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/km 2 (Alouatta guariba at Fragmento do Bugre, Paraná, Brazil) to 400 individuals/km 2 (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. © 2018 by the The Authors. Ecology © 2018 The Ecological Society of Americ

Terrestrial behavior in titi monkeys (Callicebus, Cheracebus, and Plecturocebus) : potential correlates, patterns, and differences between genera

For arboreal primates, ground use may increase dispersal opportunities, tolerance to habitat change, access to ground-based resources, and resilience to human disturbances, and so has conservation implications. We collated published and unpublished data from 86 studies across 65 localities to assess titi monkey (Callicebinae) terrestriality. We examined whether the frequency of terrestrial activity correlated with study duration (a proxy for sampling effort), rainfall level (a proxy for food availability seasonality), and forest height (a proxy for vertical niche dimension). Terrestrial activity was recorded frequently for Callicebus and Plecturocebus spp., but rarely for Cheracebus spp. Terrestrial resting, anti-predator behavior, geophagy, and playing frequencies in Callicebus and Plecturocebus spp., but feeding and moving differed. Callicebus spp. often ate or searched for new leaves terrestrially. Plecturocebus spp. descended primarily to ingest terrestrial invertebrates and soil. Study duration correlated positively and rainfall level negatively with terrestrial activity. Though differences in sampling effort and methods limited comparisons and interpretation, overall, titi monkeys commonly engaged in a variety of terrestrial activities. Terrestrial behavior in Callicebus and Plecturocebus capacities may bolster resistance to habitat fragmentation. However, it is uncertain if the low frequency of terrestriality recorded for Cheracebus spp. is a genus-specific trait associated with a more basal phylogenetic position, or because studies of this genus occurred in pristine habitats. Observations of terrestrial behavior increased with increasing sampling effort and decreasing food availability. Overall, we found a high frequency of terrestrial behavior in titi monkeys, unlike that observed in other pitheciids

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.7910COORDENAÇÃO DE APERFEIÇOAMENTO DE PESSOAL DE NÍVEL SUPERIOR - CAPESFUNDAÇÃO DE AMPARO À PESQUISA DO ESTADO DE SÃO PAULO - FAPESPSem informaçãoSem informaçã

Behavioural thermoregulation in a small neotropical primate

Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)The maintenance of body temperature in endothermic animals imposes considerable metabolic costs that vary with air temperature fluctuations. To minimise these costs, endotherms can adopt certain behaviours to adjust the pattern of heat transfer between their bodies and the environment. In this study, we evaluated whether a small Neotropical primate, the black-fronted titi monkey (Callicebus nigrifrons), living in a seasonal environment can use behavioural mechanisms to cope with fluctuations in the air temperature. We monitored the air temperature and the titi monkeys' behaviour over 1yr. When the animals were inactive, we recorded the microhabitat used, the huddling between individuals and the body postures adopted. The monkeys primarily responded to air temperature fluctuations through microhabitat selection: they spent more time in sunny places and used higher strata of forest under lower temperatures. Moreover, they used sunny microhabitats during the first hour of their active period after colder nights. The monkeys did not huddle or change body postures in response to air temperature fluctuations. Huddling behaviour seemed to be primarily influenced by social interactions, and body postures were more energy conserving, regardless of temperature. Titi monkeys, however, used more energy-conserving postures and huddling behaviour under cloudy conditions than sunny conditions, suggesting that these behaviours may be important when they are unable to thermoregulate by microhabitat selection. We concluded that fluctuations in air temperature can promote significant changes in the behaviour of titi monkeys and can impose important restrictions on mammals' activities, even in tropical regions.The maintenance of body temperature in endothermic animals imposes considerable metabolic costs that vary with air temperature fluctuations. To minimise these costs, endotherms can adopt certain behaviours to adjust the pattern of heat transfer between th1204331339FAPESP - FUNDAÇÃO DE AMPARO À PESQUISA DO ESTADO DE SÃO PAULOCAPES - COORDENAÇÃO DE APERFEIÇOAMENTO DE PESSOAL DE NÍVEL SUPERIORFundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)sem informaçãosem informaçãoWe would like to thank the Municipal Secretariat of Planning and Environment of Jundiaí for granting permission to conduct this research at Serra do Japi Municipal Reserve. We also thank J. C. Bicca-Marques, P. S. Oliveira, C. S. Martins and M. B.Nagy-Re

Estimating Primate Population Densities: The Systematic Use Of Playbacks Along Transects In Population Surveys

Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)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 Sao 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.792Sao Paulo Research Foundation FAPESP [2012/14245-2]Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP

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 strategy602113118CAPES - Coordenação de Aperfeiçoamento de Pessoal e Nível SuperiorDAAD - Deutscher Akademischer AustauschdienstFAPESP – Fundação de Amparo à Pesquisa Do Estado De São Paulonão temnão tem2010/04034-9; 2008/05127-0; 2009/12124-

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. © 2015 Wiley Periodicals, Inc

Unraveling the scales of effect of landscape structure on primate species richness and density of titi monkeys (Callicebus nigrifrons)

