Thermal Biology

The physiological distinction in animals that has the greatest ecological impact is the difference between ectotherms and endotherms. Most species are ectotherms, which have body temperatures that usually conform to the most prevalent environmental temperatures, whereas endotherms, most notably birds and mammals, have body temperatures that, within limits, are independent of ambient temperature (Figure 1). As a consequence, endotherms can be active at low ambient temperatures, but only by paying the cost via metabolism of maintaining this temperature differential (Figure 1). Ectotherms, on the other hand, are much more temperature dependent in their behavior, except as they are able to acclimate to temperature variations in the environment.

Ectotherms and endotherms differ in a large number of ways, especially in their standard rates of metabolism. These rates, which in endotherms are called the basal rate of metabolism, are approximately 10 times the standard rate of ectotherms, when measured in ectotherms at a body temperature of 30 °C (Figure 2). Only part of the difference between endotherms and ectotherms reflects the difference in body temperature, which in endotherms usually is between 36 and 42 °C. Another difference is that endotherms have a flexible insulation that permits a

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Figure 1 Body temperature and rate of metabolism in ectotherms and endotherms as a function of ambient temperature. Two insulations are indicated for the endotherm, where insulation 1 < insulation 2.

Figure 2 Log10 standard rate of metabolism in birds; eutherian, marsupial, and monotreme mammals; and lizards as a function of log10 body mass.

Figure 2 Log10 standard rate of metabolism in birds; eutherian, marsupial, and monotreme mammals; and lizards as a function of log10 body mass.

reduction in the cost of maintaining a temperature differential with the environment (Figure 1). The rate of metabolism in ectotherms falls with a decrease in ambient temperature because body temperature decreases (Figure 1). As a result, ectothermy is a much cheaper form of existence.

Endothermy has repeatedly evolved from ectothermy. How mammals evolved their endothermy from ancestral therapsids, which were presumably ectothermic, is unclear, but the large mass of therapsids may have given them some thermal constancy. The evolution of the earliest mammals was associated with a decrease in body size by a factor of up to 1000:1 (Figure 3). That decrease could have permitted the shift from ectothermy to endothermy, even with a decrease in rate of metabolism (Figure 4). Birds too underwent a reduction in size, if they really were derived from dinosaurs, although the intermediate steps in the evolution of birds are unknown, which prevents us from understanding how birds evolved endothermy.

Endothermy independently evolved in many other clades, including some otherwise ectothermic lineages, namely sharks, billfishes, tuna, and sea turtles, which gives them a degree of independence from water temperature. These aquatic vertebrates maintain in their lateral muscles (sharks, tuna) and core (sea turtles) a limited temperature differential with water, or the heat produced in the muscles is shunted to warm the brain (billfish). Endothermy also repeatedly evolved in various insect groups in which the thoracic temperature is regulated through the contraction of flight muscles: heat loss, in the case of moths and bumblebees, is reduced by the presence of a hair coat. The thermal biology of these insects contrasts with that found in most butterflies, which like some lizards are basking ectotherms. The small size of all thermoregulating insects, however, prevents them from maintaining a continuous temperature differential with the environment. The closest that insects come to that capacity is found in some bees and wasps that may maintain a thermally constant nest through the collective activity of a colony. Even some plants maintain a temperature differential with the environment in reproductive structures through the regulation of the rate of metabolism in the enclosed tissues. This may occur in cool environments, as was found in skunk cabbages (Symplocarpus foetidus), which facilitates the release of attractants for pollinating insects, but it also has been found in tropical species, including the Amazon giant water lily (Victoria amazonica), an arum lily (Philodendron selloum), and some palms.

Energetics

The quantitative physiological relationship most widely used in ecology is between rate of energy expenditure in animals and body mass (Figure 2). It is usually described as a power function: M = a ? mb, where M is the rate of metabolism, for example, in kJ h" , a is a coefficient, m is body mass, usually in grams or kilograms, and b is a dimensionless power. The fitted power b varies, but is almost always <1.00 and usually between 0.67 and 0.75. There have been various attempts to derive the power of this relationship from what is called first principles, but their success has been debated and often contradictory. What is not in question, however, is that as a result of the power being positive, rate of metabolism increases with mass and because b is less than 1.00, the rate of metabolism per unit mass decreases with mass. This has led to some

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X Pelycosauria • Therapsida O Mammalia

X Pelycosauria • Therapsida O Mammalia

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Figure 3 Skull length as a function of time in the Paleozoic, Mesozoic, and Cenozoic Periods in the phylogeny of mammals, including pelycosaurs, therapsids, and mammals. Modified from McNab BK (1971) On the ecological significance of Bergmann's rule. Ecology 52: 845-854.

