Bergmann's rule encompasses mechanism: a reply to Olalla‐Tárraga (2011)

The many definitions 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‐Tárraga 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‐Tárraga has only focused on the observed pattern and has ignored the proposed mechanism, which is inherent in the definition. 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‐Tárraga's quest for a unifying mechanism to explain body size gradients in endotherms and ectotherms.     

A Reassessment of Bergmann's Rule in Modern Humans

It is widely accepted that modern humans conform to Bergmann''s rule, which holds that body size in endothermic species will increase as temperature decreases. However, there are reasons to question the reliability of the findings on which this consensus is based. One of these is that the main studies that have reported that modern humans conform to Bergmann''s rule have employed samples that contain a disproportionately large number of warm-climate and northern hemisphere groups. With this in mind, we used latitudinally-stratified and hemisphere-specific samples to re-assess the relationship between modern human body size and temperature. We found that when groups from north and south of the equator were analyzed together, Bergmann''s rule was supported. However, when groups were separated by hemisphere, Bergmann''s rule was only supported in the northern hemisphere. In the course of exploring these results further, we found that the difference between our northern and southern hemisphere subsamples is due to the limited latitudinal and temperature range in the latter subsample. Thus, our study suggests that modern humans do conform to Bergmann''s rule but only when there are major differences in latitude and temperature among groups. Specifically, groups must span more than 50 degrees of latitude and/or more than 30°C for it to hold. This finding has important implications for work on regional variation in human body size and its relationship to temperature.     

Bergmann's rule: a biophysiological rule examined in birds

The most studied ecogeographic rule is Bergmann's rule, but aspects of the original paper are often presented incorrectly even though Bergmann (1847) is explicitly cited. The goal of this paper is to 1) summarize the contents of Bergmann's paper, supported by direct translations, and 2) to discuss the main issues surrounding Bergmann's rule based on Bergmann's intentions and early definitions of the rule. Although Bergmann himself never formulated an explicit rule, based on Bergmann's (1847) intentions and early definitions of Bergmann's rule, Bergmann's rule is: “Within species and amongst closely related species of homeothermic animals a larger size is often achieved in colder climates than in warmer ones, which is linked to the temperature budget of these animals.” Bergmann (1847) assumed that the surface area of an animal is a measure for heat dissipation and an animal's volume a measure of its heat production. As body size increases, an animal's surface area increases less than its volume; however, modifications in morphology and behaviour will also influence the temperature budget. Bergmann hypothesized that when everything but size is equal, the smaller animals should live in warmer areas. This was supported by empirical data on > 300 bird species belonging to 86 genera. Recommendations for use of the term Bergmann's rule include 1) inclusion of a thermoregulatory mechanism, 2) application only to homoeothermic animals, 3) but to any taxonomic group, 4) tests of the rule should test the assumption that larger animals have to produce less heat to increase body temperatures, and 5) future authors should either go back to the original publication (Bergmann 1847) when referring to it or simply not cite it at all. Synthesis Based on Bergmann's (1847) intentions and early definitions, Bergmann's rule is: “Within species and amongst closely related species of homeothermic animals a larger size is often achieved in colder climates than in warmer ones, which is linked to the temperature budget of these animals.” Recommendations for use of the term Bergmann's rule include 1) inclusion of a thermoregulatory mechanism, 2) application only to homoeothermic animals, 3) and to any taxonomic group, 4) tests of the rule should examine whether larger animals have to produce less heat to increase body temperatures, and 5) authors should go back to the original publication (Bergmann 1847) when referring to it.     

Patterns of within-species body size variation of birds: strong evidence for Bergmann's rule

