Biological Correlates of Extinction and Persistence of Primates in Small Forest Fragments: A Global Analysis

Introduction

Habitat loss and fragmentation are associated with fewer resources, greater isolation, and more intense and far-reaching edge effects [1], and both are considered major threats to wildlife. In brief, smaller areas often contain fewer taxa than do larger areas [2]. Conservationists have known for a longtime that the species at risk in small fragments are often not a random subset of the original community [3, 4]. Understanding of the biology of extinction, of why some species are more at risk than are others under the same environmental change, should help refine conservation efforts, [5–7]. Nevertheless, knowledge of the biology of susceptibility is far from complete.

Our aim here is to contribute to the understanding of the biology of extinction by elucidating the risky traits in an unusually well-known taxon of tropical forest mammals, primates. Primates are no different from other taxa in that they often suffer from loss and fragmentation of their habitat [8–10]. The traits that enhance extinction risk can change with the nature of the threat [11–13]. We here analyze in more detail than hitherto, and over a broader geographical range, the traits that distinguish primate taxa susceptible to fragmentation from those that are less susceptible.

We do so by comparing taxa that differ in the size of the smallest forest fragment in which they have been recorded as present. Our assumption was that taxa that are present and thereby assumed as persisting (in this study) in smaller fragments are less susceptible to extinction than are taxa that need larger fragments in which to persist.

Whether fragmentation is a threat varies not just with the size of the fragment, but of course with many other factors, such as isolation by both distance and the nature of the matrix, the amount of viable habitat within a fragment, and the nature of human-caused disturbance [14, 15]. Nevertheless, we correlate biological traits that distinguish extinct from persistent taxa only with size of fragment. Our justification is two-fold. First, the area of a fragment will often correlate with many of the other factors, such that, for example, small fragments are situated in more adverse matrices [16]. Second, the fact that the species-area relationship is usually so obvious, despite all the potential confounds, indicates that correlating only area with probability of extinction and thence biological traits of risk should be usefully informative.

From previous analyses of the biology of extinction of primates, we predicted that primates with greater body weights, greater group masses, larger group sizes, lower population densities, larger annual home ranges, slower rates of reproduction, more specialized diets and habitats, lower maximum altitudes and latitudes, and smaller geographic ranges will be more likely to suffer extinction, and therefore will be found only in larger fragments [3, 4, 8, 17–20].

Methods

Results

With a sample of 65 species globally for which we had information on the minimum size of forest fragment occupied, we found, without phylogenetic correction, only one significant biological correlate of extinction risk among the 15 biological traits tested: species with fewer categories of habitat occupied were found less in the smallest fragments (Table 1A). For South America, only the number of dietary categories significantly predicted size of the smallest fragment occupied. One of 15 variables significant is close to what one might expect by chance, and indeed Bonferroni correction produced a non-significant result.

At the level of genus, we found no significant relationships between the smallest fragment area in which genera persisted and any of the 15 biological parameters in 36 genera (Table 1B).

Accounting for phylogeny with CAIC, and after removal of outliers, only the number of dietary items was significantly related to minimum fragment size (Table 2). This variable, though, was not significant in the direction we had predicted: species with fewer dietary categories existed in smaller fragments. Again, Bonferroni correction made the result non-significant.

With no reliable significant association detected between size of smallest-fragment occupied and any one biological trait, we did not deem it useful or sensible to conduct multi-variate analyses to search for any minimum model of traits to explain contrasts between taxa in the size of the smallest fragment that they were recorded to occupy. Such analyses would find a minimum model (they always do), but we do not consider that it would be meaningful.

Discussion

Across many taxa, several variables, such as home range size, body size, population size, reproductive rate, and specialization, have fairly consistently emerged as important biological indicators of extinction risk in a variety of sorts of analysis, and despite a considerable number of ignored confounding variables. Nevertheless, in this analysis of the biology of extinction of primates in small forest fragments, we found no obvious biological trait of risk. In other words, no obvious trait distinguished taxa liable to extinction in small fragments of habitat from those able to persist. Certainly we have not tested all possible traits, nor have we used all possible statistical means to discern potential traits of risk. However, the more traits and the more tests, the more likely is a spurious finding without correction for number of traits and tests. With correction, the influence of the trait would have to be so large that any effect would, we suggest, have already been detected via its correlation with the already tested traits.

One possibility for the finding of no association between biology and risk of extinction as measured here is that, in this analysis, confounding factors were so influential that the traits of risk were hidden. Obvious ones are the variable quality of the original data (a potential problem with all comparative analyses), other influences (such as isolation of fragments), ignorance of variation of habitat quality within fragments, the surrounding habitat amount [32], and of course, the influence of the nature of the matrix between fragments. Therefore, the dependent variable (i.e., size of the smallest forest fragment occupied) could be highly limited by the fact that we did not control for all these potential confounding factors, potentially masking the effect of fragment size on the persistence of primates in fragments. However, as the sources on presence-absence of species in fragments were the same as those that indicated significant species-area relationships in a previous analysis [9] (in which both isolation and age of fragment were accounted for), we do not think that this is a sufficient explanation.

Alternatively, we suggest that many studies of primates in fragments are being conducted in fragments too small for long-term persistence of any primate (global median of 1 km²) and therefore, too small to produce a difference in probability of extinction between species. All the species in the fragments are extinction-prone. Other workers, using other approaches, have also suggested that all species will go extinct in fragments as small as the majority in which studies of effects of fragmentation are usually conducted [9, 33–39]. The fragments are in extinction debt [40].

The conclusion that most research on effects of fragmentation on primates is being conducted in fragments in which all species will eventually go extinct does not mean that research on primates in small fragments is useless. It will elucidate the biology of the immediate responses of primates to deterioration of habitat, knowledge of which is extremely useful to understanding both the process of evolution, and to more precise implementation of conservation efforts. However, the sort of comparative analysis conducted here, which is designed to detect gross contrasts between species that might indicate longer-term traits of risk, will probably be more successful if conducted in fragments of at least ten square kilometers, maybe more. We make this suggestion because a polynomial regression of proportional richness (richness in fragment as percent of richness in nearby main forest block) against area of fragment in the Americas asymptoted at about 25 km². The global analysis, however, showed no asymptote even by 100 km².

Implications for conservation

Our conclusion that data from small fragments are not useful for presence-absence analysis as a means to elucidate the biology of extinction risk most certainly does not mean that small fragments are useless for conservation. They can certainly be useful [41]. For instance, Tutin and coworkers found that some primate species might even benefit from the lack of competitors in small fragments [42, 43]. Additionally, animals in fragments can be easier to find than ones in the main forest, with the consequence that fragments can be and are valuable for purposes of conservation education and publicity, as well as providing revenue for local communities or conservation management institutions.