Higher temperatures during development reduce body size in the zebra finch in the laboratory and in the wild

The most commonly documented morphological response across many taxa to climatic variation across their range follows Bergmann's rule, which predicts larger body size in colder climates. In observational data from wild zebra finches breeding across a range of temperatures in the spring and summer, we show that this relationship appears to be driven by the negative effect of high temperatures during development. This idea was then experimentally tested on zebra finches breeding in temperature‐controlled climates in the laboratory. These experiments confirmed that those individualso produced in a hot environment (30 °C) were smaller than those produced in cool conditions (18 °C). Our results suggest a proximate causal link between temperature and body size and suggest that a hotter climate during breeding periods could drive significant changes in morphology within and between populations. This effect could account for much of the variation in body size that drives the well‐observed patterns first described by Bergmann and that is still largely attributed to selection on adult body size during cold winters. The climate‐dependent developmental plasticity that we have demonstrated is an important component in understanding how endotherms may be affected by climate change.     

Unveiling the environmental drivers of intraspecific body size variation in terrestrial vertebrates

Aim

Whether intraspecific spatial patterns in body size are generalizable across species remains contentious, as well as the mechanisms underlying these patterns. Here we test several hypotheses explaining within-species body size variation in terrestrial vertebrates including the heat balance, seasonality, resource availability and water conservation hypotheses for ectotherms, and the heat conservation, heat dissipation, starvation resistance and resource availability hypotheses for endotherms.

Location

Global.

Time period

1970–2016.

Major taxa studied

Amphibians, reptiles, birds and mammals.

Methods

We collected 235,905 body size records for 2,229 species (amphibians = 36; reptiles = 81; birds = 1,545; mammals = 567) and performed a phylogenetic meta-analysis of intraspecific correlations between body size and environmental variables. We further tested whether correlations differ between migratory and non-migratory bird and mammal species, and between thermoregulating and thermoconforming ectotherms.

Results

For bird species, smaller intraspecific body size was associated with higher mean and maximum temperatures and lower resource seasonality. Size–environment relationships followed a similar pattern in resident and migratory birds, but the effect of resource availability on body size was slightly positive only for non-migratory birds. For mammals, we found that intraspecific body size was smaller with lower resource availability and seasonality, with this pattern being more evident in sedentary than migratory species. No clear size–environment relationships were found for reptiles and amphibians.

Main conclusions

Within-species body size variation across endotherms is explained by disparate underlying mechanisms for birds and mammals. Heat conservation (Bergmann's rule) and heat dissipation are the dominant processes explaining biogeographic intraspecific body size variation in birds, whereas in mammals, body size clines are mostly explained by the starvation resistance and resource availability hypotheses. Our findings contribute to a better understanding of the mechanisms behind species adaptations to the environment across their geographic distributions.     

Reconciling ecogeographical rules: rainfall and temperature predict global colour variation in the largest bird radiation

Ecogeographical rules that associate climate with organismal form and function can reveal patterns of climatic adaptation. Two rules link animal coloration with climate: Gloger's rule (darker coloration where wet and warm), and Bogert's rule (darker coloration where cold). Whereas Gloger's rule was proposed for endotherms, and Bogert's rule for ectotherms, both rules may apply more broadly, despite their seemingly opposing effects. Here, we test this contradiction on a global scale across passerine birds. Consistent with Gloger's rule, birds were darker in wetter areas and, following Bogert's rule, lighter where warm, although birds became lighter again at very low temperatures. Rainfall and temperature had antagonistic or additive effects depending on their pattern of covariation, and this predicted whether birds followed the rules. We integrate both rules into a general framework to explain heterogeneity in climatic effects on coloration, which has implications to understand patterns of diversification, climatic adaptation and climate change impacts.     

Urbanization disrupts latitude‐size rule in 17‐year cicadas

Many ectotherms show a decrease in body size with increasing latitude due to changes in climate, a pattern termed converse Bergmann's rule. Urban conditions—particularly warmer temperatures and fragmented landscapes—may impose stresses on development that could disrupt these body size patterns. To test the impact of urbanization on development and latitudinal trends in body size, we launched a citizen science project to collect periodical cicadas (Magicicada septendecim) from across their latitudinal range during the 2013 emergence of Brood II. Periodical cicadas are long‐lived insects whose distribution spans a broad latitudinal range covering both urban and rural habitats. We used a geometric morphometric approach to assess body size and developmental stress based on fluctuating asymmetry in wing shape. Body size of rural cicadas followed converse Bergmann's rule, but this pattern was disrupted in urban habitats. In the north, urban cicadas were larger than their rural counterparts, while southern populations showed little variation in body size between habitats. We detected no evidence of differences in developmental stress due to urbanization. To our knowledge, this is the first evidence that urbanization disrupts biogeographical trends in body size, and this pattern highlights how the effects of urbanization may differ over a species’ range.     

