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

<5

11.9 a 3.4 a

17.0 2.8 a,c

16.2 f 9 c 24

18.7 a 15.4 a

3 20.8 16.3 a,c

17.2

1.6 a

32.1a,c

Percentage of diet Total Plant Albernaz (1997) Passos (1999) Valladares-Padua (1993) Peres (1986) Dietz et al. (1997) Lopes and Ferrari (1994) Rylands (1982) Rylands (1984) Egler (1992) Smith, Chap. 5 Garber (1988a) Garber (1993b) Lopes and Ferrari (1994) Peres (1993a) Porter (2001) Soini (1987) Terborgh (1983) Garber (1984a) Terborgh (1983) Porter (2001) van Roosmalen (1985b) Smith, Chap. 5 Garber (1988a) Garber (1993b) Peres (1993a) Oliveira and Ferrari (2000) Izawa (1975) Savage, personal communication to Power and Oftedal (1996)

Reference

52 A.C. Smith

Hominidae

b

a

Cords (1986) Isbell (1998)

37.4

Erythrocebus patas

Solanki et al. (2008) Johns et al. (2000) Nishida and Uehara (1983); Sugiyama and Koman (1987); Yamakoshi (1998); Ushida et al. (2006)

? ? ?

Pan troglodytes

Trachypithecus pileatus

Homo sapiens

Newton (1992)

1

Semnopithecus entellus

Bentley-Condit (2009)

Altmann (1998)

Post (1982)

15

Papio cynocephalus 28.5 

Olson (1985) Rahaman and Parthasarathy (1969)

>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 < 1.000), (c) Mico, Phaner, Leontopithecus, and Callimico (SS: 0.395 < 0.615) and (d) Saguinus, Cebulla, the C. jacchus group, Microcebus and the C. flaviceps group (SS: 0.346 < 0.542).

Discussion Prevalence of Gummivory Within the wider context of primates in general, at least 69 species are known to eat exudates. As detailed dietary information becomes available for other species, particularly for many of the recently discovered Galagidae taxa (see Grubb et al. 2003)

3  Exudativory in Primates: Interspecific Patterns

75

and the more opportunistic of the cercopithecidae, this number is expected to increase. The relatively few records for many cathemeral or nocturnal strepsirrhines in comparison to the somewhat analogous callitrichids almost certainly represent the practicalities of night-time observations rather than a true dietary picture for these species. Caution is required when in interpreting what may be an observational bias towards callitrichids; gummivory is prevalent in this taxon, but it may be no less prevalent in other less reported or less easily observed taxa. The degree to which primate species consume exudates varies considerably. Interestingly, exudates may account for 10–75% of the diet of species typically not thought of as gum specialists. While marmosets, some galagos and the fork-marked lemur have been long known to be highly gummivorous (see Nash 1986), with the exception of tamarins (Garber 1984; Heymann and Smith 1999; Smith 2000), patas monkeys (Isbell 1998), and mouse lemurs (Génin 2003) there has been less attention given to species that lack dental adaptations for gummivory but which may still consume considerable amounts of exudates. The importance of exudates in the diet of these primates may vary with life stage, for yearling yellow baboons gums may supply more energy than any other dietary category with the exception of maternal milk (assuming high fibre and sugar digestibility) (Altmann 1998). Seasonal changes in diet mean that the contribution of exudates can be even higher at certain times of the year.

Seasonality of Consumption For all but one species for which seasonal fluctuations were reported gum consumption was highest in the dry season, with gums acting as a fall back food during periods of low food availability. This pattern is relatively widespread, including several galagos and black lemurs (Eulemur macaco) in addition to numerous representatives from the majority of platyrrhine families. It may be explained by the digestive challenges posed by gums (see Power, Chapter 2) limiting their consumption at other times, when alternative more profitable foods are available. An exception to this may be the pod gums of Neotropical Parkia spp. which are produced during the dry season and function as a nutritional reward for seed dispersers (Hopkins 1983; Peres 2000). Their prevalence at this time of fruit scarcity may mark them out as a keystone resource for many New World primates, and may be the reason why more primates consume them than gums from any other genus (Table 3.5).

Pod Gums The importance of Parkia seed pod exudates as a keystone resource for a wide variety of species, not just primates, has been highlighted by Peres (2000) and by Garber and Porter (Chapter 4). The seed pods of other species, such as

76

A.C. Smith Table  3.5  Top five species, genera and families as ranked by the number of species (nc) known to consume their exudates Species nc Genus nc Family nc Parkia pendula Parkia nitida Tapirira guianensis Acacia xanthophloea Spondias mombin Acacia paniculata

15 12 9 6 6 5

Parkia Acacia Terminalia Inga Tapirira

25 17 13 11 10

Fabaceae Anacardiaceae Combretaceae Meliaceae Euphorbiaceae

48 23 16 10 6

Stryphnodendron pulcherrimum and Piptadenia spp. (Fabaceae) also produce exudates that are eaten by primates, with those of S. pulcherrimum acting as a similar dry season resource for squirrel monkeys (Saimiri sciureus) (Pook and Pook 1981; Stone 2007). Eleven platyrrhine genera are known to consume pod gums: Alouatta (two spp.), Ateles (one sp.), Cacajao (one sp.), Callimico, Callithrix (four spp.), Lagothrix (one sp.), Leontopithecus (one sp.), Mico (one sp.), Pithecia (two spp.), Saguinus (four spp.) and Saimiri (one sp.) (see Table 3.2), and for some such as black-handed tamarins (Saguinus midas niger), buffy sakis (Pithecia albicans) and golden-headed lion tamarins (Leontopithecus chrysomelas) they are the only exudates consumed (Oliveira and Ferrari 2000). Pod gums may by their nature be more seasonal than those produced by trunks and branches as a result of damage, though these too may exhibit a degree of seasonality linked to changes in climatic factors such as wind and humidity. The majority of studies linking an increase in gum consumption in the dry season to a reduction in fruit availability do not differentiate between the two types of gum. Therefore, it is not possible to determine if such increases are due to pod gums or whether feeding on trunk gum also increases significantly during this period. Differentiating between them is important because their different functions predict differences in biochemistry directly relevant to consumers such as primates. While it may be expected that endozoochorous pod gums would be richer in more easily digestible sugars, at least for Parkia pendula pod gum arabinose is the principal post-hydrolysis sugar (Anderson and de Pinto 1985). What is surprising is the natural form is l-arabinose which animals are unable to digest, and when included in the diet in small quantities significantly reduces sucrose digestion in the small intestine (Hizukuri 1999), yet gum from P. pendula pods is eaten by more species of primate than any other source of exudates. The indigestibility of l-­arabinose may explain its avoidance by pygmy marmosets, relative to galactose, in captive trials (Glaser 1978). Galactose is a principal sugar in P. bicolor and P. biglobosa trunk gums (Anderson and de Pinto 1985). While pygmy marmosets have not been recorded to eat gum from P. pendula pods there are no reports of them avoiding it either; it may be that this species does not grow at the sites where they have been studied. Its consumption by at least 15 other Amazonian primates is intruiging and may be explained if it is the only significant resource available at certain times of the year. Its role in the diet of these species and its effects on their digestion warrant further study.

3  Exudativory in Primates: Interspecific Patterns

77

Species Consumed The diversity of the exudates eaten is a reflection of their biogeography and phylogeny and that of the primates consuming them. The great majority are known to be eaten by just one or two primates (Table 3.3). The genera that were reported for the greatest number of primates, Parkia, Acacia, and Inga, stand out because they contain a relatively high number of species each contributing its own consumers to the overall total for the genus. With these genera contributing 7, 15, and 13 species of exudates, respectively, it is not surprising that the large and globally distributed family to which they belong, Fabaceae, was the most frequently reported. The particularly high number of exudate species exploited by saddleback tamarins may be explained by their dietary opportunism and a relatively large number of year-long studies of well-habituated groups at several field sites (e.g. Terborgh 1983; Norconk 1986; Soini 1987; Ramirez 1989; Peres 1993a; Knogge 1998; Heymann and Smith 1999). It is expected that the number of species reported for other primates in similar habitats will increase as detailed dietary information becomes available. Species which possess adaptations to gnaw and stimulate gum flow may be expected to concentrate their efforts on a few productive species, while opportunists may take exudates from a wider range of species. Although this may explain the relatively low number of species exploited by several galagos it does not explain why other specialists, such as common marmosets, which consume similarly large amounts of exudates, do so from many sources.

Degrees of Gummivory Within the Callitrichidae Among the anthropoid primates, the Callitrichidae contains a range of superficially similar species with marked differences in their degree of gummivory (Ferrari 1993). Cebuella and Callithrix possess dental adaptations for gouging, whereas Saguinus, Leontipithecus and Callimico do not. Mico, a group of Amazonian marmosets previously classified in Callithrix, have dentition somewhat intermediate between Callithrix and Saguinus (Hershkovitz 1977; Maier et al. 1982). These differences in dentition would predict Cebuella and Callithrix to be the most gummivorous, followed by Mico, then Saguinus, Leontipithecus, and Callimico. In addition, on the basis of both distribution and dental adaptations for gouging Rylands and Faria (1993) suggest Callithix and Mico may be split into four groups, C. jacchus and C. penicillata, C. kuhli and C. geoffroyi, C. aurita and C. flaviceps, M. humeralifer and M. argentata, in decreasing levels of gummivory. From Table 3.1, it can be seen that while gum has been reported to account for 100% of the plant-related diet of Cebuella, when time spent gouging is accounted for it may represent less than 67% of the total diet (Ramirez et al. 1978). In contrast, gum comprises more than 70% of the diet of C. flaviceps (Ferrari and Rylands 1994; Guimarães 1998; Corrêa et al. 2000), C. aurita (Ferrari and Digby 1996; Martins and Setz 2000),

78

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C. jacchus (Ferrari and Digby 1996) and C. penicillata (Fonseca and Lacher 1984). With diets containing 28–67% gum C. geoffroyi (Passamani 1998) and C. kuhli (Rylands 1989; Ferrari and Rylands 1994; Raboy et al. 2008) are the least gummivorous members of their genus. The recently reclassified Mico marmosets, represented by M.  intermedius, consume about 15% gum (Rylands 1982), a figure more similar to Saguinus. This may be explained by a lack of gouging by both M. intermedius (Rylands 1984) and Saguinus. An equivalent degree of gummivory and lack of gnawing may also explain why Mico is also more similar to Saguinus than Callithrix in terms of sensitivity and response to fructose and quinine taste characteristics (Simmen 1994). Leontopithecus is again less gummivorous, with two species consuming less than 2% (L. caissara, Prado 1999; L. rosalia, Peres 1986; Dietz et al. 1997), a figure akin to that of Callimico. These findings are broadly supportive of Rylands and Faria’s (1993) marmoset groupings with the exception that C. flaviceps and C. aurita show little basis for separation from the C. jacchus group in terms of degree of gummivory. This is surprising given the lower degree of dental specialisation in C. aurita and C. flaviceps (Natori 1986), and reports that C. aurita is unable to stimulate exudate flow by gouging (Muskin 1984; Martins and Setz 2000). The limited data also hint at significant intrageneric differences within both the tamarins and lion tamarins. While as a group lion tamarins are the least gummivorous of the callitrichids, black lion tamarins consume at least three times as much gum as their congeners (Kierulff et al. 2002). Gum may account for up to 55% of their diet in the dry season (Passos and de Carvalho 1991). This difference has been explained by the more pronounced seasonality of the semi-deciduous forests inhabited by black lion tamarins (Rylands 1993; Raboy and Dietz 2004). A similar explanation cannot explain the pattern within tamarins, where S. bicolor, S. niger, and S. oedipus consume significantly less exudates than their congeners. In fact the seasonal nature of the semi-deciduous forests in northern South America occupied by S. oedipus in comparison to the wetter forests of western Amazonia more typical of the genus would predict a higher rather than lower degree of gummivory, as is the case for the adjacent S. geoffroyi. The grouping of S. bicolor, S. niger, and S.  oedipus is, however, consistent with that proposed by Natori and Hanihara (1992) based on dental anatomy.

Patterns of Gummivory Within the Primates The groupings of primate genera suggested by cluster analysis of the plant families they exploit for exudates may be explained by the number of families each genus exploits. Genera within Group A (Mirza and Allocebus) and Group B (Otolemur, Galago, Euoticus, Cebus, and Callithrix kuhli group) exploited exudates from three or fewer plant families, those in Group C (Mico, Phaner, Leontopithecus, and Callimico) between 6 and 12 plant families, and those in Group D (Saguinus, Cebuella, Microcebus and the C. jacchus and C. flaviceps groups) between 14 and

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26 plant families. Nycticebus, consuming gums from five families, is intermediate between Groups B and C. While some primates do consume more gum than others this analysis is almost certainly biased by the degree to which the species have been observed. The genera eating exudates from the widest range of plant families have all been subject to at least several year-long studies while those in Groups A and B have typically received less attention, and this may well explain the more restricted range of plant families they’ve been observed to exploit. In contrast, the relatively few families reported for Otolemur, Galago, and Euoticus may truly represent exploitation of a narrower niche, concentrating on the relatively abundant gums of Acacia spp. within scrub forests. The high number of families exploited by Cebuella and two of the three Callithrix groupings may reflect their ability to gnaw and stimulate gum flow. However, unlike Saguinus and Microcebus which are reliant on naturally produced gums and may thus be expected to take them from a wide range of trees when they are encountered, specialists such as Cebuella and two of the three Callithrix groupings could concentrate their feeding on just a few species yet they actively harvest gum from a wide range of taxa. This may be indicative of their adaptability or an underlying physiological need to spread their gum feeding over a range of species.

Conclusion In attempting to identify and understand patterns of gummivory, this chapter has drawn on and analysed feeding records from a wide range of studies. Data were collected from many primate species which differed in their observability, at different sites, during different years, and over differing lengths of time. All of these factors may confound the results, and as such they should be interpreted with a degree of caution. Our knowledge of gummivory for many primates is almost ­certainly far from complete, both in terms of the species and amounts of gum they consume. However, for some taxa, such as Callitrichidae, there are sufficient yearlong field studies that we can examine differences in the relative degrees of gummivory between species or genera within these taxa with some confidence. To do this thoroughly across the primates requires more complete and accessible dietary datasets than are currently available. What is certain at present is that within primates gummivory is widespread, occurring in all major taxa and that this often overlooked resource contributes significantly to the diets of species not traditionally thought of as specialist gummivores. Acknowledgments  I thank Dr Anne Burrows for inviting me to participate in the symposium on the evolution of exudativory in primates at the XXIIth Congress of the International Primatological Society. This chapter benefited from Anne’s comments and those of Leanne Nash and two anonymous reviewers. Dr Philip Pugh conducted the cluster analysis and provided comments on an early draft of this manuscript. Financial support was provided by Anglia Ruskin University’s Animal and Environmental Research Group and Central Sabbatical Scheme.

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Starin ED (1978) A preliminary investigation of home range use in the Gir Forest langur. Primates 19: 551–567 Stevens JR, Hallinan EV, Hauser MD (2005) The ecology and evolution of patience in two New World monkeys. Biol Lett 1: 223–226 Stevenson MF, Rylands AD (1988) The marmosets, genus Callithrix. In Mittermeier RA, Rylands AB, Coimbra-Filho AF, Fonseca GAB (eds) Ecology and behaviour of neotropical primates World Wildlife Fund, Washington, DC Stone AI (2007) Responses of squirrel monkeys to seasonal changes in food availability in an eastern amazonian forest. Am J Primatol 69: 142–157 Sugiyama Y, Koman J (1987) A preliminary list of chimpanzees alimentation at Bossou, Guinea. Primates 28: 391–400 Sugiyama Y, Koman J (1992) The floara of Bossou: its utilization by chimpanzees and humans. Afr Study Monogr 13: 127–169. Sussman RW (1974) Ecological distinctions in sympatric species of Lemur. Ecology and feeding behaviour of five sympatric lorisids in Gabon. In Martin RD, Doyle GA, Walker AC (eds) Prosimian biology Duckworth, London Sussman RW, Kinzey WG (1984) The ecological role of the Callitrichidae: a review. Am J Phys Anthropol 64: 419–449 Swedell L, Hailemeskal G, Schreier A (2008) Composition and seasonality of diet in wild hamadryas baboons: preliminary finding from Filoha. Folia Primatol 79: 476–490 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, Vinyard J (2004) Comparative analysis of masseter fibre architecture in tree-gouging (Callithrix jacchus) and nongouging (Saguinus oedipus) Callitrichids. J Morph 261: 276–285 Terborgh J, Janson CH (1983) The ecology of primates in southeastern Peru. Nat Geogr Soc Res Rep 15: 655–662. Torres de Assumpção C (1983) An ecological study of primates in south-eastern Brazil, with a reappraisal of Cebus apella races. Unpublished PhD thesis, University of Edinburgh, Edinburgh 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 Valladares-Padua C (1993) The ecology, behavior and conservation of the black lion tamarins (Leontopithecus chrysopygus, Mikan 1823). PhD dissertation, University of Florida, Gainesville van Roosmalen MGM (1985a) Habitat preferences, diet, feeding strategy and social organisation of the black spider monkey (Ateles paniscus paniscus Linnaeus 1758) in Suriname. Sup Acta Amazon 15(3/4, suppl): 1–238 van Roosmalen MGM (1985b) Fruits of the Guianan flora. Institute of Systematic Botany, Utrecht University, Utrecht Vermes E, Weidholz A (1930) Zur vergleichenden Anatomie des Magen-Darmkanals der Primaten im Hinblick auf die Ernährungsfrage. Zool Gart 3: 28–34 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 Whitten PL (1983) Diet and dominance among female vervet monkeys (Cercopithecus aethiops). Am J Primatol 5: 139–159 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 Wrangham RW, Waterman PG (1981) Feeding behaviour of vervet monkeys on Acacia tortilis and Acacia xanthophloea: with special reference to reproductive strategies and tannin production. J Anim Ecol 50: 715–731 Yamakoshi G (1998) Dietary responses to fruit scarcity of wild chimpanzees at Bossou, Guinea: possible implications for ecological importance of tool use. Am J Phys Anthropol 106: 283–295 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 4

The Ecology of Exudate Production and Exudate Feeding in Saguinus and Callimico Paul A. Garber and Leila M. Porter

Abstract  Callitrichines are small-bodied New World primates characterized by anatomical, behavioral, and/or physiological adaptations that enable individuals to exploit plant exudates. However, little is known concerning rates of exudate production and availability of exudates to primate consumers. In this investigation, we present data on patterns of exudate feeding in a mixed species troop of tamarins (Saguinus mystax and S. fuscicollis) in northeastern Peru, and a group of callimicos (Callimico goeldii) in northwestern Bolivia. In addition, we collected data on the amount and renewal rate of exudates produced from naturally occurring and experimentally induced wounds to tree species exploited by Saguinus and Callimico. Our results indicate that exudates are available to nongouging primate foragers during most or all months of the year. In Saguinus, exudates from tree trunks, Parkia pods, and holes gouged by pygmy marmosets (Cebuella pygmaea) accounted for 16.3% of total plant feeding and foraging time. In the case of Callimico, stilt root exudates, Parkia pod exudates, and trunk exudates accounted for 35% of plant feeding time. Daily exudate production on individual trees in Bolivia (n = 17) varied from 0 to 10.75 g/day. Total monthly trunk exudate production in naturally occurring wounds present on sample trees in Peru (n = 5) ranged from 0 to 369 g. Pod exudates were available principally during the dry season, whereas trunk exudates were available during all months of the year. We argue that exudates represent a reliable and renewable resource for nongouging callitrichines, and that tamarins and callimicos effectively track the location, availability, and productivity of trunk, stilt root, and pod exudate sources in their home range.

P.A. Garber (*) Department of Anthropology, University of Illinois, 109 Davenport Hall, 607 S Mathews Ave, Urbana, IL 61801, 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_4, © Springer Science+Business Media, LLC 2010

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Introduction Theories of primate socioecology and ecological constraints have proposed that the distribution, availability, and productivity of feeding sites have a critical affect on diet, within-group feeding competition, social dominance, group size, day range, and patterns of habitat utilization (Wrangham et  al. 1993; Chapman et  al. 1995; Chapman and Chapman 2000). In many tropical forests, resources exploited by primates vary considerably in spatiotemporal predictability. For example, resources may be clumped and found in large patches across much of the landscape, or they may be distributed in small, scattered patches that are restricted to particular microhabitats (Chapman and Chapman 2000; Johnson et al. 2002; Tuomisto et al. 2003). In some cases, all or most trees of a given species may produce fruits and/or flowers during the same limited period of the year, a phenological pattern described as synchronous (Chapman et al. 2005). In other species, trees may exhibit an asynchronous production pattern, with individual trees of that species producing flowers and/or fruits across several different months of the year. In order to increase foraging efficiency, primates are expected to track and integrate phenological information concerning the spatial location of nearby and distant feeding sites with information on the quantity and quality of food in these patches, and the rates at which patches are renewed (Garber 2000). This information may allow individuals to adopt a search strategy in which food patches are revisited at a rate which offers high net energy gain (Garber 2000; Lambert 2007). Plant exudates represent an important year-round or seasonal component of the diet for a range of primates including all genera of tamarins and marmosets (Soini 1988; Stevenson and Rylands 1988; Rylands and de Faria 1993; Garber 1993a; Dietz et al. 1997; Kátia et al. 2000; Peres 2000; Miller and Dietz 2006; Digby et al. 2007; Raboy et al. 2008), several genera of African and Asian lorisoids (Euoticus, Galago, Otolemur, Perodicticus, Loris, and Nycticebus; Charles-Dominique 1977; Bearder and Martin 1980; Nash and Whitten 1989; Nekaris and Rasmussen 2003; Nekaris and Bearder 2007), Malagasy lemurs (Mirza, Microcebus, and Phaner; Radespiel et al. 2006; Gould and Sauther 2007; Joly and Zimmermann 2007), cercopithecines (Papio, Erythrocebus, Allenopithecus, and Cercopithecus; Wrangham and Waterman 1981; Isbell 1998; Enstam and Isbell 2007), cebines (Saimiri and Cebus; Peres 2000; Stone 2007), atelines (Lagothrix, Ateles, and Alouatta; Peres 2000), pithecines (Cacajao; Peres 2000), and chimpanzees (Ushida et al. 2006). Exudates exploited by nonhuman primates are produced principally from wounds present on tree trunks and branches, the stilt roots of certain species of palms, and inside the leguminous pods of trees of the genus Parkia (Ramirez et al. 1977; Garber 1993b; Peres 2000; Porter et al. 2009). Exudates present a series of foraging challenges to primate consumers, and indivi­dual taxa have evolved behavioral, anatomical, and physiological adaptations that aid in procurement and digestion. For example, the fork-crowned lemur (Phaner ­furcifer), the needle-clawed galago (Euoticus elegantulus), and all species of tamarins and marmosets are characterized by keeled or claw-like nails that

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enable ­individuals to cling to large vertical supports while consuming exudates (Charles-Dominique 1977, Garber 1980). Similarly, marmosets of the genera Callithrix possess anatomical adaptations of their lower incisors (absence of lingual enamel and thickening of buccal enamel) and jaws that serve to increase gape width and result in the production of a more vertically oriented bite force (Rosenberger 1978; Vinyard et  al. 2003; Taylor and Vinyard 2004) that enable them to gouge holes in tree bark to stimulate the flow of exudates. Finally, exudates contain difficult to digest beta-linked polysaccharides (Anninson et al. 1994; Power 1996; Power and Oftedal 1996). In this regard, common marmosets and pygmy marmosets have evolved elongated and complex hindguts (Cebuella also is characterized by long gut transit time relative to body mass) (Coimbra-Filho and Mittermeier 1977; Coimbra-Filho et  al. 1980; Ferrari et  al. 1993; Caton et  al. 1996; Power 1996; McWhorter and Karasov 2007), which serve to increase opportunities for fermentation and more efficient digestion of exudates. Although these feeding adaptations are well documented, little is known concerning the productivity or spatial and temporal availability of exudate sites, or of the behavioral tactics used by foragers to encounter and effectively exploit this resource. In this study, we present data on exudate feeding, rates of resource renewal, and the spatial and temporal patterns of exudate exploitation in a mixed species troop of mustached and saddle-back tamarins (Saguinus mystax and S. fuscicollis) in northeastern Peru and in a group of callimicos (Callimico goeldii) in northern Bolivia. Unlike marmosets (Callithrix, Cebuella, Callibella, and Mico; Soini 1988; Stevenson and Rylands 1988; Digby et al. 2007), tamarins (Saguinus), lion tamarins (Leontopithecus), and callimicos (Callimico) lack the necessary morphological adaptations of their jaws and teeth needed to gouge holes in trunks and branches to stimulate the flow of exudates (we follow Groves 2001 in placing callitrichines within the family Cebidae, the subfamily Callitrichinae, and in recognizing seven extant genera). In this regard, nongouging callitrichines face a different set of foraging challenges in exploiting exudates than do marmosets. Nongouging callitrichines may be more dependent on integrating spatial information concerning the location of a diverse set of exudate sites, with quantity information on patterns and rates of resource renewal to effectively regulate return times to productive sites and increase their food rewards. A primary goal of this research is to describe exudate feeding patterns in tamarins and callimicos and examine the degree to which exudates exploited by these primates represent renewable, predictable, and productive ­feeding sites. We addressed the following questions: 1. What are the patterns of exudate production at feeding sites exploited by tamarins and callimicos? 2. What is the quantity of exudate produced by a single exudate hole or tree over the course of a day, consecutive days, weeks, and months? 3. Are there differences in the amount of exudates produced at natural vs. experimentally induced sites? 4. How often do tamarins and callimicos revisit the same exudate trees over the course of a single day, and over the course of consecutive days?

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Methods Behavioral Data Data on the feeding behavior of a marked and habituated mixed species troop of mustached and saddle-back tamarins were collected from June through December 1984 at the Rio Blanco field site in northeastern Peru (4°05′S, 72°10′ W: for details on the study site see Garber 1993b). In this area of the Amazon, a group of saddleback tamarins and a group of mustached tamarins form a single large, cohesive troop in which individuals of both species feed, forage, travel, and rest together throughout the entire year. Troop membership changed during the course of the study due to births and migrations: the mixed species troop at its minimum contained 15 individuals and at its maximum contained 20 individuals. Over 90% of the individual feeding trees visited by mustached tamarins in our study troop also were visited by saddle-back tamarins of our study troop (Garber unpublished data). In addition, individuals of each species were located within 20 m of each other during at least 72% of the day (Garber 1988a). Given the spatial and temporal cohesiveness of our tamarin mixed species troop, in our analysis of diet we combine data for both tamarin species into a single tamarin data set. Behavioral data were collected on members of our tamarin study troop using a 2-min instantaneous focal animal technique (Martin and Bateson 1993). Feeding was defined as handling or consuming a food item. Food items were categorized as insect, fruit, nectar, legume (the tamarins consumed the arilate coat of legume seeds), trunk exudates, and legume pod exudates. Foraging was defined as localized movement within a potential feeding site and was associated with the search for and pursuit of animal prey or plant resources. Bout length was scored as the total number of 2-min point samples recorded for the focal animal while feeding and/or foraging in a food patch. Thus, we assumed that a tamarin feeding or foraging on fruits, nectar, exudates, or insects during a single interval devoted the entire 2 min of that interval to exploiting that resource. Focal troop members were followed continuously from the time they left their sleeping tree in the morning until the time they entered their sleeping tree in the afternoon. Thus our unit of study was a complete tamarin day and we present data based on 77 full days follows (approximately 800 observation hours). Data on diet and feeding behavior in callimicos are based on a year-long study (November 2002 to September 2003) conducted in northern Bolivia at Camp Callimico (11°23′S, 69°06″W; for details on the study site see Porter 2001). Total rainfall for the study period, September 2002 to August 2003 was 2,001 mm. We consider the wet season to last from November to April, and the dry season from May to October (Porter 2001). The study group was habituated prior to data collection, and was composed of one adult female, two adult males, and one female born in August 2002 (see Porter and Garber 2009). We collected complete day follows on focal individuals using point samples (Martin and Bateson 1993) at 5-min intervals from the time the animal left its sleeping site in the morning until it retired to

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its sleeping site at night on 108 observation days. On 22 additional days observation times were shorter due to loss of the group, torrential rain, or other factors. No data were collected during the month of February 2003. Additional observations of this same group were collected during 14 complete days in the dry season month of July 2005. As in the tamarin study, feeding included instances when an animal was consuming a food item, or had the food item in its hand, and foraging included instances when an animal was actively searching or examining a substrate for food. Unlike in the Rio Blanco study, however, foraging in the callimico study did not include instances when an animal was moving within a food patch. In addition, we did not calculate feeding or foraging bout lengths in this study. Rather, consecutive feeding records on the same species in the same location were scored as a single feeding bout. Food items were scored as fungus, nectar, fruit, trunk exudates, stilt root exudates, pod exudates, arthropods, and vertebrates. We acknowledge that differences in the time intervals between point samples (2 min vs. 5 min), and foraging definitions used at these two study sites could affect the results presented for tamarins and callimicos. In particular, it is possible that exudate feeding bouts lasting less than 2  min might be underrepresented in the ­callimico data relative to the tamarin data. However, our goal is not to directly compare exudate feeding and foraging in these two primate genera. Rather, we use behavioral observations of nongouging callitrichines to gain insights into patterns of exudate production, exudate availability, and exudate foraging strategies.

Exudate Production Data on exudate production were collected from tree species exploited by tamarins, pygmy marmosets, and callimicos in Peru and Bolivia. Particular trees were selected for monitoring based on the facts that (1) we had observed them to be exploited for exudates in previous years, (2) they contained active sites of exudate production, and (3) they were located within the home range of our study groups. We acknowledge that exudate production in individual trees is likely to vary considerably and that our study was not designed to identify the specific set of factors that contribute to this variation. Rather, our study was intended to be a first step in evaluating patterns of exudate production in trees exploited by nongouging callitrichines. Daily and monthly exudate production were monitored by collecting, removing, and weighing (g) the total amount of exudates present in naturally occurring holes and experimentally induced exudate sites. We also noted exudate color and consistency. Naturally occurring sites included areas of the trunk gouged by pygmy marmosets and areas damaged by insect parasites, weathering, and other injuries. Experimental sites were made using a machete either to gouge a circular hole of 1–3 cm in diameter into a trunk, generally at a depth of 0.5–2.5 cm, or to incise an angled cut of similar depth into a tree trunk or above ground tree root. Once made, experimental sites were not recut or reincised during the study.

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In order to document daily patterns of exudate production, we monitored from 1 to 15 exudate sites present on each of 17 trees of 7 different plant species: in total we monitored 9 natural exudate sites and 105 experimentally induced exudate sites. These sites were monitored for a period of up to 13 consecutive days at Camp Callimico in northern Bolivia. In addition, we also monitored monthly exudate production for a period of up to 11 consecutive months (samples were collected twice per week) from five naturally occurring sites on each of five exudate-producing trees (three tree species) exploited by tamarins in northeastern Peru (for details on the methods used at the Rio Blanco Field see Garber 1993b).

Results Exudate Feeding in Saguinus: General Results Behavioral data collected over the course of 7 months in northeastern Peru indicate that, based on total feeding and foraging time, the tamarin diet was composed ­principally of arthropods (S. mystax 40.4% and S. fuscicollis 47.7%), ripe fruits (S. mystax 42.3% and S. fuscicollis 35.1%), nectar (S. mystax 5.6% and S. fuscicollis 5.0%), legumes (S. mystax 1.8% and S. fuscicollis 1.5%), and plant exudates (S. mystax 9.7% and S. fuscicollis 10.5%). Tamarins in our mixed species study troop were observed to consume exudates during all months of the study (Table 4.1). These exudates were produced either on tree trunks (the result of naturally occurring injuries to the trunk or gouging by pygmy marmosets) or from the endosperm of seeds housed in the large leathery pods of Parkia nitida trees. Overall, trunk exudates (8.7%) and pod exudates (7.6%) accounted for 16.3% of tamarin plant feeding and foraging time (Table  4.2). Trunk exudates were consumed from 40 individual trees. Thirty-one of these trees were represented by three plant species: Inga sp. (family Leguminosae: Mimosoideae), Vochysia lomatophylla (family Vochysiaceae), and Parkia nitida (family Leguminosae: Mimosoideae). During the months of November and December, trunk exudates accounted for 12 and 11% of total tamarin plant feeding and foraging time, respectively (Table  4.1). When exploiting trunk exudates, the tamarins adopted an upright clinging posture Table 4.1  The percentage of exudates consumed by mixed species troops of mustached and saddle-back tamarins by study month (n = 181)

Month June July August September October November December

Trunk exudate (%) 5.0 3.9 10.3 7.5 8.5 12.3 11.4

Pod exudate (%) 35.2 4.5 3.8 6.5 0.0 0.0 0.0

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Table  4.2  Plant-based dietary profile of a mixed species troop of ­ ustached tamarins and saddle-back tamarins (June to December, m N = 3,810 individual activity records)a Food type

Feeding and foraging time (%)

Mean bout length (min)

Fruit Nectar Trunk exudate Pod exudate Legume

71.1 (N = 719)   9.8 (N = 68)   8.7 (N = 130)   7.6 (N = 51)   2.7 (N = 30)

6.60 ± 4.8 9.65 ± 4.7 4.46 ± 3.5 9.96 ± 5.9 6.07 ± 4.1

N = number of feeding 2 min feeding records for each food type a Based on total plant feeding and foraging time. Exploitation of insect and vertebrate prey are not included

by embedding their claw-like nails into the substrate. Generally, only one or two group members fed at a time. In most cases, the exudates were obtained directly by the mouth and licked or chewed. In other instances, trunk exudates characterized by a more jelly-like consistency (e.g. Parkia nitida and Vochysia lomatophylla) were grabbed by one hand and transferred to the mouth. Although quantitative data on scent-marking were not collected, only adult females were observed to scent-mark exudate sites (Garber 1993a). Tamarins in our mixed species troop also consumed exudates produced inside the pods of 11 Parkia nitida trees. Parkia trees are large emergent trees, and the pods are located in the uppermost part of the tree crown. These pods were a major resource for Saguinus during the dry season months of June through early September. During the month of June, Parkia pod exudates accounted for 35.2% of total tamarin plant feeding and foraging time (Table  4.1). The tamarins obtained access to Parkia pods by adopting a suspensory posture (hanging vertically down while maintaining a grasp with both feet in the upper canopy). The pods were held in the tamarins’ hands, cut into using their anterior dentition, pulled opened manually, and the liquid exudates licked and consumed.

Exudate Feeding in Callimico: General Results During the year-long field study in 2002–2003, the diet of our callimico study group consisted of arthropods (14%), fungi (42%), ripe fruits (27%), and plant exudates (15%). Based on total plant feeding time, exudates represented 35% of the plant component of callimico’s diet. Callimicos were observed to exploit pod ­exudates from two trees of Parkia velutina, and trunk exudates from seven different tree ­species: Inga chartacea (family Leguminosae: Mimosoideae), Euterpe ­precatoria, Socratea ­exorrhiza and Iriartea deltoidea (family Arecaceae), Bertholletia excelsa (family Lecythidaceae), Cedrela fissilis (family Meliaceae), Acacia martiusiana­ (family Leguminosae: Mimosoideae), and an unidentified liana. As in Saguinus, pod exudates were consumed principally in the dry season, and accounted for

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Table 4.3  Plant-based dietary profile of a group of callimicos, indicated as a percentage of plant feeding timea Month % Fruits % Pod exudates % Trunk exudates % Root exudates November 2002  0  0 0 100 (N = 9) December 100 (N = 20)   0  0 0 January 2003 100 (N = 21)   0  0 0 March   98 (N = 50)   2 (N = 1)  0 0 April   89 (N = 59)   8 (N = 5)   2 (N = 1) 2 (N = 1) May   62 (N = 44) 37 (N = 26)   1 (N = 1) 0 June   29 (N = 7) 63 (N = 15)   8 (N = 2) 0 July   22 (N = 11) 74 (N = 37)   4 (N = 2) 0 August   14 (N = 5) 86 (N = 32)  0 0 Annual total 2002–2003   65 33  2 0 July 2005   52 (N = 24)   0 41 (N = 19) 7 (N = 3) a Based on total plant feeding and foraging time. Exploitation of insect and vertebrate prey is not included

37–86% of callimico’s total plant feeding time during the months of May through August (Table 4.3). In July 2005, the same callimico group was not observed to consume Parkia pod exudates. Rather during this dry season month, trunk exudates from Inga chartacea, Cedrela fissilis, and Schefflera morotoni, and stilt root exudates from trees of three arborescent palm species (Iriartea deltoidea, Socratea exorrhiza, and Euterpe precatoria) accounted for 48% of total plant feeding observations. These palms were found at high density in disturbed areas of the forest such as tree fall gaps and stream margins. In the case of Schefflera morotoni, our callimico study group parasitized active holes gouged into the trunk by a sympatric group of pygmy marmosets. The callimicos consumed trunk exudates by clinging vertically to large trunks, or leaning from a small substrate onto a large trunk, and licking the exudates directly from the bark (Fig. 4.1). Although root exudates were located close to the ground, callimico generally avoided eating from the ground, and instead clung to the root or a neighboring root and then licked off the exudates. Callimicos, unlike tamarins, only ate exudates from Parkia pods that had fallen off the parent tree and into the understory or onto the ground. Pods found on the ground were generally carried up into a small tree for consumption. Callimicos grabbed pods in both hands to lick off the exudates from the sides of the pod, or ripped the pod open with their teeth to eat the exudates within the pod.

Exudate Production: Daily Exudate Flow In order to determine the quantity and pattern of exudate production, we first present data on daily food production in 105 experimentally induced trunk exudate sites and 9 naturally occurring trunk exudate sites from a total of 17 trees at Camp Callimico in Bolivia. During the course of this investigation we never observed tamarins, ­callimicos, pygmy marmosets, or any other diurnal animal visit our sample trees

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Fig. 4.1  Callimico consuming trunk exudates from holes gouged by pygmy marmosets, Pando, Brazil

containing experimentally induced or natural exudate sites (trees were not monitored at night). Therefore, we are confident that the patterns of exudate production reported here represent the general amount available to diurnal foragers. We found evidence of marked variation in the rate and amount of exudates produced by different tree species. Three, distinct patterns emerged. The first pattern (Pattern 1, Table  4.4) was observed in species such as Siparuna bifida (family Monimiaceae), Buchenavia punctata (family Combretaceae), and Schefflera moroto­ toni (family Araliaceae). In these species the flow rate per day was extremely limited, with 90–100% of experimentally induced sites failing to produce any measurable quantity of exudates during the 13-day sampling period. Those sites on these trees that did produce exudates tended to do so immediately after injury and then dried up. A second pattern (Pattern 2, Table  4.4), characterized both sampled trees of Cedrela odorata (family Meliaceae). In this species, no measurable amounts of exudate were produced during the first 6  days following the time we inflicted wounds into the bark. Although the amount of exudate produced at experimental sites beginning on day 7 was small (0.25–0.5 g), virtually all nine sites on each tree produced a consistent amount of exudates daily for the remainder of the sample period (total exudate produced = 0.5–1.75 g/tree/day). A third pattern of exudate production was characterized by a more continuous and reliable flow of exudates across the entire 13-day period. In Sclerolobium sp. (family Leguminosae; Caesalpinioideae) and Parkia velutina (family Leguminosae:

a

Exudates collected from all Iriartea sites were experimentally induced

Pattern 3: A more continuous and reliable flow of exudates across most of the sample period Sclerolobium sp. Experimental sites 19.75 10 × 13 days = 130 1.51 0.25–0.50 Natural sites 26.50   5 × 12 days = 60 2.20 0.25–2.0 Parkia velutina Experimental sites 12.75 10 × 13 days = 130 0.98 0.25–0.75 Natural sites 54.25   4 × 9 days = 36 6.02 0.25–5.25 Iriartea deltoideaa 32.0   4 × 9 days = 34 3.55 0.25–2.75 Iriartea deltoideaa 13.0   2 × 8 days = 16 1.62 0.50–3.25 Iriartea deltoideaa 11.25   1 × 6 days = 6 1.87 1.5–3.0 Iriartea deltoideaa 5.75   4 × 6 days = 24 0.95 0.25–0.75 Iriartea deltoideaa 3.25   2 × 4 days = 8 0.81 0.25–1.0 Iriartea deltoideaa 2.25   2 × 4 days = 8 0.56 0.25–1.0 Iriartea deltoideaa 2.0   1 × 8 days = 8 0.25 0.25–0.50 1.75   1 × 9 days = 9 0.19 0.75–1.0 Iriartea deltoideaa

48.4 13.0 76.9 16.6 23.5 0.0 0.0 16.6 37.5 37.5 37.5 77.7

0.75–2.0 0.75–4.75 0.50–2.25 1.25–10.75 0.50–5.75 1.0–3.25 1.5–3.0 0.5–1.5 0.25–1.25 0.25–1.5 0.25–0.50 0.75–1.0

Pattern 2: Absence of measurable amounts of exudates during first 6 days following experimentally induced injury, and thereafter small amounts of exudates produced at most sites Cedrela odorata 4.5 9 × 13 days = 117 0.34 0.25–0.50 0.50–1.50 56.4 Cedrela odorata 4.5 9 × 13 days = 117 0.34 0.25–0.25 0.25–1.0 52.9

Table 4.4  Daily exudate production in natural and experimentally induced exudate sites in Bolivia % Collections Mean yielding no production Min–Max per site Min–Max per tree Total Production Total sites × days exudates per day (g) per day (g) per day (g) Species (g) collected Pattern 1: Exudate production per day extremely limited with 90–100% of experimentally induced sites failing to produce any measurable quantity of exudates Siparuna bifida 0.0 10 × 13 days = 130 0.0 0.0 0.0 100 Buchenavia punctata 0.0 10 × 13 days = 130 0.0 0.0 0.0 100 Schefflera morototoni 1.5 10 × 13 days = 130 0.11 0.25–0.50 0.25–0.50 96.0 Schefflera morototoni 1.5 10 × 13 days = 130 0.11 0.25–0.25 0.25–0.50 90.7 Schefflera morototoni 3.0 10 × 13 days = 130 0.23 0.25–0.25 0.25–0.50 96.1

98 P.A. Garber and L.M. Porter

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Mimosoideae) total exudate production per tree ranged from 1.5–6.75 to 1.75– 13.0 g/day, respectively (Pattern 3, Table 4.4). Two of our sample trees, Sclerolobium sp. and Parkia velutina, contained naturally occurring exudate sites in addition to experimentally induced sites. In the case of Sclerolobium, these holes had been gouged by pygmy marmosets, who had abandoned the tree prior to our study. In the case of Parkia velutina, natural sites were characterized by injury to the trunk, possibly from wood-boring insects or infection. A comparison of experimentally induced and naturally occurring exudate sites for each of these two trees indicates significant differences in exudate production (Fig. 4.2). In both trees, natural sites (N = 9) produced a significantly greater amount of exudates per hole per day than did experimental sites (N = 20) (Sclerolobium sp., natural site mean = 0.6 ± 0.34 g/site/day, experimental site mean = 0.3 ± 0.10 g/site/day, Mann–Whitney U-test, z = 3.30, p < 0.0001; Parkia velutina, natural site mean = 1.53 ± 1.34  g/site, experimental site mean = 0.44 ± 0.17  g/site, z = 5.28, p < 0.0001). Differences between natural and experimental holes could result from a

Fig.  4.2  Comparison of daily exudate production in naturally occurring and experimentally induced sites of injury to the trunk in two species of trees

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number of factors including hole depth, length of time the injury persisted, and the agent of injury (disease, gouging monkeys, and wood-boring insects vs. a single machete cut). Moreover, whereas naturally occurring sites on these trees produced exudates in over 80% of the sample collections, experimentally induced holes produced exudates in only 25–50% of the sample collections (see Table 4.4, Pattern 3). Finally, daily exudate production was monitored in 17 experimentally induced cuts made in the stilt roots of eight Iriartea deltoidea palm trees (Table 4.4). The amount of exudate produced per day in individual Iriartea trees ranged from 0.19 to 3.55 g. In general, 60–90% of cuts produced exudates each day with from 0.25 to 3.25 g collected from each wound. These exudates were produced within 24 h of injury and the same wound continued to produce exudates for a period of at least ten consecutive days. In this regard, exudate production in the stilt roots of Iriartea palms was consistent with Pattern 3 as described for Parkia and Sclerolobium trunk exudates (Table 4.4, Pattern 3).

Exudate Production: Monthly Exudate Flow At our field site in northeastern Peru, we monitored exudate production over the course of 8–11 months (collected twice per week) from two trees of Vochysia lomatophylla, two trees of Parkia nitida, and one tree of the genus Inga sp. Tamarins in our study troop were observed to consume exudates present on each of these individual trees. Moreover, trunk exudates from trees of these species accounted for 66.4% of all exudate feeding bouts in Saguinus. Exudates were collected from areas of the trunk (at a height of up to 2 m) that exhibited signs of natural damage. Our data indicate major differences in the pattern and quantity of exudates produced by these trees. Exudate production in our sample of two Vochysia trees was characterized by a pattern of strong seasonality with a marked decrease in exudate availability during the mid-to-late dry season of August through October (Fig. 4.3a). In the case of two Parkia nitida trees, there was greater monthly variation in the amount of exudates produced by individual trees. In one Parkia nitida tree, for example, trunk exudate production was greatest during the dry season months of July and September, with over 150 g of exudate collected during each of these months (Fig. 4.3b). Although the other Parkia nitida tree also produced a greater amount of exudates in July than during any other month, the amount produced was only 45 g (Fig. 4.3b). Finally, the Inga sp. tree in our sample was characterized by relatively limited exudate production throughout most of the year (<10  g/month), with the greatest amount of exudates (65 g) produced in the early wet season month of December (Fig. 4.3c). Combining the data for all five trees (Fig. 4.4), naturally occurring trunk exudates were available during virtually all months of the year (we do not have data for January) in the home range of our tamarin mixed species study troop. Maximum availability occurred in the late wet season/early dry season (February through June) and minimum availability occurred in the late dry season/early wet season (August through December). Parkia nitida pod exudates were most available and consumed

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Fig. 4.3  Monthly trunk exudate production in five individually monitored trees in northeastern Peru

Fig. 4.4  Combined monthly trunk exudate production in five trees monitored in northeastern Peru

principally during the month of June (Table  4.1). However in July, August, and September pod exudates continued to account for between 3.8 and 6.5% of tamarin plant feeding and foraging time (Table 4.1). Based on our sample of five trees monitored in Peru, exudates provide these small-bodied primates with a reliable and

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renewable resource (see below), with individual trees producing exudates over the course of several weeks and in some cases several months (Fig. 4.3a–c).

Exudates as a Renewable Resource Given evidence of seasonal and tree species differences in exudate production, we examined patterns of exudate site selection in tamarins and callimicos in order to determine the degree to which nongouging callitrichines utilized exudates as a renewable and predictable resource. The tamarins were observed to visit exudates sites on 71.4% (55 of 77 days) of observation days. Exudate feeding in Saguinus was characterized by a foraging pattern in which particular trees were revisited during the same day or over consecutive days. For example, on 40 of 77 observation days (51.2%) multiple trees of the same exudate species were visited on the same day, and on 21 days (27.2%) the same exudate tree was revisited on two or more occasions (Table 4.5). Revisits to the same tree during the same day or over consecutive days suggest that exudate sites exploited by the tamarins represent a productive and locally renewable resource. In the case of callimicos, two trees of Parkia velutina were exploited for pod exudates during a period of 88 full days follows from March through August, 2002. A given tree was revisited on the same day or across consecutive days on 54% (48 of 88) of observation days. In addition, on 10% of days (9 of 88) both Parkia velutina trees were visited (Table 4.5). Data on revisits by callimicos to trunk and stilt root exudate sites in 2005 are not provided, as we did not mark individual trees during that study period. Table 4.5  Patterns of Exudate Site Use in a Mixed Species Troop of Mustached and Saddleback Tamarins and in a Single Species Group of Callimicos

Primate study group Saguinus

Tree Species

Parkia nitida (pod exudates) Saguinus Vochysia lomato­ phylla (trunk exudates) Saguinus Inga sp. (trunk exudates) Saguinus Parkia nitida (trunk exudate) Callimico Parkia velutina (pod exudates)

No. of Days the Same Tree No. of No. of was Visited No. of Feeding on Multiple Days Trees Occasions Exploited Visited Bouts

Visit >1 of Same Species on Same Day

Visit Same Tree on 2 or more Consecutive Days

11

27

48

7

14

10

9

26

37

3

9

6

17

40

76

9

15

7

5

05

6

2

2

0

2

48

63

2

9

10

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Discussion Plant exudates, in particular gums and saps represent a potentially “calorie-rich” food (Nash and Whitten 1989, p. 28) that is a critical year-round or seasonal component in the diet of many species of nonhuman primates. Among New World monkeys, exudate consumption is most common in callitrichines. All species of tamarins and marmosets possess specialized claw-like nails that enable these smallbodied platyrrhines to cling to large vertical trunks while exploiting plant exudates. However, callitrichines differ markedly in their exudate feeding adaptations and ecology. Tamarins (Saguinus), lion tamarins (Leontopithecus), and callimicos (Callimico) are described as facultative exudate feeders (i.e., they lack the anatomical specializations of the jaws and teeth required for gouging holes in bark), whereas marmosets (Callithrix, Cebuella, Callibella, and Mico) are considered obligate ­exudate feeders due to their ability to gouge holes into tree trunks and branches to stimulate­ the flow of exudates, and morphological adaptations ­associated with ­efficient digestion of low quality foods in the ceacum and small intestines (Power and Oftedal 1996; McWhorter and Karasov 2007). As a result, for marmosets, exudates are argued to represent stable, renewable, and available resources throughout the entire year (Ferrari and Lopes Ferrari 1989; Rylands and de Faria 1993; Ferrari and Digby 1996). For example, exudates account for as much as 50–80% of total feeding time (Yépez et al. 2005; Soini 1988; Digby et al. 2007) in some marmoset species, and a single group may intensely exploit a small number of nearby exudate sources over the course of consecutive weeks or months (Soini 1988; Stevenson and Rylands 1988; Yépez et al. 2005; Digby et al. 2007). In contrast, among nongouging callitrichines, exudates are reported to be exploited more opportunistically, consumed principally during the dry season, and account for between 5 and 15% of total feeding time (Garber 1993a; Porter et al. 2009). In the absence of quantitative data on the distribution, availability, and rate of exudate production at individual feeding sites, however, comparisons based solely on time spent feeding remain limited. In this research, we present data on exudate feeding behavior in wild groups of tamarins and callimicos, as well as quantitative information on daily and monthly patterns of exudate production in tree species used by these primates. Saguinus and Callimico lack adaptations of the jaws and teeth that facilitate tree gouging. Given their inability to create exudate sites and directly influence the flow of gum, nongouging callitrichines are dependent on locating and monitoring exudate production across their range in order to effectively exploit this resource. Overall, we found that tamarins and callimicos exploited a relatively large home range (40 ha for our mixed species tamarin troop; Garber 1993b and over 114  ha for our callimico study group, Porter et al. 2007), and had access to a set of productive and naturally occurring exudate sources during virtually all months of the year. Callimico consumed exudates in 7 of 10 study months and Saguinus consumed exudates in 7 of 7 study months. Both species, however, exhibited marked peaks in exudate consumption during the dry season and early wet season. This appeared to coincide with periods of reduced fruit availability (Garber 1993b; Porter 2001).

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Four types of exudate sources were exploited by nongouging callitrichines in this study; exudates resulting from natural wounds to tree trunks (callimicos and tamarins), exudates resulting from holes gouged by pygmy marmosets (callimicos and tamarins), exudates produced in the leguminous pods of trees of the genus Parkia (callimicos and tamarins), and exudates produced on the stilt roots of arborescent palms (callimicos only). Exudates from palms are not exclusively used by callimicos, however, as Terborgh (1983) reports that Saguinus fuscicollis and Saguinus imperator consumed exudates from Iriartea palms during the months of April and July in southern Peru. Trunk exudates exploited by tamarins and callimicos were found to exhibit a range of production patterns. Based on an examination of 105 experimentally induced and 9 naturally occurring trunk exudate sites, most of which were monitored across 13 consecutive days (Table 4.4), we documented that species such as Siparuna bifida, Buchenavia punc­ tata, and Schefflera morototoni produced only traceable amounts of exudate (<0.25 g) immediately after injury and then failed to produce any additional exudate during the remainder of our collection period. In two Cedrela odorata trees, there were virtually no exudates produced during the first 6 days postinjury, followed by daily amounts of from 0.5 to 1.75 g produced per tree for the next 7 days. In contrast, Sclerolobium sp. and Parkia velutina produced larger amounts of exudates during the entire 13-day period with individual trees secreting 1.5–6.75 and 1.75–13.0  g daily. Although the specific factors used by tamarins and callimicos to select exudate sites (e.g., quantity of exudates produced, nutritional composition, or exudate digestibility, see Porter et al. 2009) remain unclear, differences in exudate renewal rates and productivity are likely to influence group ranging and foraging patterns. We also found that on a given tree, naturally occurring exudate sites present on the trunk on average produced two to almost four times as much exudate per day as did experimentally induced injury (Fig. 4.2). Finally, monthly exudate production monitored from five trees of three species in Amazonian Peru indicate that large quantities of naturally occurring trunk exudates were available year round in the home range of our tamarin mixed species study troop. Based on this limited sample, mean monthly exudate production was 432 g (±181 g) and ranged from 676 g in April to 136 g in October. The greatest amounts of trunk exudates were available in the wet season and the least amounts were available in the mid-dry to early wet season. Using our sample of monthly exudate production in these five trees as an index of the availability of trunk exudates in the tamarins home range, there was evidence of a negative relationship between trunk exudate availability and trunk exudate consumption in tamarins (r = −0.69, p = 0.08, n = 7). Although this relationship only approached statistical significance, it suggests that during periods when trunk exudates are most available, tamarins are exploiting other resources such as pod exudates or ripe fruits. A preference for ripe fruits over exudates has been suggested for other callitrichine taxa (Rylands and de Faria 1993). For both tamarins and callimicos, exudates produced in the leguminous pods of Parkia nitida and Parkia velutina were consumed only during the dry season months of May through September, and accounted for the majority of plant feeding and foraging time. At a site in Brazil, Peres (2000) documented that this was the time of year when Parkia pod exudates were most available, and consumed by many primate taxa including tamarins, woolly monkeys, saki monkeys, capuchin

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monkeys, pygmy marmosets, uakaris, and several species of rodents, ungulates, and birds. In the case of callimicos, this involved the exploitation of two trees located approximately 180 m apart (Porter, unpublished data). In the case of Saguinus, the mean distance between nearest Parkia nitida trees was 130  m. Pod exudates are reported to consist principally of nonstructural carbohydrates (Peres 2000), and therefore may represent a more easily digestible food source than trunk exudates or stilt root exudates. However, Parkia trees do not produce pods annually, thus pod exudates are not available during all years. Compared to Callithrix, Cebuella, and Mico, tamarins (30–120 ha) and callimicos (60–150  ha) exploit large home ranges. Our data suggest that nongouging ­callitrichines such as Saguinus and Callimico have access to a large number of naturally occurring exudate sources during all or most months of the year. These exudate sites produce over the course of several days, weeks, and months. Some sites produce sufficient quantities of exudates and are revisited during the same day or are revisited across consecutive days. Thus, in a manner similar to ripe fruits, the distribution, abundance, and production pattern of exudates vary spatially and temporally. Nongouging callitrichines such as saddle-back tamarins, mustached tamarins, and possibly callimicos appear to effectively locate and track the availability of nectar (Garber 1988b), ripe fruit (Garber 1989), and exudate availability across their home range and use this information in making foraging decisions. Although seasonality in exudate feeding (dry season) may reflect a decrease in the availability of more preferred resources (fruits), it also is possible that differences in the nutritional quality or toxin-level of exudates during different times of the year influence exudate feeding behavior. For example, several authors have suggested that plant exudates may offer a needed source of minerals, in particular calcium, to primates like tamarins and galagos whose insectivorous diet is otherwise high in phosphorous (Bearder and Martin 1980; Garber 1984; but see Smith 2000). Other studies point to the potential importance of plant toxins in affecting exudate feeding behavior. For example, Wrangham and Waterman (1981) found that total phenolic content was a significant factor in vervet monkey (Cercopithecus aethiops) selection of exudate trees. Vervets preferentially fed on exudates characterized by lower phenolic content. In contrast, galagos (Galago senegalensis) and patas monkeys (Erythrocebus patas) preferred exudates high in flavonoids, a compound that contains antioxidants and therefore may provide healthrelated benefits (Nash and Whitten 1989). There is evidence that the concentration of flavonoids in exudates is greatest during periods of high heat and water stress to the parent plant (Chaves et al. 1997), conditions most common during the dry season. The degree to which exudate feeding in tamarins and callimico is driven by low fruit availability, the nutritional content of exudates, and/or seasonal differences in the presence of secondary compounds in exudates remains unclear. Given the importance of exudates in the diet of a wide range of primate species, however, we recommend that future field studies of exudativorous animals collect detailed phenological data on exudate availability, including the locations of exudate trees in the animals’ home ranges and the availability and production pattern of exudates throughout the year. A critical set of questions that remains unanswered is the degree to which exudates represent a fallback food (Porter et al. 2009) for some primates and under

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what conditions individual foragers alter their general pattern of feeding, ranging, and habitat use to acquire this resource. Furthermore, additional studies on the nutritional value of exudates should be undertaken to determine the degree to which exudates on the same tree or of the same plant species vary daily and seasonally in their nutritional composition, and whether exudates that age or harden on a trunk or branch are affected by processes of microbial fermentation causing them to differ in nutritional composition relative to more recently produced exudates. As more details are known concerning the phenology of exudates, it will be possible to determine more precisely how exudativorous animals have adapted their foraging strategies to monitor and track this critical resource. Acknowledgments  We thank the governments of Peru and Bolivia for permission to conduct this research. Assistance in data analysis was provided by Martin Kowalewski. Chrissie McKenney and Edilio Nacimento provided assistance with data collection in the field. This research was funded through grants from the National Science Foundation, Earthwatch, the University of Illinois, the Wenner-Gren Foundation for Anthropological Research, the Chicago Zoological Society, the Margot Marsh Biodiversity Fund, the Primate Action Fund, Northern Illinois University, and a National Geographic Research and Exploration grant. PAG wishes to thank Jenni Garber, Sara Garber, and Chrissie McKenney for their love and unconditional support.

References Anninson, G., Trimble, R.P., and Topping, D.L. 1994. Feeding Australian Acacia gums and gum Arabic leads to non-starch polysaccharide accumulation in the cecum of rats. J Nutr 125:283–292. Bearder, S.K. and Martin, R.D. 1980. Acacia gum and its use by bushbabies, Galago senegalensis (Primates: Lorisidae). Int J Primatol 1:103–128. Caton, J.M., Hill, D.M., Hume, I.K., and Crook, G.A. 1996. The digestive strategy of the common marmoset, Callithrix jacchus. Comp Biochem Physiol 114A:1–8. Chapman, C.A., Wrangham, R.W., and Chapman, L.J. 1995. Ecological constraints on group size: an analysis of spider monkey and chimpanzee subgroups. Behav Ecol Sociobiol 36:59–70. Chapman, C.A. and Chapman, L.J. 2000. Determinants of group size in primates: the importance of travel costs. In On the move: How and why animals travel in groups, eds. S. Boinski and P.A. Garber. Chicago: University of Chicago Press. Chapman, C.A., Chapman, L.J., Zanne, A.E., Poulsen, J.R., and Clark, C.J. 2005. A 12-year phenological record of fruiting: implications for frugivore populations and indicators of climate change. In Tropical fruits and frugivores, eds. J.L. Dew and J.P. Boubli. Dordrecht, The Netherlands: Springer. Charles-Dominique, P. 1977. Ecology and behaviour of nocturnal primates. London: Duckworth Press. Chaves, N., Escudero, J.C., and Guttierrez-Merino, C. 1997. Role of ecological variables in the seasonal variation of flavonoid content of Cistus ladanifer exudates. J Chem Ecol 23:579–603. Coimbra-Filho, A.F., da Cruz Rocha, N., and Pissinatti, A. 1980. Morphofisiologia do ceco e sua correlação o tipo odontológico em Callitrichidae Platyrrhini, Primates. Rev Bras Biol 40:177–185. Coimbra-Filho, A.F. and Mittermeier, R.A. 1977. Tree-gouging, exudates eating, and the “shorttusked” condition in Callithrix and Cebuella. In The biology and conservation of the Callitrichidae, ed. D.G. Kleiman. Washington, DC: Smithsonian Institution Press. Dietz, J.M., Peres, C.A., and Pinder, L. 1997. Foraging ecology and use of space in wild golden lion tamarins (Leontopithecus rosalia). Am J Primatol 41:289–305. Digby, L.J., Ferrari, S.F., and Saltzman, W. 2007. Callitrichines: the role of competition in cooperatively breeding species. In Primates in perspective, eds. C.J. Campbell, A. Fuentes, K.C. Mackinnon, M. Panger, and S.K. Bearder. New York: Oxford University Press.

