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Bergmann ’ s rule encompasses mechanism: a reply to Olalla-T á rraga (2011)

Cortney Watt and Volker Salewski

C. Watt (cortneywatt@gmail.com), Dept of Biological Sciences, Univ. of Manitoba, Winnipeg, MB, R3T 2N2, Canada. – V. Salewski, Behavioural Biology, Univ. of Osnabr ü ck, Barbarastr. 11, DE-49076 Osnabr ü ck, Germany.

Th e many defi nitions of Bergmann ’ s rule have resulted in confusion and debate over how and in what organisms to test the original rule. Watt et al. published a paper in 2010, based directly on Bergmann ’ s original paper, in the hopes of clarifying the rule and presenting direct translations to resolve uncertainties. Recently, Olalla-T á rraga has criticized our publication, stating that we assumed the rule was a causal law, which has narrowed our epistemological scope of the rule. We argue we did not assume the rule was a law and suggest that Olalla-T á rraga has only focused on the observed pattern and has ignored the proposed mechanism, which is inherent in the defi nition. We also discuss the proposed mechanism and describe why it cannot apply to ectotherms. Despite this, we encourage a thorough investigation of the mechanisms responsible for maintaining Bergmann ’ s pattern in ectotherms and support Olalla-T á rraga ’ s quest for a unifying mechanism to explain body size gradients in endotherms and ectotherms.

Th e defi nition of Bergmann ’ s rule has been rewritten and interpreted by a number of researchers. Currently, there are over 20 proposed defi nitions for the rule (Watt et al. 2010 Table 2), which have caused much confusion, particularly concerning what organisms the rule applies, and at what taxonomic level the rule was constructed. Watt et al. (2010)conducted a literature review and attempted to clarify Bergmann ’ s rule by providing direct translations from Bergmann ’ s original paper (Bergmann 1847). Olalla-T á rraga ’ s (2011) main disputes with the publication by Watt et al. (2010) are that 1) we have made assumptions about the rule that restrict further advancements, and 2) the ther-moregulatory mechanism proposed by Bergmann can be applied to both ectotherms and endotherms. In contrast, we argue that a mechanism is inherent in Bergmann ’ s rule and that the proposed mechanism cannot be applied to ectotherms; thus, examining Bergmann ’ s rule in these organ-isms is inappropriate.

Assumptions regarding the rule

Olalla-T á rraga (2011) recently criticized Watt et al. (2010) for assuming Bergmann ’ s rule was a concept cluster and acausal law rather than a correlative law. By defi nition Bergmann ’ s rule is a concept cluster, it has been given mul-tiple meanings and defi nitions (Peet 1974, Watt et al. 2010 Table 2). Furthermore, we did not assume Bergmann ’ s rule was a law at all, and made no assumptions about whether the rule was causal or correlative, we intended only

to represent the rule as originally stated by Bergmann (1847). We would argue that it is Olalla-T á rraga (2011) who made assumptions regarding Bergmann ’ s rule, stating that it is ‘ a broad generalization with no inherent mechanisms ’ , because according to Bergmann (1847) there is an inherent mecha-nism he discussed at length. Ollala-Tarraga ’ s assumption is likely a result of Bergmann ’ s (1847) paper being published in German, a language that many scientists are not able to read. It shows, however, and contrary to Meiri (2011), that it is necessary to refer to original publications for the under-standing of their meaning. Th erefore, it was the scope of our paper (Watt et al. 2010) to provide insights into Bergmann ’ s rule by referring to the original publication. Th at the rule is a causal law is not an assumption made by Watt et al. (2010); it is how Bergmann (1847) defi ned his rule. We agree with Olalla-T á rraga (2011) that there is hardly any law that is uni-versally true, and rules themselves are much more fl exible than laws (Lawton 1999). Bergmann ’ s rule is certainly not exempt. Bergmann specifi cally discusses exceptions to his rule and proposes potential explanations for why these cases may exist. For instance, Bergmann (1847) discussed quality of feathers and available food as some potential explanations for why not all bird species within a genus he investigated conformed to the rule. Olalla-T á rraga (2011) has a valid point, that ‘ having a rule without an inherent mechanism is indeed very useful ’ ; however, most authors (Brown and Lee 1969, McNab 1971, Mousseau 1997, Olalla-T á rraga and Rodr í guez 2007, Rodr í guez et al. 2008) touch on proposed mechanisms when they are evaluating Bergmann ’ s rule, regardless of whether or not they believe the mechanism is