The complex drivers of thermal acclimation and breadth in ectotherms

Thermal acclimation capacity, the degree to which organisms can alter their optimal performance temperature and critical thermal limits with changing temperatures, reflects their ability to respond to temperature variability and thus might be important for coping with global climate change. Here, we combine simulation modelling with analysis of published data on thermal acclimation and breadth (range of temperatures over which organisms perform well) to develop a framework for predicting thermal plasticity across taxa, latitudes, body sizes, traits, habitats and methodological factors. Our synthesis includes > 2000 measures of acclimation capacities from > 500 species of ectotherms spanning fungi, invertebrates, and vertebrates from freshwater, marine and terrestrial habitats. We find that body size, latitude, and methodological factors often interact to shape acclimation responses and that acclimation rate scales negatively with body size, contributing to a general negative association between body size and thermal breadth across species. Additionally, we reveal that acclimation capacity increases with body size, increases with latitude (to mid‐latitudinal zones) and seasonality for smaller but not larger organisms, decreases with thermal safety margin (upper lethal temperature minus maximum environmental temperatures), and is regularly underestimated because of experimental artefacts. We then demonstrate that our framework can predict the contribution of acclimation plasticity to the IUCN threat status of amphibians globally, suggesting that phenotypic plasticity is already buffering some species from climate change.     

Geographic variation and thermal plasticity shape salamander metabolic rates under current and future climates

Predicted changes in global temperature are expected to increase extinction risk for ectotherms, primarily through increased metabolic rates. Higher metabolic rates generate increased maintenance energy costs which are a major component of energy budgets. Organisms often employ plastic or evolutionary (e.g., local adaptation) mechanisms to optimize metabolic rate with respect to their environment. We examined relationships between temperature and standard metabolic rate across four populations of a widespread amphibian species to determine if populations vary in metabolic response and if their metabolic rates are plastic to seasonal thermal cues. Populations from warmer climates lowered metabolic rates when acclimating to summer temperatures as compared to spring temperatures. This may act as an energy saving mechanism during the warmest time of the year. No such plasticity was evident in populations from cooler climates. Both juvenile and adult salamanders exhibited metabolic plasticity. Although some populations responded to historic climate thermal cues, no populations showed plastic metabolic rate responses to future climate temperatures, indicating there are constraints on plastic responses. We postulate that impacts of warming will likely impact the energy budgets of salamanders, potentially affecting key demographic rates, such as individual growth and investment in reproduction.     

Broad‐scale ecological implications of ectothermy and endothermy in changing environments

Aim Physiology is emerging as a basis for understanding the distribution and diversity of organisms, and ultimately for predicting their responses to climate change. Here we review how the difference in physiology of terrestrial vertebrate ectotherms (amphibians and reptiles) and endotherms (birds and mammals) is expected to influence broad‐scale ecological patterns. Location Global terrestrial ecosystems. Methods We use data from the literature and modelling to analyse geographic gradients in energy use and thermal limits. We then compare broad‐scale ecological patterns for both groups with expectations stemming from these geographic gradients. Results The differences in thermal physiology between ectotherms and endotherms result in geographically disparate macrophysiological constraints. Field metabolic rate (FMR) is stable or decreases slightly with temperature for endotherms, while it generally increases for ectotherms, leading to opposing latitudinal gradients of expected FMR. Potential activity time is a greater constraint on the distributions of ectotherms than endotherms, particularly at high latitudes. Differences in the primary correlates of abundance and species richness for two representative taxonomic groups are consistent with the consequences of these basic physiological differences. Ectotherm richness is better predicted by temperature, whereas endotherm richness is more strongly associated with primary productivity. Finally, in contrast to endotherms, ectotherm richness is not strongly related to abundance. Main conclusions Differences in thermal physiology affect how organisms interact with and are constrained by their environment, and may ultimately explain differences in the geographic pattern of biodiversity for endotherms and ectotherms. Linking the fields of physiological and broad‐scale ecology should yield a more mechanistic understanding of how biodiversity will respond to environmental change.     

