Mammals in São Paulo State: diversity, distribution, ecology, and conservation / Mamíferos do Estado de São Paulo: diversidade, distribuição, ecologia e conservação

Abstract Mammals are charismatic organisms that play a fundamental role in ecological functions and ecosystem services, such as pollination, seed dispersal, nutrient cycling, and pest control. The state of São Paulo represents only 3% of the Brazilian territory but holds 33% of its mammalian diversity. Most of its territory is dominated by agriculture, pastures, and urban areas which directly affect the diversity and persistence of mammals in the landscape. In addition, São Paulo has the largest port in Latin America and the largest offshore oil reservoir in Brazil, with a 600 km stretch of coastline with several marine mammal species. These human-made infrastructures affect the diversity, distribution, ecology, and the future of mammals in the state. Here, we answer five main questions: 1) What is the diversity of wild mammals in São Paulo state? 2) Where are they? 3) What is their positive and negative impact on human well-being? 4) How do mammals thrive in human-modified landscapes? 5) What is the future of mammals in the state? The state of São Paulo holds 255 species of native mammals, with four endemic species, two of them globally endangered. At least six species (two marsupials, Giant otter, Pampas deer, Brazilian dwarf brocket deer, and Giant armadillo) were extirpated from the state due to hunting and habitat loss. The intense human land use in the state forced many mammalian species to change their diet to cope with the intense fragmentation and agriculture. Large-scale monoculture has facilitated the invasion of exotic species such as wild boars (javali) and the European hare. Several "savanna-dwelling" species are expanding their ranges (Maned wolf, Brocket deer) over deforested areas and probably reflect changes towards a drier climate. Because the state has the largest road system, about 40,000 mammals from 33 species are killed per year in collisions causing an economic loss of 12 million dollars/year. The diversity of mammals is concentrated in the largest forest remnants of Serra do Mar and in the interior of the State, mainly in the regions of Ribeirão Preto and Jundiaí. Sampling gaps are concentrated throughout the interior of the state, particularly in the northwest region. Wild mammals play a fundamental role in many ecosystem services, but they can also be a concern in bringing new emergent diseases to humans. Although the taxonomy of mammals seems to be well known, we show that new species are continuously being discovered in the state. Therefore, continuous surveys using traditional and new technologies (eDNA, iDNA, drones), long-term population monitoring, investigation of the interface of human-wildlife conflict, and understanding of the unique ecosystem role played by mammals are future avenues for promoting sustainable green landscapes allied to human well-being in the state. The planting of forest or savanna corridors, particularly along with major river systems, in the plateau, controlling illegal hunting in the coastal areas, managing fire regimes in the Cerrado, and mitigating roadkill must be prioritized to protect this outstanding mammal diversity.

