ARTHROPODS OF TROPICAL FORESTS. Edited by: Yves Basset Smithsonian Tropical Research Institute, Panama City, Republic of Panama

Transcription

1 ARTHROPODS OF TROPICAL FORESTS Spatio-temporal Dynamics and Resource Use in the Canopy Edited by: Yves Basset Smithsonian Tropical Research Institute, Panama City, Republic of Panama Vojtech Novotny Czech Academy of Sciences and University of South Bohemia, Ceske Budejovice, Czech Republic Scott E. Miller National Museum of Natural History, Smithsonian Institution, Washington DC, USA and Roger L. Kitching Griffith University, Brisbane, Australia

2 PUBLISHED BY THE PRESS SYNDICATE OF THE UNIVERSITY OF CAMBRIDGE The Pitt Building, Trumpington Street, Cambridge, United Kingdom CAMBRIDGE UNIVERSITY PRESS The Edinburgh Building, Cambridge CB2 2RU, UK 40 West 20th Street, NewYork, NY , USA 477 Williamstown Road, Port Melbourne, VIC 3207, Australia Ruiz de Alarcón 13, Madrid, Spain Dock House, The Waterfront, Cape Town 8001, South Africa C Cambridge University Press 2003 This book is in copyright. Subject to statutory exception and to the provisions of relevant collective licensing agreements, no reproduction of any part may take place without the written permission of Cambridge University Press. First published 2003 Printed in the United Kingdom at the University Press, Cambridge Typeface Ehrhardt MT 9.5/12 pt System L A TEX2ε [TB] A catalogue record for this book is available from the British Library Library of Congress Cataloguing in Publication data Arthropods of tropical forests : spatio-temporal dynamics and resource use in the canopy / edited by Yves Basset... [et al.]. p. cm. Includes bibliographical references (p. ). ISBN (hb) 1. Arthropoda Ecology Tropics. 2. Forest canopy ecology Tropics. I. Basset, Yves, 1960 QL434.6.A dc ISBN hardback The publisher has used its best endeavours to ensure that the URLs for external websites referred to in this book are correct and active at the time of going to press. However, the publisher has no responsibility for the websites and can make no guarantee that a site will remain live or that the content is or will remain appropriate.

3 Contents List of contributors Foreword THOMAS E. LOVEJOY Preface page viii xiii xv PART I Arthropods of tropical canopies: current themes of research Introduction 3 1 Canopy entomology, an expanding field of natural science 4 YVES BASSET, VOJTECH NOVOTNY, SCOTT E. MILLER AND ROGER L. KITCHING 2 Methodological advances and limitations in canopy entomology 7 YVES BASSET, VOJTECH NOVOTNY, SCOTT E. MILLER AND ROGER L. KITCHING 3 Vertical stratification of arthropod assemblages 17 YVES BASSET, PETER M. HAMMOND, HÉCTOR BARRIOS, JEREMY D. HOLLOWAY AND SCOTT E. MILLER 4 Determinants of temporal variation in community structure 28 RAPHAEL K. DIDHAM AND NEIL D. SPRINGATE 5 Herbivore assemblages and their food resources 40 VOJTECH NOVOTNY, YVES BASSET AND ROGER L. KITCHING PART II Vertical stratification in tropical forests Introduction 57 6 Distribution of ants and bark-beetles in crowns of tropical oaks 59 ULRICH SIMON, MARTIN GOSSNER AND K. EDUARD LINSENMAIR 7 Vertical and temporal diversity of a species-rich moth taxon in Borneo 69 CHRISTIAN H. SCHULZE AND KONRAD FIEDLER 8 Canopy foliage structure and flight density of butterflies and birds in Sarawak 86 FUMITO KOIKE AND TERUYOSHI NAGAMITSU [v]

