Climate history,human impacts and global body size of Carnivora (Mammalia: Eutheria) at multiple evolutionary scales

Aim One of the longest recognized patterns in macroecology, Bergmann’s rule, describes the tendency for homeothermic animals to have larger body sizes in cooler climates than their phylogenetic relatives in warmer climates. Here we provide an integrative process‐based explanation for Bergmann’s rule at the global scale for the mammal order Carnivora. Location Global. Methods Our database comprises the body sizes of 209 species of extant terrestrial Carnivora, which were analysed using phylogenetic autocorrelation and phylogenetic eigenvector regression. The interspecific variation in body size was partitioned into phylogenetic (P) and specific (S) components, and mean P‐ and S‐components across species were correlated with environmental variables and human occupation both globally and for regions glaciated or not during the last Ice Age. Results Three‐quarters of the variation in body size can be explained by phylogenetic relationships among species, and the geographical pattern of mean values of the P‐component is the opposite of the pattern predicted by Bergmann’s rule. Partial regression revealed that at least 43% of global variation in the mean phylogenetic component is explained by current environmental factors. In contrast, the mean S‐component of body size shows large positive deviations from ancestors across the Holarctic, and negative deviations in southern South America, the Sahara Desert, and tropical Asia. There is a moderately strong relationship between the human footprint and body size in glaciated regions, explaining 19% of the variance of the mean P‐component. The relationship with the human footprint and the P‐component is much weaker in the rest of the world, and there is no relationship between human footprint and S‐component in any region. Main conclusions Bergmannian clines are stronger at higher latitudes in the Northern Hemisphere because of the continuous alternation of glacial–interglacial cycles throughout the late Pliocene and Pleistocene, which generated increased species turnover, differential colonization and more intense adaptive processes soon after glaciated areas became exposed. Our analyses provide a unified explanation for an adaptive Bergmann’s rule within species and for an interspecific trend towards larger body sizes in assemblages resulting from historical changes in climate and contemporary human impacts.     

Patterns in body size and melanism along a latitudinal cline in the wingless grasshopper,Phaulacridium vittatum

Aim We explore geographic variation in body size within the wingless grasshopper, Phaulacridium vittatum, along a latitudinal gradient, and ask whether melanism can help explain the existence of clinal variation. We test the hypotheses that both male and female grasshoppers will be larger and lighter in colour at lower latitudes, and that reflectance and size will be positively correlated, as predicted by biophysical theory. We then test the hypothesis that variability in size and reflectance is thermally driven, by assessing correlations with temperature and other climatic variables. Location Sixty‐one populations were sampled along the east coast of Australia between latitudes 27.63° S and 43.10° S, at elevations ranging from 10 to 2000 m a.s.l. Methods Average reflectance was used as a measure of melanism and femur length as an index of body size for 198 adult grasshoppers. Climate variables were generated by BIOCLIM for each collection locality. Hierarchical partitioning was used to identify those variables with the most independent influence on grasshopper size and reflectance. Results Overall, there was no simple relationship between size and latitude in P. vittatum. Female body size decreased significantly with latitude, while male body size was largest at intermediate latitudes. Rainfall was the most important climatic variable associated with body size of both males and females. Female body size was also associated with radiation seasonality and male body size with reflectance. The reflectance of females was not correlated with latitude or body size, while male reflectance was significantly higher at intermediate latitudes and positively correlated with body size. Analyses of climate variables showed no significant association with male reflectance, while female reflectance was significantly related to the mean temperature of the driest quarter. Main conclusions Geographic variation in the body size of the wingless grasshopper is best explained in terms of rainfall and radiation seasonality, rather than temperature. However, melanism is also a significant influence on body size in male grasshoppers, suggesting that thermal fitness does play a role in determining adaptive responses to local conditions in this sex.     

