Physical and chemical properties of fruit and seeds eaten byPithecia andChiropotes in Surinam and Venezuela

Pithecia pithecia andChiropotes satanas are seed predators that eat fruits with hard pericarps. We measured resistance to puncturing and crushing of fruit and seeds eaten by these two pitheciins at two localities: in evergreen rain forest at Raleighvallen-Voltzberg, Surinam, and in tropical dry/transitional moist forest on islands in Guri Lake, Venezuela. Average measurements of pericarp hardness were similar at both sites for fruit eaten byChiropotes, but a higher maximum value was obtained at the rainforest site.Chiropotes andPithecia both ate fruits that had harder pericarps than did fruits eaten byAteles paniscus, but crushing resistances of seeds eaten were lower than values forAteles. Thus, both pitheciins selected fruits with hard pericarps and soft seeds, although there were notable intergeneric differences in hardness of fruit ingested. When fruit became scarce,Pithecia ate more flowers, whileChiropotes continued to eat fruits with hard seed coverings. Chemical analysis of species of seeds eaten byPithecia suggests that they avoided seeds with extremely high tannin levels, though they tolerated moderate tannin levels in combination with high levels of lipids. We propose that sclerocarpic harvesting (the preparation and ingestion of fruit with a hard pericarp) allows pitheciin monkeys to obtain nutritious seeds, with reduced tannins, that are softer than those ingested by other frugivores.Presented at XIIIth Congress, International Primatological Society, July 27, 1990.     

Hardness of cercopithecine foods: implications for the critical function of enamel thickness in exploiting fallback foods

We evaluate the hardness of foods consumed by sympatric Cercopithecus ascanius (redtail guenons) and Lophocebus albigena (grey-cheeked mangabeys), and consider how selection might operate to influence foraging adaptations. Since L. albigena has among the thickest dental enamel in extant primates and is commonly referred to as a hard-object consumer, we predicted that their diet would be harder than that of the guenon. Data on diet and food hardness (as measured by resistance to puncture and crushing) were collected between June-October of 1997 at Kibale National Park, Uganda, and were compared to similar data collected in Kibale between 1991-1994. Contrary to what we predicted, there was no difference in dietary hardness when the puncture resistance of all fruit consumed by the two species was compared (31 tree species in both study periods). However, in June-October 1997, L. albigena exploited a diet more resistant to puncture and crushing than C. ascanius. This difference is largely explained by the higher percentage of bark and seeds consumed by the L. albigena during this period. We suggest that it is the difference in the mechanical properties of fallback foods during critical periods that may have served as the selective pressure for thick enamel in L. albigena.     

Brief communication: Puncture and crushing resistance scores of Tana river mangabey (Cercocebus galeritus) diet items

Cercocebus mangabeys are characterized by dental traits that have been interpreted as adaptations to eat hard diet items. Although there are data that mangabeys include a large proportion of fruit and especially seeds in their diets, no hardness measurements have been done on mangabeys' food items. This study measured puncture and crushing resistance of food items in the diet of the Tana River mangabey (C. galeritus). Feeding data were collected by the use of scan samples from one mangabey group from August 2000 to July 2001 and from July 2005 to June 2006. Food items were collected during the latter period only, and from the same tree in or under which mangabeys had been observed eating. A portable agricultural fruit tester was used to measure the puncture resistance of fruit and a valve spring tester was used to measure the crushing resistance of seeds. The average puncture resistance of fruit was 1.7 kg/mm², and the average crushing resistance of seeds was 12.8 kg. There were no correlations between puncture resistance, crushing resistance, or all resistance scores and frequency contribution to the diet. Resistance scores measured in this study were within the range of hardness scores of fruit and exceeded hardness scores of seeds eaten by other hard object feeders. Although this study supports the interpretation that Cercocebus dental traits are adaptations to hard object feeding, future research should investigate other material properties of food, as well as the role hard diet items play in niche separation and as fallback foods. Am J Phys Anthropol 2009. © 2009 Wiley‐Liss, Inc.     

