Joseph Bernardo

Macrophysiology: A Conceptual Reunification

Widespread recognition of the importance of biological studies at large spatial and temporal scales, particularly in the face of many of the most pressing issues facing humanity, has fueled the argument that there is a need to reinvigorate such studies in physiological ecology through the establishment of a macrophysiology. Following a period when the fields of ecology and physiological ecology had been regarded as largely synonymous, studies of this kind were relatively commonplace in the first half of the twentieth century. However, such large‐scale work subsequently became rather scarce as physiological studies concentrated on the biochemical and molecular mechanisms underlying the capacities and tolerances of species. In some sense, macrophysiology is thus an attempt at a conceptual reunification. In this article, we provide a conceptual framework for the continued development of macrophysiology. We subdivide this framework into three major components: the establishment of macrophysiological patterns, determining the form of those patterns (the very general ways in which they are shaped), and understanding the mechanisms that give rise to them. We suggest ways in which each of these components could be developed usefully.

Determinants of maturation in animals

Maturation is a critical transition in the life cycle. Recent models have used retrospective analyses of patterns of variation in age and size at maturity in an attempt to understand the mechanisms responsible for generating phenotypic variation in maturation. Empirical work has revealed greater complexity in the biology of maturation than has been incorporated in current models, and has cast doubt on some of the assumptions and conclusions of the models. Recent insights from experimental work, coupled with theoretical advances for the analysis of growth, size and other complex characters, have great potential to elucidate evolution of maturation and how adaptive maturation phenotypes are achieved by real organisms.

Physiological constraints on organismal response to global warming: Mechanistic insights from clinally varying populations and implications for assessing endangerment.

Recent syntheses indicate that global warming affects diverse biological processes, but also highlight the potential for some species to adapt behaviourally or evolutionarily to rapid climate change. Far less attention has addressed the alternative, that organisms lacking this ability may face extinction, a fate projected to befall one-quarter of global biodiversity. This conclusion is controversial, in part because there exist few mechanistic studies that show how climate change could precipitate extinction. We provide a concrete, mechanistic example of warming as a stressor of organisms that are closely adapted to cool climates from a comparative analysis of organismal tolerance among clinally varying populations along a natural thermal gradient. We found that two montane salamanders exhibit significant metabolic depression at temperatures within the natural thermal range experienced by low and middle elevation populations. Moreover, the magnitude of depression was inversely related to native elevation, suggesting that low elevation populations are already living near the limit of their physiological tolerances. If this finding generally applies to other montane specialists, the prognosis for biodiversity loss in typically diverse montane systems is sobering. We propose that indices of warming-induced stress tolerance may provide a critical new tool for quantitative assessments of endangerment due to anthropogenic climate change across diverse species.

Experimental analysis of allocation in two divergent, natural salamander populations

I explored contributions of phenotypic plasticity and local genetic differentiation to resource allocation patterns by juvenile salamanders from populations that are known to differ in age and size at maturity. Salamanders were raised in a realistic field-experimental system with a reciprocal transplant design crossed with a prey addition treatment. This design allowed simultaneous assessment of (1) environmental effects (prey and garden), (2) genetic effects (populations), and (3) interactions between environmental and genetic effects on overall allocation patterns and on particular response variables. Genetic differences in maturity but not growth were detected, suggesting local adaptation in age at maturity. Prey supplementation accelerated growth and increased gonad and fat body mass similarly in both populations. Gonad maturation was also accelerated by supplemental food, but the populations differed in the timing of this effect. Gonad development of low-elevation salamanders, known to mature earlier in nature, responded to high prey levels at smaller sizes (younger ages) than did high-elevation animals. The plasticity of overall allocation patterns in response to supplemental prey also differed between the populations. The result that these populations differ in maturation rates but not in growth potential suggests that growth capacity and maturation timing and size are free to evolve independently. I argue that correlations between growth rates and age and size at maturity observed in many taxa do not necessarily indicate causation but probably reflect correlated responses to local environments.

Determinants of clinal variation in life history of dusky salamanders (Desmognathus ocoee): prey abundance and ecological limits on foraging time restrict opportunities for larval growth

Recent models argue that thermal environments are the major cause of ectotherm life-history clines. However, elevational clines in body size in the mountain dusky salamander Desmognathus ocoee (family Plethodontidae) shift from positive at hatching, to negative at metamorphosis to positive again as adults, and so are not consistent with this explanation. The clinal shift from hatching to metamorphosis was investigated by examining the clinal and seasonal feeding patterns of larval salamanders at high and low elevation sites in rockface and woodland habitats. Repeated cohort sampling was also used to examine clinal and seasonal patterns in body size and to estimate average growth rates. Larval growth in both rockface and woodland habitats was tightly correlated with feeding activity. Although temperature was found to vary between high and low elevation sites, the greatest growth occurred in a cold woodland habitat with a high elevation, and the lowest growth occurred in an adjacent rockface habitat. Because this difference in growth cannot be attributed to thermal differences, we conclude that local food resource levels are the predominant source of local differences in growth. These findings, clinal patterns of variation in other predatory salamanders, and experimental analyses in which both food and temperature are orthogonally manipulated, indicate that general models that single out temperature as the principle cause of ectotherm life-history clines should be viewed with caution.

