Frugivores and Seed Dispersal Tasks for Vegetation Science 15

Frugivores and seed dispersal Tasks for vegetation science 15

Series Editors

HELMUT LIETH HAROLD A. MOONEY

University of Osnabriick, F.R. G. Stanford University, Stanford, Calif., U.S.A.

1 Box, E.O. Macroclimate and Plant Forms. An introduction to predictive modelling in phytogeography. ISBN 90 6193 941 0 2 Navin Sen, D. & Singh Rajpurohit, K. Contributions to the Ecology of Halophytes. ISBN 90 61939429 3 Ross, 1. The Radiation Regime and Architecture of Plant Stands. ISBN 90 6193 607 1 4 Margaris, N.S. & Mooney, H.A. (eds) Components ofProductivity ofMediterranean - Climate, Regions. ISBN 90 6193 944 5 5 Muller, M.l. Selected Climatic Data for a Global Set of Standard Stations for Vegetation Science. ISBN 90 6193 945 3 6 Roth, I. Stratification in Tropical Forests as Seen in Leaf Structure. ISBN 90 6193 946 1 7 Steubing, L. & lager, H.l. Monitoring of Air Pollutants by Plants: Methods and Problems. ISBN 90 6193947 X 8 Teas, H.l. Biology and Ecology of Mangroves. ISBN 90 6193948 8 9 Teas, H.l. Physiology and Management of Mangroves. ISBN 90 6193 9496 10 Feoli, E., Lagonegro, M. & Orl6ci, L. Information Analysis of Vegetation Data. ISBN 90 6193 950 X 11 Sestak, Z. (ed) Photosynthesis during Leaf Development. ISBN 90 6193 951 8 12 Medina, E., Mooney, H.A. & Vazquez-Yanes, c. (eds) Physiological Ecology ofPlants ofthe Wet Tropics. ISBN 90 6193 9526 13 Margaris, N.S., Arianoustou-Faraggitaki, M. & Oech~~l.. W:~. !eds) Being Alive on Land. ISBN 90 6193 953 4 '.' .•) ;"',~'. 14 Hall, D.O., Myers, N. & Margaris, N.S. (eds) Economics ofEcosystems Management. ISBN 9061935059 15 Estrada, A. & Fleming, T.H. (eds) Frugivores and Seed Dispersal. ISBN 90 6193543 1 16 Dell, B., Hopkins, A.l.M. & Lamont, B.B. (eds) Resilience in Mediterranean-type Ecosystems. ISBN 90 61935792 Frugivores and seed dispersal

edited by

ALEJANDRO ESTRADA and THEODORE H. FLEMING

1986 DR W. JUNK PUBLISHERS ... a member of the KLUWER ACADEMIC PUBLISHERS GROUP " DORDRECHT I BOSTON I LANCASTER Distributors for the United States and Canada: Kluwer Academic Publishers, 190 Old Derby Street, Hingham, MA 02043, USA for the UK and Ireland: Kluwer Academic Publishers, MTP Press Limited, Falcon House, Queen Square, Lancaster LA1 1RN, UK for all other countries: Kluwer Academic Publishers Group, Distribution Center, P.O. Box 322, 3300 AH Dordrecht, The Netherlands

Library of Congress Cataloging in Publication Data

Main entry under tItLe:

Frugivores and seed dispersal.

(Tasks for vegetation science j 15) Includes index. 1. Seeds--Dispersal--Congresses. 2. Frugivores-• Food--Congresses. 3. Forest ecology--Congresses. 4. Adaptation (Biology)--Congresses. I. Estrada, Alejandro. II. Fleming, Theodore H. Ill. Series. QK929.F78 1986 582' .0524 85-24103 ISBN-13: 978-94-0 I 0-8633-2 e-ISBN-13: 978-94-009-4812-9 001: 10.1007/978-94-009-4812-9

Cover design: Max Velthuijs Copyright

All rights reserved. No part of this publication may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, mechanical, photocopying, recording, or otherwise, without the prior written permission of the publishers, Dr W. Junk Publishers, P.O. Box 163, 3300 AD Dordrecht, The Netherlands. v Table of contents

