The future of endemic and threatened birds of the Amazon in the face of global climate change.

The anthropogenic impacts on the environment, including deforestation and the escalating emissions of greenhouse gases, have significantly contributed to global climate change that can lead to alterations in ecosystems. In this context, protected areas (PAs) are pillars for biodiversity conservation by being able, for example, to maintain the viability of populations of endangered species. On the other hand, the species range shifts do not follow the limits of PAs, jeopardizing the conservation of these species. Furthermore, the effectiveness of PAs is consistently undermined by impacts stemming from land use, hunting activities, and illegal exploitation, both within the designated areas and in their adjacent zones. The objectives of this study are to quantify the impacts of climate change on the distribution of threatened and endemic birds of the Amazon biome, evaluate the effectiveness of PAs in protecting the richness of threatened birds, and analyze the representativeness of species within PAs. We found with our results that climate suitability loss is above 80 for 65% of taxa in the optimistic scenario and above 93% in the pessimistic scenario. The results show that PAs are not effective in protecting the richness of Amazonian birds, just as they are ineffective in protecting most of the taxa studied when analyzed individually Although some taxa are presented as "Protected," in future scenarios these taxa may suffer major shrinkages in their distributions and consequently present population unviability. The loss of climatically suitable areas and the effectiveness of PAs can directly influence the loss of ecosystem services, fundamental to maintaining the balance of biodiversity. Therefore, our study paves the way for conservation actions aimed at these taxa so that they can mitigate current and future extinctions due to climate change.

Combining camera trap surveys and IUCN range maps to improve knowledge of species distributions.

Reliable maps of species distributions are fundamental for biodiversity research and conservation. The International Union for Conservation of Nature (IUCN) range maps are widely recognized as authoritative representations of species' geographic limits, yet they might not always align with actual occurrence data. In recent area of habitat (AOH) maps, areas that are not habitat have been removed from IUCN ranges to reduce commission errors, but their concordance with actual species occurrence also remains untested. We tested concordance between occurrences recorded in camera trap surveys and predicted occurrences from the IUCN and AOH maps for 510 medium- to large-bodied mammalian species in 80 camera trap sampling areas. Across all areas, cameras detected only 39% of species expected to occur based on IUCN ranges and AOH maps; 85% of the IUCN only mismatches occurred within 200 km of range edges. Only 4% of species occurrences were detected by cameras outside IUCN ranges. The probability of mismatches between cameras and the IUCN range was significantly higher for smaller-bodied mammals and habitat specialists in the Neotropics and Indomalaya and in areas with shorter canopy forests. Our findings suggest that range and AOH maps rarely underrepresent areas where species occur, but they may more often overrepresent ranges by including areas where a species may be absent, particularly at range edges. We suggest that combining range maps with data from ground-based biodiversity sensors, such as camera traps, provides a richer knowledge base for conservation mapping and planning.

Combinación de censos con fototrampas y mapas de extensión de la UICN para incrementar el conocimiento sobre la distribución de las especies Resumen Los mapas confiables de la distribución de las especies son fundamentales para la investigación y conservación de la biodiversidad. Los mapas de distribución de la Unión Internacional para la Conservación de la Naturaleza (UICN) están reconocidos como representaciones de autoridad de los límites geográficos de las especies, aunque no siempre se alinean con los datos actuales de su presencia. En los mapas recientes de área de hábitat (ADH), las áreas que no son hábitat han sido eliminadas de la distribución de la UICN para reducir los errores de comisión, pero su concordancia con la presencia actual de las especies tampoco ha sido analizada. Analizamos la concordancia entre la presencia registrada por los censos de fototrampas y pronosticamos la presencia a partir de los mapas de la UICN y de ADH de 510 especies de mamíferos de talla mediana a grande en 80 áreas de muestreo de fototrampas. Las cámaras detectaron sólo el 39% de las especies esperadas con base en la distribución de la UICN y los mapas de ADH en todas las áreas; el 85% de las disparidades con la UICN ocurrieron dentro de los 200 km a partir del borde de la distribución. Sólo el 4% de la presencia de las especies fue detectada por las cámaras ubicadas fuera de la distribución de la UICN. La probabilidad de disparidad entre las cámaras y la UICN fue significativamente mayor para los mamíferos de talla pequeña y para los especialistas de hábitat en las regiones Neotropical e Indomalaya y en áreas con doseles forestales más bajos. Nuestros hallazgos sugieren que los mapas de distribución y ADH pocas veces subrepresentan las áreas con presencia de las especies, pero con frecuencia pueden sobrerrepresentar la distribución al incluir áreas en donde las especies pueden estar ausentes, en particular los bordes de la distribución. Sugerimos que la combinación de los mapas de distribución con los sensores de biodiversidad en tierra, como las fototrampas, proporciona una base más rica de conocimiento para el mapeo y la planeación de la conservación.

