Food availability, plant diversity, and vegetation structure drive behavioral and ecological variation in Endangered Coimbra-Filho's titi monkeys.

There is wide variability in primate behavior and ecology. Understanding how frugivorous primates behave under different habitat fragmentation levels is key for effective conservation and management of species and their habitats. We evaluated the seasonality in activity budget, diet, and ranging behavior of two groups of Endangered Coimbra-Filho's titi monkeys (Callicebus coimbrai). One group inhabited a 14-ha forest fragment, whereas the other lived in a 522-ha fragment. We measured the monthly density of trees and lianas available as food sources over 8 months. We also collected behavioral and group location data every 5 min, from dawn to dusk, using the scan sampling method. The two forest fragments differed seasonally in the number of fruiting food-resource available. In the 14-ha fragment, we found that the time spent by titi monkeys feeding, foraging, resting, and traveling differed seasonally. In the 522-ha fragment, titi monkeys exhibited seasonal differences in time spent sleeping, socializing, foraging, and revisiting food sources. In both titi monkey groups, diets varied seasonally. Our findings indicate that Coimbra-Filho's titi monkeys can exhibit behavioral flexibility in their activity budgets, diets, and movement patterns. Such flexibility is important for this species to survive in fragmented habitats and may be linked to three key factors: species-specific resource availability, plant species diversity, and the vegetation structure of each forest fragment.

Stay Gathered Rather than Scattered: Strategies of Common Marmosets during Agonistic Interactions with Birds in the Atlantic Rain Forest.

To reduce the vulnerability of their small body size, common marmosets live in large and cohesive social groups. Thus, we hypothesized that in order to compensate for small body size and predation risk, individuals of common marmosets will stay gathered rather than scattered when foraging for eggs and/or nestling birds. Furthermore, in order to avoid costly injuries and eventual predation risks, for both sides, the majority of interactions among common marmosets and small birds will not involve direct physical contact. The study was developed in a small fragment of Atlantic Forest in the northeast of Brazil. We recorded a total of 115 interactions between common marmosets (Callithrix jacchus) with 7 different bird species. As expected, agonistic interactions were significantly more frequent when the marmosets were gathered. Also, most agonistic interactions by the birds toward common marmosets involved overflights without physical contact. Apparently, the set of avoidance behavior leads to a reduced predation risk for both sides. It appears that dispersed marmosets do not represent an imminent threat that justifies an agonistic reaction by the birds as the latter appear to avoid exposing themselves to unnecessary danger during agonistic interactions, especially when the marmosets are gathered.

Can a Non-Native Primate Be a Potential Seed Disperser? A Case Study on Saimiri sciureus in Pernambuco State, Brazil.

The interaction between native fleshy-fruit plants and introduced fruit consumers contributes to the dynamics of highly fragmented environments. Such interactions can occur through pollination and seed dispersal. Here, we investigated the potential of seed dispersing by a non-native primate, the squirrel monkey (Saimiri sciureus), in an urban Atlantic forest fragment in north-eastern Brazil. Fleshy fruits from non-native plants were preferentially exploited by the squirrel monkeys. We measured 147 seeds (width and length) from 20 of 106 faecal samples. The dispersed seeds were from five plant species (four families). We found a positive correlation between the size of seeds found in faecal samples with their availability in the habitat. Only one seed was found visually damaged after passage through the squirrel monkeys' guts. The defecated seeds were uniformly distributed (variance to mean ratio index) in the home range of squirrel monkeys, and there was a lack of specific latrines (i.e., habitat preference for defecation). Our data provide evidence that non-native S. sciureus may in be (i) acting as a potential seed disperser of native plants in the Atlantic forest fragment, (ii) contributing to the ecological role of native frugivores, and (iii) potentially contributing to the regeneration process of the highly degraded study site.

Foraging with finesse: A hard-fruit-eating primate selects the weakest areas as bite sites.

