Low Levels of Fruit Nitrogen as Drivers for the Evolution of Madagascar's Primate Communities.

The uneven representation of frugivorous mammals and birds across tropical regions - high in the New World, low in Madagascar and intermediate in Africa and Asia - represents a long-standing enigma in ecology. Several hypotheses have been proposed to explain these differences but the ultimate drivers remain unclear. Here, we tested the hypothesis that fruits in Madagascar contain insufficient nitrogen to meet primate metabolic requirements, thus constraining the evolution of frugivory. We performed a global analysis of nitrogen in fruits consumed by primates, as collated from 79 studies. Our results showed that average frugivory among lemur communities was lower compared to New World and Asian-African primate communities. Fruits in Madagascar contain lower average nitrogen than those in the New World and Old World. Nitrogen content in the overall diets of primate species did not differ significantly between major taxonomic radiations. There is no relationship between fruit protein and the degree of frugivory among primates either globally or within regions, with the exception of Madagascar. This suggests that low protein availability in fruits influences current lemur communities to select for protein from other sources, whereas in the New World and Old World other factors are more significant in shaping primate communities.

Social and personal information use by squirrel monkeys in assessing predation risk.

The threat of predation can significantly influence prey behaviors through altered perceptions of risk. Prey risk perception is constantly updated via collection of personal and social information about predators. Better understanding of the links between information availability, its use, and prey species' perception of risk will aid in explaining how animals adapt to predation. The goal of this study was to determine the environmental and social cues-available to prey via personal and social information, respectively-that influence wild squirrel monkey (Saimiri sciureus) reactivity to potential predators, treated here as a proxy for risk perception. We followed squirrel monkey troops for 3 years in Suriname, South America, and accounted for environmental and social variables associated with potential predator encounters. We utilized logistic regression models applied to a robust and long-term data set to reveal relationships among factors affecting squirrel monkey anti-predator responses. Our analyses revealed that height, season, type of predator stimulus, and mixed-species associations with capuchin monkeys (Sapajus apella) were highly related to intensity of squirrel monkey anti-predator responses. Moreover, our analyses revealed that squirrel monkeys overestimate the immediate threat of predation when individuals have incomplete information regarding the potential predator.

Primates in 21st century ecosystems: does primate conservation promote ecosystem conservation?

Contributors to this issue of the American Journal of Primatology were among the participants in an invited symposium at the 2008 Association for Tropical Biology and Conservation meeting in Paramaribo, Suriname. They were asked to assess how essential primates are to tropical ecosystems and, given their research interests, discuss how primate research contributes to the broader understanding about how ecosystems function. This introduction to the issue is divided into three parts: a review of the roles that nonhuman primates play in tropical ecosystems; the implementation of large-scale landscape methods used to identify primate densities; and concerns about the increasingly porous boundaries between humans, nonhuman primates, and pathogens. Although 20th century primate research created a rich database on individual species, including both theoretical and descriptive approaches, the dual effects of high human population densities and widespread habitat destruction should warn us that creative, interdisciplinary and human-related research is needed to solve 21st century problems.

The ontogeny of handling hard-to-process food in wild brown capuchins (Cebus apella apella): evidence from foraging on the fruit of Maximiliana maripa.

We examined age-related differences in wild brown capuchins' foraging efficiency and the food-processing behaviors directed toward maripa palm fruit (Maximiliana maripa). A detailed comparison of the different foraging techniques showed that plucking the fruit from the infructescence constituted the main difficulty of this task. Foraging efficiency tended to increase with age, with a threshold at which sufficient strength allowed immatures by the age of three to reach adult-level efficiency. Youngsters spent more time than older individuals browsing the infructescence and pulling the fruit in an attempt to harvest it. Infants tried to compensate for their inability to pluck fruit by adopting alternative strategies but with low payback, such as gnawing unplucked fruit and opportunistically scrounging others' partially processed food. Although around 2 years of age, young capuchins exhibited all of the behaviors used by adults, they did not reach adult-level proficiency at feeding on maripa until about 3 years (older juveniles). We compared this developmental pattern with that of extractive foraging on beetle larvae (Myelobia sp.) hidden in bamboo stalks, a more difficult food for these monkeys [Gunst N, Boinski S, Fragaszy DM. Behaviour 145:195-229, 2008]. For maripa, the challenge was mainly physical (plucking the fruit) once a tree was encountered, whereas for larvae, the challenge was primarily perceptual (locating the hidden larvae). For both foods, capuchins practice for years before achieving adult-level foraging competence, and the timeline is extended for larvae foraging (until 6 years) compared with maripa (3 years). The differing combinations of opportunities and challenges for learning to forage on these different foods illustrate how young generalist foragers (i.e. exploiting a large number of animal and plant species) may compensate for their low efficiency in extractive foraging tasks by showing earlier competence in processing less difficult but nutritious foods, such as maripa fruit.

