Trait variation and trait stability in common marmosets (Callithrix jacchus) inhabiting ecologically distinct habitats in northeastern Brazil.

Understanding the set of factors that promote and constrain a species' ability to exploit ecologically distinct habitats is central for addressing questions of intraspecific variability in behavior and morphology. In this study, we compared newly collected data with published data on body measurements, group size and composition, daily path length, home range, and reproductive output in wild common marmosets naturally inhabiting two contrasting environments in northeastern Brazil: the Atlantic Forest (AF), which is characterized by high biodiversity and reduced seasonality in food availability and the Caatinga (CAT), which is characterized by a severe hot and dry season lasting from 5 to 11 months, drought-resistant plant species, and reduced primary productivity. Despite marked differences in ecological conditions, CAT marmosets and AF marmosets differed minimally in daily path length, home range, reproductive output, and infant survivorship. CAT marmosets were found to live in smaller groups containing fewer adult females than AF marmosets, and also were characterized by a greater surface area to body mass ratio, a trait that may represent an adaptation to the hot and dry conditions of the Caatinga. We propose that in conjunction with body mass reduction, minor adjustments in behavior, the exploitation of cacti as a source of water and nutrients, and access to exudates as a dependable year-round food resource, common marmosets successfully used the same adaptive pattern to maintain high reproductive output and infant survivorship in exploiting these two ecologically distinct environments.

Balancing contest competition, scramble competition, and social tolerance at feeding sites in wild common marmosets (Callithrix jacchus).

Models of primate sociality focus on the costs and benefits of group living and how factors such as rank, feeding competition, alliance formation, and cooperative behavior shape within-group social relationships. We conducted a series of controlled field experiments designed to investigate how resource distribution (one or three of four reward platforms) and amount of food on a reward platform affected foraging strategies and individual feeding success in four groups of wild common marmosets (Callithrix jacchus) living in the Caatinga of northeastern Brazil. At our field site, common marmoset groups are characterized by a single breeding female who can produce twin litters twice per year, strong social cohesion, and cooperative infant care provided principally by several adult male helpers. We found that except for the dominant breeding female, rank (based on aggression) was not a strong predictor of feeding success. Although the breeding female in each group occupied the highest rank position and obtained the greatest daily feeding success, all other group members, including adults and juveniles experienced relatively equal feeding success across most experimental conditions. This was accomplished using a balance of behavioral strategies related to contest competition, scramble competition (associated with a finder's advantage), and social tolerance (sharing the same feeding platform). Based on these results, the social structure of common marmosets is best described as "single female dominance," with the breeding female maximizing food intake needed to offset the energetic costs associated with reproductive twinning and the ability to produce two litters per year. Cooperative infant caregiving, in which the number of helpers is positively correlated with offspring survivorship, requires a set of behavioral strategies that serve to reduce contest competition and promote prosocial behaviors at feeding sites.

Should I store, or should I sync? The breeding strategy of two small Neotropical primates under predictable resource availability.

Primates employ many strategies to deal with the costs of reproduction. While income breeders exploit the food available in their environment during lactation, the most costly phase of reproduction, capital breeders tend to store energy for use in the period. We analyzed the relationship between resource availability and lactation in Callicebus coimbrai (n = 2 groups) and Callicebus nigrifrons (n = 2 groups) in four Brazilian Atlantic forest remnants, to assess their breeding strategy. We recorded the occurrence of births and breastfeeding events to assess birth seasonality and lactation period and length while monitoring monthly fruit availability. We recorded 11 births (five for C. coimbrai, and six for C. nigrifrons), all restricted to the end of the lean season and the beginning of the rich season. Lactation coincided with periods of increased fruit availability. We suggest that the breeding pattern of Callicebus coimbrai and C. nigrifrons is compatible with an income-based breeding strategy.

Duetting Patterns of Titi Monkeys (Primates, Pitheciidae: Callicebinae) and Relationships with Phylogeny.

Long-range vocal communication in socially monogamous titi monkeys is mediated by the production of loud, advertising calls in the form of solos, duets, and choruses. We conducted a power spectral analysis of duets and choruses (simply "duets" hereafter) followed by linear discriminant analysis using three acoustic parameters-dominant frequency of the combined signal, duet sequence duration, and pant call rate-comparing the coordinated vocalizations recorded from 36 family groups at 18 sites in Bolivia, Peru and Ecuador. Our analysis identified four distinct duetting patterns: (1) a donacophilus pattern, sensu largo, characteristic of P. donacophilus, P. pallescens, P. olallae, and P. modestus; (2) a moloch pattern comprising P. discolor, P. toppini, P. aureipalatii, and P. urubambensis; (3) a torquatus pattern exemplified by the duet of Cheracebus lucifer; and (4) the distinctive duet of P. oenanthe, a putative member of the donacophilus group, which is characterized by a mix of broadband and narrowband syllables, many of which are unique to this species. We also document a sex-related difference in the bellow-pant phrase combination among the three taxa sampled from the moloch lineage. Our data reveal a presumptive taxonomic incoherence illustrated by the distinctive loud calls of both P. urubambensis and P. oenanthe within the donacophilus lineage, sensu largo. The results are discussed in light of recent reassessments of the callicebine phylogeny, based on a suite of genetic studies, and the potential contribution of environmental influences, including habitat acoustics and social learning. A better knowledge of callicebine loud calls may also impact the conservation of critically endangered populations, such as the vocally distinctive Peruvian endemic, the San Martin titi, P. oenanthe.

