Along with reproduction, balancing energy expenditure with the limits of resource acquisition is essential for both a species and a population to survive. But energy is a limited resource, as we know well, so birds and mammals—the most energy-intensive fauna on the planet—must reduce energy expenditures to maintain this balance, some taking small steps, and others extreme measures.
Here Brian K. McNab draws on his over sixty years in the field to provide a comprehensive account of the energetics of birds and mammals, one fully integrated with their natural history. McNab begins with an overview of thermal rates—much of our own energy is spent maintaining our 98.6?F temperature—and explains how the basal rate of metabolism drives energy use, especially in extreme environments. He then explores those variables that interact with the basal rate of metabolism, like body size and scale and environments, highlighting their influence on behavior, distribution, and even reproductive output. Successive chapters take up energy and population dynamics and evolution. A critical central theme that runs through the book is how the energetic needs of birds and mammals come up against rapid environmental change and how this is hastening the pace of extinction.
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About the Author
Brian K. McNab is professor emeritus in the Department of Biology at the University of Florida. He is the author of The Physiological Ecology of Vertebrates: A View from Energetics.
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EXTREME MEASURESThe Ecological Energetics of Birds and Mammals
By BRIAN K. MCNAB
The University of Chicago PressCopyright © 2012 The University of Chicago
All right reserved.
Chapter OneBasic Energetics
The purpose of this chapter is to provide a technical framework for the thermal biology of organisms so that a description of the responses of birds and mammals to the environments in which they live can be readily understood. Most animals belong to one of two thermal groups: they either have a body temperature that is similar to, and conforms to variations in, the dominant temperatures in the environment, or they maintain a rather high body temperature that is relatively independent of environmental temperatures (although some intermediate states exist, especially at large body masses). The vast majority of animals belong to the first group, the poikilotherms (poikilos, "variegated" or "variable"; thermos, "heat" or "temperature"). These animals are often called "cold-blooded" because their body temperatures usually reflect the cool ambient temperatures in which they live, and they are therefore cool to the human touch, given our core body temperature of 37°C. The second group constitutes the homeotherms ("homoio," "similar" or "constant"). These animals are often referred to as "warm-blooded" because their body temperatures are above many ambient temperatures and they therefore feel warm to our slightly cool fingertips.
Because the body temperatures of poikilotherms conform to a predominant environmental temperature (most environments have a variety of characteristic temperatures, but for simplicity, we will consider a local air or water temperature), the rates of chemical reactions that occur in their bodies, which are collectively referred to as the rate of metabolism, increase and decrease with environmental and body temperatures (fig. 1.1). Thus, the rate of metabolism in poikilotherms (measured most commonly by oxygen consumption but also by carbon dioxide production or, potentially, by heat production; see box 1.1), is high at high environmental and body temperatures and low at low temperatures (see fig. 1.1). The heat content of poikilotherms, then, is dictated principally by environmental temperature, which leads them to be called ectotherms ("outside heat"). Many complications occur in the thermal biology of ectotherms, often associated with behavior, such as the ability of some lizards to maintain a rather constant body temperature during the day by selectively absorbing solar radiation and selecting appropriate microenvironments (both of which reemphasize the ectothermic nature of their thermal biology). Furthermore, ectotherms adjust their rate of metabolism to the ambient temperatures they encounter over long periods: extended exposure to cold temperatures (cold acclimatization) tends to increase the rate of metabolism at a particular ambient temperature, although body temperature remains unchanged, whereas warm acclimatization decreases the rate of metabolism at a particular body temperature. Consequently, ectotherms in a cool, but not cold, environment tend to be about as active as ectotherms in a warm, but not hot, environment, even though their body temperatures may be quite different.
The thermal characteristics of ectotherms are also influenced by body mass. Body temperature in small species closely follows changes in ambient temperature, but as mass increases, mass-independent rates of heating and cooling (i.e., rates expressed as a percentage of values taken from standard curves) slow because of a reduced surface-to-volume ratio and increased body heat capacity. As a result, the body temperatures of large ectotherms track changes in ambient temperature more slowly than those of small species. Large ectotherms thereby gain some independence from ambient temperatures, at least in the short term. This independence is greater in aerial environments than in aquatic ones because thermal conditions in air are more complex than those in water, and because water has much greater heat capacity and conductivity.
The thermal independence of large ectotherms may approach a homeothermic condition, but one based on the thermal inertia of a large mass and a reduction in the relative rate of heat exchange with the environment. Such thermal constancy may have occurred in the largest dinosaurs, even at mass-independent rates of energy expenditure similar to those in lizards (McNab 2009c). This thermal constancy has been called "inertial homeothermy" (McNab & Auffenberg 1976) and "gigantothermy" (Paladino et al. 1990). Although this book principally concerns the thermal behavior and energetics of the homeothermic birds and mammals, the potential role of inertial homeothermy in the evolution of mammalian (and avian?) thermal behaviors will reappear in chapter 15.