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Figure 4 Log10 standard rate of metabolism in reptiles and mammals as a function of log10 body mass with two suggested pathways by which rate of metabolism was modified in the evolution of the earliest mammals. Also indicated is the approximate time at which a complete secondary palate evolved, which suggests a partial shift from a lower (reptilian) rate of metabolism to a higher (mammalian) rate of metabolism. Modified from McNab BK (1971) On the ecological significance of Bergmann's rule. Ecology 52: 845-854.

confusion: do large species have higher or lower rates of metabolism than small species? Both statements are true, but total rates of metabolism are the relevant rates.

Although body mass is by far the most important factor influencing the standard rate of metabolism in both endotherms and ectotherms, it does not account for all of its variation. An extensive argument has been brewing as to the factors that are responsible for the residual variation in standard rates in birds and mammals. For example, at any particular mass the ratio of the highest to the lowest basal rates in mammals equals at least 3 or 4:1 and is as high as 10:1.

The disagreement on residual variation centers on whether most of it is associated with history, that is, phylogeny, or whether it is connected with the behavioral or ecological characteristics of species. The influence of phylogeny is difficult to separate from the other proposed factors on basal rate. Furthermore, all character states may not equally reflect historical factors. That rate of metabolism is determined by history without reference to resource availability in the environment is difficult to imagine. Basal rate in both birds and mammals correlates with food habits, climate, habitat, use of torpor, and an altitudinal or island distribution. Because these factors often correlate with taxonomy, basal rate also correlates with taxonomy. In ectotherms the residual variation in standard rate of metabolism is less than that found in endotherms, probably because endotherms have such high resource requirements that they often have to adjust their expenditures. Nevertheless, residual variation in lizards correlates with their food habits and climate.

Activities other than body maintenance and thermoregulation influence energy expenditure. The cost of

Figure 5 Log10 field rates of metabolism in birds, mammals, and lizards as a function of log10 body mass. Modified from Nagy KA, Girard IA, and Brown TK (1999) Energetics of free-ranging mammals, reptiles, and birds. Annual Reviews of Nutrition 19: 247-277.

terrestrial, aquatic, and aerial locomotion in animals has been documented. It increases with velocity and is much greater in runners and walkers than in fliers, which is greater than in swimmers. Swimmers have relatively low cost of transport because they are usually neutrally buoyant and use a much greater fraction of their surface area to exert a force against the environment. The cost of flight, however, depends on the degree to which a flier uses powered or gliding flight.

The cost of activity in animals contributes to the cost of existence, as measured in field energy expenditures. Field energy expenditures, like standard rates of metabolism, increase as a power function of body mass (Figure 5). Field expenditures in vertebrates, often measured with doubly labeled water, are usually between two and four times the standard rate with a high variability depending on the immediate environmental conditions and behavior of the individuals examined. Birds and mammals that have high standard rates of metabolism for their body size also tend to have high field expenditures. High expenditures in standard and field rates are correlated with high rates of reproduction in endotherms; that is, the r—K dichotomy is ultimately based on a dichotomy in energy expenditure. Ectotherms, as would be expected from their low standard rates, have low field energy expenditures (Figure 5).

Geographical Patterns

Zoologists have described a series of ecogeographic 'rules'. The best known is Bergmann's rule, which states that endotherms tend to be larger in colder climates. It has been advocated and denied repeatedly. Like other 'rules', it faces the twofold requirement of its validity and significance. Several different surveys have generally agreed that at least some mammals and birds conform to this rule. But conformation is complex: some species that conform may do so only over a limited latitudinal range. For example, the puma or mountain lion, Puma concolor, a large New World felid, conforms to this rule twice, in North America at latitudes >35 °N and in South America at latitudes >20 ° S (Figure 6). Unfortunately, few groups have been sufficiently surveyed to know the extent to which they conform to this rule. Yet, even if a minority of species follows Bergmann's rule, the increase in mass deserves an explanation.

