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use change for global amphibian diversity

Amphibian population declines far exceed those of other vertebrate groups, with 30% of all species listed as threatened by the International Union for Conservation of Nature1, 2, 3. The causes of these declines are a matter of continued research, but probably include climate change, land use change and spread of the pathogenic fungal disease chytridiomycosis1, 4, 5. Here we assess the spatial distribution and interactions of these primary threats in relation to the global distribution of amphibian species. We show that the greatest proportions of species negatively affected by climate change are projected to be found in Africa, parts of northern South America and the Andes. Regions with the highest projected impact of land use and climate change coincide, but there is little spatial overlap with regions highly threatened by the fungal disease. Overall, the areas harbouring the richest amphibian faunas are disproportionately more affected by one or multiple threat factors than areas with low richness. Amphibian declines are likely to accelerate in the twenty first century, because multiple drivers of extinction could jeopardize their populations more than previous, mono causal, assessments have suggested.

a, Spatial variation of species richness (number of species per grid cell) of frogs (n = 4,875), salamanders (n = 508) and caecilians (n = 144). b, Intensity of threat from climate change, given as the proportion of species projected to lose climatic suitability in a given area (arithmetic mean across 14 GCMs, 3 emission scenarios and 3 modelling algorithms). c, Intensity of threat from chytridiomycosis, given as the projected probability of occurrence of B. dendrobatidis (arithmetic mean across 3 GCMs and 2 emission scenarios, data from ref. 17). d, Intensity of threat from land use change, given as the proportion of a given area projected to be converted from a natural to an anthropogenic state (arithmetic mean across 4 scenarios, data from ref. 19). For further details on the quantification of threat intensities, see Methods. White areas in panels a and b indicate the absence of a given amphibian order.

Each point refers to one grid cell in Fig. 1 and represents the relative intensity of each of the three threats when considered jointly: climate change (proportion of species losing climatic suitability); chytridiomycosis (probability of occurrence of chytridiomycosis); and land use change. For details on the quantification of threat intensities, see Fig. 1 and Methods. Values of threat intensity are standardized to vary between 0 and 100%, and then transformed into relative proportions to add up to 100% (division by the sum of the three threat intensities). Darker colours indicate higher point densities.

a, Climate change and chytridiomycosis. b, Climate change and land use change. c, Chytridiomycosis and land use change. Colours indicate areas of particularly high threat intensity. These areas are defined as the 25% of all grid cells with (1) the highest proportion of species projected to lose climatic suitability, (2) the highest projected probability of occurrence of chytridiomycosis and (3) the highest proportion of land projected to be converted from a natural to an anthropogenic state. For other details see Fig. 1.

Figure 4: Spatial overlap between areas with the highest amphibian species richness and the main factors threatening global amphibian diversity, projected for 2080.

Areas with the highest species richness are defined as the 25% of all grid cells with the highest number of species. Areas where high levels of species richness coincide with high intensity of 1 of the main factors threatening amphibian diversity are coloured in yellow, orange and red, respectively (blue: no coincidence of high richness and high threat intensity). For definition of 25% areas of high threat intensity and further details see Figs 1 and 3.

Amphibians are experiencing population declines in all regions of the world2, 6. Causes for this global decline have been identified. Among the highest ranking threats are anthropogenic land use changes, leading to habitat destruction and fragmentation, and the fatal disease chytridiomycosis, which is caused by the chytrid fungus Batrachochytrium dendrobatidis. Other threats include climate change, which may interact with chytridiomycosis, environmental pollution, direct exploitation for the food, medicine and pet trades, increase in ultraviolet B irradiation due to anthropogenic ozone depletion, and the spread of invasive species4, 5.

Many studies have assessed how these threats affect amphibian populations and how they may interact at local and regional scales7, 8, 9, 10. Recent assessments have used bioclimatic envelope models to project climate change impacts on amphibian diversity on a continental scale11, 12. Attempts have also been made to assess the relative importance of different threats for large groups of species13, 14, but not in a spatially explicit way. Several hypotheses have suggested that there may be interactions of chytridiomycosis with land use change15 and climate change9, yet no final consensus has been reached10, 16. Preliminary models of the global geography of chytridiomycosis under climate change have been provided17, but an integrative, analytical, spatially explicit assessment at a global scale of the spatial interactions of the most severe threats is urgently needed.