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Enstam, K.L. and Isbell, L.A. 2007. The guenons (genus Cercopithecus) and their allies. In Primates in perspective, eds. C.J. Campbell, A. Fuentes, K.C. Mackinnon, M. Panger, and S.K. Bearder. New York: Oxford University Press. Ferrari, S. and Digby, L.J. 1996. Wild Callithrix groups: stable extended families. Am J Primatol 38:19–27. Ferrari, S. and Lopes Ferrari, M. 1989. A re-evaluation of the social organization of the Callitrichidae, with reference to the ecological differences between genera. Folia Primatol 52:132–147. Ferrari, S., Aparecida Lopes, M., and Krause, A. 1993. Gut morphology of Callithrix nigriceps and Saguinus labiatus from western Brazilian Amazonia. Am J Phys Anthropol 90:487–493. Garber, P.A. 1980. Locomotor behavior and feeding ecology of the Panamanian tamarin (Saguinus oedipus geoffroyi, Callitrichidae, Primates). Int J Primatol 1:185–201. Garber, P.A. 1984. Proposed nutritional importance of plant exudates in the diet of the Panamanian tamarin, Saguinus oedipus geoffroyi. Int J Primatol 5:1–15. Garber, P.A. 1988a. Diet, foraging patterns, and resource defense in a mixed species troop of Saguinus mystax and Saguinus fuscicollis in Amazonian Peru. Behavior 105:18–34. Garber, P.A. 1988b. Foraging decisions during nectar feeding in tamarin monkeys (Saguinus mys­ tax and Saguinus fuscicollis, Callitrichidae, Primates). Biotropica 20:100–106. Garber, P.A. 1989. The role of spatial memory in primate foraging patterns: Saguinus mystax and Saguinus fuscicollis. Am J Primatol 19:203–216. Garber, P.A. 1993a. Feeding ecology and behavior of the genus Saguinus. In Marmosets and tamarins: Systematics, behaviour and ecology, ed. A.B. Rylands. Oxford: Oxford University Press. Garber, P.A. 1993b. Seasonal patterns of diet and ranging in two species of tamarin monkeys: stability versus variability. Int J Primatol 14:145–166. Garber, P.A. 2000. The ecology of group movement: evidence for the use of spatial, temporal, and social information in some primate foragers. In On the move: How and why animals travel in groups, eds. S. Boinski and P.A. Garber. Chicago: University of Chicago Press. Gould, L. and Sauther, M. 2007. Lemuriformes. In Primates in perspective, eds. C.J. Campbell, A. Fuentes, K.C. Mackinnon, M. Panger, and S.K. Bearder. New York: Oxford University Press. Groves, C.P. 2001. Primate taxonomy. Washington, DC: Smithsonian Institution Press. Isbell, L. 1998. Diet for a small primate: insectivory and gummivory in the (large) patas monkey (Erythrocebus patas pyrrhonotus). Am J Primatol 45:381–398. Johnson, D.P., Kays, R., Blackwell, P.G., and MacDonald, D.W. 2002. Does the resource dispersion hypothesis explain group living? Trends Ecol Evol 17:563–570. Joly, M. and Zimmermann, E. 2007. First evidence for relocation of stationary food resources during foraging in a strepsirhine primates (Microcebus murinus). Am J Primatol 69:1045–1052. Kátia, H., Corrêa Mcoutinho, P.E.G., and Ferrari, S.F. 2000. Between-year differences in the feeding ecology of highland marmosets (Callithrix aurita and Callithrix flaviceps) in south-eastern Brazil. J Zool 252:421–427. Lambert, J.E. 2007. Primate nutritional ecology: feeding biology and diet at ecological and evolutionary scales. In Primates in perspective, eds. C.J. Campbell, A. Fuentes, K.C. Mackinnon, M. Panger, and S.K. Bearder. New York: Oxford University Press. Martin, P. and Bateson, P. 1993. Measuring behaviour: An introductory guide. Cambridge: Cambridge University Press. McWhorter, T.J. and Karasov, W. 2007. Paracellular nutrient absorption in a gum-feeding New World Primate, the common marmoset Callithrix jacchus. Am J Primatol 69:1399–1411. Miller, K.E. and Dietz, J.M. 2006. Effects of individual and group characteristics on feeding behaviors in wild Leontopithecus rosalia. Int J Primatol 26:1291–1319. Nash, L.T. and Whitten, P.L. 1989. Preliminary observations on the role of Acacia gum chemistry in Acacia utilization by Galago senegalensis in Kenya. Am J Primatol 17:27–39. Nekaris, A. and Bearder, S.K. 2007. The lorisiform primates of Asia and mainland Africa: diversity shrouded in darkness. In Primates in perspective, eds. C.J. Campbell, A. Fuentes, K.C. Mackinnon, M. Panger, and S.K. Bearder. New York: Oxford University Press. Nekaris, K.A.I. and Rasmussen, D.T. 2003. Diet and feeding behavior of Mysore slender lorises. Int J Primatol 24:33–46.

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Peres, C.A. 2000. Identifying keystone plant resources in tropical forests: the case of gums from Parkia pods. J Trop Ecol 16:287–317. Porter, L.M. 2001. Dietary differences among sympatric callitrichinae in northern Bolivia: Callimico goeldii, Saguinus fuscicollis and S. labiatus. Int J Primatol 22:961–992. Porter, L.M., Garber, P.A., and Nacimento, E. 2009. Exudates as a fallback food for Callimico goeldii. Am J Primatol 71:120–129. Porter, L. and Garber, P.A. 2009. Social behavior of callimico: mating strategies and infant care. In marmosets and callimico: The smallest anthropoid radiation, eds. S.M. Ford, L.M. Porter, and L.C. Davis. New York: Springer Media+Business, Inc. Porter, L., Sterr, S., and Garber, P.A. 2007. Habitat use, diet, and ranging patterns of Callimico goeldii. Int J Primatol 28:1035–1058. Power, M.L. 1996. The other side of callitrichine gummivory: digestibility and nutritional value. In Adaptive radiations of neotropical primates, eds. M.A. Norconk, A.L. Rosenberger, and P.A. Garber. New York: Plenum Press. Power, M. and Oftedal, O. 1996. Differences among captive callitrichids in the digestive responses to dietary gum. Am J Primatol 40:131–144. Ramirez, M.M., 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. Raboy, B., Canale, G.R., and Dietz, J.M. 2008. Ecology of Callithrix kuhlii and a review of eastern Brazilian marmosets. Int J Primatol 29:449–467. Rosenberger, A.L. 1978. Loss of incisor enamel in marmosets. J Mammal 59:207–208. Radespiel, U., Reimann, W., Rahelinirina, M., and Zimmermann, E. 2006. Feeding ecology of sympatric mouse lemur species in northwestern Madagascar. Int J Primatol 27:311–321. Rylands, A.B. and de Faria, D. 1993. Habitats, feeding ecology, and home range size in the genus Callithrix. In Marmosets and tamarins: Systematics, behaviour and ecology, ed. A.B. Rylands. Oxford: Oxford University Press. Smith, A.C. 2000. Composition and proposed nutritional importance of exudates eaten by saddleback (Saguinus fuscicollis) and mustached (Saguinus mystax) tamarins. Int J Primatol 21:69–83. Soini, P. 1988. The pygmy marmoset, genus Cebuella. In Ecology and behavior of neotropical primates, Vol. 2, eds. R.A. Mittermeir, A.B. Rylands, A.F. Coimbra-Filho, and G.A.B. da Fonseca. Washington, DC: World Wildlife Fund. Stevenson, M.F. and Rylands, A.B. 1988. The marmosets, genus Callithrix. In Ecology and behavior of neotropical primates, Vol. 2, eds. R.A. Mittermeir, A.B. Rylands, A.F. Coimbra-Filho, and G.A.B. da Fonseca. Washington, DC: World Wildlife Fund. Stone, A.I. 2007. Ecological risk aversion and foraging behaviors of juvenile squirrel monkeys (Saimiri sciureus). Ethology 113:782–792. Taylor, A.B. and Vinyard, C.J. 2004. Comparative analysis of masseter fiber architecture in tree-gouging (Callithrix jacchus) and nongouging (Saguinus oedipus) Callitrichids. J Morphol 261:276–285. Terborgh, J. 1983. Five New World primates: A study in comparative ecology. Princeton, NJ: Princeton University Press. Tuomisto, H., Ruokolainen, K., and Yli-Halla, M. 2003. Dispersal, environment, and floristic variation of western Amazonian forests. Science 299:241–244. Ushida, K., Fugita, 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. Vinyard, C.J., Wall, C.E., Williams, S.H., and Hylander, W.L. 2003. Comparative functional analysis of skull morphology of tree-gouging primates. Am J Phys Anthropol 120:153–170. Wrangham, R.W., Conklin, N.L., Etot, G., Obua, J., Hunt, K.D., Hauser, M.D., and Clark, A. 1993. The value of figs to chimpanzees. Int J Primatol 14:243–256. Wrangham, R.W. and Waterman, P.G. 1981. Feeding behaviour of vervet monkeys on Acacia tortillas and Acacia xanthophloea: with special reference to reproductive strategies and tannin production. J Anim Ecol 50:715–731. Yépez, P., de la Torre, S., and Snowdon, C.T. 2005. Interpopulation differences in exudates feeding of pygmy marmosets in Ecuadorian Amazonia. Am J Primatol 66:145–158.

Chapter 5

Influences on Gum Feeding in Primates Andrew C. Smith

Abstract  This chapter reviews the factors that may affect patterns of gum ­feeding by primates. These are then examined for mixed-species troops of saddleback (Saguinus fuscicollis) and mustached (Saguinus mystax) tamarins. An important distinction is made between gums produced by tree trunks and branches as a result of damage and those produced by seed pods as part of a dispersal strategy as these may be expected to differ in their biochemistry. Feeding on fruit and Parkia seed pod exudates was more prevalent in the morning whereas other exudates were eaten in the afternoon. This itinerary may represent a deliberate strategy to retain trunk gums in the gut overnight, thus maximising the potential for microbial fermentation of their b-linked oligosaccharides. Both types of exudates were eaten more in the dry than the wet season. Consumption was linked to seasonal changes in resource availability and not the tamarins’ reproductive status, providing no support for the suggestion that gums are eaten as a primary calcium source in the later stages of gestation and lactation. The role of availability in determining patterns of consumption is further supported by the finding that dietary overlap for the trunk gums eaten was greater between species within mixed-species troops within years than it was within species between years. These data and those for pygmy marmosets (Cebuella pygmaea) suggest that patterns of primate gummivory may reflect the interaction of preference and availability for both those able to stimulate gum production and those not.

Introduction Animals often eat different foods at different times, with feeding patterns varying over the course of a day as well as seasonally. Physiological requirements, availability, accessibility, and competition may all serve to shape what is eaten, how much is eaten, and when it is eaten. This chapter examines the patterns of 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_5, © Springer Science+Business Media, LLC 2010

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e­ xudativory within two associating species of tamarins (Saguinus spp.), with the aim of understanding what influences their gum feeding. When considering patterns of gummivory, it is important to note exactly what type of gum is being eaten as chemical composition and availability may vary not only between exudate species but also with the site of production. This may be particularly true when considering exudates produced at trunks and branches as a result of damage and those produced by some plants around seeds in bean-like pods as part of their seed dispersal strategy, hereafter referred to as trunk and pod gums, respectively. In the latter case, the exudates function as a reward to encourage their consumption by primates and other dispersers which then spread the seeds away from the parent tree when they defecate, a strategy referred to as endozoochory (Hopkins 1983; Peres 2000). Exudates may provide primates with a potentially significant source of carbohydrates, protein, and certain minerals, notably calcium (Bearder and Martin 1980; Garber 1984; Nash and Whitten 1989; Heymann and Smith 1999). However, they are typically composed of b-linked oligosaccharides which are not digestible by mammalian enzymes; microbial fermentation is required to unlock their energy (van Soest 1994; Power and Oftedal 1996). The nutritional composition of pod gums that has evolved to attract vertebrate consumers may be expected to 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. Primates may therefore show a difference in feeding patterns between these two categories of gums. Sugar content is not the only factor of gum biochemistry that may influence feeding, toxic and beneficial secondary compounds and elements may all play a role. Although compounds with hypolipidemic, antibiotic, and detoxifying effects may be found in some gums (Johns et al. 2000), the high calcium content of gums relative to fruits has been used to explain their inclusion in the diet of both Old and New World primates (e.g. Bearder and Martin 1980; Garber 1984). Consequently gum consumption may be expected to alter according to calcium requirements with females showing an increase in the later stages of gestation and lactation (Garber 1984). More specifically gummivory has been linked to insectivory in primates, with gums suggested to provide a year-round source of calcium to balance the functionally high phosphorus of the arthropod component of the diet of insectivorous primates [the majority of an insect’s calcium being bound in chitin (Uvarov 1966), inaccessible to the majority of anthropoid primates which lack chitinase (Garber 1984)]. However, it is now known that tropical figs (Ficus spp.) can contain higher concentrations of calcium than exudates, and as such they may represent the main dietary source of this mineral (O’Brien et al. 1998; Smith 2000). The majority of primates lack the dental adaptations that allow marmosets (Callithrix spp.) and a few other species to stimulate gum flow through gouging. As such, their patterns of exudate consumption may be principally determined by the availability and accessibility of exudates. The exudates that non-gouging primates could consume are trunk gums produced in 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) or pod gums produced as

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part of a dispersal strategy. The species and quantities of the exudates eaten will be a product of the somewhat random process of their generation and any preferences or nutritional requirements of the primates consuming them. Consequently, greater variation may be expected between groups or between years in the exudate proportion of the diet when compared to other more reliable resources such as fruit or animal prey. This chapter has two main aims. The first is to investigate patterns of gummivory, both at day and seasonal scales, taking into account trunk gums and endozoochorous pod gums. The second is to examine overlap in gum species exploited, both at a local scale for sympatric primates within and between years. These are achieved using data from field studies of associating saddleback (Saguinus fuscicollis­) and mustached tamarins (S. mystax).

Methods Three mixed-species troops of saddleback and mustached tamarins were observed at the Estación Biológica Quebrada Blanco (EBQB) (4°21¢S, 73°09¢W). The site is located approximately 1 km northwest from the right bank of the Quebrada Blanco in northeastern Peru. The Quebrada Blanco is a white water tributary of the Río Tahuayo which is, in turn, primarily a black water tributary of the Rio Amazonas (for details see Heymann and Hartmann 1991). The annual rainfall at EBQB is 2,740 ± 454 mm (n = 5 years). The climate at EBQB can be divided into wet and dry seasons. The wet season, characterized by higher rainfall, runs from February until May and the dry season from June to January (see Smith et al. 2004). Troop 1 was observed between November 1994 and December 1995 for 141 full days and initially comprised five saddleback (three males, two females) and five mustached tamarins (two males, three females). Troop 2 was observed between January and December 2000 for 112 full days and initially comprised four saddleback (two males, two females) and five mustached tamarins (three males and two females). Troop 3 was observed between July and December 2000 for 36 full days and initially comprised eight saddleback (four males, four females) and eight mustached tamarins (five males and three females). See Smith et al. (2002, 2007) for details of changes in group composition over the study period. Although comprising totally different individuals, Troops 1 and 2 occupied almost the same home range approximately 5 years apart. Troop 3’s home range was adjacent to that of Troop 2’s. Troop 1 was observed for approximately 14 days each month with each species being the focus of observations for half the time. Troop 2 was similarly observed until July 2000. From July 2000, observations were split between Troops 2 and 3 with each troop being observed for 8 days. As for Troop 1, each species was the focal for half of the time. The tamarins were followed from when they left their sleep tree in the morning until they entered their next sleep tree in the afternoon. Continuous recording was used to collect data on all observed instances of feeding on plant parts, with the number of tamarins feeding and the length of time for which they fed being noted. Feeding was defined as actively ingesting or manipulating food, and bouts were measured to the nearest minute.

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Data Analysis For each feeding bout the number of tamarin feeding minutes was calculated by ­multiplying the number of tamarins feeding by the number of minutes they fed for; one “tamarin feeding minute” equals one tamarin feeding for 1 min. Differences in group size were accounted for by dividing this value by the number of tamarins present to give the number of tamarin feeding minutes per group member. This was summed for the two halves of each day, 0500–1100 h and 1100–1700 h, to give a daily total time spent feeding per group member. The amount of time spent feeding on each of the three plant parts in the two halves of the day were compared using paired t-tests, with data restricted to days when the part in question was consumed. Data points were normally distributed, and were considered independent as there is no reason to suspect that temporal feeding itineraries would be correlated between days. The effects of troop and species on the mean time spent feeding on each of the three plant parts per day were examined using ANOVAs. Here, the unit of analysis was the month to avoid problems with repeated sampling and autocorrelation. For these analyses, data were restricted to July to December when all three groups were observed. The effect of season was analysed using unequal variance t-tests to account for the unequal number of wet and dry season months. The unit of analysis was the month, with mean daily feeding times calculated for each month. Troop 3 was excluded from this analysis as it was only observed during the dry season. It was also excluded from calculations of dietary composition for the same reason. The number of feeding bouts in the first and second half of each day was analysed using c2 with Yates’ correction. Dietary overlap was examined via Schoener’s (1968) index of niche overlap (Oij). This index takes into account the relative proportions of each item in the diet and varies between 0.00 (no overlap) and 1.00 (complete overlap). It was calculated from the formula: Oij = 1 − 0.5 ∑ pi − p j where pi is the proportion of i’s feeding records for each of a set of resources and pj is the proportion of j’s feeding records for each of a set of resources.

Results Tamarin Exudate Feeding The tamarins ate exudates from 29 plant species, with 28 being exploited by the saddlebacks and 13 by the mustached tamarins. Trunk and branch gums accounted for 6.3 ± 1.8% (n = 2 groups) of the plant-based diet of the saddlebacks and 1.3 ± 0.1% of the mustached tamarins, and pod gums accounted for 14.5 ± 1.5% of the plant-based diet of the saddlebacks and 15.7 ± 0.3% of the mustached tamarins (group 1, 16.0%; group 2, 15.4%) for the two troops that were studied year-round. Schoener’s index of overlap for non-pod exudates was greater between species for

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Fig.  5.1  Mean time spent feeding on fruit, pod gums, and trunk gums by three mixed-species troops of saddleback and mustached tamarins (error bars indicate SEM)

a given troop (Troop 1, Ofm = 0.70; Troop 2, Ofm = 0.98) than it was within species between troops (saddleback OT1T2 = 0.58; mustached 2 OT1T2 = 0.47). The mean time each tamarin spent feeding on fruit and Parkia pod exudates each day was not different between groups (fruit F35 = 1.8, p > 0.05; pods F35 = 2.5, p > 0.05) and tamarin species (fruit F35 = 1.9, p > 0.05; pods F35 = 0.1, p > 0.05) but the time feeding on exudates from other sources was significantly different between groups (F35 = 10.7, p < 0.05) and tamarin species (F35 = 10.3, p < 0.05) (Fig. 5.1). The time spent feeding on each of the three categories of plant parts showed different temporal patterns (Fig. 5.2). Fruits (saddleback t = 3.6, 160 d.f., p < 0.05; mustached t = 4.5, 149 d.f., p < 0.05) and exudates from Parkia pods (saddleback t = 4.2, 71 d.f., p < 0.05; mustached t = 4.6, 69 d.f., p < 0.05) showed a bias for consumption in the morning and exudates from other sources predominately in the afternoon (saddleback t = −8.4, 101 d.f., p < 0.05; mustached t = −4.7, 60 d.f., p < 0.05). Season had no effect on the time spent feeding on fruits (saddleback t = −1.6, 21.9 d.f., p > 0.05; mustached t = −2.1, 18.4 d.f., p > 0.05) but significantly more time was spent feeding on Parkia pod exudates during the dry season (saddleback t = 2.7, 18.2 d.f., p < 0.05; mustached t = 2.6, 21.0 d.f., p < 0.05). The same was true of exudates from other sources for saddleback but not mustached tamarins (saddleback t = 2.3, 22.0 d.f., p < 0.05; mustached t = −0.3, 12.0 d.f., p > 0.05) (Fig. 5.3).

Discussion The proportion of exudates in the plant diet of saddleback and mustached tamarins at EBQB is similar to that for other tamarins and Amazonian marmosets for which data are available (see Smith, Chapter 3). Exudates from Parkia pods

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Fig. 5.2  Temporal distribution of feeding records on (a) fruits, (b) Parkia pod gums, and (c) trunk gums (error bars indicate SEM)

contributed the majority of feeding records, although 28 other species were also observed to be eaten.

Overlap in Gums Eaten Between Species and Groups For primates that lack adaptations to stimulate gum production, such as tamarins, the degree of gummivory and which plant species are exploited may be influenced by the abundance of the various sources of gums. This is supported by the finding that the interspecific overlap between the exudate portion of the diet of associating

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Fig. 5.3  Seasonal variation in percentage feeding records allocated to fruits, Parkia pod exudates, and exudates from other sources for (a) S. fuscicollis and (b) S. mystax (error bars indicate SEM; n = 2 groups January to June, 3 groups July to December)

saddleback and mustached tamarins was greater than the intraspecific overlap between years. Interpopulation differences in exudate feeding may also exist within species able to gouge trunks, e.g. pygmy marmosets (Cebuella pygmaea) (Yépez et al. 2005). That the extent of exploitation by this species does not seem to correlate with their abundance indicates an active preference based on unknown, though probably nutritional, characteristics. Consequently, the pattern of primate gummivory may reflect the interaction of preference and availability for both those able to stimulate gum production and those not.

Seasonal Patterns of Gummivory In contrast to the year-round consumption of trunk exudates, feeding on gums from Parkia pods was markedly seasonal. Likely due to availability, they were fed upon between April and December during which they accounted for up to 32% and 38% of the saddleback and mustached tamarin monthly diets, respectively. The importance of Parkia as a keystone resource for a wide variety of species, not just

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p­ rimates, has been highlighted by Peres (2000). Pod exudates may be more ­seasonal by their nature than those produced by trunks and branches as a result of damage, though these too may exhibit a degree of seasonality, for example, trees may be damaged by high winds more prevalent during certain months. Seasonal changes in gum feeding have been reported for 21 out of 23 primates (see Smith, Chapter 3; Table 3.2); the majority (19) of which shows an increase in gum consumption in the dry season linked to a reduction in fruit availability. However, with few exceptions, these studies do not differentiate between the two gum types. As  such, it is not possible to determine if such increases are due to pod gums or whether feeding on trunk gums also increase significantly during this period. Differentiating between them is important because their different functions predict differences in biochemistry directly relevant to consumers such as primates. Variation in gum consumption over the year was linked to seasonal changes in resource availability and not the tamarins’ reproductive status. No support was found for the suggestion that exudates are consumed as a primary source of calcium in the later stages of gestation and lactation (Garber 1984). Reports that female saddleback tamarins (Garber 1993) and grey mouse lemurs (Génin 2003) dominate gum licks may be linked to a more general female feeding priority (see Young et al. 1990; Box 1997; Radespiel and Zimmermann 2001; White and Wood 2007), as opposed to calcium requirements; further Isbell (1998) reports that male patas monkeys consume more gums than females. While exudates may supply dietary calcium, some in significant amounts (Bearder and Martin 1980; Garber 1984; Smith 2000), it is unlikely that they play a key role during reproduction. In the only study to examine it to date (Smith 2000), consumption of different sources of exudates was not correlated with calcium content. Moreover, 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 (Smith 2000). However, for those primates that do not consume figs, exudates may still have a role to play.

Patterns of Gummivory Across the Day The pattern of gum feeding observed across the active period corresponds to that found by Heymann and Smith (1999) for saddleback and mustached tamarins and Ramirez (1989) for mustached tamarins, with pod gums consumed more in the mornings and those from trunks consumed more in the afternoon. This almost certainly reflects a deliberate strategy since there is no reason to suspect variation in gum production over the day (Heymann and Smith 1999), and tamarins show movement patterns consistent with mental maps, knowledge of resource availability, and rule-based foraging (Garber 1988; Garber and Dolins 1996; Bicca-Marques 2006). Lacking the dental adaptations for gouging of other gummivores, tamarins are often referred to as opportunistic consumers of exudates. While not being able to stimulate gum flow, tamarins clearly do not eat gums entirely opportunistically; they either

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pass up opportunities to ingest trunk gums in the morning or actively seek them out in the afternoon. For non-specialists lacking lower intestinal adaptations, consumption later in the day may allow for their retention in the gut over night, thus maximizing the amount of energy that can be assimilated from them via microbial fermentation of b-linked oligosaccharides (see Heymann and Smith 1999). Experimental work by Power and Oftedal (1996) suggested that gut retention time does play an important role in gum digestion but cautioned against a simple relationship. The retention of the fluid portion of digesta, containing the complex polysaccharides from gums, has since been demonstrated in captive common marmosets (Caton et al. 1996), although this ability to retain digesta may be lacking in non-specialist gummivores such as the tamarins, particularly since they often swallow large seeds that may impede retention of any part of the digesta (see Garber 1986; Garber and Kitron 1997; Oliveira and Ferrari 2000; Knogge and Heymann 2003). In addition to benefits from consuming gums later in the day, there are also potential costs of consuming them earlier. As Power (1991) noted, they can delay glucose absorption in the small intestine (Blackburn and Johnson 1981; Tsai and Peng 1981; Johnson et al. 1984; Rainbird et al. 1984) and slow both gastric emptying and small intestinal passage (Blackburn and Johnson 1981; Johnson et al. 1984; Nash 1986; Power and Oftedal 1996). Such effects may be less important during periods of reduced metabolic rate, e.g. the afternoon, when tamarins travel less and rest more, and the night when callitrichids lower their metabolic rate (Hetherington 1978; Thompson 1991; Schnell and Wood 1993; Thompson et al. 1994). In contrast to the observations of wild tamarins, Herron et  al. (2001) reported decreased consumption of gum presented late in the afternoon to eight species of captive callitrichids (Saguinus bicolor, S. oedipus, Callithrix geoffroyi, Mico argentata, Callimico goeldii, Leontopithecus rosalia, L. chrysomelas, and L. chrysopygus). Presentation time may be an important factor in this case as callitrichids are known to enter their sleeping sites from mid afternoon (Smith et al. 2007). Feeding itinerary may not be as important for specialist gummivores with intestinal adaptations; indeed several such species show either a peak of gum feeding at the start of their active period or a bimodal pattern with peaks at the start and end of their active period (e.g. C. aurita, Corrêa 1995; C. geoffroyi, Passamani 1998; C. flaviceps, Ferrari 1988; C.  pygmaea, Ramirez et  al. 1978; Yépez et  al. 2005; and P. furcifer, CharlesDominique and Petter 1980). Similarly, consuming gum towards the end of the active period may not be as important for larger species of primates with longer transit times. It is worth noting that transit times may vary by a factor of 10 between species, e.g. 20–26 h in chimpanzees (Pan troglodytes) (Ushida et al. 2006) compared to 2.2–2.5 h in saddleback and mustached tamarins (for foods voided the same day) (Knogge 1998). Consequently it is smaller species with shorter retention times that would gain most from scheduling feeding to increase the chance that gum is retained overnight. In contrast to trunk and branch exudates, pod gums are more frequently eaten in the morning. The opposing feeding patterns for these two types of gum may be linked to differences in their chemistry, particularly in terms of simple sugars and b-linked ­oligosaccharides, predicted from their respective endozoochorous and protective ­ functions (Heymann and Smith 1999). However, whether pod gums are more

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r­ eadily digested by mammalian enzymes than trunk gums, or whether they are richer in simple sugars, has yet to be investigated. Of the pod gums eaten by ­primates Parkia pendula is the most frequently exploited (Smith, Chapter 3), and the only one for which biochemistry has been investigated. Contrary to what may be expected, its principal post-hydrolysis sugar is arabinose (Anderson and de Pinto 1985), the natural L-form of which is indigestible in animals and may reduce sucrose digestion (Hizukuri 1999). However, while the pod gums of other Parkia spp. are produced around the seeds, those of P. pendula are produced at the pods’ sutures when it dehisces (HC Hopkins, personal communication to DMW Anderson, cited in Anderson and de Pinto 1985); if this corresponds to differences in function or biochemistry is unknown. Further work is required on these keystone resources and their relationship with the many primates that exploit them.

Summary Exudates may form a year-round dietary staple for primates or their exploitation may vary on a seasonal basis with consumption typically increasing during the dry season when other resources are scarce. The pattern of exudate feeding may also vary across the day to allow increased retention for microbial fermentation. The available data suggest that these feeding patterns are not influenced by the gum’s calcium content or the reproductive status of the primates consuming them, but instead reflect the interaction of preferences based on other factors. Availability is liable to be key since gum feeding was more similar between associating tamarin species within years than within species between years. Importantly feeding itineraries may be significantly different for the two main types of gum commonly fed upon by primates, namely pod and trunk/branch gums, demonstrating a clear need to avoid blindly lumping all exudates together. Acknowledgments  I thank Dr. Anne Burrows for inviting me to participate in the symposium on the evolution of exudativory in primates at the XXIIth Congress of the International Primatological Society. My thoughts on tamarins and gum feeding have benefited from discussions with Eckhard Heymann, and this chapter benefited from Anne’s comments and those of Leanne Nash and two anonymous reviewers. I thank the Dirección General Forestal y de Fauna of the Peruvian Ministry of Agriculture in Lima and the Dirección Regional de Recursos Naturales y de Medio Ambient of the Regional Government of Loreto in Iquitos for permission to carry out field research at the Estación Biológica Quebrada Blanco. I am indebted to the late Jaime Moro S. and to Enrique Montoya G., Filomeno Encarnación C., and Luis Moya I. for help and logistic support. Arsenio Calle Cordova, Camilo Flores Amasifuén, Emérita R. Tirado Herrera, and Ney Shahuano Tello all provided invaluable assistance in the field. Financial support was provided by Anglia Ruskin University’s Animal and Environmental Research Group and Central Sabbatical Scheme, The University of Reading and the BBSRC (98/S11498 to HM Buchanan-Smith).

References Adrian J, Assoumani M (1983) Gums and hydrocolloids in nutrition. In Reicheigl M (ed) CRC­ handbook of nutritional supplements: vol. II agricultural use. CRC Press, Boca Rotan

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Anderson DMW, de Pinto GL (1985) Gum polysaccharides from three Parkia species. Phytochemistry 24:77–79 Bearder SK, Martin RD (1980) Acacia gum and its use by lesser bushbabies, Galago senegalensis (Primates; Lorisidae). Int J Primatol 1:103–128 Bicca-Marques JC (2006) Distance influences the foraging decisions of emperor and saddleback tamarins. J Zool 269:221–2240 Blackburn NA, Johnson IT (1981) The effect of guar gum on the viscosity of the gastrointestinal contents and on glucose uptake from the perfused jejunum in the rat. Br J Nutr 46:239–246 Box HO (1997) Foraging strategies among male and female marmosets and tamarins (Callitrichidae): new perspectives in an underexplored area. Folia Primatol 68:296–306 Caton JM, Hill DM, Hume ID, Crook GA (1996) The digestive strategy of the common marmoset, Callithrix jacchus. Comp Biochem Physiol A 114:1–8 Charles-Dominique P, Petter JJ (1980) Ecology and social life of Phaner furcifer. In CharlesDominique P, Coper HM, Hladik CM, Petter J-J, Peter-Rousseaux A (eds) Nocturnal Malagasy primates: ecology, physiology and behaviour. Academic Press, New York Corrêa HKM (1995) Ecologia e comportamento alimentar de um grupo de suguis-da-serraescuros (Callithrix aurita E. Geoffroy 1812) no parque estudual da Serra do Mar, Nucleo Cunha, São Paulo. MS thesis, Universidade federal de Minas Gerais, Belo Horizonte Ferrari SF (1988) The behaviour and ecology of the buffy-headed marmoset Callithrix flaviceps (O. Thomas 1903). PhD thesis, University College London, London 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 (1986) The ecology of seed dispersal in two species of callitrichid primates (Saguinus mystax and Saguinus fuscicollis). Am J Primatol 10:155–170 Garber PA (1988) Diet, foraging patterns and resource defence in a mixed species troop of species Saguinus mystax and Saguinus fuscicollis in Amazonian Peru. Behaviour 105:18–34 Garber PA (1993) Seasonal patterns of diet and ranging in two species of tamarin monkeys: stability versus variability. Int J Primatol 14:145–166 Garber PA, Dolins FL (1996) Testing learning paradigms in the field: evidence for use of spatial and perceptual information and rule-based foraging in wild mustached tamarins. In Norconk MA, Rosenberger AL, Garber PA (eds) Adaptive radiations of Neotropical primates (pp. 201–216). Plenum Press, New York Garber PA, Kitron U (1997) Seed swallowing in tamarins: evidence of a curative function or enhanced foraging efficiency? Int J Primatol 18:523–538 Génin F (2003) Female dominance in competition for gum trees in the grey mouse lemur Microcebus murinus. Rev Écol (Terre Vie) 58:397–410 Glicksman M (1969) Gum technology in the food industry. Academic Press, New York Herron S, Price E, Wormell D (2001) Feeding gum Arabic to New World monkeys: species differences and palatability. Anim Welf 10:249–256 Hetherington CM (1978) Circadian oscillation of body temperature in the marmoset, Callithrix jacchus. Lab Anim 12:107–108 Heymann EW, Hartmann G (1991) Geophagy in mustached tamarins, Saguinus mystax (Platyrrhini: Callitrichidae), at the Rio Blanco, Peruvian Amazonia. Primates 32:533–537 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 Hizukuri S (1999) Nutritional and physiological functions and uses of L-arabinose. J Appl Glycosci 46:159–165 Hopkins HC (1983) The taxomony, reproductive biology and economic potential of Parkia (Leguminosae: Mimosoideae) in Africa and Madagascar. Bot J Linn Soc 87:135–167 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 Johns T, Nagarajan M, Parkipuny ML, Jones PJH (2000) Maasai gummivory: implications for Paleolithic diets and contemporary health. Curr Anthropol 41:453–459 Johnson IT, Gee JM, Mahoney RR (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

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Knogge C (1998) Zur Vkologie der Samenausbreitung durch zwei Krallenaffenarten (Saguinus mystax, Saguinus fuscicollis) in Amazonien, Nordost-Peru. Unpublished PhD thesis, University of Bielefeld, Bielefeld Knogge C, Heymann EW (2003) Seed dispersal by sympatric tamarins, Saguinus mystax and Saguinus fuscicollis: diversity and characteristics of plant species. Folia Primatol 74:33–47 Meer W (1980) Gum arabic. In Davidson RL (ed) Handbook of water soluble gums and resins. McGraw-Hill Book Co., New York Nash LT (1986) Dietary, behavioural and morphological aspects of gummivory in primates. Yearb Phys Anthropol 29:113–137 Nash LT, Whitten PL (1989) Preliminary observations on the role of Acacia gum chemistry in Acacia utilization by Galago senegalensis in Kenya. Am J Primatol 17:27–39 O’Brien TG, Kinnaird MF, Dierenfeld ES, Conklin-Brittain NL, Wrangham RW, Silver SC (1998) What’s so special about figs? Nature 392:668 Oliveira ACM, Ferrari SF (2000) Seed dispersal by black-handed tamarins, Saguinus midas niger (Callitrichinae, Primates): implications for regeneration of degraded forest habitats in eastern Amazonia. J Trop Ecol 16:709–716 Passamani M (1998) Activity budget of Geoffroy’s marmoset (Callithrix geoffroyi) in an Atlantic forest in southeastern Brazil. Am J Primatol 46:333–340 Peres CA (2000) Identifying keystone plant resources in tropical forests: the case of gums from Parkia pods. J Trop Ecol 16:287–317 Power ML (1991) Digestive function, energy intake and the response to dietary gum in captive Callitrichids. PhD thesis, University of California, Berkeley Power ML, Oftedal OT (1996) Differences among captive callitrichids in the digestive responses to dietary gum. Am J Primatol 40:131–141 Radespiel U, Zimmermann E (2001) Female dominance in captive gray mouse lemurs (Microcebus murinus). Am J Primatol 54:181–192 Rainbird AL, Low AG, Zebrowska T (1984) Effect of guar gum on glucose and water absorption from isolated loops of jejunum in conscious growing pigs. Br J Nutr 52:489–498 Ramirez M (1989) Ecology and demography of the mustached tamarin, Saguinus mystax in northeastern Peru. PhD thesis, City University of New York, New York Ramirez MF, Freese CH, Revilla CJ (1978) Feeding ecology of the pygmy marmoset (Cebuella pygmaea) in northeastern Peru. In Kleiman DG (ed) The biology and conservation of the Callitrichidae. Smithsonian Institution Press, Washington, DC Schnell CR, Wood JM (1993) Measurement of blood pressure and heart rate by telemetry in conscious, unrestrained marmosets. Am J Physiol 264:1509–1516 Schoener TW (1968) The Anolis lizards of Bimini: resource partitioning in a complex fauna. Ecology 49:704–726 Smith AC (2000) Composition and proposed nutritional importance of exudates eaten by saddleback (Saguinus fuscicollis) and mustached (Saguinus mystax) tamarins. Int J Primatol 21:69–83 Smith AC, Knogge C, Huck M, Löttker P, Buchanan-Smith HM, Heymann EW (2007) Long term patterns of sleeping site use in wild saddleback (Saguinus fuscicollis) and mustached tamarins (S. mystax). Am J Phys Anthropol 134:340–353 Smith AC, Tirado ER, Buchanan-Smith HM, Heymann EW (2002) Multiple breeding females and allo-nursing in a wild group of moustached tamarins (Saguinus mystax). Neotrop Primates 9:67–69 Smith AC, Kelez S, Buchanan-Smith HM (2004) Factors affecting vigilance within wild mixedspecies troops of saddleback (Saguinus fuscicollis) and mustached tamarins (S. mystax). Behav Ecol Sociobiol 56:18–25 van Soest PJ (1994) Nutritional ecology of the ruminant, 2nd edition. Cornell University Press, Ithaca Thompson S (1991) Biotelemetric studies of mammalian thermoregulation. In Asa C (ed) Biotelemetry applications for captive animal care and research. Wheeling, American Association of Zoological Parks and Aquariums

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Thompson SD, Power ML, Rutledge CE, Kleiman DG (1994) Energy metabolism and ­thermoregulation in the golden lion tamarin (Leontopithecus rosalia). Folia Primatol 63:131–143 Tsai AC, Peng B (1981) Effects of locust bean gum on glucose-tolerance, sugar digestion, and gastric-motility in rats. J Nutr 111:2152–2156 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 Uvarov B (1966). Grasshoppers and locusts: a handbook of general acridology, vol. 1. Cambridge University Press, Cambridge White FJ, Wood KD (2007) Female feeding priority in bonobos, Pan paniscus, and the question of female dominance. Am J Primatol 69:837–850 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 Young AL, Richard AF, Aiello LC (1990) Female dominance and maternal investment in strepsirhine primates. Am Nat 135:473–483

Chapter 6

Gummivory in Cheirogaleids: Primitive Retention or Adaptation to Hypervariable Environments? Fabien G.S. Génin, Judith C. Masters, and Jorg U. Ganzhorn

Abstract  Gummivory in cheirogaleids, apart from the specialist gummivore Phaner, is often viewed as a fall-back diet; animals are forced to consume gums when other foods are unavailable. We propose an alternative explanation that cheirogaleid gummivory is an adaptation to hypervariable environments. First, we compared morphological adaptations to gummivory evinced by cheirogaleids and other gummivorous primates. Despite convergent trends, adaptations to gummivory are quite variable. Second, a long-term field study of the reddish-grey mouse lemur, Microcebus griseorufus, in the highly variable xerophytic forest of southern Madagascar reveals this species to be the most specialized gummivore of all known mouse lemurs. Third, a comparison of the nutritional composition of gums and fruits consumed by M. griseorufus shows these two food types to be of equivalent nutritive content. Gums consumed by M. griseorufus are exuded all year round, increasing the predictability of food availability in a hypervariable habitat, while fruit availability exhibits high intraand inter-annual variation. Finally, we compared the global distributions of gummivorous mammals with a map of the regions subject to El Niño-related droughts, which indicated a strong congruence between gummivory and hypervariability.

Introduction The ecological literature pertaining to the evolution of dietary regimes is replete with contradictions. Generalists are viewed as less competitive (but more adaptable) than specialists, so harsh environments, with increased intensities of natural selection, should favour specializations rather than opportunism. On the other hand, animals broaden rather than restrict their dietary choices during times of stress (Masters and Rayner 1993), complicating models of how selection operates to drive

F.G.S. Génin (*) Department of Zoology, University of Fort Hare, Private Bag X1314, Alice 5700, South Africa 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_6, © Springer Science+Business Media, LLC 2010

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specialization, and supporting the view that opportunism is an adaptation to variable environments (Génin and Perret 2003; Génin 2008). Likewise, explanations for the evolution of gummivory are similarly beset by apparent contradictions. Many authors (e.g. Petter et al. 1977; Hladik et al. 1980; papers in this volume) frequently view gummivory as a fall-back dietary choice under stressful conditions; i.e., animals are forced to eat gum, which is neither desirable nor particularly nutritious, when other foods are unavailable (Viguier 2004). Yet successful gum exploitation requires a suite of morphological and behavioral adjustments (Nash 1986), and can alternatively be seen as an adaptive response to particular environmental pressures (Génin 2008). Within primates, partial gummivory has been documented in numerous species, whereas gum-specialists are few (Charles-Dominique 1971; Coimbra-Filho and Mittermeier 1976; Bearder and Martin 1980; Charles-Dominique and Petter 1980; Nash 1986; Isbell 1998; Heymann and Smith 1999; Peres 2000). Gums have been defined as amorphous, acidic polysaccharides of variable chemical and structural composition (Bearder and Martin 1980), and are found in various tree families including Anacardiaceae, Burseraceae, Combretaceae, and Fabaceae. Gum exudation results from structural damage or wood-boring by insects, and appears to seal wounds against infection and dehydration. It may be particularly abundant in dry and unpredictable environments (Bearder and Martin 1980; Nash 1986; Génin 2008). Because gum-eaters provide no obvious benefit to the gum-producers, whereas frugivores often assist in the dispersal of seeds, it is a logical assumption that lower levels of investment by the plants should result in gums having lower nutritive contents than fruits. However, this assumption has never been investigated. In this chapter we argue that gummivory evolved in cheirogaleids (and perhaps also in other mammals) as an adaptive response to high levels of environmental variability. We hence view the capacity for gummivory as a dietary specialization that is likely to have arisen convergently many times, rather than an ancestral, unspecialized condition. We draw data in support of this interpretation from four sources: (a) A comparison of the morphological adaptations to gummivory observed in gummivorous primates. (b) Long-term field observations of a population of reddish-grey mouse lemurs, Microcebus griseorufus, an apparent gum-specialist, although it lacks some of the specific adaptations traditionally attributed to gummivores. M. griseorufus occupies the xerophytic spiny forest fragments of southern Madagascar, an unpredictable and highly variable environment in terms of rainfall (Dewar and Richard 2007). We explored two hypotheses possibly explaining the higher attractiveness of fruits compared with gums (Génin 2008, in press): Mouse lemurs may prefer fruit for their better quality (nutritive value, i.e. nutritive content and digestibility) or for their higher quantity or profitability (spatio-temporal distribution). We tested specifically the hypothesis of Heymann and Smith (1999), who suggested that non-specialist gummivores might compensate their low capacity to digest gums by feeding on them at the end of their activity period. (c) A comparison of the nutritive composition of fruits and gums consumed by M. griseorufus, as well as a comparison of the nutritional contents of these gums

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with those of gums consumed by other cheirogaleids (particularly by Microcebus murinus and Phaner pallescens) in the more seasonal western deciduous forest. (d) A comparison of the global distributions of gummivorous mammals with a map of the regions of the world which are most susceptible to El-Niño-related droughts.

Methods Adaptations to Gummivory Gum-specialists exhibit a suite of adaptations, including relatively small body size (<1 kg), pointed and/or keeled nails, a well-developed tooth scraper, long tongue, and large caecum (Hill and Rewell 1948; Bearder and Martin 1980; Charles-Dominique and Petter 1980; Nash 1986; Lindenmayer 2002). The striking similarities observed in the skulls and the tooth combs of lorisids, Euoticus, other galagos, Phaner, and Allocebus have been interpreted as convergent adaptations to gum-feeding (Masters and Brothers 2002; Vinyard et al. 2003; Viguier 2004). We investigated museum skins and skulls of 10–20 individuals per species for strepsirhine taxa known to practice gummivory, and classified by curators under the following rubrics: Euoticus elegantulus (s.l.), Galago matschiei, G. moholi, G. senegalensis, Loris tardigradus (s.l.), Mirza coquereli, M. murinus, Nycticebus pygmaeus, Otolemur crassicaudatus, and Phaner furcifer (s.l.). We also studied four specimens of Allocebus trichotis available to us, and 40 specimens of M. griseorufus, recently recognized as a distinct species (Rasoloarison et  al. 2000) and represented by a large collection at the American Museum of Natural History (identified by us and also by Godfrey, pers. com.). The specimens we examined were housed in the following institutions: American Museum of Natural History (New York), Carnegie Museum of Natural History (Pittsburgh), Field Museum of Natural History (Chicago), Museum National d’Histoire Naturelle (Paris), Natural History Museum (London), and Royal Museum of Central Africa (Tervuren). All the specimens examined were scored for the presence of characters potentially related to gummivory (body mass < 1 kg; pointed and/or keeled nails; relatively large hands and/or feet; horizontally oriented tooth comb; tightly packed tooth comb lacking interdental spaces; coronoid process angled backwards; robust upper canines; single-rooted [caniniform] P2; and relative size of P2). Details of the cranial characters are described in Masters and Brothers (2002). Additionally, we recorded information on caecum structure taken from Hill and Rewell (1948).

The Diet of M. griseorufus In Berenty, we conducted a field study of M. griseorufus in a 5.7 ha fragment of remaining spiny forest. To assess the diet, we trapped, weighed, and equipped with radio-collars (TW4-button cell tags, Biotrack, Wareham, UK) 26 animals (12 males

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and 14 females). Animals were radio-tracked continuously in the dry season (April–August, 9 males and 11 females) or in the rainy season (November–March, seven males and seven females), or both (two males and two females), using a FRX-2001 MIZUHO receiver (Tokyo, Japan). The general method used for captures and radio-tracking has been described previously (Génin 2008). We measured the number of trees visited per night, the time spent foraging (time feeding on the trees excluding rest and social interactions) on the two main resources, fruits and gums, and mapped and identified at least to genus level all the trees visited (Schatz 2001). To test the hypothesis of low digestibility of gums (Heymann and Smith 1999) and assess the temporal distribution of foraging on different food types, we recorded all occurrences of insect hunting, and fruit and gum foraging every 15 min in all-night follows, using averages when individuals (four males and four females) were radio-tracked for more than one complete night (up to four). Focal subjects rarely were out of sight during follows, though follows were interrupted during heavy rain or thunder storms.

Energy Content of Gums and Fruits in Southern and Western Madagascar To compare the nutritive contents of fruits and gums consumed by M. griseorufus, we collected samples in Berenty out of the radio-tracking area. To compare the nutritive contents of gums consumed by other cheirogaleids, we also collected gums in the Analabe Private Reserve (Menabe, Morondava region), where we conducted nocturnal surveys to locate fruit and gum trees exploited by M. murinus and Phaner (furcifer) pallescens (10 h). Additionally, we collected gums known from other studies to be consumed by cheirogaleids (Charles-Dominique and Petter 1980; Génin 2003; Radespiel et  al. 2006). We excluded from the analyses three gum trees found in both the South and the West which exuded small amounts of gum consumed by M. murinus on rare occasions (only one observation for each): Neobeguea mahafalensis (Meliaceae), and the exotics Melia azedarach (Meliaceae) and Pithecelobium dulce (Fabaceae). With respect to fruits, we sampled all ripe fruits present on fruiting trees (<3 m) and weighed the pulp before and after drying it. Biochemical analyses were carried out with standard procedures at University of Hamburg, Department of Animal Ecology and Conservation (Bollen et al. 2004). Total nitrogen was determined using the Kjeldahl procedure, and converted to crude protein by multiplying the nitrogen concentration by 6.25. Concentrations of soluble sugars were determined as the equivalent of galactose after acid hydrolization of the 50% methanol extract. This measurement correlates well with concentrations obtained with enzymatic analyses of glucose, fructose, and galactose. Lipids were determined by the Soxleth method. About 0.5–1.0 g of sample was extracted for 4 h with petrol-ether in a Soxleth apparatus, and the dissolved fat was weighed after

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evaporation of the petrol ether. The nutritive content of the food in kilojoule was calculated using the formula (carbohydrates × 4 + proteins × 4 + lipids × 8.9) × 4.184.

Spatio-Temporal Distribution of Food and Hypervariability For each of the 26 radio-tracked M. griseorufus, we assessed the operational spatial distributions of available fruiting and gum trees using the frequency distribution of the distances from all fruit and gum trees visited to the nearest fruit or gum tree visited at least once by any individual during the same 3-week period. We observed the effect of machete cuts on two trees that did not show any trace of insect infestation: one Alantsilodendron alluaudianum (avoha) and one Commiphora orbicularis (daro mena). The gum flows and the cuts were protected against gum-feeders (mouse lemurs, crested couas, and geckos) using pieces of mosquito net. Because this species was the most abundant and preferred gum tree, we measured 30 Alantsilodendron trees (height and diameter), and counted, collected (<3 m), and weighed (±0.001 g) all drops of gum at the end of the rainy season (March) and at the end of the dry season (September). The 30 trees were individually identified, and the extent of renewal of all located gum flows was evaluated by collecting and weighing all the gum daily, within the last hour of daylight, for 7 days. We used the values of constancy (intra-annual variation = seasonality) and contingency (inter-annual variation = unpredictability) of rainfall provided by Dewar and Richard (2007) to assess the degree of variability of environments in which different cheirogaleid species occur. For each species, we chose the closest localities to the areas occupied by the study populations, and calculated a range of constancy and contingency. We considered four modalities of variability: seasonality (low constancy), unpredictability (low contingency), hypervariability (low constancy and low contingency), and predictability (high constancy and contingency). To investigate the possible influence of El Niño-related droughts on gummivory, we plotted the geographic distributions of the main groups of gummivorous mammals (primates and marsupials) on a map downloaded from http://www.pmel.noaa.gov.

Data Analyses Normality of all frequency distributions was evaluated graphically and all values are means ± SE. We carried out most statistical comparisons using analyses of variance and Student’s t-tests. Because body mass was higher in females than in males and correlated negatively with gum foraging and positively with fruit foraging (Pearson’s correlation coefficient rP), we used body mass as a covariate factor (ANCOVA) in the test of the effect of sex on diet (paired fruit and gum foraging durations). We provide exact probabilities for all tests, except when P < 0.001.

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Results Diverse Forms of Adaptation to Gummivory The distribution of morphological characters that have been linked to gummivory is presented in Table 6.1. The tooth combs of lorisids, Euoticus, and Allocebus are tightly packed, with minimal interdental spaces. Allocebus, Phaner, Euoticus, and M. griseorufus have elongated, horizontal tooth combs, and, together with lorisids, low coronoid processes. Phaner, Allocebus, Euoticus, and lorisids also share large upper canines and enlarged caniniform P2s. Most cheirogaleids (with the exception of Microcebus spp.), and indeed most lemurs, have pointed nails, as are found in Euoticus and G. matschiei. Nevertheless, Microcebus spp. climb most vertical trunks easily, suggesting that pointed nails are generally unnecessary for very small animals. Mouse lemurs do, however, appear to avoid large trees with smooth bark such as Adansonia rubrostipa used by Phaner (furcifer) pallescens (pers. obs.). Gum feeding involves at least two different strategies: gouging and scraping. Gouging, associated with robust skulls and oblique incisors, is used by South American callitrichids (Callithrix spp., Coimbra-Filho and Mittermeier 1976; Vinyard et al. 2003) and by South-east Asian slow lorises (Nycticebus spp., Tan and Drake 2001). However, gouging may be unnecessary for scrapers, which feed on gums produced in reaction to insect infestation, such as those consumed by African galagos (Euoticus spp., Galago spp. and Otolemur spp.) and by Malagasy forkmarked lemurs (Phaner spp., Bearder and Martin 1980; Charles-Dominique and Petter 1980). Scrapers are characterized by horizontal tooth combs and large upper canines, and often also by enlarged, single-rooted P2s.

Is M. griseorufus a Gum-Specialist? Cheirogaleidae is the only lemuroid family in which gummivory has been documented. Species of all five cheirogaleid genera have been observed to feed on gum at least occasionally. Phaner spp. are the only known gum-specialists, although they also include insects, fruits, and nectar in their diets (Charles-Dominique and Petter 1980). The diet of A. trichotis is poorly documented, but morphological features (Masters and Brothers 2002; Viguier 2004) and preliminary observations indicate that gum is an important part of its diet (Biebouw, pers. com.). Microcebus and Mirza spp. have been reported to feed on gum only occasionally. Nevertheless, gum may be a keystone resource, at least seasonally, for M. murinus and M. ravelobensis (Génin 2003; Radespiel et  al. 2006). The caecum of mouse lemurs has been described as large and capacious, although it is difficult to determine to which ­species the authors refer (Hill and Rewell 1948). The reddish-grey mouse lemur (M. griseorufus) is found in the most variable environments of Madagascar, the ­sub-arid xerophytic forests and thickets of the South (Génin 2008). Gum comprises

+ + + + +

+

+ + + + −

+

−

+ − − + + −

+ − − − − −

− + + + +

Inter-dental spaces

Lemuroids Phaner spp. + + + + − Allocebus trichotis + + + + − Microcebus + − − + − griseorufus + − − − + Microcebus murinus +: character present; −: character absent; 0: no tooth comb; G: gouging; S: scraping a See Stephenson et al. Chap. 12 b Meier and Albignac (1991) and Lemelin and Jungers (2007) c Viguier (2004)

Lorisoids Euoticus spp. Galago moholi Galago matscheiei Galago senegalensis Otolemur crassicaudatus Nycticebus pygmaeus

Table 6.1  Mosaic expression of adaptations to gummivory Locomotion Feeding Large Horizontal Pointed/ hands/ tooth keeled Small feetb comb nailsa Species size

+ + − −

+

+

+ + + − +

Enlarged upper canines

+ + +

+

+ + + + −

Coronoid angled backwardsc

+

+ + +

+

+ − − − −

Caniniform P2 (onerooted)

_

+ + −

+

+ − − + +

P2 >> P3

+

? ? ?

?

+ ? ? + +

Large caecum

S

S S S

G

S S S S S

Gum feeding strategy

129

130

F.G.S. Génin et al.

a major part of the diet of this species all year round (Génin 2008). In contrast, most females and only a few males feed on fruit, and fruit feeding exhibits high intra- and inter-annual variations (Génin 2008). Radio-tracked M. griseorufus fed on gum on average 78 ± 6% of the total time spent foraging (N = 26). All 26 individuals (12 males and 14 females) fed on gum, climbing both up and down the trunks, sometimes very low down, and sometimes high up on small branches. Out of 499 gum trees visited, 85% were A. alluaudianum and 15% were Commiphora spp. (four species) (Table 6.2). Alantsilodendron gum forms liquid droplets that dry and crystallize. Close observations revealed that animals scraped the bark with the tooth comb to stimulate gum flow, with old gum sources forming deep crevasses. Eleven individuals out of 26 (eight males and three females) fed exclusively on gum and insects. Animals also fed on fruit (15/26), nectar (2/26), and homopteran secretions (3/26). The total duration of foraging was longer in the dry season (366 ± 26 min/night, N = 16) than in the rainy season (156 ± 25 min/ night, N = 10) but independent of sex [respectively, F (1,22) = 13.2, P = 0.001; F (1,22) = 0.1, P = 0.7]. Moreover, animals spent significantly more time in gum foraging than in fruit foraging [F (1,22) = 18.2, P < 0.001] and the proportion of gum in the diet was higher in the dry season than in the rainy season [ANOVA with fruit and gum foraging durations paired: F (1,22) = 7.4, P = 0.013]. The duration of gum foraging was significantly higher in the dry season (276 ± 34 min/night) than in the rainy season (106 ± 22 min/night), but fruit foraging did not show any seasonal variation and averaged 55 ± 16 min/night [respectively, F (1,22) = 11.9, P = 0.002; F (1,22) = 0.0, P = 1]. Females spent more time in fruit feeding than males did, but no significant difference was observed in gum feeding [respectively, F (1,22) = 6.5, P = 0.018; F (1,22) = 0.8, P = 0.4]. On average, females were also significantly heavier than males (males: 49 ± 3 g, N = 12; females: 60 ± 2 g, N=14 (t = 3.3, df = 24, P = 0.003), and body mass (BM) co-varied with total duration of foraging and the proportions of fruit and gum in the diet [covariate effect of BM, F (1,23) = 9.0, P = 0.006; diet × BM, F (1,22) = 11.0, P = 0.003]. If BM is taken as a covariate, total foraging duration for both gum and fruit foraging was longer in females than in males, revealing a higher rate of energy acquisition [F (1,23) = 4.4, P = 0.048]. This observation suggests that fruits are generally more profitable than gum. Because all individuals consumed some gum and because the diet of the radio-tracked animals comprised more than 75% gum on average, M. griseorufus can be considered a gum-specialist.