The primate community of Cachoeira (Brazilian Amazonia): a model to decipher ecological partitioning among extinct species

Dental microwear analysis is conducted on a community of platyrrhine primates from South America. This analysis focuses on the primate community of Cachoeira Porteira (Para, Brazil), in which seven sympatric species occur: Alouatta seniculus, Ateles paniscus, Cebus apella, Chiropotes satanas, Pithecia Pithecia, Saguinus midas, and Saimiri sciureus. Shearing quotients are also calculated for each taxon of this primate community. Dental microwear results indicate significant differences between taxa, but are somewhat insufficient when it comes to discriminating between ecologically similar taxa. The primates of Cachoeira Porteira all incorporate a certain amount of fruit in their diet, entailing a definite amount of inter-specific competition as they must share food resources. Alouatta is the most folivorous taxon of this community, which is corroborated by dental microwear analysis. Ateles, although of a similar size to Alouatta, limits inter-specific competition by incorporating more fruit in its diet. Cebus has a very diverse omnivorous diet, which is highlighted in this study, as it compares to both fruit and leaf eating taxa. In some cases, microwear results need to be supplemented by other methods. For example, dental microwear seems insufficient to distinguish between Pithecia and Chiropotes, which eat foods with similar physical properties. However, other methods (i.e. shearing quotients and body mass) provide enough complimentary information to be able to highlight differences between the two taxa. On the other hand, dental microwear can highlight differences between primates which have similar diets, such as Saimiri and Saguinus. In this case, differences could be due to other exogenous factors.     

Enamel thickness and microstructure in pitheciin primates, with comments on dietary adaptations of the middle Miocene hominoid Kenyapithecus

Many living primates that feed on hard food have been observed to have thick-enameled molars. Among platyrrhine primates, members of the tribe Pitheciini (Cacajao, Chiropotes, and Pithecia) are the most specialized seed and nut predators, and Cebus apella also includes exceptionally hard foods in its diet. To examine the hypothesized relationship between thick enamel and hard-object feeding, we sectioned small samples of molars from the platyrrhine primates Aotus trivergatus, Ateles paniscus, Callicebus moloch, Cebus apella, Cacajao calvus, Chiropotes satanas, Pithecia monachus, and Pithecia pithecia. We measured relative enamel thickness and examined enamel microstructure, paying special attention to the development of prism decussation and its optical manifestation, Hunter-Schreger Bands (HSB). Cebus apella has thick enamel with well-defined but sinuous HSB overlain by a substantial layer of radial prisms. Aotus and Callicebus have thin enamel consisting primarily of radial enamel with no HSB, Ateles has thin enamel with moderately developed HSB and an outer layer of radial prisms, and the thin enamel of the pitheciins (Cacajao, Chiropotes, and Pithecia) has extremely well-defined HSB. Among platyrrhines, two groups that feed on hard objects process these hard foods in different ways. Cebus apella masticates hard and brittle seeds with its thick-enameled cheek teeth. Pitheciin sclerocarpic foragers open hard husks with their canines but chew relatively soft and pliable seeds with their molars. These results reveal that thick enamel per se is not a prerequisite for hard object feeding. The Miocene hominoid Kenyapithecus may have included hard objects in its diet, but its thick-enameled molars indicate that its feeding adaptations differed from those of the pitheciins. The morphology of both the anterior and posterior dentition, including enamel thickness and microstructure, should be taken into consideration when inferring the dietary regime of fossil species.     

Seed-eating by red leaf monkeys (Presbytis rubicunda) in dipterocarp forest of northern borneo

Data are presented on the feeding behavior ofPresbytis rubicunda at Sepilok, north Borneo. Emphasis is given to describing the fruit-eating behavior of this small colobine monkey, which specializes in eating seeds from large, dull-colored, and fleshless fruits. The seed predation is conspicuously different from the seed dispersal effected by sympatric monogastric primates and is characteristic of colobine frugivory at other forest sites. Most seed-eating occurred during the period of maximum fruit production and fewer small-seeded, animal-dispersed fruits were eaten at other times.     