Aim The aim of this study is to test whether Bergmann's rule, a general intraspecific tendency towards larger body size in cooler areas and at higher latitudes, holds for birds throughout the world. Location This study includes information on species of birds from throughout the world. Methods I gathered data on body size variation from the literature and used two general meta‐analytical procedures to test the validity of Bergmann's rule in birds: a modified vote‐counting approach and calculation of overall effect sizes. Related species may show similar body size trends, thus I performed all analyses using nonphylogenetic and phylogenetic methods. I used tests of phylogenetic signal for each data set to decide which type of statistical analysis (nonphylogenetic or phylogenetic) was more appropriate. Results The majority of species of birds (76 of 100 species) are larger at higher latitudes, and in cooler areas (20 of 22 species). Birds show a grand mean correlation coefficient of +0.32 for body size and latitude, and ?0.81 for body size and temperature, both significant trends. Sedentary species show stronger body size trends in some, but not all, analyses. Neither males nor females consistently have stronger body size trends. Additionally, the strength of body size trends does not vary with latitude or body mass. Conclusions Bergmann's rule holds for birds throughout the world, regardless of whether temperature or latitude (as a proxy) is used. Previous studies have suggested that Bergmann's rule is stronger for sedentary than migratory species, males than females and temperate than tropical taxa. I did not find strong support for any of these as general themes for birds, although few studies of tropical taxa have been conducted. The processes responsible for Bergmann's rule remain somewhat of a black box; however, fasting endurance is probably a more important factor than the traditional hypothesis of heat conservation.     

The converse to Bergmann's rule in bumblebees,a phylogenetic approach

Two patterns commonly emerge when animal body size is analyzed as a function of latitudinal distribution. First, body size increases with latitude, a temperature effect known as Bergmann's rule, and second, the converse to Bergmann's rule, a pattern in which body size decreases with latitude. However, other geographic patterns can emerge when the mechanisms that generate Bergmann's and the converse to Bergmann's clines operate together. Here, we use phylogenetic comparative analysis in order to control for phylogenetic inertia, and we show that bumblebees exhibit the converse to Bergmann's rule. Bumblebee taxa are distributed worldwide in temperate and tropical regions. The largest species are found in places with high water availability during the driest time of the year. Nonetheless, large body size is constrained by extreme temperatures. Bumblebees’ body size could be related to a higher extent to the size of food rewards to be harvested than to the energetic advantages of thermoregulation. Moreover, we found that the body size of eusocial and cuckoo species responded in the same way to environmental variables, suggesting that they have not diverged due to different selective pressures.     

Body size phenology in a regional bee fauna: a temporal extension of Bergmann's rule

Bergmann's rule originally described a positive relationship between body size and latitude in warm‐blooded animals. Larger animals, with a smaller surface/volume ratio, are better enabled to conserve heat in cooler climates (thermoregulatory hypothesis). Studies on endothermic vertebrates have provided support for Bergmann's rule, whereas studies on ectotherms have yielded conflicting results. If the thermoregulatory hypothesis is correct, negative relationships between body size and temperature should occur in temporal in addition to geographical gradients. To explore this possibility, we analysed seasonal activity patterns in a bee fauna comprising 245 species. In agreement with our hypothesis of a different relationship for large (endothermic) and small (ectothermic) species, we found that species larger than 27.81 mg (dry weight) followed Bergmann's rule, whereas species below this threshold did not. Our results represent a temporal extension of Bergmann's rule and indicate that body size and thermal physiology play an important role in structuring community phenology.     

Do New World pitvipers “scale‐down” at high elevations? Macroecological patterns of scale characters and body size

Bergmann's rule describes the macroecological pattern of increasing body size in response to higher latitudes and elevations. This pattern is extensively documented in endothermic vertebrates, within and among species; however, studies involving ectotherms are less common and suggest no consistent pattern for amphibians and reptiles. Moreover, adaptive traits, such as epidermal features like scales, have not been widely examined in conjunction with Bergmann's rule, even though these traits affect physiological processes, such as thermoregulation, which are hypothesized as underlying mechanisms for the pattern. Here, we investigate how scale characters correlate with elevation among 122 New World pitviper species, representing 15 genera. We found a contra‐Bergmann's pattern, where body size is smaller at higher elevations. This pattern was mainly driven by the presence of small‐bodied clades at high elevations and large‐bodied clades at low elevations, emphasizing the importance of taxonomic scope in studying macroecological patterns. Within a subset of speciose clades, we found that only Crotalus demonstrated a significant negative relationship between body size and elevation, perhaps because of its wide elevational range. In addition, we found a positive correlation between scale counts and body size but no independent effect of elevation on scale numbers. Our study increases our knowledge of Bergmann's rule in reptiles by specifically examining characters of squamation and suggests a need to reexamine macroecological patterns for this group.     

