology and reproductive ecology of Clusia nemorosa (Clusiaceae) in northeastern Brazil. Pl. Syst. Evol. 213:71–90. Lüttge, U. 1999. One morphotype, three physiotypes: sympatric species of Clusia with obligate C3 photosynthesis, obligate CAM, and C3-CAM intermediate behavior. Pl. Biol. 1:138–148. Lüttge, U. 2002. The genus Clusia L.: molecular evidence for independent evolution of photosynthetic ﬂexibility. Pl. Biol. 4:86–93. Maguire, B. 1972. Bonnetiaceae and Tetrameristaceae. In: Maguire, B. and Collaborators, The botany of the Guyana Highlands, part IX, pp. 131–192. Mem. New York Bot. Gard. 23:1–832. Maguire, B. 1976. Apomixis in the genus Clusia (Clusiaceae) – a preliminary report. Taxon 25:241–244. Maués, M.M., Venturieri, G.C. 1996. Ecologia de polinização do Bacurizeiro (Platonia insignis Mart.) Clusiaceae. Bol. Pesquisa 170:1–24. McKee, A.C., Covington, C.D., Fuller, R.W., Bokesch, H.R., Young, S., Cardellina, J.H. II, Kadushin, M.R., Soejarto, D.D., Stevens, P.F., Cragg, G.M., Boyd, M.R. 1996. Pyranocoumarins from tropical species of the genus Calophyllum: a chemotaxonomic study of extracts in the National Cancer Institute collection. J. Nat. Prod. 61:1252–1256. Melchoir, H. 1930. Decaphalangium, eine neue Gattung der Guttiferen aus Peru. Notizbl. Bot. Gart. Mus. BerlinDahlem 10:946–950. Mesquita, R. de C.G., Franciscon, C.H. 1995. Flower visitors of Clusia nemorosa G.F.W. Meyer (Clusiaceae) in an Amazonian white-sand campina. Biotropica 27:254– 257. Metcalfe, C.R., Chalk, L. 1950. See general references. Mori, S.A., Cremers, G., Gracie, C., de Granville, J.J., Heald, S.V. et al. 2002. Guide to the vascular plants of central French Guiana. Part 2. Dicotyledons. Mem. New York Bot. Gard. 76, 2:1–900. Mourão, K.S.M., Beltrati, C.M. 1996a. Morfologia dos frutos, sementes e plântulas de Platonia insignis Mart. (Clusiaceae). I. Aspectos anatômicos dos frutos e sementes em desenvolvimento. Acta Amazonia 25:11–31. Manaus: Instituto Nacional de Pesquisas da Amazônia. Mourão, K.S.M., Beltrati, C.M. 1996b. Morfologia dos frutos, sementes e plântulas de Platonia insignis Mart.

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(Clusiaceae). II. Morfo-anatomia dos frutos e sementes maduros. Acta Amazonia 25:33–46. Manaus: Instituto Nacional de Pesquisas da Amazônia. Mourão, K.S.M., Beltrati, C.M. 2000. Morphology and anatomy of developing fruits and seeds of Mammea americana L. (Clusiaceae). Revista Brasil. Biol. 60:701–711. Muller, J. 1981. Fossil pollen records of extant angiosperms. Bot. Rev. 47:1–142. Müller-Stoll, W.R., Mädel-Angeliewa, E. 1986. Ein neues Guttiferenholz aus dem Tertiär von Java, Calophylloxylon intermedium sp. nov. Feddes Repert. 97:225–233. Nogueira, P.C. de L., Marsaioli, A.J., Amaral, M. do C.E., Bittrich, V. 1998. The fragrant oils of Tovomita species. Phytochemistry 49:1009–1112. Notis, C. 2004. Phylogeny and character evolution of Kielmeyeroideae (Clusiaceae) based on molecular and morphological data. M.Sc. Thesis, University of Florida, Gainesville. Oliveira, P.E.A.M. de, Sazima, K. 1990. Pollination biology of two species of Kielmeyera (Guttiferae) from Brazilian cerrado vegetation. Pl. Syst. Evol. 172:35–49. Oliveira, C.M.A., Porto, A.L.M., Bittrich, V., Vencato, I., Marsaioli, A.J. 1996. Floral resins of Clusia spp.: chemical composition and biological function. Tetrahedron Lett. 37:6427–6430. Owen, P.T., Scheinmann, F. 1974. Extractives from Guttiferae, XXVI. Isolation and extraction of six xanthones, a biﬂavanoid, and triterpenoids from the heartwood of Pentaphalangium solomonse [sic]. J. Chem. Soc. Perkins Trans. 1 1974:1018–1021. Pascarella, J.B. 1992. Notes on ﬂowering phenology, nectar robbing, and pollination of Symphonia globulifera L. f. (Clusiaceae) in a lowland rain forest in Costa Rica. Brenesia 38:83–96. Passos, L., Oliveira, P.S. 2002. Ants affect the distribution and performance of seedlings of Clusia criuva, a primarily bird-dispersed rain forest tree. J. Ecol. 90:517– 528. Paula, J.E. de 1976. Anatomia de Lorostemon coelhoi Paula, Caraipa valioli Paula e Clusia aff. macropoda Klotzsch (Guttiferae da Amazônica). Acta Amazonia 6:273–291. Manaus: Instituto Nacional de Pesquisas da Amazônia. Perrier de la Bâthie, H. 1951. 136e famille Guttifères (Guttiferae). In: Humbert, H. (ed.) Flore de Madagascar et des Comores. Paris: Firmin-Didot. Petterson, S., Ervik, F., Knudsen, J.T. 2004. Floral scent of bat-pollinated species: West Africa vs. the New World. Biol. J. Linn. Soc. 82:161–168. Pierre, J.B.L. 1883–1885. Flore forestière de la Cochinchine, fasc. 5-7. Paris: Octave Doin. Planchon, J.E., Triana, J. 1860. Mémoire sur la famille des Guttifères. Ann. Sci. Nat. IV, Bot. 13:306–376, pls 15, 16. Planchon, J.E., Triana, J. 1862. Ibid. Ann. Sci. Nat. IV, Bot. 16:263–308. Porto, A.M., Machado, S.M.F., Oliveira, C.M.A., Bittrich, V., Amaral, M.C.E., Marsaioli, A.J. 2000. Polyisoprenylated benzophenones from Clusia ﬂoral resins. Phytochemistry 55:755–768. Presting, D., Straka, H., Friedrich, B. 1983. Palynologica Madagassica et Mascarenica. Familien 128 bis 146. Trop.-subtrop. Pﬂanzenwelt 44, 93 pp. Mainz: F. Steiner.

Ramirez, B.W., Gomez, P.L.D. 1978. Production of nectar and gums by ﬂowers of Monstera deliciosa (Araceae) and some species of Clusia (Guttiferae) collected by New World Trigona bees. Brenesia 14–15:407–412. Ramji, M.V. 1967. Morphology and ontogeny of the foliar venation of Calophyllum inophyllum L. Austral. J. Bot. 15:437–443. Richards, A.J. 1990a. Studies in Garcinia, dioecious tropical forest trees: agamospermy. Bot. J. Linn. Soc. 103:233– 250. Richards, A.J. 1990b. Studies in Garcinia, dioecious tropical forest trees: the phenology, pollination biology and fertilization of G. hombroniana Pierre. Bot. J. Linn. Soc. 103:251–261. Richards, A.J. 1990c. Studies in Garcinia, dioecious tropical forest trees: the origin of the mangosteen (G. mangostana L.). Bot. J. Linn. Soc. 103:301–308. Robson, N.K.B. 1961. Guttiferae. In: Exell, A.W., Wild, H. (eds) Flora Zambesiaca, vol. 1, 2. London: Crown Agents for Oversea Governments and Administrations, pp. 378–404. Robson, N.K.B. 1978. Guttiferae. In: Heywood, V.H. (ed.) Flowering plants of the world. New York: Mayﬂower Books, pp. 85–87. Rodrigues, C.M.C., Teixeira Osmond, W., Pinheiro, M.C.B., Lima, H.A. de 1999. Biologia de reprodução de Clusia lanceolata Camb. Hohnea 26:61–73. Saddi, N. 1989. Comparative external morphological study in the genus Kielmeyera Martius (Guttiferae). Publ. Avuls. Herb. Central 2, Cuiabá. Schlechter, R. 1906. Beiträge zur Flora von Neu-Kaledonien. Bot. Jahrb. Syst. 39:1–274. Schoﬁeld, E.K. 1968. Petiole anatomy of the Guttiferae and related families. Mem. New York Bot. Gard. 18:1–55. Seetharam, Y.N. 1985. Clusiaceae: palynology and systematics. Institut Franç. Pondichéry: Travaux de la section Scientiﬁque et Technique, t. 21. Seetharam, Y.N., Maheshwari, J.K. 1986. Scanning electron microscopic studies on the pollen of some Clusiaceae. Proc. Indian Acad. Sci. (Pl. Sci.) 96:217–226. Spruce, R. 1855. Note on Clusiaceae. Hooker’s J. Bot. Kew Gard. Misc. 7:347–348. Stevens, P.F. 1980. A revision of the Old World species of Calophyllum (Guttiferae). J. Arnold Arb. 61:117–699. Stevens, P.F. 2005. See general references. Stevens, P.F., Weitzman, A.L. 2004. Sladeniaceae. In: Kubitzki, K. (ed.) The Families and Genera of Vascular Plants. VI. Flowering Plants: Dicotyledons: Celastrales, Oxalidales, Rosales, Cornales, Ericales. Berlin Heidelberg New York: Springer, pp. 431–433. Stevens, P.F., Dressler, S., Weitzman, A.L. 2004. Theaceae. In: Kubitzki, K. (ed.) The Families and Genera of Vascular Plants. VI. Flowering Plants: Dicotyledons: Celastrales, Oxalidales, Rosales, Cornales, Ericales. Berlin Heidelberg New York: Springer, pp. 473–471. Taylor, H.L., Brooker, R.M. 1969. Isolation of uliginosin A and uliginosin B from Hypericum uliginosum. Lloydia 32:217–219. Vesque, J. 1889. Epharmosis, sive materiae ad instruendam anatomiam systematis naturalis. 2. Genitalia foliaque Garcinearum et Calophyllearum. Vincennes: Delapierre.

Combretaceae Combretaceae R. Br., Prodr.: 351 (1810), nom. cons.

C.A. Stace

Trees, shrubs, subshrubs or lianes, sometimes mangroves, rarely spiny. Indumentum almost always of unicellular, slender, thick-walled, pointed hairs with a distinctive basal compartment (‘Combretaceous hairs’) alone or with glandular hairs of one (or rarely both) of two types – short, capitate stalked glands, and subsessile peltate scales. Leaves opposite (or whorled) or spiral, petiolate, simple, entire, with pinnate venation, often with a pair of petiolar glands or domatia; stipules 0 or vestigial. Inﬂorescence axillary or terminal, capitate to expanded, of simple or paniculate spikes or less often racemes. Flowers with simple, usually caducous bracts, bisexual, or bisexual and male in same inﬂorescence, or rarely dioecious, 4- to 5-merous, actinomorphic, or sometimes weakly zygomorphic, epigynous or rarely semi-epigynous; hypanthium (receptacle) surrounding ovary (lower hypanthium) and extended beyond into saucer- to tube-shaped upper hypanthium, with 2 prophylls fused to lower hypanthium in Laguncularieae; sepals 4–5(–8), borne at tip of upper hypanthium, sometimes vestigial, rarely accrescent; petals 4–5, usually borne at or near tip of upper hypanthium, often small, sometimes conspicuous, or often 0; stamens usually twice as many as sepals (rarely to 16), borne inside upper hypanthium usually at two levels, sometimes as many as sepals, rarely second whorl represented by staminodes, exserted or included, with dorsiﬁxed, usually versatile, rarely adnate, 4-locular anthers; nectariferous disk often present at base of upper hypanthium; ovary 1-locular; ovules (1)2–7(–20) (usually 2), apical, pendulous, anatropous, bitegmic, crassinucellate; style simple, with usually punctiform stigma. Fruit 1-seeded, indehiscent or rarely tardily dehiscent, with dry or spongy to succulent wall, often with 2–5 papery to leathery wings; endosperm absent in mature seed; cotyledons usually 2(–5) or fused to appear 1, variously folded or twisted in seed, rarely ﬂat or hemispherical.

A pantropical family with 14 genera and c. 500 species. Characters of Rare Occurrence. Mangroves: Lumnitzera, Laguncularia (Conocarpus mangrove-associate) Branches spiny: Terminalia (former Bucida), some Combretum Semi-inferior ovary: Strephonema Slightly zygomorphic ﬂowers: some Combretum (including former Calopyxis), Lumnitzera littorea, Dansiea Dioecious ﬂowers: Combretum rupicola, Conocarpus (± so), Laguncularia (± so) Andromonoecious ﬂowers: many Terminalia, Pteleopsis Markedly accrescent calyx: Calycopteris Only one whorl of stamens: Terminalia tetrandra, some Combretum (former Thiloa and Meiostemon) Staminodes representing one whorl of stamens: Combretum gracile, some ﬂowers of the variably dioecious species and of Lumnitzera littorea Stamens with adnate anthers: Buchenavia Ovules often more than 8: Macropteranthes, Dansiea Tardily dehiscent fruits: Combretum (former Quisqualis) Fruit-wings derived from prophylls: Macropteranthes, Dansiea Cotyledons ﬂat, not folded: Strephonema, Combretum sects. Cacoucia (some) and Calopyxis (some) Cotyledons fused: some Combretum Three or more cotyledons: some Terminalia Vegetative Morphology. All species of Combretaceae are woody, varying from tall timber trees or lianes (mostly in forest) to short shrubs or subshrubs (in savannah). A few species possess stem thorns. In the ﬁre-prone savannahs of Africa and India, there are about 20 species of subshrub in the genus Combretum: plants with large underground ‘trunks’ putting up annual aerial shoots

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which are burnt to the ground during the dry season. These species belong to four different sections of the genus (Keay 1950), in two cases together with forest scandent shrub and liane species, and in the other two cases together with savannah tree and shrub species. Some of the shrubs develop into lianes or ‘scrambling shrubs’ if left ungrazed and provided with a support. The lianes often climb over 30 m high, especially in the genus Combretum, while the smallest subshrubs do not exceed 20 cm. Combretum species are mostly subshrubs, shrubs or lianes, with very few trees (exceptionally, C. leprosum and C. glaucocarpum up to 25 m in Brazil). The largest trees are over 50 m tall and are found in the genera Terminalia and Buchenavia; buttresses are present in several species. Corner (1940) described the characteristic ‘pagoda-trees’ of Malaya, belonging to nine different families, in which the main branches are held in horizontal tiers with the leaves in ﬂat bunches dispersed over the top side of each tier. This growth habit is so characteristic of several species of Terminalia (notably, T. catappa) that Corner termed the sympodial branching pattern which gives rise to it as “Terminalia-branching”. Two genera are true mangroves: Lumnitzera from East Africa to Australia and Laguncularia in West Africa and East and West America. Both develop characteristic pneumatophores – in Lumnitzera, these are looped above the mud (‘knee-roots’) whereas in Laguncularia they are simple or branched projections from the mud

Fig. 20. Combretaceae. Old specimen of Conocarpus erectus in a dune-valley of Peninsula de Paraguaná, Caribbean. (Phototograph K. Kubitzki)

(‘peg-roots’). Fruit-vivipary is, however, scarcely exhibited; in Laguncularia, the radicle is reported barely to pierce the seed-coat while the fruit is still on the tree. In addition, Conocarpus erectus, with a distribution similar to Laguncularia, is often considered a mangrove, but its lack of vivipary or pneumatophores suggests that it is best considered a ‘mangrove-associate’ (Fig. 20). Some Terminalia species are also mangrove-associates. Terminalia cuneata (India) is not one of these, but it sometimes produces erect pneumatophore-like aerial roots when the root-system is submerged (Adamson 1910). The leaves of Combretaceae are evergreen or deciduous, according to the vegetation type the plants inhabit. In some genera, notably Buchenavia, they are clustered in dense spirals at the swollen tips of twigs. A pair of sessile secretory glands is present in many species, particularly Terminalia, Buchenavia, Laguncularia and Conocarpus; their presence and position are of diagnostic value. Klucking (1991) presented an extensive survey of leaf venation in the family, providing many excellent illustrations, covering 11 genera and 223 species. His study, however, lacks an analytical element and, in several cases, specimens under different names for the same species (e.g. Terminalia amazonia and T. obovata) fell into different categories of venation pattern. Alwan (1983) covered 144 species in all 13 genera. Using the terminology of Hickey (1973), he recognized six major types within this broad pattern, ﬁve of them representing grades from brochidodromous to eucamptodromus, and the sixth being craspedodromous. There seems to be no taxonomic correlation of these types as high as genus level; all six types occur in Terminalia, and craspedodromous only in that genus. Many species bear foliar domatia – small pocket- or bowl-shaped pits in the axils of the main lateral leaf-veins on the lower leaf surface; they are particularly common in Terminalia, Buchenavia and Conocarpus, in which their presence and structure are species-constant. Pocket-shaped (‘marsupiiform’) domatia occur widely in Combretinae and Terminaliinae, but bowl-shaped (‘lebetiform’) ones are found only in the above three genera of Terminaliinae. In Strephonema, the leaves have marginal revolute domatia. Stipules are said in all ﬂoristic accounts to be absent from Combretaceae. Weberling, in Dahlgren

Combretaceae

and Thorne (1984), stated that they are present in “nearly all families of Myrtales”, although in Combretaceae he found them only as tiny “rudimentary ﬁnger-like projections” near the petiole base and only in a few of the species examined. Vegetative Anatomy. Leaves are usually dorsiventral, with no hypodermis but with 1–2 adaxial palisade layers and a broader spongy mesophyll (Tilney 2002). In the mangroves Laguncularia and Lumnitzera, in the related Macropteranthes and Dansiea to a slight degree (abaxial palisade weakly developed), in the mangrove-associate Conocarpus, and in a few other scattered taxa, the leaves have an isobilateral organization, with palisade on both sides and a central large-celled water-storage tissue; this is clearly an anatomical syndrome correlated with physiological drought (Stace 1966). Midrib structure is described by Keating (1984) and Tilney (2002). Stomata are usually present only on the lower epidermis, but are on both upper and lower surfaces in the species with fully isobilateral leaves and also in some species of Terminalia and other genera with coriaceous dorsiventral leaves. Stomata are basically anomocytic throughout the family, except in Strephonema where they are paracytic (Stace 1965). In the mangroves Lumnitzera and Laguncularia, the anomocytic stomata are cyclocytic. The trichomes of the Combretaceae are diagnostic. Non-glandular hairs are almost always in the form of ‘Combretaceous hairs’ – unicellular, pointed, very thick-walled hairs (leaving virtually no lumen) which possess a distinctive, often swollen basal compartment. Apart from Strephonema, these occur in all species (over 300) examined to date, except for the apparently completely glabrous Lummitzera littorea (but they do occur in L. racemosa). In Strephonema, they occur in S. mannii but not in the other two species (S. sericeum and S. pseudocola), where only 2armed thin-walled hairs usually with a basal compartment, as well as some intermediate forms, are present (Stace 1965). The 2-armed hairs were described by Heiden (1893) from Conocarpus, but I have been unable to conﬁrm this. A few (taxonomically scattered) species possess some simple thin-walled hairs, among a predominance of Combretaceous hairs. Combretaceous hairs have elsewhere been reported only from a few Myrtaceae and Cistaceae (Solereder 1908). Glandular trichomes are of two main types: glandular hairs with a short uniseriate stalk (rarely

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longer and multiseriate) and clavate or capitate head; and peltate scales, with a very short uniseriate stalk and a 1-cell-thick plate-like head consisting of eight to a few hundred cells (Fig. 24; Stace 1965). One or other type (extremely rarely both) is present in every species of all genera of subtribe Combretinae. The presence of these glandular trichomes, and the cell-delimitation of the scales, are extremely important taxonomic characters in this subtribe. Dome-shaped sessile glandular structures are found in Laguncularia at the base of deep, narrow-oriﬁced pits found on both leaf surfaces, usually visible as a mound on the leaf surface. The superﬁcially similar pits on the lower epidermis of Conocarpus do not contain glands and are best considered as domatia. In the latter genus, however, small stalked glands occur sparsely on both leaf surfaces; these resemble those of the Combretinae but they are perhaps related to the saline habitat of Conocarpus. In young twigs, the vascular bundles are bicollateral in almost all species examined (Dahlgren and Thorne 1984; Tilney 2002). Phloem islands (‘included phloem’) are present in the wood of only four of the six genera studied of subtribe Combretinae (van Vliet 1979). den Outer and Fundter (1976) found that both the periderm and the secondary phloem of Strephonema resemble those of the rest of the family in many characters, but differ in having type I sieve-tubes (types II or III in other genera) with longer elements than in all other genera. The sieve-tube element plastids are S-type throughout the family, as in the rest of Myrtales (Behnke 1984). Wood anatomy has been thoroughly surveyed by van Vliet (1979) and van Vliet and Raven (1984). Growth-rings are distinct or not, the wood being usually diffuse- but sometimes ring-porous, with parenchyma mostly paratracheal but often apotracheal or marginal, the ﬁrst type varying from scanty to conﬂuent-banded. Hence, virtually the whole spectrum of possibilities is covered. More interesting or unusual characters are the vestured pits, ﬁbre-tracheids, radial vessels, ray-types, vessels of two distinct sizes, and included phloem. Strephonema differs from the other genera in having distinct aggregates (tangential bands) of apotracheal parenchyma, heterocellular rays of types II–III, vestured pits of type A (type B in rest of family) and ﬁbre-tracheids (ﬁbres with distinctly bordered pits, absent from rest of family). Subtribe Combretinae (all species examined) is characterized by two characters absent from the rest of the

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family: vessels of two very distinct diameters, and uniseriate rays containing radial vessels with perforations in their tangential walls, those in the terminal elements connecting with very narrow axial vessels or tracheids. These radial vessels are, in fact, unique among all plants. Anatomy of the peg-roots of Laguncularia is described by Jeník (1970), and of normal roots of Combretum by Verhoeven and van der Schijff (1974). Inﬂorescence Structure. Weberling (1988) described the inﬂorescences as “polytelic throughout”, i.e. with indeﬁnite growth, the inﬂorescence lacking a terminal ﬂower. The commonest type of inﬂorescence is the spike, occurring in most genera including the two largest, Combretum and Terminalia (Figs. 22–24). Usually, the ﬂowers are more or less sessile but in some cases they are shortly pedicellate, conspicuously so in Strephonema and Pteleopsis, forming a raceme. In most cases, the bracts are small and caducous but sometimes they persist and occasionally are large and conspicuous, presumably to attract pollinators, e.g. red in Combretum mussaendiﬂorum, white in C. racemosum. Variations occur in two directions. Firstly, the spikes (or racemes) are often branched, sometimes forming quite large compound spikes/racemes; this is common in several genera, including Combretum, but rare or absent in others, e.g. Terminalia and Buchenavia respectively. Secondly, the spikes may be congested (Exell 1962), in extreme cases forming apparent umbels (e.g. many Combretum, Guiera, some Terminalia, Pteleopsis) or cone-like structures (Conocarpus, Anogeissus, Finetia). Flower Structure. The common ﬂower organization in the family includes an inferior 1-celled ovary with (1)2–7(–20) apical ovules leading to a 1seeded fruit and a tetramerous or pentamerous perianth with both 1-whorled calyx and corolla and an androecium of 1 or 2 stamen whorls. The hypanthium is usually divided into two parts: a lower one surrounding and fused to the ovary, and sometimes extended above it as a stalk-like support for the next (or the latter might be part of the next), and an upper one extended above it and bearing the sepals, petals and stamens. In Laguncularieae, there is scarcely any distinction between an upper and lower hypanthium. In Dansiea, the lower hypanthium is fused to the ovary only on one side.

Variation from this pattern is in four main directions: (1) loss of petals in virtually all Terminaliinae and some Combretinae; (2) loss of one whorl of stamens in some Combretum (former Thiloa, where the missing whorl is replaced by staminodes in 1/3 species, and former Meiostemon) and Terminalia tetrandra (former Terminaliopsis); (3) elaboration of the upper hypanthium into an attractive campanulate to tubular structure in some Combretum; and (4) a trend towards unisexuality – the plants andromonoecious in Terminalia and Pteleopsis, and ﬂowers/plants variably bisexual, monoecious or dioecious (probably mainly functionally dioecious) in Conocarpus, Laguncularia and Combretum rupicola. The petals are rarely large and attractive; exceptions are a few Combretum species and Lumnitzera. In some Combretum, it is the antepetalous stamens which are missing (Stace 1968) whereas in other Combretum and Terminalia tetrandra it is the antesepalous ones (Capuron 1967). In two of the three species of Combretum sect. Thiloa, there are glandular outgrowths (caruncles) on the connectives. In some taxa, e.g. Lumnitzera littorea, variable numbers of stamens are aborted or sterile, giving a total of 5–10 functional ones. In most taxa, the disk is a continuous ring of nectariferous tissue at the base of the upper hypanthium, but sometimes it is vestigial or absent. In Lumnitzera littorea, the ring is broken at the most ventral point, where the stamen is usually lacking. In Dansiea, the nectary is reduced to a bilobed outgrowth only on the dorsal side. The style is adnate to the upper hypanthium for various distances in Lumnitzera littorea and some Combretum (including former Quisqualis). In Strephonema, the ﬂowers are only semiepigynous, the lower hypanthium extending less than halfway up the ovary and the upper hypanthium arising from it at that point as a short ‘calyxtube’, and bearing the sepals, petals and stamens (Fig. 21). Floral anatomy, particularly vascular architecture, was treated by Venkateswarlu and Rao (1970). The pattern in Lumnitzera, with three traces to each sepal, was considered ancestral to the situation in Combretinae and Terminaliinae, with only one trace to each. Moreover, Lumnitzera has 8 traces in the style, said to represent the ancestral polycarpellary state, whereas the rest of the family have 2–5, and it was the only genus studied to have traces to the nectariferous disk. Subsequent work by Fukuoka et al. (1986) did not wholly conﬁrm these earlier ﬁndings, and they concluded that

Combretaceae

Lumnitzera represents a separate line of development, rather than an ancestral state. Embryology. Male and female embryological details have been summarized by Tobe and Raven (1983); seven genera have been examined. Virtually all details agree with the common situation in the Myrtales (see family description), and little variation within the family is known. The ovules lack integumental vasculature, and the embryo sac is of the Polygonum type but usually with ephemeral antipodals. Guiera, however, was found by Venkateswarlu and Rao (1972) to have persistent antipodal cells and a micropyle formed from only the inner integument, both being unique character-states in the whole of Myrtales. Endosperm formation is Nuclear but an endosperm is absent in the mature seed. Pollen Morphology. Data presented here come from work of J.H. Tallis (1963, unpubl. data), B. Batts (1969, unpubl. data), A.-R.A. Alwan (1983, and unpubl. data), Patel et al. (1985), El Ghazali (1993) and El Ghazali et al. (1998); all current genera except Finetia and Dansiea were covered. In Strephonema, Buchenavia and Laguncularia, the grains are tricolporate; these genera are not related and this type of pollen does not occur in the genera most closely related to the latter two genera (Strephonema is isolated). These three can easily be distinguished by their surface sculpturing: reticulate, echinate and psilate respectively. The grains of the other nine studied genera are heterocolpate, i.e. the three colpi (each with a central pore) alternating with three pore-less subsidiary colpi (or pseudocolpi), and exhibit a similar range of surface sculpturing. Heterocolpate grains are found in 8 of the 14 families of Myrtaceae but in very few non-Myrtalean families (Dahlgren and Thorne 1984). Apart from this important feature, it can be concluded that pollen characters are very useful at generic and lower levels, but scarcely contribute to an understanding of generic relationships in Combretaceae. Probably too much was made by Patel et al. (1985) of the distinctive reticulate grains of Strephonema, since the strikingly striate grains of Combretum rhodanthum ﬁgured by El Ghazali (1993) appear no less distinctive. Some of the other generic characteristics summarized by Patel et al. (1985) break down when more species are surveyed, e.g. echinate grains are not constant in Anogeissus, but others do not, e.g. tricolporate echinate grains in Buchenavia (quite unlike

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those in the presumably related Terminalia). The ranges found in the large genera Combretum (El Ghazali) and Terminalia (Alwan) suggest that their infrageneric classiﬁcation might be reinforced by pollen morphology. Fruit and Seed Structure and Germination. Strictly spoken, the ‘fruit’ is a 1-seeded pseudocarp formed from the inferior ovary and surrounding the lower hypanthium, except in Strephonema where the semi-inferior ovary is mostly exposed from the hypanthium at fruiting, the latter remaining adherent to the base of the fruit. Where there is a stalk-like extension at the tip of the lower hypanthium, this may or may not persist as a fruit-beak. The fruit wall (pericarp plus hypanthium) may be thin and hard, or become differentiated as spongy or succulent tissue, or develop 2–5 wings. All situations are common, often within one genus. The inner part of those pericarps which become succulent may be very hard and woody, forming a pseudodrupe, as in many Terminalia and all Buchenavia. In some cases, the fruits are aggregated into compact heads, the Alnus-like ‘cones’ of Conocarpus representing the extreme. In Calycopteris, the 5 wings are developed from the accrescent calyx, and in Macropteranthes and Dansiea the 2 wings are accrescent prophylls. Fruit anatomy in Laguncularia and Combretum is described by Valente et al. (1989, 1994). An endosperm is absent and the embryo ﬁlls the seed. In Strephonema, the two cotyledons are massive and hemispherical (conduplicate). Those of Combretum sect. Calopyxis approach this condition. In Combretum sect. Cacoucia, the cotyledons are less massive but still not folded (also conduplicate) but in all other Combretaceae they are folded, although they can be thick and succulent, e.g. Terminalia megalocarpa (Coode 1973). Folding is either convolute (spiralled together) or irregularly complicate (folded upon themselves, often complexly). The distribution of these three types in the tribes and subtribes is as follows: Strephonematoideae – conduplicate (hemispherical) Combretoideae Laguncularieae – spirally convolute Combreteae Combretinae – irregularly complicate (mostly), spirally convolute or conduplicate Terminaliinae – spirally convolute

Both epigeal and hypogeal germination is common and seems to have little taxonomic signiﬁcance

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above species level; both types are found in both Combretum (Jackson 1974) and Terminalia. Strephonema shows hypogeal germination (Jongkind 1995b). Of the two mangroves, Laguncularia is epigeal and Lumnitzera hypogeal (Tomlinson 1986) whereas Macropteranthes, a close relative of the latter, is epigeal (N. Byrnes, pers. comm.). Tomlinson reported Conocarpus and Terminalia catappa to be hypogeal, as did Brandis (1893) for T. bellirica, but several Southeast Asian species of Terminalia are epigeal. Terminalia megalocarpa, like some others from Southeast Asia, has 3–4(–5) cotyledons (Coode 1969, 1973). Species of Combretum from African ﬁre-prone savannah, e.g. C. viscosum, C. molle and C. bauchiense, have two epigeal cotyledons with long, fused petioles arising from below the soil and protecting the subterranean plumule bud (Jackson 1974, Onyekwelu 1990). In some seedlings of C. viscosum, the cotyledons are also fused, forming a deep cup with a circular rim (C.A. Stace, unpubl. data). When the shoot grows, it breaks laterally from the base of the fused petioles and emerges from the soil some centimetres from the cotyledons. This peculiar mode of germination has been termed ‘cryptogeal’, and is exhibited by pyrophytic species in other families. Karyology. About 112 chromosome counts for c. 47 species in 7 genera have been reported. By far the commonest counts are 2n = 24 and 26, the former being characteristic for Terminalia, Conocarpus, Anogeissus and Guiera and the latter for Combretum (including former Quisqualis), Calycopteris and Lumnitzera. The base numbers thus appear to be x = 12 and 13, the former in Terminaliinae and the latter in Combretinae and Laguncularieae. In addition, in both Terminalia and Combretum triploids, tetraploids, hexaploids and octoploids have been reported, the highest numbers being 2n = 96 for T. bellirica and 2n = 104 for C. celastroides. Some of the variation in ploidy level is infraspeciﬁc, e.g. 2n = 24, 48 and 72 in Terminalia chebula. Ohri (1996) reported DNA C-values for six species of Terminalia. For three diploids, 2C-values were 3.6 to 7.13 pg, for a triploid 10.19 pg, and for two tetraploids 7.3 to 12.8 pg. This gives an almost twofold variation (1.8 to 3.56 pg) in 2C-value per basic genome. In ﬁve Indian taxa, the 2C-value was 8.01 to 9.66 pg (Srivastava et al. 2001). These values are above average for tropical hardwoods (Ohri and Kumar 1986).

Pollination. Three major adaptations relevant to pollination are evident in the family: loss of petals; enlargement of upper hypanthium; and clustering of ﬂowers into groups. Large coloured petals, as in a few Combretum species, especially those formerly in Quisqualis (Fig. 25), are rare. In C. indicum the ﬂowers are sweetly scented, especially in the evening, and the long narrow hypanthium shows this to be a typical hawkmothpollinated ﬂower. In nearly all other Combretaceae, the petals are relatively small and inconspicuous, or lacking, and three major pollination syndromes can be detected. Firstly, scentless ﬂowers with large, red to yellow upper hypanthia, found in Combretum (including former Calopyxis) in West Africa and Madagascar, are presumably pollinated by sunbirds, although no direct observations have been made. The same is true of C. cacoucia regarding hummingbirds in America. Secondly, small whitish or pale fragrant ﬂowers are the commonest situation throughout the family, and are pollinated by a wide range of insects, including beetles, ﬂies, bees and butterﬂies. They usually have very well-developed nectaries inside the hypanthium, and are frequently grouped into larger clusters. In India, Srivastava (1993) found that four species of Terminalia were self-incompatible, and were visited by these orders of insects for both pollen and nectar. Thirdly, in tropical America the very widespread Combretum fruticosum and several related species (sect. Combretum) exhibit the ‘bottle-brush’ syndrome (cf. Australian Callistemon), with sessile, scentless, nectariferous ﬂowers crowded on an elongated axis and possessing long, rigid stamens, with the stigma and anthers at the same level. The whole ﬂower, of which the ﬁlaments are the most conspicuous part, starts yellow and then changes to red. These are pollinated primarily by hummingbirds (many direct observations), but other birds, butterﬂies and monkeys also play their part (Schemske 1980; Prance 1980). The species has been shown to be self-incompatible (Bernardello et al. 1994). In the self-compatible mangrove genus Lumnitzera, L. littorea has red ﬂowers with well-exposed anthers and is pollinated mainly by sunbirds and honeyeaters whereas L. racemosa has white ﬂowers and less-exposed anthers and is pollinated by various insects (Tomlinson 1986). Combretum lanceolatum is remarkable for producing a sweet, gelatinous secretion in form of pellets, rather than liquid nectar, which attracts a great diversity of bird visitors (Sazima et al. 2001).

Combretaceae

Dispersal. Present evidence suggests that species with winged fruits (mostly in savannah) are wind-dispersed, and those with succulent fruits (often riverine or in forest) are animal- or waterborne. In African savannah species of Combretum with large fruits, e.g. C. zeyheri, the wings probably act as sails as the fruit is blown along on the ground (Exell and Stace 1972). In Southeast Asia, Terminalia catappa is dispersed by both seawater and fructivorous bats (Exell 1954). Many species of Terminalia, as well as the two mangrove genera, have spongy rather than succulent fruits, often with airspaces in the mesocarp, and are well adapted for sea-dispersal. Phytochemistry. Ample phytochemical data on Combretaceae indicate that little insight is gained into relationships within the family, but that the position of the family in the Myrtales is strongly conﬁrmed (Dahlgren and Thorne 1984). Particularly characteristic are condensed tannins, gallyol-and ellagi-tannins; among the ﬂavonoids, the ﬂavonol myricetin, various O-methyl ﬂavonols, C-glycoﬂavones and proanthocyanidins (but no other ﬂavones or iridoids); only few alkaloids; and triterpene saponins. Skoczylas et al. (1994) reported long-chain rubber-like polyisoprenoid alcohols in leaves of Lumnitzera. Anderson and Bell (1977) found differences in the composition of gum exudates in seven African Combretum taxa, and Carr and Rogers (1987) described a method of identifying species of this genus from southern Africa by TLC ‘ﬁngerprints’ of polar constituents of leaf extracts. Laguncularia possesses gums similar to those of Combretum (Léon de Pinto et al. 1993). Large cells containing a single calcium oxalate druse are characteristic of the mesophyll of most (?all) genera; they frequently cause a pimple-like mound on the epidermis and/or pellucid dots when the leaf is held against the light. Subdivision and Relationships Within the Family. Strephonema, originally tentatively assigned to Lythraceae, differs from the rest of the genera in several characters and was separated as the subfamily Strephonematoideae by Engler and Diels (1899). Others have suggested a distinct family for it, but it possesses the diagnostic Combretaceous hairs and it consistently fell into the same single clade as the rest of the family in all the cladograms ﬁgured by Johnson and Briggs (1984). Most of the rest of the family (Combretoideae) forms two major groups based around Combretum

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and Terminalia respectively, ﬁrst recognized by de Candolle (1828), and later by Engler and Diels (1899, 1900) as the tribes Combreteae and Terminalieae. These have been variously distinguished (cotyledon folding, de Candolle 1828 and Engler and Diels 1899, 1900; presence of petals, Don 1832; presence of glandular trichomes, Stace 1965). Two groups of closely related, traditionally recognized genera form the cores of these two tribes respectively: Combretum, Meiostemon, Thiloa, Quisqualis and Calopyxis; and Terminalia, Terminaliopsis, Ramatuellea and Bucida. In addition, Buchenavia, Conocarpus, Anogeissus and Finetia also clearly belong to Terminalieae. Three other genera have variously been placed in tribes or subtribes of their own or subsumed into one of the above two: Guiera, tribe Guiereae (nom. nud.) (Venkateswarlu and Rao 1972); Calycopteris, tribe Calycopterideae (Engler and Diels 1899); and Pteleopsis, subtribe Pteleopsidinae (Exell and Stace 1966). All three have been placed in the Combreteae, and Pteleopsis also in Terminalieae (Vollesen 1981). In my view, Calycopteris is clearly a member of Combretinae, Pteleopsis of Terminaliinae, and Guiera is of uncertain afﬁnity. I have retained Guiera in Combretinae, as it possesses scales and petals, but it might almost equally belong to Terminaliinae or a separate subtribe; DNA sequences are highly desirable. Four additional genera, Laguncularia, Lumnitzera, Macropteranthes and Dansiea, form a well-deﬁned group which was once placed in Terminalieae or Combreteae, according to the character used to separate these tribes, but which was separated as a third tribe Laguncularieae by Engler and Diels (1899). Exell and Stace (1966) recognized 20 of the above 21 genera (Dansiea was not then described) in two subfamilies: the unigeneric Strephonematoideae and the Combretoideae. They considered Laguncularieae, with two prophylls fused to the hypanthium, to be more distinct than the rest of Combretoideae, which formed an enlarged Combreteae divided into three subtribes: Combretinae, Terminaliinae and the unigeneric Pteleopsidinae, which they thought did not fall into either of the other subtribes. Since then, Vollesen (1981) has presented clear evidence for merging the latter two subtribes. I have been unable to conﬁrm Johnson and Briggs’s (1984) assertion that Strephonema has a pair of prophylls, and therefore consider that those of Laguncularieae do indeed represent a synapomorphy. Despite this advanced character, it is likely

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that Laguncularieae are not an advanced group; the presence of petals, the ﬂoral vasculature and the hypanthium not separated into upper and lower portions are indicative of this. The main argument in Combretaceae classiﬁcation today is how many genera should be recognized among the ﬁve and four core genera listed above in Combretinae and Terminaliinae. A conservative classiﬁcation would recognize only one genus in each group, and it is probably true that separating any of the genera from Combretum or Terminalia respectively would leave the latter two paraphyletic. The types and taxonomic distribution of glandular trichomes in Combretinae support this view. Jongkind (1991, 1995a) argued for the inclusion of Quisqualis and Calopyxis in Combretum, just as Engler and Diels (1899, 1900) had done for Poivrea and Exell (1953) had done for Cacoucia, not on any theoretical basis but because the supposed differences could not be sustained; in fact, Cacoucia is as distinct from Combretum as is Calopyxis. The genera Thiloa and Meiostemon remain distinct, but they are probably no less closely evolutionarily related to Combretum subg. Combretum than are Cacoucia, Poivrea, Quisqualis and Calopyxis to Combretum subg. Cacoucia. In Terminaliinae, Terminaliopsis and Ramatuellea have few claims for separation from Terminalia, each representing specialized parts of the latter. Describing an apetalous species in the erstwhile petaliferous genus Pteleopsis, Vollesen (1981) considered that it could still be separated by the male ﬂowers being at the base of the inﬂorescence, not at the apex, as in Terminalia. However, there are species of Terminalia with basal male ﬂowers (sect. Ramatuellea), so there is no single character diagnosing Pteleopsis, although it remains a very distinctive taxon. The genus Bucida is traditionally separated from Terminalia by the retention of the upper hypanthium and calyx on the fruit. This character is, however, also found in three Madagascan Terminalia species of quite different facies (Capuron 1967), and in two other species from the Solomon Islands of yet different afﬁnity (Exell 1935), and one species of Bucida does not possess it constantly. In my view, only Combretum, Terminalia and Pteleopsis of the above 12 should be recognized at generic level. Molecular studies (plastid and rDNA ITS sequences) on eight genera and 18 species by Tan et al. (2001, 2002) have largely conﬁrmed the current suprageneric treatment. Strephonema is sister to the rest, and within the latter Laguncularieae (Lumnitzera, Laguncularia) are sister to the

remainder, which divide into Combretinae (Combretum including former Quisqualis, Calycopteris) and Terminaliinae (Terminalia, Anogeissus, Conocarpus). More recently, Sytsma et al. (2004) sequenced four genera (three at present recognized) and obtained rather different results, Conocarpus being sister to Terminalia (including Bucida) plus Combretum (as Quisqualis). Clearly, much more molecular work is required. Afﬁnities. Combretaceae were considered one of 14 “core families of Myrtales” by Dahlgren and Thorne (1984), but “any close connections [to any of the other 13 families] are not obvious”. In Johnson and Briggs’s (1984) main cladograms, based on 77 morphological and anatomical characters, the sister clade to a clade containing only Combretaceae contained seven of the other core families: Penaeaceae, Alzateaceae, Oliniaceae, Rhynchocalycaceae, Crypteroniaceae, Memecylaceae and Melastomataceae. Despite the possession of Combretaceous hairs by some of their members, Myrtaceae were more distant. In Conti et al.’s (1996) cladistic analysis of rbcL sequence data, a different result was obtained: Combretaceae formed a clade along with Onagraceae and Lythraceae which was sister to all the other Myrtales (the above seven plus four other families). Similarly, Soltis et al.’s (2000) analysis of seven of the families using 18S rDNA, rbcL and atpB sequences revealed three unresolved subclades – Combretaceae, Onagraceae and Lythraceae – and four other families. The Angiosperm Phylogeny Group classiﬁcation (APG II 2003) recognizes the Myrtales with 14 families, 13 of which are the same as those of Dahlgren and Thorne (1984) (Trapaceae merged into Lythraceae; Vochysiaceae added). Sytsma et al. (2004) found Combretaceae to be sister to all the other 13 families combined. There is thus agreement that Combretaceae are a distinct family which diverged early (perhaps ﬁrst) in the evolution of Myrtales. Distribution and Habitats. Combretaceae occur throughout the tropics, with short extensions into warm temperate zones, i.e. to 37◦ 15 S in Argentina, 33◦ 46 S in South Africa and c. 26◦ S in Australia, and to 28◦ 30 N in Florida, 29◦ N in Baja California, 32◦ 20 N in Bermuda, 29◦ 30 N in China and c. 31◦ N in India. The two large genera, Combretum and Terminalia, occur in all continents (Combretum not discovered in Australia until 1980). The greatest genetic diversity of Combretum is in Africa, that of Terminalia in Southeast Asia.

Combretaceae

One mangrove, Laguncularia, occurs in both America (east and west coasts) and West Africa, and the other, Lumnitzera, from East Africa to Australia. The mangrove-associate, Conocarpus, has a similar distribution to Laguncularia, but there is also a second non-mangrove species (C. lancifolius) in northeast Africa and Arabia. Anogeissus occurs in both Africa and Asia, but the other seven genera are conﬁned to one continent. There are only three amphi-Atlantic species: Laguncularia racemosa, Conocarpus erectus and Terminalia lucida. Combretaceae can be important constituents of forest, savannah and mangrove-swamp, and occur from sea level to (in Southeast Asia) over 3,000 m altitude. In parts of southern Africa, several species of Combretum, viz. C. zeyheri, C. molle, C. apiculatum, C. hereroense and C. mossambicense (Exell 1978), are characteristic and hence indicators of cupriferous soils. Palaeobotany. Friis et al. (1992) described ﬂowers (Esgueiria adenocarpa E.M. Friis, K.R. Pedersen & P.R. Crane and E. miraensis E.M. Friis, K.R. Pedersen & P.R. Crane) from the Late Cretaceous of Portugal which they ascribed to Combretaceae. They had an inferior unilocular ovary with three stylodia and up to six apical anatropous ovules, ﬁve sepals and ﬁve sepals borne on the top of the ovary, and eight stamens (in two whorls of three and ﬁve) borne on the top of the ovary. The ovary and sepals had abundant simple hairs and peltate scales. Overall, there is good concordance between the features of Esgueiria and Combretaceae, but conﬁrmation of the family status could only be made from anatomical analysis of the hairs; the photographs provided suggest that they might be Combretaceous. Primitive characters would be the three stylodia and the absence of an upper hypanthium. There are many earlier records of fossil supposed Combretaceae, involving wood, leaves, ﬂowers, fruits and pollen from the Mid-Cretaceous (c. 100 Ma b.p.) onwards, all ascribed to modern genera or to fossil genera based on modern names. However, the evidence of them belonging to Combretaceae is tenuous and based on gross morphology only, except perhaps in the case of the Late Cretaceous and Tertiary wood Terminalioxylon (Friis et al. 1992). Economic Importance. Combretaceae are not of great worldwide economic importance. The larger species of Terminalia are valued as timber trees, mostly for local uses but in some cases in

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the European and American markets, e.g. the West African T. ivorensis (‘idigbo’) and T. superba (‘afara’), the American T. amazonia (‘nargusta’ or ‘roblé coral’) and T. oblonga (‘sura’), and the Asian T. elliptica (‘Indian laurel’), T. cuneata (T. arjuna, ‘kumbuk’) and T. bialata (‘chuglam’). In the West Indies, Laguncularia is valued for fence-posts and Conocarpus for fuel. The fruit of several species of Terminalia (e.g. T. catappa, ‘Indian almond’) have edible kernels, as do species of Combretum sect. Calopyxis in Madagascar; in South America, Asia and Africa, several species of Combretum and Terminalia are commercial sources of gums; in Asia, the fruits of certain species (e.g. T. chebula) known collectively as ‘myrobalans’ are important for dyeing and tanning. Dalziel (1937) has 11 pages of entries for Combretaceae. Species of Terminalia, especially T. catappa throughout the tropics, are much grown as shade plants, and of Combretum (including former Calopyxis and Quisqualis) as ornamentals.

Key to the Genera 1. Ovary semi-inferior, the calyx-tube arising from its sides; seeds with massive hemispherical cotyledons 1. Strephonema – Ovary inferior, the hypanthium extended from its apex; seeds with ﬂattened, usually variously folded cotyledons 2 2. Hypanthium with 2 adnate prophylls (sometimes developed as wings) 3 – Hypanthium without adnate prophylls 6 3. Prophylls not accrescent and not forming wings to the fruit; thick-leaved mangroves 4 – Prophylls accrescent to form 2 wings to the fruit; plants not mangroves 5 4. Leaves opposite, with minute narrow-oriﬁced pits on both surfaces; hypanthium (above ovary) < 5 mm; petals pubescent, < 2 mm 2. Laguncularia – Leaves spiral, without surface pits; hypanthium (above ovary) > 5 mm; petals glabrous, > 3 mm 3. Lumnitzera 5. Hypanthium adnate to ovary all round; nectariferous disk forming an intrastaminal ring at base of hypnthium 4. Macropteranthes – Hypanthium adnate to ovary on ventral side only; nectary a 2-lobed outgrowth on inner dorsal side of hypanthium 5. Dansiea 6. Fruits aggregated into ‘cones’ (Alnus-like but without persistent bracts) 7 – Fruits not aggregated into Alnus-like ‘cones’ 9 7. Fruits without terminal beak, strongly recurved at apex 11. Conocarpus – Fruits with terminal beak, not recurved at apex 8 8. Ovary and fruit 2-winged; beak of fruit formed from whole of distal stalk-like part of lower hypanthium 9. Anogeissus

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– Ovary and fruit 4-ridged; beak of fruit formed from only lower half of distal stalk-like part of lower hypanthium 10. Finetia 9. Calyx-lobes accrescent, forming 5 terminal fruit-wings 13. Calycopteris – Calyx-lobes not or scarcely accrescent, not forming fruit-wings 10 10. Petals usually present, rarely absent; leaves and inﬂorescences with glandular trichomes (stalked glands and/or scales) 11 – Petals usually absent, sometimes present; leaves and inﬂorescences without glandular trichomes 12 11. Fruits in radiating capitate clusters, linear to narrowly fusiform, with persistent upper hypanthium 14. Guiera – Fruits not in radiating clusters, not linear, without persistent upper hypanthium 12. Combretum 12. Anthers adnate to ﬁlaments; fruit a wingless pseudodrupe 8. Buchenavia – Anthers dorsiﬁxed and versatile; fruit various 13 13. Andromonoecious, with bisexual ﬂowers restricted to apex of rhachis; all ﬂowers long-stalked 7. Pteleopsis – All ﬂowers bisexual or, if andromonoecious with bisexual ﬂowers restricted to apex of rhachis, at least bisexual ﬂowers sessile or more or less so 6. Terminalia

Genera of Combretaceae I. Subfam. Strephonematoideae Engl. & Diels (1899). Trees; ovary semi-inferior; cotyledons conduplicate, hemispherical, massive; stomata paracytic; wood with tangential bands of apotracheal parenchyma; pollen tricolporate; one- and twoarmed Combretaceous hairs present; glandular trichomes absent; petals present. 1. Strephonema Hook. f.

Fig. 21

Strephonema Hook. f. in Benth. & Hook. f., Gen. Pl. 1:782 (1867); Jongkind, Ann. Missouri Bot. Gard. 82:535–541 (1955), rev.

Characters of subfamily; leaves spiral, without petiolar glands, with basal revolute domatia; inﬂorescences axillary, subumbellate to elongated simple to compound racemes; ﬂowers (4–)5merous, bisexual, pedicellate; stamens 10, with versatile anthers; ovules 2; germination hypogeal. Three species, western tropical Africa. II. Subfam. Combretoideae Engl. & Diels (1899). Trees, shrubs, mangroves or lianes; ovary inferior; cotyledons ﬂattened, variously folded or rarely

Fig. 21. Combretaceae. Strephonema sericea. A Flowering branch. B Flower with subtending bract. C Flower, vertical section. D Fruit. E Fruit, half of pericarp and seed-coat removed. (Engler and Diels 1900)

conduplicate; stomata anomocytic (or cyclocytic); wood without tangential bands of apotracheal parenchyma; pollen tricolporate or heterocolpate; only one-armed Combretaceous hairs present; glandular trichomes present or absent; petals present or absent. II.1. Tribe Laguncularieae Engl. & Diels (1899). Trees, shrubs or mangroves; stomata anomocytic or cyclocytic; cotyledons spirally convolute; leaves with isobilateral or weakly isobilateral anatomy; stalked glandular trichomes absent; hypanthium with 2 adnate prophylls; upper and lower hypanthia scarcely differentiated; petals present; anthers versatile; chromosome base number 13 (as far as is known). 2. Laguncularia C.F. Gaertn.

Fig. 22

Laguncularia C.F. Gaertn., Suppl. Carp. 209, t. 217 (1807); Exell, Ann. Missouri Bot. Gard. 45:162–164 (1958); Stace, Fl. Venez. Guayana 4:344 (1998).

Mangroves, often with pneumatophores; leaves opposite, with pair of petiolar glands, with sessile glands in minute sunken pits, without marginal

Combretaceae

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or pedicellate; nectary a disk; petals glabrous; stamens 5–10; ovules 2–5; fruit unwinged; germination hypogeal. Two species, East tropical Africa to Australia. 4. Macropteranthes F. Muell. Macropteranthes F. Muell., Fragm. 3:151 (1863); Pedley, Fl. Australia 18:256–260 (1990).

Trees or shrubs; leaves spiral or opposite, without petiolar glands, with glands on margin near base; inﬂorescence axillary, of (1–)2 ﬂowers; hypanthium adnate all round ovary, its prophylls accrescent to form winged fruit; ﬂowers 5-merous, bisexual, sessile or pedicellate; nectary a disk; petals pubescent; stamens 10; ovules 6–12; germination epigeal. Five species, Australia. 5. Dansiea Byrnes Dansiea Byrnes, Austrobaileya 1:385 (1981); Pedley, Fl. Australia 18:260–262 (1990).

Fig. 22. Combretaceae. Laguncularia racemosa. A Fruiting branch. B Flower buds with bracts. C Petal and stamen. D Style, disk and ovules (below). E Immature fruits. F Fruit, vertical section. G Fruit, transverse section. h = hypocotyl, c = cotyledons. (Engler and Diels 1900)

glands; inﬂorescence a terminal panicle of spikes; hypanthium adnate all round ovary, its prophylls not accrescent; ﬂowers 5-merous, bisexual to dioecious, sessile; nectary a disk; petals pubescent; stamens 10; ovules 2; fruit unwinged; germination epigeal. One species, L. racemosa (L.) C.F. Gaertn., eastern and western tropical America, western tropical Africa. 3. Lumnitzera Willd. Lumnitzera Willd., Gesell. Naturf. Freunde Berlin N. S. 4:186 (1803); Exell, Fl. Males. I, 4:585–589 (1954); Gangopadhyay & Chakrabarty, J. Econ. Tax. Bot. 21:325–329 (1997), rev.

Mangroves, often with pneumatophores; leaves spiral, without petiolar glands, with glands on margin; inﬂorescence a terminal raceme or axillary spike; hypanthium adnate all round ovary, its prophylls not accrescent; ﬂowers 5-merous, bisexual, sessile

Trees; leaves spiral to subopposite, without petiolar glands, with glands on margin near base; inﬂorescence axillary, of (1–)2 ﬂowers; hypanthium adnate to ovary on ventral side only, its prophylls accrescent to form winged fruit; ﬂowers 5-merous, bisexual, subsessile; nectary a dorsal outgrowth; petals pubescent; stamens 10; ovules 14–20; germination? Two species, Australia. II.2. Tribe Combreteae DC. (1828). Trees, shrubs or lianes; stomata anomocytic; cotyledons conduplicate, spirally convolute or irregularly complicate; leaves usually with dorsiventral, sometimes with isobilateral, anatomy; stalked glandular trichomes present or absent; hypanthium without adnate prophylls; upper and lower hypanthia well differentiated; petals 4–5 or 0; anthers versatile or adnate; chromosome base number 12 or 13. II.2. a. Subtribe Terminaliinae (DC.) Exell & Stace (1966). Terminalieae [Terminaliées] DC. (1828). Pteleopsidinae Exell & Stace (1966).

Trees or shrubs; leaves usually spiral, usually with dorsiventral, sometimes with isobilateral, anatomy; petiolar glands often present; scales absent; stalked glands usually absent; ﬂowers bisexual or andromonoecious, rarely dioecious,

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sessile; petals usually absent, sometimes present; anthers versatile or adnate; cotyledons spirally convolute; fruit usually with hard sclerenchymatous endocarp; wood without vessels of 2 very distinct diameters and without rays with radial vessels; chromosome base number usually 12. 6. Terminalia L.

Fig. 23

Terminalia L., Syst. Nat., ed. 12, 2:674 (1767) & Mant. Pl. 21 (1767), nom. cons.; Alwan, Taxonomy Terminalia (Combretaceae) & related genera (1983), reg. rev.; Capuron, Combretacées arbust. arbor. Madagascar: 9–96 (1967); Coode, Man. forest trees Papua New Guinea, 1, Combretaceae: 5–78 (1969); Exell, Fl. Males. I, 4:548–584 (1954); Exell, Fl. Zambesiaca 4:166–181 (1978); Gangopadhyay & Chakrabarty, J. Econ. Tax. Bot. 21:334–362 (1997), reg. rev.; Grifﬁths, J. Linn. Soc., Bot. 55:818–907 (1959), reg. rev. Bucida L. (1759), nom. cons. Ramatuellea Kunth in Humb. (1825) (‘Ramatuela’, ‘Ramatuella’). Terminaliopsis Danguy (1923).

Trees. Leaves spiral, often with pocket-shaped or bowl-shaped domatia, frequently with petiolar glands; stalked glands 0; inﬂorescence an axillary lax to congested spike, the spikes often clustered

at branchlet-ends, rarely the spikes branched; ﬂowers bisexual or plants andromonoecious, the male ﬂowers basal, apical or mixed, at least the bisexual ones sessile, 5- or rarely 4-merous; upper hypanthium sometimes persistent in fruit; petals absent; stamens usually (4–5, 8)10; anthers versatile; fruit 2- to 5-winged or -ridged or ± terete, radially symmetrical or ﬂattened, dry or succulent; chromosome base number usually 12. About 190 species, pantropical. 7. Pteleopsis Engl. Pteleopsis Engl., Abh. Königl. Akad. Wissensch. Berlin 1894: 25 (1894); Exell, Fl. Zambesiaca 4:162–166 (1978).

Leaves spiral, subopposite or opposite, without domatia, without petiolar glands; stalked glands 0; inﬂorescence an axillary congested spike, the spikes often clustered at branchlet-ends; plants andromonoecious, ﬂowers long-stalked, 5- or 4-merous; upper hypanthium deciduous before fruiting; petals usually present (absent in P. apetala Vollesen); stamens 10 or 8; anthers versatile; fruit 2-winged, ﬂattened, dry. About 10 species, Africa. 8. Buchenavia Eichler Buchenavia Eichler, Flora 49:164 (1866), nom. cons.; Exell & Stace, Bull. Brit Mus. (Nat. Hist.), Bot. 3:1–46 (1963), rev.; Alwan, Taxonomy Terminalia (Combretaceae) & related genera (1983).

Leaves spiral, often with pocket-shaped or rarely bowl-shaped domatia, usually with petiolar glands; stalked glands 0; inﬂorescence an axillary lax to congested spike, the spikes usually clustered at branchlet-ends; ﬂowers bisexual, sessile, 5-merous; upper hypanthium deciduous before fruiting; petals absent; stamens 10; anthers adnate to ﬁlaments; fruit 5-ridged or ± terete, radially symmetrical or rarely slightly ﬂattened, succulent. Twenty species, tropical America. 9. Anogeissus (DC.) Wall. Anogeissus (DC.) Wall., Numer. List no. 4014 (1831); Scott, Kew Bull. 33:555–566 (1979), rev. Conocarpus sect. Anogeissus DC. (1828).

Fig. 23. Combretaceae. Terminalia brownii. A Flowering branch. B Flower, vertical section. C Part of infructescence. D Fruit, transverse section. (Engler and Diels 1900)

Leaves spiral, opposite or subopposite, usually with dorsiventral anatomy, sometimes with pocket-shaped domatia, without petiolar glands; stalked glands absent; inﬂorescence a solitary or a raceme or compound raceme of compact conelike spikes; ﬂowers bisexual, sessile, 5-merous; upper hypanthium deciduous before fruiting;

Combretaceae

petals absent; stamens 10; anthers versatile; fruit 2-winged, ﬂattened, dry and achene-like, retaining whole of distal stalk-like part of lower hypanthium at fruiting; chromosome base number 12. Seven species, western tropical Africa to Southeast Asia.

Finetia Gagnep., Notul. Syst. (Paris) 3:278 (1917); Scott, Kew Bull. 33:555–566 (1979), rev. Anogeissus sect. Finetia (Gagnep.) A.J. Scott (1979).

Leaves opposite or subopposite, without domatia, without petiolar glands; stalked glands 0; inﬂorescence a solitary or a raceme of compact cone-like spikes; ﬂowers bisexual, sessile, 5-merous; upper hypanthium deciduous before fruiting; petals absent; stamens 10; anthers versatile; fruit 4-ribbed, slightly ﬂattened, dry and achene-like, retaining only lower half of distal stalk-like part of lower hypanthium at fruiting. One species, F. rivularis (Gagnep.) Lecomte, Thailand and Laos. 11. Conocarpus L.

or irregularly complicate; fruit without hard sclerenchymatous endocarp; wood with vessels of 2 very distinct diameters and with rays with radial vessels; chromosome base number 12 or 13. 12. Combretum Loeﬂ.

10. Finetia Gagnep.

Fig. 20

Conocarpus L., Sp. Pl.: 176 (1753); Exell, Ann. Missouri Bot. Gard. 45:161–162 (1958), reg. rev.

Mangrove-like shrubs or trees, without pneumatophores; leaves spiral with bowl-shaped domatia and petiolar glands; minute stalked glands present; inﬂorescence a raceme or compound raceme of compact cone-like spikes; ﬂowers bisexual to dioecious, sessile, 5-merous; upper hypanthium deciduous before fruiting; petals 0; stamens (5–)10; anthers versatile; fruit 2-winged, ﬂattened, dry; chromosome base number 12. Two species, one (C. erectus L.) a mangrove-associate in western and eastern tropical America and western tropical Africa, the other (C. lancifolius Engl.) a tree of sandy soils in Northeast Africa and southern Yemen. II.2. b. Subtribe Combretinae Exell & Stace (1966). Calycopterideae Engl. & Diels (1899).

Trees, shrubs or lianes; leaves usually opposite, usually with dorsiventral anatomy; petiolar glands 0; stalked glandular trichomes (stalked glands and/or scales) present; ﬂowers bisexual (dioecious, one species of Combretum), usually sessile; petals usually present; anthers versatile; pollen heterocolpate; cotyledons conduplicate, spirally convolute

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Figs. 24, 25

Combretum Loeﬂ., Iter Hispan. 308 (1758), nom. cons.; Engler & Diels, Monographieen afrikanischer PﬂanzenFamilien und -Gattungen, III & IV (1899–1900), reg. rev.; Exell, J. Bot. 69:116–124 (1931), part. rev.; Exell, J. Linn. Soc., Bot. 55:103–141 (1953), reg. rev.; Exell & Stace, Bol. Soc. Brot. II, 40:19 (1966), part. rev.; Gangopadhyay & Chakrabarty, J. Econ. Tax. Bot. 21:297–325, 329–334 (1997), reg. rev.; Jongkind, Bull. Mus. Natl Hist. Nat., B, Adansonia 17:191–200 (1995), reg. rev.; Stace, Bull. Torrey Bot. Club 95:156–165 (1968), part. rev. Quisqualis L. (1762). Cacoucia Aubl. (1775). Poivrea Comm. ex Thouars (1811). Calopyxis Tul. (1856). Thiloa Eichler (1866). Meiostemon Exell & Stace (1966).

Shrubs or lianes, rarely trees. Leaves opposite, sometimes verticillate; stalked glands and/or scales present; ﬂowers 4-or 5-merous, usually sessile, sometimes stalked; upper hypanthium and calyx deciduous before fruiting; petals usually present, sometimes 0; stamens usually 8 or 10 (rarely more), sometimes 4; fruit 4- to 5-winged or -ridged or ± terete, dry or succulent, not achene-like; cotyledons conduplicate, spirally convolute or irregularly complicate; chromosome base number usually 13. About 255 species, pantropical except Paciﬁc islands and most of Australia. Three subgenera are recognized: subg. Combretum, with peltate scales and usually with petals (about 150 spp. in about 33 sections, including Meiostemon and Thiloa); subg. Cacoucia (Aubl.) Exell & Stace, with stalked glands and usually with petals (about 104 spp. in about 17 sections, including Poivrea, Cacoucia, Quisqualis and Calopyxis); subg. Apetalanthum Exell & Stace, with stalked glands and scales, and without petals (one species). 13. Calycopteris Lam. Calycopteris Lam., Tabl. Encycl. 1:485, t. 357 (1793); Exell, Fl. Males. I, 4:584–585 (1954). Getonia Roxb. (1798).

Scrambling shrubs. Leaves opposite or subopposite; scales present; ﬂowers 5-merous, ± sessile; upper hypanthium persistent in fruit, with accrescent

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Fig. 25. Combretaceae. Combretum poggei (subg. Cacoucia). A Flowering branch. B Flower, vertical section. C Fruit. D Fruit, transverse section. (Engler and Diels 1899) Fig. 24. Combretaceae. Combretum bongense (subg. Combretum). A Flowering branch. B Flower bud. C Flower, vertical section. D Leaf underside. E Leaf, transverse section, showing a scale. (Engler and Diels 1899)

calyx forming 5 wings; petals absent; stamens 10; fruit dry, achene-like; cotyledons irregularly complicate; chromosome base number 13. One species, C. ﬂoribunda (Roxb.) Lam., Southeast Asia.

Shrubs; leaves opposite or subopposite; scale-like glandular trichomes present; ﬂowers 5-merous, sessile; upper hypanthium persistent in fruit; petals present; stamens 10; fruit dry, achene-like; cotyledons spirally convolute; chromosome base number 12. One species, G. senegalensis J.F. Gmel., western tropical Africa.

Selected Bibliography 14. Guiera Adans. ex Juss. Guiera Adans. ex Juss., Gen. Pl.: 320 (1789).

Adamson, R.S. 1910. Note on the roots of Terminalia arjuna Bedd. New Phytol. 9:150–156.

Combretaceae Alwan, A.-R.A. 1983. The taxonomy of Terminalia (Combretaceae) and related genera. Ph.D. Thesis, University of Leicester. Anderson, D.M.W., Bell, P.C. 1977. The composition of the gum exudates from some Combretum species; the botanical nomenclature and systematics of the Combretaceae. Carbohyd. Res. 57:215–221. APG II 2003. See general references. Behnke, H.-D. 1984. Ultrastructure of sieve-element plastids of Myrtales and allied groups. Ann. Missouri Bot. Gard. 71:824–831. Bernardello, L., Galetto, L., Rodgriguez, I.G. 1994. Reproductive biology, variability of nectar features and pollination of Combretum fruticosum (Combretaceae) in Argentina. Bot. J. Linn. Soc. 114:293–308. Brandis, D. 1893. Combretaceae. In: Engler, A., Prantl, K., Die natürlichen Pﬂanzenfamilien III, 7. Leipzig: W. Engelmann, pp. 106–130. Candolle, A.P. de 1828. Combretaceae. In: Prodromus systematis naturalis regni vegetabilis, 3. Paris: Treuttel & Würtz, pp. 9–24. Capuron, R. 1967. Les Combretacées arbustives ou arborescentes de Madagascar. Madagascar: Centre Technique Forestier Tropicale. Carr, J.D., Rogers, C.B. 1987. Chemosystematic studies of the genus Combretum (Combretaceae), I. A convenient method of identifying species of this genus by a comparison of the polar constituents extracted from leaf material. S. African J. Bot. 53:173–176. Conti, E. et al. 1996. See general references. Coode, M.J.E. 1969. Manual of the forest trees of Papua and New Guinea. Part 1, revised. Combretaceae. Lae: Department of Forests. Coode, M.J.E. 1973. Notes on Terminalia L. (Combretaceae) in Papuasia. Contr. Herb. Austral. 2:1–33. Corner, E.J.H. 1940. Wayside trees of Malaya. Singapore: Government Printing Ofﬁce. Dahlgren, R., Thorne, R.F. 1984. The order Myrtales: circumscription, variation and relationships. Ann. Missouri Bot. Gard. 71:633–699. Dalziel, J.M. 1937. The useful plants of West Tropical Africa. London: Crown Agents. Don, G. 1832. Combretaceae. In: A general history of the dichlamydeous plants, 2. London: Rivington, pp. 655– 668. El Ghazali, G.E.B. 1993. A study on the pollen ﬂora of Sudan. Rev. Palaeobot. Palynol. 76:99–345. El Ghazali, G.E.B., Tsuji, S., El Ghazali, G.A., Nilsson, S. 1998. Combretaceae. In: Nilsson, S. (ed.) World Pollen and Spore Flora, 21. Oslo: Scandinavian University Press. Engler, A., Diels, L. 1899. Monographien afrikanischer Pﬂanzen-Familien und -Gattungen, III. Combretaceae africanae (I) Combretum. Leipzig: W. Engelmann. Engler, A., Diels, L. 1900. Monographien afrikanischer Pﬂanzen-Familien und -Gattungen, IV. Combretaceae africanae (II) excl. Combretum. Leipzig: W. Engelmann. Exell, A.W. 1931. The genera of Combretaceae. J. Bot. 69:113–128. Exell, A.W. 1935. Species of Terminalia from the Solomon Is. J. Bot. 73:131–134. Exell, A.W. 1953. The Combretum species of the New World. J. Linn. Soc., Bot. 55:103–141.

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Exell, A.W. 1954. Combretaceae. In: Steenis, C.G.G.J. van (ed.) Flora Malesiana I, 4:533–628. Djakarta: Noordhoff-Kolff. Exell, A.W. 1962. Space problems arising from the conﬂict between two evolutionary tendencies in the Combretaceae. Bull. Soc. Roy. Bot. Belgique 95:41–49. Exell, A.W. 1978. Combretaceae. In: Launert, E. (ed.) Flora Zambesiaca 4:100–183. London: Flora Zambesiaca Managing Committee. Exell, A.W., Stace, C.A. 1966. Revision of the Combretaceae. Bol. Soc. Brot. II, 40:5–25. Exell, A.W., Stace, C.A. 1972. Patterns of distribution in the Combretaceae. In: Valentine, D.H. (ed.) Taxonomy, phytogeography and evolution. London: Academic Press, pp. 307–323. Friis, E.M., Pedersen, K.R., Crane, P.R. 1992. Esgueiria gen. nov., fossil ﬂowers with combretaceous features from the Late Cretaceous of Portugal. Biol. Skr. 41:1–45. Fukuoka, N., Ito, M., Iwatsuki, K. 1986. Floral anatomy of the mangrove genus Lumnitzera (Combretaceae). Acta Phytotax. Geobot. 37:69–81. Grifﬁths, M.E. 1959. A revision of the African species of Terminalia. J. Linn. Soc., Bot. 55:818–907. Heiden, H. 1893. Anatomische Characteristik der Combretaceen. Bot. Centralbl. 55:353–360, 385–391; 56:1–12, 65–75, 129–136, 163–170, 193–200, 225–230. Hickey, L.J. 1973. Classiﬁcation of the architecture of dicotyledonous leaves. Amer. J. Bot. 60:17–33. Jackson, G. 1974. Cryptogeal germination and other seedling adaptations to the burning of vegetation in savanna regions: the origin of the pyrophytic habit. New Phytol. 73:771–780. Jeník, J. 1970. Root system of tropical trees, 5. The pegroots and the pneumathodes of Laguncularia racemosa Gaertn. Preslia 42:105–113. Johnson, L.A.S., Briggs, B.G. 1984. Myrtales and Myrtaceae –a phylogenetic analysis. Ann. Missouri Bot. Gard. 71:700–756. Jongkind, C.C.H. 1991. Novitates Gabonenses, 6. Some critical observations on Combretum versus Quisqualis (Combretaceae) and description of two new species of Combretum. Bull. Mus. Natl Hist. Nat., B, Adansonia 12:275–280. Jongkind, C.C.H. 1995a. Prodromus for a revision of Combretum (Combretaceae) for Madagascar. Bull. Mus. Natl Hist. Nat., B, Adansonia 17:191–200. Jongkind, C.C.H. 1995b. Review of the genus Strephonema (Combretaceae). Ann. Missouri Bot. Gard. 82:535–541. Jongkind, C.C.H. 1998. Combretaceae. In: Morat, P. (ed.) Flore du Gabon, 35. Paris: Association de Botanique Tropicale. Keating, R.C. 1984. Leaf histology and its contribution to relationships in the Myrtales. Ann. Missouri Bot. Gard. 71:801–823. Keay, R.W.J. 1950. The systematic position of suffrutescent species of Combretum Loeﬂ. Kew Bull. 5:255–257. Klucking, E.P. 1991. Leaf Venation Patterns, 5. Combretaceae. Berlin: J. Cramer. Léon de Pinto, G., Nava, M., Martínez, M., Rivas, C. 1993. Gum polysaccharides of nine specimens of Laguncularia racemosa. Biochem. Syst. Ecol. 21:463–466. Ohri, D. 1996. Genome size and polyploidy variation in the tropical hardwood genus Terminalia (Combretaceae). Pl. Syst. Evol. 200:225–232.

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Ohri, D., Kumar, A. 1986. Nuclear DNA amounts in some tropical hardwoods. Caryologia 39:303–307. Onyekwelu, S.S.C. 1990. Germination, seedling morphology and establishment of Combretum bauchiense Hutch. & Dalz. (Combretaceae). Bot. J. Linn. Soc. 103:133– 138. Outer, R.W. den, Fundter, J.M. 1976. The secondary phloem of some Combretaceae and the systematic position of Strephonema pseudocola A. Chev. Acta Bot. Neerl. 25:481–493. Patel, V.C., Skvarla, J.J., Raven, P.H. 1985. Pollen characters in relation to the delimitation of Myrtales. Ann. Missouri Bot. Gard. 71:858–969. Pedley, L. 1990. Combretaceae. In: George, A.S. (ed.) Flora of Australia 18:255–293. Canberra: AGPS Press. Prance, G.T. 1980. A note on the probable pollination of Combretum by Cebus monkeys. Biotropica 12: 239. Sazima, M., Vogel, S., Prado, A.L. do, Oliveira, D.M. de, Franz, G., Sazima, I. 2001. The sweet jelly of Combretum lanceolatum ﬂowers (Combretaceae): a cornucopia resource for bird pollinators in the Pantanal, western Brazil. Pl. Syst. Evol. 227:195–208. Schemske, D.W. 1980. Floral ecology and hummingbird pollination of Combretum farinosum in Costa Rica. Biotropica 12:169–181. Skoczylas, E., Swiezewska, E., Chojnacki, T., Tanaka, Y. 1994. Long-chain rubber-like polyisoprenoid alcohols in leaves of Lumnitzera racemosa. Pl. Physiol. Biochem. (Montrouge) 32:1–5. Solereder, H. 1908. Systematic anatomy of the dicotyledons. Transl. Boodle, L.A., Fritsch, F.E.; revised Scott, D.H. Oxford: Clarendon Press. Soltis, D.E. et al. 2000. See general references. Srivastava, P.K. 1993. Pollination mechanisms in genus Terminalia Linn. Indian Forester 119:147–150. Srivastava, P.K., Raina, S.N., Thangalevu, K. 2001. Nuclear DNA and fruit (seed) variation in section Pentaptera of genus Terminalia Linn. Indian Forester 128:289– 295. Stace, C.A. 1965. The signiﬁcance of the leaf epidermis in the taxonomy of the Combretaceae, I. A general review of tribal, generic and speciﬁc characters. J. Linn. Soc., Bot. 59:229–252. Stace, C.A. 1966. The use of epidermal characters in phylogenetic considerations. New Phytol. 65:304–318. Stace, C.A. 1968. A revision of the genus Thiloa (Combretaceae). Bull. Torrey Bot. Club 95:156–165.

Stace, C.A. 1981. The signiﬁcance of the leaf epidermis in the taxonomy of the Combretaceae; conclusions. Bot. J. Linn. Soc. 81:327–339. Sytsma, K.J. et al. 2004. See general references. Tan, F.-X., Shi, S.-H., Huang, Y.-L., Du, Y.-Q., Wang, Y.-G., Gong, X. 2001. Analysis of nrDNA ITS sequences in the subfamily Combretoideae (Combretaceae) and its systematic signiﬁcance. Acta Bot. Yunnanica 23:239– 242. Tan, F.-X., Shi, S.-H., Zhong, Y., Gong, X., Wang, Y.-G. 2002. Phylogenetic relationships of Combretoideae (Combretaceae) inferred from plastid, nuclear gene and spacer sequences. J. Pl. Res. 115:475–481. Tilney, P.M. 2002. A contribution to the leaf and young stem anatomy of the Combretaceae. Bot. J. Linn. Soc. 138:163–196. Tobe, H., Raven, P.H. 1983. An embryological analysis of Myrtales: its deﬁnition and characteristics. Ann. Missouri Bot. Gard. 70:71–94. Tomlinson, P.B. 1986. The Botany of mangroves. Cambridge: Cambridge University Press. Valente, M. da C., Marquete Ferreira da Silva, N., Guimarães, D.J. 1989. Morfologia e anatomia do fruto de Combretum rotundifolium Rich. (Combretaceae). Rodriguésia 67:45–51. Valente, M. da C., Marquete Ferreira da Silva, N., Guimarães, D.J. 1994. Morfologia e anatomia do fruto de Laguncularia racemosa (L.) Gaertn. f. (Combretaceae). Arch. Jard. Bot. Rio de Janeiro 32:39–50. Venkateswarlu, J., Rao, P.S.P. 1970. The ﬂoral anatomy of Combretaceae. Proc. Indian Natl Sci. Acad., B, 36:1–20. Venkateswarlu, J., Rao, P.S.P. 1972. Embryological studies in some Combretaceae. Bot. Notiser 125:161–179. Verhoeven, R.L., Schijff, H.P. van der 1974. Anatomical aspects of Combretaceae in South Africa. Phytomorphology 24:158–164. Vliet, C.J.C.M. van 1979. Wood anatomy of the Combretaceae. Blumea 25:141–223. Vliet, C.J.C.M. van, Raven, P.H. 1984. Wood anatomy and classiﬁcation of the Myrtales. Ann. Missouri Bot. Gard. 71:783–800. Vollesen, K. 1981. Pteleopsis apetala sp. nov. (Combretaceae) and the delimitation of Pteleopsis and Terminalia. Nordic J. Bot. 1:329–332. Weberling, F. 1988. The architecture of inﬂorescences in the Myrtales. Ann. Missouri Bot. Gard. 75:226–310.

Crassulaceae Crassulaceae DC. in Lam. & DC., Fl. Franç., ed. 3, 4, 1: 382 (1805), nom. cons. J. Thiede and U. Eggli1

Perennial or rarely annual or hapaxanthic herbs to (sub)shrubs, rarely aquatics, treelike, epiphytic or scandent, with ± succulent leaves, sometimes with succulent stems, rhizomes, underground caudices or succulent roots; indumentum of unior multicellular, often glandular hairs, or plants glabrous. Leaves (sub)sessile or rarely petiolate, usually alternate and spiral, or opposite-decussate or rarely whorled, frequently aggregated into rosettes, simple, rarely compound, usually entire or crenate to lobed, rarely dissected, estipulate. Inﬂorescences usually terminal, bracteate, usually many-ﬂowered, basically thyrsoids, also pleio-, di-or monochasia (cincinni) or rarely true panicles, racemes or spikes. Flowers hermaphrodite, rarely unisexual, actinomorphic or very rarely zygomorphic, usually proterandrous, (3–)5(–32)merous; sepals free or connate at base, sometimes distinctly unequal in size; petals free or connate to a short to long corolla tube; stamens as many as or usually twice as many as petals; ﬁlaments free or ± connate with a tubular corolla; anthers basiﬁxed in basal pit, 4-sporangiate, 2-locular at anthesis, dehiscence latrorse or slightly introrse by longitudinal slits; ovary usually ± superior to semi-inferior; carpels as many as petals, usually free or almost so, sessile or sometimes stipitate, tapering gradually to abruptly into short to long, erect to divergent stylodia, basally with a small to conspicuous dorsal nectary scale; stigma small, (sub)apical, often poorly differentiated; ovules usually many, rarely few to one, anatropous, crassi- or tenuinucellate, bitegmic, on parietal to marginal placentae. Fruits usually follicles, and usually ± completely dehiscent along the ventral suture, rarely few-seeded, indehiscent and nutlike; seeds smallish, usually 0.5–1 mm long, elongate-fusiform, longitudinally ridged (costate) or papillate (uni-or rarely multipapillate), rarely 1

U. Eggli provided the key and generic descriptions extracted from Eggli (2003) which were largely revised here.

(nearly) smooth, usually brownish; embryo small, straight; endosperm cellular, scanty. A family of 34 genera with c. 1,410 species distributed worldwide, usually in arid and/or rocky habitats, with centres of diversity in Mexico and South Africa. Vegetative Morphology. Crassulaceae are usually perennial herbs to (sub)shrubs, rarely small trees (the Malagasy Kalanchoe beharensis and K. dinklagei reach 8–10 m). The epicotyl is usually well developed; rarely does it remain very small (’t Hart 1982). In most perennials, the whole shoot system and at least some leaves survive unfavourable periods (frost, drought). Leaves are shed only when additional storage organs are present: succulent, ± elongated stems (e.g. Tylecodon) or small, tuber-like swollen stems (e.g. Dudleya subg. Hasseanthus). Rhizomes are usually sympodial, rarely monopodial (Rhodiola). In Aeonium, the modular growth form correlates with sectional classiﬁcation (Jorgensen and Olesen 2000). Some highly reduced annual Crassula are morphologically aberrant: ﬂowers of C. pageae are embedded in a short ‘disc’ derived from connate side shoots (coenosom, described in detail by Jäger-Zürn 1989), and C. aphylla forms leaﬂess, ± globular shoots reaching maturity at about 3 mm Ø; it may represent the smallest succulent plant. Few Sedum from the Mediterranean and the Mexican Sierra Madre (Clausen 1977) are strictly biennial. Facultative annuals to perennials are found in Mediterranean Sedum and Macaronesian Aichryson and Monanthes icterica. Root apices often contain anthocyanins and are reddish. Roots are usually ﬁbrous, rarely thickened-fusiform (Villadia p.p., Hylotelephium p.p.) or tuberous. Tuberous rhizomes or rootstocks may develop from the hypocotyl (Rhodiola rosea), the upper part of the main root and hypocotyl (Dudleya caespitosa), or the hypo- and epicotyl (Umbilicus). Sedum obtusifolium forms subter-

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ranean runners with tuberous thickenings, and S. amplexicaule forms propagules from the swollen leaf bases clasping the stems. Secondary growth in roots and root tubers of Sedum and Hylotelephium is described by ’t Hart (1994a). Adventitious roots are formed by many prostrate to suberect shoots (e.g. many Sedum) or ± upright shoots of shrubs, especially under conditions of high air humidity (e.g. Aeonium); this ability is used for vegetative propagation in horticulture. Thickened short roots in Sempervivum, Sedum and some other genera which are inhabited by mycorrhizal symbionts (hyphomycetes, Berger 1930) need re-study. The root-nodules recently reported for Sinocrassula (Akiyama et al. 2001) may belong here. Germination is epigaeal and cotyledons are ﬂeshy, usually petiolate and long persistent. Adult leaves are usually simple and only rarely pinnately compound (some Kalanchoe, e.g. K. pinnata), palmately lobed (Crassula alcicornis), laciniate (Kalanchoe laciniata) or peltate (Umbilicus sect. Umbilicus and a few Kalanchoe). The leaves are ± ﬂat to subulate and often ± ﬂat above and semi-terete below, partly with a ± developed keel. The leaf margin is usually entire or ± crenate (e.g. Umbiliceae), partly with cilia (e.g. many Aeonium). Heterophylly is found in some Orostachys and Rosularia (summer vs. winter rosette; Eggli 1988; Ebel et al. 1991a) and in Sedum diversifolium and S. greggii (sterile vs. ﬂowering). Leaves typically break off easily and form adventitious shoots at the place of separation, a means of vegetative propagation in nature (e.g. Adromischus) which is widely used in horticulture. Many Kalanchoe species of sect. Bryophyllum form adventitious shoots (gemmae) on leaf margins. Sedum viviparum and S. gemmiferum form gemmae in the vegetative region, and Crassula multicava, Kalanchoe miniata, etc. within the inﬂorescences. The leaf arrangement is usually alternate (most Kalanchoideae and Sempervivoideae) or decussate (most Crassuloideae), rarely whorled (e.g. a few Sedum). Leaf aggregation in ± dense rosettes evolved independently in many genera of nearly all major clades (except Umbiliceae), especially within Sempervivoideae. In spirally arranged rosettes, the number of spirostichies may be of systematic value (e.g. Monanthes; Nyffeler 1992). The rosettes may be ± stem-less, with the leaves remaining attached to the stem at least for some time, or terminal at the shoot tips of (sub)shrubs, with dried leaves being usually shed. Stolons are a means of vegetative propagation in some rosettes (e.g. Semper-

vivum, Orostachys). The rosettes become ‘closed’ and form bud-like structures (‘resting rosettes’) during drought periods in some Aeonium (Ebel et al. 1991b), Orostachys (Ebel et al. 1991a) and Rosularia (Eggli 1988). Vegetative Anatomy. A detailed account was provided by Gregory (1998, with many references), from which data were taken if not cited otherwise. Soil root hairs are usually unicellular; those of aerial adventitious roots may be uni- or biseriately multicellular. The leaves are generally bifacial, succulent (weakly so in some Crassula (Tillaea) and few Sedum with small and thin scale-like leaves) and typically centric or intermediate between centric and dorsiventral. Palisade parenchyma is normally absent; the adaxial cells are sometimes palisade-like. Most leaves are thickish and exhibit a mesophyll with continuous transition from outer chlorenchyma to inner water-storage parenchyma with large achlorophyllous, highly vacuolated cells. Thinner leaves lack this differentiation and are chlorenchymatous throughout. Vascular bundles are collateral and in ﬂat leaves in one row, in terete leaves in a circle, or irregular. Tissues often contain copious tannin. Solitary crystals and druses are common; crystal sand is found in Adromischus, Cotyledon, Kalanchoe and Umbilicus (also within secondary growth). The nodes were studied for few species only and vary even within genera (1-lacunar:1-trace; 1:2 or 1:3, 3:3, 3–multi:3–multi, or multi:3–8). Hydathodes of the ‘epithem’ type are present in many (all?) Crassulaceae. Crassuloideae typically have numerous hydathodes along the margin and/or on the leaf surface of one or both faces (Toelken 1977; Martin and von Willert 2000; see also under Physiology). Kalanchoideae and Sempervivoideae typically have one (sub)apical hydathode only (e.g. Rosularia, Eggli 1988); marginal hydathodes are rare, e.g. Aichryson p.p. (Caballero and Jiménez 1977) or Phedimus (’t Hart and Bleij 2003). The venation is pinnate or palmate and camptodromous or reticulate, usually with a distinct intramarginal vein. In ± ﬂat leaves, the midvein typically protrudes at least on parts of the lower face. The leaf epidermis is usually one-, occasionally two- (to three)-layered. Outer walls are thin (mesomorphic) to extremely thick (xeromorphic), the anticlinal walls straight (especially in xeromorphic types) or wavy to markedly sinuous (especially in mesomorphic types). Some Crassula, Monanthes

Crassulaceae

and Tylecodon species exhibit enlarged epidermal cells (bladder-cell idioblasts). The cuticle is usually smooth or with ﬁne striations (e.g. Aichryson) or distinct ridges (e.g. Aeonium). Epicuticular wax deposits are in rods, irregularly lobed platelets, threads, smooth platelets or a very thick layer ﬁssured into platelets (Fehrenbach and Barthlott 1988). Stomata are usually superﬁcial to somewhat sunken (some Crassula) or raised (some Sedum), and usually anisocytic or rarely helicocytic (Kalanchoe and Sedum) and mesogenous with 3–8(–10) subsidiary cells. Stomata are usually ± equally numerous on both faces, or more numerous abaxially (rarely adaxially) and usually irregularly orientated. The stomatal density is low, similarly to other leaf succulents, and about 5–80 per mm2 . Cystoliths are reported for Orostachys japonicus. Hairs occur usually on both leaf surfaces when present, with six types: (1) unicellular, simple, thick-walled; (2) unicellular swollen bladder-cell idioblasts with constricted base sometimes covering the epidermis completely; (3) most common are multicellular simple hairs with biseriate stalk which may be non-glandular or glandular with ± spherical heads of 2–12 secretory cells; (4) multicellular stellate hairs with 3(–6) apical arms (only in Malagasy Kalanchoe with dense-felty tomentum, e.g. K. beharensis; Boiteau and Allorge-Boiteau 1995); (5) multicellular sessile hairs with 2–3 basal cells and small head; and (6) multicellular uniseriate, simple or capitate hairs. On young stems, the periderm arises usually in the subepidermis, also in the epidermis or more deeply in the cortex and forms continuous rings or separate groups of cork cells. Additional cambia from the outer cortex sometimes lead to thick periderms (e.g. Kalanchoe beharensis). The cork is impregnated with resin in some Malagasy Kalanchoe. A peeling outer bark occurs in stem-succulent pachycauls (Tylecodon p.p., Aeonium smithii, some Sedum). The epidermal cells are thin-walled. Subepidermal collenchyma layer(s) are reported for some genera. The cortex is parenchymatous, sometimes with chlorophyll, and aerenchymatous in the semi-aquatic Crassula inanis (Moteetee and Nagendran 1997). A distinct endodermis is recorded for some genera. Secondary growth typically yields vessels, parenchyma and ligniﬁed ﬁbres in distinct bands, layers, or as ground mass. The pith is parenchymatous, later sometimes ligniﬁed. Medullar bundles

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are reported for some genera. Stem succulents often have secondary growth dominating in the parenchyma of cortex and pith. Growth rings are absent. The phloem is poorly developed. The wood structure is rather similar between unrelated genera and conspicuous in its juvenile features (raylessness, short vessels without variation in length and shape within the radius, and with secondary thickenings characteristic of the primary xylem), and differs strongly from the secondary wood of ‘normal’ woody plants. These differences were interpreted by ’t Hart and Koek-Noorman (1989) as resulting from paedomorphosis and were thought to indicate secondary woodiness derived from a primarily herbaceous ancestor (see also Phytochemistry). Vessel elements are moderately short (100–229 µm) with slightly inclined end walls. Perforation plates are simple (rarely reticulate in Sedum). Vessels have helical and annular lateral wall thickenings and/or scalariform(-reticulate) pitting. Libriform ﬁbres are non-septate with simple pits and thin to thick walls, and form the major part of the wood in most species. Axial parenchyma is usually scanty paratracheal, but may rarely constitute the entire ground tissue, as in Crassula arborescens and some Monanthes. Cortical bundles are reported for some thick-stemmed taxa but are merely leaf-traces running ± vertically for some distance. The rhizome anatomy of Sedum tuberosum and Rhodiola rosea was described by ’t Hart (1982, 1994b). Ultrastructure. Crassulaceae exhibit the S0 type of sieve element plastids (without protein inclusions and without starch) not found elsewhere in Saxifragales (Behnke 1991). Chloroplast ultrastructure differs between C3 and CAM species (Teeri and Overton 1981). Inﬂorescence structure. Detailed data can be found in Troll (1964, 1969) and especially in Troll and Weberling (1989). Inﬂorescences are usually thyrsoids (monotelic, i.e. with a terminal ﬂower). Rarely, the terminal ﬂower may be reduced, partly together with the distal part of the inﬂorescence (Adromischus, Umbilicus). The partial inﬂorescences are dichasia (frequent in Crassuloideae, Kalanchoideae, Telephieae, Umbiliceae), monochasia (double or simple cincinni; frequent in Semperviveae, Aeonieae and Sedeae) or thyrsoids. They are sometimes concaulescent and thus branch off above their subtending bracts (e.g.

