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.

Geographic comparison of plant genera used in frugivory among the pitheciids Cacajao, Callicebus, Chiropotes, and Pithecia.

Pitheciids are known for their frugivorous diets, but there has been no broad-scale comparison of fruit genera used by these primates that range across five geographic regions in South America. We compiled 31 fruit lists from data collected from 18 species (three Cacajao, six Callicebus, five Chiropotes, and four Pithecia) at 26 study sites in six countries. Together, these lists contained 455 plant genera from 96 families. We predicted that 1) closely related Chiropotes and Cacajao would demonstrate the greatest similarity in fruit lists; 2) pitheciids living in closer geographic proximity would have greater similarities in fruit lists; and 3) fruit genus richness would be lower in lists from forest fragments than continuous forests. Fruit genus richness was greatest for the composite Chiropotes list, even though Pithecia had the greatest overall sampling effort. We also found that the Callicebus composite fruit list had lower similarity scores in comparison with the composite food lists of the other three genera (both within and between geographic areas). Chiropotes and Pithecia showed strongest similarities in fruit lists, followed by sister taxa Chiropotes and Cacajao. Overall, pitheciids in closer proximity had more similarities in their fruit list, and this pattern was evident in the fruit lists for both Callicebus and Chiropotes. There was no difference in the number of fruit genera used by pitheciids in habitat fragments and continuous forest. Our findings demonstrate that pitheciids use a variety of fruit genera, but phylogenetic and geographic patterns in fruit use are not consistent across all pitheciid genera. This study represents the most extensive examination of pitheciid fruit consumption to date, but future research is needed to investigate the extent to which the trends in fruit genus richness noted here are attributable to habitat differences among study sites, differences in feeding ecology, or a combination of both.

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.

Terrestrial activity in pitheciins (Cacajao, Chiropotes, and Pithecia).

Neotropical monkeys of the genera Cacajao, Chiropotes, and Pithecia (Pitheciidae) are considered to be highly arboreal, spending most of their time feeding and traveling in the upper canopy. Until now, the use of terrestrial substrates has not been analyzed in detail in this group. Here, we review the frequency of terrestrial use among pitheciin taxa to determine the ecological and social conditions that might lead to such behavior. We collated published and unpublished data from 14 taxa in the three genera. Data were gleaned from 53 published studies (including five on multiple pitheciin genera) and personal communications of unpublished data distributed across 31 localities. Terrestrial activity was reported in 61% of Pithecia field studies (11 of 18), in 34% of Chiropotes studies (10 of 29), and 36% of Cacajao studies (4 of 11). Within Pithecia, terrestrial behavior was more frequently reported in smaller species (e.g. P. pithecia) that are vertical clingers and leapers and make extensive use of the understory than in in the larger bodied canopy dwellers of the western Amazon (e.g. P. irrorata). Terrestrial behavior in Pithecia also occurred more frequently and lasted longer than in Cacajao or Chiropotes. An apparent association was found between flooded habitats and terrestrial activity and there is evidence of the development of a "local pattern" of terrestrial use in some populations. Seasonal fruit availability also may stimulate terrestrial behavior. Individuals also descended to the ground when visiting mineral licks, escaping predators, and responding to accidents such as a dropped infant. Overall, the results of this review emphasize that terrestrial use is rare among the pitheciins in general and is usually associated with the exploitation of specific resources or habitat types.

Foraging strategies of black-fronted titi monkeys (Callicebus nigrifrons) in relation to food availability in a seasonal tropical forest.

Many primates have to cope with a temporal scarcity in food availability that shapes their foraging strategies. Here we investigated the changes in diet, activity, and ranging behavior of a group of black-fronted titi monkeys (Callicebus nigrifrons) according to the availability of the main high-nutritional-density item in their diet and the foraging strategy adopted when this food is scarce. We monitored one habituated group using instantaneous scan sampling over 1 year (533 h of observation, 61 days) in a seasonal tropical forest fragment (245 ha). We simultaneously collected data on food availability with fruit traps. The titi monkeys consumed fleshy fruits, the main high-nutritional-density item of their diet, in accordance with its availability, and the availability of this item modulated the ingestion of vegetative plant parts, a relatively low-nutritional-density food. During high fleshy fruit availability, the titi monkeys consumed more fleshy fruits, flowers, and invertebrates. They also traveled more, but concentrated their activity in a central area of their home range. Conversely, during fleshy fruit scarcity, they increased the breadth of their diet, switching to one richer in seeds and vegetative plant parts, and with greater plant diversity. At the same time, they reduced most energy-demanding activities, traveling less and over shorter distances, but using their home range more broadly. Corroborating the optimal foraging theory, titi monkeys altered foraging strategies according to temporal food fluctuations and responded to low fleshy fruit availability by changing their diet, activity, and ranging behavior. The adoption of a low-cost/low-yield strategy allowed us to classify them as energy minimizers.

