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Proc Natl Acad Sci U S A. Nov 18, 2008; 105(46): 17836–17841.
Published online Nov 10, 2008. doi:  10.1073/pnas.0803524105
PMCID: PMC2584760
Ecology

Linking global turnover of species and environments

Abstract

Patterns of species turnover are central to the geography of biodiversity and resulting challenges for conservation, but at broad scales remain relatively little understood. Here, we take a first spatially-explicitly and global perspective to link the spatial turnover of species and environments. We compare how major groups of vertebrate ectotherms (amphibians) and endotherms (birds) respond to spatial environmental gradients. We find that high levels of species turnover occur regardless of environmental turnover rates, but environmental turnover provides a lower bound for species turnover. This lower bound increases more steeply with environmental turnover in tropical realms. While bird and amphibian turnover rates are correlated, the rate of amphibian turnover is four times steeper than bird rates. This is the same factor by which average geographic ranges of birds are larger than those of amphibians. Narrow-ranged birds exhibit rapid rates of species turnover similar to those for amphibians, while wide-ranged birds largely drive the aggregate patterns of avian turnover. We confirm a strong influence of the environment on species turnover that is mediated by range sizes and regional history. In contrast to geographic patterns of species richness, we find that the turnover in one group (amphibians) is a much better predictor for the turnover in another (birds) than is environment. This result confirms the role of amphibian sensitivity to environmental conditions for patterns of turnover and supports their value as a surrogate group. This spatially-explicit analysis of environmental turnover provides understanding for conservation planning in changing environments.

Keywords: beta diversity, biodiversity, distance decay, environmental gradients, spatial turnover

Understanding patterns of species turnover is central to both applied issues of conservation planning (1, 2) and to long-standing conceptual questions on the origin and distribution of biodiversity (3, 4). Linking these species turnover patterns to changes in environmental conditions is crucial to addressing how the edges of species' ranges are delineated (5). Both environmental dissimilarity and geographic distance are central causes of species turnover (6). Along local environmental gradients, species distributions often represent the outcome of competitive sorting (7, 8). At broader scales, evolutionary histories of speciation and extinction, along with environmental conditions, constrain the richness and distribution of species (911). We examine how both the environment and species composition change over geographic space to disentangle the influence of environmental conditions and space on species turnover. This extends Whittaker's studies (8) of species turnover along environmental gradients to global scales.

We term our examination of changes in species composition along spatial and environmental gradients species turnover (8, 12). While beta diversity is often used synonymously with species turnover (13), beta diversity can also refer to mathematical partitioning of diversity into components (14, 15) and dissimilarly between paired sites (reviewed in 16, 17). Dissimilarity studies based on distance between paired sites lack spatial continuity and a link to a particular location with given environmental conditions. This limits their value in linking environmental and species turnover. For this reason, very few maps of species turnover have been produced compared with the numerous maps of species richness.

Gaston et al. (18) recently produced a map of global species turnover for birds. Species turnover was calculated between pairs of neighboring cells and then related to mean environmental conditions. Using a neighborhood to examine species turnover departs from Whittaker's (8) notion of species turnover along environmental gradients. Other authors have used distance decay in species similarity to examine spatial turnover patterns (1, 19). Qian and Ricklefs (20) calculate plant turnover as the decay of species similarity over either geographic or environmental space. While the decay of species similarity over environmental space is ecologically informative, we chose to relate the decay in species similarity over geographic space to the corresponding decay in environmental similarity. This maintains the importance of geography in both the environment and species composition.