Climate change and carnivores: shifts in the distribution and effectiveness of protected areas in the Amazon.

Background: Carnivore mammals are animals vulnerable to human interference, such as climate change and deforestation. Their distribution and persistence are affected by such impacts, mainly in tropical regions such as the Amazon. Due to the importance of carnivores in the maintenance and functioning of the ecosystem, they are extremely important animals for conservation. We evaluated the impact of climate change on the geographic distribution of carnivores in the Amazon using Species Distribution Models (SDMs). Do we seek to answer the following questions: (1) What is the effect of climate change on the distribution of carnivores in the Amazon? (2) Will carnivore species lose or gain representation within the Protected Areas (PAs) of the Amazon in the future? Methods: We evaluated the distribution area of 16 species of carnivores mammals in the Amazon, based on two future climate scenarios (RCP 4.5 and RCP 8.5) for the year 2070. For the construction of the SDMs we used bioclimatic and vegetation cover variables (land type). Based on these models, we calculated the area loss and climate suitability of the species, as well as the effectiveness of the protected areas inserted in the Amazon. We estimated the effectiveness of PAs on the individual persistence of carnivores in the future, for this, we used the SDMs to perform the gap analysis. Finally, we analyze the effectiveness of PAs in protecting taxonomic richness in future scenarios. Results: The SDMs showed satisfactory predictive performance, with Jaccard values above 0.85 and AUC above 0.91 for all species. In the present and for the future climate scenarios, we observe a reduction of potencial distribution in both future scenarios (RCP4.5 and RCP8.5), where five species will be negatively affected by climate change in the RCP 4.5 future scenario and eight in the RCP 8.5 scenario. The remaining species stay stable in terms of total area. All species in the study showed a loss of climatic suitability. Some species lost almost all climatic suitability in the RCP 8.5 scenario. According to the GAP analysis, all species are protected within the PAs both in the current scenario and in both future climate scenarios. From the null models, we found that in all climate scenarios, the PAs are not efficient in protecting species richness.

Occurrence dynamics of mammals in protected tropical forests respond to human presence and activities.

Protected areas (PAs) play a vital role in wildlife conservation. Nonetheless there is concern and uncertainty regarding how and at what spatial scales anthropogenic stressors influence the occurrence dynamics of wildlife populations inside PAs. Here we assessed how anthropogenic stressors influence occurrence dynamics of 159 mammal species in 16 tropical PAs from three biogeographic regions. We quantified these relationships for species groups (habitat specialists and generalists) and individual species. We used long-term camera-trap data (1,002 sites) and fitted Bayesian dynamic multispecies occupancy models to estimate local colonization (the probability that a previously empty site is colonized) and local survival (the probability that an occupied site remains occupied). Multiple covariates at both the local scale and landscape scale influenced mammal occurrence dynamics, although responses differed among species groups. Colonization by specialists increased with local-scale forest cover when landscape-scale fragmentation was low. Survival probability of generalists was higher near the edge than in the core of the PA when landscape-scale human population density was low but the opposite occurred when population density was high. We conclude that mammal occurrence dynamics are impacted by anthropogenic stressors acting at multiple scales including outside the PA itself.

A New Assessment of Robust Capuchin Monkey (Sapajus) Evolutionary History Using Genome-Wide SNP Marker Data and a Bayesian Approach to Species Delimitation.

