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Concepts & Synthesis CONCEPTS & SYNTHESIS EMPHASIZING NEW IDEAS TO STIMULATE RESEARCH IN ECOLOGY Ecological Monographs, 81(3), 2011, pp. 349–405 Ó 2011 by the Ecological Society of America Regulation of animal size by eNPP, Bergmann’s rule, and related phenomena 1,3 2 MICHAEL A. HUSTON AND STEVE WOLVERTON 1Department of Biology, Texas State University, San Marcos, Texas 78666 USA 2University of North Texas, Department of Geography, Denton, Texas 76203-5017 USA Abstract. Bergmann’s rule, which proposes a heat-balance explanation for the observed latitudinal gradient of increasing animal body size with increasing latitude, has dominated the study of geographic patterns in animal size since it was first proposed in 1847. Several critical reviews have determined that as many as half of the species examined do not fit the predictions of Bergmann’s rule. We have proposed an alternative hypothesis for geographic variation in body size based on food availability, as regulated by the net primary production (NPP) of plants, specifically NPP during the growing season, or eNPP (ecologically and evolutionarily relevant NPP). Our hypothesis, ‘‘the eNPP rule,’’ is independent of latitude and predicts both spatial and temporal variation in body size, as well as in total population biomass, population growth rates, individual health, and life history traits of animals, including humans, wherever eNPP varies across appropriate scales of space or time. In the context of a revised interpretation of the global patterns of NPP and eNPP, we predict contrasting latitudinal correlations with body size in three distinct latitudinal zones. The eNPP rule explains body- size patterns that are consistent with Bergmann’s rule, as well as two distinct types of contradictions of Bergmann’s rule: the lack of latitudinal patterns within the tropics, and the decline in body size above approximately 608 latitude. Both types of contradictions of Bergmann’s rule are consistent with the eNPP rule, as are a wide range of other phenomena. Key words: Bergmann’s rule; body size; fish; latitude; mammals; NPP; productivity. We are told in our first course in biology that and is often linked to other global patterns, such as the all animals are dependent on plants for food, either latitudinal gradient of species richness (Blackburn and directly or indirectly, and that plants in turn obtain Gaston 1994, 1996, 1998, Johnson 1998a) as well as their food from the soil and process it in the presence patterns of extinction (Johnson 1998b, Purvis et al. 2000, of sunshine, air, and water. This elementary law of Cardillo 2003, Cardillo et al. 2005, Olden et al. 2007) nature is so simple and obvious that its import to and evolution (Cooper and Purvis 2010). Spatial problems of wildlife conservation has been frequently variation in animal body size has been a major topic overlooked. ... What I am about to say may be since at least 1847, when Bergmann published his iconic interpreted by some as a highly controversial issue . ... paper linking large body size to cold conditions —A. H. Denney (1944) (Bergmann 1847). With the recent development of global data sets, Bergmann’s paper has spawned a small INTRODUCTION industry in body-size analyses, but there are many Variation in body size among animals is of great interpretations of this pattern and there is relatively little interest in macroecology, biogeography, and conserva- consensus (Rosenzweig 1968a, McNab 1983, Geist tion (Margalef 1955, McNab 1971, Peters 1983, Calder 1987a, b, Cousins 1989, Ashton et al. 2000, Meiri and 1984, Brown and Nicoletto 1991, Crooks 2002, Meiri Dayan 2003, Meiri et al. 2004, Rodrı´ guez et al. 2006, and Thomas 2007, Olden et al. 2007, Greve et al. 2008) Meiri and Thomas 2007, Watt et al. 2010, Meiri 2011). Numerous correlates of body-size variation have been investigated, including latitude, latitudinal range, geo- Manuscript received 6 August 2010; revised 1 March 2011; accepted 2 March 2011. Corresponding Editor: A. M. Ellison. graphical range size, temperature, temperature range, 3 E-mail: [email protected] annual precipitation, precipitation range, net primary 349 350 MICHAEL A. HUSTON AND STEVE WOLVERTON Ecological Monographs Vol. 81, No. 3 production (NPP), food supply, and species richness, the much as that of a common smaller animal. This problem last of which potentially involves a sampling effect that persists regardless of whether a species is analyzed on may skew data (Meiri and Thomas 2007). the basis of the centroid of its range or its presence in Meiri (2011) points out that Bergmann’s rule is each grid cell or region encompassed by its range (e.g., actually an empirical generalization that describes a Blackburn et al. 1999, Blackburn and Hawkins 2004). common intraspecific pattern in endotherms. An empir- The approach is unsound as currently applied and is ical generalization ‘‘is a statement concerning known unlikely to lead to a functional or mechanistic under- phenomena that is treated as a law that holds in all times standing of factors that influence either average body and places. The statement is not