Development of skilled detection and extraction of embedded prey by wild brown capuchin monkeys (Cebus apella apella).

Brown capuchin monkeys (Cebus apella apella) in Suriname forage on larvae enclosed within healthy bamboo stalks. We applied the searching versus handling dichotomy of optimal foraging models to highlight developmental processes contributing to foraging on embedded prey. Larvae acquisition begins with search; selecting an appropriate stalk and locating the embedded larvae; followed by handling, ripping the stalk open, and extracting the larvae. Although extraction behaviors were present at low rates in infant capuchins' repertoire, we found that the acquisition of adequate detection techniques was fully completed in subadults, aged around 6. Selecting appropriate foraging substrates, requiring accurate assessment of the physical properties of bamboo stalks, gradually increased with age and experience. We showed that both components of searching required extended practice beyond that required to master the handling components. We conclude that the developmental sequence of skill acquisition goes counter to the preceding logical sequence of foraging process and suggest that searching components present greater challenges than handling components in extractive foraging. Specifying the searching components of foraging more precisely will enhance understanding of species variation in the developmental schedule of foraging skills.

Possible fruit protein effects on primate communities in madagascar and the neotropics.

BACKGROUND: The ecological factors contributing to the evolution of tropical vertebrate communities are still poorly understood. Primate communities of the tropical Americas have fewer folivorous but more frugivorous genera than tropical regions of the Old World and especially many more frugivorous genera than Madagascar. Reasons for this phenomenon are largely unexplored. We developed the hypothesis that Neotropical fruits have higher protein concentrations than fruits from Madagascar and that the higher representation of frugivorous genera in the Neotropics is linked to high protein concentrations in fruits. Low fruit protein concentrations in Madagascar would restrict the evolution of frugivores in Malagasy communities. METHODOLOGY/PRINCIPAL FINDINGS: We reviewed the literature for nitrogen concentrations in fruits from the Neotropics and from Madagascar, and analyzed fruits from an additional six sites in the Neotropics and six sites in Madagascar. Fruits from the Neotropical sites contain significantly more nitrogen than fruits from the Madagascar sites. Nitrogen concentrations in New World fruits are above the concentrations to satisfy nitrogen requirements of primates, while they are at the lower end or below the concentrations to cover primate protein needs in Madagascar. CONCLUSIONS/SIGNIFICANCE: Fruits at most sites in the Neotropics contain enough protein to satisfy the protein needs of primates. Thus, selection pressure to develop new adaptations for foods that are difficult to digest (such as leaves) may have been lower in the Neotropics than in Madagascar. The low nitrogen concentrations in fruits from Madagascar may contribute to the almost complete absence of frugivorous primate species on this island.

Allelic variation in the squirrel monkey x-linked color vision gene: biogeographical and behavioral correlates.

Most Neotropical primate species possess a polymorphic X-linked and a monomorphic autosomal color vision gene. Consequently, populations are composed of both dichromatics and trichromatics. Most theories on the maintenance of this genetic system revolve around possible advantages for foraging ecology. To examine the issue from a different angle, we compared the numbers and relative frequencies of alleles at the X-linked locus among three species of Saimiri representing a wide range of geographical and behavioral variation in the genus. Exons 3, 4, and 5 of the X-linked opsin gene were sequenced for a large number of X chromosomes for all three species. Several synonymous mutations were detected in exons 4 and 5 for the originally reported alleles but only a single nonsynonymous change was detected. Two alleles were found that appeared to be the result of recombination events. The low occurrence of recombinant alleles and absence of mutations in the amino acids critical for spectral tuning indicates that stabilizing selection acts to maintain the combinations of critical sites specific to each allele. Allele frequencies were approximately the same for all Saimiri species, with a slight but significant difference between S. boliviensis and S. oerstedii. No apparent correlation exists between allele frequencies and behavioral or biogeographical differences between species, casting doubt on the speculation that the spectral sensitivities of the alleles have been maintained because they are specifically well-tuned to Saimiri visual ecology. Rather, the spectral tuning peaks might have been maintained because they are as widely spaced as possible within the limited range of middlewave to longwave spectra useful to all primates. This arrangement creates a balance between maximizing the distance between spectral tuning peaks (allowing the color opponency of the visual system to distinguish between peaks) and maximizing the number of alleles within a limited range (yielding the greatest possible frequency of heterozygotes).

