Climate change has been shown to affect the distribution of species by determining where they will, or not, occur in response to their climatic tolerances (Lenoir and Svenning, 2014). There is a growing consensus that human activity largely contributed to recent climate changes occurring worldwide. Thus, the Intergovernmental Panel on Climate Change (IPCC) presents different future climate change scenarios depending on projected greenhouse gases concentrations in the atmosphere due to human activity (IPCC, 2014). In this sense, special attention should be given to the consequences of future climate changes to areas that have a high number of endemic species (i.e. Biodiversity Hotspots) and, especially, on those that are heavily threated (e.g. Collevatti et al., 2013; Prieto-Torres et al., 2016). Additionally, there is evidence that some regions will be more quickly affected by climate change than others. This is especially true to flat biomes, such as flooded grasslands and savannas, which will have very fast rates of temperature change due to their lack of topographic complexity (Loarie et al., 2009). Thus, understanding how species will respond to future climate changes in particular flat biomes such as the Brazilian Cerrado should be a priority for conservation biology.

Most studies on climate change usually focus on how populations or species were or will be affected through time (Walther, 2010). In this sense, it is already known that effects of climatic changes on organisms depend on to which biological group they belong, their habitats, and which geographical region they occur (Bellard et al., 2014). In fact, there are evidences that some species can even respond positively (for example, expanding their ranges) to the elevation in temperature or high CO2 concentrations that are expected in the coming years (e.g. Bellard et al., 2012; Prieto-Torres et al., 2016). However, considering that species respond individually to new conditions, it is mostly expected that future climate change will affect species richness worldwide by changing the spatial distribution of environmental conditions faster than species are able to adapt (Bellard et al., 2012; Thuiller et al., 2005; Xenopoulos et al., 2005). For example, plant species richness is likely to decline in most tropical regions in the coming years (Sommer et al., 2010; Zwiener et al., 2018). Considering this scenario, one could then expect communities from warm flat biomes to experience reductions in species richness due to the inability of species to track rapid changes in the spatial distribution of their preferable environmental conditions (e.g. Collevatti et al., 2013; Prieto-Torres et al., 2016).

Several studies have explicitly investigated how future climate changes will affect whole ecological communities (Albouy et al., 2012; Ihlow et al., 2012; Sommer et al., 2010; Thuiller et al., 2005; Walther, 2010; Xenopoulos et al., 2005), including compositional and structural changes in biomes throughout the world (Nolan et al., 2018). These studies showed that, besides reducing local species richness, one of the most pervasive effects of climate change is the decreasing on beta diversity of communities. This is important because they could result in the biotic homogenizing of fauna across entire regions (Clavel et al., 2010; Magurran et al., 2015) due to the extinction of specialist species (usually with small geographic distributions) and the expansion of those generalists (usually with large geographic distributions) (McKinney, 1997; McKinney and Lockwood, 1999). In fact, changes in temperature and moisture conditions can explain the decline in both plant richness and turnover (Thuiller et al., 2005). Also, there is evidence that mammal communities from continental and oceanic islands have been and will become homogenized through time (Longman et al., 2018).

This homogenizing process has negative consequences for the functioning of ecosystems and in the goods and services provided by them (Clavel et al., 2010; Olden et al., 2004). For instance, biotic homogenization can reduce the resilience of communities to environmental disturbances by preventing the colonization of species with locally extirpated traits (Olden et al., 2004). Nevertheless, and despite the relevance about this topic, there are still few studies analysing how climate change could promote the homogenization of communities at large scales, especially in dry and warm flat biomes. For this type of biomes, one could expect communities to experience increases in their compositional similarity due to extinctions of various specialists and narrowly-distributed species but at the same time the expansion of a few generalists, broadly-distributed species (e.g. Collevatti et al., 2013; Prieto-Torres et al., 2016; Siqueira and Peterson, 2003).

Here we project the current ecological conditions for the distributions of 309 mammals from the Brazilian Cerrado under distinct scenarios of climate change in the late 21st century, assessing how the future environmental changes could promote reductions in the alpha and beta diversities across the faunistic community of this endangered biome. It is important to consider that Brazilian Cerrado is a warm flat biome classified as a Biodiversity Hotspot (Mittermeier et al., 2005) and will probably face fast rates of temperature change in the coming years (Loarie et al., 2009). Therefore, specifically, we answer the following questions: (1) Are we going to lose Cerrado mammalian species, phylogenetic clades and functional diversity due to the expected changes in climate? (2) Are mammalian communities going to become more taxonomically, phylogenetically and functionally homogenized? (3) How and where are these changes going to happen throughout the Cerrado biome? and (4) How are the frequency/incidence of future regional extinctions and immigrations among threatened and non-threatened mammal species.

