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.     

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.     

Coloration affects heating and cooling in three color morphs of the Australian bluetongue lizard,Tiliqua scincoides

The color-mediated thermoregulation hypothesis predicts that dark body color (low reflectance) allows organisms to gain heat more efficiently than does pale coloration (high reflectance). This prediction is intuitive and widely assumed to be true, but has poor empirical support. We used rare, captive-bred, mutant melanistic, albino and wild-type Australian bluetongue lizards, Tiliqua scincoides to measure the effects of skin reflectance on the heating and cooling rates. We measured heating under an artificial radiant heat source and cooling rates in an ice-cooled box using live lizards in a room with still air. The effect of skin reflectance on heat transfer was clear, despite the substantial influence of body size. Melanistic T. scincoides showed low reflectance and gained heat faster than highly reflective albinos. Melanistic lizards also lost heat faster than albinos. Wild-type lizards were intermediate in reflectance, gained heat at rates indistinguishable from melanistic lizards, and lost heat at rates indistinguishable from albino lizards. This study system allowed us to control for variables that were confounded in other studies and may explain the inconsistent support for the color-mediated thermoregulation hypothesis. Our results provide clear evidence that skin reflectance influences the rate of heating and cooling in ectotherms.     

The evolution of mammal body sizes: responses to Cenozoic climate change in North American mammals

Explanations for the evolution of body size in mammals have remained surprisingly elusive despite the central importance of body size in evolutionary biology. Here, we present a model which argues that the body sizes of Nearctic mammals were moulded by Cenozoic climate and vegetation changes. Following the early Eocene Climate Optimum, forests retreated and gave way to open woodland and savannah landscapes, followed later by grasslands. Many herbivores that radiated in these new landscapes underwent a switch from browsing to grazing associated with increased unguligrade cursoriality and body size, the latter driven by the energetics and constraints of cellulose digestion (fermentation). Carnivores also increased in size and digitigrade, cursorial capacity to occupy a size distribution allowing the capture of prey of the widest range of body sizes. With the emergence of larger, faster carnivores, plantigrade mammals were constrained from evolving to large body sizes and most remained smaller than 1 kg throughout the middle Cenozoic. We find no consistent support for either Cope's Rule or Bergmann's Rule in plantigrade mammals, the largest locomotor guild (n = 1186, 59% of species in the database). Some cold‐specialist plantigrade mammals, such as beavers and marmots, showed dramatic increases in body mass following the Miocene Climate Optimum which may, however, be partially explained by Bergmann's rule. This study reemphasizes the necessity of considering the evolutionary history and resultant form and function of mammalian morphotypes when attempting to understand contemporary mammalian body size distributions.     

Age and annual growth rate cause spatial variation in body size in Phrynocephalus przewalskii (Agamid)

Whether or not biogeographic rules dealing with spatial patterns of animal body sizes are valid for ectotherms is controversial. As the ectotherms grow all their lives, we explored the role of age and annual growth rate in body size variation in Phrynocephalus przewalskii in northern China. Morphological data were collected from 11 populations across a broad geographic gradient. Correlations between age, sex, climatic factors, and body size were analyzed using generalized linear model (GLM) and generalized linear mixed model (GLMM). GLM analysis indicated that the general body size of both sexes and the appendage size of females increased significantly with increasing temperature; however, the coefficient of determination was very small. GLMM analysis indicated that body size only correlated with age, whereas appendage size was affected by age, temperature, rainfall, and sunshine. Annual growth rates were positively correlated with temperature. We concluded that body size variation was mainly caused by age structure and plasticity of the growth rate in P. przewalskii and did not follow Bergmann''s rule; however, females followed Allen''s rule. Future studies to investigate the effect of energy restriction are needed to further understand the relationship between growth rate and body size. We also suggest that further studies on thermal advantage and sexual selection may be helpful to understand appendage size variation in P. przewalskii.     

Migratory shorebird adheres to Bergmann's Rule by responding to environmental conditions through the annual lifecycle

The inverse relationship between body size and environmental temperature is a widespread ecogeographic pattern. However, the underlying forces that produce this pattern are unclear in many taxa. Expectations are particularly unclear for migratory species, as individuals may escape environmental extremes and reorient themselves along the environmental gradient. In addition, some aspects of body size are largely fixed while others are environmentally flexible and may vary seasonally. Here, we used a long‐term dataset that tracked multiple populations of the migratory piping plover Charadrius melodus across their breeding and non‐breeding ranges to investigate ecogeographic patterns of phenotypically flexible (body mass) and fixed (wing length) size traits in relation to latitude (Bergmann's Rule), environmental temperature (heat conservation hypothesis), and migratory distance. We found that body mass was correlated with both latitude and temperature across the breeding and non‐breeding ranges, which is consistent with predictions of Bergmann's Rule and heat conservation. However, wing length was correlated with latitude and temperature only on the breeding range. This discrepancy resulted from low migratory connectivity across seasons and the tendency for individuals with longer wings to migrate farther than those with shorter wings. Ultimately, these results suggest that wing length may be driven more by conditions experienced during the breeding season or tradeoffs related to migration, whereas body mass is modified by environmental conditions experienced throughout the annual lifecycle.     