Patterns of individual diet choice and efficiency of foraging in wedge-capped capuchin monkeys (Cebus olivaceus).

Capuchin monkeys (Cebus olivaceus) exhibit extensive intragroup variability in foraging and diet. To consider how age, sex, and individual identity contribute to this variability, the authors examined foraging and diet in 18 wedge-capped capuchin monkeys in 1 social group in the wild. Age-sex classes did not differ in the time spent ingesting food, the reliance on plant foods, the foraging actions used or substrates exploited, or in the efficiency of exploiting animal foods. They did differ, however, in the time spent finding food, time devoted to animal foods and to vigorous foraging, and the efficiency of foraging. The sexes differed more than age groups. Individual differences within age-sex class were less extensive than expected and were more evident in juveniles than adults. Within-group variability in foraging reflected catholic selection and equivalent treatment of substrates by all individuals, rather than individual specializations.

Interleukin-1 induces sleep-like behavior and alters call structure in juvenile rhesus macaques.

To date, there have been no investigations of the behavioral effects of interleukin-1 (IL-1) in nonhuman primates. In this study the locomotor behavior and vocalizations of juvenile rhesus monkeys were monitored for 45 minutes following intravenous injections of recombinant human IL-1 alpha. In addition, their reaction to a broadcasted recording of infant monkey distress calls was determined 20 minutes after the beginning of each test session. IL-1 induced sleep-like inactivity and significantly diminished the monkey's behavioral and vocal responses to the broadcasted calls. The coo calls uttered by the monkeys following IL-1 treatment also had a longer duration and lower fundamental frequency than calls during the control condition. As several studies have indicated that behavioral effects of IL-1 may be mediated by corticotropin-releasing hormone (CRH), a second group of rhesus monkeys was given injections of CRH. CRH did not alter behavior or call structure at the dose administered. These results extend previous research on the behavioral effects of IL-1 to include the nonhuman primate and provide the first evidence that cytokines can affect vocal communication in rhesus monkeys. © 1995 Wiley-Liss, Inc.

Wild squirrel monkey (Saimiri sciureus) "caregiver" calls: Contexts and acoustic structure.

A field study of the vocal behavior of 22 wild adult female squirrel monkeys (Saimiri sciureus) in Parque Nacional del Manu, Peru, found that 21% of vocalizations were "caregiver" calls. Caregiver calls are brief, low frequency calls, often with numerous harmonics, that are addressed by caregivers to their own infants in three contexts: 1) prenurse, signalling the caregiver's location and willingness to nurse; 2) nurse, while nursing; and 3) end nurse, indicating the end of the nursing bout. Three measures (start, end, and peak frequency) of the acoustic structure of the fundamental frequency of the caregiver calls significantly differed across the contexts. Duration of caregiver calls, however, was not distinguished by context. Compared to other primate taxa, the specificity and importance of caregiver calls in squirrel monkey vocal behavior appears unusual, if not unique. That S. sciureus caregiver calls are highly developed and employed so extensively probably follows from an unusual combination of ecological and life history factors. These factors include delayed weaning and large infant body size, high levels of indirect foraging competition which encourages spatial separation, susceptibility to predation, and specialization on a densely foliated, branch-end microhabitat in which visual contact is often impeded. © 1995 Wiley-Liss, Inc.

Temperament in nonhuman primates.