In general, we found a reduction in mammal species richness in the future at the grid cell scale (mean of −37.231±15.732 species). This indicates that climate changes are likely to cause local extinctions of several mammalian species throughout the Cerrado biome (Fig. 1; Supplementary Material, Appendix S3). However, despite this average reduction on species richness, we observed heterogeneous patterns of phylogenetic overdispersion and clustering (mean of −0.374±4.59) across the Cerrado (Fig. 1e and f), and a general pattern of functional overdispersion (mean of 0.011±0.011; Fig. 1i and j). Such patterns indicate that even if the total phylogenetic or functional alpha diversity decreases in some areas, some of the regionally extinct species could have been phylogenetically or functionally similar to several species. After the removal of these phylogenetically or functionally redundant species, there could be an increase in the mean phylogenetic or functional distance among species.

Fig. 1.

On the left side, maps indicating the present values and the percentages of increase or decrease (future-present) in values of taxonomic alpha diversity (“a” and “b” for richness), and present and future values phylogenetic (“e” and “f” for z of MPD), and functional (“i” and “j” for z of MFD) structures. On the right side, maps indicating the temporal beta diversity and percentage of turnover (out of total beta diversity) of taxonomic (“c” and “d”), phylogenetic (“g” and “h”), and functional (“k” and “l”) beta diversities between present time and the near future. Future values were calculated for the year of 2070 under a scenario of intermediate concentration of greenhouse gases (RCP 6.0).

(1.04MB).

We observed direct relationship among the changes of alpha diversities and the compositions of communities through time (i.e. species temporal turnover). We found that there will be a higher temporal taxonomic turnover in the Northern Cerrado (Fig. 1c and d), despite the general decrease in richness. Although patterns of temporal phylogenetic and functional turnovers were similar to temporal taxonomic turnover, changes in phylogenetic and functional alpha diversities did not follow the same spatial trends. For example, there was an increase in phylogenetic alpha diversity in Eastern Cerrado, a region where there was moderate to high temporal phylogenetic turnover. Moreover, there was a decrease in the functional alpha diversity only in a small region in Southeastern Cerrado, where there was a high temporal functional turnover.

We also found regions with a decrease (indicating biotic homogenization) and an increase in spatial beta diversity of Cerrado mammals. Reductions in spatial taxonomic (Fig. 2a–d), phylogenetic (Fig. 2e–h) and functional (Fig. 2i–l) turnover were most concentrated in cells located at the Southern Cerrado (blue pixels in Fig. 2). This indicates that mammalian communities living mostly in this region will become more taxonomically, phylogenetically, and functionally homogenized in the coming years. Contrarily, several areas (mostly in Northern Cerrado) presented an increasing in taxonomic, phylogenetic, and functional turnover in the future. Thus, these areas are likely to receive species taxonomically, phylogenetically, and functionally different to those occurring in nearby areas. In this sense, we can expect to observe biotic heterogenization rather than homogenization in these areas.

Fig. 2.

Maps indicating the present values and the percentage of turnover (out of total beta), and the increase or decrease in both, of taxonomic (“a”, “b”, “c”, and “d”), phylogenetic (“e”, “f”, “g”, and “h”), and functional (“i”, “j”, “k” and “l”) beta diversities between present time and the year of 2070 under a scenario of intermediate concentration of greenhouse gases (RCP 6.0). (For interpretation of the references to color in the text, the reader is referred to the web version of the article.)

(1.2MB).

We found that nine species may become regionally extinct, from three IUCN categories: DD, LC, and EN (Kunsia fronto, Microakodontomys transitorius, Oecomys cleberi, Oligoryzomys rupestris, Oxymycterus delator, Phyllomys brasiliensis, Thrichomys inermis, Trinomys moojeni, Wiedomys cerradensis). Also, our models indicated that 138 species from other biomes can potentially immigrate to Cerrado in the coming years. Most of these potential immigrants (∼85%) were not considered as endangered. Notably, although our approach resulted in more regional immigrants than extinctions, we still had a general decrease of taxonomic alpha diversity, and a homogenization pattern in Southern Cerrado.

We found that the mammalian communities may, in general, lose species richness. However, a heterogeneous pattern of phylogenetic and functional overdispersion and clustering was observed throughout the Cerrado biome. Alongside reductions, changes in species composition will occur both temporally and spatially (Figs. 1 and 2). Specifically, the highest temporal taxonomic, phylogenetic and functional turnover will be mostly found in the Central and Northern Cerrado. Moreover, we observed that several mammalian communities from the lower part of Cerrado are going to become more taxonomically, phylogenetically and functionally homogenized. Contrarily, communities from the remaining area are mostly expected to increase in spatial beta diversity.