4 vi CONTENTS 9 Stratification of the spider fauna in a Tanzanian forest 92 LINE L. SØRENSEN 10 Fauna of suspended soils in an Ongokea gore tree in Gabon 102 NEVILLE N. WINCHESTER AND VALERIE BEHAN-PELLETIER 11 Vertical stratification of flying insects in a Surinam lowland rainforest 110 BART P. E. DE DIJN PART III Temporal patterns in tropical canopies Introduction Insect responses to general flowering in Sarawak 126 TAKAO ITIOKA, MAKOTO KATO, HET KALIANG, MAHAMUD BEN MERDECK, TERUYOSHI NAGAMITSU, SHOKO SAKAI, SARKAWI UMAH MOHAMAD, SEIKI YAMANE, ABANG ABDUL HAMID AND TAMIJI INOUE 13 Arthropod assemblages across a long chronosequence in the Hawaiian Islands 135 DANIEL S. GRUNER AND DAN A. POLHEMUS 14 Seasonality of canopy beetles in Uganda 146 THOMAS WAGNER 15 Seasonality and community composition of springtails in Mexican forests 159 JOSÉ G. PALACIOS-VARGAS AND GABRIELA CASTAÑO-MENESES 16 Seasonal variation of canopy arthropods in Central Amazon 170 JOSÉ CAMILO HURTADO GUERRERO, CLÁUDIO RUY VASCONCELOS DA FONSECA, PETER M. HAMMOND AND NIGEL E. STORK 17 Arthropod seasonality in tree crowns with different epiphyte loads 176 SABINE STUNTZ, ULRICH SIMON AND GERHARD ZOTZ PART IV Resource use and host specificity in tropical canopies Introduction Howdo beetle assemblages respond to anthropogenic disturbance? 190 ANDREAS FLOREN AND K. EDUARD LINSENMAIR 19 Organization of arthropod assemblages in individual African savanna trees 198 KARSTEN MODY, HENRYK A. BARDORZ AND K. EDUARD LINSENMAIR 20 Flower ecology in the neotropics: a flower ant love hate relationship 213 KLAUS JAFFÉ, JOSÉ VICENTE HERNANDEZ, WILLIAM GOITÍA, ANAÍS OSIO, FRANCES OSBORN, HUGO CERDA, ALBERTO ARAB, JOHANA RINCONES, ROXANA GAJARDO, LEONARDO CARABALLO, CARMEN ANDARA AND HENDER LOPEZ 21 Taxonomic composition and host specificity of phytophagous beetles in a dry forest in Panama 220 FRODE ØDEGAARD

5 CONTENTS vii 22 Microhabitat distribution of forest grasshoppers in the Amazon 237 CHRISTIANE AMÉDÉGNATO 23 Flowering events and beetle diversity in Venezuela 256 SUSAN KIRMSE, JOACHIM ADIS AND WILFRIED MORAWETZ PART V Synthesis: spatio-temporal dynamics and resource use in tropical canopies Introduction Habitat use and stratification of Collembola and oribatid mites 271 ANDREAS PRINZING AND STEFFEN WOAS 25 Insect herbivores feeding on conspecific seedlings and trees 282 HÉCTOR BARRIOS 26 Hallowed hideaways: basal mites in tree hollows and allied habitats 291 MATTHEW D. SHAW AND DAVID E. WALTER 27 Arthropod diel activity and stratification 304 YVES BASSET, HENRI-PIERRE ABERLENC, HÉCTOR BARRIOS AND GIANFRANCO CURLETTI 28 Diel, seasonal and disturbance-induced variation in invertebrate assemblages 315 TIMOTHY D. SCHOWALTER AND LISA M. GANIO 29 Tree relatedness and the similarity of insect assemblages: pushing the limits? 329 ROGER L. KITCHING, KAREN L. HURLEY AND LUKMAN THALIB 30 A reviewof mosaics of dominant ants in rainforests and plantations 341 ALAIN DEJEAN AND BRUNO CORBARA 31 Insect herbivores in the canopies of savannas and rainforests 348 SÉRVIO P. RIBEIRO 32 Canopy flowers and certainty: loose niches revisited 360 DAVID W. ROUBIK, SHOKO SAKAI AND FRANCESCO GATTESCO 33 Howpolyphagous are Costa Rican dry forest saturniid caterpillars? 369 DANIEL H. JANZEN 34 Influences of forest management on insects 380 MARTIN R. SPEIGHT, JURIE INTACHAT, CHEY VUN KHEN AND ARTHUR Y. C. CHUNG 35 Conclusion: arthropods, canopies and interpretable patterns 394 YVES BASSET, VOJTECH NOVOTNY, SCOTT E. MILLER AND ROGER L. KITCHING References 407 Index 469

