[show abstract][hide abstract] ABSTRACT: Physiological thermal-tolerance limits of terrestrial ectotherms often exceed local air temperatures, implying a high degree of thermal safety (an excess of warm or cold thermal tolerance). However, air temperatures can be very different from the equilibrium body temperature of an individual ectotherm. Here, we compile thermal-tolerance limits of ectotherms across a wide range of latitudes and elevations and compare these thermal limits both to air and to operative body temperatures (theoretically equilibrated body temperatures) of small ectothermic animals during the warmest and coldest times of the year. We show that extreme operative body temperatures in exposed habitats match or exceed the physiological thermal limits of most ectotherms. Therefore, contrary to previous findings using air temperatures, most ectotherms do not have a physiological thermal-safety margin. They must therefore rely on behavior to avoid overheating during the warmest times, especially in the lowland tropics. Likewise, species living at temperate latitudes and in alpine habitats must retreat to avoid lethal cold exposure. Behavioral plasticity of habitat use and the energetic consequences of thermal retreats are therefore critical aspects of species' vulnerability to climate warming and extreme events.
Proceedings of the National Academy of Sciences 03/2014; · 9.74 Impact Factor
[show abstract][hide abstract] ABSTRACT: Climatic factors influence the distribution of ectotherms, raising the possibility that distributions of many species will shift rapidly under climate change and/or that species will become locally extinct. Recent studies have compared performance curves of species from different climate zones and suggested that tropical species may be more susceptible to climate change than those from temperate environments. However, in other comparisons involving responses to thermal extremes it has been suggested that mid-latitude populations are more susceptible. Using a group of 10 closely related Drosophila species with known tropical or widespread distribution, we undertake a detailed investigation of their growth performance curves and their tolerance to thermal extremes. Thermal sensitivity of life history traits (fecundity, developmental success, and developmental time) and adult heat resistance were similar in tropical and widespread species groups, while widespread species had higher adult cold tolerance under all acclimation regimes. Laboratory measurements of either population growth capacity or acute tolerance to heat and cold extremes were compared to daily air temperature under current (2002-2007) and future (2100) conditions to investigate if these traits could explain current distributions and, therefore, also forecast future effects of climate change. Life history traits examining the thermal sensitivity of population growth proved to be a poor predictor of current species distributions. In contrast, we validate that adult tolerance to thermal extremes provides a good correlate of current distributions. Thus, in their current distribution range, most of the examined species experience heat exposure close to, but rarely above, the functional heat resistance limit. Similarly, adult functional cold resistance proved a good predictor of species distribution in cooler climates. When using the species' functional tolerance limits under a global warming scenario, we find that both tropical and widespread Drosophila species will face a similar proportional reduction in distribution range under future warming.
Global Change Biology 02/2014; · 6.91 Impact Factor
[show abstract][hide abstract] ABSTRACT: Poikilothermic animals are often reliant on behavioural thermoregulation to elevate core-body temperature above the temperature of their surroundings. Butterflies are able to do this by altering body posture and location while basking, however the specific mechanisms that achieve such regulation vary among species. The role of the wings has been particularly difficult to describe, with uncertainty surrounding whether they are positioned to reduce convective heat loss or to maximize heat gained through radiation. Characterisation of the extent to which these processes affect core-body temperature will provide insights into the way in which a species’ thermal sensitivity and morphological traits have evolved. We conducted field and laboratory measurements to assess how basking posture affects the core-body temperature of an Australian butterfly, the common brown (Heteronympha merope). We show that, with wings held open, heat lost through convection is reduced while heat gained through radiation is simultaneously maximized. These responses have been incorporated into a biophysical model that accurately predicts the core-body temperature of basking specimens in the field, providing a powerful tool to explore how climate constrains the distribution and abundance of basking butterflies.
