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Journal of Animal Ecology 2000, 69, 1111±1116 FORUM The relationship between local and regional species richness in birds of the Caribbean Basin ROBERT E. RICKLEFS Department of Biology, University of Missouri-St. Louis, 8001 Natural Bridge Road, St. Louis, Missouri 63121±4499, USA Srivastava (1999) recently evaluated the relationship between local and regional species richness as a tool for determining whether local assemblages of organisms are ecologically saturated or open to invasion. Srivastava also pointed out several pitfalls of sampling and interpretation in such studies. One problem arises when regional species pools are estimated by summing species richness over habitats (Method 1). In this case, the regional pool includes species that may not be capable of living in a particular local community and the species pool is thus overestimated. Terborgh & Faaborg (1980), Ricklefs (1987), and Wiens (1989) used this approach to analyse local and regional richness in the avifauna of the West Indies, where each island was considered a separate region. The local±regional tests in those studies correspond to Srivastava's Method 3, which relates diversity in `identical habitats in geographically dierent regions' to the regional species pools. One may nonetheless object to these analyses because regional species richness was estimated by summing over habitats within islands and because individual islands within an archipelago are not statistically independent, i.e. `regional', samples. The problem is largely one of scale. Loreau (2000) has pointed out that the relationship between local and regional species richness depends on the scale at which each is measured. Thus, when the concepts of `local' and `regional' are similar, for example in terms of habitat breadth, a large proportion of the regional heterogeneity is sampled within each locality and local diversity tends to vary in proportion to regional diversity. This gives the appearance of non-saturation (Cornell & Lawton 1992; Caley & Schluter 1997). When a narrower concept of `local' is applied, local diversity is relatively independent of regional diversity and the appearance of saturation is a more likely outcome. In Pearson's (1977) study of birds in tropical forests in six regions, concepts of `local' and `regional' did not dier greatly with respect to habitat breadth. Consequently, local communities contained # 2000 British Ecological Society Correspondence: Dr R.E. Ricklefs, Department of Biology, University of Missouri-St. Louis, 8001 Natural Bridge Road, St. Louis, Missouri 63121±4499, USA. 60±80% of the regional species richness and local species richness increased roughly in proportion to regional species richness. The West Indian analyses mentioned above adopted a relatively broader concept of `region', and local communities contained only 20±60% of the regional species richness, as reported in detail below. Here I would like to address the problems of estimating regional species pools and establishing the independence of these pools, and to comment more generally on the practice of regarding local±regional diversity relationships as either showing saturation or not. Data The data reported by Ricklefs (1987) and subsequently analysed by Schluter & Ricklefs (1993) were obtained by George Cox (Cox & Ricklefs 1977) and Joseph Wunderle (Wunderle 1985) on several islands (Jamaica, St. Kitts, St. Lucia, Grenada [JW], and Tobago [JW]) and within two continental areas (Trinidad and central Panama) in the Caribbean Basin. (Trinidad was connected to the mainland of South America during Pleistocene sea level lows and has a continental avifauna.) The data are similar to, but independent of, observations used by Terborg & Faaborg (1980) in their seminal appraisal of the local±regional species richness relationship. Cox and Wunderle censused birds during ten 20-minute point counts in each of nine matched habitats in each of the islands or continental areas. Local species richness (L) is the average of the number of species observed in each of the nine habitats in a single island or area. Regional species richness (R) is the number of species observed in all habitats together (Robs) or the number of species known to occur in the region (island or continental area) whether observed during point-count sampling or not (Rtotal). Ricklefs (1987) portrayed species richness for several habitats as a function of the observed regional species richness for the seven regions. As Srivastava pointed out, the regional pool for any given habitat may be overestimated because each species in the regional pool may not be capable of living in each of the habitats. Furthermore, if overestimation of the regional pool were to vary in a sys- 1112 Local and regional species richness tematic way with respect to regional species richness, this would lead to a bias in the relationship between local and regional richness. It is generally true that more diverse regions have a higher proportion of habitat specialists. Therefore, the regional richness that is relevant to a particular habitat is exaggerated compared to less diverse regions. This tends to stretch out the scale of regional diversity towards its higher