Landscape Use and Co-Occurrence Patterns of Neotropical Spotted Cats.

Small felids influence ecosystem dynamics through prey and plant population changes. Although most of these species are threatened, they are accorded one of the lowest research efforts of all felids, and we lack basic information about them. Many felids occur in sympatry, where intraguild competition is frequent. Therefore, assessing the role of interspecific interactions along with the relative importance of landscape characteristics is necessary to understand how these species co-occur in space. Here, we selected three morphologically similar and closely related species of small Neotropical cats to evaluate the roles of interspecific interactions, geomorphometry, environmental, and anthropogenic landscape characteristics on their habitat use. We collected data with camera trapping and scat sampling in a large protected Atlantic forest remnant (35,000 ha). Throughout occupancy modeling we investigated whether these species occur together more or less frequently than would be expected by chance, while dealing with imperfect detection and incorporating possible habitat preferences into the models. We used occupancy as a measure of their habitat use. Although intraguild competition can be an important determinant of carnivore assemblages, in our system, we did not find evidence that one species affects the habitat use of the other. Evidence suggested that proximity to the nature reserve (a more protected area) was a more important driver of Neotropical spotted cats' occurrence than interspecific interactions or geomorphometry and environmental landscape characteristics-even though our entire study area is under some type of protection. This suggests that small felids can be sensitive to the area protection status, emphasizing the importance of maintaining and creating reserves and other areas with elevated protection for the proper management and conservation of the group.

Run, hide, or fight: anti-predation strategies in endangered red-nosed cuxiú (Chiropotes albinasus, Pitheciidae) in southeastern Amazonia.

Although primate predation is rarely observed, a series of primate anti-predation strategies have been described. Energetic costs of such strategies can vary from high-cost mobbing, via less costly alarm calling, to low-cost furtive concealment. Here we report the anti-predation strategies of red-nosed cuxiú, Chiropotes albinasus, based on direct observations from four study sites in southeastern Brazilian Amazonia. Over a collective period of 1255 fieldwork hours, we observed nine direct interactions between raptors (all potential predators) and red-nosed cuxiús. Of these, one (11%) resulted in predation. Raptors involved were: Harpia harpyja (four events), Leucopternis sp. (two events), Spizaëtus tyrannus (one event), and unidentified large raptors (two events). Predation attempts occurred in flooded-forest and terra firme rainforest, were directed at both adult and non-adult cuxiús, and involved both adult and juvenile raptors. Anti-predation strategies adopted by the cuxiús included: (1) group defence and mobbing behaviour (two occasions), (2) dropping into dense sub-canopy (seven occasions), (3) alarm calling (eight occasions), and (4) fleeing to, and hiding in, dense vegetation (eight occasions). During each encounter at least two of these behaviours were recorded. These are the first published records of predation, predation attempts, and anti-predator behaviour involving red-nosed cuxiú.

Are Diet Preferences Associated to Skulls Shape Diversification in Xenodontine Snakes?

Snakes are a highly successful group of vertebrates, within great diversity in habitat, diet, and morphology. The unique adaptations for the snake skull for ingesting large prey in more primitive macrostomatan snakes have been well documented. However, subsequent diversification in snake cranial shape in relation to dietary specializations has rarely been studied (e.g. piscivory in natricine snakes). Here we examine a large clade of snakes with a broad spectrum of diet preferences to test if diet preferences are correlated to shape variation in snake skulls. Specifically, we studied the Xenodontinae snakes, a speciose clade of South American snakes, which show a broad range of diets including invertebrates, amphibians, snakes, lizards, and small mammals. We characterized the skull morphology of 19 species of xenodontine snakes using geometric morphometric techniques, and used phylogenetic comparative methods to test the association between diet and skull morphology. Using phylogenetic partial least squares analysis (PPLS) we show that skull morphology is highly associated with diet preferences in xenodontine snakes.

Ethological approach to autism spectrum disorders.

The purpose of the study was to develop a new ethogram for the assessment of children and adolescents with autism spectrum disorders (ASD) and intellectual developmental disorder (IDD) and to test whether this instrument accurately distinguishes ASD participants (n = 61) from IDD participants (n = 61). An ethogram with 88 behavior elements was generated, including body postures, verbalizations, facial expressions, motor stereotypies, head postures, gaze behavior, gestures, and interpersonal distance. Significant differences were detected between both groups in classic ASD behaviors; in behaviors that are deficient in ASD according to established theoretical models, such as symbolic play, gaze direction, gaze following, and use of mental state language; in atypical behaviors that have also been described previously in ethological studies with ASD; and in the nonspecific behaviors of ASD, such as walk, look own body, explore, and cry. The predictive success of a diagnosis of ASD in the logistic regression model with the ethogram's factors was 98.4%. The results suggest that this ethogram is a powerful and useful tool for both the detailed study of the social behaviors of autistic children and adolescents, and for discriminating ASD and IDD.