Journal of Thermal Biology 01/2014; · 1.38 Impact Factor
[show abstract][hide abstract] ABSTRACT: Spatio-temporal studies of hybrid zones provide an opportunity to test evolutionary hypotheses of hybrid zone maintenance and movement. We conducted a landscape genetics study on a classic hybrid zone of the south-eastern Australian frogs, Litoria ewingii and Litoria paraewingi. This hybrid zone has been comprehensively studied since the 1960s, providing the unique opportunity to directly assess changes in hybrid zone structure across time. We compared both mtDNA and male advertisement call data from two time periods (present and 1960s). Clinal analysis of the coincidence (same center) and concordance (same width) of these traits indicated that the center of the hybrid zone has shifted 1 km south over the last 40 years, although the width of the zone and the rate of introgression remained unchanged. The low frequency of hybrids, the strong concordance of clines within a time period, and the small but significant movement across the study period despite significant anthropogenic changes through the region, suggest the hybrid zone is a tension zone located within a low-density trough. Hybrid zone movement has not been considered common in the past but our findings highlight that it should be considered a crucial component to our understanding of evolution.
[show abstract][hide abstract] ABSTRACT: The microclimate experienced by organisms is determined by local weather conditions. Yet the environmental data available for predicting the effect of climate on the distribution and abundance of organisms is typically in the form of long-term average monthly climate measured at standardized heights above the ground. Here we demonstrate how hourly microclimates can be modelled mechanistically over decades at the continental scale with biologically suitable accuracy. We extend the microclimate model of the software package Niche Mapper to capture spatial and temporal variation in soil thermal properties, and integrate it with gridded soil and weather data for Australia at 0.05° resolution. When tested against historical observations of soil temperature, the microclimate model predicted 85% of the variation in hourly soil temperature across 10 years from the surface to 1 m deep with an accuracy of 2-3.3°C (~10% of the temperature range at a given depth) across an extremely climatically diverse range of sites. This capacity to accurately and mechanistically predict hourly local microclimates across continental scales creates new opportunities for understanding how organisms respond to changes in climate. This article is protected by copyright. All rights reserved.
Methods in Ecology and Evolution 12/2013; · 5.92 Impact Factor
[show abstract][hide abstract] ABSTRACT: Species distribution models (SDMs) are increasingly proposed to support conservation decision making. However, evidence of SDMs supporting solutions for on-ground conservation problems is still scarce in the scientific literature. Here, we show that successful examples exist but are still largely hidden in the grey literature, and thus less accessible for analysis and learning. Furthermore, the decision framework within which SDMs are used is rarely made explicit. Using case studies from biological invasions, identification of critical habitats, reserve selection and translocation of endangered species, we propose that SDMs may be tailored to suit a range of decision-making contexts when used within a structured and transparent decision-making process. To construct appropriate SDMs to more effectively guide conservation actions, modellers need to better understand the decision process, and decision makers need to provide feedback to modellers regarding the actual use of SDMs to support conservation decisions. This could be facilitated by individuals or institutions playing the role of 'translators' between modellers and decision makers. We encourage species distribution modellers to get involved in real decision-making processes that will benefit from their technical input; this strategy has the potential to better bridge theory and practice, and contribute to improve both scientific knowledge and conservation outcomes.
[show abstract][hide abstract] ABSTRACT: Correlative analyses predict that anthropogenic climate warming will cause widespread extinction but the nature and generality of the underlying mechanisms is unclear. Warming-induced activity restriction has been proposed as a general explanatory mechanism for recent population extinctions in lizards, and has been used to forecast future extinction. Here, I test this hypothesis using globally applied biophysical calculations of the effects of warming and shade reduction on potential activity time and whole-life-cycle energy budgets. These 'thermodynamic niche' analyses show that activity restriction from climate warming is unlikely to provide a general explanation of recent extinctions, and that loss of shade is viable alternative explanation. Climate warming could cause population declines, even under increased activity potential, through joint impacts on fecundity and mortality rates. However, such responses depend strongly on behaviour, habitat (shade, food) and life history, all of which should be explicitly incorporated in mechanistic forecasts of extinction risk under climate change.