A global assessment of Bergmann's rule in mammals and birds

Bergmann's rule states that endotherms have a large body size in high latitudes and cold climates. However, previous empirical studies have reported mixed evidence on the relationships between body size and latitude, raising the question of why some clades of endotherms follow Bergmann's rule, whereas others do not. Here, we synthesized the interspecific relationships between body size and latitude among 16,187 endothermic species (5422 mammals and 10,765 birds) using Bayesian phylogenetic generalized linear mixed models to examine the strength and magnitude of Bergmann's rule. We further assessed the effect of biological and ecological factors (i.e., body mass categories, dietary guild, winter activity, habitat openness, and climate zone) on the variations in the body mass–latitude relationships by adding an interaction term in the models. Our results revealed a generally weak but significant adherence to Bergmann's rule among all endotherms at the global scale. Despite taxonomic variation in the strength of Bergmann's rule, the body mass of species within most animal orders showed an increasing trend toward high latitudes. Generally, large-bodied, temperate species, non-hibernating mammals, and migratory and open-habitat birds tend to conform to Bergmann's rule more than their relatives do. Our results suggest that whether Bergmann's rule applies to a particular taxon is mediated by not only geographic and biological features, but also potential alternate strategies that species might have for thermoregulation. Future studies could explore the potential of integrating comprehensive trait data into phylogenetic comparative analysis to re-assess the classic ecogeographic rules on a global scale.     

Conformity to Bergmann's rule in birds depends on nest design and migration

Ecogeographical rules attempt to explain large‐scale spatial patterns in biological traits. One of the most enduring examples is Bergmann''s rule, which states that species should be larger in colder climates due to the thermoregulatory advantages of larger body size. Support for Bergmann''s rule, however, is not consistent across taxonomic groups, raising questions about what factors may moderate its effect. Behavior may play a crucial, yet so far underexplored, role in mediating the extent to which species are subject to environmental selection pressures in colder climates. Here, we tested the hypothesis that nest design and migration influence conformity to Bergmann''s rule in a phylogenetic comparative analysis of the birds of the Western Palearctic, a group encompassing dramatic variation in both climate and body mass. We predicted that migratory species and those with more protected nest designs would conform less to the rule than sedentary species and those with more exposed nests. We find that sedentary, but not short‐ or long‐distance migrating, species are larger in colder climates. Among sedentary species, conformity to Bergmann''s rule depends, further, on nest design: Species with open nests, in which parents and offspring are most exposed to adverse climatic conditions during breeding, conform most strongly to the rule. Our findings suggest that enclosed nests and migration enable small birds to breed in colder environments than their body size would otherwise allow. Therefore, we conclude that behavior can substantially modify species’ responses to environmental selection pressures.     

On the validity of Bergmann's rule

Aim We reviewed the occurrence of Bergmann's rule in birds (ninety‐four species) and mammals (149 species), using only studies where statistical significance of the results was tested. We also tested whether studies using different characters as surrogates of body size have a different tendency to conform to Bergmann's rule, whether body size and nest type (in birds) have an influence on the tendency to conform to the rule, and whether sedentary birds conform to the rule more than migratory birds. Location Worldwide. Methods We reviewed published data on geographic and temporal variation in body size, using only studies where the statistical significance of the results was tested. We asked how many species conform to the rule out of all species studied in each order and family. Results Over 72% of the birds and 65% of the mammal species follow Bergmann's rule. An overall tendency to follow the rule occurs also within orders and families. Studies using body mass in mammals show the greatest tendency to adhere to Bergmann's rule (linear measurements and dental measurements show a weaker tendency); while in birds, studies using body mass and other surrogates (linear measurements and egg size) show a similar tendency. Birds of different body mass categories exhibit a similar tendency to follow Bergmann's rule, while in mammals the lower body size categories (4–50 and 50–500 g) show a significantly lower tendency to conform to the rule. Sedentary birds tend to conform to Bergmann's rule more than migratory species. Nest type does not affect the tendency to conform to Bergmann's rule. Main conclusions Bergmann's rule is a valid ecological generalization for birds and mammals.     

Bergmann's rule in alien birds

Native bird species show latitudinal gradients in body size across species (Bergmann's rule), but whether or not such gradients are recapitulated in the alien distributions of bird species are unknown. Here, we test for the existence of Bergmann's rule in alien bird species worldwide, and investigate the causes of the observed patterns. Published databases were used to obtain the worldwide distributions of established alien bird populations, the locations of alien bird introductions, and bird body masses. Randomisation tests and linear models were used to assess latitudinal patterns in the body masses of introduced and established alien bird populations. Established alien bird species exhibit Bergmann's rule, but this is largely explained by where alien bird species have been introduced: latitudinal variation in the body masses of established alien bird species simply reflects latitudinal variation in the body masses of introduced species. There is some evidence that body mass is implicated in whether or not established species’ alien ranges spread towards or contract away from the Equator following establishment. However, most alien bird ranges are encompassed by the latitudinal band(s) to which the species was introduced. Bergmann's rule in alien birds is therefore a consequence of where humans have introduced different species, rather than of natural processes operating after population introduction.     