Decadal heat and drought drive body size of North American bison (Bison bison) along the Great Plains

Large grazers are visible and valuable indicators of the effects of projected changes in temperature and drought on grasslands. The grasslands of the Great Plains have supported the greatest number of bison (Bison bison; Linnaeus, 1758) since prehistoric times. We tested the hypothesis that body mass (BM, kg) and asymptotic body mass (ABM, kg) of Bison decline with rising temperature and increasing drought over both temporal and spatial scales along the Great Plains. Temporally, we modeled the relationship of annual measures of BM and height (H, m) of 5,781 Bison at Wind Cave National Park (WICA) from 1966 to 2015. We used Gompertz equations of BM against age to estimate ABM in decadal cohorts; both females and males decreased from the 1960s to the 2010s. Male ABM was variable but consistently larger (699 vs. 441 kg) than female ABM. We used local mean decadal temperature (MDT) and local mean decadal Palmer Drought Severity Index (dPDSI) to model the effects of climate on ABM. Drought decreased ABM temporally (?16 kg/local dPDSI) at WICA. Spatially, we used photogrammetry to measure body height (H_E) of 773 Bison to estimate BM_E in 19 herds from Saskatchewan to Texas, including WICA. Drought also decreased ABM spatially (?16 kg/local dPDSI) along the Great Plains. Temperature decreased ABM both temporally at WICA (?115 kg/°C local MDT) and spatially (?1 kg/°C local MDT) along the Great Plains. Our data indicate that temperature and drought drive Bison ABM presumably by affecting seasonal mass gain. Bison body size is likely to decline over the next five decades throughout the Great Plains due to projected increases in temperatures and both the frequency and intensity of drought.     

Ambient temperature correlates with geographic variation in body size of least horseshoe bats

Geographic variation in body size is common within many animal species. The causes of this pattern, however, remain largely unexplored in most vertebrate groups. Bats are widely distributed globally owing to their ability of powered flight. Most bat species encounter a variety of climatic conditions across their distribution range, making them an ideal taxon for the study of ecogeographic patterns in body size. Here, we used adult least horseshoe bats, Rhinolophus pusillus, to test whether geographic variation in body size was determined by heat conservation, heat dissipation, climatic seasonality, or primary productivity. We measured body mass and head-body length for 246 adult bats from 12 allopatric colonies in China. We quantified the ecological conditions inhabited by each colony, including mean maximum temperature of the warmest month, mean minimum temperature of the coldest month, temperature seasonality, precipitation seasonality, and annual net primary productivity (ANPP). Body mass and head-body length, 2 of the most reliable indicators of body size, exhibited marked differences between colonies. After controlling for spatial autocorrelation, the mean minimum temperature of the coldest month explained most of the variation in body size among colonies, regardless of sex. The mean maximum temperature, climatic seasonality, and ANPP had limited power in predicting body size of males or females in comparison with mean minimum temperature. These results support the heat conservation hypothesis and suggest adaptive responses of body size to cold climates in cave-dwelling bats.     

Climate‐driven body‐size trends in the ostracod fauna of the deep Indian Ocean

Abstract: Body size is a common focus of macroevolutionary, macroecological and palaeontological investigations. Here, we document body‐size evolution in 19 species‐level ostracod lineages from the deep Indian Ocean (Deep Sea Drilling Program Site 253) over the past 40 myr. Body‐size trajectories vary across taxa and time intervals, but most lineages (16/19) show net gains in body size. Because many modern ostracod taxa are larger in colder parts of their geographical range, we compared the timing and magnitude of these size changes to established Cenozoic deep‐water cooling patterns confirmed through δ¹⁸O measurements of benthic foraminifera in the samples studied. These data show a significant negative correlation between size changes and temperature changes (ostracods get larger as temperatures get colder), and that systematic size increases only occur during intervals of sustained cooling. In addition, statistical support for an explicit temperature‐tracking model exceeds that of purely directional evolution. We argue that this Cope’s Rule pattern is driven by secular changes in the environment, rather than any universal or intrinsic advantages to larger body sizes, and we note some difficulties in the attempts to link Cope’s Rule to observations made within a single generation.     

