Climatological correlates for body size of five species of Australian mammals

Size variation of body and skull of five species of Australian mammals (echidna, Tachyglossus aculeatus ; brush-tail possum, Trichosurus vulpecula ; eastern grey kangaroo, Macropus giganteus ; western grey kangaroo, M. fuliginosus ; red kangaroo, M. rufus ), is related to climatic factors. All five species show trends in body size that conform with Bergmann's rule, individuals from colder environments being larger than those from warmer areas. The western and eastern grey kangaroos also conform with Allen's rule, the relative size of their extremities being large in warmer areas. In four of the five species (not the red kangaroo) body size is also correlated with indices of biomass productivity. However, since biomass productivity and ambient temperature are related to some extent, it is difficult to separate the effects of these factors.     

The island rule and a research agenda for studying ecogeographical patterns

We are currently experiencing a resurgence of interest in ecogeographical rules, which describe general trends in morphology and related traits along geographical gradients. In order to develop a more comprehensive understanding of the generality and underlying causal mechanisms for these patterns, we recommend a new, more integrated research agenda. In particular, we recommend studies that simultaneously consider different clines in morphology, geographical ranges and diversity as intricately related phenomena; all being ecological, evolutionary and biogeographical responses of organisms to selection regimes that vary non-randomly over space and time, and among species with different ecological and evolutionary histories.     

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.     

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

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

The geography of body size – challenges of the interspecific approach

Recent compilations of large-scale data bases on the geographical distributions and body sizes of animals, coupled with developments in spatial statistics, have led to renewed interest in the geographical distribution of animal body sizes and the interspecific version of Bergmann's rule. Standard practice seems to be an examination of mean body sizes within higher taxa on gridded maps, with little regard to species richness or phylogeny. However, because the frequency distribution of body sizes is typically highly skewed, average size within grid cells may differ significantly between species-rich and species-poor cells even when the median and modal sizes remain constant. Species richness influences body size patterns because species are not added to communities at random in relation to their size: areas of low diversity are characterized by a higher range of body sizes than is expected by chance. Finally, a consideration of phylogenetic structure within taxa is necessary to elucidate whether patterns in the geography of size result from turnover between or within intermediate taxonomic levels. We suggest that the highest and lowest quantiles of body size distribution be mapped in order to expose possible physiological or ecological limitations on body size.     

Phylogenetic analyses of primate size evolution: the consequences of sexual selection

We have analysed the relationship between primate mating system, size and size dimorphism by utilizing several phylogenetically based methods. An independent contrast analysis of male and female size (log weight) showed that these are tightly correlated and that size dimorphism is not a simple allometric function of size. We found no relationship between mating system and sexual dimorphism in strepsirhines but a strong relationship in haplorhines. By matched-pairs analysis, where sister groups were matched according to whether the mating system predicted higher or lower intrasexual selection for male size, haplorhine species in more polygynous clades (with a predicted higher sexual selection) were significantly more dimorphic, had larger males, and also, but to a lesser degree, larger females. Both independent contrast and matched-pairs analyses are non-directional and correlational. By using a directional test we investigated how a transition in mating system affects size and dimorphism. Here, each observation is the sum of changes in dimorphism or size in a clade that is defined by a common origin of a mating system. Generally, dimorphism, as well as male and female size, increased after an expected increase in sexual selection, and decreased after an expected decrease in sexual selection. The pattern was, however, not significant for all of the alternative character reconstructions. In clades with an expected increase in sexual selection, male size increased more than female size. This pattern was significant for all character reconstructions. The directional investigation indicates that the magnitude of change in haplorhine dimorphism is larger after an increase in sexual selection than after a decrease, and, for some reconstructions, that the magnitude of size increase is larger than the magnitude of size decrease for both sexes. Possible reasons for these patterns are discussed, as well as their implications as being one possible mechanism behind Cope's rule, i.e. general size increase in many phylogenetic lineages.     