[show abstract][hide abstract] ABSTRACT: Metabolic theory specifies constraints on the metabolic organisation of individual organisms. These constraints have important implications for biological processes ranging from the scale of molecules all the way to the level of populations, communities and ecosystems, with their application to the latter emerging as the field of metabolic ecology. While ecologists continue to use individual metabolism to identify constraints in ecological processes, the topic of metabolic scaling remains controversial. Much of the current interest and controversy in metabolic theory relates to recent ideas about the role of supply networks in constraining energy supply to cells. We show that an alternative explanation for physicochemical constraints on individual metabolism, as formalised by dynamic energy budget (DEB) theory, can contribute to the theoretical underpinning of metabolic ecology, while increasing coherence between intra- and interspecific scaling relationships. In particular, we emphasise how the DEB theory considers constraints on the storage and use of assimilated nutrients and derive an equation for the scaling of metabolic rate for adult heterotrophs without relying on optimisation arguments or implying cellular nutrient supply limitation. Using realistic data on growth and reproduction from the literature, we parameterise the curve for respiration and compare the a priori prediction against a mammalian data set for respiration. Because the DEB theory mechanism for metabolic scaling is based on the universal process of acquiring and using pools of stored metabolites (a basal feature of life), it applies to all organisms irrespective of the nature of metabolic transport to cells. Although the DEB mechanism does not necessarily contradict insight from transport-based models, the mechanism offers an explanation for differences between the intra- and interspecific scaling of biological rates with mass, suggesting novel tests of the respective hypotheses.
Journal of Animal Ecology 05/2013; · 4.84 Impact Factor
[show abstract][hide abstract] ABSTRACT: Hybrid zones provide a rare opportunity to explore the processes involved in reproductive isolation and speciation. The southern hybrid zone between the southeastern Australian tree frogs Litoria ewingii and L. paraewingi has been comprehensively studied over the last 40 years, primarily using reproductive compatibility experiments and male advertisement calls. We used mitochondrial DNA (mtDNA) and eight nuclear microsatellite markers to characterize this hybrid zone along a historically studied transect and to test various dispersal-dependent and dispersal-independent hybrid zone models. The species are genetically distinct and the level of hybridization within the contact zone is low, with the majority of admixed individuals representing later-generation hybrids. Based on previous experimental genetic compatibility studies, we predicted that hybrids with L. paraewingi mtDNA would be more frequent than hybrids with L. ewingii mtDNA. Surprisingly, a greater proportion of the identified hybrids had L. ewingii mtDNA. Geographical cline analyses showed a sharp transition in allele frequencies across the transect, and both the mtDNA and microsatellite data showed concordant cline centres, but were best supported by a model that allowed width to vary. Overall, the L. ewingii-L. paraewingi hybrid zone is best characterized as a tension zone, due to the narrow cline width, concordant genetic clines and low levels of hybridization.
[show abstract][hide abstract] ABSTRACT: 1. Models of the regulatory behaviour of organisms are fundamental to a strong physiologically-based understanding of species' responses to global environmental change. Biophysical models of heat and water exchange in organisms (biophysical ecology) and nutritionally-explicit models for understanding feeding behaviour and its fitness consequences (the Geometric Framework of nutrition, GF) are providing such an underpinning. However, temperature, water and nutrition interact in fundamental ways in influencing the responses of the organism to their environment, and a priority is to develop an integrated approach for conceptualising and measuring these interactions. 2. Ideally, such an approach would be based on a thermodynamically-formalized energy and mass budgeting approach that is sparsely parameterised and sufficiently general to apply across a range of situations and organisms. Here we illustrate how mass-balance aspects of Dynamic Energy Budget theory can be applied to obtain first-principles estimates of fluxes of O 2 , CO 2 , H 2 O and nitrogenous waste. 3. Then, using an herbivorous lizard (Egernia cunninghami) as a case study, we demonstrate how these estimates can be integrated with heat/water exchange models and environmental data to provide a holistic understanding of how foraging strategy, food availability, habitat and weather interact with heat, water and nutrient/energy budgets across the life-cycle. 4. The analysis shows the potential importance of the water balance in affecting the energy budgets of 'dry skinned' ectotherms, especially early in ontogeny, and highlights a significant gap in our knowledge of the physiological and behavioural traits that affect water balance when compared with our knowledge of thermal traits. 5. In general, the modelling approach we describe can provide the thermodynamically-constrained stage on which other evolutionary and ecological interactions play out; the 'thermodynamic niche'. This in turn provides a solid foundation from which to tackle key questions about organismal responses to environmental change.
