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.     

An interspecific test of Bergmann's rule reveals inconsistent body size patterns across several lineages of water beetles (Coleoptera: Dytiscidae)

1. Bergmann's rule sensu lato, the ecogeographic pattern relating animals' body size with environmental temperature (or latitude), has been shown to be inconsistent among insect taxa. Body size clines remain largely unexplored in aquatic insects, which may show contrasting patterns to those found in terrestrial groups because of the physiological or mechanical constraints of the aquatic environment. 2. Bergmann's rule was tested using data on body size, phylogeny and distribution for 93 species belonging to four lineages of dytiscid water beetles. The relationship between size and latitude was explored at two taxonomic resolutions – within each independent lineage, and for the whole dataset – employing phylogenetic generalised least‐squares to control for phylogenetic inertia. The potential influence of habitat preference (lotic versus lentic) on body size clines was also considered. 3. Within‐lineage analyses showed negative relationships (i.e. converse Bergmann's rule), but only in two lineages (specifically in those that included both lotic and lentic species). By contrast, no relationship was found between body size and latitude for the whole dataset. 4. These results suggest that there may be no universal interspecific trends in latitudinal variation of body size in aquatic insects, even among closely related groups, and show the need to account for phylogenetic inertia. Furthermore, habitat preferences should be considered when exploring latitudinal clines in body size in aquatic taxa at the interspecific level.     

Bergmann's rule in nonavian reptiles: turtles follow it,lizards and snakes reverse it

Abstract Bergmann's rule is currently defined as a within-species tendency for increasing body size with increasing latitude or decreasing environmental temperature. This well-known ecogeographic pattern has been considered a general trend for all animals, yet support for Bergmann's rule has only been demonstrated for mammals and birds. Here we evaluate Bergmann's rule in two groups of reptiles: chelonians (turtles) and squamates (lizards and snakes). We perform both nonphylogenetic and phylogenetic analyses and show that chelonians follow Bergmann's rule (19 of 23 species increase in size with latitude; 14 of 15 species decrease in size with temperature), whereas squamates follow the converse to Bergmann's rule (61 of 83 species decrease in size with latitude; 40 of 56 species increase in size with temperature). Size patterns of chelonians are significant using both nonphylogenetic and phylogenetic methods, whereas only the nonphylogenetic analyses are significant for squamates. These trends are consistent among major groups of chelonians and squamates for which data are available. This is the first study to document the converse to Bergmann's rule in any major animal group as well as the first to show Bergmann's rule in a major group of ectotherms. The traditional explanation for Bergmann's rule is that larger endothermic individuals conserve heat better in cooler areas. However, our finding that at least one ectothermic group also follows Bergmann's rule suggests that additional factors may be important. Several alternative processes, such as selection for rapid heat gain in cooler areas, may be responsible for the converse to Bergmann's rule in squamates.     

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 explains interspecific variation in size–latitude relationships in geographically widespread beetle species

1. In most birds and mammals, larger individuals of the same species tend to be found at higher latitudes, but in insects, body size–latitude relationships are highly variable. 2. Recent studies have shown that larger‐bodied insect species are more likely to decrease in size when reared at increased temperature, compared with smaller‐sized species. These findings have led to the prediction that a positive relationship between body size and latitude should be more prevalent in larger‐bodied insect species. 3. This study measured the body size of > 4000 beetle specimens (12 species) collected throughout North America. Some beetle species increased in size with latitude, while others decreased. Importantly, mean species body size explained c. 30% of the interspecific variation in the size–latitude response. 4. As predicted, larger‐bodied beetle species were more likely to show a positive relationship between body size and latitude (Bergmann's rule), and smaller‐bodied species were more likely to show a negative body size–latitude relationship (inverse Bergmann's rule). 5. These body size–latitude patterns suggest that size‐specific responses to temperature may underlie global latitudinal distributions of body size in Coleoptera, as well as other insects.     

Body size variation among mainland populations of the western rattlesnake (Crotalus viridis)

In general, squamate reptiles follow the converse to Bergmann's rule, attaining smaller sizes in cooler environments, whereas other vertebrate groups follow Bergmann's rule, attaining larger sizes in cooler areas. Intensive studies of body size evolution for species of squamates are necessary to understand the processes responsible for this trend. Here I present data on body size variation among mainland populations of the western rattlesnake, Crotalus viridis. This species consists of two well-differentiated phylogenetic clades, therefore all analyses were performed for the C. viridis group as a whole and separately for each of the two clades within the C. viridis group. Although both phylogenetic and nonphylogenetic analyses were performed, the data did not show phylogenetic conservatism, and therefore the nonphylogenetic results are preferred. I found no significant relationships between mean adult female snout-vent length and any of the physical and climatic variables that were examined for the C. viridis group using simple linear regression analysis. Examined separately, I found that individuals of the western clade, C. oreganus, were smaller in cooler and more seasonal environments, whereas individuals of the eastern clade. C. viridis sensu stricto, were larger in cooler and more seasonal areas. Thus, the observed size trends were in opposite directions for the two clades. Multiple regression analysis revealed that seasonality was a stronger predictor of body size variation than was temperature for both clades. The differences in body size trends between these clades may be due to differences in mortality rates among populations.     