Fruit and Gum Profitability Although all individuals fed on gum, radio-tracked M. griseorufus preferred fruit (Génin 2008, in press). Fruits were mainly consumed by dominant individuals, usually females, exhibiting higher body masses than those individuals that fed exclusively on gums and insects (Génin, in press). We observed a few agonistic interactions on fruiting trees but subordinates usually deferred to dominants on the trees (Génin, in press). This higher attractiveness of fruit could be explained by higher nutritive

  4.0

17.5

0.0

20.5

B

Brassicaceae

Maerua ruda

(continued)

February–April (Mg) Year round, peak in November– December (Mg)

60.9

0.4

B

Bigniniaceae

Fruits Phylloctrenium decaryi   7.3

Year round (Mg) Year round (Mg) Year round (Mg) Year round (Mg) ? (Mm) ? (Mm) ? (Mm, Pp) ? (Mm, Pp) ? (Mm, Pp) ? (Mm, Pp) Year round (Mg) ? (Mm)

64.3 48.0 34.9 40.0 44.0 75.4 25.4 27.2 49.2 37.9 48.3 40.2 44.6 ± 4.3

55.5

Phenology/ (consumer species)

Energy content (kJ/100 g)

forest (Analabe: A); and in the southern

Table 6.2  Nutritive contents of gums and fruits (dry matter) consumed by cheirogaleids in the western deciduous spiny forest (Berenty: B) Carbohydrates Crude Species/genera Family Sites (%) protein (%) Fat (%) Gums Commiphora orbicularis Burseraceae B 55.9 11.3 0 Commiphora aprevalii Burseraceae B 43.5   6.6 0 Commiphora lamii Burseraceae B 31.4   5.0 0 Commiphora humbertii Burseraceae B 39.6   2.3 0 Commiphora sp1 Burseraceae A 30.8 15.3 0 Commiphora sp2 Burseraceae A 74.5   4.4 0 Terminalia mantaliopsis Combretaceae A 25.2   1.4 0 Terminalia mantalis Combretaceae A 26.1   2.4 0 Delonix decary Fabaceae (Cesalpinacea) A 47.6   3.9 0 Albizia mainaea Fabaceae (Mimosaceae) A 28.4 11.3 0 Allantsilodendron alluaudianum Fabaceae (Mimosaceae) B 29.5 21.0 0 Rhopalocarpus sp. Sphaerosepalaceae A 38.2   3.9 0 39.2 ± 4.4   7.4 ± 1.8 0

6  Gummivory in Cheirogaleids 131

B B B B B B B B

Burseraceae Ebenaceae Malvaceae (Tiliaceae) Malvaceae (Tiliaceae) Malvaceae (Tiliaceae) Rubiaceae

Salvadoraceae Viscosaceae

C. orbicularis Diospyros sp. Grewia saligna Grewia sp. Grewia sp. (Tabarike) Tarenna (Enterospermum) sp.

Azima tetracantha Viscum sp.

Mm, M. murinus; Mg, M. griseorufus; Pp: Phaner pallescens

Sites

Family

Species/genera

Table 6.2  (continued)

  5.3 14.9

11.0 ± 1.6

28.4 ± 8.1

16.9   3.7 11.3 14.3   7.3 12.2

65.6 33.0

  2.1 42.4   2.5 11.5 15.3 51.6 68.2 45.7

34.9 47.1 22.2 29.1 26.3 64.6

2.0 ± 0.8 42.0 ± 6.0

0.2 0.0

7.9 1.4 4.2 2.1 2.2 1.7

Carbohydrates Crude Energy content (%) protein (%) Fat (%) (kJ/100 g)

October (Mg) Year round (Mg) April–May (Mg) April (Mg) April–June (Mg) April–May (Mm, Mg) October (Mg) Year round, peak in November– December (Mg)

Phenology/ (consumer species)

132 F.G.S. Génin et al.

6  Gummivory in Cheirogaleids

133

values of fruits or by their higher profitability in terms of foraging efficiency. Moreover, local resource defence was only observed on fruiting trees (Génin, in press). The diet of M. griseorufus is dominated by the gums of two tree genera, Alantsilodendron and Commiphora, which show different patterns of gum exudation. Machete cuts had no effect on A. alluaudianum trees, which exude gum in reaction to xylophagous larvae, mainly click beetles (Elateridae) and long-horned beetles (Cerambicidae) often observed copulating on the trunks. Traces of infestation were often observed on gum-exuding trees. By contrast, Commiphora spp. (five species observed to exude edible gum, see Table 6.2) produce a gum of similar quality, but only when injured, and sometimes in large quantities and for long periods of time (up to 3 months). The experimentally injured C. orbicularis exuded gum after about a week. All Commiphora species were exploited, with the exception of Commiphora simplicifolia (daro sengatse), which exudes a very aromatic, white, resinous gum. Commiphora gums accounted for a minor part of the mouse lemur diet, possibly because they contain toxic terpenes, as suggested by their resinous smell. Commiphora gums are used as incense by local Tandroy people, who injure the trees to get the gum. In both the western deciduous forest (M. murinus) and the southern spiny forest (M. griseorufus), we observed mouse lemurs feeding on fallen Commiphora trees which exuded gum in exceptional abundance before they died. Such spectacular gum exudation was exploited by several individuals (up to four), often foraging together. We compared the short scale (nutritive content, quantity available locally) and large scale (spatial distribution and abundance) of fruits and gums. We did not find any difference in the nutritive content of gums and fruits (Table  6.2, t = 0.4, df=20, P = 0.7), nor did we observe any significant difference between the nutritive contents of gums of the spiny forest and the gums of the western deciduous forest (t = 0.5, df=10, P = 0.6). In fact, the chemical composition of gums is highly variable, with some gums (Alantsilodendron) being unexpectedly rich in proteins. Our observations suggest that gummivory in M. griseorufus does not involve any serious digestive challenge, although this point requires further investigation. Indeed, animals sometimes feed almost exclusively on gum for long periods. We never detected traces of gum in mouse lemur feces. The temporal distribution of foraging in the 26 radio-tracked individuals is represented in Fig. 6.1. It did not vary seasonally. A peak of gum foraging was observed in the first hours of the night. However, animals continuously alternated gum, fruit, and insect foraging throughout the night, suggesting that gum is rapidly assimilated. The higher attractiveness of fruits compared to gums is more likely to be due to their higher quantity than their higher quality. In Berenty the most important gum trees, Alantsilodendron, were small and often multi-trunked (height 4.5 ± 0.9  m, diameter 14 ± 6 cm, N = 30). They produced much lower quantities of food compared to fruiting trees (Table 6.3). We analysed the spatial distribution of 499 gum trees and 148 fruiting trees visited by the 26 radio-tracked animals. Fruiting trees were sparse and thus highly defendable, whereas gum trees were evenly distributed and abundant within the animals’ home ranges. Figure 6.2a indicates that gum trees were found in small dense patches, with the nearest gum-exuding neighbour always closer than 30 m, and usually closer than 10 m. In contrast, the nearest fruiting tree to a

134

F.G.S. Génin et al.

Fig. 6.1  Temporal frequency distribution of foraging on three kinds of food. Feeding events were recorded every 15 min over at least one complete night in 12 males and 14 females, and cumulated for the 26 individuals. We averaged values for individuals who were followed for several complete nights. Observations started when animals commenced their activity, and the duration of the night varied seasonally Table 6.3  Characteristics of gum and fruit trees exploited by M. griseorufus Gums Fruits 10 ± 0 m 32 ± 1 m Nearest neighbour food trees (N = 26) Quantity collected/day 0.172 ± 0.079 g dry gum/tree 2.7 ± 1.3 g dry pulp/tree Nutritive content (dry matter) 47 ± 6 kJ/100 g (5 species) 42 ± 6 kJ/100 g (10 species) Seasonality 6 spp./21b Dry season (N = 16) 10/30a trees a 17 spp./21b 16/30 trees Rainy season (N = 10) a Proportion of A. alluaudianum showing exudation b Ratio number of fruit species consumed/total number of known fruit tree species

given gum tree was most frequently found within a radius of 20 m, but often found at distances >30 m, and up to 150 m. Figure 6.2b indicates that fruiting trees were frequently found in more dispersed patches of radii »15  m. Moreover, gum trees were always closer than 50 m to a fruiting tree, and usually closer than 20 m.

Unpredictability of Rainfall: The Best Ecological Predictor for Gummivory In Berenty, food availability shows both high inter- and intra-annual variations (Génin 2008). We estimated the short-term (renewal), and long-term (seasonality) temporal variation of fruit and gum availability. Fruiting trees usually provided a rich, highly

6  Gummivory in Cheirogaleids

135

Fig. 6.2  Frequency distributions of the distances to the nearest visited fruiting tree or gum tree found away from all visited gum trees (a) N = 467 and fruiting trees (b) N = 148

localized resource for brief periods (Tarenna sp., Viscum sp., and Maerua filiformis), whereas a few species bore only small numbers of slow maturing fruits over a longer period (Maerua nuda and Phylloctenium decaryi). In contrast, Alantsilodendron gum appeared to flow for only a few days from one source, most gum flows being depleted after a week. From 11 trees out of 30, we collected on average 0.172 ± 0.079 g of dry gum on the first day, and only 0.012 ± 0.009 g after 7 days. However, new sources of gum appeared within the week of the experiment, explaining why animals tend to visit all potential trees systematically in a given area. While a fruiting peak was observed in the rainy season, gum availability showed little seasonal variation (Table  6.2). The insects causing gum exudation in Alantsilodendron trees probably breed seasonally (most observations were at the end of the rainy season), but gum availability did not show any clear seasonal variation (Table 6.3). At Berenty, although the duration of gum foraging was higher in the dry season, 16/30 Alantsilodendron trees exuded gum in the rainy season, 10/30 in the dry season, and 8/30 trees exuded gum in both the seasons. In fact, both in the southern spiny forest and the western deciduous forest, gum tended to dominate the diet of M. griseorufus and M. murinus, respectively, during dry periods (Génin 2003, 2008; Radespiel et  al. 2006). In other regions, lower seasonality of gummivory has been observed (Sauer and Sauer 1963; Charles-Dominique 1971; Doyle 1974; Bearder and Martin 1980). Further, gum trees are particularly abundant in the most climatically variable regions of Madagascar. For instance, 29 out of 37 species of Terminalia (Combretaceae) and all the species of Operculicarya (Anacardiaceae), Commiphora (Burseraceae), and Adansonia (Malvaceae) occur in the South, the West, and the extreme North

0.239–0.277 0.162 0.162 0.333 0.239–0.277 0.088–0.154

Major

0.080–0.104 0.047–0.294 0.080

Minor Major Major

Major? Null Null Null Major

0.104

Seasonal

0.116–0.233

0.131–0.163 0.259 0.259 0.068 0.131–0.163

0.275–0.320 0.111–0.249 0.275

0.320

Dammhahn and Kappeler (2008) Génin (2003) and Radespiel et al. (2006) Radespiel et al. (2006)

Seasonal Seasonal

Hypervariable

Unpredictable Predictable Predictable Predictable Unpredictable

Seasonal Hypervariable Seasonal

Génin (2008); this study

Biewbow, pers. com. Ganzhorn (1988) Atsalis (1999) Lahann (2007) Mittermeier et al. (2006)

Pagès (1980) Mittermeier et al. (2006) Charles-Dominique and Petter (1980)

Hladik et al. (1980)

Seasonal

Seasonal

References

Type of variability

ranges (arranged by main biogeographic domains) (based on

Constancy and contingency scale of 0–0.5. Low constancy indicates high seasonality (intra-annual variation) and low contingency indicates unpredictability (inter-annual variation). Taxonomy was according to Mittermeier et al. (2006)

East A. trichotis Cheirogaleus major Microcebus rufus M. murinus Phaner furcifer South M. griseorufus

Microcebus ravelobensis Mirza coquereli Phaner electromontis P. pallescens

Table  6.4  Gummivory in cheirogaleids and variability of rainfall within their geographic Dewar and Richard 2007) Constancy Contingency Genus Gummivory (intra-annual) (inter-annual) West Cheirogaleus Occasional 0.080–0.104 0.275–0.320 medius Microcebus Null 0.080 0.275 berthae M. murinus Seasonal 0.080–0.104 0.275–0.320

136 F.G.S. Génin et al.

6  Gummivory in Cheirogaleids

137

(Schatz 2001). Commiphora and Alantsilodendron are among the dominant tree ­genera of the southern xerophytic forests, and are widespread in the South (Alantsilodendron cinerea in the South-West). Moreover, Table  6.4 shows that, in cheirogaleids, gummivory is observed mainly in the most variable regions of Madagascar (for a phenological review see Bollen and Donati 2005). The west and the extreme north are characterized by marked seasonality with up to 8 months of drought (Kirindy). In the east, the low altitudes are more predictable, while high interannual variability of rainfall (unpredictability) is observed at higher altitude. The semi-arid South is characterized by both extreme seasonality and unpredictability. As a probable consequence of the geographic distribution of hypervariability in Madagascar, seasonal and occasional gummivores are mainly found in the west (Microcebus, Mirza and Cheirogaleus medius), while more specialized species are found in the south (M. griseorufus), in the west (P. pallescens), and in the east, at higher altitude (Phaner and Allocebus). In contrast, Microcebus rufus and Cheirogaleus major, which have wide distributions on the more predictable eastern coast, have never been reported to eat gum. Differences may also be observed among populations. For instance, the diet of M. murinus comprises a large proportion of gum during the dry season in the seasonal western deciduous forest (Kirindy and Ampijoroa: Génin 2003; Radespiel et al. 2006), and almost no gum in the more predictable evergreen forest of Mandena, in the south-east (Lahann 2007). In mammals, gummivory is only known in marsupials and primates living in regions in which El Niño oscillations provoke recurrent but unpredictable droughts. However, specialists also occur in more seasonal deciduous forests and in rainforests (Fig. 6.3).

Fig.  6.3  Geographic distributions of gummivorous mammals (families, genera for specialists), and zones experiencing El Niño-related droughts during the Northern summer or winter (from http://www.pmel.noaa.gov)

138

F.G.S. Génin et al.

Conclusion Gums are important resources for many cheirogaleids as well as other nocturnal strepsirhines. The classical traits associated with gummivory (large hands and feet, pointed nails, elongated tooth scraper, long tongue, and big caecum) have a mosaic expression in gummivorous taxa, suggesting they have evolved convergently in response to the pattern of gum exudation by the source trees (e.g. gouging adaptations to exploit trees that do not exude gum spontaneously; scraping adaptations to exploit trees that do). Mouse lemurs are reputed to feed on gum only occasionally, although recent studies suggest that gums are important resources for several mouse lemur species, at least seasonally (Génin 2003; Radespiel et  al. 2006). The reddish-grey mouse lemur (M. griseorufus), found in the most variable environment of Madagascar, appears to be the most specialized gummivore of this genus; all individuals feed on gum, whatever the season, and gum comprises, on an average, more than 75% of their diet. The animals feed on gum throughout the night, not only at the end of the foraging period. It therefore seems reasonable to assume that they are equipped to digest their primary food source. Further investigations on the digestibility and the possible toxicity of gums would clarify this issue. Despite the major role played by gum in their diet, M. griseorufus individuals apparently prefer fruit to gum, but as a rule, only dominant individuals (mainly females) have access to fruit (Génin, in press). There are several potential explanations for this preference. Greater digestibility of fruit seems unlikely, in light of the preponderance of gum in the diet. Fruit and gum also have very similar nutritive contents. Fruits differ from gums in that they present rich, highly localized and defendable resources; gums, by contrast, are scattered, limited in productivity, and difficult to defend. Alternatively, animals may simply prefer fruits for their better taste, perceptions of which usually have evolved to signal higher nutritive value. Since frugivores benefit the trees by aiding seed dispersal, the sweet taste of most fruits has been interpreted in terms of co-evolution between fruit producers and consumers (e.g. Martinez del Rio et al. 1992). Gums, by contrast, appear to be tasteless for O. crassicaudatus (Docherty et al. , Chap. 13), although this is a field that has yet to be explored. Gummivory is known to occur in two groups of mammals, i.e. marsupials and primates, and is clearly phylogenetically constrained. Both marsupials and nocturnal strepsirhines have been viewed as primitive, and as a consequence, the authors have explicitly or implicitly interpreted gummivory as an ancestral, nonspecialist diet (Nash 1986). However, our study suggests that gummivory evolved as an adaptation to environmental unpredictability (Fig. 6.3). Although natural selection is usually modelled as a constant directional force, rare and recurrent events that occur at unpredictable intervals, such as severe droughts, must generate strong selective effects, especially in populations showing high fluctuations in population density like M. griseorufus (Génin 2008). Indeed, most gummivores occur in highly seasonal deciduous forests and in regions which experienced recent droughts (Miocene) such as western Africa (Pickford and Senut 2000) (Fig. 6.3).

6  Gummivory in Cheirogaleids

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Acknowledgments  Fabien Génin thanks the Fondation Fyssen and the CNRS for funding; Jean and Henri de Heaulme for their welcome in Berenty and Analabe private reserves; and Annette Hladik, Njaka, Genevievy, Eden Rabeson, and Bruno Simmen for their help. Judith Masters’ research is funded by the National Research Foundation under Grant number 2053615. Any opinion, findings, and conclusions or recommendations expressed in this material are those of the authors, and the NRF does not accept any liability in regard thereto. She thanks the following curators and collections managers for access to their collections: Drs Darrin Lunde (AMNH, New York), Suzanne MacLaren (CMNH, Pittsburgh), William Stanley (FMNH, Chicago), Christiane Denys (MNHN, Paris), Paula Jenkins (NHM, London), and Marc Herremanns and Wim Wendelin (RMCA, Tervuren). Joerg Ganzhorn’s research was funded by the DFG/BMZ (Ga 342/14-1) and carried out under the Accord de Collaboration between ANGAP (now Madagascar National Parks), the Département Biologie Animale of the Université d’Antananarivo, and the Department of Biology, Hamburg University. He thanks Professors Olga Ramilijaona and Daniel Rakotondravony for their help at various stages of the study.

References Atsalis, S 1999. Diet of the brown mouse lemur (Microcebus rufus) in Ranonamafana National Park, Madagascar. Int J Primatol 20:193–229 Bearder, S.K. Martin, R.D 1980. Acacia gum and its use by bushbabies, Galago senegalensis (primates: lorisidae). Int J Primatol 1(2):103–128 Bollen, A. van Elsacker, L. and Ganzhorn J.U 2004. Tree dispersal strategies in the littoral forest of Sainte Luce (SE-Madagascar). Oecologia 139:604–616 Bollen, A. Donati, G 2005. Phenology of the littoral forest of Sainte Luce, Southeastern Madagascar. Biotropica 37:32–43 Charles-Dominique, P 1971. Eco-ethologie des Prosimiens du Gabon. Biol Gabon 7:121–228 Charles-Dominique, P. Petter, J.J 1980. Ecology and social life of Phaner furcifer. In CharlesDominique P, Cooper H.M, Hladik A et  al. (eds) Nocturnal Malagasy primates: ecology, physiology and behaviour. Academic, New York Coimbra-Filho, A.F. Mittermeier, R.A 1976. Exudate-eating and tree-gouging in marmosets. Nature 262:630 Dammhahn, M. Kappeler, P.M 2008. Comparative ecology of sympatric Microcebus berthae and M. murinus. Int J Primatol 29(6):1567–1590 Dewar, R.E. Richard, A.F 2007. Evolution in the hypervariable environment of Madagascar. PNAS 104:13723–13727 Doyle, GA 1974. The behavior of the lesser bush-baby (Galago senegalensis moholi). In Martin RD, Doyle GA, Walker AC (eds) Posimian biology. University of Pittsburg Press, Pittsburgh Docherty, B.A. Alport, L.J. Bhatnagar, K.P. Burrows, A.M. and Smith, T.D 2010. Tongue morphology in infant and adult bushbabies (Otolemur spp.). In Burrows AM, Nash LT (eds) The evolution of exudativory in primates. Springer, New York Ganzhorn, J.U 1988. Food partitioning among Malagasy primates. Oecologia 75:436–450 Génin, F. 2008. Life in unpredictable environments: first investigation of the natural history of Microcebus griseorufus. Int J Primatol 29:303–321 Génin, F 2003. Female dominance in competition for gum trees in the grey mouse lemur. Rev Ecol 58:397–410 Génin, F (in press) Venus in furs: female power in mouse lemur Microcebus murinus and M. griseorufus. In Masters J.C, Gamba M, Génin F (eds) Leaping ahead: advances in prosimian studies. Springer, New York Génin, F. Perret, M 2003. Daily hypothermia in captive grey mouse lemurs (Microcebus ­murinus): effects of photoperiod and food restriction. Comp Biochem Physiol B 136:71–81 Heymann, E.W. Smith, A.C 1999. When to feed on gums: temporal patterns of gummivory in wild tamarinds, Saguinus mystax and Saguinus fuscicollis (Callitrichinae). Zoo Biol 18:459–471

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Hill, W.C.O. Rewell, R.E 1948. The caecum of primates: its appendages, mesenteries and blood supply. Trans Zool Soc London 26(3):199–254 Hladik, C.M. Charles-Dominique, P. and Petter, J.J 1980. Feeding strategies of five nocturnal prosimians in the dry forest of the west coast of Madagascar. In Charles-Dominique P, Cooper HM, Hladik A et al. (eds) Nocturnal Malagasy primates: ecology, physiology and behaviour. Academic, New York Isbell, L.A 1998. Diet for a small primate: insectivory and gummivory in the (large) patas monkey (Erythrocebus patas pyrrhonotus). Am J Primatol 45:381–398 Lahann, P 2007. Feeding ecology and seed dispersal of sympatric cheirogaleid lemurs (Microcebus murinus, Cheirogaleus medius, Cheirogaleus major) in the littoral rainforest of south-east Madagascar. J Zool 271:88–98 Lemelin, P. Jungers, W.L 2007. Body size and scaling of the hands and feet of prosimian primates. Am J Phys Anthropol 133:828–840 Lindenmayer, D 2002. Gliders of Australia: a natural history. UNSW Press, Sydney Martinez del Rio, C. Baker, H.G. and Baker, I 1992. Ecological and evolutionary implications of digestive processes: bird preferences and the sugar constituents of floral nectar and fruit pulp. Experientia 48:554–561 Masters, J.C. Brothers, D.J 2002. Lack of congruence between morphological and molecular data in reconstructing the phylogeny of Galagonidae. Am J Phys Anthropol 117:79–93 Masters, J.C. Rayner, R.J 1993. Competition and macroevolution: the ghost of competition yet to come? Biol J Lin Soc 49:87–98 Meier, B. Albignac, R 1991. Rediscovery of Allocebus trichotis Günther 1875 (primates) in northeast Madagascar. Folia Primatol 56:57–63 Mittermeier, R.A. Konstant, W.R. Hawkins, F.E. Louis, E.E. Langrand, O. Ratsimbazafy, J. Rasoloarison, R. Ganzhorn, J.U. Rajaobelina, S. Tattersall, I. and Meyers, D.M 2006. Lemurs of Madagascar. Second edition. Conservation International, Washington, DC Nash, L.T 1986. Dietary, behavioral, and morphological aspects of gummivory in primates. Yearb Phys Anthropol 29:113–137 Pagès, E 1980. Ethoecology of Microcebus coquereli during the dry season. In Charles-Dominique P, Cooper H.M, Hladik A et al. (eds) Nocturnal malagasy primates: ecology, physiology and behavior. Academic, New York Peres, C.A 2000. Identifying keystone plant resources in tropical forests: the case of gums from Parkia pods. J Trop Ecol 16:287–317 Petter, J. Albignac, R. and Rumpler, Y 1977. Mammifères Lémuriens (Primates Prosimiens). Faune de Madagascar, vol 44. ORSTOM CNRS, Paris Pickford, M. Senut, B 2000. Geology and palaeobiology of the Namib desert Southwestern Africa. Ministry of Mines and Energy, Windhoek. Memoir 18, vol 1, Geological survey of Namibia Radespiel, U. Reimann, W. Rahelinirina, M. and Zimmermann, E 2006. Feeding ecology of sympatric mouse lemur species in northwestern Madagascar. Int J Primatol 27:311–321 Rasoloarison, R.M. Goodman, S.M. and Ganzhorn, J.U 2000. Taxonomic revision of mouse lemurs (Microcebus) in the western portions of Madagascar. Int J Primatol 21:963–1019 Sauer, E.G.F. Sauer, E.M 1963. The southwest African bush-baby of the Galago senegalensis group. J Southwest Afr Sci Soc 16:5–35 Schatz, G.E 2001. Generic tree flora of Madagascar. Royal Botanic Gardens, Kew and Missouri Botanical Garden, London Stephenson I.R. Bearder S.K. Donati G. and Karlsson, J 2010. A guide to galago diversity: getting a grip on how best to chew gum. In Burrows A.M, Nash L.T (eds) The evolution of exudativory in primates. Springer, New York Tan, C.L. Drake, J.H 2001. Evidence of tree gouging and exudate eating in pygmy slow loris (Nycticebus pygmaeus). Folia Primatol 72:37–39 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, C.J. Wall, C.E. Williams, S.H. and Hylander W.L 2003. Comparative functional analysis of skull morphology of tree-gouging primates. Am J Phys Anthropol 120:153–170

Chapter 7

Seasonality in Gum and Honeydew Feeding in Gray Mouse Lemurs Marine Joly-Radko and Elke Zimmermann

Abstract  Exudates represent an important component of the natural diets of s­ mall-bodied primates. For mouse lemurs, the impact of forest type and seasonal predictability on gum consumption has recently been intensively investigated. The goal of our study was to extend our knowledge regarding the seasonality of feeding ecology of Microcebus murinus, first, to investigate the relative consumption of gum and hemipteran honeydew, a sap-derived product, and, second to assess respective foraging strategies in a highly seasonal and quite predictable environment. We hypothesized that (1) food resources vary according to the season, (2) gum and honeydew represent keystone food resources during periods of food scarcity, and (3) lemurs revisit productive stationary feeding sites during the period of food scarcity. We studied gray mouse lemurs in the dry deciduous ­forest of the Ankarafantsika National Park in northwestern Madagascar. We radiocollared seven M. murinus females and performed focal observations on their feeding behavior during the end of the dry and the beginning of the rainy season. During the dry season, the period of food scarcity, mouse lemurs mainly consumed gum and honeydew. Subjects revisited the same feeding sites within the same and over several nights. During the rainy season, the period of food abundance, lemurs consumed mainly nectar from shrub flowers and did not show gum or honeydew feeding. To our knowledge, the consumption of honeydew by lemurs is a unique case of sap feeding by proxy in a mammal. Further investigations will focus on the characterization of the ecological consequences of such an interaction between mouse lemurs, hemipteran larvae, and host plants.

M. Joly-Radko (*) Institut fuer Zoologie, Tieraerztliche Hochschule Hannover, Buenteweg 17, Hannover 30559, Germany 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_7, © Springer Science+Business Media, LLC 2010

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Introduction Exudates represent an important food category in the natural diet of small-bodied ­primates (Nash 1986). Exudate is a global term under which one may distinguish different plant fluids as resin, latex, gum, and sap (Bearder and Martin 1980). Resin and latex may be highly poisonous, pose digestibility challenges, and have not yet been reported to be consumed by primates. Exuded gums and saps are often consumed by primates. Gum is produced by a tree when parasitized or damaged. Sap is transported by living phloem cells, the innermost layer of the tree bark and living tissue to all parts of the tree. Feeding on both of those plant fluids involves different challenges and advantages according to their nature (Nash 1986). Accessibility is variable but gums have the advantages that trees actively produce it in response to insect or mechanical damage. It is easily accessible for all arboreal animals. Saps which circulate in the innermost part of the tree can only be consumed after breakage or after efficient extraction. Numerous studies report gum consumption in primates, and especially among ­callithrichines and nocturnal strepsirhines (Coimbra-Filho and Mittermeier 1976; Ramirez et al. 1977; Heymann and Smith 1999; Petter et al. 1971; Charles-Dominique and Petter 1980; Pagès 1980; Bearder and Martin 1980; Nash 1986). Among these gummivorous species, two categories can be distinguished: (1) species that are able to incise the bark of a tree and hence elicit the flow of gum and sap and (2) species that feed by licking or scraping and prising exudate that is already secreted and present on the surface of a bark from a tree. Without dental specializations enabling incising into tree bark, it is almost impossible to exploit sap directly. However, behavioral ­adaptations may enable primates to exploit sap. Sap utilization is actually rarely reported in the animal kingdom. Only one group, insects of the Order Hemiptera, includes species that use sap as their dominant dietary component. All Hemiptera are plant feeders, with mouthparts adapted for sucking plant sap from a wide assortment of trees and wild and cultivated plants. Many of them cause injuries or destruction to plants, including fruit trees and grain crops (Wilson 2005). These species have symbiotic micro-organisms in their guts which enable the digestion and assimilation of the nutrients contained in the sap. After digestion and assimilation of ingested sap by the hemipteran gut, the residue is voided via the anus as honeydew, which is often produced in copious amounts. Honeydew is used as food by various animals which can be considered as secondary, proxy sap feeders (Douglas 2006) or cryptic herbivores (Hunt 2003) that exploit the capacity of hemipterans to access plant products. Many invertebrates, including ants, flies, wasps, bees, and butterflies, as well as vertebrates like nectarivorous birds and geckos (Fölling et al. 2001) consume honeydew that has fallen onto plants or other surfaces. Feeding on honeydew depends on its production which can vary seasonally, temporally, and with prevailing weather, but which also may offer a high energy resource during harsh periods of food scarcity. For instance, honeydew is by far the most abundant nectar-like resource in New Zealand’s beech forest which is infested by scale insects. The kaka parrot, Nestor

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meridionalis meridionalis, can obtain its daily energy requirement by feeding on honeydew for about 3 h (Beggs and Wilson 1991). The flatid planthopper, Phromnia rosea (Order: Hemiptera; Suborder: Auchenorrhyncha; Superfamily: Fulgoroidea; Family: Flatidae), is endemic to Madagascar (see Fig. 7.1). To our knowledge, no clear geographical distribution of this insect has yet been described and it may be a synonym of Flatida coccinea described in the literature (Hladik et al. 1980, ongoing estimation). These insects are nocturnal, living in large colonies, and feeding on the sap of vines (Hladik et  al. 1980). Secretions are produced in a liquid form which drops onto leaves and stems. Animals lick or scrape these secretions directly from the vegetation. White wax produced by the hemipteran larvae often abundantly covers the vegetation below the flatid colony. Previous published nutritional analysis showed that honeydew contains a high sugar concentration, but is poor in protein content (Hladik et al. 1980). Mouse lemurs (Microcebus spp.) are small-bodied nocturnal lemurs that are endemic to Madagascar. Sixteen species have been described to date (Olivieri et al. 2007; Radespiel et  al. 2008). Mouse lemurs inhabit all forest habitats (Radespiel 2006). Microcebus murinus (J.F. Miller, 1777), the gray mouse lemur, is the most widespread species. Its distribution ranges from the north-western dry deciduous forest to the spiny forest in southeastern areas (e.g., Mittermeier et al. 2008; Olivieri et al. 2007). It was first described as a solitary foraging omnivore which “occasionally and opportunistically” consumes exuded gums (Martin 1973). It also feeds on insects, fruits, seeds, and leaves (Hladik et  al. 1980; Martin 1973; Radespiel et  al. 2006). Mouse lemurs are not able to gouge, but collect exuded tree gum by licking and by scraping the bark with the tooth comb. Mouse lemurs are also seen on vines infested by flatid bugs, licking the honeydew secreted by the larvae (Corbin and Schmid 1995). During periods of food scarcity in highly seasonal environments, when foods such as fruits and nectar are absent or less abundant, gum and hemipteran larvae honeydew may represent keystone resources (Génin 2003; Radespiel et  al. 2006; Joly and Zimmermann 2007; Dammhahn and Kappeler 2008). However, no systematic

Fig. 7.1  An hemipteran larva of a flatid bug (a). An aggregate of larvae (b) during the dry season in the National Park of Ankarafantsika

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i­nvestigation of the seasonality of diet has been performed to evaluate the relative importance of these food resources for the survival of M. murinus evolving in different forest types and climate conditions. The goal of this study was thus (1) to assess exudate and honeydew consumption during the dry and the rainy seasons at a geographical location marked by a strong seasonality, (2) to investigate the relative consumption of gum and honeydew across seasons, and (3) to assess foraging strategies when mouse lemurs feed on exudates. We hypothesized that food resource use would vary according to season, that gum and/or honeydew represent keystone food resources during a period of scarcity, and that lemurs revisit productive feeding sites.

Material and Methods Study Site and Climate Conditions We conducted this study during two consecutive late dry seasons (August–October 2005 and August–October 2006) and the beginning of a rainy season (December 2006–January 2007) in the Ampijoroa Forestry Reserve (64,300  ha) in the dry deciduous forest of the Ankarafantsika National Park in northwestern Madagascar, 110 km south of Mahajanga. The climate is strongly seasonal with a cool, dry ­season from May to October and a hot, rainy season from November to April, with heavy rains in January and February (Schmelting et al. 2000, see Fig. 7.2 for ­climatic data in 2005 and 2006). The mean temperature throughout the year usually fluctuates around 27°C with a maximum average temperature of 37°C in October–November and a minimum average temperature of 16°C in June–July (Schmelting et al. 2000,

Fig.  7.2  Climatic data at Ampijoroa station in the Ankarafantsika National Park in 2005 and 2006. Monthly rainfall (bars), average monthly mean temperature (plain line), minimal ( filled circles), and maximal temperatures (open circles) are represented

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see Fig. 7.2 for 2005 and 2006). Precipitation has a yearly mean of 1,100–1,600 mm (the annual precipitation was 1,337 mm in 2005 and 1,360 mm in 2006). We worked in a 30.6 ha forest patch, Jardin Botanique A (JBA; 16°19¢S 46°48¢E), with a rectangular grid trail system allowing spatial orientation in the forest.

Focal Observation and Analysis In 2005, during a routine monthly capture session (Rendigs et al. 2003) a total of five females of M. murinus were captured and equipped with radiocollars (TW4, Biotrack, UK). In 2006, we recaptured and radiocollared two females of the previous year and radiocollared two new females. A total of seven individuals were thus radiocollared across the whole study period. With the help of a portable receiver and an antenna (TR-4 with RA-14K antenna; Telonics Inc, Mesa, AZ), we followed each animal during six consecutive nights between dusk (about 6 p.m.) and midnight (12 p.m.). With a dictaphone, we collected behaviors ad libitum, i.e., by continuously recording the start and end of each behavior bout, according to the focal-animal sampling method (Altmann 1974). The following behavioral categories were recorded: Feeding = an animal ingests a food item, Resting = an animal does not move or sleeps, Locomotion =  an animal being in motion, Social interaction = an animal was interacting affiliatively (with another adult congener or during infant care) or agonistically with another congener, and Unknown = it was impossible for the observer to determine the activity of an animal. Additional information was collected concerning the feeding activity. We noted (1) the feeding duration using a chronometer, (2) the food category, and (3) the position of a feeding site with a Global Positioning System (Magellan GPS, Explorist 100; World Geodesic System 84; mean error £ 10 m). We recorded the following major food categories: gum, honeydew, insect, nectar, flower, fruit, seed, and unknown food item. A mouse lemur was considered to be feeding on gum when it was observed biting or licking the stem of trees, on hemipteran larvae secretions when licking the leaves and branches where larvae were present, and on animal prey when chasing, catching, and eating the respective animal item. We recorded nectar, flower, fruit, and seed eating when an animal was seen licking nectar or eating flowers, fruits, and seeds. Unknown food item was recorded when it was impossible for the observer to determine an eaten food item. Each feeding site, defined as a site where the animal stopped to eat one of the items described above, was individually marked with a flag. A site was defined as revisited when it was visited more than once and on different nights. The sleeping site was localized radiotelemetrically during the daytime. Sleeping trees were also individually marked with a flag, and their spatial position determined by GPS coordinates.

Data and Statistical Analysis To calculate an activity budget for each animal for each season, we defined as ­contact time the total period during which we had visual contact with the focal animal.

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For each behavioral category (feeding, resting, locomotion, social interaction, and unknown behavior), we calculated the total duration for each animal. The activity budget was established by calculating the percentage of time an animal spent in each category in relation to the total contact time. We calculated the percentage of feeding time each animal spent eating each food item (gum, honeydew, insect, nectar, flower, fruit, seed, and unknown food item). For that purpose, we divided the total duration eating a food item by the total time spent feeding for each animal. Descriptions are presented as means across subjects (and ranges). In total, we followed mouse lemurs for 275 h during the dry season and 70 h during the rainy season. We pooled the data for both dry seasons together. For the two females that were followed during both dry seasons, we calculated an average over the both periods. During the dry seasons, we followed a total of seven females. The behavioral observations were possible in 56.5% (range 45.9–75.5%) of the time an animal spent outside the nest. During the rainy season we lost two females because of predation or emitter defects. Contact time decreased to 35.2% (range 32.2–36.1%), because of heavy rain and dense foliage, which greatly reduced visibility of the focal individual. To evaluate the location of feeding sites within home ranges of each animal for each season, we used the spatial coordinates given by the GPS of a minimum of 50 independent points, i.e., location of the animal recorded every 30  min, plus the additional feeding sites and sleeping sites where animals were observed. We performed calculations using Animal Movement Software (Hooge et  al. 1999) for Arcview GIS 3.3 (ESRI) using the Minimum Convex Polygon method. The statistical tests were performed using Statistica 6.0.

Results Activity Budget During the Dry and Rainy Season During the dry season, mouse lemurs (N = 7) mostly fed and rested (Fig.  7.3). Feeding activity represented 54.2% (range 21.7–71.2%) and resting 41.2% (range 19.7–68.9%) of the total contact time. The individuals showed lower locomotor activity (9.1% range 4.5–13.5%) than in the rainy season. During the rainy season, mouse lemurs (N = 3) fed less than in the dry season (27.5% of the time; range 23.3–37.1%). Their time in locomotion was 20.8% (range 19.7–28.6%) and resting was 17.1% (range 8.8–41.6%) of the contact time.

Food Items Consumed During the dry season, mouse lemurs spent most of the time feeding on honeydew (49.8%; range 0.0–71.8%) and gum (43.0%; range 22.9–89.8%; Friedman test,

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Fig. 7.3  Activity time budget during the dry and the rainy season

c2 = 36.7, N = 7, p < 0.00001; Wilcoxon test, N = 7, p < 0.05; see Fig. 7.4a). Mouse lemurs were never observed feeding directly on the hemipteran larvae. They fed on honeydew by licking the substrate where there were larvae or by picking up dead leaves covered by honeydew from the ground and transporting them up to a higher position in the vegetation to lick the sugar-rich nutrient. We observed great inter-individual variability in feeding time devoted to honeydew: three individuals spent 5.5% (range 0–8.5%) on this food item, whereas the other four individuals spent 57.8% (range 49.8–71.8%). Animals that spent more time on honeydew foraged within 100 m of the forest edge, in the eastern part of the study area (Fig. 7.5). The foraging area of the three other individuals was situated in the inner part of the forest (Fig. 7.5). During the rainy season, we observed a shift in the diet of the focal individuals (N = 3). No plant exudate or honeydew consumption was recorded. The subjects spent most of the time feeding on nectar (56.0%; range: 35.1–89.3%) and insects (21.8%; range: 3.9–53.5%; Fig. 7.4b). During our observations, mouse lemurs collected nectar from only one species of tree, identified as belonging to the endemic genus Evonymopsis (Family Celastraceae). The nectar largely covered the disc of the flower. It was transparent and very smelly.

Usage of Gum and Honeydew Sites We investigated the use of gum and honeydew sites during the dry season. Each female (N = 7) visited 25 gum trees (range: 10–37) over the six observation nights

Fig. 7.4  Consumed food items during the dry (a) and the rainy season (b)

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Fig. 7.5  Honeydew consumption and distribution of the home ranges in the study area. Shaded areas were ranges used by females which used more honeydew and white areas were inhabited by females which used mostly gum. Hatched area is forest edge

and revisited 24.3% of these trees (range: 13.7–46.2%) with a frequency of 3.2 visits (range 2.7–7.4) across six nights. The focal animals spent 73.0% (range: 38.87–80.5%) of the gum feeding time on these revisited trees. Six females were observed consuming honeydew and they used 8.5 (range 3–29) different honeydew sites during the six observation nights. Four females revisited honeydew sites (30.3% of the sites, range 27.3–100%). They visited these sites 4.6 times (range 3.4–6) in six nights. They spent 67.6% (range 63.8–96.9%) of the honeydew feeding time on these revisited honeydew sites.

Discussion During the dry season, female gray mouse lemurs at Ampijoroa directed their foraging activity mainly on gum trees and sites where honeydew from hemipteran larvae was available. Focal animals exploited some of the sites repeatedly, revisiting them over several nights and spending most of their time feeding on these particular trees. During the rainy season, mouse lemurs shifted their diet. In December and January, they mainly fed on the nectar of shrub flowers and did not feed on gum and honeydew. Exuded gum and sap-derived honeydew thus ­represented keystone food

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resources for these small-bodied nocturnal primates during periods of seasonal food scarcity in a high seasonal and predictable environment. Our subjects showed great inter-individual variability in honeydew vs. gum consumption. The diets of mouse lemurs may be influenced by the abundance of food items in their foraging area. The distribution of gum trees may be more or less clumped depending on the species (Nash 1986). In our study area, gray mouse lemurs fed on at least 12 different species of gum trees (see a table of the plant species in Radespiel et al. 2006). In a similar dry deciduous forest (Kirindy), Génin (2003) showed that gum trees from five different species were quite evenly distributed in the forest. Honeydew sites seem, however, to be patchily distributed, mainly depending on the presence of a forest edge. Corbin and Schmid (1995) found a significant difference in the area covered by insect honeydew between the forest edge (within 100 m) and the interior of the forest. The larvae of the flatid bug, that produce the honeydew, actually tend to infest a particular plant species Elachyptera minimiflora (Hladik et al. 1980). This plant species mostly occurred in degraded or disturbed areas and logging increased its density (Chouteau 2004). These reports support our observations. We observed that mouse lemurs foraging within 100 m of the forest edge spent more time feeding on honeydew than gum. In our 30-ha study area, the distribution of honeydew sites may be unequal and may affect the food availability for mouse lemurs. If we consider that gum trees are evenly distributed in our study area and honeydew sites are only present in the forest edge, our focal animals in the forest edge seem to prefer spending time feeding on honeydew vs. gum when both are available. M. murinus occurs in different forest types (for overview see Radespiel 2006). Our results on seasonal gummivory in M. murinus partly coincided with data collected during the same year, 2005, in a western dry deciduous forest, Kirindy (Dammhahn and Kappeler 2008). Although our data collection schedule differed from the latter study (we collected data during the core period of the rainy season instead of the late rainy season), gummivory in M. murinus from Kirindy was also found seasonal. Mouse lemurs used gum mostly during the dry season and the least during the transition between dry and rainy season. Interestingly, the authors reported highest usage of honeydew during this same transition period. To our knowledge no study assessed the activity pattern of flatid bugs larvae yet. However, this would be essential in order to assess the honeydew availability in the different study areas. From personal anecdotal field observations in Ampijoroa, the presence of flatid bug larvae was recorded until the first heavy rainfalls (end October– November). Colorful pink and winged imagos emerged and dispersed at this period. Gray mouse lemurs living in Mandena, a rainforest in south-east Madagascar, mainly relied on fruits, flowers, and arthropods during the rainy season, the period of food abundance (Lahann 2007). In this study, mouse lemurs only spent 4% of the feeding events on gum. During the dry season, mouse lemurs enter in torpor in Mandena, there is unfortunately no possibility to have information on seasonal diet, i.e., variation in gummivory or report on honeydew feeding in this study area. Few reports on gummivory and honeydew feeding of the 16 other mouse lemurs species are available so far. Dammhahn and Kappeler (2008) found that Madame Berthe’s mouse lemur, the smallest mouse lemur species, mostly relied on ­honeydew

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and animal matter all over the year, whereas gummivory was the highest during the dry season. M. berthae’s diet was thus not as seasonal as M. murinus’s in Kirindy. Génin (2008) demonstrated that M. griseorufus, living in the Berenty Private Reserve, a dry spiny forest of southern Madagascar with highly unpredictable climate condition, did feed on gum during period of droughts. Honeydew feeding was not mentioned in the latter study, but Génin mentioned that “the two most important categories of food” are gum and fruits. Flatid bugs seem to be, however, present in the Berenty reserve since Jolly et al. (2006) observed Lemur catta feeding on larvae secretions. Again, geographical distribution of flatid bugs and their activity pattern is needed to gain insight into a comparative feeding ecology in the different mouse lemur species. In contrast, mouse lemurs living in rainforest habitats seem to be mostly frugivorous and insectivorous (M. rufus, see Atsalis 2008). Sap feeding by proxy, i.e., honeydew feeding, was mainly described in invertebrates (for review, see Delabie 2001; Douglas 2006; Gullan 1997). In vertebrates, mainly birds and geckos have been observed using honeydew as food resource (birds: see Edwards 1982; Gaze and Clout 1983; Greenberg et al. 1993; Latta et al. 2001, geckos: Fölling et  al. 2001). Tending behavior is observed when animals elicit the excretion of droplets by a hemipteran. This exceptional behavior was mostly described for ants (for review, see Delabie 2001) but also for geckos (Fölling et  al. 2001). The close interaction between ants and sap-sucking insects was referred as trophobiosis (Hölldobler and Wilson 1990) and indicated a mutualistic relationship (see Delabie 2001). Ants feed on honeydew which contains high concentration of sugar. Ant attendance benefits hemipteran by deterring predators and parasitoids. Ants remove the honeydew which can serve as a substrate for sooty mould and perhaps fungi. However, whereas interactions between ants and sapsucking insects are abundant, their ecological consequences are yet poorly known (for a review see Styrsky and Eubanks 2007). Further investigations are needed for characterising the relationship between the vertebrate users of honeydew and hemipterans. Anecdotes reported that other lemurs (Lemur catta in Jolly et al. 2006, all lemurs in the Kirindy forest in Corbin and Schmid 1995), feed on honeydew. To our knowledge, lemurs seem to be the only mammals using honeydew as a food resource. Whether lemurs demonstrate a tending behavior and to what extent this relationship may be mutualistic and have ecological consequences on the local environment remains unanswered. Future studies should focus on the ecological factors that influence the consequences of honeydew-user/sap-sucking insects to provide greater insight into the role of species interactions in food web dynamics. Acknowledgments  We thank the Commission Tripartite of the Malagasy government, the Département des Eaux et Forêts, and the Association pour la Gestion des Aires for their permission to work in Ampijoroa. We also thank Dr. Daniel Rakotondravony, Faculté des Sciences, Université d’Antananarivo for logistic support. We thank the Durrell Wildlife Preservation Trust for the climatic data. For help in plant identification, we thank Hiroki Sato, University of Kyoto, Japan. For assistance in the field, we thank Dr. Blanchard Randrianambinina, Dr. Solofo Rasoloharijaona, Dr. Marina Scheumann, and Christian Schopf. The study complies with the current laws of Madagascar and was financially supported by the DAAD and financial support for women from the University of Veterinary Medicine Hannover.

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References Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267 Atsalis S (2008) A natural history of the brown mouse lemur. Prentice Hall, Upper Saddle River, NJ Bearder SK, Martin RD (1980) Acacia gum and its use by bushbabies, Galago senegalensis (Primates: Lorisidae). Int J Primatol 1:103–128 Beggs JR, Wilson PR (1991) The kaka Nestor meridionalis, a New Zealand parrot endangered by introduced wasps and possums. Biol Cons 56:23–38 Charles-Dominique P, Petter JJ (1980) Ecology and social life of Phaner furcifer. In: CharlesDominique P, Cooper HM, Hladik A, Hladik CM, Pages E, Pariente GF, Petter-Rousseaux A, Petter JJ, Schilling A (eds) Nocturnal Malagasy primates. Academic, New York Chouteau P (2004) The impacts of logging on the microhabitats used by two species of couas in the western forest of Madagascar. C R Biologies 327:1157–1170 Coimbra-Filho AF, Mittermeier RA (1976) Exudate-eating and tree-gouging in marmosets. Nature 262:630 Corbin GD, Schmid J (1995) Insect secretions determine habitat use patterns by a female lesser mouse lemur (Microcebus murinus). Am J Primatol 37:317–324 Dammhahn M, Kappeler PM (2008) Comparative feeding ecology of sympatric Microcebus berthae and M. murinus. Int J Primatol 29:1567–1589 Delabie JHC (2001) Trophobiosis between Formicidae and Hemiptera (Sternorrhyncha and Auchenorrhyncha): an overview. Neotrop Entomol 30:501–516 Douglas AE (2006) Phloem-sap feeding by animals: problems and solutions. J Exp Bot 57:747–754 Edwards EP (1982) Hummingbirds feeding on an excretion produced by scale insects. Condor 84:122 Fölling M, Knogge C, Bohme W (2001) Geckos are milking honeydew-producing planthoppers in Madagascar. J Nat Hist 35:279–284 Gaze PD, Clout MN (1983) Honeydew and its importance to birds in beech forests of South Island, New Zealand. N Z J Ecol 6:33–37 Génin F (2003) Female dominance in competition for gum trees in the grey mouse lemur Microcebus murinus. Rev Ecol (Terre Vie) 58:397–410 Génin F (2008) Life in unpredictable environments: first investigation of the natural history of Microcebus griseorufus. Rev Ecol (Terre Vie) 58:397–410 Greenberg R, Caballero CM, Bichier P (1993) Defense of Homopteran honeydew by birds in the Mexican highlands and other warm temperate forests. Oikos 68:519–524 Gullan PJ (1997) Relationships with ants. In: Ben-Dov Y, Hodgson CJ (eds) Soft scale insects – their biology, natural enemies and control. Elsevier Science B.V., Amsterdam 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 JJ (1980) Feeding strategies of five nocturnal prosimians in the dry forest of the west coast of Madagascar. In: Charles-Dominique P, Cooper HM, Hladik A, Hladik CM, Pages E, Pariente GF, Petter-Rousseaux A, Petter JJ, Schilling A (eds) Nocturnal Malagasy primates. Academic, New York Hölldobler B, Wilson EO (1990) The ants. The Belknap Press of the Harvard University Press, Cambridge, MA Hooge PN, Eichenlaub B, Solomon E (1999) The animal movement program. Version ver. 1.1. USGS, Alaska Biological Science Center, Anchorage Hunt JH (2003) Cryptic herbivores of the rainforest canopy. Science 300:916–917 Jolly A, Sussman RW, Koyama N, Rasamimanana H (2006) Ringtailed lemur biology. Springer, New York Joly M, Zimmermann E (2007) First evidence for relocation of stationary food resources during foraging in a strepsirhine primate (Microcebus murinus). Am J Primatol 69:1045–1052

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Lahann P (2007) Feeding ecology and seed dispersal of sympatric cheirogaleid lemurs (Microcebus murinus, Cheirogaleus medius, Cheirogaleus major) in the littoral rainforest of south-east Madagascar. J Zool 271:88–98 Latta SC, Gampedr HA, Tietz JR (2001) Revising the convergence hypothesis of avian use of honeydew: evidence from Dominican subtropical dry season. Oikos 93:250–259 Martin RD (1973) Comparative ecology and behaviour of primates. In: Michael RP, Crook JH (eds) A review of the behaviour and ecology of the lesser mouse lemur (Microcebus murinus). Academic, London Mittermeier RA, Ganzhorn JU, Konstant WR, Glander K, Tattersall I, Groves CP, Rylands AB, Hapke A, Ratsimbazafy J, Mayor MI, Louis EE, Rumpler Y, Schwitzer C, Rasoloarison RM (2008) Lemur diversity in Madagascar. Int J Primatol 29:1607–1656 Nash LT (1986) Dietary, behavioral, and morphological aspects of gummivory in primates. Am J Physic Anthr 29:113–137 Olivieri G, Randrianambinina B, Rakotondavony D, Zimmermann E, Radespiel U (2007) The ever-increasing diversity in mouse lemurs: three new species in north and northwestern Madagascar. Mol Phyl Evol 43:309–327 Pagès E (1980) Ethoecology of Microcebus coquereli during the dry season. In: CharlesDominique P, Cooper HM, Hladik A, Hladik CM, Pagès E, Pariente GF, Petter-Rousseaux A, Petter JJ, Schilling A (eds) Nocturnal malagasy primates. Academic, New York Petter JJ, Schilling A, Pariente G (1971) Observations éco-éthologiques sur les deux lémuriens malgaches nocturnes: Phaner furcifer et Microcebus coquereli. La Terre et la Vie 25:287–327 Radespiel U (2006) Ecological diversity and seasonal adaptations of mouse lemurs (Microcebus spp.). In: Gould L, Sauther ML (eds) Lemurs: ecology and adaptation. Springer, New York Radespiel U, Reimann W, Rahelinirina M, Zimmermann E (2006) Feeding ecology of sympatric mouse lemur species in Northwestern Madagascar. Int J Primatol 27:311–321 Radespiel U, Olivieri G, Rasolofoson DW, Rakotondratsimba G, Rakotonirainy O, Rasoloharijaona S, Randrianambinina B, Ratsimbazafy JH, Ratelolahy F, Randriamboavonjy T, Rasolofoharivelo T, Craul M, Rakotozafy L, Randrianarison RM (2008) Exceptional diversity of mouse lemurs (Microcebus spp.) in the Makira region with the description of one new species. Am J Primatol 70:1033–1046 Ramirez M, Freese CH, Revilla J (1977) Feeding ecology of the pygmy marmoset, Cebuella pygmaea in Northeastern Peru. In: Kleinman DG (ed) The biology and conservation of the Callitrichidae. SI Press, Washington, DC Rendigs A, Radespiel U, Wrogemann D, Zimmermann E (2003) Relationship between microhabitat structure and distribution of mouse lemurs (Microcebus spp.) in Northwestern Madagascar. Int J Primatol 24:47–64 Schmelting B, Ehresmann P, Lutermann H, Randrianambinina B, Zimmermann E (2000) Reproduction of two sympatric mouse lemur species (Microcebus murinus and M. ravelobensis) in north-west Madagascar: first results of a long-term study. In: Lourenço W, Goodman S (eds) Diversité et endémisme à Madagascar. Société de Biogéographie, Paris Styrsky JD, Eubanks MD (2007) Ecological consequences of interactions between ants and honeydew-producing insects. Proc Roy Soc B 274:151–164 Wilson SW (2005) Keys to the families of Fulgoromorpha with emphasis on planthoppers of potential economic importance in the Southeastern United States (Hemiptera: Auchenorrhyncha). Florida Entomol 88:464–481

Chapter 8

Comparative Ecology of Exudate Feeding by Lorises (Nycticebus, Loris) and Pottos (Perodicticus, Arctocebus) K. Anne-Isola Nekaris, Carly R. Starr, Rebecca L. Collins and Angelina Wilson

Abstract  Craniomandibular variation characterizes the five species of Asian slow loris (Nycticebus), but until now, few ecological studies have been available to understand the factors that underpin it. Here, we review feeding ecology of Asian lorises and African pottos, with emphasis on the importance of exudate feeding, including several new studies. We then present novel data on this behavior based on a 10-week study of N. coucang at Pusat Penyelamatan Satwa, Lampung, Sumatra, Indonesia. Lorises and pottos range in body size from 100 g (Loris tardigradus) to more than 2 kg (N. bengalensis). Three of the smallest species (Arctocebus calabarensis, A. aureus, L. tardigradus) rely mainly on insects and small invertebrates as dietary staples. Although Perodicticus is known to eat gum only from already open wounds, active gouging of bark to extract exudates or consumption of plant sap has now been observed in all other lorises. Five species (P. potto, N. coucang, N. bengalensis, N. javanicus, N. pygmaeus) rely on exudates as a key food source. Although at all field sites, exudates are eaten all year round, at some, they become a key resource in times of food scarcity. Exudates have been extracted from 14 different plant families; Fabaceae is possibly the most important, currently consumed by all exudativorous species. Despite the lack of keeled nails, gouging behavior of lorises closely resembles that of marmosets and fork-marked lemurs, and involves active breaking of the plant surface; the audible nature of this behavior, as well as the characteristic marks left behind, makes it useful for determining the presence of Nycticebus in a forest. The captive lorises in our study also gouged regularly, recorded 2.9 times per hour for both adults and juveniles. Urine and facial marking accompanied the majority of gouges, a behavior recorded before only for marmosets. The functions of this behavior as a resource sharing strategy are explored. The importance of providing opportunity for gouging for captive lorises is also discussed, as a way to mitigate the periodontal diseases, which plague Nycticebus

K.A.I. Nekaris (*) Nocturnal Primate Research Group, Department of Anthropology and Geography, School of Social Sciences and Law, Oxford Brookes University, Oxford OX3 OBP, 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_8, © Springer Science+Business Media, LLC 2010

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in captivity. We conclude by discussing the importance of a better understanding of this relatively unique behavior to improve our knowledge of morphological correlates to loris taxonomy and ecology, and captive management via dietary changes and enrichment.

Introduction Asian slow lorises (Lorisidae: Nycticebus) range from Northern India to the Philippines, occurring in a multitude of habitat types from 0 to 4,000 m above sea level. With a basal metabolic rate lower than 60% of the predicted value (Müller et al. 1985), cryptic behavior of these nocturnal primates has precluded their study. Until recently, large variance in body size (265–2,200 g) (Table 8.1) was explained because of clinal variation (Osman Hill 1953; Ravosa 1998). However, several characters of the craniomandibular complex indicated ecological or genetic explanations for variation within Nycticebus (Schwartz and Beutel 1995; Ravosa 1998). Diet, in particular, is predicted to vary, with large Bengal slow lorises having a tougher diet requiring more repetitive loading (i.e., more folivorous), and smaller pygmy and Bornean lorises consuming more insects (Ravosa 1998). Genetic and gross morphological studies have now shown that Nycticebus comprises at least five species (Roos 2003; Nekaris and Jaffe 2007). Several characteristics with a genetic basis, such as the persistent absence of I2 in N. menagensis, further support these divisions (Schwartz and Beutel 1995; Groves and Maryanto 2008). Until now, however, field studies have been lacking that could shed light on how dietary adaptations among Nycticebus might affect the masticatory complex. Slow loris diet has been said to resemble that of the mainly frugivorous African pottos (Perodicticus) (Charles-Dominique 1977; Fitch-Snyder et  al. 2001), a genus that ranges in size from 800 g larger than the largest slow loris species to 1,500 g, larger than the smallest Nycticebus (Nekaris and Bearder 2007). This suggestion has been in part substantiated by limited field observations of N. coucang by Barrett (1984), who found the slow loris to be relatively omnivorous, consuming fruits, flowers, invertebrates, and gum. The key role of this latter food item to Nycticebus is becoming evident (Tan and Drake 2001; Wiens et al. 2006; Streicher et al. in review). Indeed, Wiens et al. (2006) mention that toxic and/or digestion inhibiting secondary compounds found in exudates might be related to the evolution of slow life history in lorises. Here, we review the use of exudates by slow lorises as revealed by several new field studies, and compare these data to studies of the closely related slender lorises, angwantibos, and pottos. We address several questions. Is there a relationship between body size and exudativory? Is any single exudate source important across sites? Is there any pattern in what species of exudates are processed and how? We then present novel data on exudativory from a captive study of wild slow lorises (N. coucang) recently confiscated from the wildlife trade. We assimilate these data to ascertain the importance of exudativory to the comparative ecology, morphology, and captive management of slow lorises.

