Geographic gradients in body size: a clarification of Bergmann's rule

1997 marked the sesquicentenary of the publication by Carl Bergmann of the observation that, in general, large-bodied animal species tend to live further north than their small-bodied relatives. This has been dubbed Bergmann's rule in his honour. However, more than 150 years on, we appear to be little closer to a general understanding of the rule, or even to any consensus as to whether it exists. This is due in large part to confusion about the taxonomic level at which the rule is considered to operate, and to the conflation of pattern and mechanism. In this paper, we attempt to resolve this confusion by highlighting its sources, and by providing a definition of Bergmann's rule that is practical and useful, yet that retains the essential features of its original formulation. We conclude by briefly reviewing the mechanisms proposed to explain Bergmann's rule as we define it.     

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.     

Latitude, elevation and body mass variation in Andean passerine birds

• 1 Relationships between body mass and latitude, and body mass and elevation are examined in the assemblage of Andean passerine birds.
• 2 Across species, body mass is positively correlated with the mid‐point of the species elevational distribution, but there is no significant relationship between body mass and latitudinal range mid‐point.
• 3 When the assemblage is separated into Andean endemic and non‐endemic species, the former group shows a significant positive relationship between body mass and elevation, and the latter a significant positive relationship between body mass and latitude (‘Bergmann’s rule’). Andean endemic species exhibit Bergmann’s rule once elevation is controlled for using multiple regression.
• 4 These relationships are not a consequence of the phylogenetic non‐independence of species. All the effects shown are very weak, with latitude and elevation explaining only a few per cent of the variation in body mass. Relationships are strongest when phylogenetically controlled analyses are performed just within genera.
• 5 The implications of these results for the mechanistic understanding of Bergmann’s rule are discussed.

     

Bergmann's rule in the ant lion Myrmeleon immaculatus DeGeer (Neuroptera: Myrmeleontidae): geographic variation in body size and heterozygosity

Aim Geographic variation in body size and heterozygosity were surveyed for discrete populations of the ant lion, Myrmeleon immaculatus DeGeer, collected from the central and northeastern United States. Location Collection sites were located in the central and eastern United States ranging from western Oklahoma to northern New York. Methods We collected 872 M. immaculatus larvae from thirty-four collecting sites. At each site, we randomly sampled ant lion pits and collected between fifteen and fifty-two larvae in total. Larvae were preserved in 95% ETOH for morphological analysis and frozen in a ?80°C freezer for protein electrophoresis. We measured the body size of eighty-five preserved adult M. immaculatus obtained from museum collections using head width as an indicator of body size. Five enzymes [GPI (glucose phosphate isomerase), MDH (malate dehydrogenase), PEP (peptidase), DIA (diaphorase) and SOD (superoxide dismutase)] were used in the heterozygosity analyses. Results Larval and adult body size increased with latitude, but decreased with elevation. Average heterozygosity, measured at five polymorphic loci, also increased significantly with latitude. Minimum temperature variance was the best predictor of body size, whereas precipitation and maximum temperature were the best predictors of heterozygosity. Populations were genetically differentiated from one another and showed a pattern of isolation by distance, as measured by Wright's F_st values and Nei's genetic distances. Main conclusions Sampling artifacts, heat conservation, character displacement, cell-size variation, density-dependent mortality, and differential dispersal probably cannot account for latitudinal variation in ant lion body size. Our results implicate the importance of diurnal photoperiod, which varies with latitude, but not with elevation. Because photoperiod often controls growth, diapause, and metamorphosis, it may be an important determinant of latitudinal clines in body size and life history of insects.     

Carnivores, biases and Bergmann's rule

Studies of Bergmann's rule may encompass a non-random subsample of extant homeotherms. We examined patterns of correlation between skull length and geographical latitude in 44 species of carnivores in order to test the validity of Bergmann's rule in the Carnivora. Results were then compared to those of other studies. Significant positive correlation between skull length and latitude was found in 50% of carnivore species, while significant negative correlation was found in only 11% of species. These results indicate that the occurrence of Bergmann's rule in the Carnivora is less frequent than earlier published data suggest. Publication bias is not detected in published data. Therefore, previous studies of geographical size variation might be biased in favour of species known to follow Bergmann's rule.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 81 , 579–588.     

