Influência de atributos da paisagem na ocorrência de primatas e densidade de Callicebus nigrifrons no nordeste do Estado de São Paulo

Orientadores: Eleonore Zulnara Freire Setz, Rogério Grassetto Teixeira da CunhaTese (doutorado) - Universidade Estadual de Campinas, Instituto de BiologiaResumo: O processo de fragmentação da paisagem e redução da cobertura vegetal, potencializado pela expansão das atividades humanas, é hoje a maior ameaça à biodiversidade. As espécies especialistas florestais, como os primatas Neotropicais, estão entre as mais vulneráveis a esta mudança. No nordeste do estado de São Paulo, cuja vegetação sofre intensa redução e fragmentação, bugio-preto (Alouatta caraya), macaco-prego (Sapajus nigritus), sauá (Callicebus nigrifrons), e mico-estrela (Callithrix penicillata) ocorrem em simpatria. Nós estudamos a influência da estrutura da paisagem sobre essas espécies. Para isso, fizemos levantamentos da ocorrência das espécies em 17 fragmentos florestais e, nos locais onde detectamos a presença de sauá, realizamos estimativas de sua densidade populacional e avaliamos seu comportamento vocal em resposta ao estímulo de playback. Primeiramente, avaliamos o tamanho da paisagem (escala de efeito dentre paisagens de 0,2 a 28,3 km²) que melhor prediz as respostas dos primatas às variações em atributos da paisagem. Em seguida, testamos quais atributos influenciam a riqueza de espécies, a densidade de sauás e o comportamento vocal dos sauás (representando seu comportamento de defesa de recursos). As respostas dos primatas às alterações na estrutura da paisagem são dependentes da escala, que varia de acordo com o atributo da paisagem e resposta biológica avaliada. A riqueza de espécies esteve associada ao tipo de vegetação do fragmento focal e negativamente à quantidade de cobertura florestal e de borda florestal presente na paisagem. A complexidade estrutural e maior diversidade de plantas no fragmento focal possivelmente possibilita a coexistência de maior número de espécies. Além disso, a probabilidade de registro dessas espécies no fragmento avaliado é maior quando a paisagem apresenta menor disponibilidade de hábitat. A densidade de sauás foi negativamente afetada pela cobertura florestal na paisagem, relação potencializada pelo grau de fragmentação do hábitat. Este cenário, em curto prazo, pode levar a um adensamento dos indivíduos no pouco hábitat disponível. Tal aumento de densidade pode ser favorecido também por outros processos, por exemplo, a diminuição da taxa de predação. Porém, em longo prazo, essa situação pode ter um efeito negativo para a população e, portanto, deve ser avaliada com cuidado. Além disso, o comportamento vocal dos sauás foi mais intenso nos fragmentos inseridos em paisagens com maior cobertura florestal, sugerindo que a disponibilidade de recursos florestais na paisagem pode influenciar o seu comportamento de defesa de recursos. Portanto, a estrutura da paisagem afetou os primatas em vários níveis, desde seu comportamento até dinâmicas populacionais e de comunidadeAbstract: Currently, the habitat loss and fragmentation, driven by intense human land use, is the main threat to biodiversity. Forest specialists, such as the Neotropical primates, are particularly vulnerable to changes in landscape structure. In the northeast of São Paulo State, region under intense fragmentation and deforestation, four species (Alouatta caraya, Sapajus nigritus, Callicebus nigrifrons, and Callithrix penicillata) occur in sympatry. We evaluated the influence of landscape attributes on these primate species. We surveyed 17 forest patches to determine the presence of primates species, and where titi monkeys (C. nigrifrons) were detected we estimated titi monkeys density and evaluated their respose to playback stimlus. Firstly, we evaluated the landscape size (scale of effect) that best predicted the primates responses to changes in landscape attributes. After that, we tested the influence of landscape structure on species richness, titi monkeys density, and titi monkeys¿ vocal behavior (representing their resource defense behavior). Primates response to landscape change are scale dependent, having strong effects in different spatial scales according to the landscape variables and biological response evaluated. Species richness was strongly associated to the vegetation type of focal patch and negatively to the forest cover and forest edge density. The structural complexity and higher plant diversity in the focal patch possibly support a high number of species. Moreover, the probability of registering a species in the focal patches is increased in landscapes with low habitat availability. Titi monkeys density was strong and negatively affected by landscape forest cover, a relationship potentiated by the magnitude of forest partitioning. In the short term, this landscape features can lead to an increase in the number of individuals in the few remnants. But, this increase of animals density can also be promoted by other processes occurring under this landscape scenario, such as the reduction on predation rate. However, the increase of primates density should be observed with cautions, because in the long term this situation can have a negative effect to the species. Besides, the forest cover also influenced the titi monkeys¿ vocal behavior, which increased according to the increment of forest cover in the landscapes. This behavioral response suggests that resource availability in the landscape may influence the resource defense behavior of primates species. Therefore, landscape structure affected primates in different levels, from behavioral patterns to population dynamics and communityDoutoradoEcologiaDoutora em Ecologia2012/14245-2FAPES

