Mammal Ecology as an Indicator of Climate Change

Murray M. Humphries

Department of Natural Resource Sciences, McGill University, Ste Anne de Bellevue, Quebec, Canada H9X 3V9

1. Introduction: A Primer on 2.2. Spatial Approaches Mammal Thermoregulation and 3. Linking Time and Space in Climate Impacts Mammal Climate Responses

2. Demonstrated Impacts of Acknowledgements Climate Change on Mammals References

2.1. Temporal Approaches

On 12 January 2002, weather stations in New South Wales, Australia recorded air temperatures exceeding 42 °C, which is more than 16 °C hotter than the 30-year average daily maximum. On this day, more than 3500 flying foxes (large fruit bats in the genus Pteropus) from nine colonies in the region succumbed to hyperthermia. Mass die-offs of flying foxes associated with heat waves are known to have occurred 3 times in the century prior to 1990, 3 times in the decade between 1990 and 2000, and 13 times in 7 years between 2000 and 2007 [1].

1. INTRODUCTION: A PRIMER ON MAMMAL THERMOREGULATION AND CLIMATE IMPACTS

Fruit bats, like other mammals and birds, use a combination of physiological and behavioural mechanisms to regulate their body temperature [2]. This thermoregulatory capacity decouples their core body temperature from air temperature. Thus, despite exposure of the body surface to very cold or very hot air temperatures, appropriate physiological and behavioural ther-moregulatory responses ensure that core body temperature never varies by more than a few degrees centigrade between birth and death [3]. Even birds and mammals that express torpor do not abandon thermoregulation, but

Climate Change: Observed Impacts on Planet Earth

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rather lower their thermoregulatory setpoint [4]. For all endotherms, the abandonment of thermoregulation is fatal.

The capacity for mammals to thermoregulate might be expected to enable a degree of thermal independence that reduces their vulnerability to environmental conditions and their sensitivity to climate change. But 3500 dead flying foxes suggest any such expectation would be incorrect [1]. To understand why, we must broaden our consideration of how climate affects mammals, both directly and indirectly.

The defining feature of endotherms is their use of metabolic heat to regulate their body core at a constant set-point temperature that is independent of air temperature [2]. This means that under cool environmental conditions, where the body loses heat to the environment, maintenance of a constant body temperature requires that heat production, and thus metabolism, increases with declining air temperature along a slope that equals thermal conductance [2]. Under hot conditions, where the body gains heat from the environment, endotherms must begin actively dissipating heat through panting, perspiration, saliva spreading, and in the case of bats, wing fanning [2]. Because these responses increase heat production (i.e. contribute to the problem that it solves), the slope of the increase in metabolism at warm temperatures is always much steeper than the slope of the increase below the lower critical temperature. As a result of the inefficiencies of metabolic solutions to heat dissipation, endotherms are particularly vulnerable to heat stress and, whenever possible, occupy microenvironments that reduce heat stress [5]. Between the lower critical temperature (where thermoregulation begins to require heat production) and the upper critical temperature (where thermoregulation begins to require heat dissipation) is a region referred to as the thermal neutral zone where metabolic rate does not vary with air temperature because small, energetically insignificant adjustments in conductance (e.g. vasodilation, piloerection and postural changes) are sufficient to maintain a constant body temperature [2]. The metabolic rate (or energy expenditure) of an endotherm is minimised when they are at rest, in their thermoneutral zone, and not digesting food; metabolism measured under these circumstances is referred to as basal metabolic rate [2].

Thus, although endotherm thermoregulation permits maintenance of a constant body temperature that is independent of air temperature, air temperature has a direct and major effect on an endotherm's metabolic rate, which in turn determines their resource requirements. Endotherms exposed to environmental temperatures above or below their thermal neutral zone require more resources to stay alive than endotherms exposed to temperatures within their thermoneutral zone. Furthermore, the capacity for endotherms to produce and dissipate heat is not without limits. Exposure to extreme temperatures that cause thermoregulatory capacity to be exceeded, lead first to hypo- or hyperthermia, then, if exposure continues, to death.

Thus, air temperature has direct effects on the metabolism and resource requirements of endotherms and exposure to extreme air temperatures can have direct effects on survival.

Climate exerts additional, indirect effects on mammals through its effects on their resources, competitors and predators. Temperature has a fundamental effect on all biological processes [6], and thus climate variation should profoundly affect all organisms sharing the same environment. In fact, these indirect effects, acting via resources, competitors and predators, are likely to be so strong and pervasive that they will frequently supersede or mediate most direct effects of climate. The mass die off of flying foxes provides a potent example of a direct effect of climate operating independently of any indirect effects [1]. It was the heat that killed them, directly and outright. But even here, it is likely that more complex climate and biotic factors played a role. For example, although 1453 flying foxes from the Dallis Park colony succumbed to hyperthermia on 12 January 2002, more than 25 000 flying foxes present in the same colony and presumably exposed to the same thermal conditions survived [1]. Many factors are likely to dictate thermoregulatory capacity under such extreme situations, such as body size, age, social rank, reproductive condition, body composition and aerobic capacity [2], most of which will, in turn, be influenced by an individual's lifetime experience with resources, competitors and predators. More commonly, climate impacts on mammals are much more complex and multi-faceted, encompassing effects on thermoregulation and other forms of homeostasis, the distribution and abundance of resources, competitors and predators, as well as the interactions among all these biotic elements. Examples of climate impacts acting primarily on biotic interactions include the influence of snow cover on resource access [7] susceptibility to predation [8] and drought on the spatial overlap of competitors and predators [9]. Most climate impacts on mammals are perhaps best envisioned as climate setting the stage for a complex play involving competitors, resources and predators. Changing the stage changes the play, but often in indirect and nuanced ways.

2. DEMONSTRATED IMPACTS OF CLIMATE CHANGE ON MAMMALS

Demonstrated impacts of climate change on mammals is a broad topic, in evolutionary time, geographic scope and taxonomic diversity, which cannot be covered comprehensively in a short chapter. There is much research interest in this area, and many excellent reviews have appeared recently. For more detailed treatments, I refer the reader to the following reviews of climate change impacts on arctic marine mammals [10], Australian fauna [11], tropical ecosystems [12], fossil mammals [13], mammal morphology [14], mammal population dynamics [15] and mammal demographics [16].

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