Rarity and Body Size: Importance of Generality K E V I N J . G A S T O N * A N D T I M M. B L A C K B U R N t

*Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, U.K., email K.J.Gaston@Sheffield.ac.uk. ~-NERC Centre for Population Biology, Imperial College, Silwood Park, Ascot, Berkshire SL5 7PY, U.K.

The identification of those species at greatest risk of ex- tinction has been a major concern of conservation biolo- gists (Burton 1984; Munton 1987; Mace & Lande 1991; Groombridge 1993; Collar et al. 1994). A starting point in many such assessments is an understanding of the rel- ative abundances and range sizes of species, on the as- sumption that scarce and restricted species on average will have a greater likelihood of extinction than will those that are abundant and widespread, or will at least constitute a greater proportion of the species at highest risk. Because abundance and range size are insufficiently well correlated with likelihood of extinction to act as ad- equate predictors of that likelihood, assessments must often be refined further by the consideration of addi- tional variables. The question thus arises as to which variables should be used and how.

Building on work by Arita et al. (1990), Dobson and Yu (1993) have argued that comparisons of the abun- dances and range sizes of animal species would be most meaningful if they controlled for differences in body mass; they assert that "if a mouse and an elephant had the same local density, the mouse would be at relatively greater risk of extinction." They illustrated the conse- quences of controlling for body size with reference to data for 100 species of Neotropical forest mammals.

Gaston and Blackburn (1995a) urged caution in the application of such an approach on the grounds that it was unclear why body size in particular should be con- trolled for, that there were potentially serious method- ological difficulties to be overcome in attempting to con- trol for the effects of body size in many assemblages, and that it was unlikely to be applicable in many--perhaps the vast majority of--cases.

Dobson et al. (1995) have responded to a number

Paper submitted March 24, 1996; revised manuscript accepted April 22, 1996.

(though not all) of the points Gaston and Blackburn (1995a) raised. Given the importance and potentially far-reaching implications of some of the issues raised in this debate, it would seem profitable to pursue it further and to bring the results of recent studies to bear upon it.

Single Data Sets and General Patterns

At the heart of the issue of the desirability of controlling for the effect of body size on differences in the abun- dances and range sizes of species lies the question of whether simple, interspecific abtmdance-body size and range size-body size relationships exist in general. At least with regard to densities, Dobson et al. (1995) are clear in their view that small species are more abundant than large, stating that "cases of small and large species occurring at the same density are unlikely to occur in na- ture, as long as a considerable range of body mass is ex- amined."

Despite the rich vein of literature documenting inter- specific abundance-body size relationships, the empiri- cal evidence Dobson et al. (1995) draw on in support of their position derives from a single data set (for Neotro- pical forest manmials) and citation of a small number of studies showing a similar pattern. They entirely ignore the extensive debate that has surrounded the form of the abundance-body size relationship (for reviews see Lawton 1989, 1990, Cotgreave 1993, Currie 1993, Black- burn & Lawton 1994); data in these studies yield numer- ous examples of small-bodied species with lower densi- ties than larger-bodied species.

More recently, we have summarized from the litera- ture information on over 500 different plots of abun- dance versus body size from a w i d e variety of taxa, trophic groups, geographic regions and habitats (a de- tailed description and an extensive analysis of these data will be published elsewhere; Gaston and Blackburn, in

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prepara t ion) . Not all of these p lo t s are i n d e p e n d e n t , bu t the re are 133 that are and for w h i c h the coeff ic ient of de t e rmina t i on is known . The m e a n value of this coeffi- c ient is 0.18. That is, many assemblages con ta in spec ies of small b o d y size at dens i t ies as l ow if no t l o w e r than those o f la rge-bodied species .

It has b e e n sugges ted that w e a k re la t ionships p redom- inant ly resul t w h e n they e m b r a c e spec ies exh ib i t ing only a n a r r o w range of b o d y sizes (Curr ie 1993). Follow- ing f rom this, Dobson et al. (1995) r e c o m m e n d e d that spec ies w i th a w i d e range o f b o d y sizes be inc luded in analyses to avoid this p r o b l e m and to es tabl ish under ly- ing a b u n d a n c e - b o d y size re la t ionships . But, it is no t un- c o m m o n for analyses to reveal no stat ist ically significant re la t ionship b e t w e e n abundance and b o d y size w h e n the b o d y size range spans up to five o rders of magn i tude (Blackburn & Lawton 1994). Likewise, some analyses embrac ing only one o r two o rders of magni tude in b o d y size exh ib i t s t rong negat ive re la t ionships (Brown & Mau- rer 1986; Marquet e t al. 1990; Silva & D o w n i n g 1995). In mos t cases the range o f b o d y sizes in the analysis wil l be set b y the range in the t axon of interest , and w h e t h e r or no t a larger size range w o u l d improve the re la t ionship

wil l be i rrelevant . Gas ton and Blackburn (1995a) ident i f ied a n u m b e r of

