The Evolution of Exudativory in Primates (Developments in Primatology: Progress and Prospects)

Developments in Primatology: Progress and Prospects

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Anne M. Burrows    Leanne T. Nash ●

Editors

The Evolution of Exudativory in Primates

Editors Anne M. Burrows Department of Physical Therapy Duquesne University Pittsburgh, PA 15282 and Department of Anthropology University of Pittsburgh Pittsburgh, PA 15260 USA [email protected]

Leanne T. Nash School of Human Evolution and Social Change Arizona State University Tempe, AZ 85287-2402 USA [email protected]

ISBN 978-1-4419-6660-5 e-ISBN 978-1-4419-6661-2 DOI 10.1007/978-1-4419-6661-2 Springer New York Dordrecht Heidelberg London Library of Congress Control Number: 2010936362 © Springer Science+Business Media, LLC 2010 All rights reserved. This work may not be translated or copied in whole or in part without the written permission of the publisher (Springer Science+Business Media, LLC, 233 Spring Street, New York, NY 10013, USA), except for brief excerpts in connection with reviews or scholarly analysis. Use in connection with any form of information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed is forbidden. The use in this publication of trade names, trademarks, service marks, and similar terms, even if they are not identified as such, is not to be taken as an expression of opinion as to whether or not they are subject to proprietary rights. Printed on acid-free paper Springer is part of Springer Science+Business Media (www.springer.com)

Anne dedicates this volume to her family whose constant support made it possible. Leanne would like to dedicate this volume to her parents and siblings, who were always supportive even when they didn’t fully understand, and to her spouse, Mike, who does understand and without whom the work would not have happened.

Foreword

I first became involved in research into primate behavior and ecology in 1968, over 40 years ago, driven by a quest for a better understanding of the natural context of primate evolution. At that time, it was virtually unknown that primates can exploit exudates as a major food source. I was certainly unaware of this myself. By good fortune, I was awarded a postdoctoral grant to work on lemurs with Jean-Jacques Petter in the general ecology division of the Muséum National d’Histoire Naturelle in Brunoy, France. This provided the launching-pad for my first field study of lesser mouse lemurs in Madagascar, during which I gained my initial inklings of exudate feeding. It was also in Brunoy that I met up with Pierre CharlesDominique, who introduced me to pioneering observations of exudate feeding he had made during his field study of five lorisiform species in Gabon. This opened my eyes to a key feeding adaptation that has now been reported for at least 69 primate species in 12 families (Smith, Chap. 3) – almost 20% of extant primate species. So exudativory is now firmly established as a dietary category for primates, alongside the long-recognized classes of faunivory (including insectivory), frugivory, and folivory. Soon after I encountered Charles-Dominique, he published the first synthetic account of his Gabon field study in a French language journal (Charles-Dominique 1971). Convinced by the particular importance of his research, I offered to work on an English translation, which eventually appeared in book form some 6 years later (Charles-Dominique 1977). In the process, I learned more about exudativory. For my own part, I included some preliminary comments on exudate feeding in my publication on the 1968 study of lesser mouse lemurs (Martin 1972a). In an overview of the adaptive radiation of lemurs published in the same year (Martin 1972b), I made several brief comments on the general significance of exudate feeding. In particular, I suggested a connection with the tooth-scraper: “Field observations have shown that the smaller-bodied Cheirogaleinae and Galaginae use the toothscraper to gather plant exudates, and it is likely that the horizontal arrangement of these anterior teeth has been primarily developed for scraping and prising.” Although I had thus become aware of the potential significance of exudate feeding, my first really intensive exposure to it came with a 2-year radio-tracking field study of behavior and ecology of lesser bushbabies in South Africa (1975–1977).

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Simon Bearder, the postdoctoral scientist in this investigation who did the lion’s share of hands-on work in the field, had previously completed an MSc thesis on our study species, Galago moholi. As a result, he was already quite familiar with exudate feeding in this species. I still remember my first night of observations in this new study. It was a complete revelation to me as Simon led me from one Acacia tree to another, pointing out sites and traces on the trunks where the bushbabies came to feed on exudates. Despite the obvious importance of exudates in the diet, it was not at all easy to see exactly how the bushbabies harvested this key resource. On rare occasions, it proved possible to observe active use of the tooth-scraper in exudate feeding. For this, the mouth was held slightly ajar and jerky to-and-fro head movements were made with the lower jaw applied to the surface of a branch or trunk. However, the clearest evidence of tooth-scraper use in feeding came from an incidental, indirect source. In order to fit and remove radio transmitters, we had to trap our bushbabies regularly. Capture was achieved with large traps placed in trees, left permanently in situ and regularly supplied with bait poured onto a baseboard. The bait – containing honey, treacle, peanut butter and banana – was initially a fluid paste. However, bait left-overs became quite hard when dry. Bushbabies often entered traps to feed on hardened bait at times when no trapping was conducted. When the traps were taken down at the end of the 2-year study, all baseboards were densely covered with characteristic sets of short, parallel scratches that had clearly been made with the tooth-scraper (Bearder and Martin 1980). As additional field reports accumulated, notably from a major study of five sympatric nocturnal lemur species in western Madagascar (Charles-Dominique et  al. 1980), it became clear that exudate feeding was prevalent among small-­ bodied, nocturnal strepsirrhine primates (lemurs and lorises). Moreover, it emerged that fork-crowned lemurs (Phaner) in Madagascar, like needle-clawed bushbabies (Euoticus) in Africa, are specialist exudate feeders. In parallel to studies on nocturnal strepsirrhines, equally striking evidence of exudate feeding was emerging for small-bodied, diurnal, clawed New World monkeys (Callitrichidae). Napier and Napier (1967) noted that marmosets (Callithrix, Cebuella) have a “short-tusked condition,” with relatively long lower incisors and inconspicuous lower canines that do not project far above the crowns of cheek teeth. By contrast, tamarins (Saguinus, Leontopithecus) have a “long-tusked condition,” with relatively short incisors and prominent canines in the lower jaw. This morphological distinction separates marmosets not only from tamarins but also from Goeldi’s monkey (Callimico). It was later noted (Coimbra-Filho and Mittermeier 1976, 1977) that several marmoset species use their lower anterior teeth to perforate tree bark and thus actively stimulate the flow of exudates. Tamarins and Goeldi’s monkeys have never been observed to do this, although various species do feed on exudates (Garber and Porter, Chap. 4). It was also reported that enamel is lacking on the internal (lingual) face of lower incisors in marmosets (Rosenberger 1978). This resembles the condition seen in anterior gnawing teeth of lagomorphs, rodents, and Daubentonia. That condition is regarded as an adaptation for maintenance of a sharp cutting edge. The short-tusked condition in marmosets was accordingly interpreted as a special adaptation for actively gouging holes in trees to feed on exudates. New research on enamel prisms

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in the anterior lower dentition has revealed that marmosets, but not tamarins, have clear decussation patterns indicating strengthening to meet the demands of gouging (Ravosa et al., Chap. 9). Nearly 25 years ago Nash (1986) effectively reviewed dietary, behavioral, and morphological correlates of exudativory in primates, bringing together evidence for both nocturnal strepsirrhines and diurnal callitrichids. Most cases of exudativory come from relatively small-bodied, essentially arboreal primates, but there are exceptions. As a rare adaptation among adult Old World monkeys, East African patas monkeys (Erythrocebus patas) feed primarily on exudates (Isbell 1998). Exudate feeding has also been reported for yellow baboons, and this is one of the most important dietary energy sources for juveniles (Altmann 1998). Chimpanzees have also been reported to feed on exudates, although the daily energy intake from this source is quite limited (Ushida et al. 2006). Even with the more limited information available 25 years ago, Nash’s review was able to establish quite clearly the importance of exudate feeding for primates. Accumulating evidence has been accompanied by improving clarity with respect to basic concepts. In the first place, it is important to distinguish several distinct kinds of plant exudates that may be consumed by primates: gums, saps, nectar, latex, and resins (Bearder and Martin 1980; Power, Chap. 2). At the outset, I was myself confused about these different categories, referring to gums, saps, and resins interchangeably (Martin, 1972b). However, I soon realized the errors of my ways (Bearder and Martin 1980). In fact, latex is rarely consumed and resins are shunned, so the main exudates eaten by primates are gums, saps, and nectar, with gum at the forefront. Hence, the primary form of exudativory is gum feeding (gummivory). In this connection, it is also important to distinguish between primates that can gouge holes in tree trunks and branches (and therefore gain access to saps as well as gums) and those that either cannot or do not and merely scrape away superficial exudates (gums). It has long been known that marmosets actually gouge holes, and some kind of clearly identifiable dental adaptation is therefore to be expected. By contrast, most strepsirrhines do not gouge but rely on scraping and licking to harvest exudates, so dental specializations may be correspondingly more subtle. I originally believed that the tooth-scraper of small-bodied strepsirrhines such as Microcebus and Galago is too fragile to permit actual gouging. However, apical wear on the tooth-scraper is seen in relatively old individuals of Galago moholi (Bearder and Martin 1980), and gouging of some kind has been reported for Phaner (Petter et al. 1971). But there is now a convincing field report, based on close-up observations, that Microcebus griseorufus – a specialist gum-feeder among lesser mouse lemurs – definitely uses its tooth-scraper to stimulate gum flow (Génin et al., Chap. 6). In another direction, some years ago, I was quite taken by surprise by an incidental observation made at the Psychological Institute of the University of Zürich. Gustl Anzenberger, who managed a primate breeding colony, had provided housing for a pair of pygmy slow lorises (Nycticebus pygmaeus). One day, he told me that I should come and look at something that would surely interest me. On various wooden fittings taken from the cage, including both branches and plywood panels, deep pits were clearly recognizable. Gustl had unmistakably observed the

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pygmy slow lorises gouging these pits with their tooth-scrapers. I therefore confidently expected that studies of Nycticebus pygmaeus would reveal exudativory to be a prominent part of its feeding behavior. I had to wait a few years, but eventually combined circumstantial evidence from a field survey in Vietnam and from observations in captivity (at Duke University Primate Center) did indicate that Nycticebus pygmaeus may be a specialized gummivore (Tan and Drake 2001). It was explicitly suggested that pygmy slow lorises use the tooth-scraper to chisel away the cambium layer in search of exudates. In fact, it has since been reported that largerbodied slow lorises (Nycticebus coucang) also exhibit gouging behavior. Field observations in Sumatra revealed that slow lorises perforate the superficial layer of the cambium of trees or lianas with their tooth-scraper (Nekaris et al., Chap. 8). The onset of gouging is so loud that it is audible at a distance of 30 feet and can be used as a means of locating individuals at night. It is also important to distinguish between obligate (“specialist”) exudativores and facultative (“nonspecialist”) consumers (Nash and Burrows, Chap. 1). Examples are Euoticus in comparison to other galagids, Phaner as contrasted with most other cheirogaleids, and marmosets as opposed to other callitrichids. As a rule, gouging is restricted to (but not universal among) obligate consumers for which exudates typically make up a large part of the diet. By contrast, facultative consumers depend only to a relatively small extent on gums and never gouge. So their feeding on exudates is necessarily confined to gums. It is a moot point whether Microcebus griseorufus (whose diet includes more than 75% exudates) is really an obligate exudativore or merely a typical lesser mouse lemur that happens to occupy a habitat where predominant gum feeding is the only option. But there is a clear expectation that Nycticebus species, which clearly gouge, will be found to be committed exudativores when appropriate long-term field studies have been conducted. The fact remains that most gum-eating strepsirrhines do not gouge trees to obtain sap. Instead, they rely on harvesting superficial gum deposits that are produced by trees in response to damage. In our field study of Galago moholi, for example, this was true of the Acacia trees that provided the main source of gum. It emerged that wood-eating (xylophagous) larvae of various insects bored channels beneath the tree surface: long-horned beetles (Cerambycidae), jewel beetles (Buprestidae), click beetles (Elateridae) and carpenter moths (family Cossidae). Gum was then liberated through surface apertures made by the boring insects, particularly when they eventually emerged from the host tree (Bearder and Martin 1980). Similar observations have been reported for gum-flows in Madagascar. Larvae of long-horned beetles and click beetles reportedly chew tunnels in trunks of Alantsilodendron trees that serve as the main source of gum (Génin et  al., Chap. 6, this volume). However, I must admit that I simply do not understand what is going on with respect to the trees that serve as gum sources. Exudation of gum is generally seen as a tree’s response to damage, sometimes caused by wood-boring insects, but sometimes resulting from breakage of a branch. Yet it is not at all clear why only certain trees produce gum, why they sometimes produce large quantities over an extended period of time, nor why most gums are edible and quite nutritious rather than laced with toxins. Nash (1989) showed experimentally that addition of

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tannins to gum reduces acceptability. The relationship between gum-producing trees, wood-boring insect larvae, and exudativorous primates is something that surely deserves more attention in future research. Gums have one distinct advantage as a food source in that they generally seem to be available throughout the year, with no marked seasonal pattern of variation. Some primates, such as Galago moholi, use them as a year-round food source (Bearder and Martin 1980), whereas others consume them only seasonally, as in the case of Microcebus murinus (Joly-Radko and Zimmermann, Chap. 7). Overall, it seems that gums are particularly important during the dry season, when fruits are often relatively scarce. For this reason, they are often seen as a fall-back food resource. However, Génin et al. (Chap. 6) suggest the alternative hypothesis that gummivory is typical of hypervariable environments influenced by El Niño-related droughts. But in any event dry conditions seem to provide the key. Provided that they can be digested, gums provide a rich source of carbohydrates (Power, Chap. 2). Most gummivorous primates have an enlarged caecum, housing symbiotic bacteria that can digest the gums. Yet observations of Microcebus griseorufus indicate that gummivory in this species may not involve a major digestive challenge, so further study is needed (Génin et al., Chap. 6). Analysis of Acacia gums gives the misleading impression that exudate composition is fairly consistent. However, study of gums from other genera has revealed that there is in fact considerable variability. For instance gums of Alantsilodendron in Madagascar are rich in proteins, whereas protein is only present as a trace component in gums of Acacia. Minerals such as calcium represent another potentially important component of exudates (Garber 1984), although there is no direct evidence that they are nutritionally important for that reason. One early suggestion was that the high calcium: phosphorus ratio in Acacia gums may complement the reversed ratio found in insects and some fruits especially during gestation and lactation (Bearder and Martin 1980). Ushida et al. (2006) estimated that the average daily intake of Albizia gum by chimpanzees could meet the entire daily requirement of calcium and several other minerals, despite the fact that gum makes up a relatively small part of the diet (Power, Chap. 2). Exudativory is obviously an important feeding adaptation for various strepsirrhines (several cheirogeleids, galagids, and lorisids), callitrichids, and certain Old World monkeys and apes. Specialization on exudativory developed convergently at least three times during primate evolution and probably more often, particularly if plesiadapiforms are included (Rosenberger, Chap. 14). Accordingly, the adaptations associated with gouging and or scraping may differ quite markedly among taxa, notably between strepsirrhines and callitrichids. Yet there are some general similarities in skull form and jaw mechanics (Vinyard et al. 2003; Ravosa et al., Chap. 9; Mork et al., Chap. 10). Adaptation for a wide gape generally seems to be important for gum feeding, reflected by a relatively low-slung jaw joint with antero-posterior elongation of articular surfaces. On the other hand, the balance of evidence has discounted an initial expectation that gouging, if not scraping, would generate larger bite forces requiring special adaptations of the skull and jaws.

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One long-term goal is a broad evolutionary perspective on exudativory. In her 1986 review Nash aptly stated: “Understanding the biological bases of gummivory will be of value in interpreting the anatomy and modeling the behavior of early primates.” One key question that arises here is whether there is an evolutionary connection between exudativory and the tooth-scraper of strepsirrhine primates. The six-tooth scraper incorporating the canines and incisors in the lower jaw is almost certainly a shared derived feature of strepsirrhines that was present in their last common ancestor. It has long been held that the tooth-scraper evolved in specific connection with grooming behavior, living up to the alternative name “toothcomb” (Rosenberger and Strasser 1985; Rosenberger, Chap. 14). However, my own preferred hypothesis is that evolution of the strepsirrhine tooth-scraper was primarily connected with exudativory (Martin 1972b, 1979). Of course, it is quite evident that extant strepsirrhines do generally use their tooth-scrapers in grooming. And there is also abundant evidence, briefly reviewed above, that numerous strepsirrhines actively use the tooth-scraper when feeding on exudates. It is also generally accepted that the specialized gummivores Euoticus and Phaner have distinctive tooth-scrapers. However, the association between tooth-scraper dimensions and exudativory is not particularly strong when seen across strepsirrhines generally (Eaglen 1986). Moreover, comparison of specialized exudativores, moderate exudativores and nonexudativores among galagids provides only limited support for a connection between tooth-scraper dimensions and exudativory (Burrows and Nash, Chap. 11). But it must also be recognized that, other than the observation that modern strepsirrhines do generally use the lower anterior teeth in grooming, there is also no confirmatory evidence linking grooming to the tooth-scraper. Lots of mammals use whatever anterior teeth they have for grooming. Examination of hair length in strepsirrhines showed no relationship with dimensions of the tooth-scraper (Martin 1979). Indeed, the committed exudativores Euoticus and Phaner both have relatively short hair in comparison with other strepsirrhines. I see two basic problems with the hypothesis that the strepsirrhine toothcomb evolved exclusively for grooming: First, mammalian teeth are generally connected with feeding behavior, and persuasive arguments are necessary to support evolution in a nonfeeding context. Second, nobody has ever suggested why strepsirrhines should have needed a special dental adaptation for grooming. This links up with the fundamental problem that the tooth-scraper of strepsirrhine primates (including the lower canines) is unique among mammals, so we have no parallel cases to test hypotheses regarding grooming or feeding. This issue remains unresolved; the controversy continues. In closing, I will take the liberty of embarking on a flight of fancy. Bear with me and accept, for the sake of argument, that the tooth-scraper emerged in ancestral strepsirrhines in association with scraping (but not gouging) as a means of harvesting exudates. The tooth-scraper was doubtless used for grooming as well, but that does not affect my argument. Exudativory is essentially an arboreal behavior, so it would be logical for it to develop in early primates. Now let us consider the strange case of the aye-aye (Daubentonia). The aye-aye no longer has a typical strepsirrhine tooth-scraper containing six teeth. Instead, it has a continuously growing, chisellike incisor on either side of the lower jaw. The condition in Daubentonia was

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undoubtedly derived from the original strepsirrhine tooth-scraper by loss of teeth and other modifications. The chisel-like incisors and filiform, highly mobile middle finger of the aye-aye represent adaptations for finding and consuming wood-boring larvae in the trunks of trees. These are the very same larvae that provoke production of exudates by the host tree. So here’s the thing: Maybe original use of the toothcomb to scrape away exudates gradually led to longer and stronger incisors, penetration of bark and eventual feeding on the wood-boring larvae themselves. Molecular evidence has now convincingly demonstrated that the aye-aye branched away at the base of the lemuriform radiation (Pastorini et al. 2003; Horvath et al. 2008). So evolution of the condition in Daubentonia according to the scenario just presented would require an ancestral condition with a six-tooth scraper associated with exudativory. It has long been accepted that the striped possum of Australasia (Dactylopsila) provides a marsupial analog to the aye-aye (Cartmill 1974). Interestingly, Dactylopsila belongs to the same family (Petauridae) as the sugar glider (Petaurus breviceps), an Australian marsupial that feeds on exudates of Acacia trees (Smith 1982). So perhaps the evolution of Daubentonia from an ancestral, exudativorous strepsirrhine is also paralleled by the evolution of Dactylopsila from an ancestral, exudativorous marsupial. Acknowledgments  First and foremost, I would like to thank the editors of this volume – Anne Burrows and Leanne Nash – for kindly inviting me to write this foreword. The chapters grew out of their well-organized and highly informative symposium on exudativory, held at the 2008 Congress of the International Primatological Society (IPS) in Edinburgh, Scotland. Having participated in the early beginnings of research into exudativory, I made certain that attendance at that symposium was one of my top priorities. I was delighted by the quality of the presentations. It was also a pleasure to see how many advances had been made in our understanding of an important primate feeding category that was virtually unrecognized 40 years ago. I learned a great deal, both from presentations at the symposium and from the more detailed information provided in the chapters contained in this volume. My pleasure was further heightened when Anne and Leanne invited me to write a foreword straight after the symposium. I feel honoured to be involved in this way, as The Evolution of Exudativory in Primates undoubtedly represents a watershed in our understanding of this fascinating topic. The 14 chapters effectively review current information from a wide array of disciplines: behavior, ecology, nutrition, primate evolution, morphology, and conservation. They also provide pointers to future research that will hopefully answer several puzzling questions that remain open. Let me conclude by acknowledging the great debt that we owe to the dedicated primate fieldworkers who discovered the phenomenon of exudativory and have generated a continuing flow of vital information from natural habitats. Robert D. Martin The Field Museum, Chicago, IL USA

References 1. Altmann SA (1998) Foraging for survival: yearling baboons in Africa. University of Chicago Press, Chicago 2. Bearder SK, Martin RD (1980) Acacia gum and its use by bushbabies, Galago senegalensis (Primates: Lorisidae). Int. J Primatol 1:103–128

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3. Cartmill M (1974) Daubentonia, Dactylopsila and klinorhynchy. In Prosimian biology (eds Martin RD, Doyle GA, Walker AC). Duckworth, London 4. Charles-Dominique P (1971) Éco-éthologie des prosimiens du Gabon. Biol Gabon 7:121–228. 5. Charles-Dominique P (1977) Ecology and behaviour of the nocturnal primates. Prosimians of Equatorial West Africa. Duckworth, London 6. Charles-Dominique P, Cooper HM, Hladik A, Hladik CM, Pagès E, Pariente GF, PetterRousseaux A, Petter J-J, Schilling A. (eds.) (1980) Nocturnal Malagasy primates. Academic Press, New York 7. Coimbra-Filho AF, Mittermeier RA (1976) Exudate-eating and tree-gouging in marmosets. Nature, Lond. 262:630 8. Coimbra-Filho AF, Mittermeier RA (1977) Tree-gouging, exudate-eating, and the “shorttusked” condition in Callithrix and Cebuella. In The biology and conservation of the Callitrichidae (ed Kleiman DG). Smithsonian Institution Press, Washington, DC 9. Eaglen RH (1986) Morphometrics of the anterior dentition in strepsirhine primates. Am J Phys Anthropol 71:185–201 10. Garber PA (1984) Proposed nutritional importance of plant exudates in the diet of the Panamanian tamarin, Saguinus oedipus geoffroyi. Int J Primatol 5:1–15 11. Horvath JE, Weisrock DW, Embry SL, Fiorentino I, Balhoff JP, Kappeler P, Wray GA, Willard HF, Yoder AD (2008) Development and application of a phylogenomic toolkit: resolving the evolutionary history of Madagascar’s lemurs. Genome Res 18:489–499 12. Isbell LA (1998) Diet for a small primate: insectivory and gummivory in the (large) patas monkey (Erythrocebus patas pyrrhonotus). Am J Primatol 45:381–398 13. Martin RD (1972a) A preliminary field-study of the lesser mouse lemur (Microcebus murinus, J.F. Miller 1777). Z Tierpsychol Suppl 9:43–89 14. Martin RD (1972b) Adaptive radiation and behaviour of the Malagasy lemurs. Phil Trans Roy Soc Lond B 264:295–352 15. Martin RD (1979) Phylogenetic aspects of prosimian behavior. In The study of prosimian behavior (eds Doyle GA, Martin RD). Academic Press, New York 16. Napier JR, Napier PH (1967) A handbook of living primates. Academic Press, London 17. Nash LT (1986) Dietary, behavioral, and morphological aspects of gummivory in primates. Yrbk Phys Anthropol 29:113–137 18. Nash LT (1989) Galagos and gummivory. Hum Evol 4:199–206 19. Pastorini J, Thalmann U, Martin RD (2003) A molecular approach to comparative phylogeography of extant Malagasy lemurs. Proc Natl Acad Sci USA 100:5879–5884 20. Petter J-J, Schilling A, Pariente G (1971) Observations éco-éthologiques sur deux lémuriens malgaches nocturnes: Phaner furcifer et Microcebus coquereli. Terre Vie 118:287–327. 21. Rosenberger AL, Strasser ME (1985) Toothcomb origins: support for the grooming hypothesis. Primates 26:76–85 22. Rosenberger AL (1978) Loss of incisor enamel in marmosets. J Mammal 59:207–208 23. Smith AP (1982) Diet and feeding strategies of the marsupial sugar glider in temperate Australia. J Anim Ecol 51:149–166 24. Tan CL, Drake JH (2001) Evidence of tree gouging and exudate eating in pygmy slow lorises (Nycticebus pygmaeus). Folia Primatol 72:37–39 25. Ushida K, Fujita S, Ohasgi G (2006) Nutritional significance of the selective ingestion of Albizia zygia gum exudate by wild chimpanzees in Bossou, Guinea. Am J Primatol 68:143–151 26. Vinyard CJ, Wall CE, Williams SH, Hylander WL (2003) Comparative functional analysis of skull morphology of tree-gouging primates. Am J Phys Anthropol 120:153–170

Acknowledgments

This volume is a product of a symposium entitled “The evolution of exudativory in primates” held at the 22nd Congress of the International Primatological Society in Edinburgh, Scotland in 2008. We would like to offer our sincere thanks to the numerous people who assisted this edited volume throughout its various stages. The reviewers provided their expert insights and commentary. Melissa Higgs at Springer was always enthusiastic and unfailingly guided and encouraged us. Bob Martin not only provided a wonderful Foreword, but inspired much of the work represented here starting over three decades ago. Our most special thanks are due to the contributors whose steadfast labors and patience helped bring this volume to its ultimate materialization.