OBJECTIVES: Fruit husks are rarely uniformly hard, varying in penetrability via sulci and changes in thickness. We tested whether a hard-food specialist primate i) bites randomly on food fruit husk surfaces to access seeds, or ii) selects areas most easily penetrated by canines. We consider this would occur so as to minimize deployed mechanical force, energetic expenditure and risk of dental breakage when feeding. METHODS: A sulcus is the natural line of weakness where a dehiscent fruit breaks open. Using fruits dentally opened for seeds by golden-back uacaris (Cacajao ouakary) we: 1) analysed bite mark distribution on surface of four fruits types (hard-with-sulcus, soft-with-sulcus, hard-no-sulcus, soft-no-sulcus); 2) quantified the force needed to penetrate hard and soft fruits at sulci and elsewhere on fruit surface; 3) measured fruit wall thickness and correlated it with bite-mark distribution in all four categories of fruit. RESULTS: 1) Bite marks were distributed at random only on surfaces of soft fruits. For other fruits types, bite locations were concentrated at the thinnest areas of husk, either over the entire surface (non-sulcate fruits), or at sulci (sulcate fruits). 2) For hard-husked fruits, areas where uacaris concentrated their bites were significantly easier to penetrate than those where they did not. CONCLUSIONS: This hard-fruit feeding specialist primate is not biting at random on the surface of diet fruits. To access seeds they are focusing on those areas requiring less force to penetrate. This may be to save energy, to minimize the risk of breaking teeth used in food processing, or a combination of both. The study shows, for the first time, the subtlety by which these powerfully-jawed animals process their diet items.

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.

An Improved Technique Using Dental Prostheses for Field Quantification of the Force Required by Primates for the Dental Penetration of Fruit.

Tooth morphology is an important determinant of primate diet, setting potential limits on processable item size and material properties. Plunger-based commercial fruit firmness testers (penetrometers) have been used to estimate primate diet item hardness and, by proxy, bite force required for penetration. However, geometric forms and surface areas of penetrometer plungers and primate teeth differ considerably. Accurate bite force estimation is especially important with pitheciine primates as these penetrate fruit pericarps with their canines. To achieve more realistic bite force measures, we replaced a fruit penetrometer's standard plunger with a Cacajao calvus canine prosthesis. We compared indentation and penetration values for Hevea spruceana (Euphorbiaceae; hard-pericarp) and Mauritia flexuosa (Arecaceae; soft-pericarp) fruits (both natural Cacajao foods), and standard penetrometer head and canine prosthesis values for penetrating H. spruceana sulci. Compared to the canine prosthesis, a standard head overestimated the force needed to indent and penetrate H. spruceana fruit by more than twofold and, due to greater width, could not effectively penetrate a sulcus: sulcal penetrability data were easily retrieved with the canine prosthesis. We believe this new approach using dental prostheses has potential in the analysis of primate foraging mechanisms, especially for pitheciines for which canines are of paramount importance in accessing food.

A new addition to the toolbox: stone tool use in blonde capuchin monkeys (Sapajus flavius).

The use of tools played a central role in human culture and evolution. Early studies with apes demonstrated the tool use; however, currently the works have focused on Platyrrhine, particularly capuchin monkeys. Blonde capuchin monkeys, Sapajus flavius, have been observed using sticks to fish for termites in the Atlantic Forest, where this species has been extensively studied. In this study, we presented the first evidence of stone tool use by the blonde capuchin monkeys, as well as the dimensions and weight of these tools. We gathered data from three areas of Caatinga dry forest where we discovered this new tool use among the species. The mean weight of the hammers was 475.7 g (± 142 SD). The mean height of the anvils was 48.3 cm (± 18.7 SD), while the mean surface area of the anvils was 1.2 m2 (± 0.4 SD). We identified fruits and/or nuts from three plant species-Prunus dulces, Cnidoscolus quercifolius, and Syagrus coronate-near the anvils at the study sites. Additionally, we passively observed six instances of stone tool use by blonde capuchin monkeys. Their use of stones to crack encased foods mirrored behaviors previously reported in Sapajus libidinosus, a species well known for using stone tools to exploit hard nuts. Our findings place blonde capuchin monkeys among the list of primates that utilize stones as tools, highlighting the species' adaptability in exploiting resources within the Caatinga. Long-term studies are essentials to comprehend the use pattern of stone tools (across both general and seasonal perspectives) and the influence of variables, such as fruit hardness, distance to watercourses, and fruit availability on the use of this technology by this primate.