Ecogeographic variation of body size in the spectacled salamanders (Salamandrina): influence of genetic structure and local factors

Aim The patterns and causes of ecogeographical body size variation in ectotherms remain controversial. In amphibians, recent genetic studies are leading to the discovery of many cryptic species. We analysed the relationships between body size and climate for a salamander (Salamandrina) that was recently separated into two sibling species, to evaluate how ignoring interspecific and intraspecific genetic structure may affect the conclusions of ecogeographical studies. We also considered the potential effects of factors acting at a local scale. Location Thirty‐four populations covering the whole range of Salamandrina, which is endemic to peninsular Italy. Methods We pooled original data and data from the literature to obtain information on the snout–vent length (SVL) of 3850 Salamandrina females; we obtained high‐resolution climatic data from the sampled localities. We used an information‐theoretic approach to evaluate the roles of climate, genetic features (mitochondrial haplogroup identity) and characteristics of aquatic oviposition sites. We repeated our analyses three times: in the first analysis we ignored genetic data on intraspecific and interspecific variation; in the second one we considered the recently discovered differences between the two sibling species; in the third one we included information on intraspecific genetic structure within Salamandrina perspicillata (for Salamandrina terdigitata the sample size was too small to perform intraspecific analyses). Results If genetic information was ignored, our analysis suggested the existence of a relationship between SVL and climatic variables, with populations of large body size in areas with high precipitation and high thermal range. If species identity was included in the analysis, the role of climatic features was much weaker. When intraspecific genetic differences were also considered, no climatic feature had an effect. In all analyses, local factors were important and explained a large proportion of the variation; populations spawning in still water had a larger body size. Main conclusions An imperfect knowledge of species boundaries, or overlooking the intraspecific genetic variation can strongly affect the results of analyses of body size variation. Furthermore, local factors can be more important than the large‐scale parameters traditionally considered, particularly in species with a small range.     

Dynamic size responses to climate change: prevailing effects of rising temperature drive long‐term body size increases in a semi‐arid passerine

Changes in animal body size have been widely reported as a correlate of contemporary climate change. Body size affects metabolism and fitness, so changing size has implications for resilience, yet the climatic factors that drive size variation remain poorly understood. We test the role of mean and extreme temperature, rainfall, and remotely sensed primary productivity (NDVI) as drivers of body size in a sedentary, semi‐arid Australian passerine, Ptilotula (Lichenostomus) penicillatus, over 23 years. To distinguish effects due to differential growth from changes in population composition, we analysed first‐year birds and adults separately and considered climatic variation at three temporal scales (current, previous, and preceding 5 years). The strongest effects related to temperature: in both age classes, larger size was associated with warmer mean temperatures in the previous year, contrary to Bergmann's Rule. Moreover, adults were larger in warmer breeding seasons, while first years was larger after heatwaves; these effects are more likely to be mediated through size‐dependent mortality, highlighting the role of body size in determining vulnerability to extinction. In addition to temperature, larger adult size was associated with lower primary productivity, which may reflect a trade‐off between vegetative growth and nectar production, on which adults rely. Finally, lower rainfall was associated with decreasing size in first year and adults, most likely related to decreased food availability. Overall, body size increased over 23 years, strongly in first‐year birds (2.7%) compared with adults (1%), with size outcomes a balance between competing drivers. As rainfall declined over time and productivity remained fairly stable, the temporal increase in body size appears largely driven by rising mean temperature and temperature extremes. Body size responses to environmental change are thus complex and dynamic, driven by effects on growth as well as mortality.     

