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 Feeding Ecology of Woolly Monkeys in a Western Amazonian Rain Forest

I investigated the diet and feeding ecology of two social groups of woolly monkeys (Lagothrix lagotricha poeppigii) in Yasuní National Park, Ecuador between April 1995 and March 1996. Woolly monkeys in Yasuní were predominantly frugivorous, with fruits comprising ca. 77% of the yearly diet; the next most common food type in the diet was insect and other animal prey. The fruit diet of woolly monkeys in Yasuní is the most diverse yet recorded for any ateline primate, including spider monkeys (Ateles), which are often regarded as ripe fruit specialists: 208 distinct morphospecies of fruits were consumed by woolly monkeys either during the study or during several preceding months of pilot work. Nonetheless, close to one-third of the yearly diet came from just 3 plant genera—Inga, Ficus, and Spondias—and only 20 genera each contributed to 1% of the diet. For one study group, the proportion of ripe fruit in the diet each month was correlated with the habitat-wide availability of this resource, a pattern evidenced by several other ateline species. However, the relationship was not apparent in the second study group. The modal party size for feeding bouts on all food types was a single monkey, and, contrary to reports for other atelines, neither feeding party size nor the total number of feeding minutes that groups spent in food patches was well predicted by patch size. Both results highlight the independent nature of woolly monkey foraging. Given that woolly monkeys and closely-related spider monkeys focus so heavily on ripe fruits, their very different patterns of social organization are intriguing and raise the question of just how their ecological strategies differ. Two important differences appear to be in the use of animal prey and in the phytochemical composition of the ripe fruits that they consume: spider monkeys rarely forage for animal prey, and woolly monkeys seldom consume the lipid-rich fruits that are an important part of spider monkey diets.     

Geophagy in brown spider monkeys (Ateles hybridus) in a lowland tropical rainforest in Colombia

Spider monkeys and howler monkeys are the only Neotropical primates that eat soil from mineral licks. Not all species within these genera visit mineral licks, and geophagy has been restricted to populations of Ateles belzebuth belzebuth,Ateles belzebuth chamek and Alouatta seniculus in western Amazonian rainforests. With the aid of a camera trap we studied the visitation patterns of a group of brown spider monkeys (Ateles hybridus) to a mineral lick at Serrania de Las Quinchas, in Colombia. Spider monkeys visited the lick frequently throughout the year, with a monthly average of 21.7 ± 7.2 visits per 100 days of camera trapping (n = 14 months). Spider monkeys visited the mineral lick almost always on days with no rain, or very little (<3 mm) rain, suggesting that proximate environmental variables might determine spider monkeys' decisions to come to the ground at the licks. This study expands the geographical occurrence of mineral lick use by spider monkeys providing additional data for future assessments on the biogeographical correlates of mineral lick use by platyrrhines.     

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.     

Diet of the Critically Endangered Brown Spider Monkey (Ateles hybridus) in an Inter‐Andean Lowland Rainforest in Colombia

Brown spider monkeys (Ateles hybridus) are one of the least known and more threatened primates in the Neotropics. Recognized as a species about a decade ago, field studies on these endangered primates have mainly focused on estimating local population densities. Since 2006, we habituated a group of wild brown spider monkeys at Serranía de Las Quinchas, Colombia, and studied their feeding ecology during 2.5 years using focal “subgroup” sampling, and conducted phenological surveys in order to estimate habitat‐wide fruit availability. Based on 847 hr of behavioral follows, brown spider monkeys spent approximately 25% of their time in feeding activities, and fed from fruits and leaves on at least 123 plant species. Ripe fruits were the most important item in the diet of A. hybridus at Las Quinchas comprising 92% of their feeding time. Probably due to the minor variation in the monthly proportion of fruits in brown spider monkey's diet throughout this study, there was no relation between habitat‐wide fruit availability and the proportion of fruit included in their monthly diet. The diet of brown spider monkeys at Las Quinchas is toward the high end of fruit intake, even within other wild spider monkeys’ populations, suggesting that these endangered primates might also be facing the challenges of being a large bodied fruit specialist under a regional scenario of habitat loss and fragmentation. Am. J. Primatol. 74:1097‐1105, 2012. © 2012 Wiley Periodicals, Inc.     