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.     

Latitudinal variation in sexual dimorphism in life‐history traits of a freshwater fish

Sexual dimorphism is common across the animal kingdom, but the contribution of environmental factors shaping differences between the sexes remains controversial. In ectotherms, life‐history traits are known to correlate with latitude, but sex‐specific responses are not well understood. We analyzed life‐history trait variation between the sexes of European perch (Perca fluviatilis L.), a common freshwater fish displaying larger female size, by employing a wide latitudinal gradient. We expected to find sex‐dependent latitudinal variation in life‐history variables: length at age, length increment, and size at maturity, with females showing consistently higher values than males at all latitudes. We further anticipated that this gender difference would progressively decrease with the increasingly harsh environmental conditions toward higher latitude. We hypothesized that growth and length increment would decrease and size/age at maturity would increase at higher latitudes. Our results confirmed female‐biased sexual size dimorphism at all latitudes and the magnitude of sexual dimorphism diminished with increase in latitude. Growth of both sexes decreased with increase in latitude, and the female latitudinal clines were steeper than those of males. Hence, we challenge two predominant ecological rules (Rensch's and Bergmann's rules) that describe common large‐scale patterns of body size variation. Our data demonstrate that these two rules are not universally applicable in ectotherms or female‐biased species. Our study highlights the importance of sex‐specific differences in life‐history traits along a latitudinal gradient, with evident implications for a wide range of studies from individual to ecosystems level.     

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.     

Proximate causes of altitudinal differences in body size in an agamid lizard

Body size is directly linked to key life history traits such as growth, fecundity, and survivorship. Identifying the causes of body size variation is a critical task in ecological and evolutionary research. Body size variation along altitudinal gradients has received considerable attention; however, the underlying mechanisms are poorly understood. Here, we compared the growth rate and age structure of toad‐headed lizards (Phrynocephalus vlangalii) from two populations found at different elevations in the Qinghai‐Tibetan Plateau. We used mark‐recapture and skeletochronological analysis to identify the potential proximate causes of altitudinal variation in body size. Lizards from the high‐elevation site had higher growth rates and attained slightly larger adult body sizes than lizards from the low‐elevation site. However, newborns produced by high‐elevation females were smaller than those by low‐elevation females. Von Bertalanffy growth estimates predicted high‐elevation individuals would reach sexual maturity at an earlier age and have a lower mean age than low‐elevation individuals. Relatively lower mean age for the high‐elevation population was confirmed using the skeletochronological analysis. These results support the prediction that a larger adult body size of high‐elevation P. vlangalii results from higher growth rates, associated with higher resource availability.     

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.     

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.     

Global patterns of body size evolution are driven by precipitation in legless amphibians

Body size shapes ecological interactions across and within species, ultimately influencing the evolution of large‐scale biodiversity patterns. Therefore, macroecological studies of body size provide a link between spatial variation in selection regimes and the evolution of animal assemblages through space. Multiple hypotheses have been formulated to explain the evolution of spatial gradients of animal body size, predominantly driven by thermal (Bergmann's rule), humidity (‘water conservation hypothesis’) and resource constraints (‘resource rule’, ‘seasonality rule’) on physiological homeostasis. However, while integrative tests of all four hypotheses combined are needed, the focus of such empirical efforts needs to move beyond the traditional endotherm–ectotherm dichotomy, to instead interrogate the role that variation in lifestyles within major lineages (e.g. classes) play in creating neglected scenarios of selection via analyses of largely overlooked environment–body size interactions. Here, we test all four rules above using a global database spanning 99% of modern species of an entire Order of legless, predominantly underground‐dwelling amphibians (Gymnophiona, or caecilians). We found a consistent effect of increasing precipitation (and resource abundance) on body size reductions (supporting the water conservation hypothesis), while Bergmann's, the seasonality and resource rules are rejected. We argue that subterranean lifestyles minimize the effects of aboveground selection agents, making humidity a dominant selection pressure – aridity promotes larger body sizes that reduce risk of evaporative dehydration, while smaller sizes occur in wetter environments where dehydration constraints are relaxed. We discuss the links between these principles with the physiological constraints that may have influenced the tropically‐restricted global radiation of caecilians.     