Brevity is not always a virtue in primate communication.

Semple et al. (Semple et al. in press, Biol. Lett. (doi:10.1098/rsbl.2009.1062)) argued that the 'law of brevity' (an inverse relationship between word length and frequency of use) applies not only to human language but also to vocal signalling in non-human primates, because coding efficiency is paramount in both situations. We analysed the frequency of use of signals of different duration in the vocal repertoires of two Neotropical primate species studied in the wild-the common marmoset (Callithrix jacchus) and the golden-backed uakari (Cacajao melanocephalus). The key prediction of the law of brevity was not supported in either species: although the most frequently emitted calls were relatively brief, they were not the shortest signals in the repertoire. The costs and benefits associated with signals of different duration must be appreciated to understand properly their frequency of use. Although relatively brief vocal signals may be favoured by natural selection in order to minimize energetic costs, the very briefest signals may be ambiguous, contain reduced information or be difficult to detect or locate, and may therefore be selected against. Analogies between human language and vocal communication in animals can be misleading as a basis for understanding frequency of use, because coding efficiency is not the only factor of importance in animal communication, and the costs and benefits associated with different signal durations will vary in a species-specific manner.

Critically endangered blonde capuchins fish for termites and use new techniques to accomplish the task.

We report the spontaneous modification and use of sticks to fish for termites, above the ground, in wild blonde capuchins (Cebus flavius). These critically endangered Neotropical primates inhabit remnants of the Atlantic Forest. They used two previously undescribed techniques to enhance their termite capture success: nest tapping and stick rotation. The current ecologically based explanation for tool use in wild capuchins (i.e. terrestrial habits and bipedalism) must be viewed cautiously. Instead, remarkable manual skills linked to a varied diet seem important in promoting tool use in different contexts. The repertoire of tool-using techniques employed by wild capuchins has been expanded, highlighting the behavioural versatility in this genus.

Hunting strategies in wild common marmosets are prey and age dependent.

We investigated the hunting strategies of wild common marmosets (Callithrix jacchus) to determine whether the strategies differed among animals of different age classes and/or prey type. The study was conducted in a fragment of Atlantic Rain Forest, situated 40 km from Recife (PE/Brazil). Twenty-seven individuals from four social groups were observed. Captured prey items were divided into three categories. The hunting strategies of the common marmosets were ranked into four categories. The acquisition of larger prey (items more than 2.0 cm) involved the appropriate body movements and postures that concealed the approaching marmosets, whereas the acquisition of smaller prey (items under 2.0 cm) involved less concealing behaviors. Furthermore, adults and juveniles (age ≥ 5 months) were more capable of capturing larger prey than were younger (1-2 months) or older infants (3-4 months). Although older infants were successful in capturing certain prey, they often failed when they attempted to capture larger prey that jumped and/or used flight to escape. The results suggest that both the experience of the monkeys and escape behavior of the prey affect predation efficiency in wild common marmosets.

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.

Propagation of the loud "tchó" call of golden-backed uakaris, Cacajao melanocephalus, in the black-swamp forests of the upper Amazon.