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Aeonium), or the bracts are recaulescently shifted onto the partial inﬂorescences (e.g. Tylecodon reticulatus). Rarely, intercalar inhibition zones with bracts not subtending partial inﬂorescences are found (Aichryson, some Crassula). Some species produce pleiochasia (pseudowhorls of three or more distal partial inﬂorescences below the terminal ﬂower); proximal partial inﬂorescences are absent or consist of few to single ﬂowers only (e.g. Sempervivum tectorum). Cymoids with one cincinnus or two cincinni below the terminal ﬂower are also frequent. In uniﬂowered species, only the terminal ﬂower is developed. Obligately uniﬂowered inﬂorescences appear to be rare (e.g. Sedum humifusum). In Kalanchoe, all intermediates from manyﬂowered thyrsoids over racemes to solitary ﬂowers occur. True panicles (some Adromischus and Umbilicus), racemes (some Umbilicus), double racemes (Umbilicus oppositifolius) or spikes (some Adromischus) are rare. The presence of prophylls, as in the botryoids (e.g. Villadia imbricata), is interpreted as derived from thyrsoids. Lateral inﬂorescences occur in some Sedum, Aichryson, Aeonium, Rosularia, Prometheum and throughout in Afrovivella, Meterostachys, Rhodiola, Dudleya and the Echeveria group. Flower Structure. Pedicels are distinct to (nearly) wanting. Either two, one or no prophylls are present. The ﬂowers are usually upright to spreading, rarely pendent (then, again upright in the fruiting stage) and nearly always hermaphrodite (plants dioecious in Rhodiola p.p.). The length of the ﬂowers ranges from a few mm (some Crassula [Tillaea]) to 140 mm (Kalanchoe marmorata). Flowers are actinomorphic, slightly zygomorphic only in Tylecodon grandiﬂorus, Kalanchoe elizae and K. robusta, (3–)5(–32)merous, and differ strongly in the degree of sympetaly (see, for instance, Figs. 28, 30). The sepals are usually green, (nearly) free or ± connate and usually much shorter than the corolla. They are usually equal and basally connate with the receptacle, or (in Sedum subg. Sedum) often free and ± spurred at base and unequal in size. Petal aestivation is quincuncial, cochlear, or contorted in Sedum (’t Hart 1990), imbricate or contorted in Crassula, convolute in Dudleya, imbricate in Sedella, Thompsonella and most Echeveria, and valvate in a few Echeveria. The petals are typically thin-textured (rarely membranous in annual Crassula), rarely thickish-succulent (e.g. Echeve-

ria), frequently dorsally keeled and sometimes papillose to hairy, and completely free or slightly to nearly completely connate to a corolla tube. Sympetaly is found in all Kalanchoideae and is frequent in many Sempervivoideae where it is of multiple origins (’t Hart et al. 1999; Mort et al. 2001). Petals are yellow, red, white, greenish to brownish with intermediates, very rarely blue (e.g. Sedum caeruleum), often unicoloured, partly bi- to rarely tricoloured (e.g. many Echeveria), sometimes with dots (some Pachyphytum) or irregular spottings (most Graptopetalum). Petals rarely have subapical unifacial precursory tips (‘Vorläuferspitzen’; e.g. Crassula subg. Crassula, many Sedum, some Villadia). Leinfellner (1954) studied the basal petal scales of Pachyphytum, which are also found in some Echeveria. The androecium is obhaplostemonous (Crassuloideae; then, antesepalous stamens only) or more frequently obdiplostemonous (most Kalanchoideae and Sempervivoideae). In obdiplostemonous androecia, the antesepalous stamens are typically longer. In sympetalous corollas, the stamens are ± connate with the tube; the antepetalous (always?) inserted somewhat higher than the antesepalous ones. The ﬁlaments are free from each other, usually ± thin-ﬁliform, rarely broadened or thickened. The anthers are usually about 1 mm long, but are longer in long-tubed ﬂowers. Anther colours are usually yellow or red, but also orange, purple, brown, black, white, pink and green with nearly all intermediates and partly infraspeciﬁc variation; they are of some taxonomic value (Thiede, unpubl. data). The gynoecium is nearly exclusively isomerous with the perianth (oligomerous only in Sedum tricarpum and S. bonnieri). The ovary is usually superior and the carpels are (nearly) completely free, rarely connate higher up and completely connate only in Crassula pageae (Jäger-Zürn 1989). Soltis et al. (2003) suggested that the ovary in Crassulaceae is secondarily superior, according to a characterstate reconstruction based on molecular data. The carpels narrow gradually to abruptly into separate, erect to divergent stylodia which are usually short to very long in long-tubed ﬂowers. The stigma is small, often poorly differentiated, usually terminal (lateral in some Crassula, Toelken 1977). A compitum is recorded from some Echeveria. The carpels nearly always exhibit nectary scales at their dorsal bases (absent in a few Crassula, Sedum and Aeonium), which are usually less than 1 mm long and very diverse in shape and colour.

Crassulaceae

In Monanthes, Sedum surculosum, S. longipes and S. pentastamineum, the large, petaloid nectary scales are more obvious than the petals. Floral Development and Anatomy. Floral anatomy, vasculature and development have been described in general by Wassmer (1955), Jensen (1966) and Quimby (1971), for Sedum, Crassula and Phedimus by Eckert (1966), for Kalanchoe by Tillson (1940), for Hylotelephium by ’t Hart (1985c) and for Crassula pageae by Jäger-Zürn (1989). During ontogenesis, sepals develop much earlier than petals (Wassmer 1955). The haplostemonous Crassula dejecta lacks antepetalous (outer) stamens and otherwise develops as the obdiplostemonous Sedum acre, thus indicating that ﬂowers in Crassulaceae are probably basically obdiplostemonous (Eckert 1966). The anthers are median-sagittate in shape (transverse-sagittate in other Saxifragales studied by Endress and Stumpf 1991). Anthers are basiﬁxed, and the ﬁlament is attached to the connective with its very thin upper end in the basal pit (dorsiﬁxed only in Rhodiola hobsonii). Anthers are usually latrorse, slightly introrse only in Crassula, Sinocrassula yunnanensis and Umbilicus rupestris (as U. pendulinus; Wassmer 1955) and usually caducous. The anther epidermis is astomate and shows different types (Endress and Stumpf 1991). Apical connective protrusions with different shapes were found in several genera (Wassmer 1955; Endress and Stumpf 1991); in Kalanchoe they may function as secretory glands (Raadts 1979). The carpels are open in early developmental stages and postgenitally connate and are mainly plicate. Carpels within a ﬂower are congenitally connate at least for a short distance below and postgenitally above; completely free carpels have not been found. Ontogenetic studies suggest that the nectary scales represent emergences of the carpels (Wassmer 1955). They exude nectar through stomata (Said 1982). Embryology. Embryology was studied especially by Mauritzon (1930, 1933), and also by Rocén (1928), Souèges (1936) and Fétré and Lebègue (1964). Reviews are by Davis (1966) and Johri et al. (1992), from which most data were taken. The anther wall comprises a persistent epidermis, a one-layered ﬁbrous endothecium, two ephemeral middle layers, and the secretory, uninucleate tapetum. Microsporogenesis is simultaneous. Pollen is shed in monads. It is binucleate and sometimes contains starch grains. The ovules are

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anatropous, bitegmic and crassinucellate in Kalanchoideae and Sempervivoideae, and tenuinucellate in Crassuloideae. The micropyle is usually formed by both integuments which are both 2-layered. The embryo sac is usually of the normal Polygonum type. In Hylotelephium, an embryo sac of the bisporic Allium type develops from the chalazal dyad. In Prometheum, haustoria are given off from the megaspores and pass through the nucellus into the integuments; such megaspore haustoria are a rather unusual feature. The embryo sac generally contains starch grains. Endosperm formation is ab initio cellular, usually with a chalazal endosperm haustorium, and differs between Crassuloideae and Kalanchoideae/Sempervivoideae (Mauritzon 1933). The endosperm is scanty, ﬂeshy and typically reduced to a 1-layered cap surrounding the hypocotyl (Krach 1976). The zygote divides into embryo, suspensor and a suspensor-haustorium within the nucellus (Mauritzon 1933). The embryogeny conforms to the Caryophyllad type. The embryo is small, long and straight, without a plumula, and stores aleuron as well as oil (Krach 1976). Pollen Morphology. The pollen is usually 3-colporate and subspheroidal to prolate in equatorial view, ± convex-triangular in polar view, and 13–38 µm long. Apertures are lalongate. The sexine is about as thick as the nexine. The tectum is complete and usually striate, reticulate, rugulate or cerebroid (Hideux 1981). The striae have a straight or rarely irregular margin (Monanthes). More rarely, the tectum is (nearly) completely smooth (Sempervivum sect. Jovibarba; Rosularia p.p., Prometheum) or has a ﬁne OL-pattern. Colpi are tenuimarginate, with the thin exine usually protruding at the equatorial part of the colpi (Erdtman 1952). Pollen morphology may vary within the same inﬂorescence and is thus of restricted systematic applicability (Kim 1994). Data are based on an overview SEM study by Hideux (1981), more focused SEM studies for Sempervivum (incl. Jovibarba; Parnell 1991), European Sedum (’t Hart 1975), Rosularia and Prometheum (Eggli 1988), Monanthes (Nyffeler 1992), Korean Sedum (Kim 1994) and Korean Crassulaceae (Sin et al. 2002), and on light microscopy for Aeonium (Pérez de Paz 1980). Pollen morphology of Crassulaceae is similar to that of Saxifragaceae (Erdtman 1952). Karyology. Crassulaceae display an extensive variation in chromosome numbers among and often within genera and often among species,

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and possibly represent the karyologically most diverse family of angiosperms. The base number for the family and subfamilies Crassuloideae and Sempervivoideae, x(n) = 8, is also found in outgroups (Penthoraceae, Haloragaceae). The basic chromosome numbers for the major clades have been reconstructed by Mort et al. (2001). Many studies have been conducted on North American taxa (Graptopetalum and Thompsonella, Uhl 1970; Pachyphytum, Uhl and Moran 1973; Sedum, Uhl 1976–1992; Echeveria, Uhl 1994–2005; intergeneric hybrids, Uhl 1993–1995; Lenophyllum, Uhl 1996; Villadia, Uhl and Moran 1999), on European Sedum by ’t Hart (especially 1985a, 1991), on European and Macaronesian Semperviva by Uhl (1961), on Rosularia by ’t Hart and Eggli (1998), on Crassula by Merxmüller et al. (1971) and Friedrich (1973), and on Kalanchoideae by Uhl (1948). The Asian taxa are less thoroughly studied (Uhl and Moran 1972; Wakabayashi and Ohba 1999). Karyotypes are typically rather symmetrical and the chromosomes small (less than 1 or 2 µm), so that pairs and structural details can hardly be recognised. Satellites are present in Crassula subg. Crassula (Friedrich 1973) and some other genera (Sharma and Gosh 1967). Most larger and also some smaller genera exhibit different base numbers and few to many polyploids, partly including high polyploids. Closely related genera often, but not always, exhibit different base numbers. Karyological variability reaches an extreme in Sedum and especially in the Echeveria group (Uhl 1992). Among the 62 studied European/Mediterranean Sedum species, about 140 cytotypes with all base numbers from 5 to 18 and some higher ones (20, 22, 24, 25, 29, 37) have been found. The data show that 64% of these cytotypes are polyploid, and nearly half of the species exhibit polyploids among diploids, some of them high polyploids (S. rubens: 20×) or complete series (S. forsterianum: 2 to 8×), partly also dysploids (’t Hart 1991). The high degree of polyploidy is attributed at least partly to allopolyploidy (’t Hart 1991), which was demonstrated experimentally (’t Hart et al. 1993). The Mexican Sedum suaveolens exhibits the highest chromosome number in angiosperms, n = 320 (= 40×). See also under Reproductive Systems. Pollination and Reproductive Systems. Flower induction in Kalanchoe is under short-day conditions (Engelmann 1960), whereas Hylotelephium telephium is a long-day plant (’t Hart and

van Arkel 1985). In Echeveria, short- as well as long-day plants are found (Rünger and Wehr 1969). Flowers are usually proterandrous, with the anthers of the antesepalous (inner) stamens releasing pollen before the anthers of the antepetalous (outer) ones. Sometimes, anthers dehisce already within the ﬂoral bud (Wassmer 1955). Proterogyny and homogamy are rare (e.g. some European Sedum). Differentiation among the two whorls for allogamy (stamens of outer whorl bending over petals) and autogamy (inner whorl remaining erect or bending over stylodia), respectively, is common in European Sedum and Sempervivum (Günthart 1902). Stamen movements are extreme in Graptopetalum, where the stamens curve back towards the sepals and petals during anthesis (Moran 1949). Crassula (Tillaea) muscosa is autogamous, and C. aquatica appears to be cleistoand autogamous (Berger 1930); some tendency towards cleistogamy has also been observed in Sempervivum sect. Jovibarba (Günthart 1902:61). Crassulaceae appear to be usually selfincompatible but Sedum sect. Gormania shows self-compatibility in varying degrees (Denton 1979). Fecundity in Echeveria gibbiﬂora is limited by pollen and resource availability (Parra et al. 1998). In Hylotelephium telephium, di-, tri- and tetraploid cytotypes are sympatric (’t Hart 1985b). Studies on the conservation genetics of Rhodiola integrifolia subsp. leedyi (Olfelt et al. 1998, 2001) and Dudleya multicaulis (Marchant et al. 1998) revealed a high intrapopulation genetic variation, indicating little gene ﬂow among the isolated populations. Floral biology is poorly studied and largely restricted to the establishment of ﬂoral types and pollination syndromes. The carpellary nectary scales exude nectar in large quantities, which often forms glistening droplets. The few Crassulaceae without nectary scales may have deceptive ﬂowers. Five major pollination syndromes are found (mostly taken from Vogel 1954). 1. Melittophily is assumed for taxa with a free, rotately spreading (e.g. most Sedum, many Telephieae and Umbiliceae, Aeonium, Sempervivum) or short tubular corolla (e.g. many Crassula species, Kalanchoe p.p., Tylecodon p.p. (Gess et al. 1998), Umbilicus). It represents the most frequent and least specialised, possibly plesiomorphic syndrome in Crassulaceae. 2. Psychophily corresponds to long-tubed salvershaped ﬂowers (Adromischus, Pistorinia,

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Kalanchoe, e.g. K. rotundifolia) or ﬂowers with at least connivent petals forming a tube-like structure (e.g. Crassula coccinea) and intensive colouration (red, yellow) and scent production over the day. This ﬂoral type has earlier led to artiﬁcial generic segregations (e.g. Rochea for long-‘tubed’ Crassula species such as C. coccinea). 3. The sphingophilous syndrome (long, whitish corolla tubes, nocturnal scent) appears to be restricted to a few Crassula (e.g. C. fascicularis; detailed study by Johnson et al. 1993) and some Kalanchoe (e.g. K. marmorata), and thus to Africa. 4. Ornithophilous ﬂowers (red, long-tubed corollas, lack of odour, abundant nectar production, exserted anthers) are found in species of Kalanchoe, Cotyledon, Tylecodon, Echeveria (Parra et al. 1993) and Dudleya. There appears to be a gradual transition from psycho- or melittophily to ornithophily. The psychophilous Crassula coccinea is also visited by nectar birds (Vogel 1954). In Dudleya, the gradual shift from bee to hummingbird pollination has been demonstrated to be accompanied by changes in nectar amount, increase in tube length, colour shift to reddish corollas, and shift from low to high auto-fertility (Levin and Mulroy 1985). 5. Myophily is assumed for Monanthes (open ﬂowers with darkish colours, freely accessible nectar produced by large nectary scales; Vogel 1954). Carrion ﬂies are possible pollinators for the fade-coloured and foetid ﬂowers of most Graptopetalum (Moran and Meyrán 1974). In both genera, the darkish to fade ﬂower colours are accompanied by corresponding anther colours (Thiede, unpubl. data). Some Crassula and Sedum species with small, insigniﬁcant whitish ﬂowers with a musky scent are probably also ﬂy-pollinated. The report of effective ant pollination for Sedum pusillum is one of the few known cases of ant pollination in angiosperms (Wyatt and Stoneburger 1981). When exploiting the freely accessible nectar from the nectary scales, the ants ‘accidentally’ transfer pollen over the dense stands of the plant, but bee pollination also occurs. Flower visits by ants were also reported for Kalanchoe (Bahadur et al. 1986) and may be more frequent, at least accidentally. Melittophily is widespread and dominates in the northern temperate region, whereas psycho-,

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sphingo- and ornithophily are restricted to (sub)tropical or southern temperate regions. Pollination syndromes in southern Africa are more diversiﬁed than in North America. The derived pollination syndromes are certainly of multiple origin within Crassulaceae, possibly from the plesiomorphic melittophily. Hybridisation patterns in European Sedeae are strictly correlated with the presence or absence of four morphological character states (see Subdivision). Species can be hybridised only when they agree in all four character states, but not all hybrids are possible (’t Hart and Koek-Noorman 1989). In Aeonieae, hybridisation patterns correspond to present generic boundaries between Aichryson, Monanthes and Aeonium (incl. Greenovia): no hybrids between genera, but many within these genera are possible. The c. 200 species of the Echeveria group appear to be fully interfertile (though natural hybrids are rare) and form the largest comparium known among angiosperms (Uhl 1992). Fruit and Seed. Fruits are usually many-seeded follicles which dehisce xerochastically; hygrochastic opening is rare (e.g. Sedum acre). Fruit dehiscence is sometimes reversible under humid conditions (Phedimus aizoon; Huber 1961) or, vice versa, the suture opens fully only under humid conditions but closes again when drying out (Sedum acre and S. annum; Stopp 1957). The ripe follicles either remain upright (orthocarpic) or become divergent to stellate-patent (kyphocarpic). An earlier classiﬁcation of Sedum based on these features (Fröderström 1930–1935) proved to be artiﬁcial. Follicles of most genera dehisce completely along the ventral suture; other types are more rare: the suture mainly opens apically or basally only, or the plicate carpel part breaks off as a whole (Aeonium sect. Greenovia). Some species of Crassula sect. Glomeratae have only 1- or 2-seeded follicles from which the upper part breaks off with circumscissile splits and encloses one or two seeds (Stopp 1957; Toelken 1977). Similar fruits are found in Hypagophytum and some Sedum. Sedella and Sedum microcarpum have one-seeded, non-dehiscent nutlike fruits, and the fruits of Sedum smallii dehisce with a tear-shaped ﬂap unique within the family (Clausen 1975). In European Sedum, kyphocarpic follicles usually exhibit carpel walls broadened to ± distinct ‘lips’ (possibly favouring splash-cup dispersal by rain), whereas orthocarpic follicles are without lips (’t Hart 1991).

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Fig. 26. Crassulaceae. Seed surface structures. A Crassula streyi. Sinuate (unipapillate) (‘Puzzle-Modell’ of Knapp 1994): anticlinal walls sinuate, periclinal walls usually convex to centrally papillate or rarely almost smooth (Crassuloideae). Types B–D Anticlinal walls straight. B Kalanchoe brachyloba. Costate (bipapillate) (‘Leitermodell’): cells with two papillae at each distal end. The papillae remain ± free or are mostly fused to form distinct costae with those of the neighbouring cells, partly with transverse connections (Kalanchoideae and all Sempervivoideae,

except for the following). C Umbilicus horizontalis. Multipapillate (‘Warzenmodell’): cells with 2–3(–5) small papillae which are usually unequal in size and form small groups with those of adjacent cells (only genus Umbilicus within tribe Umbiliceae). D Sedum wrightii. Reticulate (unipapillate) (‘Wabenmodell’): the lateral cell-walls are always thickened and form a distinct reticulate pattern, usually with a central papilla (Acre clade). Scale: A 100 µm, B 1,000 µm, C, D 10 µm. (A, C From Knapp 1997 and B, D from Knapp 1994)

The seeds are ± oblong-fusiform, ± brownish, usually 0.5–1 mm long and weighing c. 0.02 mg (Sempervivum). The East African Sedum epidendrum and the Mexican S. botteri and related species exhibit seeds up to 3 mm in length, a possible adaptation to their epiphytic habitats (Clausen 1959: 46; Gilbert 1985). The seed coat is 4-layered: the exotestal cells have a ± thickened outer wall, the inner exotegmic cell layer is pigmented, and the two middle layers are completely crushed (Krach 1976). The chalazal region is obtusely

rounded or elongated to acute (apiculate; Fig. 26B; Knapp 1994: 163). The micropylar region is partly surrounded by the outcurved testa which forms a distinct corona (Fig. 26B; Kalanchoideae, some Sedum; ’t Hart and Koek-Noorman 1989; Knapp 1994: 163). In SEM studies of testa structures (’t Hart and Berendsen 1980, for Sedum; Knapp 1994, 1997), four main types are distinguished, differing mainly in the number and position of papillae and concurring well with phylogenetic patterns (Fig. 26A–D): A sinuate-unipapillate with

Crassulaceae

sinuate anticlinal walls, or B costate-bipapillate, C multipapillate and D reticulate-unipapillate with straight anticlinal walls. Speciﬁc SEM datasets have been published for Crassula (Bywater 1980; Wickens and Bywater 1980; Bywater and Wickens 1983), Sedum sect. Ternata (Calie 1981), Sedum sect. Gormania (Denton 1982), Rosularia and Prometheum (Eggli 1988), Monanthes (Nyffeler 1992) and East Asian taxa (Gontcharova 1999). Dispersal. The follicles usually release the seeds immediately after ripening. The seeds are dispersed by gravity and wind, but are much larger than typical anemochorous dust seeds (e.g. orchids, many parasites). Nakanishi (2002) recorded splash-cup dispersal by raindrops for the divergent follicles of two Japanese Sedum spp.; this mechanism may be more frequent. The seed number in Crassulaceae may be very high (an old inﬂorescence of Aeonium nobile was estimated to produce about 50,000 ﬂowers (Burchard 1929) and 500,000 or even much more seeds). Most seeds are dispersed over short distances as anemochorous seed rain around the mother plant (Parra et al. 1993). Anemochorous long-distance dispersal appears to be rare, as evidenced, e.g. by the closely related island vicariants on the Canary Islands, and the rarity of pronounced disjunctions. Evidence for long-distance dispersal comes from molecular data (van Ham and ’t Hart 1998; Mort et al. 2001). Berger (1930) suggested the possibility of secondary dispersal by water and ants, but evidence is wanting. Ripe seeds typically remain viable for a few years only or even less. On wet soil, seeds typically germinate within a few days (in cultivation) and generally in light. Studies on the germination ecology of the winter annuals Sedum pulchellum and S. smallii from the eastern USA revealed after-ripening of the seeds during summer, which is interpreted as an adaptation to summer-dry habitats (Baskin and Baskin 1972, 1977). Phytochemistry. Reviews are given by Hegnauer (1964, 1989) and Stevens (1995a, b). Crassulaceae accumulate large amounts of sedoheptulose, which is the most abundant sugar in most species. In contrast to many other succulents, nearly all species investigated to date contain isocitrate (Hegnauer 1964). Proanthocyanidins (condensed tannins) have been found in all clades, except for the Acre clade

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where they are absent or at least rare and replaced by alkaloids (Stevens et al. 1992, 1995; Stevens 1995a). Proanthocyanidins are widespread both in woody and herbaceous Crassulaceae. The lack of exclusivity in the woody representatives supports the hypothesis that Crassulaceae are primarily herbaceous (Stevens 1995a), which is also supported by wood anatomy (see there). Galloyl esters are common, but ellagitannins are absent, in contrast to Saxifragaceae and Penthoraceae (Jay 1971). Flavonols and ﬂavones, both unmethylated and methylated, are known to occur in Crassulaceae, but myricetin is rare (Denton and Kerwin 1980; Hegnauer 1989; Stevens et al. 1996). Wax composition (in particular, alkane and triterpene proﬁles) has been studied by Eglinton et al. (1962), Manheim et al. (1979), Bowman (1983) and Stevens et al. (1994). Since the isolation of sedamin from Sedum acre in 1939, many different pyrrolidine and piperidine alkaloids have been detected in Sedum subg. Sedum (several studies on Sedum acre; see Hegnauer 1989; Stevens et al. 1993) and in Echeveria. Alkaloids thus seem to be restricted to the Acre clade, but they are absent in its more derived members (except Echeveria; Stevens et al. 1992, 1995). Cyanogenic substances have been found in some, but not all Crassulaceae studied. Cyanogenesis is weak especially in Sedum, and several species appear to be polymorphic in this respect (Hegnauer 1989). The South African Tylecodon paniculatus contains toxic bufadienolides which may cause a lethal cattle disease (‘krimpsiekte’). Structurally similar poisons occur in Tylecodon grandiﬂorus, Cotyledon and Kalanchoe (incl. Bryophyllum; Hegnauer 1989). Bufadienolides from Kalanchoe (Bryophyllum) are reported as potent, novel antitumor agents (Yamagishi et al. 1989) and insecticidal compounds (Supratman et al. 2001). Subdivision and Relationships Within the Family. The infrafamilial classiﬁcation is under debate over the last 200 years (review by ’t Hart and Eggli 1995). Most classiﬁcations relied heavily on a few trivial characters such as habit, leaf arrangement, number of ﬂoral parts, degree of petal fusion, number of stamens, and position of ripe follicles. However, most of these characters are of restricted value due to extensive homoplasy (’t Hart 1995; van Ham and ’t Hart 1998; Mort et al. 2001). Molecular data (’t Hart et al. 1999) indicated

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that sympetaly originated six times independently in European Crassulaceae of the Leucosedum clade. The widely accepted classiﬁcation by Berger (1930) suffered strongly from such inadequacies. For instance, subfamily Cotyledonoideae, which includes Berger’s African/Eurasian sympetalous Crassulaceae, has long been revealed as artiﬁcial (e.g. Uhl 1948). ’t Hart and Koek-Noorman (1989) and ’t Hart (1991) discovered hitherto largely unrecognised characters of considerable systematic value in European Sedum and related genera: interspeciﬁc crossbreeding is possible only between species which agree in the character states for testa ornamentation (costate vs. reticulate-papillate), shape of the micropylar region (coronate vs. apiculate), sepal insertion (free vs. connate at base), and presence or absence of glandular hairs. Groups characterised by these long-overlooked characters usually agree well with those of molecular studies. Many other, such more cryptic characters have been established as synapomorphies for the major clades by Thiede (unpubl. data). Molecular data (cpDNA trnL-trnF spacer sequences: ’t Hart 1995; cpDNA RFLPs: van Ham and ’t Hart 1998; cpDNA matK sequences: Mort et al. 2001) led to the recognition of seven major clades; an eighth clade has recently been found (nuclear ITS and trnL-trnF sequences; Mayuzumi and Ohba 2004). From the six subfamilies of Berger, only the largely monogeneric Crassuloideae (Crassula) and Kalanchoideae (Kalanchoe s.l.) were found to be monophyletic. Here, the revised classiﬁcation of Thiede (unpubl. data) is adopted, which largely follows the sequencing convention (Fig. 27), i.e. it assigns the same rank to clades which branch off subsequently (three major clades: subfamilies; ﬁve major clades within Sempervivoideae: tribes). This contrasts with a previous proposal by ’t Hart (1995), who followed the ranking convention and classiﬁed the two sister-clades of subsequent di-

chotomies with formal ranks in descending order. Here, three subfamilies are recognised, as suggested earlier by Thorne (1983, 1992): the two morphologically well-supported Crassula and Kalanchoe clades are recognised as Crassuloideae (Crassula clade) and Kalanchoideae (Kalanchoe clade) respectively, and the remaining six clades are subsumed as Sempervivoideae (formerly Sedoideae). Within the latter, ﬁve tribes are recognised (Fig. 27): the Hylotelephium clade as tribe Telephieae, the Rhodiola clade as tribe Umbiliceae, the Sempervivum “clade” as tribe Semperviveae, the Aeonium clade as tribe Aeonieae, and the Leucosedum and Acre clades together as tribe Sedeae. It should be noted that the Crassula and Kalanchoe clades, which preferentially are (sub)tropical, are morphologically highly derived (see diagnoses of subfamilies Crassuloideae and Kalanchoideae), whereas the predominantly temperate Sempervivoideae largely retain the basic features of the family which have been recognised by outgroup comparison. For this reason, the taxonomic treatment starts with subfamily Sempervivoideae characterised by the basic features of the family. Molecular data (’t Hart 1995; van Ham and ’t Hart 1998; ’t Hart et al. 1999; Mort et al. 2001) indicated that Sedum, by far the largest genus of Crassulaceae, is highly paraphyletic. Sedum encompasses the least specialised species groups within the Semperviveae, Aeonieae and Sedeae, and is deﬁnable with plesiomorphic features only. All other genera in these tribes are derived from within Sedum and form a monophyletic lineage together with the latter. This implies that many segregates of Sedum are closely related to other genera in the Sempervivum, Aeonium, Acre and Leucosedum clades. In order to reﬂect phylogenetic relations within Semperviveae, Aeonieae and Sedeae, the segregates of Sedum identiﬁed to date by molecular studies are placed according to these molecular data. For most segregates, no generic names other than Se-

Fig. 27. Summary tree of Crassulaceae, showing the eight major clades, their number of genera/species (incl. Sedum), their main distribution, and the formal classiﬁcation. The number of synapomorphies for the major clades (if any) is indicated above the branches; bootstrap support below the branches (∗ = 50–70%; ∗∗ = 71–90%; ∗∗∗ = 91–100%). The genus Pistorinia of tribe Sedeae is not included. Further explanations are provided in the text. Combined from molecular data of van Ham and ’t Hart (1998), cpDNA restriction sites, Sempervivum clade; Mayuzumi and Ohba (2004) and

Mayuzumi (unpubl. data), ITS and trnL-F sequences, Hylotelephium and Rhodiola clades; Mes et al. (1995), trnLF sequences, Aeonium clade; Mort et al. (2002), matK, trnL-F, psbA-trnH and ITS sequences, Aeonium clade; and Mort et al. (2001), matK sequences, all other clades. Abbreviations: Appendic. = subsect. Appendiculatae, S. = Sedum with [G] = subg. Gormania and [S] = subg. Sedum, Medit. = Mediterranean, Eur. = Europe, N. East = Near East, Umbilic. = Umbiliceae, Semper. = Semperviveae, Kalan. = Kalanchoideae, Cras. = Crassuloideae

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dum are available (except for Petrosedum or perhaps Oreosedum, Amerosedum, etc.). However, the phylogenetic status of most of these segregates is insufﬁciently known, not to mention the dearth of morphological characters which could deﬁne them. Therefore, they are all classiﬁed here under Sedum but mentioned in the respective clades along with the genera most closely related to them. It is unlikely, and not intended, that any of these segregates will ever be elevated to generic status. The inclusion of all genera derived from within Sedum into a broadly deﬁned, then monophyletic Sedum would be highly impractical because of the dramatic morphological heterogeneity of the resulting taxon. The other course, splitting Sedum into numerous constituent monophyletic taxa, would result in a tremendous increase of very small genera usually ill-deﬁned morphologically; most of these can not be identiﬁed with present knowledge. A third option would be the inclusion of the segregates of Sedum into the existing, cladistically contiguous genera. Again, apart from presently insufﬁcient knowledge and lack of morphological characters of these clades, several consist only of species of Sedum and do not contain a genus with which these could be united taxonomically (see particularly the molecular data for European Sedum by ’t Hart et al. 1999). Here, we follow ’t Hart’s (1995) suggestion to accept Sedum as a paraphyletic grouping. Genera derived from within Sedum should be monophyletic and for practical reasons not monospeciﬁc, and morphologically well deﬁned (cf. ’t Hart 1995: 165), but this is not yet achieved for all genera (see especially the Echeveria group). A molecular clock model dates the origin of Crassulaceae at 69–77 Ma B.P., of the Crassuloideae/Kalanchoideae+Sempervivoideae split at 39–41 Ma B.P., of the Kalanchoideae/Sempervivoideae split at 25–29 Ma B.P., and of the split between the Leucosedum and Acre clades at 13–18 Ma B.P. (Wikström et al. 2001; cf. Fig. 27). A complete species-level taxonomic synopsis is provided by Eggli (2003). Afﬁnities. Crassulaceae were usually placed next to Saxifragaceae and the monogeneric Penthoraceae, either within Rosales (Cronquist 1968; Thorne 1968) or Saxifragales (Takhtajan 1969; Thorne 1992). The circumscription of Crassulaceae is nearly undisputed, except for the inclusion of Penthorum by some authors (de Candolle 1828; Torrey and Gray 1838; Schönland 1894; Hutchinson

1973). Molecular data (Morgan and Soltis 1993; Soltis and Soltis 1997; Fishbein et al. 2001) establish the monophyly of Crassulaceae. Putative morphological synapomorphies are leaf succulence, anisocytic stomata and carpellary nectary scales. Homoplasious synapomorphies are thyrsoid inﬂorescences, papillate seeds and obdiplostemony, which are shared with Saxifragaceae; papillate seeds are also found in Penthoraceae. Penthorum, formerly included in Crassulaceae, approaches some Phedimus species and its peculiar fruit is similar to that of Sedum (Diamorpha), but it differs clearly from Crassulaceae in its non-succulent leaves with anomocytic stomata, its vessel and ﬁbre structure, its diplostemonous ﬂowers, in having the follicles connate almost to the middle, the lack of carpellary nectary scales, the presence of an operculum, and in its chemistry (see Penthoraceae, this volume). Saxifragaceae differ primarily in their oligomerous gynoecium, the presence of a nectariferous disc and of non-succulent leaves with stipules or sheathing leaf bases, and usually anomocytic stomata (see Saxifragaceae, this volume). According to molecular data, Crassulaceae belong to a distinct clade within Saxifragales, from which Crassulaceae, Aphanopetalaceae, Tetracarpaeaceae, Penthoraceae and Haloragaceae branch off successively. Stevens (2005) lists an axis with endodermis, nodes 1:1 and the lack of stipules as putative morphological synapomorphies. This clade is in turn sister to a clade which includes Saxifragaceae, Grossulariaceae, Iteaceae and Altingiaceae (Savolainen, Chase et al. 2000; Savolainen, Fay et al. 2000; Soltis et al. 2000; Fishbein et al. 2001). Distribution and Habitats. Crassulaceae occur almost worldwide. General distribution patterns and centres of diversity are described by ’t Hart (1997a); for North America, a detailed survey is given by Thiede (1995), and climatic correlations are presented by Teeri et al. (1978). More focused datasets have been published for Sedum (Böttcher and Jäger 1984), European taxa (Meusel et al. 1965; Jalas et al. 1999), Mediterranean Sedum (’t Hart 1997b), Crassula (Jürgens 1995), Tylecodon and Cotyledon (van Jaarsveld 1994), and Rhodiola (Ohba 1989). Crassulaceae are often viewed as a typical northern temperate element, but species diversity is concentrated in Mexico (about 325 species) and South Africa (about 250 species). The taxa of the eastern USA and especially the Mexican upland regions represent a distinct terminal clade within

Crassulaceae

the Acre clade, including the majority of North American Crassulaceae (van Ham and ’t Hart 1998; Mort et al. 2001). Southern African Crassulaceae belong exclusively to Crassuloideae (Crassula) and Kalanchoideae (van Ham and ’t Hart 1998; Mort et al. 2001). Genera of the latter are predominantly distributed in either the winter-rainfall (Tylecodon, Adromischus) or the summer-rainfall region (Kalanchoe). Cotyledon and Crassula are distributed in both regions, but many sections in the latter are specialised (Jürgens 1995). Diversity centres of secondary importance are the wider Californian winter-rainfall region (lineage within the Leucosedum clade with Sedella, Dudleya and the American Sedum subg. Gormania), Macaronesia (Aeonieae and a few Sedum species of the Acre clade), the Mediterranean (mainly Leucosedum clade: Sedum subg. Gormania, Pistorinia and Rosularia, and a few Sedum subg. Sedum in the Acre clade), the wider Himalayan region (Telephieae and Umbiliceae and the Asian Sedum subg. Sedum), East and Northeast Africa (Crassula, Kalanchoe, Sedum, Cotyledon, Hypagophytum, Afrovivella), and Madagascar (Kalanchoe, Perrierosedum, a few Crassula). All these centres, except for the Himalayan one, exhibit at least one or two (near-)endemic genera. Crassulaceae are poorly represented in the humid tropics as well as in South America (Thiede 1995) and Australia (Toelken 1986). Most genera are conﬁned to a single continent. Exceptions are Sedum, Kalanchoe, the circumboreal Rhodiola and Hylotelephium, and the semi-aquatic Crassula (Tillaea), the worldwide distribution of which is attributed to long-distance dispersal by birds (Bywater and Wickens 1983). Of the genera restricted to the New World, only Echeveria and Villadia extend to South America, separated by a broad gap in Central America; all others are conﬁned to North America and Guatemala (Thiede 1995). Migration and diversiﬁcation of Crassulaceae principally followed the route (southern) Africa → Asia → Europe-Mediterranean → (northern) America (Fig. 27; see also van Ham and ’t Hart 1998 and Mort et al. 2001). Since Crassuloideae and Kalanchoideae are mainly southern African (Fig. 27), a ﬁrst major diversiﬁcation in southern Africa is assumed. The next branching clades, Telephieae and Umbiliceae, are mainly Asian, with Umbilicus and Phedimus extending to the eastern Mediterranean. Semperviveae extend from the Middle East to the Mediterranean and parts of Europe. Aeonieae and Sedeae are basically

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European-Mediterranean. Aeonieae are diversiﬁed in Macaronesia, and Sedeae include distinct northern American lineages within the Leucosedum and Acre clades. The northern temperate clades are poor in species; whereas northern American and southern African lineages are highly diversiﬁed (Fig. 27). Growth form zonation reﬂects the climatic conditions: hemicryptophytes (Hylotelephium, many Umbiliceae) are restricted to northern temperate regions, annuals occur in climates with short vegetation periods, especially in winter-rainfall regions (’t Hart 1997b) and in alpine regions especially in East Asia, and subshrubs are restricted to regions without severe frosts. In contrast, small, often rooting and/or mat-forming herbs as well as stem-less rosette plants occur nearly throughout all regions (cf. also Böttcher and Jäger 1984 for Sedum). Crassulaceae generally prefer azonal sites, usually with more moderate temperatures and higher air humidity. Most taxa grow in arid habitats such as rocks and rock ﬁssures under otherwise more humid climatic conditions, or in mountain regions in moderately arid areas, and are largely absent from hot deserts and arid lowlands. An exception is the arid coast of California, where many Dudleya species occur under moderate temperatures on coastal rocks exposed to sea breezes and fog (Thiede 2004), and the arid southern African Succulent Karoo, which exhibits a considerable species richness. Many rock plant communities with Crassulaceae have been described for Tenerife (Rivas-Martínez et al. 1993), Europe (Ellenberg 1996), Africa (Knapp 1973) and Arabia (Deil 1991). More unusual habitats are wet bogs (e.g. Sedum villosum), ephemeral water ponds where many Crassula (Tillaea) occur nearly hydrophytic, seasonally wet rock pools (e.g. Sedella), or moist forests with a few epiphytic Echeveria (Mexico, Central America), Sedum (Central and East Africa) and Kalanchoe (Madagascar). Edaphic specialisation is rare, e.g. Sempervivum dolomiticum is found only on dolomite, and Sedum alpestre occurs on siliceous and Sedum atratum on calcareous soil (Huber 1961). Germination and seedling establishment in rock habitats often occur within lichen or moss covers (e.g. Dudleya; Riefner et al. 2003). Crassulaceae frequently represent a ﬁrst pioneer vegetation on shallow soils (e.g. Braun-Blanquet and Sutter 1982). Parasites. Speciﬁc crassulacean fungal parasites, the powdery mildews Erysiphe sedi and

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Microsphaera umbilici (Braun 1987) and the rusts Puccinia umbilici and P. rhodiolae and Uromyces sedi, are all restricted to Telephieae and/or Umbiliceae. For further data on speciﬁc Puccinia, see Huber (1961). The rust fungi Endophyllum sempervivi and the mildews Fusarium solani and Phytophthora nicotianae var. parasitica occur on Sempervivum leaves (Ph. Neeff; in litt. 2004). The mildew Oidium kalanchoeae is known only from cultivated Kalanchoe (Braun 1987). Within angiosperms, Cuscuta campestris (Convolvulaceae) and Tapinanthus oleifolius (Loranthaceae) are unspeciﬁc parasites on Cotyledon (Visser 1981). Cuscuta spp. are occasionally found on European/Mediterranean Sedum, Petrosedum and Aeonium (U. Eggli, pers. obs.). Several mining insect larvae feed speciﬁcally on Crassulaceae: Sandia xami (Lepidoptera) on Mexican species (Jiménez and Soberón 1989), Phytomyza sedi (Diptera) and Glyphipteryx equitella (Lepidoptera) on European Sedum, and Phytomyza rhodiolae (Diptera), P. sedicola, Yponomeuta vigintipunctatus (Lepidoptera) and Apion sedi (Coleoptera) on European Telephieae and/or Umbiliceae (Huber 1961; Bland 1995). Thuleaphis sedi is a specialist aphid on Rhodiola rosea (Jacob 1964). Physiology. Nocturnal CO2 ﬁxation based on the Crassulacean acid metabolism (CAM) pathway was ﬁrst detected in Crassulaceae and named after this family, although it is now known to occur in many succulent taxa and a few non-succulents. CAM is expressed in many Crassulaceae and is either constitutive or facultatively induced under certain environmental conditions, especially under drought stress, and is found even in the weakly succulent semi-aquatic Crassula (Tillaea; Keeley 1998). Detailed data on CAM have been published for Sedum and Aeonium (Pilon-Smits 1992), Macaronesian Aeonieae (Lösch 1990), and Kalanchoe (Kluge and Brulfert 1996). Crassulaceae and other CAM plants are often highly endopolyploid (de Rocher et al. 1990), but the reason for this is unknown. Most Crassula studied by Martin and von Willert (2000) absorb water deposited on the leaf surfaces via hydathodes (see Vegetative Anatomy), which may subsequently stimulate CO2 ﬁxation rates. Palaeobotany. Probably no fossil remains are known (Thomas Bolliger, pers. comm.); leaf fossils ascribed to Crassulaceae (e.g. Crassulaceophyllum) are doubtful.

Economic Importance. Apart from their horticultural value, Crassulaceae have minimal economic importance. Kalanchoe blossfeldiana cultivars are annually produced in large quantities as popular pot plants. Species of Hylotelephium, Phedimus, Sedum and Sempervivum are frequently cultivated in rock gardens and increasingly used for ‘green roofs’. Most perennial taxa of the family are choice collectors’ plants and commonly grown by succulent plant enthusiasts. Overviews of genera and species of horticultural importance are given by Cullen (1995) and Huxley et al. (1997). Several species, especially Kalanchoe pinnata, are aggressive invaders in the tropics. Nowadays, Crassulaceae are not used for food, although especially Petrosedum rupestre (vernacular name ‘Trip-Madame’) was recommended for salad in medieval herbals (’t Hart 1997a) and has locally been used as salad or pot-herb (Lippert 1995). The ﬂeshy leaves may appear appealing in arid environments, but they are completely tasteless or bitter and are generally avoided even by cattle (’t Hart 1997a). Rhizomes of Rhodiola rosea have some use in folk medicine and were used ofﬁcinally (‘Rose Root’; Radix Rhodiolae); an ethnobotanical review for Norway lists many uses (Alm 2004). For further data on folk uses and folk names of Central European taxa, see Huber (1961). Several Asian species of Rhodiola have been the subject of intense phytochemical and pharmacological studies (e.g. Kurkin and Zapesochnaya 1986; many older Russian references listed by Clausen 1975: 531). The medicinal properties of their rhizomes were known for a long time, and recent investigations have identiﬁed a vast array of different chemical compounds (e.g. Yoshikawa et al. 1996). There exist attempts for the large-scale cultivation of at least R. sachalinensis for the improved production of certain bioactive compounds (e.g. Xu et al. 1998). Conservation. Most Crassulaceae occur in rocky places not prone to habitat destruction (’t Hart 1997a). Narrow endemics (frequent in California, Mexico, Africa, Madagascar and Macaronesia) may be seriously threatened by land development and tourism. For example, two of three accessible populations of the Madeiran Sedum fusiforme have been destroyed during the construction of tourist accommodations (’t Hart 1997a). Legal and illegal trade and collecting of wild plants do occur but appear to be rather restricted,

Crassulaceae

compared to other succulents, due to low demands and easy vegetative and generative propagation (data for South Africa: Newton and Chan 1998). Genera popular in horticulture are typically protected under state laws (e.g. Sempervivum, Aeonium and Aichryson). Sedella leiocarpa and eight Dudleya taxa are listed as endangered in the USA (U.S. Fish and Wildlife Service 2004). Many data (general and per country listings with IUCN categories) are included in Oldﬁeld (1997). Golding (2002) lists the IUCN Red Data List categories for many southern African species per country. Studies on the conservation biology (reproduction, life history, population genetics) are available for Rhodiola integrifolia and Dudleya multicaulis (see Reproductive Systems). Special ex situ propagation programs have been initiated for some endangered local endemics (e.g. the Madeiran Aichryson dumosum, Fernandes 1997). Most genera and species of horticultural appeal appear to be cultivated in specialised public and private collections.

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Stamens equal in number to petals 2. Leaves usually decussate, rarely verticillate; with hydathodes along margins and/or leaf face; seeds sinuatepapillate (Crassula type) 3 – Not as above; leaves spiral 4 3. Perennial tuberous herbs, ﬂowers 10–12-merous; fruits 2-seeded, breaking transversely (Ethiopia) 34. Hypagophytum – Not as above; when plants tuberous or ﬂowers polymerous, then fruits not few-seeded 33. Crassula 4. Plants with persistent or monocarpic rosettes 5 – Plants without rosettes 7 5. Monocarpic rosette-forming herbs (Asia) 6 – Perennial shrublets with lax rosettes at branch tips (Mexico) 25. Graptopetalum p.p. 6. Inﬂorescences broad, ﬂat-topped, corymboid thyrsoids 1. Sinocrassula – Inﬂorescences narrow-elongate thyrsoids 2. Kungia 7. Plants tuberous; leaves peltate; inﬂorescences elongate racemes 7. Umbilicus p.p. (U. heylandianus) – Not as above, annual to perennial herbs 8 8. Annual to perennial herbs; fruits many-seeded follicles (N hemisphere) 22. Sedum p.p. (e.g. S. rubens) – Minute annual herbs; fruits 1-seeded nutlets (USA: California) 20. Sedella p.p.

Stems frail or leaves caducous Conspectus of Crassulaceae I. Subfam. Sempervivoideae Arn. (1832). 1. Tribe Telephieae (’t Hart) Ohba and Thiede ined. (= Hylotelephium clade). Genera 1–5 Incertae sedis: genus 6 2. Tribe Umbiliceae Meisn. (1838) (= Rhodiola clade). Genera 7–10 3. Tribe Semperviveae Dumort. (1827) (= Sempervivum clade). Genera 11–12 and Sedum subg. Gormania p.min.p. (S. assyriacum, S. mooneyi) 4. Tribe Aeonieae Thiede ined. (= Aeonium clade). Genera 13–15 and Sedum subg. Gormania p.min.p. (series Caerulea, Pubescens and Monanthoidea) 5. Tribe Sedeae Fr. (1835). a. Leucosedum clade Genera 16–21 and Sedum subg. Gormania p.maj.p. b. Acre clade Genera 22–28 and Sedum subg. Sedum II. Subfam. Kalanchoideae A. Berger (1930) (= Kalanchoe clade). Genera 29–32 III. Subfam. Crassuloideae Burnett (1835) (= Crassula clade). Genera 33–34

Perennials with monocarpic rosettes with terminal inﬂorescences

Key to the Genera 1. Stamens equal in number to petals – Stamens double in number to petals

9. Perennials, but leaves or aboveground stems annually caducous 10 – Annual or biennial, or perennial and then with at least some perennating leaves 17 10. Stems perennial, succulent, ± elongated; leaves crowded at branch tips (southern Africa) 31. Tylecodon – Stems annual, not succulent; perennials with underground tubers, rhizomes or thickened roots (usually outside Africa) 11 11. Plants with tuberous stems 12 – Plants with rhizomes, caudices or thickened roots 13 12. Leaves not peltate; inﬂorescences axillary, cymose (W USA and Baja California) 21. Dudleya p.p. (D. sect. Hasseanthus) – Leaves usually distinctly peltate; inﬂorescences terminal, racemes or panicles 7. Umbilicus p.p. 13. Plants with thickened roots; leaves terete-subulate (America) 23. Villadia p.p. – Plants with rhizomes or caudices; leaves ﬂat 14 14. Carpels narrowed at base (stipitate-attenuate) 5. Hylotelephium – Carpels with broad base 15 15. Rhizomes thin; inﬂorescences pleiochasia 10. Phedimus p.p. – Plants with very thick rhizome; inﬂorescences thyrsoids 16 16. Petals free; ﬂowers often unisexual (plants monoecious or dioecious) 9. Rhodiola – Corolla connate at base for 1/3–2/3 8. Pseudosedum

2 9

17. Plants with perennial monocarpic rosettes with terminal inﬂorescences 18

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– Plants annual (rarely biennial or triennial), or perennial and then not with monocarpic rosettes with terminal inﬂorescences 24 18. Nectary scales larger than the insigniﬁcant petals (Canary Islands) 14. Monanthes p.p. (M. sect. Monanthes) – Nectary scales inconspicuous, much smaller than the showy petals 19 19. Flowers 5(rarely 6)-merous; inﬂorescences corymboid to much elongated and spike-like thyrsoids 20 – Flowers (5)6–32-merous; inﬂorescences corymboid to dome-shaped thyrsoids or with several cincinni, never spike-like 22 20. Inﬂorescences ﬂat-topped, corymboid thyrsoids, or cymose, few-ﬂowered (eastern Mediterranean, W Asia) 18. Prometheum p.p. – Inﬂorescences elongate, many-ﬂowered 21 21. Partial inﬂorescences helicoid (Turkey, Iraq, Turkmenistan) 17. Rosularia p.p. (R. elymaitica) – Partial inﬂorescences never helicoid (C to E Asia) 4. Orostachys 22. Leaves semi-terete, not apiculate; ﬂowers 5-merous; white (Europe/Mediterranean) 22. Sedum p.p. (e.g. S. hirsutum) – Leaves usually ﬂat and apiculate; ﬂowers 6–32-merous 23 23. Rosettes sessile, usually < 10 cm; inﬂorescences pleiochasia; ﬂowers 6–18-merous, often pink to purple, rarely white or yellow; carpels (sub)erect (Europe to Caucasus) 11. Sempervivum – Rosettes sessile or at branch tips, often > 10 cm; inﬂorescences thyrsoids or pleiochasia; ﬂowers (6–)10–32merous, often yellow or whitish, rarely reddish; carpels spreading (mainly Macaronesia, also N and NE Africa and SW Arabia) 15. Aeonium 24. Leaves decussate throughout length of stems 25 – Leaves alternate at least in upper stem parts, or in rosettes, rarely verticillate 32

Leaves decussate 25. Annual to biennial, glabrous to glandular-hairy herbs, to 15 cm; ﬂowers (4)5-merous, white, pink or purplish; petals 4–5 mm (Mediterranean) 26 – Perennial herbs (rarely monocarpic), or shrubs or small trees, or lianas; ﬂowers 4–6-merous; petals > 5 mm, in various colours 27 26. Annual glabrous herbs; inﬂorescences to 5 cm 10. Phedimus p.p. (P. stellatus) – Annual to biennial, glandular-hairy herbs; inﬂorescences to 60 cm 22. Sedum p.p. (e.g. S. cepaea) 27. Flowers 4-merous; herbs (rarely monocarpic) to shrubs or small trees, or lianas 30. Kalanchoe – Flowers 5- or 6-merous; shrublets or herbs 28 28. Flowers (5)6-merous, white 29 – Flowers 5-merous, not white (Africa, Caucasus, North America) 30 29. Shrublets to 80 cm tall (Madagascar) 6. Perrierosedum – Dwarf herbs to 10 cm tall (Europe/Mediterranean) 22. Sedum p.p. (e.g. S. dasyphyllum) 30. Herbs with creeping stems; leaves petiolate, ﬂat and thin; inﬂorescences arching over; ﬂowers yellow, narrowly urceolate (Caucasus) 7. Umbilicus p.p. (U. oppositifolius)

– Not as above 31 31. Shrubs; leaves not easily detached; ﬂowers 2–3 cm, usually pendent; corolla connate at base (Africa, Arabia) 32. Cotyledon – Herbs; leaves often easily detached; ﬂowers to 1 cm, ± upright; petals free (USA, Mexico) 24. Lenophyllum 32. Leaves verticillate (Africa) 22. Sedum p.p. (e.g. S. epidendrum) – Leaves alternate at least in upper stem parts, or in rosettes 33 33. Annual (to rarely biennial or triennial) herbs 34 – Perennial herbs to shrublets 40

Annuals 34. Flowers 6–7-merous, dirty white; nectary scales conspicuous, larger than the insigniﬁcant petals (Canary Islands) 14. Monanthes p.p. (M. icterica) – Flowers 5–12-merous; nectary scales inconspicuous and never larger than the showy petals 35 35. Flower 5-merous; corolla distinctly connate (Iberian Peninsula, N Africa) 36 – Flower 5–12-merous; petals (nearly) free 37 36. Filaments inserted at the base of the corolla tube; stylodia ±1 mm 22. Sedum p.p. (S. mucizonia) – Filaments inserted slightly below the mouth of the corolla tube; stylodia 2.5–5 mm 16. Pistorinia 37. Annual to biennial herbs; leaves ﬂat; young plants with conspicuous basal rosettes (E Mediterranean) 22. Sedum p.p. (S. lampusae, etc.) – Young plants without basal rosettes 38 38. Fruits 1-seeded nutlets (USA: California) 20. Sedella p.p. – Fruits many-seeded follicles opening at ventral suture 39 39. Annual to triennial herbs; leaves ﬂat, often ± rosulate near branch tips; ﬂowers yellow; nectary scales 2–5-ﬁd (Macaronesia) 13. Aichryson p.p. (A. sect. Aichryson) – Annual herbs; leaves ± semi-terete; nectary scales entire (northern hemisphere to E Africa) 22. Sedum p.p.

Perennials with large nectary scales 40. Nectary scales conspicuous, larger than the insigniﬁcant petals 41 – Nectary scales inconspicuous, much smaller than the showy petals 43 41. Leaves with bladder-cell idioblasts (Canary Islands) 14. Monanthes p.p. – Leaves without bladder-cell idioblasts 42 42. Flowers 5-merous; stems elongate, repent (Mexico) 22. Sedum p.p. (S. longipes) – Flowers 5–7-merous; stems short and thick; leaves in rosettes (Morocco) 22. Sedum p.p. (S. surculosum) 43. Inﬂorescences terminal; leaves not in rosettes 44 – Inﬂorescences lateral; leaves usually in distinct rosettes, or at least crowded at branch tips 49

Perennials without rosettes and with terminal inﬂorescences 44. Plants herbaceous, at highest slightly woody at base 45 – Plants shrubby 47 45. Corolla connate (Mexico, Peru) 23. Villadia p.p. (V. imbricata, etc.)

Crassulaceae – Petals free 46 46. Leaves ± densely imbricate and acuminate; ﬂowers yellow(ish); fruits erect (Europe/Mediterranean) 12. Petrosedum – Leaves not densely imbricate nor acuminate; fruits erect to spreading (northern hemisphere to E Africa) 22. Sedum p.p. (p.max.p.) 47. Stems distinctly succulent, with ± ﬂaking papery bark; inﬂorescences pleiochasia; petals free 22. Sedum p.p. (e.g. S. frutescens) – Stems not distinctly succulent, without ﬂaking papery bark; inﬂorescences elongate; corolla connate 48 48. Leaves usually soft ﬂeshy, semi-terete; inﬂorescences thyrsoids; ﬁlaments glabrous (America) 23. Villadia p.p. – Leaves ﬁrmly ﬂeshy; inﬂorescences thyrses or spikes without terminal ﬂower; ﬁlaments papillate where connate with corolla (southern Africa) 29. Adromischus

Perennials with rosettes, lateral inﬂorescences, and the corolla connate for most of its length 49. Corolla connate for most of its length; petals distinctly ﬂeshy (America) 50 – Petals free or corolla connate for less than 1/2 of its length; petals membranous 51 50. Leaves usually very thick and with strong wax bloom; inﬂorescences cincinnoid; bracts usually very large and ± covering the ﬂowers at anthesis; petals with basal scale on each margin (Mexico) 28. Pachyphytum – Inﬂorescences racemose, cymose-paniculate, spicate thyrsoids, or cincinnoid; petals usually without, rarely with small scales (southern USA to Argentina) 27. Echeveria

Perennials with rosettes, shrubby habit and lateral inﬂorescences, and petals free or corolla connate for <1/2 of its length 51. Shrublets; rosettes at branch tips 52 – Stem-less herbs 56 52. Leaves glandular-hairy; ﬂowers yellow, 7–8-merous (Canary Islands) 13. Aichryson p.p. (A. sect. Macrobia) – Leaves glabrous (America) 53 53. Leaves with intensive wax bloom; rosettes typically branching dichotomously; leaves not easily detached; seeds costate (W USA and Baja California) 21. Dudleya p.p. (e.g. D. formosa) – Not as above; seeds reticulate-papillate (mainland Mexico, Guatemala) 55 54. Petals (almost) free, yellow or white 22. Sedum p.p. (S. sect. Pachysedum) – Corolla connate at base 55 55. Inﬂorescences broad thyrsoids with cincinnoid partial inﬂorescences; inner face of petals usually with ± red to brown spottings, or whitish to yellowish 25. Graptopetalum p.p. – Inﬂorescences elongate and narrow, partly spike-like thyrsoids; petals inside ± purplish-red, unspotted 26. Thompsonella p.p.

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Perennials with stem-less rosettes and lateral inﬂorescences, and petals free or corolla connate for <1/2 of its length 56. Leaves glandular-pubescent to glandular-hairy; corolla connate at base 57 – Leaves glabrous; petals free or corolla connate at base 59 57. Plants offsetting with long brittle runners; leaf apex mucronate, margins distinctly ciliate (Ethiopia) 19. Afrovivella – Plants not offsetting or with short runners; leaf apex not mucronate, margins usually not ciliate 58 58. Leaves densely glandular-pubescent; ﬂowers 5-merous, white or pale yellow/reddish; fruits erect or spreading (E Mediterranean to W Asia) 18. Prometheum p.p. – Leaves glandular-hairy; ﬂowers 5–9-merous, white to pink(ish); fruits erect (E Mediterranean, Near East to E Asia) 17. Rosularia p.p. 59. Plants with thickened taproot; leaf apex cuspidate to spinulose; carpels connate at base, with only 4–6 ovules each (Asia) 3. Meterostachys – Not as above 60 60. Rosettes typically branching dichotomously; leaves usually with intensive wax-bloom, not easily detached; bracts semi-amplexicaul, never spurred (W USA and Baja California) 21. Dudleya p.p. – Not as above (southern USA, mainland Mexico) 61 61. Leaves usually mucronate; inﬂorescences short and broad thyrsoids; petals usually with ± red to brown spottings, or bright pink 25. Graptopetalum p.p. (G. sect. Graptopetalum) – Leaves not mucronate; inﬂorescences elongate and narrow, partly spike-like thyrsoids; petals inside ± purplish-red 26. Thompsonella p.p.

Genera of Crassulaceae Basic Features Herbaceous, arhizomatic perennials, tanniniferous, with solitary crystals or druses; shoots aerial; leaves alternate, scattered (dispersed), succulent∗ , sessile, ± ﬂat, entire, with marginal hydathodes, glabrous or with non-glandular indumentum; stomata anisocytic∗ ; inﬂorescences terminal thyrsoids∗ , partial inﬂorescences dichasial; ﬂowers ± erect, actinomorphic, 5merous, obdiplostemonous∗ ; sepals ± appressed to corolla, connate at base; corolla choripetalous, spreading; stamens with ﬁlaments free to base; anthers basiﬁxed, latrorse, yellow, without terminal connective appendage; ovary superior; carpels free (nearly) to base, with many crassinucellate ovules and carpellary nectary scales∗ at their bases; fruits erect follicles, opening along whole suture; seeds small, ± cylindrically fusiform, ± brown, testa papillate∗ . x = 8.

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Note: these features are valid for all genera of the family, unless modiﬁed in the subsequent characterisations of subfamilies, tribes, clades or informal generic groups in which their characters behave correspondingly. Putative synapomorphies for higher taxa and major clades are marked with asterisks (∗ ). Note the distinction made between taxonomic characters which are valid only for the genera included in the respective taxon (e.g. tribe), thus excluding the formalised segregates of Sedum, and cladistic synapomorphies which are valid for all members of a clade, including the segregates of Sedum. The synoptic treatments for all genera included in Eggli (2003) as well as standard ﬂora works are not cited in the descriptions of the genera. Subfamilies Sempervivoideae and Kalanchoideae Leaves usually with single (sub)apical hydathode∗ ; seeds costate∗ . Genera 1–32. (Note that basic features for family are further valid.) I. Subfam. Sempervivoideae Arn. (1832). Flowers (4)5(–32)-merous, ﬂowers obdiplostemonous (rarely haplostemonous, but then leaves never decussate); seeds costate with many (>6, usually c. 10) costae∗ in side view. Genera 1–28. Largely conﬁned to the northern hemisphere. I.1. Tribe Telephieae (’t Hart) Ohba & Thiede, ined. Leaves usually in rosettes (except Hylotelephium), rosettes usually monocarpic, leaves partly cuspidate; petals often spotted to mottled with red to brown; carpels stipitate or connate at base; ﬂowering mainly in autumn. Genera 1–5. Mainly in temperate Asia. 1. Sinocrassula A. Berger Sinocrassula A. Berger in Engler & Prantl, Nat. Pﬂanzenfam., ed. 2, 18a:462 (1930).

Perennial, sometimes annual or biennial herbs, glabrous, papillose or rarely pubescent; leaves obtuse to usually acuminate, often mottled with red; inﬂorescences broad corymbose thyrsoids, simple

to richly branched; ﬂowers campanulate-urceolate; petals free, connivent to urceolate corolla; ± whitish, greenish or rose, ± mottled with red, orange or brown; stamens 5, alternating with and slightly shorter than petals; carpels connate at base; stylodia abruptly narrowed. n = 11. Seven species, northern India (Uttar Pradesh), Bhutan, eastern Tibet, south-western China (Yunnan, Szechuan). 2. Kungia K.T. Fu Kungia K.T. Fu in J.N.W. Teachers Coll. (Nat. Sci.) 1:3 (1988). Orostachys sect. Schoenlandia H. Ohba (1978).

Herbs, glabrous or hairy; stolons present; sterile stems usually present; basal leaves in subsessile rosettes, decussate or usually alternate, obtuse; ﬂowering stems erect, very slender but strong; inﬂorescences many-ﬂowered terminal, narrow, racemiform or paniculiform thyrsoids; sepals lanceolate-triangular, much shorter than petals, spurless; petals connate at base, lanceolate, red or purple; stamens 5, alternating with petals, shorter than petals; anthers oblong-reniform; carpels nearly free, oblong, base attenuate or stalked; stylodia long. Two species, south-western China (northern Szechuan, Gansu, Shaanxi), on rocky slopes from 700–3,100 m. Sister to Sinocrassula, according to molecular data (Hideaki Ohba, unpubl. data, pers. comm. 2004); the two genera share haplostemonous ﬂowers. Formerly classiﬁed as sect. Schoenlandia within Orostachys. 3. Meterostachys Nakai Meterostachys Nakai, Bot. Mag. (Tokyo) 49:74, 210 (1935); Moran, Cact. Succ. J. (U.S.) 44:262–273 (1972); Ohba, J. Fac. Sci. Univ. Tokyo III, Bot. 12:173–174 (1978).

Herbs with thickened taproot; leaves in small rosettes, apex cuspidate to spinulose, often cartilaginous; inﬂorescences axillary, simple, cymose; ﬂowers (4)5-merous, pedicels often longer than ﬂowers; petals upright, connate at base for 1/3 to 2/5, white, often with reddish hue; stamens distinctly shorter than petals; carpels connate at base, suberect, with only 4–6 ovules each; n = 16. Only 1 species, M. sikokiana (Makino) Nakai from Japan, Korea and China (Byalt 1997). Sister to Orostachys subsect. Appendiculatae, according to molecular data (Mayuzumi and Ohba 2004).

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4. Orostachys Fischer Orostachys Fischer, Mém. Soc. Imp. Naturalistes Moscou 2:274 (1809); Byalt, Novost. Sist. Vyssh. Rast. 32:40–50 (2000), rev. (in Russian).

Biennial monocarpic herbs; leaves of ﬁrst year in solitary rosette, rosettes often dimorphic with compact winter (resting) stage, normally offsetting; leaves linear to ovate, apex cuspidate (ser. Appendiculatae) or blunt (ser. Orostachys); inﬂorescences dense, narrowly pyramidal to cylindric, many-ﬂowered thyrsoids, usually with secondary branches; sepals connate at base; corolla ± stellate; petals lanceolate, subconnate, white, pink or red; stamens longer than petals; carpels stipitate; stylodia slender. n = 12. Eleven species, Russia (East Siberia), Kazakhstan, Mongolia, China, Korea, Japan. Polyphyletic, according to molecular data (Mayuzumi and Ohba 2004): subsect. Orostachys is nested within Hylotelephium, and subsect. Appendiculatae is sister to Meterostachys but differs strongly from that genus and should possibly be given separate generic status. See also under Kungia. 5. Hylotelephium H. Ohba

Fig. 28

Hylotelephium H. Ohba, Bot. Mag. (Tokyo) 90:46–47 (1977); Fröderström, Acta Horti Gothob. suppl. 5:1–75 (1930), sub Sedum; Ohba, J. Fac. Sci. Univ. Tokyo III, Bot. 12:162–166 (1978).

Hemicryptophytes with rootstock of ﬁbrous to tuberous, often carrot-shaped roots and short, ﬂeshy or woody rhizome (H. populifolium (Pall.) H. Ohba with perennial, woody, frail stems); ﬂowering stems from adventitious buds on rootstock or basal nodes of former years’ ﬂowering stems, simple, annual, usually with numerous leaves and visible internodes, some species with additional vegetative shoots; leaves alternate, rarely decussate to 3–5-whorled, broad, ﬂat, margin entire, crenate, or lobed, apex usually blunt; inﬂorescences thyrsoids, compound or paniculate or umbellatecorymbose in shape, dense and many-ﬂowered; ﬂowers (4)5-merous; petals usually free, white, purple, pink or red, occasionally yellowish or greenish; stamens shorter to longer than petals, those opposite petals basally connate with them; carpels stipitate. n = usually 12, also 11, 23, 24, 25, 46. About 27 species, East Asia, Siberia, Caucasus, Europe, North America. A relatively recent segregate from Sedum s.l. The division into two sections with two series

Fig. 28. Crassulaceae. A–C Hylotelephium telephium. A Flowering plant with tuberous roots. B Flower seen from side. C Seed. D–F Kalanchoe grandiﬂora. D Flowering shoot. E Flower, opened out. F Ovary with hypogynous scales. (Berger 1930)

(Ohba, l.c.) is not supported by molecular data (Mayuzumi and Ohba 2004). These data also indicate that Orostachys sect. Orostachys is nested within Hylotelephium; the two taxa share blunt leaves, stipitate carpels and x = 12. This causes nomenclatural problems, since Orostachys antedates Hylotelephium. Orostachys paradoxa (A.P. Khokhr. & Vorosch.) Czerep. links both taxa (Byalt 1998).

Incertae sedis: 6. Perrierosedum (A. Berger) H. Ohba Perrierosedum (A. Berger) H. Ohba, J. Fac. Sci. Univ. Tokyo III, Bot. 12:166 (1978).

Branched shrublets 50–80 cm; stems 4-angled; leaves decussate, oblong-spathulate, base long-

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attenuate, margins crenulate; inﬂorescences terminal, corymbose-cymose, 5–10-ﬂowered, pedunculate; ﬂowers (5)6-merous; sepals free; petals free, broadly spathulate, white tinged with red; ﬁlaments shorter than petals; nectary scales conspicuous, 3–3.5 mm, tips biﬁd; carpels free, ventrally straight, tapering towards tip. Only 1 species, P. madagascariense (H. Perrier) H. Ohba from Madagascar. Possibly linking the African Kalanchoideae with the Asian Telephieae. I.2. Tribe Umbiliceae Meisn. (1838). Rhizomatic hemicryptophytes to tuberous geophytes∗ ; leaves usually crenate to dentate∗ (except Pseudosedum); ﬂowering mainly in spring to early summer. Genera 7–10. Mainly in temperate Asia. 7. Umbilicus DC. Umbilicus DC., Bull. Sci. Soc. Philom. Paris 3:1 (1801). Chiastophyllum (Ledebour) Stapf ex A. Berger (1930).

Small herbs with tubers and frail stems (sect. Umbilicus) or with short, creeping and rooting rhizomatous stems (U. oppositifolius); tissues with crystal sand; leaves alternate (sect. Umbilicus) or decussate (U. oppositifolius), suborbicular, with distinct petiole, ± peltate with central dimple (sect. Umbilicus) or not peltate (U. oppositifolius); inﬂorescences many-ﬂowered, long terminal panicles or racemes (sect. Umbilicus) or double racemes (U. oppositifolius), without terminal ﬂower, upright (sect. Umbilicus) or arching over (U. oppositifolius); ﬂowers usually ± horizontal or drooping, rarely haplostemonous (usually in U. heylandianus Webb. & Berth.); corolla tubular or campanulate; petals connate, white, green or yellow; ﬁlaments usually connate with corolla for most of their length; seeds multipapillate, papillae arranged in small groups (sect. Umbilicus) or connate (U. oppositifolius). n = 24. Thirteen species, western, southern and central Europe, Macaronesia, Mediterranean, Near East to Caucasus, Arabia, North, Central and East Africa. Divided into sect. Umbilicus, which exhibits complex patterns of variation probably due to selfpollination and is in need of revision, and sect. Chiastophyllum with U. oppositifolius (Ledeb.) Ledeb. from the Caucasus, which is also recognised at generic level by some authors.

8. Pseudosedum (Boiss.) A. Berger Pseudosedum (Boiss.) A. Berger in Engler & Prantl, Nat. Pﬂanzenfam., ed. 2, 18a:465 (1930).

Hemicryptophytes; ﬂowering stems one to numerous, arising from usually well-developed simple or branched sympodial rhizome, old stems usually persistent; leaves usually linear, (sub)obtuse, broadly spurred, subterete, entire, usually ﬂeshy; ﬂowering branches one to many, simple, usually densely leafy, 5–40 cm; inﬂorescences dense terminal thyrsoids, corymbose or umbellate, rarely paniculate, usually many-ﬂowered; ﬂowers (5)6merous; corolla campanulate to tubular; petals connate at base for 1/3 to 2/3, lobes ± divergent, pink to violet or red or pure white; fruits erect or slightly divergent follicles. Twelve species, Central Asia; stony soils in mountainous regions. Sister to Rhodiola, according to molecular data (Mayuzumi and Ohba 2004); the two genera are hemicryptophytes, with usually well-developed rhizomes. 9. Rhodiola L. Rhodiola L., Sp. Pl.: 1035 (1753); Ohba, J. Fac. Sci. Univ. Tokyo III, Bot. 12:139–198 (1978); l.c. 12:337–405 (1980); l.c. 13:65–119 (1981); l.c. 13:121–174 (1982). Clementsia Rose (1903).

Hemicryptophytes; rhizomes monopodial, massive or slender, apical part with foliage and/or scaly leaves; leaves usually ﬂat; ﬂowering stems sometimes persistent for a while; inﬂorescences usually broad thyrsoids, partly reduced to solitary ﬂowers or rarely racemes; ﬂowers hermaphrodite or plants dioecious (rarely monoecious), 4–5(6)merous, pedicellate, when dioecious: petals and ovaries opposite in male but alternate in female plants, when hermaphrodite or monoecious: petals and ovaries always opposite; calyx ﬂeshy, in female plants forming a tube divided into 4–5(6) ± equal lobes; petals free, white, reddish, deep purplish-red or pale yellow to greenish, always longer than sepals in female plants; carpels superior to semi-inferior, usually connate at base (rarely completely free), straight at anthesis, slightly patent in fruit. n = 7, 10, 11, 22, 33, 44, 55. About 58 species, East Asia, Siberia, North America, Europe; especially sub-Arctic and alpine zones. The subdivision into four subgenera with seven sections (Ohba 1978) is not supported by molecular data (Mayuzumi and Ohba 2004).

Crassulaceae

10. Phedimus Raf. Phedimus Raf., Amer. Monthly Mag. Crit. Rev. 1:438 (1817); Grulich, Preslia 56:29–46 (1984), sub Asterosedum; Chung & Kim, Korean J. Pl. Taxon. 19:189–227 (1989), rev. Korean taxa. Aizopsis Grulich (1984). Asterosedum Grulich (1984). Spathulata (A. Borissova) A. Löve & D. Löve (1985).

Perennial or rarely annual herbs, usually glabrous, sometimes stems woody at base, emerging from thin woody rhizome; leaves decussate or alternate, base narrowed; with several hydathodes on lower face along margins; ﬂowering branches erect or ascending; inﬂorescences usually dense many-ﬂowered terminal pleiochasia; ﬂowers (4)5–6(7)-merous; sepals usually unequal; petals free, usually spreading, white, pink, red, purplish (subg. Phedimus) or yellow (subg. Aizoon); anthers red (subg. Phedimus) or yellow, orange or reddish (subg. Aizoon); fruits follicles, usually spreading; seeds costate-papillate (i.e. papillae incompletely connate to costae), multipapillate in P. selskianus (Regel & Maack) ’t Hart (’t Hart and Berendsen 1980; Gontcharova 1999). n = 5, 6, 7, 8, 15–16, c. 32, 33, 34. Eighteen species, eastern Europe and Asia. Only recently re-segregated from Sedum. Divided into subg. Phedimus (stems creeping and rooting, with sterile stems; x = 5, 6, 7; 5 spp.; Mediterranean to Caucasus) and subg. Aizoon (annual shoots often woody at base, emerging from woody rhizome; follicles with distinct lips along suture; x = 8; 13 spp.; China, Japan, Korean and Central Siberia). Subg. Aizoon is distinct morphologically, karyologically and according to molecular data (Mort et al. 2001; Mayuzumi and Ohba 2004), and also recognised at generic level as Aizopsis by some authors. All other Sempervivoideae Plants often glandular-pubescent; leaves basically (semi-)terete∗ (in derived genera often ± ﬂat and thick); partial inﬂorescences typically monochasial∗ (double or single cincinni). Genera 11–28. Mainly northern temperate region, also North, Central and East Africa and southern America. I.3. Tribe Semperviveae Dumort. (1827). Leaves acuminate; inﬂorescences pleiochasial; ﬂowers poly(at least 6)-merous; base chromosome numbers high, n = 12–16.

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Genera 11 + 12. Sedum assyriacum Boiss. (Near East) and S. mooneyi M.G. Gilbert (Ethiopia) of Sedum subg. Gormania, and possibly further species related to these, also come out here according to molecular data (’t Hart 1995; van Ham and ’t Hart 1998). These two species do not share the tribal characters but their yellow ﬂowers agree with those in Petrosedum and some Sempervivum. 11. Sempervivum L. Sempervivum L., Sp. Pl.: 464 (1753); Praeger, Account Sempervivum Group (1932). Jovibarba (A.P. de Candolle) Opiz (1852).

Leaves rosulate, with glandular and non-glandular hairs, reproducing vegetatively through axillary stolons or rarely through rosette division, ﬂattened, glabrous or pubescent, with marginal cilia; inﬂorescences usually pleiochasia, partial inﬂorescences dense, with (2)3(4) single or double cincinni; ﬂowers 6–18-merous; petals spreading and pink, purple, yellow to almost white (sect. Sempervivum) or erect during anthesis, with ﬁmbriate margins and (pale) yellow to whitish (sect. Jovibarba); nectary scales ± square; carpels (sub)erect. n = 16–19, 21, 32, 34, 36, 40, 42, 54. About 63 species, Morocco (Atlas Mts.), Europe to north-western and central Russia, Balkan Peninsula, Carpathians, Turkey, northern Iran, Caucasus. Divided into sect. Sempervivum (ﬂowers 8–18merous; x = 16–21) and sect. Jovibarba (ﬂowers 6(7)-merous; x = 19; 2 spp.; ’t Hart and Bleij 1999). According to molecular data, Jovibarba is nested in Sempervivum (Philipp Neeff, pers. comm.), or both are sister groups (Mort et al. 2001). Notoriously difﬁcult in its taxonomy, due to reticulate evolution. A revision is being undertaken by Ph. Neeff (University of Essen, Germany). Sempervivum shares several features with Petrosedum. 12. Petrosedum Grulich Petrosedum Grulich, Preslia (Praha) 56:39 (1984); ’t Hart, Biosyst. stud. Acre-group and ser. Rupestria of gen. Sedum (Crassulaceae): Thesis Univ. Utrecht (1978). Sedum ser. Rupestria A. Berger (1930).

Mat-forming herbs, glabrous, inﬂorescences also glandular, perennating with branching and rooting non-ﬂowering ascending to repent shoots; leaves (semi-)terete, linear-elliptic, acuminate, spurred,

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usually densely imbricate; ﬂowering shoots erect, simple, 10–60 cm, often ± woody at base; inﬂorescences usually pleiochasia, partial inﬂorescences single or double cincinni, at anthesis erect or nodding; ﬂower (sub)sessile, 6–7(–12)-merous; sepals acute to acuminate; petals obtuse, spreading during anthesis, yellow, rarely white; ﬁlaments usually yellow; carpels erect, dark brown in fruit; stylodia long. n = 12, 13, 16, 17, 24, 26, 32, 34, 36, 44, 48, 56. Seven species, western and central Europe, Balkan, Mediterranean. Sedum ser. Rupestria is here recognised at the generic level, since morphologically it is highly distinct from European-Mediterranean Sedum, also in its embryology (Mauritzon 1933), ﬂavonoid patterns (Stevens et al. 1996) and epicuticular triterpenes (Stevens et al. 1994). According to molecular data, Petrosedum does not form a clade together with Sempervivum, but the two form a polytomy (van Ham and ’t Hart 1998; Mort et al. 2001) or place separate from each other (’t Hart 1995). I.4. Tribe Aeonieae Thiede, ined. Plants glandular-hairy; leaves usually ± ﬂat, in ± distinct rosettes; ﬂowers poly(at least 6)-merous; carpels often with glandular hairs, immersed into receptacle; seeds usually costate-papillate (i.e. papillae incompletely connate to costae) to costate. Genera 13–15. Mainly in Macaronesia. Sedum subg. Gormania ser. Caerulea, Pubescens and Monanthoidea (from North Africa) also belong here, according to molecular data (Mes and ’t Hart 1994; Mes 1995; ’t Hart 1995; van Ham and ’t Hart 1998), but do not exhibit all of the tribal characters. 13. Aichryson Webb & Berth. Aichryson Webb & Berth., Phytogr. Canar. 1:180 (1840); Bramwell, Bol. Inst. Nac. Inv. Agron. (Madrid) 28:203–213 (1968), synopsis; Fairﬁeld et al., Pl. Syst. Evol. 248:71–83 (2004); mol. phylog. Macrobia (Webb & Berth.) G. Kunkel (1977).

Annual to triennial monocarpic herbs (sect. Aichryson) or small perennial shrublets (sect. Macrobia); stems densely hairy or glabrous, branches occasionally slightly woody; leaves alternate, often ± rosulate near branch tips, sessile or petiolate, entire or crenulate, glabrous or (glandular) hairy to viscid; inﬂorescences few- to many-branched, lax thyrsoids; ﬂowers 6–12-merous; sepals glabrous

or hairy; petals pale or deep yellow; nectary scales 2–5-ﬁd; carpels glabrous or glandular-hairy; fruits erect follicles; seeds costate-papillate to costate. n = 15, 17, 30. Fourteen species, from Macaronesia (Canary Islands, Madeira, Azores [Santa Maria]), naturalised in Portugal. Divided into sect. Aichryson and sect. Macrobia (2 spp.). 14. Monanthes Haw. Monanthes Haw., Saxifrag. Enum., 2:68 (1821); Nyffeler, Bradleya 10:49–82 (1992), rev.; Nyffeler in ’t Hart & Eggli, Evol. Syst. Crassulaceae: 76–88 (1995); Mes et al., J. Evol. Biol. 10:193–216 (1997), mol. phylog.; Cartwright et al., IOS Bull. 12:23–24 (2004), mol. phylog. (abstract). Petrophyes Webb & Berth. (1841).

Herbs or shrublets, perennial, M. icterica annual; leaves alternate, rarely decussate, usually in rosettes or scattered along stems, glabrous or glandular-hairy, covered with bladder-cell idioblasts; inﬂorescences terminal from rosette or at branch tips, or lateral shoots, reduced thyrsoids of 1–3(–5) cymes with (1–)3–8 ﬂowers; ﬂowers (5)6–8(9)-merous; petals insigniﬁcant in colour and size, pale yellow, variously striped with red; nectary scales larger than petals, bilobed or ﬂabellate, pale yellow to dark red; carpels often with glandular hairs; fruits follicles, rarely breaking off transversally; seeds costate-papillate to costate or almost smooth. n = 18, 36, 54; 10 in M. icterica. Nine species, from Macaronesia (Canary and Selvagens islands). Divided into four sections (Nyffeler in Eggli 2003). The position of M. icterica (Webb ex Bolle) Christ (sect. Annuae) is equivocal, according to molecular data: sister to Aichryson (Mes et al. 1997; Mort et al. 2001; weak to moderate support), between Aichryson and Monanthes (Mort et al. 2002; strong support), or sister to the rest of Monanthes (Cartwright et al. l.c.; weak support). Monanthes is sister to Aeonium, according to molecular data; the two genera share a chromosome base number of x = 18. 15. Aeonium Webb & Berth.

Fig. 29

Aeonium Webb & Berth., Phytogr. Canar. 1:184 (1840); Liu, Syst. Aeonium, Natl Mus. Nat. Sci. (Taiwan) Spec. Publ. 3 (1989), rev.; Mes & ’t Hart, Mol. Ecol. 5:351–363 (1996), mol. phylog. Greenovia Webb & Berth. (1840). Megalonium (A. Berger) G. Kunkel (1980).

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Fig. 29. Crassulaceae. A–E Aeonium tabulaeforme. A Rosette. B Leaf from rosette. C Flowering plant. D Flower. E Carpels with hypogynous scales. F–H Sedum sedoides.

F Flowering plant. G Flower. H Carpel with detached scale. (Berger 1930)

Perennial, rarely biennial, sometimes monocarpic subshrubs or single or caespitose subshrubby rosette plants; stems glabrous, puberulent, or with reticulate pattern, leaf scars often distinct; leaves glabrous, glabrate, pubescent, or viscid, margins often ciliate; inﬂorescences terminal (axillary in A. simsii (Sweet) Stearn), often large thyrsoids or pleiochasia (esp. sect. Greenovia), scape distinct; ﬂowers (6)7–12(–16) or 18–32-merous; sepals connate at base, glabrous or pubescent; petals free, spreading or slightly recurved, usually yellow(ish) or whitish; nectary scales rarely absent; carpels sometimes distinctly immersed in the receptacle, often with glandular hairs; fruits kyphocarpic; seeds costate-papillate or most often costate. n = 18, 27, 36. About 36 species, Macaronesia (Canary Islands, Cape Verde Islands, Madeira), south-western Morocco, Northeast and East Africa and Yemen. According to molecular data (Mes 1995; Mes et al. 1996; Mort et al. 2002), paraphyletic with respect to Greenovia; the latter is recognised as one of ﬁve sections within Aeonium (Nyffeler in Eggli 2003). Aeonium is a classic example of adaptive radiation leading to a broad array of growth forms, which has been studied with regard to phylogenetics (Mes 1995; Mes et al. 1997; Mort et al. 2002), adaptive radiation (Jorgensen and Olesen 2001), growth forms (Mes and ’t Hart 1996; Mes et al. 1996; Jorgensen and Olesen 2000) and ecophysiology (Lösch 1990). A. nobile (Praeger) Praeger may exhibit the largest rosettes in the family, with up to 80 cm Ø.

