Factors influencing terrestriality in primates of the Americas and Madagascar.

Among mammals, the order Primates is exceptional in having a high taxonomic richness in which the taxa are arboreal, semiterrestrial, or terrestrial. Although habitual terrestriality is pervasive among the apes and African and Asian monkeys (catarrhines), it is largely absent among monkeys of the Americas (platyrrhines), as well as galagos, lemurs, and lorises (strepsirrhines), which are mostly arboreal. Numerous ecological drivers and species-specific factors are suggested to set the conditions for an evolutionary shift from arboreality to terrestriality, and current environmental conditions may provide analogous scenarios to those transitional periods. Therefore, we investigated predominantly arboreal, diurnal primate genera from the Americas and Madagascar that lack fully terrestrial taxa, to determine whether ecological drivers (habitat canopy cover, predation risk, maximum temperature, precipitation, primate species richness, human population density, and distance to roads) or species-specific traits (body mass, group size, and degree of frugivory) associate with increased terrestriality. We collated 150,961 observation hours across 2,227 months from 47 species at 20 sites in Madagascar and 48 sites in the Americas. Multiple factors were associated with ground use in these otherwise arboreal species, including increased temperature, a decrease in canopy cover, a dietary shift away from frugivory, and larger group size. These factors mostly explain intraspecific differences in terrestriality. As humanity modifies habitats and causes climate change, our results suggest that species already inhabiting hot, sparsely canopied sites, and exhibiting more generalized diets, are more likely to shift toward greater ground use.

An urgent call-to-action to protect the nonhuman primates and Indigenous Peoples of the Brazilian Amazon.

Primates are facing an impending extinction crisis. Here, we examine the set of conservation challenges faced by the 100 primate species that inhabit the Brazilian Amazon, the largest remaining area of primary tropical rainforest in the world. The vast majority (86%) of Brazil's Amazonian primate species have declining populations. Primate population decline in Amazonia has been driven principally by deforestation related to the production of forest-risk commodities including soy and cattle ranching, the illegal logging and setting of fires, dam building, road and rail construction, hunting, mining, and the confiscation and conversion of Indigenous Peoples' traditional lands. In a spatial analysis of the Brazilian Amazon, we found that 75% of Indigenous Peoples' lands (IPLs) remained forested compared with 64% of Conservation Units (CUs) and 56% of other lands (OLs). In addition, primate species richness was significantly higher on IPLs than on CUs and OLs. Thus, safeguarding Indigenous Peoples' land rights, systems of knowledge, and human rights is one of the most effective ways to protect Amazonian primates and the conservation value of the ecosystems they inhabit. Intense public and political pressure is required and a global call-to-action is needed to encourage all Amazonian countries, especially Brazil, as well as citizens of consumer nations, to actively commit to changing business as usual, living more sustainably, and doing all they can to protect the Amazon. We end with a set of actions one can take to promote primate conservation in the Brazilian Amazon.

Foraging networks and social tolerance in a cooperatively breeding primate (Callithrix jacchus).

Within-group competition over food resources can be a major cost of social living. In the wild, foragers are confronted with social (e.g. hierarchical rank) and ecological (e.g. food availability and distribution) challenges that affect their foraging decisions and feeding success. Exhibiting prosocial behaviours, such as tolerance at feeding sites, can benefit group members by developing affiliative social relationships, enhancing access to resources and maximizing fitness. We examined social tolerance at feeding sites in Callithrix jacchus, a cooperatively breeding primate species. We investigated the set of social (rank, age and sex) and ecological (food availability) factors that influence the structure and dynamics of within-group foraging association networks. We designed and conducted an experimental field study of four wild groups of common marmosets in which we controlled food distribution (concentrated or scattered) and productivity (high, medium or low food rewards). Then, we used social network analyses to assess the number and strength of foraging associations among group members, their effects on individual food consumption, and whether recent experiences with conspecifics during foraging affected subsequent associations. Overall, common marmoset foraging association networks were cohesive, as group members jointly occupied feeding sites. The number and strength of associations varied depending on the ecological context. Associations were stronger during conditions in which food was concentrated at a single site. Individuals obtained greater access to food resources when sharing a feeding site with conspecifics, but once a food item was obtained, the forager moved to a nearby tree and consumed it away from others. Additionally, the strength of previous foraging associations and subsequent levels of social tolerance at feeding sites were positively related, a relationship compatible with the ability of memorizing associations over time and recalling the information in future decision-making. In sum, marmosets adjusted their partner choices and the strength of foraging associations in response to food availability. They exhibited increased social tolerance at feeding sites during conditions in which opportunities for contest competition were expected to be greatest. These cooperative breeding primates appear to mutually benefit by maintaining cohesive and strong affiliative relationships, and by increasing opportunities for coordinated behaviour and offspring survival.