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Contents

1 Introduction: Advances and Remaining Sticky Issues in the Understanding of Exudativory in Primates.................................. Leanne T. Nash and Anne M. Burrows

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2 Nutritional and Digestive Challenges to Being a Gum-Feeding Primate............................................................. Michael L. Power

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3 Exudativory in Primates: Interspecific Patterns..................................... Andrew C. Smith 4 The Ecology of Exudate Production and Exudate Feeding in Saguinus and Callimico......................................................................... Paul A. Garber and Leila M. Porter

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5 Influences on Gum Feeding in Primates.................................................. 109 Andrew C. Smith 6 Gummivory in Cheirogaleids: Primitive Retention or Adaptation to Hypervariable Environments?.................................... 123 Fabian G.S. Génin, Judith C. Masters, and Jorg U. Ganzhorn 7 Seasonality in Gum and Honeydew Feeding in Gray Mouse Lemurs.............................................................................. 141 Marine Joly-Radko and Elke Zimmermann 8 Comparative Ecology of Exudate Feeding by Lorises (Nycticebus, Loris) and Pottos (Perodicticus, Arctocebus)....................... 155 K. Anne-Isola Nekaris, Carly R. Starr, Rebecca L. Collins and Angelina Wilson

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  9 Exudativory and Primate Skull Form.................................................... 169 Matthew J. Ravosa, Russell T. Hogg, and Christopher J. Vinyard 10 A Comparative Analysis of the Articular Cartilage in the Temporomandibular Joint of Gouging and Nongouging New World Monkeys................................................... 187 Amy L. Mork, Walter E. Horton, and Christopher J. Vinyard 11 Searching for Dental Signals of Exudativory in Galagos..................... 211 Anne M. Burrows and Leanne T. Nash 12 A Guide to Galago Diversity: Getting a Grip on How Best to Chew Gum..................................................................... 235 Isobel R. Stephenson, Simon K. Bearder, Guiseppe Donati, and Johann Karlsson 13 Tongue Morphology in Infant and Adult Bushbabies (Otolemur spp.).................................................. 257 Beth A. Docherty, Laura J. Alport, Kunwar P. Bhatnagar, Anne M. Burrows, and Timothy D. Smith 14 Adaptive Profile Versus Adaptive Specialization: Fossils and Gummivory in Early Primate Evolution............................ 273 Alfred L. Rosenberger Index.................................................................................................................. 297

Contributors

Laura J. Alport Department of Anthropology, University of Texas at Austin, Austin, TX 78712, USA Simon K. Bearder Nocturnal Primate Research Group, Department of Anthropology and Geography, School of Social Sciences and Law, Oxford Brookes University, Oxford,OX3 0BP, UK Kunwar P. Bhatnagar Department of Anatomical Sciences and Neurobiology, University of Louisville School of Medicine, Louisville, KY 40292, USA Anne M. Burrows Department of Physical Therapy, Duquesne University, Pittsburgh, PA 15282, USA, Department of Anthropology, University of Pittsburgh, Pittsburgh, PA 15260, USA Rebecca L. Collins Nocturnal Primate Research Group, Department of Anthropology and Geography, School of Social Sciences and Law, Oxford Brookes University, Oxford OX3 0BP, UK Beth A. Docherty Department of Physical Therapy, Duquesne University, Pittsburgh, PA 15282, USA Guiseppe Donati Nocturnal Primate Research Group, Department of Anthropology and Geography, School of Social Sciences and Law, Oxford Brookes University, Oxford OX3 0BP, UK Jorg U. Ganzhorn Department of Zoology, University of Fort Hare, Private Bag X1314, Alice 5700, South Africa

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Contributors

Paul A. Garber Department of Anthropology, University of Illinois, 109, Davenport Hall, 607 S Mathews Ave, Urbana, IL 61801, USA Fabien G.S. Génin Department of Zoology, University of Fort Hare, Private Bag X1314, Alice 5700, South Africa Russell T. Hogg Department of Pathology and Anatomical Sciences, School of Medicine, University of Missouri, Columbia, MO 65212, USA Walter E. Horton, Jr. Department of Anatomy and Neurobiology, Northeastern Ohio Universities College of Medicine (NEOUCOM), Rootstown, OH 44272, USA Marine Joly-Radko Institut fuer Zoologie, Tieraerztliche Hochschule Hannover, Buenteweg 17, Hannover 30559, Germany Johann Karlsson Nocturnal Primate Research Group, Department of Anthropology and Geography, School of Social Sciences and Law, Oxford Brookes University, Oxford OX3 0BP, UK Judith C. Masters Department of Zoology, University of Fort Hare, Private Bag X1314, Alice 5700, South Africa Amy L. Mork Department of Anatomy and Neurobiology, Northeastern Ohio Universities College of Medicine (NEOUCOM), Rootstown, OH 44272, USA Leanne T. Nash School of Human Evolution and Social Change, Arizona State University, Tempe, AZ 85287-2402, USA Angelina Wilson TRAFFIC International, 219a Huntingdon Road Cambridge, CB3 0DL, UK K. Anne-Isola Nekaris Nocturnal Primate Research Group, Department of Anthropology and Geography, School of Social Sciences and Law, Oxford Brookes University, Oxford OX3 0BP, UK Leila M. Porter Department of Anthropology, University of Illinois, 109, Davenport Hall, 607s Mathews Ave, Urbana, IL 61801, USA

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Michael L. Power Nutrition Laboratory, Smithsonian Conservation Biology Institute, National Zoological Park, P.O. Box 37012, MRC 5503, Washington, DC 20013-7012, USA Research Department, American College of Obstetricians and Gynecologists, Washington, DC 20024, USA Matthew J. Ravosa Department of Pathology and Anatomical Sciences, School of Medicine, University of Missouri, Columbia, MO 65212, USA; Division of Mammals, Department of Zoology, Field Museum of Natural History, Chicago, IL 60605-2496, USA Alfred L. Rosenberger Department of Anthropology and Archaeology, Brooklyn College, The City University of New York, Brooklyn, NY 11210, USA; The Graduate Center, The City University of New York, New York, NY, USA New York Consortium in Primatology (NYCEP), NY, USA and Department of Mammalogy, The American Museum of Natural History, New York, NY 10024-5192, USA Andrew C. Smith Animal and Environmental Research Group, Department of Life Sciences, Anglia Ruskin University, East Road, CB1 1PT Cambridge, UK Timothy D. Smith School of Physical Therapy, Slippery Rock University, Slippery Rock, PA 16057, USA; Department of Anthropology, 3302 WWPH, University of Pittsburgh, Pittsburgh, PA 15260, USA Carly R. Starr School of Animal Studies, University of Queensland, Gatton, Queensland 4072, Australia Isobel R. Stephenson Department of Anthropology and Geography, School of Social Sciences and Law, Oxford Brookes University, Gipsy Lane, Oxford, OX3 0BP, UK Christopher J. Vinyard Department of Anatomy and Neurobiology, Northeastern Ohio Universities College of Medicine (NEOUCOM), Rootstown OH 44272, USA Elke Zimmermann Institute of Zoology, University of Veterinary Medicine Hanover, Hanover, Germany

Chapter 1

Introduction: Advances and Remaining Sticky Issues in the Understanding of Exudativory in Primates Leanne T. Nash and Anne M. Burrows

Abstract  In the 25 years since the last synthesis on this topic was published, there has been a marked increase in the appreciation of exudativory as a primate dietary strategy and investigations of its morphological correlates that appear to be adaptations to exudates as food. At least 75 species of primates consume some exudates. Variability of diet among marmosets and tamarins precludes simple classifications of the former as year-round specialists vs. the latter as always facultative seasonal users of exudates. Differences in exudate use among callithrichines, now also including callimico as an exudativore, are associated with apparent adaptations in gut anatomy and functioning, a suite of dental and jaw features, and some features of socioecology and life-history. Among strepsirrhines, several Nycticebus species are newly known to gouge to eat gum, variability among mouse lemurs in gum use has been documented, but little added work has improved our knowledge of variation in exudate use in galagos. For these taxa, much less is understood about possible morphological, behavioral and life-history adaptations and detailed descriptions of behaviors associated with exudate acquisition are needed from the field. The ability to identify anatomical features that will clarify the role of exudates in the diets of fossil primates remains a major challenge.

Introduction The present book, for which this chapter serves as an Introduction, grew out of a symposium held at the 2008 Congress of the International Primatological Society (IPS) in Edinburgh, Scotland. This symposium was organized to bring together in one place and at the same time researchers from many diverse fields (ecology, behavior, morphology, nutrition, and conservation) that all converged on the topic

L.T. Nash (*) School of Human Evolution and Social Change, Arizona State University, Tempe, AZ 85287-2402, USA e-mail: [email protected] A.M. Burrows and L.T. Nash (eds.), The Evolution of Exudativory in Primates, Developments in Primatology: Progress and Prospects, DOI 10.1007/978-1-4419-6661-2_1, © Springer Science+Business Media, LLC 2010

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of primate exudativory and how it has evolved. Despite the fact that one of us (Nash 1986) published a review nearly 25 years ago on the dietary, behavioral, and morphological correlates of primate exudativory, much remains to be understood about this relatively rare dietary niche. We have envisioned this chapter as both an introduction to the other chapters in this book and as a brief overview and update of the 1986 review (Nash 1986). We have blatantly borrowed the overall structure of that review for this chapter. That review described “aspects” of “gummivory” in primates. The title we have chosen for this volume is somewhat more ambitious, as our aim is to address the “evolution of exudativory.” In 1986, exudativory as a dietary niche was relatively unknown and thoroughly under-studied. Many new developments have occurred since then including which primates consume gum, the socioecological correlates of exudativory, behavioral and morphological adaptations to locating, accessing, consuming, and digesting exudates, and even the role exudate-feeding may have played in the origin of primates. The encouraging point is that today one paper, such as this one, cannot be an exhaustive review of the current state of the work on exudativory in primates. This book approaches that. This increase in appreciation of the ramifications of exudate-feeding in primate biology is dramatic; however, so too are the remaining gaps in our knowledge on the topic. Our goal for this chapter is to provide the context of the remaining chapters. Our greatest goal for this book is to stimulate further work that lets us get unstuck from some of the questions that remain. We have chosen the term “exudativory” in preference to “gummivory” as a more inclusive term. We have left it to each author to be more specific as the context of their data and discussions dictates. Exudates consumed by primates include gums, saps, nectar, and, more rarely resins and latex (Power, Chap. 2). Nectar is not explicitly addressed in this volume, though a number of species such as Eulemur spp., Galago senegalensis, and Otolemur crassicaudatus will visit flowers and lick them without destroying them (Sussman and Raven 1978; Charles-Dominique and Bearder 1979; Nash, pers. obs.). Resins are not eaten by primates but some ­primates may consume latex. Latex is sticky, chemically complex, contains proteins and a variety of secondary compounds, and has evolved as a defense against insect damage to plants in leaves and reproductive parts (e.g., latex in figs) (Agrawal and Konno 2009). For example, two of the three most frequently eaten plants that Lepilemur leucopus consumes in southwestern Madagascar at Beza Mahafaly Reserve have sticky, milky, sometimes irritating, exudate that appears to be latex (Nash 1998). The chemical composition of such plants remains to be fully explored (Power, Chap. 2). The majority of the exudates to be discussed in this book are gums (water-soluble, viscous exudates found just deep to the bark) and saps (water-soluble, viscous ­exudates found deeper in the xylem and phloem). Most of the gums come from nonreproductive parts of the tree, are produced in response to insect or mechanical damage, and are not produced to attract animals to service the plant, in contrast to nectar (Power, Chap. 2). However, pod gums, as consumed by some neotropical primates (Power, Chap. 2, Smith, Chaps. 3 and 5; Garber and Porter, Chap. 4) may

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be exceptions to this generalization. Saps present a special problem: in order to be accessed, the bark of the tree must be broken through sufficiently to reach this deeply located resource. For the most part, only primates that can specifically gouge into the bark, such as marmosets, access sap. This leads to an important distinction between primates which can properly gouge and those which cannot or do not – a key topic in many of the chapters of this book (see below). However, Joly-Radko and Zimmermann (Chap. 7) have documented a case of “sap eating by proxy” in cheirogalieds that eat the “honeydew” produced by sap-sucking insects. To date, this form of exudativory has not received much attention and involves a potentially complex web of ecological relationships among primates, insects and plants that deserves further study. Such a complex web of ecological interactions has been described among a ­gum-eating Australian marsupial, the sugar glider (Petaurus breviceps), wattle species (Australian Acacia trees) that produce gum, sheep, beetles, and eucalyptus trees (Smith 1992). Sugar gliders are convergent with Galago moholi and G. senegalensis in their habitat preference and dependence on Acacia gum in the cold season when insects are rare (Harcourt 1986). While galagos leap, the small marsupials glide between trees. Sugar glider density is positively associated with wattle (Acacia mearnsii) density (Smith 1982; Suckling 1984). In areas with heavy sheep grazing, the seedling wattles are grazed so they regenerate poorly. Like G. moholi and G. senegalensis, gliders incorporate insects as a major portion of their diet in seasons when they are available. The gliders are an important biological control on leaf-defoliating scarab beetles. When weather conditions are suitable, beetles proliferate and may defoliate eucalyptus timber species producing a “dieback” condition that can kill the trees. Thus, key elements for maintaining forest health and dieback resistance in these rural ecosystems are sugar gliders and wattles. Keeping these species in the habitat requires controlling grazing to allow wattles to regenerate so gliders have a winter food supply of gum. To our knowledge, no primate exudativore has been shown to have such a critical role within an ecosystem, but this is due to our ignorance of their ecological webs. Ideally, we hope this book can stimulate more research on all types of exudates which will integrate information on the behavior of exudate eating, the reasons plants or other sources produce ­exudates, the composition and distribution (in time and in space) of exudates that primates eat, the ecological roles of exudates and exudate consumers, and the morphological adaptations that allow animals to access this food resource. Returning to the title of this book, by explicitly incorporating the word “evolution” in the title, we hoped contributors would address possible behavioral and morphological adaptations in primates associated with exudate consumption and address these adaptations in the fossil record. We find there is much remaining to be adequately tested in identifying such adaptations, especially with regards to the fossil record. Many of the apparent adaptations may be “clade dependant” and not occur in all primate exudativores. A major issue (see below) is whether there are, as yet, any reliable signals from the hard anatomy (i.e., skeletal and dental characters) identifiable in fossils that would truly allow us to document the history of exudate consumption in the course of primate evolution.

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A note on taxonomic usage is in order. In this chapter, we follow Groves (2001, 2005) using “strepsirrhines,” “haplorrhines” and “callithrichines.” We have not attempted to force a single taxonomic usage on all authors. Instead, we have requested that each provide citations to their choice of taxonomy for the primates. However, the main differences across chapters are in lower level taxonomy (e.g., marmosets and tamarins as a separate family or subfamily, appropriate genus and species names). Most authors follow the same subordinal taxonomy within primates as used in this chapter.

Exudates as a Primate Dietary Component Updates on Primate Exudativores The knowledge of the major genera and higher taxa of primates that consume ­considerable amounts of gum has changed over the years and good major overviews can be found in recent reviews about primates (Committee on Animal Nutrition 2003; Campbell et al. 2007) and in Smith (Chap. 3). This chapter reviews over 130 sources to document 69 primates that consume exudates from over 300 plant species. As was previously known, strepsirrhines and callithrichines consume the greatest volumes of exudates relative to their entire diet while patas monkeys, some vervets, and baboons also consume considerable volumes. Occasional use of pod exudates in Lagothrix and occasional gum consumption in some langurs, macaques, forest guenons, and chimpanzees are now also known. As Smith points out, his list likely misses a number of noncallithrichines and non-Malagasy strepsirrhines due to a lack of comparable detailed field work on such species. It is notable that the Committee on Animal Nutrition of the National Academy of Sciences has now recognized “gums” as a major component of some primates’ diets, as this has implications for captive husbandry (see below and http://www.nap.edu/catalog. php?record_id=9826#toc). Among strepsirrhines, one of the most remarkable and newly documented ­findings is the use of exudates by a number of Asian lorises which gouge or scrape to acquire them (Tan and Drake 2001). Nekaris et al. (Chap. 8) amplify these observations extensively and show that Nycticebus consumes gum. Ironically, though galagos were among the first primates to be noted as major exudativores, there has been little recent detailed fieldwork on them or any African lorisoids that has focused on feeding patterns. As some of our earliest information on primate exudativory came from galagos (Bearder and Martin 1980a) it is ironic that the African strepsirrhines are now one of the taxa where the least amount of progress has been made in understanding their diversity of exudate use (Bearder et  al. 1995; Pimley et  al. 2003, 2005a, b; Nekaris and Bearder 2007), even as the number of species recognized has exploded (Grubb et al. 2003). Thus, it is unknown how these galagos and pottos compare to Asian lorises in their consumption of exudates and why they differ.

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We greatly need more detailed information on the diversity of which exudates are eaten and how they are acquired for both African and Asian strepsirrhines. Génin has provided important novel data on gummivory in mouse lemurs in western and southern Madagascar (Génin 2003; Génin et al. 2005; Génin 2007, 2008). For example, he has shown that gray mouse lemurs compete intraspecifically for access to gum and females dominate males in accessing gum sources. He also documents the first case of Phaner dominating Microcebus murinus at gum sources in Kirindy. In western forests, mouse lemur species eat gum more seasonally or not at all. In contrast, at Berenty Microcebus griseorufus use gum year round and consume fruit seasonally, though less gum is used in wet than dry years (Génin 2008; Génin et al., Chap. 6). They argue that gum may be a more reliable and rapidly renewing carbohydrate source than fruit where rainfall is unpredictable and argue that gum use may be a primitive adaptation in all cheirogalieds. They hypothesize that El Niñoassociated unpredictable droughts are associated with the localities around the world where exudativory is particularly prominent in primates and other rare mammals that consume gums. The possible diversity among mouse lemur species and populations in consumption of gum, as with galagos, may provide opportunities for future comparative work in both behavioral and morphological adaptations to exudativory. As illustrated by Génin’s work, such comparisons allow for testing the socioecological model as applied to the ecology and behavior of a relatively nongregarious primate and may help understand the origins of primate gregariousness. The hypothesis that the evolution of gummivory is associated with an unpredictable environment is bolstered by the recent first fieldwork on Allocebus trichotis in Madagascar which suggests that, as predicted from its dental morphology, gum is probably a major part of its diet (Biebouw 2009). It is hoped that more detailed information on its feeding ecology will become available in the near future. As mentioned above, more detailed work on consumption of “honeydew” (a sap derivative) by Cheirogaleus provides another variant on exudate use for comparative work (Joly-Radko and Zimmermann, Chap. 7). Turning to haplorrhines, it was recognized in the 1980s that baboons were one of the largest-bodied primates that eat gum. What is new is the case that Altmann (1998) makes for the importance of gum in the diet of juvenile baboons. It is a very important source of energy in the juvenile’s diet, which, in turn, is one of the strongest correlates of adult female’s fitness. Some populations of chimpanzees consume gums as part of their diets (Ushida et al. 2006). While it seems that these chimpanzees gain negligible energy from the gums, they do seem to gain sufficient amounts of various minerals (calcium, magnesium, manganese, and potassium) to fulfill their daily requirements for these minerals. Body size, as well as the nature of other dietary components, may influence different nutritional advantages for exudativory across primates (Power, Chap. 2). Isbell’s work comparing gum use in sympatric vervets and patas monkeys is a model of the possibilities of comparative work in understanding the processual events in the evolution of exudativory as a dietary niche (Isbell 1998; Isbell et al. 1998). Patas monkeys in East Africa feed primarily on gums, a rarity among adult Old World monkeys. Isbell and colleagues have shown that the development of this

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odd dietary niche for a relatively large-bodied Old World monkey may have been driven in part by their notably long limbs which allow them to cover a wide geographic range in a given time to gather gums. In addition, these large monkeys seem to be able to subsist primarily on exudates because substantial volumes of arthropods are associated with the gums and consumed along with them. The consumption of gum by patas monkeys, baboons, and living humans has even been incorporated into reconstructions of the diet of early hominins (Copeland 2007). In the Neotropics, an important outcome of continuing fieldwork is that it is now clear that a simple distinction between marmosets as year-round gum specialists vs. tamarins as seasonal gum users is oversimplified, though it is a model that is very influential in morphological studies of exudativory (see below). There is considerable diversity in the extent to which gums are eaten within marmosets, within tamarins, and even within the same genus of these groups (Smith, Chap. 3). The extent to which this diversity within marmosets or within tamarins is incorporated into anatomical studies is quite variable. However, it has countered the suggestion that nails were adaptations to trunk exudativory (Sussman and Kinzey 1984) as it now appears that the ancestral callithrichine probably engaged in a variety of trunk foraging behaviors, not just gum eating (Garber et  al. 1996). Callimico, whose diet was very poorly known in 1986, was then thought not to eat exudates. As reported by Garber and Porter (Chap. 4), callimicos are now known to feed extensively on two items unusual in primate diets: fungi and both trunk and pod exudates (see also Porter and Garber 2004; Porter 2007; Porter et al. 2009). Garber and Porter elaborate here on how important various exudates may be for some nongouging callithrichines throughout all or much of the year.

Exudates as Fallback Foods and Primate Feeding Adaptations A number of authors in this volume as well as others (e.g., Harrison and Tardif 1994) draw a distinction between “specialist” or “obligate” exudativores and “facultative” or “nonspecialist” consumers of exudates. The criteria for obligate exudativores generally included use of gum across all seasons and the possession of morphological features associated with gum procurement or digestion including small body size, sharp or claw-like nails, dental features associated with gouging, and an expanded gut (especially the cecum) for fermentation (see further on anatomy below). A consumption distinction that recurs in many chapters in this volume is the extent to which gum is used by a given species or population as a “preferred food,” a “fallback food,” or as a “keystone” food – and if gum sources can fill more than one of these roles. These concepts are invoked in most chapters in this volume and sometimes are treated as if the concepts of keystone food and fallback food are interchangeable. However, it is best to keep the notions separate (Marshall and Wrangham 2007). The concept of “keystone species” refers to one that is essential to the structural and functional integrity of an ecological community, not just one species, but those keystone effects can be context dependent and may be seasonal

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(Peres 2000; Christianou and Ebenman 2005; Collinge et al. 2008). There is much discussion of how to define and to identify a keystone species in the ecological literature that is beyond our objectives here (Davic 2003; Christianou and Ebenman 2005; Hodges 2008, Fedor and Vasas 2009; Jordán et  al. 2009). To what extent exudativorous primates or the plants from which they consume exudates are keystone species, in the sense that sugar gliders may be in the example presented above, is not know for any primate. Peres (2000) has made the case for one type of exudate, the pod gums from Parkia trees, as a keystone resource in some Neotropical forests. It is clear that for many primates exudates may be important fallback food. Fallback foods are defined as foods eaten when preferred foods are not available (Marshall and Wrangham 2007) and are expected to be of poorer nutritional content and/or more difficult to process than preferred foods. These authors argue that fallback foods, while often consumed seasonally, in some cases may be eaten year round. Their key to identifying a fallback food is that it be eaten in amounts inversely related to the availability of preferred foods. This criterion requires (1) data on the availability of all food types, and (2) identification of preferred foods. Preferred foods are those eaten in excess of their availability; neither availability (rarity) nor frequency of consumption alone defines a preferred item. Preferred foods are argued to primarily drive harvesting adaptations (perception, spatial navigation, cognition, and locomotion), while fallback foods shape processing adaptations (dental and supporting morphology, gut anatomy and kinetics, body size, tool use). Marshall and Wrangham (2007) distinguish within fallback foods staple fallback foods (those that can seasonally be the sole food eaten) and filler fallback foods (those that are never the whole diet). Acacia gum would be a staple fallback food for G. moholi (Bearder and Martin 1980a). Compared to staple fallback foods, filler fallback foods are ­predicted to fluctuate less in availability through time, engender less feeding competition, allow more stable grouping patterns, and be associated with faster life-histories. Lambert (2007) emphasizes that identifying feeding adaptations requires ­establishing linkages of variables at all scales of organismal biology: individual ­intragenerational, individual intergenerational, population and species. The chapters in this volume mainly focus on the latter two levels of scale and on craniodental morphological features. Both the models of Lambert (2007) and Marshall and Wrangham (2007) may be helpful in the future in organizing approaches to understanding the adaptive pressures exudativory presents and may be able to be integrated (Constantino and Wright 2009; Lambert 2009; Marshall et al. 2009). In order to decide if exudates are fallback foods we need better information on their bioavailability of nutrients (Power, Chap. 2) and on measures of their availability across the seasons (see below). We need to decide if they are staple or filler fallback foods. For example, some of the newly studied lorises eat gum year round, and others have not yet been studied across all seasons of the year, so the role of gums as fallback foods is as yet unclear (Nekaris et al., Chap. 8). Lambert (2007, 2009) suggests we focus on both “fallback foods” and “fallback strategies.” As useful as these models may be, the situation of exudate-feeding on trunk and pod gums in Callimico may not be a close fit to either. Porter et  al. (2009) and

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Garber and Porter (Chap. 4) question to what extent gums are fallback foods. They consider evidence that the evolution of the gut’s ability to digest gum may have been a result of adaptations to another preferred diet item – fungi. Part of their critique is based on the possibility that pod gums are more digestible (see below for further discussion of this point). Thus they question to what extent different sorts of processing and harvesting adaptations are, or are not, associated with fallback foods. Génin et al. (Chap. 6) also show the complications in the “fallback” categorization in that they explicitly introduce the notion that environments that are “hypervariable” over longer time scales than a single year may be key in understanding which species eat gum and geographic variation in eating this food. Though the time scale is different, they, like Garber and Porter (Chap. 4) raise the issue that the association of “fallback foods” with adaptations to harvesting vs. processing is more complex than suggested in the Marshall and Wrangham model (Marshall and Wrangham 2007). The cognitive, social and life-history ramifications of gum use have barely been addressed. Between the obligate exudativorous marmosets and the facultative exudativorous tamarins, where there is clear morphological distinction in the dentition, exudate usage has been interpreted to have ramifications in behaviors as diverse as the ability to delay rewards, the degree of sex differences in territorial behavior, infant carrying, and group stability (Ferrari and Lopes 1989; Harrison and Tardif 1994; Stevens et al. 2005). The extent to which these differences can be generalized to other primate taxa, for example, lorisoids or lemuroids, remains to be examined. For example, while Cebuella may tend to focus their territory on one or a few gum trees in their small territories, this is not the pattern that is found among galagos. The lack of good field or captive data comparing cognitive or social differences among galagos and lorises that do and do not use gums extensively would be informative. It is clear that the general social differences among nocturnal strepsirrhines do not covary in a simple way with the use of exudates for either lemurs (Schülke and Ostner 2005) or for galagos and lorises (Bearder and Martin 1980b; Clark 1985; Harcourt and Nash 1986a; Nash and Harcourt 1986; Harcourt and Bearder 1989; Nekaris and Bearder 2007). It has been argued that Phaner and some marmosets, though not Cebuella, share a situation where the use of reliably located gum resources that are quickly depleted, rapidly renewing, and are monopolizable but not clumped, allows group members to feed near each other. This sets up a situation where the balance of within and between group scramble and contest feeding competition favors a social and life-history pattern of delayed natal dispersal (Schülke 2003; Schülke and Kappeler 2003) which is absent in sympatric relatives of these species which do not use gum (i.e., Cheirogaleus or tamarins).