I.5. Tribe Sedeae Fr. (1835). No tribal characters. Genera 16–28. This tribe includes the Leucosedum and Acre clades which both are well supported with molecular cpDNA restriction-site data (van Ham and ’t Hart 1998). With a broader sampling of matK sequence data (Mort et al. 2001), both clades are weakly supported only and together sister to Sedum magellense Tenore (cf. Fig. 27); this pattern may become even more evident with an exhaustive study. Thus, both clades for the time being are not recognised as distinct taxa but are subsumed as two informal clades within tribe Sedeae. I.5. a. Leucosedum clade Plants usually glandular-hairy (not in American taxa). Genera 16–21. Mainly in winter-rainfall regions. This clade also includes the major part of Sedum subg. Gormania, which is broadly paraphyletic according to molecular data (van Ham 1994; van Ham and ’t Hart 1998; ’t Hart et al. 1999; Mort et al. 2001). Genera 16–19 Petals connate. Genera 17 + 18 with rosettes. These taxa are independently derived from within European-Mediterranean Sedum subg. Gormania, according to molecular data (van Ham and ’t Hart 1998; ’t Hart et al. 1999; Mort et al. 2001).

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16. Pistorinia DC. Pistorinia DC., Prodr. Syst. Regni Veg. 3:399 (1828).

Small annual herbs; leaves (semi-)terete, often tinged red; inﬂorescences many-ﬂowered cymes; corolla 5.5–22(–30) mm; petals connate at base for ≥ 1|2 to distinct corolla tube, lobes spreading, yellow, pink or purple, often ﬁnely spotted; ﬁlaments inserted below oriﬁce, short; nectary scales long, 1–2 mm; stylodia slender, recurved, 2.5–5 mm; fruits slender follicles, erect. n = 7. Three species, from the Iberian Peninsula and North Africa. According to molecular data (van Ham 1994; ’t Hart 1997b), closest to Sedum ser. Monregalensia. 17. Rosularia (DC.) Stapf Rosularia (DC.) Stapf, Curtis’s Bot. Mag. 149: t. 8985, in adnot. (1923); Eggli, Bradleya suppl. 6:1–119 (1988), rev.

Dwarf perennial rosulate herbs, glabrous or glandular-hairy; caudex usually wanting (sect. Rosularia) or well developed (sect. Ornithogalopsis), often with thickened taproot; rosettes ± stem-less, solitary or with offsets; leaves oblong to broadly spathulate, glandular-hairy, setate or denticulate, partly dimorphic (summer-winter) and forming ‘resting rosettes’ (frequent in sect. Rosularia); inﬂorescences lateral or terminal, glabrous or glandular-hairy, slender spicate thyrsoids (sect. Rosularia) to corymbiform-paniculate thyrsoids (sect. Ornithogalopsis), partial inﬂorescences cincinnoid; ﬂowers 5–9-merous; corolla urceolate, tubular to funnel-shaped, campanulate or stellate; petals connate at base for 1/10 to 3/4, white, pale yellow, pink, pinkish-purple or pinkish-brown, dorsally glabrous or glandular-hairy; carpels erect, slender or massive-voluminous, normally glandular-hairy along upper ventral part, completely free or ± connate at base and sunken into the receptacle; fruits erect follicles. n = 9, 18. Seventeen species, eastern Mediterranean, Near East, Inner Asia, Karakorum-Himalaya, Altai. According to molecular data, Rosularia sensu Eggli (1988) is polyphyletic (’t Hart et al. 1999; see also under Prometheum and Sedum). The genus is divided into sect. Rosularia (ﬂowers 5-merous; Mediterranean to Near East) and sect. Ornithogalopsis (ﬂowers 5–9-merous; 5 spp.; petals whitish; Inner Asia) which is probably misplaced here. 18. Prometheum (A. Berger) H. Ohba Prometheum (A. Berger) H. Ohba, J. Fac. Sci. Univ. Tokyo III, Bot. 12:168 (1978); Eggli, Bradleya suppl. 6:1–119 (1988), sub Rosularia.

Pseudorosularia Gurgenidze (1978). Rosularia sect. Chrysanthae Eggli (1988).

Perennial or annual to biennial and monocarpic herbs with a narrow taproot and without caudex, usually densely glandular-pubescent; leaves in dense rosettes, ﬂat to semi-terete, usually with subsessile offsets; inﬂorescences usually terminal or lateral, corymbose thyrsoids or cymose, with two to many cincinni, ± glandular-hairy; ﬂowers shortly pedicellate; petals connate at base for ≤ 1|2, outside glandular, lobes spreading or suberect, yellow, cream, white, pink or red; carpels usually slender; fruits stellately patent follicles with distinct lips along suture, or erect or spreading follicles with indistinct lips; seeds with thin, distinct costae. n = 6, 7, 13, 14, 28, 35, 42, 52. Eight species, from usually high altitudes in northern Greece, Turkey, Armenia, Caucasus, northern Iran. Based on different molecular taxon samplings, Prometheum appears closest to Sedum inconspicuum Hand.-Mazz. (van Ham 1994), or S. ser. Alsinefolium and Glauco-Rubens (’t Hart et al. 1999), or S. ince ’t Hart & Alpinar of S. ser. Elegans (’t Hart and Alpinar 1999). Some species were formerly included in Rosularia by Eggli (1988). 19. Afrovivella A. Berger Afrovivella A. Berger in Engler & Prantl, Nat. Pﬂanzenfam., ed. 2, 18a:466–467 (1930); Eggli, Bradleya suppl. 6:1–119 (1988), sub Rosularia.

Perennial herbs with a narrow taproot and without caudex; rosettes sessile, ± ﬂat, offsetting; leaves spathulate, with short or long mucro, glabrous or shortly glandular-hairy, margins setate; inﬂorescences lateral, reduced, 1–5-ﬂowered thyrsoids, brownish glandular-hairy; ﬂowers 5–7-merous; corolla campanulate; petals connate at base for 1/3, outside glandular, tips mucronate, white, outside tinged reddish; nectary scales oblong-acicular; carpels slender; seeds within thin, distinct costae. Only 1 species, A. semiensis (J. Gay ex A. Rich.) A. Berger, from shaded rocks in Ethiopian highlands. Of uncertain status and thus kept separate. Classiﬁed as Rosularia by Eggli (1988). The thin, distinct costae of the seeds match those of Prometheum (Eggli 1988). Genera 20 + 21 Plants glabrous. According to molecular data (Mort et al. 2001), the two genera form a distinct clade in western North America.

Crassulaceae

Most probably, the c. 30 American species of Sedum subg. Gormania, i.e. the American Sedum with costate seeds, also belong to this clade (= sections Gormania, Lanceolata, Ternata and Tetrorum (incl. Diamorpha); cf. Knapp 1994, 1997). Molecular data are yet sparse (’t Hart 1995). 20. Sedella Britton & Rose Sedella Britton & Rose, Bull. New York Bot. Gard. 3:45 (1903); Clausen, Sedum N. Am. (1975), sub Sedum; Moran, Haseltonia 5:53–60 (1998, ‘1997’), rev. Parvisedum Clausen (1946), nom. illegit. (Art. 53.1).

Small annuals < 10 cm; stems usually branching, often red(dish); leaves decussate near base, alternate above, usually caducous before anthesis; inﬂorescences cymose with several cincinni; sepals erect, almost free; petals imbricate in bud, erect to spreading, connate at very base, bright to pale or greenish-yellow, much longer than sepals; stamens 5 or rarely 10; carpels erect, clavate, with a single basal erect ovule; fruits ﬂimsy, clavate, nutlet-like and indehiscent, each with one erect seed. n = 9. Three species, as ephemeral vernal herbs often in rock pools; USA (northern and central California, southern Oregon?).

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Divided into subg. Dudleya (leaves usually broad; petals upright), subg. Stylophyllum (leaves usually narrow; petals spreading from middle) and subg. Hasseanthus (stems tuberous; leaves vernal; petals broadly spreading). None of these is monophyletic, according to a molecular study (D. Burton, San Diego State University, USA; in litt. 2002). Dudleya is not related to Echeveria, with which it was united in subfamily Echeverioideae by Berger (1930). Possibly closest to Sedum subg. Gormania sect. Gormania with which it shares the rosulate habit. The systematics and biology are reviewed by Thiede (2004). I.5. b. Acre clade Plants glabrous or with non-glandular trichomes; seeds reticulate-papillate∗ or reticulate (except for Sedum litoreum Guss.); tannins largely absent∗ and often replaced by alkaloids. Genera 22–28.

21. Dudleya Britton & Rose Dudleya Britton & Rose, Bull. New York Bot. Gard. 3:12–13 (1903); Moran, Revision Dudleya (1951), unpubl. rev.; Bartel in Hickman, Jepson Manual 525–530 (1993), synopsis N. Amer. spp. Hasseanthus Rose (1903). Stylophyllum Britton & Rose (1903).

Stems unbranched or branched, usually dichotomously, stems usually short and erect, covered by dry leaf remains at base; leaves in rosettes, united with stem axis with broad or narrow base (subg. Hasseanthus), often densely farinose; inﬂorescences axillary, cymose, usually with 1–3(–10) cincinnoid partial inﬂorescences; sepals connate at base; petals forming ± tubular corolla or spreading, usually convolute in bud; carpels ± erect at anthesis, basally at base; stylodia slender; fruits slightly divaricate to widely spreading follicles. n = 17, also 34, 51, 68, 85, ±119, 136. About 47 species, western USA (south-western Oregon, southern Nevada, central and western Arizona, California incl. Paciﬁc Islands), Mexico (Sonora, Baja California incl. islands), predominantly coastal, rocky places to 2,200(–3,025) m.

Fig. 30. Crassulaceae. Sedum acre. A Flowering plant. B Flower seen from above. C Flower, side view. D Petal with two stamens, the antepetalous stamen epipetalous. E Carpels with hypogynous bracts. (Clausen 1975)

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This clade most probably includes all of Sedum subg. Sedum, i.e. Sedum with reticulate-papillate or reticulate seeds. Molecular data are from van Ham and ’t Hart (1998) and Mort et al. (2001). 22. Sedum L.

Figs. 29, 30

Sedum L., Sp. Pl.: 5 (1753); Fröderström, Acta Horti Gothob. suppl. 5–7 (1930–1932) & 10 (1935); Clausen, Sedum Trans-Mexican Volcanic Belt (1959); Clausen, Sedum N. Am. (1975); ’t Hart, Fl. Medit. 1:31–61 (1991). Diamorpha Nuttall (1818). Altamiranoa Rose (1903). Cremnophila Rose (1905). Sempervivella Stapf (1923). Mucizonia (DC.) A. Berger (1930). Rosularia sect. Sempervivella (Stapf) Jansson in Jansson & Rechinger (1970). Amerosedum, Breitungia, Clausenellia, Etiosedum & Hjaltalinia A.D. Löve & D. Löve (1984). Oreosedum Grulich (1984). Ohbaea Byalt & I.V. Sokolova (1999).

Glabrous or pubescent, perennial or annual herbs to subshrubs with usually much branched non-ﬂowering shoots, rarely rosulate; roots usually ﬁbrous or tuberous or taproots; stems usually without secondary thickening, sometimes (slightly) woody or with subterranean rootstock; leaves usually alternate, rarely decussate or in whorls of 3 or 4, sessile or rarely (semi-)petiolate, usually (semi-)terete, rarely ﬂat, with entire margins; inﬂorescences terminal or rarely axillary, many-ﬂowered pleiochasia with single or double cincinni, or corymboid or compound thyrsoids with many cincinni, rarely few-ﬂowered cymes with one or two cincinni; bracts usually present, often leaf-like; ﬂowers (3–)5(–12)-merous, rarely haplostemonous, sessile to pedicellate; sepals broadly sessile or free and spurred, equal or strongly unequal, usually smaller than petals; petals usually free, or connate at base for 1/3 to 2/3, usually spreading, or erect, often with distinct, frequently reddish keel and dorsal subapical appendage, yellow, white, pink, purple or reddish; ﬁlaments usually free, antepetalous stamens connate at base with petals or rarely higher up; nectary scales variable, usually whitish, or yellow or red; carpels usually sessile with broad base and slightly connate at base, or completely free, rarely stipitate; stylodia usually slender and recurved during anthesis, or short and stigma ± sessile; fruits (sub)erect or stellate-patent follicles, without lips along ventral suture, or

stellate-patent follicles with distinct lips, rarely nutlike (e.g. S. caeruleum L.); seeds ovoid to ellipsoid, costate-bipapillate (subg. Gormania) or reticulate-papillate to reticulate (subg. Sedum). n = 4–20 and many higher polyploids. About 420 species, mainly temperate and subtropical regions of North America, Europe, North Africa, Near East and Asia, a few species in South America and Central to East Africa. Tremendously variable in its morphology, with numerous exceptions from the generalised description given above which are usually conﬁned to small species groups and have often prompted generic separation. A highly paraphyletic genus, with many segregates phylogenetically basal within Semperviveae, Aeonieae and Sedeae, but formally preferably to be treated under Sedum. See also discussion under Subdivision and Relationships. Sedum as deﬁned here is divided into subg. Gormania which includes the species from the Sempervivum, Aeonium and Leucosedum clades (often glandular-pubescent; sepals broadly sessile and usually of equal length; seeds costate; c. 110 spp., 60 in Europe/Mediterranean (anthers in these usually red), 10 in Asia, 10 in East Africa and 30 in North America), and subg. Sedum which includes the species from the Acre clade (usually glabrous or rarely with non-glandular hairs; sepals free at base and spurred, or broadly sessile and often distinctly unequal in size; seeds with reticulate-papillate or reticulate testa; c. 320 spp., 30 in Europe/Mediterranean/Near East, 120 in Asia and 170 in the Americas). Genera 23–28 Genera 23–28 form a distinct American clade, together with the American species of Sedum subg. Sedum (according to molecular data of Mort et al. 2001). 23. Villadia Rose Villadia Rose, Bull. New York Bot. Gard. 3:3 (1903); Uhl & Moran, Amer. J. Bot. 86:387–397 (1999); Palmer et al., http://www.botany2002.org/section12/abstracts/189.shtml (2002), mol. phylog. (abstract).

Herbs or small shrubs; roots ﬁbrous or thickened and fusiform; stems either woody-persistent and ± erect (then, small shrubs), or herbaceous and decumbent-ascending (then, mat-forming herbs), or herbaceous and ± annual (then, geoor hemicryptophytes with thickened, persistent

Crassulaceae

roots); leaves usually terete-subulate, ± conspicuously spurred at base; inﬂorescences ± elongate thyrsoids, often spike- or raceme-like, with 6–70(–150) cincinnoid partial inﬂorescences with 1–5(–8) ﬂowers; sepals (almost) free, (always?) spurred at base; petals connate at base, lobes spreading to reﬂexed or erect, whitish to pink or reddish; stylodia ± recurved; fruits erect. n = 9–17, 20–22, 33 and higher. About 21 species in southern USA (south-western Texas), Mexico, Guatemala (Baja Verapaz), Peru, at (600–)1,500–4,000 m. Divided into seven informal species groups (Thiede in Eggli 2003). Appears to be closest to Sedum sect. Fruticisedum (Uhl and Moran, l.c.). Taxa formerly classiﬁed in sect. Altamiranoa are now placed in Sedum (Moran 1996; Thiede and ’t Hart 1999). 24. Lenophyllum Rose Lenophyllum Rose, Smithsonian Misc. Collect. 47:159 (1904); Moran, Haseltonia 2:1–19 (1994), rev.

Herbs, roots ﬁbrous or thickened; leaves decussate in few basal pairs, elliptic, roundish or rhombic; inﬂorescences thyrsoids with several cincinni, narrow thyrsoids of compact cincinni or reduced to racemes or spikes above or throughout; sepals erect or ascending, nearly equal, ± as long as open corolla; petals in upper half spreading to recurved, (ob)lanceolate, yellow(ish); stamens slightly exserted; nectary scales subquadrate; carpels erect, narrow, tapering into slender stylodia; fruits erect. n = 22, 32, 33, 44. Seven species, from USA (southern Texas) and north-eastern Mexico.

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Byrnesia Rose (1922). Tacitus Moran (1974).

Herbs (sect. Graptopetalum) to subshrubs (sect. Byrnesia); leaves obovate to (broadly) spathulate, usually mucronate in sect. Graptopetalum; usually ± glaucous-pruinose; inﬂorescences thyrsoids with few to many cincinnoid partial inﬂorescences, or pleiochasia with few cincinnoid partial inﬂorescences; ﬂowers (4)5(–10)-merous, stamens diplostemonous, rarely haplostemonous; sepals appressed, free to base and ± equal in size; petals slightly connate at base, spreading stellately, basically whitish or yellowish (to greenish), usually with reddish to brown cross-band markings or blotches becoming denser towards tips, rarely uniformly coloured; stamens ﬁrst erect, after anther dehiscence spreading and the antesepalous stamens recurved between the petals, after anthesis becoming erect again; carpels shortly connate at base; stylodia normally abruptly offset; fruits ascending to erect; seeds usually reticulate. n = 30–32, 34, 35, 62, 64, 66, 68, ±93, ±170, ±175, 192, ±204, ±208, ±244, ±270. Eighteen species, USA (central and southern Arizona), Mexico (widespread from Sonora and Chihuahua to Oaxaca); rocky places, to 2,400 m. Divided into sect. Byrnesia and sect. Graptopetalum (incl. Tacitus). According to molecular data, Graptopetalum and its sections are not monophyletic, and Tacitus, Cremnophila (= Sedum) and selected species of Sedum and Echeveria are interspersed among its species (Acevedo et al. l.c.). 26. Thompsonella Britton & Rose

Genera 25–28 Stems at least basally woody, but many taxa with sessile rosettes; leaves usually thick and strongly succulent, in ± distinct rosettes; inﬂorescences lateral; petals at least basally connate. x = 30–34 with secondary reductions. Centred in Mexico. According to molecular data (Mort et al. 2001), these genera form a distinct American clade (= ‘Echeveria group’), together with Sedum sect. Pachysedum. The latter shares the above characters, except for its choripetalous ﬂowers. 25. Graptopetalum Rose Graptopetalum Rose, Contr. U.S. Natl Herb. 13:296 (1911); Acevedo et al., Brittonia 56:185–194 (2004), morph. phylog.; Acevedo et al., Amer. J. Bot. 91:1099–1104 (2004), mol. phylog.

Thompsonella Britton & Rose, Contr. U.S. Natl Herb. 12:391 (1909); Moran, Cact. Succ. J. (U.S.) 64:37–44 (1992), synopsis.

Glabrous herbs or subshrubs; leaves in rosettes, ﬂattish, semi-amplexicaul, often glaucous, margins straight or undulate; inﬂorescences erect narrow thyrsoids or spicate above or as a whole, with 10–70, 1–12-ﬂowered cincinni; ﬂowers (almost) sessile; sepals free, (sub)equal, clavate; petals shortly connate at base, imbricate in bud, spreading from middle, outer face pale, inner face ± dark purplish-red; nectary scales minute; carpels shortly stipitate, shortly connate at base; stylodia slender; fruits erect; seeds reticulate with irregular longitudinal rows. n = 26, 52. Six species, central and southern Mexico; usually on limestone.

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Genera 27 + 28 Petals upright and connate for most of their length; sepals often strongly unequal in size; petals thickﬂeshy; anthers (light) yellow; fruits divergent. 27. Echeveria DC. Echeveria DC., Prodr. Syst. Regni Veg. 3:401 (1828); Walther, Echeveria (1972), rev. Oliverella Rose (1903). Urbinia Britton & Rose (1903). Oliveranthus Rose (1905).

Glabrous to hirsute herbs to subshrubs; stem none or tall, branching or not; leaves rarely scattered along the stems, usually (ob)lanceolate and mucronate, often glaucous or highly coloured; inﬂorescences, racemose, paniculate, or rarely spicate thyrsoids, or cymose with one to several cincinni; pedicels usually with one to several minute bracteoles; sepals reﬂexed to appressed but usually somewhat expanding, almost completely free, equal to strongly unequal; corolla cylindrical to pentagonal to urceolate; petals imbricate (valvate in Ser. Valvatae), white through yellow and orange to red, rarely green(ish), inner surface usually with nectar-cavity at base; stamens 10, 5 attached at top of nectar-cavities, 5 at top of corolla tube between petals; carpels connate at base, erect at anthesis; stylodia slender; fruits widely divergent follicles; seeds reticulate or smooth. n = 12–34, polyploid from 28–250. About 139 species, centred in (southern) Mexico, also southern USA (Texas) and Central and South America (Venezuela, Colombia, Ecuador, Peru, Bolivia, northern Argentina). Divided into 17 series (Kimnach in Eggli 2003). 28. Pachyphytum Link, Klotzsch & Otto Pachyphytum Link, Klotzsch & Otto, Allg. Gartenzeitung 9:9–10 (1841).

Subshrubs; stems ﬁrst erect, with age usually decumbent to pendent, not or few-branched; leaves obovate, spathulate, elliptic-oblong or lanceolate, usually very thick, usually conspicuously glaucous-farinose; inﬂorescences almost always simple cincinni, ﬁrst drooping, later ± erect; ﬂoral bracts 5–9 mm in sect. Diotostemon or usually 13–30 mm in sect. Pachyphytum; sepals erect, appressed, almost equal (sect. Diotostemon) or (often strongly) unequal (sect. Pachyphytum); petals erect (sect. Diotostemon) or spreading to divaricate

(sect. Pachyphytum), ± oblong to oblanceolate, white to pink, rarely orange to red(dish), inner face in upper part often with red blotch in sect. Pachyphytum, laterally near base with appendages which form two free, 1–2 mm large scales beneath ﬁlaments; antetepalous ﬁlaments connate with corolla, antesepalous ones (almost) free; nectary scales oblong, ± yellowish(-white); carpels erect at anthesis, ± free; stylodia inconspicuously offset to abruptly narrowing; fruits usually divergent follicles; seeds fairly smooth. n = 31–33, 62, 64, 66, 96, 99, ±124, ±128, ±160, ±186. Fifteen species, in eastern central Mexico, (600–)1,200–2,500 m. Divided into sections Diotostemon and Pachyphytum (Thiede in Eggli 2003). The morphology of the petal scales was studied by Leinfellner (1954); similar scales also occur in some Echeveria species. Pachyphytum may be nested within Echeveria and closest to its sect. Urceolatae (Thiede in Eggli 2003).

II. Subfam. Kalanchoideae A. Berger (1930). Shoots ± woody∗ ; tissues (always?) with crystal sand∗ ; petals connate to strongly developed corolla tube∗ ; anthers with terminal, ± spherical connective appendage∗ ; seeds with few (4–6) costae∗ in side view, coronate∗ . x = 9∗ . Genera 29–32. Note that Kalanchoideae are morphologically highly derived, although cladistically they are the second clade branching off from the remainder of the family. 29. Adromischus Lem. Adromischus Lem., Jard. Fleur. misc. 2:58–59 (1852); Pilbeam et al., Adromischus (1998), synopsis.

Shrublets to ± 20 cm; stems ﬂeshy-woody; leaves ﬂat to almost terete, glabrous or glandular-hairy, often with thick wax bloom; inﬂorescences erect spike-like thyrsoids or spikes without terminal ﬂower, to 55 cm, with few to numerous, 1–5ﬂowered dichasia; ﬂowers usually erect, rarely pendulous (A. phillippsiae (Marloth) Poelln.); corolla usually long and narrow; petals white to pink to red, rarely bright orange, lobes at sinuses joined by thin membrane; ﬁlaments slightly exserted or included, papillate where connate with corolla tube; carpels elongate; fruits follicles, (always?) dehiscing completely along ventral

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suture. n = 9. About 28 species, Namibia, South Africa (especially Succulent and Little Karoo). 30. Kalanchoe Adans.

Fig. 28

Kalanchoe Adans., Fam. Pl. 2:248 (1763); Hamet, Bull. Herb. Boiss. II, 7:870–900 (1907) & 8:17–48 (1908); Hamet & Lapostolle, Genre Kalanchoe au Jardin Botanique “Les Cèdres” (1964); Raadts, Willdenowia 8:101–157 (1977), rev. E. Afr.; Fernandes, Bol. Soc. Brot. II, 53:325–442 (1980), African taxa; Boiteau & Allorge-Boiteau, Kalanchoe de Madagascar (1995); Gehrig et al., Pl. Sci. 160:827–835 (2001), mol. phylog. Bryophyllum Salisbury (1805). Kitchingia Baker (1881).

Shrublets to shrubs, rarely rosulate or small trees, or biennial to annual; leaves usually decussate, rarely alternate, verticillate or subrosulate, ± ﬂat, rarely terete, sometimes ± incised or 3- to 5-foliate, margins usually crenate, serrate or dentate, partly with bulbils (usually in sect. Bryophyllum), rarely entire; inﬂorescences rarely axillary, corymbose or paniculate thyrsoids, partial inﬂorescences dichasial, rarely inﬂorescences few- to 1-ﬂowered; ﬂowers 4-merous, ± erect (usually in sect. Kalanchoe) or pendent (usually in sects. Kitchingia and Bryophyllum); sepals free, connate or forming long, sometimes ± inﬂated tube (usually in sect. Bryophyllum); petals usually brightly coloured, lobes shorter than corolla tube, erect, spreading or reﬂexed; ﬁlaments exserted or included, connate to corolla tube at base (sect. Bryophyllum) or at or above middle (sects. Kalanchoe and Kitchingia); carpels free to somewhat connate at base, erect or somewhat spreading (sect. Kitchingia); fruits erect follicles. n = usually 17, also 18, 20, 34, 35, 36, 51, 85. About 144 species, mainly Madagascar, eastern and southern Africa, to tropical Africa, Arabia and tropical and Southeast Asia; some taxa (especially K. pinnata (Lam.) Pers.) are neophytic invaders throughout the tropics. Divided into three sections: the widespread sect. Kalanchoe, and the Malagasy sects. Kitchingia and Bryophyllum. 31. Tylecodon Toelken Tylecodon Toelken, Bothalia 12:378 (1978); van Jaarsveld & Koutnik, Tylecodon & Cotyledon (2004), rev.

Shrublets or dwarf geophytes to pachycaul dwarf trees to 2.5 m; stems succulent, rarely woody, usually with ﬂaking bark; leaves usually crowded at stem tips, soft-herbaceous, with elongate

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epidermal cells with sinuate anticlinal walls, often (always?) with bladder-cells idioblasts, usually completely drought-deciduous; inﬂorescences thyrsoids with one to several dichasia; petals white, greenish, yellowish or mauve, rarely reddish; ﬁlaments usually exserted, hairy where connate with corolla tube; fruits follicles, dehiscing apically only; seeds with irregular costae. Forty-six species, winter-rainfall regions of Namibia and South Africa, mainly Succulent Karoo. Growing season autumn to early summer; ﬂowering ± in summer. Sister to Cotyledon, according to molecular data (Mort et al. 2001). The two genera have in common basally hairy ﬁlaments. 32. Cotyledon L. Cotyledon L., Sp. Pl.: 429 (1753); van Jaarsveld & Koutnik, Tylecodon & Cotyledon (2004), rev.; Mort et al., Amer. J. Bot. 92:1170–1176 (2005), mol. phylog.

Procumbent to erect shrublets to shrubs, rarely climbers; stems usually becoming woody; leaves decussate, ﬂat or terete, rarely lobed or orbicular, glabrous or (glandular) hairy; inﬂorescences thyrsoids with several dichasia, ending in monochasia with one to many pendent ﬂowers; corolla tube hairy or glabrous; dried calyx/corolla complex circumscissile along basal groove; ﬁlaments exserted, hairy where connate with corolla tube; carpels tapering into erect stylodia; nectary scales ± cuplike. n = 9. Eleven species, southern and eastern tropical Africa, south-western Arabian Peninsula. According to molecular data (Levsen et al., l.c.), the variable Cotyledon orbiculata L. is polyphyletic. The circumscissile calyx/corolla complex present in all Cotyledon is found also in at least some Tylecodon and Kalanchoe spp. (Moran 2000), and may represent a synapomorphy for these three genera.

III. Subfam. Crassuloideae Burnett (1835). Leaves decussate∗ , rarely ternate or whorled; ﬂowers haplostemonous∗ ; anthers slightly introrse∗ , nucellus tenuinucellate∗ ; fruits opening ± completely along whole suture, but releasing seeds through apical pore∗ ; seeds sinuate-unipapillate∗ . Genera 33 + 34. Note that Crassuloideae are morphologically highly derived, although cladistically they are the ﬁrst clade branching off from the remainder of the family.

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at base, partly with apex papillate on outer face and with distinct appendage (usually in subg. Crassula) often ± whitish; ﬁlaments shortly adnate to petals at base and alternate with these; carpels usually free; fruits rarely nutlike and indehiscent. n = 8, 7 and polyploids. About 195 species; mainly southern Africa, a few species in sub-Saharan Africa and south-western Arabia, some ephemeral herbs (‘Tillaea’) distributed worldwide, and the only genus of the family in Australia. Divided into the paraphyletic subg. Disporocarpa with nine sections (hydathodes of type I, rarely type II; n = 8, rarely 7) and subg. Crassula with eleven sections (hydathodes of type II; n = 7 with two satellites; Friedrich 1973; Toelken 1977 l.c.; Martin and von Willert 2000). The ephemeral herbs of sects. Helophytum and Glomeratae, often segregated as genus Tillaea, are nested within Crassula, according to molecular data (’t Hart unpubl. data). 34. Hypagophytum A. Berger Hypagophytum A. Berger in Engler & Prantl, Nat. Pﬂanzenfam., ed. 2, 18a:467–468 (1930); Gilbert, Opera Bot. 121:47–50 (1993). Fig. 31. Crassulaceae. Crassula columnaris. A Flowering plant. B Flower, opened out. C Young plant seen from above. (Berger 1930)

33. Crassula L.

Fig. 31

Crassula L., Sp. Pl.: 282 (1753); Toelken, Contr. Bolus Herb. 8 (1977), rev. southern African taxa; Tölken, J. Adelaide Bot. Gard. 3:57–90 (1981), rev. Austral. taxa; Bywater & Wickens, Kew Bull. 39:699–728 (1984), rev. New World taxa; Mort et. al., IOS Bull. 12:35–36 (2004), mol. phylog. (abstract). Tillaea L. (1753). Rochea DC. (1802).

Perennial or rarely annual herbs to (sub)shrubs, rarely tuberous geophytes; glabrous, papillate or hairy; leaves decussate or rarely in whorls of 4, partly with bladder-cell idioblasts and leaf bases connate within a pair (usually in subg. Crassula); inﬂorescences thyrsoids with 1 to many dichasia, sometimes partial inﬂorescences glomerate, monochasia or reduced to solitary ﬂowers; corolla urn-shaped to tubular or stellate; ﬂowers (2–)5(–12)-merous, usually small; sepals shortly connate at base; petals shortly connate

Tuberous geophytes; stems one to few, droughtdeciduous; leaves ternate, sessile or with petiolelike base, somewhat spurred at base, ﬂat; inﬂorescences usually with 3 monochasia below terminal ﬂower; ﬂowers 10–12-merous, stellate; sepals free; petals white or with faint pink tinge; carpels free, laterally compressed, constricted into two segments, upper part spiny-papillate, with long ﬁliform stylodia; fruits 2-seeded, breaking transversely at the constriction, upper seed dispersed within the upper part of the carpel, lower seed released separately. Only 1 species, H. abyssinicum (Hochst. ex A. Rich.) A. Berger in north-western Ethiopian highlands. Characterised by a unique combination of specialised features, which all occur in Crassula (tubers with annual shoots, whorled leaves, hydathodes along leaf margins, haplostemonous and polymerous ﬂowers, and the peculiar fruits). The seed surface structure was given as costate by Gilbert (1989 and l.c.) and Knapp (1994), which prompted ’t Hart (1995: 169) to place the genus in his ‘Sedoideae’. However, according to Knapp (1997), the seed surface structure in fact corresponds to the sinuate-papillate (Crassula-) type, clearly favouring the placement in Crassuloideae. Hypagophytum may be nested within Crassula and closest to

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its sect. Petrogeton, which shares the tuberous habit and exhibits in some species leaves with short petiole and in whorls of 4, monochasial inﬂorescences with stellate and polymerous ﬂowers, and long ﬁliform stylodia. The same peculiar fruit type is found in sect. Glomeratae p.p. (cf. Stopp 1957).

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Torrey, J., Gray, A. 1838. A ﬂora of North America, I. New York: Wiley & Putnan. Troll, W. 1964. Die Inﬂoreszenzen. Erster Band. Stuttgart: G. Fischer. Troll, W. 1969. Die Inﬂoreszenzen. Zweiter Band, 1. Teil. Stuttgart: G. Fischer. Troll, W., Weberling, F. 1989. Inﬂoreszenzuntersuchungen an monotelen Familien. Stuttgart: G. Fischer. Uhl, C.H. 1948. Cytotaxonomic studies in the subfamilies Crassuloideae, Kalanchoideae, and Cotyledonoideae of the Crassulaceae. Amer. J. Bot. 35:695–706. Uhl, C.H. 1961. The chromosomes of the Sempervivoideae (Crassulaceae). Amer. J. Bot. 48:114–123. Uhl, C.H. 1970. Chromosomes of Graptopetalum and Thompsonella (Crassulaceae). Amer. J. Bot. 57:1115– 1121. Uhl, C.H. 1976–1992. Chromosomes of Mexican Sedum. I–VI. Rhodora 79:629–640, 80:491–512, 82:377–402, 85:243–252, 87:381–423, 94:362–370. Uhl, C.H. 1992. Polyploidy, dysploidy, and chromosome pairing in Echeveria (Crassulaceae) and its hybrids. Amer. J. Bot. 79:556–566. Uhl, C.H. 1993–1995. Intergeneric hybrids in the Mexican Crassulaceae. I–V. Cact. Succ. J. (U.S.) 65:271–273, 66:74–80, 175–179, 214–217, 67:144–147. Uhl, C.H. 1994–2005. Chromosomes and hybrids of Echeveria (Crassulaceae). I–IX. Haseltonia 2:79–80, 3:25–33, 3:34–48, 4:66–88, 5:21–36, 6:63–90, 8:71–82, 9:121–145, 11:138–149. Uhl, C.H. 1996. Chromosomes and polyploidy in Lenophyllum (Crassulaceae). Amer. J. Bot. 83:216–220. Uhl, C.H., Moran, R. 1972. Chromosomes of Crassulaceae from Japan and South Korea. Cytologia 37:59–81. Uhl, C.H., Moran, R. 1973. The chromosomes of Pachyphytum (Crassulaceae). Amer. J. Bot. 60:648–656. Uhl, C.H., Moran, R. 1999. Chromosomes of Villadia and Altamiranoa (Crassulaceae). Amer. J. Bot. 86:387–397. U.S. Fish and Wildlife Service 2004. Threatened and Endangered Species System (TESS). http:/endangered.fws. gov/wildlife.html Visser, J. 1981. South African parasitic ﬂowering plants. Cape Town: Juta. Vogel, S. 1954. Blütenbiologische Studien als Elemente der Sippengliederung, dargestellt an der Flora Südafrikas. Bot. Stud. 1:1–338. Wakabayashi, M., Ohba, H. 1999. Chromosome numbers of seven species of Sedum and Sinucrassula indica (Crassulaceae) in East Himalaya. J. Jap. Bot 74:228–235. Wassmer, A. 1955. Vergleichend-morphologische Untersuchungen an den Blüten der Crassulaceen. Winterthur: P.G. Keller. Wickens, G.E., Bywater, M. 1980. Seed studies in Crassula subgen. Disporocarpa. Kew Bull. 34:629–637. Wikström, N., Savolainen, V., Chase, M.W. 2001. Evolution of the angiosperms: calibrating the family tree. Proc. Roy. Soc. London, ser. B 268:2211–2219. Wyatt, R., Stoneburger, A. 1981. Patterns of ant-mediated pollen dispersal in Diamorpha smallii (Crassulaceae). Syst. Bot. 6:1–7. Xu, J.F., Liu, C.B., Han, A.M., Feng, P.S., Su, Z.G. 1998. Strategies for the improvement of salidroside production in cell suspension cultures of Rhodiola sachalinensis. Pl. Cell Rep. 17:288–293.

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Yamagishi, T., Haruna, M., Yan, X.-Z., Chang, J.-J., Lee, K.-H. 1989. Antitumor agents, 110. 1,2 bryophyllin B, a novel potent cytotoxic bufadienolide from Bryophyllum pinnatum. J. Nat. Prod. 52:1071–1079. Yoshikawa, M., Shimada, H., Shimoda, H., Murakami, N., Yamahara, J., Matsuda, H. 1996. Bioactive constituents

of Chinese natural medicines. II. Rhodiolae Radix (1): chemical structures and antiallergic activity of rhodiocyanosides A and B from the underground part of Rhodiola sachalinensis (Pall.) Fisch. et Mey. (Crassulaceae). Chem. Pharmaceut. Bull. (Tokyo) 44:2086– 2091.

Crossosomataceae Crossosomataceae Engl. in Engler & Prantl, Nat. Pﬂanzenfam., Nachtr. 1:185 (1897), nom. cons.

V. Sosa

Small to large microphyllous shrubs, rarely arborescent, intricately branched; stems smooth, spinescent, or with hyaline to black trichomes. Leaves alternate or opposite, scattered or fascicled; stipules minute or 0. Flowers solitary, axillary or terminal on short shoots, bisexual or rarely unisexual, actinomorphic, perigynous, with or without a ﬂeshy or thin, glandular, crenately lobed disk; hypanthium present, short and turbinate or enlarged and tubular; sepals (3)4–5(6), equal or unequal in form, ovate, oblong or triangular, persistent; petals (3)4–5(6), distinct, deciduous or persistent, equal or unequal in form, narrowly lanceolate to round ovate, usually longer than sepals, often short-clawed; stamens 4–50, diplostemonous, haplostemonous, or polystaminate, sometimes unequal in length, rarely almost sessile; anthers basiﬁxed; gynoecium apocarpous, 1–5(–9)-carpellate; pistils stipitate or sessile, 1-celled, with 1–2 to many ovules; stylodia short or 0; stigmas capitate. Fruits follicular, ventrally dehiscent, surface smooth or rugose. Seeds disk-shaped, black or brown, with a whitish or yellowish, irregular, ﬁmbriate or ﬁmbriolate aril, 1(2)–many. A small family of four genera and ca. 10 species, restricted to North America with Mexico. Most species are in xerophytic vegetation. Characters of Rare Occurrence. Young branches turning orange-brown in Glossopetalon or with small hyaline projections turning dark in Velascoa. Hypanthium enlarged and tubular in Velascoa. Vegetative Morphology. Crossosomataceae are small to large shrubs or rarely small trees, sometimes hanging from rocks. They are usually deciduous, intricately and highly branched, often spinescent, and have angled, grooved, or ribbed branches. The bark is yellowish and glossy. The leaves are small, alternate, scattered or crowded,

simple, entire, rarely tridentate, glaucous or pubescent or with small rounded glands on both surfaces, petiolate, subpetiolate or sessile. Some taxa have minute, subulate, linear stipules, which sometimes are connate with the base of the petiole. Vegetative Anatomy. The wood of Glossopetalon and Crossosoma has solitary vessels. The vessel elements are short to medium-length and have simple perforation plates and alternate lateral wall pitting. Tracheid imperforate elements are present; the parenchyma is primarily apotracheal and diffuse, and with multiseriate and uniseriate rays. The leaves of Glossopetalon and Crossosoma have anomocytic stomata on both sufaces of the leaves. The epidermis has thick outer cell walls; the veins are sheathed by large parenchyma cells, and phloem ﬁbers as well as masses of yellow acicular crystals are present. The mesophyll has an isolateral arrangement of palisade tissue. The water storing tissue consists of large cells extending laterally between veins in the center of the leaf. The nodes of Crossosoma are trilacunar with one or three traces. The leaves of Crossosoma show a number of xerophytic features that include isolateral leaves, reduced surface and thick blade, a strongly cutinized epidermis and ledges on the guard cells (Metcalfe and Chalk 1950; DeBuhr 1978). Flower. Flowers are always solitary and borne on the ends of short shoots and are subtended by narrowed bracts, the outer being small and the inner resembling small leaves. Most taxa have pentamerous ﬂowers with a hypanthium. Perianth parts and stamens arise from the rim of the hypanthium. In Glossopetalon, some species have only three petals and three sepals, whereas their number usually varies in the range 4–6. Apacheria has four sepals and petals. The hypanthium is variable in form, cup-shaped in Apacheria, well developed in Crossosoma, deep and enlarged in Velascoa; Glos-

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sopetalum has a ﬂeshy disk. The stamen number is variable, ranging from 6 to 50; in some taxa the stamens are arranged in one to several whorls. Carpels are free, 1–5(–9). A detailed study of the ﬂoral morphology and anatomy of Crossosoma bigelovii with a discussion of the relationships among the families of Crossosomatales was given by Matthews and Endress (2005). Embryology. In Crossosoma the ovules are campylotropous, bitegmic and crassinucellar. The development of the embryo sac is of the Polygonum type. Fertilization is porogamous and the endosperm is Nuclear. Centripetal wall formation sets in at the micropylar end at the globular stage of the proembryo, and the endosperm becomes completely cellular by the time the embryo is heart-shaped and contains fatty reserves (Kapil and Vani 1983). Pollen. Pollen in the family is tricolporate. In Apacheria pollen is subspheroidal or spheroidal, the exine is semi-tectate and per-reticulate, with a heterobrochate reticulum; the colpi are elongated and rounded at ends. The endoapertures are rounded, partially hidden beneath the exine at the equator. Pollen grains in Velascoa are the smallest among Crossosomataceae. In Crossosoma, grains and endoapertures are larger.

Fig. 32. Crossosomataceae. Crossosoma californica. A Flowering branch. B Flower. C Same, vertical section. D Dehiscing fruit. E Seed. (Takhtajan 1981)

Fruit and Seed. The fruits are coriaceous, asymmetric follicles. Their surface is often striate. They dehisce along the ventral suture, and release many to 2 or 1 seeds. These are globular-reniform or obovate, white or cream, shiny black or dark brown, smooth or minutely papillate-tessellate, and arillate. In the seed coat of Crossosoma, the testa has 4–5 highly sclerotic cell layers partly derived from the outer integument, whereas the tegmen is unspecialized except for the ﬁbrous inner epidermis. The embryo is slender, curved, ﬂeshy, and often embedded in abundant endosperm. The aril is ﬁmbriate and large, or entire and rather small, yellowish or whitish. Phytochemistry. Glossopetalon and Crossosoma contain gallic and ellagic acids and cyanidin-3-glucoside; proanthocyanins were not found. Glossopetalon leaves contain acacetin 7-Oglycoside, acacetin 7-O-diglycoside, and syringin (Tatsuno and Scogin 1978; Thorne and Scogin 1978). Relationships Within the Family. Molecular and morphological studies suggest that Crossosoma is basal in the family, followed by Glossopetalon, and ﬁnally by Velascoa and Apacheria (Sosa and Chase 2003). Afﬁnities. For a long time, the position of Crossosomaceae remained controversial, but molecular analyses such as those of Soltis et al. (2000), Savolainen, Chase et al. (2000), Cameron (2003) and Sosa and Chase (2003) indicated that Crossosomataceae belong to the Crossosomatales clade that comprises Stachyuraceae, Staphyleaceae, and probably also Geissolomataceae, Ixerbaceae, Strasburgeriaceae, and perhaps Aphloiaceae. Distribution and Habitats. Crossosomataceae are mostly xerophytic and restricted to the USA and to Mexico. Apacheria is found solely on rhyolitic rock outcrops in Arizona and New Mexico. Crossosoma is restricted to the southwestern deserts of the USA and adjacent northwestern Mexico. Glossopetalon is centered in the southwestern USA to northern Mexico. Velascoa is restricted to rocks on pine-cedar-oak forests in Querétaro, Mexico. Apacheria, Crossosoma, and Glossopetalon grow on volcanic rocks in drier habitats such as juniper-pinyon forests or deserts. Velascoa is found on limestone rocks in oak-pine-cedar forests.

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aril ﬁmbriate. Three species, two of which in desert ranges of the southeastern USA and Mexico, and one restricted to the islands off the coast of southern California and Baja California. 2. Glossopetalon A. Gray

Fig. 33

Glossopetalon A. Gray in Smithsonian Contr. Knowl. 5, 6:29 (1853); Ensign, Amer. Midl. Naturalist 27:501–511 (1942); Mason, J. Arizona Nevada Acad. Sci. 26:7–9 (1992); Holmgren, Brittonia 40:269–274 (1988); Holmgren, Intermountain Flora 3:160–163 (1997). Forsellesia E. Greene (1893).

Fig. 33. Crossomataceae. Glossopetalon spinescens. A Branch. B Leaf base with stipules. C Flower. D Fruit. E Seed. (Sosa and Chase 2003)

Deciduous shrubs, intricately or divaricately branched, often spinescent with small, simple, entire leaves; petiole short; stipules minute. Flowers solitary, whitish, small; sepals and petals 4–6, persistent; hypanthium crenately lobed, stamens 4–10; carpels 1(–3); ovules 1–2; stigma sessile. Fruit striate. Seeds small; aril ﬁmbriate, white. Four or ﬁve species, mostly from desertic habitats in southwestern USA and Mexico. The names Glossopetalon and Forsellesia are both presently in use for the same taxon.

Key to the Genera 3. Apacheria C.T. Manson 1. Leaves opposite, entire or slightly trilobate; ﬂowers tetramerous; stamens 8; follicles with prominent striate veins 3. Apacheria – Leaves alternate, entire; ﬂowers 4–5-merous; stamens 4–50; follicles wrinkled, slightly veined or smooth 2 2. Flowers funnelform; hypanthium tubular, larger than petals; stamens 10, almost sessile; nectariferous disk 0 4. Velascoa – Flowers explanate; hypanthium turbinate, shorter than petals; anthers 4–50, with conspicuous ﬁlaments; nectariferous disk present 3 3. Stamens 4–10, ﬂowers axillary, follicles striate 2. Glossopetalon – Stamens 5–50, ﬂowers terminal, follicles smooth 1. Crossosoma

Apacheria C.T. Manson, Madroño 23:105 (1975); Mason, J. Arizona Nevada Acad. Sci. 26:7–9 (1992).

Shrubs with entire to 3-dentated leaves, oblanceolate to spatulate, glabrous with minute stipules. Flowers single, sessile or short, pedunculate; sepals 4; petals 4, white; stamens 8; carpels (1–)4, stigmas linear. Fruits with prominent striate veins. Seeds 1–2 with an entire or ﬁmbrillate white aril. One species, A. chiricahuensis C.T. Manson, restricted to Arizona and New Mexico. 4. Velascoa Calderón & Rzed. Velascoa Calderón & Rzed., Acta Bot. Mex. 39:54 (1997).

Genera of Crossosomataceae 1. Crossosoma Nutt.

Fig. 32

Crossosoma Nutt., Proc. Acad. Nat. Sci. Philadelphia 4:7 (1848); Mason, J. Arizona Nevada Acad. Sci. 26:7–9 (1992).

Shrubs or small trees with simple, coriaceous, subpetiolate or sessile leaves; stipules 0. Flowers solitary; sepals 5, persistent; petals 5, spatulate to orbicular-obovate, white or sometimes purplish, deciduous; stamens 15–50, inserted in 2 or 3 whorls on the hypanthium disk; carpels 2–5(–9). Fruits non-striate. Seeds subspherical to reniform;

Small shrubs with elliptic to oblanceolate leaves; stipules 0. Flowers solitary, short pedicellate, whitish or greenish; sepals 5, 3 triangular-shaped and 2 oblong; petals 5, longer than sepals; hypanthium elongated, ribbed; stamens 10; anthers almost sessile, in two whorls, 5 opposite to sepals and 5 opposite to petals; carpels 2, distinct; stylodia short or obsolete; stigma oblong; ovules several. Fruit coriaceous, striate. Seeds 1 or 2, disk-shaped; aril whitish, ﬁmbriate. One species, V. recondita Calderón & Rzed., restricted to Queretaro in Mexico.

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Selected Bibliography Calderón, G., Rzedowski, J. 1997. Velascoa (Crossosomataceae), un género nuevo de la Sierra Madre Oriental de México. Acta Bot. Mex. 39:53–59. Cameron, K.M. 2003. See general references. DeBuhr, L. 1978. Wood anatomy of Forsellesia (Glossopetalon) and Crossosoma (Crossosomataceae, Rosales). Aliso 9:179–184. Ensign, M. 1942. A revision of the celastraceous genus Forsellesia (Glossopetalon). Amer. Midl. Naturalist 27:501–511. Gray, A. 1853. Glossopetalon. In: Plantae Wrightianae Texano-Neo-Mexicanae. Part II. Smithsonian Contr. Knowl. 5: 29. Greene, E.L. 1893. Corrections in nomenclature. III. (Forsellesia). Erythea 1: 206. Holmgren, N.H. 1988. Glossopetalon (Crossosomataceae) and a new variety of G. spinescens from the Great Basin, U.S.A. Brittonia 40:269–274. Holmgren, N.H. 1997. Crossosomataceae. In: Cronquist, C., Holmgren, N.H., Holmgren, P.K. (eds) Intermountain Flora 3:158–163. New York: New York Botanical Garden.

Kapil, R.N., Vani, R.S. 1983. Embryology and systematic position of Crossosoma californicum. Nutt. Curr. Sci. 32:493–495. Mason, C.T. 1975. Apacheria chiricahuensis: a new genus and species from Arizona. Madroño 23:105–108. Mason, C.T. 1992. Crossosomataceae: Crossosoma family. J. Arizona Nevada Acad. Sci. 26:7–9. Matthews, M.L., Endress, P.K. 2005. See general references. Metcalfe, C.R., Chalk, L. 1950. See general references. Richardson, P.E. 1970. The morphology of the Crossosomataceae. I. Leaf, stem, and node. Bull. Torrey Bot. Club 97:34–39. Savolainen, V., Chase, M.W. et al. 2000. See general references. Soltis, D.E. et al. 2000. See general references. Sosa, V., Chase, M.W. 2003. Phylogenetics of Crossosomataceae based on rbcL sequence data. Syst. Bot. 28:96– 105. Takhtajan, A. (ed.) 1981. See general references. Tatsuno, A., Scogin R. 1978. Biochemical proﬁle of Crossosomataceae. Aliso 9:185–188. Thorne, R.F., Scogin, R. 1978. Glossopetalon Greene (Glossopetalon Gray), a third genus in the Crossosomataceae, Rosineae, Rosales. Aliso 9:171–178.

Crypteroniaceae Crypteroniaceae A. DC., Prodr. 16, 2:677 (July 1868), nom. cons.

S.S. Renner

Evergreen trees. Leaves glabrous, opposite, simple, entire, pinnately veined, with short petioles and with or without small stipules. Inﬂorescences with long, spicate or racemose branches, many-ﬂowered. Flowers bisexual or unisexual (populations then apparently dioecious), epigynous or perigynous, 4–5(6)-merous; calyx minute or obsolete; petals minute or obsolete, perianth 1-or 2-whorled; androecium diplostemonous or haplostemonous, anthers bithecate, dehiscing longitudinally, connective dorsally thickened or not; pistil 2–6-locular, style with a capitate stigma; ovary inferior or superior, with few or numerous ovules per locule; ovules anatropous and bitegmic. Fruits capsules; seeds few or many, ﬂat and with one or two membranous wings, endosperm absent; embryo straight, the seed coat winged. A family of three genera and 7–12 species, in humid tropical forest in continental Southeast Asia and throughout the Malesian region, most diverse in peat swamp forests in Sabah and Sarawak. Vegetative Morphology. All Crypteroniaceae are trees, some species reaching heights of 50 m, with corresponding trunk diameters. They often grow in swamps or bogs and are adapted to waterlogged soils. Among the vegetative features commonly considered important is that leaves in Crypteronia, but not in Axinandra and Dactylocladus, have stipules. The inﬂorescences in all three genera are terminal or axillary racemes, spikes or panicles of subsessile, inconspicuous ﬂowers with much reduced or obsolete petals. Vegetative Anatomy. The three genera of Crypteroniaceae share distinct ﬁbre-tracheids but are diverse in other wood anatomical characters important in Myrtales (van Vliet 1975, 1981). Vessels are diffuse and solitary and/or in radial multiples of 2 to 3; vessel perforations are simple; inter-vessel pits are alternate; vessel-ray and vessel-parenchyma pits are half-bordered or

rarely simple. Fibre walls have distinctly bordered pits (ﬁbre-tracheids). The parenchyma is diffuse in aggregates or aliform to conﬂuent. Rays are markedly heterogeneous and can be uniseriate or 1–3-seriate. There are no crystals. A cork cambium is present and can be initially deep-seated or superﬁcial (Dactylocladus). As in other Myrtales, the primary vascular tissue is bicollateral. Crypteroniaceae lack axially included phloem (van Vliet 1975, 1981); radially included phloem is visible as small ﬂecks or holes on tangential surfaces. Crypteronia paniculata yields good general-utility timber. Stomates are paracytic in Axinandra and Crypteronia but mainly anomocytic in Dactylocladus, and the leaf mesophyll may or may not have sclerenchymatous idioblasts and contain styloid calcium oxalate crystals (Mentink and Baas 1992). Floral Morphology. As in a few other Myrtales, the corolla in Axinandra falls off as a cone-shaped unit (calyptra) when the ﬂowers open whereas, in the other two genera, the petals drop individually. Apparently, this happens very soon after the petals expand and the stamens have reached their upright position, having been bent downwards in bud. It is unclear whether in Dactylocladus and Crypteronia, which have haplostemonous ﬂowers, the stamen meristems originate in front of the sepals or in front of the petals. As in other Myrtales, there is a tendency towards dorsally enlarged stamen connectives, a trait which may relate to the incurved position of the stamens in bud and the connective’s role in the unfolding of the stamens at anthesis (Fig. 34D, E). Karyology. Crypteroniaceae are unknown cytologically. Pollen Morphology. Pollen of species from all three genera has been studied (Patel et al. 1984) and found to be rather nondescript. The main distinction between the genera is that pollen in Cryptero-

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nia is bisyncolporate with two indistinct subsidiary colpi, whereas pollen in Axinandra and Dactylocladus has three or four colporate apertures which vary with three or four pseudocolpi. Embryology. Similarly to other Myrtales, Axinandra, Crypteronia and Dactylocladus have a glandular anther tapetum, crassinucellate ovules, an initially 2-layered inner integument, a micropyle which is formed by both integuments, an embryo sac with ephemeral or absent antipodial cells, endosperm formation of the Nuclear type, and exalbuminous seeds (Tobe and Raven 1983, 1987a, b). The development of the embryo sac follows the Polygonum type. In all three genera, the anther endothecium degenerates early, and the anthers therefore dehisce not via differential shrinking of endothecium cells, as in most angiosperms, but rather via rupture of walls along their thinnest sections, caused by the shrinking of connective cells (Tobe and Raven 1987a, b; H. Tobe, Kyoto University, pers. comm. 2001). A feature setting Axinandra apart from Crypteronia and Dactylocladus is an endothelium (a tapetal layer in the inner integument), which is associated with a secondary multiplication of the inner integument. Fruit and Seed. Fruits in Crypteroniaceae are capsules which open introrsely or apically by 2–5 valves, and which contain few to numerous small seeds. The seeds are exalbuminous, ﬂat, and minutely winged either only on the chalazal side or on both ends. The mature seed coat is formed by a tannin-containing exotesta, a crystal-containing endotesta, and a tannin-containing endotegmen (Tobe and Raven 1987a, b). Pollination and Other Plant/Animal Interactions. No observations on the pollination of any Crypteroniaceae have been published. Crypteronia have densely clustered, minute ﬂowers lacking petals and nectaries (judging from herbarium material), and which are often unisexual, all pointing to wind pollination. Axinandra and Dactylocladus have bisexual ﬂowers and, hence, could offer pollen as a reward for bees in both ﬂoral morphs. Although pollination remains unstudied, a tight herbivore defence mutualism between Crypteronia grifﬁthii and an aggressive ant species has received considerable attention from ecologists. Swollen nodes of young twigs in saplings and young trees are inhabited by queens of Cladomyrma maschwitzi, and the interaction

Fig. 34. Crypteroniaceae. Axinandra coriacea. A Habit. B Young ﬂower bud. C Older bud, with protruding style. D Mature ﬂower, petals dropped. E Stamen. F Old ﬂower, petals and stamens dropped. G Mature capsule. (van Beusekom-Osinga 1977)

is among the most common Cladomyrma/plant associations in a Pasoh 50-ha study plot on the Malay Peninsula (Maschwitz et al. 1991 and references therein). Seed Dispersal. The minute (1.4–3 mm long in the different species), dry and winged seeds certainly are wind-dispersed.

Crypteroniaceae

Phytochemistry. Leaves of Axinandra and Crypteronia, but apparently not of Dactylocladus, accumulate aluminium (Jansen et al. 2002). Phylogeny. van Beusekom-Osinga and van Beusekom (1975) were the ﬁrst to recognize the close relationship of Axinandra, Dactylocladus and Crypteronia, although this insight appears to have been based mostly on intuition because the three genera exhibit no uniquely shared trait. van Beusekom-Osinga and van Beusekom ranked the three genera as a subfamily within a more widely circumscribed Crypteroniaceae which also included the South American Alzatea and the South African Rhynchocalyx. Based on wood anatomy, van Vliet (1981; also van Vliet and Baas 1984) transferred Crypteronioideae into Melastomataceae (again as a subfamily). This view, however, never gained wide acceptance but rather that of Dahlgren and Thorne (1984), and Johnson and Briggs (1984) who saw the three genera as relatively isolated in Myrtales, and accordingly gave them family rank. Molecular data from three chloroplast genes (Clausing and Renner 2001; Rutschmann et al. 2004) suggest that Crypteroniaceae are sister to a clade comprising Alzateaceae, Rhynchocalycaceae, Oliniaceae and Peneaeceae, and that Dactylocladus is sister to Axinandra plus Crypteronia, albeit without solid statistical support. If the latter relationship were to be conﬁrmed, this would argue against previous assessments which saw either Axinandra as standing apart, especially in having an endothelium (Tobe and Raven, 1987b), or Crypteronia, in possessing stipules, a closed vascular pattern in the petiole and midrib (Mentink and Baas 1992), and diffuse parenchyma (van Vliet 1981). Earlier systematists had seen Axinandra as lythraceous (e.g. Bentham and Hooker 1867), melastomaceous (e.g. Baillon 1877; Cogniaux 1891; Krasser 1893; Gilg 1897; Bakhuizen van den Brink 1946/1947), or even as intermediate between these families (Meijer 1972). Dactylocladus was placed next to Axinandra by its author, and Crypteronia was usually treated as a separate family because of its stipules, a rare feature in Myrtales. Fossils and Distributional History. The only known fossils of Crypteroniaceae are Miocene pollen grains of Dactylocladus from a bog in southeastern Kalimantan (Demchuk and Moore 1993). Remarkably, the vegetation which formed this Miocene lignite is virtually identical to its presentday peat-forming counterpart in Indonesia. Based

125

on a molecular clock calibrated with Melastomataceae fossils, Conti et al. (2002, 2004; see also Rutschmann et al. 2004) suggest that Crypteroniaceae may have rafted from Gondwana to Asia on India, with an origin in the Early to Middle Cretaceous. However, substitution rate heterogeneity does not allow us to draw any ﬁrm conclusion here (Moyle 2004; F. Rutschmann, pers. comm. 2005), and a more recent separation from their African and South American closest relatives, with subsequent long-distance dispersal, remains an equally likely possibility. The family’s widespread distribution throughout the Malesian archipelago certainly attests to its high dispersal capabilities. Key to the Genera 1. Flowers with 3 bracts, the 2 outer ones minute. Stamens twice as many as sepals. Fruit big, woody. Seeds winged on one side 1. Axinandra – Flowers with 1 bract. Stamens as many as sepals. Fruits small, chartaceous. Seeds winged on both sides 2 2. Petals present, soon caducous. Ovary at least halfinferior, the lower part immersed in the receptacle, with up to 3 ovules per locule. Fruits with few seeds 2. Dactylocladus – Petals absent. Ovary superior, with many ovules per locule. Fruit with numerous seeds 3. Crypteronia

Genera of Crypteroniaceae 1. Axinandra Thwaites

Fig. 34

Axinandra Thwaites, Hooker’s J. Bot. Kew Gard. Misc. 6:66, t. 1C (1854).

Tree. Flower bracts 3 per ﬂower, persistent during anthesis; ﬂowers bisexual, 5(4)-merous, the petals falling off as a cap when the ﬂowers open. Stamen connectives broad and provided with a dorsal tubercle, anthers broad-linear, introrse. Ovary inferior, with 3(2) carpels and 6(4) locules, each with 1 or 2 ovules. Fruit an oblong-globose woody capsule, the lower part surrounded by the persistent receptacle, capsule introrsely dehiscing by 2–6 valves. Seeds 1 or 2 per locule, each with a thin narrow-oblong wing on one side of the seed. Two to four species in Sri Lanka, the Malay Peninsula and Borneo. 2. Dactylocladus Oliver Dactylocladus Oliv., Hooker’s Ic. Pl. 24: t. 2341 (1895).

Subcanopy tree or shrub. The single ﬂower bract early caducous; ﬂowers bisexual, 5(4)-merous, the petals falling off individually. Stamen connectives

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S.S. Renner

more or less orbicular, the anthers semiorbicular slightly below the upper margin of the connective, introrse. Ovary half-inferior, (3)4 or 5 carpels and (3)4 or 5 locules, each with 3 ovules. Fruit a small, thin capsule, its valves often kept together at the top by the non-splitting persistent style. Seeds usually 3 per locule, with lateral membranous wings about twice as long as the seed. A single species, D. stenostachys Oliv., in lowland peat swamp forest in Sarawak. 3. Crypteronia Blume Crypteronia Blume, Bijdr.: 1151 (Oct. 1826–Nov. 1827).

Tall trees. The single ﬂower bract linear, early caducous; ﬂowers bisexual or unisexual and trees then apparently dioecious, 4–5(6)-merous; petals 0. Stamens (staminodes?) in female ﬂowers permanently bent inwards, in bisexual ﬂowers with an orbicular connective bearing the semiorbicular anthers, more or less introrse. Ovary superior or almost so, only the lowermost part adhering to the receptacle, 2–4-carpellate, reduced in male ﬂowers; ovules many, on axile-basal placentas. Fruit a small, laterally compressed capsule, the top dehiscent by 2–4 valves. Seeds many, very small, with membranous lateral wings. Four to seven species, one endemic to the Philippines, two more or less widespread throughout the Malesian region (of which C. paniculata Bl. also reaches tropical China), and 1–4 endemic to Borneo.

Selected Bibliography Baillon, H.E. 1877. Histoire des Plantes, tome 7. Paris: Hachette. Bakhuizen van den Brink, R.C. Jr. [1943] 1946/1947. A contribution to the knowledge of the Melastomataceae occurring in the Malay Archipelago, especially in The Netherlands East Indies. Rec. Trav. Bot. Néerl. 40:1– 391. [Reprinted in Meded. Bot. Mus. Herb. Rijks Univ. 91:1–391 (1947)] Bentham, G., Hooker, J.D. 1867. Genera Plantarum. London: Lovell Reeve, pp. 725–773 [Melastomaceae by J.D. Hooker]. Beusekom-Osinga, R.J. van 1977. Crypteroniaceae. In: Steenis, C.G.G.J. van (ed.) Flora Malesiana I, 8:187–204. Alphen aan den Rijn: Noordhoff. Beusekom-Osinga, R.J. van, Beusekom, C.F. van 1975. Delimitation and subdivision of the Crypteroniaceae (Myrtales). Blumea 22:255–266. Clausing, G., Renner, S.S. 2001. Molecular phylogenetics of Melastomataceae and Memecylaceae: implications for character evolution. Amer. J. Bot. 88:486–498. Cogniaux, C.A. 1891. Melastomaceae. In: Candolle, A. de, Candolle, C. de (eds) Monographiae Phanerogamarum, 7. Paris: Masson, pp. 1–1256.

Conti, E. et al. 2002. See general references. Conti, E., Rutschmann, F., Eriksson, T., Sytsma, K., Baum, D. 2004. Calibration of molecular clocks and the biogeographic history of Crypteroniaceae: a reply to Robert G. Moyle. Evolution 58:1874–1876. Dahlgren, R., Thorne, R.F. 1984 [1985]. The order Myrtales: circumscription, variation, and relationships. Ann. Missouri Bot. Gard. 71:633–699. Demchuk, T., Moore, T.A. 1993. Palynoﬂoral and organic characteristics of a Miocene bog-forest, Kalimantan, Indonesia. Org. Geochem. 20:119–134. Gilg, E. 1897. Melastomataceae [Nachtrag]. In: Engler, A., Prantl, K., Die natürlichen Pﬂanzenfamilien, Nachträge. Leipzig: W. Engelmann, pp. 263–268. Jansen, S., Watanabe, T., Smets, E. 2002. Aluminium accumulation in leaves of 127 species in Melastomataceae, with comments on the order Myrtales. Ann. Bot. 90:53–64. Johnson, L.A.S., Briggs, B.G. 1984 [1985]. Myrtales and Myrtaceae – a phylogenetic analysis. Ann. Missouri Bot. Gard. 76:700–756. Krasser, F. 1893. Melastomataceae. In: Engler, A., Prantl, K., Die natürlichen Pﬂanzenfamilien III, 7. Leipzig: W. Engelmann, pp. 130–199. Maschwitz, U., Fiala, B., Moog, J., Saw, L.G. 1991. Two new myrmecophytic associations from the Malay Peninsula: ants of the genus Cladomyrma (Formicidae, Camponotinae) as partners of Saraca thaipingensis (Caesalpiniaceae) and Crypteronia grifﬁthii (Crypteroniaceae). 1. Colony foundation and acquisition of trophobionts. Insectes Sociaux 38:27–35. Meijer, W. 1972. The genus Axinandra – Melastomataceae: a missing link in Myrtales. Ceylon J. Sci. (Biol. Sci.) 10:72–74, 2 pls. Mentink, H., Baas, P. 1992. Leaf anatomy of the Melastomataceae, Memecylaceae, and Crypteroniaceae. Blumea 37:189–225. Moyle, R.G. 2004. Calibration of molecular clocks and the biogeographic history of Crypteroniaceae. Evolution 58:1869–1871. Patel, V.C., Skvarla, J.J., Raven, P.H. 1984 [1985]. Pollen characters in relation to the delimitation of Myrtales. Ann. Missouri Bot. Gard. 71:858–969. Pereira, J.T., Wong, K.M. 1995. Three new species of Crypteronia (Crypteroniaceae) from Borneo. Sandakania 6:41–53. Rutschmann, F., Eriksson, T., Conti, E. 2004. Did Crypteroniaceae really disperse out of India? Molecular dating evidence from rbcL, ndhF, and rpl16 intron sequences. Intl J. Pl. Sci. suppl. 165:S69–S83. Tobe, H., Raven, P.H. 1983. The embryology of Axinandra zeylanica (Crypteroniaceae) and the relationships of the genus. Bot. Gaz. 144:426–432. Tobe, H., Raven, P.H. 1987a. The embryology and relationships of Crypteronia (Crypteroniaceae). Bot. Gaz. 148:96–102. Tobe, H., Raven, P.H. 1987b. The embryology and relationships of Dactylocladus (Crypteroniaceae) and a discussion of the family. Bot. Gaz. 148:103–111. Vliet, G.J.C.M. van 1975. Wood anatomy of Crypteroniaceae sensu lato. J. Microscopy 104:65–82. Vliet, G.J.C.M. van 1981. Wood anatomy of the palaeotropical Melastomataceae. Blumea 27:395–462.

Daphniphyllaceae Daphniphyllaceae Müll.-Arg. in A. DC., Prodr. 16, 1:1 (1869), nom. cons.

K. Kubitzki

Evergreen, glabrous trees or shrubs, dioecious or rarely polygamo-dioecious; branchlets covered with circular or elliptic lenticels. Leaves simple, petiolate, estipulate, alternate, rarely opposite, sometimes fasciculate at the branch-tips and subverticillate, pinnately veined; margin entire, sometimes dentate near the apex. Inﬂorescences axillary, rarely subterminal, racemiform. Flowers unisexual, regular, hypogynous, apetalous, pedicellate; sepals 0 or 3–6 and then imbricate; stamens 5–14, subsessile or with long ﬁlaments; anthers curved (“lunate”) or straight, basiﬁxed, tetrasporangiate, latrorse, opening with valves, commonly with a shortly prolonged connective; pistillodes rarely present in staminate ﬂowers; gynoecium syncarpous of 2(–4) carpels, imperfectly 2(–4)-septate; stylodia short, connate only at the base, divaricate, recurved or circinate, with dry, papillate, decurrent stigmas; ovules (1)2 in each locule, lateral on parietal placentae, pendulous, anatropous, epitropous, bitegmic, crassinucellate. Fruit a 1(2)-seeded drupe; seeds with abundant oily and proteinaceous endosperm and some perisperm; embryo very small, straight, apical. 2n = 32. A monogeneric family with about thirty species distributed from India to Japan and from Central China to New Guinea. Vegetative Structures. A detailed description was given by Huang (1965, 1966). Wood anatomy was treated in most detail by Carlquist (1982). He describes the vessels as angular to roundish in transection, with scalariform perforation plates, tracheids with fully bordered pits, heterocellular multiseriate and uniseriate rays, and diffuse axial parenchyma. These traits are not very speciﬁc, and indicate vague similarities with “hamamelid” and “rosid” families. Reproductive Structures. The female ﬂowers are arranged in racemes. Each ﬂower is subtended by a conspicuous bract; prophylls and of-

ten also the tepals are wanting. The anthers open with valves standing off like the wings of a door (Hallier 1904). Gynoecium and ovule structure was described by Endress and Igersheim (1999); Bhatnagar and Kapil (1983) studied the development of the ovules and seeds. Embryology. The tapetum is glandular, and the pollen grains are 2-celled when shed (Bhatnagar and Garg 1977). Embryo sac development is of the Polygonum type (Bhatnagar and Kapil 1983). There is a precocious degeneration of antipodal cells. Pollen Morphology. Huang (1965) studied the pollen of eight species and several subspecies and found nearly all tricolpate, with only some samples tricolporoidate and one questionably tricolporate. Karyology. Two species have been counted as 2n = 32. Fruit and Seed. The fruit has a stony endocarp. In the seed coat of Daphniphyllum himalayense, the testa is crushed and the endotegmen is sclerotic. The nucellar epidermis and adjacent layers of subdermal cells convert into a thin perisperm surrounding the copious endosperm, in which a minute embryo is embedded (Bhatnagar and Kapil 1983). Phytochemistry. Daphniphyllum alkaloids represent a very peculiar biosynthetic group of triterpene alkaloids not found elsewhere in plants. Asperulin and another iridiod compound have also been recorded. Phenolics are represented by ubiquitous compounds; gallic and ellagic acids are wanting (Hegnauer 1966, 1989). No condensed tannins are present (pers. obs.). The absence of tannins may be related to the presence of the biologically very active alkaloids. Huang’s (1965) “tanniniferous canals”, reported to be distributed throughout all tissues, have been discredited

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Hamamelidae, although within Saxifragales these families remain unresolved (Fishbein et al. 2001). Distribution and Habitats. Daphniphyllum is a subtropical and tropical montane element. It is conﬁned to eastern Asia between about 46◦ N and 10◦ S, and 75◦ and 150◦ E, occurring mostly in humid forests from the lowland up to 3,000 m altitude, in Borneo extending into the subalpine belt at c. 4,000 m. The greatest differentiation of the genus is in southwest China, particularly in Yunnan (Huang 1965). Only one genus: Daphniphyllum Bl. Daphniphyllum Bl., (1965/1966), rev.

Fig. 35 Bijdr.

17:1153

(1826);

Huang,

Characters of the family. Fig. 35. Daphniphyllaceae. Daphniphyllum himalayense subsp. macrocarpum (ﬁgure published as D. macropodum). A Fruiting branch. B Male ﬂower. C Female ﬂower with staminodes. D Fruit. E Vertical section of fruit with seed. (Takhtajan 1980)

by Carlquist (1982) as representing fungal hyphae. Some species were found to accumulate aluminium. Afﬁnities. The question of the afﬁnities of Daphniphyllum has been discussed time and again, with little result. The older view, assuming a relationship to Euphorbiaceae, is now deﬁnitely discredited. Relationships to Geraniales, Buxales, Hamamelidales or Magnoliales, among others, have also been suggested (see, for example, Huang 1965; Bhatnagar and Garg 1977; Zhang and Lu 1989). More recently, and based on ﬂower structure, pollen morphology and wood anatomy, discussion has focussed mainly on Hamamelidales but vague alternatives have been proposed as well. Molecular evidence places Daphniphyllaceae as sister to Peridiscaceae in Saxifragales, together with Cercidiphyllaceae, Hamamelidaceae and Altingiaceae, the latter previously attributed to

Selected Bibliography Bhatnagar, A.K., Garg, M. 1977. Afﬁnities of Daphniphyllum – palynological approach. Phytomorphology 27:92–97 Bhatnagar, A.K., Kapil, R.N. 1983 (‘1982’). Seed development in Daphniphyllum himalayense with a discussion on taxonomic position of Daphniphyllaceae. Phytomorphology 32:66–81. Carlquist, S. 1982. Wood anatomy of Daphniphyllaceae: ecological and phylogenetic considerations, review of pittosporalean families. Brittonia 34:252–266. Endress, P.K., Igersheim, A. 1999. Gynoecium diversity and systematics of the basal eudicots. Bot. J. Linn. Soc. 130:305–393. Fishbein, M. et al. 2001. See general references. Hallier, H. 1904. Über die Gattung Daphniphyllum, ein Übergangsglied von den Magnoliaceen und Hamamelidaceen zu den Kätzchenblüthlern. Bot. Mag. 18:55–69. Hegnauer, R. 1966, 1989. See general references. Huang, T.-C. 1965. Monograph of Daphniphyllum, I. Taiwania 11:57–98. Huang, T.-C. 1966. Monograph of Daphniphyllum, II. Taiwania 12:137–234. Rosenthal, K. 1919. Daphniphyllaceae. In: Engler, A., Pﬂanzenreich IV, 147a. Leipzig: W. Engelmann. Takhtajan, A. 1980. See general references. Zhang, Z.-Y., Lu, A.-M. 1989. On the systematic position of Daphniphyllaceae (in Chinese). Acta Phytotaxon. Sin. 27:17–26.

Didymelaceae Didymelaceae Leandri, Ann. Sci. Nat. Bot. X, 19:316 (1937).

E. Köhler

Evergreen dioecious trees to 15 m high. Hairs small, peltate. Leaves alternate, petiolate, entire, estipulate. Inﬂorescences axillary, pedunculate, simple or compound spike-like racemes or depauperate panicles. Flowers small, apetalous; males: subtended by 0–2 scales, stamens 2, with connate ﬁlaments, anthers basiﬁxed, extrorse, dithecal, tetrasporangiate, longitudinally dehiscent; females: paired, solitary or in triads, each subtended by a bract and a minute abaxial scale, monocarpellate with an adaxial suture and a large, truncate or obliquely decurrent bilobate stigma, stylodium very short or 0, ovule solitary, hemianatropous. Fruit a sulcate, indehiscent drupe with vestigial stigma at the apex; seed solitary; endosperm 0; embryo with thick cotyledons. A monogeneric family with two species endemic to east and north Madagascar and the Comoros. Vegetative Anatomy. The young branches have chambered pith. The leaf blades are ovateacuminate, coriaceous or chartaceous, drying yellowish green; venation is derived brochidodromous with secondaries extending to a marginal vein, which is primarily composed of ﬁbres, and acute-angled tertiaries developing ex- and admedially to form polygones irregular in shape and size. Approaching the margin, these veins disintegrate into splayed-out individual bundles, which sometimes anastomose with the network of ﬁbres (Wolfe 1973). The leaves are bifacial and hypostomatic. The stomata are cyclocytic with 4–10 subsidiaries and well-developed outer ledges, halfway sunken into the thick cuticle. Calcium oxalate druses are present. Small peltate, non-glandular trichomes are recorded by Carlquist (1982). The petiole comprises a central arc-shaped and two lateral inverse traces. Vessels in radial groups of 4–6, with scalariform perforation plates of 6–30 thin bars, with well-expressed tails and bordered pits; lateral pitting is alternate to opposite

and, in wide vessels, mostly in rows; ﬁbres have minute bordered pits. Rays mixed-heterogeneous, 10–30 cells high, with long, rarely short wings of erect cells; wood parenchyma replaced by ligniﬁed cells. Tissue of bark, stem and leaves contains abundant coarse, short ﬁbres with extremely small lumina and numerous channels and bordered pits. Secretory ducts are lacking (Takhtajan et al. 1986). The wood anatomy of Didymeles displays about the same level of organisation as does the buxaceous Styloceras (Carlquist 1982). Floral Structure. Flowers are often found in dyads or triads, which may indicate that the inﬂorescences are depauperate thyrso-paniculate systems. In contrast to Drake de Castillo (1897), who illustrated a bicarpellate female ﬂower, Leandri (1937) and von Balthazar et al. (2003) tend to interpret the female ﬂower as monocarpellate. The question whether the scale-like structure below the carpel represents a perianth is controversial. The orientation of the carpel is slightly deﬂected abaxially. The carpel is ascidiate in the lower half and, at anthesis, it is completely closed by postgenital fusion. The stigma is double-crested and widely decurrent. The gynoecium is supplied by two main and two accessory bundles; two branches of a main bundle which enter the nucellus are accompanied by a tissue similar to the conductive tissue of the stylodium; hence, chalazogamy seems possible (Leandri 1937). Embryology. The ovules are crassinucellar, hemianatropous, pendulous, epitropous with an extrorse micropyle, and bitegmic. The integuments are apically ± protracted and form a collar-like exostome; the chalaza is conically prolonged (Leandri 1937). Pollen Morphology. Pollen grains are tricolpodiorate, ± spheroid, c. 23 µm. The broad colpi are covered by a sculptured operculum and contain

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von Balthazar et al. (2003) observed a rudimentary aril. Phytochemistry. Steroidal alkaloids of the aminopregnan type very similar to those of Buxaceae have been isolated from the bark of both species (Sánchez et al. 1984; Hegnauer 1989). Afﬁnities. Although Leandri (1937) considered Didymeles as allied with Leitneriaceae, it differs from them in its racemose inﬂorescence, the structure of the male ﬂower, the unique pollen type, the ovule structure, the cylocytic stomata and other important anatomical traits (Hjelmquist 1948; Takhtajan 1966). An afﬁnity with Hamamelidaceae, ﬁrst proposed by Hallier (1912), was also accepted by Takhtajan (1966), Cronquist (1981) and Barabé et al. (1987). However, pollen and ovule morphology and seed-coat anatomy (Melikian 1973) of Didymeles differ considerably from those of Hamamelidales. Moreover, the gynoecium is monocarpellate, and the leaves are estipulate. Didymeles has also variously been assigned to Buxaceae in or near Euphorbiales (Erdtman 1952; Thorne 1973; Dahlgren 1980). The close relationship with Buxaceae (but not with Euphorbiales) is supported by pollen morphology (Köhler 1980), the cyclocytic stomata type, leaf venation pattern, wood anatomy including the frequency of sclereids, and the occurrence of very peculiar steroidal alkaloids (Takhtajan 1997). The results of molecular studies suggest a sister group relationship between Didymelaceae and Buxacae, and indicate a close relationship of these two families with Proteaceae and Sabiaceae at the base of the eudicots (APG II 2003). Fig. 36. Didymelaceae. Didymeles madagascariensis. A Pollen, polar view, ×3,500. B Equatorial view, diorate colpus with operculum, ×2,700 (Köhler 1980)

two circular ora, plugged by a nexinous appendix of the operculum (Fig. 36). The exine is semitectate, reticulate, simplibaculate and has micro-spinules at the edges of the reticulum. The sexine is more than twice as thick as the nexine; sometimes, it is detached (Straka 1966; Köhler 1980). Fruit and Seed. The fruit is an indehiscent, admedially sulcate drupe; the bony endocarp contains a single, pendent seed, is apically acuminate and has a rugose surface. The seed coat is made up of the testa which consists of few layers of little-thickened cells, the tegmen being obliterated (Melikian 1973).

Past and Present Distribution. Both species of Didymeles are restricted to primary forests in eastern and northern Madagascar, and one of them (D. integrifolia) is also known from Moheli, the Comoros. Didymeles pollen has been recorded from the Palaeocene and Eocene from the Ninetyeast Ridge in the Indian Ocean, Australia, New Zealand and New Caledonia, indicating a much wider distribution of the group in the Palaeogene (Muller 1981; Hill 1994). If the similarly structured pollen of Hexaporotricolpites (Boltenhagen 1967) is related correctly to Didymeles, the origin of this lineage can be traced to the Albian of Gabon and Brazil. Conservation. First collected by Noronha before 1787, Didymeles is poorly represented in herbarium collections and may be highly endangered in the wild.

Didymelaceae

Fig. 37. Didymelaceae. Didymeles integrifolia. A Flowering male branch. B Female inﬂorescence. C Pair of female ﬂowers. D Infructescence. E Male inﬂorescence. F Male ﬂower. (Takhtajan 1980)

Only one genus: Didymeles Thouars

Fig. 37

Didymeles Thouars, Pl. îles Afrique australe: 23, tab. 1 (1804).

Description as for family. Three species.

Selected Bibliography APG II 2003. See general references. Balthazar, M. von, Schatz, G.E., Endress, P.K. 2003. Female ﬂowers and inﬂorescences of Didymelaceae. Pl. Syst. Evol. 237:199–208. Barabé, D., Bergeron, Y., Vincent, G.A. 1987. La répartition des caractères dans la classiﬁcation des Hamamelididae (Angiospermae). Canad. J. Bot. 65:1756–67.

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Boltenhagen, E. 1967. Spores et pollen de Crétacé supérieure du Gabon. Pollen Spores 9:335–355. Carlquist, S. 1982. Wood anatomy of Buxaceae: correlations with ecology and phylogeny. Flora 172:463–491. Cronquist, A. 1981. See general references. Dahlgren, R.T.M. 1980. A revised system of classiﬁcation of the angiosperms. Bot. J. Linn. Soc. 80:91–124. Drake del Castillo, E. 1897. Histoire naturelle des plantes, 6. In: Grandidier, A., Histoire physique, naturelle et politique de Madagascar, 36: pl. 308 A, Paris. Erdtman, G. 1952. See general references. Hallier, H. 1912. L’origine et le système phylétique des angiosperms exposés à l’aide de leur arbre généalogique. Arch. Néerl. Sci. Exact. Nat. III, 1:146–234. Hegnauer, R. 1989. See general references. Hill, R.S. (ed.) 1994. History of the Australian vegetation: Cretaceous to Recent. Cambridge: Cambridge University Press. Hjelmquist, H. 1948. Studies on the ﬂoral morphology and phylogeny of the Amentiferae. Bot. Notiser, suppl. 2:71–76. Köhler, E. 1980. Zur Pollenmorphologie und systematischen Stellung der Didymelaceae Leandri. Feddes Repert. 91:581–591. Leandri, J. 1937. Sur l’aire et la position systématique du genre malgache Didymeles Thouars. Ann. Sci. Nat. Bot. X, 19:304–318. Melikian, A.P. 1973. Seed-coat types of Hamamelidaceae and allied families in relation to their systematics. Bot. Zhurn. (Moscow & Leningrad) 58:350–359. Muller, J. 1981. Fossil pollen records of extant angiosperms. Bot. Rev. 45:1–142. Sánchez, V., Ahond, A., Debray, M.-M., Picot, F., Poupat, C. 1984. Alcaloïdes des écorces de tronc de Didymeles cf. madagascariensis (Didymélacées). Bull. Soc. Chim. France 2:71–76. Straka, H. 1966. Palynologia Madagassica et Mascarenica: Didymelaceae. Pollen Spores 8:242–243, 246–247. Takhtajan, A.L. 1966. Systema et phylogenia Magnoliophytorum. Moscow: Nauka. Takhtajan, A.L. 1980. See general references. Takhtajan, A. 1997. See general references. Takhtajan, A.L., Shilkina, I.A., Yatsenko-Khmelevsky, A.A. 1986. Wood anatomy of Didymeles madagascariensis in the connection with the systematic status of the family Didymelaceae (in Russian). Bot. Zhurn. (Moscow & Leningrad) 71:1203–1206. Thorne, R.F. 1973. The “Amentiferae” or Hamamelidae as an artiﬁcial group: a summary statement. Brittonia 25:395–405. Wolfe, J.A. 1973. Fossil forms of Amentiferae. Brittonia 25:335–355.

Dilleniaceae Dilleniaceae Salisb., Parad. Lond. 2, 1: ad t. 73 (1807), nom. cons. (‘Dilleneae’).