Resumo Os mamíferos são organismos carismáticos que desempenham um papel fundamental na função ecológica e nos serviços ecossistêmicos, como polinização, dispersão de sementes, ciclagem de nutrientes e controle de pragas. O Estado de São Paulo representa apenas 3% do território brasileiro, mas detém 33% da diversidade de mamíferos. A maior parte de seu território é dominado pela agricultura, pastagens e áreas urbanas que afetam diretamente a diversidade e a persistência dos mamíferos na paisagem. Além disso, São Paulo possui o maior porto da América Latina e o maior reservatório de petróleo costeiro do Brasil, com 600 km de extensão de litoral com diversas espécies de mamíferos marinhos. Essas infraestruturas afetam a diversidade, distribuição, ecologia e o futuro dos mamíferos no estado. Aqui, respondemos cinco perguntas principais: 1) Qual é a diversidade de mamíferos silvestres no Estado de São Paulo? 2) Onde eles ocorrem? 3) Qual é o seu impacto positivo e negativo no bem-estar humano? 4) Como os mamíferos persistem em paisagens modificadas pelo homem? 5) Qual é o futuro dos mamíferos no estado? O estado de São Paulo possui 255 espécies de mamíferos nativos, com quatro espécies endêmicas, duas delas globalmente ameaçadas de extinção. Pelo menos seis espécies (dois marsupiais, ariranha, veado-campeiro, veado-cambuta e tatu-canastra) foram extirpadas do estado devido à caça e perda de habitat. O intenso uso humano da terra no estado forçou muitas espécies de mamíferos a mudar sua dieta para lidar com a intensa fragmentação e agricultura. A monocultura em larga escala facilitou a invasão de espécies exóticas, como porcos selvagens (javaporco) e a lebre europeia. Várias espécies de áreas abertas estão expandindo suas áreas de distribuição (lobo-guará, veado-catingueiro) sobre áreas desmatadas e provavelmente refletem mudanças em direção a um clima mais seco. Como o estado possui o maior sistema rodoviário do Brasil, cerca de 40 mil mamíferos de 33 espécies são mortos por ano em colisões, causando um prejuízo econômico de 12 milhões de dólares/ano. A diversidade de mamíferos está concentrada nos maiores remanescentes florestais da Serra do Mar e no interior do Estado, principalmente nas regiões de Ribeirão Preto e Jundiaí. As lacunas amostrais estão concentradas em todo o interior do estado, principalmente na região noroeste. Os mamíferos silvestres desempenham um papel fundamental em muitos serviços ecossistêmicos, mas também podem ser uma preocupação em trazer novas doenças emergentes para as populações humanas. Embora a taxonomia de mamíferos pareça ser bem conhecida, mostramos que novas espécies estão sendo continuamente descobertas no estado. Portanto, pesquisas usando tecnologias tradicionais e novas (eDNA, iDNA, drones), monitoramento populacional de longo prazo, a investigação da interface do conflito homem-vida selvagem e a compreensão do papel único no ecossistema desempenhado pelos mamíferos são um caminho futuro para promover uma paisagem verde sustentável aliada ao bem-estar humano no estado. O plantio de corredores florestais ou de cerrado, principalmente junto aos principais sistemas fluviais, no planalto, o controle da caça ilegal nas áreas costeiras, o manejo dos regimes de fogo no Cerrado e a mitigação dos atropelamentos devem ser uma prioridade para proteger essa notável diversidade de mamíferos.

Common opossum population density in an agroforestry system in Bolivia

The common opossum, Didelphis marsupialis thrives near human settlements. Understanding its ecology could help planning management decisions about this species, especially in anthropogenic landscapes. Yet, there are no density estimations for this species throughout its distribution range in Bolivia. We estimated the density of D. marsupialis in a rural agricultural community, where agroforestry plantations and fallows cover most of the land. We counted individuals in line transects and used DISTANCE software to calculate density. We covered a total of 70.21 km in 143 night counts, obtaining 38 records of D. marsupialis. We estimated a density of 0.30 individuals ha-1 (SE = 0.062; range: 0.20 - 0.45 individuals ha-1), with a mean encounter rate of 0.54 individuals km-1. Encounter rate varied between habitats, with mean values of 0.20 in secondary forests and 0.64 in agroforestry plantations. Our density estimate is near the lower range of previously reported values for the common opossum in other countries. We argue that our results may reflect the response to the availability of food resources and predation pressure in agroforestry plantations. (AU)

Common opossum population density in an agroforestry system in Bolivia / Densidad de carachupas en un sistema agroforestal de Bolivia

La carachupa, Didelphis marsupialis prospera cerca de asentamientos humanos. Entender la ecología de una población puede ayudar a tomar decisiones de manejo de esta especie, especialmente en paisajes antropogénicos. Sin embargo, no existen estimaciones de la densidad de esta especie en todo su rango de distribución en Bolivia. Este estudio estimó la densidad de D. marsupialis en una comunidad agrícola, donde los sistemas agroforestales y barbechos cubren la mayoría de la tierra. Empleamos conteos en transectos lineales y usamos el programa DISTANCE para calcular la densidad. En total recorrimos 70.21 km en 143 noches de conteo y obtuvimos 38 registros de D. marsupialis. Estimamos una densidad de 0.30 individuos ha-1 (SE = 0.062; rango: 0.20 - 0.45 individuos ha-1) y una tasa de encuentro promedio de 0.54 individuos km-1. La tasa de encuentro varió entre hábitats, con valores promedio de 0.2 para bosque secundario y 0.64 para sistemas agroforestales. Nuestra estimación de densidad se encuentra cerca de los valores más bajos antes reportados para la especie en otros países. Creemos que nuestros resultados reflejan la respuesta a la disponibilidad de recursos en sistemas agroforestales y la presión de depredación en nuestro sitio de estudio.(AU)