Factors Influencing Selectivity in Exudate-Feeding Factors influencing selectivity include those involved in both the harvesting and processing of exudates. We have much to learn about which primates eat exudates, which plant species are accessed, which exudates are used, when exudates are

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consumed, and why a particular location or “glob” of exudate is chosen. Globs may be large or tiny relative to the consumer, old and hard or young and liquid, crystallized or liquid under a dried “skin,” and variously colored (and presumably varying in taste and scent). Globs may also be located in different parts of the plant. We are only beginning to understand the factors that influence why exudates are eaten by a primate at a particular place and time. Some of the main challenges are (1) understanding the nutritional gain from exudates and the problems exudates present to digestion, (2) identifying costs and benefits to the animal of harvesting different types of exudates based on where the plant produces them and whether or not harvesting exudates has any benefits to the plant producer, and (3) from the perspective of primate consumers, measuring availability of an exudate and “patchiness” of its distribution in time and space.

Digestive Challenges and Nutrients in Gum Since most of the exudates consumed by primates are gums, it is not surprising that most work on the nutritional benefits and digestive problems of exudate consumption has been directed at gums. As detailed by Power (Chap. 2), gums are water soluble, low in protein, high in some minerals, and mostly beta-linked complex polysaccharides which are not digestible by mammalian enzymes. They are assumed to mainly be eaten for their energy content, but the carbohydrates must be fermented to be bioavailable. However, both between and within plant species, there are differences in the solubility (which influences fermentability), constituent sugars, and secondary compounds (“antinutrients”) found in gums (Génin et al., Chap. 6, Hladik et al. 1980; Lambert 1998; Génin 2003; Wiens et al. 2006). For example, we know that exudates from plants of the pea-family (Fabaceae) are favored across most primates (Smith, Chap. 3) and specifically by Asian lorises (Nekaris et  al., Chap. 8) but we don’t know why. Lemurs seem to have developed the ability to tolerate a variety of secondary compounds (Ganzhorn 1992). Do they differ from other strepsirrhines in selecting exudates based on these antinutrients (Reed and Bidner 2004)? Power (Chap. 2) also points out that commonly used conversion ­factors for protein content, based on nitrogen content, may be problematic and inflated, and not the same as “bioavailability.” Though relative values within a study may be correct, this may cause problems comparing across studies of different primates and different plants. In addition to energy content, early hypotheses of gum consumption suggested that since it was high in calcium and low in phosphorus, it complemented the reversed ratio found in insects and some fruits (Bearder and Martin 1980a), especially during gestation and lactation (Garber 1984). In a review across primates, Smith (Chap. 5) does not find support for the “cost of reproduction” hypothesis of gum consumption. However, Garber and Porter (Chap. 4) argue that seasonal differences in the nutrient and the anti-nutrient contents of gums may be a factor in gum consumption.

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Digestible Energy form of Trunk Gum vs. Pod Gum vs. Honeydew There are various suggestions or direct claims that different types of exudates differ in the nutrients they provide to primates. Joly-Radko and Zimmermann (Chap. 7) indicate that when both are available in a mouse lemur’s range, honeydew is preferred to gum. This may imply that it is more nutritious than gum, since the sap has been predigested by the insects that exude the honeydew. Based on the notion that plants make their parts attractive through higher nutritional value when consumption of the part services the plant, Smith (Chap. 5) and Garber and Porter (Chap. 4) argue that pod gums should be more digestible and attractive when compared to trunk gums because pod gums are a reward to seed dispersers. However, we really do not yet know if these supposed differences are real for the exudate consumer. Power (Chap. 2) makes an important distinction between food (what is consumed) and nutrients (what the animals need and actually get out of the food). He points out that chemical analyses can be misleading if analytic methods are not fully understood, that some analyses do not reflect the results of digestion, especially where fermentation is involved, and that they do not tell you whether potentially available energy is actually used. Only feeding trials can do this. However, some field observations may be suggestive of energy payoffs of gum. Génin et al. (Chap. 6) show a lack of sex difference in M. griseorufus gum feeding but that females are both heavier and feed more on fruit than males. This suggests that the energy payoff in favor of females comes from fruit, not gum. We need to be more critical “consumers” of chemical analyses of gums as we attempt to make interpretations of their digestibility and quality as a food resource. Because of the digestive challenges presented by gums, differences in gut anatomy and kinetics have been associated with differences in gum use (see below). Heymann and Smith (1999) found that wild tamarins concentrated gum consumption late in the day. This was interpreted as behavior which held the gum in the gut during the night when defecation was less common so that it could be fermented longer. Smith (Chap. 5) replicates and extends a previous finding from the same site showing that tamarins consume trunk gum but not pod gum more in the late afternoon, when it is likely to be retained in the gut overnight. Interestingly, this would seem to be a “harvesting adaptation” that is associated with a nonpreferred, probably fallback, food (contra Marshall and Wrangham 2007). In contrast, Porter et al. (2009) did not find the temporal patterning of trunk and pod gum consumption in Callimico to correspond to the predictions that pod gums would be more digestible and thus eaten more in the morning. They found a pattern of trunk and stilt gums being eaten more in the morning and pod gums being eaten more in the afternoon. Génin et al. (Chap. 6) reverse the argument by suggesting that gums eaten by mouse lemurs are readily digestible because they are consumed throughout the active period, i.e., the night (but see below, and Powers, Chap. 2, concerning gut kinetics of liquids vs. solids).

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Measuring Distribution and Seasonality of Availability and Its Consumption The challenges of measuring exudate consumption in ways that are comparable across species and populations are not new to primatology (Altmann 1974; Ray 2007). Examples of the differences in approaches are found by contrasting the chapters in this volume by Génin et al. (Chap. 6), Garber and Porter (Chap. 4), JolyRadko and Zimmermann (Chap. 7), and Smith (Chap. 5) for different species and sites. Sampling methods, definitions of behavioral categories, and specific dependent variables used rarely are directly comparable. Some studies assess changes (e.g., seasonal) in use of different exudates without assessing availability independently of use. However, the latter is critical for testing various hypotheses about anatomical, social, and cognitive correlates of food availability. Exudates are quite challenging when it comes to measuring availability and quality. Distribution of food patches also varies on spatial scales, which can range from an intercontinental scale down to variation within a single plant. Distribution can also vary on a time scale ranging from years to the rate of renewal at a single glob. Despite these challenges several chapters do offer insights about the availability of exudate foods and the consequences of those patterns of availability (Génin et al., Chap. 6 and Joly-Radko and Zimmermann, Chap. 7). Although Garber and Porter (Chap. 4) have countered the notion that nongougers are aseasonal in use of gums, they do suggest that tamarins and callimico may have different cognitive skills to track the differing availability (renewal rates) and locations of their exudate resources. Like Nekaris et  al. (Chap. 8) and Génin et  al. (Chap. 6), their studies focus on renewal rate with various experimental approaches, though the methods used varied widely across these studies as did the results and conclusions. Clearly, some form of standardization against which to judge experiments on exudate renewal time is needed (hourly? daily? longer periods?). The difficulties in assessing gum availability and the factors that might influence foraging on exudates are illustrated by the limited success in explaining interpopulation differences among pygmy marmosets in the time spent feeding on exudates and in the specific exudate species used. Yépez et al. (2005) found that the time spent feeding on gum did not correlate with the number of exudate species available nor the abundance of exudate trees in each area. Within each population, an exudate species’ relative abundance was unrelated to its relative time of consumption and the number of species consumed was unrelated to group size, range size, or amount of sampling effort. Other factors proposed which might relate to the consumption differences were the chemical (nutritional) content of exudates, the hardness of the wood (increasing gouging time), the viscosity of the exudates, and degree of human disturbance of the animals. Approaches to measuring seasonality of exudate resources and patch sizes are quite variable. Génin et al. (Chap. 6) measured distribution of whole gum trees as patches while Garber and Porter (Chap. 4) tried to monitor individual natural and

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artificial gum “sites” within trees. Isbell (1998) went further in her study of patas monkey gum use as she measured the height of each tree, and, when gum was present, the number of gum sites and their heights in the tree. She also visually estimated the surface area of each gum site, and, for globular gum, the volume. Clearly, there is much yet to be done to assess why, where and when primates consume gum.

Anatomical Adaptations to Exudativory Just what does it mean to be a “gum specialist?” Is this defined on the basis of the amount consumed, the seasonality of use, or anatomical specializations that relate to it? Across chapters in this volume criteria are used in varying combinations and sometimes leading to contradictory classifications of different species. For example, Génin et  al. (Chap. 6) seem to use year-round consumption at a high level (diet 75% gum) as a criterion for specialist. Other chapters imply that there must be specific anatomical features associated. In a related vein, Rosenberger (Chap. 14) discusses the continuing debate about the role of frequency of use vs. “critical function” use in driving the evolution of anatomical features associated with exudate acquisition and consumption.

Cranial and Dental Anatomy: The Problem of “Gouge” vs. “Scrape” As a dietary niche exudativory presents two large challenges: accessing exudates and digesting them. In 1986 we seemed to have a fair understanding of how animals accessed exudates: callithrichines made use of their “short-tusked” anterior dentition to gouge tree trunks and elicit exudate flow, and the exudativorous strepsirrhines made some kind of use of their toothcomb to access exudates. However, chapters in this book reveal an entirely less clear picture of how the strepsirrhine exudatefeeders (which now include added taxa such as lorises and mouse lemurs) use their dentition in acquisition (Nekaris et  al., Chap. 8; Burrows and Nash, Chap. 11; Stephenson et al., Chap. 12). Génin et al. (Chap. 6) document M. griseorufus scraping bark to stimulate gum flow. Nekaris et al. (Chap. 8) describe in exemplary detail the sights (and sounds) produced by Nycticebus gum-gouging behavior. They suggest that differences in gum feeding may be associated with some of the variation in body size and craniodental morphology within Asian lorises. They report that the toothcomb may be used by Nycticebus to gouge and scrape gum and that these animals may chew on strands of gum with their molars. In contrast, among galagos, Burrows and Nash (Chap. 11) indicate that the toothcomb may not be an important acquisition tool in galagos, but that the more posterior dentition may be more useful. Part of the difficulty in understanding dental characters and acquisition behavior in strepsirrhines is that we do not have clear detailed descriptions of how these taxa

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use their teeth to gather gum. Nekaris et al. (Chap. 8) provide the kind of detailed descriptions for some of the Asian lorises that are needed for other species. They provide photographs of the holes some species gouge and descriptions of the sounds of teeth working on branches that make it clear that gouging is certainly occurring. Particularly strong “gouging” is sometimes described for Phaner, Euoticus, and Allocebus, but the descriptions we have of actual acquisition behavior and which teeth are used are minimal (see below). Among lemurs, galagos, and Asian lorisids, it is likely that there is behavioral variability across species which could easily be described as gouge, scoop, puncture, prise, scrape, or lick as well as the vague “collect,” “glean,” or “acquire.” Clearly, for these nocturnal forms it will be more difficult than with the diurnal callithrichines to get good, ideally quantified, behavioral data. With available low-light video cameras, it may be possible. Such data are critical to solving the problem of possible dental morphological “adaptations” to exudate-feeding. An anecdote from personal experience of LTN with captive G. senegalensis may be useful. They were offered a paste of Acacia gum on a fingertip. First they licked extensively and with a very long tongue extension. As the gum became depleted, they gently scraped along the finger, but probably not hard enough to break really hard dried gum. However, the very similar G. moholi will leave scrape marks from its toothcomb after some feeding activities (Bearder and Martin 1980a). Rosenberger (Chap. 14) discusses the debate about the overall function of the toothcomb, how it may have functioned in the earliest primates that possessed one, and whether a toothcomb itself is a reliable indicator of exudate-feeding in the fossil record. One of the challenges to our understanding of the dental and cranial characters involved with exudate acquisition, both in callithrichines and in strepsirrhines, is the following question: Does gouging and/or scraping require the generation of high forces at the anterior dentition? Yes, (Dumont 1997) and no (Vinyard et  al. 2003; Taylor et al. 2009) and maybe (Burrows and Smith 2005). Dumont (1997) found several cranial characteristics in both strepsirrhine and callithrichine exudativores consistent with generating high forces, but Vinyard et al. (2003) found few characters associated with generating high forces. Instead, they found features consistent with generating an increased gape size specifically in callithrichines. Using the exudativorous galago O. crassicaudatus and the frugivorous Otolemur garnettii, Burrows and Smith (2005) found a mixed bag with some characters consistent with generating a high force at the anterior dentition and some consistent with generating a larger gape. Recently, Taylor et al. (2009) have found fiber characteristics of the temporalis and masseter muscles in gouging callithrichines associated with generating a large gape size but not high forces. In the 2008 IPS symposium, Taylor, Vinyard and White presented data comparing the trigeminal nuclei (which give rise to the trigeminal nerve, the motor supply of the temporalis and masseter muscles) in Saquinus oedipus and Callithrix jacchus. These results suggested that gouging may affect the size of the proprioceptive pathways but not the motor pathways associated with the jaws. Several chapters in this volume bring the question of “increased force” vs. “increased gape” to the forefront (Ravosa et  al., Chap. 9; Mork et  al., Chap. 10).

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Ravosa and colleagues present a review of the cranial characters associated with primate exudate-feeding in both callithrichines and strepsirrhines. They synthesize results from many studies to demonstrate that there indeed are some features in the skulls of exudate-feeders associated with generating a greater force at the anterior dentition and that some are associated with generating an increased gape. They also demonstrate the anatomical trade-offs involved in generating higher forces and in generating a larger gape but they point to a greater body of evidence supporting the importance of the latter at the anterior dentition in exudativorous primates. Down at the microanatomical level of the skull, Burrows and Smith (2007) examined the cartilaginous structures of the temporomandibular joint (TMJ) in O. crassicaudatus and O. garnettii. They found characteristics that suggested the ability to withstand compressive forces at the TMJ articular cartilage that may be associated with exudate-feeding. In a similar study that used gouging and nongouging callithrichines, Mork et al. (Chap. 10) found a mix of microanatomical characters in the TMJ articular cartilage that are both consistent and inconsistent with expectations of how the articular cartilage would be loaded at large gapes. Their findings along with those of Burrows and Smith (2007) reinforce the mosaic nature of morphological associations with exudativory and the potential pitfalls of inferring behavior based upon morphological characters. In the current volume, both Ravosa et  al. (Chap. 9) and Mork et al. (Chap. 10) point to the need for more species to be studied for both behavior and morphology and the value of ontological studies of morphology. Rosenberger (Chap. 14) presents a hypothetical model of morphological characters that might be related to the biomechanical problems associated with gouging and scraping (“gleaning” in his terminology) exudates and how these characters may be reflected in the primate fossil record. He uses plesiadapiforms in his discussions of the earliest primate and evaluates the potential role exudate-feeding may have had in primate evolution and in the lifestyles of the plesiadapiforms. In his chapter, Rosenberger makes a plea for the use of tooth wear as a characteristic of considerable weight when evaluating morphological signals of exudativory. Rosenberger’s chapter continues, and certainly does not solve, the debate about the functional reasons toothcombs evolved (diet, and which diet, or social, i.e., grooming, behavior). One of the key pieces of data missing from a more complete answer to this question is material properties and hardness of the plants being gouged and/or scraped. As was found with different parts of bamboo, which sometimes have different mechanical properties and sometimes did not (Yamashita et al. 2009), different kinds and locations of gum may produce different mechanical effects that need to be accounted for in comparative work on morphological adaptations associated with exudate-feeders. As is apparent, one of the problems we face is a proper accounting of the acquisition behavior. A problem in the literature is that behaviors hypothesized based on anatomy in an original citation became “reified” in a secondary source which states the behavior happens and then a third source cites the second. This becomes analogous to the children’s game Americans call “playing telephone” or “gossip” (see http://www.Wikipedia.org “telephone game”) where a message is more garbled the more people it passes through. For example, in describing Phaner, Euoticus, and Allocebus, LTN stated.

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Phaner and Euoticus, the most gummivorous lemuroid and lorisoid, respectively, possess a caniniform first upper premolar. This has been suggested as an adaptation for gouging, but the detailed behavioral observations needed to confirm this function are lacking (Charles-Dominique 1977; Charles-Dominique and Petter 1980). A. trichotis, a cheirogalid, also shows this dental trait. It is known only from two museum specimens (Tattersall 1982). Based on head lengths of the specimens, it is about the size of G. senegalensis or Cebuella. Unfortunately, this species is exceedingly rare or extinct (Tattersall 1982), so that the extent of gummivory in its dietary adaptation may not be established with certainty. Nash (1986, p. 125)

This was based on the following, which are all that are provided by CharlesDominiques’ direct observations of Euoticus or Phaner: “The author has… (observed) Euoticus… visiting certain wound areas on trees where tiny droplets of gum were forming, and collecting the exudate by licking or scooping with the toothscraper.” (Charles-Dominique 1977, p. 42) and Phaner… uses its long tongue and also the narrow and procumbent tooth comb to scoop the gum which would otherwise be inaccessible without such a “tool.” Phaner furcifer is also characterized by the development of the upper first premolar (caniniform). This peculiarity, seen only in A. trichotis, among Malagasy lemurs and Galago (Euoticus) elegantulus, among African Lorisids, appears to be an adaptation for the extraction of vegetal exudations. Charles-Dominique and Petter (1980, p. 78)

Nevertheless, some authors use Nash (1986) as the citation to support that Phaner, Euoticus or even Allocebus gouge into bark and are known to have a diet high in gouged gums – “On the one hand, they [gums] account for the major part in the diet of P. furcifer (65%) and A. trichotis.” (Viguier 2004, p. 496). Others recognize that dietary interpretations of Allocebus are based on morphological analogy to Euoticus (e.g., Masters and Brothers 2002). We now have the very recent field work of Biebouw (2009), which indicates that a major part of the diet of Allocebus is, indeed, gum. The details of how they acquire it, though, are yet to be described. The same is true for Phaner and Euoticus.

Soft Tissues: Guts, Tongues, and Pelage The chemical structure of exudates, and certainly gums, presents digestive challenges (Power, Chap. 2). If they must be fermented in the digestive tract, we also expect, and have found, that the size, proportions, and kinetics of the gut are associated with the degree of gummivory in primates. Gum needs to remain in the gut for a longer time vs. other foods in order to be fermented. Power points out that the relationships among gut morphological variables and gut kinetics are complex. Lambert (1998) noted that there is only a weak relationship between gut transit time and body size. Gut transit time is influenced by the competing problems of absorption vs. processing (Power, Chap. 2). Another problem is to what extent primates show “modularity,” i.e., the ability of an individual or species to regulate digestion relative to the current diet (Lambert 1998).

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The best data we have on digestive adaptations of the gut, as with other morphological features, comes from contrasts within the callithrichines (Power, Chap. 2). Marmosets seem to have more capacious hindguts than tamarins. Power emphasizes the differences in how the anatomy and activity of the gut can vary independently of each other. Measuring gut kinetics can be tricky, as it is ideal to have separate markers for the solid and fluid fractions of the digesta. In addition, different size solid markers may give different results, complicating comparative studies. This is important because it has been hypothesized that gum eaters may have a “cecal-colonic separation mechanism” that selectively retains the gum (which is soluble) in the gut relative to solids (e.g., seeds, insect exoskeletons) (Caton et al. 1996, 2000). Captive G. moholi that are fed a diet mostly of gum show the expected slower gut transit time of the fluid digesta compared to the solid fraction. The ecologically similar G. senegalensis has been shown to slow overall transit rate (as indicated by solid markers) when shifted from a diet high in fruit to one high in gum (Nash 1989). Power indicates the complexity of unraveling the adaptations when he shows that within callithrichines there may not be simple correlations between proportion of gum eaten and gut kinetics. His work on marmosets and tamarins demonstrates different gut adaptations within gum consumers depending on the other foods (insects vs. fruits) consumed. Some combinations may present a diet within which there are items that would be optimally handled by the gut in different ways, presenting conflicting adaptive challenges to be solved. This recalls the issue of trade-offs in the craniofacial anatomy that may be associated with exudate use (see above). However, until we have comparable data for a wider variety of exudativores on gut anatomy, gut kinetics on different diets, and studies of net energy gain from feeding studies, we will not have a full understanding of primate digestive adaptations to the challenges of exudates. Another two areas that are still in need of more systematic study are tongue anatomy and features of the pelage. Génin et  al. (Chap. 6) and Nekaris et  al. (Chap. 8) both present data that associate relatively long tongues with exudativory (see also LTN’s anecdote, above). Nekaris et  al. echo Garber (Garber 1980) in suggesting that patterns of dorsal strips on lorises (some of which appear only seasonally) and color patterns in some callithrichines might help camouflage animals in exposed locations as they concentrate on gum acquisition. These notions beg for experimental studies of the hunting behavior of these primates’ predators using classical ethological approaches. In addition, examination of pelage features as camouflage in other trunk forages, e.g., colugos, vs. similar-sized nontrunk forages would help test the notion that trunk foragers have evolved pelage that hides then while they are particularly vulnerable. While long tongues may help in acquiring gums, exudate use may also influence taste sensitivities though there is little information on taste thresholds to specifically look at the effects of exudates (Nash 1989; Simmen and Hladik 1998). Such studies are complicated by allometric effects and the patterning of requirements to avoid secondary compounds. Docherty et  al. (Chap. 13) address detailed features of tongue papillae, the area of the tongue holding taste receptors, in Otolemur that may relate to taste sensitivity. These authors suggest that the frugivorous O. garnettii

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has a greater density of taste receptors than the exudativorous O. crassicaudatus and that this difference is consistent throughout ontogeny. Results of this study may speak to the chemical signals associated not only with finding exudates but lifehistory variables linked to exudate-feeding.

Locomotion and Limbs At the 2008 IPS symposium Ford presented findings that indicated there were few if any shared postcranial features across all gummivorous primates even though others have implicated a link to keeled, pointed, or claw-like nails. She noted the need for better studies of positional behavior in such species and their nongummivorous sister taxa that incorporated feeding and other contexts and for more biomechanical work on the problem. A practical problem for such work is the rarity of skeletons of some important taxa in museum collections (e.g., Phaner, Cebuella, Mico) and of captive colonies of living animals. Like the Taylor et al. work on the trigeminal nuclei, we look forward to the publication of this work elsewhere. Nekaris et al. (Chap. 8) present excellent qualitative descriptions of some of the positional behaviors associated with exudate eating in different lorises. She notes they use head-down postures extensively though they do not have keeled nails. This calls attention to the need to distinguish movement on angled substrates that is head-up vs. head-down (Crompton 1983; Harcourt and Nash 1986b) as this may influence the grip problems associated with gum foraging. Génin et al. (Chap. 6) note that most cheirogalieds have pointed nails. Garber and Porter (Chap. 4) point out differences between callimicos and tamarins in positional behavior during foraging on pod vs. trunk exudates. Both use vertical clinging and leaping to get to trunk gums but callimicos only use pods that have fallen to the ground while tamarins can hang by their feet in the canopy to harvest pods. Stephenson et al. (Chap. 12) examine volar pad and nail features among galagos. They confirm previous studies (Anderson 1999; Anderson et al. 2000) that indicate volar pad size and shape may be related to taxonomic issues and body size. Unfortunately, no clear association with diet is clear in their analyses for either pads or nail shapes. This may again be related to the comparative samples chosen and the need for more detailed information on the substrates and positional behaviors used in food acquisition. It may not be the food per se, but the postures and substrates that are important, as has been suggested for the evolution of claw-like nails in callithrichines (Garber et al. 1996).

Diet and Captive Husbandry of Exudativores Earlier data on primate exudativory have stimulated attempts to use natural branches and artificial gum feeders as enrichment devices for captive animals, mainly marmosets (Kelly 1993). This work has also demonstrated management

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benefits; as animals come close to keepers offering gum in feeders, they can be examined for health and welfare. In addition, some feeders provide stimulation and favorably influence activity patterns. Recently, Huber (2009a, b) surveyed a variety of zoos worldwide to see how gum was used as enrichment and/or a dietary supplement. The majority of responding zoos housing marmosets provided them with gum, but far fewer did for exudativorous tamarins and galagos. Apparently the prominence of gouging behavior influenced management decisions. Huber (2009a, b) also found that zoos do not appreciate field studies showing that the diet of patas is high in gum. She also reviews methods of presenting gum that emulate natural foraging problems and stimulate more naturalistic positional behavior. As always, there are trade-offs in management decisions. Power (Chap. 2) worries that if gum is fed as enrichment but captive animals then eat less of their carefully balanced diet of other “normal” foods, extra calcium might be ingested at the expense of vitamins from fruits. He suggests that there is no “demonstrated nutritional reasons” for giving captive primates gum beyond behavioral enrichment. In contrast, Nekaris et  al., (Chap. 8) point out that providing gum-gouging opportunities may be important in captive management of lorises, as it may improve dental health and increase activity to limit obesity, both of which are common problems of captive lorises.