end and bias the local±regional diversity analysis in favour of ®nding a curvilinear relationship, which Srivastava (1999), taking the `majority view', would accept as evidence for saturation (also see Griths 1999). The local±regional regression # 2000 British Ecological Society Journal of Animal Ecology, 69, 1111±1116 Because regional richness estimated by summing over habitats is likely to err in favour of supporting saturation, it provides a conservative evaluation of regional eects on local diversity. More importantly, because both local and regional factors can in¯uence local diversity, the degree of curvilinearity in the local±regional relationship can reveal their relative contributions. Saturation is not an either/or phenomenon. Rather, local community interactions balance the tendency of regional richness to contribute to local richness through dispersal and habitat expansion, with increasing resistance as local diversity increases. Schluter & Ricklefs (1993) reported that the slope of the logarithmic relationship between local and regional diversity based on the Cox/Wunderle data was 05 (see their Fig. 14). That is, both alpha (local) diversity and beta diversity (turnover between habitats) increased as the square root of regional species richness. In that analysis, local species richness (L) was the average species richness in each of the nine habitats on a particular island or within a particular mainland region. Regional richness was the observed number of species (Robs, or simply R). Rtotal includes birds not seen in the point counts but known to occur in the region and therefore overestimates the species pool for poorly sampled local areas when local diversity is estimated from point counts. This bias increases with increasing regional diversity because average species abundance declines and many species are missed locally. To minimize this bias, all the regressions reported here are based on Robs. The linear regression, L a bR, was signi®cant (F1,5 765, P 00003, r2 0939); however, adding a quadratic term to obtain L a bR cR2 signi®cantly increased the goodness-of-®t (F2,4 4444, P 00001, r2 0996). This suggests a curvilinear relationship between local and regional species richness. The quadratic regression statistics (a 505 091, b 0372 0031, c ÿ 000138 000019) indicate a peak local richness at R 1348 species, that is, at the highest regional richness observed in the study (Panama, R 135 species). Thus, local richness increases monotonically through the range of regional richness observed in the study. Accordingly, a power function, L aRb, should provide an appropriate description of the relationship. The linear form of this regression, logL loga blogR, was signi®cant (F1,5 2572, P 00001, r2 0981) and the slope of the regression (b 0497 0031) suggests that local diversity increases as the square root of regional diversity in this sample. The power function also can be ®t by non-linear regression to untransformed data, in which case the resulting coecients were a 312 042 and b 0470 0031 (r2 0985). The relationship between L and R was also described well by several asymptotic equations. For the logistic equation, L a/{1 exp[± b(R ± c)]}, the regression coecients were a 3076 060, b 00367 00031, and c 3198 140 (r2 0994). For the exponential equation, L a[1 ÿ bexp(± cR)], the regression coecients were a 3360 147, b 0911 0044, and c 00167 00025 (r2 0994). Both equations suggest an asymptotic local species richness of 31±34 species, which is approached only in the regions with the highest regional diversity: Panama and Trinidad (Fig. 1). Two points are evident. 1. The rate of increase in local species richness decreases as regional species richness increases. This could result in part from overestimation of the regional species pool in regions with higher species richness. If this were not an important problem, the regressions would be consistent with the hypothesis that more diverse assemblages of species are more dicult to invade than are less diverse assemblages. It would also be consistent with the hypothesis that more diverse species pools contain more habitat specialists with limited capacity to live in other habitats. Whether local species richness actually levels o at a `saturation' level is dicult to determine. The non-asymptotic power function ®ts the data almost as well as asymptotic logistic and exponential functions. If the relationship did level o, however, this would occur only at the highest diversities observed in the study. 