A competição por recursos alimentares dentro do grupo pode ser um grande custo da vida social. Na natureza, os forrageadores são confrontados com desafios sociais (e.g. posição hierárquica) e ecológicos (e.g. disponibilidade e distribuição de alimentos) que afetam suas decisões de forrageio e seu sucesso alimentar. Exibir comportamentos pró-sociais, como tolerância em sítios de alimentação, pode beneficiar os membros do grupo, desenvolvendo relações sociais afiliativas, melhorando o acesso aos recursos e maximizando sua aptidão evolutiva. Examinamos a tolerância social de um primata com reprodução cooperativa (Callithrix jacchus) em sítios de alimentação. Investigamos a influência de um conjunto de fatores sociais (hierarquia, idade, sexo) e ecológicos (disponibilidade de alimento) na estrutura e dinâmica das redes de associação de forrageio dentro do grupo social. Planejamos e conduzimos um experimento de campo com quatro grupos de saguis-comuns de vida livre, no qual controlamos a distribuição (concentrada e dispersa) e a produtividade de alimento (altas, médias ou baixas recompensas). Usamos análise de redes sociais para avaliar o número e a força das associações de forrageio entre os membros do grupo, seu efeito no consumo individual de alimento, e se experiências recentes de forrageio entre coespecíficos afetam associações subsequentes. Em geral, as redes de associação de forrageio dos saguis foram coesas e os membros de cada grupo ocuparam sítios de alimentação em conjunto. O número e a força das associações variaram dependendo do contexto ecológico. As associações foram mais fortes durante as condições em que o alimento se encontrava concentrado em um sítio. Os indivíduos obtiveram maior acesso aos recursos quando compartilharam o sítio de alimentação com coespecíficos, e uma vez que o item alimentar era obtido, o forrageador o consumia em uma árvore próxima, longe dos outros. Além disso, a força das associações recentes e os níveis subsequentes de tolerância social em sítios de alimentação foram positivamente relacionados, compatível com a capacidade de memorizar associações ao longo do tempo e relembrá-las em tomadas de decisão futuras. Em conclusão, os saguis ajustaram suas escolhas de parceiros e a força das associações de forrageio em resposta à disponibilidade de alimento. Eles exibiram uma maior tolerância social em sítios de alimentação durante as condições em que se esperava que as oportunidades de competição direta fossem maiores. Estes primatas com reprodução cooperativa parecem se beneficiar mutuamente ao manterem relações afiliativas coesas e fortes, as quais aumentam as oportunidades para comportamentos coordenados e a sobrevivência da prole.

Necropsies disclose a low helminth parasite diversity in periurban howler monkeys.