Bergmann's Rule – what's in a name?

Despite the great interest it generates, the definition of Bergmann's Rule is vague and often contested. Debate focuses on whether the rule should be described in terms of pattern or process, what taxa it should apply to and what taxonomic level it should be associated with. Here I review the historical development of studies of Bergmann's Rule. I suggest that Bergmann thought that his rule should be strongest at the intra‐specific level, rather than between closely related species as is usually thought. I argue that the rule is a pattern that can be studied regardless of mechanism in any taxon and at any taxonomic level.     

Patterns of size variation in bees at a continental scale: does Bergmann's rule apply?

Body size latitudinal clines have been widley explained by the Bergmann's rule in homeothermic vertebrates. However, there is no general consensus in poikilotherms organisms in particular in insects that represent the large majority of wildlife. Among them, bees are a highly diverse pollinators group with high economic and ecological value. Nevertheless, no comprehensive studies of species assemblages at a phylogenetically larger scale have been carried out even if they could identify the traits and the ecological conditions that generate different patterns of latitudinal size variation. We aimed to test Bergmann's rule for wild bees by assessing relationships between body size and latitude at continental and community levels. We tested our hypotheses for bees showing different life history traits (i.e. sociality and nesting behaviour). We used 142 008 distribution records of 615 bee species at 50 × 50 km (CGRS) grids across the West Palearctic. We then applied generalized least squares fitted linear model (GLS) to assess the relationship between latitude and mean body size of bees, taking into account spatial autocorrelation. For all bee species grouped, mean body size increased with higher latitudes, and so followed Bergmann's rule. However, considering bee genera separately, four genera were consistent with Bergmann's rule, while three showed a converse trend, and three showed no significant cline. All life history traits used here (i.e. solitary, social and parasitic behaviour; ground and stem nesting behaviour) displayed a Bergmann's cline. In general there is a main trend for larger bees in colder habitats, which is likely to be related to their thermoregulatory abilities and partial endothermy, even if a ‘season length effect’ (i.e. shorter foraging season) is a potential driver of the converse Bergmann's cline particularly in bumblebees.     

Body size and elevation: do Bergmann's and Rensch's rule apply in the polytypic bushcricket Poecilimon veluchianus?

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Morphological variations in a widely distributed Eastern Asian passerine cannot be consistently explained by ecogeographic rules

Ecogeographic rules that describe quantitative relationships between morphologies and climate might help us predict how morphometrics of animals was shaped by local temperature or humidity. Although the ecogeographic rules had been widely tested in animals of Europe and North America, they had not been fully validated for species in regions that are less studied. Here, we investigate the morphometric variation of a widely distributed East Asian passerine, the vinous‐throated parrotbill (Sinosuthora webbiana), to test whether its morphological variation conforms to the prediction of Bergmann''s rule, Allen''s rules, and Gloger''s rule. We at first described the climatic niche of S. webbiana from occurrence records (n = 7838) and specimen records (n = 290). The results of analysis of covariance (ANCOVA) suggested that the plumage coloration of these parrotbills was darker in wetter/warmer environments following Gloger''s rule. However, their appendage size (culmen length, beak volume, tarsi length) was larger in colder environments, the opposite of the predictions of Allen''s rule. Similarly, their body size (wing length) was larger in warmer environments, the opposite of the predictions of Bergmann''s rule. Such disconformity to both Bergmann''s rule and Allen''s rule suggests that the evolution of morphological variations is likely governed by multiple selection forces rather than dominated by thermoregulation. Our results suggest that these ecogeographic rules should be validated prior to forecasting biological responses to climate change especially for species in less‐studied regions.     