Interspecific Genetic Differences and Historical Demography in South American Arowanas (Osteoglossiformes, Osteoglossidae, Osteoglossum)

The South American arowanas (Osteoglossiformes, Osteoglossidae, Osteoglossum) are emblematic species widely distributed in the Amazon and surrounding basins. Arowana species are under strong anthropogenic pressure as they are extensively exploited for ornamental and food purposes. Until now, limited genetic and cytogenetic information has been available, with only a few studies reporting to their genetic diversity and population structure. In the present study, cytogenetic and DArTseq-derived single nucleotide polymorphism (SNP) data were used to investigate the genetic diversity of the two Osteoglossum species, the silver arowana O. bicirrhosum, and the black arowana O. ferreirai. Both species differ in their 2n (with 2n = 54 and 56 for O. ferreirai and O. bicirrhosum, respectively) and in the composition and distribution of their repetitive DNA content, consistent with their taxonomic status as different species. Our genetic dataset was coupled with contemporary and paleogeographic niche modeling, to develop concurrent demographic models that were tested against each other with a deep learning approach in O. bicirrhosum. Our genetic results reveal that O. bicirrhosum colonized the Tocantins-Araguaia basin from the Amazon basin about one million years ago. In addition, we highlighted a higher genetic diversity of O. bicirrhosum in the Amazon populations in comparison to those from the Tocantins-Araguaia basin. © 2019 by the authors. Licensee MDPI, Basel, Switzerland

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

Temperature influence on ecology and behavior of Callicebus nigrifrons (Primates: Pithecilidae)

