Estimating extinction from species–area relationships: why the numbers do not add up

The species–area relationship: an exploration of that ‘most general, yet protean pattern’¹

Evaluating the effect of habitat diversity on the species-area relationship using land-bridge islands in Thousand Island Lake, China.

Are polyploids really evolutionary dead-ends (again)? A critical reappraisal of Mayrose etal. ().

Extinction from habitat loss is the signature conservation problem of the twenty-first century. Despite its importance, estimating extinction rates is still highly uncertain because no proven direct methods or reliable data exist for verifying extinctions. The most widely used indirect method is to estimate extinction rates by reversing the species-area accumulation curve, extrapolating backwards to smaller areas to calculate expected species loss. Estimates of extinction rates based on this method are almost always much higher than those actually observed. This discrepancy gave rise to the concept of an 'extinction debt', referring to species 'committed to extinction' owing to habitat loss and reduced population size but not yet extinct during a non-equilibrium period. Here we show that the extinction debt as currently defined is largely a sampling artefact due to an unrecognized difference between the underlying sampling problems when constructing a species-area relationship (SAR) and when extrapolating species extinction from habitat loss. The key mathematical result is that the area required to remove the last individual of a species (extinction) is larger, almost always much larger, than the sample area needed to encounter the first individual of a species, irrespective of species distribution and spatial scale. We illustrate these results with data from a global network of large, mapped forest plots and ranges of passerine bird species in the continental USA; and we show that overestimation can be greater than 160%. Although we conclude that extinctions caused by habitat loss require greater loss of habitat than previously thought, our results must not lead to complacency about extinction due to habitat loss, which is a real and growing threat.

Countryside species-area relationship as a valid alternative to the matrix-calibrated species-area model.

Biological diversity

Species-area relationships underestimate extinction rates

Species loss after habitat fragmentation

The species-area relationship (SAR) has been used to predict the numbers of species going extinct due to habitat loss, but other researchers have maintained that SARs overestimate extinctions and instead one should use the endemics-area relationship (EAR) to predict extinctions. Here, we employ spatially explicit simulations of large numbers of species in spatially heterogeneous landscapes to investigate SARs and extinctions in a dynamic context. The EAR gives the number of species going extinct immediately after habitat loss, but typically many other species have unviable populations in the remaining habitat and go extinct soon afterwards. We conclude that the EAR underestimates extinctions due to habitat loss, the continental SAR (with slope ~0.1 or somewhat less) gives a good approximation of short-term extinctions, while the island SAR calculated for discrete fragments of habitat (with slope ~0.25) predicts the long-term extinctions. However, when the remaining area of land-covering habitat such as forest is roughly less than 20% of the total landscape and the habitat is highly fragmented, all current SARs underestimate extinction rate. We show how the 'fragmentation effect' can be incorporated into a predictive SAR model. When the remaining habitat is highly fragmented, an effective way to combat the fragmentation effect is to aggregate habitat fragments into clusters rather than to place them randomly across the landscape.

