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Results and Discussion
- Climate change threats to plant diversity in Europe

Many European species could be threatened by future climate change (Fig. 1). Under the assumption of no migration, more than half of the species we considered become vulnerable or committed to extinction by 2080. The impacts of climate change are, naturally, less under the universal migration because of the possibility for species to move across landscapes. Under the no-migration assumption and the most severe climate change scenario (A1-HadCM3), 22% of the species become critically endangered (>80% range loss), and 2% extinct by 2080. These numbers decrease for the other scenarios and climate models. Under the universal migration assumption, the results are, as expected, less severe. Under tA1-HadCM3, 67% of species would be classified as low risk, whereas under B1-HadCM3, 76% of the species would be at low risk.

Our results coincide with the direction of predictions made by Thomas et al. (11), although the magnitude of the risks we project is less [and note that we project distributions to 2080, whereas Thomas et al. (11) only projected to 2050].

Niche-based modeling does not address the proximate causes of species extinction. Nevertheless, any reduction in the potential geographic range of a species is likely to lead to an increased risk of local extinction (11). This conclusion is, in fact, the rationale for building IUCN Red Lists (31). A decrease in range size implies that smaller stochastic events affect a larger proportion of the species' total population, especially in fragmented landscapes. If a species becomes restricted to a few sites, then local catastrophic events (such as droughts or disease outbreaks) or an increase of land transformation by humans could easily cause the extinction of that species (32).

Rates of species' loss and turnover show great variation across scenarios (Fig. 2). In A1-HadCM3, the mean European temperature increases by up to 4.4 K, leading to a mean species loss of 42% and turnover of 63%. This scenario provides the widest range of variability across Europe for both species loss (2.5-86%) and turnover (22-90%). The percentage of species loss could exceed 80% in some areas, such as northcentral Spain and the Cevennes and Massif Central in France. B1-HadCM3 gives the lowest expected mean percentage of species loss (27%), reflecting the fact that this scenario has the lowest rate of increase in CO2 and temperature by 2080 (mean European temperature increase of 2.7 K). Other scenarios show intermediate mean rates of species loss (≈30%) and turnover (≈50%).

The relationship between the modeled percentage of species loss and the anomalies for the two most significantly correlated bioclimatic variables, growing-degree days (representing accumulated warmth) and a moisture availability index, was used to uncover the potential causes of variations in predicted changes in plant diversity across regions within and across scenarios (Fig. 3). The strong consistent linear relationship across scenarios indicates that projected species loss from our models could be estimated from these two predictors. The Spearman rank-correlation values for the separate univariate relationships were 0.73 and 0.65, respectively. Multiple-linear regression by using these two predictors explains 60% of the variance across scenarios. The temperature of the coldest month, although being an important predictor of distributions for many species (6), did not show a strong relationship with species loss overall and was therefore not used in this analysis.

Regional deviations from the inferred relationship (positive and negative residuals) can be interpreted as indications of particularly high or low species vulnerability, because of ecological and historical characteristics of the flora, and/or specific environmental conditions (Fig. 4). An excess of species loss (red color) is shown for mountain regions (mid-altitude Alps, mid-altitude Pyrenees, central Spain, French Cevennes, Balkans, Carpathians). Severe climatic conditions have occurred in mountains over evolutionary times, promoting highly specialized species with strong adaptation to the limited opportunities for growth and survival (33). The narrow habitat tolerances of the mountain flora, in conjunction with marginal habitats for many species, are likely to promote higher rates of species loss for a similar climate anomaly than in any other part of Europe (34). By contrast, the southern Mediterranean and part of the Pannonian regions have a negative residual for species loss (gray color). Both regions are characterized by hot and dry summers and are occupied by species that tolerate strong heat and drought. Under the scenarios used here, these species are likely to continue to be well adapted to future conditions.

We finally present mean percentages of species loss and turnover by environmental zones (M. Metzger, unpublished data) with the A1-HadCM3 scenario of maximum change to best illustrate the spatial patterns (Fig. 5). The major spatial patterns are similar over all scenarios. The northern Mediterranean (52%), Lusitanian (60%) and Mediterranean mountain (62%) regions are the most sensitive regions; the Boreal (29%), northern Alpine (25%), and Atlantic (31%) regions are consistently less sensitive. Species turnover shows a somewhat different pattern. The Boreal region could, in principle, gain many species from further south, leading to a high species turnover (66%). The Pannonian region could also theoretically gain eastern Mediterranean species and has a calculated turnover of 66%. Thus, these regions stand to lose a substantial part of their plant species diversity, and (in time) to show a major change in floristic composition. Projected species turnover peaks at the transition between the Mediterranean and continental regions (Fig. 5) with extirpation of Euro-Siberian species and expansion for Mediterranean or Atlantic species. Southern Fennoscandia is also an area of high potential turnover with the loss of boreal species and gain of Euro-Siberian species.

These results cannot be taken as precise forecasts given the uncertainties in climate change scenarios, the coarse spatial resolution of the analysis (35), and uncertainties in the modeling techniques used (8, 29). The relatively coarse grid scale of our study may hide potential refuges for species and environmental heterogeneity that could enhance species survival, especially in mountain areas where our estimation of risks of extinctions could be overestimated. On the other hand, landscape fragmentation could increase the vulnerability of these refuges to fire or other disturbances, which in combination with the lack of propagule flow, could compromise the survival of remnant populations. There are also major uncertainties due to lags associated with biotic processes. The recognized time scales for assigning species IUCN Red List categories are not suited to evaluating the consequences of slow-acting but persistent threats. We have substituted a time scale of 80 years (instead of 20) for critically endangered, endangered and vulnerable, respectively, over which to assess declines. The extent of species losses may be overestimated, because the plasticity of species and the survival of species in favorable microhabitats is not considered. However, even if the numbers are overestimated, patterns across regions may stand (e.g., the ranking of region in terms of vulnerability to loss). Species loss does not necessarily imply the immediate loss of a species from a site, rather it may imply a potential lack of reproductive success and recruitment that will tend to extinction on a longer time scale (36). Migration rates are likely to be species-specific, and resulting biotic interactions in “no-analogue” assemblages may alter species' realized niches.

Land use and associated habitat fragmentation are likely to generally inhibit migration rates (19). Further, future species distributions will likely be influenced by other environmental factors than changing climate. The current atmospheric CO2 concentration exceeds any experienced during the past 20 million years (12). Plant physiological responses, including growth responses to increased atmospheric CO2 and changes in wateruse efficiency, are expected to ameliorate the response of some plant functional types to climate change (37). On the other hand, nitrogen deposition, the enhanced potential for invasion by exotic species, or the promotion of more competitive native species may change competitive interactions in plant communities, yielding novel patterns of dominance and ecosystem function (38).

Despite uncertainties, our findings provide illustration of the potential importance and the likely direction of climate change effects. From a conservation perspective, a proportion of European plant species could become vulnerable. The strong positive relationship between projected species loss and changes in bioclimatic variables implies that action to reduce greenhouse gas emissions would also mitigate climate-change effects on plant diversity. However, even under the least severe scenario considered, the risks to biodiversity appear to be considerable. Different regions are expected to respond differently to climate change, with the greatest vulnerability in mountain regions and the least in the southern Mediterranean and Pannonian regions. Recent observations (39) and predictions (9) corroborate our conclusion regarding the climatic sensitivity of species in European mountain areas. We have also identified a broad transition zone where the greatest species mixing is likely to occur. During the Quaternary period, this region acted both as a crossing point and a refuge zone for Boreo-alpine and Euro-Siberian species (40). This transition zone will be a strategic region for plant-species conservation in a changing climate.



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