Murray M. Humphries

Personality and the emergence of the pace-of-life syndrome concept at the population level

The pace-of-life syndrome (POLS) hypothesis specifies that closely related species or populations experiencing different ecological conditions should differ in a suite of metabolic, hormonal and immunity traits that have coevolved with the life-history particularities related to these conditions. Surprisingly, two important dimensions of the POLS concept have been neglected: (i) despite increasing evidence for numerous connections between behavioural, physiological and life-history traits, behaviours have rarely been considered in the POLS yet; (ii) the POLS could easily be applied to the study of covariation among traits between individuals within a population. In this paper, we propose that consistent behavioural differences among individuals, or personality, covary with life history and physiological differences at the within-population, interpopulation and interspecific levels. We discuss how the POLS provides a heuristic framework in which personality studies can be integrated to address how variation in personality traits is maintained within populations.

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.

Anticipatory reproduction and population growth in seed predators.

Mast seeding, the intermittent, synchronous production of large seed crops by a population of plants, is a well-known example of resource pulses that create lagged responses in successive trophic levels of ecological communities. These lags arise because seed predators are thought capable of increasing reproduction and population size only after the resource pulse is available for consumption. The resulting satiation of predators is a widely cited explanation for the evolution of masting. Our study shows that both American and Eurasian tree squirrels anticipate resource pulses and increase reproductive output before a masting event, thereby increasing population size in synchrony with the resource pulse and eliminating the population lag thought to be universal in resource pulse systems.

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.

The determinants of optimal litter size in free-ranging red squirrels

Food availability, energetic ceilings, and life-history trade-offs have been proposed as potential determinants of offspring number in many animals. We investigated the role of these factors in determining litter size in a free-ranging population of red squirrels (Tamiasciurus hudsonicus). Long-term observational data were used to assess the influence of food availability, while experimental manipulations of litter size permitted evaluation of the importance of energetic ceilings and life-history trade-offs. Among unmanipulated litters, juvenile growth rate and survival, but not litter size, were significantly related to annual food supply. Experimental increases in offspring number were successfully sustained in a high- and a low-food year, but in both years increases in litter sizes were associated with pronounced declines in juvenile growth rates. However, the reduced size of offspring in augmented litters did not fully compensate for the increase in offspring number, so that the total litter mass supported by augmented females was much higher than that of control females. During late lactation, augmented females were characterized by increased daily energy expenditure, but not by significant changes in time budgets, relative to control females. Increases in litter size did not appear to reduce maternal survival, but were associated with declines in offspring survival. Together, these results indicate that food availability and energetic ceilings do not limit litter size in red squirrels directly, but that trade-offs between offspring number and offspring survival may eliminate any advantage of weaning larger-than-normal litters.

Life histories of female red squirrels and their contributions to population growth and lifetime fitness

ABSTRACT The potential importance of life history traits to population growth rates has been well explored theoretically but has rarely been documented in wild mammals. In this study we used 18 consecutive years of data from a population of North American red squirrels (Tamiasciurus hudsonicus) in the southwest Yukon, Canada, to examine variation in female life history traits and their consequences for population growth rate. Red squirrels in this population experienced severe juvenile mortality, but survivorship beyond age 2 followed a Type I relationship where the annual survival probability decreased with age. Maximum lifespan was 8 y. Some females initiated breeding as yearlings, but most delayed first breeding until 2 y of age or in some cases even later. Annual reproduction generally involved the production of a single litter averaging 3.1 offspring (range: 1 to 7); however, some females attempted a second litter within a single breeding season, either following reproductive failure or, in rare circumstances, after a successful first breeding attempt. Life table characteristics for the 11 cohorts born between 1987 and 1997 indicated a population growth rate close to zero (r = 0.009). Elasticity analysis as well as individual population projection matrices and lifetime reproductive success data indicated that early survival and not age at first reproduction was most strongly associated with a females contribution to population growth. Lifespan accounted for 83.9% of the variation in population growth rate and was positively correlated with age at first reproduction, such that females who bred as yearlings suffered decreased longevity. Collectively, these results emphasize the importance of female survival and not reproductive output to population growth and lifetime fitness in this system.