[show abstract][hide abstract] ABSTRACT: Assisted colonization—the deliberate translocation of species from unsuitable to suitable regions—is a controversial management tool that aims to prevent the extinction of populations that are unable to migrate in response to climate change or to survive in situ. The identification of suitable translocation sites is therefore a pressing issue. Correlative species distribution models, which are based on occurrence data, are of limited use for site selection for species with historically restricted distributions. In contrast, mechanistic species distribution models hold considerable promise in selecting translocation sites. Here we integrate ecoenergetic and hydrological models to assess the longer-term suitability of the current habitat of one of the world’s rarest chelonians, the Critically Endangered Western Swamp Tortoise (Psuedemydura umbrina). Our coupled model allows us to understand the interaction between thermal and hydric constraints on the foraging window of tortoises, based on hydrological projections of its current habitat. The process can then be repeated across a range of future climates to identify regions that would fall within the tortoise’s thermodynamic niche. The predictions indicate that climate change will result in reduced hydroperiods for the tortoises. However, under some climate change scenarios, habitat suitability may remain stable or even improve due to increases in the heat budget. We discuss how our predictions can be integrated with energy budget models that can capture the consequences of these biophysical constraints on growth, reproduction and body condition.
[show abstract][hide abstract] ABSTRACT: Abstract Metabolism is the process by which individual organisms acquire energy and materials from their environment and use them for maintenance, differentiation, growth, and reproduction. There has been a recent push to build an individual-based metabolic underpinning into ecological theory-that is, a metabolic theory of ecology. However, the two main theories of individual metabolism that have been applied in ecology-Kooijman's dynamic energy budget (DEB) theory and the West, Brown, and Enquist (WBE) theory-have fundamentally different assumptions. Surprisingly, the core assumptions of these two theories have not been rigorously compared from an empirical perspective. Before we can build an understanding of ecology on the basis of individual metabolism, we must resolve the differences between these theories and thus set the appropriate foundation. Here we compare the DEB and WBE theories in detail as applied to ontogenetic growth and metabolic scaling, from which we identify circumstances where their predictions diverge most strongly. Promising experimental areas include manipulative studies of tissue regeneration, body shape, body condition, temperature, and oxygen. Much empirical work designed specifically with DEB and WBE theory in mind is required before any consensus can be reached on the appropriate theoretical basis for a metabolic theory of ecology.
The American Naturalist 11/2012; 180(5):546-65. · 4.55 Impact Factor
[show abstract][hide abstract] ABSTRACT: A recently developed integrative framework proposes that the vulnerability of a species to environmental change depends on the species' exposure and sensitivity to environmental change, its resilience to perturbations and its potential to adapt to change. These vulnerability criteria require behavioural, physiological and genetic data. With this information in hand, biologists can predict organisms most at risk from environmental change. Biologists and managers can then target organisms and habitats most at risk. Unfortunately, the required data (e.g. optimal physiological temperatures) are rarely available. Here, we evaluate the reliability of potential proxies (e.g. critical temperatures) that are often available for some groups. Several proxies for ectotherms are promising, but analogous ones for endotherms are lacking. We also develop a simple graphical model of how behavioural thermoregulation, acclimation and adaptation may interact to influence vulnerability over time. After considering this model together with the proxies available for physiological sensitivity to climate change, we conclude that ectotherms sharing vulnerability traits seem concentrated in lowland tropical forests. Their vulnerability may be exacerbated by negative biotic interactions. Whether tropical forest (or other) species can adapt to warming environments is unclear, as genetic and selective data are scant. Nevertheless, the prospects for tropical forest ectotherms appear grim.
