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.

Seascape Genetics of the Atlantic Spotted Dolphin (Stenella frontalis) Based on Mitochondrial DNA.

The Atlantic spotted dolphin (Stenella frontalis) is endemic to tropical, subtropical, and warm temperate waters of the Atlantic Ocean. Throughout its distribution, both geographic distance and environmental variation may contribute to population structure of the species. In this study, we follow a seascape genetics approach to investigate population differentiation of Atlantic spotted dolphins based on a large worldwide dataset and the relationship with marine environmental variables. The results revealed that the Atlantic spotted dolphin exhibits population genetic structure across its distribution based on mitochondrial DNA control region (mtDNA-CR) data. Analyses based on the contemporary landscape suggested, at both the individual and population level, that the population genetic structure is consistent with the isolation-by-distance model. However, because geography and environmental matrices were correlated, and because in some, but not all analyses, we found a significant effect for the environment, we cannot rule out the addition contribution of environmental factors in structuring genetic variation. Future analyses based on nuclear data are needed to evaluate whether local processes, such as social structure and some level of philopatry within populations, may be contributing to the associations among genetic structure, geographic, and environmental distance.

Cetacean movements in coastal waters of the southwestern Atlantic ocean / Movimentos de cetáceos pelas águas costeiras do sudoeste do oceano Atlântico

Abstract: Cetaceans were monitored along ca. 700 km of the southeast coast of Brazil (22°S to 25°S) from 1995 to 2014 using photo-identification. The objective of this study was to identify any presence of long-distance movements for monitored cetacean species and discuss implications. Data on long-range movements of four of the monitored species are presented after the analysis of 321,765 photographs taken for individual identification. Seven individuals from four populations of Guiana dolphins (Sotalia guianensis) considered resident to particular estuaries or bays were reported in dispersal involving movement between pairs of protected areas over long-range distances varying between 86 and 135 km. Three cataloged rough-toothed dolphins (Steno bredanensis), first seen in Guanabara Bay, Rio de Janeiro state (22°46'S) in November 2011, were sighted 240 km southwards as members of the same group in coastal waters of São Paulo state (23°46'S) in July 2014. Water depth for those sightings ranged from 16 to 52.7 m; local sightings of rough-toothed dolphins in Brazil have frequently been in shallow waters, but the species global distribution is usually associated with deeper waters. In a 27-day interval in the spring of 2012, a group of 16 orcas (Orcinus orca) travelled ca. 277 km in shallow coastal waters ranging from 20 to 30 m deep. Orcas are commonly observed between November and February in southeast Brazil, probably in search for prey. In summer months between 2012 and 2014, three Bryde's whales (Balaenoptera edeni) sighted in waters ranging from 14 to 49 m deep, moved between 218 and 327 km. Bryde's whales are usually found in local coastal waters where they spend summer months feeding on sardines. To date, these are the longest estimated movements reported to S. guianensis, S. bredanensis, O. orca and B. edeni in the Southwestern Atlantic Ocean.