Orientadora: Eleonore Zulnara Freire SetzDissertação (mestrado) - Universidade Estadual de Campinas, Instituto de BiologiaResumo: A alteração das necessidades energéticas dos endotérmicos pela variação da temperatura ambiental devido aos custos da termorregulação pode influenciar seu comportamento. O objetivo desse estudo foi investigar a influência da temperatura nos comportamentos de sauás (Callicebus nigrifrons) na Serra do Japi, região com marcada sazonalidade e temperatura reduzida pela altitude. Para isso, relacionamos com a temperatura: o padrão de atividade, os itens alimentares e os comportamentos termorregulatórios durante o descanso (seleção de micro-hábitat, contato entre os indivíduos e postura corporal). Quanto menores as temperaturas mínimas noturnas, o que pode representar estresse térmico, os sauás iniciaram suas atividades mais tardiamente, no momento em que a temperatura ambiental já estava elevada. A distância percorrida diariamente não variou com a temperatura, mas os sauás locomoveram mais no início do dia, horário mais frio, coincidindo com o início das atividades. Entre os meses, a locomoção foi menor nos mais frios, possivelmente resultando em economia de energia. Não houve seleção por itens alimentares mais calóricos em temperaturas baixas. Entretanto, houve aumento no forrageio nos meses mais frios (não relacionado com a disponibilidade de frutos), compatível com a ideia de que os custos da termorregulação podem influenciar a ingestão de alimentos. A seleção de locais ao sol foi maior em temperaturas baixas, e tal comportamento pode estar reduzindo os custos da termorregulação com o aumento da absorção de calor da radiação solar. O contato entre os indivíduos ao longo do dia não teve relação com a temperatura e pode ter sido influenciado somente pelas interações sociais. A postura não variou em função da temperatura e aquelas que resultavam em menor perda de calor para o meio foram predominantemente adotadas. Isso, provavelmente, devido ao porte pequeno da espécie (elevada razão superfície/volume) que contribui para maior perda de calor nas baixas temperaturas registradas. Conclui-se que os sauás apresentam variação comportamental em função da temperatura ambiental quanto à escolha de micro-hábitats e padrão de locomoção e forrageioAbstract: Variations in ambient temperature can change the energy requirements of endothermics due to costs of thermoregulation. So, ambient temperature can influence animal's behavior. The aim of this work was to investigate ambient temperature influence on wild black-fronted titi monkeys (Callicebus nigrifrons) behavior. We conducted this study in Serra do Japi, region with marked seasonality and temperature reduced due to high altitude. We analyzed the relation between temperature and the following variables: activity pattern, types of food consumed and thermoregulatory behaviors observed during resting (microhabitat selection, contact between individuals and body posture). In lower night minimum temperatures, which may represent thermal stress to titi monkey, they started their activities later in the day, after ambient temperature increase. There was no correlation between path length and ambient temperature, but titis moved more at beginning of the day (at the coldest hours), when they were starting these activities. During the coldest months, titis moved less, which could be a strategy to save energy. During this period, they did not select higher-calorie food items, but there was an increase in foraging behavior (not related to fruit availability), which is consistent with the idea that the energy costs of thermoregulation can influence food intake. The sunny resting places were selected at low temperatures. This behavior could be used to reduce thermoregulation costs, allowing the increase of heat absorption from solar radiation. The contact between individuals throughout the day was not related to the temperature and may be influenced only by social interactions. Body postures were not influenced by ambient temperature and postures that avoid heat loss were predominantly adopted. This is probably due to the small size of the species (considering the high surface/volume ratio) which contributes to greater heat loss at low temperatures. We concluded that titi monkey's behaviors vary in function of ambient temperature, such as microhabitat choice and pattern of moving and foragingMestradoEcologiaMestre em Ecologi

From dropping to dropping: the contribution of a small primate to seed dispersal in Atlantic forest

The dynamic interaction between animals and plants through frugivory and seed dispersal is one of several ecological processes that modulates tropical biodiversity. Here we evaluated the potential role of a highly-frugivorous Neotropical primate, the black-fronted titi monkey (Callicebus nigrifrons), as seed disperser. We studied two titi monkey groups in semideciduous Atlantic Forest remnants. Each group fed on over 49 zoochorous plant species in about one year and ingested seeds from nearly a half of them, especially those with small seeds (< 0.5 cm). The groups of titi monkeys defecated a large number of seeds, reaching over 300 seeds per day (1-305). More than half of the total deposited seeds and seed species germinated after gut passage, however gut passage reduced germination success in three of five evaluated species. Feces were deposited in small clumps distributed across groups' home range. We suggest that the observed distribution pattern of feces may enhance plant reproductive fitness by increasing the probability of seeds being deposited far from parent plants, in novel and favorable sites. We concluded that the seed handling and deposition behavior of black-fronted titi monkey make this primate an important agent for Atlantic forest regeneration100CAPES - Coordenação de Aperfeiçoamento de Pessoal e Nível SuperiorFAPESP – Fundação de Amparo à Pesquisa Do Estado De São Paulosem informação2008/05127-0; 2010/04034-9; 2009/12124-

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

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

AbstractOver 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

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

NEOTROPICAL XENARTHRANS: a data set of occurrence of xenarthran species in the Neotropics