Acknowledgements IX

General introduction XI

Part 1: Plant strategies

Introduction 3 1. Carlos M. Herrera. Vertebrate-dispersed plants: why they don't behave the way they should 5 2. Nathaniel T. Wheelwright. A seven-year study of individual variation in fruit production in tropical bird-dispersed tree species in the family Lauraceae 21 3. Julie S. Denslow, Timothy C. Moermond and Douglas J. Levey. Spatial components of fruit display in understory trees and shrubs 37 4. Edmund W. Stiles and Douglas W. White. Seed deposition patterns: influences of season, nutrients, and vegetation structure 45 5. Mary F. Willson and William G. Hoppes. Foliar 'flags' for avian frugivores: signal or serendipity? 55 6. Carlos Vazquez-Yanes and Alma Orozco-Segovia. Dispersal of seeds by animals: effect on light- controlled dormancy in Cecropia obtusifolia 71

Part 2: Frugivore strategies

Introduction 81 7. Charles H. Janson, Edmund W. Stiles and Douglas W. White. Selection on plant fruiting traits by brown capuchin monkeys: a multivariate approach 83 8. Alejandro Estrada and Rosamond Coates-Estrada. Frugivory in howling monkeys (Alouatta palliata) at Los Tuxtlas, Mexico: dispersal and fate of seeds 93 9. Theodore H. Fleming. Opportunism versus specialization: the evolution of feeding strategies in frugivorous bats 105 10. Pierre Charles-Dominique. Inter-relations between frugivorous vertebrates and pioneer plants: Cecropia, birds and bats in French Guyana 119 11. Timothy C. Moermond, Julie S. Denslow, Douglas J. Levey and Eduardo Santana C. The influence of morphology on fruit choice in neotropical birds 137 12. Douglas J. Levey. Methods of seed processing by birds and seed deposition patterns 147 VI

13. David W. Snow and Barbara K. Snow. Some aspects of avian frugivory in a north temperate area relevant to tropical forest 159

Part 3: The consequences of seed dispersal

Introduction 167 14. Carol C. Horvitz and Douglas W. Schemske. Seed dispersal and environmental heterogeneity in a neotropical herb: a model of population and patch dynamics 169 15. K. Greg Murray. Consequences of seed dispersal for gap-dependent plants: relationships between seed shadows, germination requirements, and forest dynamic processes 187 16. E. Raymond Heithaus. Seed dispersal mutualism and the population density of Asarum cana- dense, an ant-dispersed plant 199 17. J.L. Hamrick and M.D. Loveless. The influence of seed dispersal mechanisms on the genetic structure of plant populations 211 18. Martin A. Stapanian. Seed dispersal by birds and squirrels in the deciduous forests of the United States 225 19. Rodolfo Dirzo and Cesar A. Dominguez. Seed shadows, seed predation and the advantages of dispersal 237 20. Daniel H. Janzen. Mice, big mammals, and seeds: it matters who defecates what where 251 2l. Mario Gonzalez-Espinosa and Pedro F. Quintana-Ascencio. Seed predation and dispersal in a dominant desert plant: Opuntia, ants, birds, and mammals 273 22. W. Hallwachs. Agoutis (Dasyprocta punctata), the inheritors of guapinol (Hymenaea courbaril: Leguminosae) 285

Part 4: Community aspects of frugivory and seed dispersal

Introduction 307 23. William J. Platt and Sharon M. Hermann. Relationships between dispersal syndrome and characteristics of populations of trees in a subtropical forest 309 24. Nicholas V.L. Brokaw. Seed dispersal, gap colonization, and the case of Cecropia insignis 323 25. Miguel Martinez-Ramos and Elena Alvarez-Bullya. Seed dispersal, gap dynamics and tree recruitment: the case of Cecropia obtusifolia at Los Tuxtlas, Mexico 333 26. Nancy C. Garwood. Constraints on the timing of seed germination in a tropical forest 347 27. Robin B. Foster, Javier Arce B. and Tatzyana S. Wachter. Dispersal and the sequential plant communities in Amazonian Peru floodplain 357 28. John Terborgh. Community aspects of frugivory in tropical forests 371

Index 385 VII

We dedicate this book to Barbara and David Snow in recognition of their pioneering contributions to the study of tropical frugivores and seed dispersal. IX Acknowledgements

This book is the product of a symposium-workshop held at the Los Tuxtlas Biological Station, Veracruz, Mexico, in June 1985. The conference was sponsored by funds from the Consejo Nacional de Technologia de Mexico, the Instituto de Biologia, and the Direccion General de Asuntos del Personal Academico of the Universidad Nacional Autonoma de Mexico. We thank Dr. Jose Sarukhan, Director of the Instituto de Biologia, for encouraging us to conduct the conference at Los Tuxtlas. We are grateful to the staff of the Station for providing the necessary logistical support with tireless enthusiasm. We especially thank Rosa• mond Coates- Estrada for taking care of numerous details before, during, and after the four day conference. XI General introduction