The role of extragroup encounters in a Neotropical, cooperative breeding primate, the common marmoset: a field playback experiment.

In cooperatively breeding species, encounters with intruders may serve multiple functions ranging from reaffirming group territory ranges to facilitating assessments for additional breeding opportunities. While these distinctive events offer the opportunity to investigate the delicate balance of these social dimensions within animal societies, their unpredictable occurrence makes witnessing and controlling these events in the wild particularly challenging. Here we used a field playback approach to simulate conspecific territorial incursions in cooperatively breeding common marmosets (Callithrix jacchus) to distinguish between the three following non-mutually exclusive functions of intergroup encounters in this species of New World primate: territorial defense, mate defense, and assessment of breeding opportunities. For these experiments, we systematically broadcast species-typical long-distance contact calls - phees - commonly used in intergroup interactions from the core and periphery of the groups' territories using either male or female vocalizations. Consistent with a territorial defense hypothesis, a group's reaction was independent of the simulated intruder's sex and the response strength was greater when the playback stimulus was broadcast from the core areas of groups' territories relative to stimulus broadcast from periphery areas. However, sex differences in some facets of their responses suggest that this is not the only potential function for these encounters. Mated males and females started to move first in response to simulated intruders of the opposite sex, suggesting that these events offered opportunities to assess extra-pair breeding opportunities, while the occurrence of females' piloerection towards simulated female intruders is suggestive of mate-guarding. These data provide unique experimental evidence for the theory that excursions by conspecific intruders may serve multiple functions in a cooperatively breeding vertebrate and are reflective of the known complexities of common marmoset sociobiology.

Techniques Used by Bearded Capuchin Monkeys (Sapajus libidinosus) to Access Water in a Semi-Arid Environment of North-Eastern Brazil.

The exploratory behaviour and the ability of capuchin monkeys to use tools allows them to thrive at times and places of limited food and water abundance, such as in semi-arid environments. Here, we report the behaviours employed by individuals belonging to a wild group of bearded capuchin monkeys (Sapajus libidinosus) to access natural water sources in a dry forest of north-eastern Brazil. An adult female employed a twig as a tool and her tail to gain access to accumulated rainwater in a tree hole, and other individuals used their hands and mouth to manipulate orchids' pseudobulbs and the liquid endosperm of palm nuts. The behaviour of wild Sapajus to access water from non-food sources may enable them to circumvent the risk of dehydration in environments with reduced availability of fleshy fruits and with ephemeral and rare water sources. Our findings contribute to the still scarce but accumulating reports on primate drinking behaviour and to the knowledge of tool use in wild populations of capuchin monkeys, enriching our understanding of primate strategies to gain access to a vital resource under challenging conditions.

Sleeping above the enemy: Sleeping site choice by black-fronted titi monkeys (Callicebus nigrifrons).

The costs imposed by predation may result in behavioral adaptations to reduce mortality risk, including the choice and use of sleeping sites. The threat of predation, however, is rarely the sole force shaping sleeping site choice, which is likely to reflect other factors such as foraging needs as well. Here we describe the use of sleeping sites by three groups of small Neotropical monkeys, the black-fronted titi monkeys (Callicebus nigrifrons), and evaluate the role of predation pressure and foraging optimization in their choice of sleeping sites. We monitored each group for 9-20 months at two Atlantic Forest sites in southeastern Brazil. The titi monkeys used taller and larger trees to sleep than the average trees at each study site and chose branches with high vegetation coverage and located in higher forest strata than those used during diurnal activity. Sleeping sites were randomly distributed within each group's home range, and the groups avoided using the same site on consecutive nights. The characteristics of the sleeping sites and the behavior of the titi monkeys suggest that predation avoidance, especially of scansorial carnivores, is an important factor driving sleeping site choice. We conclude that titi monkeys' strategy to avoid predation while sleeping depends on the presence of a heterogeneous forest stratum with large emergent trees and liana tangles, which offer a physical barrier against predators.

Estimating primate population densities: the systematic use of playbacks along transects in population surveys.