really known to be a size in an assemblage or the distribution of body sizes law; instead this stature is assigned to empirical (sensu Cooper and Purvis 2010, McNab 2010). generalizations based on repeated, non-contradictory A more appropriate way to calculate mean commu- observations’’ (Wolverton and Lyman 2000:237; em- nity body mass would be to scale body size by the total phasis in original). Bergmann (1847) hypothesized that mass of all individuals of each species present in an area heat conservation was the explanatory mechanism (converted to a proportion of the total mass of all underlying his rule. We note, however, that process species). Unfortunately, such data are very scarce and and pattern are often conflated in the literature, and that logistically challenging to collect, so there are few a single type of pattern may have multiple causal publications that provide a functionally relevant mean processes operating at different times and places. What assemblage biomass. Alternatively, because outlier is needed to overcome this problematic empirical species (usually with large body size) skew community generalization is an explanatory rule that ascribes an means, a simple compromise is to compare communities ecologically sound mechanism for patterns in animal using median size, which is less sensitive to problems of growth, body size, and biomass that is independent of skewness (McGrew and Monroe 2000, Weiss 2002, latitude and geographic scale. Cooper and Purvis 2010). The issue of functionally The literature on Bergmann’s rule has been described relevant proportional representation is most problemat- as ‘‘chaotic’’ (McNab 2010). In spite of intense interest ic in mammals, which have a huge range in body size. In in this subject, there is argument about whether size contrast, the relatively small body-size range of birds variation should be analyzed at the intra- or interspecific should reduce the bias introduced by variation in species YNTHESIS level, or even at higher taxonomic levels (e.g., Lindsey richness and seems to produce interpretable results (e.g., 1966). There is even disagreement over the taxonomic Blackburn and Gaston 1996). Natural selection and the &S level at which Bergmann intended his rule to apply (cf. vicissitudes of evolutionary history have led to many James 1970, Blackburn et al. 1999, Meiri and Thomas situations such as the co-occurrence of large elephants 2007, Meiri 2011). At the intraspecific level, where much and small rodents in the same habitat. Neither the mean of the recent work has been done, the focus has been on of these species summed, nor the range of body mass determining which taxa show the expected latitudinal they represent, are likely to teach us much about the ONCEPTS C pattern. Most groups of homeotherms show the pattern effects of environmental conditions on animal body size. predicted by Bergmann (Ashton et al. 2000, Meiri and Given the problems associated with the current Dayan 2003). However, many groups of poikilotherms, emphasis on the ‘‘community approach’’ to evaluating which are not subject to the heat-conservation mecha- Bergmann’s rule, we focus primarily on intraspecific size nisms underlying Bergmann’s rule, also show the same variation, which eliminates several alternative (and pattern of increasing body size with latitude (Ray 1960, therefore confounding) mechanisms that may operate Lindsey 1966, Atkinson 1994, Ashton 2002, Ashton and at the interspecific or community level. The excluded Feldman 2003). mechanisms are (1) selection for alternative life history At the interspecific, ‘‘community,’’ or assemblage strategies and body sizes in the same environment; (2) level, most studies find the expected positive correlation consequences of random ancestral colonization and between mean body size and latitude for birds (Black- diversification of large-bodied or small-bodied species; burn and Gaston 1996) and mammals (Blackburn and (3) selective advantage of traits linked to, but function- Hawkins 2004, Rodrı´ guez et al. 2006, Cooper and Purvis ally unrelated to, body size; and (4) higher migration 2010) consistent with Bergmann’s rule. However, Meiri ability of large-bodied species for recolonizing deglaci- and Thomas (2007) point out that part of the pattern ated areas (more likely to be important for mammals may be an artifact of there being fewer small-bodied than for birds). Each of these mechanisms could species where species richness is low, as at high latitudes. potentially operate on the large variation in size found This is a valid concern, and points toward fundamental between species, but is unlikely to be relevant to the problems with this approach. One critical flaw has been much smaller size range found between populations of that there is no scaling by species abundance for the same species (Blackburn and Hawkins 2004). So, determining the community mean. Any species that is what are the potential mechanisms that are relevant at present in a region, no matter how rare, is included in the intraspecific level? ‘‘average body size’’ of the assemblage in that region.
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