We can then ask how the relationship between turnover in species composition and turnover in the environment varies (i) between our focal groups of vertebrate ectotherms and endotherms; (ii) with the geographic extent considered; and (iii) between biogeographical realms with distinct regional histories. Amphibians tend to have narrow ranges and to be tightly constrained by environmental conditions, particularly the water-temperature balance (21, 22). Amphibians also respond sharply to spatial differences in environmental conditions because of limited dispersal ability (23). We thus expect that amphibian turnover will occur more rapidly than bird turnover. Broad-scale diversity patterns have been found previously to be contingent on the geographic range sizes of species (11). Given the direct link between size of ranges and their average turnover in space (24), much of the cross-taxon variation in turnover may be because of this component. We investigate whether the approximately fourfold difference in geographic range sizes between amphibians and birds can account for differential rates of turnover.

We examine constraints in the relationship between species and environmental turnover. Is a high degree of environmental turnover necessary to observe a high degree of species turnover? Is a high degree of environmental turnover always accompanied by a high degree of species turnover? How does the relationship change with the distance over which decay is examined? We expect differences in range sizes between taxa to become less important at larger scales of analysis. Whether the relationship between environmental and species turnover varies between temperate and tropical realms is central to understanding the distribution and origin of diversity. Such variation would be expected if differential rates of speciation lead to differences in niche specialization and sizes of regional species pools (10). The relationship between environmental and species turnover addresses Janzen's (3) notion that “mountain passes are higher in the tropics”—that less variable tropical climates lead to specialization and high rates of species turnover.

Congruence between taxa for areas of high species richness can facilitate conservation planning (25). Designing conservation reserves to include areas of high species turnover is a less frequently implemented conservation strategy (2), and less is known regarding congruence in patterns of species turnover between taxa (but see 1). Amphibians with their acute sensitivity to environmental conditions may be viable surrogates for species turnover of other taxa (26). Here, we provide an explicit test of this notion and examine across spatial scale whether environment or amphibian turnover is a better surrogate and predictor of geographic turnover in bird species.

Results and Discussion

We first examined the increase in environmental distance and decay in avian and amphibian species similarity with spatial distance (km) for an example location in central Africa (Fig. 1). Environmental distance (the absolute difference in the environment principle component values) increased steadily with spatial distance. The (ln) Jaccard similarity of amphibian species composition declined more rapidly than that for birds, consistent with the tendency for amphibians to have smaller range sizes (slope ± 95% CI for 1,000 km spatial window = −2.80 × 10−3 ± 2.9 × 10−4 amphibians; −1.44 × 10−3 ± 1.0 × 10−4 birds). The slopes of these relationships were reasonably stable over choices of spatial distances. For the majority of the analyses that follow, we examined an intermediate spatial distance of 1,000 km. Slopes can shallow at distances of 2,000 km because of complete dissimilarity posing a lower bound on species turnover.

Fig. 1.
Turnover of environment and species with spatial distance (km) for an example location in central Africa (depicted in Fig. 2). Environmental distance is the absolute difference in the environment principal component between locations (1,000 km slope ± ...

We used the slopes of these site-specific relationships to consider global patterns of turnover in the environment and species composition. The steeper distance decay in compositional similarity for amphibians was globally consistent (mean slope ± 95% CI = −1.90 × 10−3 ± 1.2 × 10−5 for amphibians, −1.16 × 10−3 ± 5.1 × 10−6 for birds, n = 10,529; t13128 = 74.3, P < 1.0 × 10−15). While the spatial decay relationships accounted for 89% (median) of the variation in bird species similarity, the relationship accounted for only 74% (median) of the relationship for amphibians [supporting information (SI) Fig. S1]. Over 99% of the relationships were significant (P < 0.01) for both taxa as well as for environmental turnover.

Regions with the highest rates of species turnover were largely congruent for amphibians and birds, and corresponded closely to regions of high environmental turnover rates (Fig. 2; coefficients of determination in Fig. S1). These regions of high species and environmental turnover include the Andes, Northern Africa, and Himalayas. Individual environmental variables turned over in a similar pattern to that when the four variables were combined in the principal component analysis (temperature, net primary productivity (NPP), annual evapotranspiration (AET), and precipitation, Fig. S2).