Accurate measures of animal population densities are essential to assess their status, demography, and answer ecological questions. Among several methods proposed to collect abundance data, line transect sampling is used the most. The assumptions required to obtain accurate density estimates through this method, however, are rarely met when studying primates. As most primate species are vocally active, density estimates can be improved by associating transect sampling with playback point counts to scan the entire study area. Yet, attention to playback procedure and data collection design is necessary. Here, we describe a protocol to assess primate densities using playback and test its application on surveys of Callicebus nigrifrons, a small Neotropical primate that shows site fidelity and active vocal behavior. We list important steps and discuss precautions that should be considered, from the adjustments in the recordings in the lab to field procedures in the playback broadcasting sessions. Prior to the surveys, we conducted playback trials with three habituated wild groups at three forest remnants to test their response to the playback stimuli at different distances. Based on these trials, we defined the radius distance covered by the playback sessions. Then, we conducted two surveys in 12 forest remnants, in the northeast of São Paulo State Brazil. The results of density estimates were consistent between the two surveys. As the playback survey protocol we described has proved to be a simple and useful tool for surveying vocal primate and generated reliable data, we suggest that it is a good alternative method to estimate density of species, particularly for those that are responsive to playbacks and show site fidelity.

The Role of Grunt Calls in the Social Dominance Hierarchy of the White-Lipped Peccary (Mammalia, Tayassuidae).

Grunt-like calls are present in the vocal repertoire of many group-living mammals and seem to facilitate social interactions between lower and higher-ranking members. The white-lipped peccary (Tayassu pecari) lives in stable hierarchical mixed-sex groups and like non-human primates, usually emits grunt-like calls following aggressive interactions, mainly during feeding contexts. We investigated the possible functions of peccaries' grunt-like calls and their relationship to the individuals' social rank, identity, and sexual dimorphism. We observed that low-ranking individuals emitted grunt-like calls more often than high-ranking ones, and that the alpha male never emitted this vocalization. Moreover, the mean minimum frequency of grunt-like calls decreased as the peccary's rank increased. The findings revealed differences among individual grunts, but the low accuracy of cross-validation (16%) suggests that individual recognition in peccaries may be less important than an honest signal of individual social status. In addition, the absence of differences in the acoustic parameters of grunt-like calls between males and females points to the lack of sexual dimorphism in this species. We verified that after hearing grunt calls, dominant opponents were more likely to cease attacking a victim, or at least delay the continuation of conflict, probably decreasing the severity of agonistic interactions. Our findings are particularly important to improve the current understanding of the role of grunt-like calls in herd-living mammals with linear dominant hierarchies, and strongly suggest that they are involved in the maintenance of herd social stability and cohesion.

Playback responses of socially monogamous black-fronted titi monkeys to simulated solitary and paired intruders.

Many birds and primates use loud vocalizations to mediate agonistic interactions with conspecifics, either as solos by males or females, or as coordinated duets. The extensive variation in duet complexity, the contribution of each sex, and the context in which duets are produced suggest that duets may serve several functions, including territory and mate defense. Titi monkeys (Callicebus spp.) are believed to defend their home range via solo loud calls or coordinated duets. Yet there are remarkably few experimental studies assessing the function of these calls. Observations of interactions between wild established groups and solitary individuals are rare and, therefore, controlled experiments are required to simulate such situations and evaluate the mate and joint territorial defense hypotheses. We conducted playback experiments with three free-ranging groups of habituated black-fronted titi monkeys (Callicebus nigrifrons) to test these hypotheses. We found that titi monkeys responded to the three conspecific playback treatments (duets, female solos, and male solos) and did not respond to the heterospecific control treatment. The monkeys did not show sex-specific responses to solos (N = 12 trials). Partners started to duet together in 79% of their responses to playback-simulated rivals (N = 14 calls in response to playback). Males started to approach the loudspeaker before females regardless of the type of stimulus. The strength of the response of mated pairs to all three conspecific treatments was similar. Overall, our results are consistent with the idea that black-fronted titi monkeys use their loud calls in intergroup communication as a mechanism of joint territorial defense.

Vocal behavior of black-fronted titi monkeys (Callicebus nigrifrons): acoustic properties and behavioral contexts of loud calls.

Loud calls can be heard over long distances due to their high amplitude and low frequency. These calls are commonly used for both within- and between-group communication in many bird and primate species. In the Neotropics, mated pairs of socially monogamous titi monkeys (genus Callicebus) emit conspicuous, coordinated loud calls. These vocalizations appear to play a role in territorial defense, a hypothesis derived from studies of only three of the 31 recognized Callicebus species. Here, we describe the acoustic properties and organization of the loud calls of black-fronted titi monkeys (Callicebus nigrifrons). We compare the behavioral and ecological contexts associated with these vocalizations to investigate their role in within- and between-group communication, resource defense, and mate defense. Black-fronted titi monkeys create loud calls by combining a finite number of syllables to form more complex phrases, which are assembled to compose long sequences of loud calls. Bioacoustic features distinguish the loud calls used in different contexts, involving communication within- and between-groups. We found support for the hypothesis that vocalizations used for between-group communication are cooperative displays used by the mated pair and other group members to regulate access to important food resources, such as fruits. On the other hand, we only found weak support for the mate defense hypothesis.