Primate-parasite interactions are often investigated via coprological studies given ethical and conservation restrictions of collecting primate hosts. Yet, these studies are inadequate to recover adult helminths for taxonomic identification and to accurately assess their prevalence, intensity, abundance, and site of infection. Fresh carcasses found in anthropogenic landscapes come as informative and reliable alternatives. In this study, we identified the helminths of brown howler monkeys (Alouatta guariba clamitans) and their sites of infection, and measured their prevalence, intensity, and abundance of infection. We necropsied 18 adult males, 11 adult females, and 7 juvenile males that died in conflicts with the anthropogenic environment (domestic dog attacks, n = 11; electrocutions and road-kills, n = 10 each; unknown, n = 5) in periurban landscapes of southern Brazil between 2013 and 2019. We found three nematodes (Trypanoxyuris minutus, Dipetalonema gracile, and Parabronema bonnei) and one cestode (Bertiella cf. studeri), a diversity estimated to account for a sampling completeness of 99%. Prevalence ranged from 3% for P. bonnei to 100% for T. minutus. Mean abundance ranged from 2 (D. gracile and B. cf. studeri) to 55,116 (T. minutus) and mean intensity of infection ranged from 4 (B. cf. studeri) to 55,116 (T. minutus). Trypanoxyuris minutus sex ratio was strongly male-biased. The intensity of infection with T. minutus was higher in juvenile males and adult females than in adult males. The low parasite diversity and the helminths' mode of transmission are compatible with howlers' arboreality and folivorous-frugivorous diet. The howlers were not infected with soil-transmitted helminth parasites of humans and domestic animals on the ground and probably did not eat invertebrates to complement the diet. Given the lack of evidence of howler health problems, we suggest that the causes of death of the necropsied howlers are the major threats to the long-term conservation of the species at the study periurban landscapes.

Fermented food consumption in wild nonhuman primates and its ecological drivers.

OBJECTIVES: Although fermented food use is ubiquitous in humans, the ecological and evolutionary factors contributing to its emergence are unclear. Here we investigated the ecological contexts surrounding the consumption of fruits in the late stages of fermentation by wild primates to provide insight into its adaptive function. We hypothesized that climate, socioecological traits, and habitat patch size would influence the occurrence of this behavior due to effects on the environmental prevalence of late-stage fermented foods, the ability of primates to detect them, and potential nutritional benefits. MATERIALS AND METHODS: We compiled data from field studies lasting at least 9 months to describe the contexts in which primates were observed consuming fruits in the late stages of fermentation. Using generalized linear mixed-effects models, we assessed the effects of 18 predictor variables on the occurrence of fermented food use in primates. RESULTS: Late-stage fermented foods were consumed by a wide taxonomic breadth of primates. However, they generally made up 0.01%-3% of the annual diet and were limited to a subset of fruit species, many of which are reported to have mechanical and chemical defenses against herbivores when not fermented. Additionally, late-stage fermented food consumption was best predicted by climate and habitat patch size. It was more likely to occur in larger habitat patches with lower annual mean rainfall and higher annual mean maximum temperatures. DISCUSSION: We posit that primates capitalize on the natural fermentation of some fruits as part of a nutritional strategy to maximize periods of fruit exploitation and/or access a wider range of plant species. We speculate that these factors contributed to the evolutionary emergence of the human propensity for fermented foods.

Dramatic decline in a titi monkey population after the 2016-2018 sylvatic yellow fever outbreak in Brazil.

Platyrrhini are highly vulnerable to the yellow fever (YF) virus. From 2016 to 2018, the Atlantic Forest of southeast Brazil faced its worst sylvatic YF outbreak in about a century, thought to have killed thousands of primates. It is essential to assess the impact of this epidemic on threatened primate assemblages to design effective conservation strategies. In this study, we assessed the impact of the 2016-2018 YF outbreak on a geographically isolated population of Near Threatened black-fronted titi monkeys (Callicebus nigrifrons) in two Atlantic Forest patches of the Santuário do Caraça, MG, Brazil. Extensive preoutbreak monitoring, conducted between 2008 and 2016, revealed that the home range and group sizes of the population remained stable. In 2016, the population size was estimated at 53-57 individuals in 11-12 groups. We conducted monitoring and playback surveys in 2019 and found that the population had decreased by 68% in one forest patch and completely vanished in the other, resulting in a combined decline of 80%. We discuss this severe loss of a previously stable population and conclude that it was highly likely caused by the YF outbreak. The remaining population is at risk of disappearing completely because of its small size and geographic isolation. A systematic population surveys of C. nigrifrons, along other sensible Platyrrhini species, is needed to re-evaluate their current conservation status.

Howler monkey tolerance to habitat shrinking: Lifetime warranty or death sentence?

