Climate change and bird extinctions in the Amazon

climate may directly influence the metabolism and reproductive success of birds [94,95] because it influences the incubation rates since high temperatures can reduce reproductive success [96]. Also, forest birds are particularly vulnerable to landscape changes; thus, many species are now restricted to smaller areas as a result of deforestation, and this has broader implications for ecosystem function [89]. The association between climate change and reduced habitat suitability has been a determi- nant factor in population reductions of various species worldwide, especially when it comes to endemic or species that have restricted distribution [82,97]. One of the main mechanisms used to mitigate the impacts of climate change on these species in the near future is to assess the cur- rent system of protected areas. It is necessary to ensure that these areas will continue being effective in conserving these species even under climate change [98,99,100]. Thus, the chal- lenge is to assess whether protected areas that are already established will be appropriate for the bird species in the future, or whether we will have suitable forest remnant patches in the areas that are not protected. Despite the existence of protected areas in the studied region, their effectiveness in conserving bird species is low. Only 20% of the taxon distribution falls within the protected areas in the Bele´m Area of Endemism. Such low effectiveness may be related to the low percentage of protected areas existing within the Belem Area of Endemism

[30]. Approximately 3,100 km2 of protected forests were cleared in 2016, a loss of 17.2% of their original extension [101], therefore further impacting species occurrence within the pro- tected lands in the region. Such high levels of deforestation can affect mainly taxa in the future scenario since, in all projections (mitigation and business-as-usual) and multiple dispersal sce- narios, the highest concentration of co-occurring species are within or around the protected forests (Fig 3). The “Gurupi Mosaic” (Area 1 of Fig 3), which includes the Gurupi Biological Reserve (only federal UC of Integral Protection in BAE) and a complex of six Indigenous lands (Alto Tur- iac¸u, Awa´, Caru, Arariboia, Pindare´ River and Alto Guama´ River) stands out for the protection of BAE’s endemic bird species in all the dispersal frameworks in both mitigation and business- as-usual projections. This mosaic houses the largest remnant of the Amazon forest in BAE; thus, it is of paramount biological and socio-environmental importance. Also, inside this area, there is a high diversity of plants and animals, which includes more than 46 endemic and endangered species [102]. The taxa assessed in the present work are found within this complex, including the critically endangered C. pinima and P. obscura [103,104] Additionally, Chiro- potes satanas and Cebus kaapori—the latter being among the 25 species that are at the highest risk of extinction of the World—can also be found in this region [105,106]. Despite its impor-

tance for conservation, the “Gurupi Mosaic” has undergone a dramatic reduction in forest cover due to the significant increase in illegal logging [103]. The “Rio-Capim” watershed is also an area that also deserves some attention. This region is a complex formed by private properties that also protect a large portion of the forest remnants of the BAE (Area 2 of Fig 3). Currently, Brazil has 53% of its forest areas in private properties [107], which increases the importance of these areas for the maintenance of forest-dependent fauna [108,109]. These areas can play an important role, functioning as stepping stones [110] and ecological corridors for all endemic species, as they favor their movement across the land- scape, therefore functioning as complementary conservation areas [111,112]. These ecological corridors are relevant for conservation, to connect populations inhabiting fragmented regions [111,113], facilitate gene flow between populations, and ensure species dispersal [88]. These two large areas, identified through our analyses as climate refuges, are a good alterna- tive for the conservation of BAE’s species, as they are areas of climatic stability, housing species and allowing their persistence in case of niche changes [51,114]. The climatic refuges of the BAE are mainly concentrated within protected areas, which reinforces their importance as PLOS ONE Bird extinctions in the Amazon PLOS ONE | https://doi.org/10.1371/journal.pone.0236103 July 17, 2020 11 / 18