Widespread rapid reductions in body size of adult salamanders in response to climate change

Reduction in body size is a major response to climate change, yet evidence in globally imperiled amphibians is lacking. Shifts in average population body size could indicate either plasticity in the growth response to changing climates through changes in allocation and energetics, or through selection for decreased size where energy is limiting. We compared historic and contemporary size measurements in 15 Plethodon species from 102 populations (9450 individuals) and found that six species exhibited significant reductions in body size over 55 years. Biophysical models, accounting for actual changes in moisture and air temperature over that period, showed a 7.1–7.9% increase in metabolic expenditure at three latitudes but showed no change in annual duration of activity. Reduced size was greatest at southern latitudes in regions experiencing the greatest drying and warming. Our results are consistent with a plastic response of body size to climate change through reductions in body size as mediated through increased metabolism. These rapid reductions in body size over the past few decades have significance for the susceptibility of amphibians to environmental change, and relevance for whether adaptation can keep pace with climate change in the future.     

Little effect of climate change on body size of herbivorous beetles

Ongoing climate change affects various aspects of an animal's life, with important effects on distribution range and phenology. The relationship between global warming and body size changes in mammals and birds has been widely studied, with most findings indicating a decline in body size over time. Nevertheless, little data exist on similar size change patterns of invertebrates in general and insects in particular, and it is unclear whether insects should decrease in size or not with climate warming. We measured over 4000 beetle specimens, belonging to 29 beetle species in 8 families, collected in Israel during the last 100 years. The sampled species are all herbivorous. We examined whether beetle body size had changed over the years, while also investigating the relationships between body size and annual temperature, precipitation, net primary productivity (NPP) at the collection site and collection month. None of the environmental variables, including the collection year, was correlated with the size of most of the studied beetle species, while there were strong interactions of all variables with species. Our results, though mostly negative, suggest that the effect of climate change on insect body size is species‐specific and by no means a general macro‐ecological rule. They also suggest that the intrapopulation variance in body size of insects collected as adults in the field is large enough to conceal intersite environmental effects on body size, such as the effect of temperature and NPP.     

Broad-scale patterns of body size in squamate reptiles of Europe and North America

Aim  To document geographical interspecific patterns of body size of European and North American squamate reptile assemblages and explore the relationship between body size patterns and environmental gradients.
Location  North America and western Europe.
Methods  We processed distribution maps for native species of squamate reptiles to document interspecific spatial variation of body size at a grain size of 110 × 110 km. We also examined seven environmental variables linked to four hypotheses possibly influencing body size gradients. We used simple and multiple regression, evaluated using information theory, to identify the set of models best supported by the data.
Results  Europe is characterized by clear latitudinal trends in body size, whereas geographical variation in body size in North America is complex. There is a consistent association of mean body size with measures of ambient energy in both regions, although lizards increase in size northwards whereas snakes show the opposite pattern. Our best models accounted for almost 60% of the variation in body size of lizards and snakes within Europe, but the proportions of variance explained in North America were less than 20%.
Main conclusions  Although body size influences the energy balance of thermoregulating ectotherms, inconsistent biogeographical patterns and contrasting associations with energy in lizards and snakes suggest that no single mechanism can explain variation of reptile body size in the northern temperate zone.     

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.     

Global change and carnivore body size: data are stasis

Aim  Global warming and other anthropogenic changes to the environment affect many aspects of biology and have often been invoked as causing body size changes in vertebrates. Here we examine a diverse set of carnivore populations in search of patterns in body size change that could reflect global warming (in accord with Bergmann's rule).
Location  Global.
Methods  We used > 4400 specimens representing 22 carnivore species in 52 populations collected over the last few decades to examine whether size changed with collection date when geography and sex are accounted for. We then examined several factors related to global warming, body mass, diet, and the attributes of the different datasets, to see whether they affect the standardized slope (β) of the size versus time regression.
Results  Six of 52 populations we examined show a significant effect of year of collection on body size at the 0.05 probability level. The response of size to global warming does not reflect spatial patterns of size variation, nor do diet or body mass affect tendency of populations to change in body size. Size changes are no more pronounced in populations that have been sampled more recently. However, change, where it occurs, is rapid.
Main conclusions  There may be a tendency in the literature to report only cases where recent changes are prevalent. Although in our data only a minority of populations show body size changes, we may see changes accelerating in the future in response to more drastic climatic changes and other anthropogenic changes.     