Habitat loss and fragmentation are major threats to the conservation of nonhuman primates. Given that species differ in their responses to fragmented landscapes, identifying the factors that enable them to cope with altered environments or that cause their extirpation is critical to design conservation management strategies. Howler monkeys (Alouatta spp.) are good models for studying the strategies of tolerant arboreal taxa and how they cope with spatial restriction, because they live in habitats ranging from vast pristine forests to small disturbed fragments and orchards. While some aspects of their ecology and behavior are conserved, others vary in predictable ways in response to habitat shrinking and decreasing resource availability. We argue that the ability of individual howler monkeys to inhabit low-quality environments does not guarantee the long-term persistence of the small populations that live under these conditions. Their local extirpation explains why few forest fragments below a given area threshold are frequently inhabited in landscapes where recolonization and gene flow are compromised by long isolation distances or less permeable matrices. In sum, howlers' ability to cope with habitat restriction at the individual level in the short-term may mask the inevitable fate of isolated populations, thereby compromising the persistence of the species at a regional scale in the long-term if howlers' need for protection in large forests is undervalued.

Primates Can Be a Rallying Symbol to Promote Tropical Forest Restoration.

With 60% of all primate species now threatened with extinction and many species only persisting in small populations in forest fragments, conservation action is urgently needed. But what type of action? Here we argue that restoration of primate habitat will be an essential component of strategies aimed at conserving primates and preventing the extinctions that may occur before the end of the century and propose that primates can act as flagship species for restoration efforts. To do this we gathered a team of academics from around the world with experience in restoration so that we could provide examples of why primate restoration ecology is needed, outline how primates can act as flagship species for restoration efforts of tropical forest, review what little is known about how primate populations respond to restoration efforts, and make specific recommendations of the next steps needed to make restoration of primate populations successful. We set four priorities: (1) academics must effectively communicate both the value of primates and the need for restoration; (2) more research is needed on how primates contribute to forest restoration; (3) more effort must be put into Masters and PhD level training for tropical country nationals; and finally (4) more emphasis is needed to monitor the responses of regenerating forest and primate populations where restoration efforts are initiated. We are optimistic that populations of many threatened species can recover, and extinctions can be prevented, but only if concerted large-scale efforts are made soon and if these efforts include primate habitat restoration.

Games academics play and their consequences: how authorship, h-index and journal impact factors are shaping the future of academia.

Research is a highly competitive profession where evaluation plays a central role; journals are ranked and individuals are evaluated based on their publication number, the number of times they are cited and their h-index. Yet such evaluations are often done in inappropriate ways that are damaging to individual careers, particularly for young scholars, and to the profession. Furthermore, as with all indices, people can play games to better their scores. This has resulted in the incentive structure of science increasingly mimicking economic principles, but rather than a monetary gain, the incentive is a higher score. To ensure a diversity of cultural perspectives and individual experiences, we gathered a team of academics in the fields of ecology and evolution from around the world and at different career stages. We first examine how authorship, h-index of individuals and journal impact factors are being used and abused. Second, we speculate on the consequences of the continued use of these metrics with the hope of sparking discussions that will help our fields move in a positive direction. We would like to see changes in the incentive systems, rewarding quality research and guaranteeing transparency. Senior faculty should establish the ethical standards, mentoring practices and institutional evaluation criteria to create the needed changes.

ATLANTIC-PRIMATES: a dataset of communities and occurrences of primates in the Atlantic Forests of South America.