Tool use in wild spider monkeys (<Emphasis Type="Italic">Ateles geoffroyi</Emphasis>)

Tool use has been observed in a variety of primate species, including both New and Old World monkeys. However, such reports mainly address the most prodigious tool users and frequently limit discussions of tool-using behavior to a foraging framework. Here, we present observations of novel and spontaneous tool use in wild black-handed spider monkeys (Ateles geoffroyi), where female spider monkeys used detached sticks in a self-directed manner. We introduce factors to explain Ateles tool-using abilities and limitations, and encourage the synthesis of relevant research in order to gain insight into the cognitive abilities of spider monkeys and the evolution of tool-using behaviors in primates.     

Ranging behavior and foraging ecology of lowland woolly monkeys (Lagothrix lagotricha poeppigii) in Yasuní National Park,Ecuador

In a year-long study, I investigated the ranging behavior of lowland woolly monkeys (Lagothrix lagotricha poeppigii) in a terra firma rainforest in Yasuní National Park, Ecuador, and examined the relationship between ranging, diet, food availability, and food patch use for this population. In Yasuní the total home range sizes for two social groups were 124 and 108 ha, which are much smaller than has been reported previously for Lagothrix elsewhere in its geographic distribution. The mean yearly day range estimates for these same groups were 1,792 m and 1,878 m, which are well within the range of variation previously reported. Ranging behavior was not correlated with the current habitat-wide abundance of ripe fruit, which comprises 76.3% of the yearly diet for this population, but was associated with one measure of likely insect prey abundance and with the availability of immature fruits, a minimal part of the diet. Specifically, one study group moved significantly greater distances during months of high likely insect prey abundance and when immature fruits were abundant. The second study group also traveled farther when likely insect prey abundance was high and when immature fruits were abundant, although the latter relationship only approached significance. This group also devoted significantly more of its daily activity budget to travel during these times. These results indicate that variation in ripe fruit abundance makes no meaningful contribution to explaining variation in ranging behavior for this population of woolly monkeys. Instead, the results raise the possibility that some aspects of the ranging behavior of frugivorous primates may be related to the availability of alternative food sources, such as animal prey, or to monitoring the phenological status of important fruit trees, rather than simply reflecting the degree of intragroup feeding competition.     

Costs of twins in free-ranging white-bellied spider monkeys (Ateles belzebuth belzebuth) at Tinigua National Park, Colombia

A female spider monkey (Ateles belzebuth belzebuth) that gave birth to twins was studied during 13 months, and her activity budget and diet were compared to those of females with single offspring and females with no offspring to assess selective pressures that could influence litter size. We recorded qualitative information on the development and social interactions of the twins and three other single infants. Emi, the female that had the twins, had the highest proportion of resting time and the lowest proportion of feeding and moving time compared to other adult females and males. Emi also had the lowest average daily travel distance and relied more heavily on flowers and leaves than other group members who included a higher proportion of fruits in their diets. These results suggest that twins are energetically costly to spider monkeys because of the direct energy allocated into raising and carrying the twins and, also, because these costs have direct effects in the ability of a mother to obtain high-quality resources (e.g., fruits). The twins had a slower rate of physical and social development as well as a smaller body size compared to same-aged singletons by the end of the study. Thus, the extended periods of maternal care and the costs associated with rearing and carrying offspring are some of the factors that influence the evolution and maintenance of a litter size of one in most anthropoid primates.     

Locomotor behavior of Lagothrix lagothricha and Ateles belzebuth in Yasuní National Park, Ecuador: general patterns and nonsuspensory modes.