Simple SummaryLarger areas tend to host more species. This general ecological pattern (known as the species–area relationship, SAR) can be used to calculate expected extinction rates following area (habitat) loss. Here, using data from Italian reserves, SAR-based extinction rates are calculated for beetle groups with different ecology: terrestrial predators, aquatic predators, dung feeders, herbivores, and detritivores. Reserve area was an important predictor of species richness in all cases. However, also other factors besides area were important correlates of species richness. For some groups, species richness tends to decline with elevation and/or northwards. Extinction rates are higher for dung beetles, due to their dependence on large grazing areas, and detritivores, due to their low dispersal capabilities, which reduce their ability to reach new places when environmental conditions became less favorable. The lower extinction rates predicted for other groups can be explained by their higher dispersal ability. Extinction rates by area loss are always relatively low. This means that, in reserves with few species, many extinctions might be unnoticed.The species–area relationship (SAR, i.e., the increase in species richness with area) is one of the most general ecological patterns. SARs can be used to calculate expected extinction rates following area (habitat) loss. Here, using data from Italian reserves, extinction rates were calculated for beetle groups with different feeding habits: Carabidae (terrestrial predators), Hydradephaga (aquatic predators), coprophagous Scarabaeoidea (dung feeders), phytophagous Scarabaeoidea (herbivores), and Tenebrionidae (detritivores). The importance of other factors besides area (namely latitude and elevation) was investigated. Reserve area was recovered as an important predictor of species richness in all cases. For Carabidae, Hydradephaga, and Tenebrionidae, elevation exerted a negative influence, whereas latitude had a negative influence on coprophagous Scarabaeoidea and Tenebrionidae, as a consequence of current and historical biogeographical factors. Extinction rates were higher for dung beetles, due to their dependence on large grazing areas, and Tenebrionidae, due to their low dispersal capabilities. The lower extinction rates predicted for Carabidae, phytophagous Scarabaeoidea, and Hydradephaga can be explained by their higher dispersal power. If other variables besides area are considered, extinction rates became more similar among groups. Extinction rates by area loss are always relatively low. Thus, in reserves with few species, many local extinctions might be unnoticed.

Estimation of species extinction: what are the consequences when total species number is unknown?

Communities in fragmented landscapes are often assumed to be structured by species extinction due to habitat loss, which has led to extensive use of the species-area relationship (SAR) in fragmentation studies. However, the use of the SAR presupposes that habitat loss leads species to extinction but does not allow for extinction to be offset by colonization of disturbed-habitat specialists. Moreover, the use of SAR assumes that species richness is a good proxy of community changes in fragmented landscapes. Here, we assessed how communities dwelling in fragmented landscapes are influenced by habitat loss at multiple scales; then we estimated the ability of models ruled by SAR and by species turnover in successfully predicting changes in community composition, and asked whether species richness is indeed an informative community metric. To address these issues, we used a data set consisting of 140 bird species sampled in 65 patches, from six landscapes with different proportions of forest cover in the Atlantic Forest of Brazil. We compared empirical patterns against simulations of over 8 million communities structured by different magnitudes of the power-law SAR and with species-specific rules to assign species to sites. Empirical results showed that, while bird community composition was strongly influenced by habitat loss at the patch and landscape scale, species richness remained largely unaffected. Modeling results revealed that the compositional changes observed in the Atlantic Forest bird metacommunity were only matched by models with either unrealistic magnitudes of the SAR or by models ruled by species turnover, akin to what would be observed along natural gradients. We show that, in the presence of such compositional turnover, species richness is poorly correlated with species extinction, and z values of the SAR strongly underestimate the effects of habitat loss. We suggest that the observed compositional changes are driven by each species reaching its individual extinction threshold: either a threshold of forest cover for species that disappear with habitat loss, or of matrix cover for species that benefit from habitat loss.

Determinants of orchid species diversity in world islands.

Human-driven habitat loss and fragmentation is one of the largest threats to modern biodiversity. The relationship between species and area is one of the oldest patterns observed in ecology; models based on the species–area relationship (SAR) have been used to estimate both local and global extinction rates. A critical difficulty for modern conservation studies is that they are forced to predict the future; empirical testing of these predictions puts at risk the very species the predictions are designed to protect. To help mitigate this problem, we explore the use of the species–area relationship using the paleontological record, which provides empirical data from both before and after species loss. Using species presence/absence data, and a contiguous minimal area grid system, species–area curves (SACs) were constructed for one biofacies in each phase of a transgressive–regressive package. A regression observed for the Pliocene Etchegoin Formation of the San Joaquin Basin (California) inland sea, and the effect of sea-level fall on the perched molluscan fauna, was used as an analogy for modern habitat loss. Using the equation of the species–area curve of the transgressive interval, we predicted the number of species to go extinct in the subsequent regression. To examine extinction severity, we compared these predictions to the data observed for the regressive curve. The results showed that the regressive curve had fewer species than the prediction based on the transgressive curve, suggesting that species loss was more severe than predicted. The results demonstrate an example of how the species–area relationship can be used in the fossil record, and that the paleontological record could be used to provide relevant information for modern conservation problems.