Brief communication: a preliminary study on the influence of physical fruit traits on fruit handling and seed fate by white-handed Titi monkeys (Callicebus lugens)

Callicebus and the pitheciins are closely related; however, differences in their diets and dental morphology suggest that they differ in the use of mechanically protected food. We describe physical traits of fruits consumed by white-handed titi monkeys (Callicebus lugens) and determine their influence on fruit part selection and immediate seed fate after fruit handling. We tested two hypotheses about the effects of mechanical fruit traits on fruit part selection and seed fate: (1) fruits selected for seed consumption are harder than fruits selected for their fleshy parts and (2) consumed seeds are softer than seeds with other fates. In addition, we analyzed the influence of other physical fruit traits on fruit part selection and seed fate. C. lugens included 69 species in its diet, from which it mainly consumed their fleshy parts. It also consumed seeds, alone or with fleshy fruit parts, but most of them ended up close to parent trees after being dropped or spat out. The first hypothesis was supported while the second was rejected, indicating that C. lugens tends to rely on hard fruits for obtaining seeds, while seed hardness had no influence on fruit part selection and seed fate, contrasting with the pattern reported for Pithecia and Chiropotes in other studies. Ripeness was the most influential factor for fruit part and seed fate discrimination. Results suggest a tendency to sclerocarpic foraging in C. lugens when feeding on seeds.     

Food choice and food competition among the three major primate species of French Guiana

The three most important primates of French Guiana are frugivorous species, but to different degrees. Ateles paniscus is almost exclusively frugivorous, Alouatta seniculus frugivorous-folivorous, and Cehus apellu partially insectivorous; thus, the overall specific diet spectra arc well separated. During the season when fruit production is minimal, fruit intake by all species is also minimal which results in the greatest diversities in diet and the lowest diet overlaps. Real competition for the common main food category, i.e. fruits, only occurs during the most favourable period. Nevertheless, some fruit characteristics (e.g. size…) separate the monkey species from each other in fruit choice and make the interspecific competition of little importance.     

Responses of dispersal agents to tree and fruit traits in Virola calophylla (Myristicaceae): implications for selection

Variation in traits affecting seed dispersal in plants has been attributed to selection exerted by dispersal agents. The potential for such selection was investigated in Virola calophylla (Myristicaceae) in Manú National Park, Peru, through identification of seed dispersal agents and of tree and fruit traits significantly affecting the quantity of seeds dispersed. Seventeen bird and one primate species (the spider monkey, Ateles paniscus) dispersed its seeds. Spider monkeys dispersed the majority of seeds (a minimum of 83% of all dispersed seeds). Visitation by dispersal agents depended only on the quantity of ripe fruit available during a tree observation. In contrast, seed removal increased with both greater quantity of ripe fruit and aril: seed ratio. When analyzed separately, seed removal by birds increased only with greater aril: seed ratio, whereas seed removal by spider monkeys was affected by the quantity of ripe fruit and phenological stage. The finding that dispersal agents responded differently to some tree and fruit traits indicates not only that dispersal agents can exert selection on traits affecting seed dispersal, but also that the resulting selection pressures are likely to be inconsistent. This conclusion is supported by the result that the proportion of the seed crop that was dispersed from individual trees, which accounted for cumulative dispersal by all agents, was not influenced by any tree or fruit trait evaluated. Comparing these results with those from studies of V. sebifera and V. nobilis in Panama revealed that the disperser assemblages of these three Virola species were congruent in their similar taxonomic representation. In Panama the proportion of V. nobilis seed crop dispersed was related positively to aril: seed ratio and negatively to seed mass, a result not found for V. calophylla in Peru. The greater importance of dispersal by primates versus birds in V. calophylla, relative to V. nobilis, may explain this difference. Thus, variation in disperser assemblages at regional scales can be another factor contributing to inconsistency in disperser-mediated selection on plant traits.     