Against Bergmann's rule: fly sperm size increases with temperature

A long-standing school textbook biological rule, Bergmann's rule, asserts that animals (and their constituent parts) grow bigger when it is colder. This seems to hold for many warm-blooded animals, as well as for egg, cell and body size of most cold-blooded animals. A unifying mechanism producing this pattern has not been found. We here provide the first experimental evidence that the size of an important type of cell, namely sperm, increases (rather than decreases) with temperature in a cold-blooded animal, the yellow dung fly. By pointing to an exception, our work either questions the generality of one prominent category of explanation of Bergmann's rule, that of a physiological constraint, or alternatively suggests that sperm differ fundamentally in their physiology from other cells.     

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.     

Amphibians do not follow Bergmann's rule

The tendency for organisms to be larger in cooler climates (Bergmann's rule) is widely observed in endotherms, and has been reputed to apply to some ectotherms including amphibians. However, recent reports provide conflicting support for the pattern, questioning whether Bergmann's clines are generally present in amphibians. In this study, we measured 96,996 adult Plethodon from 3974 populations to test for the presence of Bergmann's clines in these salamanders. Only three Plethodon species exhibited a significant negative correlation between body size and temperature consistent with Bergmann's rule, whereas 37 of 40 species did not display a pattern consistent with this prediction. Further, a phylogenetic comparative analysis found no relationship between body size and temperature among species. A meta-analysis combining our data with the available data for other amphibian species revealed no support for Bergmann's rule at the genus (Plethodon), order (Caudata), or class (Amphibia) levels. Our findings strongly suggest that negative thermal body size clines are not common in amphibians, and we conclude that Bergmann's rule is not generally applicable to these taxa. Thus, evolutionary explanations of Bergmann's clines in other tetrapods need not account for unique life-history attributes of amphibians.     

Bergmann's rule in amphibians: combining demographic and ecological parameters to explain body size variation among populations in the common toad Bufo bufo

Large‐scale patterns of body size variation are described by well‐known generalizations such as Bergmann’s rule; the generality and underlying causes of these patterns have been much debated. Intraspecific extension of this rule was tested in various ectotherms, and evidence was found for both Bergmann and converse Bergmann clines. In this study, we explored spatial patterns of variation in a widespread amphibian, the Common toad (Bufo bufo), along a 2240 km latitudinal gradient across Europe. We tested for covariation of adult body size, age and growth parameters with latitude, altitude, length of activity period and mean temperature during this period using both original and literature data. We selected 13 European populations, representing a latitudinal range from 43 to 63°N and altitudinal range from 15 to 1850 m a.s.l. The length of activity period (12–33 weeks) and T_mean (6.6–15.6°C) significantly decreased as latitude and altitude of these populations increased. Mean body size decreased as latitude increased (not with altitude), and increased with T_mean (not with length of activity period). Mean and minimal adult age increased with latitude and altitude, longevity increased with altitude only. Age increased as length of activity period decreased (not with T_mean). The growth coefficient (0.32–0.92 in males, 0.18–0.74 in females, available for six populations) decreased as altitude increased, and increased as both length of activity period and T_mean increased; latitudinal trend was non‐significant. Our analysis shows that B. bufo clearly exhibited a converse Bergmann cline along latitudinal gradient, but not along altitudinal gradient; the main effect of elevation was on age. The effects of ecological conditions also differed: body size increased with T_mean, while age parameters were related to the length of activity period. This study highlights that, to identify causal factors underlying general ecogeographical rules, we have to take into account different phases of the life cycle, co‐variation among life history traits and ecological factors acting on each of these traits. In amphibians with complex life cycles, lack of appropriate demographical or ecological data may affect our understanding of the variety of observed body size patterns.     

