Michael R. Kearney

Predicting species distributions for conservation decisions.

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.

Birth of a biome: insights into the assembly and maintenance of the Australian arid zone biota

The integration of phylogenetics, phylogeography and palaeoenvironmental studies is providing major insights into the historical forces that have shaped the Earths biomes. Yet our present view is biased towards arctic and temperate/tropical forest regions, with very little focus on the extensive arid regions of the planet. The Australian arid zone is one of the largest desert landform systems in the world, with a unique, diverse and relatively well-studied biota. With foci on palaeoenvironmental and molecular data, we here review what is known about the assembly and maintenance of this biome in the context of its physical history, and in comparison with other mesic biomes. Aridification of Australia began in the Mid-Miocene, around 15 million years, but fully arid landforms in central Australia appeared much later, around 1-4 million years. Dated molecular phylogenies of diverse taxa show the deepest divergences of arid-adapted taxa from the Mid-Miocene, consistent with the onset of desiccation. There is evidence of arid-adapted taxa evolving from mesic-adapted ancestors, and also of speciation within the arid zone. There is no evidence for an increase in speciation rate during the Pleistocene, and most arid-zone species lineages date to the Pliocene or earlier. The last 0.8 million years have seen major fluctuations of the arid zone, with large areas covered by mobile sand dunes during glacial maxima. Some large, vagile taxa show patterns of recent expansion and migration throughout the arid zone, in parallel with the ice sheet-imposed range shifts in Northern Hemisphere taxa. Yet other taxa show high lineage diversity and strong phylogeographical structure, indicating persistence in multiple localised refugia over several glacial maxima. Similar to the Northern Hemisphere, Pleistocene range shifts have produced suture zones, creating the opportunity for diversification and speciation through hybridisation, polyploidy and parthenogenesis. This review highlights the opportunities that development of arid conditions provides for rapid and diverse evolutionary radiations, and re-enforces the emerging view that Pleistocene environmental change can have diverse impacts on genetic structure and diversity in different biomes. There is a clear need for more detailed and targeted phylogeographical studies of Australias arid biota and we suggest a framework and a set of a priori hypotheses by which to proceed.

MAPPING THE FUNDAMENTAL NICHE: PHYSIOLOGY, CLIMATE, AND THE DISTRIBUTION OF A NOCTURNAL LIZARD

The fundamental niche can be viewed as the set of conditions and resources that allow a given organism to survive and reproduce in the absence of biotic interactions. Quantitative descriptions of the environmental variables with which organisms are asso- ciated are becoming common with the advent of geographic information systems (GIS). Although such descriptive approaches to the niche are useful for interpolating species distributions, they implicitly incorporate biotic interactions and therefore do not represent the fundamental niche. A mechanistic understanding of the fundamental niche, when com- bined with GIS data, can provide us with greater insight into the causes of distribution and abundance, a solid foundation for exploring the role of biotic interactions, and greater confidence in extrapolating to novel circumstances such as climate change and species introductions. We apply such a mechanistic approach to study the climatic component of the fundamental niche of a nocturnal lizard, Heteronotia binoei, across an entire continent. We combine physiological measurements of this species (thermal requirements for egg development, thermal preferences and tolerances, metabolic and evaporative water loss rates), and high-resolution climatic data for the Australian continent (air temperature, cloud cover, wind speed, humidity, and radiation), with biophysical models to calculate the cli- matic component of the fundamental niche of this lizard and map it onto the Australian landscape at high resolution. We also use this approach to predict the effects of a mild global warming on the degree-days in the soil for egg development and the potential for aboveground activity of the study organism.

Declining body size: a third universal response to warming?

A recently documented correlate of anthropogenic climate change involves reductions in body size, the nature and scale of the pattern leading to suggestions of a third universal response to climate warming. Because body size affects thermoregulation and energetics, changing body size has implications for resilience in the face of climate change. A review of recent studies shows heterogeneity in the magnitude and direction of size responses, exposing a need for large-scale phylogenetically controlled comparative analyses of temporal size change. Integrative analyses of museum data combined with new theoretical models of size-dependent thermoregulatory and metabolic responses will increase both understanding of the underlying mechanisms and physiological consequences of size shifts and, therefore, the ability to predict the sensitivities of species to climate change.

Thermal-safety margins and the necessity of thermoregulatory behavior across latitude and elevation

Significance We find that most terrestrial ectotherms are insufficiently tolerant of high temperatures to survive the warmest potential body temperatures in exposed habitats and must therefore thermoregulate by using shade, burrows, or evaporative cooling. Our results reveal that exposure to extreme heat can occur even at high elevations and latitudes and show why heat-tolerance limits are relatively invariant in comparison with cold limits. To survive climate warming, ectotherms in most areas may need to rely on behaviors—and have access to habitats—that provide a reprieve from extreme operative temperatures. 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.

Modelling the ecological niche from functional traits

The niche concept is central to ecology but is often depicted descriptively through observing associations between organisms and habitats. Here, we argue for the importance of mechanistically modelling niches based on functional traits of organisms and explore the possibilities for achieving this through the integration of three theoretical frameworks: biophysical ecology (BE), the geometric framework for nutrition (GF) and dynamic energy budget (DEB) models. These three frameworks are fundamentally based on the conservation laws of thermodynamics, describing energy and mass balance at the level of the individual and capturing the prodigious predictive power of the concepts of ‘homeostasis’ and ‘evolutionary fitness’. BE and the GF provide mechanistic multi-dimensional depictions of climatic and nutritional niches, respectively, providing a foundation for linking organismal traits (morphology, physiology, behaviour) with habitat characteristics. In turn, they provide driving inputs and cost functions for mass/energy allocation within the individual as determined by DEB models. We show how integration of the three frameworks permits calculation of activity constraints, vital rates (survival, development, growth, reproduction) and ultimately population growth rates and species distributions. When integrated with contemporary niche theory, functional trait niche models hold great promise for tackling major questions in ecology and evolutionary biology.