Bioenergetic Prediction of Climate Change Impacts on Northern Mammals

Abstract Climate change will likely alter the distribution and abundance of northern mammals through a combination of direct, abiotic effects (e.g., changes in temperature and precipitation) and indirect, biotic effects (e.g., changes in the abundance of resources, competitors, and predators). Bioenergetic approaches are ideally suited to predicting the impacts of climate change because individual energy budgets integrate biotic and abiotic influences, and translate individual function into population and community outcomes. In this review, we illustrate how bioenergetics can be used to predict the regional biodiversity, species range limits, and community trophic organization of mammals under future climate scenarios. Although reliable prediction of climate change impacts for particular species requires better data and theory on the physiological ecology of northern mammals, two robust hypotheses emerge from the bioenergetic approaches presented here. First, the impacts of climate change in northern regions will be shaped by the appearance of new species at least as much as by the disappearance of current species. Second, seasonally inactive mammal species (e.g., hibernators), which are largely absent from the Canadian arctic at present, should undergo substantial increases in abundance and distribution in response to climate change, probably at the expense of continuously active mammals already present in the arctic.

The Role of Energy Availability in Mammalian Hibernation: An Experimental Test in Free-Ranging Eastern Chipmunks

Reduced torpor expression by hibernating mammals is often attributed to physiological constraints that limit their hibernation ability but may instead reflect adaptive, plastic responses to surplus energy availability. We evaluated this hypothesis by supplementing the food hoards of free‐ranging eastern chipmunks (Tamias striatus) before hibernation and then documenting their use of torpor during the subsequent winter. In both years of study, chipmunks that received additional food were euthermic more than twice as frequently as nonsupplemented individuals. Furthermore, when food‐supplemented individuals did express torpor, their minimum collar temperature was 5°–10°C warmer than nonsupplemented animals. These results indicate that reduced torpor expression by hibernators can result from an absence of energetic necessity rather than a lack of physiological capability and suggest that even endotherms sequestered in a hibernaculum may benefit from maintaining an elevated body temperature whenever possible.

Estimated dietary exposure to fluorinated compounds from traditional foods among Inuit in Nunavut, Canada.

Increasing evidence shows that persistent organic pollutants such as perfluorinated compounds (PFCs) are found in the Arctic ecosystem and their prevalence is causing human health concerns. The objective of this study was to estimate dietary exposure to PFCs among Inuit in northern Canada. Perfluorooctane sulfonate (PFOS), perfluorinated carboxylates (PFCA C(7)-C(11)) and fluorotelomer unsaturated carboxylic acids (6:2, 8:2 and 10:2 FTUCA) were measured in 68 traditional foods collected in Nunavut between 1997 and 1999. Total PFC concentrations were highest in caribou liver (mean+/-standard deviation; 6.2+/-5.5 ng g(-1)), ringed seal liver (minimum, maximum; 7.7, 10.2 ng g(-1)), polar bear meat (7.0 ng g(-1)), and beluga meat (minimum, maximum; 7.0, 5.8 ng g(-1)). Inuit food intake data from 24-h recalls conducted in Nunavut between 1997 and 1999 were used for the calculation of PFC exposure. Mean daily dietary exposure was calculated to range from 210 to 610 ng person(-1) (0.6-8.5 ng kg body weight(-1)) for 754 individuals. Dietary exposure to PFCs was statistically significantly higher in men in the 41-60 year age group (p<0.05) than younger men (<40 years old) and women from the same age group. Traditional foods contributed a higher percentage to PFC exposure than market foods in all age and gender groups. Caribou meat contributed 43-75% of daily PFC dietary exposure. Health risks associated with these estimated exposure levels are minimal based on current toxicological information available from animal feeding studies. However, it is important to monitor the concentrations of PFCs in key food items given that PFCA levels have been found to be increasing in the Canadian Arctic.