In the Anthropocene, many animal populations are increasingly confined to human‐modified landscapes, in which different spatial variables describing landscape composition and configuration influence species persistence. Forest specialist species are particularly vulnerable to these landscape disturbances. Yet, landscape effects may be undetected if assessed at the wrong spatial scale. Thus, identifying the “scale of effect”, which is the optimal spatial scale for estimating ecological responses to each landscape variable, is needed to understand the impact of landscape structure modification on species. Here, we explored the scale of effect of two compositional (forest cover and anthropogenic cover) and two configurational landscape variables (forest patch density and forest edge density) on two ecological responses: primate species richness and group densities of titi monkeys (Callicebus nigrifrons). We sampled 16 study sites in northeastern São Paulo State, Brazil. For each site, we measured each landscape variable within 10 different‐sized landscapes ranging from 0.2 to 28.3 km2 to identify the scale of effect of each landscape variable. The strength of all the primate‐landscape relationships varied across spatial scales. Although both ecological responses were most strongly associated with forest cover at the largest scale, the scale of effect of the other landscape variables differed between the response variables. These results suggest that each response variable is shaped by landscape patterns and processes operating across different spatial scales. We highlight the importance of separately assessing the scale of effect of each landscape variable on each ecological response to better understand the impact of landscape structure on species persistence341150159CONSELHO NACIONAL DE DESENVOLVIMENTO CIENTÍFICO E TECNOLÓGICO - CNPQCOORDENAÇÃO DE APERFEIÇOAMENTO DE PESSOAL DE NÍVEL SUPERIOR - CAPESFUNDAÇÃO DE AMPARO À PESQUISA DO ESTADO DE SÃO PAULO - FAPESP312045/2013‐1; 312292/2016‐388881.068425/2014‐02012/14245‐2; 2013/50421‐2The authors are grateful to the landowners for granting permission to collect data on their properties. The authors would like to thank the Empresa Brasileira de Pesquisa Agropecuária and the Forest Institute of the State of São Paulo Environment Department for permission to conduct our research in forest patches from Embrapa Agropecuária Sudeste and in Parque Estadual de Vassununga, respectively. The authors would also like to thank the Zoos of the municipalities of Bauru and Piracicaba for the opportunity to test the recordings with captive animals, and the Forest Institute of the State of São Paulo Environment Department and Duratex Lençóis Paulista for permission to conduct these tests with wild animals in the forest remnants of Jataí Ecological Station and Reserva Natural Olavo Setúbal, respectively. This research was funded by São Paulo Research Foundation (FAPESP, process 2012/14245‐2). We also received field equipment from Idea Wild. M.C.R. thanks to CNPq (Brazilian Government Research Council) for research grants (312045/2013‐1 and 312292/2016‐3), to FAPESP (process 2013/50421‐2) and CAPES (Procad project # 88881.068425/2014‐0) for their financial support. The authors would finally thank B.H. Saranholi for comments on earlier versions of this manuscript, C.B. Caselli for suggestions on statistical analyses, and S. Hongo and an anonymous reviewer for their constructive suggestions that contributed to improve the manuscrip

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 required79219FAPESP - FUNDAÇÃO DE AMPARO À PESQUISA DO ESTADO DE SÃO PAULOFUNDAÇÃO DE AMPARO À PESQUISA DO ESTADO DE MINAS GERAIS - FAPEMIG2012/14245-2sem informaçãoWe thank the Municipal Secretariat of Planning and Environment of Jundiaí, the administration of the Colinas do Atibaia condominium, and C. Knogge for the permission to conduct playback trials at Serra do Japi Municipal Reserve, Ribeirão Cachoeira fores

Testing and optimizing metabarcoding of iDNA from dung beetles to sample mammals in the hyperdiverse Neotropics

Over the past few years, insects have been used as samplers of vertebrate diversity by assessing the ingested-derived DNA (iDNA), and dung beetles have been shown to be a good mammal sampler given their broad feeding preference, wide distribution and easy sampling. Here, we tested and optimized the use of iDNA from dung beetles to assess the mammal community by evaluating if some biological and methodological aspects affect the use of dung beetles as mammal species samplers. We collected 403 dung beetles from 60 pitfall traps. iDNA from each dung beetle was sequenced by metabarcoding using two mini-barcodes (12SrRNA and 16SrRNA). We assessed whether dung beetles with different traits related to feeding, nesting and body size differed in the number of mammal species found in their iDNA. We also tested differences among four killing solutions in preserving the iDNA and compared the effectiveness of each mini barcode to recover mammals. We identified a total of 50 mammal OTUs (operational taxonomic unit), including terrestrial and arboreal species from 10 different orders. We found that at least one mammal-matching sequence was obtained from 70% of the dung beetle specimens. The number of mammal OTUs obtained did not vary with dung beetle traits as well as between the killing solutions. The 16SrRNA mini-barcode recovered a higher number of mammal OTUs than 12SrRNA, although both sets were partly non-overlapping. Thus, the complete mammal diversity may not be achieved by using only one of them. This study refines the methodology for routine assessment of tropical mammal communities via dung beetle ‘samplers’ and its universal applicability independently of the species traits of local beetle communities