Donald W. Thomas

The role of energy availability in Mammalian hibernation: a cost-benefit approach.

Hibernation is widely regarded as an adaptation to seasonal energy shortage, but the actual influence of energy availability on hibernation patterns is rarely considered. Here we review literature on the costs and benefits of torpor expression to examine the influence that energy may have on hibernation patterns. We first establish that the dichotomy between food‐ and fat‐storing hibernators coincides with differences in diet rather than body size and show that small or large species pursuing either strategy have considerable potential scope in the amount of torpor needed to survive winter. Torpor expression provides substantial energy savings, which increase the chance of surviving a period of food shortage and emerging with residual energy for early spring reproduction. However, all hibernating mammals periodically arouse to normal body temperatures during hibernation. The function of these arousals has long been speculated to involve recovery from physiological costs accumulated during metabolic depression, and recent physiological studies indicate these costs may include oxidative stress, reduced immunocompetence, and perhaps neuronal tissue damage. Using an optimality approach, we suggest that trade‐offs between the benefits of energy conservation and the physiological costs of metabolic depression can explain both why hibernators periodically arouse from torpor and why they should use available energy to minimize the depth and duration of their torpor bouts. On the basis of these trade‐offs, we derive a series of testable predictions concerning the relationship between energy availability and torpor expression. We conclude by reviewing the empirical support for these predictions and suggesting new avenues for research on the role of energy availability in mammalian hibernation.

Climate-mediated energetic constraints on the distribution of hibernating mammals

To predict the consequences of human-induced global climate change, we need to understand how climate is linked to biogeography. Energetic constraints are commonly invoked to explain animal distributions, and physiological parameters are known to vary along distributional gradients. But the causal nature of the links between climate and animal biogeography remain largely obscure. Here we develop a bioenergetic model that predicts the feasibility of mammalian hibernation under different climatic conditions. As an example, we use the well-quantified hibernation energetics of the little brown bat (Myotis lucifugus) to parameterize the model. Our model predicts pronounced effects of ambient temperature on total winter energy requirements, and a relatively narrow combination of hibernaculum temperatures and winter lengths permitting successful hibernation. Microhabitat and northern distribution limits of M. lucifugus are consistent with model predictions, suggesting that the thermal dependence of hibernation energetics constrains the biogeography of this species. Integrating projections of climate change into our model predicts a pronounced northward range expansion of hibernating bats within the next 80 years. Bioenergetics can provide the simple link between climate and biogeography needed to predict the consequences of climate change.

THE DISTRIBUTION OF BATS IN DIFFERENT AGES OF DOUGLAS-FIR FORESTS

I examined the distribution of activity of bats in different-age Douglas-fir (Pseudotsuga menziesii) stands in the Pacific Northwest. Bat activity was higher (P 300 m elevation in the Washington Cascades, but were common at elevations >300 m in the Oregon Coast Range. Reductions in old-growth forests may have a more severe impact on populations of breeding bats in the Oregon Coast Range than in the Washington Cascades.