Homeotherms actively maintain a rather constant body temperature by adjusting their rates of heat production and loss (see fig. 1.1). As a consequence, these vertebrates are called endotherms ("inside heat"). Thus, whereas some ectotherms maintain a rate of metabolism somewhat independent of environmental temperatures (through acclimatization), while their body temperatures vary, endotherms maintain a constant body temperature by varying their rate of metabolism, which makes endothermy a much more energy-demanding behavior than ectothermy. Endothermy and its associated level of activity are the principal bases for the energy intensity of birds and mammals. It clearly permits endothermic vertebrates to have an active life in harsh temperate and polar climates, but only if they can afford its cost. In persistently warm environments, ectotherms may be the ecological equal of, or even replace, endotherms, a situation most common on oceanic islands because most continental endotherms have difficulty reaching oceanic islands (see chap. 9).
The energetics of birds and mammals has been often described. For body temperature to remain independent of ambient temperature, the rate of heat production must balance the rate of heat loss. Because the rate of heat loss is proportional to the temperature differential between the body and the environment (ΔT = Tb - Ta), the rate of metabolism must be proportional to ΔT for body temperature to remain constant (fig. 1.2A). Endotherms can modify heat loss and rate of metabolism by increasing or decreasing the insulation provided by the integument. This can be accomplished nearly instantaneously by the erection or compression of the feather or fur coat, thereby trapping or expelling air in the coat, and by increasing or decreasing peripheral blood flow, which functionally modifies the thickness of the integument and therefore its thermal permeability. Heat loss is also proportional to the effective surface area of an endotherm and therefore is affected by posture. Insulation can be modified on a seasonal basis in fall and spring as the feathers or fur are replaced, when the thickness of the coat can be changed.
As a result of compensatory changes in insulation, peripheral circulation, and posture, the rate of metabolism in an endotherm remains constant over a range of ambient temperatures (fig. 1.2B; see fig. 1.1), even though ΔT changes over that range. This range of temperatures is called the zone of thermoneutrality (see fig. 1.1). The rate of metabolism measured in an adult animal that is regulating its body temperature within the zone of thermoneutrality when it is inactive during the inactive period and postabsorptive (i.e., when it is not digesting a meal) is called the basal rate of metabolism (or BMR) because that is the lowest rate of metabolism normally compatible with temperature regulation (McNab 1997).
The basal rate is often used to characterize endotherms, not because an individual spends much time in the conditions required by the definition of BMR, but because the conditions under which BMR is measured are, by definition, the same for all endotherms. Therefore, BMR is an equivalent measure of energy expenditure in all endotherms, unlike measurements at some fixed ambient temperature or on free-living animals in the field. Uniformity in the definition of BMR permits the relationships of this rate to the ecology, behavior, and distribution of endotherms to be examined—an effort that has had fruitful results (see chaps. 3–10). Furthermore, mass-independent variations in the field energy expenditures of endotherms are correlated with mass-independent variations in BMR (see chap. 11), which gives BMR greater significance than would be normally expected from laboratory measurements.
Speakman et al. (1993) argued that it is nearly impossible to ensure that measurements on many species are made on animals in their "basal" state. They also maintained that Kleiber's (1961) definition of BMR did not include the stipulation that body temperature was constant or that the measurements were to be made at some period in the daily cycle. Both statements are correct, but that does not mean that basal rate of metabolism, as a practical matter, cannot be effectively used, if we add the caveat, as most people do, that it applies only to endotherms when regulating their "normal" body temperature at the inactive part of their daily cycle. This may be an extension of Kleiber's criteria, but it presents no clear problem. Anyone who has measured energy expenditure is fully aware of the difficulties of attaining a resting state, but several conditions should be required, including being in the zone of thermoneutrality, which means that one measures the rates over a range of ambient temperatures during the period of rest and when the animal is maintaining its normal body temperature. (Sometimes investigators, for simplicity, arbitrarily choose a temperature as being in thermoneutrality [e.g., 30°C by Wiersma et al. 2007], but that decision has risks, especially when applied to species of all sizes.) Of course, none of these criteria evades the difficulty of measurements taken in artiodactyls that use gut fermentation; it may be impossible to get postabsorptive values without injuring the animal.
Stephenson and Racey (1995) argued that the use of BMR is inappropriate in species that enter torpor because it gives values that are unrealistically low, especially in some insectivores. They refer to all measurements of shrews and tenrecs as "resting" rates because of the tendency of some of these species to enter torpor. This view has been followed by Symonds (1999), but presents a problem and misinterprets an observation. The problem is that the use of a "resting" rate means that the rate is not equivalent in all species, which makes species comparisons subject to arbitrary decisions. The misinterpretation, as we shall see, is that nearly all birds and mammals that enter torpor have low BMRs, even when maintaining their normal body temperature (see chaps. 3, 4, and 8). The capacity to use daily torpor is another factor that determines BMR: species that enter torpor do not have the same BMR as species of the same mass that do not enter torpor.