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.     

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.     

Rule reversal: Ecogeographical patterns of body size variation in the common treeshrew (Mammalia,Scandentia)

There are a number of ecogeographical “rules” that describe patterns of geographical variation among organisms. The island rule predicts that populations of larger mammals on islands evolve smaller mean body size than their mainland counterparts, whereas smaller‐bodied mammals evolve larger size. Bergmann's rule predicts that populations of a species in colder climates (generally at higher latitudes) have larger mean body sizes than conspecifics in warmer climates (at lower latitudes). These two rules are rarely tested together and neither has been rigorously tested in treeshrews, a clade of small‐bodied mammals in their own order (Scandentia) broadly distributed in mainland Southeast Asia and on islands throughout much of the Sunda Shelf. The common treeshrew, Tupaia glis, is an excellent candidate for study and was used to test these two rules simultaneously for the first time in treeshrews. This species is distributed on the Malay Peninsula and several offshore islands east, west, and south of the mainland. Using craniodental dimensions as a proxy for body size, we investigated how island size, distance from the mainland, and maximum sea depth between the mainland and the islands relate to body size of 13 insular T. glis populations while also controlling for latitude and correlation among variables. We found a strong negative effect of latitude on body size in the common treeshrew, indicating the inverse of Bergmann's rule. We did not detect any overall difference in body size between the island and mainland populations. However, there was an effect of island area and maximum sea depth on body size among island populations. Although there is a strong latitudinal effect on body size, neither Bergmann's rule nor the island rule applies to the common treeshrew. The results of our analyses demonstrate the necessity of assessing multiple variables simultaneously in studies of ecogeographical rules.     

The fiddler crab,Minuca pugnax,follows Bergmann's rule

Bergmann's rule predicts that organisms at higher latitudes are larger than ones at lower latitudes. Here, we examine the body size pattern of the Atlantic marsh fiddler crab, Minuca pugnax (formerly Uca pugnax), from salt marshes on the east coast of the United States across 12 degrees of latitude. We found that M. pugnax followed Bergmann's rule and that, on average, crab carapace width increased by 0.5 mm per degree of latitude. Minuca pugnax body size also followed the temperature–size rule with body size inversely related to mean water temperature. Because an organism's size influences its impact on an ecosystem, and M. pugnax is an ecosystem engineer that affects marsh functioning, the larger crabs at higher latitudes may have greater per‐capita impacts on salt marshes than the smaller crabs at lower latitudes.     

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.     

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.     

Macroecology and the hierarchical expansion of evolutionary theory

The constraint envelope describing the relationship between geographical range size and body size has usually been explained by a minimum viable population size model, furnishing a strong argument for species selection if geographical range size turns out to be ‘heritable’. Recent papers have questioned this assumption of nonzero geographical range heritability at a phylogenetic level, meaning that the logic that constraint envelopes provide support for higher‐level selection fails. However, I believe that analysis of constraint envelopes can still furnish insights for the hierarchical expansion of evolutionary theory because the fitness furnished by variation in body size, which is frequently measured as a highly ‘heritable’ trait at the species level, can be partitioned into anagenetic and cladogenetic components. The constraint envelope furnishes an explicit mechanism for large‐body biased extinction rates influencing the distribution of body size. More importantly, it is possible to envisage a scenario in which anagenetic trends driving an increase in body size in higher latitudes within species (Bergmann's rule) are counteracted by available habitat area or continental edges constraining overall species distribution in these higher latitudes, increasing the probability of extinction. Under this combined model, faunas at higher latitudes and under habitat constraints may reach equilibrium points between these opposing hierarchical adaptive forces at smaller body size than faunas with less intense higher‐level constraints and will tend to be more right‐skewed.     