2. Through most of the range of regional species richness in this data set, increase in regional richness is accompanied by an increase in local species richness. Thus, local assemblages evidently are open to invasion by additional species at least up to the maximum diversity observed in this study, even though there is also evidence of increasing resistance to invasion. Independence of samples and the problem of pseudoreplication. A potential problem with statistical appraisal of patterns within a single large area, such as the Carib- 1113 R.E. Ricklefs Fig. 1. (a) Relationship between average local within-habitat species richness and the regional species pool ®t by linear, quadratic, logistic, and exponential functions. The last three are asymptotic or reach a maximum and ®t the data equally well. (b) Logarithmic relationship ®t to the same data with slope 050. bean Basin, is lack of independence of the data (Srivastava 1999). For example, the avifauna of St. Kitts is largely a subset of the birds of St. Lucia, and Grenada shares many of its species with Tobago and Trinidad. Two considerations suggest that the distributions of birds among habitats within each of the regions are, for the most part, independent. First, many geographically separated populations of the same species within the Caribbean Basin exhibit strong genetic divergence, indicating long periods of evolutionary independence (Seutin et al. 1993; Klein & Brown 1994; Seutin et al. 1994; Lovette et al. 1998; Lovette, Bermingham & Ricklefs 1999; Ricklefs & Bermingham 1999). Secondly, increase in habitat breadth (ecological release) of colonists to the Lesser Antilles from Trinidad and northern South America appears to occur rapidly (Wunderle 1985) and is apparent even in island populations lacking genetic dierentiation in mtDNA sequences from mainland source populations (Ricklefs & Bermingham 1999). Therefore, habitat distribution and local species richness could achieve independent local equilibria within each of the regions. Estimating regional diversity by summing over habitats # 2000 British Ecological Society Journal of Animal Ecology, 69, 1111±1116 Within a region, species replacement occurs with respect to habitat and to distance within habitat (Cody 1993). Replacement within habitat presumably re¯ects subtle changes in environment, competitive exclusion by closely related taxa, and limits to dispersal over long distances. To what extent should variation between and within habitats be incorporated into the estimate of regional diversity against which a particular sample of local diversity is measured? Srivastava (1999) suggests that because many specialists cannot live in alternative habitats, summing across habitats provide an inappropriate estimate of regional diversity. Members of a regional species pool can be absent from a particular local community for many reasons. These include adaptation barriers imposed by habitat specialization, but also similar barriers raised by environmental variation within habitats (which, after all, are subjective distinctions) and barriers to dispersal over distance within habitats. Two points argue for including variation across habitats in the concept of `region.' First, habitat specialization is ¯exible and responds to the intensity of competitive interactions among species. This is particularly evident on islands in the West Indies where species on depauperate islands exhibit substantial ecological release by increasing the number of occupied habitats (see Table 1). Secondly, adjustments of species within a regional pool include evolutionary responses that potentially would permit most species access to most habitats. Comparative analyses show that most of the variation in range size (Gaston 1998) and habitat distribution (Ricklefs, unpublished) within large taxonomic groups occurs at the level of species within genera, that is, over relatively short evolutionary time frames. Thus, to the extent that the sorting of local communities out of a regional pool includes an evolutionary component, summing over habitats is appropriate. Area of regions Srivastava (1999, p.10) points out that `the ability of each species in the region to invade a given local 1114 Local and regional species richness Table 1. Species abundance, habitat distributions, local species richness, and the `regional' pools of birds of the Caribbean basin `Region' (2) Total regional pool (Rtotal) (3) Observed regional pool (Robs) (4) Species per habitat (L) (5) Local abundance per species (6) Total abundance per habitat (7) Habitats per species (8) Regional abundance per species (9) Regional abundance of avifauna St. Kitts Grenada St. Lucia Tobago Jamaica Trinidad Panama 21 34 40 64 68 186 296 20 30 34 53 55 108 135 119 155 153 214 213 288 302 59 54 57 48 49 32 29 699 842 879 1018 1038 934 887 54 47 41 36 35 24 20 315 253 233 173 170 78 59 629 758 791 916 934 841 798 (1) Note: Columns (2) (3) (4) and (5) observed directly; (6) (4)x(5); (7) 9x(4)/(3); (8) (5)x(7); (9) (3)x(8). community will be a decreasing function of the distance it must disperse.' Accordingly, summing species over area may overestimate the regional pool. This raises important issues concerning how we de®ne `region' and the temporal and spatial scales we apply to our de®nition of region. For birds on islands in the West Indies, however, distance is probably not a problem. Distances within islands are on the scale of kilometres or tens of kilometres, which are less than the distances that individuals crossed to colonize the islands. Source±sink relationships # 2000 British Ecological Society Journal of Animal Ecology, 69, 1111±1116 A potential bias in the local±regional relationship not mentioned by Srivastava (1999) could arise from diversity-dependent dierences in source±sink relationships. Under the saturation hypothesis, according to which local diversity is regulated by interactions among species, the number of species in a habitat may be further augmented by movement of