Biologically grounded predictions of species resistance and resilience to climate change

Cole (1) remarked [it is] “axiomatic that the reproductive potentials of existing species are related to their requirements for survival”; this logic applies to understanding species’ capacities to respond to anthropogenic climate change. Extant species reflect the ghost of environments past: species traits such as physiological performance and tolerance are evolutionary products of environmental selection (2). They must also have had the right traits to weather previous cycles of climate change, a perspective generally lacking in the expansive literature exploring vulnerability to warming. Can these traits be useful in predicting relative vulnerability to ongoing climate change? The only way to know is to analyze such traits of many species in the context of current and projected climates. In PNAS, Sunday et al. (3) advance this approach with a suite of sophisticated analyses in the most comprehensive and biologically realistic assessment of organismal capacity to resist climate change to date.

New macroecological insights into functional constraints on mammalian geographical range size

Understanding the determinants of variation in the extent of species distributions is a fundamental goal of ecology. The diversity of geographical range sizes (GRSs) in mammals spans 12 orders of magnitude. A long-standing macroecological model of this diversity holds that as body size increases, species are increasingly restricted to occupying larger GRS. Here, we show that the body size–GRS relationship is more complex than previously recognized. Our study reveals that the positive relationship between body size and GRS does not hold across the entire size range of mammals. Instead, there is a break point in the relationship around the modal mammal body size. For species smaller than the mode, GRS actually decreases with body size. We discuss mechanisms to account for these observations in the context of the energetics of body size. We also examine the possibility that the patterns are the result of a statistical artefact from combining two random, uni-modal, skewed distributions, but conclude that the patterns we describe are not artefactual. Our results redefine our view of the functional relationship between body size, energetics and GRS in mammals with implications for assessing vulnerability to extinction resulting from range size reductions driven by large-scale environmental change.

A Macrophysiological Analysis of Energetic Constraints on Geographic Range Size in Mammals

Physiological processes are essential for understanding the distribution and abundance of organisms, and recently, with widespread attention to climate change, physiology has been ushered back to the forefront of ecological thinking. We present a macrophysiological analysis of the energetics of geographic range size using combined data on body size, basal metabolic rate (BMR), phylogeny and range properties for 574 species of mammals. We propose three mechanisms by which interspecific variation in BMR should relate positively to geographic range size: (i) Thermal Plasticity Hypothesis, (ii) Activity Levels/Dispersal Hypothesis, and (iii) Energy Constraint Hypothesis. Although each mechanism predicts a positive correlation between BMR and range size, they can be further distinguished based on the shape of the relationship they predict. We found evidence for the predicted positive relationship in two dimensions of energetics: (i) the absolute, mass-dependent dimension (BMR) and (ii) the relative, mass-independent dimension (MIBMR). The shapes of both relationships were similar and most consistent with that expected from the Energy Constraint Hypothesis, which was proposed previously to explain the classic macroecological relationship between range size and body size in mammals and birds. The fact that this pattern holds in the MIBMR dimension indicates that species with supra-allometric metabolic rates require among the largest ranges, above and beyond the increasing energy demands that accrue as an allometric consequence of large body size. The relationship is most evident at high latitudes north of the Tropics, where large ranges and elevated MIBMR are most common. Our results suggest that species that are most vulnerable to extinction from range size reductions are both large-bodied and have elevated MIBMR, but also, that smaller species with elevated MIBMR are at heightened risk. We also provide insights into the global latitudinal trends in range size and MIBMR and more general issues of phylogenetic and geographic scale.

A new species of dusky salamander (Amphibia: Plethodontidae: Desmognathus ) from the Eastern Gulf Coastal Plain of the United States and a redescription of D. auriculatus

The Coastal Plain of the southeastern U. S. is one of the planets top biodiversity hotspots and yet many taxa have not been adequately studied. The plethodontid salamander, Desmognathus auriculatus, was originally thought to occur from east Texas to Virginia, a range spanning dozens of interfluves and large river systems. Beamer and Lamb (2008) found five independent mitochondrial lineages of what has been called D. auriculatus in the Atlantic Coastal Plain, but did not examine the extensive distribution of D. auriculatus in the Gulf Coastal Plain. We present morphological and molecular genetic data distinguishing two evolutionarily independent and distantly related lineages that are currently subsumed under the taxon D. auriculatus in the eastern Gulf Coastal Plain. We describe one of these as a new species, Desmognathus valentinei sp. nov., and assign the second one to D. auriculatus which we formally redescribe.

Sea turtle funding dries up.

In December, as we celebrated the 40th anniversary of the Endangered Species Act and all of its accomplishments, the U.S. Fish and Wildlife Service (USFWS) terminated support for the recovery of an icon: the Kemps ridley sea turtle ( Lepidochelys kempii ). This sea turtle nearly slipped into