Fig. 2.
Spatial patterns of rates of environmental turnover (A) correlate to those of rates of species turnover for birds (B) and amphibians (C). The maps depict slopes (20 quantiles, red: steeper slope) of the relationships between environmental distance or ...

When we related environmental turnover to amphibian species turnover (Fig. 3), we found that high levels of species turnover can occur regardless of the degree of environmental turnover. However, a high degree of environmental turnover tends to correspond to a high degree of species turnover. This triangular relationship between environmental and species turnover is particularly clear for birds. We used quantile (10%) regression to examine the lower bound on species turnover with increasing environmental turnover. The slope of this lower bound on avian turnover ranged from 0.18 to 0.31 and increased slightly with increasing spatial scale (Table 1). The analogous slope for amphibians was substantially steeper with a range from 0.53 to 0.69. High species turnover in homogenous environments may result from histories of vicariant evolution.

Fig. 3.
The relationships between environmental and avian or amphibian turnover and between amphibian and avian turnover (depicting a 1:1 relationship) across locations worldwide and for three distance windows. Quantile regressions (10%) are depicted for the ...
Table 1.
Quantile (QR) and linear least-squares (OLS) regressions between environmental, bird, and amphibian turnover across locations worldwide (corresponding to Fig. 3)

Despite the differences in turnover rates between groups, rates of amphibian and avian turnover highly correlated across grid cells (see Fig. 3). The association was much tighter for amphibian predicting bird turnover (Table 1; Spearman correlations: 500 km rs = 0.63, 1,000 km rs = 0.73, 2,000 km rs = 0.74) than for environment predicting bird turnover (Table 1; Spearman correlations: 500 km rs = 0.33, 1,000 km rs = 0.37, 2,000 km rs = 0.48). These results were confirmed when we accounted for spatial autocorrelation (Table 1). We note that for every increment of amphibian turnover birds turned over by a smaller increment, allowing more precise predictions by the former for the latter than vice versa. Amphibians, with their high sensitivity to environmental conditions because of ectothermy (21), have potential to serve as surrogates for avian species turnover in conservation planning (1) and are better suited to do so than environmental differences at the scale of study. The observation that another taxon is a better predictor of species turnover than environment is in contrast to findings on geographic patterns of species richness. While cross-taxon associations in richness patterns above and beyond environment are found (27), environmental variables such as temperature and productivity tend to be much stronger predictors and surrogates (28, 29).

We found that rates of amphibian turnover were ≈4 times higher than those for birds (Table 1). The rate value was consistent with their having many small ranged species and geographic ranges that on average were ≈4.75 times smaller than those of birds (medium range size = birds: 88, amphibians: 6 grid cells; median = birds: 88, amphibians: 6; mean ± SE: birds = 256.7 ± 4.6, amphibians = 53.9 ± 2.2 grid cells). The influence of birds' larger range sizes on rates of species turnover was revealed when considering avian turnover within four range size quartiles independently (Fig. 4; all distance windows in Fig. S3). The turnover patterns for larger range size quartiles more closely resembled the turnover pattern for all birds (Spearman correlations: Q1 rs = −0.10, Q2 rs = 0.15, Q3 rs = 0.39, Q4 rs = 0.92). Avian turnover within the smallest two range quartiles occurred more rapidly than amphibian turnover. Discrepancies between the turnover patterns for all birds and for those in the largest range quartiles occurred in areas that exhibit fast turnover of narrow-ranged species (Fig. 4). These findings confirm the importance of range size and with it dispersal limitation to species turnover. An alternative would be for turnover patterns to be governed by the distribution of ranges rather than their sizes. Analogous to their pronounced role in determining patterns of species richness (11), wide-ranging species strongly drive spatial patterns of species turnover (18). While the occurrence of narrow-ranged species is not independent of overall richness, considering them is essential to comprehensively identifying areas of high species turnover.