Body size variation in insects: a macroecological perspective

Body size is a key feature of organisms and varies continuously because of the effects of natural selection on the size-dependency of resource acquisition and mortality rates. This review provides a critical and synthetic overview of body size variation in insects from a predominantly macroecological (large-scale temporal and spatial) perspective. Because of the importance of understanding the proximate determinants of adult size, it commences with a brief summary of the physiological mechanisms underlying adult body size and its variation, based mostly on findings for the model species Drosophila melanogaster and Manduca sexta . Variation in nutrition and temperature have variable effects on critical weight, the interval to cessation of growth (or terminal growth period) and growth rates, so influencing final adult size. Ontogenetic and phylogenetic variation in size, compensatory growth, scaling at the intra- and interspecific levels, sexual size dimorphism, and body size optimisation are then reviewed in light of their influences on individual and species body size frequency distributions. Explicit attention is given to evolutionary trends, including gigantism, Cope's rule and the rates at which size change has taken place, and to temporal ecological trends such as variation in size with succession and size-selectivity during the invasion process. Large-scale spatial variation in size at the intraspecific, interspecific and assemblage levels is considered, with special attention being given to the mechanisms proposed to underlie clinal variation in adult body size. Finally, areas particularly in need of additional research are identified.     

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.     

The geographic distribution of mammal body size in Europe

Aims  To describe the pattern of mean body size of native mammals in Europe, and to investigate its relationships with environmental predictors related to four hypotheses: (1) dispersal; (2) heat conservation; (3) heat dissipation; and (4) resource availability.
Location  Continental western Europe and Great Britain.
Methods  We used range maps to estimate the mean body size (average log mass) of mammals in 386 cells of 12,100 km² each. Environmental conditions in each cell were quantified using nine historical, climatic and primary production variables. We attempted to tease apart the effects of these variables using correlation, multiple regression and spatial autocorrelation analyses.
Results  In the part of the continent covered by ice during the Pleistocene, body mass decreases southwards, and annual average temperature explains 73% of the variance in body size, consistent with the heat-conservation hypothesis. However, in warmer, non-glaciated areas the best predictor is an estimate of seasonality in plant production, but it explains only 18% of the variance. Carnivores, omnivores and herbivores show similar relationships, but the pattern for herbivores is substantially weaker than for the other groups.
Main conclusions  Overall, the relationship between mean body size and temperature is non-linear, being strong in cold environments but virtually disappearing above a temperature threshold.     

Body size evolution in insular vertebrates: generality of the island rule

Aim My goals here are to (1) assess the generality of the island rule – the graded trend from gigantism in small species to dwarfism in larger species – for mammals and other terrestrial vertebrates on islands and island‐like ecosystems; (2) explore some related patterns of body size variation in insular vertebrates, in particular variation in body size as a function of island area and isolation; (3) offer causal explanations for these patterns; and (4) identify promising areas for future studies on body size evolution in insular vertebrates. Location Oceanic and near‐shore archipelagos, and island‐like ecosystems world‐wide. Methods Body size measurements of insular vertebrates (non‐volant mammals, bats, birds, snakes and turtles) were obtained from the literature, and then regression analyses were conducted to test whether body size of insular populations varies as a function of body size of the species on the mainland (the island rule) and with characteristics of the islands (i.e. island isolation and area). Results The island rule appears to be a general phenomenon both with mammalian orders (and to some degree within families and particular subfamilies) as well as across the species groups studied, including non‐volant mammals, bats, passerine birds, snakes and turtles. In addition, body size of numerous species in these classes of vertebrates varies significantly with island isolation and island area. Main conclusions The patterns observed here – the island rule and the tendency for body size among populations of particular species to vary with characteristics of the islands – are actually distinct and scale‐dependent phenomena. Patterns within archipelagos reflect the influence of island isolation and area on selective pressures (immigration filters, resource limitation, and intra‐ and interspecific interactions) within particular species. These patterns contribute to variation about the general trend referred to as the island rule, not the signal for that more general, large‐scale pattern. The island rule itself is an emergent pattern resulting from a combination of selective forces whose importance and influence on insular populations vary in a predictable manner along a gradient from relatively small to large species. As a result, body size of insular species tends to converge on a size that is optimal, or fundamental, for a particular bau plan and ecological strategy.     