The richness of mammalian communities is expected to decrease in the near-future Cerrado. This result goes in line with the expected shifts in geographic ranges for several biological groups, including mammals, birds, amphibians, reptiles (Diniz-Filho et al., 2009; Lawler et al., 2009), and trees (Simon et al., 2013; Siqueira and Peterson, 2003; Zwiener et al., 2018). These studies predicted a loss in the geographic range of most of Cerrado's species due to upcoming climatic changes. In fact, there is evidence that Cerrado protected areas (PAs) are not able to keep the present levels of mammal evolutionary history and trait diversity (Carvalho et al., 2010). These authors also found that the Central and Southern Cerrado regions would need more conservation attention due to their high phylogenetic and functional diversity. However, we found that Southern Cerrado region will experience a future decrease of phylogenetic (but increase in functional) diversity (Figs. 1 and 2). Thus, we will expect that several mammalian communities to become taxonomically, phylogenetically and functionally homogenized. According to our results, more attention should be focused in the Northern Cerrado, which is today the region with the highest amount of native vegetation (Ballesteros-Mejia et al., 2018; MMA, 2011; Strassburg et al., 2017) and also where agricultural expansion will likely take place in the future (Ministério da Agricultura Pecuária e Abastecimento). Together with the expected high rates of land conversion, we found that this region may also experience a general decrease in both taxonomic and phylogenetic diversity. Therefore, homogenization is going to be strongest where human activities have already had a high impact in the ecosystem and, possibly, in the region's climate.

This homogenization could, certainly, cause several ecological and evolutionary impacts (Olden et al., 2004). For example, modifying species composition could alter community functioning, reducing the stability and resistance to environmental changes due to the narrowing of possible species specific responses, such as already observedfor insular mammal communities (Longman et al., 2018). From this perspective, evidently, the information about temporal changes in species compositions and alpha diversities represent an invaluable background that should be integrated when analysing future changes in biodiversity. This integrative approach could allow us to avoid losing or changing the composition of species, clades and species ecological traits in communities (Carvalho et al., 2010; Hidasi-Neto et al., 2015). Likewise, this is a warning that conservation actions must be urgently taken to conserve or regenerate the lower part of Cerrado, and to promote connectivity (Baguette et al., 2013) between areas where homogenization and heterogenization are expected to occur.

For example, the Serra da Bodoquena National Park is located at Southwestern Cerrado, where we found a future decrease of both taxonomic and phylogenetic alpha diversities of mammals, and an intermediate to high nestedness between present and future communities. Therefore, there will only be a taxonomic and phylogenetic “partial compensation” (see Fig. 1 in Sobral et al., 2016) of mammals in the area where the national park is located. In other words, in the future such assemblages have a great likelihood to be a poorer version of the actual fauna in terms of species and evolutionary lineages. Moreover, in the same area, there was an intermediate nestedness in the functional composition of mammals between the present and the future. However, functional diversity increased with time, indicating a functional “compensation with gain” (Sobral et al., 2016). This indicates that the potential increase in functional diversity in the future will also partially change the actual trait composition. Another example for this picture is Chapada dos Veadeiros National Park, located in Central Cerrado, which presented a future decrease in mammalian richness, and also a high turnover rate, indicating a change in the composition of species (“loss with no compensation”; Sobral et al., 2016). Also, phylogenetic and functional diversities increased with time, but their temporal turnovers were higher. This indicates that the reduced species pool in the area will have a more diverse composition of clades and species traits, but will be phylogenetically and functionally different from the species pool in the present (“gain but no compensation”; Sobral et al., 2016).

These results highlight the challenges that climate change imposes to current conservation policies and decisions. Firstly, because not only current threatened species are likely to disappear by the year 2070. In fact, interestingly, regional extinctions were not only due to endangered species disappearance, but also from the disappearance of DD and LC species (Table 1) as previously reported in other (see Nori and Loyola, 2015). Secondly, despite that our models predicted an expressive number of future immigrations that do not occur in the Cerrado nowadays, most (∼85%) of potential immigrants were from non-threatened categories. Thus, it is likely that more widely distributed species will become more common in the future (McKinney and Lockwood, 1999; Olden et al., 2004; Wilkinson, 2004).

There is still a lack of knowledge on the effects of climate change on whole communities. However, new methods are being developed, helping community ecologists to study classical and new hypotheses in order to shed light on ecology and conservation biology research agendas (Albouy et al., 2012; Diniz-Filho et al., 2009). Here, we showed a consistent prediction about both spatial and temporal alpha and beta diversities of mammal communities from an endangered biodiversity hotspot. These results are important because confirmed the idea, from a perspective conservation, that new and future efforts to maximize the performance of the current protected areas (PA) network have to be differently planned for specific regions depending on how the species pool size and its composition are expected to change through time (Prieto-Torres et al., 2016). In this sense, adding new areas to conserve both present and future ranges of species (as well as their taxonomic, phylogenetic and functional diversity) could represent a less costly strategy (in area and resources) than using a two-step process (i.e., representation of current ranges and afterwards addressing the consequences of climate change). Thus, we encourage future researchers to develop detailed studies about the current species’ representativeness within the PAs network (including the potential effects of future climate change herein identified) in order to identify and design priority conservation areas complementing national network across the Cerrado. Additionally, studies on the future effects of human impacts on biodiversity, such as habitat destruction or modification, will help us to have a better understanding about how urbanization may change ecological communities.