Foraging,Food Choice,and Food Processing by Sympatric Ripe-Fruit Specialists: <Emphasis Type="Italic">Lagothrix lagotricha poeppigii</Emphasis> and <Emphasis Type="Italic">Ateles belzebuth belzebuth</Emphasis>

Studies of interspecific competition and niche separation have formed some of the seminal works of ecology. I conducted an 18-mo study comparing the feeding ecologies of 2 sympatric, closely-related ripe-fruit specialists, Humboldt's woolly monkeys (Lagothrix lagotricha poeppigii), and the white-bellied spider monkeys (Ateles belzebuth belzebuth) in Amazonian Ecuador. Woolly monkeys in the terra firme forest live at roughly triple the density of spider monkeys (31 versus 11.5 animals/km²). Woolly monkeys spend 17% of their time foraging, while spider monkeys spend only 1% of their time foraging. Spider monkeys alone fed on soil and termitaria, which are rich in phosphorus. Woolly monkeys are not hard-fruit specialists. Their fruit diet is significantly more diverse than that of spider monkeys. Dietary overlap between the 2 species is high, yet each specializes to some degree on a different set of fruit resources. Woolly monkeys visit more food sources per unit of time, feed lower in the canopy, visit more small food patches, and prey on more seeds. Spider monkeys feed on fewer, richer food sources and are more than twice as likely to return to a particular fruit source than woolly monkeys are. Spider monkeys maximize fruit pulp intake, carrying more intact seeds in their guts, while woolly monkeys minimize seed bulk swallowed through more careful food processing. Surprisingly, several preferred spider monkey foods with high fat content and large seeds are avoided by woolly monkeys. I outline the different ecological dimensions involved in niche separation between the 2 species and discuss the possible impetus for their evolutionary divergence.     

Diet and Food Choice in Peruvian Red Uakaris (<Emphasis Type="Italic">Cacajao calvus ucayalii</Emphasis>): Selective or Opportunistic Seed Predation?

Even primates considered dietary specialists tend to eat a combination of fruit pulp, seeds, other plant parts, or animals. Specialist seed predators could either feed on seeds preferentially, or to avoid competition when ripe pulps are scarce. Pitheciin monkeys have specialized dentition that allows them to feed on seeds protected by hard shells, and the upper limit on the hardness of these is likely to be a function of jaw size. We recorded the diet of Peruvian red uakaris (Cacajao calvus ucayalii) on the Yavari River, Peru, to test the prediction that this seed predator would feed on the seeds of hard-shelled fruits preferentially over softer ones in relation to their availability in the forest. We also tested predictions that adult male, adult female, and juvenile diets would differ, with larger individuals eating more hard fruits. Uakaris ate 55.4% seeds, 38.9% pulps and arils, and 5.6% other items, but proportions varied through the year. More pulps, especially from the palm Mauritia flexuosa, were eaten when fruit availability was low, and more hard fruits were positively selected for than softer ones. Juveniles did not open the hardest fruit species opened by adults, and adult males ate harder fruits than females. These results provide evidence that seed eating in some primates has evolved beyond a means of avoiding competition for the ripe pulps typically preferred by many primates. Specialist seeding-eating primates therefore occupy divergent niches that require separate consideration from those of similar-sized primates.     

Immunodiffusion systematics of the primates. Part V. The Platyrrhini.

Evolutionary relationships between New World monkeys and marmoset genera and the place of the Ceboidea within the primates are considered in terms of the immunological specificity of ceboid proteins. Antigenic distances between the New World primates are measured using antisera produced in rabbits to nine ceboid genera: Alouatta, Aotes, Ateles, Callicebus, Cebus, Chiropotes, Lagothrix, Saimiri and Saguinus. A cladogram constructed on the basis of increasing degrees of antigenic distance between branches depicts Ceboidea as a monophyletic assemblage within which Alouatta is grouped with the Atelinae genera, Lagothrix and Ateles, Chiropotes joins Cacajao and Cebus joins Saimiri. The joining of the cebid genera Aotes and Callicebus with callithricid genera Callimico and Saguinus into a single complex lineage suggests that Cebidae is a paraphyletic or polyphyletic taxon. A phylogenetic taxonomy for Platyrrhini is proposed.     

