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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 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; Charles-Dominique and Petter 1980), and the modified anterior “tooth-comb” or “tooth-scraper” 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 β-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 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. 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 (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.

Table 3.1 Primates known to consume exudates, and the proportion of exudates in their diet
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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).

Table 3.2 Seasonal changes in gum feeding in primates
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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).

Table 3.3 Sources of exudate recorded to be consumed by primates
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Table 3.4 Numbers of plant species, genera and families exploited for exudates by 30 genera of primates
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Table 3.5 Top five species, genera and families as ranked by the number of species (n c) known to consume their exudates
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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 (S S: 0.667), (b) Otolemur, Galago, Euoticus and Cebus (S S: 0.475 < 1.000), (c) Mico, Phaner, Leontopithecus, and Callimico (S S: 0.395 < 0.615) and (d) Saguinus, Cebulla, the C. jacchus group, Microcebus and the C. flaviceps group (S S: 0.346 < 0.542).

Fig. 3.1
figure 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.

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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) 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 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.

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), 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 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 year-long 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.