Fig. 4.
Turnover patterns vary for birds divided into four range size quartiles with the most narrowly distributed birds exhibiting the fastest rates of turnover (Q1). Data are divided into the 20 quantiles mapped in Fig. 2, with red indicating faster turnover ...

How species respond to environmental turnover is predicted to depend on past histories of speciation and extinction that determine regional species pools and subsequently on how specialized species are to particular environmental conditions (10, 30, 31). This prediction is consistent with our observation that species turnover tends to increase more rapidly with environmental turnover in tropical realms (Afrotropical, Indomalay, and Neotropical) compared with temperate realms (Australasia, Nearctic, and Paleartic; Fig. 5). Quantile regressions of avian and amphibian turnover against environmental turnover were weakly significant or nonsignificant in temperate realms (temperate birds 1,000 km slope ± 95% CI = −0.02 ± 0.04, F[1, 3020] = 1.3, P = 0.2; temperate amphibians 1,000 km slope ± 95% CI = 0.21 ± 0.09, F[1, 2787] = 22.3, P < 1.0 × 10−5). Among tropical realms, the slope of the relationship between species and environmental turnover was substantially steeper for amphibians than for birds as was observed when considering all realms together (tropical birds 1,000 km slope ± 95%CI = 0.30 ± 0.02, F[1, 17504] = 1032.6, P < 1.0 × 10−15; tropical amphibians 1,000 km slope ± 95%CI = 0.75 ± 0.04, F[1,6879] = 1527.0, P < 1.0 × 10−15).

Fig. 5.
The increase in avian and amphibian turnover with increasing environmental turnover is steeper in tropical realms than in temperate realms. The 10% quantiles of species turnover depict the lower bounds on this relationship for a focal distance of 1000 ...

The differential relationship between species and environmental turnover in temperate and tropical realms provides evidence that environmental conditions and regional histories jointly constrain species turnover as has been extensively documented for species richness (6, 10). Our results are consistent with Janzen's (3) hypothesis that mountain passes are “higher” in the tropics. Tropical mountains, with more constant climates potentially resulting in limited acclimation potential, narrow climatic tolerances, and ultimately greater genetic divergence and rates of speciation, may pose substantial physiological barriers. This should favor narrower distributions and increased species turnover along altitudinal gradients (3). Janzen's assumptions have received substantial empirical support (reviewed in 21, 32). Ranges do tend to be narrower in the tropics for amphibians (33, 34) and birds (32, 35, 36).

The tight linking of environmental and species turnover in the tropics suggests that tropical communities may be particularly susceptible to climate change. Tropical organisms with narrow thermal tolerances may be closer to their thermal limits and may, thus, be more severely impacted by climate change despite the lesser projected temperature changes in tropical areas (37). Differential rates of species turnover between taxa are likely to have repercussions for species' interactions within communities following climate-induced range shifts. Our analysis provides a framework for linking spatial patterns of environmental and species turnover to understand how environmental and historical processes constrain diversity in current and potential future environments.

Methods

Distribution Data.

Species presence was established by using extent of occurrence maps for 5,634 of the ≈6,000 known amphibian species (Global Amphibian Assessment, 38) and 8,750 breeding ranges of the ≈9,713 known land birds (excluding water birds and endemics on small islands, 39). We used an equal area cylindrical projection and equal area grid cells of 12,364 km2 (approximately equivalent to 1° x 1° latitude-longitude near the equator) to examine species and environmental turnover. Following Gaston et al. (18), we emphasized equal area and a globally comparable count of species per grid cell, but acknowledged the shorter grid cell distances at high compared with low latitudes caused by the equal-area projection. We also acknowledged that range maps have the potential to overestimate species' occurrence and that this overestimation may be more severe for amphibians because of their small range sizes. We feel that 1° grid cells both accommodate amphibian's small range sizes and minimize range map overestimation. While this overestimation can influence species richness patterns for grid cells smaller than 2° (40), amphibian species richness patterns are robust to grid cell size (22).