The generality of the island rule reexamined

Aim  M.V. Lomolino and colleagues have recently reviewed the island rule in mammals and other vertebrates, claiming it is a general pattern. They have portrayed our recent analysis as weakly supporting the island rule, seeing weakness in our use of what they considered to be inadequate size indices (skulls and teeth, rather than mass or body length) and in our use of large islands. They argue that size evolution on islands points to a bauplan-specific fundamental size. We aim to test the generality of the rule and the adequacy of some of the data used to support it.
Location  Insular environments world-wide.
Methods  We collate and analyse data on skull sizes of carnivores and body masses of mammals in general to see whether there is a graded trend from dwarfism in large species to gigantism in smaller ones.
Results  The island rule is not supported with either the carnivore or the mammal data sets. Island area does not influence size change.
Main conclusions  Our results suggest that data recently advanced in support of the island rule are inadequate and that the island rule is not a general pattern for all mammals.     

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.     

Mainland size variation informs predictive models of exceptional insular body size change in rodents

The tendency for island populations of mammalian taxa to diverge in body size from their mainland counterparts consistently in particular directions is both impressive for its regularity and, especially among rodents, troublesome for its exceptions. However, previous studies have largely ignored mainland body size variation, treating size differences of any magnitude as equally noteworthy. Here, we use distributions of mainland population body sizes to identify island populations as ‘extremely’ big or small, and we compare traits of extreme populations and their islands with those of island populations more typical in body size. We find that although insular rodents vary in the directions of body size change, ‘extreme’ populations tend towards gigantism. With classification tree methods, we develop a predictive model, which points to resource limitations as major drivers in the few cases of insular dwarfism. Highly successful in classifying our dataset, our model also successfully predicts change in untested cases.     

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.     

Patterns of diversity, altitudinal range and body size among freshwater fishes in the Yangtze River basin, China

Aim To document patterns in diversity, altitudinal range and body size of freshwater fishes along an elevational gradient in the Yangtze River basin. Location The Yangtze River basin, China. Methods We used published data to compile the distribution, altitudinal range and body size of freshwater fishes. Correlation, regression, clustering and graphical analyses were used to explore patterns in diversity, altitudinal range and body size of freshwater fishes in 100‐m elevation zones from 0 to 5200 m. Results Species richness patterns across the elevational gradient for total, non‐endemic and endemic fishes were different. The ratio of endemics to total richness peaked at mid elevation. Land area on a 500‐m interval scale explained a significant amount of the variation in species richness. Species density displayed two peaks at mid‐elevation zones. The cluster analysis revealed five distinct assemblages across the elevation gradient. The relationship between elevational range size and the midpoint of the elevational range revealed a triangular distribution. The frequency distribution of log maximum standard length data displayed an atypical right‐skewed pattern. Intermediate body sizes occurred across the greatest range of elevation while small and large body sizes possessed only small elevational amplitudes. The size‐elevation relationship between the two major families revealed a very strong pattern of body size constraint among the Cobitidae with no corresponding elevational constraint and a lot of body size and elevational diversification among the Cyprinidae. Main conclusion The data failed to support either Rapoport's rule or Bergmann's rule.     

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.     

Climate change and size evolution in an island rodent species: new perspectives on the island rule

As stated by the island rule, small mammals evolve toward gigantism on islands. In addition they are known to evolve faster than their mainland counterparts. Body size in island mammals may also be influenced by geographical climatic gradients or climatic change through time. We tested the relative effects of climate change and isolation on the size of the Japanese rodent Apodemus speciosus and calculated evolutionary rates of body size change since the last glacial maximum (LGM). Currently A. speciosus populations conform both to Bergmann's rule, with an increase in body size with latitude, and to the island rule, with larger body sizes on small islands. We also found that fossil representatives of A. speciosus are larger than their extant relatives. Our estimated evolutionary rates since the LGM show that body size evolution on the smaller islands has been less than half as rapid as on Honshu, the mainland-type large island of Japan. We conclude that island populations exhibit larger body sizes today not because they have evolved toward gigantism, but because their evolution toward a smaller size, due to climate warming since the LGM, has been decelerated by the island effect. These combined results suggest that evolution in Quaternary island small mammals may not have been as fast as expected by the island effect because of the counteracting effect of climate change during this period.