Robust capuchin monkeys, Sapajus genus, are among the most phenotypically diverse and widespread groups of primates in South America, with one of the most confusing and often shifting taxonomies. We used a ddRADseq approach to generate genome-wide SNP markers for 171 individuals from all putative extant species of Sapajus to access their evolutionary history. Using maximum likelihood, multispecies coalescent phylogenetic inference, and a Bayes Factor method to test for alternative hypotheses of species delimitation, we inferred the phylogenetic history of the Sapajus radiation, evaluating the number of discrete species supported. Our results support the recognition of three species from the Atlantic Forest south of the São Francisco River, with these species being the first splits in the robust capuchin radiation. Our results were congruent in recovering the Pantanal and Amazonian Sapajus as structured into three monophyletic clades, though new morphological assessments are necessary, as the Amazonian clades do not agree with previous morphology-based taxonomic distributions. Phylogenetic reconstructions for Sapajus occurring in the Cerrado, Caatinga, and northeastern Atlantic Forest were less congruent with morphology-based phylogenetic reconstructions, as the bearded capuchin was recovered as a paraphyletic clade, with samples from the Caatinga biome being either a monophyletic clade or nested with the blond capuchin monkey.

Consistent diel activity patterns of forest mammals among tropical regions.

An animal's daily use of time (their "diel activity") reflects their adaptations, requirements, and interactions, yet we know little about the underlying processes governing diel activity within and among communities. Here we examine whether community-level activity patterns differ among biogeographic regions, and explore the roles of top-down versus bottom-up processes and thermoregulatory constraints. Using data from systematic camera-trap networks in 16 protected forests across the tropics, we examine the relationships of mammals' diel activity to body mass and trophic guild. Also, we assess the activity relationships within and among guilds. Apart from Neotropical insectivores, guilds exhibited consistent cross-regional activity in relation to body mass. Results indicate that thermoregulation constrains herbivore and insectivore activity (e.g., larger Afrotropical herbivores are ~7 times more likely to be nocturnal than smaller herbivores), while bottom-up processes constrain the activity of carnivores in relation to herbivores, and top-down processes constrain the activity of small omnivores and insectivores in relation to large carnivores' activity. Overall, diel activity of tropical mammal communities appears shaped by similar processes and constraints among regions reflecting body mass and trophic guilds.

Human density modulates spatial associations among tropical forest terrestrial mammal species.

The spatial aggregation of species pairs often increases with the ecological similarity of the species involved. However, the way in which environmental conditions and anthropogenic activity affect the relationship between spatial aggregation and ecological similarity remains unknown despite the potential for spatial associations to affect species interactions, ecosystem function, and extinction risk. Given that human disturbance has been shown to both increase and decrease spatial associations among species pairs, ecological similarity may have a role in mediating these patterns. Here, we test the influences of habitat diversity, primary productivity, human population density, and species' ecological similarity based on functional traits (i.e., functional trait similarity) on spatial associations among tropical forest mammals. Large mammals are highly sensitive to anthropogenic change and therefore susceptible to changes in interspecific spatial associations. Using two-species occupancy models and camera trap data, we quantified the spatial overlap of 1216 species pairs from 13 tropical forest protected areas around the world. We found that the association between ecological similarity and interspecific species associations depended on surrounding human density. Specifically, aggregation of ecologically similar species was more than an order of magnitude stronger in landscapes with the highest human density compared to those with the lowest human density, even though all populations occurred within protected areas. Human-induced changes in interspecific spatial associations have been shown to alter top-down control by predators, increase disease transmission and increase local extinction rates. Our results indicate that anthropogenic effects on the distribution of wildlife within protected areas are already occurring and that impacts on species interactions, ecosystem functions, and extinction risk warrant further investigation.

Site and species contribution to ß-diversity in terrestrial mammal communities: Evidence from multiple Neotropical forest sites.

In a scenario where escalating human activities lead to several environmental changes and, consequently, affect mammal abundance and distribution, ß-diversity may increase due to differences among sites. Using the ecological uniqueness approach, we analyzed ß-diversity patterns of ground-dwelling mammal communities recorded through comprehensive camera trap monitoring within eight tropical forests protected areas in Mesoamerica and South America under variable landscape contexts. We aimed to investigate whether the contribution of single sites (LCBD) and single species (SCBD) to overall ß-diversity could be explained by community metrics and environmental variables, and by species metrics and biological traits, respectively. Total ß-diversity was also partitioned into species replacement and richness difference. We related LCBD to species richness, total relative abundance, functional indices, and environmental variables (tree basal area, protected area size, NDVI, and precipitation seasonality), and SCBD to species naïve occupancy, relative abundance, and morphoecological traits via beta regression. Our findings showed that LCBD was primarily explained by variation in species richness, rather than relative abundance and functional metrics. Protected area size and tree basal area were also important in explaining variation in LCBD. SCBD was strongly related to naïve occupancy and relative abundance, but not to biological traits, such as body mass, trophic energy level, activity cycle, and taxonomic category. Local ß-diversity was a result of species replacements and to a lesser extent differences in species richness. Our approach was useful in examining and comparing the ecological uniqueness among different sites, revealing the regional scale current status of mammal diversity. High LCBD values comprised sites embedded within smaller habitat extents, hosting lower tree basal areas, and harboring low species richness. SCBD showed that relatively ubiquitous species that occur at variable abundances across sites contributed most to ß-diversity.