Using a nearly complete global data set of 5,527 amphibian species, we elucidate how the spatial interaction at the global scale of three important threats (climate change, chytridiomycosis and land use change, see Methods) could affect global amphibian diversity between a baseline period (1980) and late in the present century (2080). Threat from future climate change was estimated as the proportion of species locally losing climatic suitability ( losers per area, as given by species specific bioclimatic models (see Methods). Because the spatial distribution of species richness varies considerably among the three amphibian orders Anura (frogs and toads, hereafter), Caudata (salamanders and newts, and Gymnophiona ( (Fig. 1a), we conducted climate change analyses separately for each group. Threat from chytridiomycosis was quantified as the future probability of occurrence of B. dendrobatidis from a bioclimatic model projection17. Lastly, estimates of future land use change (that is, changes from natural to human encroached land cover) were based on the projections of the Millennium Ecosystem Assessment18, 19, 20.

a, Spatial variation of species richness (number of species per grid cell) of frogs (n = 4,875), salamanders (n = 508) and caecilians (n = 144). b, Intensity of threat from climate change, given as the proportion of species projected to lose climatic suitability in a given area (arithmetic mean across 14 GCMs, 3 emission scenarios and 3 modelling algorithms). c, Intensity of threat from chytridiomycosis, given as the projected probability of occurrence of B. dendrobatidis (arithmetic mean across 3 GCMs and 2 emission scenarios, data from ref. 17). d, Intensity of threat from land use change, given as the proportion of a given area projected to be converted from a natural to an anthropogenic state (arithmetic mean across 4 scenarios, data from ref. 19). For further details on the quantification of threat intensities, see Methods. White areas in panels a and b indicate the absence of a given amphibian order.

The three major global threats to amphibians exhibit characteristic, yet disparate geographic patterns (Fig. 1b For frogs, regions with a high projected impact of climate change (regions where high proportions of climate losers in 2080 coincide with a high level of species richness) are the northern Andes and parts of the Amazon and the Cerrado in South America, large areas of sub Saharan tropical Africa, and a small region in South East Asia (Fig. 1b and Supplementary Fig. 1a). In the northern Andes, which harbour the greatest frog diversity worldwide, the proportion of probable climate losers reaches 166 species (73% of the local frog fauna). For salamanders, western North America, northern Central America and southern and south eastern Europe are the regions projected to be most heavily affected by climate change, as are some areas in northern South America for caecilians (Fig. 1b). 1b). The regions with the highest projected probability of occurrence of chytridiomycosis are located in mostly temperate climates as well as mountainous and coastal regions (Fig. 1c). Areas with high projected land use change are mainly found in tropical Central and South America, tropical Africa and montane parts of central and southern Asia (Fig. 1d).

Geographic coincidence in the intensity of the three types of threat is highly uneven and varies strongly among the three amphibian orders (Figs 1b and 2). Within the range occupied by frogs, the spatial overlap between the top 25% affected grid cells for the three threat types is small: 6.1% of these cells (out of a 25% possible) overlap for chytridiomycosis and climate change, 9.1% for climate change and land use change and 8.6% for chytridiomycosis and land use change (Figs 2 and 3; see Supplementary Table 1 for sensitivity analyses and spatial null model tests of overlap; see also Methods and Supplementary Methods for further details). The small degree of overlap between areas of highest impact from chytridiomycosis and climate change arises because of the strong association of B. dendrobatidis with humid and cool conditions found in temperate regions21 and cool tropical high mountains, whereas the negative impacts from climate change are more prominent in the warm and wet tropics (see Fig. 1a). For salamanders, the comparable figures for spatial overlap are 12.2%, 4.6% and 10.0%, respectively (Fig. 3 and Supplementary Table 1). Globally, more than half of the distributional area of each of the three amphibian orders is likely to be highly affected by at least one of the three major threat factors. When only regions with the highest species richness are considered, then about two thirds of the areas with the richest frog and salamander faunas (half of the area for caecilians) are projected to become heavily affected by 2080 (Fig. 4).