Table 8.1  This table lists the seven species of Asian loris and three species of African potto, and whether or not exudate eating has been observed in the wild, based on information from available field reports until 2009, and trees from which exudates are eaten Wild Species Weight (g) exudativory Tree family (genus) References 150–270 No – Ambrose (1999), Schein (2008) Arctocebus calabarensis Arctocebus aureus 270–325 No – Charles-Dominique (1977) Rahm (1960), Kingdon (1974), CharlesPerodicticus potto 900–1,900 Yes Fabaceae (Albizia entada, Albizia sassa Dominique (1977), Oates (1984) Piptadenastrum, Pentacletra); Sterculiaceae Sterculia tragacantha Loris tardigradus 120–175 No – Nekaris and Jayewardene (2003) Loris lydekkerianus 200–330 Yes Fabaceae (Acacia, Prosopis), Meliaceae (Azadirachta) Rhadakrishna (2001), Nekaris and Rasmussen (2003) Nycticebus bengalensis 1,000–2,100 Yes Combretaceae (Terminalia), Moraceae (Artocarpus); Nekaris, personal observation, Pliosoengeon and Savini, (2008), Das (2008) Magnoliaceae (Manglietia); Fabaceae (Acacia, Bauhinia); Lecythidaceae (Careya arborea); Sterculiaceae (Pterospermum) Tan and Drake (2001), Streicher (2004), Starr Nycticebus pygmaeus 360–580 Yes Sapindaceae (Sapindus), Euphorbiaceae (Vernicia), and Nekaris, personal observation Fabaceae (Saraca), Anacardiaceae (Spondias); Burseraceae Nycticebus javanicus 565–1,000 Yes Fabaceae (Albizia), Arecaceae (Arenga) Winarti (2008), Nekaris et al., personal observation Nycticebus coucang 590–700 Yes Fabaceae (Parsarianthes, Albizia), Anacardiacaea Barrett (1984), Wiens (2002), Nekaris and (Anacardium, Gluta) Nijman (2007) Yes Unidentified liana Nekaris and Munds, personal observation Nycticebus menagensis 265–700 Exudativory is absent only from the three smallest species. Note also the importance of gums from the family Fabaceae for all exudativorous taxa

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Methods We follow the taxonomy of Nekaris and Bearder (2007), and explanatory ­references therein, throughout this study. For the overview of exudativory, we compiled data from all available reports on loris and potto behavior in the wild and through personal communication with individuals actively engaged in field studies. Gums and saps are included in our definition of exudates. Gums are a group of amorphous, water soluble, acidic polysaccharides that usually form a hard substance over the wounds in plants. Gums are typically obtainable from the surface of a plant, but excavation may be required to induce gum flow. Saps are juices and circulating fluids in plants; although excavation may be necessary to reach saps, they do not form a hard surface (Bearder and Martin 1980). For the captive study, we collected data from 2 April to 17 June 2007 at Pusat Penyelamatan Satwa (PPS), Lampung, Sumatra. Included in the study were 12 N. coucang (two lactating adult females, ten unweaned juveniles), all recently rescued from the pet trade. The lorises were all from Sumatra, and were confiscated as a group from a village just outside a forest near Lampung; the hunters claimed that the lorises were all from the same forest. The lorises had been in captivity at the center for 2 weeks. Animals were socially housed in an outdoor enclosure measuring 2 × 2 × 2 m. We were required to adhere to caging structure implemented by PPS. Social housing also gave a chance for the unweaned juveniles to suckle on the two lactating females (see Collins and Nekaris 2008 for further details). The enclosure contained an open floor with natural ground and foliage, and was thickly furnished with natural branches at all levels. Observations were recorded nightly from 19:00 to 05:00  h, yielding a total of 153  h of behavioral observation. In the course of constructing a general activity budget (Collins 2007), we collected all occurrences data on diet, with continuous sequence sampling used for gouging behavior (Altmann 1974). Data were entered and analyzed using SPSS 14.0. Results were analyzed using nonparametric statistical tests with significance set at p £ 0.05 (Lehner 1996).

Results Review of Exudativory in Wild Lorises and Pottos We had access to data from 12 field studies of slow lorises, three on the closely related slender loris, and five on pottos and angwantibos yielding a total of ten lorisid species (Table 8.1). Only three species have not yet been observed to consume exudates – the smallest of the slender lorises Loris tardigradus tardigradus and both species of Arctocebus. These smaller taxa seem to be primarily insectivorous (Charles-Dominique 1977; Ambrose 1999; Nekaris and Jayewardene 2003). In the case of the potto, old gums found in its stomach form a major basis for our

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knowledge of its exudate consumption (Kingdon 1974; Charles-Dominique 1977). Indeed, in Uganda, 19 stomachs obtained during 7 months held ca. 60% gum and ca. 30% insects. Kingdon (1974) suggested that gum is the main food during drier periods. Oates (1984) observed a potto licking gum, and on several occasions, noted focused searching behavior by pottos on gum bearing trees. No researcher to date, however, has observed pottos gouging to stimulate gum flow (Bearder and Martin 1980). Lorises and pottos consume exudates from 14 different families, with gum from Fabaceae, the pea family, important for all taxa. Exudate consumption by N. ­coucang in Malaysia (Wiens et  al. 2006) was a-seasonal, contrary to its seasonal use by N. pygmaeus in both Vietnam (Streicher et al. in review) and Cambodia (Starr, personal observation). Studies of N. menagensis in Sabah, Borneo (Nekaris and Munds, 2010), N. bengalensis in Assam, India (Das 2008) and Thailand (Pliosoengeon and Savini 2008), and N. javanicus in Java, Indonesia (Winarti 2008) have not yet been conducted over a whole year, although exudate consumption has been observed. Gum represented only a small proportion of the diet for L. lydekkerianus lydekkerianus (Nekaris and Rasmussen 2003) and for L. l. nordicus (Nekaris, personal observation), but no seasonal pattern was evident. Consumption of saps and gums by lorises shows a similar pattern (Tan and Drake 2001; Wiens 2002; Das 2008; Pliosoengeon and Savini 2008; Winarti 2008; Nekaris and Starr, personal observation). Lorises consume sap and gum from as low as 1  m to as high as 12  m off the ground. When consuming sap, all lorises observed perforate the superficial layer of the cambium of trees or lianas by scraping with their toothcomb. Lapping of the exposed sap with the tongue lasts from a few seconds to about 4 min, with intermittent additional breaking of the hard surface. Gum is consumed for a longer period, from 2 to 20 min, and involves active gouging with the anterior teeth. In most cases, trees already bore wounds (due to larval infestation, prior injury, or fire), although lorises can also gouge into the wood to induce gum flow (Streicher 2004; Starr and Nekaris, personal observation). By anchoring their upper incisors into the bark or into the solidified gum, lorises then scoop up the gum. By this manner, N. pygmaeus can also gouge into bamboo to reveal insects, which it then consumes; they also appear to scrape lichens and fungus off the surface of old bamboo with their toothcomb (Starr et al. 2008; Starr, personal observation). Until now, no loris has been observed to gouge gum with its molar teeth. Pygmy lorises in Cambodia, however, remove “icicles” of gum from open wounds, and while holding them in one hand, alternately chew on them with the posterior teeth and lick them (Starr and Nekaris, personal observation). Lorises actively search for their gum sources. Head down searching may accompany investigating for sap on branches, or searching along bamboo to find a location to gouge for insects. Visible and audible sniffing sometimes accompanies these searches. On gum trees without active wounds, pygmy lorises race up and down a single trunk, making up to 20 trial holes before feeding (Starr and Nekaris, personal observation). Trees with active wounds seem to be known to the animals, which will make rapid and directed movement to a feeding site (Starr and Nekaris, personal observation). When gouging begins, bark breaking can be audible even from

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a distance of 10  m (Streicher et  al. in review). The loris may turn its head from side-to-side spitting out bits of bark; this side-to-side movement is often accompanied by scent marking the wound with facial glands. Bits of bark may be consumed in this process (Wiens et al. 2006). The even more noisy process of gouging bamboo involves a loris anchoring its rear feet against the bamboo and bashing its toothcomb into the incredibly hard surface; this behavior also results in shaking of the bamboo stand, making it audible for up to 100 m away. Lorises consume exudates in an orthograde posture (the head can face up or down) when they are located on a vertical substrate, but also can stand quadrupedally over an exudate source (Wiens 2002; Nekaris and Rasmussen 2003; Streicher 2004; Starr and Nekaris, personal observation).When licking, the loris does it with gusto; its long tongue is easily visible, and licking of the nose and face is intermittent with licking the exudate source. Lorises regularly return to the same gouging site over 10 days and weeks, and multiple members of a social group may use the same gouging locality (Nekaris and Rasmussen 2003; Streicher 2004; Wiens et al. 2006). Indeed, in Cambodia, a single gum lick occurred in an area of range overlap of two groups of pygmy lorises; up to four lorises were seen at one time using this lick (Starr and Nekaris, personal observation). Overall, gouging is a very vigorous repetitive action and is unmistakable. The marks left on branches, too, are characteristic and may aid field workers in determining loris presence in an area (Tan and Drake 2001) (Figs. 8.1 and 8.2). Indeed, there is no relationship between the study duration and whether or not gouging has been observed in lorises and pottos, with two out of four short studies (less than a year) and three out of six long studies reporting gouging (Fisher Exact Probability Test, p < 1.0), suggesting that it is a behavior relatively easy to observe.

Captive Sumatran Study During the first 3 weeks of the study, juvenile N. coucang commonly chewed and gouged the timber beams of their enclosure and nest boxes, although no exudates could be obtained. We identified the timber as “sengon” (Fabaceae: Paraserianthes falcataria), and placed branches of this species throughout the enclosure. At this stage, adult females also began to gouge. The leafy branches added also contained flower buds, as P. falcataria flowers throughout the year (Gutteridge and Shelton 1998). The flowers and leaves were licked or eaten by both age classes. By the end of the study, 441 visual and auditory gouging events had occurred (adults = 44, juveniles = 397), with 23 that were auditory only, resulting in a gouging rate of 2.9 times per hour. Lorises gouged the timber beams (71%), nest boxes (13%), and sengon branches (16%) (Figs. 8.3). Clearly juveniles gouged more than adults but interestingly, adults gouged sengon branches significantly more than juveniles did (0.2 = 19.98, df = 2, p < 0.001). Gouging episodes ranged from a few seconds in duration to 2  min, but median gouging periods were short lasting 11–15  s.

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Fig. 8.1  Examples of branches gouged by N. coucang, showing the typical gnawing pattern for this genus (drawing: H. Schulze)

Gouging behavior consisted of anchoring the upper incisors into the wood, while deeply gouging with the lower anterior teeth. Gouging was ­audible, and longer sessions left impressions in the wood of about 2.5 cm diameter, and about 0.6 cm deep. The average height at which animals gouged was 1.6 m + sd 0.35. An unexpected behavior of note was that the majority of gouges (52%) were also scent marked by an individual while it chewed, either in the form of facial rubbing or urine marking, via depositing urine directly into the gouge. Of 228 observations of scent marking while gouging, urine marking accompanied 83%, significantly more than facial rubbing (c2 = 98.68, df = 1, p < 0.001). Although scent marking occurred for both age classes during daily interactions, the majority of marking occurred while gouging the enclosure timber and sengon branches. The adults scent marked more than juveniles (66 vs. 57% of observations) when gouging, but this difference only showed a trend toward significance.

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Fig.  8.2  Gouge mark (indicated by arrows) from which exudates have been consumed by N. pygmaeus from a tree in Seima Biodiversity Conservation Area, Cambodia. An adult female spent only 30 s producing this 5 × 12 mm hole. Photo: C.R. Starr

Fig.  8.3  Juvenile N. coucang at PPS Rescue Center, Sumatra, standing on a sengon branch (P. falcataria) exhibiting several small gouge marks. Photo: A. Wilson

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Discussion Tan and Drake (2001) were the first to provide strong evidence that slow lorises exhibit gouging behavior specialized to elicit sap or gum flow, and suggested that they rely on gum as an important source of nutrients. The specialized behavior of using the lower anterior teeth to gouge a hole in bark is rare among primates and occurs in only three other genera: Callithrix, Cebuella (Callitrichidae) and Phaner (Cheirogaleidae) (Coimbra-Filho and Mittermeier 1978; Petter et al. 1971). Wiens (2002) too concluded that Nycticebus belongs to a specialized exudate-feeding guild (Nash 1986). The data presented in this paper solidify this view, showing that all five species of Nycticebus and one of the two Loris species utilize this resource, with some of the taxa relying on exudates as a major food source. When the soft anatomy of lorises is examined, it is perhaps no surprise that gum should play an important role in their diets. As is the case with other exudativorous primates, both Nycticebus and Loris are characterized by a long relatively narrow tongue, large caecum, and a short duodenum (Kubota and Iwamoto 1966; Osman Hill 1953). With all species also showing a propensity to eat insects, this anatomical arrangement may be useful in breaking down “structural carbohydrates present in both gum and the chitinous exoskeletons of invertebrates (Fleagle 1999, p. 296).” A simple stomach complements this arrangement, and may aid in digestion of fruits and flowers (Chivers and Hladik 1980). All species of lorises so far lack keeled nails. A strong grip when on vertical surfaces combined with consuming exudates on more oblique and horizontal branches may reduce the need for this adaptation. On the basis of field studies conducted so far of African and Asian lorises, exudate consumption tends to be more important for the larger-bodied taxa. The potto seems to differ from Asian lorises, in that, although it seems to eat appreciable quantities of gum, it has never been observed to gouge actively but seems to extract gum from already opened wounds (Charles-Dominique 1977; Oates 1984). In a more recent study of P. potto edwardsi, it was not seen to eat gum at all, although it did extract snails from their shells with its long pointed tongue (Pimley 2002). Its exudativory seems to more closely resemble that of Galago, Saguinus, Papio, Cercopithecus, and Erythrocebus (Nash 1986). Active gouging is conducted by all species of Nycticebus and Loris seen eating gum thus far. In a study of N. coucang (probably a mixed sample of N. coucang and N. bengalensis) and N. pygmaeus, Schwartz and Beutel (1995) demonstrated that Nycticebus has the deepest mandible with the most developed gonial region and the most robust upper canine roots of the lorises and pottos. Biting forces that produce a greater magnitude of stress are thought to be important for shaping the primate masticatory complex. A deep mandible has been implicated in countering bending during heavy incisal biting in some primates (Hylander 1985), and may explain this condition in Nycticebus. Williams et al. (2001) and Vinyard et al. (2003) arrived at different results, noting that gouging primates have a masticatory complex that permits the mandibular incisors to move more vertically when the jaw gapes. The vigorous open-mouthed gouging by Nycticebus, creating large holes in a few seconds, accords well with this suggestion. Ravosa (1998) described variability of the masticatory complex of Nycticebus and

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suggested that it was clinal, predicting a variety of different diets for the species. Examination of the biomechanical force required by slow lorises to engage in gouging behavior, and comparing this with the extent to which each species relies on exudates may lend further scope to the morphological adaptations of the different species. All exudativorous taxa in our study consume exudates from the family Fabaceae, although not yet at all sites. For example, although N. bengalensis in both Thailand and Assam consume exudates of Combretaceae, Fabaceae consumption has so far only been observed for Thai N. bengalensis. We also found a tendency for seasonal use of exudates at several of the sites where long-term studies were conducted. Fabaceae, the pea family, is widely dispersed throughout Asia; species of this family often colonize edges and tree fall zones (Gutteridge and Shelton 1998), a habitat said to be preferred by some loris species (Nekaris et al. 2008). Both gum and sap from this family may provide a year-round energy source for lorises or an important readily-available fallback food source in times of food scarcity (Hladik 1979). The exudates consumed by lorises probably contain high amounts of easily digestible mono and disaccharides (high concentrations of carbohydrate) and lipids (Bearder and Martin 1980; Nash 1986). Gums from Fabaceae also are an important part of the diet of other nocturnal primates. Galago senegalensis braccatus preferred Acacia gum to other types, particularly to those containing extra tannins (Nash 1989), and both G. moholi and Otolemur crassicaudatus, whose highly seasonal environment resembles that of N. pygmaeus and N. bengalensis, relied almost wholly or extensively (respectively) on gum during some periods of the year. The process by which exudates are consumed is remarkably similar across taxa. Although slow lorises lack specialized keeled nails, they are nonetheless capable of clinging to a vertical substrate while engaged in gouging for up to 20  min. Like marmosets and fork-marked lemurs, lorises remain focused on gouging, which might leave them vulnerable to predation. This could explain the presence of a dorsal stripe in all Nycticebus (Nekaris and Jaffe 2007), and might even explain the seasonal appearance of this stripe in Vietnamese N. pygmaeus (Streicher 2004), which is only present during the harsh winter months when exudativory seems to increase. Although the closely-related African galagos are known to scrape gum from the tree surface and to extend existing wounds to get at gum, they do this with specialized cheek teeth rather than with the anterior teeth (Bearder and Martin 1980). There is still debate over whether or not pottos are more closely related to galagos or to Asian lorises (Schwartz and Beutel 1995; Nekaris and Bearder 2007). More observations of pottos are needed to see how they extract exudates, and to which of these two groups this behavior more closely resembles. A novel finding in our captive study was that urine marking or facial rubbing often accompanied gouging episodes by both adult and juvenile slow lorises. Gouging behavior has been observed among Bengal slow loris infants between 2 and 4 weeks of age, although scent marking was not reported (Zimmermann 1989). However, vigorous circumgenital scent marking the context of gouge holes is an important part of the behavioral repertoire of South American marmosets (Rylands 1984, 1985). Indeed, this behavior is used infrequently in any other context. Several explanations

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for scent marking gouges have been proposed, including territory marking, regulation of group movement, intra-group sexual dominance, deterring other groups from using a hole, or indicating the profitability of a certain hole (Rylands 1990). As gouging is essentially a risky business in terms of predation susceptibility and in terms of potential tooth damage (Bearder and Martin 1980), all of these hypotheses may be relevant to and interesting to test in the case of Nycticebus. Here we propose an additional role for marking gouges. Wiens and Zitzmann (2003) describe that young slow lorises clearly learn to eat items consumed by their parents, but did not witness any evidence of direct social learning. They suggested that information about food resources might be transferred chemically. Our observations that adult N. coucang did not begin to scent mark their gouges until presented with fresh branches that provided a better chance of producing exudates suggests that they may have been submitting information about food sources to their offspring. Because scent marking is a common part of loris behavior, it is therefore difficult to quantify (Nekaris and Jayewardene 2003, see also Rylands 1990 for marmosets), and the studies reviewed here may have overlooked scent marking of gouges in the wild. Future researchers should be alert to this possibility, and attempt to interpret its function. Our results carry implications for captive management. Captive lorises suffer from obesity (Ratajszczak 1998) and dental diseases, including abscesses, recurrent periodontal disease, facial swelling, and osteomylitis of the zygomatic arch (FitchSnyder et  al. 2001). A diet too rich in sugar, and lack of substrates on which to gouge have been implicated for both conditions (Streicher 2004). Streicher (2004) noted a high standard of dental hygiene when wild-caught N. pygmaeus were given the opportunity to gouge fresh branches regularly. Craig and Reed (2003) presented puzzle feeders to N. pygmaeus that necessitated gouging and thereby increased activity, an aid to reducing obesity. Fitch-Snyder et  al. (2001) used gum arabic placed into a treat log to stimulate activity; both N. bengalensis and N. pygmaeus gouged into the log far beyond the original diameter of the initial drill holes. In marmosets, too, the full suite of wild behaviors, including urine marking, can be stimulated by providing gum enrichment (McGrew et al. 1986). In our study, the N. coucang were ultimately released to the wild; the resident veterinarian particularly commented on the healthy state of the animals, including their dentition (Collins and Nekaris 2008). Animals were also fed on plenty of live prey, ­including birds, and local uncultivated fruits that were more likely to be lower in sugar (Streicher et  al. in review). The health of captive populations of lorises may be greatly enhanced by providing regular opportunities for gouging, and further studies should investigate this. In previous reviews of gouging behavior of primates, Asian lorises were an unstudied enigma (Bearder and Martin 1980; Nash 1986). Unique in many aspects of their behavior and anatomy, we show here that they are one of the few primate genera to engage in specialized extractive gouging of plant exudates. This specialization is reflected to some extent in their pelage, life history, masticatory complex, and social behavior. The data we present here are mainly from field studies of slow lorises still in their early stages. We hope we present many challenges to this new generation of researchers to further our knowledge of the role of exudativory in loris

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ecology and evolution, and to the improvement of the welfare and health of captive lorises through the promotion of this natural behavior in zoos and sanctuaries. Acknowledgments  We thank Annie Burrows and Leanne Nash for organizing the symposium at the International Primatology Conference in Edinburgh and for inviting us to participate in this volume. We are extremely grateful to N. Das, M. Pliosoengeon, and I. Winarti for sharing unpublished accounts of loris exudativory; to J. Oates, L. Schein, and E. Pimley for unpublished accounts on the lack of this behavior in pottos and angwantibos; and to A. Rylands and S. Bearder for sharing their observations on exudate feeding in marmosets and galagos. For the Sumatran study, we thank the staff at PPS and IAR, especially to P. Agus, F. den Haas, A. Knight, E. Rahadian, K. Sanchez, and K. Sudaryatmo. International Animal Rescue, International Primate Protection League, Primate Conservation Inc., and Oxford Brookes University provided financial support.

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Hladik CM (1979) Diet and ecology of prosimians. In: Doyle GA, Martin RD (eds) The study of prosimian behaviour. Academic Press, New York Hylander WL (1985) Mandibular function and biomechanical stress and scaling. Am Zool 25:315–330 Kingdon J (1974) East African mammals. An atlas of evolution in Africa, Vol. 1. Academic Press, London Kubota K, Iwamoto M (1966) Comparative anatomical and neurohistological observations on the tongue of slow loris (Nycticebus coucang). Anat Rec 158:163–176 Lehner PN (1996) Handbook of ethological methods. University Press, Cambridge McGrew WC, Brennan JA, Russell J (1986) An artificial “gum-tree” for marmosets (Callithrix j. jacchus). Zoo Biol 5(1):45–50 Müller EF, Nieschalk U, Meier B (1985) Thermoregulation in the slender loris (Loris tardigradus). Folia Primatol 44:216–226 Nash L (1986) Dietary, behavioural, and morphological aspects of gummivory in primates. Yearb Phys Anthropol 29:113–137 Nash L (1989) Galagos and gummivory. Hum Evol 4(2–3):199–206 Nekaris KAI, Bearder SK (2007) The strepsirrhine primates of Asia and Mainland Africa: diversity shrouded in darkness. In: Campbell C, Fuentes A, MacKinnon K, Panger M, Bearder SK (eds) Primates in perspective. Oxford University Press, Oxford Nekaris KAI, Jaffe S (2007) Unexpected diversity within the Javan slow loris trade: implications for slow loris taxonomy. Contrib Zool 76:187–196 Nekaris KAI, Jayewardene J (2003) Pilot study and conservation status of the slender loris (Loris tardigradus and Loris lydekkerianus) in Sri Lanka. Primate Conserv 19:83–90 Nekaris KAI, Nijman V (2007) Survey on the abundance and conservation of Sumatran slow lorises (Nycticebus coucang hilleri) in Aceh, Northern Sumatra. Proceedings of the European Federation of Primatology, Charles University, Prague, p. 47 Nekaris KAI, Rasmussen DT (2003) Diet and feeding behaviour of the Mysore slender loris. Int J Primatol 24(1):33–46 Nekaris KAI, Blackham GV, Nijman V (2008) Implications of low encounter rates in five nocturnal species (Nycticebus spp). Biodivers Conserv 17(4):733–747 Nekaris KAI, Munds R (2010) Using facial markings to unmask diversity: the slow lorises (Primates: Lorisidae: Nycticebus) of Indonesia. In (Gursky S & Supriatna J, eds) The Primates of Indonesia. Springer: New York. Pp. 383–396 Oates JF (1984) The niche of the potto, Perodicticus potto. Int J Primatol 5(1):51–61 Osman Hill WC (1953) Primates. Comparative anatomy and taxonomy. I. Strepsirhini. Edinburgh University Press, Edinburgh Petter JJ, Schilling A, Pariente G (1971) Observations eco-ethologiques sur deux lemuriens malgaches nocturnes: Phaner furcifer et Microcebus coquereli. Terre Vie 118:287–327 Pimley ER (2002) The behavioural ecology and genetics of the potto (Perodicticus potto edwardsi) and Allen’s bushbaby (Schiurocheirus alleni cameronensis). Unpub. Ph.D. thesis, University of Cambridge, Cambridge Pliosoengeon M, Savini T (2008) Spatial and feeding behavior of the endangered Bengal slow loris, Nycticebus bengalensis in Khao Angrunai Wildlife Sanctuary, Thailand. Unpublished report to the Primate Society of Great Britain, p. 8 Rahm U (1960) Quelques notes sur le potto de Bosman. Bull Inst Fr d’Afr Noire, Ser A 22:331–341 Ratajszczak R (1998) Taxonomy, distribution and status of the lesser slow loris Nycticebus pygmaeus and their implications for captive management. Folia Primatol 69(1):171–174 Ravosa MJ (1998) Cranial allometry and geographic variation in slow lorises (Nycticebus). Am J Primatol 45:225–243 Rhadakrishna S (2001) The social behavior of the Mysore slender loris (Loris tardigradus lydekkerianus). Unpub. Ph.D. thesis, University of Mysore, Manasagangotri

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Roos C (2003) Molekulare Phylogenie der Halbaffen, Schlankaffen, und Gibbons. Unpub. Ph.D. thesis, Technische Universität München Rylands AB (1984) Exudate-eating and tree-gouging by marmosets (Callitrichidae, Primates). In: Chadwick AC, Sutton SL (eds) Tropical rain forest. The Leeds Symposium. Leeds Philosophical and Literary Society, Leeds Rylands AB (1985) Tree-gouging and scent-marking by marmosets. Anim Behav 33(4):1365–1367 Rylands AB (1990) Scent-marking behaviour of wild marmosets, Callithrix humeralifer (Callitrichidae, Primates). In: Macdonald DW, Müller-Schwarze D, Natynczuk SE (eds) Chemical signals in vertebrates 5. Oxford University Press, Oxford Schein L (2008) Species diversity of the enigmatic nocturnal primates in the secondary Rhoko forest, Cross River State, Nigeria: Preliminary findings on densities, abundance estimates, and methods comparisons using DISTANCE. MSc Primate Conservation. Oxford Brookes University, UK Schwartz JH, Beutel JC (1995) Species diversity in lorisids: a preliminary analysis of Arctocebus, Perodicticus and Nycticebus. In: Alterman L, Doyle GA, Izard MK (eds) Creatures of the dark: The nocturnal prosimians. Plenum Press, New York Starr CR, Streicher U, Nekaris KAI (2008) The distribution and conservation of the pygmy loris (Nycticebus pygmaeus) in Eastern Cambodia. XXIIth Congress International Primatological Society Abstracts, Primate Eye:116 Streicher, U (2004) Aspects of the ecology and conservation of the pygmy loris Nycticebus pygmaeus in Vietnam. Dissertation. Ludwig-Maximilians Universität, Germany Streicher U, Collins R, Navarro-Montes A, Nekaris KAI (in review) Observations on the feeding preferences of slow lorises (N. pygmaeus, N. javanicus, N. coucang) confiscated from the trade. In: Masters J, Crompton R, Genin F (eds) Prosimians. Springer, New York Tan CL, Drake JH (2001) Evidence of tree gouging and exudate eating in pygmy slow lorises (Nycticebus pygmaeus). Folia Primatol 72:37–39 Vinyard CJ, Wall CE, Williams SH, Hylander WL (2003) Comparative functional analysis of skull morphology of tree-gouging in primates. Am J Phys Anthropol 120:153–170 Wiens F (2002) Behaviour and ecology of wild slow lorises (Nycticebus coucang): social organisation, infant care system, and diet. Dissertation. Faculty of Biology, Chemistry and Geosciences, Bayreuth University, Germany Wiens F, Zitzmann A (2003) Social dependence of infant slow lorises to learn diet. Int J Primatol 24(5):1008–1021 Wiens F, Zitzmann A, Hussein NA (2006) Fast food for slow lorises: is low metabolism related to secondary 5 compounds in high-energy plant diet? J Mammal 87(4):790–798 Williams SH, Wall CE, Vinyard CJ, Hylander WL (2001) A biomechanical analysis of skull form in gum-harvesting galagids. Folia Primatol 73:197–109 Winarti I (2008) Field research on Javan slow loris’ population in Sukakerta Ciamis and Kawungsari Tasikmalaya, West Java, Indonesia. Report to IAR Indonesia, Ciapus, Bogor, Indonesia, p. 7 Zimmermann E (1989) Reproduction, physical growth and behavioural development in slow loris (Nycticebus coucang, Lorisidae). Hum Evol 4(2–3):171–179

Chapter 9

Exudativory and Primate Skull Form Matthew J. Ravosa, Russell T. Hogg, and Christopher J. Vinyard

Abstract  We review comparative and experimental research ­regarding the musculoskeletal correlates of exudativory in primates, providing novel data on: cranial ontogeny and scaling in galagos, macroscale tests of symphyseal joint performance in platyrrhines, and histology of enamel prism organization in the anterior dentition of callitrichids. In galagos, derived configurations of jaw-joint position and jaw-muscle mechanical advantage in Otolemur and Euoticus appear to facilitate increased gape during scraping or gouging behaviors. Due to the lack of greater robusticity of loadresisting mandibular elements in Otolemur and Euoticus, there is little evidence to suggest that exudativory in galagos results in higher masticatory stresses. Compared to tamarins such as Saguinus, the marmoset Callithrix has canine enamel with a much higher degree of decussation. However, simulated jaw loading suggests a reduced ability to withstand external forces in the marmoset symphysis. The contrast between increased load-resistance ability in the anterior dentition versus relatively reduced symphyseal strength suggests both a potentially complex loading environment during gouging and a mosaic pattern of craniodental adaptations to this derived feeding behavior. As primate exudativory involves different behavioral strategies to obtain gums and sap, it is not surprising that there is some discordance among the comparative evidence regarding the impact of anterior dental loading on masticatory elements. This is compounded by the fact that gouging and scraping are critical adaptations in some taxa and only seasonally important for others. Indeed, the ecomorphological­ significance of seasonality in feeding behaviors remains poorly understood, and this negatively affects analyses of the impact of fallback foods on skull form in living and fossil primates.

M.J. Ravosa (*) Department of Pathology and Anatomical Sciences, University of Missouri School of Medicine, Medical Sciences Building, One Hospital Drive DC055.07, Columbia, MO 65212, USA 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_9, © Springer Science+Business Media, LLC 2010

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Introduction and Background Exudativory consists of a relatively specialized diet in primates focused primarily on tree gums or saps. The continuous range of exudate feeding styles can be reasonably subdivided into three types. Opportunistic exudate feeding involves consuming readily available gums or saps. Numerous primates practice opportunistic exudate feeding, which seems to be associated primarily with behavioral strategies for locating exudates rather than morphological adaptations of the skull linked to procuring these food items (Nash 1986). Given our interest in skull form, this type of exudate feeding is not considered further here. The remaining two types of exudate-feeding behaviors – gouging and scraping – involve animals actively using their masticatory apparatus to procure exudates. In primates, until recently such proclivities have been observed in only a few clades, namely cheirogaleids, galagids and callitrichines (but see new information on lorisids, Nekaris et al., Chap. 8). Gouging consists of using the upper anterior dentition to gain purchase on a tree’s outer surface, with the lower jaw directed into the bark so as to penetrate it and in turn elicit the flow of tree gum. Species known to engage in this activity include Phaner furcifer, Euoticus elegantulus, Callithrix spp., and Cebuella pygmaea (Charles-Dominique 1977; Nash 1986; Garber 1992). Scraping is a less invasive behavior whereby the mandible is used to either score the outer bark or remove previously hardened gums on a tree’s surface due to insect or other damage. Otolemur crassicaudatus (and to a lesser extent O. garnettii) as well as Galago moholi have been observed to exhibit this behavior (CharlesDominique 1977; Bearder and Martin 1980; Nash 1986). It is important to note that “gougers” may also employ scraping (Vinyard et al. 2009). Exudativory can occur on a seasonal basis, where gum serves as a fallback food (Bearder and Doyle 1974; Crompton 1984; Heymann and Smith 1999; Porter 2001) or on a consistent basis throughout the year (Charles-Dominique 1977; Nash 1986; Passamani and Rylands 2000; see also Marshall and Wrangham (2007) regarding the distinction between filler and staple fallback foods). In this regard, primates are similar to a variety of vertebrate exudativores such as the marsupial sugar-glider (Petaurus) and Kaka birds, Nestor meridionalis (e.g., Smith 1982; O’Donnell and Dilks 1989). Arguably, greater attention has been directed at understanding primate feeding behaviors and trophic adaptations other than gummivory (e.g., sclerocarpy – Kinzey 1992; folivory – Wright et  al. 2008) due to the rarity of gouging and scraping in primates (Nash 1986). However, the past decade has witnessed a considerable influx of research on the morphological and behavioral correlates of exudativory (e.g., this volume). For those interested in craniomandibular form and function, it has become increasingly evident that exudativory requires a series of masticatory features and associated behaviors related to the extraction and collection of gums and saps [see Power and Oftedal (1996) regarding the digestive system]. With this in mind, our chapter aims to review the comparative, experimental, and ecomorphological evidence regarding exudativory, specifically focusing on the musculoskeletal features

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related to gape and force generation as well as stress-resisting elements. Variation in dietary properties and processing/procurement often influences both force-generating structures as well as load-resisting features. Therefore, we will summarize both the correlates and consequences of these mechanical demands on masticatory elements. In doing so, we also present novel research on enamel prism decussation patterns of the anterior dentition in gouging and nongouging platyrrhines, macroscale tests of symphysis properties in gouging and nongouging platyrrhines, and comparative ontogenetic data on galago craniomandibular proportions that hopefully brings additional insights into our understanding of the functional and evolutionary significance of this interesting feeding behavior.

Force-Resisting Structures As noted above, exudativory can involve the active gouging of bark to elicit the flow of tree gum and/or the scraping of sap that has hardened on a tree’s surface. Following the expectation that tree bark, cambium, and phloem present particular mechanical challenges to overcome, received wisdom sets up expectations that there is a suite of morphological specializations to counter the hypothesized greater loads experienced during such behaviors. For instance, the presence of higher peak loads and/or greater cyclical loading during incisor gouging/scraping might be expected to result in (1) a relatively larger symphysis due to elevated bending and/or shear, (2) deeper corpora due to increased bilateral parasagittal bending, (3) a wider corpus due to higher bilateral axial torsion, and/ or (4) relatively larger condyles to resist elevated joint reaction forces (Vinyard et al. 2003). Similar morphological patterns have been documented for primates known to employ marked anterior dental loading during food procurement and processing (Hylander 1979; Bouvier 1986a, b; Ravosa 1991, 1996, 2000; Cole 1992; Daegling 1992). In one of the early papers regarding the craniomandibular correlates of exudativory, Dumont (1997) performed a multivariate analysis using a broad sample of mammals that emphasize gums, sap, nectar, flowers, and fruit in their diets. Such analyses were generally supportive of the notion that taxa which routinely employ gouging and/or scraping behaviors tend to exhibit deeper mandibular corpora. Increased robusticity was interpreted as an adaptation to counter elevated loads related to anterior dental loading during gouging and scraping related to the exploitation of exudates. Similar conclusions have been reached in a recent comprehensive analysis of mandibular proportions in marsupial gougers (Hogue 2008). More phylogenetically- restricted analyses in galagos and platyrrhines have ­provided notably mixed results regarding whether mandibular robusticity is ­correlated with exudativory. While observing “few consistent morphological

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p­ atterns linking skull form and the generation of high forces during gouging,” Williams et al. (2002, p. 197) did note that Euoticus and Otolemur ­crassicaudatus exhibited deeper corpora. Such deeper jaws are inferred to be linked to increased repetitive loading rather than elevated peak loads, an interpretation largely reinforced by a series of sister-taxa comparisons of jaw proportions within cheirogaleids, galagids, and callitrichines that found little evidence for relatively improved load-resisting abilities in tree-gouging primates (Vinyard et  al. 2003). A rare analysis of load-resisting soft tissues indicates that the articular cartilage of the mandibular condyle in Otolemur crassicaudatus appears able to withstand greater loading in certain regions than similar sites for its sister taxon O. garnettii (Burrows and Smith 2007). Alternatively, Mork et al. (2010) found relatively thicker articular cartilage in the anterior glenoid, but no differences in condylar cartilage of tree gouging marmosets compared to nongouging platyrrhines. Comparative ontogenetic data for 12 galago taxa, in which a majority of bivariate regressions indicate ontogenetic scaling of craniomandibular dimensions, offer additional evidence to bear on this issue (Ravosa et al. 2010). Interestingly, interspecific comparisons of growth trajectories for mandibular corpus depth do not indicate significant variation in mandibular robusticity independent of size differences among galago taxa. In other words, despite variation in dietary proclivities across galagos, the ontogeny of mandibular depth does not differ significantly between exudativores that employ scraping and gouging (Euoticus, Otolemur, Galago moholi) and their sister taxa (Fig.  9.1). That said, positive allometry of corpus depth across galagos does indicate that larger exudativores such as Euoticus and, especially, Otolemur possess relatively larger jaws than their smaller-bodied sister taxa (Ravosa et al. 2010). Interspecific microCT data for callitrichine monkeys furnish stronger evidence against the notion that gouging primates such as marmosets generate larger forces than their nongouging close relatives. Much as demonstrated via a consideration of external jaw measures (Vinyard et al. 2003), microCT analyses demonstrate that the mandibular corpus, symphysis, and temporomandibular joint (TMJ) in Callithrix are not overbuilt relative to Saguinus (Vinyard and Ryan 2006; Ryan et al. 2010). By inference, marmosets are unlikely to experience routinely larger forces along the mandible as compared to tamarins. Data collected by two of us (MJR & CJV) regarding symphyseal strength during simulated loading regimes experienced by anthropoids (cf., Hylander et al. 1998, 2000, 2005; Vinyard et al. 2008) provide further support for the interpretation of Vinyard and colleagues based on comparative data. Using an Instron Universal tester to conduct macroscale tests of symphyseal joint properties in simulated dorsoventral shear and wishboning, mean loads at structural failure for both loading regimes in Callithrix were significantly lower than means for non-marmoset (i.e., nongouging) taxa (Table 9.1). Although tamarin specimens were not available for tests of symphyseal strength in dorsoventral shear, the jaws in relatives such as Saimiri are similar enough to represent a typical morphology in a nongouging small-bodied platyrrhine.

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Fig. 9.1  A plot of ln masseter lever arm length vs. ln basicranial length in galagids (adapted from Ravosa et al., 2010). The data for Euoticus and, especially, Otolemur are transposed below those for the remaining galagos, all nine taxa of which are ontogenetically scaled (i.e., Galago, Galagoides). This divergence in Otolemur and Euoticus growth allometries results in the decreased mechanical advantage of the masseter muscle, which facilitates increased gape. This may be due to the unique tree-scraping behaviors of these genera vs. the more faunivorous and frugivorous proclivities of other galagids. The samples consist of: Galago senegalensis (filled black circle – 73 adults, 41 nonadults); G. s. braccatus (filled black square – 28 adults, 65 nonadults); G. moholi (filled black triangle – 31 adults, 43 nonadults); G. gallarum (open diamond – 5 adults, 3 nonadults); G. matschiei (filled gray triangle – 8 adults, 1 nonadult); Galagoides demidovii (filled inverted gray triangle – 33 adults, 45 nonadults); G. alleni (filled gray circle – 24 adults, 8 nonadults); G. thomasi (open hexagon – 20 adults, 6 nonadults); G. zanzibaricus (open circle – 13 adults, 6 nonadults); Otolemur crassicaudatus (filled inverted black triangle – 42 adults, 38 nonadults); O. garnettii (filled hexagon – 39 adults, 28 nonadults); Euoticus elegantus (filled gray square – 47 adults, 10 nonadults)

Tradeoffs in Jaw-Opening and Force-Generating Structures In addition to questions regarding whether masticatory elements are designed to resist elevated peak loads during gouging and/or scraping, a number of studies have focused considerable attention on whether exudativory necessitates morphological adaptations for increased gape. In marmosets, both field and lab-based studies have demonstrated that bark gouging appears to be associated with a wide gape (Nash 1986; Garber 1992; Vinyard et al. 2009). In this regard, research has focused on the potential muscular and skeletal correlates of such behaviors. For example, since increased gape often results in the decreased mechanical advantage of the jawadductor muscles for other masticatory behaviors (cf., Herring and Herring 1974; Ravosa 1996), such studies provide important evidence regarding whether exudativores­are designed to generate large anterior dental forces. Comparative analyses of mandibular morphology offer strong support for ­suggestions that increased gape is related to gouging and scraping. For instance, an anteroposteriorly elongate TMJ condyle and glenoid fossa, which would facilitate

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Table 9.1  Platyrrhine symphysis strength and between-group comparisonsa, b DV shear (N/mm2) Wishboning (N/mm2) Mean (N, SD)** Mean (N, SD)* Groups Marmosets 2.246 (6, 0.367) 3.608 (5, 0.336) Non-marmosets 3.418 (9, 0.543) 4.156 (3, 0.911) Mann–Whitney tests: **P < 0.01; *P £ 0.05 Symphyseal strength during wishboning in the transverse plane was investigated with the specimen on its side such that the left corpus was positioned above the right corpus. Immediately posterior to the joint’s lingual border, wires were bound bilaterally to the corpora so as to minimize variation in the moment arm in wishboning. Such wires were oriented orthogonal to the midsagittal plane to ensure the joint load was directed laterally. The wire around the left corpus was loaded in tension at a constant rate of 2.54 cm/min and thus pulled superiorly versus the stationary wire around the right corpus. Joint strength during dorsoventral (DV) shear in the sagittal plane was examined with the sample placed upright. The left jaw below the premolars was supported by a beveled acrylic plate attached to an adjustable acrylic plate with a screw to secure the superior aspect at the anterior-most molar. Using the compression cell, the unsupported right symphysis posterior to the central incisor was loaded in compression by a flat square metal post at 2.54 cm/min and thus sheared inferiorly versus the fixed left symphyseal plate. Data on the force required to fracture the symphysis under both jaw-loading regimes was recorded in Newtons. To accommodate size variation across the samples, an elliptical approximation of symphyseal cross-section was calculated so as to determine joint load per unit area. The sample included Callithrix jacchus in the “gouging” group, whereas the nongougers consisted of similar-sized sister taxa of Callithrix (Saguinus fuscicollis) and other largerbodied platyrrhines (Saimiri sciureus, Aotus trivirgatus, Cebus apella) a

b

greater rotation and translation of the mandible during jaw opening, respectively, are found consistently in primate and nonprimate mammal exudativores (Dumont 1997; Vinyard et al. 2003). Vinyard et al. (2003) likewise observed a relatively low TMJ above the occlusal plane in cheirogaleids, galagids, and callitrichine gougers and scrapers [but see Dumont (1997) and Burrows and Smith (2005)]. Holding other factors constant, particularly jaw-adductor attachment sites, such a configuration enables increased gape by reducing the amount of stretching in jaw-adductor muscle fibers for a given degree of angular rotation (Herring and Herring 1974; Greaves 1995). Such a finding is further reflected in comparative ontogenetic analyses of galagos, where Euoticus and Otolemur exhibit downward transpositions of their growth trajectories for ramus height as compared to other galagos (Fig. 9.2). Thus, for a given skull size, these two galago genera possess relatively lower TMJs and smaller gonial regions (Ravosa et al. 2010). Interestingly, this mirrors observations regarding reduction of the ascending ramus in cheirogaleids (Viguier 2004). Masseter in-lever arm length is likewise downtransposed in Euoticus and Otolemur, which also would facilitate increased gape by minimizing stretching of masseter muscle fibers (Fig. 9.3). This latter finding also constitutes evidence against the suggestion that exudativores necessarily generate larger bite forces than their sister taxa (Ravosa et al. 2010; see also Williams et al. 2002). The importance of increased gape has been particularly well documented in several studies of the jaw-adductor muscles in callitrichines. In a study of muscle fiber ­architecture, the masseter and temporalis in marmosets are demonstrated to have significantly­longer fibers relative to their incisal biting load arms than tamarins, which

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Fig. 9.2  A plot of ln ascending ramus height vs. ln basicranial length in galagids (adapted from Ravosa et al., 2010). The data for Euoticus and, especially, Otolemur are transposed below those for the remaining galagos, all nine taxa of which are ontogenetically scaled (i.e., Galago, Galagoides). This divergence in Otolemur and Euoticus growth allometries likely reflects a relatively lower temporomandibular joint, which further facilitates increased gape. Therefore, this also may be linked to the unique tree-scraping behaviors of these genera vs. the more generalized dietary proclivities of other galagids. The samples consist of: Galago senegalensis (filled black circle – 73 adults, 41 nonadults); G. s. braccatus (filled black square – 28 adults, 65 nonadults); G. moholi (filled black triangle – 31 adults, 43 nonadults); G. gallarum (open diamond – 5 adults, 3 nonadults); G. matschiei (filled gray triangle – 8 adults, 1 nonadult); Galagoides demidovii (filled inverted gray triangle – 33 adults, 45 nonadults); G. alleni (filled gray circle – 24 adults, 8 nonadults); G. thomasi (open hexagon – 20 adults, 6 nonadults); G. zanzibaricus (open circle – 13 adults, 6 nonadults); Otolemur crassicaudatus (filled inverted black triangle – 42 adults, 38 nonadults); O. garnettii (filled hexagon – 39 adults, 28 nonadults); Euoticus elegantus (filled gray square – 47 adults, 10 nonadults)

is interpreted as an adaptation to facilitate wide gapes and maintain sufficient incisor bites at these wide gapes (Taylor and Vinyard 2004; Taylor et  al. 2009; Eng et  al. 2009). This is particularly important as maximum bite force appears to decrease with widely increased gapes as jaw-muscle fibers are stretched beyond the plateau regions of their length–tension curves (Nordstrom and Yemm 1974; Dechow and Carlson 1990; Dumont and Herrel 2003). Marmosets also are observed to have relatively smaller physiological cross-sectional areas for these jaw adductors as an architectural trade-off of having relatively longer fibers, which further argues against the notion that the masticatory apparatus of these exudate specialists is designed to produce ­relatively larger muscle and bite forces (Taylor and Vinyard 2004; Taylor et al. 2009).

Anterior Dentition A number of dental features have been linked to an exudativorous lifestyle. In Euoticus, this includes procumbent lower incisors and caniniform upper anterior premolars (Charles-Dominique 1977; Nash 1986). Fork-marked lemurs (Phaner

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Fig. 9.3  A plot of In M2 corpus height vs. ln basicranial length in galagids (adapted from Ravosa et al., 2010). The postnatal data for all 12 taxa are ontogenetically scaled. This suggests that interspecific variation in gouging and scraping behavior in galagids does not differentially influence variation in features related to load resistance (due likely to minimal variation in loading parameters across galagids). The samples consist of: Galago senegalensis (filled black circle – 73 adults, 41 nonadults); G. s. braccatus (filled black square – 28 adults, 65 nonadults); G. moholi (filled black triangle – 31 adults, 43 nonadults); G. gallarum (open diamond – 5 adults, 3 nonadults); G. matschiei (filled gray triangle – 8 adults, 1 nonadult); Galagoides demidovii (filled inverted gray triangle – 33 adults, 45 nonadults); G. alleni (filled gray circle – 24 adults, 8 nonadults); G. thomasi (open hexagon – 20 adults, 6 nonadults); G. zanzibaricus (open circle – 13 adults, 6 nonadults); Otolemur crassicaudatus (filled inverted black triangle – 42 adults, 38 nonadults); O. garnettii (filled hexagon – 39 adults, 28 nonadults); Euoticus elegantus (filled gray square – 47 adults, 10 nonadults)

furcifer) possess relatively large upper incisor occlusal edges, relatively thick and elongated tooth combs, and caniniform upper anterior premolars (Eaglen 1986; Nash 1986). Among greater galagos, Otolemur crassicaudatus exhibits more robust and less procumbent incisors than O. garnettii, related presumably to a greater emphasis on gum-scraping behaviors (Nash 1986; Burrows and Smith 2005). An increasing body of comparative evidence has focused on modifications of marmoset anterior teeth that facilitate tree-gouging behaviors. Marmoset incisors have thickened labial enamel and appear to lack lingual enamel, the latter condition existing presumably to ensure the maintenance of sharp edges as the teeth wear (Rosenberger 1978, 1992; Garber 1992; Vinyard et  al. 2009). Marmoset canines also have been reduced in size relative to the remainder of the anterior dentition so that the canine tips are in level with the incisors (irrespective of whether such changes happened in one or both tooth classes – Rosenberger 1992). It is likely this increases the size of the mechanical wedge during gouging by facilitating the use of a greater number of dental elements (Fig.  9.4). Rosenberger (1992) has argued that this crown shape “is conditioned by mechanical consequences related to bark prizing,” (p. 554) in contrast to the tamarins who maintain large, tusk-like canines much more similar to those of non-callitrichine platyrrhine relatives such as Saimiri. Vinyard et al. (2009) concur that the anterior dentition is altered in

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Fig.  9.4  SEM micrograph of anterior dental morphology in a tree-gouging callitrichine (Cebuella). The canine (second tooth from left) and incisors (four teeth to the right of it) have had their cusp tips brought in line with one another so that these teeth can act as a functional unit in gnawing tree bark

marmosets for gouging, emphasizing that it seems to have been modified to maintain sharpness in the cutting edge so as to reduce the amount of force needed to penetrate bark [see also Rosenberger (1978)]. As noted above, there is yet to be any indication that marmoset mandibles resist increased bite forces versus their tamarin cousins. However, it is clear that the anterior dentition of marmosets has undergone evolutionary transformations. Not only are the crown shapes and the enamel distribution different but the anterior teeth are also more procumbent. Thickened labial enamel, coupled with changes in tooth form, suggest that the marmoset teeth themselves must resist increased loading over those of their tamarin relatives. Load resistance during gouging should affect marmoset tooth root morphology, which should, in turn, have some impact upon the bony morphology serving as a framework for these teeth. Even if marmosets do not produce higher bite forces, tree-gouging could still place high stresses on the anterior teeth themselves – higher, at least, than the forces experienced by the anterior dentition of tamarins. Indeed, thickened enamel in marmosets appears to indicate that, even though their bite force ability may be similar to that of tamarins, the loading regime on the anterior dentition of marmosets has changed significantly. Perhaps this represents a putative adaptation to what still seems to be a mechanically demanding feeding regime, especially when considered from a cyclical or repetitive loading standpoint. If the type/location of loading, rather than the magnitude, has affected marmosets in this way, we should expect to find other morphological signs in addition to enamel thickness and tooth form. First, at the histological level, we should expect to see a difference in the patterns of enamel prism orientations between tamarins and marmosets. Enamel prisms are basic microstructural units of mammalian enamel, each one representing a more or less cylindrical bundle of individual enamel crystallites (Boyde 1990; Risnes 1998). Primitive and small mammals with soft, undemanding

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diets generally possess a radial prism pattern in which enamel prisms take a direct path from the enamel–dentine junction (EDJ) to the tooth surface. Larger mammals as well as those with more mechanically demanding diets tend to have a pattern wherein prisms crisscross one another, undulate, and/or travel in bundles whose orientations crisscross relative to adjacent bundles, i.e., Hunter–Schreger bands (von Koenigswald et al. 1987; Boyde 1990). Such crisscrossing enamel is described as decussating. By changing the position of prisms relative to one another, decussating enamel is able to prevent crack propagation through the enamel because any crack that forms between prisms will be more likely to stop when it reaches a prism or group of prisms with a different orientation (e.g., Maas and Dumont 1999; Rensberger 2001). Cracks in radial enamel, on the other hand, are free to travel throughout the enamel from the EDJ to the surface without any sort of structural barrier. Thus, decussating enamel is more likely to save the tooth as a functional structure when mechanical failures such as cracks occur (Figs. 9.5 and 9.6). Based on this mechanical contrast, if the anterior teeth of marmosets resist higher, more frequent and/or more cyclical forces, then one should expect to find more decussation and more organized decussation (i.e., more discrete Hunter–Schreger bands) in the incisors and canines of marmosets as compared to tamarins and other small platyrrhine frugivore/insectivores such as Saimiri. Indeed, this does seem to be the case. Although callitrichine primates are unusual for small mammals in that they contain some decussating enamel among their anterior and posterior teeth unlike such relatives as Saimiri and Aotus (Nogami and Natori 1986; Maas and Dumont 1999; Hogg 2010), histological preparation by one of us (RTH) of canines in Callithrix and Saguinus reveals clear differences with regard to complexity of prism orientation patterns in these teeth. This corroborates the interpretations of an earlier study (Nogami and Natori 1986), which used scanning electron microscopy (SEM) to demonstrate that Callithrix and Cebuella exhibit a greater degree of decussation in their incisors than Saguinus. However, this study did not address any functional or other adaptive significance in these enamel patterns. Circularly polarized light (CPL) microscopy, however, is a better imaging modality than SEM when one is interested in visualizing overall patterns of prism orientation, as CPL emphasizes differences of orientation in crystalline structures over 360° via changes in color contrast which stand out much more readily to the human eye than the patterns visible in SEM or even linearly polarized light [for further discussion see Hogg (2010)]. Imaged in this modality, the Callithrix canine in Fig. 9.7 clearly reveals light and dark bands across large groups of prisms which run from dentine to surface and alternate down the tooth crown. That is, groups of prisms are organized with alternating orientations in Hunter–Schreger bands, as predicted. The Saguinus canine in Fig. 9.8, however, displays a relatively homogenous color scheme which suggests that the structural complexity here is much less (though some crisscrossing of individual prisms can be observed). Other nongouging relatives such as Saimiri and Aotus also display much simpler prism patterns in the anterior dentition (Nogami and Natori 1986; Hogg 2010). Using different imaging modalities, therefore, we can observe that both canines and incisors of marmosets appear to have been remodeled relative to those of nongouging sister taxa.

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Fig. 9.5  Radial prismatic enamel. (a) SEM micrograph of a Saguinus oedipus premolar; (b) Light micrograph of a Saimiri sciureus premolar (field width = 134 mm); (c) Light micrograph of crack propagation in radial enamel of a Saimiri sciureus deciduous premolar. A crack can be seen moving from the tooth surface at the left, all the way to the EDJ. Field width = 110 mm, unmarked arrows indicate prism paths. All teeth imaged using light microscopy were imaged in transmitted light, with phase contrast and circularly polarizing filters. Polarized light is an ideal imaging modality for dental enamel due to the birefringent nature (i.e., ability to decompose light into two rays) of the enamel matrix, which differentially refracts light of different polarizations such that varying orientations of the crystalline enamel matrix cause color variation among regions with differing prism orientations. See Hogg (2010) for more complete imaging and preparation methods

Thus, although musculoskeletal elements of the masticatory apparatus in treegouging marmosets may be better designed to increase gape versus increasing load resistance, the anterior dentition of these animals is specialized for more efficient load transmission and resistance. Whether this adaptation extends across other tree-gouging and scraping primates (e.g., galagos) and mammals, with their varied array of morphologies and behaviors, remains to be further explored, as do adaptations in tooth root form and alveoli for accommodating anterior dental loads. For instance, perhaps one reason marmosets need not produce or dissipate higher masticatory loads when gouging may relate to the fact that they employ a chisel-like, obliquely oriented anterior

Fig.  9.6  Backscattered SEM micrograph of Hunter–Schreger bands, from a Cebus albifrons premolar, revealing details of alternating prism orientation. Note the differing zones in which prisms are transversely oriented with respect to the viewer versus those where they approach the viewer more directly and are more circular in appearance. Also, note the crack moving into the enamel from the dentine on the left, whose propagation has not been able to continue through the enamel

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Fig. 9.8  By contrast, this Saguinus fuscicollis canine reveals little in the way of organized decussation or Hunter–Schreger banding. Some slight differences in prism orientation can be seen, but the homogenous yellow color seen in the enamel in this image reveals that there are no major transitions in direction among large groups of prisms. The lack of prism banding suggests that the enamel of this tooth is not as well adapted to resist high or repetitive loading or to minimize crack propagation under such loads. EDJ enamel–dentine junction (field width = 489 mm)

dentition and shallow angle of jaw closure to puncture and peel apart wood. This contrasts with different behaviors and morphologies employed by platyrrhines that cut or tear across bark fibers (e.g., tufted capuchins – Wright 2005).

Summary and Conclusions This chapter aimed to synthesize available information on exudativory and skull form in primates, reviewing recent comparative and experimental research regarding the musculoskeletal correlates of gouging and scraping behaviors. Indeed, as primate exudativory involves different behavioral strategies to obtain gums and sap, one should not be too surprised that there is some discordance among the comparative evidence regarding the impact of anterior dental loading on load-bearing elements of the masticatory complex. This issue is almost certainly compounded by the fact that gouging and scraping are critical feeding adaptations in some taxa and only seasonally important for others. Put simply, the ecomorphological significance of seasonality in feeding

Fig. 9.7  Numerous distinct Hunter–Schreger bands can be seen here in this canine of a Callithrix humeralifer. These bands appear as alternating light and dark (brownish) areas extending along the crown to the cervix (bottom left corner) and represent an adaptation to fracture resistance under high, more frequent, or repetitive loads in this type of tooth (field width = 1,336 mm; top inset = 380; bottom inset = 384)

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behaviors remains poorly understood (Ravosa et al. 2008), which negatively influences analyses of the impact of fallback foods on skull form as well as our ability to infer feeding behaviors in the fossil record. Perhaps the most clear morphological signal is the evidence regarding a suite of features of the TMJ, ascending ramus, and jawadductor muscles designed to facilitate increased gape and the application of bite forces at wide gapes. As the muscular data are presently available only for marmosets, it is especially important to extend similar analyses to strepsirrhine exudativores. Any review of the state of our knowledge regarding a particular topic would be remiss if it did not it at least attempt to identify outstanding questions that require further attention and potential solutions. As championed by several of the authors cited above, we emphasize an evolutionary morphology approach to more fully understand an exudativore’s lifestyle. For instance, the influence of gouging and scraping on the primate skull is hindered by the lack of studies on feeding performance, food mechanical properties, and mandibular kinematics/kinetics that can be integrated with existing morphological and behavioral data (e.g., Vinyard et  al. 2009). It is our hope that an integrative perspective will prove mutually beneficial to the myriad researchers interested in the evolution of exudativory. Acknowledgments  Anne Burrows and Leanne Nash are thanked for inviting us to contribute to their volume on primate exudativory. For access to cranial collections, thanks are offered to the following curators and staff: M. Rutzmoser (Harvard Museum of Comparative Zoology); R. MacPhee, E. Westwig, G. Musser, S. Anderson, W. Fuchs (American Museum of Natural History); L. Heaney, B. Patterson, W. Stanley, J. Kerbis (Field Museum of Natural History); R. Thorington, L. Gordon (Smithsonian National Museum of Natural History); P. Jenkins (British Museum of Natural History); M. Tranier, J. Roche, D. Goujet, D. Robineau, J. Cuisin, F. Renoult, F. Petter (Muséum National d’Histoire Naturelle); C. Smeenk, M. Hoogmoed, D. Reider (Rijksmuseum van Natuurlijke Historie); R. Angermann (Museum für Naturkunde – Humboldt Universität); T. Daeschler (Academy of Natural Sciences of Philadelphia); C. Cicero, B. Stein (University of California Museum of Vertebrate Zoology); A. Friday (University of Cambridge Department of Zoology); S. McLaren, D. Schlitter (Carnegie Museum of Natural History); W. Van Neer (Koninklijk Museum voor Midden-Afrika); C. Grigson (Odontological Museum – Royal College of Surgeons); G. Lenglet (Institut Royal des Sciences Naturelles de Belgique); R. Kraft (Zoologische Staatssammlung München); G. Storch (Forschungsinstitut und Naturmuseum Senckenberg); and D. Howlett, M. Harman (Powell-Cotton Museum of Natural History). For comments, advice, and the gracious use of their facilities, we thank Alfred Rosenberger, Tim Bromage, John Wahlert, Laurie Godfrey, Tara Peburn, Terence Capellini, Barth Wright, the late Gene Lautenschlager, an anonymous reviewer, as well as the Department of Biomaterials and Biomimetics at NYU College of Dentistry. The research herein was supported by the NSF (BCS0924592 & BCS-0622479), Leakey Foundation, American Philosophical Society, and American Museum of Natural History.

References Bearder, S.K. Doyle, G.A. (1974) Ecology of bushbabies, Galago senegalensis and G. crassicaudatus, with some notes on their behavior in the field. In Martin, R.D., Doyle, G.A. & Walker, A.C. (eds.): Prosimian biology. London: Duckworth. Bearder, S.K. Martin, R.D. (1980) Acacia gum and its use by bushbabies, Galago senegalensis (Primates: Lorisidae). Int. J. Primatol. 1:103–128.