Correction: Climate change and bird extinctions in the Amazon.

[This corrects the article DOI: 10.1371/journal.pone.0236103.].

Climate change and bird extinctions in the Amazon.

In recent years, carbon dioxide emissions have been potentiated by several anthropogenic processes that culminate in climate change, which in turn directly threatens biodiversity and the resilience of natural ecosystems. Tropical rainforests are among the most impacted biological realms. The Belém endemism center, which is one of the several endemism centers in Amazon, is located in the most affected area within the so-called "Deforestation Arc." Moreover, this region harbors a high concentration of Amazonian endangered bird species, of which 56% of them are considered to be under the threat of extinction. In this work, we sought to evaluate the current and future impacts of both climate change and deforestation on the distribution of endemic birds in the Belém Area of Endemism (BEA). Thus, we generated species distribution models for the 16 endemic bird species considering the current and two future gas emission scenarios (optimistic and pessimistic). We also evaluated climate change impacts on these birds in three different dispersal contexts. Our results indicate that BAE, the endemic taxa will lose an average of 73% of suitable areas by 2050. At least six of these birds species will have less than 10% or no future suitable habitat in all emission scenarios. One of the main mechanisms used to mitigate the impacts of climate change on these species in the near future is to assess the current system of protected areas. It is necessary to ensure that these areas will continue being effective in conserving these species even under climate change. The "Gurupi Mosaic" and the "Rio-Capim" watershed are areas of great importance because they are considered climate refuges according to our study. Thus, conservation efforts should be directed to the maintenance and preservation of these two large remnants of vegetation in addition to creating ecological corridors between them.

Wild dogs at stake: deforestation threatens the only Amazon endemic canid, the short-eared dog (Atelocynus microtis).

The persistent high deforestation rate and fragmentation of the Amazon forests are the main threats to their biodiversity. To anticipate and mitigate these threats, it is important to understand and predict how species respond to the rapidly changing landscape. The short-eared dog Atelocynus microtis is the only Amazon-endemic canid and one of the most understudied wild dogs worldwide. We investigated short-eared dog habitat associations on two spatial scales. First, we used the largest record database ever compiled for short-eared dogs in combination with species distribution models to map species habitat suitability, estimate its distribution range and predict shifts in species distribution in response to predicted deforestation across the entire Amazon (regional scale). Second, we used systematic camera trap surveys and occupancy models to investigate how forest cover and forest fragmentation affect the space use of this species in the Southern Brazilian Amazon (local scale). Species distribution models suggested that the short-eared dog potentially occurs over an extensive and continuous area, through most of the Amazon region south of the Amazon River. However, approximately 30% of the short-eared dog's current distribution is expected to be lost or suffer sharp declines in habitat suitability by 2027 (within three generations) due to forest loss. This proportion might reach 40% of the species distribution in unprotected areas and exceed 60% in some interfluves (i.e. portions of land separated by large rivers) of the Amazon basin. Our local-scale analysis indicated that the presence of forest positively affected short-eared dog space use, while the density of forest edges had a negative effect. Beyond shedding light on the ecology of the short-eared dog and refining its distribution range, our results stress that forest loss poses a serious threat to the conservation of the species in a short time frame. Hence, we propose a re-assessment of the short-eared dog's current IUCN Red List status (Near Threatened) based on findings presented here. Our study exemplifies how data can be integrated across sources and modelling procedures to improve our knowledge of relatively understudied species.

Prey availability and temporal partitioning modulate felid coexistence in Neotropical forests.