Recent spatial and temporal changes in body size of terrestrial vertebrates: probable causes and pitfalls

Geographical and temporal variations in body size are common phenomena among organisms and may evolve within a few years. We argue that body size acts much like a barometer, fluctuating in parallel with changes in the relevant key predictor(s), and that geographical and temporal changes in body size are actually manifestations of the same drivers. Frequently, the principal predictors of body size are food availability during the period of growth and ambient temperature, which often affects food availability. Food availability depends on net primary productivity that, in turn, is determined by climate and weather (mainly temperature and precipitation), and these depend mainly on solar radiation and other solar activities. When the above predictors are related to latitude the changes have often been interpreted as conforming to Bergmann's rule, but in many cases such interpretations should be viewed with caution due to the interrelationships among various environmental predictors. Recent temporal changes in body size have often been related to global warming. However, in many cases the above key predictors are not related to either latitude and/or year, and it is the task of the researcher to determine which particular environmental predictor is the one that determines food availability and, in turn, body size. The chance of discerning a significant change in body size depends to a large extent on sample size (specimens/year). The most recent changes in body size are probably phenotypic, but there are some cases in which they are partly genetic.     

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.     

Shrinking body size and climate warming: Many freshwater salmonids do not follow the rule

Declining body size is believed to be a universal response to climate warming and has been documented in numerous studies of marine and anadromous fishes. The Salmonidae are a family of coldwater fishes considered to be among the most sensitive species to climate warming; however, whether the shrinking body size response holds true for freshwater salmonids has yet to be examined at a broad spatial scale. We compiled observations of individual fish lengths from long-term surveys across the Northern Hemisphere for 12 species of freshwater salmonids and used linear mixed models to test for spatial and temporal trends in body size (fish length) spanning recent decades. Contrary to expectations, we found a significant increase in length overall but with high variability in trends among populations and species. More than two-thirds of the populations we examined increased in length over time. Secondary regressions revealed larger-bodied populations are experiencing greater increases in length than smaller-bodied populations. Mean water temperature was weakly predictive of changes in body length but overall minimal influences of environmental variables suggest that it is difficult to predict an organism's response to changing temperatures by solely looking at climatic factors. Our results suggest that declining body size is not universal, and the response of fishes to climate change may be largely influenced by local factors. It is important to know that we cannot assume the effects of climate change are predictable and negative at a large spatial scale.     

Disentangling the effects of spring anomalies in climate and net primary production on body size of temperate songbirds

Body size is implicated in individual fitness and population dynamics. Mounting interest is being given to the effects of environmental change on body size, but the underlying mechanisms are poorly understood. We tested whether body size and body condition are related to ambient temperature (heat maintenance hypothesis), or/and explained by variations in primary production (food availability hypothesis) during the period of body growth in songbirds. We also explored whether annual population‐level variations of mean body size are due to changes of juvenile growth and/or size‐dependent mortality during the first year. For 41 species, from 257 sites across France, we tested for relationships between wing length (n = 107 193) or body condition (n = 82 022) and local anomalies in temperature, precipitation and net primary production (NDVI) during the breeding period, for juveniles and adults separately. Juvenile body size was best explained by primary production: wings were longer in years with locally high NDVI, but not shorter in years with low NDVI. Temperature showed a slightly positive effect. Body condition and adult wing length did not covary with any of the other tested variables. We found no evidence of climate‐driven size‐dependent mortality for the breeding season. In our temperate system, local climatic anomalies explained little of the body size variation. A large part of wing length variance was site‐specific, suggesting that avian size was more dependent on local drivers than global ones. Net primary production influenced juvenile size the most through effects on body growth. We suggest that, during the breeding season in temperate systems, thermoregulatory mechanisms are less involved in juvenile growth than food assimilation.