Functional adaptation rather than ecogeographical rules determine body-size metrics along a thermal cline with elevation in the Chinese pygmy dormouse (Typhlomys cinereus)

Phenotypic plasticity is crucial for how organisms respond to variation in their environment, affecting their diversity and distribution, especially in the light of rapid environmental change. Ecogeographical rules predict an association between specific adaptive morphological and physiological traits with cooler conditions due to higher latitude, elevation, or climate change. Such ecogeographical effects are often most evident in ancient species due to continuous selective adaptation occurring over long periods of time. Here, we use the suitably ancient Chinese pygmy dormouse (Typhlomys cinereus) to test whether body-size, appendage length and heart size vary in accordance with Bergmann's, Allen's and Hesse's rule, respectively. Based on a sample of 67 adult individuals (female, n = 29; male n = 38) trapped at 37 sites transcending an elevational range from 414 to 1757 m, we tested for trait concordance with Bergmann's rule (body mass, length and SMI), Allen's rule (length of tail, foot, ear, snout), and Hesse's rule (wet and dry heart mass). Effects of elevation (and thus temperature lapse rate; calculated as 0.61 °C per 100 m) on body size, appendage length and heart size, were tested by fitting Standardized Major Axis (SMA) models. We observed substantial heterogeneity in morphometric traits allowing for the detection of ecogeographical clines. However, none conformed with Bergmann's, Allen's (except ear size), or Hesse's rule. However, our results indicate some support for Geist's rule of net primary productivity. We conclude that pervasive functional life-history adaptations in this blind, arboreal, echolocating ancient species exceeded selection for morphological energy efficiency constraints, with the notable exception of reduced ear pinnae size at colder, elevated sites. This is an important consideration for predicting how species, and populations in general, may adapt to human induced rapid environmental change, contrary to expectations of warming driving selection for smaller body-size.     

Bergmann's and Rensch's rules and the spur‐thighed tortoise (Testudo graeca)

Body size is an ecologically important variable in animals. The geographical size variation of most snakes and some lizards counters Bergmann's rule in that, among related taxa, the larger ones live at warmer latitudes. However, exceptions notwithstanding, and despite being ectothermic, turtles as a group tend to obey Bergmann's rule. We examined this idea in Testudo graeca, ranging from Morocco to Romania and to Iran with disputed systematics, both at the global scale (using literature) and within the focal area of Israel (using museum specimens). Both globally and locally, carapace length correlated with latitude, in accordance with Bergmann's rule. The scant data on reproduction fully support the hypothesis that Bergmann's rule enables larger clutches where the climate would limit repeated clutches. The sexual size dimorphism (SSD) was approached using two methodologies: (1) ‘conventional’, using globally literature data and locally museum samples and (2) ‘innovated’, using photographs of copulating tortoises from Israel and Turkey. By each methodology, SSD emerged as being male biased in the larger‐bodied populations and female biased in the smaller‐bodied populations, obeying Rensch's rule. Some observations support the hypothesis that the evolution of large males serves intermale combating. Finally, Rensch's rule was found to apply separately within Anatolia and within the Levant, possibly indicating that these populations are separate.     

Multiple selection pressures generate adherence to Bergmann's rule in a Neotropical migratory songbird

Aim Bergmann's rule, the tendency for body size to be positively correlated with latitude, is widely accepted but the mechanisms behind the patterns are still debated. Bergmann's originally conceived mechanism was based on heat conservation; other proposed mechanisms invoke phylogeny, migration distance and resource seasonality. With the goal of examining these mechanisms, we quantified morphological variation across the breeding range of a Neotropical migratory songbird, the cerulean warbler (Dendroica cerulea). Location Deciduous forests of eastern North America. Methods We sampled nine cerulean warbler populations, spanning the species’ breeding range. We captured 156 males using targeted playback and model presentation, and included 127 adult males in our analyses of morphological variation. We used an information‐theoretical approach to identify climatic variables associated with geographical variation in body size. Results Cerulean warbler body size adheres to Bergmann's rule: individuals in northern populations are larger than those in southern populations. Variation in body size is best explained by variation in dry and wet‐bulb temperature and actual evapotranspiration. Main conclusions Adherence to Bergmann's rule by the cerulean warbler appears to be linked to thermodynamics (heat conservation in the north, evaporative cooling in the south) and resource seasonality. Multiple selection pressures can interact to generate a single axis of morphological geographical variation, and even subtle fluctuations in climatic variables can exert significant selection pressures. We suggest that the influence of selection pressures on migrants might be enhanced by migratory connectivity, providing further support for the important role played by this phenomenon in the ecology, evolution and population dynamics of migratory songbirds.