VARIATION IN BLUE TIT BREEDING PERFORMANCE ACROSS GRADIENTS IN HABITAT RICHNESS

Food supply is widely considered to be a major factor in determining life history traits and reproductive performance of birds. However, large spatial and temporal variation in natural available food supply is not always paralleled by proportional changes in energy demand by breeding birds. This necessarily results in variation in the supply–demand ratio and the amount of food available per unit mass of nestling. Because reproductive performance should respond to increases in available supply as a saturation curve, reaching a plateau above a certain threshold of food supply, we predict that variation in supply should change the intensity of selection on reproductive traits. We first tested this prediction using long-term data on nestling growth and survival in Blue Tits (Parus caeruleus) breeding over a gradient of habitat richness in Corsica, France. This long-term data analysis evaluates the effect of variation in food supply available to breeding tits using three surrogate variables: interannual variation in peak caterpillar abundance (caterpillar frass fall), offset between breeding date and peak caterpillar abundance, and natural variation in clutch size. We also used an experimental brood size manipulation (±3 chicks) to test the effect of varying brood demand on nestling growth. Results of the long-term data analysis show that all three variables affect fledging mass and fledging success in poor habitats, while only fledging mass is affected by variation in offset in rich habitats. Moreover, mean annual fledging success and fledging mass is strongly affected by annual variation in peak caterpillar abundance at low levels of abundance, but these effects disappear when food becomes abundant (saturation threshold level of 373 and 560 mg frass·m−2·d−1 for fledging success and fledging mass, respectively). Brood size manipulations confirm these results. In rich habitats, breeding birds can raise three extra chicks without any apparent effects on chick growth, while in poor habitats, chick growth is significantly reduced with brood enlargement. Our study shows that although food limitation can play an important role, it may not always be the primary force shaping life history traits.

A Thirty-Year Study of Phenotypic and Genetic Variation of Blue Tits in Mediterranean Habitat Mosaics

Abstract In recent years, the study of phenotypic and genetic variation has been enhanced by combining genetic, physiological, demographic, and behavioral components of life histories. Using these new approaches, we address the problem of adaptation to environmental heterogeneity by examining in detail the variation of several fitness-related traits in a small passerine bird, the blue tit, which has been extensively studied in habitat mosaics of the Mediterranean region. The response of blue tits to spatial habitat heterogeneity depends on their range of dispersal relative to the size of habitat patches. Dispersal over short distances leads to local specialization, whereas dispersal over long distances leads to phenotypic plasticity. Gene flow between habitats of different quality may produce local maladaptation and a source–sink population structure. However, when habitat-specific divergent selection regimes are strong enough to oppose the effects of gene flow, local adaptation may arise on a scale that is much smaller than the scale of dispersal.

Foraging Distances and Home Range of Pregnant and Lactating Little Brown Bats (Myotis Lucifugus)

Abstract As income breeders, lactating female bats rely on current resource intake to support costs of reproduction and so must reconcile the conflicting demands of foraging and nursing. We documented changes in the movement of female little brown bats (Myotis lucifugus) around roosts between pregnancy and lactation. Home-range size dropped by 51% between pregnancy and lactation, resulting in a 35% decrease in flight distances. Although pregnant females rarely returned to roosts during the night, lactating females returned 1–2 times, which led to an increase in activity at the roosts beginning about 3 h after initial emergence. We argue that their high mass-specific milk production forces lactating females to nurse at night, which in turn imposes a constraint on foraging distances. The shift to a smaller home range is probably facilitated by the concomitant increase in insect biomass during the July lactation period.

Repeatability of daily field metabolic rate in female Meadow Voles (Microtus pennsylvanicus)

1. Repeated measurements of daily field metabolic rate (FMR) were made on 11 Meadow Voles (Microtus pennsylvanicus Ord.) by means of the doubly labelled water technique. The objective was to quantify the individual consistency of FMR by calculating the repeatability of successive measures on the same individuals. One more general goal was to test whether FMRs are sufficiently repeatable to be convenient for field studies of natural selection. 2. Voles were all non-reproductive females, 5-7-months old. They were maintained individually in outdoor enclosures 25m 2 and were injected 1-3 times with doubly labelled water. Two to six measures of daily FMR were thus obtained per individual (x = 4.09, SD = 1.51, n = 11) over a period of 42 days in July and August 1994. 3. Body mass and rate of change in body mass accounted for 31.6% of the observed variation in FMR; ground-temperature variations had no significant effect on FMR, probably owing to the small range of temperatures experienced by voles. 4. Repeatability of mass-corrected log 10 FMR measurements was low (r=0.261). This low repeatability was very consistent with the results of a previous study on consistency of mass-specific daily energy expenditures of caged pouched mice. 5. A partition of the total variance observed in mass-corrected FMR showed that 63.0% of the variance originated from differences within individuals, 27.6% from differences among individuals, and 9.4% from measurement error. FMR was not consistently higher or lower on the first or second day of measurement, indicating no clear effect of handling stress. 6. A practical implication of these results is that single measurements of daily field metabolic rates are not necessarily a good predictor of the average 24 h energy budget for a given individual. On a more theoretical basis, these results indicate that, although the ability of an animal to manage its energy economics may largely determine its selective value, daily FMR seems to be a poor candidate variable to relate this ability to individual fitness in experimental studies. 7. We suggest that future studies of repeatability of FMR should concentrate on energetically constraining periods. This would allow further evaluation of the potential role of interindividual differences in FMR as a tool for understanding evolutionary pathways that shaped energy economics of animals.