Primates play an important role in ecosystem functioning and offer critical insights into human evolution, biology, behavior, and emerging infectious diseases. There are 26 primate species in the Atlantic Forests of South America, 19 of them endemic. We compiled a dataset of 5,472 georeferenced locations of 26 native and 1 introduced primate species, as hybrids in the genera Callithrix and Alouatta. The dataset includes 700 primate communities, 8,121 single species occurrences and 714 estimates of primate population sizes, covering most natural forest types of the tropical and subtropical Atlantic Forest of Brazil, Paraguay and Argentina and some other biomes. On average, primate communities of the Atlantic Forest harbor 2 ± 1 species (range = 1-6). However, about 40% of primate communities contain only one species. Alouatta guariba (N = 2,188 records) and Sapajus nigritus (N = 1,127) were the species with the most records. Callicebus barbarabrownae (N = 35), Leontopithecus caissara (N = 38), and Sapajus libidinosus (N = 41) were the species with the least records. Recorded primate densities varied from 0.004 individuals/km2 (Alouatta guariba at Fragmento do Bugre, Paraná, Brazil) to 400 individuals/km2 (Alouatta caraya in Santiago, Rio Grande do Sul, Brazil). Our dataset reflects disparity between the numerous primate census conducted in the Atlantic Forest, in contrast to the scarcity of estimates of population sizes and densities. With these data, researchers can develop different macroecological and regional level studies, focusing on communities, populations, species co-occurrence and distribution patterns. Moreover, the data can also be used to assess the consequences of fragmentation, defaunation, and disease outbreaks on different ecological processes, such as trophic cascades, species invasion or extinction, and community dynamics. There are no copyright restrictions. Please cite this Data Paper when the data are used in publications. We also request that researchers and teachers inform us of how they are using the data.

Detection of antibodies against Icoaraci, Ilhéus, and Saint Louis Encephalitis arboviruses during yellow fever monitoring surveillance in non-human primates (Alouatta caraya) in southern Brazil.

BACKGROUND: Free-ranging non-human primates (NHPs) can host a variety of pathogenic microorganisms, such as arboviruses, which include the yellow fever virus (YFV). This study aimed to detect the circulation of YF and other arboviruses in three wild Alouatta caraya populations in forests in southern Brazil. METHODS: We collected 40 blood and serum samples from 26 monkeys captured/recaptured up to four times from 2014 to 2016, searching for evidence of arboviruses by virus isolation, PCR, and neutralization tests. RESULTS: Viral isolation and genome detection were negative; however, we detected neutralizing antibodies against the Saint Louis, Ilhéus, and Icoaraci viruses in three NHPs. CONCLUSIONS: Saint Louis Encephalitis, Ilhéus, and Icoaraci viruses circulated recently in the region. Future studies should investigate the role of NHPs, other vertebrate hosts and wild vectors in the region's arbovirus circulation and the potential risks of the arboviruses to wildlife, domestic animals, and humans.

Supplemented howler monkeys eat less wild fruits, but do not change their activity budgets.

Research on the influence of food supplementation on primate behavior has focused on terrestrial and semiterrestrial species. Its effects on highly arboreal species are poorly known. We assessed the influence of food supplementation on the feeding behavior and activity budget of four adult female and two adult male brown howler monkeys (Alouatta guariba clamitans) belonging to two groups (JA and RO) that inhabited periurban forest fragments in southern Brazil. We used the "focal-animal" method during 6-8 full days per month from March to August 2017 (916 h of observation) to record the behavior of the study subjects. The feeding events of the focal individual were recorded using the "all occurrences" method. The supplementation was unevenly distributed during the day and accounted for 5-6% of all feeding events of male and female howlers, respectively. JA always received fruit in a platform, whereas RO had access to fruits and processed foods on roofs and directly from humans. The mean biomass of wild foods ingested by each adult per day was >300% higher than the ingested biomass of supplemented foods (females: 395 vs. 109 g/day; males: 377 vs. 120 g/day), but the ingestion rate of supplemented foods was ca. 400% higher than that of wild foods (females: 17 vs. 4 g/min; males: 19 vs. 5 g/min). The activity budgets of females and males were dominated by resting (66-72%) followed by feeding (18-14%), moving (12-11%), and socializing (2%). We found that food supplementation reduced the ingestion of wild fruits, but it did not affect the howlers' need to ingest a given amount of leaves per day and the time spent resting, feeding, moving, and socializing.

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.

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.

Fruit availability drives the distribution of a folivorous-frugivorous primate within a large forest remnant.