J.W. Horn

Trees, shrubs, or lianas, rarely subshrubs or rhizomatous herbs; vestiture of scleriﬁed and/or siliciﬁed simple and sometimes also fasciculate trichomes; glandular trichomes very rare. Leaves spirally arranged, very rarely opposite; blades petiolate or uncommonly sessile, simple, or rarely threefold pinnatisect to pinnately compound; margins entire or toothed; venation craspedromous, semicraspedromous, brochidodromous, or eucamptodromous, frequently with ± straight, parallel secondaries terminating in the teeth (when present), and rigidly percurrent tertiaries; stipules 0, but the petiole sometimes with persistent or caducous amplexicaul wings, and often with a broad insertion. Plants synoecious, or rarely structurally androdioecious and functionally dioecious. Inﬂorescences terminal, axillary, or ramiﬂorous, determinate; frequently a thyrsoid with cincinnate or modiﬁed dichasial partial inﬂorescences, a panicle, or monad, sometimes a botryoid or cincinnus; pedicels commonly with apical articulation. Flowers small to very large, actinomorphic or (mainly in the androecium) monosymmetric, hypogynous or very rarely partly epigynous, without nectar; receptacle ﬂat or infrequently conical; sepals (3)4–5(–18), equal to unequal, typically free, membranaceous to coriaceous, imbricate (quincuncial when 5), always persistent, slightly to substantially accrescent in fruit; petals (2)3–5(–7), free, elliptic to obovate, often emarginate, typically white or yellow, frequently crumpled in bud, imbricate (quincuncial when 5), typically caducous; stamens (1 or 3–)5–400(–900), occasionally partly staminodial, typically marcescent, free or sometimes the ﬁlaments basally to nearly fully connate and then typically grouped into 1, 2, 3, or 5 fascicle(s), rarely forming a short tube; anthers basiﬁxed, dithecal and tetrasporangiate, linear to oblong to subglobose, dehiscing via longitudinal slits, apical clefts, or apical pores; connective sometimes thickened, distinctly separating the thecae, and occasionally

protruding apically as a short mucro; gynoecium apocarpous to, less frequently, hemisyncarpous, of 1–10(–20) carpels arranged in 1 whorl (very rarely 2 whorls); stylodia free; stigmas punctiform, minute, and not differentiated in shape from the stylodia, or the stigmas peltate with an annuliform or, infrequently, irregular margin; ovules 1–80, anatropous to campylotropous, when 1, apotropous, when 1–2, 1 apotropous and 1 epitropous, erect, or when 4 or more, pleurotropous and syntropous, bitegmic, crassinucellate; placentation submarginal, in 2(4, 6) vertical rows, or basal when ovules 1–2. Fruit most frequently a follicle or aggregate of follicles (sometimes basally coherent), or indehiscent and enclosed by the ﬂeshy, accrescent sepals, less often a ﬂeshy capsule, berry, or aggregate of nutlets; aril ﬂeshy to scarious and oily or waxy, funicular, rarely vestigial; seed coat with typically heavily sclerotized or sometimes cutinized endotesta; raphe short; endosperm ﬂeshy, oily or sometimes also starchy, abundant; embryo straight, minute. A pantropical family with a largely Gondwanic distribution, extending into temperate Australia, containing 10 genera and c. 500 species. Characters of Rare Occurrence. Rhizomatous herbs in Acrotrema. Subshrubs mostly or only with cataphylls and always with green, photosynthetic, sympodial, aerial stems that are terete and ephedroid to ﬂattened and phyllocladous (sometimes dimorphic) in Hibbertia subg. Pachynema. Lignotuberous shrubs in several species of Hibbertia and Tetracera masuiana. Stilt roots occasionally present in several Dillenia spp. and consistently present in D. borneensis, D. grandifolia, and D. reticulata (Hoogland 1952, 1959). Leaves pinnatisect to pinnate in a few Sri Lankan Acrotrema spp., sessile and rarely amplexicaul to entirely perfoliate (some Hibbertia). Leaves opposite in Doliocarpus pruskii and Hibbertia coriacea and with persistent (Davilla spp., Didesmandra, Dillenia spp., Schumacheria) or caducous (Acrotrema, Dillenia

Dilleniaceae

spp.) amplexicaul wings. Leaf domatia in Doliocarpus spp. and Tetracera spp. Leaves turning yellow or golden brown during extreme drought and regreening after rain (diallagy; George 2002) in Hibbertia hypericoides and H. spicata subsp. leptotheca (and perhaps other Hibbertia spp. in regions with arid climates). Plants structurally androdioecious and functionally dioecious in neotropical Tetracera spp. Petals absent in Dillenia celebica, D. grandifolia, and D. serrata (Hoogland 1952, 1959). Corolla orange in Hibbertia comptonii, H. miniata, and H. stellaris, pink to deep red in several species of Hibbertia subg. Pachynema, and deep red in Dillenia pteropoda, inconsistently deep red in a few Dillenia or pink in a few Asian Tetracera (Hoogland 1953). Corolla not spreading at anthesis in Dillenia papuana and several putatively related Dillenia. Fertile androecium distinctly heterantherous in Didesmandra, many Dillenia, Hibbertia heterotricha, H. margaretae, H. nana, H. pulchella. Stamens fewer than 5 in Hibbertia hirsuta (1–3), some populations of H. fasciculata and H. racemosa (3), Hibbertia (Pachynema) praestans (4), and H. rufa (4). Floral receptacle conical in the region of the gynoecium in Dillenia and Hibbertia baudoinii. Carpels more than 5 in most Dillenia spp., Hibbertia grossulariifolia, and some populations of H. scandens. Vegetative Morphology. The family varies from tall, sometimes buttressed trees (Dillenia spp.), small to medium-sized, tortuous trees (Curatella), small to medium-sized rosette trees (New Caledonian Hibbertia), to shrubs (Hibbertia; some Davilla, Doliocarpus, and Tetracera), lianas (e.g., Davilla, Doliocarpus, Neodillenia, Pinzona, Tetracera, some Hibbertia), subshrubs with ephedroid or phyllocladous, photosynthetic aerial shoots and foliage typically of cataphylls (Hibbertia subg. Pachynema), and perennial herbs with a woody rhizome (Acrotrema). The bark often has a characteristic rich red- or orange-brown color and abundantly exfoliates in thin, papery plates, ﬂakes, or strips, or the outer bark is gray, and exfoliates in ﬂakes to reveal a rich-brown younger bark. Scandent species climb by twining, and the extension growth of large, climbing individuals of Delimoideae and Doliocarpoideae is often conspicuously curved or hooked. Virtually the entire aerial plant body of Hibbertia subg. Pachynema, which consists of photosynthetic stems with cataphylls, represents inﬂorescences, as is shown by the occasional production

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of ‘normal’ foliage leaves at the basalmost nodes of a developing shoot in a few species (Craven and Dunlop 1992): the shoot systems can be compared with a compound thyrsoid or panicle. Foliage of some early branches of, e.g., Hibbertia subg. Pachynema, are mostly the prophylls of singleﬂowered sympodia, and the leaves of Hibbertioideae may represent heterotopic inﬂorescence bracts. As in some Dillenioideae, the β-prophyll is displaced onto the branch borne in its axil. Sympodia of other species of H. subg. Pachynema have several cataphyll-bearing nodes between the base of the branch and the ﬂower. Shoot systems in Hibbertia subg. Adrastaea are fundamentally similar, though they do not show metatopic displacement of the prophylls. In Dillenia spp., axillary buds are sometimes accompanied by two serial buds that are displaced (by concaulescence), sometimes a considerable distance up the stem. The foliage is typically evergreen, though in some Dillenia indigenous to parts of monsoonal Southeast Asia, it is deciduous. Young leaves exhibit conduplicate or plicate-conduplicate ptyxis. The petioles are usually distinct, and often have a broad, adaxial groove or channel. The bases of the petiolar wings completely ensheath the stem in Acrotrema, Davilla alata and allied species, Didesmandra, Dillenia spp., and Schumacheria. These petiolar wings, which may be persistent or caducous, enclose the developing terminal bud; they do not receive an independent trace from the cauline stele, and are not stipular (Dickison 1969). In all subfamilies except Hibbertioideae, higher orders of leaf venation are typically very regularly organized; rigidly percurrent, scalariform tertiary venation and well-developed areoles, oriented with the lower orders of venation, are common. Leaf venation in Hibbertioideae is distinctly less organized; percurrent tertiaries are rare and never rigidly scalariform, and areolation is typically incomplete or lacking (Rury and Dickison 1977). Ericoid leaves are characteristic of many species of Hibbertia subg. Hemistema and the H. hemignosta complex (sect. Candollea, subg. Hibbertia: Wheeler 2004a). Vestiture type and density, and leaf texture and degree of toothing may differ between juvenile and adult foliage (Hoogland 1952; Veillon 1990; Toelken 1998). In Hibbertia spp. and Dillenia spp. growing in ﬁre-prone ecosystems, a reversion to juvenile growth is characteristic of ﬁre sprouts. Vegetative Anatomy. The primary stem anatomy is generally characterized by a uniseriate

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epidermis, a cortex composed of large, thinwalled parenchyma cells, a continuous cylinder of perivascular ﬁbers and sclereids (absent or scanty in Acrotrema, Didesmandra, Hibbertia spp., and Tetracera spp.), a cylinder of discrete, collateral vascular bundles (or complete vascular cylinder, due to early cambial initiation in Acrotrema, Doliocarpus, Hibbertia, and Tetracera spp.), and a pith containing large, thin-walled parenchyma cells and often also (sometimes mostly) sclerenchymatous idioblasts (Dickison 1970b). Throughout the ground tissue of the stem occur raphid idioblasts and cells with dark-staining contents. Periderm initiation is typically deep-seated, but is sub-epidermal in Dillenia and one Doliocarpus. Nodes are uniformly trilacunar in Delimoideae, multilacunar (7–27) or trilacunar (Sri Lankan Acrotrema) in Dillenioideae, mostly pentalacunar (with a few spp. 3- or 7-lacunar) in Doliocarpoideae, and uni- or trilacunar in Hibbertioideae; there is one trace per gap. Cotyledonary nodes are unilacunar, two trace, except in Hibbertia, where they are unilacunar, one trace. Dickison (1969) describes petiole anatomy; patterns of petiole vasculature correlate poorly with both nodal type and family-level phylogeny. Leaves are bifacial. The adaxial epidermis is siliciﬁed in Curatella, Davilla spp., Didesmandra, Dillenia spp., and Tetracera spp., and in species of Hibbertia subg. Hemistema, it may be scleriﬁed as well (Dickison 1970a; Rao and Das 1979). Stomata are conﬁned to the abaxial leaf surface and are anomocytic, but in Didesmandra and Tetracera they are paracytic and in Acrotrema they are anisocytic; Hibbertia cuneiformis has cyclocytic stomata. In Hibbertia, stomata may be conﬁned to crypts, or in species with ericoid leaves, conﬁned to two longitudinal grooves, the lamina being recurved almost all the way to the midrib. An adaxial hypodermis is present in Acrotrema costatum, Dillenia spp., and Hibbertia spp. Mesophyll is differentiated into a palisade layer 1–3(4) cells thick and a spongy layer. Leaves have an unusually diverse array of idioblasts, especially in Hibbertia. Raphid idioblasts occur in all genera except Schumacheria; calcium oxalate crystals also occur as crystal sand and cuboidal or prismatic crystals. Silica bodies are reported from Curatella, Davilla, Doliocarpus, Hibbertia, and Tetracera. Cells described as ‘mucilaginous’ or ‘secretory’, but with uncharacterized contents, occur throughout the family. Tracheoidal or sclerenchymatous idioblasts surround free-

ending veinlets in many species of Hibbertia (Rao and Das 1979). Trichomes are commonly scleriﬁed, and are occasionally encrusted with silica as well; they are of three basic types. 1. Simple, unicellular trichomes are present in all genera; in Dillenia, they are frequently papillate and highly siliciﬁed. Simple trichomes in Acrotrema are sometimes uni- or multicellular, and raised on a pedestal of enlarged, epidermal cushion cells. 2. Fasciculate trichomes occur in Curatella (Fig. 38), Didesmandra, many species of Hibbertia subg. Hemistema, and Tetracera sect. Tetracera. In species included here in Hibbertia subg. Hemistema (cf. Wheeler 2002), the vestiture consists of (in part) trichomes that are stalked and multiradiate to truly peltate. 3. Short-stalked, glandular trichomes occur on the abaxial leaf surfaces of Dillenia philippinensis and D. reifferscheidia, and on the leaves and sepals of Acrotrema. For wood anatomy, see especially Dickison (1967a, 1979, 1984), Dickison et al. (1978), and BarettaKuipers (1972). Woods typically lack growth rings and are diffuse-porous (excepting a few xeromorphic Hibbertia spp.). Vessels are predominantly exclusively solitary. Vessel elements range in dimension from c. 70–120 × c. 1,740–2,610 µm in

Fig. 38. Dilleniaceae. Curatella americana, various forms of fasciculate hairs on lower leaf surface, ×400. (Photograph K. Kubitzki)

Dilleniaceae

Schumacheria to c. 150–450 µm × c. 690–1,250 µm in Doliocarpus. Tyloses are infrequently present in the vessel elements of Dillenia spp. only. Intervascular pitting is mostly sparse; pits are circular to elongate, without vestures, and are mostly opposite to transitional (sub-alternate) in arrangement. Perforation plates are exclusively scalariform in Dillenioideae, with 5–160 bars that are completely bordered and occasionally branched. In Hibbertioideae, perforation plates are predominantly scalariform, with 2–42 bars that are frequently branched; simple plates rarely occur, mixed with scalariform plates with few bars, in the woods of a few Hibbertia indigenous to regions with arid climates. In Delimoideae and Doliocarpoideae, perforation plates are mostly simple, with scalariform (1–20 bars, usually less than 10; Doliocarpoideae) or reticulate (Delimoideae) plates occurring only in the smallest vessel elements of a given individual. Imperforate tracheary (‘ﬁber-tracheids’) are non-septate, thin- to thick-walled, and very short to very long (625–4,375 µm). These wood ﬁbers have distinctly bordered pits that are common on both radial and tangential walls, and frequently have slit-like, crossed, aperture pairs. Vasicentric tracheids occur in the woods of Tetracera. Axial parenchyma is mostly apotracheal diffuse. Rays are typically of two distinct sizes. The uniseriate rays are homocellular, consist of upright cells, and are 1–33 cells high. The multiseriate rays are heterocellular. The ray bodies consist of procumbent to square, infrequently upright, cells; the uniseriate ends are comprised of upright cells and are extended into long wings in Dillenioideae and Hibbertioideae, or in Delimoideae and Doliocarpoideae, may only be one or few cells high. Multiseriate rays vary in width from 1–13 cells in Delimoideae, to 18 cells in Dillenioideae, to 41 cells in Doliocarpoideae, and to 5 cells in Hibbertioideae; in height from 20–152 cells in Delimoideae, 14– 200+ cells in Dillenioideae, 32–500+ cells in Doliocarpoideae, and 7–34 cells in Hibbertioideae. Rays of the whole of Dilleniaceae frequently exceed 1 mm in height; rays of Doliocarpoideae commonly exceed 10 mm in height. The ray parenchyma contains raphid idioblasts in all genera, except possibly Schumacheria; in most New Caledonian Hibbertia, solitary silica bodies commonly occur as inclusions in ray parenchyma cells. Secondary xylem is without storied structure. In mature, secondary stems of probably all Doliocarpus, lianescent Davilla, Neodillenia, Pinzona, and many neotropical Tetracera, successive, con-

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centric cambia are initiated (apparently rather tardily) that produce interxylary cylinders of secondary phloem, conjunctive parenchyma, raphid idioblasts, islets of thick-walled, rather short sclereids, and in Tetracera, apparently ﬁbers as well. The early-formed secondary phloem of all genera is composed of sieve tube members, companion cells, scattered parenchyma cells with crystal inclusions, and phloem ray cells (Dickison 1970b). Sclerenchyma is absent. Sieve tube members are usually short (< 300 µm) in all genera of the family. Sieve plates are oblique to occasionally transverse in Delimoideae, Doliocarpoideae, and Hibbertioideae, with typically 2–5 sieve areas, or occasionally the sieve plate is simple. Sieve tube plastids are of the S-type. Inﬂorescence Structure. Inﬂorescences of Dilleniaceae are always determinate. It can be difﬁcult to understand the structure of these inﬂorescences because of the absence of prophylls (Doliocarpoideae), the production of only a single transverse prophyll (some Tetracera), the recaulescence of many bracts and prophylls (Didesmandra, Dillenia spp., Hibbertia spp., Schumacheria, Tetracera spp.), and the production of serial branches resulting in supernumerary ﬂowers or partial inﬂorescences (Didesmandra, Dillenia spp., Hibbertia spp.). Inﬂorescences of Delimoideae (Tetracera) are characteristically thyrsoids or double-thyrsoids with partial inﬂorescences consisting of cincinni or dichasia (Kubitzki 1970; sometimes modiﬁed and partly monochasial). Inﬂorescences are terminal and often also axillary, but then only in the axils of the most distal foliage leaves. In cincinni of many neotropical species of sect. Tetracera, one prophyll of each ﬂower is suppressed. In a few species, panicles, botryoids, or dichasia occur. Such inﬂorescences perhaps represent impoverished thyrsoids. Within Doliocarpoideae, the paniculate inﬂorescences of Davilla most closely resemble those of Tetracera. They are also both terminal and axillary. In many species, the partial inﬂorescences are composed of 3-ﬂowered paraclades, each of which is subtended by a bract. The ﬂowers within each paraclade are without prophylls, though the central ﬂower is terminal, and the whole triad appears to develop like a dichasium. Thus, the panicles of many Davilla are basically thyrsoids without prophylls. Subsequent ﬂushes of inﬂorescences may be produced on the primary inﬂorescence axis by accessory buds (to a limited

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extent in Davilla). In large-ﬂowered Davilla and in all other Doliocarpoideae, only a single ﬂower is produced in the axil of each inﬂorescence bract. In these other Doliocarpoideae, the inﬂorescences are never terminal (with one possible exception) and are mostly ramiﬂorous. At each node, subsequent ﬂushes of inﬂorescences are produced by accessory buds, with nodes producing up to two inﬂorescence ﬂushes a year for several years. The inﬂorescences of Curatella and Pinzona are panicles. The inﬂorescences of Doliocarpus are similar, though less-branched, and perhaps show a reductive trend from an impoverished panicle, to a botryoid, to a monad (Kubitzki 1971). Due to the large number of accessory buds produced by older, leaﬂess nodes of Doliocarpus stems, the inﬂorescences of this genus are often compound and appear distinctly fasciculate. In cincinnate inﬂorescences or partial inﬂorescences of Dillenioideae and Hibbertioideae, the β-prophyll is displaced onto the branch borne in its axil. Terminal and axillary thyrsoids with cincinnate partial inﬂorescences are characteristic of Didesmandra and Schumacheria castaneifolia; other Schumacheria spp. have axillary cincinni. Most Dillenia have terminal inﬂorescences, and in all species they are probably determinate. Cincinni (D. ferruginea and D. triquetra) and thyrsoids (D. albiﬂos and D. suffruticosa; Corner 1978) occur, though several species have few-ﬂowered cymose inﬂorescences that need further descriptive work. Solitary, terminal ﬂowers occur in several species with large ﬂowers and are probably impoverished but derived versions of other inﬂorescence types. The few deciduous species of Dillenia often bloom shortly before leaﬁng out, and produce their inﬂorescences in axillary or apparently sometimes terminal positions on lateral short shoots (Hoogland 1952). Inﬂorescences of Acrotrema are either solitary terminal ﬂowers or terminal (and sometimes also axillary), scapose cincinni. Hibbertioideae are characterized by the prevalence of terminal monads. Indeed, here whole plant architectures may be related to the inﬂorescence architectures of other subfamilies. Thus, many species of two subgenera of Hibbertia have branching that is prophyllate alone (cymose) for a substantial part of their growth. The case of H. subg. Pachynema has been mentioned (Vegetative Morphology). Species of this subgenus with terete axes show an abrupt, early transition from (1/3)2/5 phyllotaxis to 1/2 phyllotaxis. Prophylls are sometimes the only foliar organs of the adult plant body

(Wagner 1906b), which is made up of a compound thyrsoid or paniculate inﬂorescence. Thus, in H. conspicua, the partial inﬂorescences (paraclades of ﬁrst order) are sympodia that terminate in a ﬂower and bear only two prophylls. Hibbertia (Adrastaea) salicifolia, while a wiry scrambler and appearing very different from plants of H. subg. Pachynema, is similarly constructed. Plants undergo an initial phase of extension growth with long shoots producing leaves in a 2/5-spiral, and with ﬂowers conﬁned to (and terminal on) axillary short shoots. These long shoots eventually terminate in a ﬂower. Short shoots of second order may be borne in the axils of leaves of the original short shoots, or axillary branches may be long shoots of a second type, consisting of single-ﬂowered, 2-prophyllate sympodia. In Hibbertia subg. Hemistema and subg. Hibbertia, sympodia often have both an extended zone of vegetative growth with 2/5 phyllotaxis and frequently produce axillary ﬂowers, which obscures the inﬂorescence-like construction of their plant bodies. Exclusively prophyllate branching is absent as well. Inﬂorescences of these two subgenera are thus best considered to be terminal and/or axillary monads (or in aggregation, spiciform or corymbiform polymonads; Toelken 2000), though terminal cincinni and thyrsoids (with cincinnate partial inﬂorescences resulting from sylleptic, serial branches; Wagner 1906a) also occur in subg. Hemistema. Although no comprehensive study of inﬂorescence structure has been undertaken for Dilleniaceae, the limited investigation undertaken for the preparation of this treatment suggests that inﬂorescence structure is perhaps the most informative source of structural data enabling the diagnosis of clades above the genus level. Further study is clearly needed. Floral Morphology. Perianth aestivation is always imbricate, and in 5-merous ﬂowers is quincuncial. The calyx is persistent and slightly to substantially accrescent after anthesis, enclosing the fruit for at least the early stages of its development. However, in Curatella, Pinzona, and some Doliocarpus, the sepals reﬂex immediately after anthesis and are only slightly if at all accrescent. The corolla is often very showy, and, along with the androecium (and less often the gynoecium), has a prominent role in pollination. A few species of Hibbertia with monosymmetric androecia also have subtly monosymmetric corollas (e.g., H. hyperi-

Dilleniaceae

coides), but this is variable at the population level. Excepting the above, perianths of Dilleniaceae are polysymmetric. There is instability in merosity and frequent heteromery of the calyx and corolla in Delimoideae (Tetracera) and Doliocarpoideae, but the mostly uniformly 5-merous perianth in Dillenioideae and Hibbertioideae is probably derived. In Delimoideae, the calyx is typically 4–5-merous, with the number of petals often equal to the number of sepals. Several species of Tetracera, however, possess ﬂowers with an unequal calyx of two small outer sepals and three large inner sepals, and have only three petals alternating with the inner sepals. At least ﬁve species of Tetracera have a calyx of 7–15 helically arranged sepals; their corolla merosity (3–5) is apparently related to the number of orthostichies in the sepals. Doliocarpoideae are the most variable subfamily with respect to perianth merosity; heteromery is frequent. Within Dillenioideae and Hibbertioideae, deviations from pentamery are almost certainly derived. Calyces of 7–18 sepals occur in at least six species of Dillenia, while a corolla is absent in a few other species. While the calyx of Hibbertia is uniformly 5merous, in ﬁve New Caledonian species (formerly sect. Trisema) the corolla is often only 3-merous. The androecium has mostly 10–300 stamens, although a few Hibbertia have as few as 1–5, some Tetracera have 500, and Dillenia ovalifolia has up to 900 stamens. Polymerous androecia may be plesiomorphic for Dilleniaceae, and androecia with fewer than 11 stamens or greater than 200 stamens appear to be derived. Androecia of Delimoideae and Doliocarpoideae are uniformly polysymmetric. Constitutional androecial monosymmetry occurs in Dillenioideae (Didesmandra and Schumacheria) and Hibbertioideae (most species of Hibbertia subg. Hemistema), and is independently derived within each of these subfamilies. Except in a few Hibbertia species, this monosymmetry is conspicuous, manifested by the formation of only a single group (or 2 groups in Didesmandra) of fertile stamens between the gynoecium and the petal that is presented in the median plane of the ﬂower. Thus, the group(s) of fertile stamens is (are) presented either abaxially or (less commonly) adaxially. The androecium is always without staminodes in Delimoideae and Doliocarpoideae, whereas in many species of Dillenioideae (many Dillenia) and Hibbertioideae (species of all subgenera of Hibbertia except Adrastaea), there are also staminodes. Staminodes are ± ﬁlamentous in form (infre-

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quently with a vestigial anther) and are as long as to, commonly, much shorter than the fertile stamens. In polysymmetric androecia, staminodes are most commonly external to the stamens, though in some species of Hibbertia subg. Pachynema and Dillenia fagifolia they are internal. In species of Hibbertia subg. Hemistema with monosymmetric androecia, staminodes may be external to the group of fertile stamens (e.g., sect. Hemistema), lateral to them (numerous spp.), or may partly or entirely encircle both androecium and gynoecium as a ± uninterrupted ring (e.g., H. hypericoides, H. spicata). The stamens are characteristically entirely free. In polysymmetric androecia, the stamens are evenly distributed around the gynoecium, either arranged without apparent order or distinctly antesepalous. In Hibbertia (subg. Adrastaea) salicifolia alone, the androecium is obdiplostemonous (Tucker and Bernhardt 2000; cf. Baillon 1865). Androecia sectoralized into stamen fascicles the members of which are free occur in Acrotrema spp., and in both polysymmetric- and monosymmetricﬂowered species of Hibbertia. More commonly, there is basal to nearly complete connation of the ﬁlaments in each fascicle, as in Didesmandra, Hibbertia (many species of subg. Hemistema and most species of subg. Hibbertia sect. Candollea), and Schumacheria. A single stamen fascicle occurs in many species of Hibbertia subg. Hemistema and in Schumacheria; there are two fascicles in Didesmandra and three or ﬁve fascicles in Hibbertia sect. Candollea. In Hibbertia salicifolia and some species of both subg. Hibbertia and subg. Pachynema, the ﬁlaments of the outer whorl of stamens are basally connate, forming a short tube. Stamens of all Dilleniaceae have clearly differentiated anthers and ﬁlaments. Filaments are typically terete and vary from being c. 10× shorter than the anthers, as in some Dillenia, to c. 10× longer than the anthers, as in a few species of Tetracera and Davilla. The ﬁlaments of Tetracera gradually dilate in their distal 1/4, grading into the connective. In Hibbertia subg. Pachynema, ﬁlaments may be dorsiventrally ﬂattened (H. conspicua), or frequently have an expanded, bulbous base that distally abruptly tapers into a narrow, terete cylinder. Anthers are always basiﬁxed, dithecal and tetrasporangiate. They commonly dehisce via latrorse or (infrequently) introrse longitudinal slits, but in Dillenioideae and Hibbertioideae anther dehiscence is frequently via apical pores or clefts. The apically porose anthers in many Dillenia are extrorse (Endress 1997; but not always, cf. Hoogland 1952).

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Anthers range from slightly wider than long and c. 1 mm in length in Tetracera spp. to the narrow, linear anthers of some Dillenia that are over 20 mm in length. In Tetracera and many Doliocarpoideae (especially Davilla), the anther connective is laterally broadened, separating the thecae especially toward the base. Other Doliocarpoideae (Curatella; some spp. of Doliocarpus sect. Doliocarpus, especially D. grandiﬂorus and D. magniﬁcus; Neodillenia) have anthers with parallel thecae and a rather narrow connective, and approach in form those of Hibbertioideae and Dillenioideae. These latter nearly all have parallel thecae (slightly basally divergent in a few Hibbertia subg. Pachynema) and narrow connectives. In Didesmandra, Dillenia spp., Hibbertia spp, Tetracera spp., and Schumacheria, the connective apically protrudes as a short mucro. In many Dillenia, there is an internal group of stamens (which are reﬂexed in bud) with anthers that are much longer and sometimes differently colored than those of the external stamens. In several New Caledonian Hibbertia (Veillon 1990), the internal stamens have large, often red or lavender, falcate anthers that are distinctly larger than the ± straight, often yellow anthers of the outer stamens, while in Didesmandra each stamen fascicle consists of one large stamen with a long, apically uncinate anther and four smaller stamens with comparatively short, straight or slightly curved anthers. The gynoecium is characteristically apocarpous and hypogynous, and excepting Dillenia, nearly always consists of 1–5 carpels; the gynoecia of Dillenia (with (4)5–15(–20) carpels), Hibbertia grossulariifolia (with (5–)10(–15) carpels), and some populations of H. scandens (with up to 7–8 carpels) are clearly derived. Carpels are arranged in a single whorl, except in Hibbertia grossulariifolia, where two distinct whorls are present (Tucker and Bernhardt 2000). Carpels are most frequently entirely free or shortly basally connate in the ascidiate region of each carpel; there is no compitum. However, the gynoecia of Acrotrema, Curatella, many (perhaps all) Dillenia, and Pinzona are hemisyncarpous – a syncarpous zone occurs where pollen tubes may cross between carpels. Stylodia are always free, and are erect, or in some Dillenia and Hibbertia, are laterally exserted. In Dillenia and also apparently Hibbertia baudouinii (Wilson 1965), the carpels are basally adnate to the ﬂoral receptacle, which is conical in the region of the gynoecium and often apically protrudes from the center of the whorl of carpels. Endress (1997) interprets this as a byproduct

of a secondary increase in carpel number. The ﬂowers of Hibbertia grossulariifolia, H. lasiopus, H. miniata, H. montana, and H. quadricolor (all immediately related; J.W. Horn, unpubl. data) are perigynous. The carpels have a very short ascidiate zone and a large, well-developed symplicate zone. The ventral suture of each carpel, which is always conspicuous and extends to the tip of (or sometimes just below) the stylodium, is sometimes not fully (morphologically) sealed (Dickison 1968). The stigma is punctiform, minute, and not differentiated in shape from the stylodium (or rarely minutely capitate) in Dillenioideae and Hibbertioideae. Stigmas of Doliocarpoideae are peltate, the even margin being interrupted only by the ventral suture of the carpel. In Delimoideae, stigmas are mostly punctiform or otherwise small and indistinct, though in a few neotropical Tetracera they are peltate, but with irregular, somewhat jagged margins. Placentation is submarginal with ovules in two (sometimes four in Dillenia, or to six in Tetracera; Dickison 1969) vertical rows when there are four or more ovules in each carpel. Species with only 1–2 ovules per carpel have basal placentation. Ovule number per carpel ranges from 1, as in Didesmandra and Schumacheria, to c. 80 in some Dillenia; Doliocarpoideae characteristically have two ovules per carpel. Ovules at anthesis are anatropous to campylotropous. When ovules are numerous, they are pleurotropous (borne sideways) and more or less syntropous (curved with the carpel margin). When there are 1–2 ovules per carpel, they are always erect and may be uniformly apotropous (abaxially curved), or, in most Doliocarpoideae, with one ovule apotropous and the other epitropous (adaxially curved). Flowers are oriented so that their median petal is abaxial. Carpels are opposite the petals when isomerous with the corolla, (commonly) median when two, and in 3-carpellate species of Schumacheria, the odd carpel is abaxial-median. The single carpel of many species of Davilla and Doliocarpus is variably obliquely oriented. While the bicarpellate gynoecia of Hibbertia subg. Adrastaea and subg. Pachynema are clearly median, species of subg. Hemistema with two carpels present their ﬂowers such that the carpels are transverse, as does Didesmandra. In fact, monosymmetric ﬂowers of Dilleniaceae are presented 90◦ from their true morphological orientation, the plane of symmetry of the ﬂower being transverse (cf. Eichler 1878); this is most clearly seen in species

Dilleniaceae

with cincinnate inﬂorescences. The obliquely oriented, bicarpellate gynoecia of Didesmandra may be caused by the loss of the (as presented) median carpel of an ancestrally 3-carpellate ﬂower, as in Schumacheria (Stebbins and Hoogland 1976) – indeed, Schumacheria and Didesmandra are sister taxa. However, the oblique orientation of the carpels in species of Hibbertia subg. Hemistema is independently derived there and is expressed late in development (Tucker and Bernhardt 2000). Floral Anatomy and Development. Sepals are (fundamentally) vascularized by three traces, with the lateral sepal traces commonly commissural, or there is a single trace from the stele that branches into three traces below the sepal base, or remains unbranched (some Hibbertia; Sastri 1958). Calyx vascularization in Delimoideae and Doliocarpoideae is frequently irregular (Wilson 1973). The petals are each vascularized by a single trace that is either fused with a commissural lateral sepal trace or is discrete. Androecial vasculature is typically discrete from that of the perianth, with the traces to the stamens almost always basally fused into (1–)3–15(–25) trunk bundles (Wilson 1937, 1965, 1973). The stamen trunk bundles typically branch 2–3 times, with the individual stamens or staminodes each receiving a single trace. Rarely, as in Hibbertia subg. Pachynema, each stamen receives its trace directly from the stele. Gynoecial vasculature is separate from that of the androecium, with each carpel characteristically vascularized by 3 traces – a single dorsal trace and 2 ventral traces. In Curatella and Doliocarpus spp., a pair of accessory ventral traces is present that supply the ovules. Ovules are otherwise vascularized by branches from the carpel ventrals, or in Didesmandra and Schumacheria, by vascular tissue remaining in the ﬂoral receptacle after the departure of the carpellary traces (Dickison 1968). In Dillenia spp. and Hibbertia spp., residual stelar tissue remains in the ﬂoral receptacle above or internal to the point where the carpel ventrals depart. Floral development is known mainly in Hibbertia and Dillenia (Endress 1997; Tucker and Bernhardt 2000; and references therein). The sepals are always spirally initiated (2/5 when 5), and in Dillenia, long plastochrons occur between the initiation of each sepal. The initiation of the corolla follows, with the petal primordia arising simultaneously or nearly so (many Hibbertia spp.), or initiated in the same phyllotactic spiral as the calyx (Dillenia; H. salicifolia). In species of Hibbertia subg.

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Hemistema with monosymmetric androecia, the three petals on the same side of the ﬂower as the fertile stamens are initiated before the two on the other side of the ﬂower. The innermost stamen primordia are typically next to arise, and are commonly antesepalous, though in species of Hibbertia subg. Hemistema with monosymmetric androecia, they are ± opposite the median petal. These ﬁrst stamen primordia appear on either a ring meristem (Dillenia, H. salicifolia, H. scandens) or on ± discrete, common primordia that may be spirally initiated (other polysymmetric-ﬂowered Hibbertia spp.; cf. H. perfoliata, Tucker and Bernhardt 2000). Additional stamen primordia are initiated centrifugally, with concomitant growth of the ﬂoral receptacle, increasing its diameter, in species with particularly large numbers of stamens. In Tetracera nordtiana, the developing androecium also has a minor centripetal zone, with a few stamen primordia arising in sequence toward the center of the ﬂower (Endress 1997). The carpel primordia initiate simultaneously (or in H. grossulariifolia, the internal carpel primordia after the external), most commonly when stamen primordia are being centrifugally initiated. In Tetracera, the carpel primordia arise prior to the initiation of individual stamen primordia (Corner 1946; Endress 1997). In monosymmetric-ﬂowered species of Hibbertia subg. Hemistema, the ﬁrst initiated stamen primordia arise as a ± terminal ridge on the ﬂoral apex. In fact, subsequent to the initiation of the corolla, the ﬂoral apex functionally splits in the transverse plane of the ﬂower (at least as the ﬂowers are presented). The side adjacent to the median petal gives rise to the primordia of the fertile androecium (sometimes also staminodes) and the other half gives rise to the carpel primordia (rarely also staminodes). Later in ﬂoral development, the stamens are either straight, contorted (most of the family), or become partly reﬂexed (several Dillenia species with a heterantherous fertile androecium, see above; Corner 1946; Hoogland 1952; Endress 1997) or wholly reﬂexed in bud (Doliocarpus sect. Doliocarpus, Kubitzki 1971). Embryology. Embryological investigations have focused on only three genera and few species (Paetow 1931; Swamy and Periasamy 1955; Rao 1957; Sastri 1958; Lakshmanan and Lakshmanan 1984; Imaichi and Kato 1996); Delimoideae and Doliocarpoideae are embryologically almost unknown. The immature microsporangium wall is 4–5 cell layers thick, and middle layers become

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crushed during development. The mature microsporangium wall is unusual in that the epidermal layer is always most prominent, the cells typically being tanniniferous or, at least, with dark-staining contents. The endothecium is often poorly developed; ﬁbrous thickenings are absent in Dillenia spp., inconsistently developed in Acrotrema arnottianum and several Hibbertia spp., but apparently consistently present in H. stricta. The tapetum is probably of the secretory type, and microsporogenesis is simultaneous. Pollen grains are shed as monads at the 2-celled stage. Anthetic ovules are anatropous to campylotropous, bitegmic, crassinucellate, and have a zigzag or, less often, exostomal micropyle. The outer integument is hood-shaped, and is 2–3 cells thick at anthesis. The inner integument is 3–4 cells thick at anthesis. Both integuments are thickened in the region of the micropyle. The raphe is often short, especially in Doliocarpoideae. Nucellar cells in the region of the chalaza retain their meristematic potential and continue to divide during a period from megagametophyte development to a point well after fertilization; this extended nucellar growth is probably primarily responsible for the eventual conspicuous curving of the ovule body. After fertilization, cells in the region of the raphe also continue to divide (becoming multinucleate in A. arnottianum, Swamy and Periasamy 1955), and this region grows inward against the nucellus and developing endosperm, which perhaps also helps effect the eventual curvature of the ovule body. Hence, post-anthetic ovules become truly amphitropous in all species examined. Spiral thickenings appear in cells of the outer epidermis of the inner integument at the time of fertilization, or shortly after. The mature megagametophyte is 7-celled and 8-nucleate, and its development is of the Polygonum type. The synergids are obpyriform in shape, or in Hibbertia, are hooked. The polar nuclei fuse before fertilization, and the three antipodal cells are ephemeral in Hibbertia and Dillenia. The primary endosperm nucleus divides before the zygote; endosperm formation is Nuclear. Embryogeny probably follows the Onagrad type. A zygotic mantle, formed by the swelling and structural modiﬁcation of the zygotic membrane, is reported from Acrotrema, Dillenia, and Hibbertia, and persists during early embryogeny, sometimes projecting with irregular, ﬁnger-like protuberances among the adjacent endosperm cells (Swamy and Periasamy 1955; Sastri 1958;

Ioffe and Zhukova 1974). This unusual elaboration of the zygotic membrane has been reported from all three genera embryologically examined, and is apparently restricted to the family. Pollen Morphology. Pollen grains are mostly spheroidal in shape, though they may vary from subprolate to suboblate. Grains vary in size from 15–34×16–32 µm, with the largest grains observed in Hibbertia stricta (34 × 32 µm), and the smallest in Schumacheria castaneifolia (15 × 16 µm; Dickison 1967b). Exine structure is tectate-perforate to semitectate, with ﬁnely punctate or foveolate to coarsely reticulate sculpturing. Exines of Davilla and Doliocarpus are the most coarsely reticulate, and very ﬁnely punctate exine sculpturing occurs in pollen of all subfamilies recognized here (Dickison et al. 1982). The tectum is typically well-developed, accounting for up to one-third of the total thickness of the exine, and lies above a layer of prominent, infratectal bacula. The foot layer and endexine region of the nexine (nexine 1 and 2) are often poorly differentiated from one another. The sexine is as thick as to c. 4× as thick as the nexine; the nexine is, however, considerably thickened in the region of the apertures in all taxa (Dickison et al. 1982). Viable pollen grains are triaperturate in all genera, except Didesmandra and Schumacheria in which the grains are mostly tetracolpate. Apertures of Delimoideae and Doliocarpoideae are compound (colporate), with mostly circular endoapertures that are sometimes poorly differentiated from the colpal membrane. Apertures in Dillenioideae and Hibbertioideae are simply colpate; endoapertures have evidently been lost in these two subfamilies. The length of the colpi varies from very short in some Dillenioideae to very long in some Doliocarpoideae. In the neotropical species of Tetracera, which are structurally androdioecious, the pollen is strikingly dimorphic (Kubitzki 1970). Plants bearing only staminate ﬂowers produce conventional tricolporate pollen, whereas plants with structurally perfect ﬂowers produce pollen that is indistinctly 5–8-pantoporate to nearly inaperturate (‘cryptoporate’) and always empty, obviously forming a deceptive attractant for the visitors of the functionally female ﬂowers. Pollination. Early investigations (Keighery 1975; Gottsberger 1977) suggested beetles were the primary pollinators of ﬂowers of individual species of Hibbertia, as well as those of Dilleniaceae as a whole. However, more recent work indicates that

Dilleniaceae

their ﬂowers are principally bee pollinated. As the ﬂowers are apparently uniformly without nectar, pollen serves as the sole reward. In Dillenia spp. and Hibbertia spp. with (at least functionally) apically porose anthers, bees actively remove pollen from the anthers via thoracic vibrations (Bernhardt 1984, 1986; Keighery 1991; Endress 1997; Tucker and Bernhardt 2000). In Hibbertia, bees sometimes also use their forelegs to scrape pollen from the anther pores (Bernhardt 1986). Tucker and Bernhardt (2000) outline four pollinator syndromes in Hibbertia that are related to the diverse ﬂoral architectures in this genus. Thus, although different species of Hibbertia (H. fasciculata and H. stricta) may be pollinated by bees of the same genus, pollen is deposited in different places on the bees’ bodies from where it is picked up by stigmas that intercept the bees on the appropriate parts of their bodies (Bernhardt 1996). Hence, variation in ﬂoral architecture among sympatric Hibbertia species may function as an interspeciﬁc isolating mechanism (Bernhardt 1996). While bees of the families Colletidae and Halictidae are apparently the primary pollinators of Hibbertia spp., pollen-eating ﬂies of the family Syrphidae may be secondary pollinators in some species (Bernhardt 1996; Tucker and Bernhardt 2000). Endress (1997) reports revolver ﬂowers and roundabout ﬂowers, correlated with two distinct pollination modes (both of which involve buzz pollination by Xylocopa bees) in Dillenia spp. (mostly observed in cultivation). Observations of the pollination biology of Dillenia spp. in native habitats also indicate visitation or pollination by bees (Apis, Ceratina, Melipona, and especially Xylocopa; summarized by Endress 1997; Momose et al. 1998). The scarce reports on pollination biology of other Dilleniaceae also indicate visitation by bees; Tetracera akara is visited by Apis koschevnikovii (Momose et al. 1998), and Davilla nitida is visited by Trigona sp. (Croat 1978). Fruit and Seed. Fruits are most commonly follicles or aggregates of follicles. In Dillenia spp. with dehiscent fruits and Acrotrema, the fruits may technically be considered capsules on account of the hemisyncarpous gynoecia of these genera. They are, however, probably best described as an aggregate of basally coherent follicles dehiscing along the ventral suture in Dillenia, or irregularly in Acrotrema. In several species of Dillenia, the pericarps remain dry while the accrescent sepals, which become ﬂeshy, form a tough, persistent envelope

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around the fruit (Fig. 48E, F); these are called pseudocarps (Hoogland 1952). In all species of Davilla, the function of the fruit wall, which remains very thin, is taken over by the two innermost sepals, which are accrescent and enclose the fruit completely like a pair of clam shells. The two accrescent sepals become distinctly cartilaginous and often turn orange at maturity; the whole accessory fruit thus resembling a globose capsule. Baccate or leathery, capsular fruits occur in Curatella and Pinzona. In these genera, the dorsal part of each carpel grows more than the ventral part, so in fruits nearing maturity, the stylodia are crossed. The fruits of Doliocarpus are also ﬂeshy, and are either ﬂeshy follicles that are dehiscent (sometimes irregularly) along both the dorsal and ventral portions of the carpel, or indehiscent and berry-like; the pericarps typically ripen red. In many species of Acrotrema, Dillenia, Hibbertia, and Tetracera, several seeds per carpel reach maturity, whereas in most other genera, carpels are 1–2-seeded. Funicular arils are present on the seeds of all genera. However, the aril is vestigial in many Dillenia spp. with indehiscent fruits and is represented only by a slight annular thickening on the funiculus. The cells of the aril of Acrotrema arnottianum are reported to be coenocytic (Swamy and Periasamy 1955). Arils are red, white, or (rarely) orange, ﬂeshy, and typically oily or waxy, or in many Hibbertia spp., are scarious, beige, and waxy. The margin of the aril varies from being deeply incised with long, thin laciniae (most Tetracera) to shallowly incised (many Dillenia, Hibbertia cuneiformis, and H. scandens), or is subentire to undivided in all other genera. The aril may be asymmetrical. Seeds are spheroidal to reniform and are characteristically of a lustrous black or dark brown color, owing to the presence of pigments and tannins in the exotesta. The exotesta of many New Caledonian Hibbertia is red. The testa is 2(–4) cell layers thick and is not multiplicative. The exotesta is always unligniﬁed and may be slightly pulpy or, in at least some Davilla and Dillenia spp., it dries up. In some Acrotrema and Dillenia, the exotesta is provided with slender, unicellular trichomes that may be mucilaginous. The principal mechanical layer of the seed coat is the endotesta, whose cells are heavily ligniﬁed and strongly pitted, or in some Hibbertia are heavily cutinized (Corner 1976; Schatral 1995). In Tetracera, the endotesta is poorly differentiated from other layers of the testa over much of the seed. Many of the cell layers of the inner integument of the ovule become crushed during seed

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development; hence, the tegmen is typically only 1–2(–4) layers thick. The exotegmen is distinctive as its cells have spiral or annuliform thickenings in all genera examined (i.e., a tracheidal exotegmen; Corner 1976; Vyshenskaya and Oganezova 1991). The chalaza is massive; its cells are often ligniﬁed or cutinized. The raphe is short. Endosperm is nuclear, abundant, ﬂeshy and oily, or in Hibbertia, also with starch granules. The embryo is straight, often very minute, and not fully differentiated when the seed is mature. Germination is phanerocotylar (Ozenda 1949).

if present at all (Hegnauer 1966). Betulinic acid, mostly accumulated in the bark, appears to be a regular feature of the family (Pavanasasivam and Sultanbawa 1974). The diversity of ﬂavonoids is high, and besides the common aglycones and glycosides, some unusual O-methylated compounds plus ﬂavonol sulphates have been found, the latter two, in a close association (Kubitzki 1968; Gurni and Kubitzki 1981). Relationships Within the Family. The principal characters used for earlier subdivisions of Dilleniaceae include anther structure (linear

Dispersal. Seed dispersal is probably mostly by animals. Birds probably disperse the arillate seeds produced by species of Delimoideae, Doliocarpoideae, and Dillenioideae with dehiscent fruits. The ornithochorous syndrome is well-displayed by many species of Dillenia and Tetracera, in which a red aril contrasts with the shining, black testa, and a follicle colored in a different red. In Curatella and Doliocarpus, the combination of the red color of the pericarp, white aril, and black testa provides a visual display that is also probably attractive to birds. Only few species of Hibbertia have red arils and are ornithochorous (H. scandens and H. cuneiformis), but many others are myrmecochorous (Berg 1975; Schatral et al. 1994). The large, indehiscent fruits of several Dillenia, which have accrescent sepals and lack arils, are eaten by mammals; D. indica, speciﬁcally, is often eaten and dispersed by elephants, but also transported by water. Reproductive Biology. Flowers of Dilleniaceae (despite their sometimes very large size) have a short period of anthesis, only one to few days (Endress 1997; Tucker and Bernhardt 2000). Hybridization within Hibbertia, and perhaps throughout the whole family, is apparently extremely rare (Toelken 1998; Tucker and Bernhardt 2000). Hibbertia hypericoides is protogynous, and this and other species of the genus are self-fertile, although autogamy does not seem to occur (Keighery 1975). The functional dioecy present in the neotropical species of Tetracera (see Pollen Morphology) enforces cross-pollination. The ﬂowers of Hibbertia hirsuta typically possess only a single stamen, and are probably cleistogamous. Phytochemistry. Polyphenols are prominent and diversiﬁed and include hydrolyzable tannins and ellagitannins, while alkaloids seem to be rare,

Fig. 39. Dilleniaceae. Summary tree of relationships in Dilleniaceae. The branches shown here have bootstrap support of ≥ 99% and Bayesian posterior probability values of 100%, except those indicated with a dashed line, where bootstrap values are < 70% and Bayesian posterior probability values are < 95% (from Horn 2005).

Dilleniaceae

vs. globose), leaf architecture (lateral nerves welldeveloped and often parallel vs. small, sometimes 1-nerved leaves), anther dehiscence (longitudinal slits vs. apical pores), and degree of carpel fusion (carpels entirely free vs. ± synovarious). Their application has led to three slightly different subdivisions: (1) that of de Candolle (1824), who recognized two tribes, Delimeae and Dillenieae, which Hoogland (1952) informally elevated to the rank of subfamilies; (2) that of Gilg and Werdermann (1925), into the tribes Tetracereae, Hibbertieae, Acrotremeae, and Dillenieae; (3) the division of Hutchinson (1964), who modiﬁed Gilg and Werdermann’s classiﬁcation by merging Acrotremeae into Dillenieae. Molecular phylogenetic data are highly informative as to the infrafamilial relationships of Dilleniaceae, and largely corroborate the classiﬁcations based on structural data mentioned above. Following Horn (2005; Fig. 39), Dilleniaceae are best divided into the subfamilies Delimoideae, Doliocarpoideae, Hibbertioideae, and Dillenioideae. Delimoideae, here taken to include only the genus Tetracera, are sister to the rest of the family. Doliocarpoideae, containing the neotropical endemic genera Curatella, Davilla, Doliocarpus, Neodillenia, and Pinzona, are sister to a clade containing the Old World genera. The Old World clade contains the sister clades Hibbertioideae, here taken to include only the broadly circumscribed Hibbertia (Adrastaea and Pachynema included), and Dillenioideae, containing Acrotrema, Didesmandra, Dillenia, and Schumacheria. Morphological circumscriptions of major clades of Dilleniaceae are indicated in the taxonomic section. Characters supporting hypotheses of relationship for both Didesmandra and Neodillenia, which were not available to include in the phylogenetic study, are also indicated in this section. The clade containing all genera of Dilleniaceae, exclusive of Tetracera, is strongly supported by molecular data (Horn 2005), but as yet no structural characters have been identiﬁed to diagnose this group. Afﬁnities. In previous systems of angiosperm classiﬁcation (Dahlgren 1983; Cronquist 1981, 1988; Takhtajan 1997; Thorne 2000), Dilleniaceae were accorded a position of great evolutionary importance as being, on one hand, directly liked with magnoliid dicots, and even more signiﬁcantly on the other, as being the progenitor of an entire radiation of dicots that were, in part, characterized by their centrifugal stamen initiation – the Dilleni-

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idae. Part of this confused notion is attributable to a problem that still stands: Dilleniaceae are one of the most isolated lineages of eudicots of which the relationship to other major eudicot lineages cannot (currently) be robustly supported by any source of character information. Dilleniaceae are currently most conservatively treated as an unresolved, early eudicot branch, and are accordingly contained within the monofamilial Dilleniales (APG II 2003). There is, however, a growing consensus of molecular data suggesting Dilleniaceae are sister to Caryophyllales (Soltis et al. 2003). Dilleniaceae and many Caryophyllales share deep-seated phellogen initiation, successive cambia, persistent calyces, and campylotropous ovules. Within Caryophyllales, Dilleniaceae are perhaps most similar to Rhabdodendraceae, probably sister to all other Caryophyllales (Cuénoud et al. 2002). Both families share the following character states of limited distribution among eudicots: leaf mesophyll containing silica bodies, a broad petiole with at least a somewhat sheathing insertion, anthers with a persistent, tanniniferous epidermis, and a seed coat with a tanniniferous outer epidermis and a layer or layers of cells developing spiral thickenings (for Rhabdodendraceae: Prance 2003). Distribution. Tetracera, the sole genus of subfamily Delimoideae, is the only genus with a pantropical distribution, as well as the only genus of the family present on continental Africa. Doliocarpoideae, containing 4–5 genera, are endemic to the neotropics, with a center of diversity in Brazil. Hibbertioideae are mostly endemic to Australia, and are the largest subfamily, perhaps containing more species than the rest of the family as a whole. Their distribution in Madagascar (1 sp.), New Caledonia (24 spp.), Fiji (1 sp.), and New Guinea (2 spp.) is the result of long distance dispersal, rather than vicariance (J.W. Horn, unpubl. data). Hibbertioideae have a signiﬁcant temperate distribution in southern Australia, and the Southwest Botanical Province of Western Australia is the region of greatest species richness for both the subfamily and, perhaps, for the entire family as well. Dillenioideae have a distribution from Madagascar and the Seychelles to Sri Lanka and southern and eastern India, to Southeast Asia and the Paciﬁc (northern Australia and Fiji). The distribution of Dillenia is equivalent to that of the subfamily. Schumacheria is endemic to Sri Lanka. Didesmandra is known from only

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a few populations in Sarawak, Borneo. Acrotrema contains seven species endemic to Sri Lanka, one species in the Western Ghats of India, and another ranging from southern Thailand and Myanmar to northern Sumatra. The biogeographic history of Dillenioideae is probably congruent with the out-of-India hypothesis (Ashton and Gunatilleke 1987; Conti et al. 2002). Key to the Genera 1. Fertile androecium exclusively on one side of the ﬂower 2 – Fertile androecium ± evenly distributed around the carpels 4 2. Stamens 10, grouped into 2 fascicles, each of 5 connate members; (fertile) androecium conspicuously heterantherous 8. Didesmandra – Stamens 1–c. 70, with fertile stamens clustered into a single fascicle; anthers ± isomorphic, stamen ﬁlaments free or fused 3 3. Carpels (2)3; staminodes 0; stamen ﬁlaments connate; anthers with ﬁne, simple hairs; ﬂowers in secund, cinncinate inﬂorescences or partial inﬂorescences 7. Schumacheria – Carpels 2; staminodes present or not; stamen ﬁlaments free or connate; anthers glabrous; inﬂorescences typically of a single ﬂower, or the few species with ﬂowers organized into secund, cinncinate inﬂorescences always bearing ﬂowers with staminodes 6. Hibbertia (p.p.) 4. Stigma peltate, the margin even and annuliform. Inﬂorescences terminal, axillary, or (frequently) ramiﬂorous, prophylls absent or (very rarely) minute. Aril always well-developed, entire or shortly and irregularly lacerate distally, typically ﬂeshy. Lianas and scandent shrubs, less commonly shrubs or tortuous trees 5 – Stigma punctiform, rarely minutely capitate, or if irregularly peltate (a few Tetracera), then the plants with terminal, prophyllate inﬂorescences and laciniate arils. Inﬂorescences commonly terminal; 1–2 prophylls/ﬂower. Arils well-developed or vestigial, ﬂeshy or scarious, entire to deeply ﬁmbriate or laciniate. Large trees to shrubs or lianas, rarely rhizomatous herbs 9 5. Sepals uniformly 5, the inner 2 opposite one another, deeply concave, and distinctly larger than the outer 3 ± ﬂattened sepals; the two inner sepals accrescent, enclosing the fruit completely; carpels 1–2(3); inﬂorescences terminal and axillary, a panicle, commonly with 3 ﬂowers per bract 2. Davilla – Sepals 2–7 (frequently 5), ± equivalent in size and shape, or if unequal, then the inner 2 sepals not as above, either all sepals are accrescent and ± surround the fruit, but never completely, or they reﬂex, becoming at most slightly accrescent; inﬂorescences axillary and/or (commonly) ramiﬂorous (very rarely terminal), a panicle (always with 1 ﬂower per bract), fascicle of panicles or botryoids, or rarely ﬂowers single; carpels 1–2(–5), gynoecium apocarpous or hemisyncarpous 6 6. Carpels 2, hemisyncarpous 7 – Carpels 1, rarely 2–5, the carpels free or at most shortly synovarious 8

7. Small to medium-sized, tortuous trees; hairs both simple and fasciculate; carpels with long, persistent, hispid hairs; aril white 3. Curatella – High-climbing lianas; hairs simple only (plants often mostly glabrous); carpels glabrous; aril orange 4. Pinzona 8. Aril white; carpel 1(2); inﬂorescences exclusively axillary and ramiﬂorous 5. Doliocarpus – Aril red; carpels 1–5, if carpel 1, then the inﬂorescence terminal 5a. Neodillenia 9. Anthers with a conspicuously expanded connective separating the thecae; thecae basally outwardly divergent; stamen ﬁlaments increasing in thickness in distal 1/4, grading into the connective 1. Tetracera – Anthers with a narrow connective, the thecae often immediately next to one another and always parallel; stamen ﬁlaments of even thickness throughout their lengths, or rarely with an expanded and bulbous base and then abruptly narrowing 10 10. Rhizomatous herbs with a single rosette of leaves at ground level, or uncommonly with a short, aerial nonphotosynthetic stem that is densely pubescent and terminated by a rosette of leaves 9. Acrotrema – Large trees to small shrubs, or rarely subshrubs or lianas; if plants are subshrubs, then the above ground axes are green and photosynthetic, ephedroid or conspicuously ﬂattened, and appearing leaﬂess 11 11. Portion of ﬂoral receptacle bearing the carpels conical; carpels (4)5–15(–20), gynoecium hemisyncarpous; petiole bases with 7 or more vascular bundles; leaves moderate in size to typically large and broad (never long and strap shaped), with ± straight, parallel secondaries and frequently regularly percurrent tertiaries; areoles typically well-developed 10. Dillenia – Portion of the ﬂoral receptacle bearing the carpels ﬂat, or if conical, then the leaves long and strap-shaped; carpels 1–5(–15), entirely free, or at most shortly synovarious; petiole bases (or lamina bases if blade is sessile) with 1 or 3 vascular bundles; leaves of moderate to very small size, sometimes ericoid, uncommonly (mostly) only scale-like and the plant appearing leafless; tertiary venation rarely percurrent and never regularly so; areoles typically poorly developed 6. Hibbertia (p.p.)

Genera of Dilleniaceae Plesiomorphic states: Vessel elements with mostly simple perforation plates. Multiseriate wood rays with uniseriate ends both fewer and greater than 4 cells in height (Kribs Type I and IIA). Leaves without completely amplexicaul petiolar wings, but sometimes the leaf insertion with a broad, slightly sheathing petiolar ﬂange. Venation craspedromous or semicraspedromous; the secondaries ± straight and parallel, the tertiaries rigidly percurrent and scalariform, areoles well-developed. Vestiture exclusively of simple, unicellular trichomes. Inﬂorescences termi-

Dilleniaceae

nal, determinate, not branching from the previous ﬂush via proleptic proliferation buds. Androecium polysymmetric. Functional pollen grains tricolporate. Gynoecium apocarpous, or only very shortly synovarious by the ascidiate region of each carpel and without a compitum. Stigmas small and punctiform, not differentiated in shape from the stylodia. Fruit a follicle or aggregate of follicles.

I. Subfam. Delimoideae Burnett (1835). 1. Tetracera L.

Fig. 40

Tetracera L., Sp. Pl. 1:533 (1753); Hoogland, Reinwardtia 2:185–224 (1953), rev. Australasian spp.; Kubitzki, Mitt. Bot. Staatssamml. München 8:1–98 (1970), rev.; Hoogland, Fl. Thailand 2, 2:95–108 (1972); Aymard in Fl. Venez. Guayana 4:671–685 (1998).

Lianas or scandent shrubs, rarely lignotuberous subshrubs; mature, secondary stems often with successive cambia; small vessel elements with reticulate plates; nodes uniformly trilacunar, 3-trace; stomata paracytic; trichomes often fasciculate. Plants synoecious or functionally dioecious. Inﬂorescences mostly both terminal and in the axils of the upper foliage leaves, very rarely exclusively axillary, with (1–)3–150(–200+) ﬂowers, a thyrsoid or double thyrsoid with either (modiﬁed) dichasial or cincinnate partial inﬂorescences, rarely a dichasium or impoverished

panicle; prophylls 1–2/ﬂower; sepals (3)4–5(–15), free, unequal to equal; petals 3–5; stamens 50– 200(–500), free; anthers with a short, mucronate appendage or not; the connective emarginate or not; carpels 1–5(–8), glabrous or pubescent; stigmas infrequently irregularly peltate with jagged margins; ovules 2–20, pleurotropous and syntropous, in 2(4, 6) submarginal rows. Follicles pyriform. Seeds 1–6 per follicle, arillate; aril ﬂeshy, red (drying beige), ± evenly ﬁmbriate or laciniate in its distal (1/8–)1/3 to (more commonly) nearly its full length. n = 12. About 50 species, southern Mexico to Paraguay, Antilles, equatorial Africa, Madagascar, Sri Lanka and southern India, Southeast Asia to northeastern Australia, New Caledonia; most speciose in Brazil. Section Tetracera with many-ﬂowered thyrsoids with cincinnate partial inﬂorescences, small petals, and both simple and fasciculate trichomes; pantropical; sect. Akara Kubitzki with few(up to 12)-ﬂowered thyrsoids, large, emarginate petals, and exclusively simple trichomes; Old World. II. Subfam. Doliocarpoideae J.W. Horn (2005). Smaller vessel elements with scalariform plates, commonly with fewer than 10 bars; rays extremely high, often > 10 mm, some with uniseriate ends 1 or few cells high. Mature secondary stems producing successive cambia (except Curatella and perhaps also suffruticose Davilla spp.). Nodes (3)5(7)-lacunar; nodes bearing inﬂorescence axes, or in Davilla the primary inﬂorescence axis itself, producing subsequent ﬂushes of inﬂorescences via proleptic proliferation buds. Inﬂorescences without prophylls, or prophylls irregularly produced in a few large-ﬂowered species of Davilla; stigma conspicuously peltate, the margin annuliform and even; ovules 2 per carpel, typically 1 epitropous and 1 apotropous but the direction of ovule curvature variable among ﬂowers of a given individual. When gynoecium apocarpous, fruits or partial fruits globose. Aril margin mostly entire; ﬂeshy. 2. Davilla Vand.

Fig. 40. Dilleniaceae. Tetracera boiviniana. A Flowering branch. B Stamens. C Gynoecium, vertical section. D Carpel, transverse section. E Fruit. F Arillate seed. (Gilg and Werdermann 1925)

145

Fig. 41

Davilla Vand., Fl. Lusit. Brasil.: 35 (1788); Kubitzki, Mitt. Bot. Staatssamml. München 9:1–105 (1971), rev.; Aymard in Fl. Venez. Guayana 4:671–685 (1998).

Scandent shrubs or lianas. Leaves sometimes with amplexicaul petiolar wings. Inﬂorescence a pani-

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abaxial sides of the carpels. Sepals reﬂexing after anthesis and hardly accrescent. 3. Curatella Loeﬂ.

Fig. 38

Curatella Loeﬂ., It. Hispan.: 260 (1758); Kubitzki, Mitt. Bot. Staatssamml. München 9:1–105 (1971), rev.

Fig. 41. Dilleniaceae. Davilla ﬂexuosa. A Flowering branch. B Petal. C Androecium and gynoecium. D Stamen. E Carpel, vertical section. F Same, transverse section. G Fruit enclosed by inner sepals. H Same after removal of one sepal. I Arillate seed. (Gilg and Werdermann 1925)

cle with ultimate paraclades of triads or (less often) monads, never ramiﬂorous; sepals 5, free, the innermost 2 deeply concave, oppositely arranged, conspicuously larger than the ± ﬂattened outer 3, and prominently accrescent; petals (3–)5; stamens 25–300, free; carpels 1–2(3). Fruit irregularly dehiscent, with very thin, papery walls, completely and indeﬁnitely enclosed by the inner 2 accrescent sepals. Seeds partially or completely enclosed by a membranous, white aril. About 25 species, from southern Mexico to southern Brazil, Bolivia, and Paraguay; Antilles. Section Homalochlaena Kubitzki, inner sepals with their margins pressed against each other; sect. Davilla, innermost sepals with reﬂexed margin and overlapped at margin by the second innermost sepal.

A small to medium-sized tree. Vestiture also including fasciculate trichomes. Leaves coarsely scabrous, owing to the presence of siliciﬁed epidermal cells and trichomes. Sepals (3)4(5), subequal, free; petals (3–)5, the median petal adaxial, or occasionally reduced or missing; stamens c. 80, free; carpels covered with fasciculate and hispid, simple trichomes. Pericarp outer surface green, inner surface scarlet. Seed completely enclosed by a membranous to slightly ﬂeshy white aril. n = 13. One species, C. americana L., a tortuous savanna tree widespread from southern Mexico to southern Brazil and Bolivia, Antilles. 4. Pinzona Mart. & Zucc. Pinzona Mart. & Zucc., Abh. Math.-Phys. Kl. Königl. Bayer. Akad. Wissensch. 1:371 (1832); Kubitzki, Mitt. Bot. Staatssamml. München 9:1–105 (1971), rev.; Aymard & Miller, Candollea 49:169–182 (1994).

A high-climbing liana, largely glabrous at maturity except for inﬂorescence axes. Sepals 3–4, subequal, shortly basally connate; petals (2)3; stamens 25–35, free; carpels glabrous. Seed completely enclosed within a ﬂeshy orange aril. One species, P. coriacea Mart. & Zucc., throughout Central and South America from Belize to northeastern Brazil; Antilles. 5. Doliocarpus Rol.

Other Doliocarpoideae: Inﬂorescences exclusively axillary and (mostly) ramiﬂorous (possibly terminal in one Neodillenia sp.). Fruits with ﬂeshy or leathery, typically brightly colored pericarps.

Curatella + Pinzona: Leaf lamina decurrent on the petiole. Inﬂorescence a panicle. Gynoecium hemisyncarpous; carpels 2. Fruit a ﬂeshy or leathery capsule, the stylodia crossing as the fruit matures on account of an unequal amount or rate of growth between the adaxial and

Doliocarpus Rol., Kong. Svenska Vetensk. Acad. Handl. 17: 260 (1756); Kubitzki, Mitt. Bot. Staatssamml. München 9:1– 105 (1971), rev.; Aymard & Miller, Candollea 49:169–182 (1994); Aymard, Anales Jard. Bot. Madrid 55:17–30 (1997); Aymard in Fl. Venez. Guayana 4:671–685 (1998).

Shrubs, mostly scandent, or lianas. Inﬂorescence a panicle, botryoid, or uncommonly a monad; the inﬂorescences at each node often appearing fasciculate due to the large number of accessory buds produced; sepals 3–6, free; petals 3–7; stamens c. 25– 250, free; carpel 1(2). Fruit typically ripening red, baccate, dehiscing along both the dorsal and ventral side of the carpel (sometimes irregularly so), or indehiscent and berry-like. Seeds with a ﬂeshy, entire, white aril. About 45 species, from southern Mexico

Dilleniaceae

and the Antilles to southern Brazil and Paraguay, with the center of species diversity in Brazil. In sect. Calinea Eichl., the stamens are straight to slightly contorted in bud; in sect. Doliocarpus, the stamens are all reﬂexed in bud.

Genus dubium 5a. Neodillenia Aymard Neodillenia Aymard, Harvard Pap. Bot. 10:121–131 (1997); Aymard in Fl. Venez. Guayana 4:671–685 (1998).

Lianas with successive cambia. Trichomes simple. Inﬂorescences axillary (and sometimes also ramiﬂorous) and consisting of a solitary ﬂower or botryoid, or terminal and consisting of a solitary ﬂower or impoverished panicle (botryoid). Flowers large; sepals 3–6, unequal; corolla unknown; stamens 80–300, free; gynoecium apocarpous or merely shortly synovarious of (1)2–5 carpels; ovules (1)2 per carpel, said to be orthotropous (but, confusingly, also with a ventral raphe), though in N. peruviana Aymard they are clearly campylotropous, with one ovule epitropous and the other apotropous in each carpel. Seeds enclosed in a ﬂeshy, entire, red aril. Fruit an aggregate of follicles, unknown in N. venezuelana Aymard. Three species, in the Amazonian regions of Colombia, Ecuador, Peru, and Venezuela. Note that the stamens are entirely free (not shortly basally connate into a ring) and the ovules campylotropous (not orthotropous, cf. the orig. description). Neodillenia is clearly a member of subfamily Doliocarpoideae, as evidenced by its successive cambia, conspicuously peltate stigma with an even, annuliform margin, and ovular details. Neodillenia coussapoana and N. peruviana appear to be closest to large-ﬂowered species of Doliocarpus sect. Doliocarpus, particularly D. grandiﬂorus and D. magniﬁcus. The anther connectives of Neodillenia are of the same thickness as those of Doliocarpus magniﬁcus and contain abundant raphid idioblasts, like Doliocarpus anthers. The only features that keep these two species separated from Doliocarpus are their red arils and gynoecia with typically 4–5 carpels. The monocarpellate N. venezuelana would be readily referable to Doliocarpus, except that it (apparently) has terminal inﬂorescences. Further work is needed to clarify both the structure and phylogenetic position of these plants.

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Rest: Vessel elements with exclusively scalariform perforation plates, or rarely also with few simple plates in a few xeromorphic Hibbertia species. Multiseriate wood rays with uniseriate ends always extended into long wings 4 or more cells in height (Kribs Type I). When inﬂorescences consisting of more than 1 ﬂower, the β-prophyll often displaced onto the branch borne in its axil. Perianth nearly always 5-merous. Pollen grains uniformly with simple, colpate apertures, typically 3-aperturate. III. Subfam. Hibbertioideae J.W. Horn (2005). 6. Hibbertia Andrews

Figs. 42–44

Hibbertia Andrews, Bot. Rep.: t. 126 (1800); Bentham, Fl. Austral. 1:17–41 (1863); Hoogland, Fl. Males. I, 4:141–174 (1951); Stanley in Stanley & E.M. Ross, Fl. SE Queensland 1:185–189 (1983); Jessop in Jessop & Toelken, Fl. S. Australia 4th edn, 1:354–358 (1986); J.R. Wheeler in N.G. Marchant et al., Fl. Perth Region 1:119–133 (1987); G.J. Harden & J. Evrett in G.J. Harden, Fl. New South Wales 1:293–303 (1990); Veillon in Fl. Nouv.-Caléd. Dépend. 16:3–86 (1990); Craven & Dunlop, Austral. Syst. Bot. 5:477–500 (1992), rev. of subg. Pachynema, p.p.; Wheeler in Fl. Kimberley Region 151–155 (1992); Toelken in Walsh & Entwisle, Fl. Victoria 3:300–313 (1996); Lewington & Cobb in Grieve, How to know Western Australian wildﬂowers, 2nd edn, 2:35–56 (1998); Murray in Fl. New South Wales suppl. 1:32–36 (2000); Wheeler in Fl. South West: Bunbury-Augusta-Denmark 2:570–579 (2002); Wheeler, Nuytsia 15:311–320 (2004), key to W. Austral. spp. Hemistema Thouars (1804). Candollea Labill. (1806). Pleurandra Labill. (1806). Adrastaea DC. (1817). Pachynema R. Br. ex DC. (1817). Trisema Hook. f. (1857).

Shrubs, uncommonly small to medium-sized trees, or subshrubs, sometimes rhizomatous, with mostly or only cataphylls and with photosynthetic function transferred to the stems, rarely vines or lianas; nodes 1- or 3-lacunar. Leaves frequently ericoid, sometimes also with fasciculate, rarely peltate trichomes; venation semicraspedromous to brochidodromous, very rarely craspedromous, secondaries only occasionally parallel, and tertiaries rarely percurrent and never scalariform; areolation typically incomplete or lacking. Inﬂorescence commonly a monad, infrequently a cincinnus or thyrsoid with serial,

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cincinnate partial inﬂorescences, terminal and often also axillary, or infrequently apparently only axillary, uncommonly most of the plant body overtly inﬂorescence-like, and then a compound thyrsoid or panicle; sepals 5, unequal to ± equal, free or shortly fused; petals (3–)5, free; androecium of (1–)5–100(–300+) members, sometimes partly staminodial, basically polysymmetric or monosymmetric; polysymmetric androecia with the stamens all free, rarely all shortly basally connate, and ± evenly distributed around the carpels, or the stamens grouped into 3 or 5 distinct fascicles in which the stamen ﬁlaments may be all free, all shortly connate, or sometimes with 1 stamen free and the others in the fascicle connate; staminodes (when present) external to the fertile stamens, or (rarely) internal (subg. Pachynema); monosymmetric androecia always have the fertile stamens presented in the median plane of the ﬂower and exclusively opposite the median petal, where they are free or fused into a single fascicle; staminodes, when present, external to and/or lateral to the fertile androecium, and uncommonly partly to entirely encircling the fertile stamens as a unit; anthers dehiscence via longitudinal slits or, sometimes, via apical pores; carpels 1–5(–10), glabrous or pubescent; ovules 1–25 per carpel. Seeds 1–8 per follicle; aril subﬂeshy or pulpy and oily or waxy, whitish, subentire, or rarely red and ﬂeshy. About 225 species, from Madagascar (1 sp.) to Fiji (1 sp.), c. 200 species in Australia incl. Tasmania, 24 species in New Caledonia, 2 species in New Guinea. The division into four subgenera, presented here, is strongly supported by both molecular and morphological data (Horn 2005; J.W. Horn, unpubl. data). 6a. Hibbertia subg. Pachynema (R. Br. ex DC.) J.W. Horn (2005). Fig. 42 Subshrubs, sometimes rhizomatous; true leaves (if present) conﬁned to basalmost nodes of a shoot, with craspedromous venation (the only instance of this within the genus); aerial axes green and photosynthetic, often caespitose and sometimes dimorphic, provided with mostly or (typically) only cataphylls. Inﬂorescence (which constitutes nearly the whole of the shoot system) a compound thyrsoid or panicle, commonly with serial branches or ﬂowers; androecium typically bicyclic, with an outer whorl of 7(–10) fertile stamens and an inner whorl of 2 stamens or staminodes in the transverse plane of the ﬂower; infrequently the androecium unicyclic and

Fig. 42. Dilleniaceae. A Hibbertia (subg. Pachynema) dilatatum, ﬂowering shoot. B Hibbertia (subg. Pachynema) junceum, ﬂowering shoot. C–F Hibbertia (subg. Pachynema) complanatum. C Flower bud. D Same seen from below. E Flower. F Androecium and gynoecium, vertical section. (Gilg and Werdermann 1925)

consisting of 4–5 stamens, apparently by reduction; carpels 2, ovules 2 per carpel. n = 12; 2n = 30. Nine species, including all species recognized by Craven and Dunlop (1992) in Pachynema, plus Hibbertia conspicua (Harv.) Gilg and H. goyderi F. Muell., in Australia, mostly conﬁned to the Northern Territory (especially the Arnhem Plateau) and adjacent regions of the Kimberley of Western Australia, and in the Geraldton sandplains of the Southwest Botanical Province of Western Australia. 6b. Hibbertia subg. Hemistema (Thouars) J.W. Horn (2005). Fig. 43 Small shrubs to medium-sized trees; mature axes non-photosynthetic. Leaves moderately large and broad to (frequently) small and ericoid; vestiture frequently also including fasciculate trichomes (sometimes only), or infrequently including multiradiate to peltate trichomes. Inﬂorescence commonly a terminal monad (often also axillary, or terminal on sometimes exclusively axillary short shoots), less often a terminal (and also often axillary) cincinnus or thyrsoid; androecium monosymmetric or less frequently polysymmetric and then the stamens not aggregated into either clearly deﬁned cycles or fascicles; carpels basi-

Dilleniaceae

Fig. 43. Dilleniaceae. Hibbertia (subg. Hemistema) baudouini. A Flowering branch. B Androecium spread out and gynoecium. C Stamen. D Carpel, vertical section. E Carpel, transverse section. F Arillate seed. (Gilg and Werdermann 1925)

149

Fig. 44. Dilleniaceae. Hibbertia (subg. Hibbertia) scandens. A Flowering branch. B Flower bud. C Androecium and gynoecium, vertical section. D Stamen. E Gynoecium, transverse section. F Fruit. G Seed enclosed by aril. H Same, vertical section. (Gilg and Werdermann 1925)

just south of Sydney north to the Bundaberg area in southeastern Queensland. cally and commonly 2, uncommonly 3–5 due to a secondary increase in number, rarely 1; ovules 1–25 per carpel. n = 9; 2n = 26, 36. Estimated 160 species, including all species with monosymmetric androecia, all New Caledonian species, all species included in, or attributable to, Gilg and Werderman’s (1925) section Cyclandra series Ochrolasiae, Tomentosae, and Vestitae, plus Hibbertia arcuata J.R. Wheeler, H. graniticola J.R. Wheeler, and the H. exasperata group (Wheeler 2004b), which has been previously associated with section Candollea. Distribution equivalent to that of the whole genus.

6c. Hibbertia subg. Adrastaea (R. Br. ex DC.) J.W. Horn (2005). A wiry shrub, becoming scandent with age; mature axes non-photosynthetic. Leaves laminar, small and linear. Inﬂorescence a terminal monad; ﬂowers initially produced on axillary short shoots, later on sympodial long shoots consisting mostly of 1-ﬂowered, 2-prophyllate modules; stamens 10 in 2 cycles, obdiplostemonous; carpels 2, ovule 1 per carpel. Only one species, H. salicifolia (DC.) F. Muell., in wallum heath near the coast of temperate to subtropical eastern Australia, from

6d. Hibbertia subg. Hibbertia Fig. 44 Shrubs or, uncommonly, vines or lianas; mature axes non-photosynthetic. Leaves laminar, or ericoid in the Hibbertia hemignosta species complex within sect. Candollea. Stamens not aggregated into obvious cycles, or rarely 1 cycle in the few cases where there are 3 stamens, but sometimes grouped into 3 or 5 alternipetalous fascicles; carpels (1–)3(4)5(–15), fundamentally and commonly 3 or 5; ovules 1–10 per carpel. n = 4, 5, 8, 16, 32, 64; 2n = 20. Estimated 80–90 species, containing all species included in or attributable to the series of Gilg and Werdermann’s (1925) sect. Cyclandra not accounted for above, plus those in or attributable to their sect. Candollea (except the H. exasperata group, see above). Occurring throughout Australia, but particularly concentrated in the southeast and southwest, New Guinea. IV. Subfam. Dillenioideae Burnett (1835) (‘Dillenidae’). Nodes multilacunar (7–27), or probably secondarily trilacunar in the Sri Lankan species of Acrotrema. Leaves with persistent or deciduous,

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amplexicaul petiolar wings (perhaps secondarily lost in one Dillenia clade).

8. Didesmandra Stapf

Schumacheria + Didesmandra:

Vestiture also including fasciculate trichomes. Inﬂorescence a terminal (less often also axillary) thyrsoid with cincinnate partial inﬂorescences, at least some of which represent supernumerary branches; sepals 5; petals 5; stamens grouped in 2 fascicles presented in the median plane of the ﬂower, opposite the median petal with the ﬁlaments in each fascicle connate to form a ± cylindrical staminal column, the two stamen fascicles very shortly connate with one another at their base; each of the two stamen fascicles consists of 1 larger stamen with a conspicuously uncinate anther with dehiscence by longitudinal slits and 4 smaller stamens with unbent anthers that dehisce by apical pores; carpels 2, presented in the transverse plane of the ﬂower. Fruit an aggregate of nutlets. Seed with a membranous aril. One species, D. aspera Stapf, endemic to Sarawak, Borneo.

Shrubs to small, spindly trees; androecium monosymmetric; pollen commonly 4-aperturate; ovule 1 per carpel, campylotropous, apotropous; vascularized by a massive bundle of traces that remain in the ﬂoral receptacle above the point where the ventral carpel bundles depart. 7. Schumacheria Vahl

Fig. 45

Schumacheria Vahl, Skr. Naturhist.-Selsk. 6:122 (1810); Wadhwa, Rev. Handb. Fl. Ceylon 10:109–135 (1996).

Inﬂorescence both terminal and axillary, a thyrsoid with a paniculate arrangement of cincinnate partial inﬂorescences in S. castaneifolia, or consisting of axillary cincinni in the other species. Sepals 5; petals 3–5; androecium of c. 20–35 stamens, grouped in a single fascicle located opposite the abaxial-median petal; stamen ﬁlaments nearly fully connate, forming a liguliform column; anthers with a vestiture of simple trichomes and with a short, mucronate, apical appendage, dehiscing by 2 apical pores; carpels (2)3. Seed with small, membranous aril. Three species, endemic to Sri Lanka.

Fig. 45. Dilleniaceae. Schumacheria castaneifolia. A Flowering branch. B Flower bud. C Androecium and gynoecium. D Anther. E Carpel, vertical section. F Carpel, transverse section. G Seed. (Gilg and Werdermann 1925)

Didesmandra Stapf in Hooker’s Ic. Pl.: t. 2646 (1900); Hoogland, Fl. Males. I, 4:152, Fig. 7 (1951).

Acrotrema + Dillenia: Gynoecium hemisyncarpous. Ovules 2 or more per carpel. 9. Acrotrema Jack

Fig. 46

Acrotrema Jack, Mal. Misc. 1, 5:36 (1820); Hoogland, Fl. Males. I, 4:141–174 (1951); Hoogland, Fl. Thailand 2, 2:95– 108 (1972); Wadhwa, Rev. Handb. Fl. Ceylon 10:109–135 (1996).

Rhizomatous herbs with leaves in a basal rosette or terminal on a very short, erect stem. Leaves simple, pinnatisect, or pinnate, sometimes variegated, the base sometimes auriculate; vestiture of simple, unicellular or multicellular trichomes. Inﬂorescence terminal, or sometimes also axillary, a raceme, or the ﬂower solitary; sepals 5; petals 5; androecium of 15–50 free stamens, usually grouped in 3 fascicles positioned alternate with the carpels, or stamens evenly distributed around the gynoecium; anthers short and dehiscing via longitudinal slits, or long, linear, and dehiscing via 2 apical pores; carpels (2)3; ovules 2–6(–20) per carpel. Fruit an aggregate of basally coherent follicles, dehiscing irregularly at maturity. Seed with a white and membranaceous aril. n = 28 (Mathew 1972). About 9 species, c. 7 in Sri Lanka, 1 in the Western Ghats of India, and 1 in southern Myanmar, southern Thailand, Malay Peninsula, and northern Sumatra.

Dilleniaceae

151

with indehiscent fruits. n = 13, 16, 24, 27. About 65 species, from Madagascar and the Seychelles to Fiji, c. 45 species in Malesia, 1 in Australia. The non-amplexicaul species group, recognized by Hoogland (1952), is monophyletic (Horn 2005), but some of the amplexicaul species group (e.g., D. triquetra of Madagascar and Sri Lanka; possibly D. ferruginea of the Seychelles) may be most closely related to Acrotrema.

Fig. 46. Dilleniaceae. A Acrotrema thwaitesii. B Acrotrema lanceolatum. (Gilg and Werdermann 1925)

Further work is needed to determine whether this genus is derived within, or is sister to, Dillenia. 10. Dillenia L.

Figs. 47, 48

Dillenia L., Sp. Pl. 1:535 (1753); Hoogland, Fl. Males. I, 4:141–174 (1951), in Blumea 7:1–145 (1952), rev., ibid. 9:577–589 (1959), and Fl. Thailand 2, 2:95–108 (1972).

Trees, rarely shrubs, mostly evergreen, rarely deciduous. Leaves with or without persistent or deciduous amplexicaul petiolar wings. Inﬂorescences 1–10(–30)-ﬂowered, a cincinnus, thyrsoid with (apparently) cincinnate partial inﬂorescences, panicle (often depauperate), or monad, terminal or rarely axillary; ﬂowers infrequently borne on cataphyll-bearing short shoots; sepals (4)5(–18), unequal to ± equal; petals (0, 4)5(–7); androecium of (60–)100–700(–900) members, sometimes partly staminodial; fertile stamens often distinctly heterantherous (the inner group of stamens bearing anthers overtly longer than those of the outer group); anthers dehiscence frequently via 2 apical or subapical pores, less frequently via 2 longitudinal slits; staminodes, when present, typically external to the fertile androecium, rarely internal; gynoecium typically (always?) hemisyncarpous; carpels (4)5–15(–20), forming one whorl on a conical, centrally protruding part of the receptacle; ovules 5–80 per carpel, borne in 2(4) vertical rows on submarginal placentae. Fruit an aggregate of basally coherent follicles, or the fruit indehiscent and completely enclosed by the ﬂeshy, accrescent calyx. Seeds with a white or red, ﬂeshy aril, or the aril vestigial in some species

Fig. 47. Dilleniaceae. Dillenia excelsa. A Flowering branch. B Flower. C Dehiscing fruit. (Koorders and Valeton 1913)

152

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Fig. 48. Dilleniaceae. Dillenia indica. A Flowering branch. B Androecium and gynoecium, vertical section. C Half gynoecium, transverse section. D Outer and inner stamen. E Fruit enclosed by ﬂeshy sepals. F Same, vertical section. G Seed. H Same, vertical section. (Gilg and Werdermann 1925)

Selected Bibliography APG II 2003. See general references. Ashton, P.S., Gunatilleke, C.V.S. 1987. New light on the plant geography of Ceylon. I. Historical plant geography. J. Biogeogr. 14:249–285. Aymard, C., G.A. 1997. Dilleniaceae novae Neotropicae IX: Neodillenia, a new genus from the Amazon basin. Harvard Pap. Bot. 10:121–131. Aymard, C., G.A. 2002. Davilla papyracea (Dilleniaceae), a new species from Brazil. Kew Bull. 57:487–490. Baillon, H.E. 1865. Remarques sur les Dilléniacées. Adansonia 6:255–281. Baretta-Kuipers, T. 1972. Some remarks on the wood structure of Pinzona and allied genera of the subfamily Tetraceroideae (Dilleniaceae). Acta Bot. Neerl. 21:573– 577.

Berg, R.Y. 1975. Myrmecochorous plants in Australia and their dispersal by ants. Austral. J. Bot. 23:475–508. Bernhardt, P. 1984. The pollination biology of Hibbertia stricta (Dilleniaceae). Pl. Syst. Evol. 147:267–277. Bernhardt, P. 1986. Bee-pollination in Hibbertia fasciculata (Dilleniaceae). Pl. Syst. Evol. 152:231–241. Bernhardt, P. 1996. Anther adaptation in animal pollination. In: D’Arcy, W.G., Keating, R.C. (eds) The anther: form, function, and phylogeny. Cambridge: Cambridge University Press, pp. 192–220. Conti, E. et al. 2002. See general references. Corner, E.J.H. 1946. Centrifugal stamens. J. Arnold Arb. 27:423–437. Corner, E.J.H. 1976. See general references. Corner, E.J.H. 1978. The inﬂorescence of Dillenia. Notes Roy. Bot. Gard. Edinburgh 36:341–353. Craven, L.A., Dunlop, C.R. 1992. A taxonomic revision of Pachynema (Dilleniaceae). Austral. Syst. Bot. 5:477– 500. Croat, T. 1978. Flora of Barro Colorado Island. Stanford: Stanford University Press. Cronquist, A. 1981. See general references. Cronquist, A. 1988. The evolution and classiﬁcation of ﬂowering plants, 2nd edn. Bronx: New York Botanical Garden. Cuénoud, P., Savolainen, V., Chatrou, L.W., Powell, M., Grayer, R.J., Chase, M.W. 2002. Molecular phylogenetics of Caryophyllales based on 18S rDNA and plastid rbcL, atpB, and matK DNA sequences. Amer. J. Bot. 89:132–144. Dahlgren, R.M.T. 1983. General aspects of angiosperm evolution and macrosystematics. Nordic J. Bot. 3:119– 149. de Candolle, A.P. 1824. Prodromus systematis naturalis regni vegetabilis, I. Paris: Treuttel et Würtz. Dickison, W.C. 1967a. Comparative morphological studies in Dilleniaceae, I. Wood anatomy. J. Arnold Arb. 48:1– 29. Dickison, W.C. 1967b. Comparative morphological studies in Dilleniaceae, II. The pollen. J. Arnold Arb. 48:231– 240. Dickison, W.C. 1968. Comparative morphological studies in Dilleniaceae, III. The carpels. J. Arnold Arb. 49:317– 333. Dickison, W.C. 1969. Comparative morphological studies in Dilleniaceae, IV. Anatomy of the node and vascularization of the leaf. J. Arnold Arb. 50:384–410. Dickison, W.C. 1970a. Comparative morphological studies in Dilleniaceae, V. Leaf anatomy. J. Arnold Arb. 51:89– 113. Dickison, W.C. 1970b. Comparative morphological studies in Dilleniaceae, VI. Stamens and young stem. J. Arnold Arb. 51:403–422. Dickison, W.C. 1971. Comparative morphological studies in Dilleniaceae, VII. Additional notes on Acrotrema. J. Arnold Arb. 52:319–333. Dickison, W.C. 1979. A note on the wood anatomy of Dillenia (Dilleniaceae). IAWA Bull. 2/3:57–60. Dickison, W.C. 1984. On the occurrence of silica grains in the woods of Hibbertia (Dilleniaceae). IAWA Bull. II, 5:341–343. Dickison, W.C., Rury, P.M., Stebbins, G.L. 1978. Xylem anatomy of Hibbertia (Dilleniaceae) in relation to ecology and evolution. J. Arnold Arb. 59:32–49.

Dilleniaceae Dickison, W.C., Nowicke, J.W., Skvarla, J.J. 1982. Pollen morphology of the Dilleniaceae and Actinidiaceae. Amer. J. Bot. 69:1055–1073. Dyer, A.G. 1996. Reﬂection of near-ultraviolet radiation from ﬂowers of Australian native plants. Austral. J. Bot. 44:473–488. Eichler, A.W. 1878. Blüthendiagramme, II. Leipzig: W. Engelmann. Endress, P.K. 1997. Relationships between ﬂoral organization, architecture, and pollination mode in Dillenia (Dilleniaceae). Pl. Syst. Evol. 206:99–118. George, A.S. 2002. The south-western Australian ﬂora in autumn: 2001 Presidential Address. J. Roy. Soc. W. Australia 85:1–15. Gilg, E., Werdermann, E. 1925. Dilleniaceae. In: Engler, A., Prantl, K., Die natürlichen Pﬂanzenfamilien, ed. 2, 21. Leipzig: W. Engelmann, pp. 7–36. Gottsberger, G. 1977. Some aspects of beetle pollination in the evolution of ﬂowering plants. Pl. Syst. Evol., suppl. 1:211–226. Gurni, A.A., Kubitzki, K. 1981. Flavonoid chemistry and systematics of the Dilleniaceae. Biochem. Syst. Ecol. 9:109–114. Hegnauer, R. 1966. Chemotaxonomie der Pﬂanzen, 4, pp. 19–23. Basel: Birkhäuser. Hickey, L.J., Wolfe, J.A. 1975. The bases of angiosperm phylogeny: vegetative morphology. Ann. Missouri Bot. Gard. 62:538–589. Hoogland, R.D. 1952. A revision of the genus Dillenia. Blumea 7:1–145. Hoogland, R.D. 1953. The genus Tetracera (Dilleniaceae) in the eastern Old World. Reinwardtia 2:185–225. Hoogland, R.D. 1959. Additional notes on Dilleniaceae 1–9. Blumea 9:577–589. Horn, J.W. 2005. The phylogenetics and structural botany of Dilleniaceae and Hibbertia Andrews. Ph.D. Thesis, Duke University, Durham, NC, 171 p. Hutchinson, J. 1964. The genera of ﬂowering plants, 1. Oxford: Clarendon. Imaichi, R., Kato, M. 1996. A scanning electron microscopic study of ovule development in Dillenia suffruticosa (Dilleniaceae). Phytomorphology 46:45–51. Ioffe, M.D., Zhukova, G.Y. 1974. Modiﬁcation of zygote cell wall during its development in Dillenia Dilleniaceae. Bot. Zhurn. (Moscow & Leningrad) 59:1409–1416. Keighery, G.J. 1975. Pollination of Hibbertia hypericoides (Dilleniaceae) and its evolutionary signiﬁcance. J. Nat. Hist. 9:681–684. Keighery, G.J. 1991. Pollination of Hibbertia conspicua (Dilleniaceae). W. Austral. Naturalist 18:163–165. Koorders, S.H., Valeton, T. 1913. Atlas der Baumarten von Java, 1. Leiden: P.W.M. Trap. Kubitzki, K. 1968. Flavonoide und Systematik der Dilleniaceen. Ber. Deutsch. Bot. Gesell. 81:238–251. Kubitzki, K. 1970. Die Gattung Tetracera (Dilleniaceae). Mitt. Bot. Staatssamml. München 8:1–98. Kubitzki, K. 1971. Doliocarpus, Davilla und verwandte Gattungen (Dilleniaceae). Mitt. Bot. Staatssamml. München 9:1–105. Lakshmanan, J.D.E., Lakshmanan, K.K. 1984. Further contributions to the embryology of Dillenia suffruticosa (Griff.) Martelli. J. Indian Bot. Soc. 63:353–359. Mathew, P.M. 1972. Cytology of Acrotrema. Curr. Sci. 41:751.