Formerly applied to studies of responsivity in children, in more recent years the concept of temperament has been applied to nonhuman primates at the individual, species, and now population levels. While the concepts of temperament and personality have been less distinguished in nonhuman primate studies than in the human literature, temperamental and personality differences have now been identified among individual primates and among primate species in a number of studies. At the individual level, certain temperamental characteristics have been associated with age, sex, and most frequently rank. At the species level, temperamental profiles have been linked to intraspecific differences in social systems, sociodemographics, and features of life history and ecology. In this report we discuss the application of the temperament concept to nonhuman primates and review findings from studies of primate temperament at the individual, population, and species level. We also cite evidence for genetic and experiential influences on temperament in primates, outline concepts related to possible evolutionary influences on temperament, and discuss the possible relation of temperamental characteristics to social behavior and ecology in selected species. © 1995 Wiley-Liss, Inc.

Male residence and association patterns in Costa Rican squirrel monkeys (Saimiri oerstedi).

A model is developed to interpret the evolution of the unusual pattern of male residence and social structure in the Costa Rican squirrel monkey (Saimiri oerstedi). Observations of a wild population document that males 1) maintain close spatial and social associations with other males, especially other males in their birth cohort, but not females and infants; 2) exhibit negligible within-troop male-male aggression, high levels of antipredator vigilance, and frequent predator deterrence; 3) cooperate in aggressive olfactory investigation of females; and 4) maintain residence in their natal troop with their male birth cohort, eventually succeeding to reproductive positions in their natal troop. Less commonly, male age-cohorts leave the troop well past reproductive maturity and usurp the reproductive male cohort in another troop. We suggest that this divergence from the social structure typical of male squirrel monkeys in Peru (males transient between troops, weak male-male bonds, high within-troop male aggression, little investment in anti-predator behavior) arose because female S. oerstedi in Costa Rica are not philopatric. In Costa Rica, long term reproductive cooperation is likely advantageous to males, because of the frequent movement of female S. oerstedi between troops; the potential costs of inbreeding are reduced. Male S. oerstedi of all ages residing in the same troop, but especially those of the same age cohort, are predicted to have a much higher degree of genetic relatedness than adult females. © 1994 Wiley-Liss, Inc. This article is a US Government work and, as such, is in the public domain in the United States of America.

Vocal coordination of troop movement among white-faced capuchin monkeys, Cebus capucinus.

Coordinated travel by social groups is well documented, often with evidence that cognitive spatial maps are employed. Yet the mechanisms by which movement decisions are made and implemented within social groups are poorly known. In a field study of white-faced capuchin monkeys in Costa Rica it was demonstrated that a specific call, the "trill," is used by adults in the initiation and directing of troop movement. The trills of subadults were restricted to vocal exchanges with other subadults. Continuous vocal recordings were collected of the vocalizations of the 14 members of the study troop. A cumulative 33.7 h of continuous samples and 1,892 sonagrams were analyzed. In addition to vocalizations clearly associated with alarm, distress, or agonistic contexts, two distinct call types were identified, trills and huhs. Age-sex classes differed in the rate at which both types of calls were produced in different spatial positions within the troop. Adult females and males produced higher rates of trills when in the leading edge compared to all other spatial positions in a traveling troop. Trills at the edge of a stationary troop represented 36 "successful" and 3 "unsuccessful" start attempts; the troop usually moved in the trajectory predicted by a trilling adult's location on the troop periphery within 10 min of the initiation of trilling. Adults also altered the trajectory of traveling troops by trilling at the side and back of the troop (10 "successful" and 4 "unsuccessful" attempts). Huh vocalizations were most predictably produced when a capuchin is in a dense fruit patch. These results emphasize the role vocalizations serve in the coordination and trajectory of group movement in nonhuman primates, especially those populations that are arboreal or in which visual contact is otherwise impeded. © 1993 Wiley-Liss, Inc. This article is a US Government work and, as such, is in the public domain in the United States of America.

Predation by squirrel monkeys and double-toothed kites on tent-making bats.

Central American squirrel monkeys (Saimiri oerstedi) appear to recognize the modified leaves that phyllostomid bats utilize for diurnal roost sites. The monkeys visually and manually search these bat tents for both bats and insects. Adult males are the most successful at capturing bats. Nonvolant juvenile bats are more vulnerable to monkey predation than are adults. Bats that escape monkey predation frequently are captured by doubletoothed kites (Harpagus bidentatus) that tend foraging troops of monkeys. Predation by squirrel monkeys, coupled with that of double-toothed kites, may be a significant source of mortality for tent-making bats.