Environmental Data.

We selected four environmental variables known to constrain amphibian and bird distributions (11, 22) and extracted them across the same grid used to assess species turnover. We used mean annual temperature and precipitation data from 1961 to 1990 with 10′ resolution (41). As estimates of energy availability, we used consensus mean annual NPP estimates compiled from numerous models by the Potsdam institute (gC m−2, 30′ resolution, 42) and AET, which is closely tied to the water-temperature balance (30′ resolution, 43). We then combined the data in a principal component analysis to define the environmental gradient. Principal component analysis transforms a number of (possibly) correlated variables into a smaller number of uncorrelated variables (principal components, PC). The first principal component accounts for as much of the variability in the data as possible. In our analysis, this first PC axis accounted for a very large amount (76.2%) of the variance in environmental space and loaded the variables approximately equally (loadings: temperature = 0.33, NPP = 0.54, AET = 0.56, and precipitation = 0.54). This variable then enabled us to examine the combined environmental turnover along a single gradient. This allowed us to calculate the environmental distance between a focal site i and a compared site j as the absolute difference between the values of the PC variable at those two points, i.e., as abs(PCj-PCi). Results are qualitatively similar when temperature was omitted despite the strong latitudinal temperature gradient.

Species Turnover.

Species similarity metrics are a function of the species shared by two areas, a; the species gained by an area relative to the focal area, b; and the species loss by an area relative to a focal area, c. We employed the Jaccard similarity index, which reflects the compositional dissimilarity between two sites as the likelihood that a species occurs in just one site: βj = (b+c)/(a+b+c) (44). We used distance decay relationships to assess rates of decline in species similarity and increases in environmental distance as a function of geographic distance (reviewed in 19, 20, 45, 46). The absolute value of the slope (linear least-squares) of the relationship between environmental distance or (ln transformed) species similarity and distance was used as the metric for species and environmental turnover (19). This approach produced similar species turnover rate maps to that of McKnight et al. (1), but we feel it allows for a more straightforward comparison of environmental and species turnover rates. The regression intercept was fixed at zero (complete similarity at 0 km). We used the R function spDistsN1 to calculate the great circle distance (km) between the centers of grid cells. We examine distance decay within three spatial windows (500, 1,000, and 2,000 km). Grid cells were subsampled by using a probability of selection inverse to distance to maintain a constant sample density as a function of distance. The total number of grid cells selected was set to four times the number of grid cells within a distance radius of 500 km. All coefficients are reported in the text with 95% confidence intervals (CI). We accounted for spatial autocorrelation in error terms by using maximum-likelihood spatial autoregressive models with 1,000-km neighborhoods and row standardization (R package spdep; Bivand 2005).

Supplementary Material

Supporting Information:

Acknowledgments.

We thank all of the contributors and supporters to the bird distribution database, namely Jane Gamble, Hilary Lease, Terressa Whitaker, Josep del Hoyo (Lynx Ediciones), Andrew Richford (Academic Press, Elsevier), Cathy Kennedy (Oxford University Press), Chris Perrins, Robert Ridgely, Tzung-Su Ding, Rob McCall, Paul H. Harvey, Stuart Pimm, and James H. Brown, and Allen Hurlbert, Frank La Sorte, and anonymous reviewers for helpful comments. This work was supported by postdoctoral fellowships at the Santa Fe Institute and the National Center for Ecological Analysis and Synthesis, a center funded by National Science Foundation Grant DEB-0553768, the University of California Santa Barbara, and the State of California (L.B.B.), and National Science Foundation Grant BCS-0648733 (to W.J.).

Footnotes

The authors declare no conflict of interest.

This article is a PNAS Direct Submission. T.L.R. is a guest editor invited by the Editorial Board.

This article contains supporting information online at www.pnas.org/cgi/content/full/0803524105/DCSupplemental.

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