Field study of the locomotor behavior of sympatric woolly monkeys (Lagothrix lagothricha) and spider monkeys (Ateles belzebuth) in undisturbed rainforest of northern Ecuador revealed similar patterns in use of plant forms (categorized tree and liana structure), and substantial differences in the frequencies of use of different grouped modes (aggregates of kinematically similar specific modes). Lagothrix progressed more than Ateles by leaping/dropping and quadrupedal walking/running, whereas Ateles exhibited more suspensory locomotion. Grouped modes are associated with different plant forms in similar ways in the two species. In contrast, the species differed in use of tree zone (trunk/bole, major branches, intermediate branches, and terminal branches), with Lagothrix using intermediate branches and Ateles terminal branches more. Correlated with this difference was greater use by Lagothrix of quadrupedal movement, especially on intermediate branches, and greater use of suspensory modes by Ateles, especially in the terminal zone. Further research is needed to determine how these patterns are facilitated and constrained by morphological mechanisms. Analysis of specific locomotor modes within groups shows several interspecific differences in relative frequencies.     

Suspensory locomotion of Lagothrix lagothricha and Ateles belzebuth in Yasuní National Park,Ecuador

A comparative field study of the locomotion of woolly monkeys (Lagothrix lagothricha) and spider monkeys (Ateles belzebuth) in undisturbed rainforest of northeastern Ecuador reveals substantial differences in their use of suspensory modes. Ateles performed both more brachiation (by forelimbs and tail, with trunk rotation), and forelimb swing (similar to brachiation, but without trunk rotation) than Lagothrix. In contrast, in Lagothrix 20% of suspensory movement was by pronograde forelimb swing, which resembles forelimb swing except that the body is held in a pronograde orientation due to the tail and/or feet intermittently grasping behind the trailing forelimb. Ateles never exhibited this mode. Both brachiation and forelimb swing by Ateles were more dynamic than in Lagothrix, consisting of higher proportions of full-stride bouts (versus single-step). Both species used smaller supports for suspensory than for quadrupedal locomotion, and Ateles used both smaller and larger supports for suspension than did Lagothrix. Analysis of support inclination shows that both species tended to perform more above-support movement on horizontal supports and more below-support (suspensory) movement from oblique supports. Our attempt to elucidate the aspects of canopy structure that favor suspension suggests the need for additional kinds of observational data, focusing on the "immediate structural context" of positional events.     

Male and female range use in a group of white‐bellied spider monkeys (Ateles belzebuth) in Yasuní National Park,Ecuador

Spider monkeys (Ateles sp.) live in a flexible fission–fusion social system in which members of a social group are not in constant association, but instead form smaller subgroups of varying size and composition. Patterns of range use in spider monkeys have been described as sex‐segregated, with males and females often ranging separately, females utilizing core areas that encompass only a fraction of the entire community range, and males using much larger portions of the community range that overlap considerably with the core areas of females and other males. Males are also reported to use the boundary areas of community home ranges more often than females. Spider monkeys thus seem to parallel the “male‐bonded” patterns of ranging and association found among some groups of chimpanzees. Over several years of research on one group of spider monkeys (Ateles belzebuth) in Yasuní National Park, Ecuador, we characterized the ranging patterns of adult males and females and evaluated the extent to which they conform to previously reported patterns. In contrast to ranging patterns seen at several other spider monkey sites, the ranges of our study females overlapped considerably, with little evidence of exclusive use of particular areas by individual monkeys. Average male and female home range size was comparable, and males and females were similar in their use of boundary areas. These ranging patterns are similar to those of “bisexually bonded” groups of chimpanzees in West Africa. We suggest that the less sex‐segregated ranging patterns seen in this particular group of spider monkeys may be owing to a history of human disturbance in the area and to lower genetic relatedness between males, highlighting the potential for flexibility some aspects of the spider monkeys' fission–fusion social system. Am. J. Primatol. 72:129–141, 2010. © 2009 Wiley‐Liss, Inc.     

Nuclear DNA variation in spider monkeys (Ateles)