Each point refers to one grid cell in Fig. 1 and represents the relative intensity of each of the three threats when considered jointly: climate change (proportion of species losing climatic suitability); chytridiomycosis (probability of occurrence of chytridiomycosis); and land use change. For details on the quantification of threat intensities, see Fig. 1 and Methods. Values of threat intensity are standardized to vary between 0 and 100%, and then transformed into relative proportions to add up to 100% (division by the sum of the three threat intensities). Darker colours indicate higher point densities.

a, Climate change and chytridiomycosis. b, Climate change and land use change. c, Chytridiomycosis and land use change. Colours indicate areas of particularly high threat intensity. These areas are defined as the 25% of all grid cells with (1) the highest proportion of species projected to lose climatic suitability, (2) the highest projected probability of occurrence of chytridiomycosis and (3) the highest proportion of land projected to be converted from a natural to an anthropogenic state. For other details see Fig. Second, other threats not investigated here may also cause declines in amphibian populations, including pollution, direct exploitation, spread of invasive species, or increased ultraviolet B irradiation5. These additional factors give reason for further concern, especially when they interact with one another4. Third, modelled presence of chytridiomycosis does not always cause local declines or extinctions and interspecific as well as regional differences in amphibian susceptibility to chytridiomycosis exist22. Fourth, the spatial resolution of our analysis is relatively coarse, yet several factors allow population persistence at finer scales (see also discussion in refs 23, 24). In particular, our analyses disregard dispersal, biotic interactions and adaptive potential, and rely on the assumption that coarse scale projections from bioclimatic envelope models provide a good surrogate for species climatic requirements at finer scales. However, in some cases, species might persist owing to increased climatic stability in fine grain refugia25, or to local adaptations of amphibian populations26. Our projections thus provide measurements of the exposure of global amphibian species distributions to key threatening processes but, because the species responses to these threats are not investigated, projections overestimate the impacts of multiple threats on the persistence of local amphibian populations (see also Supplementary Discussion).

Despite these uncertainties, our results reveal an intriguing pattern of non overlap between key threatening factors. The implication is that risk assessments focusing on a single threat, such as just climate change or only chytridiomycosis, are probably picturing an optimistic view. As such, they fail to identify the key actions required to curb the ongoing global decline in amphibian diversity. The low coincidence between regions projected to have high prevalence of chytridiomycosis and climate or land use change emphasizes the potential for silent extinctions away from the regions where the current human footprint is larger. In turn, the higher coincidence between land use and climate change bvlgari black and gold ring replica highlights the existence of potential synergies between the two threatening factors that are often neglected18, 27, 28. The substantial overlap of threats with many of the world centres of amphibian richness further underlines the pessimistic long term perspective for global amphibian diversity1, 5. It reinforces the realization that prioritization of conservation efforts needs to be based on knowledge of the spatial distribution both of the different key threats and of biodiversity.

DataWe fitted bioclimate envelope models (BEMs) for 5,527 amphibian species from the three amphibian orders Anura (frogs and toads), Caudata (salamanders and newts) and Gymnophiona (caecilians), which for simplicity are henceforth referred to as frogs, salamanders and caecilians. Distribution data were compiled from the Global Amphibian Assessment31. 1a). This resolution approximates the average of the original resolutions of the climate data sets (see later).

Climatic data were obtained from the World Climate Research Programme (WCRP) Coupled Model Intercomparison Project phase 3 (CMIP3) multi model data set30 of the Fourth Intergovernmental Panel on Climate Change (IPCC) report. Data were derived from 14 coupled Atmosphere Ocean GCMs and 3 emission scenarios (see Supplementary Table 2 for an overview of the used data sets). Outputs for each model were obtained for three SRES32 emission scenarios A1B, A2 and B1, but A2 and B1 scenarios were not available for all of the GCMs (Supplementary Table 2; see ref. 33 for a description of the different scenario storylines). Inclusion of these three scenarios ensures that the models cover a wide range of likely climatic changes.