6 1 Canopy entomology, an expanding field of natural science Yves Basset, Vojtech Novotny, Scott E. Miller and Roger L. Kitching In 1929, O. W. Richards and his colleagues hoisted light traps into the canopy of a Guyana forest and became the first to collect arthropods quantitatively from the canopy of any tropical rainforest (Hingston, 1930, 1932). Today, canopy science has become a novel, burgeoning and exciting field in the natural sciences, as evidenced by the ever increasing number of publications focussing on this habitat (Nadkarni & Parker, 1994; Nadkarni et al., 1996). The vitality of canopy science can be traced back to a series of studies about the canopy flora and fauna in tropical forests performed about 20 years ago, in which entomology figured prominently (e.g. Hallé et al., 1978; Perry, 1978; Wolda, 1979; Erwin & Scott, 1980; Nadkarni, 1981; Lowman & Box, 1983; Adis et al., 1984; Stork, 1987a). This sparked a lively and continuing scientific interest in tropical forest canopies and their inhabitants (e.g. Nadkarni & Parker, 1994; Stork & Best, 1994; Lowman et al., 1995; Stork et al., 1997a,c). The term canopy has been used by different authors to mean rather different things. A definition gaining acceptance is the aggregate of every tree crown in the forest, including foliage, twigs, fine branches and epiphytes (Nadkarni, 1995). In a recent review of definitions, Moffett (2000) promotes the view that canopy should be regarded as all elements of the vegetation above the ground and urges us to distance ourselves from the anthropocentric view that only high tree canopies deserve that designation. He supports this view by reference to agricultural science, in which even meadows are regarded as having canopies (e.g. Monteith, 1965). He reminds us of the tacit assumption underlying much of ecological science that processes and dynamics can be scaled up across many orders of magnitude. Of course, if this highly inclusive view of canopy is adopted, then the science needs a careful set of definitions for the height subdivisions to which we must refer for descriptive clarity. The term understorey may be defined as the vegetation immediately above the forest floor and reachable by the observer or, if such measurements are available, the zone with less than 10% light transmittance (Parker & Brown, 2000). The French word canopée denotes the interface between the uppermost layer of leaves and the atmosphere (e.g. Hallé & Blanc, 1990). It has been translated as canopy surface (e.g. Bell et al., 1999) or outer canopy (Moffett, 2000). Further, upper canopy refers to the canopy surface and the volume immediately below (a few metres) that may be occupied by arthropods foraging specifically in the upper region of the canopy. This zone may be distinct only in tall, wet and closed tropical forests and its occurrence is discussed by several contributions in this volume (Chs. 22 and 27). Emergent trees and the air above the canopy may be termed the overstorey as this layer is important for the dispersal of several arthropod groups (Amédégnato, 1997; Compton et al., 2000). Note that use of the above terms does not necessarily mean that the forest is stratified: they are convenient to describe the origin of the material collected. Forest strata are best described in terms of segments of gradients, rather than height above the ground (Parker & Brown, 2000). For cogent descriptions of the canopy structure and canopy surface, see Bongers (2001) and Birnbaum (2001), respectively. The expression canopy arthropods also needs a brief explanation. Although some species spend their entire life cycle in the canopy ( canopy residents sensu Moffett, 2000), others may live in the soil/litter habitat as immature stages and may move later into the canopy to feed on other resources as adults (Ch. 3). We use the term canopy arthropods to refer to all those species that are dependent in any way on the canopy at least at some stage of their life cycle. The role of forest canopies in key ecosystem processes within the biosphere, such as energy flows, [4]