Arboreal primates use loud vocalisations to transmit information in densely vegetated habitats. These vocalisations are likely to show adaptations to increase their propagation and to transmit information. Golden-backed uakaris, Cacajao melanocephalus, emit a loud vocalization termed the "tchó" call, which seems to function as a contact call and encodes information on the individual signaler and behavioural context. Because the call is often used for communication over relatively large distances, we were interested in its propagation in the wild. The aim of the present study was to investigate the degradation patterns of the tchó call in the flooded igapó forest. We examined via playback experiments how the acoustic parameters of this call changed with increasing distance from the playback speaker. We broadcast 12 tchó calls and rerecorded them along a transect at distances of 10, 20, 40, 80 and 160 m from the speaker in two igapó forest patches in Jaú National Park, Amazonas, Brazil. At 160 m from the speaker, the tchó call degraded in both patches and was barely recordable. Up to a distance of 80 m, the bandwidth and number of harmonics in the call decreased with increasing distance, while the lowest frequency increased. The highest frequency (HF) did not gradually decrease with increasing distance. However, when we compared the HF at distances of 10 and 80 m, we could see a clear decrease in this parameter. Call duration increased compared with the broadcast signal up to 40 m because of reverberation, but decreased at 80 m as the weaker echoes of the call attenuated. These changes may reveal information about the signaler's distance during signal transmission. The frequency of maximum energy (FME) of the tchó call decreased significantly when comparing recordings made at 10 and 80 m. Nevertheless, it did not show a consistent and gradual decrease with increasing rerecording distance (at least up to 80 m). FME remained relatively stable (±50 Hz on average, at least up to 80 m) when compared to the other call parameters, suggesting that the tchó call may be adapted to transmit information with some efficiency throughout the igapó forest.

Responses of golden-backed uakaris, Cacajao melanocephalus, to call playback: implications for surveys in the flooded Igapó forest.

We investigated the potential use of call playback for surveying the elusive golden-backed uakari (Cacajao melanocephalus), a diurnal social primate that typically inhabits the relatively inaccessible black-water swamp forests of the upper Amazon (Igapó forest) during the wet season. Furthermore, our objective was to understand better the functions of vocalisations of these rare and threatened monkeys. We focussed on the "tchó" call, a loud vocalisation that varies in temporal and frequency characteristics according to behavioural context and individual signaller (Bezerra et al. in Int J Primatol, 2010b). We investigated the vocal and behavioural responses of golden-backed uakaris from three Igapó areas to three different playback stimuli: own group calls (OGC); neighbouring group calls (NGC); and control (background noise). The call stimuli were used to simulate the unexpected presence of monkeys from the monkeys' own and neighbouring Igapó areas. Playback of OGC and NGC increased calling and altered behaviour in golden-backed uakaris, whereas no noticeable response occurred to the control stimuli. Furthermore, there was no evidence of habituation to the call stimuli and the natural behavioural pattern of the groups was not obviously affected. Hence, call playback seems to be a valuable tool for locating these elusive monkeys in river surveys. Most of the agonistic-related behaviour observed after NGC playback was also observed after OGC playback. As golden-backed uakaris are not territorial, the presence of strange conspecifics to the area may not necessarily represent a more threatening situation. Our methods and results may also be useful for surveys of other primate species living in the Igapó forest and in other habitat types.

Alcohol intoxication reduces detection of asymmetry: an explanation for increased perceptions of facial attractiveness after alcohol consumption?

Ratings of physical attractiveness are related to degree of facial symmetry. Acute alcohol consumption affects ratings of physical attractiveness and also attenuates aspects of visual perception. We tested the hypothesis that increases in ratings of attractiveness associated with alcohol intoxication can be attributed at least in part to a reduced ability to discern facial asymmetry due to reductions in levels of visual perception. We examined whether alcohol intoxication reduces ability to detect asymmetry in approximately symmetrical images. Sober and intoxicated subjects were shown a series of simple geometric images to which they responded on whether they perceived each one to be symmetrical or asymmetrical. Intoxicated subjects were significantly less able to detect asymmetry than were sober subjects, providing support for the hypothesis.