Global biogeography and ecology of body size in birds

In 1847, Karl Bergmann proposed that temperature gradients are the key to understanding geographic variation in the body sizes of warm-blooded animals. Yet both the geographic patterns of body-size variation and their underlying mechanisms remain controversial. Here, we conduct the first assemblage-level global examination of 'Bergmann's rule' within an entire animal class. We generate global maps of avian body size and demonstrate a general pattern of larger body sizes at high latitudes, conforming to Bergmann's rule. We also show, however, that median body size within assemblages is systematically large on islands and small in species-rich areas. Similarly, while spatial models show that temperature is the single strongest environmental correlate of body size, there are secondary correlations with resource availability and a strong pattern of decreasing body size with increasing species richness. Finally, our results suggest that geographic patterns of body size are caused both by adaptation within lineages, as invoked by Bergmann, and by taxonomic turnover among lineages. Taken together, these results indicate that while Bergmann's prediction based on physiological scaling is remarkably accurate, it is far from the full picture. Global patterns of body size in avian assemblages are driven by interactions between the physiological demands of the environment, resource availability, species richness and taxonomic turnover among lineages.     

Subterranean rodents of the genus Ctenomys (Caviomorpha, Ctenomyidae) follow the converse to Bergmann's rule

Aim We analysed body‐size variation in relation to latitude, longitude, elevation and environmental variables in Ctenomys (tuco‐tucos), subterranean rodents in the Ctenomyidae (Caviomorpha). We tested the existence of inter‐ and intraspecific size clines to determine if these rodents follow Bergmann's rule, to compare intra‐ and interspecific size trends and to assess the relevance of the subterranean lifestyle on these trends. Location South America, south of 15° latitude. Methods This paper is based on 719 specimens of tuco‐tucos from 133 localities of Argentina, Bolivia, Chile, Paraguay, Peru and Uruguay, representing 47 named species and 32 undescribed forms. Intraspecific analyses were performed for Ctenomys talarum Thomas, 1898 and the Ctenomys perrensi Thomas, 1896 species complex. Head and body length and weight were used for estimating body size. Geographical independent variables included latitude, longitude and altitude. Environmental independent variables were mean minimal and maximal monthly temperature, mean annual temperature, mean minimal and maximal precipitation, and total annual precipitation. To estimate seasonality, the annual variability of the climatic factors was calculated as their coefficients of variation and the difference between maximum and minimum values. Mean annual actual evapotranspiration (AET), and mean annual, January (summer) and July (winter) potential evapotranspiration (PET) values were also calculated for each locality, as well as annual, summer and winter water balance (WB). Statistical analyses consisted of simple and multiple regression and nonparametric correlation. Results Body size of Ctenomys decreases interspecifically from 15°00′ S to 48°15′ S and from 56°33′ W to 71°46′ W, and is positively correlated with ambient temperature and precipitation. The best predictors of body size according to multiple regression analyses were mean annual temperature, the difference between mean maximum and minimum annual temperatures, annual PET, the difference between summer and winter PET, and annual and winter water balance. These patterns are repeated, but not identically, at a smaller geographical scale within the species C. talarum and the superspecies C. perrensi. Main conclusions Tuco‐tucos follow the converse to Bergmann's rule at the interspecific level. At the intraspecific level some parallel trends were observed, but the smaller scale of these analyses, involving a very reduced variation of environmental factors, necessitates caution in interpreting results. The subterranean lifestyle probably insulates these rodents from the external temperature. The observed latitudinal body‐size gradients are more probably related to seasonality, ambient energy, primary productivity and/or intensity of predation.     

Latitudinal and altitudinal body size variation among north-west European land snail species

Aim To investigate latitudinal and altitudinal patterns in body size variation among north‐west European land snail species, as well as factors influencing such patterns. Location Latitudinal patterns were investigated in north‐west Europe from the British Isles and France in the west to Finland, Poland, Slovakia and Hungary in the east and from Norway in the north to France (with the exception of the Mediterranean part of the country), Switzerland, Austria and Hungary in the south. Altitudinal patterns were examined in the Alps in Austria and Switzerland. Methods Data on latitudinal ranges of 366 north‐west European land snail species, on altitudinal ranges of 175 species from Austria and 150 species from Switzerland, and on their body sizes were used to test for the presence of interspecific latitudinal or altitudinal body size patterns. Four methods, Stevens’ method, the midpoint method, the across‐species method, and a phylogenetically controlled analysis (CAIC) were applied. Results As a result of the predominance of some small bodied clades at higher latitudes and some large bodied clades at lower latitudes, body size of north‐west European land snails decreases significantly with increasing latitude. However, little of the body size variation across species is explained by latitude and the phylogenetically controlled analysis showed that the decrease of body size with increasing latitude is not a result of repeated and independent evolution of an association between body size and latitude in many clades. There is no significant correlation between body size of land snail species and altitude in the Alps although a negative correlation of body size and altitude is frequent within species. Main conclusion If phylogenetic effects are controlled for, neither latitudinal nor altitudinal patterns in body size could be found. Bergmann's rule, which predicts a positive correlation between body size of species and latitude, could not be confirmed for north‐west European land snails.     