The common opossum, Didelphis marsupialis thrives near human settlements. Understanding its ecology could help planning management decisions about this species, especially in anthropogenic landscapes. Yet, there are no density estimations for this species throughout its distribution range in Bolivia. We estimated the density of D. marsupialis in a rural agricultural community, where agroforestry plantations and fallows cover most of the land. We counted individuals in line transects and used DISTANCE software to calculate density. We covered a total of 70.21 km in 143 night counts, obtaining 38 records of D. marsupialis. We estimated a density of 0.30 individuals ha-1 (SE = 0.062; range: 0.20 - 0.45 individuals ha-1), with a mean encounter rate of 0.54 individuals km-1. Encounter rate varied between habitats, with mean values of 0.20 in secondary forests and 0.64 in agroforestry plantations. Our density estimate is near the lower range of previously reported values for the common opossum in other countries. We argue that our results may reflect the response to the availability of food resources and predation pressure in agroforestry plantations.(AU)

ATLANTIC BIRDS: a data set of bird species from the Brazilian Atlantic Forest.

South America holds 30% of the world's avifauna, with the Atlantic Forest representing one of the richest regions of the Neotropics. Here we have compiled a data set on Brazilian Atlantic Forest bird occurrence (150,423) and abundance samples (N = 832 bird species; 33,119 bird individuals) using multiple methods, including qualitative surveys, mist nets, point counts, and line transects). We used four main sources of data: museum collections, on-line databases, literature sources, and unpublished reports. The data set comprises 4,122 localities and data from 1815 to 2017. Most studies were conducted in the Florestas de Interior (1,510 localities) and Serra do Mar (1,280 localities) biogeographic sub-regions. Considering the three main quantitative methods (mist net, point count, and line transect), we compiled abundance data for 745 species in 576 communities. In the data set, the most frequent species were Basileuterus culicivorus, Cyclaris gujanensis, and Conophaga lineata. There were 71 singletons, such as Lipaugus conditus and Calyptura cristata. We suggest that this small number of records reinforces the critical situation of these taxa in the Atlantic Forest. The information provided in this data set can be used for macroecological studies and to foster conservation strategies in this biodiversity hotspot. No copyright restrictions are associated with the data set. Please cite this Data Paper if data are used in publications and teaching events.

Assessing the population density of the spotted paca, Cuniculus paca, (Rodentia: Cuniculidae) on an Atlantic Forest island, southeastern Brazil

The spotted paca, Cuniculus paca (Linnaeus, 1766), is a Neotropical, opportunistic, frugivorous caviomorph rodent, that inhabits primarily broadleaf forests. We aimed to provide the first estimates of density of C. paca for the Ilha Grande, an island located in the Atlantic Rain Forest biome of Brazil. Density and population size were estimated using the total number of individuals observed along each trail through the program DISTANCE 7. Our estimates of density and population size reinforces the importance of the Ilha Grande as an important reservoir of the species. Therefore, the results presented herein can be a starting point to support future action plans for the species, making predictions regarding the ecosystem and management and conservation of the spotted paca. Furthermore, the results can be used as a surrogate for other regions in which the species occurs.

Assessing the population density of the spotted paca, Cuniculus paca, (Rodentia: Cuniculidae) on an Atlantic Forest island, southeastern Brazil

The spotted paca, Cuniculus paca (Linnaeus, 1766), is a Neotropical, opportunistic, frugivorous caviomorph rodent, that inhabits primarily broadleaf forests. We aimed to provide the first estimates of density of C. paca for the Ilha Grande, an island located in the Atlantic Rain Forest biome of Brazil. Density and population size were estimated using the total number of individuals observed along each trail through the program DISTANCE 7. Our estimates of density and population size reinforces the importance of the Ilha Grande as an important reservoir of the species. Therefore, the results presented herein can be a starting point to support future action plans for the species, making predictions regarding the ecosystem and management and conservation of the spotted paca. Furthermore, the results can be used as a surrogate for other regions in which the species occurs.(AU)

Biological traits, rather than environment, shape detection curves of large vertebrates in neotropical rainforests.