Phylogenetic relationships based on DNA sequence variation for the aldolase A intron V nuclear genomic region were evaluated and compared to phylogenies based on mitochondrial DNA sequence variation among spider monkeys (Ateles). Samples of Ateles ranging from Central America throughout the Amazon Basin were sequenced to determine phylogenetic relationships among geographically widely distributed populations. Analysis of nuclear DNA sequences using parsimony, maximum-likelihood, and genetic distance analyses produced similar phylogenies. Four previously proposed monophyletic species of spider monkeys were: (1) Ateles paniscus, composed of haplotypes from the northeastern Amazon Basin; (2) A. belzebuth, found in the western and southern Amazon Basin; (3) A. hybridus, located primarily along the Magdalena River valley of Colombia; and (4) A. geoffroyi, including all haplotypes found in the Choco region of South America and throughout Central America. The nuclear phylograms were analyzed based on associated bootstrap support and confidence probabilities. Support from the nuclear DNA genome was less robust than support from the mitochondrial DNA data, most likely due to a level of sequence variation, which was 90% less than that of the mitochondrial DNA genome. Nuclear DNA congruencies with mitochondrial DNA-based phylogenies, as supported by the incongruence length difference and winning sites tests, provide further support for the suggested revisions in Ateles taxonomy that are contradictory to long-held taxonomies based on pelage variation.     

Patterns of mineral lick visitation by spider monkeys and howler monkeys in Amazonia: are licks perceived as risky areas?

Mineral licks--also known as "salados," "saladeros," or "collpas"--are specific sites in tropical and temperate ecosystems where a large diversity of mammals and birds come regularly to feed on soil. Although the reasons for vertebrate geophagy are not completely understood, animals are argued to obtain a variety of nutritional and health benefits from the ingestion of soil at mineral licks. We studied the temporal patterns of mineral lick use by white-bellied spider monkey (Ateles belzebuth) and red howler monkey (Alouatta seniculus) in a lowland rain forest in Amazonian Ecuador. Using camera and video traps at four different mineral licks, combined with behavioral follows of one group of spider monkeys, we documented rates of mineral lick visitation by both primate species and the relative frequency and intensity of mineral lick use by spider monkeys. On the basis of 1,612 days and 888 nights of mineral lick monitoring, we found that A. belzebuth and A. seniculus both visit mineral licks frequently throughout the year (on average ～14% of days for both species), and mineral lick visitation was influenced by short-term environmental conditions (e.g. sunny and dry weather). For spider monkeys, the area surrounding the lick was also the most frequently and most intensively used region within the group's home range. The fact that spider monkeys spent long periods at the lick area before coming to the ground to obtain soil, and the fact that both species visited the lick preferentially during dry sunny conditions (when predator detectability is presumed to be relatively high) and visited simultaneously more often than expected by chance, together suggest that licks are indeed perceived as risky areas by these primates. We suggest that howler and spider monkeys employ behavioral strategies aimed at minimizing the probability of predation while visiting the forest floor at risky mineral lick sites.     

Ecological constraints on group size in three species of neotropical primates

The foraging strategies and association patterns of 3 species of primates (Ateles geoffroyi, Alouatta palliata, Cebus capucinus) were studied over a 5-year period. The objective of the study was to provide a quantitative test of the hypothesis that the size, density and distribution of food resources influence the size of animal groups. In examining the assumptions of this hypothesis, it was shown that these primates used resources that occurred in patches, depleted the patches through their use, and that membership in large subgroups was associated with increased travel costs. The howler and spider monkey groups formed subgroups, the size of which could be predicted from the size, density and distribution of their plant food resources. When resources were clumped and at a low density, both the howler and spider monkeys were found in small subgroups, whereas when patches were uniformly distributed and at high density they formed larger subgroups. Capuchin monkeys, in contrast, did not respond to changes in these ecological variables by forming subgroups or changing the cohesion of their group.     

The Influence of Feeding Patch Size and Relative Fruit Density on the Foraging Behavior of the Black Spider Monkey Ateles chamek

Black spider monkey Ateles chamek foraging data from eastern Bolivia are examined in relation to the size of fruit patches and the relative fruit density within the patch. In general, spider monkeys exhibited a preference for larger fruit patches and foraged for longer and in larger subgroups as patch size and relative fruit density increased. Nevertheless, results for specific resources revealed considerable variation in the primary variables influencing foraging behavior and subgroup size with certain specific resources more influenced by patch size, and others more influenced by relative fruit density. The results are discussed in relation to the foraging ecology of fission–fusion primate social systems and previous studies on the influence of patch size on primate foraging decisions.     