Understanding the ecological factors that influence the presence, abundance, and distribution of species within their habitats is critical for ensuring their long-term conservation. In the case of primary consumers, such as most primates, the availability and richness of plant foods are considered key drivers of population density at these variables influence the spatial distribution of social units within a finer, habitat patch level scale. We tested the hypothesis that the spatiotemporal availability and richness of plant foods, drive the spatial distribution of brown howler monkeys (Alouatta guariba clamitans) at a fine spatial scale. We established five line transects (2.6-4.3 km long) to census the population of brown howlers in Morro São Pedro, a 1,200 ha Atlantic forest remnant in southern Brazil, every 2 weeks from January to June 2015. We used data from tree inventories performed in sighting and control plots, and phenological surveys of 17 top food tree species to estimate bi-weekly food availability. We recorded a total of 95 sightings. The number of sightings per sampling period ranged from 2 to 12. The availability of fruit (ripe and unripe) was higher in sighting than in control plots, whereas leaf availability and the richness of food tree species was similar. We conclude that the spatial distribution of fruiting trees and the availability of fruit drive the pattern of habitat use, and spacing of brown howler groups in Morro São Pedro.

Ambient temperature and humidity modulate the behavioural thermoregulation of a small arboreal mammal (Callicebus bernhardi).

Maintaining a constant body temperature is critical to the proper functioning of metabolic reactions. Behavioural thermoregulation strategies may minimize the cost of energetic balance when an animal is outside its thermoneutral zone. We investigated whether ambient temperature and relative air humidity influence the use of behavioural strategies by a group of Prince Bernhard's titi monkeys (Callicebus bernhardi) living in a forest fragment. We monitored a social group composed of four individuals (an adult couple and two juveniles) for 1010h from March to September 2015. We used the instantaneous scan sampling method to record the body posture, the microhabitat, and the occurrence of huddling with group mate(s) when animals were resting. We recorded ambient temperature and relative humidity in the shade every 10min with a data logger hanging at a height of approximately 5m. Daytime temperature ranged from 18.5°C to 38.5°C and relative humidity ranged from 21% to 97%. Titi monkeys avoided sunny places at higher temperatures, especially above 31°C. Minimum night temperature did not influence the choice of resting microhabitats during the first hour after sunrise. Sitting was the major resting posture during the day (62%). Titi monkeys increased the use of heat-dissipating postures at ambient temperatures >27°C. In addition, an increase in relative humidity increased the use of these postures at 26°C, 27°C, 29°C and 33°C, but caused a decrease at 24°C. On the other hand, the ambient temperature did not influence the occurrence of huddling. We conclude that microhabitat choice and postural behaviour are important for titi monkeys to prevent overheating and suggest that these behavioural adjustments might also be critical for other tropical arboreal mammals.

Two cases of polydactyly in wild brown howler monkeys (Alouatta guariba clamitans).

We report the first two cases of polydactyly in an atelid species: (i) a wild ca. 16-week-old infant female presenting seven digits in both feet and other bone malformations and (ii) a wild newborn male presenting six digits in both feet with the extra digit fused to the hallux.

Ranging behavior drives parasite richness: A more parsimonious hypothesis.

Parasitism is a ubiquitous interspecific interaction that may play an important role in the evolution of hosts and parasites, molding many aspects of their behavior and ecology. Detecting behavioral changes of hosts infected with parasites is not a straightforward task. Extrapolating from individual-level responses to group-level decision-making is still a much more complex challenge. The ranging behavior of hosts that live in social groups is a good example. Many hypotheses of the cause-effect relationship between this behavior and parasite diversity and load have been proposed. For instance, Brockmeyer et al. [2015, Am. J. Primatol. 77:1036-1048] recently suggested that the richness of protozoan parasites influences the daily path length of free-ranging mandrills. We believe that this explanation for the relationship contains several implicit assumptions. Therefore, we offer an alternative, more parsimonious hypothesis in which daily path length is the driver of parasite richness rather than its consequence. Our hypothesis only assumes that ranging farther exposes animals to a richer parasite diversity. We discuss the data required to test these alternative hypotheses and recall empirical evidence and theoretical modeling results supporting or rejecting their assumptions. We also propose a model of the expected outcomes in terms of species richness, load, intensity of infection, and within-group community similarity of non-lethal environmentally transmitted parasites in social animal groups showing distinct patterns of range use. Am. J. Primatol. 78:923-927, 2016. © 2016 Wiley Periodicals, Inc.

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.