Seasonal variation in basal and plastic cold tolerance: Adaptation is influenced by both long‐ and short‐term phenotypic plasticity

Understanding how thermal selection affects phenotypic distributions across different time scales will allow us to predict the effect of climate change on the fitness of ectotherms. We tested how seasonal temperature variation affects basal levels of cold tolerance and two types of phenotypic plasticity in Drosophila melanogaster. Developmental acclimation occurs as developmental stages of an organism are exposed to seasonal changes in temperature and its effect is irreversible, while reversible short‐term acclimation occurs daily in response to diurnal changes in temperature. We collected wild flies from a temperate population across seasons and measured two cold tolerance metrics (chill‐coma recovery and cold stress survival) and their responses to developmental and short‐term acclimation. Chill‐coma recovery responded to seasonal shifts in temperature, and phenotypic plasticity following both short‐term and developmental acclimation improved cold tolerance. This improvement indicated that both types of plasticity are adaptive, and that plasticity can compensate for genetic variation in basal cold tolerance during warmer parts of the season when flies tend to be less cold tolerant. We also observed a significantly stronger trade‐off between basal cold tolerance and short‐term acclimation during warmer months. For the longer‐term developmental acclimation, a trade‐off persisted regardless of season. A relationship between the two types of plasticity may provide additional insight into why some measures of thermal tolerance are more sensitive to seasonal variation than others.     

Diatoms can be an important exception to temperature–size rules at species and community levels of organization

Climate warming has been linked to an apparent general decrease in body sizes of ectotherms, both across and within taxa, especially in aquatic systems. Smaller body size in warmer geographical regions has also been widely observed. Since body size is a fundamental determinant of many biological attributes, climate‐warming‐related changes in size could ripple across multiple levels of ecological organization. Some recent studies have questioned the ubiquity of temperature–size rules, however, and certain widespread and abundant taxa, such as diatoms, may be important exceptions. We tested the hypothesis that diatoms are smaller at warmer temperatures using a system of geothermally heated streams. There was no consistent relationship between size and temperature at either the population or community level. These field data provide important counterexamples to both James’ and Bergmann's temperature–size rules, respectively, undermining the widely held assumption that warming favours the small. This study provides compelling new evidence that diatoms are an important exception to temperature–size rules for three reasons: (i) we use many more species than prior work; (ii) we examine both community and species levels of organization simultaneously; (iii) we work in a natural system with a wide temperature gradient but minimal variation in other factors, to achieve robust tests of hypotheses without relying on laboratory setups, which have limited realism. In addition, we show that interspecific effects were a bigger contributor to whole‐community size differences, and are probably more ecologically important than more commonly studied intraspecific effects. These findings highlight the need for multispecies approaches in future studies of climate warming and body size.     

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.     

Ovarian dynamics, egg size, and egg number in relation to temperature and mating status in a butterfly

Although the temperature‐size rule, that is, an increase in egg (and body) size at lower temperatures, applies almost universally to ectotherms, the developmental mechanisms underlying this consistent pattern of phenotypic plasticity are hitherto unknown. By investigating ovarian dynamics and reproductive output in the tropical butterfly Bicyclus anynana (Butler) (Lepidoptera: Nymphalidae: Satyrinae) in relation to oviposition temperature and mating status, we tested the relevance of several competing hypotheses for temperature‐mediated variation in egg size and number. As expected, females ovipositing at a lower temperature laid fewer but larger eggs than those ovipositing at a higher temperature. Despite pronounced differences in egg‐laying rates, oocyte numbers were equal across temperatures at any given time, while oocyte size increased at the lower temperature. In contrast, there were greatly reduced oocyte numbers in mated compared to virgin females. Our results indicated that temperature‐mediated plasticity in egg size cannot be explained by reduced costs of somatic maintenance at lower temperatures, enabling the allocation of more resources to reproduction (reproductive investment was higher at the higher temperature). Furthermore, there was no indication for delayed oviposition (no accumulation of oocytes at the lower temperature, in contrast to virgin females). Rather, low temperatures greatly reduced the oocyte production (i.e., differentiation) rate and prolonged egg‐maturation time, causing low egg‐laying rates. Our data thus suggested that oocyte growth is less sensitive to temperature than oocyte production, resulting in a lower number of larger eggs at lower temperatures.     

A general model for effects of temperature on ectotherm ontogenetic growth and development

The temperature size rule (TSR) is the tendency for ectotherms to develop faster but mature at smaller body sizes at higher temperatures. It can be explained by a simple model in which the rate of growth or biomass accumulation and the rate of development have different temperature dependence. The model accounts for both TSR and the less frequently observed reverse-TSR, predicts the fraction of energy allocated to maintenance and synthesis over the course of development, and also predicts that less total energy is expended when developing at warmer temperatures for TSR and vice versa for reverse-TSR. It has important implications for effects of climate change on ectothermic animals.     