Concluding Remarks It now seems clear that exudativory has evolved multiple times within primates, although the issue of whether it was a feature in the earliest primates remains unresolved, and possibly unresolvable (Rosenberger, Chap. 14). Compared to 1986, it seems less clear that exudativory was ancestral within all callithrichines. The variability within both marmosets and tamarins suggests that the morphological differences between them would be profitably examined at a finer scale. As we learn more about exudativory, the diversity of both morphological and behavioral features that are associated with it in different types of primates are likely to become more complex. The ability to generalize from the better known callithrichine features to other primates mostly remains to be established. It is not entirely clear that the craniodental morphological differences between the gouging and nongouging callithrichines will be informative about the contrasts among strepsirrhines that vary in their use of gums. Similarly, the evolution of the digits (claws, keeled or pointed nails) does not easily “track” patterns of exudativory. The work in this volume highlights several directions for future work. It is clear that more detailed observations are needed in the field of how strepsirrhines actually use their mouth and dentition to acquire gum. Unfortunately, a major limitation on work in strepsirrhines will be their scarcity in captivity where biomechanical studies are more feasible. Also, more work on the costs and benefits of exudates as enrichment for captive primates is needed. We also need more detailed fieldwork on all the exudativores to allow comparative studies of how the distribution of their foods in time and space influences social and

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cognitive evolution. Here we include not only primates, but the few other mammals that eat exudates such as sugar gliders (see above) and some didelphids (Génin et al., Chap. 6). Such work is predicated on knowing better how exudates are distributed and what they really provide in the way of nutrition. A more complete understanding of the temporal and spatial availability of this food resource is required to understand how it is adapted to behaviorally. Are there continental differences in the role of primate exudativores in their communities (Reed and Bidner 2004)? More detailed understanding of the role of exudates in primate diets can more fully inform conservation efforts for these species, too many of which are rapidly disappearing. If exudativory is indeed an adaptation to hypervariable environments, will primate exudativores fare better in the face of climate change (Wright 1999) or will the effects of exudativory on species survival also be “clade dependent?” Acknowledgments  First, we thank all of the authors whose hard work tackling the sticky issue of exudativory – and their patience with our nagging – make this an exciting volume. To all the reviewers of the chapters in the book, we are most grateful for the improvements they helped us make to the chapters. We are very grateful to Melissa Higgs at Springer for her endless advice and assistance. Michael Power and George Perry provided helpful comments on this chapter. We would also like to thank our families who put up with our rants and occasional absences as well as providing us with much needed support.

References Agrawal AA, Konno K (2009) Latex: A model for understanding mechanisms, ecology, and ­evolution of plant defense against herbivory. Annu Rev Ecol Evol Syst 40:311–331 Altmann J (1974) Observational study of behaviour: Sampling methods. Behaviour 49:227–267 Altmann SA (1998) Foraging for survival: Yearling baboons in Africa. University of Chicago Press, Chicago Anderson MJ (1999) The use of hand morphology in the taxonomy of galagos. Primates 40:469–478 Anderson MJ, Ambrose L, Bearder SK et al (2000) Intraspecific variation in the vocalizations and hand pad morphology of southern lesser bush babies (Galago moholi): A comparison with G. senegalensis. Int J Primatol 21:537–556 Bearder SK, Honess PE, Ambrose L (1995) Species diversity among galagos with special reference to mate recognition. In: Alterman L, Doyle GA, Izard MK (eds) Creatures of the dark: The nocturnal prosimians. Plenum Publishing Co., New York Bearder SK, Martin RD (1980a) Acacia gum and its use by bushbabies, Galago senegalensis (Primates Lorisidae). Int J Primatol 1:103–128 Bearder SK, Martin RD (1980b) The social organization of a nocturnal primate revealed by radio tracking. In: Amlaner CJ, MacDonald DW (eds) A handbook on biotelemetry and radio tracking. Pergamon Press, Oxford Biebouw K (2009) Home range size and use in Allocebus trichotis in Analamazaotra Special Reserve, Central Eastern Madagascar. Int J Primatol 30:367–386 Burrows AM, Smith TD (2005) Three-dimensional analysis of mandibular morphology in Otolemur. Am J Phys Anthropol 127:219–230 Burrows AM, Smith TD (2007) Histomorphology of the mandibular condylar cartilage in greater galagos (Otolemur spp.). Am J Primatol 69:36–45 Campbell CJ, Fuentes A, Mackinnon KC et al (2007) Primates in perspective. Oxford University Press, New York

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Caton JM, Hill DM, Hume ID et  al (1996) The digestive strategy of the common marmoset, Callithrix jacchus. Comp Biochem Phys A114:1–8 Caton JM, Lawes M, Cunningham C (2000) Digestive strategy of the south-east African lesser bushbaby, Galago mohol. Comp Biochem Phys A127:39–48 Charles-Dominique P (1977) Ecology and behaviour of nocturnal prosimians. Duckworth, London Charles-Dominique P, Bearder SK (1979) Field studies of lorisid behavior: Methodological aspects. In: Doyle GA, Martin RD (eds) The study of prosimian behavior. Academic Press, New York Charles-Dominique P, Petter JJ (1980) Ecology and social life of Phaner furcifer. In: CharlesDominique P, Cooper HM, Hladik A, Hladik CM, Pagès E, Pariente GF, Petter-Rousseaux A, Petter J-J, Schilling A (eds) Nocturnal Malagasy primates: Ecology, physiology, and behavior. Academic Press, New York Christianou M, Ebenman B (2005) Keystone species and vulnerable species in ecological communities: Strong or weak interactors? J Theor Biol 235:95–103 Clark AB (1985) Sociality in a nocturnal “solitary” prosimian: Galago crassicaudatus. Int J Primatol 6:581–600 Collinge SK, Ray C, Cully JF, Jr. (2008) Effects of disease on keystone species, dominant species, and their communities In: Ostfeld RS, Keesing F, Eviner VT (eds) Infectious disease ecology: Effects of ecosystems on disease and of disease on ecosystems. Princeton University Press, Princeton, NJ Committee on Animal Nutrition (2003) Nutrient requirements of nonhuman primates, 2nd rev. edn. National Academy Press, Washington, DC Constantino PJ, Wright BW (2009) The importance of fallback foods in primate ecology and evolution. Am J Phys Anthropol 140:599–602 Copeland SR (2007) Vegetation and plant food reconstruction of lowermost bed II, Olduvai Gorge, using modern analogs. J Hum Evol 53:146–175 Crompton RH (1983) Age differences in locomotion of two subtropical Galaginae. Primates 24:241–259 Davic RD (2003) Linking keystone species and functional groups: a new operational definition of the keystone species concept. Conserv Ecol 7:r11. [online] URL: http://www.consecol.org/ vol7/iss1/resp11/ Dumont ER (1997) Cranial shape in fruit, nectar, and exudate feeders: Implications for interpreting the fossil record. Am J Phys Anthropol 102:187–202 Fedor A, Vasas V (2009) The robustness of keystone indices in food webs. J Theor Biol 260:372–378 Ferrari SF, Lopes FMA (1989) A re-evaluation of the social organization of the Callitrichidae, with reference to the ecological differences between genera. Folia Primatol 52:132–147 Ganzhorn JU (1992) Leaf chemistry and the biomass of folivorous primates in tropical forests: Test of a hypothesis. Oecologia 91:540–547 Garber PA (1980) Locomotor behavior and feeding ecology of the Panamanian tamarin (Saguinus oedipus geoffroyi, Callitrichidae, Primates). Int J Primatol 1:185–201 Garber PA (1984) Proposed nutritional importance of plant exudates in the diet of the Panamanian tamarin, Saguinus oedipus geoffroyi. Int J Primatol 5:1–15 Garber PA, Rosenberger AA, Norconk MA (1996) Marmoset misconceptions. In: Norconk MA, Rosenberger AA, Garber PA (eds) Adaptive radiations of neotropical primates. Plenum Press, New York Génin F (2003) Female dominance in competition for gum trees in the grey mouse lemur. Rev Ecol – Terre Vie 58:397–410 Génin F (2007) Energy-dependent plasticity of grey mouse lemur social systems: Lessons from field and captive studies. Rev Ecol – Terre Vie 62:245–256 Génin F (2008) Life in unpredictable environments: First investigation of the natural history of Microcebus griseorufus. Int J Primatol 29:303–321 Génin F, Schilling A, Perret M (2005) Social inhibition of seasonal fattening in wild and captive gray mouse lemurs. Physiol Behav 86:185–194

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Groves C (2001) Primate taxonomy. Smithsonian Institution Press, Washington, DC Groves CP (2005) Order primates. In: Wilson DE, Reeder DM (eds) Mammal species of the world: A taxonomic and geographic reference, 3rd edn. Johns Hopkins University Press, Baltimore Grubb P, Butynski TM, Oates JF et al (2003) An assessment of the diversity of African primates. Int J Primatol 24:1301–1357 Harcourt CS (1986) Seasonal variation in the diet of South African galagos. Int J Primatol 7:491–506 Harcourt CS, Bearder SK (1989) A comparison of Galago moholi in South Africa with Galago zanzibaricus in Kenya. Int J Primatol 10:35–45 Harcourt CS, Nash LT (1986a) Social organization of galagos in Kenyan coastal forests: I. Galago zanzibaricus. Am J Primatol 10:339–355 Harcourt CS, Nash LT (1986b) Species differences in substrate use and diet between sympatric galagos in two Kenyan coastal forests. Primates 27:41–52 Harrison ML, Tardif SD (1994) Social implications of gummivory in marmosets. Am J Phys Anthropol 95:399–408 Heymann EW, Smith AC (1999) When to feed on gums: Temporal patterns of gummivory in wild tamarins, Saguinus mystax and Saguinus fuscicollis (Callitrichinae). Zoo Biol 18:459–471 Hladik CM, Charles-Dominique P, Petter J-J (1980) Feeding strategies of five nocturnal prosimians in the dry forest of the west coast of Madagascar. In: Charles-Dominique P (ed) Nocturnal Malagasy primates: ecology, physiology and behavior. Academic Press, New York Hodges KE (2008) Defining the problem: Terminology and progress in ecology. Front Ecol Environ 6:35–42 Huber HF (2009a) Environmental enrichment for gummivorous primates. M.A. Thesis. Texas State University, San Marcos, San Marcos, TX Huber HF (2009b) Gum’s the word: applying knowledge from the wild to improve environmental enrichment for captive gummivores. Am J Phys Anthropol S48, Suppl:153 Isbell LA (1998) Diet for a small primate: Insectivory and gummivory in the (large) patas monkey (Erythrocebus patas pyrrhonotus). Am J Primatol 45:381–398 Isbell LA, Pruetz JD, Young TP (1998) Movements of vervets (Cercopithecus aethiops) and patas monkeys (Erythrocebus patas) as estimators of food resource size, density and distribution. Behav Ecol Sociobiol 42:123–133 Jordán F, Liu W-c, Mike Á (2009) Trophic field overlap: A new approach to quantify keystone species. Ecol Modell 220:2899–2907 Kelly K (1993) Environmental enrichment for captive wildlife through the simulation of gum feeding. Anim Welf Inf Cent Newsl 4:1–2, 5–10 Lambert JE (1998) Primate digestion: Interactions among anatomy, physiology, and feeding ecology. Evol Anthropol 7:8–20 Lambert JE (2007) Seasonality, fallback strategies, and natural selection: a chimpanzee and cercopithecoid model for interpreting the evolution of the hominin diet. In: Ungar PS (ed) Evolution of the human diet: The known, the unknown, and the unknowable. Oxford University Press, Oxford Lambert JE (2009) Summary to the symposium issue: Primate fallback strategies as adaptive phenotypic plasticity – scale, pattern, and process. Am J Phys Anthropol 140:759–766 Marshall A, Wrangham R (2007) Evolutionary consequences of fallback foods. Int J Primatol 28:1219–1235 Marshall AJ, Boyko CM, Feilen KL et  al (2009) Defining fallback foods and assessing their importance in primate ecology and evolution. Am J Phys Anthropol 140:603–614 Masters JC, Brothers DJ (2002) Lack of congruence between morphological and molecular data in reconstructing the phylogeny of the Galagonidae. Am J Phys Anthropol 117:79–93 Nash LT (1986) Dietary, behavioral, and morphological aspects of gummivory in primates. Yearb Phys Anthropol 29:113–137 Nash LT (1989) Galagos and gummivory. Hum Evol 4:199–206 Nash LT (1998) Vertical clingers and sleepers: Seasonal influences on the activities and substrate use of Lepilemur leucopus at Beza Mahafaly Special Reserve, Madagascar. Folia Primatol 69, Suppl 1:204–217

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Nash LT, Harcourt CS (1986) Social organization of galagos in Kenyan coastal forests: II. Galago garnettii. Am J Primatol 10:357–369 Nekaris A, Bearder SK (2007) The lorisiform primates of Asia and mainland Africa: Diversity shrouded in darkness. In: Campbell CJ, Fuentes A, Mackinnon KC, Panger MA, Bearder SK (eds) Primates in perspective. Oxford University Press, New York Peres CA (2000) Identifying keystone plant resources in tropical forests: the case of gums from Parkia pods. J Trop Ecol 16:287–317 Pimley E, Bearder SK, Dixson AF (2003) Patterns of ranging and social interactions in pottos (Perodicticus potto edwardsi) in Cameroon. Folia Primatol 74:367–368 Pimley ER, Bearder SK, Dixson AF (2005a) Home range analysis of Perodicticus potto edwardsi and Sciurocheirus cameronensis. Int J Primatol 26:191–206 Pimley ER, Bearder SK, Dixson AF (2005b) Social organization of the Milne-Edward’s potto. Am J Primatol 66:317–330 Porter LM (2007) The behavioral ecology of callimicos and tamarins in northwestern Bolivia. Prentice Hall, Upper Saddle River, NJ Porter LM, Garber PA (2004) Goeldi’s monkeys: A primate paradox? Evol Anthropol 13:104–115 Porter LM, Garber PA, Nacimento E (2009) Exudates as a fallback food for Callimico goeldii. Am J Primatol 71:120–129 Ray E (2007) Research questions. In: Campbell CJ, Fuentes A, Mackinnon KC, Panger MA, Bearder SK (eds) Primates in perspective. Oxford University Press, New York Reed KE, Bidner LR (2004) Primate communities: Past, present, and possible future. Yearb Phys Anthropol 47:2–39 Schülke O (2003) To breed or not to breed – food competition and other factors involved in female breeding decisions in the pair-living nocturnal fork-marked lemur (Phaner furcifer). Behav Ecol Sociobiol 55:11–21 Schülke O, Kappeler PM (2003) So near and yet so far: Territorial pairs but low cohesion between pair partners in a nocturnal lemur, Phaner furcifer. Anim Behav 65:331–343 Schülke O, Ostner J (2005) Big times for dwarfs: Social organization, sexual selection, and cooperation in the Cheirogaleidae. Evol Anthropol 14:170–185 Simmen B, Hladik CM (1998) Sweet and bitter taste discrimination in primates: Scaling effects across species. Folia Primatol 69:129–138 Smith AP (1982) Diet and feeding strategies of the marsupial sugar glider in temperate Australia. J Anim Ecol 51:149–166 Smith AP (1992) Sugar gliders, wattles and rural eucalypt dieback. Aust Netw Plant Conserv Newsl 1:7–10 Stevens JR, Hallinan EV, Hauser MD (2005) The ecology and evolution of patience in two New World monkeys. Biol Lett 1:223–226 Suckling GC (1984) Population ecology of the sugar glider, Petaurus breviceps, in a system of fragmented habitats. Wildl Res 11:49–75 Sussman RW, Kinzey WG (1984) The ecological role of the Callitrichidae: A review. Am J Phys Anthropol 64:419–449 Sussman RW, Raven PH (1978) Pollination by lemurs and marsupials: An archaic coevolutionary system. Science 200:731–736 Tan CL, Drake JH (2001) Evidence of tree gouging and exudate eating in pygmy slow lorises (Nycticebus pygmaeus). Folia Primatol 72:37–39 Taylor AB, Eng CM, Anapol FC et al (2009) The functional correlates of jaw-muscle fiber architecture in tree-gouging and nongouging callitrichid monkeys. Am J Phys Anthropol 139:353–367 Ushida K, Fujita S, Ohashi G (2006) Nutritional significance of the selective ingestion of Albizia zygia gum exudate by wild chimpanzees in Bossou, Guinea. Am J Primatol 68:143–151 Viguier B (2004) Functional adaptations in the craniofacial morphology of Malagasy primates: Shape variations associated with gummivory in the family Cheirogaleidae. Ann Anat 186:495–501 Vinyard CJ, Wall CE, Williams SH et al (2003) Comparative functional analysis of skull morphology of tree-gouging primates. Am J Phys Anthropol 120:153–170

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Wiens F, Zitzmann A, Hussein NA (2006) Fast food for slow lorises: Is low metabolism related to secondary compounds in high-energy plant diet? J Mammal 87:790–798 Wright PC (1999) Lemur traits and Madagascar ecology: Coping with an island environment. Yearb Phys Anthropol 42:31–72 Yamashita N, Vinyard CJ, Tan CL (2009) Food mechanical properties in three sympatric species of Hapalemur in Ranomafana National Park, Madagascar. Am J Phys Anthropol 139:368–381 Yépez P, De La Torre S, Snowdon CT (2005) Interpopulation differences in exudate feeding of pygmy marmosets in Ecuadorian Amazonia. Am J Primatol 66:145–158

Chapter 2

Nutritional and Digestive Challenges to Being a Gum-Feeding Primate Michael L. Power

Abstract  Gum is an unusual food that presents significant challenges to animals that feed on it. Gum is limited in availability; trees generally secrete it only in response to damage. Gum is a b-linked complex polysaccharide, and as such is resistant to mammalian digestive enzymes and requires fermentation by gut microbes. It contains little or no lipid, low amounts of protein, and no appreciable levels of vitamins. As a food, gum can be characterized as difficult to obtain, potentially limited in quantity, difficult to digest, and primarily a source of energy and minerals. Despite these drawbacks, many primates feed extensively on gums. Among mammals, gum-feeding largely appears to be a primate dietary adaptation. Why are there so many primate gum-feeders and what adaptations have allowed them to make a living on such a problematic food? This is the central question of this book. This chapter examines digestive and nutritional aspects of gum. Specific examples of biological adaptations found in common and pygmy marmosets (Callithrix jacchus and Cebuella pygmaea), small New World primate gum-feeding specialists, will be examined. These marmoset species have many similarities in their behavior, morphology and metabolism, but also some instructive differences in their digestive function. C. pygmaea is the smallest of the marmosets but has the slowest passage rate of digesta. This might represent an adaptation to retain difficult-to-digest material, such as gum, within the gut to allow fermentation. In contrast, C. jacchus has a rapid passage rate. Passage rate in C. jacchus appears adapted more for rapidly excreting indigestible material (e.g., seeds) than for retaining gum within the gut to enable more complete digestion. Fruit is a rare component of C. pygmaea’s diet; hence any constraint on feeding caused by filling the gut with ingested seeds is greatly relaxed, apparently enabling digestive kinetics that favor digestive efficiency over maximizing food intake. Interestingly, however, these marmosets share M.L. Power (*) Nutrition Laboratory, Smithsonian Conservation Biology Institute, National Zoological Park, P.O. Box 37012, MRC 5503, Washington, DC 20013-7012, USA and Research Department, American College of Obstetricians and Gynecologists, Washington, DC 20024, USA e-mail: [email protected] A.M. Burrows and L.T. Nash (eds.), The Evolution of Exudativory in Primates, Developments in Primatology: Progress and Prospects, DOI 10.1007/978-1-4419-6661-2_2, © Springer Science+Business Media, LLC 2010

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an ability to digest gum despite their differences in gum kinetics. In captivity both species have been shown to be more able to digest Acacia gum than related species that feed less often on gum in the wild.

Introduction All life has a common biochemical underpinning. Because of this, everything living potentially is food. Indeed, for every living organism there are other organisms that feed off of it. However, because of the immense amount of time over which life has diverged and radiated, the common biochemical underpinning has accumulated a tremendous amount of variation in specific characteristics among taxa. Everything may be food for something; but for any given organism most of what is in its environment is not food. Animals eat food; they require nutrients. A significant proportion of anatomy and physiology has as its primary purpose the transformation of food that animals select from their environment into the nutrients required for life. These challenges can be external ones such as finding and acquiring food, and they can be internal challenges, such as digesting, assimilating, and metabolizing food, and then finally excreting the associated waste products (Chivers et al. 1984). My research focus is on the internal challenges different foods provide. All foods provide challenges; there is no perfect food. Different foods provide different challenges. For example, carnivores are confronted with very different challenges in obtaining nutrients than are herbivores. Animals and plants share an evolutionary history, and thus are biochemically similar; however, they are also very different, reflecting the billions of years of evolutionary separation. Thus, in general it is assumed that carnivores are faced with a less difficult nutritional challenge than are herbivores. If you are what you eat, then eating other animals should provide fewer difficulties than eating plants. As is true for most generalities in biology, the one above is an oversimplification. Although other animals certainly contain all the nutrients an animal needs to consume, they do not contain them in the correct proportions. Animals contain far more protein than is necessary for another animal to consume, and far less glucose and other carbohydrate than is needed to survive. Strict carnivores must deal metabolically with an excess of protein and insufficient carbohydrate. For herbivores the situation is possibly reversed. Protein can be a limiting nutrient but carbohydrate is usually in plentiful supply, though not always in a readily metabolizable form. Many plant carbohydrates are difficult to digest. Animals that feed largely on plant material generally face greater digestive challenges; for strict carnivores the challenges are primarily metabolic. Of course all plant foods are not alike, and thus provide different digestive and metabolic challenges. This essay concerns the challenges presented by a rather unusual plant food, gum, a type of exudate produced by certain trees and lianas. The number of animals known to regularly feed on tree exudates is not large,

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though the list is slowly expanding. Among mammals, the primate order contains a considerable number of species that utilize tree exudates as a food resource, including many that appear to specialize on exudates. The only other (known) exudate-feeding mammals are a guild of small marsupials native to Australia (Hume 1982; Smith and Lee 1984), where there are no native nonhuman primates. Why are there so many primate gum-feeders and what adaptations have allowed them to make a living on such a problematic food? That is the interesting question that has inspired this book. My contribution will be limited to examining the nutritional, digestive and metabolic advantages and challenges from eating gum, and is further constrained by a focus on the biology of the marmosets, small gum-feeding New World primates. Hopefully this chapter will provide a broad enough context that the value of gum as food for other species can be evaluated as well. This chapter will start with a general assessment of gum as food, with some comparison to other plant foods including other exudates. Gum is dietary fiber; as such it presents digestive difficulties. The advantages and disadvantages of foreand hind-gut fermentation for obtaining nutrients from gum are briefly reviewed. The chapter then focuses on marmosets, specifically their digestive function and how that may or may not be adapted to gum-feeding.

Exudates as Food There are primate species, our own especially, that incorporate a substantial amount of animal matter in the diet; but in general, primates feed predominantly on plant foods. Plants are complex structures. A tree is composed of many different parts that vary widely in chemical and physical composition. Its wood, bark, leaves, flowers, fruits, and exudates all provide food for something but any given animal species generally will feed only on certain parts and will ignore the rest. A tree may have many species visiting it, each feeding on a different tree product. These are obvious statements; the point is that different plant products need to be categorized in ways that reflect the kind of nutrition they provide in order to explore the dietary adaptations of our subject species. To say that gum is a plant product doesn’t help to determine what nutrition it can or cannot provide for a species. Ideally gum should be chemically assayed to determine its constituents, and then fed to animals in controlled trials to determine the bioavailability of those constituents. However, there are general principles that can be used to predict what nutritional category a plant product is likely to occupy. There are many ways to categorize plant foods. For the purposes of this essay I propose two simple categorizations: alive vs. not alive, and primarily reproductive vs. primarily nonreproductive. The first categorization separates exudates from other plant foods such as leaves, flowers, and fruit in a fundamental way. Exudates are created by living things but they themselves are not alive. More to the point, exudates do not contain living cells. Cells, by necessity, contain the required chemical

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components for life. Foods such as leaves, flowers and fruit that are composed predominantly of living cells in theory should provide excellent nutrition. Of course, there might be some difficulty in accessing the cell contents and obtaining the nutrients; but they are there. Exudates are created by living things and therefore it is not surprising that they contain nutrients; however, there is no expectation that exudates will contain all the nutrients necessary for life. And indeed they do not. Gums and other exudates are not complete foods. Plants produce a number of exudates; in this essay I will be primarily concerned with gum; however, the other types of exudates are briefly considered here. Tree exudates are generally categorized as sap, gum, latex, and resin (Nash 1986). In addition, nectar can be considered a plant exudate. All these exudates have different functions, which influence their characteristics as food. Consider nectar, an exudate produced by flowering plants. Flowering plants arose more than a 100 million years ago (Soltis and Soltis 2004), greatly diversified in the Cretaceous, and have been coevolving with animals ever since. Nectar serves as a reward to pollinators. The plant provides food in exchange for assistance in sexual reproduction. Nectar has evolved to be food. Therefore, it is not surprising that nectar has characteristics that make it edible and that it provides some nutrition, in most cases primarily energy. These are characteristics of many, but not all plant parts that primarily serve a reproductive function. Nectar and fruit are the principal examples. In both cases the plant produces a food-like substance to reward animals that assist in the plant’s reproduction. But seeds also can provide high quality nutrition. It is true that for many plants it is beneficial if their seeds are ingested; but not if the seeds are actually digested. There are seed dispersers and there are seed predators. For the predators, seeds are food and quite good food for the basic reason that seeds must contain most if not all the molecules necessary for life. They are incipient life. Most exudates other than nectar generally don’t serve the reproductive needs of plants, and have not evolved to be food. Sap perhaps is closest to nectar in constitution. Sap contains the simple sugars from photosynthesis, and other nutrients that are required by the plant cells to survive. The main difference between sap and nectar is that nectar is concentrated. There are animals (mainly insects) that feed on sap. The challenges sap presents are mainly related to acquiring it in the first place; however, it is dilute and thus a large quantity of water must be ingested to provide a fairly small amount of nutrition. Cicadas are an insect that feeds on sap; the author has walked through the mist created by millions of cicadas feeding on tree sap, and necessarily excreting large amounts of water into the air. Joly-Radko and Zimmermann (Chap. 7) describe “sap eating by proxy” in mouse lemurs consuming the excretions produced by hemipteran insects feeding on sap. Resins are phenol and terpene derivatives. They are generally considered noxious and even toxic. There are animals that are tolerant of resins, however. The desert wood rat (Neotoma lepida) feeds extensively on creosote bush leaves, at least in certain areas of its range (Mangione et al. 2000). These leaves can contain as much as 25% of the dry mass as phenolic resin (Rhoades and Cates 1976).