Comparative use of color vision for frugivory by sympatric species of platyrrhines

Ateles spp. and Alouatta spp. are often sympatric, and although they are mainly frugivorous and folivorous, respectively, they consume some of the same fruit species. However, they differ in terms of color vision, which is thought to be important for fruit detection. Alouatta spp. have routine trichromatic color vision, while Ateles spp. presents the classic polymorphism of platyrrhines: heterozygous females have trichromatic color vision, and males and homozygous females have dichromatic vision. Given these perceptual differences, one might expect Alouatta spp. to consume more reddish fruits than Ateles spp., since trichromats have an advantage for detecting fruits of that hue. Furthermore, since Ateles spp. have up to six different color vision phenotypes, as do most other platyrrhines, they might be expected to include fruits with a wider variety of hues in their diet than Alouatta spp. To test these hypotheses we studied the fruit foraging behavior of sympatric Alouatta palliata and Ateles geoffroyi in Costa Rica, and modeled the detectability of fruit via the various color vision phenotypes in these primates. We found little similarity in fruit diet between these two species (Morisita = 0.086). Furthermore, despite its polymorphism, A. geoffroyi consumed more reddish fruits than A. palliata, which consumed more greenish fruits. Our modeling results suggest that most fruit species included in the diet of A. geoffroyi can be discriminated by most color vision phenotypes present in the population. These findings show that the effect of polymorphism in platyrrhines on fruit detection may not be a disadvantage for frugivory. We suggest that routine trichromacy may be advantageous for other foraging tasks, such as feeding on young leaves.     

Effects of Seed Dispersal by Three Ateline Monkey Species on Seed Germination at Tinigua National Park, Colombia

We examined the effect of seed ingestion by three ateline primates: woolly monkeys, Lagothrix lagothricha; spider monkeys, Ateles belzebuth; and, red howler, Alouatta seniculus on germination rates and latency periods of seeds of several plant species in Tinigua National Park, Colombia. We collected dispersed seeds from feces and control seeds from the parental trees and washed them for germination trials. For the majority of plants, dispersed seeds germinated as well or better than control seeds did. Although spider monkeys depend more heavily on fruits than the other monkey species do, they were not more efficient than howlers or woolly monkeys at improving germination rates. A considerable proportion of the seeds dispersed by howlers and woolly monkeys showed reduced latency periods to germination, but spider monkeys showed less effect on reducing germination time. This result may be related to longer gut retention times, but such a trend has not been observed in other primate species. We conclude that, like many other primates, ateline monkeys are effective seed dispersers in terms of their effects on the seeds they swallow because they rarely decrease their germination rates. We discuss problems that make interspecific comparisons difficult, such as inappropriate control seeds and differences associated with germination substrates, and we stress the importance of studying other components of seed dispersal effectiveness.     

Dispersión Primaria de Semillas por Primates y Dispersión Secundaria por Escarabajos Coprófagos en Tikal,Guatemala1

We linked primary dispersal by spider monkeys (Ateles geoffroyi) and howler monkeys (Alouatta pigra) to post‐dispersal seed fate by studying the effects of dung type and defecation pattern on secondary seed dispersal by dung beetles. First, we described the defecation patterns for both primate species. Howler monkeys generally defecated in groups (88% of observed defecations), with each individual producing on average 31 g of dung, resulting in a large area of the forest floor (31 m²) covered by large amounts of dung (clumped spatial pattern). Spider monkeys generally (96% of observed defecations) defecated individually, each individual producing an average of 11 g of dung, resulting in a small area of the forest floor (2 m²) covered by small amounts of dung (scattered spatial pattern). Secondly, we captured dung beetles using as bait the dung of both primate species, to detect differences in the assemblages of these secondary seed dispersers attracted to the dung of both primates. More individual dung beetles, but not more species, were attracted to howler monkey dung than to spider monkey dung. Finally, we assessed experimentally (using plastic beads as seed mimics) how dung type (Ateles vs. Alouatta) and defecation pattern (scattered vs. clumped) affect secondary seed dispersal by dung beetles. We found that post‐dispersal seed fate was affected by dung type, with more seeds being buried when present in howler monkey dung, than in spider monkey dung, but was not affected by defecation pattern. It is important to consider post‐dispersal processes, such as secondary seed dispersal by dung beetles, when comparing species of primary dispersers.     