t echn ica l p r o b l e m s that may arise in a t t empt ing to re- move the effects of b o d y size f rom popu l a t i on dens i ty and range size. Dobson et al. (1995) r e s p o n d e d by dem- ons t ra t ing that these may no t be major c o n c e r n s in the c o n t e x t of Neo t rop ica l mammals . The po in t s w e raised, however , w e r e based on our unde r s t and ing o f abun- d a n c e - b o d y size re la t ionships at large (in par t icu la r that t hey are of ten w e a k and violate assumpt ions o f least squares regress ion) and w e r e no t i n t e n d e d as cr i t ic isms of the a p p r o a c h Dobson et al. (1995) had taken w i th re- spec t to the i r data. The general pa t t e rns in a b u n d a n c e - b o d y size re la t ionships w e have d i scussed serve to con- f i rm our be l ie f that the p r o b l e m s w e r ecogn i ze d may be e n c o u n t e r e d frequent ly; w h e t h e r o r no t t hey a p p l y to the Neo t rop ica l mammal data set is i rrelevant .

The po ten t ia l hazards o f bas ing r e c o m m e n d a t i o n s on the data set for Neo t rop ica l forest mammals are fur ther emphas i zed by the fact that this exhib i t s a s ignif icant negat ive re la t ionsh ip b e t w e e n in terspec i f ic a b u n d a n c e and range size. Such a pa t t e rn is unusual . Based on a col- la t ion of all k n o w n pub l i shed e x a m p l e s of analyses of in- te rspec i f ic re la t ionsh ips b e t w e e n a b u n d a n c e and range size ( > 40 studies, many d o c u m e n t i n g analyses o f m o r e than one data set), negat ive re la t ionships cons t i tu te less than 8% of all s ignif icant re la t ionships and less than 6% of all analyses (Gas ton 1996); in genera l the p r o p o r t i o n s are p r o b a b l y m u c h smal ler (negat ive re la t ionships have a t t rac ted some d i sp ropo r t i ona t e in teres t because they are unusual; Gas ton & Lawton 1990). In mos t instances , local a b u n d a n c e and range size are pos i t ive ly co r re l a t ed (Brown 1984; Gas ton &. Lawton 1990; Hanski e t al.

1993; Lawton 1993; Gas ton 1994), such that spec ies may face a doub le j e o p a r d y of l ow a b u n d a n c e and re- s t r ic ted d is t r ibu t ion (Lawton 1995).

Finally, w e stress that w e do no t suggest that rar i ty is an abso lu te p r o p e r t y of spec ies (Gas ton & Blackburn 1995a; Gas ton [1994] d iscusses at l eng th the relat ive na- ture o f rarity). But w e p o i n t ou t that a ranking classifica- t ion wil l a lways ident i fy some spec ies as at risk, w h i c h may no t be espec ia l ly he lpfu l in conse rva t ion terms. Thus, ranking might suggest that House Spar rows are m o r e at risk of ex t i nc t i on in Britain than are Starlings and feral p igeons , bu t w e w o u l d be was t ing our t ime managing habi ta ts to conse rve spar rows . Likewise, a ranking s tudy of un i fo rmly t h r e a t e n e d g roups will iden- tify some as safe, de sp i t e the relat ive na ture of rarity.

Density, Population Size, and Study Area

Cons ide ra t ion o f in te rspec i f ic a b u n d a n c e - r a n g e size re- la t ionships leads to a fu r the r issue, namely the advisabil- i ty o f assessing ex t inc t i on risks on the basis of relat ive densi ty . It is c lear to D o b s o n et al. (1995) that if a mouse and an e l ephan t o c c u r at the same p o p u l a t i o n densi ty, t hen the m o u s e is at re la t ively g rea te r risk of ex t inc t ion . It is no t so c lear to us, however . For example , the m o u s e cou ld have a m u c h larger ge og ra ph i c range size, and h e n c e p o p u l a t i o n size. Popu la t ion size may be a more a p p r o p r i a t e measu re of a b u n d a n c e for assessments of rarity. Even ignor ing the c o m p l i c a t i o n of range size, it is deba t ab l e w h e t h e r the l ikely h igher r e p roduc t i ve rate o f the m o u s e will be a m o r e effect ive buffer against ext inc- t ion than the l ikely l o w e r mor ta l i ty rate o f the e lephant . This p r o b l e m has b e e n d e b a t e d at cons ide rab le length, and s tudies can be f o u n d r epo r t i ng posi t ive, negat ive, and no re la t ionship b e t w e e n b o d y size and p robab i l i ty of or t ime to ex t inc t i on (Gas ton & Blackburn 1995b).