individuals from adjacent habitats, thereby establishing source±sink relationships (Pulliam 1988; Stevens 1989). If this were true, diversity within habitats could be closer to the local saturation point on islands than at mainland sites where diversity could be maintained locally above saturation by movement of individuals between source and sink populations. This would shift the local±regional regression to resemble proportional sampling more closely than it would saturation. This bias seems unlikely, however, inasmuch as species in continental regions have narrower rather than wider habitat distributions. Individual species also exhibit lower population densities on continents (Fig. 2), and perhaps less intimate juxtaposition of varied habitat types, which weighs further against a role for source populations maintaining diversity in sink areas. Indeed, it is equally plausible that movement of individuals between habitats augments local diversity on small islands given the higher average popu- Fig. 2. Decrease in habitat breadth and local abundance of speccies with increasing species richness of the regional pool. lation densities and frequent proximity of many habitats within small areas. Discussion Rather than asking whether local communities are ecologically saturated or not, it may be more useful to ask how dierences in the regional pool of species are expressed in (i) the pattern of local diversity within habitats, and (ii) turnover of species between habitats within the region. Birds of the West Indies show that these measures respond to change in size of the regional pool approximately equally. Ecological release suggests that ecological interactions within local communities make invasion of additional species more dicult. Presumably, reduced 1115 R.E. Ricklefs # 2000 British Ecological Society Journal of Animal Ecology, 69, 1111±1116 habitat breadth within regions having large species pools results from the lower productivity of populations within their most productive habitats and stronger interspeci®c competition in habitats that are marginal for them. However, in spite of local ecological pressure, there is no apparent upper saturation point for species richness within avifaunas of the Caribbean Basin. As species are added to the regional pool, species richness within local assemblages continues to increase, although not at a proportional rate. Dierences in `regional' diversity in this data set are established by barriers to dispersal from continental sources of colonists and by higher rates of extinction on small islands (Ricklefs & Lovette 1999). Thus, dierences in regional diversity are caused in part by factors external to the regions themselves (colonization) and in part by factors characteristic of the region but external to local habitats (extinction of island populations). As Srivastava (1999) suggests, dierences in `regional' species pools caused by barriers to dispersal and by extinction may not be comparable to dierences accumulated over long periods of independent evolutionary history, as would occur between the southern continents in the case of birds. However, comparison with Pearson's (1977) studies on tropical forest birds from six regions on three continents suggest that these relationships may be general. The logarithmic slope of the local±regional relationship in Pearson's data is 065 (Srivastava 1999), which is similar to slopes calculated from the Cox/Wunderle data for comparable habitats in the Caribbean Basin using Robs as the estimate of regional diversity (young secondary forest, b 0714 0065; old secondary forest, b 0476 0176; mature lowland forest, b 0616 0103). Srivastava (1999) makes the important point that local±regional richness plots should be used in conjunction with other evidence pertaining to the eects of local ecological interactions within assemblages. Such evidence would include density compensation and ecological release, which are well documented in the data of Cox & Ricklefs (1977) and Wunderle (1985). Furthermore, densities of bird populations within the Caribbean Basin may be limited by local resources, as indicated by the similar total abundance of birds in all regions regardless of the species pool or number of species per habitat (Table 1, column 9). Local diversity does not re¯ect only ecological saturation or only proportional sampling of a regional species pool. Interactions between species constrain membership in local assemblages but do not place an upper limit on their size. Local and regional diversity are connected through the pressure of intraspeci®c competition, which compels individuals to disperse from crowded to less crowded habitats and populations to evolve adaptations that promote broader habitat occupancy. Ecologists should be less concerned about whether populations interact within local assemblages than with the mechanisms responsible for (i) generating the regional pool of species, (ii) the distribution of those species over habitats within the region, and (iii) evolutionary adjustments that accompany invasion of a local assemblage. Acknowledgements I am grateful to D. S. Srivastava and a referee for helpful comments. References Caley, M.J. & Schluter, D. 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