Line transect surveys are widely used in Neotropical rainforests to estimate the population abundance of medium- and large-sized vertebrates. The use of indices such as encounter rate has been criticized because the probability of animal detection may fluctuate due to the heterogeneity of environmental conditions among sites. In addition, the morphological and behavioral characteristics (biological traits) of species affect their detectability. In this study, we compared the extent to which environmental conditions and species' biological traits bias abundance estimates in terra firme rainforests in French Guiana. The selected environmental conditions included both physical conditions and forest structure covariates, while the selected biological traits included the morphological and behavioral characteristics of species. We used the distance sampling method to model the detection probability as an explicit function of environmental conditions and biological traits and implemented a model selection process to determine the relative importance of each group of covariates. Biological traits contributed to the variability of animal detectability more than environmental conditions, which had only a marginal effect. Detectability was best for large animals with uniform or disruptive markings that live in groups in the canopy top. Detectability was worst for small, solitary, terrestrial animals with mottled markings. In the terra firme rainforests that represent ~80% of the Amazonia and Guianas regions, our findings support the use of relative indices such as the encounter rate to compare population abundance between sites in species-specific studies. Even though terra firme rainforests may appear similar between regions of Amazonia and the Guianas, comparability must be ensured, especially in forests disturbed by human activity. The detection probability can be used as an indicator of species' vulnerability to hunting and, thus, to the risk of local extinction. Only a few biological trait covariates are required to correctly estimate the detectability of the majority of medium- and large-sized vertebrates. Thus, a biological trait model could be useful in predicting the detection probabilities of rare, uncommon, or localized species for which few data are available to fit the detection function.

Population density and primate conservation in the Noroeste Biosphere Reserve, Tumbes, Peru / Densidad poblacional y conservación de los primates de la Reserva de Biosfera del Noroeste, Tumbes, Perú

The Noroeste Biosphere Reserve (NBR) is home to at least 22 species of medium and large mammals including the primates Alouatta palliata aequatorialis and Cebus albifrons aequatorialis. Previous estimates of A. p. aequatorialis population density vary from 2.3-8.6 ind/km² in 1983 to 17-19 ind/km² in 2005 and 2006, respectively. While for C. a. aequatorialis there are no estimates of population density in the NBR. In order to calculate the population density estimates for both species we installed six transects in 10.5 km² within the Cerros de Amotape National Park (belonging to the NBR) from August 2012 to March 2013. Based on 112.3 km of transects we obtained a population density of 8.3 ± 3.6 ind/km² for A. p. aequatorialis. However, for the reduced number of Cebus albifrons aequatorialis sightings we were only able to calculate a group size from three to 12 individuals and an encounter rate of 0.3 ind/km. Even though A. p. aequatorialis has potentially increased in population density, it is not feasible to make comparisons with previous estimates in the same area because of the different employed methodologies and the lack of randomness in the data collection. We recommend a long-term monitoring plan, including C. a. aequatorialis which makes it a conservation priority for the NBR, this monitoring plan should include mitigation of potential threats such as illegal hunting and trapping for the pet trade.

La Reserva de Biósfera del Noroeste (RBN) alberga por lo menos 22 especies de mamíferos medianos y grandes entre las cuales se encuentran los primates Alouatta palliata aequatorialis y Cebus albifrons aequatorialis. Los estimados previos de la densidad poblacional de A. p. aequatorialis varían de 2.3‒8.6 ind/km² en 1983 a 17‒19 ind/km² en 2005 y 2006, respectivamente. Mientras que para C. a. aequatorialis no existen estimados poblacionales para la RBN. Para calcular la densidad poblacional de estas dos especies instalamos seis transectos lineales en 10.5 km² dentro del Parque Nacional Cerros de Amotape (perteneciente a la RBN) de agosto del 2012 a marzo del 2013. En base a 112.3 km de transectos se obtuvo una densidad poblacional de 8.3 ± 3.6 ind/km² para A. p. aequatorialis; sin embargo, por el reducido número de avistamientos de Cebus albifrons aequatorialis solo se pudo calcular el tamaño de grupo que varió de tres a 12 individuos y la tasa de encuentro de 0.3 ind/km. A pesar que la población del A. p. aequatorialis aparentemente ha aumentado, no es factible hacer comparaciones con los estimados anteriores debido a las diferentes metodologías empleadas y a la falta de aleatoriedad en la toma de datos. Recomendamos un plan de monitoreo a largo plazo, que incluya a C. a. aequatorialis como objeto y prioridad de conservación para la RBN, el cual debería incluir la mitigación de posibles amenazas como caza y captura para comercio de mascotas.