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Momose, K., Yumoto, T., Nagamitsu, T., Kato, M., Nagamasu, H., Sakai, S., Harrison, R.D., Itioka, T., Hamid, A.A., Inoue, T. 1998. Pollination biology in a lowland dipterocarp forest in Sarawak, Malaysia. I. Characteristics of the plant-pollinator community in a lowland dipterocarp forest. Amer. J. Bot. 85:1477–1501. Ozenda, P. 1949. Recherches sur les dicotylédons apocarpiques. Publications des laboratoires de l’École Normale Supérieure, Série Biologie, fasc. 2. Paris: Jouve. Paetow, W. 1931. Embryologische Untersuchungen an Taccaceen, Meliaceen und Dilleniaceen. Planta 14:441– 470. Parmentier, M.P. 1895. Contribution à l’étude de la famille des Dilléniacées. C. R. Assoc. Franç. Avancem. Sci. pt. 2:626–630. Pavanasasivam, G., Sultanbawa, M.U.S. 1974. Betulinic acid in the Dilleniaceae and a review of its natural distribution. Phytochemisty 13:2002–2006. Prance, G.T. 2003. Rhabdodendraceae. In: Kubitzki, K., Bayer, C. (eds) The Families and Genera of Vascular Plants, 5. Flowering plants, dicotyledons: Malvales, Capparales and non-betalain Caryophyllales. Berlin Heidelberg New York: Springer, pp. 339–341. Rao, A.N. 1957. A contribution to the embryology of Dilleniaceae. Proc. Iowa Acad. Sci. 64:172–176. Rao, T.A., Das, S. 1979. Comparative typology and taxonomic value of foliar sclereids in Hibbertia Andr. (Dilleniaceae). Proc. Indian Acad. Sci., B 88:161–174. Rury, P.M., Dickison, W.C. 1977. Leaf venation patterns of the genus Hibbertia (Dilleniaceae). J. Arnold Arb. 58:209–256. Sastri, R.L.N. 1958. Floral morphology and embryology of some Dilleniaceae. Bot. Notiser 111:495–511. Schatral, A. 1995. The structure of the seed in some Western Australian species of the genus Hibbertia (Dilleniaceae). Bot. J. Linn. Soc. 119:257–263. Schatral, A. 1996. Dormancy in seeds of Hibbertia hypericoides (Dilleniaceae). Austral. J. Bot. 44:213–222. Schatral, A., Kailis, S.G., Fox, J.E.D. 1994. Seed dispersal of Hibbertia hypericoides (Dilleniaceae) by ants. J. Roy. Soc. W. Australia 77:81–85. Soltis, D.E. et al. 2003. See general references. Stebbins, G.L., Hoogland, R.D. 1976. Species diversity, ecology and evolution in a primitive angiosperm genus: Hibbertia (Dilleniaceae). Pl. Syst. Evol. 125:139–154. Steppuhn, H. 1895. Beiträge zur vergleichenden Anatomie der Dilleniaceen. Bot. Centralbl. 62:337–342, 369–378, 401–413. Swamy, G.L., Periasamy, K. 1955. Contributions to the embryology of Acrotrema arnottianum. Phytomorphology 5:301–314. Takhtajan, A. 1997. See general references. Thorne, R.F. 2000. The classiﬁcation and geography of ﬂowering plants: dicotyledons of the class Angiospermae. Bot. Rev. (Lancaster) 66:441–647. Toelken, H.R. 1998. Notes on Hibbertia (Dilleniaceae): 2. The H. aspera–empetrifolia complex. J. Adelaide Bot. Gard. 18:107–160. Toelken, H.R. 2000. Notes on Hibbertia (Dilleniaceae): 3. H. sericea and associated species. J. Adelaide Bot. Gard. 19:1–54.

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Tucker, S.C., Bernhardt, P. 2000. Floral ontogeny, pattern formation, and evolution in Hibbertia and Adrastaea (Dilleniaceae). Amer. J. Bot. 87:1915–1936. Veillon, J.-M. 1990. Dilleniaceae. In: Morat, P., MacKee, H.S. (eds) Flore de la Nouvelle-Calédonie et Dépendances, 16, pp. 3–86. Paris: Muséum National d’Histoire Naturelle. Vyshenskaya, T.D., Oganezova, G.G. 1991. Dilleniaceae. In: Takhtajan, A. (ed.) Anatomia seminum comparativa (in Russian), 3, pp. 163–171. Leningrad: Nauka. Wagner, R. 1906a. Über den Bau der Rispen des Trisema Wagapii Vieill. Sitzungsber. Kaiserl. Akad. Wissensch., Math.-Naturwissensch. Kl., Abt. 1, 115:857– 880. Wagner, R. 1906b. Untersuchungen über den morphologischen Aufbau der Gattung Pachynema R. Br. Sitzungsber. Kaiserl. Akad. Wissensch., Math.-Naturwissensch. Kl., Abt. 1, 115:1039–1080.

Wheeler, J.R. 1984. New species of Hibbertia (Dilleniaceae) from the northern wheatbelt area of Western Australia. Nuytsia 9:427–437. Wheeler, J.R. 2002. Miscellaneous new species of Hibbertia (Dilleniaceae) from the wheatbelt and pastoral areas of Western Australia. Nuytsia 15:139–152. Wheeler, J.R. 2004a. A review of Hibbertia hemignosta and its allies (Dilleniaceae) from Western Australia. Nuytsia 15:277–298. Wheeler, J.R. 2004b. An interim key to the Western Australian species of Hibbertia (Dilleniaceae). Nuytsia 15:311–320. Wilson, C.L. 1937. The phylogeny of the stamen. Amer. J. Bot. 24:686–699. Wilson, C.L. 1965. The ﬂoral anatomy of the Dilleniaceae. I. Hibbertia Andr. Phytomorphology 15:248–274. Wilson, C.L. 1973. The ﬂoral anatomy of the Dilleniaceae. II. Genera other than Hibbertia. Phytomorphology 23:25– 42.

Geissolomataceae Geissolomataceae Endl., Ench. Bot.: 214 (1841), nom. cons.

F. Forest

Densely leafy low shrub, 50–120 cm high, aluminium-accumulating. Leaves coriaceous, decussate, subsessile, simple, entire, ovate, base cordate, apex acute, margin thickened; stipules small, subulate, situated on the sides of the short, petiole-like leaf base. Flowers solitary, terminal on lateral short shoots, subtended by 3 pairs of decussate, persistent bracts, these increasing in size and petaloid above; vestigial ﬂower buds often present in axils of uppermost bracts. Flowers with short, sharply 4-angled pedicels, hermaphrodite, actinomorphic, monochlamydeous, hypogynous; tepals 4, decussate, basally shortly connate, persistent, pink, turning carmine when older; stamens 4 + 4, attached basally to the ﬂoral tube; ﬁlaments slender, free; anthers 4-sporangiate, dorsiﬁxed, introrse, longitudinally dehiscent; nectary intrastaminal on ﬂoral cup with 4 nectary recesses opposite the tepals; gynoecium 4-carpellate; ovary superior, 4-lobate in transection, sessile, 4-locular; stylodia 4, free above the base but, at anthesis in apical part, postgenitally fused and twisted; stigma common to the four stylodia and punctiform; ovules 2 per locule, anatropous, pendulous from the apex. Fruit a hard, 4-lobed, loculicidal capsule enclosed in the persistent perianth; seeds 1 per locule, reniform, oblong, whitish, smooth; endosperm present; embryo straight, central; cotyledons long and linear. A single genus and species, Geissoloma marginatum (L.) A. Juss., restricted to the southern Langeberg mountains in the Cape of South Africa from the Swellendam to Riversdale divisions, on moist south-facing sandstone slopes at elevations of 600–1,200 m in “fynbos” scrub; ﬂowering from June to September. Vegetative Anatomy. The leaves of Geissoloma have a multiple epidermis with intracellular pectates found in the epidermal cells. The thickened margin consists of large epidermal cells and thickwalled mesenchymatous cells, some of which con-

tain druses. Stomata are anomocytic and restricted to the abaxial side of the leaf. The abaxial surface of the leaf is covered with waxy scales or strands, and young leaves have dense, unicellular T-shaped trichomes (Dahlgren and Rao 1969; Carlquist 1990). The wood of Geissoloma, as studied by Carlquist (1975), has long vessel elements with oblique scalariform perforation plates. The imperforate elements of the axial secondary xylem is made up of tracheids only. Axial parenchyma is diffuse and scanty; rays are multiseriate and uniseriate, the former with procumbent and square to erect cells, the latter lacking procumbent cells. One or two large or several small calcium oxalate crystals are present in ray cells. Floral Structure. Dahlgren and Rao (1969) found little resemblance between Geissoloma and Penaeaceae, and could not ﬁnd vestigial traces of other perianth whorls in Geissoloma. The stylodia are twisted (Fig. 49G) and thus form a compitum comparable to the situation in some Malvaceae. Matthews and Endress (2005) gave a detailed analysis of the ﬂoral morphology of Geissoloma and compared it with that of the other members of Crossosomatales. Embryology (from Stephens 1910). The ovules are anatropous, bitegmic and crassinucellate; the micropyle is formed by the outer integument. The embryo sac is 8-nucleate and probably formed according to the Polygonum type. The antipodals early decrease in size and lose their staining properties. The copious endosperm is partly resorbed by the developing embryo. No endosperm haustoria develop. In the ripe seed, the endosperm is ﬂeshy. The funicular part of the seed becomes whitish and swollen and forms a collar-like caruncle. Seed coat structure is unknown. Pollen Morphology. The pollen grains are 3-colporate, ± spheroidal, and the exine is

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baculate-tectate and ﬁnely perforate (Erdtman 1952; Dahlgren and van Wyk 1988). Karyology. The chromosome number is unknown. Attempts to germinate seeds in order to determine the chromosome number from root tips failed because of the low seed production and viability. Because of a sticky opaque substance produced by the pollen grains, chromosome counting from germinating pollen also failed (McDonald 1998). Afﬁnities. The single species, ﬁrst described as Penaea marginata by Linnaeus, was placed in Penaeaceae or Celastraceae by early botanists. After elevation to family rank, placements in Pittosporales, close to Bruniaceae and Grubbiaceae (Thorne 1983), Geissolomatales (Dahlgren 1983; Takhtajan 1987) and Celastrales (Cronquist 1981) were suggested. In recent phylogenetic analyses based on the plastid gene rbcL (Savolainen, Fay et al. 2000), Geissolomataceae emerged as the sister-group to the monotypic Ixerbaceae (New Zealand) and Strasburgeriaceae (New Caledonia). Savolainen, Fay et al. (2000) suggested that these three families could be included in an expanded order Crossosomatales. A single genus: Geissoloma Lindl. ex Kunth

Fig. 49

Geissoloma Lindl. ex Kunth, Linnaea 5:678 (1830).

Characters as for the family. Monotypic, see above.

Selected Bibliography Carlquist, S. 1975. Wood anatomy and relationships of the Geissolomataceae. Bull. Torrey Bot. Club 102:128–134. Carlquist, S. 1990. Leaf anatomy of Geissolomataceae and Myrothamnaceae as a possible indicator of relationship to Bruniaceae. Bull. Torrey Bot. Club 117:420–428. Cronquist, A. 1981. See general references. Dahlgren, R. 1983. General aspects of angiosperm evolution and macrosystematics. Nordic J. Bot. 3:119–149. Dahlgren, R., Rao, V.S. 1969. A study of the family Geissolomataceae. Bot. Notiser 122:207–227.

Fig. 49. Geissolomataceae. Geissoloma marginatum. A Flowering branch. B Leaf. C Leaf base with stipules. D Flower. E Stamen. F Anthers in dorsal and ventral view. G Pistil. H Upper part of ovary and bases of stylodia. I Apices of stylodia. J Young capsule. K Seed. L Hair from young leaf. (Dahlgren and van Wyk 1988)

Dahlgren, R., van Wyk, A.E. 1988. Structures and relationships of families endemic to or centred in South Africa. Monogr. Syst. Bot. Missouri Bot. Gard. 25:1–94. Erdtman, G. 1952. See general references. Matthews, M.L., Endress, P.K. 2005. See general references. McDonald, D.J. 1998. The enigma of the Geissolomataceae. Veld & Flora 84:122–123. Savolainen, V., Fay, M.F. et al. 2000. See general references. Stephens, E.L. 1910. The embryo-sac and embryo of Geissoloma marginata. New Phytol. 8:345–348. Takhtajan, A. 1987. See general references. Thorne, R.F. 1983. Proposed new realignments in the angiosperms. Nordic J. Bot. 3:85–117.

Geraniaceae Geraniaceae Adans., Fam. Pl. 2:384 (1763), nom. cons. Hypseocharitaceae Wedd. (1861).

F. Albers and J.J.A. Van der Walt

Herbs, sometimes shrublets or shrubs, occasionally with succulent stems, sometimes geophytic. Leaves alternate or opposite, mostly palmately or pinnately lobed or compound, lobes deeply serrate or lobulate; stipules present or (Hypseocharis) absent. Inﬂorescences pseudoumbellate, or ﬂowers solitary. Flowers perfect, actinomorphic or zygomorphic, pentamerous; sepals free or united at base, imbricate with valvate tips, persistent; petals 5 (4, 2 or 0), free, imbricate; stamens 5 or 10 and 15, then in two whorls, sometimes a few sterile, ﬁlaments free or more or less connate at base; gynoecium of 5(4) carpels; style with 5 stigmatic branches (unbranched with capitate stigma in Hypseocharis); ovary 5-lobed, with 1–2(–12) pendulous, anatropous ovules in each locule; placentation axile. Fruits schizocarps with ﬁve 1-seeded awned mericarps which separate elastically from a central beak (rostrum), or (Hypseocharis) with ﬁve 1–few-seeded mericarps not connected by a central column or loculicidal capsules; seeds with a more or less curved embryo with green cotyledons or (Hypseocharis) with a cochlear embryo with spirally folded cotyledons; endosperm absent or scanty. A family of ﬁve genera and about 835 species, sub-cosmopolitan but mainly in temperate and subtropical regions. Vegetative Morphology. Erodium and Geranium are generally annual or perennial herbs, often with a basal rosette, occasionally subshrubs. Tall shrubs (to 4 m) are found only in the Hawaiian endemic Geranium sect. Neurophyllodes. Monsonia and Pelargonium exhibit a wide range of different growth forms. Monsonia comprises small xerophytic shrubs, geophytes, perennials and ephemeral annual herbs. Pelargonium exhibits a wide range of growth habits, from short-lived annuals to scrambling herbs and tall shrubs (Van der Walt 1977; Van der Walt and Vorster 1981, 1988), but xerophytes, stem succulents and

geophytes are the dominant type (Albers 2002). Leaﬂess stem succulents are unknown in Erodium and Geranium. Species of Erodium and Geranium usually have fusiform roots or, more rarely, root tubers. In some sections of Geranium, the branched rootstock is covered with pale brown stipules and petiole bases. Xerophytic Monsonia and Pelargonium are characterised by fusiform roots, roots with a series of small tubers or thick rhizomes. Pelargonium sect. Hoarea has tubers with a cover of paper-like sheaths of exfoliating periderm. Hypseocharis forms thick taproots or large tubers. Most of the species of Erodium and Geranium are small herbaceous plants with numerous erect or decumbent stems, except for a few higher-growing species in Geranium with a single vegetative axis. Hypseocharis is an acaulescent or short-stemmed hemicryptophyte. In some Pelargonium, the stem is very short (e.g. P. sect. Polyactium) or totally reduced (P. sect. Hoarea). The differential development of the hypocotyl, internode elongation and branching system of various life forms in Pelargonium have been studied by Jones and Price (1996). The species of Monsonia sect. Sarcocaulon are short-stemmed, semi-erect to decumbent shrublets whereas the remaining sections of Monsonia are herbaceous; only the perennials are woody at the base. A few annuals form carpets by producing stolons. The shape and size of the leaves vary extremely within genera, subgenera and even sections. The leaves are opposite or alternate, not rarely changing position on the same stem. Especially in Pelargonium, a high diversity in leaf shapes and patterns occurs. The margin can be entire, toothed or lobed. The adaxial and abaxial leaf blades can differ in being glabrous or carrying non-glandular and/or glandular hairs of different types. Leaves are stipulate, except in Hypseocharis. Especially in Monsonia sect. Sarcocaulon, long petioles can persist as blunt or sharp spines.

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Vegetative Anatomy. In most genera, the vascular bundles are arranged in one ring, which is often surrounded by a sheath of sclerenchyma. The pith parenchyma contains starch granules. Starch storage sometimes also occurs in the cortical parenchyma. Clustered crystals are frequent. In addition to the primary growth, a continuous vascular cambium produces secondary elements in a normal way. In woody pelargoniums, the secondary xylem contains vessels with simple perforations plates; reticulate plates seem to be rare. Living and septate ﬁbres as well as both paratracheal and apotracheal axial parenchyma are present. The rays are heterogeneous, consisting mainly of square and upright cells (Van der Walt et al. 1987). Especially in Pelargonium sect. Hoarea, a phellogen originating in the outermost cortical parenchyma produces numerous periderm layers. In Monsonia sect. Sarcocaulon, a thick, waxy bark develops from the periderm, which is ﬂammable and therefore called “bushmen candle”. Stem succulence in Pelargonium cotyledonis is mainly brought about through the production of parenchyma, whereas in Pelargonium sect. Otidia and sect. Cortusina primary and secondary tissues take part in its formation (Jones and Price 1996). Leaves are bifacial, rarely aequifacial. Stomata are anomocytic throughout. Roots are mainly diarch or less often triarch. Inﬂorescences. In Erodium and Pelargonium, normally a cluster of several pedicels arises from a single point, producing a pseudoumbel of two to many ﬂowers, with the younger ﬂowers at the periphery. In Pelargonium, the inﬂorescences are sometimes borne on a peduncle, which is often branched and forms a compound inﬂorescence with several pseudoumbels. In most species of Geranium and Hypseocharis, the inﬂorescence is cymose, composed of axillary, two-ﬂowered cymules. Often, the cymules arise on aerial, leafy or leaﬂess stems. In some geraniums and Hypseocharis, ﬂowers arise directly from the short hypocotyl or rootstock. In Monsonia sect. Sarcocaulon, the ﬂowers are solitary and the peduncles axillary. Floral Structure. Flowers are usually actinomorphic, apart from some Erodium and most Pelargonium. Petal aestivation is usually contort in bud. The corolla is usually pentamerous, but the number of petals can be reduced to two in

the zygomorphic ﬂowers of Pelargonium. The androecium is obdiplostemonous with 5 + 5 stamens in Erodium, Geranium and Pelargonium, whereas Monsonia has 15 (10 staminodial in one species) and Hypseocharis has 5 or 15 stamens. In Erodium, only 5 and in Pelargonium 2–7 stamens are fertile. In Monsonia and Hypseocharis, the 15 stamens are arranged in two whorls, and in both genera the outer (and later developing) stamens form ﬁve antepetalous pairs (Ronse Decraene and Smets 1995) and are shorter than the antesepalous stamens. In one Hypseocharis, the androecium is reduced to 5 antepetalous stamens (Slanis and Grau 2001), whereas Aldasoro et al. (2001) report a reduction to 5 fertile antesepalous stamens for one species of Monsonia. In Erodium, Geranium and Monsonia, generally ﬁve hemispherical nectaries are present which alternate with the ﬁlaments of the outer staminal whorl. In some Geranium there is a ring-like disk, rather than isolated nectaries. Some Erodium and Monsonia have ﬁve nectaries more or less deeply submerged into antesepalous hypanthial tubes. In Pelargonium, there is usually only one nectary concealed in an adaxial-episepalous area in the hypanthium (Link 1990; Vogel 1998). A lobed extrastaminal nectary disk is well developed in Hypseocharis (Slanis and Grau 2001). Embryology. The tapetum in the mature anthers is glandular. Pollen grains are shed at the two-celled stage in Erodium and Monsonia and at the three-celled stage in Erodium, Pelargonium and Geranium. The ovules are anatropous, bitegmic and crassinucellate. Embryo sac development is of the Polygonum type; the early endosperm conforms to the Nuclear type, and both endosperm and nucellus are later resorbed by the embryo. The endospermless seeds of most Geraniaceae contain a large embryo which is bent in the region of the hypocotyl, so that the radicle is folded against one of the cotyledons. The embryo in Geranium is chlorophyllous and has a particularly long radicle (Yeo 1990). Erodium and Monsonia in principle share this morphology whereas in Pelargonium the cotyledons are ﬂat (Aedo et al. 1998). The seeds of Hypseocharis have cochlear embryos with spirally folded cotyledons and scanty endosperm. Pollen Morphology. Pollen is tricolpate (Monsonia, Hypseocharis) or tricolporate (Erodium, Geranium and Pelargonium). The exine sculpture

Geraniaceae

is reticulate in Monsonia (Verhoeven and Venter 1986), reticulate-striate in Hypseocharis (Huynh 1969) and Erodium, or reticulate with supratectal processes in Geranium (Bortenschlager 1967; Verhoeven and Marais 1990). Exine sculpture of Pelargonium varies from striate-reticulate, reticulate-striate to striate (Stafford and Gibby 1992), and only a few subgroups can be identiﬁed by differences in their reticulum and ornamentation. The ultrastructure of the exine of some

Fig. 50. Geraniaceae. Diversity of ﬂower morphs and coadapted pollinators in Pelargonium. A P. magenteum (long-proboscid hovering ﬂies). B P. ternifolium (bees). C P. longiﬂorum (?long-proboscid hovering ﬂies). D P. bowkeri (hawkmoths). E P. lobatum (hawkmoths). F P. scabrum (hemiphilic). G P. fulgidum (birds). H P. grossularioides (facultatively or obligatorily autogamous). I P. triandrum (long-proboscid hovering ﬂies). J P. laxum (bees). K P. multicaule (bees). L P. rapaceum (bees). (Drawn by U. Meeve; Struck 1997)

159

Erodium and Geranium was studied by Stafford and Blackmore (1991). The surface of the exine is covered by pollenkitt and underlain by a compact layer of pollen-coating vesicles (Weber 1996). Karyology. Geraniaceae are karyologically highly diverse, well studied (except Hypseocharis), and illustrate the taxonomic importance of karyology at the generic and subgeneric level. The four genera present different patterns of basic chromosome numbers, with one dominating base number and several derived numbers (Albers 1990): Erodium: 8, 9, 10 (e.g. Guittonneau 1990). Geranium: 9, 10, 11, 13, 14 (e.g. Van Loon 1984a, b). Monsonia: 8, 9, 10, 11, 12 (Albers 1990; Touloumenidou et al., in prep.). Pelargonium: 4, 7, 8, 9, 10, 11 (e.g. Albers et al. 1992; Gibby et al. 1996). Additional numbers have resulted from losses of chromosomes in higher polyploids or from hybridization of polyploids with different chromosome numbers (e.g. in the Pelargonium alchemilloides complex: 32 × 36 = 34). Polyploidy ascends sometimes to dodekaploidy (Erodium tocranum 2n = 12x = 120; Pelargonium schizopetalum 2n = 10x = c. 108; Geranium canariense, G. rubescens 2n = 8x = 128; Monsonia ignorata 2n = 6x = 60). Pelargonium is the karyologically best known genus in the family, and base numbers and chromosome sizes are often indicators for natural groups within the genus and have led to several taxonomic rearrangements at sectional level (e.g. Albers et al. 1992), although morphological features are sometimes not congruent with the karyological results. Albers and Van der Walt (1984) proposed x = 11 as the basic chromosome number of Pelargonium; this was conﬁrmed by Bakker et al. (2000). Most of the other base numbers in infrageneric groups of Pelargonium are derived from x = 11 (e.g. in sect. Hoarea 11 → 10 → 9, Gibby et al. 1996); such changes have taken place several times independently. Pollination. All genera are protandrous. In Erodium and Geranium, most of the species are pollinated by insects but self-pollination is frequent. Only the Hawaiian G. arborescens is ornithophilous. The two main groups of insects observed in Europe visiting Erodium are Diptera and Hymenoptera. Monsonia seems to be mostly pollinated by beetles (Albers, pers.

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obs.). Pelargonium species predominantly have protandrous-allogamous ﬂowers, which appear to be essentially pollinated by long-tongued bees and long-tongued ﬂies (Fig. 50). The more basal sections of the genus show exclusively hemiphilous to melittophilous syndromes. Sphingophilous ﬂoral syndromes are expressed in the night-scented Pelargonium sect. Polyactium. Bird pollination is known only from P. fulgidum (Struck 1997). Autogamy is frequent in Pelargonium, and the different forms of self-pollination systems involved were treated by Meve (1995). Fruit and Seed. In Geranium, Erodium, Monsonia and Pelargonium, the ﬁve carpels form a syncarpous ovary maturing into a schizocarp. The mature fruit falls into ﬁve, usually one-seeded mericarps. The central column consists of the fused septa. Awned mericarps are capable of hygroscopic movements. Mericarps in Pelargonium as well as some Erodium and Monsonia develop hairs on the adaxial side of the awns. Awn morphology is of high diagnostic value (Guittonneau 1972; Yeo 1984, 1990). Most Hypseocharis have loculicidal capsules with several small seeds in each locule; H. tridentata has a schizocarp but the mericarps are not beaked; they contain one to few seeds (Slanis and Grau 2001). The seeds are strongly campylotropous with large embryos and strongly folded coytyledons, when viewed in transverse section. They are rich in lipid substances and poor in starch. Seed coat structure is uniform throughout the family, and characterised by a crystalliferous endotesta and a strongly thickened but scarcely ligniﬁed exotegmen (Corner 1976; Boesewinkel and Ben 1979; Boesewinkel 1988). For the light line of the endotesta, see Meisert et al. (2001). Dispersal. Most Geraniaceae are autochorous, active ballists, some are (exo)zoochorous or anemochorous. Based on beak morphology, three main seed-dispersal mechanisms can be distinguished (Yeo 1990). In the Erodium type, the entire mericarp including the awn is ejected, and the mericarps are able to bury themselves in the soil by hygroscopic movements of the twisted awn. This type is found in Pelargonium, Erodium, Monsonia and some Geranium. Two additional types are found in Geranium: in the carpel-projection type, the basal part of the mericarp containing the seed is thrown whereas the awn remains attached to the beak; in the seed-ejection type, the seed is ejected

by curving of the awn, and the entire mericarp remains on the plant. The diaspores of Erodium and Geranium are dispersed by cattle, birds and ants whereas the disapores of Pelargonium, Erodium subg. Erodium and Monsonia sections Monsonia and Plumosa have plumose awns and are wind-dispersed. The small, papillose seeds of Hypseocharis may also be anemochorous (Boesewinkel 1988). Vegetative Reproduction. Sexual reproduction predominates but asexual propagation occurs as well. In sprawling species of Erodium, Geranium and Pelargonium, rooting at the nodes is frequent and gives rise to new individuals. Pelargonium crassicaule, P. articulatum and others produce rhizomes from which new aerial shoots are formed. If individual tubers of Pelargonium sipthorpiifolium become separated, they give rise to new plantlets (F. Albers, pers. obs.). The propagation of Pelargonium species and cultivars by cuttings in commercial horticulture is being superseded by cell culture techniques. Phytochemistry. Common ﬂavonols, proanthocyanidins, free ellagic acid and ellagitannins are widely distributed in the family; myricetin, C-glycosyl ﬂavones and ﬂavones have been less frequently recorded (Bate-Smith 1973; Williams et al. 2000). Their distribution was often found to be in accord with sectional classiﬁcation, and has led to the reinstatement of the sect. Reniformia which had long been sunken in sect. Cortusina (Dreyer and Marais 2000). Alkaloids are less important as chemotaxonomic markers. Whereas most Pelargonium accumulate high quantities of tartaric acid, all studied species of Erodium and Geranium lack this compound or contain only small amounts of it. Bauer (1991) used ﬂavonol glycosides and hydroxycinnamic acid derivatives for the identiﬁcation of Pelargonium cultivars. High polyploids and cultivars of Pelargonium contain large amounts of “geranium oil” composed of citronellol, geraniol, citronellyl, and geranyl formate and citronellic acid (Demarne 1990). Subdivision and Relationships Within the Family and Afﬁnities. Geraniaceae in their traditional circumscription have been revealed as a heterogeneous assemblage. Morphological evidence (Hallier 1923; Bortenschlager 1967; Boesewinkel 1997) and molecular data (Price and

Geraniaceae

Palmer 1993) have led to the segregation of several elements. Ledocarpaceae are still included in Geraniales, whereas Biebersteiniaceae are part of Sapindales, and Dirachmaceae belong to Rosales (see volume VI of this series). Geraniaceae in the restricted sense are supported as monophyletic by molecular analyses of various plastid and nuclear genes (Price and Palmer 1993; Savolainen, Fay et al. 2000; Soltis et al. 2000; see also Angiosperm Phylogeny Group APG II 2003). Hypseocharis, formerly included in a monotypic family, is sister to the remaining four genera, Erodium, Geranium, Pelargonium and Monsonia incl. Sarcocaulon. The fusion of the latter two genera was suggested by Price and Palmer (1993) and formally carried out by Albers (1996; see also Aldasoro et al. 2001; Touloumenidou et al., in prep.), but the taxonomic changes were rejected by Moffett (1997) and by Dreyer et al. (1997). The infrageneric subdivision in Geraniaceae is based mainly on ﬂower morphology, fruit-discharge mechanisms and karyology. Comprehensive molecular studies are available only for Monsonia (Touloumenidou et al., in prep.) and Pelargonium (Bakker et al. 2000). A cladistic analysis of morphological characters showed two major clades in Monsonia: one is formed by Monsonia sect. Monsonia including Sarcocaulon, the other contains species of Monsonia sect. Olopetalum (Aldasoro et al. 2001). On the basis of a molecular study, Touloumenidou et al. (in prep.) propose ﬁve sections in Monsonia, with Sarcocaulon included at sectional rank. The subdivision of Pelargonium is based on morphology and different chromosome numbers and sizes. The basal split into two clades, as proposed by Albers (1988), is supported by molecular studies (Bakker et al. 2000) and led to the recognition of two subgenera, Pelargonium and Ciconium. Within these subgenera, the established sections represent natural entities. The subdivision of Erodium and Geranium is based exclusively on morphology. The limited rbcL data of six species of Geranium (Price and Palmer 1993) showed that Neurophyllodes (incl. Geranium grandiﬂorum) does not deserve generic status, since it is embedded in Geranium. The monospeciﬁc genus California newly described by Aldasoro et al. (2002) is not accepted until a complete molecular study of Erodium is available. The authors argued in terms of the unique androecium of the species (total reduction of the sterile stamens) but their trnL-F analysis provides low bootstrap support.

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As a consequence of extensive molecular studies, Geraniales are restricted to Geraniaceae, Melianthaceae and Ledocarpaceae, which are the sister group of Crossosomatales. The position of these two orders within rosids is still unresolved (see Introduction to Geraniales, this volume). Distribution and Habitats. Erodium subg. Erodium has a Saharo-Sindian distribution but is absent from southern Europe; small annual and perennial anemochorous herbs predominate. Subg. Barbata is distributed all around the Mediterranean and extends to Central Asia, southern North America, southern Africa and Australia (Carolin 1958). Subg. Barbata is restricted to more mesic habitats than the more xerotolerant subg. Erodium. Erodium incarnatum, the only indigenous South African species of the genus, has been transferred into Pelargonium. Geranium is the most pronouncedly mesophytic genus of the family and is largely restricted to north temperate regions. The distribution of Geranium subg. Erodioideae is circumMediterranean, whereas subg. Robertium extends from Macaronesia to the Far East. Most sections of subg. Geranium consist of perennials of the east Mediterranean region but extend to the western Himalayas. Other subgenera contain annuals, biennials and summer-dormant tuberous species. Geranium sect. Geranium, by far the largest subgroup of the genus, is mesophytic and is worldwide in distribution, but is most speciose in tropical and subtropical mountain regions (Asia, Australia, Indonesia, Hawaiian Islands: e.g. Carolin 1964; North and South America: e.g. Robertson 1972, and Correa 1988; East and southern Africa: Laundon 1963, Müller 1963, Kokwaro 1971, Hilliard and Burtt 1985, and Gilbert and Vorster 2000). Three further sections comprise low, often acaulescent perennials restricted to higher altitudes of the Central and Northern Andes (Aedo et al. 2002). Today, several ruderal species of Erodium and Geranium are cosmopolitan weeds. Monsonia is mainly southern African; members of some sections including sect. Sarcocaulon show remarkable adaptations to arid conditions, especially in the Namib region. Their distribution extends from southern Africa via North Africa to India (Venter 1990). The vast majority of the species of Pelargonium occurs in Africa, whereas Australia has only few species. About 90% are endemic to the winter rainfall region of the western part of southern Africa.

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The centre of diversity lies in the Cape Floristic Region. Most of the sections are conﬁned to regions with regular rainfall and are part of the Coastal Fynbos. Several species survive in mountainous areas up to the alpine zone in the Drakensberg Mts., in karroid vegetation types and even in extremely dry areas in the north-western parts of southern Africa. Here, they are deciduous or die back and become dormant for the duration of the unfavourable season (Van der Walt and Vorster 1983). Species occurring in tropical East Africa are often associated with cooler highlands; those of Australia prefer regions of temperate to Mediterranean climate close to the southern coast. Hypseocharis occurs in the sub-alpine zone of the Andes from Peru through Bolivia into North Argentina at altitudes of about 2,000–4,000 m. This Andean genus may be a relic of the ancestors of Geraniaceae s.str. which occurred in Gondwana before South America separated from Africa (Boesewinkel 1988). Palaeobotany. Pollen attributed to Geranium and Pelargonium is known from the Upper Miocene of Spain, and to Pelargonium from the Pliocene of south-eastern Australia (Muller 1981). Parasites. Xanthomonas campestris pv. Pelargonii (Proteobacteria subcl. “beta/gamma”) infects both Pelargonium and Geranium species. This bacterial blight is the most serious disease of the garden geraniums (Dunbar and Stephens 1992). Economic Importance. Species and cultivars of Pelargonium and, to a lesser extent, of Geranium and Erodium are of high commercial value as ornamentals worldwide. Pelargoniums were introduced into The Netherlands and England at the beginning of the 17th century. Only ﬁve of the c. 280 species are the ancestors of the thousands of hybrids and cultivars now available. The “Royal Geraniums” are the result of crossings of P. cucullatum and P. grandiﬂorum. P. zonale and P. inquinans are the ancestors of the “Zonal Geraniums”. Different varieties of P. peltatum form the “Ivy Geraniums”. The food industry utilizes geranium oil as ﬂavour or fragrance in non-alcoholic beverages, ice-cream, candy, baked goods, puddings, jams and chewing gums (Lis-Balchin 1990). Leaf extracts of Pelargonium species show antimicrobial effects. The scented-leaf pelargoniums are highly important for the perfume industry. The reported use of Pelargonium and Monsonia species as

Fig. 51. Geraniaceae. Hypseocharis tridentata. A Habit. B Flower, with petals removed. C Schizocarp. D Same, transverse section. E Mericarp, outer and inner view. F Seed. (Slanis and Grau 2001)

antispasmodics, antidysenterics, astringents and abortifacients is mainly limited to folk medicine. Only an extract of P. sidoides and P. reniforme roots is successfully employed in modern phytotherapy in Europe to cure infectious diseases of the respiratory tract (Kolodziej and Kayser 1998). Some efforts have been made concerning genetic transformation in Pelargonium species/cultivars (Boase et al. 1998). Conservation. Pelargonium cotyledonis, endemic to the St. Helena Islands, is one of the most endangered species of this genus. Hilton-Taylor (1997) listed four Pelargonium and three Monsonia sect. Sarcocaulon species for the southern African region which are under threat. The conservation status of the latter is also reported by Craib (1995). Species of the Pelargonium sect. Hoarea which mainly occur in the southwest of South Africa are becoming rare or are already extinct due to the extensive agriculture in that area, and other species of that genus are under threat by the extension of residential areas in the coastal regions.

Geraniaceae

Key to the Genera 1. Style simple, stigma capitate; fruits not beaked; leaves estipulate 1. Hypseocharis – Style with stigmatic style branches; fruits beaked; leaves stipulate 2 2. Flowers with hypanthium and a nectariferous tube in the hypanthium 5. Pelargonium – Flowers without hypanthium and without a nectariferous tube 3 3. Perfect stamens 5, ﬂowers actinomorphic or zygomorphic 4 – Perfect stamens 10 or 15, ﬂowers actinomorphic 5 4. Stamens free 3. Erodium – Each stamen grouped with two staminodes and connate with them at the base 4. Monsonia 5. Perfect stamens 10, free 2. Geranium – Perfect stamens 15, connate at base 4. Monsonia

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Amer. spp.; Aedo, Syst. Bot. 26:205–215 (2001), rev. sect. Brasilensia; Aedo et al., Blumea 47:205–297 (2002), rev. sects. Azorelloideae, Neoandina and Paramensia; Aedo et al., Brittonia 55:93–126 (2003), rev. sect. Gracilia.

Annual or perennial herbs, occasionally subshrubs; stems herbaceous, erect to decumbent. Leaves opposite or alternate, palmatiﬁd to palmatisect, segments entire to variously lobed, stipulate. Inﬂorescences 1–3-ﬂowered pedunculate cymes. Flowers actinomorphic, only G. arboreum zygomorphic; petals white to purple, with markings; stamens 5 + 5, all fertile, connate at base; nectar glands 5, alternating with outer stamen whorl;

Genera of Geraniaceae 1. Hypseocharis J. Remy

Fig. 51

Hypseocharis J. Remy in Ann. Sci. Nat., Bot. III, 8:238– 240 (1847); Knuth, Bot. Jahrb. Syst. 41:170–174 (1908); MacBride, Field Mus. Nat. Hist. Chicago, Bot. 13, 3, no. 2:606–608 (1949); Slanis & Grau, Darwiniana 39:343–352 (2001).

Perennial acaulescent herbs with thick taproots or tubers. Leaves rosulate, pinnatiﬁd, or upper ones pinnately incised, the leaﬂets subentire or 3-lobulate or pinnate-incised, estipulate. Inﬂorescences 1–many-ﬂowered pedunculate cymes. Flowers actinomorphic; petals white, yellow, orange, brilliant red; nectary disk well developed, extrastaminal, lobed; stamens 5 or 15, all fertile, 10 short, antepetalous, 5 longer, antesepalous; ovary 5-lobed, 5-locular; ovules many per locule, axile, biseriate, anatropous to campylotropous; style simple, with capitate stigma. Fruit a tardily and irregularly loculicidal capsule, many small (c. 2 mm) seeds (schizocarpic); H. tridentata with unbeaked schizocarp, mericarps without awns, each with 1–few seeds. Six described species in high altitudes of the Andes, from Peru to northern Argentina. 2. Geranium L.

Fig. 52

Geranium L., Sp. Pl.: 676 (1753); Aedo et al., Anales Jard. Bot. Madrid 56:211–252 (1998), checklist; Knuth in Pﬂanzenreich IV, 129 (1912); Yeo, Bot. J. Linn. Soc. 67:285– 346 (1973), rev. sects. Anemonifolia and Ruberta; Aedo, Syst. Bot. Monogr. 49:1–104 (1996), rev. subg. Erodioidea; Aedo et al., Ann. Missouri Bot. Gard. 85:594–630 (1998), rev. sects. Batrachioidea and Divaricata; Aedo, Anales Jard. Bot. Madrid 58:39–82 (2000), et ibid. 59:3–65 (2001), N.

Fig. 52. Geraniaceae. Geranium maculatum. A Plant with annual shoot and perennial rhizome. B Flower at anthesis, with whorl of inner stamens dehiscing and style branches still closed. C Stamen of outer whorl. D Gynoecium with recurved style branches and nectar glands on receptacle below pubescent ovary. E Same, semidiagrammatic vertical section to show placentation. F Dehisced fruit with mericarps attached to recurved hygroscopic awns. G Transverse section of ovary, with two superposed ovules in each locule. H Seed. I Embryo. J Same, transverse section to show folding of cotyledons. (Robertson 1972)

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ovary 5-lobed, 5-locular, 2 ovules per locule. Fruit beaked, of 5 mericarps, these 1-seeded, with a spirally twisted awn; seeds ellipsoidal, keeled with two growes. About 430 species, distributed throughout the world. Yeo (1990) proposed three subgenera which are based on the mode in which the fruit break at maturity: subg. Geranium (3 sections with more than 380 species), subg. Robertium (Picard) Rouy (8 sections with 30 species) and subg. Erodioidea (Picard) Yeo (3 sections with 19 species). 3. Erodium L’Hérit. Erodium L’Hérit. in Ait. Hort. Kew. ed. 1, 2:414 (1789). California Aldasoro, Navarro, Vargas, Sáez & Aedo, Anales Jard. Bot. Madrid 59:213 (2002).

Annual or perennial herbs, rarely subshrubs; stems herbaceous, erect to decumbent. Leaves opposite or alternate, simple to pinnatisect to pinnate, stipulate. Inﬂorescences 1–many-ﬂowered pedunculate cymes. Flowers actinomorphic, rarely zygomorphic; petals white to purple, equal but sometimes unequal, when equal, then all petals often with a central marking, when unequal, then only the upper petals with markings; stamens 5, antesepalous, alternating with 5 staminodes; nectar glands 5, antesepalous; ovary 5-lobed, 5-locular, 2 ovules per locule. Fruit beaked, of 5 mericarps, these 1-seeded, with a spirally twisted and hairy awn; seeds oblongate, keeled with two grooves. About 80 species, with fairly cosmopolitan distribution and a high concentration in Mediterranean climate regions worldwide, often synanthropic. Two subgenera: subg. Erodium, anemochorous mericarps with long plumose ﬁbres on the inner surface of the awn; subg. Barbatum (Boiss.) Guitt., zoochorous mericarps, awn with unequal but rigid ﬁbres; 2 or 3 sections with subsections (Guittonneau 1990).

Fig. 53. Geraniaceae. Monsonia patersonii. A Habit. B Lateral branch armed with petioles of fallen leaves. C Leaf blade. D Flower. E Fruit. (Knuth 1912)

persisting as spines, stipulate. Inﬂorescences 1–15-ﬂowered pedunculated cymes, or ﬂowers solitary. Flowers actinomorphic; petals white to yellow, pink, mauve, bluish, often only with faint markings; stamens 15, in groups of 3, all fertile, or rarely (in one sp.) 10 sterile; nectar glands 5, alternating with outer stamen whorl; ovary 5-lobed, 5-locular, 2 ovules per locule. Fruit beaked, of 5 mericarps, these 1-seeded with a spirally twisted and, in several species, hairy awn; seeds oblongate, keeled with two grooves. About 40 species, Africa, Madagascar and southwest Asia, but most species in the drier parts of southern Africa. Albers (1996) demonstrated that Monsonia and Sarcocaulon are congeneric, and considered Sarcocaulon as a section of Monsonia. 5. Pelargonium L’Hérit.

4. Monsonia L.

Fig. 53

Monsonia L., Mant.: 14 (1767); Venter, Meded. Landbouwhogesch. Wageningen 79:1–128 (1979); Albers, S. African J. Bot. 62:345–347 (1996). Sarcocaulon (DC.) Sweet, Hort. Brit. ed. 1:73 (1826); Rehm in Bot. Jahrb. Syst. 67:264–274 (1935); Moffett, Bothalia 12:581–613 (1979); Craib, Hystrix 1:1–60 (1995).

Prostrate, decumbent or erect annual herbs or perennial subshrubs; stems herbaceous, succulent or woody. Leaves alternate or opposite, simple or rarely pinnately incised, petioles sometimes

Fig. 54

Pelargonium L’Hérit. in Ait. Hort. Kew. ed. 1, 2:417 (1789).

Perennial shrubs, subshrubs, herbs, geophytes with root tubers (rhizomes, climbers or annual herbs); stems herbaceous, subsucculent, succulent or woody, erect to decumbent. Leaves alternate, petiolate, entire to much divided to compound, often heteroblastic, petioles rarely persisting as spines; stipules membranous, herbaceous or spiny, caducous or persistent. Scape often branched with several inﬂorescences; inﬂorescences 1-manyﬂowered, pedunculate pseudoumbels. Flowers zy-

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the Arabian Peninsula, Asia Minor, Madagascar and Australia incl. New Zealand. One species on Tristan da Cunha and one on St. Helena. Two subgenera, supported by chromosomal and molecular data: subg. Pelargonium and subg. Ciconium (Bakker et al. 2000), both with several sections and subsections.

Selected Bibliography

Fig. 54. Geraniaceae. Pelargonium squamulosum. (Kunth 1912)

gomorphic, receptacle modiﬁed in a hypanthium with a nectariferous tube; sepals connate at base; petals 5(2, 4), usually unequal, white, cream, yellowish, greenish, pinkish, pink, pinkish-purple or red, upper 2 petals often with markings; androecial members 10, connate at base, 3–8 staminodial; ovary 5-lobed, 5-locular, 2 ovules per locule. Fruit beaked, of 5 mericarps, these 1-seeded, with a spirally twisted and hairy awn; seeds ellipsoidal, keeled with 2 grooves. About 280 species, of which more than 200 occur in southern Africa. The remaining are spread over East Africa,

Aedo, C., Muñoz-Garmendia, F., Pando, F. 1998. World checklist of Geranium. Anales Jard. Bot. Madrid 56:211–252. Aedo, C., Aldasoro, J.J., Navarro, C. 2002. Revision of Geranium sections Azorelloidea, Neoandina, and Paramensia (Geraniaceae). Blumea 47:205–297. Albers, F. 1988. Strategies in chromosome evolution in Pelargonium (Geraniaceae). Monogr. Syst. Bot. Missouri Bot. Gard. 25:499–502. Albers, F. 1990. Comparative karyological studies in Geraniaceae on family, genus, and section level. In: Vorster, P. (ed.) Proc. 1st International Geraniaceae Symposium, Stellenbosch University, South Africa, pp. 115–122. Albers, F. 1996. The taxonomic status of Sarcocaulon (Geraniaceae). S. African J. Bot. 62:345–347. Albers, F. 2002. Geraniaceae. In: Eggli, U. (ed.) Illustrated Handbook of Succulent Plants. Dicotyledons, pp. 241– 272. Berlin Heidelberg New York: Springer. Albers, F., Van der Walt, J.J.A. 1984. Untersuchungen zur Karyologie und Mikrosporogenese von Pelargonium sect. Pelargonium (Geraniaceae). Pl. Syst. Evol. 147:177–188. Albers, F., Gibby, M., Austmann, M. 1992. A reappraisal of Pelargonium sect. Ligularia (Geraniaceae). Pl. Syst. Evol. 179:257–276. Aldasoro, J.J., Navarro, C., Vargas, P., Aedo, C. 2001. Anatomy, morphology, and cladistic analysis of Monsonia L. (Geraniaceae). Anales Jard. Bot. Madrid 59:75–100. Aldasoro, J.J., Navarro, C., Vargas, P., Saez, L., Aedo, C. 2002. California, a new genus of Geraniaceae endemic to the southwest of North America. Anales Jard. Bot. Madrid 59:209–216. APG II 2003. See general references. Bakker, F.T., Culham, A., Pankhurst, C.E., Gibby, M. 2000. Mitochondrial and chloroplast DNA-based phylogeny of Pelargonium (Geraniaceae). Amer. J. Bot. 87:727– 734. Bate-Smith, E.C. 1973. Chemotaxonomy of Geranium. Bot. J. Linn. Soc. 67:347–359. Bauer, H. 1991. Untersuchungen zur Anwendbarkeit von Phenol-Bestimmungen bei der Charakterisierung von Genotypen unter dem Aspekt des Sortenschutzes. Ph.D. Thesis, Technische Universität München, 196 p. Boase, M.R., Bradley, J.M., Borst, N.K. 1998. An improved method for transformation of regel pelargonium (Pelargonium X domesticum Dubonnet) by Agrobacterium tumefaciens. Pl. Sci. 139:59–69. Boesewinkel, F.D. 1988. The seed structure and taxonomic relationships of Hypseocharis Remy. Acta Bot. Neerl. 37:111–120.

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Boesewinkel, F.D. 1997. Seed structure and phylogenetic relationships of the Geraniales. Bot. Jahrb. Syst. 119:277– 291. Boesewinkel, F.D., Ben, W. 1979. Development of ovule and testa of Geranium pratense L. and some other representatives of the Geraniaceae. Acta Bot. Neerl. 28:335– 348. Bortenschlager, S. 1967. Vorläuﬁge Mitteilungen zur Pollenmorphologie in der Familie der Geraniaceen und ihre systematische Bedeutung. Grana Palynol. 7:400– 468. Carolin, R.C. 1958. The species of the genus Erodium L’Hér. endemic to Australia. Proc. Linn. Soc. New South Wales 83:92–100. Carolin, R.C. 1964. The genus Geranium L. in the south western Paciﬁc area. Proc. Linn. Soc. New South Wales 89:326–361. Corner, E.J.H. 1976. See general references. Correa, M.N. 1988. Geraniaceae. In: Flora Patagonica 5:30– 39. Buenos Aires: INTA. Craib, C. 1995. The sarcocaulons of southern Africa. Hystrix 1:1–60. Demarne, F.-E. 1990. Essential oils in Pelargonium, sect. Pelargonium. In: Vorster, P. (ed.) Proc. 1st International Geraniaceae Symposium, Stellenbosch University, South Africa, pp. 245–268. Dreyer, L.L., Marais, E.M. 2000. Section Reniformia, a new section in the genus Pelargonium (Geraniaceae). S. African J. Bot. 66:44–51. Dreyer, L.L., Leistner, O.A., Burgoyne, P., Smith, G.F. 1997. Sarcocaulon: genus or section of Monsonia (Geraniaceae)? S. African J. Bot. 63: 240. Dunbar, K.B., Stephens, C.T. 1992. Resistance in seedlings of the family Geraniaceae to bacterial blight caused by Xanthomonas campestris pv. pelargonii. Pl. Disease 76:693–695. Gibby, M., Hinnah, S., Albers, F., Marais, E.M. 1996. Cytological variation and evolution within Pelargonium sect. Hoarea. Pl. Syst. Evol. 203:111–142. Gilbert, M.G., Vorster, P. 2000. Geraniaceae. In: Edwards, S., Tadesse, M., Demissew, S., Hedberg, I. (eds) Flora of Ethiopia and Eritrea, vol. 2, 1, pp. 364–378. Addis Ababa: Ethiopian National Herbarium. Guittonneau, G.-G. 1972. Contribution à l’étude biosytématique du genre Erodium L’Hér. dans le bassin méditerranéen occidental. Boissiera 20:9–154. Guittonneau, G.-G. 1990. Taxonomy, ecology, and phylogeny of the genus Erodium L’Hér. in the Mediterranean region. In: Vorster, P. (ed.) Proc. 1st International Geraniaceae Symposium, Stellenbosch University, South Africa, pp. 69–91. Hallier, H. 1923. Beiträge zur Kenntnis der Linaceae (DC. 1819) Dumort. 25. Lepidobotrys Engl., die Oxalidaceen und die Geraniaceen. Beih. Bot. Centralbl. 39, 2:1– 178. Hilliard, O.M., Burtt, B.L. 1985. A revision of Geranium in Africa south of the Limpopo. Notes Roy. Bot. Gard. Edinburgh 42:171–225. Hilton-Taylor, C. 1997. Threatened succulents recorded for the Flora of Southern Africa (FSA) region. In: Oldﬁeld, S. (comp.) Cactus and succulent plants. Status Survey and Conservation Action Plan. IUCN/SSC Cactus and Succulent Specialist Group, IUCN, Gland, Switzerland, 212 pp.

Huynh, K.-L. 1969. Etude du pollen des Oxalidaceae, 1. Bot. Jahrb. Syst. 89:272–303. Jones, C.S., Price, R.A. 1996. Diversity and evolution of seedling Baupläne in Pelargonium (Geraniaceae). Aliso 14:281–295. Knuth, R. 1912. Geraniaceae. In: Pﬂanzenreich IV, 129. Leipzig: W. Engelmann. Kokwaro, J. 1971. Geraniaceae. In: Milne, E., Polhill, R.M. (eds) Flora of Tropical East Africa. London: Government Printer, pp. 1–24. Kolodziej, H., Kayser, O. 1998. Pelargonium sidoides DC. Neueste Erkenntnisse zum Verständnis des Phytotherapeutikums Umckaloabo. Zeitschr. Phytotherapie 19:141–151. Laundon, J.R. 1963. Geranium. In: Exell, A.W., Fernandes, A., Wild, H. (eds) Flora Zambesiaca 2:131–136. Royal Botanic Gardens, Kew. Link, D. 1990. The nectaries of Geraniaceae. In: Vorster, P. (ed.) Proc. 1st International Geraniaceae Symposium, Stellenbosch University, South Africa, pp. 215–225. Lis-Balchin, M. 1990. The commercial usefulness of the Geraniaceae, including their potential in the perfumery, food manufacture, and pharmacological industries. In: Vorster, P. (ed.) Proc. 1st International Geraniaceae Symposium, Stellenbosch University, South Africa, pp. 269–277. Meisert, A. Schulz, D., Lehmann, H. 2001. The ultrastructure and development of the light line in the Geraniaceae seed coat. Pl. Biol. 3:351–356. Meve, U. 1995. Autogamie bei Pelargonium-Wildarten. Palmengarten 59:100–108. Moffett, R.O. 1997. The taxonomic status of Sarcocaulon. S. African J. Bot. 63:239–240. Müller, T. 1963. Pelargonium. In: Exell, A.W., Fernandes, A., Wild, H. (eds) Flora Zambesiaca 2:140–149. Royal Botanic Gardens, Kew. Muller, J. 1981. See general references. Price, R.A., Palmer, J.D. 1993. Phylogenetic relationships of the Geraniaceae and Geraniales from rbcL sequence comparisons. Ann. Missouri Bot. Gard. 80:661–671. Robertson, K.R. 1972. The genera of Geraniaceae in the southeastern United States. J. Arnold Arb. 53:182–201. Ronse DeCraene, L.P., Smets, E.F. 1995. The distribution and systematic relevance of the androecial character oligomery. Bot. J. Linn. Soc. 118:193–247. Savolainen, V., Fay, M.F. et al. 2000. See general references. Slanis, A.C., Grau, A. 2001. El genero Hypseocharis (Oxalidaceae) en la Argentina. Darwiniana 39:343–352. Soltis, D.E. et al. 2000. See general references. Stafford, P.J., Blackmore, S. 1991. Geraniaceae. In: Punt, W., Blackmore, S. (eds) The Northwest European Pollen Flora 6:49–78. Amsterdam: Elsevier. Stafford, P.J., Gibby, M. 1992. Pollen morphology of the genus Pelargonium (Geraniaceae). Rev. Palaeobot. Palynol. 71:79–109. Struck, M. 1997. Floral divergence and convergence in the genus Pelargonium (Geraniaceae) in southern Africa: ecological and evolutionary considerations. Pl. Syst. Evol. 208:71–97. Van der Walt, J.J.A. 1977. Pelargoniums of Southern Africa. Cape Town: Purnell. Van der Walt, J.J.A., Vorster, P.J. 1981. Pelargoniums of Southern Africa, vol. 2. Cape Town: Juta.

Geraniaceae Van der Walt, J.J.A., Vorster, P.J. 1983. Phytogeography of Pelargonium. Bothalia 14:517–523. Van der Walt, J.J.A., Vorster, P.J. 1988. Pelargoniums of Southern Africa, vol. 3. Kirstenbosch: National Botanical Gardens. Van der Walt, J.J.A., Werker, E., Fahn, A. 1987. Wood anatomy of Pelargonium (Geraniaceae). IAWA Bull. N.S. 8:95–108. Van Loon, J.C. 1984a. Chromosome numbers in Geranium from Europe. I. The perennial species. Proc. Koninkl. Ned. Akad. Wetensch. C, 87:263–277. Van Loon, J.C. 1984b. Chromosome numbers in Geranium from Europe. II. The annual species. Proc. Koninkl. Ned. Akad. Wetensch. C, 87:279–296. Venter, H.J.T. 1990. An account of Monsonia. In: Vorster, P. (ed.) Proc. 1st International Geraniaceae Symposium, Stellenbosch University, South Africa, pp. 331–351. Verhoeven, R.L., Marais, E.M. 1990. Pollen morphology of the Geraniaceae. In: Vorster, P. (ed.) Proc. 1st International Geraniaceae Symposium, Stellenbosch University, South Africa, pp. 137–173.

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Verhoeven, R.L., Venter, H.J.T. 1986. Pollen morphology of Monsonia. S. African J. Bot. 52:361–368. Vogel, S. 1998. Remarkable nectaries: structure, ecology, organophyletic perspectives, IV. Miscellaneous cases. Flora 193:225–248. Weber, M. 1996. The existence of a special exine coating in Geranium robertianum pollen. Intl J. Pl. Sci. 157:195– 202. Williams, Ch.A., Newman, M., Gibby, M. 2000. The application of leaf phenolic evidence for systematic studies within the genus Pelargonium (Geraniaceae). Biochem. Syst. Ecol. 28:119–132. Yeo, P.F. 1973. The biology and systematics of Geranium, sections Anemonifolia Knuth and Ruberta Dum. Bot. J. Linn. Soc. 67:285–346. Yeo, P.F. 1984. Fruit-discharge-type in Geranium (Geraniaceae): its use in classiﬁcation and its evolutionary implications. Bot. J. Linn. Soc. 89:1–36. Yeo, P. 1990. The classiﬁcation of Geraniaceae. In: Vorster, P. (ed.) Proc. 1st International Geraniaceae Symposium, Stellenbosch University, South Africa, pp. 1–22.

Grossulariaceae Grossulariaceae DC. in Lam. & DC., Fl. Franç., ed. 3., 4, 2:405 (1805), nom. cons.

M. Weigend

Shrubs, sometimes dioecious, 0.1–7 m tall, erect, prostrate or lianescent with regular and very short internodes, unarmed or with simple or ternate nodal and/or simple internodal spines, stem initially with white pith, terete, bark dark brown to black, later often exfoliating in strips; horizontal underground stems often present; indumentum of subsessile and/or unicellular and pluriseriate, glandular or eglandular trichomes on young shoots, leaves, ﬂowers and fruits. Leaves deciduous or evergreen, alternate, petiolate, rarely subsessile; stipules usually dry, brown and ﬁmbriate; bud scales dry and brown, rarely membranaceous, usually pubescent and/or glandular; lamina ovate to subcircular, rarely ﬂabellate, membranaceous to coriaceous, 0.5–25 cm in diameter, base cuneate to deeply cordate, usually trilobate, or subpalmately lobed, rarely undivided; margin irregularly lobulate and coarsely serrate with hydathode teeth, rarely subentire, usually pubescent at least abaxially, sometimes densely covered with resin or wax; venation palmate with usually three major veins; ptyxis mostly plicate, rarely convolute. Inﬂorescences usually on short shoots, racemose, pendulous, or rarely erect, (1–)5–50-ﬂowered, axis sometimes with very short, sometimes distally contracted and inﬂorescence appearing corymbose, each ﬂower with a pubescent and often ﬁmbriate bract and usually two smaller prophylls, rarely with a single, amplexicaul prophyll. Flowers hermaphroditic or unisexual, chasmogamous, proterandric or protogynous, erect or pendulous, actinomorphic, (4)5-merous; hypanthium distinct, patelliform to long-cylindrical and usually persistent in fruit; calyx lobes usually oblong-acuminate, erect, spreading or reﬂexed, rarely erect with reﬂexed apex, green, white, yellow or red; petals distinct, rarely absent, erect or spreading, margin entire, ovate or oblong with narrowed base, rarely ﬁliform or ﬂabellate, ﬂat or sometimes involute, membranaceous, green, white, yellow or red, aestivation apert; androecium haplostemonous, stamens an-

tesepalous, all fertile or all staminodial; ﬁlaments ﬁliform, insertion episepalous; anthers included or long-exserted, basiﬁxed, with 4 microsporangia; connective undifferentiated or with distal nectary, staminodia undifferentiated with poorly developed thecae, or fully developed thecae but without viable pollen; nectary a well-developed, often 5-lobed disc; ovary in hermaphroditic and female ﬂowers well developed, completely inferior to 1/3 superior, conical to globose, glabrous to densely glandular and/or pubescent, with 2 parietal, slightly intrusive placentae, in male ﬂowers very small, undifferentiated or with poorly developed ovules; style conical to ﬁliform with two stigmatic branches and two papillose stigmas, included or exserted, basally often densely pubescent; ovules numerous, anatropous, bitegmic, crassinucellar with well-developed chalazal haustoria. Fruit a soft berry crowned with the persistent perianth, often covered with unicellular or glandular trichomes, yellow, orange, red, black, rarely white and/or covered with waxy bloom, acidic or insipid; seeds (3–)10–60, with outer mucilaginous layer and a hard, brown to black seed coat; embryo small, straight, embedded in copious starch-free, oily endosperm; seedlings with 2 ovate to elliptical cotyledons, these apically emarginate with midvein ending in hydathode tooth, often pubescent and glandular. One genus with 150–200 species in the northern temperate zone and South America, with outliers in northern Africa, Southeast Asia and Central America. Vegetative Morphology. Ribes consists exclusively of shrubs typically differentiated into short shoots and long shoots. The vast majority of taxa branches at the base and has numerous strong, self-supported, widely spaced branches. Prostrate stems or underground runners are occasionally found in all major groups of Ribes but are particularly typical of subg. Symphocalyx and subg. Ribes sect. Heritiera. Many species form large clonal

Grossulariaceae

stands in this way. Species with this type of growth are especially abundant in riparian forests and swamps (R. glandulosum, R. nigrum) and in alpine habitats (e.g. R. nitidissimum in Patagonia). At least one species forms dwarf shrubs only c. 15 cm high in high Andean habitats, some species have very dense and squarrose branching (i.e. many short shoots: R. cuneifolium), while others make very long internodes on thin shoots and thus climb in cloud forests (R. incarnatum and allied South American taxa). The epidermis of the shoots often exfoliates in long strips in the second year, and is then replaced by a well-developed periderm. Exfoliation is particularly striking in many species of subg. Ribes (sect. Berisia and sect. Ribes). Ribes subg. Ribes sect. Berisia, subg. Grossularioides and subg. Grossularia have spines, which are usually found at the leaf nodes (nodal spines) but also scattered over the entire shoot (internodal spines, e.g. R. horridum). Spines seem to have evolved twice independently, once in the Berisia lineage and once in the Grossularioides/Grossularia lineage. They are typical emergences developing from the epidermis and the subjacent parenchyma; internodal spines are sometimes gland-tipped (especially in R. subg. Grossularioides) and are derived from conical setae (see below). Foliage of Ribes is mostly deciduous, rarely evergreen. Evergreen species are found in alpine habitats in the Himalayas (R. laurifolium, R. davidii) and in Mediterranean habitats in California (R. viburnifolium), semi-evergreen species in South America (R. cuneifolium, R. ovalifolium) and East Asia (R. fasciculatum). Evergreen and semievergreen taxa generally have coriaceous and undivided or shallowly lobed leaves, while most Ribes have 3–5-lobed laminas. This leaf type is found in all infrageneric groups and can be considered as plesiomorphic. Leaf venation is always palmate with three veins entering the lamina, irrespective of leaf outline. Vegetative Anatomy. The plants are usually covered with different types of trichomes, some of which are informative in classiﬁcation (Weigend and Binder 2001). Unicellular trichomes are usually white and lack a glandular apex. Glandular trichomes are very widespread and always have a pluricellular head. Sessile glands are disc-shaped, rarely globose, and are found in two different subtypes: sessile resin glands (surrounded by a persistent layer of resinous secretion) and non-resinous sessile glands (lacking any visible secretion in the

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Fig. 55. Grossulariaceae. Ribes viburnifolium. Sessile nonresinous gland and unicellular trichomes from inferior portion of ovary, SEM micrograph. (Orig.)

dry stage and with at most a clear secretion at their tip in the living stage; Fig. 55). Subsessile glands are non-resinous and have a short, pluriseriate stalk which is shorter than or equal in length to the diameter of the glandular head of the trichome; they are often characteristic of certain species (cf. ovary of R. andicola). Stalked glands are pluriseriate trichomes c. 1 mm long with a well-developed secretory head. Conical setae differ in having a conical stalk 2–10 mm long. The tip of the conical setae is usually glandular, but the development of the apical gland can be retarded or suppressed. They are not usually found on leaf surfaces but are frequently present on stipules and stems, and the entire distal margin of the stipule can be laciniate and divided into conical setae. Plumose setae are conical setae which are densely covered with unicellular trichomes and are thus compound trichomes. There is a more or less gradual transition from conical setae to internodal spines in a few species (e.g. sect. Grossularioides, sect. Berisia). Nodal spines are apparently of different derivation, but their ontogeny has not been studied so far. The nodes are always trilacunar, and three veins enter the lamina. The lamina is usually hypostomatic, very rarely amphistomatic (R. cereum); stomata are anomocytic. Both the adaxial and abaxial epidermis is uniseriate. The mesophyll has usually 1–2, rarely up to 4 layers of palisade parenchyma with a few interspersed tanniniferous cells. Crystal druses 6–35 µm in diameter are found in the spongy and palisade parenchyma and the collenchyma along the leaf veins. Hydathodes are universally present at the leaf teeth.

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The stem anatomy of Ribes has been studied in a few, mostly North American and European taxa (Janczewski 1907; Metcalfe and Chalk 1950; Stern et al. 1970). Young shoots are ﬁlled with a distinct white pith of spongy parenchyma. Growth rings are usually present in the wood, but not very distinct. The xylem cylinder is interspersed with clear narrow, medullary or ligniﬁed rays. The xylem has scalariform perforation plates, rarely also simple plates and transitional to opposite intervascular pitting; axial xylem parenchyma is usually absent. Vessels are very narrow (25–50 µm in diam.) and form a tangential pattern in some species. Both homocellular and heterocellular vascular rays are present, as are more or less distinctly septate ﬁbre tracheids. Underground stems have a well-differentiated endodermis. The hypodermis is usually massively developed, and has either thickened cells walls (subg. Grossularia) or consists of thin-walled cells (all other subgenera, Weigend et al. 2002). Tanniniferous cells are common in the leaves, petiole, cortex, phloem, pith and medullary rays. Cystoliths are frequently present in non-ligniﬁed tissues of the stems (Stern et al. 1970). Inﬂorescence and Flower Structure. The inﬂorescences of Ribes are very uniform and usually racemose (Fig. 56A); additional racemes arise very rarely from the usually sterile bracts on the main axis, but reductions to few-ﬂowered racemes and apparently axillary ﬂowers are pronounced in some Asian taxa (R. ambiguum, R. fasciculatum) and most gooseberries (R. subg. Grossularia, Fig. 56K). Ribes viburnifolium from California has very short internodes in the inﬂorescence, and these appear corymbose. The inﬂorescences usually arise on short shoots but the terminal bud on long shoots also usually produces an inﬂorescence, albeit not in subg. Ribes sects. Ribes and Heritiera. The inﬂorescences are nearly universally pendulous, irrespective of size, but both dioecious groups in Ribes (subg. Parilla sect. Andina and subg. Ribes sect. Berisia) have a few species with stifﬂy erect inﬂorescences elevated above the foliage. The bracts are typically ovate to narrowly ovate and more or less equal to the pedicel in length, but in subg. Ribes they are often much shorter than the pedicel and have a truncate apex. Prophylls are usually present. The ﬂowers of Ribes are simple and uniform. The petals are always small and often included in the calyx (Fig. 56D), so that the attractive function of the perianth is usually shared by, or com-

Fig. 56. Grossulariaceae. A–D Ribes incarnatum. A Flowering shoot. B Vegetative shoot. C Stipulate petiole base. D Flower. E–G R. sanguineum, heteroblastic series from bud scale to foliage leaf, with gradually reduced stipular portion. H R. roezlii, ﬂowering branch. I R. triste, ﬂower, nectary dotted. R. speciosum. J Spiny fruit. K Flower. (A–D Weigend and Binder 2001; E–K orig.)

pletely relegated to the calyx. Flower colours are highly variable and most major groups have a wide range of colours. The hypanthium is sometimes very short and ﬂat (Fig. 56I, typically in subg. Ribes, subg. Grossularioides, and individual species in all other subgenera except Grossularia), bowl-shaped (all groups), or rarely long and more or less cylindrical (subg. Symphocalyx, subg. Grossularia). The only structural variation of the hypanthium is the occurrence of small invaginations above the point of petal insertion and sometimes the point of ﬁl-

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171

1977). The inner integument is usually 2–3-layered, and the outer 3–5-layered. The outer epidermis of the outer integument and sometimes also the inner epidermis of the inner integument consist of tanniniferous cells. The exact fate of the different integumentary layers during seed ontogeny is still unknown. Endosperm formation is ab initio cellular in subg. Ribes (R. orientale, R. rubrum, R. spicatum) and helobial in subg. Grossularia (R. burejense, R. uva-crispa, R. divaricatum, R. missouriense, R. oxyacanthoides; Davis 1966), but has not been studied for the other groups.

Fig. 57. Grossulariaceae. Ribes multiﬂorum. Hypanthium with ﬁlament bases, tiny petals and wide calyx lobes and the invaginations of the nectary, SEM micrograph. (Orig.)

ament insertion (Fig. 57, R. multiﬂorum, R. manshuricum). The calyx lobes are usually spreading or reﬂexed, occasionally erect and forming a tube (R. speciosum, Fig. 56K). Many species of subg. Grossularia have reﬂexed calyx lobes and porrect petals (Fig. 56H), and some species of subg. Ribes have porrect calyx lobes with a strongly ciliate margins (e.g. R. meyeri). Petals are often ovate or oblong with a narrowed base (most species), rarely ﬂabellate (e.g. subg. Ribes, subg. Grossularioides), long-acuminate (some species of subg. Coreosma), ﬁliform (R. fasciculatum) or involute (many species of subg. Grossularia). The anthers are usually included when a long hypanthium is present, but often distinctly exserted (e.g. subg. Symphocalyx, Grossularia, Fig. 56H). The presence of nectar glands on the connective has been used as an important character in classiﬁcation (Janczewski 1907), but its systematic relevance has yet to be critically evaluated. The ovary is usually completely inferior and the receptacle is planar, but one group in subg. Ribes has a 1/3 superior ovary with a conical style. The nectary is very strongly developed and forms an extensive disc or cup; nectar is secreted from modiﬁed stomata. Embryology. Only a few species of Ribes have been subject to embryological studies. Ovules are anatropous, crassinucellar and bitegmic, and have a distinct chalazal haustorium. The funicle develops an obturator opposite the micropyle (Weigend et al. 2002), which has been termed “aril” (Krach

Pollen Morphology. Pollen morphology of Ribes has not been extensively studied with SEM, and relatively few useful data have been published. Verbeek-Reuvers (1980) studied the pollen of European species corresponding to three subgenera (subg. Grossularia, subg. Ribes sects. Ribes and Berisia, subg. Coreosma). These are here supplemented by a few original observations from the other subgenera. The pollen grains are 15–40 µm in diameter, prolate, ellipsoidal or globose in outline, and always have characteristic ectoapertures (i.e. rugose areas around the endoapertures). The apertures are rarely symmetrical and regular; more often they are of different sizes and without clear symmetry. The pollen grains are pantoporate with 5–6 pori (R. alpinum, R. nigrum), zonocolporate with 8 or more pori (R. uva-crispa), pantoporate with (6–)8–14 pori

Fig. 58. Grossulariaceae. Ribes multiﬂorum. Pollen grain, SEM micrograph. (Orig.)

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(R. rubrum, R. spicatum, R. petraeum, Fig. 58), or pentacolpo-di-orate (R. divaricatum). The exine is either nearly smooth (R. alpinum), shallowly and irregularly rugulose to punctate (most species), or reduced to irregularly rugulose remnants (R. inebrians) or distinct spines (R. lacustre). Karyology and Hybridization. Chromosome counts are available for c. two thirds of the species and uniformly show a chromosome complement of 2n = 16 (compiled in Sinnott 1985). The chromosomes are small (c. 1.5–2.5 µm long) and relatively uniform. Natural polyploidy has not been documented. Hybridization has been extensively studied both in artiﬁcial and natural hybrids. Natural hybridization has been documented mostly within narrowly related species groups such as the subg. Coreosma (Andersson 1943) and the “western gooseberries” of subg. Grossularia (Mesler et al. 1991). Natural hybridization is locally important in the South American Andes, where as many as three distinct species may locally form complex hybrid swarms (pers. obs.). Some degree of pollen sterility is observed even in hybrids between closely related species (Mesler et al. 1991). Various horticultural hybrids have been successfully established, and hybrid viability and fertility depend strongly on the closeness of the phylogenetic relationship between parental species (Janczewski 1907; Keep 1962). Hybrids between distantly related taxa often die at the seedling stage (Keep 1962), or have an irregular meiosis and strongly reduced pollen viability (Meurman 1928). Pollination and Breeding systems. The ﬂowers of Ribes are usually small and either homogamous, proterandric or protogynous. Most Ribes have hermaphroditic ﬂowers but two groups are dioecious: the female ﬂowers of subg. Parilla produce poorly differentiated pollen which remains in a compact mass, and the male ﬂowers produce abortive ovules in an externally normal ovary. Dioecy is further derived in subg. Berisia where the female ﬂowers have sterile anthers without a clear sporogenous tissue, and the male ﬂowers lack a differentiated ovary. Pollen sterility has been documented from a range of apparently hermaphroditic species in Ribes (Janczewski 1907), and this indicates that gynodioecy may be widespread in Ribes which would, in turn, render the independent evolution of dioecy in two unrelated groups more plausible. This may

also explain why fruit set is higher with crosspollination, despite the fact that some selﬁng does occur in species with hermaphroditic ﬂowers (e.g. R. nigrum, R. rubrum, R. uva-crispa, Free 1993). Most species are entomogamous. Observations on ﬂower visitors have been published for European species (Knuth 1898; Free 1993; Schweitzer 1996) and for a few North American species from cultivation in Europe (Knuth 1898); less detailed data are available on North American taxa in their natural habitats (Catling et al. 1998). There is broad congruence across the Atlantic and across a wide range of distantly related species; pollination seems to be largely unspecialized. Diptera and Hymenoptera predominate amongst ﬂower visitors in typical, open Ribes ﬂowers. All Ribes species are visited by honey bees and bumblebees (Hymenoptera: Apidae: Apis, Bombus, Nomada), and frequently various other bee groups (Hymenoptera: Andrenidae, Halictidae, Anthrophoridae). Blowﬂies (Diptera: Calliphoridae) are also often observed, and the ﬂat and open ﬂowers of many members of subg. Ribes are frequently visited by dung ﬂies (Diptera: Scatophagidae) and hoverﬂies (Diptera: Syprhidae). Conclusive evidence for effective pollination has been presented only for honey bees. Some species in three groups of Ribes (subg. Parilla, Grossularia and Calobotrya) have progressed towards hummingbird pollination; they have mostly red, or red and green ﬂowers with a long and tubular hyphanthium and/or porrect calyx lobes and/or petals, and stigmas and anthers usually exserted from the perianth. In (south-)western North America (subg. Grossularia and Calobotrya), numerous species are exclusively (R. speciosum) or mostly (R. lobbii, R. divaricatum, R. sanguineum) pollinated by hummingbirds (Pojar 1975). Fruit and Seed. Ribes is uniform in fruit morphology and all species have berries, which differ essentially in indumentum, size, shape, colour and seed number. The dry perianth and androecium persist on the developing berry. The exocarp is thinly membranaceous, often covered with a thin, white wax layer and more or less numerous trichomes, rarely with thin spines. Meso- and endocarp are soft and juicy in the mature fruit. Seed numbers vary between (3–)10 and 60; species with many seeds usually have small seeds (< 1 mm, R. ambiguum = sect. Microsperma) whereas those with few seeds have much larger ones (c. 4 mm long, R. nitidissimum). The seeds are covered with

Grossulariaceae

a mucilaginous outer testa (myxotesta) of 3–6 layers of large cells with thin cell walls, and a hard, inner testa of one layer of small cells containing calcium oxalate crystals with thick but not ligniﬁed cell walls and an innermost layer of narrow, longitudinally elongate, tanniniferous cells. The cells of the endosperm have walls of storage cellulose 5–10 µm thick and cell lumina ﬁlled with oil droplets. The embryo is weakly differentiated and very small. The fruits usually disarticulate at the point of prophyll attachment in most subgenera but remain ﬁrmly attached to the pedicel in subg. Grossularia. The fruits of Ribes are eaten by many mammals (incl. humans) and birds, and the seeds are endozoochorous. Phytochemistry. Phytochemistry of Ribes has been repeatedly studied and compiled (Hegnauer 1973, 1990; Bate-Smith 1976), but only R. nigrum has been screened for a wide range of compounds. Iridoids are absent; ﬂavonoids and tannins (ellagitannins) are widespread. Flavonoids are abundant and varied, and are found both in the leaves and on their surfaces. Proanthocyanidins (prodelphinidin and procyanidin), quercetin, kaempferol and myricetin glycosides are nearly universally found, but more exotic compounds such as galangin, pinocembrin 7-methyl ether (Bohm 1993) and ﬂavonoid acylglycosides (Gluchoff-Fiasson et al. 2001) have also been documented. Anthocyanins have been found in fruits (Le Lous et al. 1975). Ribes is usually weakly cyanogenic; nitrile-containing compounds such as nigrumin-5-p-coumarate (Lu 2002) have been identiﬁed. Volatile oils are widespread in the subg. Coreosma and Calobotrya and subg. Parilla sect. Parilla, all of which have essentially the same odour. R. nigrum (subg. Coreosma) yielded a complex mixture of monoand sesquiterpenes (i.a. ∆3 -carene, caryophyllene, geraniol) plus various other components (methyl salicylate, benzaldehyde, oct-1-en-3-ol). The volatile oils are secreted from the sessile yellow oil glands. The volatile components of the numerous odoriferous species in other groups (subg. Ribes sect. Berisia, subg. Parilla sect. Andina) have so far not been identiﬁed. A single report concerns a diterpenic acid, hardwickiic acid, identiﬁed in R. nigrum (George et al. 1974). The endosperm of Ribes seeds consists mainly of storage cellulose, proteins and c. 10–20% oil. The oil fraction of Ribes nigrum is very high in unsaturated fatty acids (47–49% linoleic acid, 12– 14% (α- & γ-) linolenic acid, 3–4% stearidonic acid, Artaud 1992).

173

Distribution and Ecology. Ribes is found in temperate regions of Eurasia, North America and Patagonia. In the Mediterranean region, Southeast Asia, Central and South America, the genus is restricted to montane and alpine habitats. Northtemperate, mesophilic species were evidently the starting point of the evolution of the xerotolerant and xerophilic species (Janczewski 1907). Morphologically, they are most similar to the closely related Saxifragaceae s.str. Occasionally, Ribes can be an important and even dominant element of scrub forests (evergreen, sclerophyllous species in Mediterranean climates, such as R. viburnifolium in Baja California and R. punctatum in Chile), but is more typically found in the undergrowth of broad-leaved and conifer forests. Pure stands of Ribes in the form of small forests are extremely rare (R. cuneifolium and R. viscosum in Peru) but are of crucial importance for the Andean avifauna. Some species are frost-hardy, and the genus is distributed far into the north of Siberia (R. fragrans) and also represents some of the highest-growing woody plants in the Andes (over 4,000 m). The major centres of species diversity (with approximately equal species numbers) are in the Himalayas, North America and the Andes. The South American subg. Parilla shows the widest range of habitats and growth habits, and displays extraordinary morphological diversiﬁcation (leaf morphology, indumentum, inﬂorescence and ﬂoral characters), indicating a massive and relatively recent adaptive radiation. Parasites. The genus Ribes is subject to attack by a large number of pests both in nature and in cultivation. A co-evolution of some parasites with the plants is likely, since many pests are speciﬁc to the genus or certain subgroups. Breeding efforts aim at developing multiply resistant cultivars of Ribes. The economically most important pest is the white pine blister rust (Cronartium ribicola, Basidiomycetes), which has Ribes and certain Pinus species (subg. Strobus sect. Quinquaefoliae) as alternate hosts. White pine blister rust can destroy entire pine forests, and large-scale eradication programs of Ribes have been carried out in the USA to control this pest. Consequently, the cultivation of Ribes is banned in many federal states. Some Ribes are highly susceptible to Cronartium while other species or cultivars are largely or completely resistant; resistance follows no systematic pattern. Puccinia caricina (Basidiomycetes) is another speciﬁc rust of Ribes, with

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M. Weigend

the alternate generation on Carex (Cyperaceae). There is also a whole range of highly host-speciﬁc invertebrate pests which attack only Ribes and are often restricted to gooseberries or currants, such as individual species of midges (Diptera, Cecidomyiidae: Dasyneura), sawﬂies (Diptera, Tenthredinidae: Nematus, Pteronidea), aphids (Homoptera, Aphididae: Aphidula, Cryptomyzus) and moths (Lepidoptera, Pyralididae: Zophodia; Incurviidae: Incuvaria). Subdivision. Ribes falls into a number of readily distinguished groups which have been variously treated as independent genera, subgenera or sections. The entities themselves have hardly changed in the past 200 years. They are retrieved by both morphological (Janczewski 1907) and molecular (Weigend et al. 2002) analyses. The only entity which has found wide acceptance at genus level outside Ribes are the gooseberries (Grossularia), but this group can be clearly shown to be a very derived lineage within Ribes linked to the morphologically more typical representatives via the spiny currants (subg. Grossularioides). The relationships between the readily deﬁned subgroups have proved enigmatic but have been partially clariﬁed by molecular data. Afﬁnities. Grossulariaceae have been treated as a monogeneric family (Takhtajan 1997), as a family comprising some, or all woody Saxifrages (Cronquist 1981), or as part of the very broadly deﬁned Saxifragaceae (Engler 1890). A presumed afﬁnity of Ribes to other woody Saxifragales (Itea, Pterostemon, Tetracarpaea) found no support from, e.g. phytochemistry (phenolic compounds: Bate-Smith 1962, 1976; iridoids: Hegnauer 1973, 1990), serology (Grund and Jensen 1981) or embryology (Takhtajan 1996). All these lines of evidence more or less unequivocally pointed to the herbaceous Saxifragaceae as the closest relatives of Ribes. Striking similarities are found in ﬂoral structure, which is nearly indistinguishable between Ribes and most Saxifragaceae s.str. (Bensel and Palser 1975), and in vegetative morphology: the leaves of most Saxifragaceae s.str. and Ribes show a highly characteristic heteroblastic series from brown, chartaceous bud scales to leaves with membranaceous and laciniate stipules to apparently estipulate distal leaves (stipules reduced to ﬁmbriate petiole margins, Fig. 56E–G). Mature leaves are similar in shape and structure (long-petiolate with cordate base, lamina membranaceous, with two dominant

lateral veins). The shoots of Saxifragaceae s.str. are differentiated into inﬂorescence-bearing short shoots (= leaf rosettes, with elongating internodes only in the inﬂorescence) and elongating branches, which are responsible for vegetative growth. This pattern is identical to that found in Ribes, with the only exception that most branches are here stiff and erect, while they are creeping and often rhizomatous in Saxifragaceae. The ﬁrst internodes of Ribes seedlings are very short (atypical for woody plants; Janczewski 1907) and the seedlings are subrosulate and thus strongly reminiscent of seedlings and mature plants in Saxifragaceae s.str. The vegetative axes in both Saxifragaceae and Ribes are typically lignescent to ligneous. The inﬂorescences are simple racemes in most Saxifragaceae s.str. and in Ribes, with additional racemes appearing only very occasionally, the proximal internodes in both taxa being elongated. Pluriseriate, gland-tipped trichomes are present in the Saxifragaceae and are ontogenetically the ﬁrst trichome type to be found on Ribes (Janczewski 1907). Growth patterns and mature leaf morphology of the other woody Saxifragales are all very different (petioles short, stipules absent or very different in shape and structure, lamina with pinnate venation without dominant pair of secondary veins, ovate in outline with rounded or mostly cuneate bases). The basic phytochemical inventory of Ribes (absence of iridoids, dominance of linoleic and linolenic acid in the seed oils, presence of ﬂavonoids, proanthocyanidins, ellagic acid and tannins) is very similar to that of Saxifragaceae. A close and exclusive afﬁnity of Ribes to Saxifragaceae s.str. has recently found additional support from molecular data (Soltis and Soltis 1997; Soltis et al. 2001). Economic Uses. Nearly all species of Ribes have edible fruits, some are used in the making of jams, preserves, ice cream, cakes, fruit juices, fermented drinks and liquors. The fruits are generally high in ascorbic acid (up to 0.15%) and other organic acids, but relatively low in sugar. Some species have insipid or mucilaginous, inedible fruits (esp. in subg. Parilla); very few species have bitter and possibly poisonous fruits. Tanaka (1976) and Moerman (1998) list over 60 edible species from Asia, Europe and North America, and additional edible species are known from South America (Rapoport et al. 1999). Fruits are often collected from wild plants and up to 11 edible Ribes species are reported from a single, medium-sized country (Dzhangaliev 2002). Ribes is cultivated primarily in the north-

Grossulariaceae

ern temperate zone, and world production of Ribes fruits amounts to over 500,000 tons, more than 3/4 of which is produced and consumed in Poland and Germany. The several thousand cultivars can be roughly subdivided into four groups: red currants (R. rubrum and hybrids with, e.g. R. petraeum, R. spicatum), black currants (Ribes nigrum), gooseberries (Ribes uva-crispa and hybrids with various North American species of subg. Grossularia) and currant-gooseberry hybrids (e.g. “Josta” – Ribes nigrum x R. hirtellum). North American native ethnic groups use leaves, roots, wood and bark of nearly all native Ribes species as condiments, for a wide range of medicinal and technical applications, and/or the fruits are eaten fresh and preserved, mainly by drying (Moermann 1998). The aromatic leaves of Ribes nigrum are used as tea mainly in Northeast Asia, and are attributed medicinal properties in the traditional Central European medicine. They form a rapidly expanding segment on the international tea market. In spite of the abundance of Ribes species in South America, their uses are very limited and restricted largely to the very high Andean species: these are a locally important source of ﬁrewood (R. cuneifolium, R. viscosum) and also provide good browsing to livestock (R. brachybotrys). Only one genus: Ribes L.

Figs. 55–58

Ribes L., Sp. Pl.: 200 (1753); Berger, New York Agric. Exp. Sta. Tech. Bull. 109:3–118 (1924), rev.; Lingdi & Alexander, Fl. China 8:428–452 (2001), reg. rev.; Pojarkova, Fl. U.S.S.R. 9 (English edn): 175–208 (1971), reg. rev.; Weigend & Binder, Bot. Jahrb. Syst. 123:111–134 (2001), reg. rev. Grossularia Mill. (1754).

Characters as for family. Seven subgenera are currently recognized (Weigend et al. 2002): subg. Ribes, including the hermaphroditic sect. Ribes (red currants) and sect. Heritiera (skunk currants) and the dioecious alpine currants (sect. Berisia); subg. Coreosma (black currants); subg. Calobotrya (ornamental currants, the paraphyletic sect. Calobotrya includes sect. Cerophyllum); subg. Symphocalyx (golden currants); subg. Grossularioides (spiny currants); subg. Grossularia (gooseberries); subg. Parilla (South American currants). The recognition of these well-deﬁned groups at generic level is conceivable but seems unnecessary, given the overall morphological coherence of the genus.