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Latex is a chemically complicated exudate that certain plants exude in response to damage. Indeed, as a category it is the most phytochemically diverse exudate (Agrawal and Konno 2009). About 10% of flowering plants produce latex (Agrawal and Konno 2009), which translates to tens of thousands of latex-producing plant species (Farrell et al. 1991). Latex is produced by specialized cells called laticifers, and is released upon damage to the plant. Because latex performs no known metabolic functions in plants it has been suggested to perform a defense function, mainly against herbivorous insects (Agrawal and Konno 2009). In some instances the defense function is related to toxic chemicals in the latex; however, the majority of latex-producing plants have not been found to produce toxic substances in their latex, or to be intrinsically toxic to animals (Konno et al. 2004). Indeed, latex from different species range from highly toxic (e.g., milkweed) to edible (e.g., latex from Brosimum galactodendron, called the milk tree or cow tree in Venezuela). Some researchers have suggested that the sticky nature of latex may serve as a feeding deterrent for insects; a physical defense in addition to any chemical defense (Farrell et al. 1991). Latex is also known to contain proteases. For example, papaya latex contains papain, which is used as a meat tenderizer. Papain has been shown to be toxic to several species of lepidopteran larvae (Konno et  al. 2004), though it is unclear how it would affect vertebrates. Latex, as a category, is not very helpful when assessing the potential food value of an exudate, primarily because latex does not appear to have a particular chemical definition. Rather, what unites latex from different species and separates latex from other exudates is that latex is produced and secreted by laticifers, specialized plant cells that respond to tissue damage. Other exudates come from intercellular spaces. Typically latex will be opaque and sticky, and will coagulate upon exposure to air. Latex from many species is milky in appearance; but it can be yellow, orange, red, or even clear (Agrawal and Konno 2009). Thus, for the field ecologists witnessing his focal species feeding on an exudate, being able to distinguish latex from gum would likely require particular botanical knowledge. Latex from certain plants undoubtedly provides significant nutrition to many animals including primates. Latex from other plants probably deters feeding due to the presence of toxic chemicals. Simply labeling an exudate latex gives little insight into its potential nutritional role in an animal’s diet. The focus of this chapter is gum as food. Gum is an unusual food that presents significant challenges to animals that feed on it. The amount of gum available to most animals can be limited, since trees generally secrete it only in response to damage and gum usually hardens fairly rapidly to seal the wound site (Nash 1986). Gum is comprised mainly of a b-linked complex polysaccharide (Monke 1941; Booth et al. 1949; Booth and Henderson 1963; Hove and Herndon 1957); complex carbohydrates of this form (e.g., cellulose) require fermentation by gut microbes before the nutrients are available to animals that feed on it. In other words, gum is dietary fiber (Van Soest 1982; Kritchevsky 1988). Dietary fiber is neither inert nor indigestible, and its ingestion has many and varied physiological consequences (Wrick 1979; Van Soest 1982; Kritchevsky 1988). For example, insoluble fiber (e.g., cellulose) generally has a laxative effect on humans and other nonruminant mammals

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(Kritchevsky 1988). In contrast, soluble fiber (e.g., gum, pectin) can slow gastric emptying and the rate of passage through the small intestine by increasing the viscosity of digesta (Johnson et al. 1984). Soluble fiber also has been shown to reduce the rate of glucose absorption (Johnson et al. 1984). Gums are not nutritionally complete, although they can contain significant quantities of mineral salts (e.g., calcium, potassium, magnesium, but not usually phosphorus) (e.g., Génin et al., Chap. 6; Smith 2000; Peres 2000). As a food, gum can be characterized as difficult to obtain, potentially limited in quantity, difficult to digest, and primarily a source of energy and minerals. Despite these drawbacks, many primates feed extensively on gums, as do some birds (e.g., Kori bustards (Ardeotis kori); Skead 1969; Urban et al. 1978; cited in Lichtenberg and Hallager 2008). Among mammals, gum-feeding largely appears to be a primate dietary adaptation, though that might represent a greater knowledge of primate feeding behavior than that of nocturnal arboreal rodents and bats, other taxa that would have access to gum and might benefit from eating gum. Some African rodents eat small quantities of gum in their diets (Emmons 1980). Laboratory rats have been shown to be able to digest gum arabic, i.e., Acacia senegal gum (McLean Ross et  al. 1984). In theory, insectivorous bats might benefit from the calcium found in gums, assuming it was biologically available to them. There are some plant products referred to as gums that appear to serve a reproductive function. These are gums produced in seed pods, for example, in the genus Parkia, and appear to act as a food reward to attract potential seed dispersers (Peres 2000; Feldmann and Heymann 2001). Many callitrichid primates (and probably other animals) feed on these pod gums. The chemical structure of these gums is uncertain; but they may be more digestible than other tree gums (Peres 2000). That would certainly be the prediction from an evolutionary perspective. However, the current biochemical evidence does not address this issue with any certainty. The statement in Peres (2000) that the carbohydrates in Parkia pod gum are “nonstructural” is meaningless. Structural carbohydrates are constituents of cell walls. Since gums do not contain cells of course their carbohydrates are nonstructural. That does not mean that they are not complex b-linked polysaccharides resistant to vertebrate digestive enzymes. The chemical assay technique used to determine the constituent sugars in Parkia pod gum reported in Peres (2000) is also used to determine the sugar constituents of cellulose (e.g., Kajiwara and Maeda 1983). A technique capable of hydrolyzing cellulose into its constituent monosaccharides likely would be successful at breaking a gum into its monosaccharides, regardless of its chemical structure. Interestingly, the monosaccharides identified in Parkia pod gum (arabinose, rhamnose, galactose, and glucuronic acid) are the same sugars that comprise gum arabic (A. senegal gum). Thus, the current evidence indicates that Parkia pod gum has similarities to Acacia gum. The structure of A. senegal gum has been determined; this gum consists of a proline-rich glycoprotein with multiple sugar residues consisting of arabinose (as a mono-, di-, or polysaccharide) or of the four constituent monosaccharides listed above in a complex polysaccharide (Goodrum et al. 2000). A comparison of the relative quantities of sugars reported in Peres (2000) for Parkia pod gum and Goodrum et al. (2000) for A. senegal gum indicates a higher

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proportion of arabinose in Parkia pod gum. Assuming similar structure between these gums, this result implies a higher proportion of arabinose sugar residues attached to the gum glycoproteins in Parkia pod gum. If true, then this finding might imply that Parkia pod gum is less resistant to mammalian digestive enzymes; but this is merely conjectural at this time.

Fore-Gut and Hind-Gut Digestion The plant constituents that are defined to be dietary fiber are not digested by vertebrate digestive enzymes (Kritchevsky 1988). These include cellulose, hemicellulose, lignin (a non-carbohydrate fiber), and a variety of soluble fibers such as pectins and gums (Van Soest 1982). Many gut microbes do produce enzymes that can break the carbohydrate fibers into simple sugars. Animals that obtain significant amounts of nutrition from the internal fermentation of fiber by symbiotic gut microbes generally have evolved expanded regions of the gut where the digesta is fermented. A detailed discussion of the varied and complex adaptations for fermentation chambers in vertebrates is outside of the scope of this chapter; for those interested an excellent resource is Stevens and Hume (1995) and the computer version of this work is available through the Comparative Nutrition Society website (http://www.cnsweb.org). For primates, the simplest division is between what are called fore-gut fermenters and hind-gut fermenters. The terms refer to the area of the gut that has been expanded to permit fermentation: the stomach for fore-gut fermenters (colobines) and the cecum and colon for hind-gut fermenters. Most primates are hind-gut fermenters to a greater or lesser extent. The small gummivorous primates are all hind-gut fermenters. Gum is dietary fiber; it shares the biochemical characteristics that make all carbohydrate fibers largely indigestible by endogenous mammalian digestive enzymes. Thus gum needs to be fermented by gut microbes before its nutrients can be used. The ability of gut microbes to ferment a particular fiber depends in part on its water solubility (Cummings 1981). If the gum is water-soluble fermentation will be rapid; water insoluble gums are difficult to ferment, because there is a low surface area to volume ratio. In either case, both fore and hind-gut fermenters are capable of digesting gum. There are differences between fore- and hind-gut fermenters that affect their ability to utilize the nutrients in gum, however. Fore-gut fermenting animals gain significant advantages for certain nutrients (Hume 1989). The microbes in their stomachs produce many essential nutrients, a significant proportion of which escape into the small intestine and are assimilated and utilized by the host animal. In addition, when a microbe dies it will be digested and its constituents will be available to its host. These constituents include many vitamins but also protein. There are some disadvantages to fore-gut fermentation, however, if the diet contains a significant amount of easily digestible carbohydrate. A fore-gut fermenting animal gains energy in the form of short-chain fatty acids from indigestible and difficult-to-digest carbohydrates (e.g., cellulose and hemicellulose) that otherwise would be unavailable, but loses part of the potentially

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available energy from simple sugars and other easily digestible carbohydrates via the same process. A hind-gut fermenting animal can utilize the energy from easily digestible carbohydrates because they are digested and absorbed in the small intestine, before the microbes in the lower gut can feed on them (Hume 1989). The indigestible carbohydrates pass into the hind gut, are fermented and the resulting short-chain fatty acids are absorbed and used by the host animal in metabolism just as in the fore-gut fermenters. However, the hind gut does not absorb all nutrients to the same extent that the small intestine does. Therefore many nutrients (e.g., vitamins, proteins) produced by the gut microbes are not as available to a hind-gut fermenter, unless the animal practices coprophagy.

Body Size Body size has several influences on the challenges of utilizing gums as food. Larger animals need absolutely more energy to survive. Due to the relative low availability of gum in the environment gum would be expected to be a smaller proportion of the diet of large animals compared with smaller species, even though an individual from the larger species may eat absolutely more gum than does any individual from the smaller species. Above a certain body size there just wouldn’t be enough gum in the environment to sustain an animal. That does not mean that gum will be unimportant to the diets of large primates. On the contrary, gum is an important component for many species of large-bodied primates (e.g., patas monkeys (Erythrocebus patas), baboons (Papio spp.), and chimpanzees (Pan spp.)) But it will be rare that a large primate will be able to obtain the majority of needed energy from gum, unlike the situation for small gum-feeding specialists (e.g., pygmy marmosets, C. pygmaea). However, large body size likely will provide an advantage in digesting gum. Gut capacity generally increases in direct proportion to body mass (Demment and Van Soest 1985). This generally means that the retention time of digesta also increases with body size (Demment 1983), assuming that the digestive strategies of the species being compared are not radically different. A longer retention time in the gut would aid gum digestion; thus larger animals should be better able to digest gum. Humans appear to completely digest gum arabic (McLean Ross et al. 1983; Wyatt et al. 1986). Thus, for large primate species the challenge gum presents as a food is likely more regarding the quantity that can be obtained and not its digestive difficulties. Gums could provide important quantities of minerals for large species, even if the total amount of energy from ingested gum is small relative to requirement (Ushida et al. 2006).

Protein Gums contain protein. That isn’t surprising, since they are a biological material. Indeed, the chemical properties of economically valuable gums such as gum arabic that are important to their functions (both as a wound-sealing substance in trees and

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in human food industry as an emulsifier) derive from the presence of glycoproteins with multiple saccharides (mono, di, and poly) attached (Goodrum et  al. 2000). For example, in gum arabic (gum from A. senegal) the glycoprotein is a hydroxyproline-rich peptide with multiple sugar residues consisting of arabinose molecules or the main sugar of gum arabic which is a rhamnoglucuronoarabinogalactan polysaccharide (i.e., a polysaccharide containing rhamnose, glucuronic acid, arabinose, and galactose; Goodrum et  al. 2000). So glycoproteins appear to be an intrinsic component of gums. There is a great deal of variation in the amount of protein reported among various gums, ranging from trace amounts to as much as 9–10% on a dry matter basis. So do some gums serve as an important source of protein for primates? Possibly; but certain aspects of gum protein suggest that the answer is not simple. The amount of protein in gum may be overestimated by standard assay techniques; the biological availability of that protein may be problematic for many gum-feeders; and finally, many gum-feeders are also highly insectivorous (e.g., marmosets, Galago senegalensis, Galago moholi), so it is not likely that protein is a limiting nutrient. Biological materials aren’t usually assayed for protein per se; usually the assay determines the amount of nitrogen in the sample, and then that value is converted to an estimate called crude protein using an accepted conversion value. For forages used to feed domesticated animals (e.g., alfalfa or hay) that value is 6.25 g protein/g nitrogen; for milk protein the value is 6.38. Most values of estimated protein in leaves, fruit, and exudates collected from the wild are derived from 6.25 times the amount of nitrogen determined by chemical assay. Other values have been proposed for wild plant materials, usually significantly lower than 6.25. For example, Milton and Dintzis (1981) found that appropriate conversion factors for many tropical leaves were as low as 70% of 6.25. Partly that can be explained by the amino acid composition of the proteins; but also, protein is not the sole nitrogenous substance found in plant material. There are amino sugars, lignin, and various plant secondary compounds that contain nitrogen. For example, alkoloids are nitrogenous. These are usually found in relatively low levels in the cultivated forages that are the results of generations of artificial selection to produce efficient feed for domesticated herbivores, and therefore contribute little to the nitrogen content of the plants from which the 6.25 conversion factor was derived. It is not at all certain what conversion factor is appropriate to estimate protein from nitrogen for gums. Thus most estimates of the amount of protein in gums must be considered to be preliminary, and quite possibly inflated. The second issue is bioavailability. If the protein is not incorporated within the indigestible carbohydrate matrix of gum, but is simply dissolved in an aqueous fraction, then the protein should be readily available. However, if the protein is actually incorporated into the chemical structure of the gum, then the gum likely needs to be fermented before that protein is available to the primate that ingests it. Most of the protein in gums probably is in the form of glycoproteins, as described above for A. senegal gum, and thus is incorporated into the polysaccharide structure. However, it is not known to what extent those sugar residues are resistant to cleavage from the peptide, though the sugars themselves are likely resistant to mammalian digestive enzymes. So the bioavailability of gum protein is uncertain.

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If the primate eating the gum is a fore-gut fermenting colobine, then the protein will become available indirectly, regardless of how the protein is incorporated into the carbohydrate structure, through the digestion of fore-gut microbes that pass into the small intestine. For a hind gut fermenting primate, however, if the protein is resistant to digestive enzymes in the upper intestinal tract due to its sugar residues, then the protein will pass into the lower gut to become available to the microbes in the cecum and colon; but unless the animal practices some form of coprophagy, the protein is unlikely to be digested and assimilated by the ingesting primate. Finally, primates that feed on gums all have other sources of protein in their diets, usually insects and other small animals. Primate protein requirements are not particularly high. For most Old World anthropoids, 12% of energy in the diet coming from protein is more than adequate for growth and reproduction (NRC 2003). Even the small New World monkeys, such as common marmosets, can be maintained on diets of 16% of energy from protein and show normal growth and reproduction (Tardif et al. 1998). In the wild, with higher energy expenditures due to activity and thermoregulation, the required percent of energy from protein is likely lower, provided, of course, that sufficient energy to match expenditure can be obtained. Thus it is not clear that most gum-feeding primates are protein limited. This doesn’t mean that the protein in gums is irrelevant; it does imply that protein content is unlikely to be the determining factor of whether animals eat a gum or not.

Calcium Gums often contain significant amounts of minerals, but not all minerals. Calcium is often found in significant quantities; phosphorus is not. Thus gums have been proposed to be a source of calcium in the diet that may be particularly important to insectivorous gum-feeders (e.g., Bearder and Martin 1980), since insects generally contain significant amounts of phosphorus and little calcium. Assuming that the calcium in gum is bioavailable, which probably requires the gum to be fermented, gums can provide a significant source of calcium for wild animals. The cecum and colon will absorb most minerals, so the calcium in gum is available to hind-gut fermenters. It has been estimated that chimpanzees that feed on Albizia zygia tree gum could obtain their entire daily requirement of calcium and several other minerals from their mean daily intake of gum, even though that amount of gum provides a fairly trivial amount of their daily energy intake (Ushida et al. 2006). Should captive small gum-feeding primates be provided with gum as a calcium source? The levels of calcium in the gums that have been assayed range from below 0.5% to around 1% on a dry matter basis. These are fairly good levels for wild foods but most manufactured primate diets contain 0.8–1.2% calcium on a dry ­matter basis. If feeding gum reduces consumption of the nutritionally complete feed that should form the base of any captive animal’s diet, then calcium intake may not be increased. In contrast, substituting gum for fruit in the diet may indeed increase

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calcium consumption. However that will come at the expense of decreasing the consumption of vitamins in fruit. At present, there are no demonstrated nutritional reasons for including gum in the diet of captive gum-feeding primates. There are hypothetical advantages, such as providing a fermentable substrate that would increase butyrate production in the colon; butyrate is known to enhance colonic health (Wong et  al. 2006). However, some starches and pectins in captive callitrichid diets probably already reach the colon to be fermented, providing a source of butyrate. Gum added to the diets of common and pygmy marmosets appeared to slow the passage rate of digesta (Power 1991; Power and Oftedal 1996). Whether a slower passage rate of digesta would have any positive health benefits in captivity is unknown. Based on the lack of evidence that gum has a nutritional purpose in captive callitrichid diets, it should be treated as an enrichment food.

Callitrichid Digestive Function The monophyletic primate family Callitrichidae includes marmosets (genera Callithrix, Mico and Cebuella), tamarins (genus Saguinus), lion tamarins (genus Leontopithecus), and Goeldi’s monkey (Callimico goeldii). All callitrichids are omnivorous, and feed on fruit, gum, other plant exudates including nectar, invertebrates, and small vertebrates. As a general rule, marmosets are more likely than the other callitrichids to feed extensively on gums. Marmosets have dental adaptations that allow them to gouge trees and stimulate the flow of gum (Coimbra-Filha and Mittermeier 1977), thus reducing the problem of gum availability. This appears to have allowed marmosets to colonize drier forests and small forest fragments where there is little fruit (Fonseca and Lacher 1984). Because wild callitrichids typically feed on a variety of foods they are faced with a variety of digestive challenges. The digestive challenges posed by fruit would appear to favor different digestive adaptations than does those posed by gum. A substantial proportion of the ingested mass of fruits often consists of seeds (Garber 1986; Heymann and Smith 1999), which are passed relatively unchanged through the digestive tract (Garber 1986; Knogge and Heymann 2003). These seeds represent indigestible bulk to marmosets, and could inhibit food intake if they are not eliminated rapidly. In contrast, gums are b-linked polysaccharides that require microbial fermentation; thus their digestion would benefit from an extended residence time within the gut. The “optimal” digestive strategies for fruit and gum appear to be in conflict. Fruit-eating would favor a rapid passage of digesta through the gut to eliminate the indigestible seeds, while gum digestion would benefit from a slower passage rate, retaining the gum within the gut to allow fermentation to proceed. Previous work on digestive function in five callitrichid species (Power 1991) indicated that, in general, the ability to digest a common diet and the amount of time it took for digesta to pass through the digestive tract were associated with body size. Transit time of particulate digesta (defined as the time to first appearance of

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an indigestible particulate marker) and the apparent digestibility of both dry matter and energy declined with mean body mass for four of the species: golden lion tamarins (Leontopithecus rosalia, ca. 700 g), cotton-top tamarins (Saguinus oedipus, ca. 500 g), common marmosets (Callithrix jacchus, ca. 350  g), and saddle-back tamarins (Saguinus fuscicollis, ca. 300 g). Thus any differences in digestive function between common marmosets and other callitrichids appeared to be explained by allometry. In contrast, the mean value for transit time for the smallest callitrichid species, the pygmy marmoset (Cebuella pygmaea, ca. 125 g), was greater than for any of the other species, and the mean values for apparent digestibility of dry matter and energy were equal to those of Leontopithecus (Figs. 2.1 and 2.2). In addition to being the smallest callitrichid, C. pygmaea is also the marmoset most dependent on gum as a dietary staple in the wild and the least likely to feed on fruit (Ramirez et al. 1977; Soini 1982; Yépez et al. 2005). A comparison of digestive function between C. jacchus, a species that eats a substantial amount of both fruit and gum in addition to animal prey, and C. pygmaea which largely feeds on gum and animal prey, and rarely on fruit, provides instructive insight into the adaptive conflict between digestive strategies for fruit and gum. C. jacchus has rapid passage rates for both solid and liquid markers of digesta (Caton et  al. 1996; Power and Myers 2009); indeed C. jacchus does not differ in passage rate from similar-sized tamarins (Power 1991). Passage rate in C. jacchus appears adapted more for rapidly excreting seeds than for retaining digesta within the gut to enable more complete digestion. For wild C. jacchus, seeds represent indigestible bulk, which provide essentially no nutrients, but may inhibit feeding by filling the digestive tract. There is a potential opportunity cost in retaining seeds within the gut and little benefit.

Fig. 2.1  Transit time (time to first appearance of a particulate marker) with respect to body mass in five callitrichid species

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Fig.  2.2  Apparent digestibility of energy (ADE) with respect to body mass in five callitrichid species (Cp = Cebuella pygmaea; Cj = Callithrix jacchus; Sf = Saguinus fuscicollis; So = Saguinus oedipus; Lr = Leontopithecus rosalia)

The adaptive advantage to eliminating seeds rapidly appears to have driven the evolution of a rapid passage rate in most callitrichids (Power 1991; Power and Oftedal 1996). In contrast, wild C. pygmaea feed extensively on gums, and possibly saps, and rarely feed on fruit (Ramirez et al. 1977; Soini 1982; Yépez et al. 2005). C. pygmaea’s divergence from the pattern of digestive function exhibited by the other callitrichids may be related to the digestive advantage of retaining gum within the digestive tract for fermentation to occur, as well as to a relaxation of the adaptive constraint from the need to eliminate seeds from the gut (Power 1991; Power and Oftedal 1996). Interestingly, despite their differences in passage rates, the two marmosets did not differ in their ability to digest gum arabic (Power 1991; Power and Oftedal 1996), a highly water-soluble Acacia gum that should ferment relatively rapidly. In contrast, two tamarin (S. oedipus and S. fuscicollis) and one lion tamarin (L. rosalia) species digested this gum poorly (Power 1991; Power and Oftedal 1996). Both marmoset species appear to have adaptations for gum digestion which tamarins and lion tamarins lack (Fig. 2.3). Thus retention of digesta does not appear to be the most important aspect of digestive function in regards to gum digestion in callitrichids. A study of passage rate in C. jacchus using both a particulate (chromium mordanted fiber) and a liquid marker (cobalt EDTA) indicated that the fluid passed through the marmoset digestive tract more slowly than did particulate matter (Caton et al. 1996). Caton and colleagues hypothesized that C. jacchus has a cecal– colonic separation mechanism, in which particulate matter is largely excluded from the cecum, flowing directly to the colon, and liquid digesta (e.g., gum) is preferentially retained within the cecum, allowing fermentation to proceed.

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Fig. 2.3  When powdered gum arabic was added to a single-item homogeneous diet at 9% of dry matter, marmosets showed no significant change in digestive efficiency while the tamarin and lion tamarin species all had declines in mean apparent digestibility of energy (ADE). Data from Power 1991. (Cp = Cebuella pygmaea; Cj = Callithrix jacchus; Sf = Saguinus fuscicollis; So = Saguinus oedipus; Lr = Leontopithecus rosalia)

In contrast to the findings of Caton et al. (1996), Power and Myers (2009) found no difference in the mean retention time (MRT) of solid and liquid markers. The values from the Power and Myers study for MRT of CoEDTA and chromium mordanted fiber were similar to the values in Caton et al.; indeed there was no statistical difference between the values from the two studies (Fig.  2.4). The excretion curves published in Caton et al. (1996) were similar to the excretion curves in Power and Myers (2009); concentrations of both markers were similar over time, and for both markers a majority was excreted before the animals retired for the night. Interestingly, MRT for polystyrene beads in C. jacchus is shorter than the values found for chromium mordanted fiber, even in the Caton et al. study (Power 1991; Fig. 2.4). A cecal–colonic separation mechanism is not the only potential strategy to increase gut residence time for gum. Passage rate may vary as a function of physical characteristics of the diet. Both C. jacchus and C. pygmaea fed a diet containing 9% gum arabic on a dry matter basis had longer transit times than when fed the diet without gum (Power 1991; Power and Oftedal 1996). As mentioned earlier, adding gum and other soluble fiber to the diet slows passage rate (Johnson et al. 1984). Wild tamarins and lion tamarins feeding extensively on fruit, and hence swallowing many seeds, often have estimated transit times under 1  h (P. Garber, personal communication). Humans fed plastic pellets have shorter transit times (Tomlin and Read 1988). The mechanical stimulation of the gut from such particles (seeds or plastic pellets) may increase the rate of passage of digesta. Thus, temporally separating gum-feeding from feeding on fruit might allow different residence times for digesta.