An addi t ional p r o b l e m is that , across the range o f b o d y masses that Dobson et al. (1995) regard as des i rable for con t ro l l ing for the effects of size, it is e x c e e d i n g l y un- l ikely that the dens i t ies o f spec ies wil l have b e e n ob- ta ined f rom censuses ove r areas of similar ex tent . In fact, w h e r e it has b e e n sought , a s t rong posi t ive relat ion- sh ip has b e e n found b e t w e e n the b o d y mass of a spec ies and the area over w h i c h its dens i ty was d e t e r m i n e d (Schonewald-Cox et al. 1991; Smal lwood & Schonewa ld 1996; Blackburn & Gas ton 1996a, 1996b). For mamma- lian p r imary consumers , the area ove r w h i c h a spec ies is c ensused has b e e n found to be a be t t e r p r e d i c t o r of its a b u n d a n c e than its b o d y mass (Blackburn & Gas ton in p ress 1996a, 1996b). This f inding raises the poss ib i l i ty tha t d e n s i t y - b o d y size re la t ionships de r ived f rom colla- t ions o f dens i ty data f rom mul t ip le s tudies are deter- mined, at least in par t , by sys temat ic var iance in census area. Certainly, it gives rise to ser ious doub t s that con- t rol l ing for b o d y size in such a re la t ionship addresses a

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strictly biological issue. The ramifications are much wider, however, stimulating more general concerns about how best to determine biologically meaningful comparisons of the densities of different species (Lawton 1989). Across moderate to very large areas, with increasing area the density of any individual species declines, but the appropriate points to compare on different intraspecific density-area plots remain unclear.

Other Variables

A large number of variables are correlated with the abundances and range sizes of species (for reviews see Kunin & Gaston 1993, 1996; Gaston 1994). Gaston and Blackburn (1995a) argued that there seemed to be no strong a priori reason for controlling for the effects of body size rather than some of these other variables. At the time, analyses exploring the relative strengths of re- lationships between the abundances and body sizes of species and between abundances and other variables had not explicitly been explored. We have now carried out such analyses for two species assemblages, British birds and all extant wildfowl (Blackburn et al. 1996; Gas- ton & Blackburn 1996). In both cases, life-history vari- ables (notably those concerned with developmental rates) were better predictors of abundance than was body size. We do not know the extent to which such re- sults generalize, although it would not be surprising if they applied widely. In any case, they serve to further highlight the difficulty in justifying, on the basis of em- pirical or theoretical evidence, the primacy of control- ling for the effects of body size on abundances and range sizes. An argument could be constructed on the pragmatic grounds that data on body size are more likely to be available than data on most life-history variables, and that body size is correlated with many facets of life history (Peters 1983; Calder 1984). If so, body size would have to be employed explicitly as a proxy variable.

Phylogeny

Gaston and Blackburn (1995a) stated that it is important to determine the effect of the phylogenetic relatedness of species on abundance-body size and range size-body size rela~onships in order to ensure that the correct rela- tionships are being controlled for. In contrast, Dobson et al. (1995) argue that for conservation purposes it might be most useful to examine associations of rarity and phylogeny in a post-hoc manner. This, contradicts another of their assertions, however, that removal of the influence of body mass is appropriate when evidence of a statistically significant association with population density or range size exists (Dobson & Yu 1993). With- out taking phylogeny into account, the degrees of free-

dom of these relationships will be inflated because spe- cies are not independent data points, potentially making them appear statistically significant when, if correctly analyzed, they would not be.

The abundance-body size relationship is often quite different within subsets of species. In British birds, for example, there is a general though weak negative rela- tionship between body mass and abundance (popula- tion size or density). But, there is no significant relation- ship within passerines or nonpasserines if they are analyzed separately (Nee et al. 1991). British bats and nonvolant mammals exhibit different abundance-body size relationships (Greenwood et al. 1996). Which spe- cies are considered rare depends on which taxa are con- sidered in any assessment. If the rarity of bats should be assessed separately from other mammals, why not carni- vores? The taxonomic level at which to conduct statisti- cal assessments of rarity is a key issue, and it is not clear to us which level should have precedence.

Conclusion

Like Dobson et al. (1995), we accept that time is too short to wait for complete biological knowledge or for elucidation of every possible bias or complication in sci- entific analyses before attempting to identify those spe- cies at greatest risk of extinction. But, we also suggest that it is strenously inadvisable to expound the virtues of techniques that may not prove appropriate for achieving this end, particularly when there is ample evidence to suggest that they may have little generality.

Various avenues are being explored through which the relative extinction risks that species face can be as- certained (Mace & Lande 1991; Mace et al. 1992; Durant & Mace 1994; World Conservation Union 1994). In par- ticular, many of these emphasize the overriding impor- tance of considering trends (observed, inferred, or pro- jected) in abundances and range sizes. We remain convinced that these approaches are likely to prove more fruitful than those advocated by Dobson et al.

Acknowledgments

K.J. Gaston is a Royal Society University Research Fellow. T. M. Blackburn was supported by NERC grant GST/03/ 1211. J. Lawton kindly commented on the manuscript.

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