Latitudinal shifts in body size of Enallagma cyathigerum (Odonata)

Aim Survey of the latitudinal body size pattern for populations of Enallagma cyathigerum (Odonata) across a south‐north transect. Location A transect covering the whole distribution range from south to north across Europe was sampled. Methods Newly emerged adults were collected from five major sites across Europe and one to four localities were sampled within each site. In total 253 adults were collected from fourteen localities. Body size was measured using thorax length, length of right front wing and length of right hind tibia. These body size estimates were thereafter related to latitude and mean temperature in January and July. Results Body size showed a U‐shaped pattern with latitude, being large at low and high latitudes and small at intermediate latitudes. The same U‐shaped pattern was found for mean January and July temperature, with large animals at low and high temperatures. Conclusion The U‐shaped relationship between body size and latitude is suggested to be a combination of two effects: (1) the length of the season favourable for growth and development, and (2) variation in life cycle length with latitude.     

Geographical variation in size of an Australian honeyeater (Aves: Meliphagidae): an example of Bergmann's rule

The singing honeyeater, a nectar-feeding bird, is common throughout most of Australia. There is considerable geographical variation in weight, the heaviest birds (30 g) living at the highest latitudes (35°S) and the lightest birds (19 g) at the lowest latitudes (16°S). Clinal variation in weight is apparently related to climatic factors (e.g. potential evapotranspiration) in accord with Bergmann's rule. The exceptions are populations on islands and peninsulas which are about 13% heavier than those on the adjacent mainland.     

What determines conformity to Bergmann's rule?

Aim  Bergmann's rule, the tendency of body size within species in bird and mammal populations to be positively correlated with latitude, is among the best known biogeographical generalizations. The factors behind such clines, however, are not well understood. Here we use a large data base of 79 mammalian carnivore species to examine the factors affecting latitudinal size clines.
Location  Worldwide.
Methods  We measured the skulls and teeth of carnivores in natural history museums, and calculated the amount of variation in size explained by latitude, supplementing our measurements with published data. We examined the effects of a number of variables on the tendency to show latitudinal clines.
Results  We found that geographical range and latitudinal extent are strongly related to size clines. Minimum temperatures across the range, net primary productivity and habitat diversity also have some, albeit much less, influence.
Main conclusions  We suggest that species with large geographical ranges are likely to encounter significant heterogeneity in those factors that influence body size, and are thus likely to exhibit size clines. However, the key factors that determine body size may not always operate along a latitudinal (or other geographical) cline, but be spatially linked to patches in the species range. One such important factor is likely to be food availability, which we show is a strong predictor of size in the brown bear ( Ursus arctos ) but is not associated with a latitudinal cline. We argue that the spatial distribution of key resources within the species range constitutes a significant predictor of carnivore body size.     

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.     

Energy and interspecific body size patterns of amphibian faunas in Europe and North America: anurans follow Bergmann's rule, urodeles its converse

Aim To describe broad‐scale geographical patterns of body size for European and North American amphibian faunas and to explore possible processes underlying these patterns. Specifically, we propose a heat balance hypothesis, as both heat conservation and heat gain determine the heat balance of ectotherms, and test it along with five other hypotheses that have a possible influence on body size gradients: size dependence, migration ability, primary productivity, seasonality and water availability. Location Western Europe and North America north of Mexico. Methods We processed distribution maps for native amphibian species to estimate the mean body size in 110 × 110 km cells and calculated eight environmental predictors to explore the relationship between environmental gradients and the observed patterns. We used least squares regression modelling and model selection approaches based on information theory to evaluate the relative support for each hypothesis. Results We found consistent body size gradients and similar relationships to environmental variables within each amphibian group in Europe and North America. Annual potential evapotranspiration, a measure of environmental energy, was the strongest predictor of mean body size in both regions. However, the contrasting responses to ambient energy in each group resulted in opposite geographical patterns, i.e. anurans increased in size from high‐ to low‐energy areas in both continents and urodeles showed the opposite pattern. Main conclusions Our results support the heat balance hypothesis, suggesting that the thermoregulatory abilities of anurans would allow them to reach larger sizes in colder climates by optimizing the trade‐off between heating and cooling rates, whereas a lack of such strategies among urodele faunas would explain why these organisms tend to be smaller in cooler areas. These findings may also have implications for the role of climate warming on the global decline of amphibians.     