Oikos 120: 1445–1447, 2011 doi: 10.1111/j.1600-0706.2011.19968.x

© 2011 Th e Authors. Oikos © 2011 Nordic Society Oikos Subject Editor: Bradford Hawkins. Accepted 10 May 2011

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inherent in the rule, suggesting they do value mechanistic explanations. Th e discrepancy in personal opinion regard-ing the usefulness of patterns with no mechanism does not change the fact that Bergmann ’ s (1847) rule was originally defi ned as a pattern with an inherent mechanism.

The mechanism

Olalla-T á rraga ’ s (2011) main argument is centered on the fact that he believes Bergmann ’ s heat conservation mechanism should be distinctly recognized as separate from the pattern, suggesting that a problem arises because ‘ a sim-ple falsifi cationist test of the mechanism might be enough to invalidate (we assume Olalla-T á rraga (2011) intended to use ‘ invalidate ’ rather than ‘ validate ’ in his summary) the rule ’ . Although we do believe a falsifi cation test of the mechanism would counter Bergmann ’ s rule, we do not sug-gest it would invalidate the pattern. Where we believe the problem arises is when researchers claim the rule is invalid, when in fact it has not been tested under the conditions proposed by Bergmann. For instance, Blanckenhorn and Hellriegel (2002) found that fl y sperm increases in size with increasing temperature, and suggest this is evidence ‘ against Bergmann ’ s rule. ’ It is incorrect to disprove a rule without testing it within the framework it was originally proposed. Invalidation of Bergmann ’ s rule under investiga-tion in the wrong circumstances occurs far more frequently in the literature than invalidation based on Bergmann ’ s pro-posed mechanism (references in Watt et al. 2010 Table 1). By testing the rule as originally proposed, we can prevent opponents of the rule from claiming to have invalidated it without proper investigation.

Olalla-T á rraga (2011) asks Watt et al. (2010) how we reconcile single versus multiple hypothesis tests for Bergmann ’ s rule if the mechanism is inherent in the rule. In hindsight our quote ‘ it is time research focuses on the mechanisms underlying Bergmann ’ s rule rather than the constant evidence that the pattern does or does not exist ’ , should instead read ‘ it is time research focuses on the mecha-nisms underlying Bergmann ’ s pattern ’ , and we apologize for this oversight. We believe multiple hypotheses should be investigated for Bergmann ’ s pattern, but because he defi ned his rule with a clear and stated mechanism, the rule itself can only be tested within this framework. At the very least, this mechanism should be tested prior to reformulating the rule.

Even if one argues the pattern is separate from the mechanism, the defi ned rule clearly states the pattern should exist in ‘ homoiotherm ’ animals (Bergmann 1847). (Olalla-T á rraga 2011 stated Bergmann ’ s rule was formulated for mam-mals; however, the rule was formulated for ‘ homoiotherm ’ animals (Bergmann 1847 p. 601) and a quest for the occur-rence of geographic size clines was conducted on birds (Berg-mann1847 p. 646–676). It is here where we believe there has been a misunderstanding with our original paper; we do notdismiss a thermoregulatory mechanism to explain body size clines in ectotherms, or particularly support other mechanisms, we simply state that this is not Bergmann ’ s rule (Watt et al. 2010 p. 96). Th e intention of our paper was not to fully encapsulate all potential mechanisms for why Bergmann size clines exist in any organism, and it is likely that