Latitudinal and climatic variation in body size and dorsal scale counts in Sceloporus lizards:a phylogenetic perspective

Squamates often follow an inverse Bergmann's rule, with larger-bodied animals occurring in warmer areas or at lower latitudes. The size of dorsal scales in lizards has also been proposed to vary along climatic gradients, with species in warmer areas exhibiting larger scales, putatively to reduce heat load. We tested for these patterns in the diverse and widespread lizard genus Sceloporus. Among 106 species or populations, body size was associated positively with maximum temperature (consistent with the inverse of Bergmann's rule) and aridity, but did not covary with latitude. Scale size (inferred from the inverse relation with numbers of scales) was positively related to body size. Controlling for body size via multiple regression, scale size was associated negatively with latitude (best predictor), positively with minimum temperature, and negatively with aridity (similar results were obtained using scores from a principal components analysis of latitude and climatic indicators). Thus, lizards with larger scales are not necessarily found in areas with higher temperatures. Univariate analyses indicated phylogenetic signal for body size, scale counts, latitude, and all climate indicators. In all cases, phylogenetic regression models fit the data significantly better than nonphylogenetic models; thus, residuals for log(10) number of dorsal scale rows exhibited phylogenetic signal.     

The validity of ecogeographical rules is context‐dependent: testing for Bergmann's and Allen's rules by latitude and elevation in a widespread Andean duck

Consistent responses by various organisms to common environmental pressures represent strong evidence of natural selection driving geographical variation. According to Bergmann's and Allen's rules, animals from colder habitats are larger and have smaller limbs than those from warmer habitats to minimize heat loss. Although evidence supporting both rules in different organisms exists, most studies have considered only elevational or latitudinal temperature gradients. We tested for the effects of temperature associated with both elevation and latitude on body and appendage size of torrent ducks (Merganetta armata), a widespread species in Andean rivers. We found a negative relationship between body size and temperature across latitude consistent with Bergmann's rule, whereas there was a positive relationship between these variables along replicate elevational gradients at different latitudes. Limb‐size variation did not support Allen's rule along latitude, nor along elevation. High‐elevation ducks were smaller and had longer wings than those inhabiting lower elevations within a river. We hypothesize that temperature is likely a major selective pressure acting on morphology across latitudes, although hypoxia or air density may be more important along elevational gradients. We conclude that the effect of temperature on morphology, and hence the likelihood of documenting ecogeographical ‘rules’, depends on the environmental context in which temperature variation is examined. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111, 850–862.     

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.     

Interrelations of global macroecological patterns in wing and thorax size,sexual size dimorphism,and range size of the Drosophilidae

Support for macroecological rules in insects is mixed, with potential confounding interrelations between patterns rarely studied. We here investigate global patterns in body and wing size, sexual size dimorphism and range size in common fruit flies (Diptera: Drosophilidae) and explore potential interrelations and the predictive power of Allen's, Bergmann's, Rensch's and Rapoport's rules. We found that thorax length (r² = 0.05) and wing size (r² = 0.09) increased with latitude, supporting Bergmann's rule. Contrary to patterns often found in endothermic vertebrates, relative wing size increased towards the poles (r² = 0.12), a pattern against Allen's rule, which we attribute to selection for increased flight capacity in the cold. Sexual size dimorphism decreased with size, evincing Rensch's rule across the family (r² = 0.14). Yet, this pattern was largely driven by the virilis–repleta radiation. Finally, range size did not correlate with latitude, although a positive relationship was present in a subset of the species investigated, providing no convincing evidence for Rapoport's rule. We further found little support for confounding interrelations between body size, wing loading and range size in this taxon. Nevertheless, we demonstrate that studying several traits simultaneously at minimum permits better interpretation in case of multiple, potentially conflicting trends or hypotheses concerning the macroecology of insects.     

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.     

Knitting patterns of biodiversity,range size and body size in aquatic beetle faunas: significant relationships but slightly divergent drivers

1. Ecogeographical rules refer to recurring patterns in nature, including the latitudinal diversity gradient (LDG), Rapoport's rule and Bergmann's rule, amongst others. In the present study, the existence of these rules was examined for diving beetles (Coleoptera: Dytiscidae), a family of aquatic predatory beetles. 2. Assemblage‐level data were analysed for diving beetles, focusing on species richness, local contribution to beta diversity (LCBD), mean range size and mean body size across the biogeographical provinces of Northern Europe. First, each of these variables was correlated with latitude, and then variation in each variable was modelled using actual environmental variables in boosted regression tree analysis. 3. Species richness was found to decrease with latitude, LCBD increased with latitude, mean range size did not show a significant relationship with latitude, and mean body size decreased with latitude. The latter finding was in contrast to Bergmann's rule. The actual environmental variables best predicting variation in these four response variables varied among the models, although they generally included temperature‐related and land use variables as the most influential ones. 4. The results obtained in the present study suggest that diving beetles conformed to the LDG, did not follow Rapoport's rule, and showed a reversed latitudinal gradient in the context of Bergmann's rule. In addition, species‐poor provinces harboured ecologically most unique faunas, suggesting that species richness and LCBD are complementary measures of biodiversity. 5. Even though general support was not found for most of the ecogeographical rules examined, the findings of the present study are interesting because they suggest that aquatic ectothermic invertebrates may show patterns different from those originally described for terrestrial endothermic vertebrates.