For each of the GCMs and emission scenarios, five climatic variables were obtained to characterize the baseline period (averaged across a 30 year time period from 1970 to 1999) that was used to calibrate the models. The same variables were then used to make projections into a 30 year time period between 2070 and 2099, subsequently referred to as 2080. The variables used were mean annual rainfall and precipitation seasonality, annual temperature range, minimum temperature and maximum temperature. These variables are known to impose constraints on amphibian physiology and survival34 and are often used to model amphibian species distributions and richness12, 35. All climate variables were resampled to the 2 using a global extent approach and given the grain of our analysis, we (1) avoid asserting artificial data quality by inappropriate downscaling of the climatic data, and (2) minimize the problem of false absences in the species distribution data36 as many species in the data set have only been identified in a few localities, with no knowledge about the true occurrence of the species2. However, the coarse resolution precludes detailed local assessments of threat interactions and processes; therefore our focus is on documenting coarse bvlgari mens wedding rings imitation spatial patterns.

Projections of the probability of occurrence of B. dendrobatidis were obtained from climate based consensus projections previously described17. These projections (standardized probability of occurrence given by a consensus of MaxEnt BEMs across three GCMs and two emission scenarios; Supplementary Fig. 3) were resampled to the 2 by weighted averaging. In contrast to the climate change and land use change projections, for chytridiomycosis we did not use values of the change of the probability of occurrence, as many regions are not infected yet by chytridiomycosis, which makes the absolute value of probability of occurrence a better estimate of future risk of B. dendrobatidis infection. For the subsequent analyses, we used a consensus map calculated as the arithmetic mean across all the projections (Fig. 1b). Generally, averaging across different scenarios may be problematic. 3), we used the consensus map.

For the projections of potential land use change, we used data from the Millennium Ecosystem Assessment20, 37. Ecosystems and Human Well Being: Scenarios. The Millennium Ecosystem Assessment maps provide information on current and future distributions of 18 different land cover types at a 0.5 latitude resolution. For a quantification of potential land use change we identified grid cells that are projected to change from a natural to an anthropogenic land cover state (change of any land cover type to land cover type 3 pasture and calculated the proportion of area changed for each cell of our 2 for 2080, as a consensus map (arithmetic mean across all four scenarios, Fig. 1c) and separately for each of the four scenarios (Supplementary Fig. 4). As for the projections of chytridiomycosis, for practical reasons and because a separate use of different Millennium Ecosystem Assessment scenarios does virtually not affect the results, we used the consensus map in the subsequent analyses.

ModellingThree different modelling algorithms, Euclidean distance (ED), Mahalanobis distance (MD) and MaxEnt (MX), were used to run BEMs. These presence only algorithms were selected owing to the large number of species with uncertain distributions or very small range sizes to be modelled (see also Supplementary Discussion). The two distance based methods (ED and MD) measure the similarity of each species occurrence to the mean (or centre) of the available climatic space. Accordingly species niches are defined as circular (for ED) or elliptical (for MD) shapes in climatic hyperspace38. BioEnsembles, a computer software which is able to optimize and take advantage of high speed parallel processing, was used to run the ED and MD models39. MaxEnt version 3.2.440, 41, a machine learning technique based on the principle of maximum entropy, was used to run the MX models. In MaxEnt, we used a regularization multiplier of 0.5 (a model parameter which allows for adjustment of the degree of model overfitting), because this value represents a balance between being able to fit models for species with very few records while avoiding an unreliable degree of overfitting. Standard BEM validation procedures were not applicable bvlgari yellow gold ring imitation in our study (but note that a validation for future scenarios is in any case not possible42). However, we cautiously assessed patterns of variation in bvlgari mens wedding rings replica model results that may have resulted from different sources of uncertainty, such as species with small numbers of occurrence records, different mo

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