Resumo: Cetáceos foram monitorados em cerca de 700 km da costa sudeste do Brasil (22°S a 25°S) entre 1995 e 2014 com o uso da fotoidentificação. O objetivo deste estudo foi de identificar quaisquer presenças de movimentos de longa distância de indivíduos das espécies monitoradas e discutir suas implicações. Dados de movimentos de longa distância de quatro das espécies monitoradas são apresentados após a análise de 321.765 fotos obtidas para identificações individuais. Sete indivíduos de quatro populações de boto-cinza (Sotalia guianensis) consideradas residentes a estuários e baías particulares foram reportados em movimentos de dispersão envolvendo pares de áreas protegidas em distâncias que variaram entre 86 e 135 km. Três golfinhos-de-dentes-rugosos (Steno bredanensis) catalogados e avistados primeiramente na Baía de Guanabara, Rio de Janeiro (22°46'S), em novembro de 2011, foram avistados 240 km mais ao sul como membros de um mesmo grupo nas águas costeiras do Estado de São Paulo (23°46'S) em julho de 2014. A profundidade da água onde essas avistagens aconteceram variou entre 16 e 52,7 m; avistagens de golfinhos-de-dentes-rugosos têm sido efetuadas em águas rasas na costa sudeste do Brasil, embora a distribuição global da espécie esteja associada a águas profundas. Em um intervalo de 27 dias na primavera de 2012, um grupo de 16 orcas (Orcinus orca) se desclocou cerca de 277 km em águas rasas variando entre 20 e 30 m. Orcas são comumente avistadas entre novembro e fevereiro no sudeste do Brasil, possivelmente em busca de presas. Nos meses de verão entre 2012 e 2014, três baleias-de-Bryde (Balaenoptera edeni) avistadas em águas de 14 a 49 m de profundidade, moveram-se entre 218 e 327 km. baleias-de-Bryde são encontradas em águas costeiras locais onde passam os meses de verão se alimentando de sardinhas. Até o presente momento, esses são os deslocamentos estimados como os de maiores distâncias observados para S. guianensis, S. bredanensis, O. orca and B. edeni no Atlântico Sudoeste.

Contamination status by persistent organic pollutants of the Atlantic spotted dolphin (Stenella frontalis) at the metapopulation level.

The Atlantic spotted dolphin (Stenella frontalis) is an endemic species of the tropical-temperate Atlantic Ocean with widespread distribution. Although this species has been the subject of a large number of studies throughout its range, it remains in the "data deficient" category of the International Union for Conservation of Nature (IUCN). Chemical pollution by persistent organic pollutants (POPs) has been listed as one of the major threats to this species, however, there is no information on a wide scale. Thus, the aim of the present study was to investigate the contamination status of spotted dolphins on the metapopulation level as well as determine spatial and temporal variations in POP concentrations and bio-accumulation. A total of 115 blubber samples collected from a large part of the Atlantic basin were analysed for PCBs, DDTs, PBDEs, chlordanes, HCB and mirex. Although PCBs and DDTs were the predominant compounds in all areas, inter-location differences in POP concentrations were observed. Dolphins found at São Paulo, southeastern coast of Brazil, had the highest PCB concentrations (median: 10.5 µg/g lw) and Canary Islands dolphins had the highest DDT concentrations (median: 5.13 µg/g lw). Differences in PCB patterns among locations were also observed. Dolphins from the Azores and São Paulo demonstrated a similar pattern, with relatively highly contributions of tetra- (6.8 and 5.2%, respectively) and penta-CBs (25.6 and 23.8%, respectively) and lower contributions of hepta-CBs (20.8 and 23.5%, respectively) in comparison to other areas. Moreover, the sex of the animals and the year in which sampling or capture occurred exerted an important influence on the majority of the POPs analysed. Comparisons with toxicity thresholds available in the literature reveal that the São Paulo and Canary Island dolphins are the most vulnerable populations and should be considered in future conservation and management programs for the Atlantic spotted dolphin.

The evolutionary origins of Lévy walk foraging.

We study through a reaction-diffusion algorithm the influence of landscape diversity on the efficiency of search dynamics. Remarkably, the identical optimal search strategy arises in a wide variety of environments, provided the target density is sparse and the searcher's information is restricted to its close vicinity. Our results strongly impact the current debate on the emergentist vs. evolutionary origins of animal foraging. The inherent character of the optimal solution (i.e., independent on the landscape for the broad scenarios assumed here) suggests an interpretation favoring the evolutionary view, as originally implied by the Lévy flight foraging hypothesis. The latter states that, under conditions of scarcity of information and sparse resources, some organisms must have evolved to exploit optimal strategies characterized by heavy-tailed truncated power-law distributions of move lengths. These results strongly suggest that Lévy strategies-and hence the selection pressure for the relevant adaptations-are robust with respect to large changes in habitat. In contrast, the usual emergentist explanation seems not able to explain how very similar Lévy walks can emerge from all the distinct non-Lévy foraging strategies that are needed for the observed large variety of specific environments. We also report that deviations from Lévy can take place in plentiful ecosystems, where locomotion truncation is very frequent due to high encounter rates. So, in this case normal diffusion strategies-performing as effectively as the optimal one-can naturally emerge from Lévy. Our results constitute the strongest theoretical evidence to date supporting the evolutionary origins of experimentally observed Lévy walks.