7 CANOPY ENTOMOLOGY, AN EXPANDING FIELD OF NATURAL SCIENCE 5 biogeochemical cycling and the dynamics of regional and global climates, cannot be understated. The forest canopy is the principal site of energy assimilation in primary production, with ensuing intense interchange of oxygen, water vapour and carbon dioxide. Most photosynthetic activity in the biosphere occurs in the canopy, and forest canopies account for almost half of the carbon stored in terrestrial vegetation (e.g. Lowman & Nadkarni, 1995; Wright & Colley, 1996; Malhi & Grace, 2000). In addition, scientists and the media have been captivated even more by the near countless species of animals and plants sustained by tropical forest canopies. The majority of these organisms is still unknown or undescribed. Erwin (1983a) termed the canopy of tropical forests the last biotic frontier, referring to the vast, but poorly studied, richness of organisms, particularly arthropods, resident in the canopy. This epithet and the underlying idea was seized upon and expanded by authors including Wilson (1992) and Moffett (1993). This volume focusses on arthropods of tropical canopies. Yet, canopies of all types, including temperate and tropical forests, play a crucial role in the maintenance of ecological processes and biodiversity. Since different forces may structure tropical and temperate systems (e.g. Turner et al., 1996), comparative research is vital. We hope that this book will stimulate similar parallel efforts to bring together most of the information on arthropods of temperate canopies. Tropical forest canopies represent fascinating environments for entomologists and ecologists for many reasons. First, with the exceptional diversity of their arthropod communities, tropical forest canopies may be the most species-rich habitat on Earth (e.g. Erwin, 1983a), although the soil/litter of tropical forests is another strong contender (e.g. André et al., 1994; Hammond, 1994; Stork, 1988). Most of the contributions in this volume confirm the impressive diversity of canopy arthropods in the tropics. Second, despite increasing interest in their study, the fauna of tropical canopies remains largely unknown and has been the subject of much controversy among entomologists and ecologists. Even the simplest questions remain unanswered, such as: how many arthropod species live in the canopy of various tree species and forest types, what is their resource base, or how have their ecological niches evolved (e.g. May, 1994). For example, the deceptively simple question as to whether tropical canopy herbivores are more or less specialized than their temperate counterparts, or than counterparts foraging in the understorey, is far from answered (e.g. Basset, 1992a; Gaston, 1993). Several contributions in this volume address these issues (Chs. 5, 21, 22 and 29). Third, tropical canopies represent a key arena in which biologists can study the interactions of multiple species within communities and test hypotheses on evolution and coevolution. Studies of tropical environments and their organisms have contributed significantly to the advancement of modern ecology (Chazdon & Whitmore, 2002). Canopy ecology is a young, frontier science, exploring a largely unknown environment, establishing basic patterns and developing nascent theories. We expect that synecological studies of canopy organisms, documenting the rich variety of their interactions in this complex habitat, will boost our ability to generate and test evolutionary scenarios. Because of the high diversity of canopy arthropods, they also represent model organisms for studying macroecology and discovering general patterns and rules in nature (Lawton, 1999). The synecology of arthropod assemblages in the canopy is a central theme of several contributions in this volume (Chs. 19, 20, 26, 29, 30 and 33). Last, rapid habitat loss in tropical forests makes their canopy inhabitants particularly vulnerable to endangerment or even extinction. Dissemination of scientific information to foster scientific interest in canopy arthropod communities is crucial for the survival of canopy communities, as well as for those who study them. For example, sound estimates of species loss cannot be inferred from ground-based studies alone; data on the distribution and ecology of canopy arthropods are essential to predict the effects of forest disturbance and fragmentation on species loss (e.g. Willott, 1999; Kitching et al., 2000). These issues are discussed in Chs. 18, 28 and 34. Most of the biological activity in tropical rainforests is concentrated in the upper canopy rather than the understorey (e.g. Hallé & Blanc, 1990; Parker, 1995). Many abiotic and biotic characteristics of the canopy are different from those in the underlying understorey. The higher illumination levels in the canopy promote rapid rates of photosynthesis, which, in turn, promotes high plant production, thereby sustaining a more abundant and diverse community of animals than in the understorey (Wright & Colley, 1996). The vertical

8 6 Y. BASSET, V. NOVOTNY, S. E. MILLER & R. L. KITCHING stratification of resources and organisms is one of the key characteristics of tropical forests, particularly of wet forests. Many contributions in this volume explore how different and unique canopy arthropods are compared with their counterparts in the understorey (Chs. 6 8, 11, 25 and 27), or in the soil/litter habitat (Chs. 9, 10, 24 and 26). Other characteristics promoting a distinctive canopy fauna relate to the discrete distribution of resources in the canopy. The high rate of plant production in the canopy is often not continuous (e.g. van Schaik et al., 1993), thus shaping specific strategies and life histories in insect herbivores and their associated assemblages of predators and parasitoids. This important theme is addressed by several contributions (Chs. 4, 12, 14 16). Others emphasize the temporal scale at which these complex interactions occur, from diel activity patterns (Chs. 23, 27 and 28) to transannual effects (Ch. 13). Arthropods and their food resources may experience different microclimates within the heterogeneous environment of tropical forests (e.g. Lowman, 1995; DeVries et al., 1999a). This is most apparent along the vertical gradients of closed wet tropical forests, but it also occurs horizontally when natural tree falls modify the structure of the canopy. Several contributions examine the spatial distribution of particular resources and its consequences for canopy arthropods: the physical qualities of leaves (Ch. 31), the accumulation of litter (Ch. 10) and the presence of epiphytes (Ch. 17), vines (Ch. 31) or flowers (Chs. 20 and 23). Many of the earlier studies of canopy arthropods took primarily a faunistical approach (reviews in Erwin, 1989, 1995; Stork & Hammond, 1997; Basset 2001b). They often relied upon indirect sampling methods, such as light trapping or pyrethrum knockdown (canopy fogging). Workers were limited to ground level and arthropod life histories and population dynamics could only be inferred indirectly from their data. In addition to improvements in fogging techniques, recent methodological developments in canopy access (some reviewed in Moffett & Lowman, 1995) allow the observation of canopy arthropods in situ and their live collection. Today, methods of canopy access that are favoured by entomologists include construction cranes, canopy towers, canopy rafts, aerial sledges, aerial walkways or single rope techniques (see Ch. 2). Collecting methods are accordingly more diverse and reflect the increasing complexity of the questions that are pursued by canopy biologists and entomologists. The contributions in the present volume truly reflect this revolution in canopy access, sampling methodologies and the consequent maturation of research.