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Fig.  2.4  Mean retention time (MRT) of liquid and particulate markers for Callithrix jacchus. MRT for cobalt EDTA in Power and Myers (2009) was not different from the results in Caton et  al. (1996). MRT for particulate markers were variable, with the mean values being different among all three studies, indicating an effect of the type of particulate marker on the results

Heymann and Smith (1999) suggest that the temporal pattern of gum-feeding can be a behavioral mechanism to increase the gut residence time of gum. They found that Saguinus mystax and S. fuscicollis concentrated their gum-feeding in the late afternoon, shortly before retiring. Gum would thus be within the intestinal tract at night, when passage rate may have slowed due to the decreased metabolic rate (Power 1991; Power et  al. 2003). Peak gum-feeding and bark gouging bouts in common marmosets are reported to be early in the morning (when guts are likely empty) and at the end of the day (Alonso and Langguth 1989). The same pattern was found in four pygmy marmoset groups in Ecuadorian Amazonia (Yépez et al. 2005). Both of these patterns would be likely to result in longer gut residence time for gum than if it was ingested during the middle of the day. An examination of the temporal pattern of gum-feeding in gum-feeding species is warranted. So what does this all mean? Well, for starters, the MRT of fluid digesta in C. jacchus can be considered to be well established at approximately 14–15  h (Caton et al. 1996) as confirmed by Power and Myers (2009). This is not a particularly long MRT; it does, however, appear to be sufficient to allow fermentation of water-soluble gums (Power 1991; Power and Oftedal 1996). The MRT for particulate matter in C. jacchus is variable. This is as expected, based on the sizable literature for passage rate and retention time in a large number of species. The retention time of particulate matter in a hind-gut fermenter is inversely proportional to particle size. Small particles are preferentially retained; large particles are more rapidly excreted (Van Soest 1982; Hume 1989; Stevens and Hume 1995). Thus it would appear that large particles, such as seeds, will pass through the marmoset digestive tract more rapidly than will soluble material such as gum. Are seeds actually

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excluded from the cecum? The answer to that question isn’t known, though it is reasonable to hypothesize that seeds will be less likely to enter the cecum than will fluid. Do marmosets differ in this fashion from other callitrichids? Again, the answer to that question is not yet known. It is possible that all callitrichids retain soluble digesta longer than large particles.

Marmoset Digestive Tracts C. pygmaea has longer retention times for digesta than any other callitrichid so far studied, despite being the smallest species. This lengthened retention time is not accomplished by having a longer than expected digestive tract. The length of the intestinal tract including the cecum is appropriate for its body size, with the same gut proportions as found in C. jacchus (Power 1991). Thus, in C. pygmaea gut kinetics have changed from the common callitrichid pattern of rapid passage through the gut. This adaptation has several benefits, as well as at least one cost. The cost is that total food intake is more likely to be limited in C. pygmaea. They are more likely to fill their guts, and thus be forced to refrain from feeding. This happens to callitrichids in the wild, even with L. rosalia and Saguinus spp., much larger callitrichids with rapid passage rates. An intensive fruit-eating session can come to a halt, with animals resting, grooming or engaged in other nonfeeding behaviors. The resumption of feeding is preceded by a rain of seeds being defecated (P. Garber, personal communication). C. pygmaea would be more likely to experience such a feeding interruption when feeding on fruit; of course C. pygmaea rarely feeds intensively on fruit in the wild (Soini 1982). The main advantage of the longer retention time in C. pygmaea is more complete digestion of ingested food. The longer retention time would likely increase digestion of gums but also of the animal matter in the diet (mainly invertebrates). The data displayed in Figs. 2.1 and 2.2 indicates that if C. pygmaea retained the common callitrichid gut kinetics then time to first appearance of markers (transit time) would be about 100 min, and, more importantly, the apparent digestibility of energy of this captive diet would have been below 65%, in contrast to the mean value of about 84% the animals achieved with their adapted gut kinetics. That is a substantial difference. Mean digestible energy intake (DE) of the five animals in this study was 27.6 kcal/ day (Power 1991). The animals achieved that DE by ingesting a mean of 32.9 kcal of food. To achieve the same DE at 65% ADE the animals would have had to increase food intake by 30% to 42.7  kcal of food. Wild animals would almost certainly require more food to survive than would captive animals. The DE of these captive animals was equal to twice metabolic rate (Power 1991). Small wild animals will often have daily energy expenditures closer to three times metabolic rate. The increased digestive efficiency C. pygmaea achieves with its longer retention time substantially reduces the amount of food needed for survival. Although gut kinetics of C. jacchus did not appear to differ from that of Saguinus and Leontopithecus and did differ from the more dietarily similar C. pygmaea, both

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common and pygmy marmosets were similar in being better able to digest gum when it was added to the diet (Fig. 2.3; Power 1991; Power and Oftedal 1996). This implies that there is indeed some difference in digestive function between common marmosets and tamarins and lion tamarins despite their similar gut kinetics. Marmoset gut morphology does differ from that of other callitrichids; both Callithrix spp. and C. pygmaea have a larger proportion of the intestinal tract represented by the cecum and colon than do Saguinus and Leontopithecus (Power 1991; Ferrari and Martins 1992; Ferrari et  al. 1993). C. jacchus has a more complex cecum than does L. rosalia (Coimbra-Filha et  al. 1980). These are precisely the differences in gut morphology that would be expected if gum fermentation is a more important component of dietary ecology in marmosets compared to tamarins and lion tamarins. These differences are not dramatic, however. The cecum and colon of marmosets is not particularly capacious. It is more a matter of relative proportions. The total length of the digestive tract in callitrichids appears to be strongly correlated with body mass (Power 1991). The larger species had longer total gut length. This correlation held for the small intestine but not for the colon and cecum (Power 1991). After accounting for body mass, total intestinal length did not differ between marmosets (C. pygmaea and C. jacchus), tamarins (S. oedipus), and lion tamarins (L. rosalia and Leontopithecus chrysomelas). However, the ratio of small intestine to the cecum plus colon was significantly lower in the marmoset species (Power 1991). Thus marmoset gut morphology does appear to be adapted more for fermentation. The marmoset cecum may be performing another function in addition to acting as a fermentation chamber. Marmosets likely are cecal-colon fermenters, with gum fermentation taking place in the upper colon as well as within the cecum. Common marmoset ceca are more complex in internal structure than are ceca of lion tamarins (Coimbra-Filha et al. 1980). The strictures within C. jacchus ceca produce multiple small pockets, where bacterial populations may be protected from washout. The smoother walls of Saguinus and Leontopithecus ceca may result in greater bacterial loss due to the passage of digesta. The marmoset ceca may serve as a reservoir of bacteria to recolonize the proximal colon after the resident bacterial populations have been reduced, perhaps due to the passage of large, hard seeds. The human appendix has been recently suggested to perform such a function, harboring a reservoir of gut microbes that can recolonize the colon (Bollinger et  al. 2007). The greater ability of marmosets to ferment gums may, in part, derive from an enhanced ability to maintain large microbial populations within the upper colon.

Summary Gum is a problematical food; difficult to digest, limited in availability, and likely providing little beyond energy and some minerals. It is not a complete food; but it could complement an insectivorous diet, providing carbohydrate and calcium. Animals that feed extensively on gum would benefit from having a region of the

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gut where high concentrations of gut microbes could act to ferment the gum, producing short-chain fatty acids and liberating the minerals (and possibly protein) so that they can be absorbed and used in metabolism. The fore-gut fermenting colobines should have no difficulty digesting gums. It is not clear how much gum ingestion would benefit colobines; however, as leaves already provide a source of fermentable carbohydrate, likely contain sufficient calcium, and would provide more protein than could gum. The primates known to extensively feed on gum are hind-gut fermenters that often include a substantial amount of invertebrates in their diet. The calcium content of gums may be an important dietary component for these species, as was hypothesized by Bearder and Martin (1980). Differences in digestive function among small New World monkeys (callitrichids) that feed on gum to a greater (C. jacchus and C. pygmaea) or lesser extent (S. oedipus, S. fuscicollis, and L. rosalia) indicate the gum-feeding monkeys have digestive adaptations that favor fermentation. The cecum and colon, gut regions where fermentation can occur in these species, account for a larger proportion of the gut in C. jacchus and C. pygmaea. The structure of the cecum in C. jacchus also suggests that this species will be more able to maintain large microbial populations by recolonizing the colon after washout of microbes by material such as large seeds. Interestingly, gut kinetics in C. jacchus differ from those of C. pygmaea, and are similar to those of the non-gum-specialists. Gut kinetics in most callitrichids appear more adapted to eliminating indigestible material (e.g., seeds) rapidly from the gut than to retaining digesta within the gut to maximize digestion. As C. pygmaea rarely feeds extensively on fruit in the wild this constraint appears to have been relaxed, and their gut kinetics have changed to favor digestive efficiency over maximizing food intake.

References Agrawal, A.A., Konno, K. 2009. Latex: a model for understanding mechanisms, ecology, and evolution of plant defense against herbivory. Annu Rev Ecol 40:311–331. Alonso, C., Langguth, A. 1989. Ecologia e comportamento de Callithrix jacchus (Primates: Callitrichidae) numa ilha de floresta Atlantica. Rev Nordestina Biol 6:105–137. Bearder, S.K., Martin, R.D. 1980. Acacia gum and its use by bushbabies, Galago senegalensis (Primates: Lorisidae). Int J Primatol 1:103–128. Bollinger, R.R., Barbas, A.S., Bush, E.L., Lin, S.S., and Parker, W. 2007. Biofilms in the large bowel suggest an apparent function for the human vermiform appendix. J Theor Biol 249:826–831. Booth, A.N., Elvehjem, C.A., and Hart, E.B. 1949. The importance of bulk in the nutrition of the guinea pig. J Nutr 37:263–274. Booth, A.N., Henderson, A.P. 1963. Physiologic effects of three microbial polysaccharides on rats. Toxicol Appl Pharmacol 5:478–484. Caton, J.M., Hill, D.M., Hume, I.D., and Crook, G.A. 1996. The digestive strategy of the common marmoset. Comp Biochem Physiol A 114:1–8. Chivers, D.J., Wood, B.A., and Bilsborough, A. 1984. Food acquisition and processing in primates. New York: Plenum Press. Coimbra-Filha, A.F., Mittermeier, R.A. 1977. Tree-gouging, exudate-eating, and the short-tusked condition in Callithrix and Cebuella. In The biology and conservation of the Callitrichidae, ed. D.G. Kleiman. Washington (DC): Smithsonian Institution Press.

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Coimbra-Filha, A.F., Rocha, N.D.C., and Pissinatti, A. 1980. Morfofisiologia do ceco e sua correlacao com o tipo odontologico em Callitrichidae (Platyrrhini, Primates). Rev Brasil Biol 40:177–185. Cummings, J.H. 1981. Dietary fibre. Br Med Bull 57:65–70. Demment, M.W. 1983. Feeding ecology and the evolution of body size in baboons. Afr J Ecol 21:219–233. Demment, M.W., Van Soest, P.J. 1985. A nutritional explanation for body-size patterns of ruminant and nonruminant herbivores. Am Nat 125:641–672. Emmons, L.H. 1980. Ecology and resource partitioning among nine species of African rain forest squirrels. Ecol Monogr 50:31–54. Farrell, B.D., Dussourd, D.E., and Mitter, C. 1991. Escalation of plant defense: do latex and resin canals spur plant diversification. Am Nat 138:881–900. Feldmann, M., Heymann, E.W. 2001. The effect of tamarin seed dispersal on the recruitment of Parkia panurensis. Folia Primatol 72:158–159. Ferrari, S.J., Martins, E.S. 1992. Gummivory and gut morphology in two sympatric callitrichids (Callithrix emilae and Saguinus fuscicollis weddelli) from Western Brazilian Amazonia. Am J Phys Anthropol 88:97–103. Ferrari, S.J., Lopes, M.A., and Krause, E.A.K. 1993. Gut morphology of Callithrix nigriceps and Saguinus labiatus from Western Brazilian Amazonia. Am J Phys Anthropol 90:487–493. Fonseca, G.A.B., Lacher, T.E. 1984. Exudate feeding by Callithrix jacchus penicillata in semideciduous woodland (cerrado) in central Brazil. Primates 25:441–450. Garber, P.A. 1986. The ecology of seed dispersal in two species of callitrichid primates (Saguinus mystax and Saguinus fuscicollis). Am J Primatol 10:155–170. Goodrum, L.J., Patel, A., Leykam, J.F., and Kieliszewski, M.J. 2000. Gum arabic glycoprotein contains glycomodules of extension and arabinogalactan-glycoproteins. Phytochemistry 54:99–106. Heymann, E.W., Smith, A.C. 1999. When to feed on gums: temporal patterns of gummivory in wild tamarins, Saguinus mystax and Saguinus fuscicollis (Callitrichinae). Zoo Biol 18:459–471. Hove, E.L., Herndon, F.J. 1957. Growth of rabbits on purified diets. J Nutr 63:193–199. Hume, I.D. 1982. Digestive physiology and nutrition of marsupials. Cambridge: Cambridge University Press. Hume, I.D. 1989. Optimal digestive strategies in mammalian herbivores. Physiol Zool 62:1145–1163. Johnson, I.T., Gee, J.M., and Mahoney, R.R. 1984. Effect of dietary supplements of guar gum and cellulose on intestinal cell proliferation, enzyme levels and sugar transport in the rat. Br J Nutr 52:477–487. Kajiwara, S., Maeda, H. 1983. The monosaccharide composition of cell wall material in cassava tuber (Manihot utilissima). Agric Biol Chem 47:2335–2340. Knogge, C., Heymann, E.W. 2003. Seed dispersal by sympatric tamarins, Saguinus mystax and Saguinus fuscicollis diversity and characteristics of plant species. Folia Primatol 74:33–47. Konno, K., Hirayama, C., Nakamura, M., Tateishi, K., Tamura, Y., Hattori, M., and Kohno, K. 2004. Papain protects papaya trees from herbivorous insects: role of cysteine proteases in latex. Plant J 37:370–378. Kritchevsky, D. 1988. Dietary fiber. Ann Rev Nutr 8:301–328. Lichtenberg, E.M., Hallager, S. 2008. A description of commonly observed behaviors for the kori bustard (Ardeotis kori). J Ethol 26:17–34. Mangione, A.M., Dearing, M.D., and Karasov, W.H. 2000. Interpopulational differences in tolerance to creosote bush resin in desert woodrats (Neotoma lepida). Ecology 81:2067–2076. McLean Ross, A.H., Eastwood, M.A., Brydon, W.G., Anderson, J.R., and Anderson, D.M. 1983. A study of the effects of dietary gum arabic in humans. Am J Clin Nutr 37:368–375. McLean Ross, A.H., Eastwood, M.A., Brydon, W.G., Busuttil, A., and McKay, L.F. 1984. A study of the effects of dietary gum arabic in the rat. Br J Nutr 51:47–56. Milton, K., Dintzis, F. 1981. Nitrogen-to-protein conversion factors for tropical tree samples. Biotropica 13:177–181. Monke, J.V. 1941. Non-availability of gum arabic as a glycogenic foodstuff in the rat. Proc Soc Exp Biol Med 46:178–179.

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Nash, L.T. 1986. Dietary, behavioral, and morphological aspects of gummivory in primates. Yearb Phys Anthropol 29:113–137. National Research Council. 2003. Nutrient requirements of nonhuman primates. Washington (DC): The National Academies Press. Peres, C.A. 2000. Identifying keystone plant resources in tropical forests: the case of gums from Parkia pods. J Trop Ecol 16:287–317. Power, M.L. 1991. Digestive function, energy intake and the response to dietary gum in captive callitrichids [dissertation]. Berkeley (CA): University of California at Berkeley. 235 pp. Power, M.L., Oftedal, O.T. 1996. Differences among captive callitrichids in the digestive responses to dietary gum. Am J Primatol 40:131–144. Power, M.L., Tardif, S.D., Power, R.A., and Layne, D.G. 2003. Resting energy metabolism of Goeldi’s monkey (Callimico goeldii) is similar to that of other callitrichids. Am J Primatol 60:57–67. Power, M.L., Myers, E.W. 2009. Digestion in the common marmoset (Callithrix jacchus), a gummivore–frugivore. Am J Primatol 71:957–963. Ramirez, M.F., Freese, C.H., and Revilla, J.C. 1977. Feeding ecology of the pygmy marmoset, Cebuella pygmaea, in northeastern Peru. In The biology and conservation of the Callitrichidae, ed. D.G. Kleiman. Washington (DC): Smithsonian Institution Press. Rhoades, D.F., Cates, R.G. 1976. Towards a general theory of plant antiherbivory chemistry. Recent Adv Phytochem 10:168–213. Skead, C.J. 1969. Gompou, Ardeotis kori, eating gum. Bokmakierie 21:48. Smith, A.C. 2000. Composition and proposed nutritional importance of exudates eaten by saddleback (Saquinus fuscicollis) and mustached (Saguinus mystax) tamarins. Int J Primatol 21:69–84. Smith, A.P., Lee, A.K. 1984. The evolution of strategies for survival and reproduction in possums and gliders. In Possums and gliders, eds. A. Smith, I. Hume. Chipping North, Australia: Surrey Beatty and Sons Pty Limited. Soini, P. 1982. Ecology and population dynamics of the pygmy marmosets, Cebuella pygmaea. Folia Primatol 39:1–21. Soltis, P.S., Soltis, D.E. 2004. The origin and diversification of angiosperms. Am J Bot 91:1614–1626. Stevens, C.E., Hume, I.D. 1995. Comparative physiology of the vertebrate digestive system. Cambridge: Cambridge University Press. Tardif, S., Jaquish, C., Layne. D., Bales, K., Power, M., Power, R., and Oftedal, O. 1998. Growth variation in common marmoset monkeys fed a purified diet: relation to care-giving and weaning behaviors. Lab Anim Sci 48:264–269. Tomlin, J., Read, N.W. 1988. Laxative properties of indigestible plastic particles. Br Med J 297:1175–1176. Urban, E.K., Brown, L.H., Brown Mrs., and Newman, K.B. 1978. Kori bustard eating gum. Bokmakierie 30:105. Ushida, K., Fujita, S., and Ohashi, G. 2006. Nutritional significance of the selective ingestion of Albizia zygia gum exudate by wild chimpanzees in Bossou, Guinea. Am J Primatol 68:143–151. Van Soest, P.J. 1982. Nutritional ecology of the ruminant. Corvalis, Oregon: O and B Books Inc. Wong, J.M.W., de Souza, R., Kendall, C.W.C., Emam, A., and Jenkins, D.J.A. 2006. Colonic health: fermentation and short chain fatty acids. J Clin Gastroenterol 40:235–243. Wrick, K.L.F. 1979. The influence of dietary fibers on intestinal passage, laxation and stool characteristics in humans [dissertation]. Ithaca (NY): Cornell University. 330 pp. Wyatt, G.M., Bayliss, C.E., and Holcroft, J.D. 1986. A change in human faecal flora in response to inclusion of gum arabic in the diet. Br J Nutr 55:261–266. Yépez, P., de la Torre, S., and Snowdon, C.T. 2005. Interpopulation differences in exudate feeding of pygmy marmosets in Ecuadorian Amazonia. Am J Primatol 66:145–158.

Chapter 3

Exudativory in Primates: Interspecific Patterns Andrew C. Smith

Abstract  This chapter reviews the extent of primate gummivory, identifies phylogentic patterns in the degree of gummivory across primates, and examines overlap in the plant species whose exudates are consumed. Plant exudates are exploited both routinely and opportunistically by at least 69 species of strepsirrhine, platyrrhine, and catarrhine primates. Gummivory is particularly prevalent among the callitrichids, cheirogaleids, and galagos in terms of the number of species reported to consume gum, its contribution to their diet, and the number of plant species they exploit for it. While some marmosets, galagos and the fork-marked lemur are thought of as gum specialists, exudates may account for more than 10% of the diet in many other species. Gum feeding may increase further during periods of dry season resource scarcity with some, most notably Parkia pod gums, acting as a keystone resource for many New World monkeys. Exudates from at least 250 plant species in 170 genera and 63 families are eaten, with Fabaceae and Anacardiaceae being the most frequently exploited. The Callitrichidae were examined for patterns in the amount of gum they consumed. Differences in the prevalence of gummivory were linked to morphological adaptations, particularly dentition, and habitat seasonality. Cluster analysis of the plant families exploited by different primate genera revealed similarities based on the number of families they exploited for gums.

Introduction Exudates are an important part of the diet of a wide range of primates. The three main aims of this chapter are to review the extent of primate gummivory, to identify phylogentic patterns in the degree of gummivory across primates, and to examine overlap in the plant species whose exudates are consumed. Though often overlooked, gummivory has been suggested to have major implications for the ecology and A.C. Smith (*) Animal and Environmental Research Group, Department of Life Sciences, Anglia Ruskin University, East Road, CB1 1PT Cambridge, UK e-mail: [email protected] A.M. Burrows and L.T. Nash (eds.), The Evolution of Exudativory in Primates, Developments in Primatology: Progress and Prospects, DOI 10.1007/978-1-4419-6661-2_3, © Springer Science+Business Media, LLC 2010

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A.C. Smith

social organization of primates (Neyman 1978; Nash 1986; Stevenson and Rylands 1988; Ferrari and Lopes Ferrari 1989; Harrison and Tardif 1994), and more recently has been linked to psychological differences between species, such as the evolution of patience (Stevens et al. 2005). Nash (1986) reviewed the dietary, behavioural, and morphological aspects of gummivory in primates. She noted that exudates do not fit easily into the three commonly used primate dietetic types: frugivore, folivore, and insectivore, and present a unique set of difficulties to be overcome by those feeding upon them both in terms of harvesting and digestion. Morphological adaptations linked to gummivory include small body size and sharp claws or nails, procumbent incisors and an enlarged ceacum, and/or proximal colon. The small body size and sharp claws or nails of callitrichids, galagos, and some lemurs allow them to cling on the vertical trunks from which exudates are produced. The short incisiform canines and procumbent incisors of Callithrix marmosets permit gouging of tree bark to stimulate exudate flow (Sussman and Kinzey 1984), the caniniform first upper premolar of fork-marked lemurs (Phaner spp.) and needle-clawed galagos (Euoticus spp.) may similarly be an adaptation for gouging (Charles-Dominique 1977; CharlesDominique and Petter 1980), and the modified anterior “tooth-comb” or “toothscraper” dentition of several lemurs and lorisids may aid piercing and scraping of gum deposits (Martin 1979; Bearder and Martin 1980; Rosenberger et  al. 1985). Other changes to craniofacial morphology relate to higher load-resistance and larger gape linked to gouging of tree bark to stimulate exudate production and a reduction in the lower leverage capabilities of the jaw adductor muscles for mastication linked to the soft, semi-liquid nature of exudates (Taylor and Vinyard 2004; Viguier 2004). However, there may be differences in morphology associated with gouging vs. scraping as a strategy for gummivory (Burrows and Smith 2005). The enlarged ceacum and/or proximal colon seen in fork-marked lemurs, Southern needle-clawed galagos and some marmosets, provide an increased area for microbial fermentation and is thought to be an adaptation to improve the digestion of b-linked oligosaccharides (Vermes and Weidholz 1930; Chivers and Hladik 1980; Coimbra-Filho et  al. 1980; Martin et  al. 1985; Power 1991; Ferrari and Martins 1992; Ferrari et al. 1993). While the majority of primates lack such adaptations and are thus likely to obtain fewer nutritional rewards from exudates than specialist gummivores, many still consume exudates to a greater or lesser extent throughout the year and may turn to them at certain times as a fallback or even keystone resource. Consequently, the density and distribution of exudate resources may influence the spatial distribution, population density, and home range size and shape of the primates consuming them (Ramirez et al. 1978; Maier et al. 1982; Terborgh 1983; Rylands 1984; Hubrecht 1985; Scanlon et al. 1989; Génin 2003). The consumption of exudates will be influenced by their accessibility; this would be particularly true for the majority of primates which lack dental adaptations to stimulate their production. As with other resources, feeding may be influenced by gum biochemistry, including toxic or beneficial secondary compounds, calcium and other elements. While compounds with hypolipidemic, antibiotic, and detoxifying effects may be found in some gums (Johns et  al. 2000), the high proportion of

3  Exudativory in Primates: Interspecific Patterns

47

calcium in gums relative to that of fruits has been previously cited as a potential reason for their inclusion in the diet of both Old and New World primates (e.g. Bearder and Martin 1980; Garber 1984). However, the relative importance of exudates as a source of calcium has been called into question by the finding that fruits of tropical figs (Ficus spp.) are significantly higher in calcium than non-fig fruits (O’Brien et  al. 1998), and can contain levels greater than those found in exudates (see Smith 2000). Exudates may still have a role to play as a source of calcium, particularly for those primates that do not consume figs. Some gums, such as those of Acacia spp. and perhaps Albizia spp., can have other beneficial physiological effects, such as trapping bile acids. Albizia zygia gum may be actively selected by chimpanzees despite having tannin levels higher than the plant leaves and stems they ingest (Ushida et al. 2006). In addition to beneficial components, exudates may contain toxic secondary compounds which may limit their consumption by primates. For example vervets (Cercopithecus aethiops) choose gums on the basis of low total phenolic content or low levels of one or more constituent phenolics such as tannins rather than high protein content (Wrangham and Waterman 1981). In contrast, Senegal lesser galagos (Galago senegalensis), and possibly patas monkeys (Erythrocebus patas), may select on the basis of flavonoids or other beneficial compounds (Nash and Whitten 1989). Differences in sensitivity and response to bitter or astringent compounds may be linked to dietary composition. Within callitrichids the more gummivorous marmosets are the most tolerant of quinine; this may be adaptive when gnawing bark defended with distasteful alkaloids, saponins, or cyanogenic glycosides (Simmen 1994). Secondary compounds may be detoxified using a mechanism based on glucose as a cosubstrate; however, such a mechanism would reduce the amount of glucose available to be expended as energy. The need for glucose as a detoxification cosubstrate could explain the sugar-rich diet of slow lorises (Nycticebus coucang) and other exudativores which their low basal metabolic rates and often low rates of locomotion would otherwise not predict (Wiens et al. 2006). Exudates may be produced by plants for a variety of reasons including as a response to a pathological condition, insect or other mechanical damage, or the unhealthy state of the plant due to other environmental factors (Glicksman 1969; Meer 1980; Adrian and Assoumani 1983). They may be produced over a time period of minutes to more than 18 h (Fonseca and Lacher 1984). They may also be deliberately produced by some plants as part of their seed dispersal strategy, as in Parkia spp. (Fabaceae) (Hopkins 1983). In such cases, exudates are produced around the seeds inside non-dehiscescent, bean-like pods. These exudate-coated seeds are eaten directly from the pods by primates and other animals, which deposit them far from the parent tree when they defecate, a process referred to as endozoochory (Hopkins 1983; Peres 2000). Among Parkia spp. the exception is P. pendula, which produces exudates at the pod’s sutures when it dehisces (Hopkins, personal communication to DMW Anderson, cited in Anderson and de Pinto 1985). It may be expected that the nutritional composition of endozochorous pod gums would differ from those produced from trunks and branches as a result of damage, with the former having a greater proportion of more easily digested simple sugars.