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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, C.J., Ryan, T.M. (2006) Cross-sectional bone distribution in the mandibles of gouging and non-gouging Platyrrhini. Int. J. Primatol. 27:1461–1490. Vinyard, C.J., Wall, C.E., Williams, S.H., Hylander, W.L. (2003) Comparative functional analysis of skull morphology of tree-gouging primates. Am. J. Phys. Anthropol. 120:153–170. Vinyard, C.J., Wall, C.E., Williams, S.H., Hylander, W.L. (2008) Patterns of variation across primates in jaw-muscle electromyography during mastication. Int. Comp. Biol. 48:294–311. Vinyard, C.J., Wall, C.E., Williams, S.H., Mork, A.L., Garner, B.A., Melo, L.C.O., ValençaMontenegro, M.M., Valle, Y.B.M., Monteiro da Cruz, M.A.O., Lucas, P.W., Schmitt, D., Taylor, A.B., Hylander, W.L. (2009) The evolutionary morphology of tree gouging in ­marmosets. In Ford, S.M., Davis, L.C. & Porter, L.M. (eds.): The smallest anthropoids: The marmoset/ callimico radiation. New York: Springer Academic Publishers. Von Koenigswald, W., Rensberger, J.M., Pretzschner, H.U. (1987) Changes in the tooth enamel of early Paleocene mammals allowing increased diet diversity. Nature 328:150–152. Williams, S.H., Wall, C.E., Vinyard, C.J., Hylander, W.L. (2002) A biomechanical of skull form in gum-harvesting galagids. Folia Primatol. 73:197–209. Wright, B.W. (2005) Craniodental biomechanics and dietary toughness in the genus Cebus. J. Human Evol. 48:473–492. Wright, B.W., Ulibarri, L., O’Brien, J., Sadler, B., Prodham, R., Covert, H.H., Nadler, T. (2008) It’s tough out there: Variation in the toughness of ingested leaves and feeding behavior among four colobine in Vietnam. Int. J. Primatol. 29:1455–1466.

Chapter 10

A Comparative Analysis of the Articular Cartilage in the Temporomandibular Joint of Gouging and Nongouging New World Monkeys Amy L. Mork, Walter E. Horton, and Christopher J. Vinyard

Abstract  Both laboratory and field data demonstrate that marmosets gouge trees with wide jaw gapes to elicit exudate flow. Tree gouging distinguishes marmosets from other platyrrhines and presents a natural experiment for studying the morphological consequences of this derived feeding behavior. We utilize comparative histomorphometrics to determine whether loading of the TMJ at wide jaw gapes impacts articular cartilage form in two habitual gouging species, common (Callitrix jacchus) and pygmy marmosets (Cebuella pygmaea), compared to nongouging cotton-top tamarins (Saguinus oedipus) and squirrel monkeys (Saimiri sciureus). Our histological comparisons found no difference in articular cartilage form along the posterior condyle between gouging and nongouging species. Alternatively, the anterior glenoid of gouging species was relatively larger and deeper compared to nongouging species. These findings suggest that the articular cartilage of the anterior glenoid in gouging species possesses improved load resistance ability and points to the mosaic nature of functional responses to tree gouging in the marmoset masticatory apparatus.

Introduction Callitrichids are an ecologically diverse radiation of small-bodied primates (100–750 g) inhabiting Central and South America (Fleagle 1999). Callitrichids include three groups: Goeldi’s monkeys (Callimico), tamarins (Saguinus, Leontopithecus), and marmosets (Callithrix, Cebuella). Members of all the three groups are adept at clinging to large vertical supports to access a high-energy diet of fruit, insects, and tree exudates (Sussman and Kinzey 1984; Rosenberger 1992; Garber et al. 1996).

A.L. Mork (*) Department of Anatomy and Neurobiology, Northeastern Ohio Universities College of Medicine (NEOUCOM), Rootstown, OH 44272, USA 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_10, © Springer Science+Business Media, LLC 2010

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Marmosets differ from other callitrichids in that they actively stimulate tree exudate flow by biting trees with their anterior teeth (Kinzey et al. 1975; CoimbraFilho and Mittermeier 1977). This type of biting behavior has been defined as gouging (Stevenson and Rylands 1988). The mechanics of tree gouging involve anchoring the maxillary incisors into the tree and using the mandibular incisors to remove layers of bark from the tree’s surface, resulting in the flow of sap or gum from the tree as a protective response (Coimbra-Filho and Mittermeier 1977). Marmosets return to feed on these exudates. Seasonally, exudates comprise a significant part of the marmoset diet suggesting the possibility of functional adaptive and/or natural selective changes in masticatory apparatus form related to this feeding behavior.

The Marmoset Masticatory Apparatus and Gouging at Wide Jaw Gapes It has been demonstrated in both the laboratory and the field that marmosets gouge using wide gapes, but not necessarily relatively large bite forces (Vinyard et  al. 2009). Marmoset skulls and jaw muscles exhibit musculoskeletal features that facilitate biting at wide jaw gapes during gouging compared to closely related, nongouging taxa (Vinyard et al. 2003, 2009; Taylor and Vinyard 2004; Taylor et al. 2009). Skull features facilitating tree gouging at wide gapes include lower condylar heights relative to the tooth row and anterior–posterior elongated mandibular condyles and glenoid (i.e., temporal) articular surfaces. Lower relative condylar heights have been posited to reduce the amount of masseter muscle stretch at wide gapes, thus potentially increasing maximum gapes (Herring and Herring 1974) as well as increase bite force at wide gapes (Eng et  al. 2009). The anteroposterior elongation of the mandibular condyle and glenoid articular surfaces facilitate wide gape by increasing the articular surface area available for condylar rotation and translation, respectively (Vinyard et  al. 2003). Jaw-muscle features facilitating wide gapes during tree gouging include relatively longer jaw-muscle fiber lengths that allow increased whole-muscle stretch (Taylor and Vinyard 2004; Taylor et al. 2009).

Form and Function of Temporomandibular Joint Articular Cartilage and Gouging The observed differences in musculoskeletal morphology between tree-gouging and closely related, nongouging species provide expectations for subsequent functional comparisons of temporomandibular joint (TMJ) cartilage form. The goal of this study is to determine whether the TMJ articular cartilage of marmosets exhibits morphological differences, relative to nongouging platyrrhines, that can be

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f­ unctionally linked to tree gouging. Habitual tree gouging at wide gapes likely involves novel articular surface contacts and hence different loading patterns in the TMJ relative to nongouging primates. These novel patterns of load distribution throughout the TMJ may affect the structural composition of the articular cartilage layers that overlie the condylar and glenoid articular surfaces. Articular cartilage is a specialized connective tissue with a large extracellular matrix component composed of a dense collagen fiber network, high concentration of proteoglycans, as well as a smaller amount of other matrix proteins (Mow et al. 1992; Dijkgraaf et al. 1995; Benjamin and Ralphs 2004). The physical and mechanical properties of articular cartilage are dependent upon the integrity of the collagen network as well as the synthesis and retention of a high concentration of proteoglycans (Dijkgraaf et al. 1995; Silver 2006; Kuroda et al. 2009; Singh and Detamore 2009a). The articular cartilage of the TMJ provides both the condylar and the glenoid articular surfaces with joint mobility at low frictional coefficients and the ability to withstand compressive forces (Mow et al. 1992; Knudson and Knudson 2001; Kuroda et al. 2009). This capacity to resist compressive forces during routine loading is achieved by safely distributing loading stresses throughout the tissue without incurring permanent tissue damage (Freeman and Kempson 1973). Physical properties of connective tissues depend on differing proportions of proteoglycans and structural proteins (e.g., collagen) and how these constituent molecules are organized within the extracellular matrix (Kuettner and Kimura 1985; Mow et al. 1992; Kuroda et al. 2009; Singh and Detamore 2009a). While the tensile strength of articular cartilage is primarily ascribed to the collagen fiber network, the compressive stiffness of articular cartilage is often linked to the percentage of proteoglycans (Kempson et al. 1970; Mizoguchi et al. 1996; Huang et al. 2001; Singh and Detamore 2009a). Proteoglycans provide hydration and swelling pressure to the tissue to enable it to withstand compressive forces (Mow et al. 1992; Yanagishita 1993; Dijkgraaf et al. 1995; Knudson and Knudson 2001; Silver 2006). Proteoglycans are macromolecules composed of glycosylated core proteins and covalently attached highly anionic ­glycosaminoglycans. The highly negatively charged glycosaminoglycans attract and bind water molecules within the articular cartilage. The osmotic swelling pressure of the proteoglycan-laden cartilage enables the tissue to resist compressional forces in load bearing joints (Hardingham and Bayliss 1990; Mow et al. 1992). Cartilage subjected to high (but not pathological) levels of loading can display increased proteoglycan content compared to cartilage exposed to low levels of loading (Slowman and Brandt 1986; Kiviranta et  al. 1987). Articular cartilage can respond to regular loading by increasing thickness at the site of loading (Kiviranta et al. 1987, 1988). Thickening of the articular cartilage has been interpreted as a localized tissue adaptation to loading (Tanaka et  al. 2006; Singh and Detamore 2009b) and may result from stimulation of cartilage cells to increase the synthesis of extracellular matrix components (Mussa et  al. 1999; Singh and Detamore 2009a). Furthermore, Singh and Detamore (2009b) report that increased cartilage thickness is correlated with increased stiffness in pig condylar cartilage. Proteoglycan distribution and compressive stiffness differ across regions of TMJ cartilage

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(Mizoguchi et al. 1996; Hu et al. 2001; Patel and Mao 2003; Tanaka et al. 2006; Singh and Detamore 2009a, b). Collectively, these functional studies highlight the possibility of differential loading within the joint as well as tissue responses to loading involving increased cartilage thickness and proteoglycan content. As a caveat, however, it is important to recognize that articular cartilage in the TMJ can also degrade both in quantitative dimensions and proteoglycan content as loading persists and/or becomes pathological (Ravosa et al. 2007; Chen et al. 2008).

Hypothesis and Predictions We use histomorphometrics to compare TMJ articular cartilage in tree-gouging common (Callithrix jacchus) and pygmy marmosets (Cebuella pygmaea) to nongouging cotton-top tamarins (Saguinus oedipus) and squirrel monkeys (Saimiri sciureus). Both common and pygmy marmosets habitually gouge trees to elicit exudate flow prior to consumption of the gums and saps (Nash 1986). Like marmosets, cotton-top tamarins rely on fruit and insects for large portions of their diet, but only opportunistically feed on previously exuded gums and saps (Nash 1986; Fleagle 1999). Squirrel monkeys are almost exclusively frugivorous and insectivorous, consuming little if any sap or gum except on an opportunistic basis (Sussman and Kinzey 1984; Garber 1980, 1992; Ferrari 1993). Therefore, while marmosets and tamarins both consume tree exudates in their diets, methods of procurement differ in such a way to create a natural experiment for determining the influence of habitual tree-gouging on TMJ articular cartilage form by comparing marmosets to tamarins and squirrel monkeys. We test the hypothesis that regions of the articular cartilage potentially subjected to increased loading (either percentage or magnitude) during gouging will exhibit relatively increased cartilage thickness and total area as well as relatively higher densities of proteoglycans in gouging species compared to nongouging species. Tree-gouging marmosets load their TMJs at wide gapes (Vinyard et al. 2003, 2009). When biting at these wide gapes, the mandibular condyle is rotated to contact the glenoid on the posterior condylar surface and translated onto the anterior extent of the glenoid. This wide-gaped position may create novel loading environments in the posterior portion of the condyle and anterior extent of the glenoid articular cartilage. Relatively thicker and/or proteoglycan-rich articular cartilage in these regions of gouging species would suggest a relatively increased capacity to resist compressive loads. Based on these functional observations, we examine three predictions.

Prediction One Gouging primates will exhibit relatively larger total articular cartilage area in the posterior condyle and anterior glenoid regions of the TMJ compared to nongouging tamarins and squirrel monkeys.

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Prediction Two Gouging primates will display relatively thicker cartilage in the posterior condyle and anterior glenoid portions of the TMJ when compared with nongouging tamarins and squirrel monkeys. Prediction Three Gouging primates will display relatively increased proteoglycan densities in the posterior condyle and anterior glenoid articular surfaces of the TMJ compared with nongouging tamarins and squirrel monkeys.

Materials and Methods Samples We analyzed ten individuals from gouging species (five Callithrix jacchus, five Cebuella pygmaea) and eight individuals from nongouging species (five Saguinus oedipus, three Saimiri sciureus). A near equal ratio of males and females was examined in each species. All specimens were captive bred adults with known ages ranging from 4 to 15 years (Table 10.1). Table 10.1  Gouging and nongouging platyrrhine sample Speciesa Sexb Age at death (in years) M 12 Callithrix jacchus Callithrix jacchus M 5 Callithrix jacchus F 11 Callithrix jacchus F 12 Callithrix jacchus F 10 Cebuella pygmaea M 4 Cebuella pygmaea F 4 Cebuella pygmaea F – Cebuella pygmaea M – Cebuella pygmaea F 4 Saguinus oedipus F 4 Saguinus oedipus M 15 Saguinus oedipus M >14 years Saguinus oedipus F 14 Saguinus oedipus – – Saimiri sciureus F >12 years Saimiri sciureus F – M – Saimiri sciureus a  Gouging species include C. jacchus and C. pygmaea. Nongougers include S. oedipus and Sa. sciureus b  M = male, F = female, “–” = unknown

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Histology TMJs were removed en bloc from formalin-fixed specimens and decalcified in 10% EDTA for an average of 6 weeks. Following decalcification, one TMJ from each individual was selected for paraffin embedding based on which joint demonstrated the most intact association of the joint capsule after being trimmed of excess tissue. We then processed and embedded TMJs in paraffin, using standard histological techniques (Presnell et al. 1997). TMJs were serially sliced in a sagittal orientation into 10-µm thick sections. Every other set of three sections was slide mounted. We stained TMJ sections with Thionin (0.1%) to observe basic cartilage morphology and to determine the relative distribution of proteoglycans in the articular cartilage (Bulstra et  al. 1993). Thionin has been demonstrated to be an effective cationic dye for proteoglycan density analysis (Király et al. 1996). We identified a representative section for analysis that was within five percent of the midline based on serial sectioning data and morphological details. We created a 10× montage image for this section for subsequent measurement using BioQuant Osteo II version 8.00.20 software.

Histomorphometric Measurements of Temporomandibular Joint Cartilage Measurements were performed on 10× digital montages of each histological section. We measured length, area, and depth of the articular cartilage, as well as proteoglycan density, multiple times and reported the average for each. The anterior and posterior limits of the functional articular surface for both the condyle and glenoid were defined as the anterior and posterior insertion points of the TMJ disc, providing morphological boundaries for the measurements included in this analysis (Fig. 10.1a). Cartilage Arc Lengths We measured the arcs of the condylar and glenoid articular surfaces as the linear distance from anterior to posterior fibrous insertions of the disc (Fig. 10.1b). This arc was then used to equally divide the articular cartilage of the condyle and glenoid surfaces into anterior, middle, and posterior segments (Fig. 10.1a). We used these regional designations to divide the articular cartilage into functional zones for subsequent measurement and hypothesis testing.

Cartilage Area We measured condylar cartilage cross-sectional area in lateral view as the area bounded by the anterior and posterior disc insertions, the superior articular surface

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Fig. 10.1  A lateral-view schematic through the midline of a primate TMJ depicting our (a) designation of cartilage regions and (b) metric dimensions. In (a), the anterior and posterior boundaries for the cartilage articular surface are taken from the anterior and posterior attachment sites of the articular disc to the articular cartilage, respectively (white arrows). Based on these defined limits for the articular cartilage, we divided the condylar and glenoid cartilage into anterior, middle, and posterior zones (black arrows). In (b), the arc length of the cartilage is demonstrated for the glenoid (dotted white line) as the distance between anterior and posterior attachment sites. Schematic representations of cartilage area (hatched space) in the anterior condylar zone and cartilage depth throughout the posterior condylar zone (spaced white arrows) are also shown

of the condylar cartilage, and the inferior depth of the articular cartilage as ­distinguished from subchondral bone (Fig. 10.1b). The glenoid cartilage area was measured as the area bounded by the anterior and posterior disc insertions, the inferior articular surface of the articular cartilage, and the superior border that ­distinguishes articular cartilage from subchondral bone. We measured condylar and

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glenoid ­cartilage areas for the total cartilage area, as well as anterior, middle, and posterior zones. Each of these boundaries was traced on a montage image and areas were calculated using Bioquant software. Cartilage Depth We measured cartilage depth for the condylar and glenoid articular surfaces as the distance from the articular surface of the cartilage to the transition from articular cartilage to subchondral bone (Fig. 10.1b). Depths were taken at 10 µm intervals beginning at the anterior insertion of the disc. The mean of these values was used to estimate average depth for the total articular cartilage, as well as for each of the three designated zones. Proteoglycan Density Metachromasia, a chromatic shift of Thionin staining that occurs in the presence of proteoglycans (Bulstra et al. 1993; Király et al. 1996), was evaluated following the establishment of a standardized specimen-specific threshold, using maximum staining intensity observed within the anterior zone of each specimen as a minimum criterion for the presence of metachromasia (Fig. 10.2). The area of metachromatic proteoglycan staining was measured, based on this specimen-specific threshold, for the total condylar and glenoid articular cartilage, as well as within each of the divisional zones. Proteoglycan staining density is reported as the percentage of the area of the cartilage that is metachromatic.

Fig.  10.2  A lateral-view section through the midline of a Saguinus oedipus TMJ stained with 0.1% Thionin. The arrow points to a more darkly stained region in the condylar articular cartilage demonstrating metachromasia (magnification = 10×)

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Analysis We created ratios of anterior to posterior cartilage dimensions for each specimen and used these ratios in testing our hypothesis rather than absolute dimensions. By analyzing ratios created from the same individual, we adjust for variation in body size (which was largely unavailable for these specimens), age-related changes in joint morphology, tissue preservation and tissue fixation, and histological staining. Our approach assumes that areas of the TMJ not routinely loaded during gouging at wide gapes (i.e., the anterior surface of the condyle and posterior surface of the glenoid) are relatively similar across gouging and nongouging species. Initially, we applied a one-way analysis of variance (ANOVA) to determine whether the two gouging species (C. jacchus and C. pygmaea) and the two nongouging species (S. oedipus and Sa. sciureus) differed from each other in their anteroposterior ratios for different cartilage dimensions. In both cases, we found no significant differences within gouging or within nongouging species. Therefore, we grouped the two gouging species together and the two nongouging species in a second group for hypothesis testing. We used one-way ANOVA to determine whether anteroposterior ratios differed significantly between gougers and nongougers as predicted by our hypothesis. All statistical tests were performed in Systat (11.0).

Results Histomorphology of the TMJ and Cartilage Arc Length The four monkey species share a basic similarity in the histomorphology of their TMJs (Fig. 10.3). Like most other primates, the articular surface of the glenoid is markedly longer and flatter than the articular surface of the condyle in each species (Table 10.2). The articular disc maintains a narrow central region that fans out both anteriorly and posteriorly at the discal attachments. The lateral pterygoid muscle attaches to the anterior extent of this disc. In summary, we see little evidence that tree-gouging marmosets have undergone a major reorganization of the soft tissue structures in their TMJs. A more in depth examination of the quantitative details of articular cartilage form begins to uncover subtle differences between gouging and nongouging species. Although the average arc length of the articular cartilage does not differ significantly among species for the condyle (P = 0.89) or glenoid (P = 0.24) (Table 10.2), the comparison of absolute size suggests that gougers often have relatively longer arc lengths. Despite their small size, the absolute length of the condylar articular surface in C. pygmaea is equal to S. oedipus (Table 10.2). Thus, the ratio of condylar arc length to jaw length is much larger in C. pygmaea compared to the other species. Both gouging species maintain relatively longer glenoid articular surfaces compared with nongouging species. These relatively longer articular surfaces may

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Fig.  10.3  Lateral-view histological slides of (a) Callithrix jacchus, (b) Cebuella pygmaea, (c) Saguinus oedipus, and (d) Saimiri sciureus. (Note the tear in the posterior articular disc of this specimen). In each slide, anterior is to the left and superior is at the top. All slides were stained with 0.1% Thionin (magnification = 10×)

facilitate increased range of motion at the TMJ related to generating wide jaw gapes during gouging.

Area The anteroposterior ratio for condylar area shows no significant difference in articular cartilage area between gouging and nongouging species (Table  10.3a; Fig. 10.4a). These results fail to support the predicted relative increase in articular cartilage area in the posterior condyle of tree gouging marmosets. Only C. jacchus among marmosets follows the predicted pattern in displaying the lowest anteroposterior condylar area ratio (Fig. 10.4a). Glenoid anteroposterior area ratios differ significantly between gouging and nongouging species (ANOVA, P < 0.0007) (Table  10.3b; Fig.  10.4a). The ­significantly larger ratio in marmosets, indicating a relatively increased anterior

Saguinus oedipus 2.22 (0.97) 4.14 (1.39) Saguinus oedipus 30.41 0.073 0.136

Cebuella pygmaea 2.22 (0.40) 3.04 (0.55) Cebuella pygmaea 19.53 0.114 0.156

Saimiri sciureus 32.30 0.058 0.137

Saimiri sciureus 1.87 (1.22) 4.41 (0.52)

b

a

 P-values from one-way ANOVA comparing arc lengths among species  Mean (S.D.) c  Jaw length data taken from adult skeletons of C. jacchus (n = 30), C. pygmaea (n = 26), S. oedipus (n = 22), and Sa. sciureus (n = 19) d  Arc length to jaw length ratios are based on species means as jaw length measurements were unavailable for the histological sample

(a) Arc lengths Arc length (mm) Callithrix jacchus Condylar arc 1.86 (0.89)b Glenoid arc 4.23 (1.07) (b) Ratios of arc length to jaw length Variable (mm) Callithrix jacchus Jaw lengthc 26.78 Condyle arc/jaw lengthd 0.069 Glenoid arc/jaw length 0.158

Table 10.2  Condyle and glenoid cartilage (a) arc lengths and (b) ratios of arc length to jaw length for gouging and nongouging species

– – –

–

ANOVAa P = 0.89 P = 0.24

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Callithrix jacchus 0.158 (0.06) 0.143 (0.03) 0.45 (0.10) 1.08 (0.16)

(b) Glenoid areas Area measurements (mm2) Anterior area Posterior area Total area Anterior/posterior ratio Cebuella pygmaea 0.132 (0.04) 0.104 (0.04) 0.34 (0.11) 1.31 (0.29)

Cebuella pygmaea 0.063 (0.02) 0.068 (0.01) 0.21 (0.03) 0.96 (0.37) Saguinus oedipus 0.056 (0.03) 0.073 (0.04) 0.18 (0.09) 0.79 (0.10)

Saguinus oedipus 0.062 (0.04) 0.059 (0.03) 0.19 (0.10) 0.99 (0.23)

Saimiri sciureus 0.230 (0.07) 0.402 (0.23) 0.94 (0.35) 0.67 (0.30)

Saimiri sciureus 0.061 (0.05) 0.070 (0.05) 0.22 (0.20) 0.81 (0.12)

ANOVA – – – P = 0.0007 G > NG

ANOVAa – – – P = 0.17

a

 P-values from one-way ANOVA comparing anteroposterior area ratios between gouging and nongouging species. Bold P-values are significant. “G” = gouging species. “NG” = nongouging species b  Mean (S.D.)

Callithrix jacchus 0.059 (0.04)b 0.103 (0.08) 0.25 (0.20) 0.61 (0.28)

(a) Condyle areas Area measurements (mm2) Anterior area Posterior area Total area Anterior/posterior ratio

Table 10.3  Comparison of (a) condyle and (b) glenoid area measurements and ratios for gouging and nongouging species

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Fig.  10.4  Boxplots comparing the anteroposterior ratios for (a) area, (b) depth, and (c) percent metachromasia in the condyle and glenoid articular cartilage of gouging and nongouging platyrrhines

cartilage area, supports the predicted increase in load resisting ability along the anterior surface of the glenoid linked to tree gouging at wide gapes.

Depth Prediction two states that gouging primates will display increased relative articular cartilage thickness in the posterior condyle and anterior glenoid, compared to nongouging primates. Ratios of anteroposterior articular cartilage depth for the condyle follow the pattern observed for anteroposterior area ratios and fail to demonstrate any statistical difference between gouging and nongouging groups (Table  10.4b, Fig.  10.4b). Common marmosets exhibit posterior condylar depths

Cebuella pygmaea 0.100 (0.03) 0.101 (0.03) 0.103 (0.02) 1.04 (0.38) Cebuella pygmaea 0.143 (0.02) 0.127 (0.03) 0.131 (0.02) 1.19 (0.43)

Callithrix jacchus 0.089 (0.05)b 0.169 (0.11) 0.131 (0.08) 0.60 (0.27)

Callithrix jacchus 0.137 (0.05) 0.129 (0.05) 0.130 (0.05) 1.05 (0.11)

Saguinus oedipus 0.073 (0.03) 0.081 (0.04) 0.074 (0.03) 0.94 (0.14)

Saguinus oedipus 0.088 (0.02) 0.088 (0.01) 0.090 (0.01) 0.99 (0.13)

Saimiri sciureus 0.153 (0.05) 0.279 (0.16) 0.209 (0.08) 0.67 (0.32)

Saimiri sciureus 0.101 (0.01) 0.099 (0.02) 0.113 (0.03) 1.04 (0.19)

ANOVA – – – P = 0.046 G > NG

ANOVAa – – – P = 0.20

a

P-values from one-way ANOVA comparing anteroposterior depth ratios between gouging and nongouging species. Bold P-values are significant. “G” = gouging species. “NG” = nongouging species b Mean (S.D.)

(a) Condyle depths Depth measurements (mm) Anterior depth Posterior depth Total depth Anterior/posterior ratio (b) Glenoid depths Depth measurements (mm) Anterior depth Posterior depth Total average depth Anterior/posterior ratio

Table 10.4  Comparison of (a) condyle and (b) glenoid depth measurements and ratios for gouging and nongouging species

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that are nearly twice the anterior depth, while the remaining species maintain near equal ratios of cartilage depths between regions. The glenoid anteroposterior depth ratios support the predicted pattern as the gouging species exhibit a significantly higher ratio compared to the nongouging platyrrhines (Table 10.4b; Fig. 10.4b). Both relative depth and area of the glenoid articular cartilage would provide increased load resistance ability for loading along the anterior extent of the glenoid articular surface.

Proteoglycan Density (Metachromasia) Prediction Three states that gouging primates will display relatively greater proteoglycan density in the articular cartilage of the posterior condyle and the anterior glenoid. Neither of the anteroposterior ratios for condyle or glenoid metachromasia exhibit significant differences between gouging and nongouging species (Table 10.5, Fig. 10.4c). We see little evidence linking variation in proteoglycan density to novel loading patterns related to tree gouging.

Discussion Tree gouging marmosets load their TMJs at wide jaw gapes when biting trees to remove bark layers and provoke exudate flow (Vinyard et al. 2009). Because opening the jaw involves condylar rotation and anterior translation on the glenoid, gouging at wide gapes likely results in a relatively unusual loading pattern in the TMJ where the posterior surface of the condyle and the anterior surface of the glenoid experience an increased frequency of loading compared to nongouging primates. Based on these functional and behavioral scenarios, we predicted that the articular cartilage in the posterior condyle and anterior glenoid would be relatively larger, thicker and show a higher percentage of proteoglycans to provide increased load resistance abilities in gouging marmosets. Our comparative analysis of articular cartilage morphology in gouging and nongouging platyrrhines yielded mixed results. Marmosets demonstrated relatively larger and thicker articular cartilage in the anterior glenoid compared to nongougers. The posterior condylar articular cartilage did not differ consistently between gouging and nongouging species. The relative density of proteoglycans did not differ in either the condyle or glenoid cartilages. As typical of many comparative studies, it is difficult to provide a single straightforward interpretation of this mixed pattern of results. In part, we lack sufficient comparative data from other species to assess whether these findings are characteristic of primates exhibiting similar variation in feeding behaviors. Additionally, experimental studies have yielded a range of different, and sometimes conflicting, results when addressing how loading impacts TMJ articular cartilage form

Cebuella pygmaea 0.43 (0.10) 0.30 (0.11) 0.41 (0.06) 1.63 (0.91) Cebuella pygmaea 0.29 (0.10) 0.46 (0.19) 0.40 (0.09) 0.86 (0.78)

Callithrix jacchus 0.46 (0.18)b 0.27 (0.15) 0.38 (0.16) 1.92 (0.65)

Callithrix jacchus 0.09 (0.07) 0.34 (0.23) 0.24 (0.21) 0.27 (0.04)

Saguinus oedipus 0.22 (0.16) 0.37 (0.22) 0.33 (0.17) 0.60 (0.31)

Saguinus oedipus 0.34 (0.06) 0.22 (0.08) 0.32 (0.09) 1.82 (0.91)

Saimiri sciureus 0.19 (0.14) 0.20 (0.09) 0.22 (0.12) 0.91 (0.51)

Saimiri sciureus 0.41 (0.04) 0.14 (0.05) 0.23 (0.05) 3.17 (0.87)

b

a

 P-values from one-way ANOVA comparing anteroposterior% metachromasia ratios between gouging and nongouging species  Mean (S.D.)

(a) Condyle metachromasia Percentage metachromasia (%) Anterior metachromasia Posterior metachromasia Total metachromasia Anterior/posterior ratio (b) Glenoid metachromasia Percentage metachromasia (%) Anterior metachromasia Posterior metachromasia Total metachromasia Anterior/posterior ratio

ANOVA – – – P = 0.53

ANOVAa – – – P = 0.22

Table 10.5  Comparison of (a) condyle and (b) glenoid percentage areas of metachromasia measurements and ratios for gouging and nongouging species

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(e.g., Bouvier and Hylander 1982; Ravosa et al. 2007). We consider both of these issues in assessing how tree gouging impacts TMJ articular cartilage. In the end, we acknowledge that the strength of our results will be documenting the interspecific variation in articular cartilage form and highlighting areas for future work studying the evolutionary morphology of TMJ articular cartilage in primates.

The Evolutionary Morphology of TMJ Articular Cartilage in Primates In vivo studies demonstrate that the TMJ is a load-bearing joint with the largest loads often occurring during incision (Hylander 1979a; Hylander and Bays 1979; Boyd et  al. 1990). Numerous comparative analyses of TMJ skeletons across primates have correlated dietary and behavioral variation with the relative area, width, and length of the condyle as well as anteroposterior glenoid length (Hylander 1979b; Smith et al. 1983; Bouvier 1986; Wall 1999; Williams et al. 2002; Vinyard et al. 2003; Taylor 2005). As a relevant example, marmoset skulls possess relatively elongated condyles and glenoids compared to tamarins (Vinyard et al. 2003). There have been far fewer studies that consider morphological variation in TMJ articular cartilage of primates. A significant percentage of the studies examining TMJ articular cartilage across primates assess a single species, such as macaques (Tong and Tideman 2001), baboons (Milam et al. 1991), or marmosets (Wilson and Gardner 1982; Robinson and Poswillo 1994), often considering their potential as clinical models for studying human TMJs. There have been relatively few studies of articular cartilage growth with available studies documenting embryonic and/or postnatal ontogeny in macaques (Kanouse et  al. 1969; Carlson et  al. 1978; Hinton and Carlson 1983; Luder and Schroeder 1990, 1992) and marmosets (Wilson and Gardner 1982; Robinson and Poswillo 1994). Burrows and Smith (2007) provide the only other interspecific analysis of articular cartilage in primates. They compare articular cartilage in Otolemur crassicaudatus and O. garnetti and generate hypotheses relating variation between species to differences in diet and joint loading. Quantitative data on articular cartilage morphology only exists for macaques (Carlson et  al. 1978; Bouvier and Hylander 1982; Hinton and Carlson 1983). Given the paucity of descriptive studies of TMJ articular cartilage, we have limited opportunities to compare results from these four platyrrhines to other primates. The major qualitative differences observed between galago species by Burrows and Smith (2007) involved relative cartilage thickness and cellularity between midline and lateral regions. We focused on variation along an anteroposterior axis making it difficult to compare results between these two studies. We can compare quantitative measures of articular depth at homologous sites in these four platyrrhines to similar data collected on rhesus macaques (Macaca mulatta) (Carlson et al. 1978; Hinton and Carlson 1983). Adult rhesus macaques exhibit much larger condylar cartilage depths at anterior (0.26 mm) and posterior (0.25 mm) sites

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along the midline (Carlson et  al. 1978; see also Bouvier and Hylander 1982) ­compared to the four platyrrhines (Table 10.4a). This is a reasonable outcome given the larger size of macaques. With the exception of the low anteroposterior condylar depth ratio in C. jacchus (0.60), macaques maintain a similar anteroposterior ratio (1.05) to the remaining platyrrhines (Table 10.4a). When scaled relative to jaw length (80  mm for adult rhesus macaques; n = 19), the relative anteroposterior depth in macaques (0.0031) is similar to S. oedipus (0.0029) and Sa. sciureus (0.0031), but noticeably smaller than both C. jacchus (0.0063) and C. pygmaea (0.0052). These results suggest a relative similarity among macaques, tamarins, and squirrel monkeys and point to a potential increase in load resistance ability relative to an external load arm during incisal biting (i.e., jaw length) in the two marmosets. The glenoid of rhesus macaques is absolutely thin anteriorly (0.077 mm) and intermediate posteriorly (0.184 mm) compared to the four platyrrhines (Table 10.4b). This translates into a much lower anteroposterior glenoid depth ratio (0.42) in M. mulatta compared with New World monkeys (Table  10.4b). When scaled to jaw length, the relative anterior depth of macaques (0.00096) is markedly smaller than S. oedipus (0.0024), Sa. sciureus (0.0047), C. jacchus (0.0051), and C. pygmaea (0.0073). Interestingly, marmosets exhibit the largest anterior depths relative to jaw length supporting the hypothesis tests comparing anteroposterior depth ratios. In sum, we see preliminary evidence suggesting a size-related decrease in relative articular depth across anthropoids coupled with a relative increase in load resistance ability in marmosets compared to other monkeys. Despite these interesting preliminary comparisons, we still know very little about the evolutionary morphology of TMJ articular cartilage in primates. In fact, most of what we know comes from non-histological studies. In vivo experiments demonstrate that articular cartilage bears loads, and comparative morphometrics of the underlying TMJ skeleton suggest that morphological variation relates to diet and function. Given that it has been at least 40 years since the earliest descriptions of primate articular cartilage (Kanouse et al. 1969) and this study nearly doubles the interspecific primate sample, future progress in understanding the evolutionary morphology of primate TMJ articular cartilage hinges on gathering additional data across primates.

Unraveling the Complexity of Articular Cartilage Function The mosaic nature of our hypothesis test results lends itself to multiple interpretations. We can reasonably argue that the increased relative thickness and size of the anterior glenoid in tree gouging marmosets provides increased load-resisting ability compared to nongouging platyrrhines. Although we cannot definitively identify where the glenoid is loaded during gouging at wide gapes, these results support the hypothesis that relative increases in anterior cartilage size and thickness are responses to repetitive gouging at wide gapes. The interpretation of our results comparing condylar articular cartilages is less clear. The lack of statistically significant differences suggests a similarity in relative

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load resisting capacity in the posterior condyle across these four species. Relative to our hypothesis, we could interpret this similarity to indicate that condylar articular cartilage is not loaded as we hypothesize, that the cartilage is overbuilt relative to the increased loading frequency experienced during gouging, and/or that the magnitude of loading in the posterior condyle during gouging is not sufficient to elicit a physiological or evolutionary response in these tissues. Deciding among these various interpretations relies on incorporating our results with existing comparative and experimental evidence describing articular cartilage form and function. We have already noted the lack of comparative data from primates. Experimental studies on articular cartilage form and function also leave a number of questions that need to be addressed to further our understanding of articular cartilage function. In large part, these questions relate to identifying where loads are in the joint, quantifying their magnitude and frequency as well as how they impact cellular responses, and determining how cellular responses change with age. There is no doubt the articular cartilage in the primate TMJ is load bearing (Hylander 1979a; Hylander and Bays 1979; Boyd et  al. 1990). It is, however, unclear what the magnitude, location, and distribution of these loads are during various behaviors. Early strain gage studies suggested that reaction forces are unevenly distributed throughout the TMJ during chewing (Hylander and Bays 1979). More recent work has used a combination of in vivo data and modeling to approximate stress concentrations within the joint and document how these stresses shift locations during chewing (Gallo et al. 2000; Gallo 2005). Furthermore, there is some relationship between condyle morphology and both stress location and distribution (Colombo et  al. 2008). These data, however, are only available for humans. It should be possible to conduct similar studies in nonhuman primates attempting a relatively straightforward kinematic behavior such as tree gouging. Evidence for an anteroposterior migration of stresses along the articular cartilage with changing jaw gape and a characterization of mediolateral location of these stresses would greatly benefit our ability to identify appropriate sites in the joint for histomorphological comparison. A number of studies attempt to manipulate the loading environment in the joint, primarily through altering dietary properties, to study how cartilage responds to these changes (Bouvier and Hylander 1982; Bouvier 1987; Sasaguri et  al. 1998; Pirttiniemi et al. 1996; Huang et al. 2002; Ravosa et al. 2007; Chen et al. 2008). Not unexpectedly, the results from these studies can vary markedly. While it is certainly possible that the articular cartilage may display multiple responses to alterations in loading, there are several potential influencing factors that are often unaccounted for in these studies. Foremost among these limitations is the failure to determine where peak loading is occurring. Without knowing where maximum stresses are, given that they can change with shifts in dietary properties, then it is nearly impossible to determine functionally homologous regions of cartilage for comparison (as noted here). We also know little about the thresholds for loading magnitudes and frequency that elicit physiological responses from chondrocytes (Ravosa et  al. 2007). What is clear is that articular cartilage responses can change over time and with the extent of loading.

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Finally, changes in articular cartilage throughout ontogeny also influence the ability of articular tissue to resist and respond to loading stresses. In macaques, the articular and growth (i.e., chondroblastic) layers of the condylar and glenoid cartilages change in absolute and relative thickness during ontogeny (Carlson et al. 1978; Hinton and Carlson 1983). Metric changes are mirrored by age-related changes in collagens, proteoglycans, and chondrocytes (Luder and Schroeder 1990, 1992; Haskin et al. 1995; Klinge 2001). These age-related changes impact how the zones of articular cartilage respond to loading stresses (Hinton and McNamara 1984). Future studies are needed that identify how and where loads are changing with experimental manipulation followed by examining the time course of cartilage response throughout ontogeny. Comparative studies can use these results as a baseline for interpreting morphological and histological variation in articular cartilage across primate TMJs.

Limitations and Future Directions It was impossible to control several factors known to influence articular cartilage morphology in this comparative study of primate cadavers. Thus, we suffer from several limitations typical of comparative work on non-laboratory animal models. Sample sizes were regrettably small for each species limiting our statistical power. All of the animals used in this analysis were captive bred. We do not know how frequently these marmosets gouged in captivity (if at all). Similarly, we had no control over diet and related physiological responses in the TMJ to masticatory loading. Given the small sample sizes, we included a range of ages, despite known trends for age-related decreases in cartilage thickness, proteoglycans, and cellularity (Haskin et al. 1995). We found no association between specimen age and our metric dimensions suggesting that age was not a major covariate in our analysis. We identify several future analyses comparing articular cartilage in gouging and nongouging primates that would build on the results presented here. First, it would be beneficial to explore articular cartilage regions outside of the midline. While we predicted major differences along an anteroposterior axis, we do not know where peak loads are located and may find different patterns at medial or lateral locations in the joint. Because metachromatic staining is an indirect measure of proteoglycan density, we need to employ immunohistochemical approaches to determine whether the patterns observed here persist with a more direct assessment. We also would extend these immunohistochemical approaches to examine collagen content across the different zones of articular cartilage. Finally, we can improve our age control in comparing articular cartilages across species. Here we are aided by the natural history of callitrichids in that these species frequently triplet in captivity with one individual often stillborn. Examination of these perinatal tissues would allow us to control loading and behavior at this specific age to provide insights into largely genetic differences established early in development between gouging and nongouging species during callitrichid evolution.

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Conclusions Experimental in  vivo evidence, behavioral field data, and mechanical properties estimates from gouging trees collectively suggest that tree gouging in marmosets involves significant mandibular excursion but not necessarily relative large bite forces (Vinyard et al. 2009). Both mandible and jaw-muscle morphology in marmosets facilitate jaw opening compared to nongouging tamarins (Vinyard et  al. 2003; Taylor and Vinyard 2004; Taylor et  al. 2009). Alternatively, mandible and jaw-muscle morphologies do not facilitate load resistance or force production compared with tamarins. Based on these comparative morphological patterns, we have concluded that the marmoset masticatory apparatus evolved to increase jaw opening linked to gouging performance (Vinyard et al. 2009). While this overarching conclusion may accurately represent much of the masticatory apparatus, it is rare that an entire complex system is adapted to a single mechanical function. More reasonably, the morphology of the marmoset masticatory apparatus represents compromises among multiple demands placed on it during various feeding behaviors. Our results suggest that the articular cartilage of the anterior glenoid represents one of these compromise morphologies by providing increased load resistance abilities linked to novel loading regimes in the TMJ during gouging. The derived, wedge-like morphology of the anterior dentition of marmosets (Rosenberger 1978) linked to improved cutting performance provides a second example of a morphological change unrelated to jaw excursion. Collectively, these morphologies highlight the complex functional challenges that tree gouging poses to marmosets and their masticatory apparatus. Acknowledgments  We thank Anne Burrows and Leanne Nash for inviting us to contribute to this volume, and Anne for asking us to participate in the symposium “The Evolution of Exudativory in Primates” held at the XXII Congress of the International Primatological Society in Edinburgh, Scotland (Aug. 2008). We are grateful to Elizabeth Curran (NEPRC), Amanda Trainor (WPRC), Suzette Tardiff (SFBR), Donna Layne (SFBR), and Susan Gibson (SMBRR) for supplying the specimens used in this analysis. We thank A. Burrows, T. Smith, S. Ward, and D. McBurney for suggestions and advice throughout this project. N. Robl assisted in collecting the histological data. This research was supported by NSF (BCS-0412153) and (BCS-0412153) and the NEOUCOM Department of Anatomy.

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Hylander WL (1979b) The functional significance of primate mandibular form. J Morphol 160:223–40. Hylander WL, Bays R (1979) An in  vivo strain-gauge analysis of the squamosal-dentary joint reaction force during mastication and incisal biting in Macaca mulatta and Macaca fascicularis. Archs Oral Biol 24:689–97. Kanouse MC, Ramfjord SP, Nasjleti CE (1969) Condylar growth in rhesus monkeys. J Dent Res 48:1171–6. Kempson GE, Muir H, Swanson SAV, Freeman MAR (1970) Correlations between stiffness and the chemical constituents of cartilage on the human femoral head. Biochim Biophys Acta 215:70–7. Kinzey WG, Rosenberger AL, Ramirez M (1975) Vertical clinging and leaping in a neotropical anthropoid. Nature 255:327–8. Király K, Lapveteläinen T, Arokoski J, Törrönen K, Módis L, Kiviranta I, Helminen HJ (1996) Application of selected cationic dyes for the semiquantitative estimation in histological sections of articular cartilage by microspectrophotometry. Histochem J 28:577–90. Kiviranta I, Jurvelin J, Tammi M, Säämänen AM, Helminen HJ (1987) Weight bearing controls glycosaminoglycan concentration and articular cartilage thickness in the knee joints of young beagle dogs. Arth Rheum 30:801–9. Kiviranta I, Tammi M, Jurvelin J, Säämänen AM, Helminen HJ (1988) Moderate running exercise augments glycosaminoglycans and thickness of articular cartilage in the knee joint of young beagle dogs. J Orthop Res 6:188–95. Klinge RF (2001) The structure of the fibrous tissue on the articular surface of the temporal bone in the monkey (Macaca mulatta). Micron 32:551–7. Knudson CB, Knudson W (2001) Cartilage proteoglycans. Cell Develop Biol 12:69–78. Kuettner KE, Kimura JH (1985) Proteoglycans: an overview. J Cell Biochem 27:327–36. Kuroda S, Tanimoto K, Izawa T, Fujihara S, Koolstra JH, Tanaka E (2009) Biomechanical and biochemical characteristics of the mandibular condylar cartilage. Osteoarth Cart 17:1408–1415. Luder HU, Schroeder HE (1990) Light and electron microscopic morphology of the temporomandibular joint in growing and mature crab-eating monkeys (Macaca fascicularis): the condylar articular layer. Anat Embryol 181:499–511. Luder HU, Schroeder HE (1992) Light and electron microscopic morphology of the temporomandibular joint in growing and mature crab-eating monkeys (Macaca fascicularis): the condylar calcified cartilage. Anat Embryol 185:189–99. Milam SB, Klebe RJ, Triplett RG, Herbert D (1991) Characterization of the extracellular matrix of the primate temporomandibular joint. J Oral Maxillofac Surg 49:381–91. Mizoguchi I, Takahashi I, Nakamura M, Sasano Y, Sato S, Kagayama M, Mitani H (1996) An immunohistochemical study of regional differences in the distribution of Type I and Type II collagens in rat mandibular condylar cartilage. Arch Oral Biol 41:863–9. Mow VC, Ratcliffe A, Poole AR (1992) Cartilage and diarthrodial joints as paradigms for hierarchical materials and structures. Biomaterials 13:67–97. Mussa R, Hans MG, Enlow DH, Goldberg J (1999) Condylar cartilage response to continuous passive motion in adult guinea pigs: A pilot study. Am J Orthod Dentofacial Orthop 115:360–7. Nash LT (1986) Dietary, behavioral, and morphological aspects of gummivory in primates. Yrbk Phys Anthropol 29:113–37. Patel RV, Mao JJ (2003) Microstructural and elastic properties of the extracellular matrices of the superficial zone of neonatal articular cartilage by atomic force microscopy. Front Biosci 8:a18–a25. Pirttiniemi P, Kantomaa T, Salo L, Tuominen M (1996) Effect of reduced articular function on deposition of type I and type II collagens in the mandibular condylar cartilage of the rat. Archs Oral Biol 41:127–31. Presnell JK, Schriebman M, Humason GL (1997) Humason’s animal tissue techniques, John Hopkins University Press, Baltimore. Ravosa MJ, Kunwar R, Stock SR, Stack MS (2007) Pushing the limit: masticatory stress and adaptive plasticity in mammalian craniomandibular joints. J Exp Biol 210:628–41. Robinson PD, Poswillo DE (1994) Temporomandibular joint development in the marmoset – A mirror of man. J Craniofac Genet Dev Biol 14:245–51.

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Rosenberger AL (1978) Loss of incisor enamel in marmosets. J Mammal 59:207–8. Rosenberger AL (1992) Evolution of feeding niches in New World monkeys. Am J Phys Anthropol 88:525–62. Sasaguri K, Jiang H, Chen J (1998) The effect of altered functional forces on the expression of bone-matrix proteins in developing mouse mandibular condyle. Arch Oral Biol 43:83–92. Silver FH. (2006) Mechanosensing and mechanochemical transduction in extracellular matrix: Biological, chemical, engineering, and physiological aspects, Springer, New York. Singh M, Detamore MS (2009a) Biomechanical properties of the mandibular condylar cartilage and their relevance to the TMJ disc. J Biomech 42:405–17. Singh M, Detamore MS (2009b) Stress relaxation behavior of mandibular condylar cartilage under high-strain compression. J Biomech Eng 131:0610081–5. Slowman SD, Brandt KD (1986) Composition and glycosaminoglycan metabolism of articular cartilage from habitually loaded and habitually unloaded sites. Arth Rheum 29:88–94. Smith RJ, Petersen CE, Gipe DP (1983) Size and shape of the mandibular condyle in primates. J Morphol 177:59–68. Stevenson MF, Rylands AB (1988) The marmosets, Genus Callithrix. In Mittermeier RA, Rylands AB, Coimbra-Filho AF, Fonseca GAB (eds) Ecology and behavior of neotropical primates. World Wildlife Fund, Washington DC. Sussman RW, Kinzey WG (1984) The ecological role of the Callitrichidae: a review. Am J Phys Anthropol 64:419–49. Tanaka H, Yamano E, Dalla-Bona DA, Watanabe M, Inubushi T, Shirakura M, Sano R, Takahashi K, van Eijden T, Tanne K (2006) Dynamic compressive properties of the mandibular condylar cartilage. J Dent Res 85:571–5. Taylor AB (2005) A comparative analysis of temporomandibular joint morphology in the African apes. J Hum Evol 48:555–74. Taylor AB, Vinyard CJ (2004) Comparative analysis of masseter fiber architecture in tree-gouging (Callithrix jacchus) and nongouging (Saguinus oedipus) callitrichids. J Morphol 261:276–85. Taylor AB, Eng CM, Anapol FC, Vinyard CJ (2009) The functional correlates of jaw-muscle fiber architecture in tree-gouging and nongouging callitrichid monkeys. Am J Phys Anthropol 139:353–67. Tong ACK, Tideman H (2001) The microanatomy of the rhesus monkey temporomandibular joint. J Oral Maxillofac Surg 59:46–52. Vinyard CJ, Wall CE, Williams SH, Hylander WL (2003) Comparative functional analysis of skull morphology of tree-gouging primates. Am J Phys Anthropol 120:153–70. Vinyard CJ, Wall CE, Williams SH, Mork AL, Armfield BA, Melo LCO, Valença-Montenegro MM, Valle YBM, Borstelmann de Oliveira MA, Lucas PW, Schmitt D, Taylor AB, Hylander WL (2009) The evolutionary morphology of tree gouging in marmosets. In Ford SM, Davis LC, Porter LM (eds) The smallest anthropoids: The marmoset/callimico radiation, Springer, New York. Wall CE (1999) A model of temporomandibular joint function in anthropoid primates based on condylar movements during mastication. Am J Phys Anthropol 109:67–88. Williams SH, Wall CE, Vinyard CJ, Hylander WL (2002) A biomechanical analysis of skull form in gum-harvesting galagids. Folia Primatol 73:197–209. Wilson NHF, Gardner DL (1982) The postnatal development of the temporomandibular joint of the common marmoset (Callithrix jacchus). J Med Primatol 11:303–11. Yanagishita M (1993) Function of proteoglycans in the extracellular matrix. Acta Pathol Japon 43:283–93.

Chapter 11

Searching for Dental Signals of Exudativory in Galagos Anne M. Burrows and Leanne T. Nash

Abstract  Consumption of exudates requires acquiring exudates. Exudate-feeding marmosets possess a distinct dental signal consisting of the “short-tusked” anterior dentition, which they use to gouge tree bark and elicit exudate flow. Observations of exudate-feeding galagos have indicated that these animals use the toothcomb in some fashion to acquire exudates, but behavioral observations of galago exudate acquisition are incomplete. The present study was designed to assess dental morphometrics of galagos in an effort to search for a more complete dental signal of exudate-feeding in this group. Cleaned and dried skulls from 137 galago specimens were selected representing seven species with varying proportions of exudates in their diets. Two-dimensional measurements were taken from the toothcomb, maxillary canine, mandibular and maxillary first premolars, and the last mandibular molar. Surface areas of these teeth were calculated except for the molar and a biomechanical shape variable to estimate the resistance ability of the toothcomb to bending loads was created. Analyses of variance on residuals of the plots of dental dimensions against a measure of body size indicated that relative toothcomb height and the ability to resist bending loads were significantly greater in exudate-feeding galagos relative to galagos that do not consume exudates. Additionally, the other teeth emerged as being significantly different among galagos, depending on the amount of exudates consumed. While the toothcomb may be used in some exudate acquisition fashion in galagos, it is clear that other teeth, especially in combination, may provide a dental signal to exudate feeding in galagos. As a dietary niche among primates, exudativory is among the rarest (Nash 1986; Napier and Napier 1994). While many primate species include exudates as a ­portion of their dietary intake (Nash and Burrows, Chap. 1), only a few taxa (marmosets, A.M. Burrows (*) Department of Physical Therapy, Duquesne University, Pittsburgh, PA, USA and Department of Anthropology, University of Pittsburgh, Pittsburgh, PA, 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_11, © Springer Science+Business Media, LLC 2010

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Euoticus, and Phaner) rely on exudates as a very large portion of their diets (CharlesDominique 1974, 1977; Hladik 1979; Nash 1986; Garber 1993; Rylands and de Faria 1993; Nekaris and Bearder 2007). In order to make a living on exudates, primates must have some morphologic adaptations for acquiring them and digesting them. It has clearly been shown that exudativorous marmosets and strepsirrhines have specific gut adaptations, such as an enlarged, capacious caecum, to promote digestion of exudates (Power, Chap. 2; Nash 1986; Caton et  al. 1996; Power and Oftedal 1996; McWhorter and Karasov 2007). Studies on the adaptive morphology of the skull and temporomandibular joint, however, have been equivocal (Ravosa et al., Chap. 9; Mork et al., Chap. 10; Dumont 1997; Williams et al. 2002; Vinyard et al. 2003; Viguier 2004; Burrows and Smith 2005, 2007; Vinyard 2007). Form of the dentition in primates has been associated with dietary niche and foraging behavior and represents direct interactions between an individual and its environment (Kay 1975; Kinzey 1992; Rosenberger 1992; White 2009). Studies of anthropoid dentition have revealed distinctive dental adaptations to varying dietary niches but have been done only in frugivorous and folivorous species (Hylander 1975; Kay 1975; Kinzey 1992; Anapol and Lee 1994; Uchida 1998). However, studies focusing on dental adaptations to exudate feeding are generally lacking, despite the growing documentation of the importance of exudates in the diets of numerous primate species, especially in the strepsirrhines (Nash and Burrows, Chap. 1; Génin et  al., Chap. 6; Nekaris et  al., Chap. 8). By comparison to the “long-tusked” tamarins that do not gouge (e.g., Saguinus), the “short-tusked” anterior dentition in the exudativorous marmosets Callithrix and Cebuella is a welldocumented adaptation to exudate acquisition, as is their method of exudate acquisition. In comparison, little is known about strepsirrhine dental adaptations to exudativory and their mechanism of acquisition. The toothcomb has frequently been cited as a dental adaptation for exudate acquisition in the strepsirrhines (Martin 1972, 1979; Gingerich 1975; Charles-Dominique 1977; Bearder and Martin 1980). Eaglen (1986) noted, though, that there were few morphometric adaptations in the toothcomb that distinguished exudativorous strepsirrhines from those that occupied other dietary niches. However, he did find that the most highly exudativorous strepsirrhines, Euoticus, Phaner, and Otolemur crassicaudatus (termed Galago crassicaudatus therein), tended to have high [cementoenamel junction to tip (CEJ-tip)] and mesiodistally narrow toothcombs relative to other strepsirrhines. While Euoticus, Phaner, and O. crassicaudatus are among the most highly exudativorous strepsirrhines, there are other species that consume relatively high percentages of exudates such as Go. senegalensis, Go. moholi, and many Microcebus species (in the present study, Galago is abbreviated as Go. and Galagoides as Gs. after Masters and Brothers 2002). However, Eaglen (1986) found no trends in morphological adaptations in the toothcombs of any of these taxa that reflect exudate acquisition. Examinations of the mandibular posterior dentition (premolars & molars) in exudativorous strepsirrhines have revealed an even less consistent pattern. Boyer (2008) found that surface relief of strepsirrhine molars was generally successful

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at separating folivores from frugivores but produced inconsistent results for ­exudativores. Similarly, a recent study (White 2009) that included the exudativorous lorisid Nycticebus coucang (see Nekaris et al., Chap. 8) did not find any distinguishing molar cusp patterns to separate it from the non-exudativorous lorisid species. It is generally agreed that there are two methods of acquiring exudates. Gouging is used by the marmosets Callithrix and Cebuella. When contrasted with tamarins, these marmosets possess a clear dental signal, the “short-tusked” anterior dentition where the tips of the mandibular canine and the mandibular incisors are on the same level (Garber 1992). The animal anchors the maxillary incisors and canines to the tree and “gouges” up with the mandibular incisors and canines to create a wound in the bark, which oozes exudates that the animal then licks (Coimbra-Filho and Mittermeier 1977; Rylands 1989; Garber 1992; Passamani and Rylands 2000; Vinyard et al. 2003). The other method, scraping, is a description typically applied to the exudativorous strepsirrhines in general. Unlike marmoset gouging, there is little agreement as to how this method of acquisition may work, which teeth are used, and which exudativorous strepsirrhines use scraping vs. which may indeed gouge. “Scraping” has been described as using the toothcomb to flick away loose bark, fracture off bits of brittle dried exudates (Acacia gum), or “scoop up” flowing liquid exudates (Stephenson et  al., Chap. 12; Charles-Dominique 1977; Williams et al. 2002) and has been shown to produce significant toothcomb damage in Go. moholi (Bearder and Martin 1980). The toothcomb has long been cited as a dental adaptation for exudate acquisition in the strepsirrhines (Martin 1972, 1979; Gingerich 1975; Charles-Dominique 1977; Bearder and Martin 1980). Unlike marmoset exudate feeders, though, detailed behavioral observations of strepsirrhine exudate feeding are unquantified, of minimal detail, and altogether lacking in some species. While there is evidence in the galagos that the toothcomb is used in some fashion during exudate acquisition (Charles-Dominique 1977; Martin 1979; Bearder and Martin 1980), it seems likely that there may be adaptations in other teeth for acquiring exudates. In contrast, among Asian lorises, it is now clear that gouging occurs in some species (Nekaris et al., Chap. 8). Charles-Dominique (1977) and Eaglen (1986) noted that Euoticus and Phaner had a uniquely mesiodistally narrow and high (CEJ-tip) toothcomb among strepsirrhines and suggested that these dimensional characteristics may be useful in accessing difficult-to-reach exudates relative to a wide and low toothcomb, forming an efficient “gouge” or “scoop” (Martin 1990; Kinzey 1992). In general, though, it is unclear what posterior dental morphologies characterize exudativorous galagos (or other strepsirrhines) and which teeth they may use to acquire exudates besides the toothcomb. The galagos (Primates: Strepsirrhini: Galagidae, following Groves 2005) represent a natural model for searching for dental signals of exudate acquisition in strepsirrhines. This taxonomic group has high species diversity with at least 13 species, possibly considerably more (Groves 2001, 2005; Grubb et  al. 2003), and high

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diversity of dietary niches including faunivory, frugivory, and exudativory (Nash 1986; Harcourt and Nash 1986; Harcourt and Bearder 1989; Nekaris and Bearder 2007). In addition, recent studies have indicated variation in craniofacial adaptations and craniofacial suture fusion patterns in galagos with differing dietary niches and foraging behavior (Williams et  al. 2002; Vinyard et  al. 2003; Burrows and Smith 2005, 2007; Stump 2007; Reinholt et al. 2009).