Thermodynamics Constrains Allometric Scaling of Optimal Development Time in Insects

Development time is a critical life-history trait that has profound effects on organism fitness and on population growth rates. For ectotherms, development time is strongly influenced by temperature and is predicted to scale with body mass to the quarter power based on 1) the ontogenetic growth model of the metabolic theory of ecology which describes a bioenergetic balance between tissue maintenance and growth given the scaling relationship between metabolism and body size, and 2) numerous studies, primarily of vertebrate endotherms, that largely support this prediction. However, few studies have investigated the allometry of development time among invertebrates, including insects. Abundant data on development of diverse insects provides an ideal opportunity to better understand the scaling of development time in this ecologically and economically important group. Insects develop more quickly at warmer temperatures until reaching a minimum development time at some optimal temperature, after which development slows. We evaluated the allometry of insect development time by compiling estimates of minimum development time and optimal developmental temperature for 361 insect species from 16 orders with body mass varying over nearly 6 orders of magnitude. Allometric scaling exponents varied with the statistical approach: standardized major axis regression supported the predicted quarter-power scaling relationship, but ordinary and phylogenetic generalized least squares did not. Regardless of the statistical approach, body size alone explained less than 28% of the variation in development time. Models that also included optimal temperature explained over 50% of the variation in development time. Warm-adapted insects developed more quickly, regardless of body size, supporting the “hotter is better” hypothesis that posits that ectotherms have a limited ability to evolutionarily compensate for the depressing effects of low temperatures on rates of biological processes. The remaining unexplained variation in development time likely reflects additional ecological and evolutionary differences among insect species.     

Adaptive thermoregulation in endotherms may alter responses to climate change

Climate change is one of the major issues facing natural populations and thus a focus of recent research has been to predict the responses of organisms to these changes. Models are becoming more complex and now commonly include physiological traits of the organisms of interest. However, endothermic species have received less attention than have ectotherms in these mechanistic models. Further, it is not clear whether responses of endotherms to climate change are modified by variation in thermoregulatory characteristics associated with phenotypic plasticity and/or adaptation to past selective pressures. Here, we review the empirical data on thermal adaptation and acclimatization in endotherms and discuss how those factors may be important in models of responses to climate change. We begin with a discussion of why thermoregulation and thermal sensitivity at high body temperatures should be co-adapted. Importantly, we show that there is, in fact, considerable variation in the ability of endotherms to tolerate high body temperatures and/or high environmental temperatures, but a better understanding of this variation will likely be critical for predicting responses to future climatic scenarios. Next, we discuss why variation in thermoregulatory characteristics should be considered when modeling the effects of climate change on heterothermic endotherms. Finally, we review some biophysical and biochemical factors that will limit adaptation and acclimation in endotherms. We consider both long-term, directional climate change and short-term (but increasingly common) anomalies in climate such as extreme heat waves and we suggest areas of important future research relating to both our basic understanding of endothermic thermoregulation and the responses of endotherms to climate change.     

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.     

Plastic collective endothermy in a complex animal society (army ant bivouacs: Eciton burchellii parvispinum)

Endothermic animals do not always have a single adaptive internal temperature; some species exhibit plastic homeostasis, adaptively allowing body temperature to drop when thermoregulatory costs are high. Like large‐bodied endotherms, some animal societies exhibit collective thermal homeostasis. We tested for plasticity of thermoregulation in the self‐assembled temporary nests (bivouacs) of army ants. We measured core bivouac temperatures under a range of environmental conditions and at different colony developmental (larval vs pupal brood) stages. Contrary to previous assertions, bivouacs were not perfect thermoregulators in all developmental stages. Instead, bivouacs functioned as superorganismal facultative endotherms, using a combination of site choice and context‐dependent metabolic heating to adjust core temperatures across an elevational cline in ambient temperature. When ambient temperature was low, the magnitude of metabolic heating was dependent on colony developmental stage: pupal bivouacs were warmer than larval bivouacs. At cooler high elevations, bivouacs functioned like some endothermic animals that intermittently lower their body temperatures to conserve energy. Bivouacs potentially conserved energy by investing less metabolic heating in larval brood because the high costs of impaired worker development may require more stringent thermoregulation of pupae. Our data also suggest that site choice played an important role in bivouac cooling under high ambient temperatures at low elevations. Climate warming may expand upper elevational range limits of Eciton burchellii parvispinum, while reducing the availability of cool and moist bivouac sites at lower elevations, potentially leading to future low‐elevation range contraction.     