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As such, these two types of gum should be distinguished and analysed separately wherever possible. This chapter aims to document which primates are known to eat exudates, the extent to which they contribute to their diets, and any patterns in their consumption through a thorough review of the literature. Cluster analysis of the feeding records from the literature will be used to identify groups of primate genera which are similar in the plant families they exploit for gums. This analysis will show whether biogeography, phylogeny or degree of specialisation for gummivory has the greatest influence on the gums eaten.

Literature Analysis Data on the contribution of gum to the diet and the species of exudates consumed by a variety of primates were extracted from 130+ published sources. Plant taxonomy was checked and follows that published by the Missouri Botanical Garden TROPICOS website (Anon 2008). The taxonomy of African primates follows Grubb et al. (2003), that of Asian primates follows Brandon-Jones et al. (2004), and that of Neotropical primates follows Rylands et al. (2000). These records were used to calculate the total number of exudate species exploited by each primate and the number of primates exploiting each exudate species. To examine patterns of similarity in the exudates consumed by different primates data were reformatted for cluster analysis via the MultiVariate Statistical Package (MVSP; Kovach 1999). They were collapsed to the level of plant family and primate genus, with the exception of Callithrix which was split into three groups following Rylands and Faria (1993); the C. jacchus group (C. jacchus and C. penicillata), C. flaviceps group (C. flaviceps and C. aurita), and C. kuhli group (C. kuhli and C. geoffroyi). Analysis was restricted to the strepsirrhines and Callitrichidae as the majority of other primate genera are known to feed on gums from two or fewer families. Cluster analysis was performed using a UPGMA cluster algorithm and a Sorensen (Ss) presence/no record (1/-) algorithm (Krebs 1989). Sorensen’s coefficient, the out-put statistic of the analysis, is a measure of the similarity between the primate genera in terms of the plant families exploited for gum. Sorensen’s algorithm was chosen as it provides a presence/no record criterion rather than a presence/absence criterion and as such is more robust where data are missing (false absence) (Pugh and Convey 2008).

Results Prevalence of Gummivory Exudates are eaten by at least 69 species of primates, including members of at least five strepsirrhine families, five platyrrhine families, and both catarrhine families

3  Exudativory in Primates: Interspecific Patterns

49

(Table 3.1). Some are considered to be specialist gummivores; these species ­typically have morphological adaptations for gummivory, and exudates constitute the majority of their diet. Examples include fork-marked lemurs (Phaner furcifer), southern needle-clawed galago (Euoticus elegantulus), thick-tailed galagos (Otolemur crassicaudatus), marmosets (e.g. Callithrix spp.), pygmy marmosets (Cebuella pygmaea) and possibly the hairy-eared dwarf lemur (Allocebus trichotis) (Martin 1972; Doyle and Bearder 1977; Charles-Dominique and Petter 1980; Harcourt 1980; Soini 1982; Ferrari and Digby 1996; Corrêa et al. 2000; Viguier 2004; Biebouw 2009). However, it is clear from Table 3.1 that exudates form a regular and significant food for other primates, accounting for up to 15% of the diet in yellow baboons (Papio cynocephalus), 21% in pottos (Perodictus potto), 37% in patas monkeys (Erythrocebus patas) and 75% in grey mouse lemurs (Microcebus murinus) (Charles-Dominique and Bearder 1979; Post 1982; Isbell 1998; Génin 2003). Many more primates have also been reported to include them in their diet.

Seasonality of Consumption Many species of primates show seasonal changes in the amount of time spent feeding on exudates, typically increasing consumption in the dry season (Table  3.2). However, not all show the same pattern. For example while red-­ bellied (Saguinus labiatus) and saddleback tamarins (S. fuscicollis) increased gum consumption in the dry season, sympatric Goeldi’s monkeys (Callimico goeldi) increased mycophagy (Porter 2000). Some, such as fork-marked lemurs, may show no significant seasonal variation in gummivory (Schülke 2003), and others such as Geoffroy’s tamarins (S. geoffroyi) may consume more in the wet season (Garber 1984).

Species Consumed At least 250 species (plus 75 identified to genus) of exudates from 170 genera in 63 families have been reported to be consumed by primates (Table 3.3). Saddleback tamarins are known to consume exudates from 62 species of plant, more than any other primate. Species for which exudate feeding has been reported in the ten genera, Callimico, Callithrix, Cebuella, Mico, Microcebus, Papio, Phaner, Saguinus, Semnopithecus, and Homo all exploit exudates from a mean of ten or more species of plant (Table 3.4). The majority, 91.9%, of exudate species have been reported to be exploited by just one or two primate species. In contrast, the two most frequently recorded exudates, those from Parkia pendula and P. nitida pods, are eaten by 15 and 12 primates, respectively. Overall Parkia and Acacia are the most frequently exploited genera, and Fabaceae and Anacardiaceae are the families most frequently exploited for exudates (Table 3.5).

Lemuridae

0–2 ? ? ?

Varecia variegata

? 10.5 ?

Eulemur macaco Lemur catta L. fulvus

G. senegalensis Galagoides demidovii Otolemur crassicaudatus

33.3 a,d

Table 3.1  Primates known to consume exudates, and the proportion of exudates in their diet Percentage of diet Clade Family Species Total Plant Strepsirrhini Cheirogaleidae 19 Allocebus trichotis Cheirogaleus major 1 1.0 a C. medius 2 2.1a Microcebus berthae 0.2 M. griseorufus 55–95 a,b c M. murinus 75.0  93.0 a,c 9.2 4 4.9a a 12.5 0–43 M. ravelobensis 30 Mirza coquereli ? Phaner furcifer 85.8 P. pallescens ? Daubentoniidae Daubentonia madagascarensis ? Lepilemuridae Lepilemur leucopus ? Galaginae Euoticus elegantalus 75 93.4 a,d Galago moholi ? Reference Biebouw (2009) Lahann (2007) Lahann (2007) Dammhahn and Kappeler (2008a) Génin (2008) Génin (2003) Dammhahn and Kappeler (2008b) Lahann (2007) Radespiel et al. (2006) Joly-Radko and Zimmermann, Chap. 7 Radespiel et al. (2006) Hladik (1979); Nash (1986); Pages (1980) Schülke (2003) Génin, personal communication Petter (1977) Charles-Dominique and Hladik (1971) Charles-Dominique and Bearder (1979) Bearder and Martin (1980); Harcourt (1986); Harcourt and Bearder (1989) Nash and Whitten (1989) Charles-Dominique and Bearder (1979) Charles-Dominique and Bearder (1979); Clark (1978); Crompton (1984); Harcourt (1986) Simmen et al. (2007) Sussman (1974) Sussman, personal communication in Coimbra-Filho and Mittermeier (1977) Ratsimbazafy et al. (2002)

50 A.C. Smith

Platyrrhini

Clade

Callitrichidae

C. jacchus C. penicillata Cebuella pygmaea Leontopithecus caissara L. chrysomelas

C. geoffroyi C. kuhli

C. flaviceps

Callithrix aurita

Nycticebus coucang N. pygmaeus Perodictus potto Aloutatta belzebul A. palliata A. seniculus Aotus trivirgatus Ateles paniscus Lagothrix lagotricha Callimico goeldii

Lorisidae

Atelidae

Species

Family

67e 1.3

53 28 73.2a

76c 67.1a

43.3a ? 21d ? ? ? ? ? 5.9 1.0 14 29.8 50.5 0 65.7a 82.2

3–11c

79.7 70+ 100

33.8

42.4a 82.1a 0 82 96.4 82.0

23.3a,d

Percentage of diet Total Plant Wiens et al. (2006) Tan and Drake (2001) Charles-Dominique and Bearder (1979) Bonvicino (1989) Hladik and Hladik (1969) Izawa (1975) Hladik and Hladik (1969) van Roosmalen (1985a, b) Peres (1994b) Porter (2001) Porter et al. (2007) Corrêa et al. (2000) Martins and Setz (2000) Muskin (1984) Ferrari and Digby (1996) Corrêa et al. (2000) Ferrari and Rylands (1994) Guimarães (1998) Passamani (1998) Ferrari and Rylands (1994) Raboy et al. (2008) Rylands (1989) Ferrari and Digby (1996) Fonseca and Lacher (1984) Ramirez et al. (1978) Prado (1999) Rylands (1989)

Reference

(continued)

3  Exudativory in Primates: Interspecific Patterns 51

Clade

Family

Table 3.1  (continued)

S. niger S. nigricollis S. oedipus

S. geoffroyi S. imperator S. labiatus S. midas S. mystax

Mico emiliae M. intermedius M. melanurus Saguinus bicolor S. fuscicollis

L. rosalia

L. chrysopygus

Species

1.5c 11.1a,b,c 10.4 3.1 ?

14.4 ? 8.0 ?

7.6 c 11.9 a,b,c 15.8 14.4 12.0

? 15.5 a ?

15.2 13.5 1.5 c

20 ?

Macaca radiata

0.87

Chapman et al. (2002) 2.3 a

? 1.9

C. ascanius

C. mitis

g

Whitten (1983); Wrangham and Waterman (1981)

3.7 a

0.8

?

Cercopithecidae

Pitheciidae

Peres (1994a, 2000) Hladik and Hladik (1969) Stone (2007) Heymann (1990) Peres (1993b) Izawa (1975) Cords (1986)

C. aethiops

Reference

? ? 4.6 ? 0.8 ? 2.8

Cebus apella C. capucinus Saimiri sciureus Cacajao calvus Pithecia albicans P. monachus Cercopithecus ascanius

Cebidae

Percentage of diet Total Plant

Species

Family

Calculated by this author Includes foraging c Dry season only d Stomach contents e Includes gouging f Not including pod gums g Yearling diet, based on mass

Catarrhini

Clade

3  Exudativory in Primates: Interspecific Patterns 53

Catarrhini

Platyrrhini

Clade Strepsirrhini

Cercopithecidae

Cebidae

Lemuridae Callitrichidae

Galaginae

Family Cheirogaleidae

   

  

Leontopithecus chrysopygus Mico intermedius S. bicolor bicolour Saguinus fuscicollis

S. labiatus S. midas niger S. mystax S. geoffroyi Cebus apella Lagothrix lagotricha Saimiri sciureus Semnopithecus entellus   

       



Seasonal increase Dry None  

Phaner furcifer Galago moholi Otolemur crassicaudatus Eulemur macaco Callithrix aurita C. flaviceps C. humeralifer Callimico goeldi

Species Microcebus griseorufus M. murinus

Table 3.2  Seasonal changes in gum feeding in primates





Wet

Reference Génin (2008) Dammhann and Kappeler (2008b); Joly and Zimmermann, this volume Schülke (2003) Bearder and Martin (1980); Harcourt (1986) Harcourt (1986) Simmen et al. (2007) Ferrari et al. (1996) Ferrari et al. (1996) Rylands (1984) Porter et al. (2007) Porter (2000) Albernaz (1997); Passos (1997) Rylands (1982) Egler (1992) Garber (1980); Norconk (1986); Soini (1987); Ramirez (1989); Lopes and Ferrari (1994); Peres (1994a); Porter (2000); Soini (1987) Porter (2000) Oliveira and Ferrari (2000) Ramirez (1985); Peres (1994a) Garber (1984) Peres (1994a) Peres (1994a, b) Stone (2007) Newton (1992)

54 A.C. Smith

Sclerocarya birrea Spondias macropcarpa S. mombin (= S. lutea)

Buchanania arborescens B. lanzan B. sessifolia Gluta curtisii Lannea coromandelica L. schweinfurthii L. triphylla Mangifera griffithi Ocrantomelon dao Operculicarya gummifera Poupartia minor P. silvatica

Anacardium sp. Astronium fraxinifolium (= A. graveolens)

Reference Garber (1980, 1984a) Rylands (1982) Coimbra-Filho and Mittermeier (1977); Scanlon et al. (1989); Stevenson and Rylands (1988) Simmen et al. (2007) Wiens et al. (2006) Rylands (1984) Torres de Assumpção (1983) Stevenson and Rylands (1988); Scanlon et al. (1989) Wiens et al. (2006) Newton (1992) Wiens et al. (2006) Wiens et al. (2006) Ripley (1970); Newton (1992) Norton et al. (1987) Johns et al. (2000) Wiens et al. (2006) Wiens et al. (2006) Schülke (2003) Génin, personal communication Radespiel et al. (2006) Radespiel et al. (2006) Schülke (2003) Norton et al. (1987) Stevenson and Rylands (1988) Stevenson and Rylands (1988) Soini (1982); Yépez et al. (2005) Soini (1987)

Eulemur macaco Nycticebus coucang Callithrix penicillata Callithrix aurita Callithrix jacchus Nycticebus coucang Semnopithecus entellus Nycticebus coucang Nycticebus coucang Semnopithecus entellus Papio cynocephalus Homo sapiens Nycticebus coucang Nycticebus coucang Phaner furcifer Microcebus griseorufus Microcebus murinus Microcebus ravelobensis Phaner furcifer Papio cynocephalus Callithrix jacchus Callithrix jacchus Cebuella pygmaea Saguinus fuscicollis

Table 3.3  Sources of exudate recorded to be consumed by primates Family and speciesa Consumer Anacardiaceae Anacardium excelsum Saguinus geoffroyi A. giganteum Mico intermedius A. occidentale Callithrix jacchus

3  Exudativory in Primates: Interspecific Patterns 55

Arecaceae

Araliaceae

Apocynaceae

Annonaceae

Family and speciesa

Table 3.3  (continued)

Callimico goeldii Mico intermedius Semnopithecus entellus Varecia variegata Varecia variegata Leontopithecus rosalia

Tapirira sp. Unidentified sp. Duguetia spixiana Neo-Uvaria foetida Forsteronia benthamiana Forsteronia sp. Hancornia speciosa Schefflera macrocarpa (=Didymopanax)

S. morotoni (=Didymopanax) Schefflera sp. (=Didymopanax) Borassus flabellifer Dypsis nauseosa Dypsis sp. Euterpe edulis

Garber (1980, 1984a) Rylands (1982) Rylands (1984) Porter et al. (2009) Coimbra-Filho and Mittermeier (1977); Stevenson and Rylands (1988) Raboy et al. (2008) Lacher et al. (1984) Passos and de Carvalho (1991) Coimbra-Filho and Mittermeier (1976) Egler (1992) Smith (1997) Smith (1997) Rylands (1982) Rylands (1982) Oppenheimer (1977) Knogge (1998) Wiens et al. (2006) Knogge (1998) Rylands (1982) Rizzini and Coimbra-Filho (1981) Fonseca and Lacher (1984); Miranda and de Faria (2001) Porter et al. (2009) Rylands (1981, 1982) Hrdy (1977) Ratsimbazafy et al. (2002) Ratsimbazafy et al. (2002) Peres (1986) Saguinus geoffroyi Mico intermedius Mico melanurus Callimico goeldii Callithrix jacchus Callithrix kuhlii Callithrix penicillata Leontopithecus chrysopygus Leontopithecus rosalia Saguinus bicolor Saguinus fuscicollis Saguinus mystax Mico intermedius Mico intermedius Semnopithecus entellus Saguinus fuscicollis Nycticebus coucang Saguinus fuscicollis Mico intermedius Callithrix penicillata Callithrix penicillata

Tapirira guianensis

Reference

Consumer

56 A.C. Smith

Asteraceae Bombacaceae

Aristolochiaceae Ascelpiadaceae

Family and speciesa

Adansonia sp.

W. drudei (= Catoblastus) Aristolochia sp. Pentarrhinum insipidumb Sarcostemma viminaleb Unidentified sp. Aspilia mossambicensis Adansonia rubrostipa

Wettinia augusta

O. bataua (=Jessenia bataua)

Oenocarpus bacaba

I. setigura

Iriartella retisera

I. exorrhiza (=Socratea)

Heteropsis spruceana Iriartea deltoidea (=I. ventricosa)

E. precatoria

Consumer

Saguinus fuscicollis Saguinus mystax Saguinus mystax Cebuella pygmaea Papio hamadryas Papio hamadryas Semnopithecus entellus Homo sapiens Phaner furcifer Phaner pallescens Mirza coquereli

Callimico goeldii Saguinus fuscicollis Saguinus fuscicollis Saguinus mystax Saguinus fuscicollis Saguinus mystax Saguinus fuscicollis Saguinus mystax

Callimico goeldii Saguinus fuscicollis Saguinus fuscicollis Callimico goeldii Saguinus fuscicollis Saguinus imperator Saguinus fuscicollis Saguinus mystax

Porter (2001); Porter et al. (2009) Porter (2001) Smith (1997) Porter et al. (2009) Terborgh (1983); Peres (1993a) Terborgh (1983); Peres (1993a) Peres (1993a); Smith (1997) Peres (1993a); Smith (1997); Heymann and Smith (1999) Porter (2001) Porter (2001) Peres (1991) Peres (1991) Peres (1993a) Peres (1993a) Peres (1993a); Smith (1997); Knogge (1998) Peres (1993a); Smith (1997); Knogge (1998); Heymann and Smith (1999) Smith (1997) Heymann and Smith (1999) Heymann and Smith (1999) Yépez et al. (2005) Swedell et al. (2008) Swedell et al. (2008) Oppenheimer (1977) Johns et al. (2000) Schülke (2003) Génin, personal communication Pages (1980) (continued)

Reference 3  Exudativory in Primates: Interspecific Patterns 57

Capparaceae

Burseraceae

Bromeliaceae

Boraginaceae

Family and speciesa

Table 3.3  (continued)

Dacryodes rugosa Unidentified sp. Maerua cylindrocarpa

C. habessinica C. humbertii C. lamii C. orbicularis C. schimperi Commiphora sp.

Commiphora africana C. aprevalii C. arafy

Ceiba samauma C. speciosa (=Chorisia) Eriotheca pubescens Matisia cordata (=Quararibea) Quararibea rhombifolia Quararibea sp. Scleronema sp. Cordia latifolia C. myxa C. nodosa Unidentified sp.

Reference Charles-Dominique and Petter (1980) Soini (1988) Hardie (1995) Miranda and de Faria (2001) Moynihan (1976) Ramirez et al. (1978) Ramirez (1989) Knogge (1998) Newton (1984) Newton (1984) Smith (1997) Peres (1993a) Peres (1993a) Johns et al. (2000) Génin, personal communication Schülke (2003) Dammhahn and Kappeler (2008b) Johns et al. (2000) Génin, personal communication Génin, personal communication Génin, personal communication Johns et al. (2000) Génin (2003); Radespiel et al. (2006) Radespiel et al. (2006) Charles-Dominique and Petter (1980) Wiens et al. (2006) Tan and Drake (2001) Radespiel et al. (2006)

Consumer Phaner furcifer Cebuella pygmaea Saguinus labiatus Callithrix penicillata Cebuella pygmaea Cebuella pygmaea Saguinus mystax Saguinus fuscicollis Semnopithecus entellus Semnopithecus entellus Saguinus fuscicollis Saguinus fuscicollis Saguinus mystax Homo sapiens Microcebus griseorufus Phaner furcifer Microcebus murinus Homo sapiens Microcebus griseorufus Microcebus griseorufus Microcebus griseorufus Homo sapiens Microcebus murinus Microcebus ravelobensis Phaner furcifer Nycticebus coucang Nycticebus pygmaeus Microcebus murinus

58 A.C. Smith

Smith (1997) Peres (1993a) Peres (1993a) Crompton (1984) Norton et al. (1987) Norton et al. (1987) Norton et al. (1987) Carvalho and Carvalho (1989) Rylands (1982) Radespiel et al. (2006) Schülke (2003) Starin (1978); Newton (1984) Génin (2003) Coimbra-Filho and Mittermeier (1977) Saguinus mystax Saguinus fuscicollis Saguinus mystax Otolemur crassicaudatus Papio cynocephalus Papio cynocephalus Papio cynocephalus Leontopithecus chrysopygus Mico intermedius Microcebus murinus Phaner furcifer Semnopithecus entellus Microcebus murinus Callithrix jacchus

Clusiaceae Combretaceae

Mammea punctata Terminalia aff. diversipilosa T. bellirica T. bownii T. catappa

Combretum erthrophyllum C. hereroense C. mossambicense C. zeyheri Combretum sp.

Buchenavia sp.

Kielmeyera coriacea Anogeissus latifolia Buchenavia guianensis (=Terminalia pamea/Pamea guinanensis)

Coussapoa sp. Pourouma cercropiifolia Hirtella grisilipes H. pilosissima Licania sp.

Cercropiaceae

Chrysobalanceae

Miranda and de Faria (2001) Fonseca and Lacher (1984) Ripley (1970) Radespiel et al. (2006) Radespiel et al. (2006) Soini (1982) Smith (1997) Lacher et al. (1984) Knogge (1998) Smith (1997) Present studyc Miranda and de Faria (2001) Newton (1984) Smith (1997)

Callithrix penicillata Callithrix penicillata Semnopithecus entellus M. murinus M. ravelobensis Cebuella pygmaea Saguinus fuscicollis Callithrix penicillata Saguinus fuscicollis Saguinus fuscicollis Saguinus mystax Callithrix penicillata Semnopithecus entellus Saguinus fuscicollis

Caryocar brasiliense Austroplenckia populniab Elaeodendron glaucum Mystroxylon aethiopicum

Caryocaraceae Celastraceae

Reference

Consumer

Family and speciesa

(continued)

3  Exudativory in Primates: Interspecific Patterns 59

Cunoniaceae Cupressaceae Dilleniaceae

Compositae Convolvulaceae

Family and speciesa

Table 3.3  (continued)

Belangera sp. Juniperus procera Doliocarpus brevipedicellatus D. dentatus Unidentified sp.

Terminalis sp. Unidentified sp. Maripa sp.

T. ombrophila T. spinosa T. tomentosa Terminalia sp.

T. neotaliala (=T. mantaly) T. oblonga

T. mantaliopsis

Consumer

Microcebus ravelobensis Phaner furcifer Phaner pallescens Mirza coquereli Cebuella pygmaea Cebuella pygmaea Saguinus fuscicollis Saguinus mystax Callithrix penicillata Homo sapiens Mico intermedius Mico intermedius Cebuella pygmaea

Microcebus murinus Phaner furcifer Microcebus murinus Cebuella pygmaea Saguinus fuscicollis Phaner furcifer Papio cynocephalus Semnopithecus entellus Allocebus trichotis Callithrix aurita Callithrix jacchus Cebuella pygmaea Leontopithecus chrysopygus Microcebus murinus

Reference Génin (2003) Hladik et al. (1980) Génin, personal communication Yépez et al. (2005) Soini (1987); Terborgh (1983) Schülke (2003) Norton et al. (1987) Newton (1984) Biebouw (2009) Ferrari et al. (1996); Martins and Setz (2000) Stevenson and Rylands (1988) Soini (1982) Albernaz (1997) Dammhahn and Kappeler (2008b); Radespiel et al. (2006) Radespiel et al. (2006) Charles-Dominique and Petter (1980) Génin, personal communication Pages (1980) Soini (1982) Soini (1982) Soini (1987); Present studyc Present studyc Lacher et al. (1984) Johns et al. (2000) Rylands (1982) Rylands (1982) Soini (1982)

60 A.C. Smith

Fabaceae

Erythroxylaceae Euphorbiaceae

Euphorbia candelabrum E. spinescens Euphorbia sp. Jatropha sp. Micrandra spruceana Monadenium stapelioides Acacia brevispica var. schweinfurthii

Vallea stipularis Erythroxylum sp. Croton cuneatus Croton sp.