The Pace of Life under Artificial Selection: Personality, Energy Expenditure, and Longevity Are Correlated in Domestic Dogs

The domestic dog has undergone extensive artificial selection resulting in an extreme diversity in body size, personality, life‐history, and metabolic traits among breeds. Here we tested whether proactive personalities (high levels of activity, boldness, and aggression) are related to a fast “pace of life” (high rates of growth, mortality, and energy expenditure). Data from the literature provide preliminary evidence that artificial selection on dogs (through domestication) generated variations in personality traits that are correlated with life histories and metabolism. We found that obedient (or docile, shy) breeds live longer than disobedient (or bold) ones and that aggressive breeds have higher energy needs than unaggressive ones. These correlations could result from either human preference for particular trait combinations or, more likely, correlated responses to artificial selection on personality. Our results suggest the existence of a general pace‐of‐life syndrome arising from the coevolution of personality, metabolic, and life‐history traits.

Hibernating Bats are Sensitive to Nontactile Human Disturbance

I measured natural baseline activity and the response of hibernating bats to human presence in a hibernaculum containing ca. 1,300 bats of the species Myotis lucifugus and Myotis septentrionalis . Infrared detectors registered baseline flight movements in the hibernaculum over 62 days in January to March and over 8 days in April, when no observer was present, and they also registered the increase in flight movements following six visits of 1–2 h each to the hibernaculum. Visits to the mine resulted in a dramatic increase in flight activity of bats beginning within 30 min of the visit, peaking 1.0–7.5 h later, and remaining signifi-candy above baseline level for 2.5–8.5 h. These results show that, contrary to previously published studies, hibernating bats are sensitive to nontactile stimuli and arouse and fly following human visits. To avoid increased mortality due to the premature depletion of fat reserves, human visits to hibernacula should be kept to a minimum.

Habitat quality as a predictor of spatial variation in blue tit reproductive performance: a multi-plot analysis in a heterogeneous landscape.

Vertebrate studies have rarely investigated the influence of spatial variation in habitat richness on both short-term (breeding) and long-term (offspring recruitment) reproductive performance using simultaneously multi-patch, multi-habitat type and multi-year approaches at landscape level. Here we present results of such an approach using the influence of two oak tree (Quercus ilex, Q. humilis) species on reproductive performance in Corsican blue tits (Parus caeruleus ogliastrae) as a model system. We found that blue tits breeding in rich broad-leaved deciduous patches consistently laid eggs earlier in the season, and produced larger clutches and more fledglings of higher quality, than those breeding in poor evergreen patches. Also, parents, especially males, were in better physical condition in the broad-leaved deciduous than in the evergreen patches. Surprisingly, estimates of long-term effects of reproduction, such as recruitment rates of locally born offspring, did not differ between the two habitat types. Our results suggest that short-term breeding performance and phenotypic quality of both chicks and parents do not necessarily provide reliable information about contributions to following generations at a scale larger than that of the local study plot. Differences in reproductive performance between the two oak habitat types could not be attributed to density-dependent effects, differences in levels of nest predation, or differences in age structure of the birds. We suggest that habitats that are optimal for breeding are not necessarily optimal for survival after the breeding season.