Previous studies have indicated that similar species-area curves can be expected in undisturbed saxicolous lichen communities despite differences in species composition and location. However, significant differences in the regression parameters of these curves, especially the slope of the log S/log A line, were found to be caused by disturbance. In an attempt to investigate the possible reasons for this difference, random communities were assembled using species composition data from three natural saxicolous lichen communities differing in the level ofdisturbance. These random communities had the same percent coverage of species and bare area as their natural counterparts; however, the spatial distribution of species was randomized. For the undisturbed locations, the random communities had significantly steeper log S/log A regression lines than natural communities. However, no significant difference between random and natural species-area curves was observed for the community simplified by pollution. These results suggest that simplification results in alterations of community composition that make it more random. They also suggest that undisturbed natural saxicolous lichen communities are assemblages regulated not by random processes, but rather by interactions that limit the number of species that can co-occur in the habitat. The species-area relationship has been investigated for nearly 75 years, and a number of theoretical models have been published (reviews by Conner & McCoy 1979; Kilburn 1966). The most popular of these is the power function model first proposed by Arrhenius (1921) but most closely associated with MacArthur and Wilson (1967) and Preston (1960, 1962): S = CAz in which S = species number, A = area, C is the intercept and z is the power constant. This model is frequently approximated by the log S/log A transformation (log S = log C + log A*z), and assumes a dynamic equilibrium between immigration and extinction rates on habitat islands that vary in size and distance away from colonizing sources. Although there is still much discussion about the biological meaning of the relationship between species number and habitat area, the power function model has been used to explain species-area patterns in hundreds of studies involving a variety of organisms and island situations (Conner & McCoy 1979). A recent study of the species-area relationship in saxicolous lichen communities (Lawrey 1991b), which reviewed original and previously-published (Armesto & Contreras 1981; Orwin 1970, 1972) data, yielded two interesting results: 1) Species-area curves of undisturbed communities do not differ significantly despite obvious differences in species richness, composition and location; however, 2) communities simplified by pollution exhibit significantly steeper curves, suggesting an alteration of the processes that regulate community development. These results demonstrate the utility of the species-area curve as an indicator of disturbance, but also suggest profitable methods of studying the dynamics of saxicolous lichen communities. In attempting to explain why simplified saxicolous lichen communities have steeper species-area 0007-2745/92/137-141$0.65/0 This content downloaded from 157.55.39.83 on Sun, 09 Oct 2016 04:14:46 UTC All use subject to http://about.jstor.org/terms 138 THE BRYOLOGIST [VOL. 95 curves, one must consider factors that accentuate differences in species number between rocks of large and small size. Two potential factors are: 1) A lower diversity of potential colonizers caused by the elimination of sensitive species and a reduced growth of tolerant species; and 2) a reduced level of competition within and between species, which would allow higher species numbers in the largest habitats containing the most numerous colonists. Taken together, these factors might account for the observed differences in species-area curves of disturbed and undisturbed saxicolous lichen communities. Furthermore, if true, these hypotheses indicate the importance of biotic factors (colonizing and competitive abilities of species) in directing development of natural saxicolous lichen communities, and suggest an absence of such factors in pollution-simplified communities. Difficult to test directly, these hypotheses are nevertheless testable if one assumes that the absence of species interactions in communities will tend to randomize species composition. This assumption is reasonable given the rarity of observed random spatial patterns in all but the least developed of natural plant communities. As a general rule, pioneer communities exhibit little regulation by biotic interactions, but tend to become less random as community development continues and species interactions intensify (discussed by Lawrey 1991 a). If pollutioninduced community simplification tends to eliminate biotic interactions and randomize community composition, it should be possible to compare natural and randomly-assembled communities from polluted and unpolluted locations using the speciesarea curve. The present paper presents results of such a comparison.