there will be new mechanisms proposed and discovered in the future. We agree with Olalla-T á rraga (2011) that ‘ we should avoid confl ation of pattern and process if we are to gain fur-ther insights into the main … . determinants of geographic body size gradients ’ , but Bergmann did not only propose body size gradients, he proposed a mechanism for why these gradients existed in ‘ homoiotherm ’ vertebrates. For investiga-tions of body size gradients, we agree many hypotheses should be investigated, and we have no qualms with authors investi-gating body size gradients in all organisms at a variety of taxo-nomic levels (Watt et al. 2010 p. 95). Olalla-T á rraga (2011)refers to a well and carefully written paper by Chown and Gaston (2010) as a prime example of the numerous mecha-nisms that may underlie Bergmann ’ s rule; however, Chown and Gaston (2010) only discuss Bergmann size clines, not the rule itself (although Bergmann ’ s rule is mentioned, albeit briefl y, when discussing how ‘ size increases with latitude and altitude are often referred to as Bergmann ’ s rule ’ ). Th us, the authors have in their own way separated pattern from process.

Olalla-T á rraga (2011) also discusses a potential thermo-regulatory mechanism that may be responsible for maintain-ing Bergmann size clines in both ectotherms and endotherms. We did not intend to dismiss a thermoregulatory mechanismfor maintaining body size gradients in ectotherms and state that ‘ ectotherms can be homoiotherms ’ and that ‘ the terminology used to defi ne the rule is vital ’ (Watt et al. 2010 p. 94). Despite this, ectotherms do not meet the criteria for the thermoregulation mechanism as presented by Bergmann (1847). He proposed ‘ animals have to produce less warmth in relation to their size to raise their temperature above that of their surrounding the larger they are ’ (Bergmann 1847 p. 601), and thus ‘ creating warmth ’ was a prerequisite for Bergmann ’ s proposed mechanism. We understand that ‘ ecto-therms regulate their body temperatures … through behav-ior, physiology and morphology ’ (Olalla-T á rraga 2011), and Bergmann (1847) discusses these methods of temperature control for ectotherms at length. Nevertheless, Bergmann formulates the rule for endotherms only.

Th e heat balance hypothesis (Olalla-T á rraga and Rodr í guez 2007) may be a valid explanation for body size gradients in both endotherms and ectotherms, we never assumed that it would not, but again, this could not be Bergmann ’ s rule. In our original paper (Watt et al. 2010) we highlighted two general mechanisms that may explain Bergmann size clines and by no means was this an inclusive list. For ease of read-ing it was logical to describe the two mechanisms separately; however, in no way did we mean to assume that the hypoth-eses regarding food availability were mutually exclusive from the thermoregulation mechanism proposed by Bergmann. It is likely that geographic body size gradients in endotherms are defi ned by a combination of these mechanisms, and in ectotherms it is likely that a combination of thermoregula-tion (although not in the sense defi ned by Bergmann) andother mechanisms can describe body size gradients. McNab (2010) suggests that the ‘ resource rule ’ may account for the tendency of mammals to increase or decrease body size with response to geography. Th is rule would encompass Bergmann ’ s rule, the island rule, Dehnel ’ s phenomenon, and Cope ’ s rule, and, although not discussed by McNab (2010), may be a unifying rule to account for body size changes in both endotherms and ectotherms.

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Conclusion

Bergmann ’ s rule, as defi ned by Bergman (1847), encom-passes only those studies that investigate heat conservation mechanisms in endotherms as a mechanism for the observed pattern. We argue to use multiple approaches to investigate Bergmann ’ s size clines, but if these studies investigate other mechanisms they are not studies testing Bergmann ’ s rule. We explicitly state that researchers should ‘ test for possible mechanisms responsible for body size trends in ectotherms and endotherms ’ (Watt et al. 2010); thus, we very much support multiple hypothesis testing, but these tests would not be evaluating Bergmann ’ s rule, but rather geographic body size patterns, or Bergmann size clines. Bergmann ’ s rule, as stated by Bergmann, inherently includes mecha-nism (James 1970, Geist 1990). Over time, researchers have either ignored this portion of the rule to suit their needs, or have not realized the rule inherently encompassed mecha-nism because it has been redefi ned so many times. Perhaps the answer to the contention between pattern and process is that future studies examining Bergmann ’ s observed pattern in ectotherms, plants, or even endotherms with alternative mechanistic explanations, should refer to Bergmann ’ s size clines, as was done by Chown and Gaston (2010), or as geographic body size gradients, and not feel obliged to refer to Bergmann ’ s rule.

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