Explanations for Bergmann's rule have been varied. The original explanation given by C. Bergmann was that large mammals have a low rate of metabolism and low cost of body maintenance. But, as seen above, that explanation uses mass-specific rates, which is a doubtful basis: large individuals and species have higher total rates of metabolism than small individuals and species. Furthermore, some ectotherms are larger at higher latitudes, which cannot be explained by a reduction in the cost of thermoregulation.

In some cases a latitudinal increase in body mass in a smaller carnivore occurs beyond the latitudinal limits to the distribution of a larger, lower-latitude competitor (Figure 6), implying that the size difference is due to character displacement and that the increase in mass at higher latitudes of the smaller competitor is due to the absence of the larger species. Thus, the puma is smaller in the presence of the larger jaguar (Panthera onca), which is limited to tropical and warm-temperate regions. Body size in the puma correlates with prey size: pumas feed on smaller prey in the presence of jaguars and on larger prey in their absence (Figure 7). In other cases, the correlation of body size with latitude in some predators (e.g., Canis lupus) reflects changes in the size of the prey. In general, then, Bergmann's rule may reflect food quality, quantity, and availability, and will occur only if it is energetically affordable.

In contrast to Bergmann's rule, Dehnel's phenomenon describes a decrease in winter of the skeleton and nervous system in small mammals that are committed to continuous endothermy. This pattern was originally described in soricine shrews and has been subsequently seen in arvicoline rodents. The decrease in mass leads to a decrease in rate of metabolism, which presumably is its rationale. In this sense, Dehnel's phenomenon is parallel to Bergmann's rule in reflecting resource availability in the environment, an increase in body size if resources are available, or a decrease in body size if they are not. Another way of reducing energy expenditure in small mammals is to enter torpor. A significant difference, however, exists between small endotherms that conform to

Figure 6 Head and body length in pumas (Puma concolor) and jaguars (Panthera onca) as a function of latitude. Modified from McNab BK (1971) On the ecological significance of Bergmann's rule. Ecology 52: 845-854.

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Figure 7 Prey body mass as a function of puma body mass. Data from Iriarte JA, Franklin WL, Johnston WE, and Redford KH (1990) Biogeographic variation in food habits and body size of the American puma. Oecologia 85: 185-190.

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Figure 7 Prey body mass as a function of puma body mass. Data from Iriarte JA, Franklin WL, Johnston WE, and Redford KH (1990) Biogeographic variation in food habits and body size of the American puma. Oecologia 85: 185-190.

Dehnel's phenomenon and those that enter torpor: the first group is characterized by very high basal rates, whereas the latter is characterized by lower basal rates, a difference that can be seen between soricine and croci-durine shrews.

Another ecogeographic rule is the 'island rule', which states that large continental mammals are smaller if established on islands, whereas small continental species are larger on islands. The various explanations that have been given for this pattern have a common element: resource availability, which may account for the radical decrease in the size of mammoths (Mammuthus primigenius) on

Wrangel island (Siberia); elephants and hippopotamuses on Mediterranean islands; and hippopotamuses on Madagascar. Small species, especially in the absence of species with which they share resources, become larger because of the relative abundance of resources. However, island endemics can become very large. This has occurred on elephant birds (Aepyornithidae) in Madagascar and moas (Emeidae) and herbivorous rails in New Zealand, which was permitted by the absence of any endemic terrestrial, herbivorous mammals on these large islands. Large brown bears (Ursus arctos) occur on Kodiak Island (Alaska) in the presence of huge salmon (Oncorhynchus spp.) populations. The 'island rule', depending as it does on resource availability, is parallel to the combination of Bergmann's rule and Dehnel's phenomenon.