Linking life‐history theory and metabolic theory explains the offspring size‐temperature relationship

Temperature often affects maternal investment in offspring. Across and within species, mothers in colder environments generally produce larger offspring than mothers in warmer environments, but the underlying drivers of this relationship remain unresolved. We formally evaluated the ubiquity of the temperature–offspring size relationship and found strong support for a negative relationship across a wide variety of ectotherms. We then tested an explanation for this relationship that formally links life‐history and metabolic theories. We estimated the costs of development across temperatures using a series of laboratory experiments on model organisms, and a meta‐analysis across 72 species of ectotherms spanning five phyla. We found that both metabolic and developmental rates increase with temperature, but developmental rate is more temperature sensitive than metabolic rate, such that the overall costs of development decrease with temperature. Hence, within a species’ natural temperature range, development at relatively cooler temperatures requires mothers to produce larger, better provisioned offspring.     

Post-hatch heat warms adult beaks: irreversible physiological plasticity in Japanese quail

Across taxa, the early rearing environment contributes to adult morphological and physiological variation. For example, in birds, environmental temperature plays a key role in shaping bill size and clinal trends across latitudinal/thermal gradients. Such patterns support the role of the bill as a thermal window and in thermal balance. It remains unknown whether bill size and thermal function are reversibly plastic. We raised Japanese quail in warm (30°C) or cold (15°C) environments and then at a common intermediate temperature. We predicted that birds raised in cold temperatures would develop smaller bills than warm-reared individuals, and that regulation of blood flow to the bill in response to changing temperatures would parallel the bill''s role in thermal balance. Cold-reared birds developed shorter bills, although bill size exhibited ‘catch-up’ growth once adults were placed at a common temperature. Despite having lived in a common thermal environment as adults, individuals that were initially reared in the warmth had higher bill surface temperatures than cold-reared individuals, particularly under cold conditions. This suggests that blood vessel density and/or the control over blood flow in the bill retained a memory of early thermal ontogeny. We conclude that post-hatch temperature reversibly affects adult bill morphology but irreversibly influences the thermal physiological role of bills and may play an underappreciated role in avian energetics.     

The balance between predictions and evidence and the search for universal macroecological patterns: taking Bergmann’s rule back to its endothermic origin

Geographical variation in environmental temperatures is expected to impose clinal phenotypic selection that results in the expression of large-scale gradients of body mass variation within animal clades. Body size is predicted to increase with increasing latitude and elevation, and hence, with decreasing temperature, a pattern broadly known as Bergmann’s rule. However, empirical observations are highly conflicting. Whilst most studies support this prediction in endotherms (birds and mammals), analyses conducted on ectotherms often fail to report this pattern. Does it reduce the validity of this macroecological rule? Since the original formulation of Bergmann’s rule only involved endothermic organisms, I argue that the controversy is not a consequence of its predictive power, but a result of the later inclusion of ectotherms as part of the prediction. Here, I propose that the common conception of Bergmann’s rule maintained for half a century is changed back to its original definition restricted to endotherms. This temperature–size relationship might therefore consolidate as a well-established macroecological rule if its original formulation is respected. Finally, I develop these claims on my initial suggestion that Bergmann’s rule should be recognized as the evolutionary outcome of a general process with no phylogenetic scale distinction of species or populations, being equally applicable amongst and within species.     

Temperature, growth rate, and body size in ectotherms: fitting pieces of a life-history puzzle

The majority of ectotherms grow slower but mature at a larger body size in colder environments. This phenomenon has puzzled biologists because classic theories of life-history evolution predict smaller sizes at maturity in environments that retard growth. During the last decade, intensive theoretical and empirical research has generated some plausible explanations based on nonadaptive or adaptive plasticity. Nonadaptive plasticity of body size is hypothesized to result from thermal constraints on cellular growth that cause smaller cells at higher temperatures, but the generality of this theory is poorly supported. Adaptive plasticity is hypothesized to result from greater benefits or lesser costs of delayed maturation in colder environments. These theories seem to apply well to some species but not others. Thus, no single theory has been able to explain the generality of temperature-size relationships in ectotherms. We recommend a multivariate theory that focuses on the coevolution of thermal reaction norms for growth rate and size at maturity. Such a theory should incorporate functional constraints on thermal reaction norms, as well as the natural covariation between temperature and other environmental variables.