At ambient temperatures below the zone of thermoneutrality, the rate of metabolism of endotherms increases (see fig. 1.2B) because ΔT has increased to the point where changes in insulation, posture, and peripheral circulation can no longer compensate for the increased heat loss dictated by ΔT. The rate of metabolism increases at temperatures below thermoneutrality as long as ΔT increases, or better stated, ΔT increases as long as the rate of metabolism adequately increases with a fall in Ta. When the curve of rate of metabolism plotted on Ta below thermoneutrality extrapolates to zero metabolism at Tb = Ta, its slope equals thermal conductance (see fig. 1.1), which is the inverse of insulation. Thus, the lower limit of thermoneutrality is an ambient temperature that separates the responses of endotherms at higher temperatures—by changes in insulation, posture, or peripheral circulation (the region of "physical" thermoregulation) from their responses at lower ambient temperatures, which require a change in rate of metabolism (the region of "chemical" thermoregulation).
At least that is how things are supposed to be in this idealized relationship, a condition most often seen in small species. Large species, however, often do not sharply distinguish the ambient temperatures at which physical and chemical thermoregulation occur (McNab 1980a). When that is the case, the metabolism-temperature curve below thermoneutrality usually extrapolates to Ta > Tb , and its slope is not a measure of thermal conductance and insulation (dashed curve, fig. 1.3). Under these circumstances, the curve below thermoneutrality is normally broken into a series of curves, each of which extrapolates to the mean Tb that corresponds to the appropriate curve, as is seen in data from the Auckland Island flightless teal (Anas a. aucklandica). Under this condition, conductance decreases with a decrease in ambient temperature below thermoneutrality until a minimal conductance is attained.
The ability of an endotherm to maintain a constant body temperature is limited at both low and high ambient temperatures. The increase in rate of metabolism with a decrease in Ta continues until a limit to ΔT is reached, which usually defines the minimal Ta that can be tolerated. This means that a further increase in rate of metabolism with the further decrease in ambient temperature is inadequate to maintain the additional increase in ΔT or that an increase in insulation does not compensate for the increased heat loss. Below this limit, body temperature decreases.
At high ambient temperatures, heat loss must increase to prevent overheating. Overheating at high ambient temperatures can be avoided by decreasing insulation, increasing peripheral circulation, and principally by increasing evaporative water loss. Unless adequate evaporation of water occurs at high ambient temperatures, heat will be stored, and the body temperature and rate of metabolism will increase, which threatens heat stroke if the increase in body temperature continues. Heat loss at cold ambient temperatures and heat storage at high ambient temperatures, then, define the limits of the zone of thermoneutrality.
Many of these relationships are summarized by the simplistic, but informative, Scholander-Irving equation:
M = C (Tb - Ta), (1.1)
where M is rate of metabolism (kJ/h), ITLITL is thermal conductance (kJ/h · °C), Tb is body temperature (°C), and Ta is ambient temperature (°C) (Scholander et al. 1950b). The ability of an endotherm to maintain a temperature differential with the environment, ΔT = Tb - Ta, is proportional to the ratio of the rate of heat production to thermal conductance, M/C, or alternatively, to the product of heat production and insulation, M · I, where I = 1/C. This relationship is simplistic in the sense that evaporative heat loss is ignored, as are heat exchange with a radiational source, such as the sun or a cold sky, and convective exchange in terrestrial or aquatic environments. These complications have been dealt with elsewhere (Porter & Gates 1969; Tracy 1972; Gates 1980). These "physical" topics are obviously important, but usually under restricted environmental conditions.
All four components of the relationship described by equation (1.1), M, C, Tb, and Ta, vary. Ta depends on the environment in which a species lives, time of day, and season. The other three components characterize and vary with species, and it is the exploration of these components that has given rise to our (limited) understanding of the energetics of endotherms, which is the basis of this book and its attempt to explore the consequences that these variations have for endotherms. We will examine the variation in each of these terms. We begin by examining what determines the basal rate of metabolism, and we will see how it can be used as a standard for comparing the performance of various endotherms. The same approach will be used to examine the factors that influence thermal conductance and body temperature.
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Table of Contents
PART I. FUNDAMENTALS
Chapter One. Basic Energetics
Chapter Two. Controversies in the Analysis of Quantitative Data
PART II. ECOLOGICAL CONSEQUENCES
Chapter Three. A General Analysis of BMR
Chapter Four. Small and Large
Chapter Five. A Diversity of Food Habits
Chapter Six. Life in the Cold
Chapter Seven. Life in Hot Dry and Warm Moist Environments
Chapter Eight. Evasions
PART III. FIELD EXISTENCES
Chapter Nine. Island Life
Chapter Ten. An Active Life
Chapter Eleven. Life in the Field
Chapter Twelve. The Limits to Geographic Distribution
PART IV. POPULATION CONSEQUENCES
Chapter Thirteen. A Pouched (and Egg-Laying) Life
Chapter Fourteen. Energetics and the Population Biology of Endotherms
PART V. EVOLUTIONARY CONSEQUENCES
Chapter Fifteen. The Evolution of Endothermy
Chapter Sixteen. The Restrictions and Liberations of History
PART VI. THE FUTURE
Chapter Seventeen. Global Issues: The Limitation to a Long-Term Future