Gustatory Responsiveness to food-associated acids in the spider monkey (Ateles geoffroyi)

The gustatory responsiveness of four adult spider monkeys to five food-associated acids was assessed in two-bottle preference tests of brief duration (3 min). The animals were given the choice between a 30 mM sucrose solution and defined concentrations of citric acid, ascorbic acid, malic acid, acetic acid, or tannic acid dissolved in a 30 mM sucrose solution. With this procedure,Ateles geoffroyi was found to significantly discriminate concentrations as low as 5 mM ascorbic acid, citric acid, and acetic acid, 10 mM malic acid, and 0.1 mM tannic acid from the alternative stimulus. With the latter two substances, the monkeys rejected all suprathreshold concentrations tested, whereas with the former three substances, the animals showed an inverted U-shaped function of preference, i.e. they rejected high concentrations, but significantly preferred low but detectable concentrations of these acidic tastants over the alternative sweet stimulus. The results showed (1) the spider monkey to respond to the same range of acid concentrations as other nonhuman primate species; (2) thatAteles geoffroyi, is able to detect food-associated acids at concentrations well below those present in most fruits; and (3) that unlike most other primate species tested so far, spider monkeys do not generally reject acidic tastants but show a substanceand concentration-dependent change in responsiveness that may range from rejection to preference. The results support the assumptions that spider monkeys may use sourness and/or astringency of food-associated acids as a criterion for food selection, and that the gustatory responsiveness ofAteles geoffroyi to acidic tastants might reflect an evolutionary adaptation to frugivory.     

Intra-community infanticide and forced copulation in spider monkeys: a multi-site comparison between Cocha Cashu, Peru and Punta Laguna, Mexico

We describe two cases of infanticide, two suspected infanticides, and a forced copulation by familiar resident males in two populations of wild spider monkeys (Ateles belzebuth chamek and A. geoffroyi yucatanensis). These are the first known infanticides and forced copulation in spider monkeys. Data were gathered from four neighboring communities of spider monkeys in Manu National Park at the Cocha Cashu Biological Station, Peru and two communities in the Otoch Ma'ax Yetel Kooh Reserve at Punta Laguna, Mexico, during intensive field studies of over 2,000 hr each. These are rare behaviors, but results suggest that mating history and sexual coercion are important in spider monkey social relationships.     

Diets of some French guianan primates: Food composition and food choices

We studied food choices of black spider monkeys (Ateles paniscus) and red howlers (Alouatta seniculus) in an undisturbed tropical forest of French Guiana for 6 months in the rainy season. We made additional observations on tufted capuchins (Cebus apella) and examined the differences and similarities in feeding behavior with respect to the plant specific composition of the habitat and the biochemical characteristics of their food. Capuchins and spider monkeys mainly fed on ripe fruit pulp, to which they added invertebrates (capuchins) or young leaves (spider monkeys); their plant diet was more varied than that of howlers, which contained approximately equal proportions of ripe fruits and young leaves of many species, with large monthly variations in these food categories. BothAteles andAlouatta tended to feed preferentially on abundant plant species, with a large overlap in their fruit choices. The former species included a high proportion of soluble sugars and a low proportion of protein in its diet compared, to howlers. Leaves of several species selected byAlouatta reacted positively when screened for alkaloids and phenolic compounds. Besides specific metabolic requirements and adaptations to deriving nutrients from distinct food types, we hypothesize that the ability to taste sugars, which varies among primates, affects the range of foods appearing to be palatable and, consequently, contributes to the differentiation of feeding niches.     

Seasonal Variations in Diet and Foraging Behavior of <Emphasis Type="Italic">Ateles chamek</Emphasis> in a Southern Amazonian Tropical Forest

I present data regarding the diet and feeding ecology of a spider monkey community at Lago Caiman in northeastern Bolivia. The community was highly frugivorous, only consuming significant amounts of folivorous material during times of relative fruit resource scarcity. Spider monkeys fed on parts of 86 plant species, but the majority of the diet comprised a few dominant fleshy fruit species that were available at temporally distinct periods across the year. Accordingly, I identified candidate keystone resources for the region and discuss the results with reference to previous studies on Ateles and the importance of considering keystone fruit resources in the management of forestry concessions.