Philosophical Transactions of The Royal Society B Biological Sciences 06/2012; 367(1596):1665-79. · 6.23 Impact Factor
[show abstract][hide abstract] ABSTRACT: Tropical ectotherms are regarded as being especially threatened by global warming, but the extent to which populations vary in key thermal physiological traits is little known. In general, central and peripheral populations are most likely to differ where divergent selection pressures are un-opposed by gene flow. This leads to the prediction that persistent and long-isolated lineages in peripheral regions, as revealed by phylogeography, may differ physiologically from larger centrally located lineages. We test this prediction through comparative assays of critical thermal limits (minimum and maximum critical thermal limits, CT(min), CT(max)) and optimal performance parameters (B80 and T(opt)) across central and peripheral lineages of three species of ground-dwelling skinks endemic to the rainforests of northeast Australia. Peripheral lineages show significantly increased optimal performance temperatures (T(opt)) relative to central populations as well as elevated CT(min), with the latter trait also inversely related to elevation. CT(max) did not vary between central and peripheral lineages, but was higher in a forest edge species than in the forest interior species. The results suggest that long-isolated populations in peripheral rainforests harbour genotypes that confer resilience to future warming, emphasizing the need to protect these as well as larger central habitats.
Philosophical Transactions of The Royal Society B Biological Sciences 06/2012; 367(1596):1680-7. · 6.23 Impact Factor
[show abstract][hide abstract] ABSTRACT: Developmental energetics are crucial to a species' life history and ecology but are poorly understood from a mechanistic perspective. Traditional energy and mass budgeting does not distinguish between costs of growth and maturation, making it difficult to account for accelerated development. We apply a metabolic theory that uniquely considers maturation costs (Dynamic Energy Budget theory, DEB) to interpret empirical data on the energetics of accelerated development in amphibians. We measured energy use until metamorphosis in two related frogs, Crinia georgiana and Pseudophryne bibronii. Mass and energy content of fresh ova were comparable between the species. However, development to metamorphosis was 1.7 times faster in C. georgiana while P. bibronii produced nine times the dry biomass at metamorphosis and had lower mass-specific oxygen requirements. DEB theory explained these patterns through differences in ontogenetic energy allocation to maturation. P. bibronii partitioned energy in the same (constant) way throughout development whereas C. georgiana increased the fraction of energy allocated to maturation over growth between hatching and the onset of feeding. DEB parameter estimation for additional, direct-developing taxa suggests that a change in energy allocation during development may result from a selective pressure to increase development rate, and not as a result of development mode.
Comparative biochemistry and physiology. Part A, Molecular & integrative physiology 05/2012; 163(1):95-102. · 2.20 Impact Factor
[show abstract][hide abstract] ABSTRACT: The emerging field of mechanistic niche modelling aims to link the functional traits of organisms to their environments to predict survival, reproduction, distribution and abundance. This approach has great potential to increase our understanding of the impacts of environmental change on individuals, populations and communities by providing functional connections between physiological and ecological response to increasingly available spatial environmental data. By their nature, such mechanistic models are more data intensive in comparison with the more widely applied correlative approaches but can potentially provide more spatially and temporally explicit predictions, which are often needed by decision makers. A poorly explored issue in this context is the appropriate level of temporal resolution of input data required for these models, and specifically the error in predictions that can be incurred through the use of temporally averaged data. Here, we review how biomechanical principles from heat-transfer and metabolic theory are currently being used as foundations for mechanistic niche models and consider the consequences of different temporal resolutions of environmental data for modelling the niche of a behaviourally thermoregulating terrestrial lizard. We show that fine-scale temporal resolution (daily) data can be crucial for unbiased inference of climatic impacts on survival, growth and reproduction. This is especially so for species with little capacity for behavioural buffering, because of behavioural or habitat constraints, and for detecting temporal trends. However, coarser-resolution data (long-term monthly averages) can be appropriate for mechanistic studies of climatic constraints on distribution and abundance limits in thermoregulating species at broad spatial scales.