Galago Diets Numerous studies have shown that different species of a single mammalian taxon can practice widely divergent foraging behavior and occupy differing dietary niches (Clutton-Brock 1974; Kay et  al. 1978; Chapman 1987; Kinzey 1992; Doran and McNeilage 1997). Galagos represent an example of high dietary diversity within a single taxon. The greater bushbaby Otolemur crassicaudatus has a diet that consists of over 60% gums, while its congener O. garnettii reportedly consumes no gums (Harcourt and Nash 1986; Bearder 1987; Masters et al. 1988; Nekaris and Bearder 2007). Galago sp. include the exudativorous Go. senegalensis and Go. moholi (≥ 50% of the diet consisting of gums – Bearder 1987; Harcourt and Bearder 1989; Nash and Whitten 1989; Nekaris and Bearder 2007) while species such as Gs. alleni and Go. demidoff include close to 0% exudates in their diets (Charles-Dominique 1977; Harcourt and Nash 1986; Nekaris and Bearder 2007). The most highly exudativorous galago is Euoticus elegantulus, the needle-clawed bushbaby, which has a diet consisting of approximately 75% exudates (Charles-Dominique 1977; Nash 1986; Nekaris and Bearder 2007). Galago exudativores consume gums produced primarily by trees of the genus Acacia (Smith, Chap. 3; Nash 1986). Note that all galago exudativores must have a diet that consists of nutrients other than exudates as exudates consist primarily of complex beta-linked carbohydrates and minerals with little to no proteins (Power, Chap. 2; Power and Oftedal 1996; Mbuna and Mhinzi 2003). While all galago exudativores supplement their diets with fauna and/or fruits, we use data displayed in Table 11.1 as a guide to classify galagos into “intensive exudativore” species (over 50% of diet consists of exudates), “moderate exudativore” species (around 50% of diet consists of exudates), and “nonexudativores” (diet consisting of <50% exudates). It is also clear that seasonal variation in fruit availability may cause a typically frugivorous species to exploit exudates as fallback foods when fruits are scarce (Bearder and Martin 1980; Sussman 1999). Data on dietary category presented here are drawn from studies that indicate a “typical” dietary pattern for each species (Charles-Dominique 1977; Bearder and Martin 1980; Harcourt and Nash 1986; Harcourt and Bearder 1989; Nash and Whitten 1989). It is unclear as to whether galago exudate feeders acquire exudates primarily by generating a greater force at the toothcomb (Dumont 1997), by generating a larger gape at the temporomandibular joint (Vinyard et al. 2003), by “gouging” a wound into the bark, or by “scraping,” but it is clear that they use their teeth to access

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Table 11.1  Dietary niches for galago species (number in parentheses indicates mixed sex sample size used in the present study) Primary dietary Other main food Species (N) category (% of diet) sources (%) Exudativory category Exudates (>75) Fauna (~20) Intensive Euoticus elegantulus exudativore (19) Otolemur Exudates (>60) Fruits (~33) Intensive exudativore crassicaudatus (19) Galago senegalensis Exudates (~50) Fauna (~50) Moderate exudativore (23) Go. moholi (29) Exudates (~50) Fauna (~50) Moderate exudativore Gs. demidoff (27) Fauna (~70) Fruit (~20) Nonexudativore O. garnettii (7) Fruit (50) Fauna (50) Nonexudativore Fruit (50) Fauna (50) Nonexudativore Gs. alleni (13) All dietary data derived from Bearder and Martin (1980), Charles-Dominique (1977), Harcourt and Nash (1986), Harcourt and Bearder (1989), Nash and Whitten (1989), Nekaris and Bearder (2007); sex breakdown of sample sizes: E. elegantulus (m = 13; f = 6); O. crassicaudatus (m = 14; f = 5); Go. senegalensis (m = 11; f = 10; unknown = 2); Go. moholi (m = 17; f = 9; unknown = 3); Gs. demidoff (m = 22; f = 4; unknown = 1); O. garnettii (m = 4; unknown = 3); Gs. alleni (m = 8; f = 4; unknown = 1)

exudates. Which teeth and how they are being used are the questions. Previous observations of Go. senegalensis feeding behavior have provided evidence that they use their toothcombs in some fashion to access exudates (Bearder and Martin 1980). Charles-Dominique (1977) and Eaglen (1986) observed that E. elegantulus and O. crassicaudatus have relatively narrow and high toothcombs compared with galagos that do not intensively exploit exudates. If exudativorous galagos are using the toothcomb to acquire difficult-to-reach exudates by using a high, narrow toothcomb, we predict that this morphological dental signal would be seen in a large sample of galago exudate feeders. If the toothcomb is being used to acquire exudates, it is reasonable to assume that the enamel of the toothcomb is being loaded in some fashion. Thus, we would expect to see adaptive signals in the toothcomb of exudativorous galagos that would indicate resistance to such loading. It is reasonable to assume that enamel mechanical properties are similar across galago taxa and they respond to stresses similarly (see Teaford 2000 for a discussion of primate enamel microstructure). With this assumption in hand, we can make some generalizations about how the toothcomb may be loaded if it is being used to access exudates. First, the toothcomb is probably bent in the parasagittal plane if it is being used for exudate acquisition with the stress being placed upon the toothcomb at the tips of the teeth, the point of contact with the substrate (see Fig. 11.1a). The distance between the tip of the tooth and the CEJ represents the load arm. As that distance increases, the bending load is increased such that the greatest load would be experienced at the CEJ (see Fig. 11.1a). In order to resist such parasagittal bending loads, we would expect the toothcomb to be superoinferiorly thickest at the CEJ region, and we would expect to see the thickest toothcomb in species that use it to acquire exudates. Note that

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Fig. 11.1  (a) Lateral view of the right dentary in a generic galago, demonstrating linear measurements used in the present study. Distance from A to B represents height of the toothcomb (measured on I2); distance from C to D represents superoinferior thickness of toothcomb (measured on I2); distance from E to F represents mesiodistal width of P2 (the first mandibular premolar); distance from G to H represents height of P2. The unlabelled arrow represents the assumed location of the force on the tip of the toothcomb during exudate acquisition activities. The shaded triangle under the toothcomb represents the bending strain increase on the toothcomb from the tip to the cementoenamel junction (CEJ). Note that this bending strain is greatest at the CEJ. While this figure shows only mandibular dentition, the maxillary canine and first premolar measurements were taken in a similar fashion. (b) Occlusal view of right dentary in a generic galago, demonstrating linear measurements used in the present study. Distance from I (right mandibular canine) to the left mandibular canine on the left dentary represents width of the toothcomb; distance from L to M represents buccolingual thickness of M3. Thickness of P2 was measured as the maximum buccolingual dimension of P2. While this figure shows only mandibular dentition, the maxillary canine and first premolar measurements were taken in a similar fashion

for the toothcomb, “thickness” is a superoinferior dimension due to the somewhat horizontal arrangement of the teeth; in non-toothcomb teeth, “thickness” is a buccolingual dimension. If exudativorous galagos are using the toothcomb in forceful exudate acquisition, we predict that galago exudativores will show increased

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superoinferior thickness of the toothcomb relative to non-exudativores to resist parasagittal bending loads experienced during exudate acquisition. The toothcomb may also be compressed in line from the tip to the CEJ in species that use the toothcomb to forcefully acquire exudates. This compressive deformation may be best resisted by adding surface area to the toothcomb, which was noted by Eaglen (1986) in Phaner, E. elegantulus, and O. crassicaudatus. If exudativorous galagos are using the toothcomb to forcefully acquire exudates (by scraping or gouging with it), we predict that galago exudativores will show increased surface area of the toothcomb relative to nonexudativores to resist any in-line compressive forces experienced during exudate acquisition. It is possible that teeth in addition to the toothcomb are being used to access exudates. If these teeth are being used, we would expect them to differ from those of nonexudativores in dimensions that would reflect the ability to access difficultto-reach exudates and/or the ability to resist loads. Additionally, we would expect these other teeth to show increased surface area relative to nonexudativores to resist potential in-line compressive loads (Eaglen 1986). The present study was designed to explore morphometrics of the toothcomb and other dentition in galago exudate feeders in an effort to search for a dental signal for exudativory. Selected morphometrics of the toothcomb were measured, as were those of the maxillary canine, the first maxillary premolar (P2), the first mandibular premolar (P2), and the last mandibular molar (M3) to assess the following predictions:

Prediction 1: The Toothcomb If exudativorous galagos are using the toothcomb to acquire difficult-to-reach exudates as a “gouge” or “scoop” (Charles-Dominique 1977; Eaglen 1986; Martin 1990; Kinzey 1992), then we expect the most intensively exudativorous galagos (E. elegantulus and O. crassicaudatus) to possess the significantly narrowest (mesiodistally) and highest (CEJ-tip) toothcombs. If exudativorous galagos are using the toothcomb to forcefully acquire exudates (by gouging or scraping), we expect the toothcomb to be loaded during these activities. In order to resist any parasagittal loading and bending of the toothcomb during exudate acquisition activities, we predict that the most intensive exudativores will possess significantly greater superoinferior thickness of the toothcomb. In addition, the most intensively exudativorous galagos should display increased toothcomb surface area to resist in-line compression from the tip of the tooth to the CEJ (Eaglen 1986).

Prediction 2: Non-toothcomb Dentition If exudativorous galagos use additional teeth to acquire exudates, we expect to see adaptations in these teeth that reflect the ability to access difficult-to-reach exudate resources and the ability to resist loads. If exudativorous galagos are using these

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teeth to access difficult-to-reach exudate sources, the intensive exudativores should possess teeth that are significantly higher (CEJ-tip) and narrower (mesiodistally) than that of nonexudativores. If exudativorous galagos are using these other teeth in forceful acquisition activities, we expect that these teeth will be loaded in some fashion. In order to resist any parasagittal loading and bending of the tooth during exudate acquisition activities, we predict that the most intensive exudativores will possess greater buccolingual thickness of the teeth. In addition, the most intensively exudativorous galagos should display increased surface area of the other teeth to resist in-line compression from the tip of the tooth to the CEJ.

Materials and Methods Cleaned and dried skulls from 137 galago specimens representing seven species were used from museum holdings (Carnegie Museum of Natural History, Pittsburgh, PA; Field Museum of Natural History, Chicago, IL; Museum of Vertebrate Zoology, Berkeley, CA; and Cleveland Museum of Natural History, Cleveland, OH) and only materials from wild-caught specimens were used. Table 11.1 displays sample sizes and sex ratios used from each species. In order to assess dental morphometrics among the species, 13 two-dimensional measurements were taken from the following teeth, all from the right side of the dentary and maxilla (from Eaglen 1986), as shown in Figs. 11.1a, b for the dentary: (1) mesiodistal width of the toothcomb was assessed by measuring the widest distance from the right and left lateral-most teeth of the toothcomb, widely regarded to be the canines (Ankel-Simons 2000; Swindler 2002); (2) the middle tooth of the toothcomb, widely regarded as the second incisor (Ankel-Simons 2000; Swindler 2002), was measured for height (distance from CEJ-tip) to represent height of the toothcomb; (3) superoinferior thickness of the toothcomb was assessed by measuring the distance between the superior and inferior surfaces of the second incisor at the CEJ; (4) mesiodistal width of maxillary canine; (5) maxillary canine height; (6) buccolingual thickness of the maxillary canine at the CEJ; (7) mesiodistal width of P2 (the first maxillary premolar); (8) height of P2; (9) buccolingual thickness of P2 at the CEJ; (10) mesiodistal width of P2 (first mandibular premolar); (11) height of P2; (12) buccolingual thickness of P2 at the CEJ; and (13) buccolingual width of M3 at the CEJ. All measurements were taken by a single investigator (AMB) and were taken using digital sliding calipers to the nearest 0.01 cm. Measurements were only taken on teeth that exhibited no gross signs of dental wear. In addition to these 13 direct dental measurements, surface areas were also calculated on each maxillary canine, P2, and P2 by multiplying tooth height by mesiodistal width (Eaglen 1986). For toothcomb surface area, height of I2 was multiplied by mesiodistal width of the toothcomb following Eaglen (1986). A biomechanical shape variable for the ability of the toothcomb to resist bending in the parasagittal plane during exudate-acquisition activities was also created (Vinyard, personal communication). While the direct superoinferior thickness of I2

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was measured, this shape variable was created to further estimate the ability of the toothcomb to resist loads. This shape variable was created in the following manner: First, the second moment of area for the toothcomb (Ixx) was calculated. This is the cross-sectional property of the toothcomb (as measured from I2 and assumed to be rectangular) that describes its resistance to bending when loaded at the tip: I xx = (superoinferior thickness at I 2 ) × ( mesiodistal width of the toothcomb ). 3

Second, the resulting second moment of area (Ixx) was divided by height of the toothcomb at I2 to estimate the load resistance capability of the toothcomb: Ixx/height of I2 = biomechanical shape variable of the toothcomb for resisting bending loads at the tip of the toothcomb. If exudativorous galagos are using the toothcomb to forcefully acquire exudates (by gouging or scraping), we expect exudativorous groups to possess the significantly greatest shape variable of the toothcomb. All species were grouped according to dietary niche (see Table 11.1). Euoticus elegantulus and Otolemur crassicaudatus were grouped into an “intensive exudativore” category as the percentage of their diet devoted to exudates is reported to be well in excess of 50% (Charles-Dominique 1977; Nekaris and Bearder 2007). Go. senegalensis and Go. moholi were grouped into a “moderate exudativore” category as the percentage of their diet devoted to exudates is reported to be around 50% (Charles-Dominique 1977; Harcourt and Nash 1986; Harcourt and Bearder 1989). Gs. demidoff, Gs. alleni, and O. garnettii were all grouped into a “nonexudativore” category as 0–10% of their diets are reported to be composed of exudates (Charles-Dominique 1977; Harcourt and Nash 1986; Nekaris and Bearder 2007). Since there is a high degree of variation in body size among the galago species, from the large O. crassicaudatus (around 1 kg – Kappeler 1991) to the diminutive Gs. demidoff (around 70 g – Kappeler 1991), it was necessary to account for size in all raw measurements and surface areas to compare them among dietary categories. While body mass is often used as a scaling variable to evaluate the relative size of other continuous linear variables, individuals’ body mass data are often unavailable for museum-held specimens. Thus, another proxy for body size is necessary in the present study. Scalers such as total skull length, total dentary length, or palatal length are often chosen for size adjustment of the measured variables of interest, but it is unclear how each of these potential scalers may perform in such widely divergent body-size taxa as galagos. In such cases, an appropriate proxy for body size may be the geometric mean of a number of variables (Jungers et  al. 1995; Coleman 2008). The geometric mean, the nth root of the product of n numbers, is a mechanism used to estimate body mass as a scaler for a variable of interest and calculated using a number of variables (Mosimann 1970; Sokal and Rohlf 1995). In choosing the variables for inclusion in calculating the geometric mean, a relatively high number should be chosen to construct the most complete surrogate for body size (Mosimann 1970; Coleman 2008). In the present study, 24 craniodental variables were used to compute the geometric mean of each specimen (see Table 11.2).

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Table 11.2  Variables used to compute geometric mean Toothcomb mesiodistal width Total skull length Toothcomb height Dentary length Toothcomb superoinferior thickness Width of the mandible across the mandibular condyles Maxillary canine mesiodistal width Width of the mandible across the P2s Maxillary canine height Height of the mandibular condyle Maxillary canine buccolingual thickness Width of the maxilla across the P2s 2 P mesiodistal width Toothcomb surface area P2 height Maxillary canine surface area P2 buccolingual thickness P2 surface area P2 mesiodistal width P2 surface area P2 height M3 buccolingual thickness Palatal length P2 buccolingual thickness

The log10 of each geometric mean for each specimen and the log10 of each of the 13 linear dental variables were computed. Residuals were calculated for each of the log10 dental variables using the log10 geometric means as the independent variable via standardized major axis regression in SPSS v. 16.0 (see Warton et  al. 2006). Means and standard error of the means were calculated for each dental variable residual, and all means were compared among the three dietary groups using a oneway ANOVA with significance set a priori at p < 0.05 (Sokal and Rohlf 1995). Where there were significant (p < 0.05) experiment-wide differences in a variable among dietary groups, means were compared between groups post hoc using the Hochberg GT2 statistical test (Sokal and Rohlf 1995). This post hoc test is called for when there are multiple comparisons to be made and the sample sizes are unequal. All post hoc tests were considered to be statistically significant if p < 0.05. All statistical comparisons were executed using SPSS v. 16.0.

Results The Toothcomb Figures  11.2 and 11.3 display dentition of species used in the present study. Table 11.3 displays means for raw dental variables, and Table 11.4 displays mean residuals with results of statistical analyses. Results of the ANOVAs on mean residuals for the toothcomb variables among dietary categories revealed significant differences for toothcomb height only. Pairwise post hoc comparisons between dietary categories revealed that both the intensive and moderate exudativores had significantly higher toothcombs than the nonexudativores (Fig. 11.4).

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Fig. 11.2  Lateral views of dentaries from species used in present study. Scale bars represent 1 cm

Fig. 11.3  Lateral views of the cranium from species used in the present study. Scale bars represent 1 cm

For the biomechanical shape variable, estimating the ability of the toothcomb to resist bending in the parasaggital plane, ANOVA results indicated that there was a significant experiment-wide difference among the three dietary groups (F = 37.710, df = 2, p = 0.000). Post hoc Hochberg GT2 testing revealed that the intensive exudativores had the significantly greatest ability to resist this type of bending (Fig. 11.5).

Maxillary Dentition All species displayed maxillary canines that were dagger-like in appearance (Fig. 11.3). All maxillary canine variables, except for buccolingual thickness, were significantly different among the dietary categories (Fig.  11.6). Post hoc testing revealed that both exudativore groups had the highest maxillary canine and the greatest maxillary canine surface area. Maxillary canine width was the largest in the moderate exudativores and intermediate, as well as not larger than expected for size, in the intensive exudativores.

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Table  11.3  Means (+SEM) for raw dental variables (in mm and in mm2 for surface areas) Moderate exudativores Intensive Nonexudativores exudativores (N = 38) (N = 52) (N = 47) Variable Mean (+SEM) Mean (+SEM) Mean (+SEM) TCW 4.60 (0.18) 2.96 (0.03) 3.14 (0.16) TCH 4.80 (0.13) 3.24 (0.03) 3.12 (0.14) TCT 1.60 (0.05) 1.09 (0.02) 1.12 (0.05) TCSA 22.90 (1.52) 9.62 (0.17) 11.03 (1.08) maxCW 3.68 (0.17) 2.12 (0.03) 1.99 (0.14) maxCH 6.32 (0.23) 3.61 (0.07) 3.48 (0.24) maxCT 2.17 (0.09) 1.27 (0.02) 1.28 (0.08) maxCSA 24.45 (1.97) 7.72 (0.22) 8.40 (1.26) maxPW 3.31 (0.07) 1.72 (0.04) 1.94 (0.10) maxPH 3.63 (0.06) 1.93 (0.04) 2.06 (0.08) maxPT 1.93 (0.05) 1.06 (0.02) 1.19 (0.06) maxPSA 12.03 (0.33) 3.35 (0.12) 4.49 (0.54) mandPW 2.70 (0.09) 1.50 (0.03) 1.44 (0.10) mandPH 5.56 (0.17) 3.31 (0.04) 3.31 (0.19) mandPT 2.29 (0.10) 1.34 (0.03) 1.35 (0.10) mandPSA 15.44 (0.88) 5.00 (0.13) 5.58 (0.73) mandMT 2.04 (0.08) 1.56 (0.08) 1.69 (0.06) TCW toothcomb mesiodistal width, TCH toothcomb height, TCT toothcomb superoinferior thickness, TCSA toothcomb surface area, maxCW maxillary canine mesiodistal width, maxCH maxillary canine height, maxCT maxillary canine buccolingual thickness, maxCSA maxillary canine surface area, maxPW first maxillary premolar mesiodistal width, maxPH first maxillary premolar height, maxPT first maxillary premolar buccolingual thickness, maxPSA first maxillary premolar surface area, mandPW first mandibular premolar mesiodistal width, mandPH first mandibular premolar height, mandPT first mandibular premolar buccolingual thickness, mandPSA first mandibular premolar surface area, mandMT third mandibular molar buccolingual thickness

Figure 11.7 shows results for the first maxillary premolar (P2). Morphology of the first maxillary premolar among the species varied greatly (Fig.  11.3). Previous observations have noted the strongly caniniform P2 in E. elegantulus (e.g., Swindler 2002). The other intensive exudativore, O. crassicaudatus, had a P2 that appeared to be similar to the other galagos, somewhat caniniform but much less so than Euoticus. Results of the ANOVA were unexpected and revealed that both the intensive exudativores and the nonexudativores had significantly mesiodistally wider and buccolingually thicker first maxillary premolars than the moderate exudativores. Intensive exudativores had the significantly highest P2, and both groups of exudativores had the significantly greatest surface area for P2. Thus, intensive and moderate exudativores achieved greater surface area in different ways.

Table 11.4  Means (+SEM) for dental variable residuals with results of statistical analyses (degrees of freedom in all one-way ANOVA analyses was always 2) Intensive exudativores Moderate exudativores Nonexudativores (N = 38) (N = 52) (N = 47) Variable Mean (+SEM) Mean (+SEM) Mean (+SEM) F-values p-value TCW −0.08 (0.22) −0.04 (0.10) 0.12 (0.16) 0.436 0.648 TCH 0.12 (0.15)+ 0.22 (0.12)+ −0.34 (0.09) 4.46 0.013 a TCT 0 (0.20) −0.01 (0.13) 0.02 (0.14) 0.012 0.988 TCSA −0.02 (0.19) 0.12 (0.11) −0.12 (0.18) 0.662 0.518 maxCW 0.03 (0.14)+ ↓=⇟ 0.38 (0.09)+ −0.44 (0.18) ↓=⇟ 9.251 0.000 a maxCH 0.18 (0.12)+ 0.20 (0.12)+ −0.36 (0.17) 4.914 0.009 a maxCT 0.07 (0.10) 0.07 (0.13) −0.13 (0.18) 0.630 0.534 maxCSA 0.11 (0.12)+ 0.33 (0.11)+ −0.45 (0.18) 8.564 0.000 a maxPW 0.49 (0.14)+ −0.47 (0.12) 0.12 (0.15)+ 12.499 0.000 a + + maxPH 0.52 (0.20) −0.33 (0.10) −0.05 (0.13) 8.981 0.000 a maxPT 0.53 (0.12)+ −0.60 (0.12) 0.23 (0.14)+ 20.542 0.000 a mandPW 0.21 (0.16)+ 0.22 (0.12)+ −0.41 (0.15) 6.626 0.002 a mandPH 0.19 (0.13) 0.05 (0.13) −0.21 (0.17) 1.769 0.175 mandPT −0.14 (0.12) 0.21 (0.97) −0.12 (0.17) 1.865 0.159 mandPSA 0.24 (0.14)+ 0.17 (0.12)+ −0.39 (0.16) 5.807 0.004 a mandMT −0.30 (0.21)+ −0.17 (0.10)+ 0.42 (0.13) 7.313 0.001 a Abbreviations as in Table 11.3 a  Indicates that the ANOVA was statistically significant at p < 0.05; mean residuals with the same symbol indicate that these groups were not significantly different from one another in post hoc testing

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Fig. 11.4  Box plot of results from post hoc GT2 analyzes of mean toothcomb height residuals among dietary groups. The outer whiskers represent the standard error of the mean and the black rectangle is centered on the mean. IE: intensive exudativores; ME: moderate exudativores; NE: nonexudativores. Asterisks represent dietary groups where the means do not differ from one another at the p < 0.05 level of significance

Fig. 11.5  Box plot of results from post hoc GT2 analyses of the toothcomb biomechanical shape variable for resistance to bending. The outer whiskers represent the standard error of the mean and the black rectangle is centered on the mean. Conventions as in Fig.  11.4. Asterisks represent dietary groups where the means do not differ from one another at the p < 0.05 level of significance. Note that the standard error of the mean was so small in the moderate exudativore group that the range does not appear in the figure

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Fig.  11.6  Box plot of results from post hoc GT2 analyzes of mean maxillary canine residuals among dietary groups. The outer whiskers represent the standard error of the mean and the black rectangle is centered on the mean. Conventions as in Fig. 11.4. Asterisks [and double dagger in (a)] represent dietary groups where the means do not differ from one another at the p < 0.05 level of significance

Non-toothcomb Mandibular Dentition Figure 11.2 shows first mandibular premolars (P2) in all species used in the present study. Clearly, E. elegantulus and O. crassicaudatus have first mandibular premolar morphologies that are similar. Both of these intensive exudativores have near vertically oriented first mandibular premolars, while the other species have first mandibular premolars that are closer to the plane of the toothcomb. Figure 11.8 shows results for the first mandibular premolar. Only width and surface area of the P2 was significantly different among dietary groups, with the exudativores having the widest teeth and greatest surface area. Lastly, in contrast to the other teeth described above, the buccolingual width of M3 was significantly greatest in the non-exudativores (Fig. 11.9).

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Fig. 11.7  Box plot of results from post hoc GT2 analyses of mean P2 (first maxillary premolar) residuals among dietary groups. The outer whiskers represent the standard error of the mean and the black rectangle is centered on the mean. Conventions as in Fig. 11.4. Asterisks represent dietary groups where the means do not differ from one another at the p < 0.05 level of significance

Fig. 11.8  Box plot of results from post hoc GT2 analyzes of mean P2 (first mandibular premolar) residuals among dietary groups. The outer whiskers represent the standard error of the mean and the black rectangle is centered on the mean. Conventions as in Fig. 11.4. Asterisks represent dietary groups where the means do not differ from one another at the p < 0.05 level of significance

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Fig.  11.9  Box plot of results from post hoc GT2 analyzes of mean M3 (last mandibular molar) residuals among dietary groups. The outer whiskers represent the standard error of the mean and the black rectangle is centered on the mean. Conventions as in Fig. 11.4. Asterisks represent dietary groups where the means do not differ from one another at the p < 0.05 level of significance

Discussion The results of the present study revealed a mixed picture of dental use in exudativorous galagos relative to galagos that do not consume exudates. Previous reports (Charles-Dominique 1977; Bearder and Martin 1980; Eaglen 1986) indicated that exudate-feeding galagos may have higher, narrower toothcombs to access difficultto-reach resources. The results of the present study partially support this. Both intensive (E. elegantulus and O. crassicaudatus) and moderate exudativores (Go. senegalensis, Go moholi, and Gs. demidoff) had significantly higher, but not narrower, toothcombs relative to nonexudativores (O. garnettii and Gs. alleni). However, the biomechanical shape variable created to estimate the ability of the toothcomb to resist bending did reveal significantly greater resistance capabilities in the intensive exudativores. Clearly, intensive and moderate exudativores have higher toothcombs, but without narrower toothcombs. These taxa may, then, be limited in reaching restricted locations as previously suggested. However, with a greater resistance capability to bending forces, E. elegantulus and O. crassicaudatus may use the toothcomb as a means of forcefully acquiring exudates by scraping or prising away at brittle, dried exudates or at tree bark, in agreement with previous observations (Charles-Dominique 1977; Bearder and Martin 1980). The strepsirrhine toothcomb has been described as a specific adaptation for exudate acquisition (e.g., Martin 1972, 1990; Gingerich 1975). However, few actual field studies have described specific use of the toothcomb in exudate acquisition

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activities in any strepsirrhine. Petter et al. (1975) describe Phaner furcifer as licking at oozing exudates and specifically using the canines, which we can only infer to be the maxillary canines, to gnaw at the bark to elicit flow. Microcebus sp. are reported to be highly exudativorous (e.g., Génin et  al., Chap. 6; Joly-Radko and Zimmermann, Chap. 7; Radespiel et al. 2006; Joly and Zimmermann 2007; Génin 2008), but there are no accounts of whether or not they use the toothcomb to acquire exudates. Recent studies have demonstrated that lorises include exudates in their diets and specifically gouge to acquire exudates (Nekaris et al. Chap. 8; Tan and Drake 2001). However, there are as of yet no indications as to which teeth are used in this acquisition. While there are reports of toothcomb use in exudate-feeding galagos, there are no published reports of how other dentition may be used by these animals. The results of the present study indicate significant differences among the maxillary canine and first premolar, mandibular first premolar, and the last mandibular molar. It is notable that for most of the nontoothcomb variables that showed a significant difference among our dietary groups, the effect size (as estimated by the range from the highest group mean to the lowest) exceeded the effect size for toothcomb height. In the maxillary canine, exudativores had the highest and widest tooth with the greatest surface area. Nonexudativores did share a wide canine with intensive exudativores. The first maxillary premolar was a mix of results with intensive exudativores having the highest tooth and the greatest surface area. However, they shared the widest and buccolingually thickest teeth with nonexudativores. Overall, the maxillary dentition showed characteristics both for reaching difficult-to-access resources (high and narrow canine and a high premolar) and for resisting in-line compression during forceful acquisition activities (high canine surface area, buccolingually thick premolar, and high premolar surface area). A possible pattern that emerges is that the intensive exudativores, and Euoticus in particular, may involve both the maxillary canine and first premolar in exudate acquisition but the moderate exudativores may emphasize the canine in particular. However, the possible agonistic use of canines in these animals has not been accounted for in this analysis and bears further study for group and species differences, which might confound the dietary interpretations here. The first mandibular premolar was only significantly different for width, with exudativores having the widest tooth with the greatest surface area, characteristics that would seem to be related more to resisting in-line compression than to reaching difficult-to-access resources. Interestingly, the last mandibular molar buccolingual width was significantly narrowest in the exudativores. It may indicate that there is decreased selective pressure in these species for molar size due to the lack of its use in exudativory. Exudates consumed by strepsirrhines are characterized as being water (or saliva) soluble and often nearly fluid in nature (Crompton 1984) or resembling soft fruit (Kay 1984), which would require little to no mastication with molars. Insects, as consumed by Gs. alleni and Gs. demidoff, the species with the significantly greatest last mandibular molar buccolingual width, most likely require greater mastication than exudates.

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The reduction in buccolingual width of the last mandibular molar should be assessed in nongalago strepsirrhine exudativores to determine its state. It may be a potentially valuable signal of exudativory that could be applied to interpretation of the fossil record. In general, the present study finds mixed dental signals of exudativory in galagos. While some results show support for adaptations for reaching difficult-toaccess sources, others show support for resisting bending loads and in-line compression. This is especially vexing when compared to the clear dental signals possessed by the gouging marmosets Cebuella and Callithrix. While further studies on an expanded phylogenetic sample of strepsirrhine exudate feeders are necessary to address this dilemma, the answer may partially lie in the words of our foreword author, Robert Martin: As strepsirrhines rely more on scraping and licking to acquire exudates rather than gouging, we may expect dental specializations to be correspondingly more subtle.

Implications for Exudativory Signals in the Fossil Record It has been widely suggested that the stem primates were very similar to extant galagos and/or mouse lemurs: nocturnal, small-bodied, arboreal animals (e.g., Jones 1916; Le Gros Clark 1949; Cartmill 1974; Sussman 1991; Soligo and Martin 2006). It has also been suggested that these stem primates included exudates as part of their diets (Nash 1986; Martin 1990). Thus, an understanding of how exudativory may be interpreted in the fossil record would increase our understanding of primate origins. Reconstruction of diet from morphological features in the fossil record provides salient information on lifestyle and has been largely successful in many mammalian taxa. Such reconstruction depends upon preservation of traits that reflect dietary adaptations but can only include hard-tissue traits, bone and teeth. These traits must also be recognized in extant taxa that exploit that diet. Such signals for folivory and frugivory in extant and fossil primate taxa have been relatively well agreed upon and include features associated with the mandible, anterior and posterior dentition, and features associated with the limbs. For extant exudativores, though, the most reliable morphological signal comes from the gut tube (Caton et  al. 1996, 2000; Power and Oftedal 1996), a feature not represented in the fossil record. No other recognized hard-tissue morphological signals consistently exist as a unifying feature for this dietary niche. While presence of a toothcomb in and of itself cannot be a signal for exudativory, as all strepsirrhines by definition possess one, it is possible that the specific attributes of a high toothcomb with the ability to resist parasagittal bending loads may be a signal. We can also further investigate the potential signal value of the maxillary canine and first premolar, the mandibular first premolar, and mandibular last molar. While more detailed and quantified behavioral observations for use of these teeth in exudate acquisition are much needed, these teeth may provide a valuable signal in assessing

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dietary reconstruction in fossil strepsirrhines. In the future, in addition to more detailed behavioral information, we need more comparative morphological studies of strepsirrhines incorporating differing amounts of exudates in the diet and information on the physical properties (liquid, sticky, hard, and brittle) and locations (crevices?) of the exudates consumed. As Rosenberger (Chap. 14) points out, as in all biomechanical studies, we need analyses that can discriminate between frequency of use and the peak mechanical demands as being the more important selective factors on morphological adaptations. Finally for galagos, we need both information on more galago species and a consensus phylogeny for them so that a more phylogenetically controlled analysis of dental morphology could be accomplished. Acknowledgments  The authors would like to express their deep gratitude to Gary Schwartz for handling the review process of this chapter and his generous advice on statistical methodology. We thank Valerie DeLeon, Betsy Dumont, Bob Martin, and Tim Smith, for comments on various drafts of this chapter, and we especially thank Chris Vinyard for his assistance with creating the shape variable formula for the toothcomb. We also thank John Wible and Sue McLaren (Carnegie Museum of Natural History), Lyman Jellema (Cleveland Museum of Natural History), Bill Stanley (Field Museum of Natural History), and Chris Conroy (Museum of Vertebrate Zoology) for access to specimens.

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Kay R.F., Sussman R.W., and Tattersall I. 1978. Dietary and dental variations in the genus Lemur, with comments concerning dietary–dental correlations among Malagasy primates. Am J Phys Anthropol 9:119–128. Kinzey W.G. 1992. Dietary and dental adaptations in Pitechiinae. Am J Phys Anthropol 88:499–514. Le Gros Clark W.E. 1949. History of the primates. Chicago: The University of Chicago Press. Martin R.D. 1972. Adaptive radiation and behaviour of the Malagasy lemurs. Phil Trans Royal Soc Lond B 26:295–352. Martin R.D. 1979. Phylogenetic aspects of prosimian behaviour. In: The study of prosimian behavior, eds. G.A. Doyle, R.D. Martin, New York: Academic Press. Martin R.D. 1990. Primate origins and evolution: a phylogenetic reconstruction. Princeton: Princeton University Press. Masters J.C., Brothers D.J. 2002. Lack of congruence between morphological and molecular data in reconstructing the phylogeny of the Galagonidae. Am J Phys Anthropol 117:79–93. Masters J.C., Lumsden W.H.R., and Young D.A. 1988. Reproduction and dietary parameters in wild greater galago populations. Int J Primatol 9:573–592. Mbuna J.J., Mhinzi G.S. 2003. Evaluation of gum exudates from three selected plant species from Tanzania for food and pharmaceutical applications. J Sci Food Agr 83:142–146. McWhorter T.J., Karasov W.H. 2007. Paracellular nutrient absorption in a gum-feeding new world primate, the common marmoset Callithrix jacchus. Am J Primatol 69:1399–1411. Mork A.L., Horton W.E., Jr., and Vinyard C.J. 2010. A comparative analysis of the articular cartilage in the temporomandibular joint of gouging and nongouging New World monkeys. In: The evolution of exudativory in primates, eds. A.M. Burrows, L.T. Nash. pp. 187–210. New York: Springer. Mosimann J.E. 1970. Size allometry: size and shape variables with characterizations of the lognormal and generalized gamma distributions. J Am Stat Assoc 65:930–945. Napier J.R., Napier P.H. 1994. The natural history of the primates. Cambridge, MA: MIT Press. Nash L.T. 1986. Dietary, behavioural, and morphological aspects of gummivory in primates. Yrbk Phys Anthropol 29:113–137. Nash L.T., Burrows A.M. 2010. Introduction: advances and remaining sticky issues in the understanding of exudativory in primates. In: The evolution of exudativory in primates, eds. A.M. Burrows, L.T. Nash. pp. 1–24. New York: Springer. Nash L.T., Whitten P.L. 1989. Preliminary observations on the role of Acacia gum chemistry in Acacia utilization by Galago senegalensis in Kenya. Am J Primatol 17:27–39. Nekaris A., Bearder S.K. 2007. The lorisiform primates of Asia and Mainland Africa: diversity shrouded in darkness. In: Primates in perspective, eds. C.J. Campbell, A. Fuentes, K.C. MacKinnon, M. Panger, and S.K. Bearder, pp. 24–45. New York: Oxford University Press. Nekaris K.A.I., Collins R. L., and Navarro-Montes A. 2010. Comparative ecology of exudate feeding by Asian slow lorises (Nycticebus). In: The evolution of exudativory in primates, eds. A.M. Burrows, L.T. Nash. pp. 155–168. New York: Springer. Passamani M., Rylands A.B. 2000. Feeding behaviour of Geoffroy’s marmoset (Callithrix geoffroyi) in an Atlantic forest fragment of south-eastern Brazil. Primates 41:27–38. Petter J.-J., Schilling A., and Pariente G. 1975. Observations on the behaviour and ecology of Phaner furcifer. In: Lemur biology, eds. I. Tattersall, R.W. Sussman, New York: Plenum Press. 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. 2010. Nutritional and digestive challenges to being a gum-feeding primate. In: The evolution of exudativory in primates, eds. A.M. Burrows, L.T. Nash. pp. 25–44. New York: Springer. Radespiel U., Reimann W., Rahelinirina M., and Zimmermann E. 2006. Feeding ecology of sympatric mouse lemur species in northwestern Madagascar. Int J Primatol 27:311–321. Ravosa M.J., Hogg R.T., and Vinyard C.J. 2010. Exudativory and primate skull form. In: The evolution of exudativory in primates, eds. A.M. Burrows, L.T. Nash. pp. 169–187. New York: Springer. Reinholt L.E., Burrows A.M., Eiting T., Dumont E.R., and Smith T.D. 2009. Microanatomical assessment of fusion in facial sutures by histological and microCT methods. Am J Phys Anthropol 138:499–506.

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Rosenberger A.L. 1992. Evolution of feeding niches in New World monkeys. Am J Phys Anthropol 88:525–562. Rosenberger A.L. 2010. Adaptive profile vs. adaptive specialization: fossils and gummivory in early primate evolution. In: The evolution of exudativory in primates, eds. A.M. Burrows, L.T. Nash. pp. 273–295. New York: Springer. Rylands A.B. 1989. Sympatric Brazilian callitrichids: the black tufted-ear marmoset, Callithrix kuhli, and the golden-headed lion tamarin, Leontopithecus chrysomelas. J Hum Evol 18:679–695. Rylands A.B., de Faria D.S. 1993. Habitats, feeding ecology, and home range size in the genus Callithrix. In: Marmosets and tamarins: systematics, behaviour, and ecology, ed. A.B. Rylands, Oxford: Oxford University Press. Smith A.C. 2010. Exudativory in primates: interspecific patterns. In: The evolution of exudativory in primates, eds. A.M. Burrows, L.T. Nash. pp. 45–88. New York: Springer. Sokal R.R., Rohlf F.J. 1995. Biometry, 3rd edition. New York: W.H. Freeman and Company. Soligo C, Martin R.D. 2006. Adaptive origins of primates revisited. J Hum Evol 50:414–430. Stephenson I.R., Bearder S.K., Donati G., and Karlsson, J. 2010. A guide to galago diversity: getting a grip on how best to chew gum. In: The evolution of exudativory in primates, eds. A.M. Burrows, L.T. Nash. pp. 235–255. New York: Springer. Stump D.P. 2007. Variation in craniofacial suture fusion in the Galagidae. Am J Phys Anthropol Suppl 44:227. Sussman R.W. 1991. Primate origins and the evolution of angiosperms. Am J Primatol 23:209–223. Sussman R.W. 1999. Primate ecology and social structure. Volume 1: lorises, lemurs and tarsiers. Needham Heights, MA: Pearson Custom Publishing. Swindler D.R. 2002. Primate dentition. Cambridge: Cambridge University Press. Tan C.L., Drake J.H. 2001. Evidence of tree gouging and exudate eating in pygmy slow lorises (Nycticebus pygmaeus). Folia Primatol 72:37–39. Teaford M.F. 2000. Primate dental functional morphology revisited. In: Development, function and evolution of teeth, eds. M.F. Teaford, M.M. Smith, M.W.J. Ferguson, Cambridge: Cambridge University Press. Uchida A. 1998. Variation in tooth morphology of Gorilla gorilla. J Hum Evol 34:55–70. 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 C.J. 2007. An interspecific analysis of covariance structure in the masticatory apparatus of galagos. Am J Primatol 69:46–58. Vinyard C.J., Wall C.E., Williams S.H., and Hylander W.L. 2003. Comparative functional analysis of skull morphology of tree-gouging primates. Am J Phys Anthropol 120:153–170. Warton D.I., Wright I.J., Falster D.S., Westoby M. 2006. Bivariate line-fitting methods for allometry. Biol Rev 81:259–291. White J. 2009. Geometric morphometric investigation of molar shape diversity in modern lemurs and lorises. Anat Rec 292:701–719. Williams S.H., Wall C.E., Vinyard C.J., and Hylander W.L. 2002. A biomechanical analysis of skull form in gum-harvesting galagids. Folia Primatol 73:197–209.

Chapter 12

A Guide to Galago Diversity: Getting a Grip on How Best to Chew Gum Isobel R. Stephenson, Simon K. Bearder, Guiseppe Donati, and Johann Karlsson

Abstract  Disputes over galago taxonomy have meant that studies often use d­ ifferent names for identical populations, making comparative analysis difficult for the untrained researcher. A main objective of this study was to assess whether hand and foot pad morphology, nail shape and toothscraper structure reveal adaptations to exudate eating and show differences which reflect taxonomy in order to identify species. A total of 714 museum specimens were examined between May and July 2007, revealing six pads on each hand and foot which vary in shape and orientation across taxa. Three nail shapes and two variations in toothscraper position were identified. The results indicate that variance in pad size reflects species boundaries and shows adaptations to allow access to large-diameter substrates. No consistent dental variation was identified when comparing species with high and low proportions of exudates in their diet, although the highly gummivorous Euoticus elegantulus possessed a relatively longer, more procumbent toothscraper than other species.

Introduction Galago Diversity For accurate identification of species, it is important to know which characteristics reflect phylogeny, so understanding local niche differentiation is vital for studying species-specific adaptations. Unfortunately, the galagos of mainland Africa (family Galagidae) have been the subject of a highly disputed taxonomy due to the ­difficulty of studying them in their natural habitats (Burrows and Nash 2007). Galagos are nocturnal and inherently cryptic, being morphologically similar but reproductively

I.R. Stephenson (*) Department of Anthropology and Geography, School of Social Sciences and Law, Oxford Brookes University, Gipsy Lane, Oxford, OX3 0BP, 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_12, © Springer Science+Business Media, LLC 2010

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isolated (Mayr 1963). Phylogenetic reconstructions based on characteristics used to analyse diurnal taxa therefore failed to reveal the extent of their diversity, which now includes 24 species (Grubb et al. 2003).

Morphological Aspects of Niche Differentiation Where morphology reflects an adaptation to specific selection pressures of the environment it is likely that differences will emerge between species due to niche separation. Galagos are distributed across a vast range of habitats throughout subSaharan Africa, where they exploit a diverse array of dietary items. Many galagos consume exudates to some extent, but by far the most gum-dependent are the needle-clawed galagos (Euoticus spp.), with exudates comprising around 75% of their nutritional intake (Viguier 2004). Due to varying dependence on exudates, adaptations may have evolved which reflect the ability to exploit them.

Adaptations to Exudate Exploitation To harvest gum deposits, galagos use their specialized toothscraper, made up of the four lower incisors and two incisiform canines. Within primates, exudate-eating species fall into two major categories: those that actively damage the trees to initiate gum-flow, the gougers, and those that harvest gum released from the holes made by wood-boring arthropods, the scrapers. Some galagos fall into the scraping category, using their toothscraper to puncture the surface of hardened gum to stimulate new flows (Williams et  al. 2002). Morphogical features have suggested that Euoticus species use their caniniform upper first premolars to damage the tree surface (Charles-Dominique and Petter 1980), unlike the more typically gouging pygmy marmosets (Callithrix spp.) which actively gouge bark using the anterior dentition to release exudates (Taylor and Vinyard 2004). Large gum resources are often found on relatively inaccessible broad trunks due to the constraints of grip (Bearder, personal observation). Previous studies have indicated that grip may be enhanced by the expansion of volar pads increasing frictional forces; therefore, more exudate-dependent galagos may have also developed adaptations of the hands and feet, particularly on the tactile surfaces which interact with the substrate to facilitate grip (Cartmill 1974, 1979).

Methods All specimens were part of the primate collections at the Powell-Cotton Museum, Kent, and the London Natural History Museum. A total of 714 adult wild and ­captive specimens were examined between May and July 2007, including 443 skins

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(for pads and nails) and 271 skulls (for toothscrapers). Specimens were ­photographed using a 5.0-megapixel Canon Powershot S2IS with macro ring light, and analysed using “ImageJ 1.38x” for Windows. All images included a scale for calibration. Any specimen found to be damaged during the preservation procedure was discarded from the analysis.

Toothscraper Analysis Four species which rely heavily on exudates were compared respectively with four species of similar size that do not rely on exudates for a significant proportion of their diet (Table 12.1). For the purpose of this study, these are referred to as “exudate-dependent” (ED) and “exudate-independent” (EI) species. Images were analysed to identify differences in shape and relative position of the toothscraper. The angles of the toothscraper and first premolar from the plane of the tooth row were measured from lateral images using ImageJ, and variation between species identified using one-way ANOVA or Kruskal–Wallis (KW), depending on sample sizes. Relative toothscraper length (RTL) was investigated using greatest skull length as an indicator of body size, measured from the most posterior point of the skull to the most anterior part of the rostrum. Toothscraper length was corrected for body size in SPSS version 13.0 using reduced major axis regression due to the random nature of both variables, using a plot of log (base 10) toothscraper length against log (base 10) skull length. Table 12.1  Sample sizes used to compare toothscraper morphology of four exudate-dependent and exudate-independent sized matched pairs (e.g. E. elegantulus with S. alleni) of galago species Sample size (n) Toothscraper Premolar Averagea body mass (g) RTL angle angle Species ED/EI ED 300b 24 20 22 Euoticus elegantulus Sciurocheirus alleni EI 220–455c 7 6 7 Galago moholi ED 160–229d 15 20 39 Galagoides granti EI 135e 9 10 10 Otolemur crassicaudatus ED 1,130f 11 15 13 Otolemur garnettii EI 550–1,200g 12 20 49 Galago matschiei ED 170–250g 1 1 1 23 20 43 EI 112–300h Galago senegalensis Ranges given where data unavailable Charles-Dominique (1977) c Ambrose (2003) d Bearder and Martin (1980) e Courtenay and Bearder (1989) f Bearder (1999) g Kingdon (2003) h Nash et al. (1989) a

b

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Species were initially split into male and female specimens to test for sexual d­ imorphism using KW. Where no significant differences were identified, sexes were pooled for further analyses to increase sample size within a species. For each species the mean RTL was then calculated to allow cross-comparisons. Significant differences between species were identified using one-way ANOVA, or KW where sample sizes fell below the minimum required for parametric tests. All tests used a 0.05 significance level.

Hand and Foot Morphology For the purpose of this study, a pad was defined as a raised area on the palmar or plantar surface. Data were obtained for left and right hands and feet where possible to analyse variation due to distortion during storage. Left and right data sets were not considered independent data but were used as a repeat study to check significant differences found between species. Samples were initially split into sexes to test for sexual dimorphism. Body size was estimated by head-body length to account for allometric variation, and was used due to its availability on museum specimens (Anderson et al. 2000). Pad shape was analysed qualitatively by tracing the outline of each pad to identify variation in shape and orientation. For this stage, a representative specimen per species was chosen for its clarity of pad structure. The pad area for all specimens was then determined using “ImageJ 1.38x,” and corrected for body size to allow allometric comparisons using SPSS version 13.0. This was achieved by plotting a linear regression of the log (base 10) of pad size against the log (base 10) of headbody length for each specimen, using reduced major axis regression due to the random nature of both variables. Standardized pad size residuals were calculated and tested for normality using one-sample Kolmogorov–Smirnov (KS) test. These values were used in further tests. Pad residuals were analysed for variation between sexes for each species using ANOVA. Where no significant variation was detected, male and female data sets in each species were pooled for further analyses. Intrageneric and intraspecific variation was examined to see if pad size is a conservative character using the KW test. Intergeneric and interspecific variation were tested for using ANOVA. To further investigate differences within and between taxa, a Mann–Whitney U-test was conducted to identify significant variation between each genus and species.

Results Toothscraper Morphology A total of 189 specimens were suitable for toothscraper analyses, although note that for the three variables examined only three species pairs could be included in the quantitative analyses due to the sample size of Go. matschiei. No sexual ­dimorphism

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Fig.  12.1  Toothscraper morphology of (a) exudate-dependent and (b) exudate-independent galago species

was ­identified within species, so data sets were pooled when testing variation across taxa. Comparative analyses indicated differences in toothscraper angle (Fig.  12.1), with Euoticus elegantulus being most procumbent (Table 12.2). When comparing size-matched pairs, however, ED species did not consistently possess more procumbent toothscrapers than EI species. Similarly, the angle of the premolar did not distinguish between the ED and EI species. Although no patterns emerged to consistently differentiate between ED and EI species, E. elegantulus did possess a unique characteristic in that the toothscraper protruded beyond the upper incisors. In all other species, the distal end of the toothscraper sat behind the upper incisal row when the tooth rows locked. Consequently, further analyses revealed E. elegantulus to have a significantly longer toothscraper than the size-matched Sciurocheirus alleni, whose RTL resembled that of all other species investigated (c2 = 17.3, df = 1, p < 0.001).

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Table 12.2  Comparative toothscraper and premolar morphology of eight galago species Mean Mean pre-molar toothscraper angle angle Species ED/EI Mean RTL ED 18° 63° 0.10 Euoticus elegantulus Sciurocheirus alleni EI 22° 35° 0.06 Galago moholi ED 27° 42° 0.07 Galagoides granti EI 23° 34° 0.07 Otolemur crassicaudatus ED 34° 56° 0.07 Otolemur garnettii EI 25° 57° 0.08 Galago matschiei ED 23° 33° 0.06 EI 28° 45° 0.07 Galago senegalensis

Fig. 12.2  Reference numbers applied to galago hand pads

Hand Pad Morphology A total of 101 specimens of the left hand and 106 of the right were analysed. Six hand pads were identified in all species (Fig. 12.2). Qualitative Analysis of Pad Shape Comparisons of hand pads revealed differences in the proportion of the palm covered by pads across genera. In Otolemur, the pads covered almost the whole palm, contrasting those of S. alleni whose pads are distinct and suggesting pad shape to

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be related to body size rather than diet. All other genera display distinct pads, but to a lesser degree than in Sciurocheirus. Pad shape also enables Otolemur to be identified, as the interdigital pads appear elongated proximo-distally, contrasting the rounded pads of Galago and Galagoides (Fig. 12.3).

Fig. 12.3  Hand pad morphology of 11 galago species using a representative specimen from each species. Other species examined lacked a single good quality specimen showing all pads. Images have been scaled to the same height

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Statistical Analyses of Hand Pad Size One-way ANOVA on pad residuals within each species revealed no sexual dimorphism, so data were pooled and mean pad size calculated for each species (Table 12.3). Variation in Hand Pad Size at the Species Level Pooled data for each species were then tested for intraspecific variance. No significant differences were identified in any pad size residual (KW, p > 0.05). One-way ANOVA across species found significant differences in pad size residuals two to six of both hands, and pad 1 in the left only (Table 12.4). Pair-wise comparisons revealed the most significant differences between species in pads 4 and 6 of the left hand, and 4 and 5 of the right (Mann–Whitney U-test). Together, these pads can discriminate between 75% of the pair-wise cases. Pads 4, 5 and 6 are therefore most indicative of niche differentiation and should be used for species classification. Variation in Hand Pad Size at the Genus Level Pad size residuals for species within the same genus were pooled and tested for intrageneric differences. A KW test revealed no significant differences within genera in any pad size residual on the left or right hands. Initial comparisons of mean pad size residuals across genera for all pads on the left and right hands revealed significant differences in pad size residuals in all but three cases (Table 12.5). The results indicate that pads 5 and 6 are most useful at distinguishing between genera. Significant variation between genera was further investigated using pair-wise comparisons (Mann–Whitney U-test). The results reiterated findings that pads 5 and 6 are the best discriminators at the genus level. Both pads successfully distinguished 80% of pair-wise cases, suggesting a potential use for galago classification.

Foot Pad Morphology After discarding distorted samples, data were collected from 133 left and 124 right feet, identifying six pads in all species (Fig. 12.4). Comparative Analysis of Foot Pad Shape Qualitative comparisons revealed differences in pad shape and distinction, particularly in pads 4 and 5 (Fig. 12.5). Otolemur and Galago display rounded and distinct

Table 12.3  Mean left and right hand pad size for 15 galago species Mean pad size (mm²) Species 1 2 L 33.18 (10) 47.27 (13) Otolemur crassicaudatus R 43.90 (4) 52.09 (5) Otolemur garnettii L 35.02 (3) 43.24 (7) R 32.13 (3) 43.22 (2) Otolemur monteiri L 48.33 (3) 65.18 (4) R 36.91 (3) 59.47 (2) Euoticus elegantulus L 29.04 (11) 30.54 (12) R 27.81 (10) 29.20 (12) Euoticus pallidus L 17.59 (8) 20.32 (8) R 18.62 (6) 21.73 (6) Sciurocheirus alleni L 14.57 (10) 18.65 (12) R 13.22 (9) 17.76 (11) Sciurocheirus gabonensis L – – R 12.27 (1) 14.08 (2) Galago senegalensis L 15.21 (5) 16.82 (8) R 16.37 (6) 16.51 (8) Galago gallarum L 11.01 (2) 12.30 (2) R 15.76 (1) 17.18 (1) Galago moholi L 14.44 (4) 14.09 (7) R 12.06 (8) 12.31 (14) Galago matschiei L – 16.88 (1) R 18.05 (2) 15.66 (2) 3 23.00 (14) 25.62 (10) 19.24 (8) 20.77 (11) 26.90 (4) 24.21 (3) 14.59 (15) 14.24 (12) 10.38 (10) 11.80 (9) 10.32 (14) 9.43 (14) – 8.08 (3) 6.89 (14) 6.73 (8) 5.82 (2) 7.84 (1) 5.24 (10) 4.70 (17) 6.39 (2) 7.18 (2)

4 31.72 (14) 30.27 (13) 26.70 (11) 27.84 (13) 36.94 (2) 39.24 (2) 16.42 (16) 16.10 (10) 12.76 (8) 13.99 (8) 11.72 (15) 10.70 (14) 9.35 (1) 10.51 (3) 8.56 (12) 8.72 (11) 7.80 (2) 10.41 (2) 7.16 (10) 6.56 (16) 7.78 (2) 10.43 (2)

5 65.64 (16) 75.10 (12) 60.07 (11) 66.05 (12) 114.65 (3) 87.97 (4) 36.86 (13) 39.36 (10) 37.79 (8) 40.29 (9) 25.46 (15) 25.21 (13) – 21.65 (2) 21.46 (12) 23.53 (12) 19.48 (2) 24.62 (2) 19.52 (9) 17.43 (15) 18.16 (2) 27.89 (2) (continued)

6 29.06 (12) 33.13 (11) 29.75 (11) 32.23 (13) 38.72 (3) 31.14 (2) 22.36 (12) 22.43 (8) 20.65 (10) 21.33 (9) 15.66 (12) 15.78 (14) – 12.55 (2) 8.21 (7) 8.17 (4) 8.37 (2) 11.87 (2) 8.06 (5) 7.17 (11) 5.83 (2) 11.28 (2)

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Galagoides demidovii

7.07 (13) 7.19 (14) 11.10 (3) 10.64 (4) 14.89 (1) 14.77 (1) 10.55 (4) 10.16 (3)

Mean pad size (mm²) 1 2

L 6.27 (13) R 7.26 (12) Galagoides thomasi L 10.12 (3) R 10.63 (3) Galagoides granti L 10.57 (2) R 15.09 (1) L   9.71 (3) Galagoides zanzibaricus R   8.69 (1) Numbers in parentheses represent sample size

Species

Table 12.3  (continued)

3.43 (15) 4.00 (14) 5.78 (4) 5.00 (3) 6.55 (1) 6.80 (1) 5.40 (5) 5.66 (5)

3 4.05 (19) 4.35 (15) 7.58 (4) 7.31 (4) 7.56 (1) 7.46 (1) 6.96 (7) 6.06 (5)

4

5 10.02 (16) 10.51 (18) 16.11 (3) 12.75 (4) 15.13 (2) 13.88 (2) 16.48 (7) 16.32 (5)

4.55 (17) 5.49 (16) 4.42 (4) 4.75 (4) 8.07 (2) 9.65 (1) 6.82 (5) 9.46 (4)

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12  A Guide to Galago Diversity: Getting a Grip on How Best to Chew Gum Table 12.4  One-way between species Pad number Hand One L R Two L R Three L R Four L R Five L R L Six R

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ANOVA of hand pad size residuals Significance 0.007** 0.073 0.013* 0.016* 0.000*** 0.004** 0.000*** 0.000*** 0.000*** 0.000*** 0.000*** 0.001***

df 12 12 12 12 12 13 12 13 12 13 12 12

F 2.843 1.860 2.441 2.415 4.471 2.676 4.797 3.570 3.861 3.450 4.209 3.247

Due to small sample sizes, the following species were omitted from the tests: LH: Go. matschiei and S. gabonensis. RH: Go. matschiei (pads 1–6), Gs. zanzibaricus (pad 1), O. monteiri (pads 2 and 6) *Significant at 0.05, **significant at 0.01, ***significant at 0.001 Table  12.5  One-way ANOVA of mean pad size residuals between five genera in the left and right hands (df = 4) Pad number Hand Significance F One L 0.009**   3.815 R 0.200   1.562 Two L 0.011*   3.561 R 0.081   2.203 Three L 0.000***   6.450 R 0.016*   3.254 Four L 0.003**   4.462 R 0.059   2.372 Five L 0.000***   7.527 R 0.001***   5.508 L 0.000*** 11.323 Six R 0.001***   5.315 *Significant at 0.05, **significant at 0.01, ***significant at 0.001

pads 4 and 5, contrasting with the more elongated pads of Euoticus, Galagoides and Sciurocheirus which almost merge with neighbouring pads. Statistical Analyses of Foot Pad Size Reduced major axis regressions for log (base 10) pad size against log (base 10) head-body length allowed calculations of pad size residuals. KS tests of residuals

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Fig. 12.4  Labels applied to the foot pads of all galago species

were not significant, indicating normal distribution of data. ANOVA conducted between sexes revealed no significant differences in pad size for males and females of the same species in all but two right pads (3: F = 4.89, df = 1, p < 0.05; 6: F = 6.129, df = 1, p < 0.05), so data were pooled for further analyses and a mean pad size calculated for each species (Table 12.6). Variation in Foot Pad Size at the Species Level Pooled species data were investigated for variation within each species, revealing no significant differences in pad size (KW). ANOVA across species identified significant interspecific variation in all pads (Table 12.7), suggesting that pad size is a conservative feature within species. Pair-wise comparisons were conducted to further investigate significant differences between species (Mann–Whitney U-test). Once again, pads 4 and 5 revealed the most significant differences, discriminating between 27 of 28 pair-wise cases when used together, and failing only to differentiate between Go. senegalensis and Go. moholi which only showed significant differences in pad 6 of the left foot (U = 14, n1 = 13, n2 = 8, p < 0.01). These pads are therefore the most divergent and are potential tools for classification. Variation in Foot Pad Size at the Genus Level Pad size residuals for species within the same genus were pooled and tested for intrageneric differences to assess whether variation is significantly greater between

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Fig. 12.5  Foot pad morphology of 15 galago species. Images scaled to the same height

than within genera. A KW test on each genus revealed no significant variation. Between genera, significant differences occurred in all pads except pad 3 on the right foot (Table 12.8). Significant variation was investigated further through pairwise comparisons (Mann–Whitney U-test). Pads 4 and 5 were identified as the most useful for discriminating between genera, and when used together could discriminate between all but one pair-wise case, Sciurocheirus and Euoticus (U = 22, n1 = 11, n2 = 10, p > 0.05). This reiterates initial findings that pads 4 and 5 are most reflective of niche differentiation and potentially useful for species identification.