175

Selected Bibliography Agababian, W.Sch. 1963. Pollen morphology of genus Ribes. Izvest. Akad. Nauk Armajanskoj S.S.R. 16:93–98. Andersson, J.P. 1943. Two notable plant hybrids from Alaska. Proc. Iowa Acad. Sci. 50:155–157. Artaud, J. 1992. Identiﬁcation of α-linolenic acid-rich oils. Ann. Falsiﬁcations Expertise Chim. Toxic. 85/909:231–239. Bate-Smith, E.C. 1962. See general references. Bate-Smith, E.C. 1976. Chemistry and taxonomy of Ribes. Biochem. Syst. Ecol. 4:13–23. Bensel, C.R., Palser, B.F. 1975. Floral anatomy of Saxifragaceae s.l. II: Saxifragoideae and Iteoideae. Amer. J. Bot. 62:661–675. Berger, A. 1924. A taxonomic review of currants and gooseberries. New York Agric. Exp. Sta. Tech. Bull. 109:3–118. Bohm, B.A. 1993. External and vacuolar ﬂavonoids of Ribes viscosissimum. Biochem. Syst. Evol. 21:745. Börner, K., Heinze, K., Kloft, W., Lüdicke, M., Schmutterer, H. 1957. Tierische Schädlinge an Nutzpﬂanzen 2, Homoptera 2. In: Appel, O., Blunck, H., Richter, H. (eds) Handbuch der Pﬂanzenkrankheiten V/4:1– 577. Britton, N.L., Brown, A. 1913. An illustrated ﬂora of the northern United States and Canada 3:236–241. New York: Dover. Catling, P.M., Dumouchel, L., Brownell, V.R. 1998. Pollination of the Miccosukee Gooseberry (Ribes echinellum). Castanea 63:402–407. Cronquist, A. 1981. See general references. Davis, G.L. 1966. See general references. Döhler, W., Heddergott, H., Menhofer, H., Müller, F.P., Schmidt, G., Speyer, W., Weidner, H. 1953. Tierische Schädlinge an Nutzpﬂanzen 1. In: Appel, O., & Blunck, H., (eds.). Handbuch der Pﬂanzenkrankheiten IV/2:1–518. Dzhangaliev, D., Salova, T.N., Turekhanova, P.M. 2002. The wild fruit and nut plants of Kazachstan. In Janick, J. (ed.) Horticult. Rev. 29:305–371. Engler, A. 1890. Saxifragaceae. In: Engler, A., Prantl, K., Die natürlichen Pﬂanzenfamilien III, 2a:42–93. Leipzig: Engelmann. Francke-Grosmann, H., Gößwald, K., Hennig, W., Maercks H., Otten, E. 1953. Tierische Schädlinge an Nutzpﬂanzen 2. In: Appel, O., Blunck, H., Richter, H. (eds) Handbuch der Pﬂanzenkrankheiten V/1:1–311. Free, J.B. 1993. Insect pollination of crops, ed. 2. London: Academic Press. George, G., Candela, C., Quinet, M., Fellous, R. 1974. Identiﬁcation of the diterpenic acid of Ribes nigrum buds. Helv. Chim. Acta 57:1247–1249. Gluchoff-Fiasson, K., Fenet, B., Leclerc, J.-C., Reynaud, J., Lussignol, M., Jay, M. 2001. Three new ﬂavonol malonylrhamnosides from Ribes alpinum. Chem. Pharmceut. Bull. 49:768–70. Grund, C., Jensen, U. 1981. Systematic relationships of the Saxifragales revealed by serological characteristics of seed proteins. Pl. Syst. Evol. 137:1–22. Hassebrauk, K., Niemann, E., Schuhmann, G., Zycha, H. 1962. Basidiomycetes. In: Appel, O., Blunck, H., Rademacher, B., Richter, H. (eds) Handbuch der Pﬂanzenkrankheiten III/4:1–747. Hegnauer, R. 1973, 1990. See general references.

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Janczewski, E. 1907. Monographie de Groseillier. Mém. Soc. Phys. Genève 35/13:199–517. Keep, E. 1962. Interspeciﬁc hybridization in Ribes. Genetica 33:1–23. Knuth, P. 1898. Handbuch der Blütenbiologie, II, 1. Leipzig: Engelmann. Krach, J.E. 1977. Seed characters in and afﬁnities among the Saxifraginae. In: Kubitzki, K. (ed.) Flowering plants evolution and classiﬁcation at higher categories. Berlin Heidelberg New York: Springer, pp. 141–153. Le Lous, J., Majoie, B., Moriniere, J.L., Wulfert, E. 1975. Study of the ﬂavonoids of Ribes nigrum. Ann. Pharmceut. Franç. 33:393–9. Lercker, G., Cocchi, M., Turchetto, E. 1988. Ribes nigrum seed oil. Rivista Italiana Sostanze Grasse 65, 1:1–6. Lingdi, L., Alexander, C. 2001. 29. Ribes. In: Wu, Zheng-yi, Raven, P.H. (eds) Flora of China 8:428–452. Beijing: Science Press. Lu, Y.R., Foo, L.Y., Wong, H. 2002. Nigrumin-5-p-coumarate and nigrumin-5-ferulate, two unusual nitrilecontaining metabolites from black currant (Ribes nigrum) seed. Phytochemistry 59:465–468. Mesler, M.R., Cole, J.C., Wilson, P. 1991. Natural hybridization in western gooseberries (Ribes subg. Grossularia, Grossulariaceae). Madroño 38:115–129. Metcalfe, C.R., Chalk, L. 1950. See general references. Meurman, O. 1928. Cytological studies in the genus Ribes. Hereditas 11:289–356. Moerman, D.E. 1998. Native American ethnobotany. Portland/OR: Timber Press. Pojar, J. 1975. Hummingbird ﬂowers of British Columbia. Syesis 8:25–28. Pojarkova, A.I. 1971. Ribes. In: Komarov, V.L., Yuzepchuk, S.V. (eds) Flora of the U.S.S.R. 9 (English edn): 175–208. Springﬁeld, VA: U.S. Department of Commerce.

Rapoport, E.H., Ladio, A.H., Sanz, E.H. 1999. Plants comestibles de la Patagonia andina. Bariloche: Imaginaria. Schweitzer, L. 1996. Zur Kenntnis der Wildbienen (Apoidea) im Landkreis Peine: ein naturnaher Garten in Vechelde. Beitr. Naturk. Niedersachsen 49:1–9. Sinnott, Q.P. 1985. A revision of Ribes L. subg. Grossularia (Mill.) Pers. sect. Grossularia (Mill.) Nutt. (Grossulariaceae) in North America. Rhodora 87:189–286. Soltis, D.E., Soltis, P.S. 1997. Phylogenetic relationships in Saxifragaceae sensu lato: a comparison of topologies based on 18S rDNA and rbcL sequences. Amer. J. Bot. 84:504–522. Soltis, D.E., Kuzoff, R.K., Mort, M.E., Zanis, M., Fishbein, M., Hufford, L., Koontz, J., Arroyo, M.K. 2001. Elucidating deep-level phylogenetic relationships in Saxifragaceae using sequences for six chloroplastic and nuclear DNA regions. Ann. Missouri Bot. Gard. 88:669– 693. Stern, W.L., Sweitzer, E.M., Philipps, R.E. 1970. Comparative anatomy and systematics of woody Saxifragaceae. Ribes. Bot. J. Linn. Soc. 63, suppl. 1:215–237. Takhtajan, A.L. 1996. See general references. Takhtajan, A. 1997. See general references. Tanaka, T. 1976. Tanaka’s cyclopedia of edible plants of the world (ed. S. Nakao). Tokyo: Keigaku. Verbeek-Reuvers, A.A.M.L. 1980. Grossulariaceae. In: Punt, W., Clarke, G.C.S. (eds) The northwest European pollen ﬂora. New York: Elsevier, pp. 107–116. Weigend, M., Binder, M. 2001. A revision of the genus Ribes (Grossulariaceae) in Bolivia. Bot. Jahrb. Syst. 123:111– 134. Weigend, M., Motley, T., Mohr, O. 2002. Phylogeny and classiﬁcation in the genus Ribes (Grossulariaceae) based on 5S-NTS sequences and morphological and anatomical data. Bot. Jahrb. Syst. 124:163–182.

Gunneraceae Gunneraceae Meissner, Pl. Vasc. Gen., tab. diagn.: 345, 346; Comm.: 257 (1842), nom. cons.

H.P. Wilkinson and L. Wanntorp

Perennial herbs, either with ascending or creeping pachycaulous stems, covered with large leaf scars, apically with large to gigantic, long-petioled leaves reaching up to c. 5 m in height (G. magniﬁca), and between these often covered with conspicuous bracts protecting the inﬂorescence and vegetative buds, or stoloniferous and mat-forming, with short, upright stem portions bearing leaf-rosettes, reaching from 4 cm to about 1 m in height, or in one case (G. herteri), diminutive annuals. Leaves alternate, crowded at stem tips; petioles short to very long; lamina oblong to reniform or peltate, dentate, crenate or palmately lobed, the crenations and lobes with protruding hydathodes; venation in large-leaved species palinactinodromous with veins very prominent and projecting as ribs on abaxial surface, in smaller-leaved species actinodromous or pinnate and less prominent. Sometimes with more or less conspicuous, simple to much divided scales between the leaf-bases, stolons with paired, or single ochrea-like, bracts apically. Inﬂorescences axillary or pseudoterminal, erect, simple or compound racemes, or spikes; lower ﬂowers mostly pistillate, upper ones staminate, the middle ones sometimes perfect, or ﬂowers all unisexual, in a few cases plants dioecious. Flowers small, bracteate or not, epigynous, sepals 2, anteri-posterior, valvate, sometimes obsolete, petals 2, transversal, mitre-shaped, slightly exceeding the sepals, caducous, in female ﬂowers wanting; stamens 2(1), transversal, with short ﬁlaments; anthers dithecal and tetrasporangiate, opening by longitudinal slits; carpels 2, united to form an inferior, unilocular ovary; stylodia 2, transversal; stigmas dry, papillate; ovule solitary, pendulous from apex of locule. Fruit drupaceous, coriaceous to ﬂeshy, oval to globose, green or bright red, rarely white or yellow. Seeds with a very small obcordate embryo embedded in copious, oily endosperm. Specialized organs containing endosymbiontic Nostoc cells are located in the stem between the leaf-bases of all species.

A monogeneric family with about 60 species, growing in cool and wet or damp habitats, from low altitudes to above 3,000 m, in South and Central America, Mexico, Hawaii, Africa, Madagascar, Tasmania, New Zealand, New Guinea and the Malayan archipelago Vegetative Morphology. Gunnera comprises a wide spectrum of growth forms from giant to dwarf herbs, usually perennial, with erect or creeping stems, often forming mats or clumps by stolons originating from leaf axils on the stems and bearing leaf-rosettes apically, or more rarely by branching of the stems themselves (Figs. 59, 63). The main stem of the dwarf G. herteri is interpreted as a chain of sympodial units each consisting of a leaf and an extra-axillary inﬂorescence (Rutishauser et al. 2004), a structural pattern which may also be valid for other species of Gunnera (see Skottsberg 1928). Stolons occur in subg. Pseudogunnera, Milligania and Misandra. In Pseudogunnera and Milligania, two bud scales at the tip of the stolons precede the foliage leaves on the erect stem. These cataphylls are regarded by Wanntorp et al. (2003) to be homologous with a cap-like “ochrea”, which in subg. Misandra occurs on the stolon as well as between the leaves of the upright stem. In subg. Panke, in which no stolons are formed, the stems are covered by numerous, large bract-like scales. Skottsberg (1928) and Wanntorp et al. (2003) consider also these scales to be cataphylls. Vegetative Anatomy. (Information mostly from Wilkinson 1998, 2000). Nodes are multilacunar and multitrace. Leaves are bifacial, hypostomatous or amphistomatous; stomata are anomocytic. The lower leaf surface has always a smooth wax cover; the cuticle is smooth or (in some species of subg. Milligania) ﬁnely striate. Marginal leaf hydathodes with an epithem are found in all subgenera (Fig. 59D), while laminar hydathodes are restricted to subg. Panke. The leaf axils of Gun-

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nera herteri contain 2–5 inconspicuous glandular colleters (Rutishauser et al. 2004). Unicellular hairs are widespread and lacking only in G. herteri; other hair types including uniseriate and multiseriate, stalked and globular hairs are found in subg. Panke. Domes of raised siliciﬁed cells (“warts”) on the upper leaf surface and spine-like emergences on petioles and the larger veins of the lower leaf surface are characteristic of subg. Panke (Fig. 59C, E). The vascular systems of stems and petioles are typically polystelic. The bundles have the xylem surrounded by about six portions of phloem (amphicribal) and are sheathed by a well-deﬁned endodermis with Casparian thickenings. In the stems of the pachycaulous, non-stoloniferous subg. Panke, the bundles may amount to several hundred per stem and in subg. Gunnera to about 60. Among the stoloniferous subgenera, the large-leaved subg. Pseudogunnera and the small-leaved subg. Milligania and Misandra have only few (3–5) larger and some smaller bundles, the latter to leaves and inﬂorescences. The vascular tissue of the stolons is not polystelic but siphonostelic (-modiﬁed); it consists of a single tube of xylem and phloem (G. densiﬂora), or of tubes of internal and external phloem separated by two tubes of xylem, and is surrounded by an endodermis. Vessel elements are usually very to moderately small; perforation plates in stolons and roots are mainly scalariform with few to many bars, and in the stems of large-leaved species simple perforation plates are more common. Cluster crystals (druses) are widespread in various tissues. Behnke (1986) found sieve element plastids containing protein crystals and starch grains (Pcs type).

Embryology. In Gunnera macrophylla and G. chilensis, the pollen grains are two-celled at anthesis. The ovule is anatropous, bitegmic and crassinucellate, and the micropyle is formed by the inner integument alone. The embryo sac is tetrasporic and 16-nucleate (Peperomia-type) and, apart from the egg and the synergids, contains six antipodal cells and a group of cells fusing to form the secondary embryo sac nucleus. Endosperm development is cellular; the suspensor forms no haustorium (Modilewski 1908). Pollen Morphology. Pollen of Gunnera is very distinctive, tricolpate, suboblate spheroidal (Fig. 60), and can be recognised by the fossaperturate shape with bulging mesocolpia and the microreticulate exine, usually 20–28 × 25–37 µm (Erdtman 1952; Praglowski 1970; Jarzen 1980; Wanntorp et al. 2004). Karyology. Beuzenberg and Hair (1963) reported 2n = 34 for Gunnera monoica, G. prorepens, G. densiﬂora, G. dentata and G. hamiltonii, and several hybrids (all in subg. Milligania); the same number was counted for various South American species by Dawson (1983) and Pacheco et al. (1993) Pollination. Gunnera perpensa shows all attributes of wind pollination (the general condition in the genus), such as high pollen/ovule ratio, strong protandry in the hermaphroditic ﬂowers, and starch storage in pollen (Lowrey and Robinson 1988).

Flower Structure. The ﬂoral symmetry of Gunnera is most remarkable: the petals, stamens and carpels – at least the stylodia – are located in the transverse plane (Wantrop and Ronse De Graene 2005), reminiscent of the position of these ﬂoral organs in Sabiaceae and, to some degree, in Proteaceae.

Fruit and Seed. The fruit is drupaceous, greenish-reddish, dry and relatively small (1–2 mm long) in subg. Panke, Pseudogunnera and Gunnera, in subg. Misandra and Milligania larger (up to 8 mm long), and often brightly coloured; G. magellanica is called “frutilla del diablo”, devil’s strawberry. In the maturing seed, the integuments and nucellus disappear, with the exception of the outer epidermis of the outer integument which is made up of thin-walled cells ﬁlled with red sap; mechan-

Fig. 59. Gunneraceae. A–C Gunnera manicata growing in the Royal Horticultural Society’s garden at Wisley, Surrey, UK. A Whole plant. B One leaf measuring 94 in. (237.5 cm) in width and 77 in. (195.5 cm) in length. C An inﬂorescence (in spring) c. 2 ft. tall; note petiole with spine-like emergences to the right. D Marginal hydathodes

with terminal glandular tubes from a very young leaf of G. chilensis, scale bar = 1 mm. E “Warts” on the adaxial surface of a mature leaf of G. chilensis, scale bar = 0.25 mm. F Nostoc heterocysts in two large cells from a stem of G. lobata, scale bar = 50 µm. G Heterocysts from F at arrows, scale bar = 10 µm. (Orig. H. Wilkinson)

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Fig. 61. Gunneraceae. Summary tree of Gunnera, based on Wanntorp et al. (2002, 2003).

Fig. 60. Gunneraceae, pollen grains. A, B, E, F Gunnera chilensis, SEM micrographs. C, D G. macrophylla, light micrographs. A Polar view. B, E Equatorial view. C, D Optical sections showing thickened exine at colpi margins (C) and poles (D). F Equatorial view of one colpus and reticulate ornamentation. A–E ×1,000; F ×51,500. (A, B, E, F Photographs H. Wilkinson; C, D photographs M.M. Harley)

ical protection of the seed is taken over by the pericarp. The endosperm is copious, its cells containing oil, starch and aleurone with crystalloids. The embryo is very small, heart-shaped and lies excentric (Netolitzky 1926). Phytochemistry. The leaves of Gunnera manicata contain high concentrations of an unidentiﬁed ellagitannin (Doyle and Scogin 1988); in G. chilensis, the tannin content of the rhizomes amounts to 9.3% (Hegnauer 1966). Pacheco et al. (1993) have studied the ﬂavonoid variation of various South American species Relationships Within the Family. Cladistic analyses of Gunnera based on nuclear and plastid

gene regions by Wanntorp et al. (2002), and Wanntorp and Wanntorp (2003) resolved Gunnera as monophyletic and conﬁrmed the sectional classiﬁcation proposed by Schindler (1905). Moreover, subg. Ostenigunnera with the diminutive G. herteri was recovered as sister to all remaining sections, with subg. Gunnera subsequently sister to the remaining subclades. Figure 61 represents this topology with an indication of gains and losses of several characters. Gunnera herteri lacks the polystelic condition characteristic of the rest of the genus (the bundles are not sheathed by an endodermis; Wilkinson 2000); it is unique in being an annual, and possibly in the concaulescence of vegetative branches and inﬂorescences with the main axis for some distance above the axil. Afﬁnities. Gunnera has traditionally been included in Haloragaceae but has often been elevated to family rank, although its afﬁliation has remained uncertain; Takhtajan (1997) included it in his Saxifraganae. Numerous molecular studies have now recovered Gunneraceae in close association with Myrothamnaceae in a clade at the base of the eudicots, more precisely as sister to all remaining core eudicots (Soltis et al. 2000, 2003). A comparison of the characters of Gunnera and Myrothamnus (Wilkinson 2000) shows that there exists very little agreement morphologically between the two genera. Distribution and Habitats. Gunnera is mostly southern hemispheric in distribution, but in South and Central America, the Hawaiian islands and Malesia it extends into low northern latitudes.

Gunneraceae

The species prefer wet or damp, cool places from low altitudes in cool climates to above 3,000 m in the tropics, mostly on mineral soil or peat, and are found on riverbanks, beside waterfalls, on steep slopes, in precipitous, small hanging valleys at the head of streams and in extremely rainy, wet regions, sometimes also in dense shade and mossy forests. Gunnera hamiltonii and G. dentata occur in damp sand hollows by the sea and G. herteri grows in seepages of emerging groundwater between coastal dunes (Wanntorp et al. 2003). Gunnera-Nostoc Symbiosis. All species have peculiar organs (often called “glands”) breaking through the epidermis immediately below very young developing leaves. These organs were identiﬁed by Miehe (1924) as arrested adventitious roots (Fig. 62). They produce copious mucilage through which cyanobacteria of the genus Nostoc

Fig. 62. Gunneraceae. Arrested roots infected with Nostoc algae (“phycorhizas”), occurring in groups of three below the leaf-bases on the axes of Gunnera macrophylla. (Miehe 1924)

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gain entrance to the plant stem. Nostoc-infected tissue consists of isolated groups of larger and more rounded cells than those of the ordinary stem parenchyma surrounding them (Fig. 59F, G). In young stems, Nostoc colonies appear as bright blue-green structures. In slightly older parts of the stem, they take on a dark appearance and in even older parts appear as whitish, amorphous masses and are said to be “degenerate” (Bergman et al. 1992; Wilkinson 2000) Distributional History. Gunnera has an ample microfossil record in the southern hemisphere and parts of the northern hemisphere, dating nearly uninterruptedly back to the early Late Cretaceous (Jarzen 1980; Jarzen and Dettmann 1989; Wanntorp et al. 2004). During Upper Cretaceous and Early Tertiary times, the genus was more widely distributed than it is today. The earliest pollen record attributable to Gunnera (as Tricolpites reticulatus) is from the Turonian of South America; in the Campanian and Maastrichtian, the

Fig. 63. Gunnera magellanica. A Male plant. B Male ﬂower. C Stamen. D Female plant. E Female ﬂower. F Same, vertical section. G Infructescence. H Fruit, vertical section. I Fruit, transverse section. (Schindler 1905)

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genus was represented in Antarctica, New Zealand, continental Australia (from where it is absent today), West Africa and, strangely enough, in North America. In the Palaeogene, the genus appeared additionally in southernmost South America, the Indian Ocean and the Indian Plate. In the Neogene, it retreated southwards in North America (where at present it is represented by a single species in Mexico) and appeared in New Guinea. Wanntorp and Wanntorp (2003) analysed the present distribution of Gunnera within the framework of a cladistic study and the fossil record. Most distributional facts are in agreement with viewing Gunnera as a Gondwana element, which obtained its present distribution mostly by vicariance. However, its widespread and abundant occurrence in North America from the Late Cretaceous to Eocene calls for an additional explanation. Wanntorp and Wanntorp (2003) propose a dispersal event out of South America before the Campanian as leading to the colonization of North America. From there, not only may the Hawaiian islands have been reached by long-distance dispersal but also South America may have been re-colonized by the lineage now corresponding to subg. Panke, where it met with subg. Misandra.

of single anther. One species, G. herteri Osten, coastal southern Brazil and Uruguay.

Uses. Species of subg. Panke are sometimes used as garden ornamentals; a few of the smaller species are grown in rock-gardens. Gunnera perpensa has been reported to have antifertility and antiabortifacient properties in rats by Mafatle and Joseph (1992). The stems and petioles of Gunnera chilensis are used by indigenous people on a small scale for tanning and dyeing, and petioles are eaten as salad (“nalca” or “rahuay”).

Subg. Milligania (J.D. Hook.) Schindler. Low stoloniferous, mat-forming herbs; leaves in rosettes on short upright stems, petiole 0.5–2 cm long, blade orbicular-reniform, subcordate, ovate or elliptic, 1–3.5(5) cm long. Plants monoecious, usually with staminate and pistillate ﬂowers on separate racemes, except in G. monoica Raoul which has bisexual racemes with staminate ﬂowers apically. Racemes 1–5 cm long, pistillate ﬂowers with sepals only, staminate ﬂowers with sepals and petals. About six species, one from Tasmania, all others from New Zealand.

Only one genus: Gunnera L.

Figs. 59–63

Gunnera L., Syst. Nat. ed. 12:587, 598 (Oct. 1767); Mant.: 16, 121 (Oct. 1767); Schindler in Engler, Pﬂanzenreich IV, 225:194–128 (1905); Mora-Osejo, Flora de Colombia 3:1– 178 (1984).

Description as for family; six subgenera: Subg. Ostenigunnera Mattfeld. Diminutive glabrous annual herb; leaf blades to 1.4 cm, ﬂabelliform, with up to 20 lobes each ending in a hydathode; indumentum, bracts, stolons and rhizome 0. Inﬂorescences interaxillary, racemes, c. 1 cm long, pistillate ﬂowers basally, without perianth, staminate ﬂowers apically, often consisting

Subg. Gunnera (= subg. Perpensum [Burman] Schindler). Moderately large herb; rhizome horizontal, intermittently branching, 1–2 cm thick; bracts and stolons 0, leaves with long petiole, blade cordate or reniform, to 17 × 28 cm, densely dentate-crenate; young parts pubescent. Inﬂorescence thyrsoid, up to 40 cm long; ﬂowers hermaphroditic. One species, G. perpensa L., South Africa to Ethiopia, Madagascar. Subg. Pseudogunnera (Oersted) Schindler. Moderately large-leaved, herb with long stolons; upright stems short, 1–2 cm diameter; leaves sheathlike at the base, petiole 0.3–1 m, blade reniform to cordate, irregularly lobed, acutely irregularly sphacelate-dentate and bullate, up to 50 cm wide, with strongly prominent reticulate venation beneath. Inﬂorescences up to 50 cm long, basal ﬂowers pistillate with sepals only, apical ﬂowers staminate with sepals and petals. One species, G. macrophylla Blume, Malayan archipelago (New Guinea, Solomon Islands, Sulawesi, Java, Sumatra, Borneo and Philippine islands).

Subg. Misandra (Comm.) Schindler. Low stoloniferous, dioecious herbs (Fig. 63); leaves from short upright stems with ochrea-like scales alternating with the leaves; petiole 2–25 cm long, blade, reniform or reniform-orbicular, to 11 cm wide indistinctly lobed. Inﬂorescences up to 15 cm, staminate as well as pistillate ﬂowers without petals. Differing from subg. Milligania in the possession of ochrea-like scales on shoots. Two species, from Tierra del Fuego and Falkland Islands to Colombia. Subg. Panke (Molina) Schindler. Large to giant, pachycaulous perennials (Fig. 59A) with ﬂeshy

Gunneraceae

stems, up to 3 m long and 40 cm thick, upright, with age often becoming decumbent, rarely branching; youngest parts of stem and terminal bud covered by numerous linear-lanceolate, ± laciniate or entire, often brightly orange-coloured bracts or scales up to 40 cm long, bearing mucilageproducing glands on the adaxial surface. Petioles up to 2.7 m long, blades mostly palmately lobed (Fig. 59B), from 25 cm up to 3 m in diameter. Inﬂorescences up to 0.5 m compound spikes or racemes (Fig. 59C). Pistillate ﬂowers with sepals only, perfect and staminate ﬂowers with sepals and petals. About 50 species, South and Central America, Mexico, the Juan Fernandez Islands and Hawaii; G. manicata Linden and G. chilensis Lam. often cultivated in gardens.

Selected Bibliography Behnke, H.-D. 1986. Contributions to the knowledge of sieve-element plastids in Gunneraceae and allied families. Pl. Syst. Evol. 151:215–222. Bergman, B., Johansson, C., Söderbäck, E. 1992. The NostocGunnera symbiosis. New Phytol. 122:379–400. Beuzenberg, E.J., Hair, J.B. 1963. Contributions to a chromosome atlas of the New Zealand Flora, 5. N. Z. J. Bot. 1:53–67. Boutique, R. 1968. Haloragaceae. In: Flore du Congo, du Rwanda et du Burundi. Meise: Jardin Botanique National de Belgique. Dawson, M.I. 1983. Chromosome numbers of three South American species of Gunnera (Gunneraceae). N. Z. J. Bot. 21:457–459. Doyle, M.F., Scogin, R. 1988. A comparative phytochemical proﬁle of the Gunneraceae. N. Z. J. Bot. 26:493–496. Erdtman, G. 1952. See general references. Fuller, D.G., Hickey, L.T. 2005. Systematics and leaf architecture of the Gunneraceae. Bot. Rev. 7:295–353. Hegnauer, R. 1966. See general references. Jarzen, D.M. 1980. The occurrence of Gunnera pollen in the fossil record. Biotropica 12:117–123. Jarzen, D.M., Dettmann, M.E. 1989. Taxonomic revision of Tricolpites reticulatus Cookson ex Couper, 1953 with notes on the biogeography of Gunnera L. Pollen Spores 31:97–112. Johri, B.M. et al. 1992. See general references. Lowrey, T.K., Robinson, E.R. 1988. The interaction of gynomonoecy, dichogamy, and wind-pollination in Gunnera perpensa L. (Gunneraceae) in South Africa. Monogr. Syst. Bot. Missouri Bot. Gard. 25:237–246. Mafatle, T.J.P., Joseph, M.M. 1992. Antifertility and antiabortifacient properties of Gunnera perpensa. In: Abstract Volume South African Association of Botanists 18th Annual Congress, p. 33. Mattfeld, J. 1933. Weiteres zur Kenntniss der Gunnera herteri Osten. Montevideo: Ostenia (Coleccion de Trabajos Botanicos), pp. 102–118.

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Miehe, H. 1924. Entwicklungsgeschichtliche Untersuchungen der Algensymbiose bei Gunnera macrophylla. Bl. Flora 117:1–15. Modilewski, J. 1908. Zur Embryobildung von Gunnera chilensis. Ber. Deutsch. Bot. Gesell. 26a: 550–556. Morgan, D.R., Soltis, D.E. 1993. Phylogenetic relationships among members of the Saxifragaceae sensu lato based on rbcL sequence data. Ann. Missouri Bot. Gard. 80:631–660. Netolitzky, F. 1926. Anatomie der Angiospermen-Samen. Berlin: Borntraeger. Pacheco, P., Crawford, D.J., Stuessy, T.F., Silva, O.M. 1993. Flavonoid chemistry and evolution of Gunnera (Gunneraceae) in the Juan Fernandez Islands, Chile. Gayana Bot. 50:17–28. Praglowski, J. 1970. The pollen morphology of the Haloragaceae with reference to taxonomy. Grana 10:159– 239. Rutishauser, R., Wanntorp, L., Pfeifer, E. 2004. Gunnera herteri – developmental morphology of a dwarf from Uruguay and S Brazil (Gunneraceae). Pl. Syst. Evol. 248:219–241. Schindler, A.K. 1905. Halorrhagaceae. In: Engler, A. (ed.) Das Pﬂanzenreich IV, 225. Leipzig: W. Engelmann, pp. 1–133. Skottsberg, C. 1928. Zur Organographie von Gunnera. Svensk Bot. Tidskr. 22:392–415. Soltis, D.E. et al. 2000. See general references. Soltis, D.E. et al. 2003. See general references. St. John, H. 1957. Gunnera magniﬁca, a new species from the Andes of Colombia. Svensk Bot. Tidsk. 51:521–528. Takhtajan, A. 1997. See general references. Van der Meijden, R., Caspers, N. 1971. Haloragaceae. Flora Malesiana I, 7:239–263. Leiden: Noordhoff. Wanntorp, L., Wanntorp, H.-E. 2003. The biogeography of Gunnera L.: vicariance and dispersal. J. Biogeogr. 30:979–987. Wanntorp, L., Wanntorp, H.-E., Källersjö, M. 2002. Phylogenetic relationships of Gunnera based on nuclear ribosomal DNA ITS region, rbcL and rps16 intron sequences. Syst. Bot. 27:512–521. Wanntorp, L., Wanntorp, H.-E., Rutishauser, R. 2003. On the homology of the scales in Gunnera (Gunneraceae). Bot. J. Linn. Soc. 142:301–308. Wanntorp, L., Dettmann, M.E., Jarzen, D.M. 2004. Tracking the Mesozoic distribution of Gunnera: comparsion with the fossil pollen species Tricolpites reticulatus Cookson. Rev. Palaeobot. Palyn. 132:163–174. Wanntorp, L., Praglowski, J., Grafström, E. 2004. New insight into the pollen morphology of Gunnera (Gunneraceae). Grana 43:15–21. Wanntorp, L., Ronse De Graene, L.P. 2005. The Gunnera ﬂower: key to eudicot diversiﬁcation or response to pollination mode? Intl. J. Plant Sci. 166:945–953. Wilkinson, H.P. 2000. A revision of the anatomy of Gunneraceae. In: Rudall, P.J., Gasson, P. (eds) Under the microscope: plant anatomy and systematics. Bot. J. Linn. Soc. 134:233–266. Wilkinson, H.P. 1998. Gunneraceae. In: Cutler, D.F., Gregory, M. (eds), Anatomy of the dicotyledons. 2nd edn, Vol. IV. Saxifragales. Oxford: Clarendon Press, 260– 272.

Haloragaceae Haloragaceae R. Br. in Flinders, Voy. Terra Austral. 2: 549 (1814), nom. cons.

K. Kubitzki

Small trees, shrubs, subshrubs, or perennial or annual terrestrial or aquatic herbs, glabrous or scabrous with simple uniseriate hairs; stems erect, ascending, procumbent or creeping, often rooting at lower nodes; nodes unilacunar. Leaves opposite, alternate or verticillate, sessile or petiolate, simple or deeply dissected, entire or toothed, estipulate, heterophyllous in Proserpinaca and Myriophyllum. Inﬂorescence thyrso-paniculate, thyrsoid or racemose, or ﬂowers solitary; partial inﬂorescences usually dichasial; prophylls persistent or caducous. Flowers regular, hermaphroditic or unisexual-monoecious, epigynous, 4(–2)-merous; sepals valvate, persistent (0 in female ﬂowers of Myriophyllum); petals imbricate, keeled, hooded, ± unguiculate, falling with the stamens (0 or rudimentary in Proserpinaca and female ﬂowers of Myriophyllum and Laurembergia); stamens equal to or twice the number of sepals; ﬁlaments short, slender; anthers 4-sporangiate, dehiscing by slits; gynoecium 4(–2)-carpellate; stylodia free, clavate, from bulbous base; ovary 4(–1)-locular but septa sometimes weakly developed and present only at base and apex of ovary or reduced; ovules 2 or 1 per loculus (if 2, then one aborts at an early stage), anatropous or hemitropous, bitegmic, crassinucellar, with weakly developed funicular obturator. Fruit an indehiscent, 4–1-seeded nutlet, or indehiscent and comprising 4 pyrenes (Meziella), or splitting septicidally into (2–)4 mericarps (Myriophyllum), the exocarp often ornamented with tubercles, wings or ribs; seeds with straight, cylindrical embryo and usually with ± copious, ﬂeshy endosperm. x = 7 (9, 21, 29). A subcosmopolitan family of 8 genera and c. 150 species, most south hemispheric, particularly Australian Morphology. In terrestrial forms, the primary root persists and builds a root system whereas, in the aquatic/amphibious genera Proserpinaca and Myriophyllum, it is replaced by adventitious roots which fasten the plant in the substrate, rather than

taking up water; they lack root hairs (Schindler 1905). In the northern hemisphere species of Myriophyllum, condensed vegetative shoots act as overwintering and dispersal units (turions). From most species of Myriophyllum, near the leaf axils and also in other positions, small ﬁliform appendages are known which have been called hydathodes or pseudostipules, although nothing is known as to their function. The leaf blades are simple in terrestrial species but more or less deeply dissected in the aquatic genera; on aerial shoots of the latter, the degree of dissection is gradually diminished. The phenotypic plasticity of Proserpinaca and Myriophyllum, as expressed in changes of their shoot organisation, permits them to cope with, or anticipate, environmental changes such as desiccation of their aquatic habitats; in P. palustris, short photoperiods induce the submersed, and long photoperiods the aerial leaf form (Bowes 1987). Heterophylly may also be advantageous in giving direct access to gaseous CO2 from the air, and dissolved CO2 from the water. Anatomy (from Schindler 1905 and Orchard 1975). Hairs are simple and unicellular or multicellular. The leaves of the aquatic and helophytic species are amphistomatic and their mesophyll is little differentiated. Stomata are usually anomocytic. The primary cortex of the stems contains numerous air-cavities, which are particularly well developed in aquatic species. The vessels have simple perforations with narrow lumina and simple pits. Rays are heterogeneous to homogeneous. The wood is ring-porous with scanty or no wood parenchyma, bordered pits and both uniseriate and multiseriate homogeneous and heterogeneous wood rays. In Haloragis, the inner parts of the rays are uniseriate and homogeneous, and composed of vertically elongated cells. In Haloragodendron, the multiseriate rays are reduced in width and have lengthened uniseriate tails. In Glischrocaryon and Gonocarpus, multiseriate rays are entirely

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lacking in the stems but retained in the roots. Sieve element plastids are of the S-type. Inﬂorescences. Their structure has been analysed by Schindler (1905) and more fully by Orchard (1975). Most genera have thyrsoids, i.e. determinate systems with usually multiﬂorous dichasia as lateral inﬂorescences. In the thyrses of Haloragis, the main axis lacks the terminal ﬂower. Proserpinaca has thyrses similar in structure to those of Haloragis, and with hermaphroditic ﬂowers. Laurembergia inﬂorescences are structured likewise but the ﬂowers are unisexual and, in the dichasia, the distal positions are occupied mostly by male or hermaphrodite ﬂowers, which stand out on a long pedicel from the almost sessile female ﬂowers (Fig. 64B; Orchard 1975). In Gonocarpus, the individual dichasia are reduced to single ﬂowers which, however, retain a pair of prophylls. Similarly, Myriophyllum has the bracteolate ﬂowers in racemes, with females in the lower part of the inﬂorescence, and males in the upper. Flower Structure. The epigynous, 4-merous ﬂowers with valvate sepals and imbricate petals, a diplostemonous androecium with 4-locular anthers, and a gynoecium provided with four stylodia represent the basic condition in the family. With or within several genera, various reductions have occurred, such as the complete or near loss of petals, the loss of the antepetalous or antesepalous stamen whorl and of part of the carpels, or the transition to unisexual ﬂowers. Embryology (Corner 1976, and the literature cited in Orchard 1975 and Takhtajan 1997). In Laurembergia and probably in Haloragis, anther wall formation follows the Monocotyledonous type, in Myriophyllum the Dicotyledonous type. The tapetum is glandular, and pollen is shed in the 3-celled stage. The ovules are anatropous, bitegmic and crassinucellate; the raphe is dorsal. In Myriophyllum, the integuments are very short. Embryo sac development is of the Polygonum type; both cellular and nuclear endosperm development have been reported (Johri et al. 1992). Pollen Morphology. This section is based on the detailed, well-documented study by Praglowski (1970), which has been related to the modern classiﬁcation of the family by Orchard (1975). Pollen of Haloragaceae is isopolar to slightly anisopolar, spheroidal to oblate, 4–6(–20)-colpate or -porate,

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and usually radially symmetric; columellae are distinct, and the tectum is microperforate and provided with minute processes. Three main pollen types can be distinguished. 1. Glischrocaryon and Haloragodendron have isopolar, subspheroidal, 4–6-colpate pollen grains; the colpi are relatively long and usually tenuimarginate; the sexine is thicker than the nexine. 2. Among the remaining genera (Meziella excepted, of which the pollen is unknown), Haloragis, Gonocarpus, Lauremburgia, Proserpinaca and most Myriophyllum have usually shortly 4–6-colpate or -porate pollen grains which are isopolar to slightly anisopolar; the apertures are short colpi or, more rarely, pores and are crassimarginate and frequently protruding. 3. Two species of Myriophyllum, M. alterniﬂorum and M. muelleri, are peculiar in having comparatively large apertures, which are restricted to part of the circumference of the grain and thus make the pollen radially asymmetric. Karyology. Counts from several Myriophyllum species document a polyploid series based on x = 7, extending from the diploid to the hexaploid state. This agrees with the single count available for Haloragis (2n = 14) and a possibly octoploid Gonocarpus (2n = 56), although another Gonocarpus has been counted as having 2n = 12. Pollination. Haloragaceae are usually anemophilous, which to some degree correlates with the mostly small, inconspicuous, greenish petals and extensive papillosity of the stigmatic surfaces. Glischrocaryon species are exceptional in having showy, bright yellow or reddish ﬂowers with plane petals and unilaterally papillose stigmas, which Schindler (1905) considered indicative of entomophily. Fruit and Seed. The inferior ovary of Haloragaceae is enclosed in a receptacle, which in the fruiting stage forms the often conspicuously ornamented or sometimes winged pericarp. Aircavities, which are found in the pericarp of wind(Glischrocaryon spp.) or water- (Laurembergia) dispersed fruits, develop early at ﬂowering. In Haloragis, Haloragodendron and Gonocarpus, the ovaries initially have four locules each with one ovule; sometimes reduction to 3 or 2 locules occurs. In Haloragis, all four ovules can develop

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into seeds, and the septa and endocarp become woody, forming a single, indehiscent, 4-seeded fruit. Haloragodendron differs in that only a single seed is formed in the fruit, which crushes the septa to the side. In both genera, the endocarp becomes strongly woody, and the fruit increases in size after anthesis. In Gonocarpus, the septa are incomplete and are crushed by the single developing seed. The ovary wall becomes crustaceous in fruit, but hardly woody. In Laurembergia, the ovary is imperfectly 4-celled when young but later becomes 1-celled with a central columella; the 1-seeded fruit has a variable sculpture. Prosepinaca stands out in having trimerous ﬂowers and ellipsoid anthers; the septa are solid and the fruit is 3-seeded (Schindler 1905; Orchard 1975). In Meziella, the ovary is 4-locular with welldeﬁned septa and a single ovule in each locule, each of which can develop into a seed. The endocarp around each locule becomes woody but, in contrast to Haloragis where a single 4-locular woody mass is formed, in Meziella four separate woody, 1seeded pyrenes develop, which are held together by the spiny exocarp. This is similar to Myriophyllum where, however, the fruit disintegrates into normally four mericarpic pyrenes each surrounded by a portion of the exocarp which often is tuberculate, aculeate or spiny (Orchard and Keighery 1993). At the apex of the mericarp, the woody exocarp is replaced by an operculum, which is formed by tissue of the funiculus (Fauth 1903). The seeds are small, albuminous and exarillate. The seed coats are reduced to the tabular thinwalled cells of the exotesta, and the remains of the testa and tegmen are crushed. The endosperm is cellular or nuclear (Lauremburgia) and starchy; the embryo is straight and large (Corner 1976).

globular bodies, which turn red upon the addition of vanillin/HCl and contain a special derivative of leucoanthocyanin, myriophyllin. Further compounds recorded include saponins and cyanogenic glycosides, the latter apparently formed on the valin-isoleucin pathway. Calcium oxalate druses are widespread in the family, and hairs are often siliciﬁed (Hegnauer 1966, 1989). Afﬁnities. The formerly considered relationship between Haloragaceae and Myrtales has now been discarded and, indeed, was untenable in view of the strong morphological differences between them (Takhtajan 1997: 268). The rbcL sequence data of Morgan and Soltis (1993) support a close rela-

Dispersal. The aptitude of the mericarps of Myriophyllum and the fruits of Proserpinaca for dispersal by ﬁsh or waterfowl, and of the winged propagules of Haloragodendron and Glischrocaryon by wind is obvious. Fauth (1903) observed that the pyrenes of Myriophyllum sink to the ground where they can overwinter, and also pointed to the possibility of their dispersal by ice ﬂoes. Phytochemistry. Haloragaceae contain large amounts of tannins diffusely distributed in various tissues; both proanthocyanins (‘leucoanthocyanins’) and ellagic acid have been reported. The trichomes of Myriophyllum contain refracting

Fig. 64. Haloragaceae. Laurembergia tetrandra. A Habit. B Detail of ﬂowering branch. C Hermaphrodite ﬂower. D Female ﬂower. E Fruit from hermaphrodite ﬂower. F Fruit from female ﬂower. (Mendes 1978)

Haloragaceae

187

tionship between Haloragaceae and Saxifragales, in particular between Myriophyllum and Penthorum. This suggestion has now been put on a ﬁrm basis by the ﬁve-gene study of Fishbein et al. (2001), in which Haloragis and Myriophyllum are sequentially sister to Penthorum, Tetracarpaea (these two sometimes reversed), Aphanopetalum and Crassulaceae. The Angiosperm Phylogeny Group (APG II 2003) suggested the inclusion of Penthoraceae and Tetracarpaeaceae in Haloragaceae but this is not followed here because it would lead to the loss of the morphological proﬁle of Haloragaceae, with the combination of epigyny and an essentially 4merous ﬂoral organisation. Distribution and Habitats. The almost cosmopolitan family has its centre of distribution in Australia, where six of the eight genera and 105 of the 150 species are found, with a high degree of endemism at the species level (Orchard 1990). The genera Haloragodendron and Glischrocaryon are entirely endemic to Australia, and so are most species of Haloragis, Gonocarpus and Myriophyllum which, above being restricted to Australia, there usually occupy only small distributional areas (see maps in Orchard 1990). The extra-Australian Myriophyllum and Proserpinaca, both aquatic, are distributed much more widely, the former from eastern South America through Africa to Southeast Asia, and the latter from western North America to the West Indies. Ecologically, genera such Haloragis, Haloragodendron and Gonocarpus have radiated into a wide variety of terrestrial habitats, preferably in warm-temperate to Mediterranean regions; Glischrocaryon is notable for recovering well after soil disturbance by ﬁre and light (Orchard 1990). Little is known to me about the trophic preferences of the aquatic members of the family. In northern and central Europe, Myriophyllum alterniﬂorum is bound to oligotrophic freshwater habitats (Godwin 1975), and most of the Australian species of Myriophyllum and also Meziella triﬁda seem to be bound to seasonally moist, nutrient-poor, sandy habitats Palaeobotany. Fossil pollen attributable to Haloragaceae include ‘haloragoid’ pollen from the Upper Cretaceous of Europe, the Eocene of Burma, the Eocene and Palaeocene of Europa, and the Oligocene of New Zealand (see references in Praglowski 1970, and Gruas-Cavagnetto and Praglowski 1977). The oldest pollen ﬁnd of Myrio-

Fig. 65. Haloragaceae. Myriophyllum balladoniense. A Habit. B Inﬂorescence. C Male ﬂower, in situ. D Female ﬂower, in situ. E Apex of female ﬂower. F Fruit. (Orchard 1985)

phyllum-like pollen known to me is from the Upper Eocene of the southeast United States (Frederiksen 1980). Fruiting structures of a waterplant from the Upper Cretaceous (Maastrichtian/Campanian) of Mexico have also been attributed to the family; they are thought to combine characters of Haloragodendron, Meziella and Myriophyllum (Hernández-Castillo and Cevallos-Ferriz 1999). If correctly identiﬁed, this ﬁnding would be of high phytogeographical signiﬁcance. Proserpinaca macrofossils are known from European beds up to the Pliocene (cf. references in Praglowski 1970).

Key to the Genera 1. Fruit an indehiscent 1–4-seeded nut not subdivided into 1-seeded pyrenes 2 – Fruit made up of 1-seeded pyrenes 7 2. All ﬂowers with petals 3 – At least female ﬂowers lacking petals (petals vestigial in Myriophyllum and Proserpinaca) 6

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3. Petals hooded; anthers non-apiculate; inﬂorescences indeterminate 4 – Petals navicular; anthers usually apiculate; inﬂorescences determinate 5 4. Fruits (2–)4-locular; pericarp woody with solid septa; ﬂowers in (1)3–7-ﬂowered dichasia in the axils of alternate bracts 1. Haloragis – Fruits 1-locular; pericarp crustaceous; septa 0 (crushed by single seed); ﬂowers 1(–3) in the axils of opposite or alternate bracts 4. Gonocarpus 5. Leaves serrate; inﬂorescence narrow, spike-like; shrubs or small trees with 1–few woody stems/trunks 2. Halorgodendron – Leaves entire; inﬂorescence broad, umbelliform; subshrubs with numerous annual stems arising from a perennial rootstock 3. Glischrocaryon 6. Fruit 1-locular; ﬂowers predominantly unisexual, in dichasia of up to about 11 ﬂowers per axil, the terminal one in each dichasium usually male, the others female or rarely hermaphroditic; anthers linear-oblong 5. Laurembergia – Fruit 3-locular; ﬂowers hermaphroditic, solitary or in dichasia of up to 3 ﬂowers per axil; anthers ellipsoid 7. Proserpinaca 7. Fruit splitting at maturity into mericarps; sepals less than half length of petals (frequently 0), ﬂat, lanceolate to ovate; ﬂowers frequently unisexual 8. Myriophyllum – Fruit not splitting at maturity into mericarps; sepals almost equalling petals in length, subulate, developing into soft spines; ﬂowers hermaphrodite 6. Meziella

Genera of Haloragaceae 1. Haloragis Forst. & G. Forst. Haloragis Forst. & G. Forst., Char. Gen.: 61, t. 31 (1775); Orchard, Bull. Auckland Inst. Mus. 10:64–150 (1975), rev., and Fl. Australia 18:6–27 (1990). Halorrhagis, orthogr. var.

Annual or perennial herbs or subshrubs from taproots or stolons, glabrous, scabrous or with simple hairs; stems ascending or creeping, some growing in water. Leaves usually opposite below and alternate above, petiolate or sessile, simple to pinnatiﬁd, entire or serrate. Inﬂorescences indeterminate compounded of 3–7-ﬂowered dichasia in axils of alternate bracts; ﬂowers hermaphroditic, (2–)4-merous on short pedicels; sepals deltoid; petals hooded, ± unguiculate, keeled; usually diplostemonous, anthers linear, not apiculate; ovary 2–4-locular, each locule with 1(2) pendulous ovules; stylodia 2 or 4. Fruits smooth, ribbed or winged, and/or with protuberances opposite the sepals or on the entire fruit, or tuberculate between ribs or wings, with persistent sepals, (2–)4-locular with solid septa and woody endocarp and membranous or spongy exocarp, and with (1–)4 seeds. A genus of 28 species conﬁned almost entirely to

Australia and New Zealand, with a few species on S Paciﬁc Islands eastward to Juan Fernandez Islands, in a wide variety of terrestrial habitats, H. brownii (J.D. Hook.) Schindler an obligate aquatic. 2. Haloragodendron Orchard Haloragodendron Orchard, Auckland Inst. Mus. Bull. 10:140–150 (1970), and Fl. Australia 18:27–30 (1990).

Glabrous shrubs or small trees; branches strongly 4-angled, glabrous or glandular; leaves decussate, petiolate or almost sessile, juvenile leaves sometimes pinnatisect or pinnatiﬁd, mature leaves linear or narrow-oblong to lanceolate, [bi]serrate. Inﬂorescence a narrow, spike-like thyrsoid with simple or compound dichasia. Flowers showy, sessile or shortly pedicellate, showy, cream or red; sepals deltoid; petals navicular or planar, not hooded; stamens 8, anthers apiculate; ovary longitudinally 4-ribbed or -angled, septa solid; 1 ovule per locule. Fruit 1-seeded, 4-ribbed or -angled, smooth between angles, pericarp ± spongy. Five species, all narrow endemics, Australia. 3. Glischrocaryon Endl. Glischrocaryon Endl., Ann. Wien. Mus. 2:209 (1839); Orchard, Bull. Auckland Inst. Mus. 10:150–163 (1975), rev., and Fl. Australia 18:30–34 (1990). Loudonia Lindl. (1840).

Glabrous perennial herbs from woody, branched rootstock. Leaves alternate, often deciduous, terete to narrow lanceolate or linear, sessile, entire. Inﬂorescence dense, terminated by a many-ﬂowered compound dichasium with (2–)5 alternately arranged many-ﬂowered dichasia below. Flowers yellow or cream, 2(3)–4-merous; sepals deltoid, decurrent in wings of ovary or free; petals 2 or 4, torsive, navicular or hooded; stamens 4 or 8; ovary ovoid to obpyriform, 2- or 4-winged, with a central columella and the body of the ovary swollen or not; the single locule with 4 pendulous ovules; septa 0. Fruit 2- or 4-winged or -ribbed, with pericarp between wings swollen or membranous, endocarp slightly woody; seed 1, occupying the entire locule. Four species, scattered throughout Australia. 4. Gonocarpus Thunb. Gonocarpus Thunb., Nov. Gen. 3:55 (1783); Orchard, Bull. Auckland Inst. Mus. 10:164–277 (1975), rev., and Fl. Australia 18:34–59 (1990).

Annual or perennial herbs or shrubs up to 4 m tall, often twiggy and multistemmed, glabrous,

Haloragaceae

scabrous, or with indumentum of simple hairs; leaves sessile or petiolate, opposite or rarely in whorls of 3(–5). Inﬂorescence an indeterminate raceme or spike in the axil of alternate, opposite or whorled primary bracts or from axils of upper leaves; pedicels with prophylls; ﬂowers (3)4-merous, shortly pedicellate; sepals often with pronounced midrib and prominent median basal callus; petals hooded, ± unguiculate, keeled; stamens usually twice the number of petals; anthers 4-locular; ovary smooth or ribbed opposite sepals and/or petals, incompletely (3)4-locular, with 1(2) pendulous ovules per locule (the second aborting at an early stage); stylodia clavate, stigmas capitate. Fruit glabrous or scabrous with ± membranous pericarp and persistent sepals; septa ± 0, seed 1, occupying entire fruit. About 41 species, from Australia and New Zealand extending through New Guinea and Malesia to Borneo, the Philippines, Japan, Formosa and coastal south-eastern Asia; G. micranthus subsp. micranthus found almost throughout the range of the genus. Two sections: sect. Gonocarpus, styles clavate, not or only barely exceeding sepals; ﬂowers all sessile; sect. Simplum Orchard (1977), stylodia subulate, greatly exceeding sepals, bisexual ﬂowers sessile, male long-pedicellate. 5. Laurembergia Bergius

Fig. 64

Laurembergia Bergius, Descr. Pl. Cap.: 350 (1767); Schindler in Pﬂanzenreich IV, 225:61 (1905); A. Raynal, Webbia 19:683–695 (1965), African spp.; van der Meijden & Caspers, Fl. Males. I, 7:246–248 (1971). Serpicula L. (1767).

Perennial herbs from woody rhizome, some helophytic; stems ascending or prostrate. Leaves opposite or rarely (sub)verticillate or alternate, sessile or shortly petiolate, simple, entire or dentate. Inﬂorescences axillary 1–11-ﬂowered fascicles, sometimes of 1–3 pedicellate hermaphrodite ﬂowers and the others female and (sub)sessile, or 1 long-pedicellate male and the others female and (sub)sessile, or long-pedicellate male ﬂowers in the axils of the upper leaves and female (sub)sessile ﬂowers in the axils of lower leaves. Flowers with calyx-tube ellipsoid or urceolate, with longitudinal nerves and also longitudinal, often strongly mamillate ribs, sepals persistent, petals sometimes rudimentary or 0 in female ﬂowers; stamens 4 or 8, anthers linear, not apiculate; ovary 4-locular, becoming 1-locular through dissolution of the septa; ovules 4; stylodia 4 or 0, stigmas plumose. Fruit 1-locular, a small, hard

189

indehiscent nut, ribbed or not; seed 1, pendulous. About four species, (sub)tropical Africa and Madagascar, tropical Asia from India to Java, and eastern South America, from 0 to 2,700 m a.s.l., L. tetrandra (Schott) Kanitz amphi-Atlantic, polymorphic. 6. Meziella Schindler Meziella Schindler in Engler, Pﬂanzenreich IV, 23:60 (1905); Orchard & Keighery, Nuytsia 9:111–117 (1993).

Glabrous annual or perennial semiaquatic herb; stems prostrate, rooting at nodes; leaves alternate, the lowermost entire, upper triﬁd with hydathodes on tips and in axils of lobes, lobes ± terete, with a short tooth in the angles between them. Inﬂorescence a spike; ﬂowers with prophylls, bisexual, sepals and petals red, the latter hooded; stamens 4, antesepalous, apiculate; stylodia 4; ovary small, globular, with clusters of short subulate processes below the sepals. Fruit red, indehiscent, of 4 woody pyrenes contained within a dry, spiny exocarp. A single species, M. triﬁda (Nees) Schindler, in slightly submerged ﬂats in Western Australia. 7. Proserpinaca L. Proserpinaca L., Sp. Pl. 1:88 (1753); Fernald in Gray’s Manual, 8th edn; Fasset, Commun. Inst. Trop. Invest. Ci. Univ. El Salvador 2:139–162 (1953).

Submerged, emergent or seasonally terrestrial rhizomatous perennials; stems ascending or prostrate, the lower parts branched and somewhat woody. Leaves alternate, subsessile, the submerged pinnatiﬁd, the aerial occasionally simple but distinctly toothed. Flowers trimerous, hermaphrodite, sessile, solitary in leaf axils; calyx-tube triquetrous, petals rudimentary; stamens 3; anthers ellipsoidal; connectives apiculate; ovary tricarpellate. Fruit nut-like, 3-angled, 3-seeded. Two species, P. palustris L. strongly polymorphic, eastern North America from Canada to Florida and the West Indies, and Colombia, south-eastern Brazil. 8. Myriophyllum L.

Fig. 65

Myriophyllum L., Sp. Pl.: 992 (1753); van der Meijden & Caspers, Fl. Males. I, 7:239–263 (1971); Orchard, Brunonia 2:247–287 (1980), New Zealand spp.; ibid. 4:27–65 (1981), Amer. spp.; ibid. 8:173–291 (1985), Austral. spp. Vinkia van der Meijden (1975).

Perennial, rarely annual, aquatic or littoral herbs, free-ﬂoating or rhizomatous. Leaves basally sometimes with 1(–3) ﬁliform to subulate deciduous

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stipule-like outgrowths (‘hydathodes’), usually in whorls of 3–6, sometimes opposite or alternate, usually dimorphic with pectinately divided submerged leaves and ± simple, entire emergent leaves, or, more rarely, leaves all similar, of one type or another. Inﬂorescences a simple, rarely branched spike with the ﬂowers borne singly (occasionally in dichasia) in the axils of emergent leaves and provided with 2 prophylls; ﬂowers rarely also in axils of submerged leaves, unisexual or rarely transitionally bisexual, plants monoecious or dioecious, in monoecious plants the upper ﬂowers commonly male, the lower female; ﬂowers (2–)4-merous, in males sepals and petals usually present, petals usually hooded, stamens (1–)4 or 8, ovary and stylodia vestigial or 0, in females sepals present or 0, petals vestigial or 0, stamens 0, ovary (2–)4-carpellate, stylodia 1 per carpel, clavate, rarely subulate, stigma usually capitate and ﬁmbriate. Fruit dry, variously ornamented, splitting at maturity into 1seeded mericarps. Almost cosmopolitan, although absent from most of Africa, the Middle East and much of southern Asia and north-eastern South America; about 60 species, with centres in Australia (36 spp., 31 endemic), North America (13 spp., 7 endemic), and India/Indo-China (10 spp., 7 endemic); M. aquaticum (Vellozo) Verdc. native to South America and adventive throughout tropical and warm-temperate regions of the world.

Selected Bibliography APG II 2003. See general references. Bowes, G. 1987. Aquatic plant photosynthesis: strategies that enhance carbon gain. In: Crawford, R.M.M. (ed.) Plant life in aquatic and amphibic habitats. Oxford: Blackwell, pp. 79–98. Corner, E.J.H. 1976. See general references.

Fauth, A. 1903. Beiträge zur Anatomie und Biologie der Früchte und Samen einiger einheimischer Wasser- und Sumpfpﬂanzen. Beih. Bot. Centralbl. 14:327–373. Fishbein, M. et al. See general references. Frederiksen, N.O. 1980. The mid-Tertiary spores and pollen grains from Mississippi and Alabama. Tulane Stud. Geol. Palaeontol. 10:65–86. Godwin, H. 1975. The history of the British ﬂora, 2nd edn. Cambridge: Cambridge University Press. Gruas-Cavagnetto, C., Praglowski, J. 1977. Pollen d’Haloragacées dans le Thanétien et le Cuisien du bassin de Paris. Pollen Spores 19:299–308. Hegnauer, R. 1966, 1989. See general references. Hernández-Castillo, G.R., Cevallos-Ferriz, S.R.G. 1999. Reproductive and vegetative organs with afﬁnities to Haloragaceae from the Upper Cretaceous Huepac chert locality of Sonora, Mexico. Amer. J. Bot. 86:1717–1734. Johri, B.M. et al. 1992. See general references. Mendes, E.J. 1978. Haloragaceae. In: Launert, E. (ed.) Flora Zambesiaca 4:74–81. Royal Botanic Gardens, Kew. Moody, M.L., Les, D.H. 2000. Phylogenetic relationships in Myriophyllum (Haloragaceae). Amer. J. Bot. 87, 6:177. Morgan, D.R., Soltis, D.E. 1993. Phylogenetic relationships among members of Saxifragaceae sensu lato based on rbcL sequence data. Ann. Missouri Bot. Gard. 80:631– 660. Orchard, A.E. 1975. Taxonomic revisions in the family Haloragaceae. I. The genera Haloragis, Haloragodendron, Glischrocaryon, Meziella and Gonocarpus. Bull. Auckland Inst. Mus. 10:1–293. Orchard, A.E. 1985. Myriophyllum (Haloragaceae) in Australasia. II. The Australian species. Brunonia 8:173– 291. Orchard, A.E. 1990. Haloragaceae. In: Flora of Australia 18:5–85. Canberra: Australian Government Publishing Service. Orchard, A.E., Keighery, G.J. 1993. The status, ecology and relationships of Meziella (Haloragaceae). Nuytsia 9:111–117. Praglowski, J. 1970. The pollen morphology of the Haloragaceae with reference to taxonomy. Grana 10:159–239. Schindler, A.K. 1905. Haloragaceae. In: Engler, A., Pﬂanzenreich IV, 225. Leipzig: W. Engelmann. Takhtajan, A. 1997. See general references.

Huaceae Huaceae A. Chev., Rev. Intl Bot. Appl. Agric. Trop. 27:28 (1947).

C. Bayer

Trees, sometimes tall, or shrubs, with strong odour of garlic. Leaves alternate, simple, with few roundish glands, elliptic, tip acuminate to cuspidate, base cuneate to obtuse, margin entire; stipules caducous. Flowers hermaphroditic, actinomorphic, hypogynous, in dense or few-ﬂowered axillary cymes or solitary; sepals 5, valvate in bud, free or partly united, with glands on adaxial surface; petals 5, free, induplicate-valvate, with long simple hairs on adaxial side; stamens (8)10, of equal length, all fertile, free, apparently arranged in one whorl; anthers basiﬁxed, dithecal, inner pollen sacs smaller than outer ones, dehiscence lengthwise or by apical slits; gynoecium 5-carpellate with terminal style and entire stigma; ovary unilocular; ovules solitary (Hua) or 5–6, basal, anatropous. Fruit capsular or indehiscent, 1(2)-seeded; seeds large, with a basal hilum; embryo straight; surrounded by copious endosperm. A family of two quite distinct genera from tropical Central and West Africa. Vegetative Structures. Simple, branched, and/or stellate hairs and peltate scales occur mainly on young twigs, leaves and petioles. Minute circular or oval glands are frequent near the base of the leaf blade, and in Afrostyrax kamerunensis mainly along the margin. They are made up by epidermal palisade-like cells. Anatomical characteristics which indicate a close relationship between Hua and Afrostyrax include paracytic stomata, occurrence of cristarque cells in various tissues, complex petiole vasculature, wood with libriform ﬁbres and conﬂuent parenchyma, vessels with simple perforations, and dilating rays in the bark. In contrast to Malvales, mucilage is lacking and the bark is not stratiﬁed into ﬁbrous and not-ﬁbrous layers (Baas 1972). Reproductive Structures. In both genera, the inﬂorescences arise from the axils of foliage leaves on indeterminate shoots. The inﬂorescences

are dense cymose ﬂower clusters with dichasial or monochasial ramiﬁcations. In Afrostyrax kamerunensis, these inﬂorescences are few- or even single-ﬂowered. Floral ontogeny (pers. obs.) starts in both genera with a successive, not quincuncial development of sepal primordia. Subsequently, the primordia of the other pentamerous whorls appear in the following succession: petals, alternipetalous stamens, alternisepalous stamens, and alternisepalous carpels. Deviations from the pentamerous structure can frequently be observed, for instance, in the gynoecium of Afrostyrax. In both genera, circular to oval epithelial glands are present on the ventral surface of the sepals. The petals of Hua are clawed and have ventral hispid projections which close together at anthesis (Fig. 67A), leaving access to the stamens and stigma only between the petal claws. On the basis of the petal projections, which are lacking in Afrostyrax, a relationship between Hua and Malvaceae-Byttnerioideae has been constructed. The anthers of Hua are short and open only at the apex; they expose the pollen on their reﬂexed inner surface. In Afrostyrax, the anthers are much longer and the connective is prolonged by an apical appendage. Here, the thecae open by long lateral slits. The unilocular ovary of Hua has only a single basal ovule. At maturity, it shows no vestiges of a pentamerous origin, which is detectable only in early ontogenetic stages (pers. obs.). Depending on the number of carpels per ﬂower, the ovary of Afrostyrax contains ﬁve to six ovules, of which usually only one or two develop into seeds. Embryology. Ovules are anatropous and bitegmic. In Hua, the seed coat is covered with simple unicellular hairs. The outer epidermis of the inner integument forms a ligniﬁed palisade layer. Endosperm is abundant and contains starch and oil droplets. The embryo is straight with ﬂat cotyledons (Baas 1972).

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on the rest of the surface of the grains. The folds do not seem to open, and can be interpreted neither as colpi nor as artefacts but may be pseudocolpi. Phytochemistry. Beijersbergen’s (1972) tests for hydrolysable and condensed tannins were negative for both genera, more detailed data being unknown.

Fig. 66. Huaceae. Hua gaboni, pollen, SEM ×1,700. (Photograph C. Bayer)

Pollen Morphology. The pollen grains of both genera agree even in details. They are mediumsized, oblate to suboblate, rounded-triangular and anguloaperturate (Fig. 66). The three rounded to oval, crassimarginate pores are provided with opercula. Additionally, three folds are usually found on both polar sides. Oltmann (1971) interpreted these as colpi in Hua but Baas (1972), who observed similar structures in acetolysed grains, rejected this view. Critical point-dried, unacetolysed pollen grains show a more delicate micro-granulate sculpture along these folds than

Afﬁnities. Hua was originally placed in Sterculiaceae, Afrostyrax in Styracaceae, each genus in a separate tribe or subfamily within the respective family to emphasize their isolated positions. Mildbraed (1913) was the ﬁrst to propose a close relationship between the two genera, which formally were united as Huacaceae by Chevalier (1947a). Afﬁnities with Malvales, Styracaceae, Olacaceae, Icacinaceae and Opiliaceae have been suggested; Cronquist (1981, 1983) included Huaceae in Violales. On the basis of a broad comparison of anatomical and other characters, Baas (1972) found most agreement between Huaceae and taxa now included in Malvaceae, whereas other members of Malvales as well as of Geraniales and Malpighiales showed fewer similarities. However, Huaceae differ from Malvaceae and other Malvales families in important characters such as the lack of palmate venation of the leaves – a negative result of the Halphen reaction, the absence of mucilage cavities, in inﬂorescence morphology, the type of glands, the structure of the androecium, and the

Fig. 67. Huaceae. A Hua gaboni, ﬂower. B Afrostyrax lepidophyllum, ﬂower, ×7. (Orig. C. Bayer)

Huaceae

unilocular gynoecium with basal placentation. Therefore, malvalean afﬁnities are unlikely and the position of Huaceae remains obscure. Molecular studies (Soltis et al. 2000; Savolainen, Chase et al. 2000; Savolainen, Fay et al. 2000) indicated afﬁnities with Celastraceae, albeit with low statistic support, and The Angiosperm Phylogeny Group (APG II 2003) left the family unassigned to order within the Eurosid I clade. More recently, Zhang and Simmons (2006) have provided some evidence for a possible sister relationship between Huaceae and Oxalidales. Distribution and Habitats. Both genera include trees and shrubs in forests and woodlands of Cameroon, Gabon, Congo, Zaire; Afrostyrax lepidophyllus extends to the Central African Republic and Ghana. Economic Importance and Conservation. For their garlic ﬂavour and scent, the bark, leaves, roots and seeds of Huaceae are locally used as a spice and for medical purposes (Bouquet 1969; Hegnauer 1989). Like many other taxa of tropical Africa, the family is endangered by deforestation. Key to the Genera 1. Petioles densely covered with stellate or peltate scale hairs; ventral petal projection lacking; connective with apical appendage; ovary with 5–6 ovules; fruit indehiscent 1. Afrostyrax – Petioles glabrous or covered with few simple or stellate hairs; petals with ventral projections; connective without apical appendage; ovary with 1 ovule; fruit dehiscent 2. Hua

1. Afrostyrax Perkins & Gilg

Fig. 67B

Afrostyrax Perkins & Gilg, Bot. Jahrb. Syst. 43:216 (1909).

Calyx splitting in 3(–5) segments, each sepal with 1–2 central glands on adaxial surface; petals elliptical to oblong, abaxial side bearing peltate or stellate hairs; ovary containing 5–6 ovules; fruit 1(2)seeded, indehiscent. Two or three species, A. lepidophyllus Mildbr. and A. kamerunensis Perkins &

193

Gilg (probably including A. macranthus Mildbr.; Chevalier 1947b); tropical West and Central Africa. 2. Hua L. Pierre ex De Wild.

Figs. 66, 67A

Hua L. Pierre ex De Wild., Ann. Mus. Congo V, 1:287 (1906).

Sepals free, glands in a row near the margin; petals dark red, with ventral projections and simple hairs, apical part of petals bending outwards; ovary with 1 ovule; fruit dehiscent, opening with 5–6 valves. A single species, Hua gabonii L. Pierre ex De Wild., tropical West and Central Africa.

Selected Bibliography APG II 2003. See general references. Baas, P. 1972. Anatomical contributions to plant taxonomy, II. The afﬁnities of Hua Pierre and Afrostyrax Perkins et Gilg. Blumea 20:161–192. Beijersbergen, A. 1972. Note on the chemotaxonomy of Huaceae. Blumea 20:160. Bouquet, A. 1969. Féticheurs et médicines traditionnelles du Congo (Brazzaville). Mém. O.R.S.T.O.M. 36. Chevalier, A. 1947a. La famille des Huacaceae et ses afﬁnités. Rev. Intl Bot. Appl. Agric. Trop. 27:26–29. Chevalier, A. 1947b. Arbres à ail, Huacacées et Styrax à benjoin. Rev. Intl Bot. Appl. Agric. Trop. 27:401–407. Cronquist, A. 1981. See general references. Cronquist, A. 1983. Some realignments in the dicotyledons. Nordic J. Bot. 3:75–83. Germain, R. 1963. 89. Huaceae. In: Flore du Congo, du Rwanda et du Burundi 10:317–319. Meise: National Botanic Garden of Belgium. Hegnauer, R. 1989. See general references. Mildbraed, J. 1913: Über die Gattungen Afrostyrax Perk. et Gilg und Hua Pierre und die “Knoblauch-Rinden” Westafrikas. Bot. Jahrb. Syst. 49:552–559. Oltmann, O. 1971. Pollenmorphologisch-systematische Untersuchungen innerhalb der Geraniales. Diss. Bot. 11. Perkins, J. 1909. Eine neue Gattung der Styracaceae aus dem tropischen Afrika. Bot. Jahrb. Syst. 43:214–217. Robyns, A. 1976. Huaceae. In: Flore d’Afrique Centrale (Zaire–Rwanda–Burundi). Meise: National Botanic Garden of Belgium. Savolainen, V., Chase, M.W. et al. 2000. See general references. Savolainen, V., Fay, M.F. et al. 2000. See general references. Soltis, D.E. et al. 2000. See general references. Zhang, L.-B., Simmons, M.P. 2006. Phylogeny and delimitation of the Celastrales inferred from nuclear and plastid genes. Syst. Bot. 31:122–137.

Hypericaceae Hypericaceae Jussieu, Gen. Pl.: 254 (1789) (“Hyperica”).

P.F. Stevens

Evergreen or sometimes deciduous herbs, shrubs or trees; glands or canals in most parts of the plant; xanthones widespread; hairs uni- or multicellular, eglandular, colleters common; terminal bud scaly or naked; leaves opposite, occasionally whorled or alternate, entire, estipulate; inﬂorescences terminal, more or less cymose, rarely axillary or ﬂowers single, ﬂowers polysymmetric, perfect, usually with prophylls; sepals free, (2–)4–5; petals (3)4–5, free; stamens (9–)∞, free or variously fasciculate or connate, anthers < 1(–1.2) mm long, dithecate, extrose, opening by slits, connective often with glands, staminodes alternipetalous or 0; nectary absent; ovary superior, 3–5-locular, placentation axile to parietal, ovules 1–∞/carpel, anatropous, bitegmic, tenuinucellate; stylodia free or basally more or less fused or style single, stigmas more or less expanded, smooth and sticky or ± punctate and papillate; fruit baccate or capsular, rarely a drupe; seeds small, winged or not, exotegmen ligniﬁed, with sinuous anticlinal walls; embryo straight or rarely curved; endosperm initially nuclear, often absent at maturity; germination epigeal, phanerocotylar. A family with 9 genera and 540 species; ± worldwide. Vegetative Morphology. Hypericaceae are mostly shrubs to trees, but there are some annual herbs (Hypericum). Taxa growing in drier regions (Hypericum, Psorospermum [= Harungana]) tend to develop a lignotuber, from which they sprout after ﬁre or drought; root suckering occurs in Hypericum (Hagemann 1989 and references therein; Hagemann and Meusel 1984) and Vismia. Architectural models within Vismia vary (Vester 1999). Roots of some Hypericeae inhabiting swamps (e.g., Triadenum, Hypericum) are swollen and with air spaces. The terminal bud may lack scales, but in many species of Harungana, Cratoxylum, etc., it has two or more pairs of scales; in Cratoxylum it may abort. Leaves are opposite, rarely more or

less irregularly spiral (e.g., Harungana [Psorospermum alternifolium]) or whorled. There are often colleters, but no stipules. Multicellular stellate hairs characterize Vismieae; Hypericeae may be glabrous, but unicellular hairs are found in some Hypericum. Buds in taxa that lack scales are sometimes covered with dense indumentum, as in Vismieae; colleters then appear to be lacking. The lamina is usually petiolate, although often sessile in Hypericum; the midrib is nearly always well-developed. Venation is commonly eucamptodromous or brochidodromous; it is close to parallelodromous or acrodromous in some species of Hypericum. The leaf margin is usually entire, but it may be crenate by glands (Harungana), or even lobate – and this can be true of the calyx as well – as in some species of Hypericum. Vegetative Anatomy. Metcalfe and Chalk (1950) summarize early literature; more recent studies include those of Spirlet (1959), Baas (1970), and Gibson (1980). There is a complex system of spherical to more or less elongated schizogenous glands and canals associated with the vascular tissue, and also found in both the cortex and pith. In the appendicular organs of the plant, these may be more or less independent of the vascular tissue (e.g., Cicarelli et al. 2001a). There are also reddish to black glands (as in Hypericum) containing hypericin and related compounds (Robson 1977; Cicarelli et al. 2001b; Onelli et al. 2002); these are clusters of cells that initially have meristematic features but that eventually become ﬁlled with black material. Variation in such glands, schizogenous structures and epidermal features in the leaves is of taxonomic interest (Lü and Hu 2001; Lü et al. 2001). Cotyledons, ﬁlaments and petals commonly have canals. The phellogen is always initiated in the deep-seated position in the pericycle (which may be ligniﬁed or not), both in stem and root. In

Hypericaceae

the stem, layers of cells, often with endodermal thickenings, are commonly interspersed with layers of unthickened cells in a polyderm (Mylius 1913); aerenchyma may develop (Schenck 1889). Hypericum has a clearly developed endodermis in the stem (cf. also some Bonnetiaceae). Nodes are single trace from a single gap. The petiole bundle varies from simple, commonly being arcuate in Hypericum, to more complex, annular, with additional vascular tissue inside the annulus, as in Vismia. Similarly, the midrib bundle varies from arcuate to more or less annular, with phloem toward the outside. The vascular bundles of even the higher-order veinlets vary from being more or less transcurrent, joined to at least one surface of the lamina by echlorophyllous and often ligniﬁed tissue, to embedded; the latter condition is common. Anticlinal epidermal cell walls are straight to sinuous. Leaves are nearly always hypostomatic, but amphistomatic in some Hypericum (e.g., Lü et al. 2001); stomates are usually paracytic, but in Hypericeae they may be anomocytic or even cyclocytic (Vestal 1937). In Harungana [Psorospermum membranaceum], stomata occur in small groups. Vessels are either single or in multiples, sometimes being in oblique lines. Perforation plates are usually simple, although they are sometimes scalariform. Pitting on tangential walls is generally alternate. Vasicentric tracheids have been recorded from a number of taxa. Wood parenchyma usually occurs, except perhaps in Hypericum. Septate ﬁbers occur, either with or without nuclei, but their distribution is very sporadic. Inﬂorescence Structure. The inﬂorescence in most species is modiﬁed cymose or thyrsiform, and a terminal ﬂower is nearly always present. Flowers have both bracts and prophylls. In Harungana, bracts are recaulescent, being borne on the pedicel where the lateral ﬂowers of the cymose inﬂorescence diverge (the prophylls are in turn borne along the pedicels of the ﬂowers they subtend); Vismia tends to show this behavior. In some Harungana from mainland Africa, the vegetative and ﬂoral parts of the stem are not clearly separated, and the relationship of branches to subtending leaves is very complex. Floral Structure. Sepals and petals are always present and free. Sepals are commonly ﬁve in number and quincuncial in aestivation, or four and decussate. When there are ﬁve petals, they are often

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contorted. Indumentum on the corolla in particular is uncommon, but all Vismieae have dense, unicellular hairs on the adaxial surface of the corolla. The androecium is fasciculate, often with ﬁve antepetalous fascicles (Fig. 68), but there may be only three or four (Fig. 69; see below). Staminodes, representing the alternipetalous whorl of the androecium, are common (rare in Hypericum itself), and are either three or ﬁve in number. Filaments are slender, the anthers are extrose, < 1(–1.2) mm long, and often with simple anther glands at the apex between the thecae. There is no nectary at the base of the ovary, but the staminodes have been described as “nectariferous scales”, and their vascular supply lacks xylem elements, as would be expected for nectaries (Ronse Decraene and Smets 1991). There are usually three or ﬁve carpels; when there are as many carpels as perianth members, they are opposite the sepals. Placentation is basically axile, although the placentae may fail to meet in the middle, and it varies from axile to parietal within Hypericum. Stylodia are usually long and free (Figs. 68, 69), or are more or less fused to a single style (this varies infragenerically within Hypericum). The ovules are anatropous, tenuinucellate, and the micropyle is bitegmic; the inner integument may be up to seven cells thick, and there is an endothelium (Mourão and Beltrati 2001). In Hypericeae, the stigma is more or less punctate and the surface is papillate (Shivanna et al. 1989). In the rest of the family, the stigma is punctiform to more or less expanded, and the surface is more or less smooth. Floral Anatomy and Development. Little is known about ﬂoral development and anatomy, the study by Payer (1857) still being useful; see also Sattler (1973). The androecium is basically diplostemonous. The stamen fascicles are antepetalous, and may originate with the corolla as complex primordia, or separately, or separately and subsequently forming complex primordia; the anther primordia may coalesce to form a ring primordium (see Ronse Decraene and Smets 1991 for a summary). Stamen development is centrifugal on the fascicles in those few taxa in which this feature has been observed (e.g., Leins 1964; Ronse Decraene and Smets 1991). The fascicles are supplied by a single vascular bundle. In taxa with three fascicles, vascular evidence (and gross morphology) shows that two of the fascicles, slightly larger than the others, are a fused pair of fascicles of a basically 5-fasciculate androecium (Baas 1970; Robson 1972, 1974, 1981). Staminodes

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may develop opposite the sepals; whether they represent single stamens of a basically diplostemonous androecium or fascicles is unknown. Those of Hypericum differ from those in other Hypericaceae in that they lack a vascular connection (Robson 1977), and have been described as an example of “evolutionary recall” (Robson 1972). Robson’s work should be consulted for details of the vasculature of ﬂoral parts. Pollen Morphology. Knowledge of the palynology of Clusiaceae is largely based on a general survey by Seetharam (1985; see also Yi 1979; Seetharam and Maheshwari 1986). The pollen is in monads, triporate or tricolporate, there being some disagreement in the recording of this character. Costae colpi are usually present, and there is considerable variation in endaperture type and orientation; the endexine around the aperture may be markedly thinned, as in Vismieae, and the apertural membrane may have numerous granules. The pollen surface shows considerable variation, and there is also some variation in nexine thickness; in most taxa it is < 1 µm thick, but in the monotypic Eliea it is slightly thicker. Karyology. Within Hypericum, haploid numbers of 6–12, 14, 16, and 18–24 have been recorded (e.g., Robson and Adams 1968); Robson (1981) suggests that x = 12 is the primitive number, although in the absence of a phylogeny, this is somewhat speculative. Triadenum has n = 18, 19. Pollination and Reproductive Systems. Apospory is reported from Hypericum and Triadenum (Noack 1939; Myers 1964), and polyembryony from Hypericum (see Johri et al. 1992 for references). For information about hybridization in Hypericum, see Robson (1981). Little is known about pollination. Staminodes have been implicated in the opening of the ﬂower (Hochreutiner 1918; Robson 1981). The predominant petal color is yellow, whereas white, pink, and red are less common; in European species of Hypericum, butterﬂies, ﬂies, and bees are visitors. The ﬂowers are usually perfect, and distyly appears to be quite common (Robson 1974); nothing further seems to be known about the latter. Anther glands are simple when they occur; dianthrones such as hypericin are found in the glands of Hypericum (Robson 1981). However, the ﬂowers of many genera, perhaps even of those with glands, may offer predominantly pollen as a reward; the presence of

nectar remains to be demonstrated (but see Ronse Decraene and Smets 1991). Fruit and Seed. Fruits are commonly capsular, dehiscence being septicidal, loculicidal, or a mixture of both (Eliea). Hypericum (rarely) and Vismieae have several-seeded berries (see Mourão and Beltrati 2001 for their anatomy), while the endocarp is notably scleriﬁed in Harungana madagascariense. The seed coat consists of a testa with a rather thin-walled epidermis that often contains tannins, as well as a low, ligniﬁed exotegmen with sinuous anticlinal walls (see also Corner 1976). There is a single chalazal vascular bundle. In some Harungana [Psorospermum] in particular, but also in Vismia, there are large, swollen, orange or black glands in the testa, and here the exotegmen may be inconspicuous in the mature seed. The endosperm often persists as a thin layer around the embryo. The embryo is usually white and straight, but in some Harungana it is green, and in others it may be curved. The embryo is 1–2 mm long, the cotyledons being about 25–40% the total length, but in some Madagascan species of Harungana the embryos are up to 6 mm long, the cotyledons being about 80% of their lengths. Germination is epigeal and phanerocotylar where known (e.g., Brandza 1908), although there are very few records. Dispersal. Taxa with capsules and small, dry seeds, and those with winged seeds, are probably wind-dispersed; the taxa with berries or drupes are probably animal-dispersed. Phytochemistry. Hypericaceae produce xanthones and anthraquinones. Xanthones such as mangiferin (e.g., Kitanov and Nedialkov 1998) have a wide distribution, but most others have narrower distributions. Prenylated xanthones are known from some, but not all, African species of Vismieae examined; only simple xanthones (and prenylated benzophenones) are known from American species (Habib et al. 1987). Emodin derivates, the naphto-dianthrones hypericin and pseudohypericin, show interesting distributions around and within Hypericum (Mathis and Ourisson 1963; Robson 1981). Anthrones, biemodyls, and related compounds occur in Vismieae, and the substitution patterns of prenylated anthranoids appear to help distinguish between African and American members of the

Hypericaceae

tribe (F. delle Monache, pers. comm.). There are distinctive coumarin derivates substituted at position 4 (Taylor and Brooker 1969). Relationships Within the Family. In the 19th century Clusiaceae and Hypericaceae were normally kept separate by, e.g., Planchon and Triana (1862, and references therein), Vesque (1893), and Engler (1925, see Robson 1981 for discussion). More recently, Clusiaceae have been included in Hypericaceae (the latter name is conserved, although Clusiaceae is generally the name that has been used: e.g., Robson 1978; Cronquist 1981); a variety of data can be interpreted to support this (e.g., Vestal 1937, who thought that Hypericaceae represented two separate lines derived from Clusiaceae). However, Hypericaceae are circumscribed narrowly here (Stevens on Clusiaceae-Guttiferae, this volume; see also Takhtajan 1997). Within the Hypericaceae, Vismieae are distinct; other groupings are less clear. Robson (1977, 1981) included Hypericum and Santomasia alone as Hypericeae. This tribe is circumscribed more broadly below (see Robson 2001), and includes all genera with papillate stigmas; generic limits need study. Cratoxyleae are the third tribe of the subfamily, and are phenetically distinct. Afﬁnities. There is little doubt that Clusiaceae, Bonnetiaceae, and Hyperiaceae are closely related, but details are unclear (e.g., Gustafsson et al. 2002). They all produce distinctive xanthones (Kubitzki et al. 1978) and have similar, exotegmic seeds; for further details, see Clusiaceae-Guttiferae (this volume). What was unexpected was the association of Podostemaceae with Hypericaceae, perhaps in particular Hypericum (e.g., Chase et al. 2002; Gustafsson et al. 2002). Although at ﬁrst sight there is little in common between the two (but this is true of practically any family with which Podostemaceae have been compared), Podostemaceae have cells that contain secretory products, tenuinucellate ovules, and papillate stigmas; xanthones are known to occur, and the pollen is sometimes tricolpate (see Podostemaceae, this volume, and Stevens 2005). A few Hypericeae are more or less aquatic plants. Distribution and Habitats. Hypericaceae are widely distributed. Hypericum itself includes shrubby to herbaceous plants, and grows both in more temperate regions and subalpine tropical habitats. Harungana in Africa grows in more

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open and drier vegetation; Vismia, as well as some species of Harungana such as H. madagascariensis, ﬂourish in secondary habitats; H. madagascariensis is apparently also sometimes lianescent. Pending a more detailed phylogeny, little can be said about the biogeography of the family. Vismieae are amphi-Atlantic, with Vismia in America, Harungana as here delimited in Africa–Madagascar (the one species of Harungana growing in Queensland is introduced). Hypericeae may have basal taxa endemic to Central America and east tropical Africa, while the Cratoxyleae are Madagascan-Malesian. Economic Importance. Several species of Hypericum are cultivated for their ﬂowers. Several species are important in local pharmacopeias, while in western medicine anti-tumor activity has been detected in xanthones, benzophenones (Bennett and Lee 1989) and vismiones (Casinelli et al. 1986; see also Amonkar et al. 1981). A number of prenylated anthranoids show anti-feedant activity, especially in oliogophagous insects (e.g., Simmonds et al. 1985). Hypericin and pseudohypericin are involved in photosensitive reactions in animals, and species such as Hypericum perforatum are noxious weeds (attempts have been made to control this species with chrysomelid beetles in North America). At the same time, photoactivated hypericin is a potent anti-proliferative agent of potential value in medicine; Hypericum perforatum extract may alleviate depression, and there are many other potential applications of Hypericum in medicine (Onelli et al. 2002; see Ernst 2003 for references).

Classiﬁcation of Hypericaceae I. Tribe Vismieae Choisy (1821). Genera 1–2 II. Tribe Hypericeae Choisy (1821). Genera 3–7 III. Tribe Cratoxyleae Bentham (1862). Genera 8–9

Key to the Genera 1. Indumentum on leaves and stem stellate; fruit baccate or drupaceous 2 – Plants usually glabrous, hairs simple; fruit capsular, rarely baccate 3 2. Bracts not (slightly) adnate to the pedicels; staminodes pubescent 1. Vismia – Bracts adnate to the pedicels (inﬂorescences capitate); staminodes glabrous 2. Harungana

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3. Petals often with adaxial scales; fruit dehiscing loculicidally (at least partly); seeds winged 4 – Petals usually lacking adaxial scales; fruit dehiscing septicidally; seeds barely or not winged 5 4. Fruit dehiscing septicidally and loculicidally; ovary loculi with inpushings 9. Eliea – Fruit dehiscing loculicidally; ovary loculi lacking inpushings 8. Cratoxylum 5. Petals yellow; stamens usually > 20/ﬂower, staminodes very uncommon 6 – Petals pink or white; stamens < 18/ﬂower, staminodes 3 7 6. Staminodes 5; petals subsymmetric 6. Santomasia – Staminodes 0(3); petals asymmetric or subsymmetric 3. Hypericum 7. Petals white; lamina with elongate glands abaxially; androecium with 10–18 stamens 4. Lianthus – Petals rose to ﬂesh-colored, or pink and white; lamina lacking elongated glands abaxially; androecium with < 12 stamens 8 8. Rhizomatous herb of marshes; ﬁlaments in each fascicle 1/3–1/2 united 5. Triadenum – Evergreen shrub; ﬁlaments in each fascicle largely free 7. Thornea

H. Perr., Fl. Madag. Comores 135e & 136e fam., 10–50 (1951); Bamps, Bull. Jard. Bot. Bruxelles 36:440–453 (1966). Vismia Vand. subg. Afrovismia P. Bamps, Bull. Jard. Bot. Bruxelles 36:428–440 (1966).