Xenarthrans—anteaters, sloths, and armadillos—have essential functions forecosystem maintenance, such as insect control and nutrient cycling, playing key roles as ecosys-tem engineers. Because of habitat loss and fragmentation, hunting pressure, and conflicts withdomestic dogs, these species have been threatened locally, regionally, or even across their fulldistribution ranges. The Neotropics harbor 21 species of armadillos, 10 anteaters, and 6 sloths.Our data set includes the families Chlamyphoridae (13), Dasypodidae (7), Myrmecophagidae(3), Bradypodidae (4), and Megalonychidae (2). We have no occurrence data onDasypus pilo-sus(Dasypodidae). Regarding Cyclopedidae, until recently, only one species was recognized,but new genetic studies have revealed that the group is represented by seven species. In thisdata paper, we compiled a total of 42,528 records of 31 species, represented by occurrence andquantitative data, totaling 24,847 unique georeferenced records. The geographic range is fromthe southern United States, Mexico, and Caribbean countries at the northern portion of theNeotropics, to the austral distribution in Argentina, Paraguay, Chile, and Uruguay. Regardinganteaters,Myrmecophaga tridactylahas the most records (n=5,941), andCyclopessp. havethe fewest (n=240). The armadillo species with the most data isDasypus novemcinctus(n=11,588), and the fewest data are recorded forCalyptophractus retusus(n=33). Withregard to sloth species,Bradypus variegatushas the most records (n=962), andBradypus pyg-maeushas the fewest (n=12). Our main objective with Neotropical Xenarthrans is to makeoccurrence and quantitative data available to facilitate more ecological research, particularly ifwe integrate the xenarthran data with other data sets of Neotropical Series that will become available very soon (i.e., Neotropical Carnivores, Neotropical Invasive Mammals, andNeotropical Hunters and Dogs). Therefore, studies on trophic cascades, hunting pressure,habitat loss, fragmentation effects, species invasion, and climate change effects will be possiblewith the Neotropical Xenarthrans data set. Please cite this data paper when using its data inpublications. We also request that researchers and teachers inform us of how they are usingthese data

NEOTROPICAL ALIEN MAMMALS: a data set of occurrence and abundance of alien mammals in the Neotropics

Biological invasion is one of the main threats to native biodiversity. For a species to become invasive, it must be voluntarily or involuntarily introduced by humans into a nonnative habitat. Mammals were among first taxa to be introduced worldwide for game, meat, and labor, yet the number of species introduced in the Neotropics remains unknown. In this data set, we make available occurrence and abundance data on mammal species that (1) transposed a geographical barrier and (2) were voluntarily or involuntarily introduced by humans into the Neotropics. Our data set is composed of 73,738 historical and current georeferenced records on alien mammal species of which around 96% correspond to occurrence data on 77 species belonging to eight orders and 26 families. Data cover 26 continental countries in the Neotropics, ranging from Mexico and its frontier regions (southern Florida and coastal-central Florida in the southeast United States) to Argentina, Paraguay, Chile, and Uruguay, and the 13 countries of Caribbean islands. Our data set also includes neotropical species (e.g., Callithrix sp., Myocastor coypus, Nasua nasua) considered alien in particular areas of Neotropics. The most numerous species in terms of records are from Bos sp. (n = 37,782), Sus scrofa (n = 6,730), and Canis familiaris (n = 10,084); 17 species were represented by only one record (e.g., Syncerus caffer, Cervus timorensis, Cervus unicolor, Canis latrans). Primates have the highest number of species in the data set (n = 20 species), partly because of uncertainties regarding taxonomic identification of the genera Callithrix, which includes the species Callithrix aurita, Callithrix flaviceps, Callithrix geoffroyi, Callithrix jacchus, Callithrix kuhlii, Callithrix penicillata, and their hybrids. This unique data set will be a valuable source of information on invasion risk assessments, biodiversity redistribution and conservation-related research. There are no copyright restrictions. Please cite this data paper when using the data in publications. We also request that researchers and teachers inform us on how they are using the data