S. multiflora S. stipitata Sloanea sp.

S. fragrans S. guianensis

Saguinus labiatus Mico intermedius Cebuella pygmaea Microcebus murinus Cebuella pygmaea Callithrix aurita Callithrix flaviceps Callithrix kuhlii Eulemur macaco Homo sapiens Homo sapiens Microcebus murinus Callithrix jacchus Saguinus fuscicollis Homo sapiens Microcebus murinus Microcebus ravelobensis

Microcebus ravelobensi Saguinus fuscicollis Saguinus mystax Saguinus fuscicollis Cebuella pygmaea Saguinus fuscicollis Saguinus fuscicollis Callithrix flaviceps Callithrix penicillata Cebuella pygmaea Saguinus fuscicollis

Ebenaceae Elaeocarpaceae

Diospyros sp. Sloanea floribunda

Consumer

Family and speciesa

(continued)

Radespiel et al. (2006) Smith (1997) Smith (1997) Knogge (1998) Soini (1988) Soini (1987) Knogge (1998) Ferrari (1988); Ferrari et al. (1996) Rylands (1984) Terborgh (1983) Terborgh (1983); Smith (1997); Knogge (1998); Porter (2001) Porter (2001) Rylands (1982) Izawa (1975) Radespiel et al. (2006) Soini (1982, 1988) Ferrari et al. (1996) Ferrari (1988); Ferrari et al. (1996) Raboy et al. (2008) Simmen et al. (2007) Johns et al. (Johns et al., 2000) Johns et al. (2000) Martin (1973) Stevenson and Rylands (1988) Present studyc Johns et al. (2000) Radespiel et al. (2006) Radespiel et al. (2006)

Reference 3  Exudativory in Primates: Interspecific Patterns 61

Family and speciesa

Table 3.3  (continued)

A. sieberiana A. tortilis

A. robusta A. senegal A. seyal

A. polyphilla A. riparia

A. loretensis A. martiusiana A. nilotica A. paniculata

A. elatior A. karroo

Acacia catechu A. drepanolobium

Consumer

Otolemur crassicaudatus Saguinus fuscicollis Callimico goeldii Galago moholi Callithrix aurita Callithrix flaviceps Callithrix geoffroyi Callithrix jacchus Mico intermedius Callithrix aurita Cebuella pygmaea Saguinus fuscicollis Papio cynocephalus Papio hamadryas Erythrocebus patas Homo sapiens Papio cynocephalus Cercopithecus aethiops Galago moholi Homo sapiens Papio cynocephalus

Semnopithecus entellus Erythrocebus patas Galago senegalensis Homo sapiens Cercopithecus aethiops Galago moholi

Reference Starin (1978) Isbell (1998) Nash and Whitten (1989) Johns et al. (2000) Whitten (1983) Bearder and Martin (1980); Harcourt (1986); Harcourt and Bearder (1989) Crompton (1984); Harcourt (1986) Soini (1987) Porter et al. (2009) Bearder and Martin (1980) Martins and Setz (2000) Ferrari (1988); Ferrari et al. (1996) Passamani (1996) Scanlon et al. (1989) Rylands (1982) Martins and Setz (2000) Soini (1982) Soini (1982, 1987) Norton et al. (1987) Swedell et al. (2008) Isbell (1998) Johns et al. (2000) Norton, personal communication Wrangham and Waterman (1981) Bearder and Martin (1980) Johns et al. (2000) Whitten (1983); Altmann (1998)

62 A.C. Smith

Family and speciesa

Bauhinia sp.

Anadenanthera sp. Baudouinia fluggeiformis

Anadenanthera colubrine (=A. macrocarpa/Piptadenia colubrine) A. peregrina (=Piptadenia peregrina)

A. versicolor A. mainaea A. zygia Albizia sp.

Callithrix penicillata Callithrix penicillata Microcebus murinus Microcebus ravelobensis Callithrix aurita

Callithrix flaviceps

Callithrix jacchus

Euoticus elagantalus Microcebus ravelobensis Otolemur crassicaudatus Microcebus murinus Pan troglodytes Pan troglodytes

Callithrix jacchus Mico intermedius E. patas Callithrix penicillata Daubentonia madagascarensis Microcebus griseorufus Microcebus murinus

Acacia sp.

Acosmium dasycarpum Afzelia bijuga Alantsilodendron alluaudianum Alantsilodendron sp. (A. cinereum not recognised) Albizia gummifera

Cercopithecus aethiops Erythrocebus patas Galago senegalensis Homo sapiens Papio cynocephalus

A. xanthophloea

Consumer

(continued)

Charles-Dominique (1977) Radespiel et al. (2006) Charles-Dominique and Bearder (1979) Génin, personal communication Ushida et al. (2006) Nishida and Uehara (1983); Sugiyama and Koman (1987, 1992); Yamakoshi (1998) Coimbra-Filho et al. (1973); Stevenson and Rylands (1988); Scanlon et al. (1989) Coimbra-Filho et al. (1981); Ferrari (1988); Ferrari et al. (1996) Rizzini and Coimbra-Filho (1981) Miranda and de Faria (2001) Radespiel et al. (2006) Radespiel et al. (2006) Martins and Setz (2000)

Wrangham and Waterman (1981) Isbell (1998) Nash and Whitten (1989) Johns et al. (2000) Hausfater and Bearce (1976); Post (1982); Whitten (1983); Altmann (1998) Stevenson and Rylands (1988) Rylands (1982) Olson (1985) Miranda and de Faria, (2001) Petter (1977) Génin, personal communication Génin, personal communication

Reference 3  Exudativory in Primates: Interspecific Patterns 63

Family and speciesa

Table 3.3  (continued)

Chamaecrista sp. Colvillea racemosa Dalbergia brasiliensis D. frutescens D. nigra Dalbergia sp. Delonix decary D. floribunda Dioclea sp Diplotropis purpurea Diplotropis sp. Dipteryx sp. Entada gigas E. polystachya E. scelerata Enterolobium contorsiliquum E. cyclocarpum E. ellipticum E. maximum E. schomburgkii Enterolobium sp. Erythrina glauca Hymenaea parvifolia

Campsiandra laurifolia Cassia sp.

Reference Soini (1982) Soini (1982) Soini (1982) Ramirez (1989) Miranda and de Faria (2001) Charles-Dominique and Petter (1980) Martins and Setz (2000) Martins and Setz (2000) Ferrari (1988); Ferrari et al. (1996) Ferrari (1988); Ferrari et al. (1996) Génin, personal communication Schülke (2003) Soini (1982) Rylands (1982) Rylands (1984) Yépez et al. (2005) Charles-Dominique (1977) Soini (1982) Charles-Dominique (1977) Carvalho and Carvalho (1989) Hladik and Hladik (1969) Miranda and de Faria (2001) Rylands (1981, 1982) Rylands (1982) Stevenson and Rylands (1988) Smith (1997) Peres (1993a) Peres (1993a)

Consumer Cebuella pygmaea Cebuella pygmaea Cebuella pygmaea Saguinus mystax Callithrix penicillata Phaner furcifer Callithrix aurita Callithrix aurita Callithrix flaviceps Callithrix flaviceps Microcebus murinus Phaner furcifer Cebuella pygmaea Mico intermedius Mico melanurus Cebuella pygmaea Euoticus elagantalus Cebuella pygmaea Euoticus elagantalus Leontopithecus chrysopygus Saguinus geoffroyi Callithrix penicillata Mico intermedius Mico intermedius Callithrix jacchus Saguinus fuscicollis Saguinus fuscicollis Saguinus mystax

64 A.C. Smith

Family and speciesa

Lonchocarpus glabrescens

I.ruiziana I.sessilis I.spectabilis I.splendens I.thiabaudiana Inga sp.

I.fagifolia (=I. marginata) I.ingoides I.marginata I.nobilis

H. stigonocarpa Hymenolobium sp. Inga barbata I. cf affinis I. chartacea I.edulis (=I. benthamiana)

Consumer

Mico intermedius Saguinus fuscicollis Saguinus imperator Saguinus mystax S. nigricollis Saguinus fuscicollis

Callithrix penicillata Mico intermedius Callithrix aurita Callithrix aurita Callimico goeldii Callithrix kuhlii Cebuella pygmaea Saguinus fuscicollis Cebuella pygmaea Saguinus fuscicollis Callithrix aurita Cebuella pygmaea Saguinus fuscicollis Cebuella pygmaea Callithrix aurita Cebuella pygmaea Saguinus imperator Mico intermedius Callithrix aurita Callithrix flaviceps Callithrix penicillata Cebuella pygmaea

Reference

(continued)

Miranda and de Faria (2001) Rylands (1982) Ferrari et al. (1996) Martins and Setz (2000) Porter et al. (2009) Raboy et al. (2008) Yépez et al. (2005) Terborgh (1983) Yépez et al. (2005) Soini (1987) Ferrari et al. (1996) Terborgh (1983); Yépez et al. (2005) Terborgh (1983) Yépez et al. (2005) Ferrari et al. (1996) Soini (1988) Terborgh (1983) Rylands (1982) Ferrari et al. (1996); Martins and Setz (2000) Ferrari (1988); Ferrari et al. (1996) Rylands (1984); Miranda and de Faria (2001) Moynihan (1976); Ramirez et al. (1978); Soini (1982) Rylands (1982) Terborgh (1983); Soini (1987); Smith (1997) Terborgh (1983) Ramirez (1989) Izawa (1975) Soini (1987)

3  Exudativory in Primates: Interspecific Patterns 65

Family and speciesa

Table 3.3  (continued)

P. nitidapod + trunk (=P. oppositifolia)

P. multijugapod

Parkia balslevii P. discolourpod (=P. auriculata) P. igneiflora

Machaerium sp. Macrolobium acaciifolium Mimosa sp. Myroxylon balsamum

Consumer

Mico intermedius

Saguinus mystax

Cebus apella Lagothrix lagotricha Pithecia albicans Pithecia monachus Saguinus fuscicollis

Saimiri sciureus Lagothrix lagotricha Saguinus bicolor Alouatta seniculus Ateles paniscus Cacajao calvus Cebuella pygmaea

Leontopithecus rosalia Cebuella pygmaea Saguinus mystax Saguinus fuscicollis Saguinus labiatus Cebuella pygmaea Saguinus bicolor Saguinus fuscicollis Saguinus mystax

Reference Peres (1989) Soini (1988) Ramirez (1989) Porter (2001) Porter (2001) Yépez et al. (2005) Egler (1992) Smith (1997); Knogge (1998); Present studyc Smith (1997); Knogge (1998); Heymann and Smith (1999); Present studyc Smith (1999) Defler and Defler (1996); Peres (2000) Egler (1992) Izawa (1975) van Roosmalen (1985a) Heymann (1990) Izawa (1975); Soini (1988); Soinin, personal communication to Peres (2000) Peres (2000) Izawa (1975); Peres (2000) Peres (1993b) Izawa (1975) Izawa (1978); Norconk (1986); Monge (1987); Soini (1987); Castro (1991); Garber (1993a, b); Peres (1993a); Smith (1997); Knogge (1998) Norconk (1986); Ramirez (1989); Garber (1993b); Peres (1993a, 2000); Smith (1997); Knogge (1998) Rylands (1982)

66 A.C. Smith

Family and speciesa

Pithecellobium dulce

Piptadenia sp.pod

Piptadenia gonoacantha P. pteroclada

Parkia sp. Peltogyne altissima

P.velutina

P. pendula

pod

Bonvicino (1989) van Roosmalen (1985b) Bonvicino (1989) Rylands (1982, 1984); Raboy et al. (2008) Rylands (1984) Peres (1994a) Peres (1994a, b) Rylands (1982, 1989); Raboy and Dietz (2004) Lopes and Ferrari (1994) Rylands (1981, 1982) Buchanan-Smith (1991); Lopes and Ferrari (1994); Peres (2000); Porter (2001) Buchanan-Smith (1991); Porter (2001) Rylands, personal communication; Sussman and Kinzey (1984); van Roosmalen (1985b) Peres (2000) Oliveira and Ferrari (2000) Porter et al. (2009) Porter (2001); Present study Porter (2001) Hernandez-Camacho and Cooper (1976) Smith (1997) Smith (1997) Ferrari (1988); Ferrari et al. (1996) Yépez et al. (2005) Soini (1987) Pook and Pook (1981) Fonseca et al. (1980 Génin, personal communication (continued) A. belzebul A. paniscus Callithrix jacchus Callithrix kuhlii Callithrix penicillata Cebus apella Lagothrix lagotricha Leontopithecus chrysomelas Mico emiliae Mico intermedius Saguinus fuscicollis

Saguinus mystax Saguinus niger Callimico goeldii Saguinus fuscicollis Saguinus labiatus Cebuella pygmaea Saguinus fuscicollis Saguinus mystax Callithrix flaviceps Cebuella pygmaea Saguinus fuscicollis Callimico goeldii Callithrix penicillata Microcebus murinus

Saguinus labiatus Saguinus midas

Reference

Consumer

3  Exudativory in Primates: Interspecific Patterns 67

Linacea

Icacinaceae Lacistemataceae Lauracea Lecythidaceae

Flacourtaceae Gnetaceae Hippocrateaceae

Table 3.3  (continued) Family and speciesa Consumer

Cebuella pygmaea Saguinus fuscicollis Plathymenia reticulata Callithrix penicillata Pterocarpus marsupium Semnopithecus entellus Sclerobium aureumb Callithrix penicillata Sclerolobium melinonii (=S. paniculatum) Callithrix penicillata Stryphnodendron pulcherrimumpod Saimiri sciureus Swartzia sp. Cebuella pygmaea Mico intermedius Unidentified sp. Leontopithecus chrysomelas Leontopithecus rosalia Semnopithecus entellus Unidentified sp. Cebuella pygmaea Gnetumsp. Cebuella pygmaea Cheiloclinium cognatum Cebuella pygmaea Cheiloclinium sp. Cebuella pygmaea Salacia elliptica Callithrix penicillata S. macrantha Saguinus fuscicollis Saguinus mystax Emmotum nitens Callithrix penicillata Lacistema sp. Mico intermedius Nectandra cf. nitidula Callithrix aurita Bertholletia excelsa Callimico goeldii Eschweilera sp. Saguinus fuscicollis Saguinus mystax Lecythis sp. Saguinus fuscicollis Hebepetalum sp. Saguinus fuscicollis Saguinus mystax

P. latifolium

Soini (1988) Soini (1987) Rizzini and Coimbra-Filho (1981) Newton (1984) Fonseca and Lacher (1984) Miranda and de Faria (2001) Stone (2007) Soini (1982) Rylands (1982) Rylands (1989) Peres (1986) Oppenheimer (1977) Soini (1982) Soini (1982) Ramirez et al. (1978) Soini (1982) Lacher et al. (1984) Present studyc Present studyc Miranda and de Faria (2001) Rylands (1982) Martins and Setz (2000) Porter et al. (2009) Peres (1993a) Peres (1993a) Soini (1987) Peres (1993a) Peres (1993a)

Reference

68 A.C. Smith

Myrtaceae Nyctaginaceae

Moraceae

Quivisianthe papinae Reinwardtiodendron humile Trichila guianensis T. claussenii Trichila sp. Unidentified spp. Artocarpus heterophyllus Ficus ingens Helicostylis tomentosa Pseudolmedia laevis Trophis sp. (T. occidentalis not recognised) Blepharocalyx salicifolius Bougainvillea spectabilis

Neobeguea mahafaliensis

Chisocheton macrophyllus Guarea macrophylla Guarea sp.

C. odorata

Callithrix penicillata Callithrix flaviceps

Semnopithecus entellus Callithrix penicillata Callithrix aurita Microcebus griseorufus Callimico goeldii Callithrix aurita Cebuella pygmaea Saguinus fuscicollis Saguinus imperator Nycticebus coucang Cebuella pygmaea Cebuella pygmaea Mico intermedius Phaner furcifer Microcebus griseorufus Phaner furcifer Nycticebus coucang Mico intermedius Callithrix aurita Cebuella pygmaea Microcebus murinus Callithrix jacchus Homo sapiens Saguinus fuscicollis Cebuella pygmaea Microcebus ravelobensis

Lythraceae Malphighiaceae Melastomataceae Meliaceae

Lagerstroemia parviflora Byrsonima ligustrifolia Miconia sp. Azadirachta indica (=Melia azaderach) Cedrela fissilis

Consumer

Family and speciesa

Miranda and de Faria (2001) Ferrari (1988); Ferrari et al. (1996)

Newton (1984) Lacher et al. (1984) Martins and Setz (2000) Génin, personal communication Porter et al. (2009) Martins and Setz (2000) Moynihan (1976); Yépez et al. (2005) Terborgh (1983) Terborgh (1983) Wiens et al. (2006) Yépez et al. (2005) Terborgh (1983) Rylands (1981, 1982) Schülke (2003) Génin, personal communication Schülke (2003) Wiens et al. (2006) Rylands (1982) Martins and Setz (2000) Ramirez et al. (1978) Génin (2003) Coimbra-Filho and Mittermeier (1977) Johns et al. (2000) Present studyc Yépez et al. (2005) Radespiel et al. (2006)

Reference

(continued)

3  Exudativory in Primates: Interspecific Patterns 69

Zanthoxylum sp.

Callithrix flaviceps Mico intermedius

Ripley (1970) Yépez et al. (2005) Yépez et al. (2005) Martins and Setz (2000) Passos and de Carvalho (1991) Rylands (1982) Radespiel et al. (2006) Yépez et al. (2005) Charles-Dominique and Petter (1980); Schülke (2003) Ferrari (1988); Ferrari et al. (1996) Rylands (1982) Semnopithecus entellus Cebuella pygmaea Cebuella pygmaea Callithrix aurita Leontopithecus chrysopygus Mico intermedius Microcebus ravelobensis Cebuella pygmaea Phaner furcifer

Rutaceae

Rubiaceae

Rhamnaceae Rosaceae

Smith (1997) Radespiel et al. (2006) Terborgh (1983) Carvalho and Carvalho (1989) Soini (1982) Yépez et al. (2005) Chapman et al. (2002) Wiens et al. (2006) Ferrari et al. (1996); Martins and Setz (2000) Ferrari (1988); Ferrari et al. (1996) Radespiel et al. (2006) Radespiel et al. (2006) Kinzey et al. (1975) Martins and Setz (2000) Lacher et al. (1984) Radespiel et al. (2006)

Reference

Consumer Saguinus fuscicollis Microcebus ravelobensis Cebuella pygmaea Leontopithecus chrysopygus Cebuella pygmaea Cebuella pygmaea Cercopithecus ascanius Nycticebus coucang Callithrix aurita Callithrix flaviceps Microcebus murinus Microcebus murinus Cebuella pygmaea Callithrix aurita Callithrix penicillata Microcebus murinus

Ochnaceae Passifloraceae Polygonaceae

Cespedesia spathulata Adenia firingalavensis Coccoloba sp. Ruprechtia laxiflora Unidentified sp. Colubrina arborescens Prunus africana P. polystachya P. sellowii Alseis sp. Canthium sp. (C. larorum not recognised) Gaertnera sp. Palicourea macrobotrys Psychotria sp. Richardia sp. Rothmannia sp. (R. reiniformis not recognised) Chloroxylon faho Citrus maxima C. medica Metrodorea stipularis Pilocarpus pauciflorus Spathelia excelsa Vepris arenicola Zanthoxylum riedelianum Z. tsihanimposa

Family and speciesa

Table 3.3  (continued)

70 A.C. Smith

Callithrix penicillata

Cucullaria tomentosa (=Vochysia)

Karomia macrocalyx Leonia cymosa

Cissus sicyoides Callisthene major

Styracaceae

Verbenaceae Violaceae

Vitaceae Vochysiaceae

S. apetala S. foetida S. stipulifera

S. urens Unidentified sp. Styrax ferrugineus

Sterculiaceae

Sphaerosepalaceae

Simaroubaceae

Rhopalocarpus sp. Sterculia africana S. aff. rugosa S. apeibophylla

Sapindaceae

Sapotaceae

Consumer Callithrix penicillata Callithrix aurita Saguinus fuscicollis Saguinus fuscicollis Saguinus fuscicollis Mico intermedius Callithrix penicillata Microcebus murinus Microcebus ravelobensis Microcebus murinus Papio cynocephalus Cebuella pygmaea Saguinus fuscicollis Saguinus labiatus Cebuella pygmaea Semnopithecus entellus Mico melanurus Mico intermedius Semnopithecus entellus Saimiri sciureus Callithrix penicillata Callithrix penicillatab Microcebus murinus Saguinus fuscicollis Saguinus mystax Saguinus fuscicollis Callithrix penicillata

Cupania sp. Paullinia carpopoda Pouteria sp. Undidentified sp. Picramnia sp. Simaba sp. Simarouba versicolor Rhopalocarpus similis

Family and speciesa

(continued)

Rylands (1984) Ferrari et al. (1996) Present studyc Smith (1997) Snowdon and Soini (1988); Terborgh (1983) Rylands (1982) Fonseca et al. (1980) Radespiel et al. (2006) Radespiel et al. (2006) Génin, personal communication Norton, personal communication Soini (1988) Porter (2001) Porter (2001) Yépez et al. (2005) Ripley (1970) Rylands (1984) Rylands (1982) Newton (1992) Izawa (1975) Miranda and de Faria (2001) Fonseca and Lacher (1984) Radespiel et al. (2006) Smith (1997) Smith (1997) Smith (1997) Rizzini and Coimbra-Filho (1981); Lacher et al. (1984) Lacher et al. (1984)

Reference 3  Exudativory in Primates: Interspecific Patterns 71

Norton et al. (1987)

Callithrix aurita Saguinus fuscicollis Saguinus fuscicollis Callithrix penicillata Saguinus fuscicollis Saguinus mystax Cebuella pygmaea Saguinus fuscicollis Saguinus mystax Callithrix aurita Saguinus bicolor Callithrix penicillata Callithrix penicillata Callithrix penicillata Callithrix penicillata Saguinus mystax Homo sapiens Papio cynocephalus

Qualea sp. Ruizterania trichanthera Vochysia diversa V. elliptica V. cf. guinensis

V. thyrsoidea

V.tucanorum Vochysia sp. Balanites aegyptiacus

V. magnifica V. obscura V. pyramidalis V. rufa

V.lomatophylla

Callithrix penicillata Callithrix penicillata

Q. multiflora Q. parviflora

Reference Soini (1982) Lacher et al. (1984) Fonseca and Lacher (1984); Miranda and de Faria (2001) Miranda and de Faria (2001) Rizzini and Coimbra-Filho (1981); Fonseca and Lacher (1984); Miranda and de Faria (2001) Ferrari et al. (1996) Smith (1997) Snowdon and Soini (1988) Miranda and de Faria (2001) Peres (1993a) Peres (1993a) Ramirez et al. (1978); Soini (1982) Garber (1993b) Ramirez (1989) Ferrari et al. (1996) Egler (1992) Lacher et al. (1984); Miranda and de Faria (2001) Rizzini and Coimbra-Filho (1981); Miranda and de Faria (2001) Fonseca and Lacher (1984); Miranda and de Faria (2001) Lacher et al. (1984) Ramirez (1989) Johns et al. (2000)

Consumer Cebuella pygmaea Callithrix penicillata Callithrix penicillata

Qualea amoena Q. dichotoma Q. grandiflora

a

Exudates produced at trunk or branches except: podproduced by seed pod: pod + trunkproduced by seed pods and trunk b Sampled only, exudate not fed upon Latex c Methods given in Smith (Chapter 5)

Zygophyllaceae

Family and speciesa

Table 3.3  (continued)

72 A.C. Smith

Hominidae

Cercopithecidae

Pitheciidae

Callitrichidae

Lorisidae Atelidae

Lemuridae

Allocebus (1) Microcebus (3) Mirza (1) Phaner (2) Daubentonia (1) Euoticus (1) Galago (2) Otolemur (1) Eulemur (1) Varecia (1) Nycticebus (1) Alouatta (2) Ateles (1) Lagothrix (2) Callimico (1) Callithrix (7) Cebuella (1) Leontopithecus (3) Mico (2) Saguinus (9) Cebus (1) Saimiri (1) Cacajao (1) Pithecia (2) Cercopithecus (2) Erythrocebus (2) Papio (1) Semnopithecus (1) Homo (1) Pan (1)

Genus (no. spp.a) 1 26 2 15 1 3 5 3 1 1 11 2 2 3 11 80 51 9 30 73 2 2 1 1 4 4 14 15 15 2

Speciesb

b

a

1 27 2 10 1 2 1 3 2 1 10 1 1 1 11 53 38 9 22 50 1 2 1 1 2 2 9 13 9 1

Genera

Total no. of exploited

Number of species within primate genus reported to consume exudates from known species Includes only those identified to a known species

Catarrhini

Platyrrhini

Cheirogaleidae

Strepsirrhini

Daubentoniidae Galagidae

Family

Clade 1 17 2 7 1 1 1 2 2 1 5 1 1 1 6 28 19 6 12 25 1 2 1 1 2 2 6 10 8 1

Families

Table 3.4  Numbers of plant species, genera and families exploited for exudates by 30 genera of primates

1 ± 0 1 ± 0 2 ± 0

3.3 ± 2.1 12.5 ± 9.5 9.1 ± 13.7

3.3 ± 2.1 15.5 ± 12.5 12.1 ± 19.2

1.0 ± 0 2.0 ± 1 4.0 ± 1

10.9 ± 10.5

1 ± 0

2 ± 1.0 13.6 ± 13.4

1 ± 0

1.0 ± 0

1 ± 0

6.0 ± 4.0

8.0 ± 7.0

2.5 ± 0.5

12.3 ± 6.3

10.3 ± 3.3

Genera

Mean no. of exploited Species

1 ± 0 1 ± 0 2 ± 0

3.0 ± 1.6

6.7 ± 6.1

1±0

1±0

1±0

4.5±2.5

9.0 ± 3.7

Families

3  Exudativory in Primates: Interspecific Patterns 73

0.04

0.20

0.36

0.52

0.68

0.84

Group B

Allocebus (1) Otolemur (2) Galago (1) Euoticus (1) Cebus (1) Callithrix kuhli grp (3) Nycticebus (5) Mico (12) Phaner (7) Leontopithecus (6) Callimico (6) Saguinus (26) Cebuella (22) Callithrix jaccus grp (23) Microcebus (17) Callithrix flaviceps grp (14)

Group C

Mirza (2)

Group A

A.C. Smith

Group D

74

1

Sorensen's Coefficient

Fig. 3.1  Cluster diagram showing the relationships between seventeen primate taxa based on the plant families they are known to exploit for exudates. Figures in brackets indicate number of families exploited by the genus.

Patterns of Gummivory Within the Primates Cluster analysis based on the plant families of exudates eaten by 17 primate genera implies the presence of four significant cluster groups, plus Nycticebus which does not group with any other genus (Fig. 3.1). The four principal clusters are (a) Mirza and Allocebus (SS: 0.667), (b) Otolemur, Galago, Euoticus and Cebus (SS: 0.475