Table 12.6  Mean left and right foot pad size for 15 galago species Mean pad size (mm²) Species 1 2 L 61.85 (9) 23.84 (10) Otolemur crassicaudatus R 58.29 (6) 20.65 (7) Otolemur garnettii L 47.04 (12) 16.91 (12) R 45.25 (6) 16.26 (4) Otolemur monteiri L 73.89 (3) 17.46 (2) R 76.41 (1) 20.52 (1) Euoticus elegantulus L 32.88 (14) 12.20 (12) R 32.21 (16) 12.83 (14) Euoticus pallidus L 32.68 (11) 11.81 (11) R 35.42 (7) 12.63 (10) Sciurocheirus alleni L 27.46 (11) 12.06 (11) R 28.04 (11) 10.51 (13) Sciurocheirus L 28.76 (3) 6.82 (2) gabonensis R – 17.72 (1) Galago senegalensis L 23.92 (5) 7.30 (11) R 24.44 (5) 8.06 (11) Galago gallarum L 21.08 (2) 7.36 (2) R 19.01 (4) 9.06 (3) Galago moholi L 19.54 (8) 5.92 (9) R 19.72 (12) 6.00 (15) 3 41.90 (9) 38.12 (6) 30.42 (10) 24.05 (6) 36.02 (10) 39.57 (1) 15.69 (15) 14.64 (15) 17.65 (12) 17.21 (10) 15.27 (11) 12.15 (13) 13.95 (3) 21.30 (1) 12.01 (11) 10.79 (10) 13.23 (2) 12.36 (3) 10.33 (9) 9.82 (14)

4 36.30 (10) 26.69 (7) 23.20 (7) 20.39 (6) 23.04 (3) 21.27 (2) 23.03 (10) 20.18 (10) 25.74 (12) 26.31 (10) 23.49 (10) 20.58 (12) 17.35 (3) 17.56 (1) 13.41 (9) 14.08 (5) 8.79 (1) 12.98 (2) 12.47 (9) 12.23 (10)

5 28.32 (8) 22.69 (5) 10.70 (6) 11.45 (4) 24.48 (3) 17.30 (2) 24.14 (11) 25.66 (12) 25.43 (12) 24.05 (9) 17.69 (11) 14.48 (12) 21.26 (1) 17.21 (1) 13.34 (11) 13.00 (12) 11.95 (2) 12.52 (4) 12.70 (8) 12.16 (8)

6 82.78 (8) 74.21 (7) 72.27 (8) 84.95 (3) 130.82 (2) 77.58 (1) 41.16 (10) 37.71 (13) 35.99 (10) 48.47 (6) 33.48 (9) 37.42 (10) 34.84 (3) 26.09 (1) 43.97 (14) 43.43 (15) 31.03 (2) 27.81 (2) 30.66 (10) 32.44 (12)

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L R L R L R L R L R

24.95 (2) 25.40 (1) 11.48 (16) 11.68 (18) 16.41 (6) 14.86 (5) 24.41 (1) 23.40 (1) 17.59 (4) 22.39 (1)

Numbers in parentheses represent sample size

Galagoides zanzibaricus

Galagoides granti

Galagoides demidovii Galagoides thomasi

Galago matschiei

6.62 (2) 6.64 (1) 4.09 (15) 4.27 (19) 5.88 (5) 5.89 (5)   8.86 (1)   5.96 (1)   6.05 (4)   9.73 (1)

11.39 (2) 12.04 (1) 5.72 (15) 6.28 (17) 8.53 (6) 8.92 (4) 10.59 (1) –   7.50 (4)   8.77 (1)

17.75 (2) 13.55 (1) 6.28 (14) 6.43 (16) 8.05 (5) 6.40 (2)   8.09 (1) – 11.88 (4) 14.35 (1)

15.09 (2) 17.96 (1) 4.39 (12) 4.22 (10) 6.51 (5) 4.27 (2)   8.09 (1) – 10.22 (4)   6.65 (1)

30.89 (2) 40.66 (1) 15.62 (14) 16.54 (13) 19.72 (5) 17.44 (4) 29.32 (1) – 24.68 (4) 25.33 (1)

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I.R. Stephenson et al. Table  12.7  One-way ANOVA of foot pad size residuals between species Pad number Foot Significance df F One L 0.000*** 13   3.755 R 0.005** 10   2.991 Two L 0.000*** 13   4.499 R 0.000*** 10   3.833 Three L 0.000*** 13   4.172 R 0.014*  9   2.581 Four L 0.000*** 13   9.560 R 0.000***  9 11.225 Five L 0.000*** 12 13.980 R 0.000***  9 12.210 Six L 0.000*** 12   5.086 R 0.000***  9   5.434 Due to small sample sizes, the following species were omitted from the tests: LF: Go. matschiei (1–6), S. gabonensis (5), E. elegantulus (6). RF: Go. matschiei (1–6), O. monteiri (1–6), S. gabonensis (1–6), Gs. zanzibaricus (1–6), Gs. granti (3–6) Significance levels: *0.05, **0.01, ***0.001 Table  12.8  One-way ANOVA of foot pad size residuals between genera (df = 4) Pad number Foot Significance F One L 0.000***   6.668 R 0.001***   5.213 Two L 0.000***   5.660 R 0.000***   6.054 Three L 0.001***   5.414 R 0.120   1.907 Four L 0.000*** 16.081 R 0.000*** 19.592 Five L 0.000*** 22.533 R 0.000*** 22.244 L 0.000***   9.344 Six R 0.001***   5.307 *Significant at 0.05, **significant at 0.01, ***significant at 0.001

Nail Shape Initial observations revealed three nail shapes – convex, concave and keeled/ pointed (Fig. 12.6). Otolemur exhibited nails with concave distal ends terminating in a sharp point at either side on digits 2–5 of the hand and 3–5 of the foot, and to a lesser extent on the pollex. Conversely, the hallux was convex. Examinations of Euoticus species revealed a pointed and keeled shape in nails 2–5 of the hand and pedal digits 3–5, with the keel running down the proximo-distal midline. In all

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Fig.  12.6  The three nail forms identified in galagos (a) concave (Otolemur crassicaudatus), (b) keeled and pointed (Euoticus elegantulus), and (c) convex (Sciurocheirus gabonensis)

other species, nails were convex, with the exception of Go. matschiei whose nails were pointed and keeled, though not to the extent of the Euoticus species.

Discussion Dental Adaptations to Exudate Eating Comparative statistical analysis of toothscrapers failed to identify characteristics that indicate adaptations to diet, and were unable to differentiate between ED and EI species. Eaglen (1986) suggests that this is to be expected because galagos are typically scrapers. While the toothscraper is used to harvest gum, because the scraping method only requires the teeth to puncture hardened gum and not to inflict direct damage to the bark, the small forces required have not led to specific adaptations for exudate eating. In the case of E. elegantulus, it may damage trees using the caniniform premolars (Charles-Dominique and Petter 1980), which may explain the difference found in the orientation of the lower premolar. The relatively long toothscraper may then increase efficiency of gum harvesting in this species.

Implications for the Evolution of the Toothscraper The results suggest that although the toothscraper is used during exudate feeding, adaptations do not appear to have evolved in the dentition of all ED species, suggesting exudate-eating was not the stimulus for its evolution. An alternative hypothesis is that the alignment of the anterior dentition allows the teeth to be used as a comb during grooming (Buettner-Janusch and Andrew 1962). Although galagos are often grouped under “solitary foragers,” their gregarious habits during the resting phase are often overlooked. E. elegantulus for example can be found in

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groups of up to seven (Charles-Dominique 1977). It is plausible, therefore, that the ­toothscraper may aid in social and self-grooming. Although this study has not identified the toothscraper as evolving for dietary needs, it should not be assumed that the grooming hypothesis is the correct alternative. One of the reasons for rejecting the diet hypothesis (Martin 1972) is that the toothscraper appears unable to withstand the forces required to damage bark. If the toothscraper is used primarily to puncture hardened gum, and if that requires less force than gouging bark, this may account for the results (Williams et al. 2002). Further research into toothscraper morphology using alternate comparative measurements may also be worth investigating. It is important therefore to take a holistic view of adaptations to increasing efficiency of exudate harvesting.

Hand and Foot Pad Morphology The identification of six pads on the palms and soles reiterates findings in much of the existing literature, although two studies contradicted this, detecting five hand pads (Anderson 1999; Anderson et al. 2000). One possible explanation is that in several species the pads fuse, and are therefore interpreted as one. Where some degree of merging occurred we kept pads distinct as the dermatoglyphic ridges, where visible, clearly distinguished the pads due to the concentric patterns formed around each pad. The implications of these findings are that any further examinations of the pads may be incorrect if pads are misidentified. However, the results of this study suggest that pad shape and size are conservative within taxa but vary significantly across taxa at the genus and species level, suggesting a potential use for species identification. The comparative study of pad size identified hand pads 5 and 6, and 4 and 5 in the feet, as potentially the best taxonomic indicators, supporting earlier studies that found significant differences in volar pad positions across taxa (Anderson 1999; Anderson et al. 2000). Functional Significance of Pad Morphology Differences in the degree of pad merging support Cartmill’s (1974, 1979) theory that larger bodied galagos should possess more coalesced pads because their viscous properties allow a degree of deforming when in contact with a substrate, meaning frictional forces are reduced to a fraction of the load. Larger galagos therefore produce lower frictional forces relative to size, requiring more coalesced pads to increase the extent of interlocking and produce enough force to boost stability on supports (Cartmill 1974, 1979). The evolution of expanded volar pads is thought to have occurred with the reduction of claws in ancestral primates (Soligo and Martin 2006). Although claws allow locomotion on arboreal substrates, on small diameter supports it is possible to grasp branches using muscular strength coupled with frictional forces (Soligo

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and Martin 2006). This force is enhanced by increasing the contact area by adapting the size and shape of pads. A problem arises with small-bodied prosimians, as the theory suggests claws would have a greater advantage as they could cling to larger supports that cannot be grasped. As galagos are known to exploit a wide variety of substrates, they must have evolved other mechanisms of increasing the adhesive properties of the hands. Behavioral activity such as urinating on the hands and feet has been recorded in many species and is thought to improve grip (Clark 1982). One exception to this is the genus Euoticus, which has not been reported to urine wash, yet exploits broad, vertical supports to access gum deposits. However, they appear to have developed morphological specializations to the nails to enhance grip.

Nail Shape and the Exploitation of Exudates The comparative study of nail shape highlighted a diversity of shapes, supporting Thorndike’s (1968) hypothesis of a gradient from nails to claws. The results lend weight to the hypothesis that larger primates require additional mechanisms of increasing grip due to the loss of claws. As well as increasing pad coalescence and moistening pads with urine, it seems that adaptations have arisen in the nails to enhance grip on large-diameter supports where exudates are prevalent. Otolemur species possess concave nails with lateral points which act similarly to a claw, allowing locomotion on steeper, broader supports. Euoticus species have also developed pointed and keeled nails which allow them to exploit much larger supports which are inaccessible to other species, thereby reducing competition for resources and allowing them to gain almost all their daily nutritional or caloric requirements from exudates.

Hand and Foot Morphology and Niche Differentiation The variation identified in the hands and feet is likely to have arisen through adaptations to specialist niches or “adaptive zones” (Van Valen 1976). According to Gause’s Law of Competitive Exclusion (1934), two species cannot stably coexist if they share exactly the same niche, meaning that there must be some degree of divergence in the exploitation of resources to avoid competition. Through habitat differentiation, selection pressures acting upon populations promote specialization to a particular niche, resulting in species-specific adaptations that allow foraging and locomotion on the substrates within that environment (Schluter 1996). In this case, we were interested in whether these differences reflected adaptations to increasing the ability to exploit exudates. As hands and feet function as the interface between the animal and its environment, it seems that each species has developed specific hand and foot pad morphologies and nail specializations to optimize

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the degree of interlocking with the substrate, allowing exploitation of large-branch niches (Anderson 1999). Such variation in hand and foot morphology also has implications for classification, so it should be investigated further to examine the possibilities for species-identification in this otherwise cryptic group. Acknowledgments  Many thanks to Dr. Nekaris for her invaluable help, and to the Powell-Cotton (Kent) and Natural History (London) museums, in particular Malcolm Harman and Paula Jenkins.

References Ambrose, L. (2003). Three Acoustic Forms of Allen’s Galagos (Primates; Galagonidae) in the Central African Region. Primates 44, 25–39. Anderson, M. J. (1999). The Use of Hand Morphology in the Taxonomy of Galagos. Primates 40(3), 469–478. Anderson, M. J., Ambrose, L., Bearder, S. K., Dixson, A. F. and Pullen, S. (2000). Intraspecific Variation in the Vocalisations and Hand Pad Morphology of Southern Lesser Bush Babies (Galago moholi): A Comparison with G. senegalensis. International Journal of Primatology 21(3), 537–555. Bearder, S. K. (1999). Physical and Social Diversity Among Nocturnal Primates: A New View Based on Long Term Research. Primates 40(1), 267–282. Bearder, S. K. and Martin, R. D. (1980). Acacia Gum and Its Use by Bushbabies, Galago senegalensis (Primates Lorisidae). International Journal of Primatology 1, 103–128. Buettner-Janusch, J. and Andrew, R. J. (1962). The Use of Incisors by Primates in Grooming. American Journal of Physical Anthropology 20, 127–129. Burrows, A. M. and Nash, L. T. (2007). Introduction: Evolution, Morphology, and Behaviour of Lorisoid Primates. American Journal of Primatology 69, 1–5. Cartmill, M. (1974). Pads and Claws in Arboreal Locomotion. In: Jenkins, F. A. Jr. (ed.) Primate Locomotion, 45–84. New York: Academic Press Inc. Cartmill, M. (1979). The Volar Skin of Primates: Its Frictional Characteristics and Their Functional Significance. American Journal of Physical Anthropology 50, 497–510. Charles-Dominique, P. (1977). Ecology and Behaviour of Nocturnal Prosimians. London: Duckworth. Charles-Dominique, P. and Petter, J.J. (1980). Ecology and social life of Phaner furcifer. In: Charles-Dominique, P. (ed.) Nocturnal Malagasy Primates, 75–96. New York: Academic Press Inc. Clark, A. B. (1982). Scent Marks as Social Signals in Galago crassicaudatus: I. Sex and Reproductive Status as Factors in Signals and Responses. Journal of Chemical Ecology 8, 1133–1151. Courtenay, D. O. and Bearder, S. K. (1989). The Taxonomic Status and Distribution of Bushbabies in Malawi with Emphasis on the Significance of Vocalisations. International Journal of Primatology 10(1), 17–34. Eaglen, R. H. (1986). Morphometrics of the Anterior Dentition in Strepsirhine Primates. American Journal of Physical Anthropology 71, 185–201. Gause, G. F. (1934). The Struggle for Existence. Baltimore, MD: Williams and Wilkins. Grubb, P., Butynski, T. M., Oates, J. F., Bearder, S. K., Disotell, T. R., Groves, C. and Struhsaker, T. (2003) Assessment of the Diversity of African Primates. International Journal of Primatology 24(6), 1301–1357. Kingdon, J. (2003). The Kingdon Field Guide to African Mammals, New Edition. London: A&C Black.

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Martin, R. D. (1972). Adaptive Radiation and Behaviour of the Malagasy Lemurs. Philosophical Transactions of the Royal Society of London 264, 295–352. Mayr, E. (1963). Animal Species and Evolution. Cambridge: Harvard University Press. Nash, L. T., Bearder, S. K. and Olson, T. R. (1989). Synopsis of Galago Species Characteristics. International Journal of Primatology 10(1), 57–80. Schluter, D. (1996). Ecological Causes of Adaptive Radiation. The American Naturalist 148, S40–S64. Soligo, C. and Martin, R. D. (2006). Adaptive Origins of Primates Revisited. Journal of Human Evolution 50, 414–430. Taylor, A. B. and Vinyard, C. J. (2004). Comparative Analysis of Masseter Fiber Architecture in Tree-Gouging (Callithrix jacchus) and Non-Gouging (Saguinus oedipus) Callitrichids. Journal of Morphology 261(3), 276–285. Thorndike, E. (1968).A Microscopic Study of the Marmoset Claw and Nail. American Journal of Physical Anthropology 28, 247–262. Van Valen, L. (1976). Ecological Species, Multispecies, and Oaks. Taxon 25(2/3), 233–239. Viguier, B. (2004). Functional Adaptations in the Craniofacial Morphology of Malagasy Primates: Shape Variations Associated with Gummivory in the Family Cheirogaleidae. Annals of Anatomy 186, 495–501. Williams, S. H., Wall, C. E., Vinyard, C. J. and Hylander, W. L. (2002). A Biomechanical Analysis of Skull Form in Gum-Harvesting Galagids. Folia Primatologica 73, 197–209.

Chapter 13

Tongue Morphology in Infant and Adult Bushbabies (Otolemur spp.) Beth A. Docherty, Laura J. Alport, Kunwar P. Bhatnagar, Anne M. Burrows, and Timothy D. Smith

Abstract  Lingual fungiform papillae are the only structures on the anterior two-thirds of the tongue that contain taste receptor cells and are the first gustatory structures to encounter food items. In humans, density of fungiform papillae is associated with taste sensitivity and food selection. Nonhuman primates also use the sense of taste to detect the nutritional contents of potential food items. The present study examines the ontogeny, distribution, and density of fungiform papillae in two species of greater bushbaby that differ in dietary specialization. Using light and electron microscopic methods, adult and infant cadaveric specimens (n = 4) of the frugivorous Otolemur garnettii and the exudativorous O. crassicaudatus were examined. The density of fungiform papillae was measured in an additional three adults of each species using 0.5% methylene blue. Observations by light and scanning electron microscopy (SEM) indicate that receptor pores are open in neonates. One adult O. crassicaudatus examined by SEM shows a high number of anterior fungiform papillae on which one or more open taste pores can be observed. The mean density of fungiform papillae was more than 50% greater in O. garnettii (162.4 ± 70.63/ cm2) compared to that in O. crassicaudatus (101.9 ± 20.63/cm2). These results suggest that greater bushbabies may have precocious ability to detect taste stimuli, based on the presence of open taste pores at birth. The apparent difference in fungiform papillae density between species requires further exploration.

Introduction The function of the primate gustatory system is to detect the chemical contents of potential food items. In particular, taste sensitivity in nonhuman primates is thought to be associated with food selection and dietary niche (Bonnaire and Simmen 1994;

T.D. Smith () School of Physical Therapy, Slipperg Rock University, Slipperg Rock, PA 16057, 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_13, © Springer Science+Business Media, LLC 2010

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Riba-Hernández et al. 2003; Simmen 1994; Laska 1996, 1999; Laska et al. 1996; Simmen and Hladik 1998; Laska et al. 1999, 2000). Transduction of chemical compounds within the gustatory system occurs within taste receptor cells. Taste receptor cells are clustered in groups along with other cell types to form taste buds. Taste buds are located in the lingual epithelium of gustatory papillae on the tongue and soft palate and have been reported in other locations along the upper digestive tract (Buck 2000). There are four types of lingual papillae on the primate tongue, three of which contain taste buds (Fig. 13.1a–d). Filiform papillae are located across the superior surface of the tongue and are nongustatory. They may serve to move food around the mouth. Circumvallate and foliate papillae are located on the posterior one-third of the tongue surface, while fungiform papillae are located on the anterior two-thirds of the tongue (Purves et al. 1997; Buck 2000). Taste buds access chemical stimuli via openings (“taste pores”) on their surface (Fig. 13.1e). Among humans, taste sensitivity is linked to lingual anatomy. Specifically, density of fungiform papillae is positively correlated with taste sensitivity to numerous natural and synthetic compounds (Miller and Whitney 1989; Miller and Bartoshuk 1991; Reedy et  al. 1993; Bartoshuk et  al. 1994; Hosako-Naito et  al. 1996; Smith 1971; Tepper and Nurse 1997, 1998; Tepper 1999; Prutkin et al. 2000; Delwiche et al. 2001; Doty et al. 2001; Yakinous and Guinard 2001, 2002; Essick et al. 2003). Fungiform papillae are formed early in fetal development and remain intact throughout adulthood (Mistretta 1991). Fungiform papillae are the only structures on the anterior two-thirds of the tongue containing taste buds. As the first papillae to come in contact with food entering the mouth

Fig. 13.1  (a) Schematic diagram of three types of gustatory lingual papillae (modified from Fain 2003). Taste buds are congregations of taste receptor cells on each papilla (b–d). Each taste bud receives taste stimulants through an opening (taste pore (e))

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(Dodd and Castellucci 1991; Purves et al. 1997), these structures are sentinels of taste perception, and are probably critical to food selection. Indeed, the density of fungiform papillae has been associated with food selection in humans (Anliker et  al. 1991; Drewnowski and Rock 1995; Tepper 1998; Drewnowski et  al. 1998, 1999, 2000; Kaminski et  al. 2000; Ly and Drewnowski 2001; Dinehart et al. 2006). Certain microanatomical features of the mammalian tongue have been wellstudied. The distribution of fungiform papillae in mammals, including primates, has been qualitatively studied (e.g., Kobota and Hayama 1964). However, as more than one taste bud may be found on a single fungiform papilla, the actual number of taste buds remains a more complicated question, and is unknown for most taxa. In addition, the time at which taste bud openings (pores), through which they receive stimuli, become patent has been studied for some mammals (e.g., Robinson and Winkles 1990; Mbiene and Farbman 1993; Iwasaki et  al. 1997). However, detailed microanatomical observations on the tongue of nonhuman primates are relatively lacking, especially in strepsirrhines. This is unfortunate, given the great dietary diversity of primates. To that end, this report provides a preliminary analysis of the ontogeny, distribution, and density of fungiform papillae in two species of greater bushbaby (Otolemur) that differ in dietary specialization.

Methods Light Microscopy Half tongues (after each tongue was bisected in the mid-sagittal plane) of two adult and two infant greater bushbabies (O. crassicaudatus and O. garnettii; taxonomy following Groves 2001) were investigated. These specimens were available from a collection used to study nasal structures, and were fixed and stored in 10% buffered formalin (Smith et al. 2007). The two adults were prepared for examination in the sagittal plane as follows. Each tongue was transected along the midline and the right side was further divided into two to three segments anteroposteriorly. These segments were paraffin embedded and sectioned in the sagittal plane at 10 µm. The infant tongues had previously been sectioned in the coronal plane when half heads were prepared in a previous study (Smith et  al. 2007). Every tenth section was stained with hematoxylin–eosin or Gomori trichrome procedures. Each series of sections was examined using a DMLB Leica photomicroscope at X100–X630. The fungiform papillae were examined for the presence of taste buds on their external surface.

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Scanning Electron Microscopy Half tongues (contralateral side of the above specimens) of two adult greater bushbabies (O. crassicaudatus and O. garnettii) and one infant (O. garnettii) were prepared for study by scanning electron microscopy (SEM) as follows. The left side of the three tongues used for light microscopy (LM) (see below) was prepared. The tongues were rinsed in distilled water for 5 min. The tissues were then dehydrated in a series of ethanol washes, immersed in two hexamethyldisilazane (HMDS) baths for 15 min, and air-dried at ambient temperature. After air-drying, the sample was mounted on a stainless steel stub and sputter-coated with gold in a Blazers MED model 010 Turbo Mini Deposition System. Secondary electron (SE) images were taken with a CamScan Series 4 scanning electron microscope operated at an accelerating voltage of 5–20 kV and a working distance of 15 mm. Images were acquired digitally using Princeton Gamma-Tech’s (PGT) IMIX system. The PGT system was calibrated using an MRS-3 SEM magnification calibration grid, purchased from Ted Pella, Inc., Redding, CA.

Quantification of Fungiform Papillae in Adult Otolemur For a preliminary quantitative analysis, the density of fungiform papillae was measured in three adults of each species. The methods for identifying fungiform papillae followed the protocol established by Miller and Reedy (1990a, b). Methylene blue biological stain (0.5% in ethanol) was applied to the superior surface of the tongue and extra methylene blue was wiped off with Kim Wipes (Fischer Scientific, Pittsburgh, PA). The stain adheres to all papilla types except fungiform papillae, permitting visual identification of this papilla type. After staining, a digital photograph of the tongue was taken, using the macro function of a Canon A80. A scale was included in each image. Using Adobe Photoshop software, a 0.5 cm line was drawn on the scale and moved to the medial line of the tongue so that the line began at the anterior-most point at the tip of the tongue. A square was then drawn starting at the posterior edge (top) of the 0.5 cm line and the left vertical edge of the square was aligned along the vertical 0.5 cm line. This provided a right angle from the vertical line. The horizontal (top) edge of the square, located 0.5 cm from the tongue tip, was used as a guide to draw a horizontal line across the right side of the tongue. This procedure was repeated on the left side of the tongue using the square to provide a right angle. Once a continuous horizontal line was drawn across the tongue 0.5  cm posterior to the tip, the vertical 0.5  cm line was removed. Subsequently, all fungiform papillae anterior to that line were counted. Each counted papilla was marked with a colored dot in order to avoid repeated counting of papillae. NIH ImageJ software was used to determine the area (square centimeters) in which fungiform papillae were counted and the density of fungiform papillae was calculated.

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Results Microscopic Characteristics of the Tongue in Otolemur SEM reveals elongated, columnar filiform papillae in adults of both species of Otolemur (Fig. 13.2). In O. garnettii, anterior and posterior projections of filiform papillae appear proportionally longer than in O. crassicaudatus, especially the anterior, bifid process (Fig. 13.2b). Fungiform papillae are similar in shape in both species. Taste pores are visible by randomly viewing fungiform papillae at high magnifications, though not all of them exhibit clearly patent taste pores. When visible, taste pores are approximately 5 µm or less in diameter (Fig. 13.3). Relative to the adult O. crassicaudatus, the adult O. garnettii appeared to have more fungiform papillae with two or more patent taste pores. However, the O. crassicaudatus specimen appeared to have been coated too thickly with gold, leaving identification of some taste pores tentative (Fig. 13.3a). In both species, infant Otolemur has at least some patent taste pores (Fig. 13.4). However, this is only inferred from LM observations of O. garnettii, based on the lack of apical closure of a single taste bud (Fig.  13.4a). Clear visualization of taste pores in the specimens in our sample is

Fig. 13.2  SEM micrographs of the anterior tongue in adult specimens of Otolemur spp. Low and intermediate magnifications are shown. (a, b) In O. garnettii, note the proportionately longer filiform papillae (FiP), including longer bifid anterior processes (arrows) compared to that in O. crassicaudatus (c, d). Asterisks, fungiform papilla

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Fig. 13.3  SEM micrographs of fungiform papillae on the anterior tongue in adult specimens of Otolemur spp. Small arrows indicate taste pores. In (a), multiple small depressions appear to be taste pores that were overcoated during the preparation for SEM

unlikely because the opening would be obscured within a 10 µm thick section. In the infant O. crassicaudatus, clear taste pores are seen using SEM (Fig. 13.4b, c). In adult Otolemur, taste buds are clearly visible as lightly stained cellular masses on the dorsum of fungiform papillae (Figs. 13.5 and 13.6). Taste pores are rarely apparent in this sample due to sectional thickness, but could sometimes be inferred (Fig. 13.5c). Instances of more than one taste bud within the same fungiform papillae occur (Fig. 13.5a, b). Based on this sampling of sections, this occurred more frequently in the adult O. garnettii specimen compared to the adult O. crassicaudatus. Examination of the infant specimens yields a similar impression (Fig. 13.7). In fewer cases, more than one taste bud was noted in two fungiform papillae of O. crassicaudatus (Fig. 13.8).

Quantitative Findings In the adult tongue specimens, mean density of fungiform papillae appears to differ by about 50%, with a larger number in O. garnettii. In O. garnettii, fungiform papillae density is 162.4 ± 70.63/cm2. Mean density of fungiform papillae in O. crassicaudatus is 101.9 ± 20.63/cm2. The high degree of variation is possibly due to a small sample

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Fig. 13.4  Light microscopy and SEM micrographs of fungiform papillae on the anterior tongue in infant specimens of Otolemur spp. Taste pores could not be clearly visualized in O. garnettii but probably were obscured by section thickness. However, the apical location of the taste pore shown above ((a) O. garnettii), indicates that open pores are likely. In O. crassicaudatus (b, c), some taste pores were clearly patent

size in each species. Therefore, statistical analyses will be carried out in a future study using a broader array of species (Alport 2009).

Discussion Comparative Morphology of Tongue Papillae in Mammals Tongue papillae have been studied in a broad array of mammals, and can be seen grossly. In diverse mammals, fungiform papillae are morphologically similar (Frappier 1998). They are most dense anteriorly (Miller and Preslar 1975; Davies et al. 1979; Robinson and Winkles 1990), except in pigs where they are denser along lateral margin (Mack et al. 1997). Filiform papillae vary greatly, especially in the length of projection (Frappier 1998). These are generally regarded as having mechanical

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Fig.  13.5  Light microscopy micrographs of fungiform papillae on the anterior tongue in adult specimens of Otolemur garnettii. Small arrows indicate taste buds. In (c), a taste pore is visible (arrow head)

functions (Jackowiak and Godynicki 2007; Pastor et al. 2008). Otolemur species resemble most mammals with respect to distribution of papillae over the anterior tongue. Filiform papillae cover most of the tongue surface area and fungiform papillae are scattered over the dorsum of the tongue. Finer morphological features are only visible by microscopy. Microscopic methods have revealed variations in the number of taste buds or their pores on fungiform papillae among mammals (e.g., Mack et al. 1997; Jackowiak and Godynicki 2007). Taste buds and pores in primates will be considered further below. Few reports have described primate filiform papillae in detail. For that reason, a few comparative statements concerning Otolemur are merited here. Kobota and Iwamoto (1967) described filiform papillae of the loris but provided few details (poorly innervated, highly keratinized) and Kobota and Hayama (1964) provided no morphological description of marmosets. Kobayashi et  al. (2004) describe electron microscopic characteristics of lingual papillae in tamarins, macaques, mandrills, and humans. All of these primates possessed slender tips to filiform papillae. Some subtle differences in connective tissue cores were described, but these observations should be verified

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Fig.  13.6  Light microscopy micrographs of fungiform papillae on the anterior tongue in adult specimen of Otolemur crassicaudatus. Small arrows indicate taste buds

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Fig. 13.7  Light microscopy micrographs of fungiform papillae (FP), as well as filiform papillae (FiP) on the anterior tongue in infant specimen of Otolemur garnettii. Small arrows indicate taste buds

to ensure that the differences were not due to artifact. SEM studies rely on small sample sizes, so Otolemur should be viewed within a broad context. Possessing long slender filiform papilla appears to be common among diverse primate taxa, and may well have a similar (nongustatory) function in all primates. Other particulars, such as the apparent difference in relative length of the papilla, or the pronounced bifid anterior prominence in O. garnettii, require further study to determine if these are true species differences and functional correlates of such differences.

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Fig. 13.8  Light microscopy micrographs of fungiform papillae on the anterior tongue in infant specimen of Otolemur crassicuadatus. Small arrows indicate taste buds

Taste Buds and Pores Descriptive accounts of taste buds in fungiform papillae of different mammals are numerous, and illustrate the gustatory importance of fungiform papillae on the anterior part of the tongue of diverse mammals (Murray and Murray 1960; Kobota and Hayama 1964; Kobota et al. 1966; Kobota and Iwamoto 1967; Miller and Preslar 1975; Davies et al. 1979; Robinson and Winkles 1990; Mack et al. 1997; Pastor et al. 2008). Far fewer studies have identified taste pores, which are difficult to view except by electron microscopy. Kobota and colleagues (Kobota and Hayama 1964; Kobota and Iwamoto 1967; Kobota et  al. 1966) published a series of studies and found no visible taste pores in several adult samples of mammals, including a loris and marmoset. These negative findings cannot be trusted however, as these studies relied on light microscopic examination of thick sections. Taste pores would be obscured within thickness of the sections used by Kobota et al. (30 µm). In other studies, taste pores have been used as indicators for the presence of taste buds. Some mammals may have numerous taste buds in each fungiform papilla (3–26 in pigs; Mack et al. 1997), while others may have a single taste bud per papilla (feathertail glider; Jackowiak and Godynicki 2007). While we have not yet quantified taste buds

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in Otolemur, adults of both species studied here have fungiform papillae with two or more taste buds. Although taste buds are of a size (10–20 µm) that they are rarely missed, it is possible to miss taste buds in intervals between stained sections. Accurate quantification of the number of taste buds per fungiform papilla demands the availability of serial sections, or SEM imaging. The preliminary data of this study suggest that this may be a worthwhile pursuit. The more frequent observation of multiple taste buds, pores, and fungiform papillae in O. garnettii, if a true characteristic of the species, may relate to its high degree of frugivory. The SEM and LM observations herein also allow an ontogenetic comparison of bushbabies to other mammals. Available evidence indicates that gustatory capacity may increase with postnatal age in at least some mammals. Kittens have a similar number of fungiform papillae as adults, but each with fewer taste buds (Robinson and Winkles 1990). In rats there is a delay in the opening of taste pores, which occurs after postnatal day 0, and as late as 10 days after birth (Mbiene and Farbman 1993; Iwasaki et  al. 1997). These observations do not rule out chemoreceptive capacity, as it is suggested that the cells overlying taste pores in rats are water permeable, allowing prenatal gustatory capabilities in rats (Mbiene and Farbman 1993). Still, there appears to be a postnatal maturation of taste bud/pore morphology in some mammals. Without quantification, we can make no assessment of age-related changes in Otolemur. However, infant greater bushbabies likely have gustatory capability at birth (or earlier), as indicated by the open taste pores observed in the two neonates. Further work is needed to verify other functional aspects of taste buds in these and other primates. Generally, sensory organs are highly precocious at birth in primates relative to some other mammals (Derrickson 1992; Starck and Ricklefs 1998; Steiner et al. 2001).

Summary and Conclusions Microanatomical examination suggests that both species of Otolemur have the potential for precocious gustatory abilities, as indicated by open taste pores in newborns. Several lines of evidence suggest that the highly frugivorous O. garnettii may have more taste buds overall than the less frugivorous, exudativorous O. crassicaudatus. Quantitative results indicate that the O. garnettii has more fungiform papillae (mean density was more than 50% greater). Qualitative observations suggest that this species may also have more taste buds per fungiform papilla. In sum, these may correlate with greater gustatory perception in O. garnettii. The bushbabies differ in dietary specialization, each species having a specific dietary emphasis (O. garnettii: fruit; O. crassicaudatus: exudates) (Charles-Dominique 1977). Interestingly, density of fungiform papillae may not relate to frugivory (Alport, unpublished observations). However, number of taste buds per fungiform papilla in frugivores versus nonfrugivores remains poorly known. This report emphasizes the need for more similar microanatomical observations in larger samples and a broader range of taxa.

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Acknowledgments  We thank PPG Industries, Inc., especially Kelly Wiley, for coating some of the specimens examined by SEM. George Harding of University of Louisville coated two others. Lauren Reinholt stained some of the specimens used for LM study. Lastly, we thank the staff of the Duquesne University Instrumentation Department for numerous courtesies in troubleshooting difficulties with equipment and maintaining the SE microscope system.

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Iwasaki S-I, Yoshizawa H, Kawahara I (1997) Study by electron microscopy of the morphogenesis of three types of lingual papilla in the rat. Anat Rec 247:528–541. Jackowiak H, Godynicki S (2007) Light and scanning electron microscopic study on the structure of the lingual papillae of the feathertail glider (Acrobates pygmeus, Burramyidae, Marsupialia). Anat Rec 290:1355–1365. Kaminski LC, Henderson SA, Drewnowski A (2000) Young women’s food preferences and taste repsonsiveness to 6-n-porpylthiouracil (PROP). Physiol Behav 2000:691–697. Kobota K, Fukuda N, Asakura S (1966) Comparative anatomical and neurohistological observations on the tongue of the porcupine (Histrix cristata). Anat Rec 155:261–268. Kobota K, Hayama S (1964) Comparative anatomical and neurohistological observations on the tongues of pygmy and common marmosets. Anat Rec 150:473–485. Kobota K, Iwamoto M (1967) Comparative anatomical and neurohistological observations on the tongue of slow loris (Nycticebus coucang). Anat Rec 158:163–175. Kobayashi K, Kumakura M, Yoshimura K et al. (2004) Comparative morphological studies on the stereo structure of the lingual papillae of selected primates using scanning electron microscopy. Ann Anat 186:525–530. Laska M (1996) Taste preference thresholds for food-associated sugars in the squirrel monkey (Saimiri sciureus). Primates 37:91–95. Laska M (1999) Taste responsiveness to food-associated acids in the squirrel monkey (Saimiri sciureus). J Chem Ecol 25:1623–1631. Laska M, Carrera Sanchez E, Rodriguez Luna E (1996) Gustatory thresholds for food associated sugars in the spider monkey (Ateles geoffroyi). Am J Primatol 39:189–193. Laska M, Schull E, Scheuber H-P (1999) Taste preference thresholds for food associated sugars in baboons (Papio hamadryas anubis). Int J Primatol 20:25–34. Laska M, Hernandez Salazar LT, Rodriguez Luna E (2000) Food preferences and nutrient composition in captive spider monkeys, Ateles geoffroyi. Int J Primatol 21:671–683. Ly A, Drewnowski A (2001) PROP (6-n-propylthiouracil) tasting and sensory responses to caffeine, sucrose, neohesperidin dihydrochalcone and chocolate. Chem Senses 26:41–47. Mack A, Singh A, Gilroy C et al. (1997) Porcine lingual taste buds: a quantitative study. Anat Rec 247:33–37. Mbiene JP, Farbman AI (1993) Evidence for stimulus access to taste cells and nerves during development: an electron microscopic study. Microsc Res Tech 26:94–105. Miller IJ, Bartoshuk LM (1991) Taste perception, taste bud distribution, and spatial relationships. In: Getchell TV, Doty RL, Bartoshuk LM, and Snow JBJ (eds.) Smell and taste in health and disease. Raven Press, New York. Miller IJ, Preslar AJ (1975) Spatial distribution of rat Fungiform papillae. Anat Rec 181:679–684. Miller IJ, Reedy FE (1990a) Variations in human taste bud density and taste intensity perception. Physiol Behav 47:1213–1219. Miller IJ, Reedy FE (1990b) Quantification of fungiform papillae and taste pores in living human subjects. Chem Senses 15:281–294. Miller IJ, Whitney G (1989) Sucrose octaacetate-taster mice have more vallate taste buds than non-tasters. Neurosci Lett 100:271–275. Mistretta CM (1991) Developmental neurobiology of the taste system. In: Getchell TV, Doty RL, Bartoshuk LM, Snow JJ (eds.) Smell and taste in health and disease, Raven Press, New York. Murray RG, Murray A (1960) The fine structure of the taste buds of Rhesus and cynomalgus monkeys. Anat Rec 138:211–233. Pastor JF, Barbosa M, De Paz FJ (2008) Morphological study of the lingual papillae of the giant panda (Ailuropoda melanoleuca) by scanning electron microscopy. J Anat 212:99–105. Prutkin J, Duffy VB, Etter L et al. (2000) Genetic variation and inferences about perceived taste intensity in mice and men. Physiol Behav 69:161–173. Purves D, Fitzpatric D, Katz LC et  al. (1997) Neuroscience. Sinaur Associates, Inc., Sunderland, MA.

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Reedy FE, Bartoshuk LM, Miller IJ et al. (1993) Relationships among papillae, taste pores, and 6-n-propythiouracil (PROP) suprathreshold taste sensitivity. Chem Senses 18:618–619. Riba-Hernández P, Stoner KE, Lucas PW (2003) The sugar composition of fruits in the diet of spider monkeys (Ateles geoffroyi) in tropical humid forest in Costa Rica. J Trop Ecol 19:709–716. Robinson PP, Winkles PA (1990) Quantitative study of fungiform papillae and taste buds on the cat’s tongue. Anat Rec 225:108–111. Simmen B (1994) Taste discrimination and diet differentiation among New World primates. In: Chivers DJ, Langer P (eds.) The digestive system of mammals: Food, form, and function, Cambridge University Press, Cambridge. Simmen B, Hladik CM (1998) Sweet and bitter taste discrimination in primates: scaling effects across species. Folia Primatol 69:129–138. Smith DV (1971) Taste intensity as a function of areas and concentration: differentiation between compounds. J Exp Psychol 87:163–171. Smith TD, Alport LJ, Burrows AM et al. (2007) Perinatal size and maturation of the olfactory and vomeronasal neuroepithelia in lorisoids and lemuroids. Am J Primatol 69:74–85. Starck JM, Ricklefs RE (1998) Patterns of development: the altricial–precocial spectrum. In: Starck JM, Ricklefs RE (eds.) Avian growth and development. Evolution Within the Altricial– Precocial Spectrum, Oxford University Press, New York. Steiner JE, Glaser D, Hawilo ME et al. (2001) Comparative expression of hedonic impact: affective reactions to taste by human infants and other primates, Neurosci Biobehav Rev 25:52–74. Tepper B (1998) 6-n-Propylthiouracil: a genetic marker for taste with implications for food preference and dietary habits. Am J Hum Genet 63:1271–1276. Tepper BJ (1999) Does genetic taste sensitivity to PROP influence food preferences and body weight? Appetite 32:422. Tepper BJ, Nurse RJ (1997) Fat perception is related to PROP taster status. Physiol Behav 61:949–954. Tepper BJ, Nurse RJ (1998) PROP taster status is related to fat perception and preference. Ann N Y Acad Sci 855:802–804. Yakinous CA, Guinard J-X (2001) Relation between PROP taster status and fat perception, touch, and olfaction. Physiol Behav 72:427–437. Yakinous CA, Guinard J-X (2002) Relation between PROP (6-n-propythiouracil) taster status, taste anatomy, and dietary intake measure for young men and women. Appetite 38:201–209.

Chapter 14

Adaptive Profile Versus Adaptive Specialization: Fossils and Gummivory in Early Primate Evolution Alfred L. Rosenberger

Abstract  Gummivory, a rare dietary habit among modern primates, has figured prominently in interpretations of the earliest primates (plesiadapiforms) largely on the basis of a morphological analogy with sugar gliders, and it has also been proposed as a key adaptation pertaining to early strepsirrhines (Adapis, Leptadapis) and the origins of the toothcomb, partly by analogy with marmosets. In reexamining these hypotheses, it is important to consider the following: distinguish gum-gouging from gum-gleaning; assess adaptive compromise and preadaptation; examine system-wide linkages between gum harvesting and collateral behaviors relating to diet; reevaluate the morphological correspondence between purported analogs; empirically evaluate tooth wear, perhaps the most direct morphological signal of gouging behavior. A distinction is drawn between facultative gummivory as part of a species’ Adaptive Profile and obligate gummivory as an Adaptive Specialization, and the testability of both notions. Using marmosets as the most stringent morphological and behavioral model of an obligate modern primate gummivore – exhibiting a distinctive functional suite of features and evidence of heavy upper and lower anterior tooth wear – none of the test cases present cogent examples of gum-gouging adaptation. The sugar glider Petaurus breviceps also differs from marmosets in tooth morphology and wear; they appear to be gum-gleaners. The derived “gracilization” of upper incisors in all strepsirrhines living and extinct, possibly indicative of an obligatorily folivorous ancestry, may have been ­preadaptive to a shift from harvesting to socio-sexual biological roles in anterior tooth use, presaging the toothcomb’s evolution as a

A.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 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_14, © Springer Science+Business Media, LLC 2010

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grooming adaptation. The procumbent, often styliform, large lower incisors of many plesiadapiforms may have served as precision probes and pincers for these primitive face-feeding primates that likely lacked the advanced hand–eye coordination of euprimates. Working with the uppers in beak-like fashion, they would probably have been well suited to harvesting and ingesting small seeds, a prelude to the full-blown coevolutionary relationship established between euprimates and angiosperms as the latter evolved a diverse array of larger and more fleshy fruits. Then non-tarsiiform primates, with more discriminating eyes, touch-sensitive prehensile hands, mobile athletic bodies, and more versatile front teeth, could reinvent themselves as a unique mammalian guild of obligate arboreal frugivores and folivores.

Introduction The purpose of this chapter is to address the idea that the fossil record may provide evidence of gum-eating among early primates. Although I am enthusiastic about the prospects, my contention is that primate paleobiology may not yet be ready to tackle this question decisively: fossils are rare, fragmentary, and scattered while the groups in question are abundant taxonomically, and our methods for inferring dietary adaptation may not be sharp enough. This is a very real problem with regard to gummivory, or exudativory, a feeding strategy that came into the mainstream during the 1970s when field workers reported this behavior among various strepsirrhines and platyrrhines (e.g., Petter et al. 1971; Martin 1972; Kinzey et al. 1975; Charles-Dominique 1977). Morphologists have ever since been trying to catch up – an entrée to this rich literature may be gleaned from other chapters in this volume – for teasing out gummivorous adaptations at the macro level has proven difficult. The irony here is that there appears to be no published study that has taken the most direct route toward resolving the question, by looking for a signature wear pattern on the anterior teeth that reflects one of the hardest exogenous materials that gummivorous primates are likely to encounter in their everyday arboreal lives – wood. Recent functional morphological studies of living primates illustrate the difficulty of demonstrating gummivorous adaptations. In a primate-wide assessment, for example, Vinyard et al. (2003) argued that 13 of the anatomical features in the skull predicted to be correlates of gummivory failed the test of commonality. In a narrower study that compared two species of the galago Otolemur, one a frugivore and the other a gummivore, Burrows and Smith (2005) were perplexed by overlapping similarities and differences that either met or conflicted with expectations. They raised questions about analytical methods and assumptions and also emphasized likely differences in the harvesting methods behind gummivory, i.e., gum-gouging and gum-scraping with the toothcomb (see also Eaglen 1986). Thus the notion of a unitary form of primate gummivory has been called into question, just as the

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c­ oncept of “frugivory” is too broad to explain the varied ways primates have adapted to harvesting fruits and masticating their contents (e.g., Rosenberger 1992). For paleobiology, where tests to illuminate how things work are often difficult, it is understood that inferring what morphology means in terms of selection and adaptation is problematic (see Ross et al. 2001). However, this situation is not much different from the analysis of living species. Primatologists have collected a large body of data on the dietary habits of wild primates and on craniodental morphology, but we have perhaps not sufficiently considered the limits of our resolving power when it comes to recognizing adaptation. For some of the most interesting species and food types, questions loom large. For example, in a classic study Kay (1975) showed that frugivores and folivores were neatly distinguishable by molar form. But insectivores were not distinguishable from folivores without factoring in body mass (see Kay 1984), soft- and hard-fruit eaters were not separable, and gummivores were unresolved. Using a similar methodology but focusing only on platyrrhines, where better phylogenetic control would be expected to be more revealing, Anthony and Kay (1993) again found good discrimination of folivores by molar shearing proportions and relative incisor size, but little or no definition of insect eaters, sclerocarpic frugivores, or gummivores. In a more targeted investigation, Kay et al. (2001) found that molar shearing metrics did not distinguish seed, fruit, and gum-eating platyrrhines. To wit, we know quite well how to pull out the leaf-eaters but what about the rest – and the gum-eaters, specifically? While the aforementioned studies filled many gaps in our knowledge, if their overall results regarding the predictive power of morphology turn out to be correct it dampens hope of probing the fossil record in an effort to determine the importance of exudativory in the remote evolutionary history of primates (Fig.  14.1), which pointedly impacts my core questions: Were the enigmatic plesiadapiforms gum-eaters? Was gummivory a major factor in the origins of toothcombed strepsirrhines and the toothcomb itself, one of the primates’ more remarkable anatomical features?

Objectives, Principles, and Methods Given these complexities, in this paper I take a different approach. (1) I present a model of adaptational analysis, based on the narrow problem of gummivory but extensible to other matters, that avoids the pitfall of associating form with a dietary category or a food type which in and of itself cannot be considered a selective force. (2) I propose that we revise, or dial back, our “search image” concerning dietary adaptation on the basis of the understanding that morphological patterns are often compromises enabling a variety of biological roles, meaning the actions or uses of a feature by the organism during the course of its life history (Bock and von Wahlert, 1965:278). But specifying which role(s) may have evolved as an evolutionary adaptation via natural selection may not always be possible. (3) I limit the question to one that is conveniently testable.

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Fig. 14.1  Models of early primate groups proposed to be gummivorous. Top: A partial mandible of the plesiadapiform Plesiolestes problematicus, with a moderately enlarged lower central incisor (slightly damaged at the tip). This may be generally primitive plesiadapiform morphology. Bottom: Lateral (left) and occlusal views (right) of the strepsirrhine Adapis parisiensis (from Gingerich and Martin 1981). The low-crowned canines are functionally integrated with the transversely wide, spatulate incisors. Upper incisors are similarly low-crowned and wide but also thin buccolingually

1. While the concept that morphology and natural selection are sensitive to the physical properties of foods is widely accepted and clearly influenced the ­morphologists mentioned above, the notion is applied in various ways, with potentially different implications for inferring dietary adaptation and modeling the evolutionary processes behind it. For example, Kay (1975) and Rosenberger and Kinzey (1976) each argued that molars were adapting to the physical properties of foods. However, Kay related this principle to selection deriving from the most commonly eaten foods whereas Rosenberger and Kinzey proposed that novel items comprising fractionally small proportions of a diet could have a more powerful selective impact – the “critical function” hypothesis. These authors may thus reach diametrically opposed dietary inferences from morphology as well as behavior. Needless to say, we have little empirical information about how feeding or dental form relate to fitness in primates, so both propositions remain difficult to test; both, in fact, may have high explanatory value in different situations. Another difficulty relates to the assumption of universality in adaptive outcomes without considering preadaptation. Whether a food item is commonly or rarely

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eaten, the adaptive differences between species may reflect not a food’s physical properties per se but the methods animals use to access or process it (e.g., Anthony and Kay 1993; Burrows and Smith 2005), which may be a function of heritage. Case in point: an unreinforced, horizontal toothcomb (see below) may not be an effective gum-gouge in Otolemur, but its high-crowned, vertically posted, pointed P2 may potentially represent an alternative harvesting tool used in its own way, recruited by selection because the anterior teeth are biomechanically unavailable. Here, factors relating to both heritage and habitus may distinguish Otolemur gum harvesting techniques from the approaches used by the marmosets, Callithrix and Cebuella, for example. In another sense, gummivory that relies on gum-gleaning, i.e., collecting congealed exudates, may not present the biomechanical challenges envisioned by Rosenberger and Kinzey (1976) as driving adaptation, in contrast with gum-gouging, but there is evidence that gleaning is ecologically sustainable and potentially of selective value in less modified callitrichines. However, if there are no evident antemolar or postcanine dental adaptations underlying gummivory, gum-gleaning may remain invisible to functional dental morphology. Indeed, working backwards in a way, looking at callitrichines from the perspective of the most derived, gum-gouging marmosets, it may seem difficult for the morphologist to acknowledge that gummivory is important in the lives of tamarins. Consequently, in the realm of paleobiology most would probably agree that there is a higher likelihood of identifying gum-gouging than gum-gleaning adaptations. 2. I suggest we modify our search image for dietary adaptation by making a distinction between “adaptive profile” and “adaptive specialization,” as further explained below (see Fig.  14.2). This acknowledges several interrelated points already implied or mentioned above: the great variety of foods primate species tend to eat, often without leaving an anatomical trace; that morphologies often involve compromises reflecting a varied diet; that taxa may or may not present in such a way as to allow a clear recognition of a primary overriding dietary-selectional influence. The concepts of adaptive profile and adaptive specialization are compatible working hypotheses, to some extent reflecting a continuum, but each one focuses on different facets of evolutionary adaptation and stresses different protocols for stipulating hypotheses. 3. My final strategy is to construct the central question of this paper to make it more manageable and more robust in terms of testability. Thus taxonomically I restrict the discussion to plesiadapiforms, adapiforms and, by extension, to the toothcombed morphotype of lemuriforms. The latter is relevant because it serves as evidence for the beginnings of the strepsirrhine toothcomb, which some have interpreted as a gummivorous adaptation originally. Concerning adapiforms, a varied group, the taxa of interest are Adapis and Leptadapis. Both have been discussed as having gum-eating adaptations. Regarding the plesiadapiforms, I caution that this analysis adopts the conceit that these fossils are morphologically uniform and taxonomically coherent when they are not actually. The plesiadapiforms are currently classified in as many as 12 families and they may not be monophyletic (e.g., Silcox et al. 2007). They are highly diverse anatomically

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Fig.  14.2  Top: A modified model of the form–function/biological role concept of adaptation (modified from Bock and von Wahlert 1965) applied to feeding. “Function” refers not to action, but to the biomechanical potential arising from the shape, arrangement, materials, etc., of an anatomical part or feature. Via selection, adaptation aligns these attributes with the biomechanical characteristics of the food source. “Target objects” are the non-trivial materials encountered in harvesting, such as wood-bark, or in masticating materials such as chitin or cellulose, that are likely sources of the selective pressures that determine form and function. Bottom: A generalized model of the analytical steps involved in assessing (lower) incisor adaptations by finding the potential correlations between specific functional properties of tooth morphology and the foods being accessed. “Biological roles” in this usage, broader than Bock and von Wahlert’s for ease of elaboration, specifies the couplings of behaviors and food types. These lists can be extended. The sum combination of biological roles observed or inferred is the adaptive profile of a species. Analyses that narrow the potential range of realized biological roles by excluding some or emphasizing others (arrows 1–3) lead to the inference that a species has an adaptive specialization

and adaptively, and they vary in what must be the cornerstone of any gum-eating primate, the incisors. Thus the question itself – were plesiadapiforms gummivores? – is also too general, but it is a useful starting point. Many present puzzling enlarged lower incisors regarded by some scholars as a gummivorous adaptation. In a separate vein, some workers do not consider plesiadapiforms primates at all – I do – even though they are perhaps the only known mammals in the running for being the euprimates’ (strepsirrhines and haplorhines) closest relatives. Either way, their historical role in the study of early primates is now fixed, and they hold great value for addressing the ecological and adaptive nature of arboreality in primate origins. Methodologically, I also narrow the question by focusing on the most falsifiable working hypothesis. Rather than attempting to generalize gum-eating diagnostics comparatively (e.g., Vinyard et al. 2003; Burrows and Smith 2005), I use a simplified model. My comparisons are with the most ­specialized

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primate gum-eaters, the gum-gouging marmosets Cebuella and Callithrix, and I use this as a frame-of-reference comparative test. Gum-gouging is my focus, not the more elusive question of gum-gleaning.

Adaptational Analysis: Gummivory – Adaptive Profile Versus Adaptive Specialization Semantic and theoretical difficulties are encountered when attempting to test the hypothesis that gummivory was important in the early evolution of primates. We now recognize that two types of gum-accession behavior are demonstrated by the living species (e.g., Vinyard et al. 2003; Burrows and Smith 2005), gum-gleaning and gum-gouging, but earlier discussions of the fossil record are not specific about harvesting method. As indicated above, there is also a question as to the likelihood of being able to infer a gum-gleaning adaptation in the fossils without the ancillary information that is available to field researchers where biological roles are more apparent and ecological context can be established – critical functions may be absent without the mechanical challenges of gouging. Gum-gleaning may be a facultative (optional) biological role and adaptation, as opposed to an obligate (necessary or constrained) biological role and adaptation. Facultative roles arise from morphology but are not necessarily the primary or limiting focus of natural selection. As they may not leave an obvious physical footprint but are instead part(s) of an organized pattern of functional aptitudes, facultative biological roles will often equate with the dietary profile of a species, not with its basic adaptive specialization. The broad-spectrum Ateles diet, for example, is its adaptive profile, made possible by selection but without leaving any detailed anatomical pointers. Are there specific dento-gnathic correlates to the following items that Ateles eats (DiFiore and Campbell 2007): leaves, prey, flowers, and a miscellany that may include seeds, seed pod exudates, bark, fungi, aquatic plants, termitaria soil, and ground soil? Probably not, but the dentition provides a signal of soft-fruit specialization: relatively small molars and low crown relief, suggesting a limited need for precise mastication; moderately large incisors, suggesting important harvesting biological roles that do not require high-pressure force applications; and, reduced lower jaws overall, suggesting a lack of emphasis on force production. But the high confidence in the soft-fruit hypothesis comes from the postcranium as well, which contributes collateral benefits to the feeding system’s adaptive complex, the capacity to roam efficiently in search of such fruits (see Rosenberger et al. 2008). Being able to recognize these collateral adaptations (the assumption here is that obligatory diets involve adaptations outside the digestive system: think aye-aye) increases the likelihood that soft-fruit feeding is an obligate biological role, an adaptive specialization under the intense focus of selection. A similar set of collateral adaptations may help us define the intensity of gummivory in living and fossil species.

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It follows that discerning an obligate adaptive specialization becomes a hypothesis that is more easily falsifiable, while identifying a facultative behavior involves a less cogent argument and more difficult tests. On the other hand, this distinction offers an interesting compromise between two different schools of thought. As noted above, Kay (1975) proposed that the majority of the average annual intake characterizes a species’ diet and the physical properties so encountered select for its form. Rosenberger and Kinzey (1976) (see also Rosenberger (1992)) suggested that even relatively small fractions of a diet, the physically most challenging ones, select for form. Obviously, the latter may be encountered every day or at certain times of the year, often as a so-called fallback food (see Constantino and Wright 2009). These concepts may now be reformulated as part of an adaptive model, not as an either-or proposition but as a synthesis between the two. The average annual intake, when shown to correspond with the form–function complex, may be viewed as the set of biological roles interacting with selection to produce a species’ adaptive profile. The critical functions, on the other hand, are aspects of a narrower set of biological roles that have an overriding influence on selection, and so produce more definitive, recognizable adaptive consequences. Gum-gleaning may exemplify a part of the adaptive profile of a species whose anterior dentition is conditioned as an evolutionary specialization to perform other biological roles as well, including some that may have little to do with feeding. The toothcomb comes to mind. The mechanical difficulties associated with gum-gouging would suggest that it requires a reorganization of form by natural selection at a larger scale and under more intense natural selection. Analytically, the inference of facultative gum-gleaning within the adaptive profile may benefit from the study of analogies. Determining a gum-gouging adaptive specialization requires assessments based on the form–function model. This involves a relatively precise explication of the biomechanical performance potential of the various functions (mechanical properties; Bock and Von Wahlert 1965) made possible by the incisors/canine complex, and a similarly precise description of the physical properties of the target objects encountered in accessing food orally and feeding – together these describe the form–function linkage behind the biological roles. But this is feasible only in the abstract. Obviously, the anterior teeth are capable of a wide range of non-trivial roles made possible by their shapes and other properties (Fig.  14.2). Examples: nipping with precise distributed loading but low occlusal pressure; incising horizontally with high pressure; gouging with minimal abrasion because of reinforced enamel; holding to stabilize large objects; breaching by wedging the incisors into a fruit casing and using tip and shaft of crown to apply force; scraping over a large contact zone by applying a continuous long edge; combing by delicately inserting hairs into the multiple, narrow linear slits between teeth. Similarly, we can hypothetically describe the physical properties or construction of the target object as well, which is necessary to balance the model, e.g., nipping compliant leaves; incising softbodied insects; gouging fibrous bark; holding large fleshy fruit; breaching into dehiscent slits of woody pods; scraping exfoliating bark; combing fine pliant hairs.

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It is against such sets of adaptational hypotheses that we consider the evidence for gum-gouging among marmosets and in the early fossil primates.

The Gum-Gouging Model: Marmoset Behavior and Functional Morphology It is widely acknowledged that among callitrichines, the marmosets Cebuella and Callithrix present a dramatic suite of morphological differences in teeth and jaws relative to the more primitive conditions exhibited by Leontopithecus, Saguinus, and Callimico. On the basis of several early anatomical and behavioral observations (e.g., Kinzey et al. 1975; Coimbra-Filho and Mittermeier 1977; Rosenberger 1978; Gantt 1980; Hershkovitz 1977), it is also generally held that these “marmoset” features probably relate to gummivory, although there is no comprehensive functional analysis that addresses the whole package of traits in a unified manner. Indeed, detailed morphological assessments (e.g., Vinyard et  al. 2003) of individual features also raise questions about several suppositions by finding few parallels between the Cebuella/Callithrix pattern and the morphology of strepsirrhine gum-eaters. Still, these animals – even if we consider their behavior only – present the best available model for gum-gouging among living primates. While a comprehensive analysis of their morphology is beyond the scope of this paper, I present a functional interpretation – a related set of hypotheses for further testing – of some of their most salient features on the basis of integrating morphology and behavior. It is plainly evident in the field that gum-gouging in Cebuella and Callithrix is a vigorous activity involving much more than a simple elevation of the lower jaws (Kinzey et al. 1975; Coimbra-Filho and Mittermeier 1977). The animals will often anchor the skull against the substrate by firmly fixing the upper central incisor(s) in the bark, and they also recruit muscular force from the neck and limbs to assist, producing a rocking motion of the head. As the lower jaws are V-shaped, the head is often turned to the side and rotated in order to engage the lower lateral incisor and canine. In this position, the animals also appear to be working off the I2 to anchor the head on the lateral side of the face. This very general behavioral description appears to coincide with anatomical features that clearly distinguish marmosets from the tamarin Saguinus which, for convenience, is a fair model of the ancestral callitrichine condition, one that is not specialized for gum-gouging. The essentials are summarized in Fig. 14.3. I hypothesize that the underlying morphology and biomechanics of the pattern are organized to optimize or maximize several functions: (1) orientation and application of relatively high pressure at the apical margins of crowns; (2) resistance to tooth attrition; (3) minimizing bending at the alveoli from the reaction forces incurred during gouging; (4) allowing for a large gape; (5) stabilizing the head to maximize torque; (6) arranging an efficient use of chewing muscles; and (7) recruiting extra-masticatory muscle leverage in these small-bodied primates.