Trees to very small shrubs, sometimes sprouting from basal burl; terminal bud rarely aborting, or with scales; bracts recaulescent; petals usually white; 1–∞ stamens/fascicle, staminodes glabrous; 1–8(-∞) ovules/carpel; testa often glandular; cotyledons 1/2–6/7 length of embryo. Perhaps 50 species, in seven groups, Africa, Madagascar (26 spp.); low alt. The genus needs revision.

Basic characters: Leaves opposite, entire, exstipulate, with glandular dots (short lines); inﬂorescence terminal, cymose; ﬂowers polysymmetric, calyx and corolla free, androecium ± fasciculate, gynoecium superior. I. Tribe Vismieae Choisy (1821). Indumentum stellate; terminal bud lacking scales; ﬂowers usually heterostylous, petals with hairs on the adaxial surface, contorted to cochleate, lacking scales; fascicles and staminodes 5; stigma expanded, smooth; fruits berries. 1. Vismia Vand. Vismia Vand., Fl. Lusit. Brasil. Spec.: 51, t. 3, f. 24 (1788); Ewan, Contr. U.S. Natl Herb. 35:293–377 (1962), rev.

Trees or shrubs; bracts not to hardly recaulescent; ﬂowers homostylous or heterostylous; petals white to yellow or green; 3–∞ stamens/fascicle, staminodes hairy; 2–∞ ovules/carpel; testa rarely glandular; cotyledons 1/4–1/2(–3/5) length of the embryo. Circa 52 species, Central and South America; sea level to 2,800 m alt. 2. Harungana Lamarck

Fig. 68

Harungana Lamarck, Tab. Encycl. Méth., Bot. 2, 3: t. 645 (1796). Psorospermum Spach, Ann. Sci. Nat. Bot. II, 5:157 (1836);

Fig. 68. Hypericaceae. Harungana madagascariensis. A Flowering branch. B Flower. C The same, with a sepal and two petals removed. D Staminode. E Pistil. F Stamen fascicle. G Part of infructescence. H Drupe. I Coherent pyrenes. J The same, cut open to show seed. K Seed. (Milne-Readhead 1953)

Hypericaceae

II. Tribe Hypericeae Choisy, Prodr. Monogr. Hypéric.: 32 (1821). Plant usually glabrous, sometimes with unicellular or uniseriate hairs; terminal bud lacking scales; ﬂowers usually homostylous, petals glabrous, yellow, sometimes white to red, contorted, lacking scales; fascicles 3, free or variously united, staminodes 0(3, 5); stigma usually not or only little expanded, with rounded papillae; fruit a septicidal capsule, rarely a berry; seeds usually unwinged. 3. Hypericum L. Hypericum L., Sp. Pl.: 783 (1753); Robson, Bull. Brit. Mus. Nat. Hist. (Bot.) 5:291–355 (1977), 8:55–226 (1981), 16:1–106 (1987), 12:163–325 (1985), 20:1–151 (1990), and Bull. Nat. Hist. Mus. (Bot.) 26:75–217 (1996), 31:37–88 (2001), 32:61–123 (2002). Ascyrum L., Sp. Pl.: 787 (1753). Androsaemum Duhamel du Monceau (1755).

Large shrubs or small trees to rhizomatous, sometimes annual herbs; inﬂorescences rarely umbellate, with 1–∞ ﬂowers, these sometimes heterostylous; sepals 4 or 5, decussate or cochleate; petals 4, 5, yellow, sometimes red; fascicles sometimes 4, 5, or all united, 2–∞ stamens/fascicle, ﬁlaments free to connate, staminodes 0(3, 5); carpels 2–5, 2–∞ ovules/carpel, stylodia free to connate, stigmas punctate, sometimes expanded; cotyledons 1/4–1/2 length of embryo. Four hundred and twenty species, 32 sections: temperate regions generally (but few in Australia) and montane tropics. Scales on the petals are very rare. 4. Lianthus N. Robson Lianthus N. Robson, Bull. Nat. Hist. Mus. (Bot.) 31: 38 (2001).

Shrub, lamina with adaxial punctiform glands and abaxial linear glands; inﬂorescences with 5–7 ﬂowers; petals white, ?aestivation; 3–6 stamens/fascicle, ﬁlaments united at base, staminodes 3; carpels 3, ∞ ovules/carpel, stylodia free; cotyledons unknown. One species, L. ellipticifolius (H.L. Li) N. Robson, China (Yunnan); 1,800–2,200 m alt. 5. Triadenum Raf. Triadenum Raf., Fl. Tellur. 3:78. 1837, non Triadenia Spach (1836).

Rhizomatous herbs; inﬂorescences also axillary; petals also cochleate, pink to purple or white; 3

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stamens/fascicle, ﬁlaments fused, staminodes 3; carpels 3, ∞ ovules/carpel, stylodia free; cotyledons 1/4–1/2 length of embryo; n = 18, 19. Six species, Assam, East Asia, temperate North America; low alt. 6. Thornea Breedlove & McClintock Thornea Breedlove & McClintock, Madroño 23:369 (1976).

Shrubs; petals pink or pink and white; 3–4 stamens/fascicle, ﬁlaments at most basally united, anthers with glands or not; carpels 3, c. 15 ovules/carpel, stylodia free; cotyledons 1/4–1/2 length of embryo. Two species, southern Mexico (Chiapas) and northern Guatemala; montane. 7. Santomasia N. Robson Santomasia N. Robson, Bull. Brit. Mus. Nat. Hist. (Bot.) 8:61, Fig. 1 (1981).

Shrubs; ﬂower single, rarely in small groups, terminal; petals yellow; fascicles 5, 7–∞ stamens/fascicle, ﬁlaments almost free, staminodes 5; carpels 5, ∞ ovules/carpel, stylodia free; cotyledons 1/2–2/3 length of embryo. One species, S. steyermarkii (Standley) N. Robson, Guatemala and Mexico; 2,500–2,700 m alt. III. Tribe Cratoxyleae Bentham & J.D. Hooker, Gen. Pl. 1:164 (1862). Plant woody, glabrous; terminal bud perulate; ﬂowers homostylous or heterostylous; petals glabrous, rarely yellow, usually with scales; fascicles 3, staminodes 3; carpels 3, stigma slightly expanded, not papillate; fruit a more or less loculicidal capsule; seeds winged; cotyledons 1/2–2/3 length of embryo. 8. Cratoxylum Blume

Fig. 69

Cratoxylon Blume, Verh. Bat. Gen. 9:174 (1823); Gogelein, Blumea 15:453–475 (1967).

Tree to shrub; rarely pubescent and terminal bud aborting; ﬂowers homostylous or heterostylous; petals cochleate, red, purple, pink to white, rarely green; rarely scales 0; ∞ stamens/fascicle; 3–∞ ovules/carpel; capsule loculicidal. Three sections, six species, northeastern India and southern China to western Malesia; low alt., occasionally submontane.

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Fig. 69. Hypericaceae. Cratoxylon arborescens. A Flowering branch. B Flower. C Petal, ventral side, with basal scale. D Stamen. E Androecium and gynoecium, one of the three stamen fascicles cut away, between them the staminodes. F Young fruit. G Dehisced capsule. H Seed. (Gogelein 1967)

9. Eliea Cambess. Eliea Cambess., Ann. Sci. Nat. I, 20:400, t. 13 (1830); H. Perr. in Fl. Madag. Comores 135e & 136e fam.: 8–10 (1951).

Tree; ﬂowers heterostylous; petals contorted or cochlear, white; c. 15 stamens/fascicle; 2 ovules/ carpel, loculi almost completely subdivided; capsule septicidal and loculicidal. One species, E. articulata Cambess., Madagascar; low alt.

Selected Bibliography Amonkar, A., Chang, C.-J., Cassady, J.M. 1981. 6geranyloxy-3-methyl-1,8-dihydroxyanthrone, a novel anti-leukemic agent from Psorospermum febrifugum Sprach var. ferugineum (Hook. ﬁl.) [sic]. Experienta 37:1138–1139.

Baas, P. 1970. Floral and vegetative anatomy of Eliaea from Madagascar and Cratoxylum from Indomalesia (Guttiferae). Blumea 18:369-391. Bennett, G.J., Lee, H.-H. 1989. Xanthones from Guttiferae. Phytochemistry 28:967–998. Brandza, G. 1908. Recherches anatomiques sur la germination des Hypéricacées et des Guttifères. Ann. Sci. Nat. Bot. IX, 8:221–300, pls 5–15. Cassinelli, G., Geroni, C., Botta, B., delle Monache, G., delle Monache, F. 1986. Cytotoxic and antitumor activity of vismiones isolated from Vismieae. J. Nat. Prod. 49:929– 931. Chase, M.W. et al. 2002. See general references. Cicarelli, D., Andreucci, A.C., Pagni, A.M. 2001a. Translucent glands and secretory canals in Hypericum perforatum L. (Hypericaceae): morphological, anatomical and histochemical studies during the course of ontogenesis. Ann. Bot. 88:637–644. Cicarelli, D., Andreucci, A.C., Pagni, A.M. 2001b. The black nodules of Hypericum perforatum L. ssp. perforatum: anatomical and histochemical studies during the course of ontogenesis. Israel J. Pl. Sci. 49:33–40. Corner, E.J.H. 1976. See general references. Cronquist, A. 1981. See general references. Engler, A. 1925. Guttiferae. In: Engler, A., Prantl, K., Die natürlichen Pﬂanzenfamilien, ed. 2, 21. Engelmann, Leipzig, pp. 154–237. Ernst, E. (ed.) 2003. Hypericum: the genus Hypericum. New York: Taylor & Francis. Gibson, A. C. 1980. Wood anatomy of Thornea, including some comparisons with other Hypericaceae. I.A.W.A. Bull. n.s. 1:87–92. Gogelein, A.J.F. 1967. A revision of the genus Cratoxylum Bl. (Guttiferae). Blumea 15:453–475. Gustafsson, M.H.G., Bittrich, V., Stevens, P.F. 2002. Phylogeny of Clusiaceae based on rbcL sequences. Intl J. Pl. Sci. 163:1045–1054. Habib, A.M., Reddy, K.S., McCloud, T.G., Chang, C.-J., Cassady, J.M. 1987. New xanthones from Psorospermum febrifugum. J. Nat. Prod. 50:141–145. Hagemann, I. 1989. Wuchsformen einiger HypericumArten, ein Beitrag zum morphologischen und zum ökologischen Anliegen der Wuchsformen-Forschung. Flora 183:225–309. Hagemann, I., Meusel, H. 1984. Hypericum triquetrifolium Turra, ein Wurzelspross-geophyt: Wuchsform und Verbreitung. Flora 175:385–405. Hegnauer, R. 1966. See general references. Hochreutiner, B.P.G. 1918. La formation lodiculaire des corpuscles hypogynes chez les Guttifères. C. R. Soc. Phys. Hist. Nat. Genève 35:82–85. Johri, B.M. et al. See general references. Kitanov, G.M., Nedialkov, P.T. 1998. Mangiferin and isomangiferin in some Hypericum species. Biochem. Syst. Ecol. 26:647–653. Kubitzki, K., Mesquita, A.A.L., Gottlieb, O.R. 1978. Chemosystematic implications of xanthones in Bonnetia and Archytaea. Biochem. Syst. Ecol. 6:185–187. Leins, P. 1964. Die frühe Blütenentwicklung von Hypericum hookerianum Wight et Arn. und Hypericum aegyptiacum L. Ber. Deutsch. Bot. Gesell. 77:112– 123.

Hypericaceae Lü, H.-F., Hu, Z.-H. 2001. Comparative anatomy of secretory structures of leaves in Hypericum (in Chinese). Acta Phytotax. Sin. 39:393–404. Lü, H.-F., Chu, Q.-G., Hu, Z.-H. 2001. Comparative study on the epidermal micromorphology of Hypericum and Triadenum (in Chinese). Acta Bot. Bor.-Occ. Sin. 21:693–699. Mathis, C., Ourisson, G. 1963. Étude chimiotaxonomique du genre Hypericum, 1. Répartition de l’Hypéricine. Phytochemistry 2:157–171. Metcalfe, C.R., Chalk, L. 1950. See general references. Milne-Readhead, E. 1953. Hypericaceae. In: Turrill, W.B., Milne-Readhead, E. (eds) Flora of tropical East Africa. London: Crown Agents. Mourão, K.S.M., Beltrati, C.M. 2001. Morphology and anatomy of developing fruits and seeds of Vismia guianensis (Aubl.) Choisy (Clusiaceae). Revista Brasil. Biol. 61:147–158. Myers, O. 1964. Megasporogenesis, megagametophyte development and endosperm development in Hypericum virginicum. Amer. J. Bot. 51: 664 (Abstract). Mylius, G. 1913. Das Polyderm, eine vergleichende Untersuchung über die physiologischen Scheiden Polyderm, Periderm und Endodermis. Bibl. Bot. 18, 79:1–119, pls 1–4. Noack, K.L. 1939. Fortpﬂanzungsverhältnisse und Bastarde von Hypericum perforatum L. Zeitsch. Indukt. Abstamm. Vereb. 76:569–601. Onelli, E., Rivetta, A., Giorgi, A., Bignami, M., Cocucci, M., Patrignani, G. 2002. Ultrastructural studies on the developing secretory nodules of Hypericum perforatum. Flora 197:92–102. Payer, J.-B. 1857. Traité de organogénie comparée de la ﬂeur. Paris: Masson. Planchon, J.E., Triana, J. 1862. Mémoire sur la famille des Guttifères. Ann. Sci. Nat. Bot. IV, 16:263–308. Robson, N.K.B. 1972. Evolutionary recall in Hypericum. Trans. Bot. Soc. Edinburgh 41:365–383. Robson, N.K.B. 1974. Hypericaceae. In: van Steenis, C.G.G.J. (ed.) Flora Malesiana I, 8:1–29. Leiden: Noordhoff. Robson, N.K.B. 1977. Studies in the genus Hypericum L. (Guttiferae) 1. Infrageneric classiﬁcation. Bull. Brit. Mus. Nat. Hist. (Bot.) 5:291–355. Robson, N.K.B. 1978. Guttiferae. In: Heywood, V.H. (ed.) Flowering plants of the world. New York: Mayﬂower, pp. 85–87. Robson, N.K.B. 1981. Studies in the genus Hypericum L. (Guttiferae), 2. Characters of the genus. Bull. Brit. Mus. Nat. Hist. (Bot.) 8:55–226.

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Robson, N.K.B. 2001. Studies in the genus Hypericum L. (Guttiferae), 4, 1. Sections 7. Roscyna to 9. Hypericum sensu lato (part 1). Bull. Nat. Hist. Mus. (Bot.) 31:37–88. Robson, N.K.B., Adams, W.P. 1968. Chromosome numbers in Hypericum and related genera. Brittonia 20:95–106. Ronse Decraene, L.P., Smets, E. 1991. Androecium and ﬂoral nectaries of Harungana madagascariensis (Clusiaceae). Pl. Syst. Evol. 178:179–194. Sattler, R. 1973. Organogenesis of ﬂowers, a photographic text-atlas. Toronto: University of Toronto Press. Schenck, H. 1889. Ueber das Aërenchym, ein dem Kork homologes Gewebe bei Sumpfpﬂanzen. Jahrb. Wissensch. Bot. 20: 526-574, pls 23–28. Seetharam, Y.N. 1985. Clusiaceae: palynology and systematics. Pondichéry: Travaux de la Section Scientiﬁque et Technique, Institut Français, t. 21. Seetharam, Y.N., Maheshwari, J.K. 1986. Scanning electron microscopic studies on the pollen of some Clusiaceae. Proc. Indian Acad. Sci. (Pl. Sci.) 96:217–226. Shivanna, K.R., Ciampolini, F., Cresti, M. 1989. The structure and cytochemistry of the pistil of Hypericum calycinum: the stigma. Ann. Bot. 63:613–620. Simmonds, M.S.J., Blaney, W.M., delle Monache, F., Marquina Mac-Quhae, M., Marini Bettolo, G.B. 1985. Insect antifeedant properties of anthranoids from the genus Vismia. J. Chem. Ecol. 11:1593–1599. Spirlet, M. 1959. Étude taxonomique des épidermes foliaires des Hypéricacées et des Guttiféracées du bassin du ﬂeuve Congo. Bull. Inst. Franç. Afr. Noire 29:5–91. Stevens, P.F. 2005. See general references. Takhtajan, A. 1997. See general references. Taylor, H.L., Brooker, R.M. 1969. Isolation of Uliginosin A and Uliginosin B from Hypericum uliginosum. Lloydia 32:217–219. Vesque, J. 1893. Guttiferae. In: Candolle, A.C.P. de (ed.) Monographiae Phanerogamarum, vol. 8. Paris: Masson, pp.1–699. Vestal, P.A. 1937. The signiﬁcance of comparative anatomy in establishing the relationship of the Hypericaceae to the Guttiferae and their allies. Philipp. J. Sci. 64:199– 256. Vester, H. 1999. Architectural diversiﬁcation within the genus Vismia (Clusiaceae) in the Amazonian rainforest (Ararucuara, Colombia). In: Kurmann, M.H., Hemsley, A.R. (eds) The evolution of plant architecture. Royal Botanic Gardens, Kew, pp. 147–158. Yi, X.-Z. 1979. Pollen morphology of Guttiferae in China (in Chinese). Acta Bot. Sin. 21:36–41.

Iteaceae Iteaceae J. Agardh, Theoria Syst. Pl.: 151 (1858), nom. cons.

K. Kubitzki

Trees and shrubs, sometimes climbing; pith lamellate; axillary buds sometimes superposed. Leaves alternate, glandular-serrate (spiny-dentate in Itea ilicifolia) or rarely entire, pinnately veined; stipules minute, subulate, or 0. Inﬂorescences manyﬂowered terminal or axillary panicles or racemes, often superposed in groups of 2 or 3. Flowers small, regular, hermaphrodite or polygamous; sepals 5, basally connate into a short, turbinate or obconic tube adnate to base of ovary, lobes valvate or apert, persistent; petals 5, valvate, persistent; stamens 5, alternating with the petals, inserted at the margin of the annular nectary disk; anthers small, oblong to ovoid, dorsiﬁxed, introrse, at the apex with a globular protrusion of the connective; gynoecium of 2 united carpels, ovary 2-locular, nearly superior to more than 3/4 inferior; style undivided (postgenitally united?) or more or less deeply divided into two stylodia but then, at anthesis, apically coherent with globular stigmas; stigmas capitate, cohering but separating in fruit; ovules numerous on axile placentas, bitegmic and crassinucellate. Fruit a capsule with persistent perianth, dehiscing septicidally; seeds with large, curved embryo surrounded by sparse, ﬂeshy endosperm. n = 11. A single genus with about 27 species in Southeast Asia, one in Africa and one in North America. Morphology and Anatomy. Itea has simple, acutely pointed and glandular hairs, in contrast to the relatively complex trichomes present in other members of Saxifragales. The subulate stipules have been ﬁgured by Weberling (1976). Ovary position varies from nearly superior to more than 3/4 inferior. The carpels are connate through their entire length (Ge at al. 2002) or free from where the ﬂoral cup becomes free from the ovary wall (Bensel and Palser 1975). Nectariferous tissue (a disk) was found to be present in all species examined. Nodes are trilacunar–3-trace. Stomata are anomocytic. Leaf teeth are glandular. Druses are present in cortex and pith. Cork arises superﬁcially. Vessel

elements have scalariform perforations with numerous slender bars; lateral pitting is scalariform. Rays are uniseriate, heterocellular. Embryology. In Itea virginica, Mauritzon (1939) found the ovules bitegmic and crassinucellate, and the embryo sac 8-nucleate. For Choristylis rhamnoides, the crassinucellate condition was also determined (Mauritzon 1933). Pollen Morphology. Pollen is bilateral/heteropolar and biporate, 14–23 × 20–33 µm; the exine is tectate (Erdtman 1952; Agababian 1960). Karyology. For Itea virginiana and four Asian species, 2n = 22 has been reported. Fruit and Seed. Seeds are narrowly fusiform or more or less ovoid, which Engler (1891) used to separate his sections of Itea, sect. Sempervirentes with evergreen leaves and fusiform seeds, and sect. Deciduae with deciduous leaves and ovoid seeds. The inclusion of I. rhamnoides, which is evergreen and has ± ovoid seeds, makes this distinction untenable. In Itea virginica and I. sinensis, the testa is strongly thickened and tanniniferous but apparently not ligniﬁed; all other tissues of the seed coat are crushed. The endosperm is moderately developed and contains fat and aleuron. The embryo has a length of about 3/4 of the seed (Krach 1976; Nemirovich-Danchenko 1994). Afﬁnities. Formerly included in Escalloniaceae, Iteaceae differ from them in their peculiar diporate pollen grains, bitegmic and crassinucellate ovules, basic chromosome number, chambered pith and ﬂoral anatomy (Takhtajan 1997). The globular anther protrusion (Fig. 70D) may be compared with the apical nectaries on the anthers of Grossulariaceae. Molecular analyses place Itea and Choristylis into the Core Saxifragales sister to

Iteaceae

Pterostemon (Savolainen, Fay et al. 2000; Fishbein et al. 2001). Phytochemistry. Itea (3 spp. examined) lacks ﬂavonols and consistently contains C-glycosyl ﬂavones, an unusual feature in Saxifragales (Bohm et al. 1988). Distribution and Habitats. Itea occurs mainly in temperate and tropical South and Southeast Asia from the Himalayas to China, Japan, Java and the Philippines, mostly in colline and montane habitats, rarely ascending up to an altitude of 3,000 m; one species is found in East, Central and South Africa, where it grows in evergreen forest margins, riverine and valley forests, rock crevices and by streams at an altitude of 900–2,300 m; another species is known from eastern North America, where it occupies moist and wet sites preferably in the Coastal Plain.

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Fossil Record. Fossil pollen referable to Itea has been reported from the Eocene through Pliocene in Europe, and the Oligocene and Pliocene in North America (see references in Hermsen et al. 2003). Uses. Itea ilicifolia, I. yunnanensis and the more hardy I. virginica are cultivated as garden ornamentals. Only one genus: 1. Itea L. Itea L., Sp. Pl.: 199 (1753). Choristylis Harv. in Hook., London J. Bot. 1:19 (1842); Verdcourt, Fl. Zambesiaca 7, 1:1–3 (1983).1

Description as for the family.

Selected Bibliography Agababian, V.S. 1960. On the palynosystematics of the family Iteaceae (in Russian). Bull. Armenian Acad. Sci., Biol. 13:99–102. Bensel, C.R., Palser, B.F. 1975. Floral anatomy in the Saxifragaceae sensu lato. II. Saxifragoideae and Iteoideae. Amer. J. Bot. 62:661–675. Bohm, B.A., Chalmers, G., Bhat, U.G. 1988. Flavonoids and the relationships of Itea to the Saxifragaceae. Phytochemistry 27:2651–2653. Cutler, D.F., Gregory, M. (eds) 1998. Anatomy of the dicotyledons, 2nd edn. IV. Saxifragales. Oxford: Clarendon Press. Elst, P. van der 1909. Beiträge zur Kenntnis der Samenanlage der Saxifragaceae. Ph.D. Dissertation, University of Utrecht. Engler, A. 1891. Saxifragaceae. In: Engler, A., Prantl, K., Die natürlichen Pﬂanzenfamilien III, 2a. Leipzig: W. Engelmann. pp. 41–93. Erdtman, G. 1952. See general references. Fishbein, M. et al. 2001. See general references. Ge, L.-P., Lu, A.-M., Pan, K.-Y. 2002. Floral ontogeny in Itea yunnanensis (Iteaceae). Acta Bot. Sin. 44:1261– 1267. Hermsen, E.J., Gandolfo, M.A., Nixon, K.C., Crepet, W.L. 2003. Divisestylus gen. nov. (aff. Iteaceae), a fossil saxifrage from the late Cretaceous of New Jersey, USA. Amer. J. Bot. 90:1373–1383.

Fig. 70. Iteaceae. Itea rhamnoides. A Habit. B Inﬂorescence. C Flower, opened out. D Stamen. E Vertical and transverse section of ovary. F Fruit, note the coherent stigmas. G Seed. (Drawn by E. Margaret Stones; Verdcourt 1973)

1 When Bentham (in Benth. & Hook., Gen. Pl. 1865) kept separate Itea and Choristylis, only two species of Itea were known. The addition of more than 20 species to Itea since then has greatly broadened its range of variation of characters, such as ovary position, the degree of fusion of the stylodia, and ramiﬁcation of the inﬂorescences, and makes the maintenance of Choristylis virtually impossible. The pollen of the two genera is identical, and earlier claims of unitegmic ovules in Choristylis (still maintained in Cutler and Gregory 1998) are erroneous. Itea rhamnoides, comb. nov., based on Choristylis rhamnoides Harv. in Hook., London J. Bot. 1: 19 (1842).

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Hideux, M.J., Ferguson, I.K. 1976. See general references. Krach, J.E. 1976. Die Samen der Saxifragaceae. Bot. Jahrb. Syst. 97:1–60. Mauritzon, J. 1933. Studien über die Embryologie der Families Crassulaceae und Saxifragaceae. Ph.D. Thesis, University of Lund. Lund: H. Olssson. Mauritzon, J. 1939. Contributions to the embryology of the orders Rosales and Myrtales. Lunds Univ. Årsskr. N.F. 2, 35, 2. Lund: Gleerup, 121 p. Nemirovich-Danchenko, E.N. 1994. Morphology and anatomy of the seeds of Iteaceae (in Russian). Bot. Zhurn. (Moscow & Leningrad) 79:83–87. Petrov, S., Drazheva-Stamatova, T. 1973. Itea L. fossil pollen in Tertiary sediments of Europe and North America. C. R. Acad. Bulg. Sci. 26:811–814.

Rylova, T.B. 1994. Morphological features of pollen in some fossil and extant species of Itea (Iteaceae) (in Russian). Bot. Zhurn. (Moscow & Leningrad) 74:694–699. Savolainen, V., Fay, M.F. et al. 2000. See general references. Takhtajan, A. 1969. Flowering plants. Origin and dispersal. Edinburgh: Oliver and Boyd. Verdcourt, B. 1973. Escalloniaceae. In: Polhill, R.M. (ed.) Flora of Tropical East Africa. London: Crown Agents, pp. 1–3. Weberling, F. 1976. Weitere Untersuchungen zur Morphologie des Unterblattes bei den Dikotylen. IX, Saxifragaceae s.l., Brunelliaceae and Bruniaceae. Beitr. Biol. Pﬂanzen 52:163–181. Wolfe, J.A. 1970. Neogene ﬂoristic and vegetational history of the Paciﬁc Northwest. Madroño 20:83–110.

Ixerbaceae Ixerbaceae Griseb., Grundr. Syst. Bot.: 122 (1854).

J.V. Schneider

Small, evergreen trees; unicellular ligniﬁed Tshaped trichomes present both on vegetative and ﬂoral parts. Leaves alternate, opposite or verticillate, simple, petiolate, estipulate, coriaceous, serrate, gland-tipped, venation pinnate-reticulate. Inﬂorescences terminal, few-ﬂowered, corymbose panicles, the pedicels articulated. Flowers actinomorphic, perfect, the calyx tube short, adnate to base of ovary; sepals 5, persistent, imbricate, the outer ones shorter, the three inner ones enclosing the inner organs in bud; petals 5, imbricate, free, clawed, white, inserted on ﬂoral cup; stamens 5, free, antesepalous, alternating with disk lobes; anthers dorsiﬁxed, sagittate, introrse, versatile, opening by longitudinal slits, with a hypogynous 5-lobed disk; gynoecium 5-carpellate; ovary superior to semi-inferior, syncarpous, 5-locular; style simple, apical, hollow; stigma punctiform; placentation axile, ovules 2 per carpel, pendant, collateral, bitegmic, crassinucellar, anatropous. Fruit a few-seeded, loculicidal capsule; seeds 1(2) per locule, large, shiny blackish with a red aril; embryo large, with thick cotyledons and small radicula; endosperm scanty. A single genus and species (Ixerba brexioides A. Cunn.), endemic to the North Island of New Zealand Vegetative Morphology. Ixerba is an evergreen tree up to 15 m in height. The leaves are pseudoverticillately arranged. The venation corresponds to the semicraspedodromous type; the intersecondaries are poorly deﬁned (Gornall et al. 1998). Vegetative Anatomy. The leaf epidermis is one-layered. The stomata are anomocytic and restricted to the abaxial surface (Philipson 1967). The mesophyll consists of 1–3 layers of palisade parenchyma and is reported to contain crystal druses as well as simple crystals. The nodes are trilacunar

with three traces (Thouvenin 1890; Watari 1939; Hils 1985; Gornall et al. 1998). Cork arises in subepidermal layers. There are scattered groups of sclerenchymatous cells as well as simple crystals and druses in the cortex. The wood is hard, heavy, diffuse-porous, and vessels are solitary, rarely in multiples or clusters of 2–3. The vessel elements are up to 1,090 µm long. Perforation plates are scalariform and oblique. Intervessel pits are scanty, opposite and up to 39 µm in diameter. Helical thickenings are inconspicuous. Fibre-tracheids are eseptate, 8–35 mm in diameter, and have bordered pits on the tangential and radial walls. Wood parenchyma is sparse, apotracheal, rarely vasicentric. Rays are 1–5 cells wide (Watari 1939; Patel 1973; Meylan and Butterﬁeld 1975; Gornall et al. 1998). Flower Structure. The ﬂowers of Ixerba are large, bisexual and pentamerous. All organs are united into a cup. The ﬁve sepals are spirally arranged and the two outer sepals are smaller than the inner ones. Aestivation is imbricate but in petals may vary from quincuncial to cochlear or contort. There are ﬁve fertile antesepalous stamens which alternate with the ﬁve basal nectary lobes. The anthers show a connective protrusion. The gynoecium is syncarpous and consists of ﬁve antepetalous carpels. The ovary is superior to halfinferior and is characterised by ﬁve pronounced dorsal ridges and ﬁve less conspicuous ones in between. In the upper style, the ﬁve carpels are postgenitally united (Fig. 71C) and end in a single, punctiform stigmatic surface. The style is hollow. Placentation is axile and there are two collateral, antitropous ovules per carpel; some of the ovules may abort. Unicellular ligniﬁed, T-shaped hairs are present on the sepals and petals. Special mucilage cells are observed in the petals (Bensel and Palser 1975; Matthews and Endress 2005). The antepetalous staminodia of Ixerba reported by Takhtajan (1997) could not be veriﬁed.

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Embryology. Pollen grains are two-celled. Ovules are bitegmic, anatropous and crassinucellar. The embryo sac is of the Polygonum type (Kamelina 1992). Pollen. The pollen is 4–5-colporate and oblate to suboblate. The exine is thickened. The sexine is thinner than the nexine (Erdtman 1952; Pastre and Pons 1973). Fruit and Seed. The fruits are loculicidal capsules with few blackish seeds. The tips remain together while the bases are already separated (Fig. 71D). The seeds bear an incipient aril which contains fatty oils (Matthews and Endress 2005). Pollination and Dispersal. Ixerba is reported to be predominantly bird-pollinated. The diaspores are probably dispersed by birds and feral pigs (McEwen 1978; Thomson and Challies 1988). Phytochemistry. Proanthocyanidins are reported from the cortex. Urolic acid, a free triterpenic acid, occurs in the leaves (Hegnauer 1973). Afﬁnities. Ixerba was often considered a member of Saxifragaceae or allied families. A close relationship with Brexia or Roussea, as suggested by Engler (1930) and others, is supported neither by molecular (e.g. Koontz and Soltis 1999) nor by detailed morphological/anatomical studies, since these genera differ markedly in ﬂoral vasculature, ovary position, number of ovules, disposition of sepals, embryology and/or wood and seed anatomy (Bensel and Palser 1975; Krach 1976; Kamelina 1992; Gornall et al. 1998), whereas their shared characters are few and probably plesiomorphic. According to the updated classiﬁcation of the Angiosperm Phylogeny Group (APG II 2003), Ixerbaceae are included in Crossosomatales, which is supported by various molecular studies (Nandi et al. 1998; Savolainen, Fay et al. 2000; Soltis et al. 2000; Cameron 2003; Sosa and Chase 2003). Cameron (2003) emphasised the similarities in wood anatomy between Ixerbaceae and Strasburgeriaceae, and morphological and anatomical studies of the ﬂoral structure support the close relationship of Ixerbaceae and Strasburgeriaceae as well as that of Ixerbaceae, Strasburgeriaceae and Geissolomataceae (Cameron 2003; Matthews and Endress 2005). According to Matthews and

Fig. 71. Ixerbaceae. Ixerba brexioides. A Habit. B Flower. C Immature Fruit. D Dehiscing fruit. (Engler 1930)

Endress (2005), potential ﬂoral synapomorphies for both families may be the comparatively large ﬂowers, stamens with long ﬁlaments and sagittate anthers, the pentamerous conical gynoecium with streamlined transition from ovary to style, the antitropous ovules, unicellular ligniﬁed T-shaped hairs on the perianth, and the presence of idioblasts with striate mucilaginous inner tangential walls in ﬂoral organs. Distribution and Habitats. Ixerba is endemic to New Zealand and occurs in mountainous forests (e.g. Podocarp-Tawa forests) of the North Island. Flowering is from September to December. Palaeobotany. Reports on fossil Ixerba from New Zealand date back to the Mid-Miocene (Lee et al. 2001). Economic Importance. Ixerba brexioides, locally called Tawari by the Maori, is economically not important, except for the honey produced from its ﬂowers. Only one genus: Ixerba A. Cunn.

Fig. 71

Ixerba A. Cunn., Ann. Nat. Hist. 3:249 (1839).

Characters as for family. Ixerba brexioides A. Cunn. is the only species.

Ixerbaceae

Selected Bibliography APG II 2003. See general references. Bensel, C.R., Palser, B.F. 1975. Floral anatomy in the Saxifragaceae sensu lato. I. Introduction, Parnassioideae and Brexioideae. Amer. J. Bot. 62:176–185. Cameron, K.M. 2003. See general references. Engler, A. 1930. Brexioideae. In: Engler, A., Prantl, K., Die natürlichen Pﬂanzenfamilien, ed. 2, 18a. Leipzig: W. Engelmann, pp. 185–187. Erdtman, G. 1952. See general references. Gornall, R.J., Al-Shammary, K.I.A., Gregory, M. 1998. Escalloniaceae. In: Cutler, D.F., Gregory, M. (eds) Anatomy of the dicotyledons, 2nd edn. IV. Saxifragales. Corby, UK: Oxford University Press. Hegnauer, R. 1973. See general references. Hils, M.H. 1985. Comparative anatomy and systematics of twelve woody Australasian genera of the Saxifragaceae. Ph.D. Thesis, University of Florida, FL. Kamelina, O.P. 1992. K embriologii roda Ixerba v svyazi s ego sistematicheskim polozheniem. (On the embryology of the genus Ixerba in relation to its systematic position). Bot. Zhurn. (Moscow & Leningrad) 77:112–117. Koontz, J.A., Soltis, D.E. 1999. DNA sequence data reveal polyphyly of Brexioideae (Brexiaceae; Saxifragaceae sensu lato). Pl. Syst. Evol. 219:199–208. Krach, J.E. 1976. Samenanatomie der Rosiﬂoren, I. Die Samen der Saxifragaceae. Bot. Jahrb. Syst. 97:1–60. Lee, D.E., Lee, W.G., Mortimer, N. 2001. Where and why have all the ﬂowers gone? Depletion and turnover in the New Zealand Cenozoic angiosperm ﬂora in relation to

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palaeogeography and climate. Austral. J. Bot. 49:341– 356. Matthews, M.L., Endress, P.K. 2005. See general references. McEwen, W.M. 1978. The food of the New Zealand Pigeon (Hemiphaga novaeseelandiae novaeseelandiae). N. Z. J. Ecol. 1:99–108. Meylan, B.A., Butterﬁeld, B.G. 1975. Occurrence of simple, multiple, and combination perforation plates in the vessels of New Zealand woods. N. Z. J. Bot. 13:1– 18. Nandi, O.I. et al. 1998. See general references. Pastre, A., Pons, A. 1973. Quelques aspects de la systématique des Saxifragacées à la lumière des données de la palynologie. Pollen Spores 15:117–133. Patel, R.N. 1973. Wood anatomy of the dicotyledons indigenous to New Zealand. 2. Escalloniaceae. N. Z. J. Bot. 11:421–434. Philipson, W.R. 1967. Griselinia Forst. ﬁl.: anomaly or link. N. Z. J. Bot. 5:134–165. Savolainen, V., Fay, M.F. et al. 2000. See general references. Soltis, D.E. et al. 2000. See general references. Sosa, V., Chase, M.W. 2003. See general references. Takhtajan, A. 1997. See general references. Thomson, C., Challies, C.N. 1988. Diet of feral pigs in the Podocarp-Tawa forests of the Urewera ranges. N. Z. J. Ecol. 11:73–88. Thouvenin, M. 1890. Recherches sur la structure des Saxifragacées. Ann. Sci. Nat., Bot. VII, 12:1–174. Watari, S. 1939. Anatomical studies on the leaves of some saxifragaceous plants, with special reference to the vascular system. J. Fac. Sci. Univ. Tokyo, Sect. 3, Bot. 5:195– 316.

Krameriaceae Krameriaceae Dumort., Anal. Fam. Pl.: 20, 23 (1829), nom. cons.

B.B. Simpson

Rhizomatous shrubs, subshrubs, or perennial herbs semiparasitic on the roots of a wide array of ﬂowering plants. Leaves alternate, simple or trifoliolate, estipulate, entire, variously vestitured. Flowers axillary and single or in botryoid panicles, bisexual, zygomorphic, hypogynous with 5(4) purple, pink, or yellow showy, imbricate sepals and 5(4) petals, the 2 abaxial of which are reduced to glandular, lipid-secreting structures and the remaining 3(2) small and forming a ﬂag inserted adaxially above the ovary. Stamens 4(3), 4-locular, curved, with stout ﬁlaments usually united basally, and anthers dehiscing by terminal pores; ovary superior, unilocular; carpels 2 but appearing singular due to the early abortion of one carpel; style stout, curved; stigma recessed; ovules 2, pendulous from the top of the ovary, anatropous, bitegmic. Fruits globose, nut-like, spiny capsules with the thin pericarp splitting irregularly, 1-seeded; seed large, lacking endosperm; cotyledons orbicular, ventrally ﬂattened. One genus with 18 species, primarily in warm arid and semiarid areas of North, Central, and South America, and sporadically in the West Indies. Vegetative Morphology. Krameria species range from small trees (to 6 m) to sprawling herbaceous perennials. The root system consists of the remnants of the original tap root, and a series of lateral, adventitious roots (Musselman 1975) that branch sparingly. Individual roots are ﬂexible, covered with a thick, soft bark. The shoots of some shrubby species are stiff, forming thorns at the branch tips. In a few woody species, the stems can be lax. The herbaceous species are invariably prostrate, dying back to a woody caudex during the winter or in dry periods. Leaves are alternate, usually simple, and entire. They can be sessile or petiolate, range in shape from linear to ovate, and vary between 3 and 35 mm in length. One species has trifoliolate, petiolate leaves. Leaf surfaces in all species are vestitured with trichomes ranging from sparsely strigose to densely tomentose. Vestiture

is most pronounced on the young portions of the stems, with individual trichomes unicellular and thick-walled (Metcalfe and Chalk 1950). Some woody species loose their leaves during extremely dry periods. Vegetative Anatomy. All Krameria species examined to date are obligate semiparasites. Young woody stems have an epidermis with highly cutinized cell walls. The cork arises deep in the stem, sometimes even within the pericycle (Metcalfe and Chalk 1950). The phloem appears to lack ligniﬁed elements. The xylem forms a continuous cylinder with faint rays. Both the diameter of xylem elements and the amount of pith vary between species (Metcalfe and Chalk 1950). The seedlings do not produce root hairs (Cannon 1910), and haustorial attachment must occur within a few months of germination, or seedlings die (Simpson 1989). Haustoria are formed only by young, adventitious roots. Penetration of the haustoria appears to be shallow (Cannon 1910), with connections to the xylem only (Kuijt 1969). The vasculature of the haustoria consists of elongate, storied vessel elements (Musselman 1975). Stomates are present on both surfaces of the leaves. The outer epidermal walls and bases of the trichomes are cutinized. The leaves have three principal veins, each of which branches to form a network of veins supplying the entire leaf. The mesophyll includes scattered sclereids, and tanniferous material and crystals are common in unligniﬁed cells. The xylem of the leaves lacks vessels and consists of tracheids overlain by a thin layer of poorly developed sieve tube elements (Sterling 1912; Metcalfe and Chalk 1950). Petiolar anatomy consists of a single, crescent-shaped (almost circular in some) vascular strand (Metcalfe and Chalk 1950). Inﬂorescence Structure. The ﬂowers are borne singly in the axils of leaves, or in terminal racemes or panicles. Individual ﬂowering stalks

Krameriaceae

consist of a combined peduncle-pedicel with a pair of transversal prophylls where the two join. The ﬂowering stalk contains a single undissected vascular cylinder (Musselman 1975). The pedicel and bracts persist if the ﬂower is shed. The lengths of the peduncle and pedicels vary between species. Flower Structure. Flowers are extremely modiﬁed, which led to almost 200 years of misunderstanding about the ﬂoral morphology and biology (Simpson 1982). It is now recognized that the ﬂowers are not resupinate, and that the showy portions consist of the ﬁve (rarely four) free sepal lobes. The sepals have three principal veins, like the leaves. Only the upper surface, at least in K. lanceolata, bears stomata (Milby 1971). Two of the petals are modiﬁed into thick, orbicular to cuneate glands ﬂanking, or slightly abaxial to, the ovary. Each of these small, ﬂeshy structures is traversed by several veins (Milby 1971). The dorsal face of the glandular petals bears patches of secretory epidermal cells that secrete fatty oils under the cuticle. Once secreted, the oils are trapped until the cuticle is ruptured. The glandular cells can cover the dorsal petal surface or be restricted to the distal portion. The petaloid petals are small, strap-shaped or clawed, free or fused at the base, and form a ﬂag inserted adaxially at the base the ovary. Each petal has a single vein (Milby 1971). All of the stamens are inserted on the base of the petaloid petals above the ovary. The veins of the sepals and petals are separated by a wide gap but, as suggested by the position of the stamens, those of the petals and stamens are close together (Milby 1971). In the common condition of four stamens, the stamens are didynamous, each supplied by a single vascular trace. The ovary is ovoid, densely vestitured and surmounted by a stout, glabrous style with a sunken stigma. The style and the stamens are curved and project outward from the plane of the ﬂower. The ﬂowers are nectar-less and fragrant. Fragrance appears to be concentrated in the glands, indicating that small amounts of volatile oils are dissolved in secreted lipids. The anthers have four locules that dehisce into a common, slightly conical terminal chamber through which the pollen is shed in a cylindrical mass. The ovary is bicarpellate, but early in ontogeny, the posterior carpel aborts. The abortive carpel has a vestigial locule, however, and a suture line demarks the boundary between the two, even in the mature ovary (Milby 1971). The fertile carpel bears two ovules, only one of which

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ever forms a seed. The ovules are crassinucellate and bitegmic, with the micropyle formed by the inner integument alone (Verkerke 1985). Pollen Morphology. The pollen grains are shed as monads. Individual grains are isopolar, spheroidal, 26–38 µm in diameter, and striate with the striae perpendicular to the equatorial axis, tricolporate, triporate, or lalongate, or synorate (Fig. 72). The striae appear to be supported on stalks that penetrate a dense layer and then branch (Simpson and Skvarla 1981). The endexine is very thick. Karyology. Chromosome counts have been made for eight of the 18 species. All species have a haploid number of n = 6 (Turner 1958; Simpson 1989). Individual chromosomes are metacentric (Teppner 1984) and large, with those of K. secundiﬂora recorded to be 24.6 µm long (Lewis et al. 1962) and those of K. lappacea to be 10–14 µm long in metaphase (Teppner 1984). Pollination. All species of Krameria are pollinated by female solitary bees of the genus Centris (Apidae). These bees visit the ﬂowers to collect oils secreted by the glandular petals. During oil collection, a female bee orients with the main axis of the ﬂower, grasps the ﬂag petals with her mandibles, straddles the stigma and anthers, and rubs her foreand midlegs over the glandular patches, rupturing

Fig. 72. Krameriaceae. Krameria lappacea, pollen grain, SEM ×2,400. (Photograph B.B. Simpson)

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B.B. Simpson

the cuticle. The bee then backs off from the ﬂower, and transfers the oil to dense patches of setae on the tarsi of the hind legs for transport to the nest. When landing on a ﬂower, a female transfers pollen from a previously visited ﬂower to the stigma, which is exerted slightly from the anthers. While collecting oils, pollen is extruded from the terminal pores and deposited on the ventral side of the bee’s head and at the juncture of the ﬁrst pair of legs. Oils are used as a component of the larval food and may also be used in lining the walls of the individual nest cells. The bees do not actively collect Krameria pollen, but may carry combined loads of oils, Krameria pollen inadvertently collected, and pollen of other species to the nest. Sixteen species of Centris have been recorded visiting Krameria species, but there is no one-to-one speciﬁcity between Centris and Krameria, other than that resulting from limited geographical distribution of both partners. Likewise, Krameria-visiting Centris females can visit other genera for oil, nectar, and/or pollen. Non-oilcollecting species of bees have also been recorded visiting Krameria for pollen and for the collection of trichomes for nest materials (Simpson 1989). Fruit and Seed. Fruits are ovoid, 5–12 mm in diameter, and usually adorned with a mixture of spines and trichomes. The fruits are dry at maturity, the thin pericarp splitting irregularly and releasing the smooth, brown, slightly heart-shaped seed. The seed coat is formed by the inner and outer integuments, with a cuticular layer over the reduced inner integument (Verkerke 1985). The epidermal cells of the testa are rich in tannins. The mature seed consists of two large cotyledons and has no endosperm. There are four auricles at the junction of the cotyledons, which cover all but the tip of the radicle (Verkerke 1985). Many apparently mature fruits contain no seed. It is not clear whether this results from early abortion of a fertilized seed. Dispersal. Dispersal of Krameria fruits is by animals to which fruits adhere. Fruits of most species have spines with retrorse barbs that catch on feathers, fur, or clothing. If fruits are not pulled from the tree by a passing animal, they eventually fall to the ground. Over time, the pericarp splits and releases the seed, which can then be transported further by rain or wind. Reproductive Biology. The bisexual ﬂowers of Krameria appear to be receptive while they are shedding pollen. Self-pollination is prevented to

some extent by the slight herkogamy. The extent of self-compatibility is unknown. One shrubby species (K. grayi) appears self-incompatible, and one herbaceous species (K. lanceolata) has been found to be self-compatible (Simpson 1989). Phytochemistry. There has been extensive work on the chemistry of Krameria because of its early use as a medicinal plant. The medicinally important compounds are tannins, principally those of the catechin type. In addition, N-methyl tyrosine and apiitol have been identiﬁed in leaf extracts (Simpson 1991). The former has been reported from Phorodendron and from rotting meat but otherwise appears uncommon in plants. In addition, neolignans and nor-neolignans have been documented in several species (Achenbach et al. 1987a, b, 1989). These compounds have been found to be effective in ﬁltering ultraviolet radiation, prompting workers (Stahl and Ittel 1981) to suggest that the compounds might be effective in sun screen products. The ﬂoral oils of Krameria species have been shown to consist of free β-acetoxy fatty acids with carbon chain lengths of C16 to C20 (Simpson et al. 1977, 1978; Seigler et al. 1978). Afﬁnities. Prior to 1960, Krameria was generally considered to be a member of Polygalaceae (de Candolle 1824; Bentham and Hooker 1862) or Fabaceae, placed in its own tribe (Taubert 1892). This latter placement, which prevailed during the ﬁrst half of the 20th century, was based on the possession of trifoliolate leaves by one species of Krameria, and on the erroneous interpretation of the fruit as unicarpellate. However, cytological studies prompted Turner (1958) to re-segregate the genus into a monotypic family. Anatomical work by Milby (1971) strengthened this position. However, relationships of the family remained problematic. On the basis of serological studies (Busse-Jung 1979), Simpson (1989) suggested a relationship with Polygalaceae. By contrast, recent molecular data from rbcL sequences suggest that the sister group to Krameriaceae are Zyophyllaceae (Chase et al. 1993; Gadek et al. 1996; Savolainen, Fay et al. 2000), although this relationship does not appear to be close. Using three members of Zygophyllaceae (Guiaicum angustifolium, Kallostroemia parviﬂora, and Tribulus terrestris) as outgroups, Simpson et al. (2004) produced a phylogeny of the genus based on ITS DNA sequence data that

Krameriaceae

showed that there were two major clades in the genus, each with two subclades, all supported by one or more synapomorphies. One of the two major clades, characterized by rugose elaiophores, and fruits with spines that have one or two whorls of barbs at the tip, consists of two subclades. The ﬁrst subclade contains two South American species and is deﬁned by sepals borne perpendicular to the peduncle, tricolporate pollen, and spines of the fruit with two terminal whorls of barbs. The second subclade contains ﬁve North American species that share the characters of reﬂexed sepals, free, strap-shaped ﬂag petals, triporate pollen with equatorially elongate pores, and fruits with spines that have a single apical whorl of barbs. The second major clade, characterized by connivent sepals and triporate pollen with broad, oval-shaped pores, also has two subclades. One of these subclades has ﬁve species in South America that share the character of elaiophores with striate dorsal surfaces. The second subclade contains six North American species characterized by elaiophores that have secretory areas restricted to the distal portion, and petaloid petals that are fused at the base and have cordate blades. Distribution and Habitats. Krameria species occur from Kansas in the USA southward across the USA southwest into Mexico, Central, and South America as far south as northern Chile and Argentina. One species also occurs sporadically in the West Indies. Eleven species occur in Mexico and four in eastern Brazil. Species are rarely sympatric, however, and if two co-occur, they generally differ in habit or blooming time. All species, except K. cytisoides and K. sonorae, are found in open grassy or arid habitats. Krameria cytisoides is found primarily in the short oak or oak-pine shrublands in the Sierra Madre Oriental of Mexico, but it also ranges into desert scrubland at lower elevations. Krameria sonorae occurs in the Sinoloan thornscrub and tropical deciduous forest of Sonora, Mexico. Most species occur at elevations below 1,500 m, but K. lappacea occurs in the Peruvian and Bolivian Andes at elevations up to 3,600 m above sea level. The phylogenetic study of Simpson et al. (2004) showed that each of the major clades contains a North American and a South American subclade. While it was not possible to determine on which continent the genus arose, it is obvious that two intercontinental dispersal events are required to explain the current distribution.

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Fig. 73. Krameriaceae. Krameria grandiﬂora. A Habit. B Flowering branch. C Flower and ﬂower buds. D Elaiophore. E Fruit. (Drawn by M.C. Ogorzaly; Simpson 1989)

Economic Importance. From the end of the 18th century until the beginning of the 20th century, Krameria was used medicinally in Europe and European North America externally as an astringent, eye wash, and oral styptic. Taken internally as a tea or decoction, it was used to induce menstruation, to cure excessive menstrual bleeding, as an abortifacient, for kidney problems, and to treat various cancers. Krameria species were used by traditional peoples of both North and South America, primarily for their styptic properties (Ruiz 1797) and as a dye (Felger and Moser 1985). Ruiz (1797), on the basis of a few experiments conducted in Peru, extolled the virtues of K. lappacea in Europe, which resulted in its incorporation into most European pharmacopoeias. During the 1970s, Krameria was suspected of causing esophageal cancer, which precipitated a series of studies by the U.S. National Institutes of Health (Dunham et al. 1974, O’Gara et al. 1974). Both its purported beneﬁcial qualities and its presumed carcinogenic properties are now discounted. Its sole remaining uses are as a dye

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plant, and as an ingredient in dental and some cosmetic products (Simpson 1991). Only one genus: Krameria Loeﬂing

Figs. 72, 73

Krameria Loeﬂing, Iter hispanicum: 195 (1758).

Description as for family. Eighteen species, ranging across open habitats in the southwestern United States, Central America, tropical and subtropical South America, Hispaniola, and in the Greater and Lesser Antilles.

Selected Bibliography Achenbach, H., Gross, J, Dominguez, X.A., Cano, G., Star, J.V., Brussolo, L. d. C., Muñoz, F.S.G., López, L. 1987a. Lignans, neolignans, and nor-neolignans from Krameria cytisoides. Phytochemistry 26:1159–1166. Achenbach, H., Gross, J., Dominguez, X.A., Star, J.V., Salgado, F. 1987b. Ramosissin and other methoxylated nor-neolignans from Krameria ramosissima. Phytochemistry 26:2041–2043. Achenbach, H., Gross, J., Bauereiss, P., Dominguez, X.A., Vega, H.S., Star, J.V., Rombold, C. 1989. Nor-lignans and nor-neolignans from Krameria lanceolata. Phytochemistry 28:1959–1962. Bentham, G., Hooker, J.D. 1862. Polygaleae. Genera Plantarum 1, 1:134–140. London: Reeve. Busse-Jung, F. 1979. Phytoserologische Untersuchungen zur Frage der systematischen Stellung von Krameria triandra Ruiz et Pav. Dissertation, Christian-Albrechts University, Kiel, Germany. Candolle, A.P. de 1824. Krameria. Prodomus systematis naturalis regni vegetabilis 1:14. Paris: Treuttel and Würtz. Cannon, W.A. 1910. The root habits and parasitism of Krameria canescens Gray. Pages 5–24 in Macdougal, D.T., Cannon, W.A., The conditions of parasitism in plants. Publ. Carnegie Inst. Wash. 129:1–60. Chase, M.W. et al. 1993. See general references. Dunham, L.J., Sheets, R.H., Morton, J.F. 1974. Proliferation lesions in cheek pouch and esophagus of hamsters treated with plants from Curaçao. J. Natl Cancer Inst. 53:1259–1269. Felger, R.S., Moser, M.B. 1985. People of the desert and sea. Ethnobotany of the Seri Indians. Tucson: The University of Arizona Press. Gadek, P.A., Fernando, E.S., Quinn, C.J., Hoot, S.B., Terrazas T., Sheahan, M.C., Chase, M.W. 1996. Sapindales: molecular delimitation and infraordinal groups. Amer. J. Bot. 83:802–811. Kuijt, J. 1969. The biology of parasitic ﬂowering plants. Berkeley, CA: University of California Press.

Lewis, W.H., Stripling, H.L., Ross, R.G. 1962. Chromosome numbers for some angiosperms of the southern United States and Mexico. Rhodora 64:147–161. Metcalfe, C.R., Chalk, L. 1950. See general references. Milby, T.H. 1971. Floral anatomy of Krameria lanceolata. Amer. J. Bot. 58:569–576. Musselman, L.J. 1975. Parasitism and haustorial structure in Krameria lanceolata (Krameriaceae). A preliminary study. Phytomorphology 25:416–422. O’Gara, R.W., Lee, C.W., Morton, J.F., Kapadia, G.J., Dunham, L.J. 1974. Sarcoma induced in rats by extracts of plants and by fractionated extracts of Krameria ixina. J. Natl Cancer Inst. 52:445–448. Ruiz, H. 1797. Memoria sobre la ratánhia. Acad. Nac. Med. (Madrid) 1:349–366. Savolainen, V., Fay, M.F. et al. 2000. See general references. Seigler, D., Simpson, B.B., Martin C., Neff, J.L. 1978. Free 3acetoxy fatty acids in ﬂoral glands of Krameria species. Phytochemistry 17:995–996. Simpson, B.B. 1982. Krameria (Krameriaceae) ﬂowers: orientation and elaiophore morphology. Taxon 31:517– 528. Simpson, B.B. 1989. Krameriaceae. Flora Neotropica Monograph 49:1–109. New York Botanical Garden Press. Simpson, B.B. 1991. The past and present uses of rhatany (Krameria, Krameriaceae). Econ. Bot. 45:397–409. Simpson, B.B., Skvarla, J.J. 1981. Pollen morphology and ultrastructure of Krameria (Krameriaceae): utility in questions of intrafamilial and interfamilial classiﬁcation. Amer. J. Bot. 68 277–294. Simpson, B.B., Neff, J.L., Seigler, D. 1977. Krameria, free fatty acids and oil-collecting bees. Nature 267:150–151. Simpson, B.B., Seigler, D.S., Neff, J.L. 1978. Lipids from the ﬂoral glands of Krameria. Biochem. Syst. Ecol. 7:193– 194. Simpson, B.B., Weeks, A., Helfgott, D.M., Larkin, L.L. 2004. Species relationships in Krameria (Krameriaceae) based on ITS sequences and morphology: implications for character utility and biogeography. Syst. Bot. 29:97–108. Stahl, E., Ittel, I. 1981. Neue lipophile Benzofuranderivate aus Ratanhiawurzeln. Pl. Med. 42:144–154. Sterling, C.M. 1912. Krameria canescens Gray. Kansas Univ. Sci. Bull. 6:363–372. Taubert, P. 1892. Leguminosae. II. 6. Caesalpinioideae-Kramerieae. In: Engler, A., Prantl, K., Die natürlichen Pﬂanzenfamilien, III, 3. Leipzig: W. Engelmann, pp. 166–168. Teppner, H. 1984. Karyologie von Krameria triandra (Krameriaceae). Mitteilungsbl. Kurzfassungen Beiträge, Botaniker-Tagung, 1–14 September, Wien, #0623. Turner, B.L. 1958. Chromosome numbers in the genus Krameria: evidence for familial status. Rhodora 60:101–106. Verkerke, W. 1985. Ovule ontogeny and seed coat development in Krameria Loeﬂing (Krameriaceae). Beitr. Biol. Pﬂanzen 60:341–351.

Ledocarpaceae Ledocarpaceae Meyen, Reise 1:308 (1834). Vivianiaceae Klotzsch (1836). Rhynchothecaceae Endl. (1841).

M. Weigend

Shrubs, rarely subshrubs or perennial or annual herbs, 0.3–1.5(–4) m tall, stems erect or ascending, strongly branched, often differentiated into sometimes spinescent brachyblasts and dolichoblasts, stems tough, initially with white or brownish pith, terete, with greyish brown bark, underground stems occasionally present. Indumentum of simple, unicellular trichomes and uniseriate trichomes with a single-celled gland-tip, usually very dense on leaves, stems, calyx and ovary. Leaves evergreen or semi-deciduous, opposite or subopposite, rarely in whorls of three, shortly petiolate to sessile, petiole with clasping base, estipulate, lamina entire or pinnatiﬁd to pinnate to trifoliolate, margin entire or serrate; interpetiolar line often present. Inﬂorescences terminal cymoids or pleiothyrsoids, with monochasial to asymmetrically dichasial paraclades, often reduced to 2–3 ﬂowers, or a terminal ﬂower only, frondose-bracteose, individual ﬂowers of Balbisia subtended by prophylls. Flowers perfect, actinomorphic, pentamerous; sepals free or united in proximal half, imbricate with valvate tips, persistent in fruit; petals 5(4 or 0), free, with contort aestivation; stamens (4, 5, 4 + 4)5 + 5, usually obdiplostemonous and heterantherous, typically 5 long and 5 short; ﬁlaments sometimes with pair of basal appendages; gynoecium of 3–5 carpels; style single, very short, with 3–5 long stigmatic branches; ovary 3–5-lobed, with 1–20, pendulous, campylotropous ovules in each locule; placentation axile. Fruits septicidal or septifragous capsules with ﬁve 1–many-seeded locules; embryo straight or cochlear with spirally folded cotyledons; endosperm present, exotesta poorly developed or absent, occasionally mucilaginous. A family of four genera and about 18 species, mostly in Andean South America. Vegetative Morphology. Ledocarpaceae are exclusively or predominantly shrubby. The shoots are strongly branched, and the shrubs regenerate with long and relatively thick and large-leafed

dolichoblasts arising from the basal portion. In Rhynchotheca and some Viviania, some or most of the short lateral shoots turn into spines. In all shrubby species, the vegetative lateral axes have 1– several pairs of opposite, scale-like cataphylls, followed by progressively larger, regular foliage leaves. In Balbisia, most species have very short brachyblasts (<< 10 mm) with very densely crowded, often very short (<< 5 mm) leaves, which in some cases (B. microphylla) have the aspect of tiny hairy cones. Annual Viviania tenuicaulis lacks cataphylls, since it has no vegetative renewal shoots and its lateral axes develop in the distal portion of the shoot and immediately give rise to ﬂowers. Viviania elegans has a slightly ligniﬁed, more or less plagiotropic axis with ascending ﬂowering shoots. The herbaceous taxa in Viviania appear to be derived from a shrubby ancestor, which is supported by, for example, their highly derived inﬂorescence structure (see below). The root system of Balbisia (the only taxon in which I studied it) consists of a very extensive system of very ﬁnely branched roots. The shape and size of the leaves are rather conserved in Ledocarpaceae. Leaves are always small with the lamina (2–)5–15(–25) mm long, usually opposite but occasionally in whorls of three on some or most nodes, and with always very short petioles (< 5 mm). Leaf venation is weakly brochidodromous to craspedodromous, secondary veins directly entering the tips of leaf lobes or leaﬂets in Balbisia and Rhynchotheca but, in Viviania, the secondaries running towards the sinuses between the leaf lobes/serrations and branching there, so that one branch each of two neighbouring secondaries enters each leaf lobe. Leaf dissection is variable in all genera and even within individuals in Rhynchotheca (heterophyllous; the different leaf types have led to the description of three “varieties”; Knuth 1912). Some species of Viviania and Balbisia and ﬂowering branches of Rhynchotheca have undivided leaves, whereas other species of these genera and the vegetative branches of Rhyn-

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chotheca have pinnately lobed or – in the case of Balbisia – pinnate to trifoliolate leaves. The indumentum consists mainly of simple, unicellular and usually acroscopic trichomes with an acute apex and relatively few uniseriate glandular trichomes with a single-celled glandular head. Branched, but unicellular “arbuscular” trichomes are found on the ovaries and abaxial leaf surfaces of Viviania marifolia and the leaves of Balbisia peduncularis and B. microphylla, giving these organs a densely tomentose appearance. Vegetative Anatomy. Wood anatomy has been studied in detail in Viviania (Carlquist 1986), and is very similar in the other genera (pers. obs.). The shoots have a more or less extensive wood cylinder with a white or brown pith. The pith is parenchymatous with thin walls and extensive wall pitting in Rhynchotheca and Viviania, but sclerenchymatous with very thick, pitted walls in Balbisia. The wood of Balbisia and Viviania has distinct growth rings with wider vessels in early wood, but these are absent in Rhynchotheca (which is from permanently humid habitats). Axial parenchyma is absent in all three genera (contrary to Carlquist (1986), I was unable to conﬁrm its presence in Balbisia). Rays are clearly absent from all three genera. Vessels are densely spaced in Viviania and more or less loosely spaced in the other two genera, where they tend to aggregate into radial rows of 3–4 (Rhynchotheca) or 6–10 (Balbisia). Vessels have simple perforation plates; lateral vessel pits are circular to elliptical, pit apertures are interconnected by grooves, and spherical tyloses are present in some vessels. Imperforate tracheary elements are present in the form of ﬁbre tracheids, which have bordered (Viviania) or simple (Balbisia) pits and are occasionally septate. Sieve plastids are of the S-type (Behnke and Mabry 1977). The cortex is parenchymatous and lacks sclerenchymatous elements. The bark is well developed with regular, tanniniferous cork cells. Carlquist (1986) considers the wood anatomy of Viviania as strongly xeromorphic and indicative of secondary woodiness, i.e. indicating that the last common ancestor of Ledocarpaceae and Geraniaceae was herbaceous. Leaf anatomy has been studied for Balbisia (Xifreda 1973), and I here supplement original observations in Viviania marifolia and Rhynchotheca. The lamina is ﬂat, sometimes revolute in Balbisia, and variously lobed, serrate or entire. Both sides of the lamina are usually densely pubescent with simple or branched, unicellular trichomes, the abax-

ial side usually much more densely so, and often white from dense trichome cover, especially in Viviania. The epidermis is one-layered with distinctly papillose cells, especially on the abaxial side and above the leaf veins (e.g. W. calycina, W. aphanifolia, R. spinosa). Stomata are anomocytic. The lamina is bifacial, but the palisade parenchyma extends onto the abaxial surface along the lateral leaf margins in some species of Balbisia with very narrow leaf lobes (e.g. B. verticillata, B. stitchkinii). In both Rhynchotheca and Viviania, there is a more or less regular layer of cells closely resembling the palisade parenchyma above the abaxial epidermis, but with shorter cells. Otherwise, palisade parenchyma and spongiose parenchyma are approximately equal in thickness in all taxa, and the palisade parenchyma consists of 2–3 layers of relatively irregularly elongated cells. Crystal druses are frequent, especially in the spongiose parenchyma towards the abaxial surface in Viviania or in the palisade parenchyma towards the adaxial surface in Balbisia. The veins themselves have a distinct parenchymatous sheath in most species, and a sclerenchymatous sheath in B. gracilis. A pronounced collenchymatous tissue is found above the veins towards the abaxial surface in Rhynchotheca, towards the adaxial surface in Balbisia integrifolia, and towards both surfaces in B. calycina and B. aphanifolia. Inﬂorescences. The inﬂorescences have not been subject to any detailed study so far, only those of Viviania have been illustrated (Lefor 1975), and an integrated interpretation is here offered for all three genera. The inﬂorescences are terminal and 1-ﬂowered (often in Balbisia), (1)2–3-ﬂowered (Rhynchotheca) or many-ﬂowered (Viviania, most Balbisia). The many-ﬂowered inﬂorescences are readily recognized as thyrsoids, with typically two very unequal pairs of paraclades; the distal pair is less developed whereas the proximal pair is more strongly developed and often overtops the distal dichasium. The paraclades are dichasial or show varying degrees of reduction towards a monochasial terminal portion, and are usually also frondose. Well-developed inﬂorescences of Viviania marifolia have two opposite pairs of more or less equally developed, dichasial paraclades; all internodes and the pedicels are well developed, and all bracts are developed like regular foliage leaves (frondose inﬂorescence). In some inﬂorescences, the distal paraclade pair is lost but its frondose bracts are still present; the lower paraclade pair is more or less reduced but both paraclades still

Ledocarpaceae

develop at least one ﬂower each; a further reduction then leads to single terminal ﬂowers. In these reduced inﬂorescences, the internode between the two paraclade pairs is very short, and the four pherophylls of the paraclades (which are preserved irrespective of the development of their corresponding paraclades) are thus present as a whorl of four bracts, two of which (cf. the pherophylls of the distal paraclade pair) are distinctly smaller. In Viviania crenata both paraclade pairs are present, the lower paraclades being larger, but the internodes in and between the paraclades and pedicels are very short, leading to a superﬁcially capitate inﬂorescence. In Viviania tenuicaulis, V. elegans and V. albiﬂora, the internode between the distal and lower paraclade pairs is relatively short (V. tenuicaulis) or completely lost (the other two species), and both distal paraclades are reduced to their terminal ﬂower. The lower paraclades are well developed and overtop the distal dichasium, so there are three long-pedicellate ﬂowers and two long paraclades arising from a whorl of four bracts. The lower paraclades are often asymmetrically developed (with one paraclade more strongly developed or even showing proliﬁcation) and repeat the pattern of the main axis. In most Balbisia, the distal paraclades are reduced together with the pedicel of the terminal ﬂower, so that their pherophylls are situated directly below the calyx. These bracts have been interpreted as an epicalyx, and have given rise to speculations. The lower paraclades (= solitary terminal ﬂowers) are also lost in some specimens of B. gracilis and B. aphanifolia; other individuals of these two species and of B. calycina have the lower paraclades present but one-ﬂowered, with their ﬂowers also subtended by a pair of prophylls at the base of the calyx. In some specimens of B. gracilis, the lower paraclades are either well developed and dichasial (thyrsoidal, the terminal dichasia reduced to monads) or, rarely, additional third and fourth pairs of paraclades are present, which are all reduced to 1–2 ﬂowers, showing a trend towards racemisation. Rhynchotheca essentially shows the pattern of a reduced Viviania marifolia inﬂorescence with three ﬂowers: the distal paraclades are absent, the lower paraclades usually reduced to a single ﬂower, all ﬂowers have long pedicels, and the pherophylls of the paraclades are all present in a whorl of 4. The only striking difference is the presence of tiny, scale-like cataphylls at the base of the pedicels of the lateral ﬂowers, testifying to their derivation from paraclades.

215

The inﬂorescences of Ledocarpaceae show a complex pattern of condensation (reduction of internodes) and basitonic growth, often leading to complex sympodial systems with reduced distal dichasia (often displaced into a more or less lateral position) in the taxa with many-ﬂowered inﬂorescences. Floral Structure. The perfect, pentamerous, radially symmetrical ﬂowers are superﬁcially very different in size and colouration but show few derivations in structure. Flowers are usually open (saucer-shaped), but campanulate in Viviania. Typically, there are ﬁve sepals, which are occasionally united for about half their length in Viviania and free to base in the other genera. The sepals are ovate-acuminate with a thin, awn-like tip or a distinct, dorsally displaced awn (Rhynchotheca). They are densely pubescent, slightly chartaceous, and pale green to beige. The basally united calyx of Viviania sometimes has a toroidal basal appendage forming a ring around the apex of the pedicel (Lefor 1975). Petals are obovate or triangular with a truncate, rounded or acuminate apex forming a usually shallow bowl much larger than the calyx but they can be erect with a spreading or reﬂexed apex (Viviania), and are thinly membranaceous, shiny, yellow, red, pink or white. Some Balbisia have relatively small petals (equalling or shorter than the calyx, B. gracilis); Rhynchotheca is apetalous. Nearly all taxa have an obdiplostemonous androecium, some Viviania have 5 or 5 + 5 + 5 stamens; the inner stamens are generally shorter, and reductions to (4)5 stamens are known in some species of Viviania. Stamens are usually included in the corolla (Viviania) or very short (< than petals), only Rhynchotheca having long-exserted, pendulous ﬁlaments. Anthers are small (c. 1 mm long) in Viviania and some Balbisia, larger (c. 3–4 mm long) in Rhynchotheca, and very large (6–8 mm long) in other Balbisia. The ﬁlaments are often basally dilated and united into a ring. The ﬁlaments of Viviania often have well-developed, paired basal ﬁlament appendages which apparently function as nectaries (staining darkly red with safranin), and are apparently homologous to similar structures found in Geranium (“Basaldrüsen” = basal glands; Eichler 1878; Knuth 1912). No evidence for nectaries has so far been reported for the other three genera. The ovaries are spherical, shallowly (2)3–5lobed and very densely covered with unicellular, usually simple, sometimes branched, white tri-

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chomes. Each locule contains usually 1–20, rarely more ovules. The style is generally very short and has 3–5 erect, oblong stigmatic lobes. The papillose stigmatic surface is commonly restricted to the adaxial surface of the stigmatic lobes but sometimes the lobes are revolute, so that the papillose surface extends also to the functionally abaxial side. The papillose stigmatic surface is usually dry, but wet and covered with copious amount of mucilage in Rhynchotheca. Embryology. Embryology (and seed anatomy) of Ledocarpaceae has been studied in much detail by Boesewinkel (1997). The ovule is anatropous (Rhynchotheca) or twisted and campylotropous (Viviania), or hemianatropous to campylotropous (Balbisia), bitegmic, and crassinucellate. The integuments are 2–3-layered, the micropyle being formed by the inner integument. The ovules are tannin-rich, especially the outer cell layer of the inner integument, sometimes also the chalaza and/or the raphal bundle. All genera have obturator hairs at the funicle, and these are directed towards the micropyle of the neighbouring ovule in Viviania. In some Viviania, the embryo has a long suspensor pointing towards the micropyle. Especially in Balbisia and Rhynchotheca, the integuments are conspicuously thickened near the micropyle. Pollen Morphology. (Information mainly from Bortenschlager 1967.) Pollen grains are spheroidal and inaperturate (Balbisia) or pantoporate with 21–60 pores and a pore diameter of 2–4.5 µm (Viviania, Rhynchotheca); the pores are with or without annulus and operculum. The exine is semitectate to rarely pertecate (some Viviania) and typically reticulate, often with very regular hexagonal reticulations (Viviania), often additionally ﬁnely echinate (B. gracilis, most Viviania). Infratectal bacula are 0.5–2 µm high, the tectum has a thickness of 0.5–0.8(–1.2) µm and the nexine is 0.4–0.6(–1.2) µm thick. The spheroidal, pantoporate or inaperturate pollen of Ledocarpaceae is clearly discordant in Geraniales, and should be considered as synapomorphic for the family, since the afﬁnity of the family to other groups (with mostly tricolporate pollen) can not be doubted. Pollination. The plants are probably proterandrous, but detailed studies are not available. The showy ﬂowers of most Balbisia and of Viviania are certainly entomophilous, especially the nectar-

iferous ﬂowers of Viviania. The ﬂowers of Rhynchotheca show a whole range of features typical of anemophily: the plants are found in large, often more or less monospeciﬁc stands which ﬂower simultaneously in a very short period of time, the corolla is lost, the anthers are long-exserted and pendulous, the pollen grains are large and without distinct sculpturing, the stigmas are also larger than in other taxa, more strongly exposed (beaked ovary), with the stigmatic surface wet (dry in other taxa) and the stigmatic surface extending onto the outside of the lobes (revolute). This combination of characters renders anemophily extremely likely for this taxon. Fruit and Seed. All Ledocarpaceae have septicidal or septifragous capsules with caducous stigmas but a persistent calyx. Frequently, there are two seeds per locule (Rhynchotheca, most Viviania) but, occasionally, there are numerous seeds (most Balbisia) or only a single one (B. gracilis). The seeds are released through apical apertures which correspond to ventral sutures. The fruits usually remain on the plants and the seeds released from there, but fruits are dispersed whole in Viviania tenuicaulis. They usually lack the characteristic beak of Geraniaceae fruits, with the exception of Rhynchotheca which has a distinct sterile ovary apex, closely resembling Geraniaceae fruits in shape but not in functional morphology. Seed morphology and anatomy have been studied by Boesewinkel (1997). The seeds are usually oblong to obovoidal, rarely subspherical or compressed (only Viviania). The seeds have a 4–5-layered, tannin-rich seed coat, occasionally with a thick-walled exotegmen, and a distinct raphe is present, which is also tanniniferous in Viviania. Some species of Viviania have a tuft of hair in the raphal region, apparently derived from obturator hairs. In Balbisia meyeniana, the exotesta consists of mucilage cells. The endosperm is moderately well developed, has thick-walled cells with extensive wall layering and pitting. The embryo is green, and straight in Rhynchotheca, heart-shaped to cochlear in Viviania, and strongly spirally twisted in Balbisia. Seed Dispersal and Vegetative Reproduction. No studies have been published on seed dispersal in Ledocarpaceae, and their seeds appear to be essentially barochorous; the smaller seeds of Viviania and Balbisia may occasionally be dispersed by wind. Conditions for wind dispersal

Ledocarpaceae

are particularly good for the seeds of the Andean slope species and the Patagonian species of Balbisia, which are exposed to frequent and steady high winds, and for the seeds of Viviania with their hairy surface projections (Boesewinkel 1997). The mucilaginous seeds of Balbisia may be epizoochorous during wet periods. Anemochory can be safely ruled out for Rhynchotheca, since its habitats have little air movement and the dense vegetation should further prohibit transport. A functional investigation of the dehiscence of its beaked fruit and subsequent seed dispersal would be clearly of interest. Vegetative propagation is poorly developed in the family, and only the creeping stems of some Viviania (especially V. albiﬂora and V. elegans) facilitate the formation of small clonal stands. Phytochemistry. This topic has received very little attention. Ellagitanins have been reported from leaves of Balbisia (Bate-Smith 1962), and are apparently widespread in the stems (especially in the bark), parts of the ﬂower and the seed coat. They may be responsible for the medicinal value attributed to some taxa. Volatile oils appear to be absent or, if at all, present in only minor amounts, since the plants are not notably odoriferous. Anthocyanins have been reported as petal pigments (Behnke and Mabry 1977). Subdivision. Only two genera of Ledocarpaceae have consistently been considered as closely related, Wendtia and Balbisia, and these were usually placed in one tribe (Wendtieae, in Geraniaceae, e.g. Knuth 1912, together with Rhynchotheca). Hunziker and Ariza Espinar (1973) reduced the genus Wendtia under Balbisia and argued that Ledocarpaceae should be re-established as a monogeneric family, including only the expanded Balbisia and without Rhynchotheca and Viviania. The latter two genera have been variously treated as either distinct tribes (Knuth 1912) or families (e.g. Takhtajan 1997). Moreover, Viviania has either been treated in a wider sense (Knuth 1912) or segregated into a total of four genera (three monotypic: Cissabryon, Caesarea and Araeoandra; Lefor 1975). The basic structure of the inﬂorescences, ovule and seed morphology, wood and leaf anatomy, habit, and ﬂoral morphology are largely congruent within this family. The various sources of morphological and anatomical evidence thus justify the present circumscription of Ledocarpaceae, which is conﬁrmed by molec-

217

ular data (Price and Palmer 1993), rendering the recognition of monotypic families superﬂuous. The separation of Wendtia and Balbisia on morphological grounds is difﬁcult (Balbisia integrifolia and Balbisia (Wendtia) calycina are strikingly similar), and they share clear apomorphies in pollen (intectate?), seed (Boesewinkel 1997) and inﬂorescence (sessile pairs of prophylls at the base of the calyx) morphology, so that the fusion of the two genera, as proposed by Hunziker and Ariza Espinar (1973), is here accepted. The segregate genera of Lefor (1975) may or may not be natural entities, but Viviania s.l. including the segregates appears to be a natural unit, so that the recognition of monotypic segregates seems unwarranted. Only three genera are therefore here recognized, Balbisia (incl. Wendtia), Viviania (incl. Cissarobryon, Caesarea and Araeoandra) and monotypic Rhynchotheca. Each of the genera is very well characterized, and it is difﬁcult to evaluate which could be more closely allied, especially since the anemophilous Rhynchotheca shows many ﬂoral autapomorphies which obscure its afﬁnities. Afﬁnities. The genera have been mostly treated as members of Geraniaceae (Knuth 1912), although their aberrant pollen morphology and typically campylotropous ovules have also led to suggestions that they belong near the “Centrospermae” (= Caryophyllales, e.g. Bortenschlager 1967) or Pittosporales (Hutchinson 1969). Recent molecular studies clearly indicate that the family belongs near Geraniaceae, but it is currently placed on a polytomy together with Geraniaceae and a wide range of other families (Price and Palmer 1993; Sosa and Chase 2003). The data on ovule and seed morphology (campylotropous ovules, tanniniferous seed coat, green embryos; Boesewinkel 1997), wood anatomy (e.g. rayless wood; Carlquist 1986; pers. obs.), and the ﬂoral morphology as here compiled (acuminate to awned sepals, contorted, membranaceous petals, obdiplostemonous androecium with basally widened ﬁlaments and occasionally basal nectariferous appendages, sessile, superior, densely pubescent ovary with subsessile stigmatic lobes or style branches) agree well with a close and possibly exclusive relationship between Geraniaceae and Ledocarpaceae. Most Ledocarpaceae show a trend towards sterile upper ovules in the ovary, and in some (Rhynchotheca, some Balbisia) there either are only 1–2 ovules at the base of each locule or the upper ovules abort, leading to a fruit which closely resembles that

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of Geraniaceae, apart from the opening mode. Their basitonic thyrsoids are very similar to those of herbaceous Geranium, and the cataphylls on lateral axes are probably homologous to the bud scales and stipules (better, “Scheidenlappen”) of Geraniaceae. Apart from growth habit, the families differ only in pollen morphology and fruit dehiscence. Pollen morphology seems to be the only clear apomorphy of Ledocarpaceae, whereas they have retained the plesiomorphic condition in fruit morphology. Hypseocharis, which is sister to the rest of Geraniaceae, also has capsular fruits with abortive upper ovules, showing that schizocarps arose in Geraniaceae from a condition identical to that found in Ledocarpaceae.

Fig. 74. Ledocarpaceae. A–C Balbisia peduncularis. A Flowering branch. B Flower, male phase. C Mature fruit. D Balbisia gracilis, ﬂower. (Orig. Weigend)

Distribution and Habitats. All three genera are restricted to South America, and all but one species are found in scrub communities of the Andes and their foothills. In the southern part of their range, they are restricted to relatively low elevations (< 2,000 m) whereas they reach high elevations of over 3,000 m in the northern (tropical) part. Viviania is found roughly between 28◦ and 38◦ S, and four of the ﬁve species are from the western slopes and foothills of the Andes in Chile (V. marifolia also – possibly introduced – in adjacent Argentina), the ﬁfth species being endemic to southeast Brazil and Uruguay (Lefor 1975). Balbisia ranges from the Department of Lima (western slope of the Andes in Peru, 12◦ S; Jørgensen and Yanez León 1999) to the Province of Chubut (Argentinean Patagonia, 44◦ S; Correa 1988). It occurs in dry habitats and, therefore, is to be found on the western slopes of the Andes throughout its range but restricted to the region south of central Bolivia on the eastern slopes. Isolated populations of one species (B. peduncularis) are reported from the dry inner Andean valleys of the departments of Apurímac and Ayacucho (Peru), where many western-slope taxa have isolated populations (e.g. Grindelia–Asteraceae; Malesherbia– Malesherbiaceae). Balbisia is found from sea level to over 3,000 m but, in the northern part of its range (Peru), is most speciose and most abundant at elevations between 1,500 and 3,000 m. It is often a dominant member of the vegetation, e.g. on the western Andean slopes of Peru near Arequipa. Both Viviania and Balbisia are found in at least seasonally very dry habitats whereas Rhynchotheca, the northernmost representative of the family, is from habitats without a pronounced dry season. The latter ranges from the Province of Cotopaxi (Ecuador,

Ledocarpaceae

near the Equator; Jørgensen and Yanez León 1999) to the Department of Cuzco (Peru, 12◦ S; Brako and Zarucchi 1993), and is found mostly in Andean scrub communities which have replaced former cloud forests. It can be extremely abundant, making up much of the shrubbery and hedges present

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in a given area (e.g. Peru, Department of Huánuco, around the city of Huánuco). Economic Importance. Ledocarpaceae are rarely cultivated, and to date no important uses have been documented. Infusions of dried shoots of V. marifolia, B. aphanifolia, B. calycina and B. gracilis are consumed in Chile and Argentina, pure or mixed with other herbs, under various names such as té de burro, té andino, té del país, té morado or oreganillo (San Martín 1983; Boelcke 1989; Ariza Espinar 1995a, b). The infusion is considered as medicinal and is used against renal and hepatic disorders and stomach complaints. Both the large-ﬂowered Balbisia (B. peduncularis, B. weberbaueri) and Viviania (Viviania marifolia) have a spectacular and long-lasting ﬂoral display and, thus, considerable potential as ornamental plants but are essentially not cultivated, even in botanical collections. Conservation. All species of this family tend to have relatively wide ranges and are often at least subdominant or even dominant members of their respective plant communities and, thus, in no danger of extinction. Viviania tenuicaulis may represent an exception, since it is very narrowly endemic to the region of Coquimbo in Chile and may be potentially endangered. Key to the Genera 1. Each ﬂower sessile in a pair of trifoliolate bracts; corolla bowl-shaped 1. Balbisia – Flowers with long pedicel; bracts situated at base of pedicel, sometimes reduced to scale-like cataphylls; bracts always entire; corolla campanulate, or absent 2 2. Flowers apetalous; sepals free; fruit beaked 2. Rhynchotheca – Flowers with large petals, these longer than calyx; calyx united at least at base or for half its length; fruit not beaked 3. Viviania

Genera of Ledocarpaceae 1. Balbisia Cav.

Fig. 75. Ledocarpaceae. A–D Rhynchotheca speciosa. A Vegetative branch. B Flowering branch, female phase. C Flower, male phase. D Immature fruit. E, F Viviania marifolia. E Branch of inﬂorescence. F Flower, perianth partly removed. (Orig. Weigend)

Fig. 74

Balbisia Cav., Anales Ci. Nat. 7: 61 (1804); Knuth in Pﬂanzenreich IV, 129:550–558 (1912); Ricardi, M., Bol. Soc. Argent. Bot. 7:20–28 (1957); Ariza Espinar, Flora Fanerog. Argent. 18:1–5 (1995). Ledocarpon Desf. (1818). Wendtia Meyen (1834).

Shrubs 0.3–2 m tall. Leaves opposite, entire, pinnatiﬁd to trifoliolate. Inﬂorenscences 1- or many-

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M. Weigend

ﬂowered thyrsoids, each ﬂower subtended by a pair of trifoliolate bracts. Sepals free to base, 4–25 mm long; petals obovate to subcircular, base cuneate, apex rounded, 5–40 mm long, yellow, pink or red; stamens 5 + 5, ﬁlaments connate at base, usually short, often shorter than anthers; anthers oblong with cordate base; nectaries 0; ovary 3–5-lobed, 3– 5-locular, with 1–15 ovules per locule. Fruit a septicidal capsule; seeds oblong with distinct raphe. Eleven species, in Peru, Bolivia and Argentina. Hunziker and Ariza Espinar (1973) propose three sections, one of which corresponds to the former genus Wendtia, based on leaf morphology, petal size and colour. 2. Rhynchotheca Ruiz & Pav.

Fig. 75

Rhynchotheca Ruiz & Pav., Fl. Peruv. Chil. Prodr.: 82 (1794).

Shrubs 0.5–2 m tall. Leaves opposite, pinnatiﬁd on dolichoblasts and entire on brachyblasts. Inﬂorenscences typically 3-ﬂowered, subtended by four bracts and with small, scale-like cataphylls in some pedicels. Sepals free to base, 4–10 mm long; petals 0; stamens 5 + 5; ﬁlaments free at base, very long; anthers exserted and pendulous, oblong with cordate base and emarginate apex; nectaries 0; ovary 5-lobed, 5-locular, with 2 ovules per locule, with distinct sterile beak especially in fruit. Fruit a septicidal capsule; seeds oblong with distinct raphe. One species, R. spinosa Ruiz & Pav., in Peru and Ecuador. 3. Viviania Cav. Viviania Cav., Anales Ci. Nat. 7:211 (1804); Lefor, Univ. Connecticut Occ. Pap., Biol. Sci. Ser. II, 15:225–255 (1975). Caesarea Camb. (1829). Cissabryon Kunze ex Poepp., Fragm. Syn. Pl. Chile: 29 (1833). Araeoandra Lefor (1975).

Shrubs 0.3–4 m tall, or perennial or rarely annual herbs. Leaves opposite, entire, serrate or lobed. Inﬂorescences typically basitonic thyrsoids with 3-ﬂowered distal dichasium, or cymoid with only (1–)3 ﬂowers. Sepals united for c. half their length, 3–10 mm long; petals obovate from cuneate base and occasionally with basal appendages, apex rounded to obtuse, 5–15 mm long, white, yellow or pink; stamens in 1 or 2 whorls of 5; ﬁlaments united at base, occasionally with basal appendages, long; anthers included or reaching the mouth of the campanulate ﬂower; anthers shortly oblong with cordate base and emarginate apex; ovary (2)3-lobed, (2)3-locular, with 2 ovules per locule,

without distinct sterile beak in fruit. Fruit a septicidal capsule; seeds compressed to spherical, with distinct, sometimes pubescent raphe. Five species in Chile, and 1 species in Argentina, Uruguay and southern Brazil.