Spatial patterns in the size of Chinese lizards are driven by multiple factors

BackgroundFor almost two centuries, ecologists have examined geographical patterns in the evolution of body size and the associated determinants. During that time, one of the most common patterns to have emerged is the increase in body size with increasing latitude (referred to as Bergmann''s rule). Typically, this pattern is explained in terms of an evolutionary response that serves to minimize heat loss in colder climates, mostly in endotherms. In contrast, however, this rule rarely explains geographical patterns in the evolution of body size among ectotherms (e.g., reptiles).LocationChina.AimIn this study, we assembled a dataset comprising the maximum sizes of 211 lizard species in China and examined the geographical patterns in body size evolution and its determinants. Specifically, we assessed the relationship between body size and climate among all lizard species and within four major groups at both assemblage and interspecific levels.ResultsAlthough we found that the body size of Chinese lizards was larger in warmer regions, we established that at the assemblage level, size was correlated with multiple climatic factors, and that body size–climate correlations differed within the four major groups. Phylogenetic analysis at the species level revealed that no single climatic factor was associated with body size, with the exception of agamids, for which size was found to be positively correlated with temperature.Main conclusionsGeographical patterns in Chinese lizard body size are driven by multiple factors, and overall patterns are probably influenced by those of the major groups. We suggest that our analyses at two different levels may have contributed to the inconsistent results obtained in this study. Further studies investigating the effects of altitude and ecological factors are needed to gain a more comprehensive understanding of the evolution of ectotherm body size.     

The Impact of Phenotypic Characteristics on Thermoregulation in a Cold-Climate Agamid lizard,Phrynocephalus guinanensis

Physiological and metabolic processes of ectotherms are markedly influenced by ambient temperature. Previous studies have shown that the abdominal black-speckled area becomes larger with increased elevation in plateau Phrynocephalus, however, no studies have verified the hypothesis that this variation is correlated with the lizard's thermoregulation. In this study, infrared thermal imaging technology was first used to study the skin temperature variation of torsos, heads, limbs and tails of a cold-climate agamid lizard, Phrynocephalus guinanensis. The heating rates of the central abdominal black-speckled skin area and peripheral non-black-speckled skin area under solar radiation were compared. Our results showed that the heating rates of limbs and tails were relatively faster than the torsos, as heating time was extended, rates gradually slowed before stabilizing under solar radiation. Under the environment without solar radiation, the cooling rates of limbs and tails were also relatively faster than the torsos of lizards, the rates slowed down and finally became stable as the cooling time was extended. We also found that the heating rate of the abdominal black-speckled skin area was faster than the nearby non-black-speckled skin area. These results increased our insights into the functional significance of these phenotypic traits and help explain their covariation with the thermal environment in these cold-climate agamid lizards.     

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.     

Gross mismatch between thermal tolerances and environmental temperatures in a tropical freshwater snail: Climate warming and evolutionary implications

The relationship between acute thermal tolerance and habitat temperature in ectotherm animals informs about their thermal adaptation and is used to assess thermal safety margins and sensitivity to climate warming. We studied this relationship in an equatorial freshwater snail (Clea nigricans), belonging to a predominantly marine gastropod lineage (Neogastropoda, Buccinidae). We found that tolerance of heating and cooling exceeded average daily maximum and minimum temperatures, by roughly 20 °C in each case. Because habitat temperature is generally assumed to be the main selective factor acting on the fundamental thermal niche, the discordance between thermal tolerance and environmental temperature implies trait conservation following ‘in situ’ environmental change, or following novel colonisation of a thermally less-variable habitat. Whereas heat tolerance could relate to an historical association with the thermally variable and extreme marine intertidal fringe zone, cold tolerance could associate with either an ancestral life at higher latitudes, or represent adaptation to cooler, higher-altitudinal, tropical lotic systems. The broad upper thermal safety margin (difference between heat tolerance and maximum environmental temperature) observed in this snail is grossly incompatible with the very narrow safety margins typically found in most terrestrial tropical ectotherms (insects and lizards), and hence with the emerging prediction that tropical ectotherms, are especially vulnerable to environmental warming. A more comprehensive understanding of climatic vulnerability of animal ectotherms thus requires greater consideration of taxonomic diversity, ecological transition and evolutionary history.     

Evaluating thermoregulation in reptiles: an appropriate null model

Established indexes of thermoregulation in ectotherms compare body temperatures of real animals with a null distribution of operative temperatures from a physical or mathematical model with the same size, shape, and color as the actual animal but without mass. These indexes, however, do not account for thermal inertia or the effects of inertia when animals move through thermally heterogeneous environments. Some recent models have incorporated body mass, to account for thermal inertia and the physiological control of warming and cooling rates seen in most reptiles, and other models have incorporated movement through the environment, but none includes all pertinent variables explaining body temperature. We present a new technique for calculating the distribution of body temperatures available to ectotherms that have thermal inertia, random movements, and different rates of warming and cooling. The approach uses a biophysical model of heat exchange in ectotherms and a model of random interaction with thermal environments over the course of a day to create a null distribution of body temperatures that can be used with conventional thermoregulation indexes. This new technique provides an unbiased method for evaluating thermoregulation in large ectotherms that store heat while moving through complex environments, but it can also generate null models for ectotherms of all sizes.