Carnivores have long been used as model organisms to examine mechanisms that allow coexistence among ecologically similar species. Interactions between carnivores, including competition and predation, comprise important processes regulating local community structure and diversity. We use data from an intensive camera-trapping monitoring program across eight Neotropical forest sites to describe the patterns of spatiotemporal organization of a guild of five sympatric cat species: jaguar (Panthera onca), puma (Puma concolor), ocelot (Leopardus pardalis), jaguarundi (Herpailurus yagouaroundi) and margay (Leopardus wiedii). For the three largest cat species, we developed multi-stage occupancy models accounting for habitat characteristics (landscape complexity and prey availability) and models accounting for species interactions (occupancy estimates of potential competitor cat species). Patterns of habitat-use were best explained by prey availability, rather than habitat structure or species interactions, with no evidence of negative associations of jaguar on puma and ocelot occupancy or puma on ocelot occupancy. We further explore temporal activity patterns and overlap of all five felid species. We observed a moderate temporal overlap between jaguar, puma and ocelot, with differences in their activity peaks, whereas higher temporal partitioning was observed between jaguarundi and both ocelot and margay. Lastly, we conducted temporal overlap analysis and calculated species activity levels across study sites to explore if shifts in daily activity within species can be explained by varying levels of local competition pressure. Activity patterns of ocelots, jaguarundis and margays were similarly bimodal across sites, but pumas exhibited irregular activity patterns, most likely as a response to jaguar activity. Activity levels were similar among sites and observed differences were unrelated to competition or intraguild killing risk. Our study reveals apparent spatial and temporal partitioning for most of the species pairs analyzed, with prey abundance being more important than species interactions in governing the local occurrence and spatial distribution of Neotropical forest felids.

Limited carbon and biodiversity co-benefits for tropical forest mammals and birds.

The conservation of tropical forest carbon stocks offers the opportunity to curb climate change by reducing greenhouse gas emissions from deforestation and simultaneously conserve biodiversity. However, there has been considerable debate about the extent to which carbon stock conservation will provide benefits to biodiversity in part because whether forests that contain high carbon density in their aboveground biomass also contain high animal diversity is unknown. Here, we empirically examined medium to large bodied ground-dwelling mammal and bird (hereafter "wildlife") diversity and carbon stock levels within the tropics using camera trap and vegetation data from a pantropical network of sites. Specifically, we tested whether tropical forests that stored more carbon contained higher wildlife species richness, taxonomic diversity, and trait diversity. We found that carbon stocks were not a significant predictor for any of these three measures of diversity, which suggests that benefits for wildlife diversity will not be maximized unless wildlife diversity is explicitly taken into account; prioritizing carbon stocks alone will not necessarily meet biodiversity conservation goals. We recommend conservation planning that considers both objectives because there is the potential for more wildlife diversity and carbon stock conservation to be achieved for the same total budget if both objectives are pursued in tandem rather than independently. Tropical forests with low elevation variability and low tree density supported significantly higher wildlife diversity. These tropical forest characteristics may provide more affordable proxies of wildlife diversity for future multi-objective conservation planning when fine scale data on wildlife are lacking.

Standardized Assessment of Biodiversity Trends in Tropical Forest Protected Areas: The End Is Not in Sight.

Extinction rates in the Anthropocene are three orders of magnitude higher than background and disproportionately occur in the tropics, home of half the world's species. Despite global efforts to combat tropical species extinctions, lack of high-quality, objective information on tropical biodiversity has hampered quantitative evaluation of conservation strategies. In particular, the scarcity of population-level monitoring in tropical forests has stymied assessment of biodiversity outcomes, such as the status and trends of animal populations in protected areas. Here, we evaluate occupancy trends for 511 populations of terrestrial mammals and birds, representing 244 species from 15 tropical forest protected areas on three continents. For the first time to our knowledge, we use annual surveys from tropical forests worldwide that employ a standardized camera trapping protocol, and we compute data analytics that correct for imperfect detection. We found that occupancy declined in 22%, increased in 17%, and exhibited no change in 22% of populations during the last 3-8 years, while 39% of populations were detected too infrequently to assess occupancy changes. Despite extensive variability in occupancy trends, these 15 tropical protected areas have not exhibited systematic declines in biodiversity (i.e., occupancy, richness, or evenness) at the community level. Our results differ from reports of widespread biodiversity declines based on aggregated secondary data and expert opinion and suggest less extreme deterioration in tropical forest protected areas. We simultaneously fill an important conservation data gap and demonstrate the value of large-scale monitoring infrastructure and powerful analytics, which can be scaled to incorporate additional sites, ecosystems, and monitoring methods. In an era of catastrophic biodiversity loss, robust indicators produced from standardized monitoring infrastructure are critical to accurately assess population outcomes and identify conservation strategies that can avert biodiversity collapse.