A. ESTRADA and T. FLEMING

Our goal in this Introduction is to briefly review the conceptual history of the fruit-frugivore seed dispersal mutualism and to point out currently important research areas. At the beginning of each of the four sections into which this book is divided, we will provide a brief overview of the major points of each chapter and will highlight what we believe to be the new ideas and insights that emerge from these papers. The focus of the Los Tuxtlas conference and the subject matter of this book - ecological and evolutionary interactions between frugivorous animals and their food plants - has been of long-standing interest to mankind. Primitive man surely was familiar with the feeding habits of many species of fruit-eating animals and used this knowledge to guide his own search for food. The domestication of a wide variety of tropical, subtropical, and temperate fruit species has had a long history. But the scientific study of fruits, frugivores, and seed dispersal from an ecological and an evolutionary perspective is relatively new an_d can be dated from the publication in 1930 of H. N. Ridley's classic volume on seed dispersal mechanisms around the world. Except for Salisbury's (1942) pioneering analysis of the reproductive strategies of British plants, however, the intellectual seeds sown by Ridley lay dormant for nearly 30 years. This dormancy was broken in the late 1950s by two events. The first was the publication of van der Pijl's descriptive book on seed dispersal mechanisms, which has since undergone three revisions but remains largely non-theoretical in its approach. The second was the fieldwork of Barbara and David Snow on the frugivorous birds of Trinidad. The history of this work is recounted in D. Snow's (1976) book entitled 'The Web of Interactions.' In addition to providing detailed information about the importance of frugivory in the lives of a wide array of tropical birds, the Snow's work on Trinidad and elsewhere in the neotropics produced two important conceptual advances in this field: (1) in 1965 David Snow suggested an evolutionary explana• tion for the apparently displaced fruiting periods of sympatric members of the genus Miconia (Melastoma• taceae) and (2) in 1971 he proposed that there exists a basic dichotomy between generalist and specialist frugivores that coincides with differences in the nutritional quality of the fruits which they eat. This latter idea gave rise to two other important conceptual contributions in the 1970s, namely McKey's (1975) insightful review of the coevolution of fruits and frugivores in which he elaborated upon Snow's generalist-specialist dichotomy and Howe and Estabrook's (1977) discussion of the evolution of fruit crop size and fruiting behavior in response to avian frugivore food choices and foraging behavior. Both of these papers stimulated a quantum increase in studies of avian (and other vertebrate) frugivory, but until recently, most of these studies have paid little attention to the fate of the seeds ingested by birds and other animals. The fate of dispersed seeds and the role of granivorous animals in shaping 'seed shadows' (which actually is an inappropriate analogy because 'shadow' means lack of light) was brought into clear focus by Daniel Janzen in three seminal publications (Janzen, 1969, 1970 and 1971). Much of Janzen's work has dealt with XII documenting levels of pre- and post-dispersal seed predation suffered by large-seeded plants of the Legumi• nosae. Since the mid-1970s, however, his research has expanded to include the fate of seeds of fleshy-fruited plants. Early conceptual treatments of the evolution of fruits and frugivores assumed that plant and animal traits w~re the products of coevolution. For example, McKey (1975) hypothesized that the protein- and lipid-rich pulp of certain kinds of fruit evolved to meet the nutritional needs of certain reliable, specialized (avian) frugivores that provided high quality dispersal services to their food plants by treating seeds in a predictably gentle fashion and by depositing them in suitable germination sites. Current thinking, however, downplays the idea that the frugivory mutualism involves one-on-one coevolution between plants and animals. Instead, current theory stresses the diffuse nature of this interaction for reasons discussed by Wheelwright and Orians (1982), Howe (1984), and Herrera (1985, this volume). These and other authors have pointed out that evolutionary interactions between fruits and their legitimate frugivores can be weakened by a variety of counter-pressures, including non-legitimate frugivores (e.g. insects, granivorous vertebrates, fungi), poh lination and breeding systems, seed germination requirements, and the stochastic nature of the availability of 'safe sites'. Furthermore, phylogenetic inertia in fruit and seed traits seems to be much stronger in some groups of plants than in others. This inertia provides prima facie evidence against ongoing coevolution between plants and their current frugivores. Discovering possible reasons for why some groups of plants are evolutionarily less plastic than others will be a major contribution to our understanding of the process of adaptation. Forest dynamics and the role played by gap formation in affecting seed dispersal success has recently come under intensive study. Gaps are crucial for successful recruitment of new plants in both shade-tolerant and shade-intolerant species. Gap formation appears to be more predictable in time than in space. This suggests that plant phenology should be sensitive to the temporal aspects of gap formation but that plants should basically playa 'crap game' regarding the spatial dissemination of their seeds. That is, both large- and small• seeded plants should disperse as many seeds as widely as possible to maximize the probability of encounter• ing an actual or incipient gap. Plant demography is the mechanism through which frugivory and dispersal ultimately influence the evolution of plant traits. Mortality rates of seeds and seedlings are high in all plants. To the extent that it influences survival probabilities of these key life stages, dispersal will have a major selective impact on the adaptations of plants. Workers are just beginning to investigate the mortality consequences of different temporal and spatial patterns of dispersal. We can expect to see much more of this work in the future as a logical follow-up to the descriptive phases of seed dispersal mechanisms. The above studies, when coupled with genetic studies using biochemical techniques, will provide much new information about the genetic consequences of different seed dispersal patterns. With the right study system, it will be possible to estimate the relative reproductive success of males and females in plant populations and to forge a link between flower, fruit, and seed characteristics and reproductive success. The completion of this link will require intensive and extensive work, but the rewards of this labor will be great because this type of research will ultimately provide us with deep insights into the adaptive significance of intra- and inter-specific variation in seed dispersal mechanisms. To the extent that the Los Tuxtlas con• ference has helped us to more rapidly attain this goal, it will be viewed as a resounding success. As is evident from the papers in this volume, rapid progress is being made in understanding the role played by frugivory and seed dispersal in the demography of plants and in the dynamics of forests, particularly those in tropical regions. This research, however, is in a desperate race against time. At a rate of 2-3% per year, tropical forest destruction is occurring faster than is our understanding of how to manage these complex ecosystems so as to minimize rates of species extinctions. Although most of the papers in this volume deal with the basic or esoteric side of the fruit-frugivore interaction, it should be evident that such studies have important practical implications regarding the conservation of habitats and species interactions. Among XIII other things, these studies suggest that the continued existence of tropical forests whose primates and frugivorous birds and bats have been shot out or otherwise persecuted by native hunters is just as precarious as if their trees had been chain-sawed and bulldozed by lumber companies or cattle ranchers.