Ecotypic variation in the context of global climate change: revisiting the rules

Patterns of ecotypic variation constitute some of the few 'rules' known to modern biology. Here, we examine several well-known ecogeographical rules, especially those pertaining to body size in contemporary, historical and fossil taxa. We review the evidence showing that rules of geographical variation in response to variation in the local environment can also apply to morphological changes through time in response to climate change. These rules hold at various time scales, ranging from contemporary to geological time scales. Patterns of body size variation in response to climate change at the individual species level may also be detected at the community level. The patterns underlying ecotypic variation are complex and highly context-dependent, reducing the 'predictive-power' of ecogeographical rules. This is especially true when considering the increasing impact of human activities on the environment. Nonetheless, ecogeographical rules may help interpret the likely influences of anthropogenic climate change on ecosystems. Global climate change has already influenced the body size of several contemporary species, and will likely have an even greater impact on animal communities in the future. For this reason, we highlight and emphasise the importance of museum specimens and the continued need for documenting the earth's biological diversity.     

Bergmann's rule in shrews: geographical variation of body size in Palearctic Sorex species

According to Bergmann's rule, individuals of a given species tend to be larger in colder (northern) climates. Traditional explanation points to the relatively lower surface‐to‐volume ratio in larger animals and, consequently, relatively lower costs of thermoregulation. We examined intraspecific covariation of body size with geographical location and climate in five species of Sorex shrews, animals that are among the smallest extant mammals. The condylobasal length of skull (CBL), compiled from literature data and measured on museum specimens, was used as an indicator of the overall body size of shrews. Surprisingly, in three out of five shrew species, the CBL was negatively correlated with latitude, and the same trend, although not statistically significant, was found in the fourth species. In general, shrews were smaller in colder areas, as evidenced by the positive correlations between the CBL and temperature. In two species, these positive correlations appeared when the effect of longitude was held constant in the partial correlation analysis. Characteristically, the strongest negative correlation with latitude and positive with temperatures was found in S. minutus, the smallest species under study. Shrews were in general larger in environments with high actual evapotranspiration. Body mass reviewed in S. araneus paralleled the pattern found in the CBL variation in this species, i.e. it decreased northward, both in summer‐ and winter‐caught animals. In addition, contrary to the widely accepted ? but not rigorously tested ? belief, body mass recession from summer to winter (the Dehnel Effect) did not correlate with latitude. We concluded that shrews followed the converse to Bergmann's rule, and hypothesize that part of their body size variation along the west‐east axis may be explained by character displacement. We also hypothesize that scarcity of food, especially in winter, is a major factor selecting for small body size in shrews in northern areas, as smaller individuals should require less food. © 2003 The Linnean Society of London, Biological Journal of the Linnean Society, 2003, 78 , 365–381.     

Bergmann's rule in larval ant lions: testing the starvation resistance hypothesis

Abstract.  1. Body size of the ant lion Myrmeleon immaculatus follows Bergmann's rule – an increase in body size towards higher latitudes. The hypothesis that ant lion body size is larger in the north as an adaptation for starvation resistance was tested.
2. In a laboratory experiment testing starvation resistance, survivorship curves differed among 10 ant lion populations for both a starved and a fed treatment.
3. The average number of months survived by each population was correlated positively with latitude for both treatments. Across both treatments and all populations, large individuals survived longer than small individuals; however individuals from high latitudes had higher survivorship, even after factoring out variation due to initial body size.
4. These results suggest that starvation resistance may be an adaptation for coping with reduced prey availability in high latitudes. Starvation resistance may contribute to latitudinal gradients in body size of ant lions and other ectotherms.