Selected Bibliography Ariza Espinar, L. 1995a. Flora Fanerogámica Argentina fasc. 8, 129b. Vivianiaceae. Córdoba, Argentina: CONICET. Ariza Espinar, L. 1995b. Flora Fanerogámica Argentina fasc. 18, 129a. Ledocarpaceae. Córdoba, Argentina: CONICET. Bate-Smith, E.C. 1962. The phenolic constituents of plants and their taxonomic signiﬁcance, I. Dicotyledons. J. Linn. Soc., Bot. 58:95–173. Behnke, H.-D., Mabry, T.J. 1977. S-type sieve plastids and anthocyanins in Vivianiaceae: evidence against its inclusion into Centrospermae. Pl. Syst. Evol. 126:371– 375. Boelcke, O. 1989. Plantas vasculares de la Argentina. Buenos Aires: Hemisferio Sur. Boesewinkel, F.D. 1997. Seed structure and phylogenetic relationships of the Geraniales. Bot. Jahrb. Syst. 119:277– 291. Bortenschlager, S. 1967. Vorläuﬁge Mitteilungen zur Pollenmorphologie in der Familie der Geraniaceen und ihre systematische Bedeutung. Grana Palynol. 7:400–468. Brako, L., Zarucchi, J.L. 1993. Catalogue of the ﬂowering plants and gymnosperms of Peru. Monogr. Syst. Bot. Missouri Bot. Gard. 45. Carlquist, S. 1986. Wood anatomy and familial status of Viviania. Aliso 11:159–65. Correa, N.M. 1988. Flora Patagonica, 5. Buenos Aires: INTA. Eichler, A.W. 1878. Blüthendiagrame konstruiert und erläutert, 2. Leipzig: W. Engelmann. Hunziker, A.T., Ariza Espinar, L. 1973. Aporte a la rehabilitación de Ledocarpaceae, familia monotipica. Kurtziana 7:233–240. Hutchinson, J. 1969. The genera of ﬂowering plants, 2. Oxford: Clarendon Press. Jørgensen, P.M., Yanez León, S. 1999. Checklist of the vascular plants of Ecuador. Monogr. Syst. Bot. Missouri Bot. Gard. 75. Knuth, R. 1912. Geraniaceae. In: Pﬂanzenreich IV, 129. Leipzig: W. Engelmann. Lefor, M.W.M. 1975. A taxonomic revision of the Vivianiaceae. Univ. Connecticut Occ. Pap., Biol. Sci. Ser. II, 15:225–255. Price, R.A., Palmer, J.D. 1993. Phylogenetic relationships of the Geraniaceae and Geraniales from rbcL sequence comparisons. Ann. Missouri Bot. Gard. 80:661–671. San Martín, J. 1983. Medicinal plants in central Chile. Econ. Bot. 37:216–227. Sosa, V., Chase, M.W. 2003. Phylogenetics of Crossosomataceae based on rbcL sequence data. Syst. Bot. 28:96– 105. Takhtajan, A. 1997. See general references. Weigend, M. 2005. Notes on the ﬂoral morphology in Vivianiaceae. Pl. Syst. Evol. 253:125–131. Xifreda, C.C. 1973. Anatomia foliar de Wendtia y Balbisia (Geraniaceae). Kurtziana 7:213–232.

Leeaceae Leeaceae Dumortier, Anal. Fam. Pl.: 27 (1829), nom. cons.

J. Wen

Trees, shrubs, scramblers, or large perennial herbs; stems unarmed or with rows of prickles; tendrils 0. Leaves 1–4-pinnate to trifoliate or simple; stipules sheathing the petiole margins with conspicuous, persistent or caducous stipular wings; leaﬂets glabrous to pubescent with simple hairs, crenate to serrate to dentate at margin, teeth with small glandular apex, lower surface usually with specialized multicellular, stellate or globular caducous “pearl” glands. Inﬂorescence paniculate, often corymbiform, terminal or axillary, erect or pendulous. Flowers hermaphroditic, 5(4)-merous; calyx campanulate with triangular lobes and glandular tips; petals valvate, apically often cucullate, reﬂexed at anthesis, basally connate, adnate to staminal tissue and the lower portion of ﬂoral disc; ﬂoral disc tubular, intrastaminal; stamens 5 or 4, antepetalous, alternating with the lobes of ﬂoral disc, anthers tetrasporangiate and 2-locular, introrse and sometimes appearing extrorse; ovary superior but sometimes partly sunken in the disc, 2–3(–5)-carpellate but with a secondary septum in each carpel and 4–6(–10)-locular; ovule 1 per locule, anatropous, bitegmic and crassinucellate; style elongate; stigma discoid and capitate. Fruit a berry, rather dry, subglobose, purple, black or orange; seeds endotestal; endosperm ruminate with roughly 5 ingrowths; embryo linear. 2n = 24 or 48 (rarely 20, 22, or 28). A monogeneric family with 34 species in tropical and subtropical Asia, extending into the Himalayan region and Australia, and with two species in Africa and Madagascar. Vegetative Morphology. Leeaceae are usually shrubs, herbs or small trees, sometimes with armed stems (L. aculeata and L. angulata). Unlike many Vitaceae, Leeaceae do not have tendrils. Stem growth is monopodial. Leaf form varies greatly, from simple to once to thrice pinnately compound (Fig. 77A–C). In most species, leaf morphology is highly variable and thus taxonomically unreliable

for species distinction (Ridsdale 1974). In the past, leaf morphology was considered to be taxonomically important, which led to a proliferation of species being recognized. Gerrath and Lacroix (1997) documented that seedlings of Leea guineensis exhibit a variable sequence of heteroblastic leaves, with simple leaves at the ﬁrst four nodes, followed by compound trifoliate, pinnate and ﬁnally highly complex multipinnate leaves. In this species, at successive nodes the leaves become progressively more complex. There are no deeply lobed transitional forms as intermediates. Beyond the developmental variation associated with age and position, Ridsdale (1974) argued that leaves in Leea varied strongly according to habitat and ecological conditions. In some species, the leaf form is constant, such as in Leea aculeata, which has only once-pinnate leaves. The petiole or base of the petiole expands to bear a stipular structure (Fig. 77D, E). Stipules are well developed in the family, enclosing the next youngest leaf and the rest of the shoot apex (Lacroix et al. 1990). They are caducous or persistent, and show a wide range of variation in shape from narrowly sheathing to short and obovate (Ridsdale 1974). Forest species mostly have elongated sheathing stipules, and those of secondary vegetation predominantly have short and obovate stipules. Stipules can also enclose the terminal inﬂorescence at its early developmental stage (Lacroix et al. 1990). Vegetative Anatomy. There are usually globular or stellate “pearl” glands on the lower leaf surface. Stomata are cyclocytic, actinocytic, or rarely anomocytic (Ren et al. 2003). The mesophyll contains mucilage cells sometimes with raphides and usually with calcium oxalate crystals. Sieve-tube plastids are P-type I(b) (Behnke 1981). The wood of Leea has numerous broad rays separating the narrow ﬁbro-vascular bundles and vasicentric parenchyma. The vessels are small in

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comparison with those in members of Vitaceae (Metcalfe and Chalk 1950; Wheeler and LaPasha 1994; Poole and Wilkinson 2000), and are intercalated in the radial rows of woody elements. Between the bundles are linear uniseriate rays with small cells (Adkinson 1913). Most species have raphides present in the wood (Watari 1951; Prakash and Dayal 1963). Inﬂorescence and Floral Morphology. The inﬂorescences are usually terminal, and sometimes both terminal and axillary (Gerrath et al. 1990). They are basically strongly corymbiformmodiﬁed panicles in which repeatedly the basal internodia of the two lateral ﬂorescences elongate as strongly as the next internodium of the main axis. Sometimes the inﬂorescence is large and ﬂattopped, as in L. indica and L. guineensis. Reduction of the peduncles and/or lateral branches gives rise to condensed inﬂorescences, as in L. congesta. The anthers are connivent laterally; at anthesis, they continue to reﬂex, separate from each other, and abscise at the base. Thus, depending on the developmental stage of ﬂowering, the anther may appear introrse or extrorse. Many workers (e.g., Ridsdale 1974, 1976; Cronquist 1981; Li 1998) have stated that Leeaceae do not have a ﬂoral disc, and Ridsdale (1974) was of the opinion that there is a “staminodial tube” that he considered to be a whorl of modiﬁed stamens inserted in the corolla. Gerrath et al. (1990), however, demonstrated the presence of a ﬂoral disc, and found it inappropriate to designate the tube structure inside the stamen whorl as staminodial tube. They found that the ﬂoral disc is initiated from the base of the ovary in the regions between the stamens, and that its growth is also greatest between the stamens. The distinctive ﬂoral tube of Leeaceae is the result of intercalary growth of a meristem located below the points of insertion of the petals, stamens and the ﬂoral disc, uniting the lower portions of these organs (Gerrath et al. 1990).

Karyology. The vast majority of chromosome counts in Leeaceae corresponds to 2n = 24 (Ridsdale 1974; Sandhu and Mann 1989; Karkamkar and Patil 1992); some species are tetraploid with 2n = 48. Karkamkar and Patil (1992) reported for L. macrophylla 2n = 24, and for L. robusta 2n = 48, whereas Ridsdale (1974) treated L. robusta as a synonym of L. macrophylla. Leea indica (including L. sambucina) was reported to have n = 24 (Gill et al. 1990; Karkamkar and Patil 1992), n = 20 (Nair and Namnisan 1957), or n = 22 (Vatsala 1960). Secondary constrictions, which are present in L. aculeata, may account for the aneuploid-like differences in L. indica (Ridsdale 1974). Reproductive Biology. The hermaphroditic ﬂowers of Leea are markedly protandrous (Gerrath et al. 1990). Their pollination biology is unknown. The occurrence of “water calyces” in Leea amabilis is noteworthy: this Bornean plant has ﬂower buds that are tightly closed by the valvately appressed calyx lobes, which are interdigitated with epidermal papillae. A liquid ﬁlls the space between the calyx and corolla; secretion of the liquid seems to take place from trichomes on the inner surface of the calyx lobes (Suessenguth 1953). Fruit and Seed. Fruits in Leeaceae are subglobose, ﬂeshy, 4–6-seeded berries. The seeds have a ruminated endosperm, which usually has roughly ﬁve ingrowths: one along the median plane, two from the raphe, and one at each lateral face (Fig. 76). The ingrowths may become more pronounced due to further branching as a result of localized meristematic activity. As in Vitaceae, the endosperm is

Embryology. Pollen grains are trinucleate or rarely binucleate when shed. Embryo-sac development is of the Polygonum type. Endosperm formation is Nuclear, and embryogeny is Asterad. Pollen Morphology. Pollen grains are tricolporate, angulaperturate, suboblate to subprolate, and have a mainly triangular amb; the tectum is reticulate and the colpi are generally 2/3 or 3/4 of the grain radius (Tarnavschi and Petria 1968).

Fig. 76. Leeaceae. Median transverse section of seeds, showing variation of endosperm rumination. A Leea acuminatissima. B L. coryphantha. C L. magnifolia. D L. compactiﬂora. E L. indica. (Ridsdale 1974)

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oily and contains druses, and the seed coat has a thick ligniﬁed endotesta 2–4 cells wide, and an inconspicuous tegmen in which the 1–2 outer layers consist of ligniﬁed tracheids (Corner 1976). Unlike Vitaceae, Leeaceae usually do not have raphides in the seed coat. Seed Dispersal. Whilst seed dispersal is probably mostly by bird, Ridley (1930) reported that Leea rubra and L. sambucina (= L. indica) are dispersed by the sea. Distribution and Habitats. Leea is primarily distributed in Malesia, Indochina, South and Southwest China, and India, extending to Micronesia, Melanesia, Australia, and tropical Africa. Most species grow in lowland evergreen forests, montane forests up to an altitude of about 2,500 m, with some species such as L. alata preferring dry woodlands. Several species of Leea, including L. indica, L. guineensis, L. aequata, L. angulata, and L. rubra, have a wide distributional range and are morphologically highly variable, but most species of the genus are of restricted distribution. Paleobotany. Prakash and Dayal (1963) reported a fossil wood, Leeoxylon multiseriatum, from the early Tertiary (probably the Eocene) of India. Another fossil wood of Leea was recorded from the Miocene of Japan (L. eojaponica, Watari 1951). Kramer (1974) reported another species of Leeoxylon, L. altiradiatum, from the Neogene of Java. Economic Importance. Leea guineensis and L. indica have been cultivated in tropical regions as ornamentals, and the former is often marketed under the name of L. coccinea. Leea guineensis and L. rubra were tested for their morphological and physiological responses to various light conditions, and were suggested to be potentially suitable

Fig. 77. Leeaceae. A–C Leea simplicifolia. A Unifoliolate leaf. B Multipinnate leaf. C Trifoliolate and pinnate leaves. D Leea magnifolia. Inﬂorescence and leaf petiole, showing sheathing and elongate stipule. E Leea guineensis. Obovate stipule. F–N Leea indica. F Flower. G Composite tube of fused tissues of lower portion of petals, stamens and ﬂoral disc, also showing an anther. H Outside view of composite tube, showing primarily the ﬂoral disc. I Sepals, ovary, style, and stigma. J Longitudinal section of the ﬂower shortly before anthesis, also showing the cucullate petal tip. K Fruit. L Transverse section of fruit. M, N Seed. (A–J from Ridsdale 1974; K–N from Suessenguth 1953)

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indoor foliage plants (Sarracino et al. 1992a, b). Leaves of a few species of Leea have been used as traditional medicines by Asians and Africans. Leea hirta contains essential oils with tuberculostatic activity, and Leea guineensis is used for its cardiac and analgesic properties (Op de Beck et al. 2000). Afﬁnities. Leeaceae are most closely related to Vitaceae. Both families have “pearl” glands, raphides, antepetalous stamens, and ruminate seeds with oily endosperm. Most workers have now separated Leeaceae from Vitaceae (e.g., Planchon 1887; Gagnepain 1912; Suessenguth 1953; Ridsdale 1974; Cronquist 1981; Takhtajan 1997; Naithani 2000; Latiff 2001; Ren et al. 2003), although APG (1998) and APG II (2003) placed Leea in Vitaceae (also see Ingrouille et al. 2002). In contrast with Vitaceae, Leeaceae are characterized by the highly distinctive ﬂowers including a specialized ﬂoral disc, the absence of nectar production, the presence of secondary septa in the ovary, the absence of tendrils, the terminal inﬂorescence position, distinct wood anatomical characters, the unusual stipular structure, and the erect habit. For the phylogenetic position of the Leeaceae/Vitaceae clade, see discussion under Vitaceae in this volume. Only one genus: Leea van Royen ex L.

Figs. 76, 77

Leea van Royen ex L., Mant. 1:17, 124 (1767); Ridsdale, Blumea 22:57–100 (1974), rev.

Ridsdale (1974) distinguished 34 species, but some authors of regional studies tend to recognize a higher number.

Selected Bibliography Adkinson, J. 1913. Some factors of the anatomy of the Vitaceae. Ann. Bot. 27:133–139. APG 1998. See general references. APG II 2003. See general references. Behnke, H.-D. 1981. Sieve-element characters. Nordic J. Bot. 1:381–400. Corner, E.J.H. 1976. See general references. Cronquist, A. 1981. See general references. Gagnepain, F. 1912. Leeacées. Flore générale de l’Indochine, 1. Paris: Masson, pp. 934–944. Gagnepain, F. 1950. Leeacées. Flore générale de l’Indochine, suppl. vol. 7. Paris: Masson, pp. 844–855. Gerrath, J.M., Lacroix, C.R. 1997. Heteroblastic sequence and leaf development in Leea guineensis. Intl J. Pl. Sci. 158:747–756.

Gerrath, J.M., Lacroix, C.R., Posluszny, U. 1990. The developmental morphology of Leea guineensis. II. Floral development. Bot. Gaz. 151:210–220. Gill, B.S., Singhal, V.K., Bedi, Y.S., Bir, S.S. 1990. Cytological evolution in the woody taxa of Pachmarhi Hills. J. Cytol. Genet. 25:308–320. Ingrouille, M.J., Chase, M.W., Fay, M.F., Bowman, D., van der Bank, M., Bruijn, A.D.E. 2002. Systematics of Vitaceae from the viewpoint of plastid rbcL sequence data. Bot. J. Linn. Soc. 138:421–432. Karkamkar, S.P., Patil, V.P. 1992. Karyotype variation in Leea L. J. Indian Bot. Soc. 71:217–220. Kramer, K. 1974. Die Tertiär-Hölzer Südost-Asiens (unter Ausschluss der Dipterocarpaceae). 2. Teil. Palaeontographica B 145:1–150. Lacroix, C.R., Gerrath, J.M., Posluszny, U. 1990. The developmental morphology of Leea guineensis. I. Vegetative development. Bot. Gaz. 151:204–209. Latiff, A. 2001. Diversity of the Vitaceae in the Malay Archipelago. Malayan Nat. J. 55 (1&2): 29–42. Li, C.L. 1998. Vitaceae. In: Flora Reipublicae Popularis Sinicae, 48, 2. Beijing: Science Press, pp. 1–177. Metcalfe, C.R., Chalk, L. 1950. See general references. Nair, N.C., Namnisan, P.N.N. 1957. Contributions to the ﬂoral morphology and embryology of Leea sambucina Willd. Bot. Notiser 110:160–172. Naithani, B.D. 2000. Leeaceae. In: Singh, N.P., Vohra, J.N., Hajra, P.K., Singh, D.K. (eds) Flora of India, 5. Calcutta: Botanical Survey of India, pp. 325–342. Op de Beck, P., Bessière, J.M., Dijoux-Franca, M.-G., David, B., Mariotte, A.-M. 2000. Volatile constituents from leaves and wood of Leea guineensis G. Don (Leeaceae) from Cametoon. Flavour Fragrance J. 15:182–185. Planchon, J.E. 1887. Monographie des Ampélidées vrais. In: de Candolle, A.F.P.P., de Candolle C. (eds) Monographiae Phanaerogamarum 5, 2. Paris: Masson, pp. 305–654. Poole, I., Wilkinson, H.P. 2000. Two early Eocene vines from south-east England. Bot. J. Linn. Soc. 133:1–26. Prakash, U., Dayal, R. 1963. Fossil wood resembling Elaeocarpus and Leea from Deccan Intertrappean Beds of Mahurzari near Nagpur. Palaeobotanist 12:121–127. Ren, H., Pan, K.-Y., Chen, Z.-D., Wang, R.-Q. 2003. Structural characters of leaf epidermis and their systematic signiﬁcance in Vitaceae. Acta Phytotax. Sin. 41:531– 544. Ridley, H.N. 1930. The dispersal of plants throughout the world. Kent: L. Reeve. Ridsdale, C.E. 1974. A revision of the family Leeaceae. Blumea 22:57–100. Ridsdale, C.E. 1976. Leeaceae. In: van Steenis, C.G.G.J. (ed.) Flora Malesiana I, 7:759–782. Leiden: Noordhoff. Sandhu, P.S., Mann, S.K. 1989. SOCGI plant chromosome number reports, VIII. J. Cytol. Genet. 24:179–183. Sarracino, J.M., Merritt, R., Chin, C.K. 1992a. Morphological and physiological-characteristics of Leea coccinia and Leea rubra in response to light-ﬂux. HortScience 27:400–403. Sarracino, J.M., Merritt, R., Chin, C.K. 1992b. Light acclimatization potential of Leea coccinia and Leea rubra grown under low light-ﬂux. HortScience 27:404–406.

Leeaceae Suessenguth, K. 1953. Leeaceae. In: Engler, A., Prantl, K., Die natürlichen Pﬂanzenfamilien, 2nd edn, 20d. Berlin: Duncker & Humbolt, pp. 372–390. Takhtajan, A. 1997. See general references. Tarnavschi, I.T., Petria, E. 1968. Contribution to the knowledge of the microsporial structures in the family Leeaceae. Pollen Spores 10:221–249.

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Vatsala, P. 1960. Chromosome studies in the Ampelidaceae. Cellule 61:191–206. Watari, S. 1951. Studies on the fossil woods from the Tertiary of Japan. VII. Leea (Vitaceae) from the Miocene of Simane. Bot. Mag. Tokyo 64:1–7. Wheeler, E.A., LaPasha, C.A. 1994. Woods of the Vitaceae – fossil and modern. Rev. Palaeobot. Palynol. 80:175–207.

Lythraceae Lythraceae J. St.-Hil., Expos. Fam. Nat. 2:175 (1805), nom. cons. Trapaceae Dumort. (1829). Punicaceae Horan. (1834). Sonneratiaceae Engl. (1897). Duabangaceae Takht. (1985).

S.A. Graham

Trees, shrubs or herbs, frequently with the younger stems quadrangulate; nodes unilacunar. Leaves opposite, seldom whorled or alternate, simple, entire (dentate in Trapa), stipulate or estipulate, glandular processes present in the axil at the base of the petiole in most genera; blades membranous or coriaceous, venation brochidodromous. Inﬂorescences determinate or indeterminate, forming cymes, axillary or terminal racemes, spikes, or thyrses, rarely ﬂowers solitary; the pedicels with prophylls. Flowers generally odorless, actinomorphic, or tending to zygomorphic by increased abaxial orientation of stamens and pistil, truly zygomorphic in Pleurophora and Cuphea, perfect (dioecious in Capuronia), typically perigynous, seldom epigynous or hemi-epigynous, 4–6(8–16)-merous, mono-, dior trimorphic; ﬂoral tube campanulate to tubular, often conspicuously nerved, persistent (except Lafoensia), membranous to thick and coriaceous; sepals one half or less the length of the ﬂoral tube, valvate, triangular-ovate, acute, often alternating with external appendages (the epicalyx); petals (0–)4–6(–many), inserted on the inner rim of the ﬂoral tube, alternating with the sepals, crumpled, pinnately veined, frequently clawed, caducous; stamens typically diplostemonous, sometimes reduced to a single antesepalous or antepetalous whorl, when diplostemonous, then the ﬁlaments of the antesepalous whorl longest, inserted near the base of the ﬂoral tube or above, anthers dorsiﬁxed, versatile, rarely basiﬁxed, introrse, bilocular, longitudinally dehiscent; gynoecium syncarpous, encircled at the base by nectariferous tissue or the nectary enlarged, forming a unilateral free-standing nectary, or nectary 0; stigma capitate or punctiform, dry or wet; style simple, slender, commonly exserted; ovary superior or less often semi-inferior to inferior, thin- or thick-walled, 2–4(–many)-locular, the septa incomplete at the apex or vestigial and reduced to thin threads; placentation axile, the placenta slender or globose

and nearly free-central at capsule maturity; ovules 2–many. Fruit a dry, thin- to thick-walled capsule enclosed by the persistent ﬂoral tube, rarely leathery and berrylike, dehiscing loculicidally, septicidally, or splitting irregularly, infrequently circumscissile or indehiscent. Seeds obpyramidal or oblong to obovoid and convex-concave or lenticular-compressed, winged or not; seed coat with or without inverted epidermal hairs; embryo straight, cotyledons planar (rolled in Lagerstroemia and Punica), often auriculate or cordate, partially enveloping the short radicle, oily. x = 8. Widely distributed in the subtropics and tropics of both hemispheres, some temperate representatives, comprising 31 genera and c. 600 species. Vegetative Morphology. The family is predominantly woody, with the majority of genera small trees, large shrubs or single to multistemmed subshrubs to 15 m. Six genera include tall tree species up to 30 m or more: Duabanga, Sonneratia, Lagerstroemia, Lafoensia, Ginoria, and Physocalymma. Bark in the larger forms is frequently plate-like, pale and smooth, ﬂaking in large irregular ﬂakes to reveal green or coral inner bark. Also common in the family is rough, dark, ridged bark, excorticating in ﬁbrous strips. Young stems of most genera are four-angled, becoming terete with age. Annual and perennial herbs less than 50 cm tall occur in Ammannia, Nesaea, Rotala, Didiplis, Lythrum, Peplis, Cuphea, and Pleurophora. Most small herb species are associated with aquatic or marsh habitats. In Pleurophora, however, the diminutive species are highly adapted desert inhabitants. Trapa, with vegetatively distinctive ﬂoating and submersed leaves, is unique in the family in having inﬂated petioles on the leaves at the ends of the branches, which form ﬂoating rosettes, and highly dissected leaf-like organs at submerged nodes. Extensive aerenchymatous tissue develops on submerged stems of several marsh-inhabiting or wetland gen-

Lythraceae

Fig. 78. Lythraceae. Stand of Sonneratia alba in the Marshall Islands, Paciﬁc, with pneumatophores. (Photograph Nancy Vandervelde)

era (e.g., Ammannia, Cuphea, Decodon, Heimia, Lythrum, Peplis, Trapa), by production of phellem (Lempe et al. 2001; Stevens et al. 2002), or in Trapa by proliferation of the outer cortex (Timonin 1999). The mangrove genus Sonneratia develops an extensive subaerial horizontal root system from which arise numerous vertical pneumatophores (Fig. 78). The pneumatophores are not respiratory organs per se but function by producing two other root types: anchor roots that grow downward, and subaerial, ﬁnely branched nutrition roots that extend horizontally outward from the pneumatophore into the uppermost silt layer to absorb incoming nutrients (Troll 1930). Leaves are predominantly decussate and membranous to coriaceous. The margin is entire, excepting for Trapa where the ﬂoating leaves are coarsely toothed distally. Venation is typi-

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cally brochidodromous. Seemingly uni-nerved, in-rolled heath-like leaves are convergent in white sand-inhabiting species of two sections of Cuphea, and in some Diplusodon of sandy and rocky campos. Slight leaf dimorphism, mainly in leaf shape, occurs in amphibious species of Rotala and Didiplis and is pronounced in the aquatic Trapa where submerged leaves are linear, entire margined, opposite on the stem, and caducous and ﬂoating leaves are rhombic, toothed, alternate in rosettes, and persistent. The leaf-like organs on submerged stems of Trapa appear to be highly modiﬁed, photosynthetic adventitious roots (Couillault 1973). In Pleurophora, the leaf, prophyll, and sepal apices of the desert species are modiﬁed to rigid spines. In Lawsonia and Punica, branch tips become hardened spines, reﬂecting the dry eastern MediterraneanEurasian origins of these well-known cultivated plants. Subapical, porate chambers are present on the undersides of leaves of Lafoensia (Fig. 84C), Capuronia, Galpinia, Sonneratia, and Punica (Ross and Suessenguth 1926; Rao and Chakraborti 1982; Belin-Depoux 1989). These act as hydathodes, salt-secreting glands, or nectaries. Stipules, when present, are minute and caducous. Trapa is exceptional in bearing stipules that split to the base and appear as multiple scarious stipules at a node. Weberling (1984) has described intrapetiolar stipular processes in Lythraceae and other families of Myrtales that are ﬂeshy, sometimes secretory, hair-like appendages at the base of the petiole in the leaf axil. Vegetative Anatomy. Most genera are glabrous or, at most, pubescent. Diplusodon can have unusual, tufted trichomes and Lagerstroemia sect. Trichocarpidium has dendritic trichomes. The trichomes of Pleurophora and Cuphea include multicellular hairs secreting resinous exudates, and in Cuphea especially, other unicellular types, including malpighiaceous cystolitic hairs. Globose, multicellular glands with elongate necks or with spinulose surfaces characterize Adenaria, Koehneria, Pehria, Woodfordia, Pleurophora, Cuphea, and Lourtella. Leaf structure in the family has been studied by Keating (1984). It is relatively homogeneous and most closely resembles that of Onagraceae, excepting for Trapa. Leaves are dorsiventral with adaxial and abaxial epidermal layers the same size, except in Punica p.p. and Duabanga; mucilage cells large, frequent; stomata on one or both surfaces, seldom sunken, mainly anomocytic; palisade lay-

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ers mostly 1 or 2 (3 or 4 in Sonneratia), occupying (25–)30–50% of the lamina, spongy mesophyll 3–5layered (–11-layered in Sonneratia); midvein often prominently rounded abaxially, bicollateral; secondary veins collateral; sclereids absent except in Duabanga, and astrosclereids in Sonneratia; druses common; large prismatic crystals in the mesophyll of Punica. The ﬂoating leaves of Trapa reﬂect their aquatic habit by the presence of adaxial stomata and well-developed aerenchyma. Wood anatomy has been extensively surveyed at the generic level (Graham and Lorence 1978; Bridgwater and Baas 1978; Baas and Zweypfenning 1979; Baas 1986; Rao et al. 1987). Lythraceae have vestured pits in the secondary xylem and internal phloem in the secondary tissues, a rare combination in angiosperms that is diagnostic for Myrtales. There is much general wood anatomical agreement among the genera, which extends to the families of the order as well. Growth rings are absent to distinct; mostly diffuse-porous but semi-ring to ring porous in a third of the genera. Vessels number 6–300(–500)/mm2 , highest in woody herbs, solitary or in radial multiples of 2–8(–10), round to weakly angular, tangential diameter 30–220 µm, vessel member length (130–)200–580(–630) µm, sometimes with dark gummy contents; spiral thickenings present in Heimia, Nesaea, and Pleurophora; perforations simple in oblique to horizontal end walls. Intervessel pits are crowded, alternate, vestured, round, oval, or weakly polygonal, 3–12 µm diam. Vascular tracheids are rare (Heimia, Woodfordia, and Pleurophora). Fibers are typically libriform with simple pits, 380–1,850 µm, septate (except Ammannia, Diplusodon, Nesaea, Pemphis, and Pleurophora) and sometimes chambered crystalliferous (Capuronia, Galpinia, Ginoria, Lagerstroemia, Lawsonia, Pehria, Punica); gelatinous ﬁbers common; ﬁbers dimorphic (common type plus distinctly shorter, thinner ones) in Physocalymma, Lawsonia, and some Lagerstroemia. Parenchyma is typically scanty paratracheal, absent in Pleurophora and Sonneratia, vasicentric to aliform and conﬂuent in Pemphis and Duabanga, and banded in some Lagerstroemia. Rays are typically heterogeneous, rarely homogeneous, 1(–3)-seriate, in the woody herbs cells exclusively erect and 1-seriate. Crystals are present or absent, rhomboidal, in chambered ﬁbers or chambered axial parenchyma. Sieve-element plastids are uniformly of the S-type common to the order Myrtales (Behnke 1984).

The basic anatomical state of the family includes: solitary vessels or short radial multiples, heterogeneous type I rays, septate ﬁbers, and scanty paratracheal parenchyma. Lagerstroemia is regarded as the most wood-anatomically advanced genus of the family (van Vliet and Baas 1984). The commonality of many anatomical features among the genera, and even with other members of the order, especially Oliniaceae and Psiloxylaceae, restricts their phylogenetic usefulness. At the same time, the derived character states appear to be highly subject to parallelism and reversibility, so relationships based on wood anatomical characters must be interpreted with caution. Inﬂorescence Structure. The family is divided into genera with anthotelic (∼determinate) inﬂorescences, in which the apex of the inﬂorescence axis terminates in a ﬂower (Duabanga, Galpinia, Lagerstroemia, Lawsonia, Punica, Sonneratia, and Trapa), and the rest with blastotelic (∼indeterminate) inﬂorescences in which the shoot apex remains vegetative. Weberling (1988) considered the anthotelic form ancestral in Myrtales, and hence plesiomorphic in the genera named above. Great variation in form occurs in both basic inﬂorescence types (Koehne 1884; Weberling 1988). Most common is the thyrse (blastotelic with lateral cymes). Proliﬁcation is widespread. Cymes multiply to form an umbelliform cluster in Adenaria, Pehria, Decodon; they are reduced to uniﬂory in some species of Ammannia, Rotala, Lythrum, Peplis, Diplusodon, Heimia, Pleurophora, and Cuphea. Condensation in some species of Nesaea and Pleurophora results in terminal or lateral capitula. In genera with long-shoot/short-shoot forms (Physocalymma, some Ginoria), long shoots remain vegetative while ﬂowers form on axillary shoots, ﬂowering prior to vegetative growth of the new season. In most species of Cuphea (except in oppositeﬂowered sect. Cuphea), the ﬂowers are alternate and interpetiolar. Accessory ﬂowering shoots are common in the genus. Flower Structure. Flowers are actinomorphic or weakly to strongly zygomorphic. Pleurophora and Cuphea are the most zygomorphic, with zygomorphy extending to reduction of the ventral locule of the bilocular ovary. Cuphea has additional autapomorphies, such as reduction of the septal walls to two threads, dorsal (adaxial) petals and the dorsalmost sepal enlarged in many spe-

Lythraceae

cies, reduction or loss of the two dorsalmost stamens, a free-standing unilateral nectary, and dehiscence of the capsule and ﬂoral tube via a longitudinal dorsal slit. Woodfordia and Pehria, although actinomorphic, display stamens and style ventrally (as do some other genera to a lesser degree, e.g., Koehneria, Lagerstroemia, and Lythrum), and capsules tend to dehisce dorsally. Flowers are bisexual, except in Capuronia where remnants of the ovary or stamens are present in functionally unisexual ﬂowers. Calyx lobes are valvate. In many species, the margins of the calyx lobes at the sinus are congenitally fused and enlarge, forming “appendages” of an epicalyx (Mayr 1969). Development of the androecium is highly variable, although considered ancestrally obdiplostemonous. Stamen development is centrifugal in Lagerstroemia and centripetal in Punica, with the difference dependent on where the greatest amount of receptacular (ﬂoral tube) growth occurs following initiation of the androecial primordia (Ronse Decraene and Smets 1991). Petals develop late, shortly before anthesis (Mayr 1969). Basic ﬂoral structure consists of: persistent perigynous 4–6-parted ﬂoral tube; petals inserted on the inner margin of the ﬂoral tube between the calyx lobes, commonly caducous, typically rose-purple, less often cream white to yellow; androecium typically obdiplostemonous, alternating whorls of stamens inserted near but not at the base of the ﬂoral tube, anthers dorsiﬁxed, introrse, 4-locular, with persistent endothecium, opening by 2 longitudinal slits; stigma small and dry, but in Lagerstroemia, Punica, Sonneratia, Heimia and possibly other genera, the stigma wet; ovary typically superior, few-locular with axile placentation and septal walls incomplete near the apex of the ovary, very slightly to fully inferior in Duabanga, Physocalymma, Punica, Sonneratia, Trapa; annular or unilateral nectary at the base of the ovary; fruits capsular or less often berrylike; seeds many, typically less than 3 mm long, morphologically diverse within the family. The tetramerous and hexamerous states are found in approximately equal numbers among the genera, and merosity is ﬂexible within populations, even on single plants. Only Decodon is typically pentamerous, and if this proves basal in the family and derived from an earlier pentamerous Combretaceae lineage as some molecular phylogenetic analyses indicate, then pentamery is ancestral for Lythraceae. Evolutionary ﬂoral changes include: increase or decrease in length or thickness of the ﬂo-

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ral tube; spur formation; ﬂoral tube coloration, loss or multiplication of petals, stamens and carpels; haplostemony or obhaplostemony; increasing adnation of the ovary to the ﬂoral tube (hemi-epigyny or epigyny); enlargement of the placenta, resulting in a false free-central placenta; positional change and gain or loss of nectaries. Embryology. Tobe and Raven (1983) summarized embryology in the order Myrtales. Although observations are limited, the following characteristics are considered typical of Lythraceae: anthers with a ﬁbrous endothecium; multicelled archesporium (1-celled archesporium in most other Myrtalean families); glandular 2–6-nucleatecelled tapetum; pollen 2-celled; ovules anatropous, crassinucellate, bitegmic, the outer integument 2- to multilayered, inner integument 2-layered, both forming the micropyle; megaspores arranged linearly, the chalazal one functional; embryo sac formation of the 8-nucleate Polygonum type but with antipodals ephemeral; endosperm Nuclear, ultimately wanting. Trapa presents several embryological conditions not otherwise known in the order, including: the micropyle formed by a long nucellar beak, rather than by the integuments, development of a coiled suspensor that functions as a collar to support the embryo, and unequal cotyledon development. Pollen Morphology. Lythraceae are palynologically the most diverse family in Myrtales, with nearly all genera having a distinct morphology (Fig. 79). Pollen of all genera has been described (Patel et al. 1984; Graham et al. 1985, 1987, 1990).

Fig. 79. Lythraceae. Pollen. A Cuphea nitidula, polar view of tricolporate grain. Actual size: 19 µm. B Lythrum rotundifolium, equatorial view of tricolporate/heterocolpate grain, note granular membrane of colpi and pseudocolpi. Actual size: 22 µm. (Orig.)

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Typical lythracean pollen is: prolate to prolatespheroidal; tricolporate, pseudocolpi absent; exine psilate to scabrate or ﬁnely verrucate; diameter 23 µm or less. In TEM, the extexine is mostly columellar, with the tectum, foot layer, and endexine continuous and moderately thick. Specializations include development of 3 or 6 pseudocolpi (extra furrows lacking pores and thought to have a harmomegathic function), present or incipiently present in 15 genera. Pollen of Cuphea is compressed at the poles (oblate) and is exceptionally diverse at the species level. Pollen of Duabanga and Sonneratia, uniquely for the family, is triporate. Pollen of Trapa is distinctive due to the three prominent meridional ridges that pass over the colpi to fuse at the poles and form enlarged triangular caps. Pollen and anther sacs are typically yellow but can also be green, orange, or red. Lagerstroemia and Lythrum are exceptional in having some species with both di- or trimorphic stamens and pollen. In many Lagerstroemia, ﬁlaments of the antesepalous stamens are longer, thicker, and bear larger anthers of a different color than the antepetalous ones. The pollen is smaller with a thinner exine, and the pseudocolpi are less conspicuous than in the antepetalous stamens (Kim et al. 1994). In dimorphic Lagerstroemia and some Lythrum, anthers of the antesepalous whorl are purple-red and enclose green dry pollen, while those of the antepetalous whorl are yellow with yellow, oilor starch-ﬁlled pollen. A number of studies on Lagerstroemia have veriﬁed the fact ﬁrst observed by Darwin (1877) that only the green pollen is capable of emitting pollen tubes and fertilizing ovules whereas the yellow pollen serves as “feeding” pollen, attracting pollinators to the nectarless ﬂowers (Faegri and van der Pijl 1979; Pacini and Bellani 1986). Green pollen is sucrose-rich; yellow pollen is fructose-rich (Nepi et al. 2003). Karyology. Chromosomes are mostly small, 1–4 µm long, with median or submedian centromeres. Approximately half of the genera are diploids or ancient polyploids based on x = 8 (Tobe et al. 1986; Graham and Cavalcanti 2001). Pleurophora is an aneuploid with x = 7, and Lythrum and Peplis are x = 5. Diplusodon, with x = 15, is most likely an aneuploid derived from x = 16. Other generic basic numbers (or in polyploid genera, secondarily basic numbers) include 12, 24, 28, and 32. Hionanthera and Lourtella are uncounted. Ammannia, Cuphea, Lagerstroemia, Lythrum, and Rotala display diverse and wide-ranging aneuploid

and polyploid numbers. In Cuphea, counts for 127 species include 23 different numbers ranging from n = 6 to c. 86 (Graham 1989a, 1992; Graham and Cavalcanti 2001). The basic number of the family may have been derived through aneuploid reduction from a higher x = 12, the basic number for the order Myrtales (Graham et al. 1993b). The basic number of the clade Sonneratia-Trapa + Duabanga-Lagerstroemia, x = 12, however, is considered secondarily derived within the family, independent of the ancestral chromosome basic number of the order. Reproductive Biology. The typical reproductive system is one of homomorphic ﬂowers that are self-compatible but rely on pollinators for outcrossing. Flowers are protandrous in most genera, with the stigma being carried past introrse, dehiscent anthers prior to stigma receptivity, thus reinforcing outcrossing. Some species of the herbaceous genera Ammannia, Cuphea, Didiplis, Lythrum, Nesaea, Peplis, and Rotala are autogamous, although in Cuphea fewer than 20 of the c. 260 species are self-fertilizing. Trapa is primarily self-pollinated and self-compatible; apomixis is also reported (Kadono and Schneider 1986). Species recognition in the herbaceous aquatic/amphibious genera Ammannia, Nesaea, and Rotala is often difﬁcult due to evolutionary convergence in aquatic habitats and inbreeding in many members. Flowers of most genera are odorless, entomophilous and promiscuously visited by a variety of small to large bees, butterﬂies, day-ﬂying moths, and hummingbirds. Lawsonia is fragrant. Bat pollination occurs in Lafoensia and Sonneratia, whose night-blooming ﬂowers have yellow to white petals and many long-exserted stamens. Only Capuronia is dioecious, and Adenaria is functionally so. Genetic self-incompatibility is noted in four species of Rotala (Cook 1979), and in three species of Diplusodon (Barros 1989). Self-incompatibility occurs to varying degrees in the heterostylous members of the family. Lythraceae are one of only about 25 families with distylous species, and one of ﬁve with tristylous species (Lloyd and Webb 1992). Floral morphs differ in style length, anther height, size of the pollen grains, and stigma papillae (Dulberger 1970). This unusual breeding system is generally thought to promote outcrossing and reduce inbreeding depression, although the selective basis for its evolution is not completely understood (Barrett 1992). In the tristylous Decodon, Eckert

Lythraceae

(2002) found up to 30% of progeny were the result of selﬁng. Morphological evidence suggests distyly is derived in Pemphis and within Lythrum from tristylous ancestors (Lewis and Rao 1971; Lewis 1975; Ornduff 1979), but this possibility needs to be put to a phylogenetic test. Tristyly occurs in Adenaria, Decodon, four species of Lythrum, and possibly four species of Nesaea. Distyly occurs in Pemphis, and within Lythrum (in c. 10 species), Rotala (four species) and Nesaea (in c. 14 species). On the basis of the most recent phylogenetic studies (Graham et al. 2005), heterostyly has arisen independently at least ﬁve times in the family.

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Fruits and Seeds. The most common fruit form is a capsule with a moderate to very thin dry wall and loculicidal dehiscence. Thick-walled, leathery or woody, dehiscent capsules occur in the woody shrub/tree genera Duabanga, Lafoensia, and Lagerstroemia. In Trapa, two or more of the four persistent sepals become hardened into spiny horns; other small projections may develop from the surface, and the entire fruiting structure becomes an indurated single-seeded drupe. Berrylike fruits with a tough, indehiscent pericarp apparently evolved independently in Adenaria, Capuronia, Lawsonia, and Punica. Capsules of small wetland herbs Ammannia, Didiplis, Hionanthera, Nesaea, Peplis, and Rotala, as well as Cuphea, Pleurophora, and Woodfordia have exceptionally

thin, papery walls that rupture irregularly (regular longitudinal slit in Cuphea) as seeds enlarge to maturity. Uniquely, the capsule walls of Rotala are microscopically transversely striated; the striations are the primary diagnostic morphological character separating the genus from Ammannia. Seeds of Lythraceae are numerous and mostly less than 3 mm long, although in Lafoensia seeds can reach 35 mm. Seed anatomy is relatively uniform throughout the family, in contrast to external morphology that is extremely diverse, including wings, ﬂeshy or mucilaginous seed coats, and ﬂoat tissue. The testa is multiplicative, except in the highly simpliﬁed 2-layered seed coat of Duabanga. Dual-reinforced layers composed of a sclerotic endotesta and adjacent tracheidal or ﬁbrous exotegmen form a hard shell around the embryo. The ﬁbrous exotegmen is one of the few synapomorphies that phylogenetically closely links the Lythraceae (including Trapa), Onagraceae, and Combretaceae (Corner 1976; Conti et al. 1997). In Decodon, Lawsonia, and Pemphis, the mesotesta develops small-celled spongy internal aerenchyma while seeds of the herbaceous marsh genera Ammannia, Nesaea, and Rotala ﬂoat by means of a unilateral exotestal aerenchymatous tissue of large cells. Seeds are distinctly obpyramidal in Decodon, Lagerstroemia, Lawsonia, Pemphis, and Punica. Weakly to strongly bilaterally compressed seeds

Fig. 80. Lythraceae. Seeds of Ammannia latifolia. A Seed covered by hairs that have everted from the seed coat ex-

otestal cells upon soaking in water. B Close-up of everted hairs. Scale: left bar = 100 µm; right bar = 14 µm. (Orig.)

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are characteristic of the rest of the family. The acquisition of a bilaterally compressed form, which enhances the seed’s ﬂoating capacity, appears to have occurred early in the history of the family and suggests an early adaptation to wet habitats. Among the compressed-seed genera, a feature has evolved in the seed coat that is possibly unique to all angiosperms – internal, epidermal cell hairs that develop by a ﬁngerlike extension of the plasma membrane into the cell. Upon wetting of the mature seed, the hairs evert through the cell wall, extend from the seed surface, and become mucilaginous (Fig. 80; Correns 1892; Panigrahi 1986; Graham 1995b). Presumably, the hairs hasten the softening of the seed coat for germination by increasing osmosis. Seventeen genera have internal epidermal cell hairs. The hairs are straight in 11 genera: Ammannia, Crenea, Didiplis, Diplusodon, Ginoria, Heimia, Hionanthera, Lythrum, Nesaea, Peplis, Rotala; and spirally twisted in ﬁve: Cuphea, Lafoensia, Pehria, Pleurophora, Woodfordia. Molecular phylogenetic hypotheses indicate straight seed hairs were also an early acquisition in the family whereas spiral hairs arose later from the hairless state (Graham et al. 2005). The single seed formed in the fruit of Trapa lacks a radicle and consists of two unequal cotyledons, one large and starchy, the other scale-like. Phytochemistry. Tannins are common in the family (Mole 1993). Flavonoids are mainly ﬂavonols and their methyl derivatives. Flavones are rare, although C-glycoﬂavones are reported (Gornall et al. 1979). Complex ﬂavonoid patterns occur in Cuphea that are not present in Diplusodon and Lafoensia (Salatino et al. 2000). Alkaloids have been characterized in Decodon, Lythrum, Heimia, Lagerstroemia, and Punica, and are especially well-studied in the ﬁrst three genera (Raffauf 1970). Distribution and Habitats. The family is mostly subtropical to tropical in distribution. Decodon, Didiplis, Lythrum, and Peplis have a Northern Hemisphere range. Endemic genera are about evenly divided between the Old and New World. Fourteen genera are exclusively Old World and the same number exclusively New World. In addition, four genera, Ammannia, Lythrum, Nesaea, and Rotala, are Old World in origin but have 1–few species endemic to North or South America. Genera occupy diverse habitats ranging from aquatic to xeric. The majority of genera grow in mesophytic to semixeric habitats, such as open woodlands, forest mar-

gins, low tropical semi-evergreen forests, grasslands, rocky campos, along margins of streams; several genera and some species of the largest genus Cuphea inhabit wetlands or temporary pools of water and their margins. Pemphis is an oceanic strand genus; Crenea grows in mud ﬂats bordering the Paciﬁc Ocean and southern Caribbean Sea. Sonneratia is a constituent of Asian mangroves. Members of the family are found from sea level to elevations over 3,000 m (species of Cuphea) in the mountains of Mexico, and Central and South America. Fossil History. The geological history of the family was reviewed by Graham and Graham (1971). The fossils are diverse in nature; fossil wood, leaves, ﬂowers, pollen or seeds are attributed to several genera. Among the oldest remains are: (1) partial leaf impressions (Lagerstroemia?) and wood (Sonneratia?) with associated fruits (Enigmocarpon) and ﬂowers (Sahnianthus) considered to have lythraceous afﬁnities, all from the Deccan intertrappean beds of western India with an age of c. 66–63.7 Ma, i.e., late Cretaceous or early Paleocene (Shukla 1950; Verma 1950; Widdowson et al. 2000); (2) distinctive Sonneratia/Florschuetzia pollen grains from the late Paleocene of France (Gruas-Cavagnetto et al. 1988); (3) two fossil genera of fruits with lythracean afﬁnities from the Eocene London Clay Flora, assignable at the family level (Collinson 1983); and (4) seeds of Decodon from lower Eocene beds in England (Chandler 1960) and the Eocene in Russia (Dorofeev 1970, as cited in Eyde 1972). The commonly recorded fossil pollen form genus Florschuetzia is regarded as the precursor of modern Sonneratia (Germeraad et al. 1968; Morley 2000). Florschuetzia pollen occurs in Borneo deposits, beginning in the upper Eocene and continuing through the stratigraphic record with morphological transitions leading to the modern Sonneratia pollen type by the middle Miocene (Fig. 16 in Germeraad et al. 1968). Florschuetzia pollen is also known from the late Eocene to Mid-Tertiary of northern India, Israel, and Egypt, in addition to the Paleocene of France, revealing a wide Tethyean distribution for this lineage prior to the establishment of Sonneratia in southeastern Asia (Morley 2000). Trapa and Decodon have long, nearly continuous fossil records. Fossil Trapa pollen and fruits are distributed stratigraphically and geographically in northern latitudes, especially from the Miocene to the present (Mai 1985; Zetter and Ferguson

Lythraceae

2001). Some Miocene fossil pollen forms from Vietnam have been considered transitional from Florschuetzia to Trapa, supporting the sister relationship of Trapa and Sonneratia recovered in molecular phylogenetic analyses (Morley 2000; Graham et al. 2005). The Maastrichtian record of Paleotrapa (Goloneva 1991) is based on fruits associated with leaves of an unknown taxon having distinctly different morphology than Trapa, and Paleotrapa is not ancestral to modern Trapa (Stockey and Rothwell 1997). The extensive fossil record of Decodon extends from the Eocene to the present, based on seeds and vegetative parts (Tiffney 1981; Cevallos-Ferriz and Stockey 1988; Little and Stockey 2003). Like Trapa, it was widely distributed stratigraphically and geographically in the northern latitudes, especially from the Miocene onward. Today, Decodon is limited to a single living species in eastern North America. Fossil pollen attributed to Lagerstroemia is reported from the Middle Eocene of Java (Morley 2000), and Crenea, or an ancestral form of the genus, is reported from the Upper Eocene of northern South America (Germeraad et al. 1968; Graham and Graham 1971; Muller 1981). Upper Eocene-Lower Oligocene deposits from Cameroon have yielded pollen of Rotala or Crenea (SalardCheboldaeff 1981). Pollen of the New World genus Cuphea ﬁrst appears later in the fossil record from the Miocene of northern South America and the southern United States, and is abundant in the Amazon Basin in some local deposits of possible Pleistocene age (Absy 1982). Fossil woods with relationships to Sonneratia and Duabanga have been described from the Paleogene of India (Guleria 1991) and the Tertiary of Pakistan (Ahmed et al. 1991), and Duabanga-like leaves from the Middle Eocene of British Colombia (Little et al. 2004). Other fossils with afﬁnities to the Lythraceae but not directly comparable to modern genera were also present by the Middle Eocene in western North America (Pigg and Wehr 2002). The geographical origins of modern Lythraceae are uncertain because the earliest branching events in the phylogeny of the family are not yet resolved. One hypothesis places Decodon at the base of the family, followed by Lythrum and Peplis, which suggests a Laurasian, rather than Gondwanan, origin (Graham et al. 2005). Afﬁnities. Results of molecular studies (Conti et al. 1996, 1997; Sytsma et al. 2004; Graham et al. 2005) and morphological phylogenetic analyses

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by Johnson and Briggs (1984) and Graham et al. (1993a, 2005) agree that Onagraceae are sister to Lythraceae. Summary evidence indicates that Combretaceae are the sister family to all other Myrtales, and that the Lythraceae + Onagraceae lineage constitutes one of two large clades in Myrtales that diverged from ancestral combretaceous stock in the Albian at ∼ 109 Ma. Separation of Lythraceae and Onagraceae from a common ancestor is dated at ∼ 93 Ma (Sytsma et al. 2004). The position of Trapa, generally acknowledged as most closely related either to Onagraceae or Lythraceae, occurs as sister to Sonneratia within a four-member clade composed of DuabangaLagerstroemia + Sonneratia-Trapa in phylogenetic studies of multiple gene sequences (Huang and Shi 2002; Graham et al. 2005). This strongly supported sister relationship nested well within Lythraceae is the basis for the taxonomic inclusion of Trapaceae within Lythraceae. The genera Alzatea and Rhynchocalyx, sometimes placed in Lythraceae, have been removed to their own families (Graham 1984; Johnson and Briggs 1984; Conti et al. 1997; Clausing and Renner 2001; Schönenberger and Conti 2003). Relationships Within the Family. The only complete classiﬁcation of the family is that of Koehne (1903) who delimited the family narrowly, rejecting a number of genera earlier accepted in Lythraceae, including Sonneratia, Duabanga, and Punica. Thorne (1976) and Dahlgren and Thorne (1984) recognized these as subfamilies of Lythraceae. Koehne’s classiﬁcation of Lythraceae s.str. consists of two tribes each with two subtribes. The sole basis on which the tribes were erected, septal walls complete vs. incomplete, was negated by Tobe et al. (1998) who found that the septa in all genera are incomplete to some degree. Morphological characters are highly homoplasious in the family, and consequently morphologically based phylogenetic hypotheses are poorly resolved. Relationships based on comparisons of DNA sequences are more resolved but still incomplete taxonomically. The Bayesian consensus tree generated from chloroplast genome (rbcL, trnL-F, psaA-ycf 3) and nuclear genome (ITS) data of 20 genera places Decodon at the base of the family and indicates an early split into two major lineages (Fig. 81; Graham et al. 2005). The sister relationship of Didiplis, which has been uncertain because there are so few morphological characters for comparison, is with Rotala, based

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on analysis of nuclear ITS and cp atpB-rbcL spacer data (Morris et al. 2005). Deep branches of the phylogeny are weakly supported; terminal clades, in contrast, are strongly supported. This makes a taxonomic restructuring of the family virtually impossible, and genera are here formally treated in alphabetic order, although comments on closest relatives are added where possible. The difﬁculty in reconstructing the basal and near-basal branches is attributed to early, rapid evolution and multidirectional dispersal of the family. Multiple cases of sister genera today widely separated geographically in the Old and New World suggest that the ancestral lythracean stock had radiated widely by the late Cretaceous, and that early lineages have been subject to extensive extinction. Uses and Economic Importance. A few genera are widely employed in horticulture, others are a source of timber, natural dyes, and folk medicines. Lagerstroemia indica, crape myrtle or reseda, is a popular street and landscaping tree in warm temperate to tropical regions of the world. Other Lagerstroemia, especially L. speciosa, are also cultivated (Egolf and Andrick 1978). Ellagitannins isolated from leaves of L. speciosa show promise in reducing blood sugar levels in people with type 2 diabetes (Judy et al. 2003). Lawsonia inermis is the source of the cosmetic dye henna, and is grown also for its fragrant ﬂowers. Leaves of the Asian Woodfordia fruticosa (dhawa, sidowayah) are used in the treatment of dysentery, dermal lesions, infertility, as an aphrodisiac and as a sedative (Graham 1995a). In Heimia salicifolia, eight alkaloids have been identiﬁed that have a synergistic action with auditory hallucinogenic effects. The alkaloids have signiﬁcant anti-inﬂammatory properties (Malone and Rother 1994). Several species of Cuphea are well-known Latin American folk remedies for syphilis, fevers, and as diuretics or laxatives. Crushed leaves of C. aequipetala are applied to open wounds to promote healing. Active compounds in C. carthagenensis lower blood pressure and affect muscle tone and membrane permeability to calcium (Ericeira et al. 1984). Cuphiin, a macrocyclic tannin isolated from C. hyssopifolia, shows promising anti-tumor activity (Wang et al. 2002). Several species are popu-

Fig. 81. Lythraceae. Bayesian consensus tree of combined molecular data of 19 genera of Lythraceae, plus the outgroups Onagraceae and Combretaceae. (Graham et al. 2005)

Lythraceae

lar garden plants, especially C. hyssopifolia (Mexican heather) and C. ignea (ﬁrecracker or cigar ﬂower), a ﬂower of Hawaiian leis, and more recently, C. llavea (bat ﬂower or tiny mice). The seeds of Cuphea contain signiﬁcant amounts of medium-chain fatty acids such as lauric acid that are used extensively by the food and chemical industries (Graham 1989b). Genetic engineers and plant physiologists employ Cuphea as a source of genes to alter fatty acid chain lengths in agriculturally established oilseed crops such as rape, and as a model organism to study fatty acid biosynthetic pathways (Töpfer et al. 1995; Schuett et al. 2002). In seed lipids of other genera of Lythraceae, linoleic acid is the dominant fatty acid, as it is in most angiosperm seed oils (Graham and Kleiman 1987).

Key to the Genera 1. Stamens all or in part positioned at the rim of the ﬂoral tube; ﬂoral tube epigynous or hemi-epigynous to perigynous; stamens usually many, seldom as few as 12 2 – Stamens all positioned below the rim of the ﬂoral tube; ﬂoral tube perigynous or hemi-epigynous; stamens usually 4–12, seldom numerous 4 2. Floral tube epigynous, orange-red or yellow; fruiting ﬂoral tube completely enveloping the fruit, crowned by erect, persistent sepals; seeds ﬂeshy 26. Punica – Floral tube perigynous or hemi-epigynous, greenish; fruiting ﬂoral tube half-enveloping the fruit or ﬂattened, the sepals spreading; seeds dry 3 3. Flowers 1–3(–5) in terminal racemose clusters; petals linear or absent; fruits indehiscent, globose, leathery berries 28. Sonneratia – Flowers 5–many in terminal corymbiform panicles; petals oblong to obovate; fruits loculicidally dehiscent, thick-walled capsules 9. Duabanga 4. Fruits bearing 2–4 prominent hardened spines; leaf margins coarsely toothed distally 30. Trapa – Fruits without spines or horns; leaf margins entire 5 5. Inﬂorescences terminating in a ﬂower bud 6 – Inﬂorescences terminating in a vegetative bud 8 6. Apices of leaves bearing an abaxial porate chamber; stamens 6; seeds bilaterally compressed, encircled by a thin wing 10. Galpinia – Apices of leaves unmodiﬁed; stamens 8–many; seeds obyramidal, winged or not 7 7. Stamens (4–)8(–12), paired, antesepalous; seeds not winged 17. Lawsonia – Stamens 12–many, in two whorls; seeds unilaterally winged 16. Lagerstroemia 8. Flowers unisexual; branchlets terminating in sturdy spines 3. Capuronia – Flowers bisexual; branchlets without spines 9 9. Leaves glandular-punctate, the punctae translucent and secretory, or orange-ﬁlled, turning black and non-secretory 10

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– Leaves non-punctate, glabrous or variously indumented 14 10. Leaves translucent-punctate, varnished by abundant resinous secretions; inﬂorescences simple, 3-ﬂowered axillary cymes 18. Lourtella – Leaves orange or black-punctate, the punctae non-secretory; inﬂorescences solitary ﬂowers or multi-ﬂowered clusters 11 11. Inﬂorescences solitary ﬂowers; stamens 18, the antesepalous ones paired 14. Koehneria – Inﬂorescences multi-ﬂowered clusters; stamens 8 or 12 12 12. Flowers 6-merous, stamens 12, of two lengths; ovary stipe absent or very short 30. Woodfordia – Flowers 4-merous, stamens 8, of one length; ovary stipe conspicuous 13 13. Flowers in compact umbelliform clusters; ﬂoral tube campanulate, greenish; capsule indehiscent 1. Adenaria – Flowers in loose cymose clusters; ﬂoral tube cyathiform, deep red; capsule loculicidally dehiscent 21. Pehria 14. Floral tube campanulate to globose or cyathiform, about as long as to slightly longer than wide, actinomorphic 15 – Floral tube cylindrical, at least twice as long as wide, actinomorphic or zygomorphic 30 15. Seeds regularly or somewhat irregularly obpyramidal, the embryo embedded in dense small-celled aerenchyma 16 – Seeds elongated to nearly globose, concave-convex, or bilaterally compressed, the embryo surrounded by a few-layered seed coat, aerenchyma absent or present as a large-celled exotestal ﬂoat on the raphal side of the seed 17 16. Flowers in dense axillary clusters in the upper axils, tristylic, 5-merous 6. Decodon – Flowers solitary or paired in the axils, distylic, 6-merous 22. Pemphis 17. Seeds encircled by a broad, thin wing 18 – Seeds not winged 20 18. Floral tube caducous in fruit, 25–55 mm long including sepals; seeds 8–35 mm long 15. Lafoensia – Floral tube persistent in fruit, 5–15 mm long including sepals; seeds 2–4 mm long 19 19. Flowers 8-merous; ovary 4-locular, placenta globose, septa thin-walled 24. Physocalymma – Flowers 6-merous; ovary 2-locular, placenta bipartite, septa thick at the ovary wall, thinning toward the center of the ovary, lunate 8. Diplusodon 20. Subshrubs, shrubs, or trees, 1–40 m 21 – Annual or perennial herbs, 2 cm–2 m, commonly less than 50 cm 24 21. Stamens 4; ﬂoral tube longitudinally 4-winged; apetalous 29. Tetrataxis – Stamens 8–many, ﬂoral tube wingless; petals 4–6 22 22. Stamens basiﬁxed; capsules indehiscent, 4-loculed 4. Crenea – Stamens dorsiﬁxed, capsules loculicidally or septifragally dehiscent, 2–6-loculed 23 23. Petals yellow; appendages of the epicalyx corniform, nearly as long as to longer than the sepals; ﬂowers solitary, sessile or subsessile in the axils; pedicels stout, 0–4 mm long 12. Heimia

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– Petals rose, purple, or white; appendages of the epicalyx corniform, or united to form an undulating ﬂange, or absent; ﬂowers solitary or several on axillary short shoots; pedicels slender, 10–40 mm long 11. Ginoria 24. Flowers 4-merous 25 – Flowers 6-merous 29 25. Capsules septicidally dehiscent, the wall microscopically transversely striated; ﬂowers solitary in the axils of the main stem or in lateral or terminal racemes 27. Rotala – Capsules indehiscent, irregularly splitting or initially circumscissile, then irregularly splitting, the wall smooth; ﬂowers solitary in the axils or in few- to many-ﬂowered axillary dichasia 26 26. Flowers solitary in the axils, broadly campanulate, apetalous; sepals 1/2 the length of the ﬂoral tube 7. Didiplis – Flowers (1–)3–many in the axils, campanulate to urceolate, petalous or apetalous; sepals 1/3 or less the length of the ﬂoral tube 27 27. Petals persistent in fruit; ovules (2–)5; seeds dark brown to black-violet, 1.5–2 mm long 13. Hionanthera – Petals caducous; ovules many; seeds 1 mm long or less, golden brown 28 28. Capsules irregularly splitting 2. Ammannia – Capsules initially circumscissile near the apex, then irregularly splitting below 20. Nesaea 29. Nectaries absent; ﬂowers 0.75–3 mm long including sepals 23. Peplis – Nectaries narrow to wide hypogynous rings; ﬂowers 4–14 mm long including sepals 19. Lythrum p.p. 30. Floral tube actinomorphic; ovary with two equal locules; capsules dehiscing from the apex 19. Lythrum p.p. – Floral tube slightly to distinctly zygomorphic, bilateral; ovary with the ventral (abaxial) locule reduced; capsules indehiscent, or dehiscing dorsally together with the ﬂoral tube by a longitudinal slit 31 31. Stamens attached near the base of the ﬂoral tube, anthers basiﬁxed; capsules indehiscent, the placenta and seeds retained within 25. Pleurophora – Stamens attached at midlevel or higher in the ﬂoral tube, anthers dorsiﬁxed; capsule dehiscing dorsally together with the ﬂoral tube by a longitudinal slit, the placenta and seeds ultimately exserted 5. Cuphea

Genera of Lythraceae 1. Adenaria Kunth Adenaria Kunth in Humboldt, Bonpland & Kunth, Nov. Gen. Sp. 6, ed. folio: 147 (1823); ed. qu.: 185 (1824).

Shrubs or small trees with slender, cernuous branches and distichous, lanceolate-oblong leaves; young stems, leaves, and ﬂowers clothed with glandular, orange or black punctae. Flowers in umbelliform cymes, 4(5)-merous, 3 mm long, weakly trimorphic and incipiently dioecious, sepals short; petals 4, white or light rose; stamens 8; ovary stipitate, 2-locular. Fruit indurate, indehiscent, globose. Seeds numerous, obovoid, c. 1 mm long.

x = 16. One species, A. ﬂoribunda Kunth, from Mexico to Argentina, in evergreen forests. Sister genus to Pehria. 2. Ammannia L.

Fig. 80

Ammannia L., Sp. Pl.: 119 (1753); Graham, J. Arnold Arb. 66:395–420 (1985), rev. of Western Hemisphere spp.

Glabrous annual herbs. Leaves sessile, linear to lanceolate or oblanceolate, the base clasping cordate or auriculate. Flowers in axillary cymes, 4(5)-merous, campanulate to urceolate, 1.5–5 mm long, with 4 pronounced ribs, sepals short; petals 0–4, purple, rose, or white; stamens (2)4(8), inserted at midlevel in the ﬂoral tube or lower; ovary 2–4-locular. Capsule dry, thin- and smoothwalled, irregularly splitting. Seeds many, obovoid, c. 1 mm long or less, an aerenchymatous ﬂoat on the concave surface. Circa 25 species, aquatic or marshinhabiting herbs of worldwide tropical to temperate distribution, especially Africa to Southeast Asia. Probably congeneric with Nesaea. Although placed in different tribes, only irregular capsule dehiscence in Ammannia vs. circumscissile followed by irregular dehiscence in Nesaea separates them. This distinction may not hold under closer scrutiny of all members. 3. Capuronia Lourteig Capuronia Lourteig, C. R. Hebd. Séances Acad. Sci. Paris 25a:1033 (1960).

Small glabrescent shrubs to 4 m, with brittle branchlets terminating in sturdy spines, terminal buds abortive. Leaves leathery, elliptic to ovate, the apex often with an abaxial, porate chamber. Flowers in inconspicuous axillary dichasia, cyathiform, 1–2 mm long, 6-merous, unisexual, sepals very short; petals white; stamens 6, deeply inserted at the nectariferous ring; ovary 4(5)-locular. Capsule globose, indehiscent, tightly enveloped by the persistent ﬂoral tube. Seeds 4–5, obovate, bilaterally strongly compressed, c. 3 mm. x = 8. One species, C. madagascariensis Lourteig, mesophytic and xerophytic regions of Madagascar. Closely related to Galpinia of East Africa. 4. Crenea Aubl. Crenea Aubl., Hist. Pl. Guiane: 523 (1775); Lourteig, Caldasia 15:121–142 (1986), rev.

Glabrous subshrubs to small trees, 1–4 m, with spathulate or lanceolate leaves. Flowers 1–5 in long-

Lythraceae

pedunculate, axillary dichasia, broadly campanulate, 4–6 mm long, 4-merous; sepals up to 1/2 the ﬂoral tube; petals cream-white; stamens 8 or 12–15, anthers basiﬁxed; ovary 4(5)-locular. Capsule globose, indehiscent, exceeding the persistent ﬂoral tube. Seeds many, narrowly elongated, compressed, c. 2 mm. x = 32. Two allopatric species, inhabiting sand and mud ﬂats, mangroves and estuaries of the Colombian and northern South American coasts. Close to Ginoria and Tetrataxis. 5. Cuphea P. Browne

Figs. 79A, 82D–F

Cuphea P. Browne, Civ. Nat. Hist. Jamaica: 216 (1756); Graham, Syst. Bot. Monogr. 20:1–168 (1988), 53:1–94 (1997), Syst. Bot. 14:43–76 (1989), rev. Mexic. spp.

Herbs or subshrubs, with diverse indumentum. Leaves opposite or verticillate, ﬁnely scabrous. Flowers in racemes or thyrses, 1 ﬂower always interpetiolar at a node, the others on axillary branchlets; ﬂoral tube cylindrical, bilateral, 12nerved, green, red or purple, zygomorphic, often spurred at base; sepals very short; petals 6(–0); stamens (6–)11; ovary subtended by a free-standing, unilateral nectary, 2-locular, the ventral locule

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reduced, septa ﬁliform. Capsule dry, thin-walled, dehiscing by a dorsal longitudinal slit together with dehiscence of the ﬂoral tube, the placenta and seeds ultimately exserted. Seeds 2–many, bilaterally compressed, orbicular to obovoid, 0.7–3 mm. x = 8. About 260 species, from the United States to Argentina and the Caribbean, primarily in the subtropics to tropics in open, mesophytic habitats. Sister to Pleurophora (Graham et al. 2006). 6. Decodon J.F. Gmel.

Fig. 82A, B

Decodon J.F. Gmel., Syst. Nat. 2:656, 677 (1791).

Glabrous to velutinous shrubs to 3 m, spreading by arching branches that root at the tips. Leaves decussate or verticillate, lanceolate. Flowers whorled at the nodes in short-pedunculate dichasia, campanulate, (4)5-merous, 4–8 mm long, heteromorphic, tristylic; appendages of the epicalyx c. 2× the length of the sepals; petals (4)5(–7), rose-purple; stamens (8)10, 2 lengths per ﬂower; ovary 3(4)-locular. Capsule globose, loculicidally dehiscent. Seeds 20–30, obpyramidal, 1.5–2 mm, the embryo surrounded by dense, small-celled aerenchyma. x = 16. One species, D. verticillatus (L.) Elliott, southeastern Canada and eastern United States but with a more extensive north-temperate fossil record; at lake margins and in other wet habitats. 7. Didiplis Raf. Didiplis Raf., Atlantic J.: 177 (1833).

Aquatic or amphibious herbs with thin, linear leaves truncate-based when submersed, tapering when emersed. Flowers minute, axillary, solitary, 4-merous, broadly campanulate; sepals broadly triangular, 1/2 of the ﬂoral tube; petals 0; stamens 2–4, deeply inserted; ovary 2-locular. Capsule globose, thin-walled, irregularly dehiscent. Seeds numerous, elongate, bilaterally compressed, abaxially convex, reaching 1 mm. x = 16. One species, D. diandra (DC.) A.W. Wood, endemic to eastern United States, frequenting ponds and shallow ephemeral waters. Based on nuclear ITS and atpB-rbcL intergeneric spacer data, Didiplis is sister to Rotala (J.A. Morris and S.A. Graham, unpubl. data). Fig. 82. Lythraceae. A, B Decodon verticillatus. A Branch. B Individual ﬂower minus petals. C Lythrum salicaria, ﬂoral diagram. D–F Cuphea teleandra. D Flowering shoot. E Side view of ﬂower. F Flower opened out, ovary and nectary removed. (Orig.)

8. Diplusodon Pohl Diplusodon Pohl, Flora 10:150 (1827); Cavalcanti, Ph.D. Diss., Univ. São Paulo (1995), rev.

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S.A. Graham

Glabrous or pubescent subshrubs or shrubs. Leaves of diverse textures, venation patterns, and indumentum. Flowers in thyrses, racemes, cymes, or solitary, obconic to oblong, 6-merous; sepals short, erect or spreading; petals 6, showy; stamens (6–)12–38; ovary 2-locular, the placenta bipartite, the septa lunate and overlapping. Capsule dry, septicidally dehiscent. Seeds 6–60, bilaterally compressed, circular-winged, c. 2–3 mm. x = 15. Circa 70 species, endemic to Brazil, except for 1 Bolivian species; especially well represented in Minas Gerais and Goias, in campos cerrados, campos rupestres and margins of gallery forests.

9. Duabanga Buch.-Ham.

Fig. 83

Duabanga Buch.-Ham., Trans. Linn. Soc. London 17:177 (1837); Jayaweera, J. Arnold Arb. 48:89–100 (1967), rev.

Tall trees with pendulous branches, glabrous or glabrescent, the leaves with a prominent intramarginal vein. Flowers in terminal corymbiform panicles, 4–6(–8)-merous, 2–2.5 cm long, funnel-or cup-shaped, sepals spreading in fruit; petals yellowish or greenish white; stamens 12–50, uniseriate on a circular rim around the ovary or biseriate; ovary half-inferior, locules 4–9. Fruit a loculicidally dehiscent, thick-walled capsule. Seeds many, fragile, 2-tailed, 4 mm. x = 24. Two species and putative hybrid, Southeast Asia and Malaysia and Java, Borneo, the Philippine islands, Celebes, Moluccas, and New Guinea; early successional trees of subtropical humid forests and primary forests. Sister to Lagerstroemia. 10. Galpinia N.E. Br. Galpinia N.E. Br., Bull. Misc. Inform. 1894:345 (1894).

Small trees to 7 m, glabrous. Leaves subcoriaceous with a subterminal, abaxial, porate chamber. Flowers many, small, clustered in large terminal panicles; ﬂoral tube campanulate, (5)6-merous; sepals 1/3 of the ﬂoral tube; petals 6, white; stamens 6, antepetalous, encircling the nectary at the base of the ovary; ovary depressed apically, 2-locular, the placenta globose. Capsule dry, thin-walled, splitting irregularly. Seeds 3–10, bilaterally compressed, circular-winged, c. 2.5 mm. x = 8. One species, G. transvaalica N.E. Br., Zimbabwe, Mozambique, and eastern South Africa in the Transvaal, Swaziland, Zululand, and Natal; woods, thickets, savannas. Sister to Capuronia. 11. Ginoria Jacq. Ginoria Jacq., Enum. Pl. Carib.: 5 (1760); S. Graham, (in prep.), rev. Haitia Urb. (1919).

Fig. 83. Lythraceae. Duabanga grandiﬂora. A Inﬂorescence and leaf. B Flower. C Petal. D Dehiscing fruit. E Seed. F Fivemerous ﬂoral tube. G Four-merous ﬂoral tube. (Jayaweera 1967)

Glabrous shrubs or trees, young stems prominently buttressed at the nodes, terminal buds of the lateral branches abortive or caducous, nodal spines in some spp. Leaves membranous to coriaceous, with a prominent intramarginal vein or the intramarginal vein forming the leaf margin. Flowers in axillary few-ﬂowered short shoots, in umbelliform clusters, or solitary, 4-or 6-merous,

Lythraceae

campanulate to cupuliform; sepals to 1/2 the ﬂoral tube; appendages of the epicalyx corniform, or united in an undulating ﬂange at the base of the sepals, or absent; petals 4 or 6, pale to intense rose; stamens (8–)12–28(–55), deeply inserted, connate or not; ovary (2–)3–6-locular, placenta subglobose. Capsule dry, septifragal. Seeds many, obovoid to fusiform, c. 1 mm. x = 28. Caribbean with 13 species: Mexico (1), Cuba (6), Hispaniola (5), Puerto Rico and Virgin Islands (1); stream margins, dry forests, serpentine and limestone habitats. 12. Heimia Link Heimia Link, Enum. Horti Berol. 2:3 (1822); Link in Link & Otto, Ic. Pl. Select.: 63 (1822).

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Slender shrubs producing a strong, skunk-like odor. Leaves glandular black-punctate, abaxially densely tomentose. Flowers solitary (rarely 2), axillary, pubescent and glandular black-punctate, campanulate, (5)6-merous; sepals short, strongly reﬂexed; petals 6, rose-purple, showy; stamens (16–)18(–20), antesepalous stamens paired, antepetalous stamens single and inserted higher in tube; ovary stipitate, globose, 2- or 3-locular. Capsule dry, thin-walled, septifragally dehiscent. Seeds many, cuneate-compressed, c. 2 mm. x = 24. One species, K. madagascariensis S.A. Graham, H. Tobe & P. Baas, endemic to the southern half of Madagascar, in semi-arid savannas. Sister genus to Woodfordia.

Slender-stemmed, glabrous shrubs with lanceolate-linear leaves. Flowers sessile or subsessile, axillary, solitary, (5)6-merous, campanulate to turbinate; sepals to 1/2 the ﬂoral tube, alternating with prominent corniform epicalyx appendages; petals 6, yellow; stamens (10)12(–22), deeply inserted; ovary 4-locular. Capsule dry, globose, loculicidally dehiscent. Seeds many, oblong, c. 1 mm. x = 8. Three very similar species, New World, lower montane slopes, stream margins and other wet places, H. salicifolia Link distributed from Texas to Argentina. Sister to Rotala. 13. Hionanthera A. Fern. Hionanthera A. Fern. & Diniz, Bol. Soc. Brot. II, 29:90 (1955).

Grass-like herbs to 50 cm with sessile, long, narrowly linear leaves. Flowers in few- to manyﬂowered axillary cymes, enveloped by subtending leaf bases, (3)4(5)-merous; campanulate or urceolate, conspicuously 4-nerved; sepals short; petals persistent, violet; stamens 4, antesepalous, deeply inserted; anthers and pollen deep violet; ovary sessile or shortly stipitate, incompletely 2-locular. Capsule thin-walled, irregularly dehiscent. Seeds 2–5, oblong, bilaterally compressed, brown or black-violet, 1.5–2 mm. One or 2 species, southern Tanzania, Mozambique, and Zimbabwe, inhabiting small pools in granite rocks in grasslands. Close to Ammannia and Nesaea. 14. Koehneria S.A. Graham, H. Tobe & P. Baas Koehneria S.A. Graham, H. Tobe & P. Baas, Ann. Missouri Bot. Gard. 73:805 (1986).

Fig. 84. Lythraceae. Lafoensia punicifolia. A Branch. B Detail of branch at node. C Abaxial side of leaf tip with porate chamber. D Flower bud, longitudinal section. E Anther. (Lourteig 1986)

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15. Lafoensia Vand.

S.A. Graham

Fig. 84

Lafoensia Vand., Fl. Lusit. Brasil.: 33 (1788); Lourteig, Mem. Soc. Ci. Nat. La Salle 45:115–157 (1986), rev.

Glabrous shrubs or trees, the leaves with subapical, abaxial porate chamber. Flowers in terminal racemes or thyrses, large, showy, (8–)10–12(–16)merous, the ﬂoral tube coriaceous, thick, distally pleated, caducous; sepals very short; petals 10–12, cream to white; stamens (11–)20–24(–40), uniseriate, long ﬁlaments and style well-exserted; ovary stipitate, vestigially 2-locular, appearing unilocular. Capsule woody, loculicidally dehiscent, 2–4valved. Seeds numerous, bilaterally compressed, oblong, circular-winged, 8–35 mm. x = 8. Five or six species, southern Mexico to southern Brazil; montane forests and cerrados. The heavy wood of all species is utilized in local construction; L. acuminata DC. in Ecuador is a valuable timber tree. The wood and leaves of the genus provide a yellow dye. The only New World member in a clade of Afro-Asian genera, as sister to Galpinia and Capuronia. 16. Lagerstroemia L.

Fig. 85

Lagerstroemia L., Syst. Nat. ed. 10, 2:1068, 1076, 1372 (1759); Furtado and Srisuko, Gard. Bull. (Singapore) 24:185–334 (1969), rev. Orias Dode (1909).

Shrubs or trees, glabrous or variously indumented, the leaves subalternate to opposite. Flowers in axillary or terminal panicles, 6-merous, semi-globose to pyriform, superﬁcially or deeply ridged; sepals short; petals 6–12, clawed, crumpled, rose, purple, or white; stamens dimorphic in most species, 6 antesepalous with thickened ﬁlaments and large anthers, 12–c. 200 antepetalous with thin ﬁlaments and smaller anthers inserted singly or in clusters; ovary (3–)6-locular. Capsule indurated, 4–6valved, loculicidally dehiscent. Seeds numerous, obpyramidal, unilaterally winged from the raphe, 8–10 mm incl. wing; cotyledons rolled. x = 24. About 56 species, India, China, Southeast Asia, Malesia, New Guinea, northern Australia, Japan; riverine forests, montane and secondary forests. Sister to Duabanga. 17. Lawsonia L. Lawsonia L., Sp. Pl.: 349 (1753).

Small glabrous shrubs, branches stifﬂy divaricate, often terminating in a rigid spine. Flowers in terminal or axillary panicles, fragrant, broadly cam-

Fig. 85. Lythraceae. Lagerstroemia speciosa. A, B Flowering branch. C Flower, opened out. D Dehiscing fruit. E Seed. (Koorders and Valeton 1918)

panulate, 4-merous; sepals 1/2 or more of the ﬂoral tube, spreading; petals white to cream; stamens 8, paired opposite the sepals; ovary superior, (2–)4-locular. Capsule globose, indurate, indehiscent. Seeds many, obpyramidal, the broad apex ﬁlled with dense, small-celled aerenchyma, 2 mm. n = 12, 15, 16, 17, 18. One species, L. inermis L., of East African or Eurasian origin, widely cultivated for centuries in warm climates as an ornamental and for henna dye. In a clade with Ammannia/Nesaea, Tetrataxis, and Ginoria. 18. Lourtella S.A. Graham, P. Baas & H. Tobe Lourtella S.A. Graham, P. Baas & H. Tobe, Syst. Bot. 12:519 (1987).

Shrubs to 4 m, pith enclosing a large central secretory duct, branches stifﬂy divaricate, the youngest bilaterally compressed, bearing multicellular, spinulose, globose hairs; young stems and leaves resin-coated. Leaves subcoriaceous, translucentpunctate. Flowers in axillary, 3-ﬂowered cymes, campanulate, 4-merous; sepals short, broad; petals white; stamens (4)8(12), deeply inserted, included;

Lythraceae

ovary incompletely 2-locular. Capsule thin-walled, irregularly dehiscent. Seeds c. 50, obpyramidal, 1 mm. One species, L. resinosa S.A. Graham, P. Baas & H. Tobe, northern Peru and disjunctly in southern Bolivia, in dry open deciduous woods with cacti. Relationships unknown. 19. Lythrum L.

Fig. 82C

Lythrum L., Sp. Pl.: 446 (1753).

Herbs or small shrubs with opposite, alternate or verticillate leaves. Flowers in terminal spikes or racemes, 6-merous, mono-, di-, or tristylous; ﬂoral tube twice as long as wide to scarcely longer than wide (in species sometimes included in Peplis), 8– 12-nerved; sepals very short, appendages of the epicalyx sometimes more conspicuous than the sepals; petals 6, purple, rose, or white; stamens 6 or 12, in 1 or 2 whorls, complementing style lengths; ovary 2-locular, encircled by a basal nectary. Capsule dry, septicidally or septifragrally dehiscent, 4-valved. Seeds many, elongate, bilaterally compressed, abaxially convex, c. 1 mm. x = 5. About 35 species of wet places, nearly worldwide distribution especially in temperate Europe, Asia, and North America. Sometimes including one or more species of Peplis in synonymy. 20. Nesaea Comm. ex Kunth Nesaea Comm. ex Kunth in Humboldt, Bonpland & Kunth, Nov. Gen. Sp. 6, ed. folio: 151 (1823); ed. qu.: 191 (1824), nom. cons.

Herbs, rarely subshrubs. Flowers solitary or in loose to dense axillary cymes or in capitulae subtended by enveloping prophylls, 4–8-merous, mono-, di-, or tristylous, campanulate to turbinate, 8(16)-ribbed; sepals short; petals 0–8, purple, rose, or white; stamens 4–27, in 1 or 2 whorls, inserted midlevel or deeper in the ﬂoral tube; ovary 2–4(5)locular. Capsule dry, thin-walled, circumscissile near the apex, then irregularly splitting below. Seeds many, abaxially convex, c. 1 mm. About 55 species, primarily African-Asian but also with North American and Australian representatives, in wet places. Probably congeneric with Ammannia. 21. Pehria Sprague

Flowers in subterminal, axillary, loose cymose clusters of 2–15, cyathiform, deep red, 4(5)-merous; sepals very short; petals 4, rose-red; stamens 8, exserted; ovary stipitate, 2-locular. Capsule subglobose, thin-walled, loculicidally dehiscent, the 2 valves bilobed. Seeds many, narrowly obovate to oblong, abaxially convex, c. 1 mm. x = 16. One species, P. compacta (Rusby) Sprague, Honduras, Nicaragua, Venezuela, Colombia, in secondary vegetation, pastures, roadsides, margins of forests at low to mid-elevations. Sister to Adenaria. 22. Pemphis J.R. Forst. & G. Forst. Pemphis J.R. Forst. & G. Forst., Charact. Gen.: 67, pl. 34, Fig. a–i, k (1776).

Shrubs to densely branched, spreading trees, the stems, leaves and ﬂowers covered by silky, appressed hairs. Flowers solitary or paired, fragrant, turbinate, 6-merous, 12-ribbed, distylic; sepals very short; petals white; stamens 12, deeply inserted, alternately unequal; ovary vestigially 3–4-locular, appearing 1-locular with free-central placentation. Capsule dry, circumscissile. Seeds c. 20, irregularly obpyramidal, dense small-celled aerenchyma within, 3 mm. x = 16. One species, P. acidula J.R. Forst. & G. Forst., Indian and Paciﬁc oceans from shores of East Africa west to the Marshall Islands and north to the Ryukyu Islands, as solitary shrubs or thickets along inlets and on shores. Closely related to Punica. 23. Peplis L. Peplis L., Sp. Pl.: 332 (1753).

Annual herbs, decumbent or creeping and adventitiously rooting at the nodes. Leaves opposite or subalternate, membranous or slightly succulent. Flowers solitary or less often paired, (5)6-merous, broadly campanulate, wider than long; sepals short; petals 0 or 6, purple; stamens 2 or (5)6, deeply inserted, style none or very short; ovary 2-locular. Capsule dry, thin-walled, indehiscent, irregularly splitting. Seeds numerous, obovoid, convex-concave, reaching 1 mm. x = 5. One to three species, western Europe to Russia, in wet places. Arguably distinct from Lythrum (Webb 1967; Graham et al. 1993a).

Pehria Sprague, J. Bot. 61:238 (1923).

Shrubs or small trees, stems often ﬂushed wine-red, puberulent, and globose, glandular, black punctate.

241

24. Physocalymma Pohl Physocalymma Pohl, Flora 10:152 (1827).

242

S.A. Graham

Trees, with strongly divaricate, subopposite, 4-angled branches. Flowers produced before the leaves, in racemes or thyrses, enclosed by caducous, paired bracts, 8-merous, globose-campanulate; sepals 8; petals 8, lilac or rose, showy; stamens 24, deeply inserted in a single whorl; ovary slightly inferior, 4-locular, the placenta appearing free-central. Capsule thin-walled, dehiscent, surrounded by the inﬂated persistent ﬂoral tube. Seeds numerous, bilaterally compressed, circular-winged, 4 mm. x = 8. One species, P. scaberrimum Pohl, central South America, in dry forests and savannas. Relationships unknown. 25. Pleurophora D. Don Pleurophora D. Don, Edinburgh New Philos. J. 12:112 (1837).

Herbs to 1 m, indumentum of unicellular eglandular and multicellular glandular hairs. Leaves appearing uni-nerved, terminating in a sharp, indurated apex in some species. Flowers in terminal racemes or spiciform heads, 6-merous, zygomorphic, slightly bilateral; sepals very short; petals 4 or 6, purple, rose, or white; stamens 6(7) or 11, deeply inserted, uniseriate, anthers basiﬁxed; ovary subtended by a circular nectary, 2-locular, the ventral locule reduced. Fruit indehiscent. Seeds numerous, bilaterally compressed, obovate, reaching 1 mm. x = 7. South American, Seven–10 species in South America, 3–6 with reduced spiny parts in arid regions of Chile and Argentina. Sister to Cuphea (Graham et al. 2006).

smaller ﬂowers and fruits, and a 3-locular, semiinferior ovary. Related to Pemphis. 27. Rotala L.

Fig. 86

Rotala L., Mant.: 143, 175 (1771); C.D.K. Cook, Boissiera 29:1–156 (1979), rev.

Glabrous, aquatic, amphibious, or terrestrial herbs with decussate or verticillate leaves. Flowers racemose, or rarely in multi-ﬂowered axillary clusters, 3–6-merous, monomorphic or distylous, urceolate to campanulate; sepals short; petals 0–6; stamens (1–)4(–6), inserted at midlevel or lower in the ﬂoral tube; ovary 2–4-locular. Capsule dry, septicidally dehiscent, the wall microscopically transversely striated. Seeds few-numerous, obovoid, large-celled exotestal ﬂoat tissue on the concave surface, c. 1 mm or less. About 45 species,

26. Punica L. Punica L., Sp. Pl.: 472 (1753).

Glabrous shrubs or small trees, branches often terminating as spines. Leaves small, shining. Flowers solitary, terminal or 1–5 in axillary clusters or terminal, campanulate, leathery, red or yellow, 2–3 cm long; sepals 5–8, persistent; petals showy, crumpled, red or white; stamens many, covering the inner �