Literature cited Gilbert and P.H. Raven), pp. 159-191. Univ. of Texas Press, Austin. Herrera, C.M. 1985. Determinants of plant-animal coevolution: Pijl, L. van der. 1957. Seed dispersal mechanisms. Springer• the case of mutualistic dispersal of seeds by vertebrates. Verlag, Berlin. Oikos 44: 132-141. Ridley, H.N. 1930. The dispersal of plants throughout the Howe, H.F. 1984. Constraints on the evolution of mutualisms. world. Reeve, Ashford. Am. Nat. 123: 764-777. Salisbury, E.J. 1942. The reproductive capacity of plants. Bell, Howe, H.F. and F.F. Estabrook. 1977. On interspecific compe• London. tition for avian dispersers in tropical trces. Am. Nat. 111: 817- Snow, D. W. 1965. A possible selective factor in the evolution of 832. fruiting seasons in tropica1 forest. Oikos 15: 274-281. Janzen, D.H. 1969. Seed eaters versus seed size, number, tox• Snow, D.W. 1971. Evolutionary aspects of fruit-eating by birds. icity and dispersal. Evolution 23: 1-27. Ibis 113: 194-202. Janzen, D.H. 1970. Herbivores and the number of tree species Snow, D.W. 1976. The web of interactions. Collins, London. in tropical forests. Am. Nat. 104: 501-528. Wheelwright, N.T. and G.H. Orians. 1982. Seed dispersal by Janzen, D.H. 1971. Seed predation by animals. Ann. Rev. Ecol. animals: contrasts with pollen dispersal, problems of termi• Syst. 2: 465-492. nology, and constraints on coevolution. Am. Nat. 119: 402- McKey, D. 1975. The ecology of coevolved seed dispersal sys• 413. tems. In: Coevolution of animals and plants (eds. L.E.