An ecogeographical pattern, which has not been dignified as a rule, is the increase in species diversity with a decrease in latitude. This pattern has been given a wide variety of explanations, but here the question is whether it has a physiological component. One is that tropical mammals and nonpasserine and passerine birds have lower rates of metabolism than temperate and polar species. Why that is the case may be complicated, but the reproductive output of birds and eutherian mammals correlates with rate of metabolism: a high rate of metabolism at high latitudes may be the means by which reproduction can be increased to compensate for high mortalities associated with harsh climatic conditions and, in the case of birds, high mortalities related to migratory habits. In contrast, resident tropical species tend to have longer life spans and lower rates of reproduction.

Limits to Geographical Distributions

As might be expected from the correlation of species diversity and energy expenditure with latitude, energy expenditure may be an important factor involved with the thermal limits to geographic distribution. For example, the limits to the winter distribution of birds in North America is closely associated with thermal isotherms, which implies that it correlates with long-term maximal rates of energy expenditure. Equally, some bats are limited to tropical and warm-temperate environments apparently in response to thermal conditions in the environment and not simply related to food habits, as might be the case in frugivores. The common vampire bat (Desmodus rotundus), which would not face a food shortage in temperate environments, is limited to regions in which the mean minimal temperature during the coldest month is >10 0C. At 10 °C D. rotundus has a rate of metabolism that is 65% greater than at 25 °C as a result of poor body insulation. A further long-term increase in metabolism is possibly prohibited by the need to transport the ingested food, its high water content (which is often excreted during feeding), and the loss of much of the energy in ingested protein as urea.

Another aspect of energetics in relation to distribution is found in island endemics: they tend to have low rates of metabolism, produced either through a decrease in body mass, or by a decrease in metabolism independent of body mass. These decreases may reflect reduced resource availability or life in environments with low species diversity, where predation and competition are greatly reduced and a high reproductive output unnecessary. This response occurs in the two groups of endotherms that are found on oceanic islands, birds and bats. Ectothermic vertebrates, including lizards, tortoises, and crocodiles, as might be expected from their low energy expenditures, are prominent on oceanic islands, often with a large mass. But even large ectotherms reduce energy requirements with a smaller mass on small islands (Figure 8).

The geographical limits to distribution in ectotherms may also reflect physiological limitations. Although rate of metabolism may acclimate to various temperatures, this response is limited, and such limitations may set the thermal and geographical limits to distribution. Ectotherms that show behavioral temperature regulation, like many insects and lizards, are able to move into cool environments by differentially absorbing solar radiation, but they still face thermal limits dictated by ambient temperature. Thus, lizards of the genus Liolaemus are able to move to altitudes as high as 4300 m in the Andes by continuously basking in the sun, which is required to maintain a viable body temperature because ambient temperatures are as low as 5 °C. At low altitudes basking time is reduced to prevent overheating.

Figure 8 Body mass in the Komodo dragon (Varanus komodensis) as a function of island area. Data from Jessop TS Madsen T, Sumner J, etal. (2006) Maximum body size among insular Komodo dragon populations covaries with large prey density. Oikos 112: 422-429.

The necessity of maintaining a water balance may also limit the geographical distribution of species. The well-known capacity of some rodents to eat dry, protein-rich seeds and live in some of the most extreme deserts derives in part from behavioral adjustments, including being nocturnal and spending the day in closed burrows, but also requires the ability to conserve water by producing a highly concentrated urine. Some small mammals tolerate deserts by consuming foods with high water contents, especially insects, and therefore do not require the capacity to produce highly concentrated urines. Obviously, species with high rates of integumental evaporative water loss, such as amphibians, face serious problems in xeric environments, where they either are active only during wet periods and sequester during dry periods, often hibernating in cocoons constructed of multiple layers of shedded skin and dried mud, or they are prevented from living in such environments. Some arboreal anurans respond to seasonally dry conditions by spreading a lipid layer on their skin, becoming stationary, switching from integumental to pulmonary gas exchange, and switching nitrogenous waste products from urea to uric acid, all of which reduce water loss.

Distribution in aquatic environments may be limited by both temperature and the osmotic concentration of water. These two factors, however, are not independent of each other because the ability to tolerate an external concentration different from that in a species' blood and tissues requires an expenditure of energy, which is temperature dependent. As a result of these limitations, some aquatic species are limited to high external concentrations, as in marine environments, whereas others are restricted to freshwater.

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