Fruit Traits in Baboon Diet: A Comparison with Plant Species Characteristics in West Africa

Primate fruit choice among plant species has been attributed to different morphological plant and fruit characteristics. Despite a high abundance of animal-dispersed plant species in the savanna–forest mosaic of West Africa, few data are available on the interplay between morphological fruit traits and primate fruit consumers in this ecosystem. We tested whether olive baboons (Papio anubis) at Comoé National Park, north-eastern Ivory Coast, prefer fruit species with particular characteristics relative to the availability of these traits among the woody plant species at the study site. Specifically we were interested in the suites of traits that best predict fruit choice and seed handling by baboons. The baboons ate fruit/seeds from 74 identified plant species, representing 25 percent of the regional pool of woody plant species. They preferred trees to shrubs and lianas as fruit sources. Otherwise, baboons seemed to consume whatever fruit type, color, and size of fruit and seeds available, though they especially included larger fruit into their diet. Against expectations from the African bird–monkey fruit syndrome of brightly colored drupes and berries, baboons ate mostly species having large, dull-colored fruit. Fruit type and color best described whether baboons included a species into their diet, whereas fruit type and seed size best predicted whether baboons predated upon the seeds of their food plant species. As most plant species at the study site had medium-sized to large fruits and seeds, large frugivores like baboons might be particularly important for plant fitness and plant community dynamics in West African savanna–forest ecosystems.     

Fallback Foods of Red Leaf Monkeys (Presbytis rubicunda) in Danum Valley, Borneo

Animals in Southeast Asia must cope with long periods of fruit scarcity of unpredictable duration between irregular mast fruiting events. Long-term data are necessary to examine the effect of mast fruiting on diet, and particularly on the selection of fallback foods during periods of fruit scarcity. No such data is available for colobine monkeys, which may consume substantial amounts of fruits and seeds when available. We studied the diet of red leaf monkeys (Presbytis rubicunda, Colobinae) in Danum Valley, Sabah, northern Borneo, using 25 mo of behavioral observation, phenology and vegetation surveys, and chemical analysis to compare leaves eaten with nonfood leaves. The monkeys spent 46% of their feeding time on young leaves, 38% on seeds, 12% on whole fruits, 2.0% on flowers, 1.0% on bark, and 1.2% on pith. They spent more time feeding on seeds and whole fruit when fruit availability was high and fed on young leaves of Spatholobus macropterus (liana, Leguminosae) as fallback foods. This species was by far the most important food, constituting 27.9% of the total feeding time, and the feeding time on this species negatively correlated with fruit availability. Consumed leaves contained more protein than nonconsumed leaves, and variation in time spent feeding on different leaves was explained by their abundance. These results suggest that red leaf monkeys show essentially the same response to the supra-annual increase in fruit availability as sympatric monogastric primates, increasing their seed and whole-fruit consumption. However, they depended more on young leaves, in particular Spatholobus macropterus, as fallback foods during fruit-scarce periods than did gibbons or orangutans. Their selection of fallback food appeared to be due to both nutrition and abundance.     

The unique kidney of the spider monkey (Ateles geoffroyi).

Among nonhuman primates, the renal anatomy of the spider monkey (Ateles geoffroyi) is unique, as it is multipyramidal and multipapillary. Renal function parameters (glomerular filtration rate, renal plasma flow, and concentrating ability) are compared to man and other primates. The kidneys of the spider monkey are similar both anatomically and functionally to man.