Diversidade de mamíferos de médio e grande porte da região do rio Urucu, Amazonas, Brasil / Diversity of medium and large sized mammals in the Urucu basin, Amazonas, Brazil

Entre abril de 2008 e maio de 2009 foram realizadas expedições para o estudo sobre a riqueza, a composição e a abundância relativa dos mamíferos de médio e grande porte na região do rio Urucu (Amazonas, Brasil). Foram empregados três métodos de amostragem: censo por transecção linear, busca ativa por vestígios e armadilhas fotográficas. No total foram registradas 41 espécies de mamíferos pertencentes a 17 famílias e oito ordens. As ordens com maior riqueza foram Primates, com 13 espécies registradas, e Carnivora, com 11 espécies registradas. Entre os grupos mais abundantes se destacaram as ordens Primates, Perissodactyla, Artiodactyla e Rodentia. A alta diversidade de espécies de mamíferos de médio e grande porte encontrada em Urucu reforça a importância desta região para a conservação da mastofauna amazônica.

Between April 2008 and May 2009, studies on the species richness, composition and relative abundance of the medium and large sized mammals were carried out in the Urucu basin (Brazilian Amazon). The survey was conducted using line transect sampling method, active search for signs and camera-traps. A total of 41 species of 17 families and eight orders were recorded. Primates was the group with the highest species richness in sympatry (13 species), followed by carnivores (11 species). Primates, Perissodactyla, Artiodactyla and Rodentia were the most abundant groups. The high diversity of medium and large sized mammals presented here indicates the importance of the region for mammals conservation in Amazonia.

Hyper abundant mesopredators and bird extinction in an Atlantic forest island

Islands can serve as model systems for understanding how biological invasions affect native species. Here we examine the negative effects of mesopredator mammals on bird richness at Anchieta Island, an 826 ha offshore island in the coast of Brazil. Anchieta Island has the highest density of mammals of the entire Atlantic forest, especially nest predators such as marmosets and coatis, introduced more than 20 years ago. This indiscriminate introduction of mammals may have affected directly the bird community, nowadays represented by 100 species comprised mainly by water-crossing birds, being 73 forest-dwelling species. A small component of these remnant bird species nests in tree holes and on the forest floor, null model analysis suggest that birds within these two nest types are under-represented on Anchieta Island. All guilds were affected negatively, but "opportunist insectivorous/omnivorous". Experiments using artificial nests showed a predation of 73% of nests on the floor while only 26% on the mainland. Camera traps recorded predation by coatis, agoutis, and opossums. The restoration of the bird community on this island is highly constrained by the high density of hyper abundant nest predators.

Hyper abundant mesopredators and bird extinction in an Atlantic forest island

Islands can serve as model systems for understanding how biological invasions affect native species. Here we examine the negative effects of mesopredator mammals on bird richness at Anchieta Island, an 826 ha offshore island in the coast of Brazil. Anchieta Island has the highest density of mammals of the entire Atlantic forest, especially nest predators such as marmosets and coatis, introduced more than 20 years ago. This indiscriminate introduction of mammals may have affected directly the bird community, nowadays represented by 100 species comprised mainly by water-crossing birds, being 73 forest-dwelling species. A small component of these remnant bird species nests in tree holes and on the forest floor, null model analysis suggest that birds within these two nest types are under-represented on Anchieta Island. All guilds were affected negatively, but "opportunist insectivorous/omnivorous". Experiments using artificial nests showed a predation of 73% of nests on the floor while only 26% on the mainland. Camera traps recorded predation by coatis, agoutis, and opossums. The restoration of the bird community on this island is highly constrained by the high density of hyper abundant nest predators.

Hyper abundant mesopredators and bird extinction in an Atlantic forest island

Islands can serve as model systems for understanding how biological invasions affect native species. Here we examine the negative effects of mesopredator mammals on bird richness at Anchieta Island, an 826 ha offshore island in the coast of Brazil. Anchieta Island has the highest density of mammals of the entire Atlantic forest, especially nest predators such as marmosets and coatis, introduced more than 20 years ago. This indiscriminate introduction of mammals may have affected directly the bird community, nowadays represented by 100 species comprised mainly by water-crossing birds, being 73 forest-dwelling species. A small component of these remnant bird species nests in tree holes and on the forest floor, null model analysis suggest that birds within these two nest types are under-represented on Anchieta Island. All guilds were affected negatively, but "opportunist insectivorous/omnivorous". Experiments using artificial nests showed a predation of 73% of nests on the floor while only 26% on the mainland. Camera traps recorded predation by coatis, agoutis, and opossums. The restoration of the bird community on this island is highly constrained by the high density of hyper abundant nest predators.