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Fig. 14.3  Schematic summary of leading anatomical, functional, and biological role differences between gum-gouging marmosets (Callithrix) and gum-gleaning tamarins (Saguinus). Not all of the features are independent of one another. The gum-gouging pattern complex and its underlying individual features are all derived among callitrichines

The V-shaped mandible and staggered arrangement of the anterior teeth isolate the lower central incisors of marmosets at the very front of the face while spatially shifting the adjacent crowns closer to the midline than the U-shaped anterior jaw of Saguinus, where the incisors are transversely arrayed. Having midline or nearmidline “bite points” for the full array of teeth involved in gouging may be advantageous in exerting and balancing the forces generated by chewing muscles on either side of the head. This is because the adductors have more nearly equal moment arms than would be the case if, say, the point(s) of force application would be more lateral to the midline, or outside the body of the mandible at the tip of the everted lower canine of Saguinus, for example. Positioning these teeth close to the midline may also minimize eccentric, bending loads incurred by the mandible while gouging. The staggered arrangement of lower incisors and canine also maintains separations between the points or surfaces along the apical margins of the incisor and canine crowns where each tooth applies force. The effect of this is that each tooth apex serves to concentrate loads at a localized point, reducing the surface area of force application and maximizing applied pressure. At the same time, reaction forces incurred by bodies of the individual adjacent crowns could be distributed along the surfaces of interstitial contact at the stylar cusps marmosets tend to have at the widest span of their lower incisors, below the inverted V-shaped apical margins.

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The integration of lower incisors, which are derivedly tall, with the canine, which is nearly homomorphic, vertical in orientation, and equally tall, produces a serrate row of edges on the lateral aspect of the face. This is unlike the continuous, arcuate, frontally arranged incisal edge formed by I1,2 of Saguinus, where the markedly heteromorphic lower canine is posted away from the incisal block. Thus Callithrix and Cebuella are able to engage their front teeth as a unit of separated elements, which also includes the canine. Each individual tooth is mechanically advantaged by position and shape to affect high pressure loads. Saguinus, in contrast, would use the continuous strip of flat incisors as a singleelement unit, theoretically affecting less pressure overall, while the canine, given its contrasting shape, alignment, and offset position, remains functionally dissociated from the incisors. This pattern helps explain why marmoset jaws are narrow anteriorly and head-turning is an important behavioral element of gumgouging. Incisor–canine integration also clarifies the benefits gained by reorienting the lower canine crown into a vertical plane. A laterally splayed, Saguinus-like lower canine would eccentrically load the alveolus and jaw if force were applied to its tip. Reduction or loss of lingual enamel and thickening of buccal enamel (Rosenberger 1978; Gantt 1980) probably strengthen the crowns against damage and reduce the rate of crown attrition, lengthening the tooth’s functional lifetime. In spite of this, anterior tooth wear is a significant factor among marmosets. Figure 14.4 plots the height of central incisor crowns in a sample of Cebuella pygmaea selected to represent the full range of tooth wear on the basis of observations of I1 morphology. Surprisingly, tooth substance is steadily lost from the I1. Its crown height decreases by nearly two-third its maximum dimension in the most severely worn cases in this sample. In contrast, the lower central incisors of the same individuals present a more erratic spectrum of crown height, while tending to vary within a narrower band of 2–3 mm. Overall, a decrement of no more than one-third appears to be the pattern for the lowers. Additional work is necessary to explain the uneven rates of wear in uppers and lowers. However, it is clear from inspection that lower crowns are very heavily damaged as well; in advanced wear they are basically root stubs. These data clearly underscore the role of the upper incisors in anchoring the skull during gouging. This indicates that force is applied between the upper and lower jaws as in biting, as opposed to chiseling with the lowers. The application of loads on opposite ends of a structure imparts torque, a twisting action with a force that is proportional to the distance between the points of application (actually in proportion to the radii measured between the points of application and the center of rotation of the object). Thus the amount of torque the animals can apply is a direct function of jaw gape, which is enhanced in marmosets by a low temporomandibular joint relative to the length of the toothrow (see Vinyard et al. 2003; Lucas 1981) and by the proportions of the anterior basicranium plus palate (Forsythe and Ford 2008). Torque is also probably magnified by the marmosets recruiting muscular force from the limb skeleton. Their heads rock vigorously, their forelimbs tense up, and their shoulders seem to shimmy while they gouge.

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Fig. 14.4  Measurements of central incisor crown height in samples of wild-shot pygmy marmosets and sugar gliders. C. pygmaea individuals were selected to represent natural wear stages but the P. breviceps population was selected at random, and all individuals were found to be essentially lacking crown wear. The data are sorted according to crown heights of the upper incisors (triangles). Note the large disparity in heights of uppers and lowers in P. breviceps. Individual P. breviceps outliers reflect technical difficulties in measuring crown height of lowers because of variation in the shape of the enamel line. The gum-gouging marmosets are more prone to wearing excessively the upper and lower crowns. The relatively erratic distribution of lower heights in C. pygmaea attests to the damaging work involved in gnawing at bark, in spite of numerous morphological adaptations. The more uniform decline in height of the uppers relates to their role as a stabilizer of the head and jaws

Testing Hypotheses Plesiadapiforms and the Sugar Glider Analogy Several prominent assessments of plesiadapiform fossils, many of which exhibit an impressively enlarged lower central incisor (Fig. 14.5), have suggested that gumeating was an important adaptation for this group. That and the presence of clawed digits in a small-body size package are the set similarities that have attracted the attention of primatologists (see Rassmussen and Sussman 2007 for a review). Szalay and Delson (1979), for example, suggested that several forms belonging to the very small-bodied picrodontids and micromomyids ate an energy rich diet that included gums. Beard (1990), citing a dentition convergent on sugar gliders as well as his controversial interpretation that paromomyids also resembled Petaurus in sporting a patagium, maintained that these animals were gum-eating gliders related to colugos rather than primates. Boyer and Bloch (2008), while strongly refuting Beard’s locomotor and phylogenetic hypotheses of a plesiadapiform–dermopteran

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Fig. 14.5  Examples of the diversity of incisor morphology among plesiadapiforms, in occlusal and lateral views (modified from Rose and Bown 1996). Inset: Dryomoys szalayi (modified from Boyer and Bloch 2007), a micromomyid plesiadapiform, a group identified by some as being exudates-feeding specialists

link, stressed additional postcranial resemblances of micromomyids and paromomyids with callitrichines, which meant to them that the gum-eating complex of these plesiadapiforms was supported collaterally by the skeleton. These ideas drew on Gingerich (1974), Cartmill (1974), and Kay and Hylander (1978), who first popularized the favorable anatomical comparisons of plesiadapiforms with phalangeroid marsupials, which also have an enlarged lower incisor and an enlarged posterior premolar that resembles that of various plesiadapiforms. The diet of the sugar glider Petaurus breviceps (e.g., Fleay 1947; Smith 1982), which species relies on gums and insects, thus became a focal point of the argument, which was essentially one of analogy. Information on P. breviceps feeding behavior is somewhat ambiguous, but it suggests a less dramatic form of gummivory than is the case with marmosets. There are reports that they damage bark with the incisors (e.g., Fleay 1947). However, Smith’s (1982) detailed account resembles the description of the feeding resources and gum-feeding strategies of Perodicticus potto and Euoticus elegantulus given by Charles-Dominique (1977:148, closely paraphrased): Gums form principally… at the site of old wounds and holes made by the mouth parts of homopterans. E. elegantulus spend most of their time visiting trees which are gum producers. They follow veritable “rounds” which permits them to collect, with the aid of the tooth-scraper, tiny droplets of gum formed after their last visit. Each animal must visit a very large number of production sites (about 300) in order to collect sufficient quantities of gums.

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Smith’s description suggests sugar gliders rely on gum-gleaning. Focusing principally on two tree species, he says that the sugar gliders nightly invest a great deal in traveling to visit a large number of feeding sites where they evidently harvest relatively little over a brief period of time. Again, closely paraphrasing: A small proportion of foraging time (2.6%) was devoted to stripping bark from eucalypts (p. 159). Gliders tend to chew holes more in the winter when feeding on eucalypt (p. 155). “The four principal eucalypts in the study area had loose decorticating bark” (p. 158). Unusually only 10 s (but a maximum of 5 min) was spent licking at (solidified) Acacia gum sites, and over 100 sites… may be visited in one night (pp. 153, 159). The Acacia sites are holes originally made by borer insects where gum has accumulated, though Petaurus will prise the holes open (p. 153).

Morphological evidence appears consistent with the notion of sugar gliders as gum-gleaners. The upper incisors of Petaurus lack obvious specializations of the crown and are quite simple in shape. Proportionately, I1 is large relative to body size, which Kay and Hylander (1978) implicitly considered an adaptation to gnawing gummivory. However, my preliminary assessment of crown usage based on museum specimens does not easily align with this notion (Fig. 14.4). In a homogenous sample of 16 individuals of P. breviceps ariel, the subspecies described as a gum-eater by Fleay (1947), I identified only two with more than modest wear surfaces at the apical margin that exposed dentin on I1. None of the other individuals presented more than a pinpoint of dentin exposed at the delicate tip of I1. This is a surprising finding and requires further investigation, but measurements of these teeth also indicate negligible crown wear. The variation in crown height in the sample is attributable to size differences between individuals as well as difficulties in measurement technique, which partly pertains to irregularities in the position of the cementoenamel junction. As this pattern is strikingly different from the heavily worn upper and lower central incisors of marmosets, it is difficult to see how Petaurus could physically gouge into tree bark the way marmosets do. In surveying the plesiadapiform incisors in museum collections, I have also been struck by finding few specimens in which either uppers or lowers are seriously worn. This assessment is surely an oversimplification, and influenced by taphonomic bias and the limitations of my informal sampling methods. However, once again by analogy with marmosets, it is hard to reconcile with gum-gouging behavior. The morphology of the incisor set of plesiadapiforms and Petaurus does not compare well with that of marmosets in a range of functionally important features. The resemblances are of a unitary rather that a patterned nature, involving little more than high-crowned, robust upper centrals. But in other ways, Petaurus and the fossils profoundly differ from gum-gouging marmosets. For example, neither plesiadapiforms nor Petaurus incisors appear to have, or have been reported elsewhere to have, specialized enamel reinforcement. Their lowers have disproportionately tall crowns – not simply tall, i.e., canine-comparable, as in marmosets – and they tend to have a continuously tapered crown shaft that ends in a pointed tip (Caveat: there is interesting variability here among plesiadapiforms; some crowns are flat and chisel-like, some are also more scoop-like; see Gingerich 1976; Rose and Bown 1996; Fig. 14.5). The crowns are very tall relative to mandible length and

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they are very tall relative to the crown height of the reciprocal I1. And, rather than being vertical, the lowers curve gently upward from a horizontally disposed root and alveolus, although in some fossils the shaft remains quite horizontal. These last points deserve elaboration. In the more horizontal orientations, the anchor-and-torque technique used by marmosets may not be effective. For a plesiadapiform, when lowers are shelf-like, as the animal applies force at the tip and along the long axis of the lower incisor crown, which is the manner least likely to cause damage to the system, and eccentrically loads the alveolus, the jaw motion involved would have a strong protraction or propalinal component rather than being a simple upward, orthal lift about the temporomandibular joint. This might not be effective in gouging unless, among other modifications to the musculoskeletal organization, there are temporomandibular specializations to enable the jaw to thrust forward and retract without damage to the joint. If, on the other hand, the animal applies force at the tip normal to the long axis of a relatively horizontal incisor, which would approximate the loading pattern when applying torque by working against the uppers, loads on the I1 alveolus would be substantial and they would impose serious bending moments on the bone, which would have to be reinforced. In view of such contrasts with marmosets (Table 14.1), before attaching more importance to the morphological analogy of plesiadapiforms and sugar gliders behavioral studies of gum harvesting are essential. I emphasize that my assessment of tooth wear in the gliders, which tends to question a gum-gouging habit, should be regarded as provisional as it is confined to one population of museum specimens whose prior circumstances in the wild are not known. Nor have I sampled other species of Petaurus, which include larger animals that would be more muscular and may have incisors better designed to handle wear by virtue of tissue thickness and organization, if nothing else. However, my analysis does cast doubt on the capacity of the lower incisors of Petaurus, and by extension plesiadapiforms, to withstand and endure the loads expected of a vigorous gouging habit. This does not eliminate the possibility that gum-gleaning is part of the fossils’ adaptive profile, however.

Strepsirrhines: Toothcombs and Their Origins Martin (1972) was perhaps first to advance forcefully the idea that the strepsirrhine toothcomb was significant in exudate acquisition, calling the lower anterior teeth a “tooth-scraper.” He proposed that a dietary transition was involved in the transformation of a pre- or non-toothcomb morphology in early forms to a bona fide toothcomb in the last common ancestor of lemuriforms (lemuroids, lorisoids, indrioids, etc.). Martin stated (p. 329), “There is no doubt that the tooth-scraper is used by many (if not all) lemurs and lorises for grooming; but this is probably a secondary function.” Later, he (Martin 1990) concluded that both grooming and feeding were important to modern strepsirrhines since their ancestry, without coming down on one side or the other as an explanation for the origins of the complex. Alternative views strongly favoring the grooming hypothesis and attempting to falsify the

The “p” notation in the parenthesis indicates that the characteristic is likely to be primitive in the group indicated. Negatives in the lemuriform morphotype relate to the pervasive form–function contrast of the toothcomb, as discussed in the text. As further explanation: (1) The claw-clinging behavior of plesiadapiforms is probably primitive and, while preadaptive to it and potentially maintained by stabilizing selection, it would not have been directly part of a derived gum-gouging syndrome. (2) Low mandibular condyles are probably primitive in plesiadapiforms and euprimates. (3) Given the variability of incisors among plesiadapiforms, one cannot rule out the possibility that some forms were so modified. Essentially all strepsirrhines save for a few moderns (e.g., Phaner, Daubentonia) have flimsy, low-crowned upper incisors, the opposite of expectations based on the GG model. (4) The diastema-isolated anterior teeth of some plesiadapiforms may conform; a V-shaped jaw is likely primitive. The Adapis–Leptadapis lower canines do not conform morphologically, but they are realigned from the primitive, projecting pattern. (5) See (4) re-plesiadapiforms. (6) See (4) re-plesiadapiforms, but conical crowns are likely primitive among plesiadapiforms. (7) Presence of accessory cuspules on upper central incisors of some plesiadapiforms may conform. The close-packed incisor–canine complex of adapiforms may conform to this function. (8) Canines are low-crowned or lost in plesiadapiforms. See (4) regarding adapiforms. (9) Robust, tall crowns in plesiadapiforms may conform. (10) See (9) for plesiadapiforms.

Table 14.1  A comparison of gum-gouging features of marmosets with plesiadapiforms, the early strepsirrhines Adapis and Leptadapis, and the toothcomb morphology of the ancestral lemuriform morphotype Adapis– Lemuriform Marmosets (Callithrix, Cebuella) Plesiadaps Leptadapis Morphotype 1 Enhance leverage via positional behaviors Yes (p) No No 2 Enhance torque by maximizing gape via lowered condyle Yes (p) ? ? 3 Enhance torque by modifying form–function of upper incisors No No No 4 Orient applied forces by modifying jaw shape and realigning lower canines and Yes (p) No No incisors 5 Enhance mechanical advantages by altering jaw shape and tooth position Yes (p) No No 6 Enhance pressure applied by individual teeth by spacing Yes No No and shape modifications 7 Minimize eccentric alveolar loading by reorienting canine teeth ? Yes No 8 Minimize tooth wear and breakage by enamel deposition, crown height, and Yes? No No cross section

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dietary hypothesis have been presented by Szalay and Seligsohn (1977), Rosenberger and Strasser (1985), and Eaglen (1986). They emphasized the fragility of these lower teeth as gum-gouging structures, stressing the structural–functional similitude and behavioral analogy with human combs, e.g., compact narrow interstitial spacing; extraordinarily slender, high-crowned tines; recruiting the canines as end members to increase the number of operational slots from three to five. Rosenberger and Strasser (1985) suggested that the proximity of the body of the toothcomb to the vomeronasal organ could signify a dramatic shift in incisal–canine function in strepsirrhines as these teeth became annexed to the intense oral–olfactory communication system of lemuriforms, transforming them into an instrument designed to help collect scent and distribute pheromones by licking and parting the fur. Gingerich (1975) presented a paleontological perspective on toothcomb origins on the basis of an intriguing anatomical pattern shared by lemuriforms and the Eocene fossils Adapis and Leptadapis. They are the only non-lemuriform strepsirrhines in which the lower canine is integrated into the morpho-functional field of the incisors, vaguely like a modern toothcomb (Fig. 14.1). Gingerich and Martin (1981) pressed this idea further by proposing that the Adapis–Leptadapis morphology resembled the “short-tusked” condition of marmosets. They argued that it was possible that these early strepsirrhines, which Gingerich and Martin regarded as folivores, may have employed gums seasonally, when leafy stuff was insufficient, as a preadaptation to evolving the tooth-scraping, toothcomb configuration. It is difficult to falsify the notion of the toothcomb’s original adaptation as a facultative gleaning instrument for there may not be any unique biomechanical requirements associated with collecting semi-solid goop that is freely available, or if the activity requires a minimal amount of pressure applied using a scraping action. Comparative evidence based on the derived feeding specializations of toothcombs in living strepsirrhines, however, suggests that the default ancestral pattern, which by definition lacked adjunct specializations, was not selected for gumgouging. For example, Propithecus is a folivore that relies heavily on bark and/or dead wood during the lean season. Richard (1978:527–528), who reports that almost 15% feeding time can be spent on bark, describes how: “Animals gouged out the thin bark, soft moist wood with their ‘toothcombs, leaving scars on the trunk up to 1  cm deep and 4  cm long…each group would cluster around one of two stumps in their range… and spend half an hour to an hour tearing off splinters of woods with their toothcombs and premolars. This wood was very dry, very hard and dense, and did not appear to contain any kind of insect life.” Propithecus has an unusually robust, four-tooth toothcomb. Another example is the gouging adaptations in forms such as Phaner, where the toothcomb is unusually large relative to body size (Martin 1979; Kay and Hylander 1978; Eaglen 1986). Neither of these patterns is expected to resemble the ancestral lemuriform condition. A critical component of the anterior dentition of strepsirrhines, the upper incisors, is brought newly into focus by the marmoset model of gum-gouging discussed here, which emphasizes their role in stabilizing the head to gain mechanical advantage. This extends a previous argument. Rosenberger and Strasser (1985) (see also Rosenberger et al. (1985)) reasoned that the small size and reduced morphology of

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adapiform and lemuriform upper incisor teeth – low crowns, buccolingually thin with a mesiodistally wide, pronged I1 – are unusual in primates and that they evolved before the toothcomb arose, as they appear to be universal when known in adapiforms. Eaglen (1986) presented confirmation morphometrically, showing that the uppers of modern strepsirrhines are the smallest of all living primates. He also suggested that their reduction served to minimize potential damage by occlusion with the fragile toothcomb. Recent discoveries of North American adapiforms fossils corroborate this notion by showing that the lowers are often similarly delicate (Fig. 14.6). Thus the entire incisal battery of the early strepsirrhines, as far as they are known, does not appear to be suited for gum-gouging. Unlike marmosets, they are not enlarged, reinforced by specialized enamel deposition, arranged in a manner to exert high apical pressure, or organized to deliver torque by uppers biting against the lowers (Table 14.1). This view conflicts with the proposition that Eocene adapiforms presage an ancestral tooth-scraping adaptation because they include animals like Adapis and Leptadapis which are thought to resemble the marmosets in having “short-tusked” lower canines (Gingerich and Martin 1981). In fact, marmosets have high-crowned lower incisors not low-crowned canines, so the analogy is in error. The fossils also have distinctly broadened lower incisors arranged tamarin-like, in a continuous row, contrasting the apically tapering (when unworn), point-pressure design of the marmosets. Additionally, the relatively large body sizes of the Adapis and

Fig. 14.6  Examples of North American adapiforms anterior dentitions in lateral view. Modified from Rose et  al. (1999). Clockwise from top left: Cantius abditus, C. nunienus, Notharactus rostratus, N. tenebrosus (male), N. tenebrosus (female), Smilodectes gracilis

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Leptadapis, roughly 2–10 kg (Martin 1990), markedly contrast with the normally small-bodied platyrrhines gummivores, which weigh in at 100–250 g. Thus these fossils are unlikely to have been gum-gougers, but a tooth-scraping modality cannot be refuted by the gross morphology. Perhaps a better analogy that might be tested compares these adapids with the bark-prising folivore Propithecus, which has stout canines forming the toothcomb’s lateral toothcomb elements. I agree with Gingerich and Martin (1981) in a different respect, that folivory factored into the origins of the toothcomb – but in a different manner, as a preadaptation. A key notion behind the grooming model (Rosenberger and Strasser 1985) is that the lower anterior teeth were redirected from their role in feeding and toward the domain of self-maintenance and sociality. In other words, the incisors were coopted to serve principally socio-sexual biological roles. How could they have been “freed up” to become part of this transition? Logically, selection for incisal harvesting would have had to be relaxed in order for this to occur. Perhaps, the preadaptation which enabled this transformation was dietary, and the ancestors of toothcombed lemuriforms were quite folivorous and had already experienced incisor reduction, which is essentially universal among leaf-eating primates. With dietary selectional forces relaxed, a non-dietary selection regime could have taken hold. The relatively large body sizes of many Eocene adapiforms, and their crested, folivore-like molar teeth, are features consistent with this hypothesis. Another source of corroboration relates to bioenergetics. Snodgrass et al. (2007) have shown that modern strepsirrhines, even small bodied forms that are highly insectivorous, are hypometabolic (20–30% below predicted values). Perhaps this may be a consequence of an ancestry that was specially adapted physiologically to a low quality, leafy diet. The pervasive adaptive inertia of such an ancestral condition may also be seen in the relatively low relative brain size values that persist among strepsirrhines (Martin 1990). Strategically, strepsirrhines may be energy minimizers predicated on a folivory base.

Conclusions While small primates tend to eat almost anything that is cheap and nonpoisonous and within their biomechanical reach, like gums, it is unlikely that the toothcomb evolved as an evolutionary adaptation to collect gums by vigorous incision or gnawing of bark, as with the gum-gouging marmosets. As the first toothcomb evolved, it may have been useful in scraping at freely available gums as part of the facultative adaptive profile of the lemuriform ancestral morphotype, but this is not a hypothesis that can be falsified biomechanically at this time and so it has little standing. There is also no morphological evidence that the antecedent fossil adapiforms were obligate, specialized gum-eaters. On the other hand, the most highly corroborated hypothesis is consistent with the notion that the toothcomb is a toiletry tool by design. The evidence further indicates that folivory, with its attendant de-emphasis on incisal biting, was a widespread condition among adapiforms, sug-

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gesting that a “gracilized” incisal battery likely set the stage as a preadaptation to the evolution of the lemuriform toothcomb. Sociality may thus have played a unique role in shaping the anatomy and function of their anterior teeth, and the origins of the strepsirrhine adaptive zone. Among the first lemuriforms, gum-gleaning biological roles were probably of limited selective value when measured against the snuffling behaviors associated with dental grooming, which were probably critical rituals when it came to keeping clean, keeping social order, and managing to cop a mate – especially if that was allowed only during a brief window of time once a year. The diverse plesiadapiforms, whose anterior teeth were better suited mechanically to gum-gouging if only because they were stout and not so reduced, are more likely to have included some taxa that did employ gum-gouging. However, neither plesiadapiforms nor their popular marsupial analog, the sugar glider P. breviceps, show adaptations to resist crown wear or impart forceful bark-prising loads in the manner of marmosets. Other gum-gouging methods were possible among plesiadapiforms, but this requires further study. Tooth wear studies might provide a welcome method for testing this interpretation. So, if it wasn’t primarily for gum-gouging, to what end were the plesiadapiform incisors adapted biomechanically? It is well to keep in mind that on some level these teeth may appear to require a special explanation because they differ so much from those of most modern primates, and our homocentric anticipations. However, on a gross level they are not so different from modern tree shrews, nor are they so different from early dermopterans, which is consistent with the idea that large, procumbent lower central incisors were widespread, ancestral, and of dietary value among euarchontans sensu lato. There is also another structural analogy for styliform incisors among arborealists that may prove instructive for plesiadapiforms – beaks. Bird beaks of a wide variety of sizes and shapes are well adapted as jabbing instrument often used for scoring and flaking bark to uncover insects or access sap. But fundamentally, they are manipulatory probes and pincers, designed for biological roles like nudging and separating small objects from their material background, like small seeds from their lodges, without the benefit of manual fine-motor control or much handling at all. Plesiadapiform lower incisors – jutting, tapered, sometimes flat-edged but mostly pointy – may have served a similar purpose. Small non-fleshy seeds, which early in angiosperm history were probably their largest edible biomass output and still remain their most densely packed nutritional product, may have been a major, selectively advantageous food source for the first primates. Their value as a staple for mammals is evident by the enormous diversity of small-bodied rodents that feed off them, most without any conspicuous locomotor adaptations for arboreality, in addition to the birds. Clearly, small seeds do not require handling to recover and they do not require high visual acuity to find. But a face-feeding primate not having the benefit of a stabilizing platform of spatulate front teeth would be advantaged with a dentition that efficiently eased access, i.e., precise, probe-like incisors for harvesting, as well as bunodont, non-shearing molars for mastication. The “ultimate” success for a plesiadapiform occupying such a feeding niche may be exemplified by the carpolestids, a family that is also outfitted with highly specialized

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posterior premolars that seem well suited to serve as a small nut-cracker. Perhaps they are one highly derived lineage of an adaptive radiation which has at its base a group of arboreal seed-eaters. Additional work may determine if seed ingestion was part of the plesiadapiform adaptive profile or an adaptive specialization. Either way, a reliance on seeds would predispose the earliest primates to a growing dependence on woody trees, eventually to branch out and take in other angiosperm edibles. More specialized resources such as fruits and leaves and exudates were yet to become established among the non-tarsiiform euprimates, as would the decisive euprimate breakthroughs of superior hand–eye coordination, manual dexterity, and locomotor athleticism, all of which would allow more efficiency in a larger bodied primate enjoying a broader dietary spectrum. Enticing the first primates to continue ingesting seeds by offering them fleshy fruit coverings as the major energy source would have led to the coevolutionary synergy of euprimates and angiosperms from the Eocene onwards. Acknowledgments  Special thanks to Chris Vinyard for sharing his videos of Callithrix jacchus and to Marci Muskin for producing critical illustrations. To Annie Burrows and Siobhan Cooke. I am grateful to the museums that have made collections and facilities available for research, especially the American Museum of Natural History, United States National Museum, Field Museum and Museu Nacional do Rio de Janeiro. I appreciate the financial support from the Professional Staff Congress, CUNY.

References Anthony MRL, Kay RF (1993) Tooth form and diet in Ateline and Alouattine primates: Reflections on the comparative method. Am J Sci 293A:356–382. Beard KC (1990) Gliding behaviour and palaeoecology of the alleged primate family Paromomyidae (Mammalia, Dermoptera). Nature 345:340–341. Bock WJ, von Wahlert G (1965) Adaptation and the form–function complex. Evolution 19: 269–299. Boyer DM, Bloch JI (2007) Evaluating the mitten-gliding hypothesis for Paromomyidae and Micromomyidae (Mammalia, “Plesiadapiformes”) using comparative functional morphology of new Paleogene skeletons. In: Sargis EJ, Dagosto M (eds.) Mammalian evolutionary morphology: A tribute to Frederick S. Szalay. Springer, Dordrecht, the Netherlands. Burrows AM, Smith TD (2005) Three-dimensional analysis of mandibular morphology in Otolemur. Am J Phys Anthropol 127:219–230. Cartmill M (1974) Rethinking primate origins. Science 184(1974):436–443. Charles-Dominique P (1977) Ecology and behaviour of nocturnal primates: prosimians of equatorial west Africa. Columbia University Press, New York. Coimbra-Filho AF, Mittermeier RA (1977) Tree-gouging, exudate-eating and the “short-tusked” condition in Callithrix and Cebuella. In: Kleiman DG (ed.) The biology and conservation of the Callitrichidae. Smithsonian Institution 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. DiFiore A, Campbell CJ (2007) The atelines: Variation in ecology, behavior, and social organization. In: Campbell CJ, Fuentes A, MacKinnon KC, Panger M, Bearder S (eds.) Primates in perspective. Oxford University Press, New York.

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Eaglen RH (1986) Morphometrics of the anterior dentition in strepsirhine primates. Am J Phys Anthropol 71:185–201. Fleay DH (1947) Gliders of the gum trrees. Bread and Cheese Club, Melbourne. Forsythe EC, Ford SM (2008) Craniofacial adaptations to tree-gouging in marmosets: biomechanics and implications for platyrrhine evolution. Am J Phys Antropol Supplement 46:97. Gantt DG (1980) Implications of enamel prism pattern for the origin of the New World monkeys. In: Ciochon RL and Chiarelli AB (eds.) Evolutionary biology of New World Monkeys and continental drift. Plenum Press, New York. Gingerich PD (1974) Function of pointed premolars in Phenacolemur and other mammals. J Dent Res 53:497. Gingerich PD (1975) Dentition of Adapis parisiensis and the evolution of lemuriform primates. In: Tattersall I, Sussman RW (eds.) Lemur biology. Plenum Press, New York. Gingerich PD (1976) Cranial anatomy and evolution of early tertiary Plesiadapidae: University of Michigan Papers on Paleontology 15:140. Gingerich PD, Martin RD (1981) Cranial morphology and adaptations in Eocene Adapidae. II. The Cambridge skull of Adapis parisiensis. Am J Phys Anthropol 56:235–257. Hershkovitz P (1977) Living New World Monkeys (Platyrrhini): With an introduction to primates. University of Chicago Press, Chicago. Kay RF (1975) The functional adaptations of primate molar teeth. Am J Phys Anthropol 43:195–216. Kay RF (1984) On the use of anatomical features to infer foraging behavior in extinct primates. In: Rodman PS, Cant JGH (eds.) Adaptations for foraging in nonhuman primates. Columbia University Press, New York. Kay RF, Hylander WL (1978) The dental structure of mammalian folivores with special reference to Primates and Phalangeroidea (Marsupialia). In: Montgomery GG (ed.) The ecology of arboreal folivores. Smithsonian Institution Press, Washington, DC. pp. 173–196. Kay RF, Williams BA, Anaya F (2001) The adaptations of Branisella boliviana, the earliest South American monkey. In: Plavcan JM et al. (eds.) Reconstructing behavior in the primate fossil record. Kluwer Academic/Plenum Publishers, New York. Kinzey WG, Rosenberger AL, Ramirez M (1975) Vertical clinging and leaping in a neotropical anthropoid. Nature 225:327–328. Lucas PW (1981) An analysis of canine size and jaw shape in some Old and New World nonhuman primates. J Zool 195:437–448. Martin RD (1972) Review lecture: Adaptive radiation and behaviour of the malagasy lemurs. Philos Trans R Soc Lond B Biol Sci 264:295–352. Martin RD (1979) Phylogenetic aspects of prosimian behavior. In: Doyle GA, Martin RD (eds.) The study of prosimian behavior. academic Press, New York. pp. 45–77. Martin RD (1990) Primate origins and evolution: A phylogenetic reconstruction. Princeton University Press, Princeton, New Jersey. Petter JJ, Schilling A, Pariente G (1971) Observations eco-ethologiques sur deux lemuriens malgaches nocturnes: Phaner furcifer et Microcebus coquereli. Terre Vie 25:287–327. Rassmussen TD, Sussman RW (2007) Parallelisms among primates and possums. In: Ravosa MJ, Dagosta M (eds.) Primate origins: Adaptations and evolution. Springer, New York. Richard AF (1978) Variability in the feeding behavior of a Malagasy prosimian, Propithecus verrauxi: Lemuriformes. In: Montgomery GE (ed.) The ecology of arboreal folivores. Smithsonian Institution Press, Washington, DC. Rose KD, Bown TM (1996) A new plesiadapiform (Mammalia; Plesiadapiformes) from the early Eocene of the Bighorn Basin. Ann Carnegie Mus 65:305–321. Rose, KD, MacPhee, RDE, Alexander, JP (1999) Skull of early Eocene Cantius abditus (Primates: Adapiformes) and its phylogenetic implications, with a reevaluation of “Hesperolemur” actius. Am J Phys Anthropol 109:523–539. Rosenberger AL (1978) Loss of incisor enamel in marmosets. J Mammal 59:207–208. Rosenberger AL (1992) The evolution of feeding niches in New World monkeys. Am J Phys Anthropol 88:525–562.

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Rosenberger AL, Halenar L, Cooke S, Tejedor MF, Hartwig WC (2008) Morphology and evolution of the spider monkeys, genus Ateles. In: Campbell CJ (ed.) Spider monkeys: Behavior, ecology and evolution of the genus Ateles. Cambridge University Press, Cambridge. Rosenberger AL, Kinzey WG (1976) Functional patterns of molar occlusion in platyrrhine primates. Am J Phys Anthropol 45:281–298. Rosenberger AL, Strasser ME (1985) Toothcomb origins: Support for the grooming hypothesis. Primates 26:76–85. Rosenberger AL, Strasser ME, Delson E (1985) Anterior dentition of Notharctus and the adapid– anthropoid hypothesis. Folia Primatol 44:15–39. Ross CF, Lockwood C, Fleagle J, Jungers WL (2001) Adaptation and behavior in the primate fossil record. In: Plavcan JM, Kay RF, Jungers WL, van Schaik CP (eds.) Reconstructing behavior in the primate fossil record. Kluwer, New York. Silcox MT, Sargis EJ, Bloch JI, Boyer DM (2007) Primate origins and supraordinal relationships: Morphological evidence. In: Henke W, Tattersall I (eds.) Handbook of paleoanthropology. Springer, New York. Smith AP (1982) Diet and feeding strategies of the marsupial sugar glider in temperate Australia. J Anim Ecol 51:149–166. Snodgrass JJ, Leonard WR, Robertson ML (2007) Primate bioenergetics: An evolutionary perspective. In: Ravosa MJ, Dagosto M (eds.) Primate origins: Adaptations and evolution. Springer, New York. Szalay FS, Delson E (1979) Evolutionary history of the primates. Academic Press, New York. Szalay FS, Seligsohn D (1977) Why did the strepsirhine tooth comb evolve? Folia Primatol 27:75–82. 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.

Index

A Acacia, 3, 47, 49, 61–63, 75, 77, 79, 95, 157, 214 Acacia gum, 3, 7, 13, 26, 37, 164, 213, 286 Acidic polysaccharide, 124, 158 Activity period, 124 Adaptations, 1, 3, 5–8, 12, 16, 27, 31, 35, 37, 46, 49, 75, 77, 89–91, 116, 117, 123, 125, 129, 156, 170, 179, 212, 229, 235–236, 251, 253, 274, 277 Adaptive profile, 273–293 Adaptive specialization, 273–293 African pottos, 155, 156 Alantisolodendron, 63, 127, 130, 133, 137 Albizia, 34, 47, 63, 131, 157 Alkoloids, 33 Allenopithecus, 90 Allocebus, 5, 13–15, 49, 50, 60, 73, 125, 128, 129, 137 Allometry, 36, 172 Alouatta, 66, 73, 76, 90 Anacardiaceae, 49, 55, 76, 124, 135, 157 Angwantibo, 156, 158 Antibiotic, 46, 110 Apparent dry matter digestibility, 36, 38 Arabinose, 30, 33, 76 Araliaceae, 56, 97 Arctocebus, 155–165 Arctocebus aureus, 157 Arctocebus calabarensis, 155, 157 Ardeotis kori, 30 Areacacea, 56, 95, 157 Arthropods, 6, 93–95, 150, 236 Ateles, 51, 66, 73, 75, 90, 279 B Baboon, 4–6, 32, 49, 75, 203 Bacteria, 41

Beetles, 3, 133 Bioavailability, 7, 9, 27, 33 Biochemical analysis of foods, 26 Biogeography, 48, 77 Body size, 5, 12, 15, 32, 40, 46, 156, 195, 219, 237, 238, 284, 286 Buchenavia, 59, 97, 98, 103 Burseraceae, 58, 124, 131, 132, 135, 157 Bushbaby, 214, 259 C Cacajao, 53, 66, 73, 76, 90 Caecum, 125, 128, 129, 138, 163, 212 Calcium, 5, 9, 30, 34–35, 105, 110, 116 Callibella, 91, 102 Callimoco, 6, 10, 11, 17, 35, 49, 51, 54, 56, 57, 62, 65, 67–69, 73, 76–78, 89–105, 187, 281 Callimico goeldii, 35, 51, 56, 57, 62, 67–69, 91, 117 Callithrichines, 4, 6, 12–14, 16, 18 Callithrix, 35, 41, 46, 48, 54, 73, 75, 76, 78, 91, 102, 110, 128, 163, 170, 172, 174, 178, 212, 213, 229, 236, 277, 279, 281–283 Callithrix jacchus, 13, 36–39, 55, 56, 59–64, 67, 69, 190, 191, 196–198, 200, 202 Callithrichidae, 30, 35–42, 46–48, 51, 54, 73, 77–78, 117, 128, 187, 206 Calltrichid, 35–37, 40–42, 46, 47, 75, 78, 117, 128, 187, 189, 206 Canine teeth, 125, 128, 218, 288 Captive management, 18, 156, 165 Captive, 4, 8, 13, 16–18, 34, 35, 40, 76, 117, 158, 160–162, 164–166, 191, 206, 236 Carnivores, 26 Cartilage, 14, 172, 187–207

297

298 Ceacum or cecum, 6, 31, 34, 37, 40–42, 46, 103 Cebuella, 8, 15, 17, 35, 49, 73, 77, 78, 92, 102, 104, 163, 177, 178, 187, 213, 229, 277, 279, 281, 283, 288 Cebuella pygmeae, 36–38, 49, 51, 55, 57–62, 64–72, 115, 170, 190, 191, 196–198, 200, 202, 283 Cebus, 53, 54, 66, 67, 73, 74, 78, 90, 180 Cecal-colonic separation mechanism, 16, 37, 38 Cedrela, 69, 95–98, 104 Cells, 27–30, 142, 189, 257–259, 268 Cellulose, 29–31, 278 Cercopithecus, 53, 62, 63, 70, 73, 90, 105, 163 Cheek teeth, 164 Cheirogaleidae, 50, 54, 73, 123–138, 170, 172, 174 Cheirogalid, 15 Chemical defence (by plants), 2, 29 Chemosensation, 268 Chimpanzee, 4, 5, 32, 34, 47, 90, 117 Circumgenital scent marking, 164 Claw-like nails, 6, 17, 90, 95, 97, 102 Claws, 18, 46, 252, 253 Climatic variability, 76, 135 Clinal variation, 156 Cluster analysis, 48, 74, 78 Colon, 31, 34, 35, 37, 41, 42, 46 Combretaceae, 59, 76, 97, 131, 157, 164 Commiphora, 58, 127, 130, 131, 133, 135, 137 Common marmosets, 36, 39, 41, 91, 117, 199 Complete food, 28, 41 Continuous recording sampling, 145 Convergence, 3, 124, 125, 284 Conversion factors for protein content, 9 Coprophagy, 32, 34 Cranial-dental features, 12–15 Craniofacial morphology, 46 Craniomandibular morphology, 170–171 Crude protein, 33, 126, 131–132 D Daily exudate production, 89, 98–100 Daily pattern of exudate consumption, 94 Daily time scale, 11 Day range, 90 Degraded or disturbed area or habitat, 96, 150 Dental adaptations, 35, 46, 75, 77, 110, 116, 212, 251, 277 Dental disease, 165

Index Dentition, 8, 12–14, 18, 46, 77, 95, 165, 171, 175–179, 181, 212, 213, 216–218, 220–225, 228, 229, 251, 279, 280, 284, 289, 290, 292 Diet, 276, 277, 279, 285 Dietary adaptations, 276, 277, 279, 280, 284 Dietary fiber, 27, 29, 31 Dietary opportunism, 77 Dietary overlap, 109, 112 Dietary overlap between species, 109 Dietary overlap between years, 109 Dietary staple, 36, 118, 155 Digesta passage rate, 35, 38, 41 Digestability, 10, 36, 38, 40, 75, 104, 124, 126, 142 Digestible energy intake, 10, 32, 40 Digestion, 6, 9, 10, 15, 25, 31–32, 34–37, 40, 42, 46, 76, 90, 91, 103, 117, 118, 142, 156, 163, 212 Digestive challenges, 9, 10, 15, 25–42, 75, 133 Digestive efficiency, 38, 40 Digestive enzymes, 25, 31, 33, 34 Digestive function, 27, 35–40 Digestive kinetics, 25 Dry deciduous forest, 143, 144, 150 E Ecological constraint, 90 Ecology, 41, 89–105, 155–166 El Niño related drought, 125, 127, 137 Energy digestibility, 10, 36–38, 40 Enrichment food, 35 Environmental constancy = intra-annual variation = seasonality, 127, 134 Environmental contingency = interannual variation = unpredictability, 127 Erythrocebus, 73, 90, 163 Euoticus, 13, 15, 73, 74, 78, 90, 125, 128, 169, 172–175, 212, 213, 222, 228, 245, 247, 253 Euterpe, 56, 95, 96 Excretion curves, 38 Experimental cuts on trees, 93, 94 Experimental sites for exudate production, 93, 94, 96–100, 103 Exudates, 2–12, 14–19, 26–33, 35, 46–50, 73–79, 90–105, 110–113, 115–118, 142, 144, 156–160, 162–165, 170, 171, 187, 188, 190, 212–215, 217, 219, 227–230, 236–237, 253, 279, 285, 293

Index Exudativorous, 7, 8, 12–14, 17, 18, 105, 175, 212–219 Exudativory, 1–19, 45–79, 157–160, 169–182, 211–230, 275 F Fabaceae, 9, 47, 49, 61, 76, 77, 124, 126, 131, 157, 159, 160, 164 Facial marking, 160, 161 Fallback food, 6–8, 10, 105, 164, 170, 214, 280 Fallback resource, 46 Fatty acids, 31, 32 Feeding bout length, 92, 93, 95 Feeding ecology, 5, 151 Feeding site availability, 90, 103 Feeding site distribution, 90, 103 Fermentation, 6, 10, 27, 29, 31, 35, 37, 39, 41, 46, 91, 105, 110, 117 Field studies, 18, 111, 156, 158, 163, 165, 227 Field study, 95, 125 Flatida coccinea, 143 Flatidae, 143 Flowers, 2, 27, 28, 145, 160, 171, 279 Fluid passage rate, 37 Focal observations, 145 Focal sampling, 145 Folivore, 46, 213, 274, 275, 289, 291 Food, 3, 6–8, 10, 11, 15–18, 26–30, 32–35, 40, 41, 49, 75, 90–93, 95, 96, 102–105, 111, 124, 126, 127, 133, 134, 142–151, 159, 164, 165, 171, 215, 258, 259, 275–278, 280, 292 Food availability, 11, 75, 134, 150 Food preference, 6, 7 Food quality,10, 90, 103 Foot pad, 242–250, 252–254 Foraging efficiency, 90, 133 Fore-gut fermenter, 31, 32 Forest edge habitat, 147, 149, 150 Fork-marked lemur, 46, 49, 75, 164, 175 Frugivorous, 13, 16, 46, 124, 151, 173, 178, 190, 212–214, 275 Fruits, 5, 9, 10, 16, 18, 27, 28, 33–38, 40, 47, 75, 92–95, 103–105, 113–116, 124, 126–128, 130, 131, 133–135, 143, 145, 146, 150, 156, 171, 190, 214, 215, 228, 275, 279, 280 Fungus, 93, 159

299 G Galagidae, 73, 74, 170, 173, 175, 176, 213, 235 Galaginae, 50, 54 Galago, 3, 13, 15, 47, 50, 54, 62, 63, 73, 74, 78, 105, 125, 129, 164, 171–176, 203, 212–219, 227, 235–254, 274 Galagoides, 50, 173, 175, 176, 212, 215, 219, 227, 228, 237, 240–241, 244, 245, 249, 250 Galagos, 3–5, 12–13, 46–47, 77, 105, 164, 171–176, 179, 211–230, 235–236, 251–253 Gape, 13–14, 46, 91, 171, 173–175, 179, 181, 188, 205, 214, 281, 283, 288 Gestation, 9, 110, 116 Gleaning, 14, 277, 279–280, 282, 286, 287, 289, 292 Global distributions of gummivorous mammals, 125 Glucose, 26, 30, 47, 117, 126 Glycoprotein, 30–31, 33 Goeldi’s monkey (=callimico), 6, 7, 10, 11, 35, 49, 77, 89–105, 187 Gouge, gouging, 3, 4, 6, 12–15, 18, 35, 39, 46, 53, 77, 91, 93, 94, 96–97, 99, 100, 102, 103, 110, 115, 116, 128, 129, 138, 143, 158–165, 170–174, 176–177, 179, 181–182, 187–207, 213, 217, 219, 228, 229, 236, 252, 274, 277, 279–284, 286–292 Grey mouse lemur, 49, 116, 124, 128, 138 Group size, 11, 90, 112 Gum, 3–19, 25–42, 46–49, 54, 75–79, 103, 109–118, 124–138, 141–151, 158–160, 163–165, 170, 171, 188, 190, 213, 235–254, 274–275, 277–282, 284–292 Gum Arabic, 30, 32–33, 37–38, 165 Gum chemistry, 46, 76, 110, 116–118 Gum eating marsupials, 3, 27, 137, 285, 292 Gum feeding, 10, 12, 25–42, 54, 79, 109–118, 125, 129–130, 149, 285 Gum specialist, 6, 12, 124, 125, 128–130 Gum-feeding specialist, 32 Gummivory, 5, 15, 46, 48–49, 74, 77–78, 110, 111, 114–116, 123–138, 150–151, 170, 273–293 Gustatory, 257–258, 267–268 Gut kinetics, 15–16, 40–42 Gut length, 41 Gut proportions, 15–16, 40 Gut retention time, 32, 117 Gut transit time, 15–16, 40, 91

300 H Habitat edges, 147, 149, 164 Hairy-eared dwarf lemur, 49 Hand pad, 240–243, 245, 252 Hand/foot relative size, 252 Hemicelluloses, 31 Hemiptera, 28, 142–143, 145, 147 Hemipteran insects, 28 Hemipteran larval secretion, 143, 145 Herbivore, 26, 33, 142 Hind-gut fermenter, 31–32, 34, 39, 42 Histomorphometrics, 190 Home range, 46, 93, 101, 103–105, 111, 133, 146, 149 Home range size, 46, 103 Homo, 49, 73 Homopteran secretions, 130 Honeydew feeding, 141–151 Human appendix, 41 Hydrolysis of carbohydrates, 126 Hypervariable environment, 19, 123–138 I Inga, 65, 76, 77, 94–96, 100 Insectivore, 46, 178 Insectivorous, 30, 33, 34, 41, 105, 110, 151, 158, 173, 291 Insoluble fiber, 29 Instantaneous sampling, 92 Interpopulation differences (in exudate feeding), 11, 115 Intrageneric differences in exudate/gum consumption, 11 Invertebrates, 40, 42, 142, 151, 163 Iriartea, 57, 95, 96, 98, 100, 103 K Kaka parrot, 142 Keeled nails, 125, 129, 163, 164, 253 Keystone resource, 46, 75, 115, 128, 143 Kori bustard, 30 L Lactation, 9, 110, 116 Lagothrix, 4, 51, 54, 66, 67, 76, 90 L-arabinose, 76 Latex, 2, 28–29, 72, 142 Laticifers, 29 Lecythidaceae, 68, 95, 157 Leguminosae, 94, 95, 99 Lemur catta, 50

Index Leontopithecus, 35, 40, 41, 73, 74, 76, 78, 281 Life history, 8, 156, 275 Lignin, 31, 33 Lingual papillae, 258, 264 Lion tamarin, 35–38, 41, 76, 78, 91 Lipid content, 126–127, 164 Load-resistance, 46 Long tongue, 13, 16, 125 Loris, 125, 158–160 Loris tardigradus, 125, 157, 158 Lorises, 4, 7–9, 12, 13, 16–18, 47, 128, 155, 166, 213, 228, 287 Lorisids, 13, 15, 46, 125, 128, 158, 170, 213 Lorisidae, 51, 73, 156 Lorisoid, 4, 15, 90, 129, 287 M Madagascar, 5, 50, 63, 124, 126–128, 135, 137, 143, 144, 150, 151 Madame Berthe’s mouse lemur, 150 Marks and signs of gouging on plants, 160 Marmosets, 3, 6, 8, 11, 16–18, 27, 32, 35–41, 46, 47, 49, 74, 76, 77, 90, 91, 93, 94, 96, 97, 99, 102–104, 110, 113, 117, 164, 165, 172–179, 181, 190, 195, 196, 199, 201, 203, 204, 206, 212, 213, 229, 236, 264, 277, 279, 281–292 Marsupial gummivores, 127, 137, 138 Marsupials, 3, 27, 127, 137, 138, 285 Masticatory complex, 156, 163, 165 Meliaceae, 69, 76, 95, 97, 126, 157 Metabolize, 26 Metachromasia, 194, 201, 202 Mico, 17, 35, 49, 73, 74, 77, 78, 91, 102, 104, 117 Microbial fermentation, 35, 46, 105, 110, 117 Microcebus, 49, 73, 74, 78, 90, 128, 137, 143, 212, 228 Microcebus berthae, 50, 136 Microcebus griseorufus, 5, 54, 55, 58, 63, 69, 124, 129 Microcebus murinus, 5, 49, 55, 58–61, 63, 64, 67, 69–71, 125, 129, 143 Mineral content, 9, 110 Mineral source, 30, 105 Minerals, 5, 9, 30, 32, 34, 105, 110, 214 Mirza, 74, 78, 128, 137 Mixed species troop, 91, 92, 94, 95, 111, 113 Monimiaceae, 97

Index

301

O Obesity, 18, 165 Omnivorous, 35, 156 Ontogeny, 17, 172, 203, 206, 259 Ontogeny of gum consumption, 9, 110 Otolemur, 16, 74, 78, 172–176, 240–242, 250, 253, 257–268, 274, 277

Papio, 32, 49, 73, 90, 163 Paraserianthes, 160 Parkia, 7, 30, 47, 49, 67, 75, 76, 90, 95, 100, 103, 104, 115, 118 Parkia pod, 30–31, 95, 96, 104, 113–115 Particulate passage rate, 35–37, 39 Patas monkey, 4–6, 12, 47, 49, 75, 105, 116 Pattern of habitat utilization, 90 Pectin, 30, 31, 35 Pelage, 15–17, 165 Perodicticus, 90, 155–166 Perodicticus potto, 157, 285 Phaner, 5, 8, 13–15, 46, 49, 74, 78, 90, 125, 128, 129, 137, 163, 212, 213, 217, 289 Phenology, 105, 131–132 Phenology, phenological pattern, 90 Phosphorus, 34, 110 Phromnia rosea, 143 Phylogeny, 48, 77, 230, 235 Physical defense (by plants), 29 Pithecia, 53, 66, 73, 76 Pod exudates, 4, 6, 75, 89, 93–96, 101–102, 104, 109, 113, 115, 116 Pod exudate production, 96–102 Pod gum, 7–8, 10, 30–31, 45, 47, 75–76, 110–114, 116–118 Point sampling, 92–93 Polysaccharide, 29, 30, 33, 35, 91, 117, 124, 158 Population density, 46, 138 Positional behavior during exudate feeding, 2, 8–9, 13–14, 17, 27, 49, 89–105, 112–113, 115, 155–166 Posture, 17, 95, 160 Potto, 49, 51, 155–166, 285 Predictable, 91, 102, 136–137, 141, 150 Predictable food, 91, 102, 141, 150 Preference, 3, 104, 115, 118 Preferred food, 6–7 Prevalence of gummivory across primates, 45–79 Protease, 29 Proteins, 2, 9, 26, 32–34, 110, 126, 131–133, 143, 189, 214 Protein content, 9, 34, 143 Proteoglycans, 189–192, 194, 201, 206 Pygmy marmosets, 11, 25, 35, 36, 39, 41, 49, 76, 89, 91, 93, 96, 97, 99, 103, 104, 109, 187, 190, 236, 284

P Paleobiology, 274, 275, 277 Pan, 32, 73

R Radiotracking, 126, 127, 130, 133 Rate of exudate production, 89–105

Morphological adaptations, 2, 3, 5, 14, 46, 49, 91, 103, 124, 164, 170, 173, 212, 284 Morphological correlates of behavior, 170 Morphometrics, 204, 217, 218 Mouse lemur, 5, 10, 28, 49, 75, 116, 124, 127, 128, 133, 141–151, 229 Muscles of mastication, 46 N Nails, 6, 17, 46, 90, 95, 102, 125, 128, 129, 163, 164, 237, 250–251, 253 Natural sites of exudate production, 98–100 Nectar, 2, 28, 35, 92–95, 105, 128, 130, 142, 143, 145–147, 149, 171 Needle-clawed galago, 46, 49, 90, 236 Neotoma, 28 Nestor meridionalis, 170 New World monkeys, 34, 102, 187–207 Niche overlap, 112 Nitrogen content, 9, 33 Nocturnal, 8, 13, 30, 75, 126, 142, 143, 150, 156, 164, 229, 235 Nocturnal strepsirrhines, 8, 75 Non-gouging, 110 Non-gouging primate, 110 Non-living plant product, 27 Nutrients, 7, 9–10, 26–32, 36, 142, 163, 214 Nutritional analysis, 143 Nutritional content (gum versus fruit), 124 Nutritional value, 10, 105 Nutritive value, 124, 138 Nycticebus, 4, 12, 73, 74, 79, 90, 128, 155–166 Nycticebus bengalensis, 157 Nycticebus coucang, 47, 51, 55, 56, 58, 69, 70, 157, 213 Nycticebus javanicus, 157 Nycticebus pygmaeus, 58, 125, 129, 157

302 Reddish-grey mouse lemur, 123, 124, 128, 138 Reliability of a resource, 8, 89, 102, 111 Renewability, 89, 91, 102, 103 Resin, 2, 28, 142 Resource defendability, 133, 138 Resource renewal, 11, 89, 91 Revisit feeding site, 90–91, 102, 105, 141, 144, 145, 149 S Saguinus, 35, 40, 41, 49, 73–75, 77, 78, 89–106, 110, 178, 187, 281–283 Saguinus fuscicollis, 36–39, 49, 54–62, 64–72, 109, 111, 174, 181 Saguinus mystax, 39, 56–61, 64–68, 71–72, 89, 91, 109 Saimiri, 53–54, 66, 68, 71, 73, 76, 172, 174, 176, 178–179, 187, 190–191, 196–198, 200, 202 Sap, 2–3, 10, 28, 37, 102, 141–143, 149, 151, 155, 158, 159, 169–171, 181, 188, 190, 292 Sap feeding, 141, 142, 151 Sap feeding by proxy, 141, 142, 151 Scent marking, 95, 160, 161, 164–165 Schefflera, 56, 96–98, 103 Schoener’s index of niche overlap, 112 Sclerolobium, 68, 98–100, 104 Scrape, 4, 12–15, 128, 130, 138, 143, 159, 164, 174, 236, 251 Scraping, 12–14, 46, 128, 129, 138, 142, 143, 169–176, 179, 181, 182, 213, 214, 217, 219, 227, 229, 236, 251, 280, 289, 291 Search strategy, 90 Season of food abundance, 141, 150 Season of food scarcity, 141–143, 155, 164 Seasonal environment, 143, 164 Seasonal time scale, 11 Seasonality, 11–12, 45, 49, 74–75, 78, 100, 105, 116, 134–137, 141–151, 169, 181 Seasonality of exudate consumption, 3, 9, 11–19, 102–104, 110, 159 Seasonality of exudate production, 89–105 Seasonality of exudate use, 1, 5, 16 Seasonality of gum consumption, 9, 10, 49, 76, 110, 116, 141, 142

Index Seasonality of gum production, 109, 114–116 Seasonality of resource production, 102, 116 Secondary compounds, 2, 9, 16, 33, 46, 47, 105, 110, 156 Seeds, 25, 28, 30, 35–41, 47, 72, 75, 92, 94, 109, 110, 117, 118, 124, 138, 143, 145, 274, 292–293 SEM, 113–115, 177–180, 222–223, 257, 260–263, 266, 268 Simple sugars, 28, 31–32, 47, 110, 117–118 Siparuna, 97–98, 103 Site of production, 110, 285 Skull, 14, 125, 128, 169–182, 188, 203, 211, 212, 218–220, 237, 274, 281, 283 Social dominance, 90 Socratea, 57, 95–96 Soluble fiber, 29–31, 38 Soluble polysaccharide, 9, 158 Soluble sugars, 126 Spatial variability, 19 Spatio-temporal distribution of food, 127 Spatio-temporal predictability, 90, 127 Special senses, 257, 277 Specialization, 12, 102, 123–124, 142, 171, 229, 253, 254, 257, 259, 268, 273–293 Spiny forest, 124, 125, 131, 133, 135, 143, 151 Stage of reproduction, 109, 116 Standard assay techniques (of foods), 33 Stilt root exudates, 89, 93, 96, 104 Structural carbohydrate, 30, 163 Sucrose digestion, 76, 118 Sugar glider, 3, 7, 19, 170, 273, 284–287, 292 T Tamarins, 1, 6, 8, 10, 11, 16–18, 35–38, 41, 49, 75–78, 89–97, 100–105, 109–117, 169, 172, 175–178, 187, 190, 203, 204, 207, 212, 264, 277, 281–282 Taste, 16–17, 47, 78, 138, 257–259, 261–268 Taxonomic patterns of gummivory, 74, 78, 110–111, 115–118, 136, 273–293 Taxonomy, 4, 48, 136, 156, 158, 235 Temporal pattern of exudate production, 91, 113–118 Temporal pattern of gum consumption, 10, 142 Temporal pattern of gum feeding (daily), 25–42, 109–118, 134

Index Temporal variability, 134 Temporomandibular joint, 14, 172, 175, 187–207, 212, 214, 283, 287 Time spent feeding, 11, 49, 103, 112–113, 146 Tongue, 13, 15–17, 125, 159–160, 163, 257–269 Tongue anatomy, 16, 258–259 Toothcomb, 12–14, 46, 125, 128–130, 143, 159–160, 176, 211–230, 273–275, 277, 280, 287–293 Toothscraper, 15, 46, 125, 138, 235–252, 285, 287 Toxin, toxic, 4, 28, 29, 46, 47, 105, 110, 133, 138, 156 Tree fall zones, 164 Trunk exudates, 17, 89, 92–97, 100–101, 103–104, 115 Trunk exudate production, 89, 100–102 Trunk gum, 10, 17, 76, 109–111, 113, 114, 116–118

303 U Urine marking, 161, 164–165 V Variabilty of gum or fruit availability, 75, 116, 214 Vertebrates, 29–31, 35, 40, 93, 95, 96, 110, 142, 151, 170, 218 Vertical clinging, 17, 96 Vervet, 4, 5, 47, 105 Vitamins, 18, 31, 32, 35 Vochysia, 71, 72, 94–95, 100 W Within-group competition, 90 X Xerophytic forest, 128, 137