Validating the use of biopsy sampling in contamination assessment studies of small cetaceans.

Remote biopsy sampling is the most common technique for acquiring samples from free-ranging marine mammals. However, such techniques may result in variable sampling being sometimes superficial skin and blubber biopsies. For decades, blubber has been used to monitor the exposure of marine mammals to persistent organic pollutants (POPs), but little is known regarding the variability of POPs as a function of blubber depth in small cetaceans and the available literature offers variable results. Thus, the aim of the present study was to validate biopsy sampling for monitoring contaminant concentrations in small, free-ranging cetaceans. Samples from the dorsal blubber of 10 incidentally captured Atlantic spotted dolphins (Stenella frontalis) were separated into two different layers (outer and inner) to investigate the influence of sampling depth on POP concentrations. POP concentrations were compared to those of the full blubber layer. The results revealed no significant differences in lipid content between males and females or among the inner, outer and full blubber layers (p>0.05). Moreover, the wet and lipid weight concentrations of all POP classes analysed [i.e. polychlorinated biphenyls (PCBs), dichlorodiphenyltrichloroethanes (DDTs), polybrominated diphenyl ethers (PBDEs), hexachlorobenzene (HCB), hexachlorocyclohexanes (HCHs), chlordanes (CHLs) and mirex] did not differ significantly with blubber depth (p>0.05). POP classes followed the same decreasing order of wet weight concentrations in blubber layers and full blubber: PCBs>DDTs>PBDEs>mirex>HCB>HCHs>CHLs. Moreover, there was a low degree of differentiation in the accumulation of POP congeners. The present findings indicated that the distribution of contaminants was homogenous with blubber depth, which validates the use of biopsy sampling for the assessment of contaminants in small cetaceans.

Survival in patchy landscapes: the interplay between dispersal, habitat loss and fragmentation.

Habitat loss and fragmentation are important factors determining animal population dynamics and spatial distribution. Such landscape changes can lead to the deleterious impact of a significant drop in the number of species, caused by critically reduced survival rates for organisms. In order to obtain a deeper understanding of the threeway interplay between habitat loss, fragmentation and survival rates, we propose here a spatially explicit multi-scaled movement model of individuals that search for habitat. By considering basic ecological processes, such as predation, starvation (outside the habitat area), and competition, together with dispersal movement as a link among habitat areas, we show that a higher survival rate is achieved in instances with a lower number of patches of larger areas. Our results demonstrate how movement may counterbalance the effects of habitat loss and fragmentation in altered landscapes. In particular, they have important implications for conservation planning and ecosystem management, including the design of specific features of conservation areas in order to enhance landscape connectivity and population viability.

Contamination by chlorinated pesticides, PCBs and PBDEs in Atlantic spotted dolphin (Stenella frontalis) in western South Atlantic.

Chlorinated pesticides, PCBs and PBDEs were analysed in nine blubber samples of Atlantic spotted dolphins, Stenella frontalis, incidentally captured during fishing operations in southern and southeastern Brazil between 2005 and 2007. The majority of compounds analysed were detected, suggesting widespread contamination over the region. Although the samples came from a location far from main coastal industrial areas, the results revealed an influence from such sources. Therefore, levels of PCBs (774-23659 ng g(-1) lipid wt.) and PBDEs (23-1326 ng g(-1) lipid wt.) detected seem to be related to the movement of individuals throughout near-shore and offshore waters. The sample from a lactating female exhibited a lower level of contamination and a distinct pattern, indicating selective transfer favouring less lipophilic compounds.