DO NOCTURNAL ECTOTHERMS THERMOREGULATE? A STUDY OF THE TEMPERATE GECKO CHRISTINUS MARMORATUS

Current paradigms relating to reptilian temperature regulation are derived almost entirely from data on diurnally active species, although many reptile species are nocturnal. We investigated the extent and behavioral mechanisms of temperature regulation in the nocturnal, rock-dwelling marbled gecko Christinus marmoratus during spring and summer. During the daytime, we recorded body temperatures of lizards sheltering beneath rocks, as well as operative temperatures (the equilibrium body temperatures that animals would attain in given microclimates) beneath randomly chosen rocks available to the lizards. These measurements were compared with reference to the lizards set-point (or target) temperature range (Tset), which we determined in a laboratory thermal gradient. In both seasons, lizard body temperatures were closer to set than were randomly sampled operative temperatures, despite mean operative temperatures being 7?C below and 6?C above Tset in spring and summer, respectively. The mean body temperature of geckos was 7?C higher, and the accuracy and effectiveness of temperature regulation were also much higher, during summer than during spring. The more severe physiological consequences of thermocon- formity during summer, as well as a more constraining thermal environment during spring, are advanced as reasons for this seasonal pattern. At least two behavioral mechanisms allow C. marmoratus to achieve a regulated body temperature. First, operative temperatures within retreat sites selected by geckos were closer to Tset than were operative temperatures beneath available rocks, suggesting retreat-site selection as a thermoregulatory mechanism. Second, lizard body temperatures were closer to Tset than were operative temperatures at random positions within selected retreat sites. This observation, together with correlative evidence relating lizard body temperature to the maximum and minimum operative temperatures beneath selected retreat sites, indicates that positional and/or postural adjustments were also employed as thermoregulatory mecha- nisms. This study suggests that nocturnal lizards are capable of regulating body temperature to an extent that is comparable to that of diurnal lizards. Our findings have implications for understanding the thermal physiology and ecology of nocturnal ectotherms.

Realized niche shift during a global biological invasion.

Significance Species’ distributions result from dispersal and physiological constraints, interactions with other species, and ultimately, evolution. Biological invasions result from the deliberate or accidental movement of species between regions they would not reach through natural dispersal and can cause major conservation, economic, and human health issues. However, invasions also provide fascinating insights into species’ distribution limits. We investigate the invasion of the cane toad from South America to Australia by comparing the results of two modeling approaches: one considering physiological constraints and the other considering the joint influences of physiology, dispersal, and biotic interactions. Our findings demonstrate that the cane toad is limited in its native distribution by biotic interactions but, in Australia, is free to fill its climatic potential. Accurate forecasts of biological invasions are crucial for managing invasion risk but are hampered by niche shifts resulting from evolved environmental tolerances (fundamental niche shifts) or the presence of novel biotic and abiotic conditions in the invaded range (realized niche shifts). Distinguishing between these kinds of niche shifts is impossible with traditional, correlative approaches to invasion forecasts, which exclusively consider the realized niche. Here we overcome this challenge by combining a physiologically mechanistic model of the fundamental niche with correlative models based on the realized niche to study the global invasion of the cane toad Rhinella marina. We find strong evidence that the success of R. marina in Australia reflects a shift in the species’ realized niche, as opposed to evolutionary shifts in range-limiting traits. Our results demonstrate that R. marina does not fill its fundamental niche in its native South American range and that areas of niche unfilling coincide with the presence of a closely related species with which R. marina hybridizes. Conversely, in Australia, where coevolved taxa are absent, R. marina largely fills its fundamental niche in areas behind the invasion front. The general approach taken here of contrasting fundamental and realized niche models provides key insights into the role of biotic interactions in shaping range limits and can inform effective management strategies not only for invasive species but also for assisted colonization under climate change.

Determinants of inter-specific variation in basal metabolic rate

Basal metabolic rate (BMR) is the rate of metabolism of a resting, postabsorptive, non-reproductive, adult bird or mammal, measured during the inactive circadian phase at a thermoneutral temperature. BMR is one of the most widely measured physiological traits, and data are available for over 1,200 species. With data available for such a wide range of species, BMR is a benchmark measurement in ecological and evolutionary physiology, and is often used as a reference against which other levels of metabolism are compared. Implicit in such comparisons is the assumption that BMR is invariant for a given species and that it therefore represents a stable point of comparison. However, BMR shows substantial variation between individuals, populations and species. Investigation of the ultimate (evolutionary) explanations for these differences remains an active area of inquiry, and explanation of size-related trends remains a contentious area. Whereas explanations for the scaling of BMR are generally mechanistic and claim ties to the first principles of chemistry and physics, investigations of mass-independent variation typically take an evolutionary perspective and have demonstrated that BMR is ultimately linked with a range of extrinsic variables including diet, habitat temperature, and net primary productivity. Here we review explanations for size-related and mass-independent variation in the BMR of animals, and suggest ways that the various explanations can be evaluated and integrated.

Biomechanics meets the ecological niche: the importance of temporal data resolution

SUMMARY 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.