Integrative and Comparative Biology Advance Access originally published online on July 11, 2006
Integrative and Comparative Biology 2006 46(6):1159-1168; doi:10.1093/icb/icl016
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The energetics of reproduction in endotherms and its implication for their conservation
Department of Zoology, University of Florida Gainesville, FL 32611, USA
Correspondence: 1E-mail: bkm{at}zoo.ufl.edu
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The energy expenditure of endotherms, through its impact on the rate of reproduction, affects their ability to withstand competition, to tolerate environmental disturbances, and to endure predation. The fecundity of eutherian mammals increases with rate of metabolism because the post-natal growth rate increases and the gestation and conception-to-weaning periods decrease with a mass-independent increase in basal rate of metabolism. These correlations account for the observation that species that have large population fluctuations have high rates of metabolism and reproduction. Species with high rates of metabolism out-compete species with low rates when using resources that permit consumers to have high rates of metabolism, which explains why eutherian carnivores replace marsupial carnivores, none of which have high basal rates as a result of their form of reproduction. Fecundity in birds also appears to correlate with energy expenditure, which may account for the huge die-off of birds endemic to oceanic islands after the invasion of humans: island endemics, many of which have low rates of metabolism, are unable to increase fecundity in response to a human-based increase in mortality. The long-term protection for endotherms characterized by low rates of energy expenditure requires their isolation from high levels of predation and competition, conditions that are likely to occur only on islands free from eutherian predators and with low species diversity. Such endotherms may survive on continents if they are ecologically isolated from the general fauna.
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Introduction |
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Many factors contribute to the endangerment of species. They include life in extreme environments, a restricted distribution, a change in climate, and a human modification of the environment, which are factors "external" to the species of concern. In addition, some "internal" factors influence the ability of species to tolerate changes in the environment, to compete with other species, and ultimately to have a fecundity that can compensate for an externally driven mortality. These internal factors are most clearly seen in species that have high resource requirements, especially birds and mammals, because all responses to an environmental challenge require an expenditure of energy. A shortage of resources often characterizes many environments and some habits, which means that endotherms under these circumstances must limit their energy expenditures and therefore compromise their capacity to respond to conditions in the environment. All compromises have their distinctive consequences.
Extreme environments include high latitudes, high altitudes, and deserts. Because these environments tend to be resource limited and cool to cold, or hot and dry, the number of species present and the diversity of acceptable character states are greatly limited. Life in some environments is vulnerable as a result of their spatial limitations, including mountain tops, caves, and oceanic islands.
Some species have been threatened by the human modification of the environment in which they lived, a process that continues. This impact is especially marked in species specialized for old-growth communities. For example, the barred owl (Strix varia), a species tolerant of modified forests, may be replacing the spotted owl (Strix occidentalis), an old-growth specialist, as the old-growth coniferous forests in the Pacific Northwest are being logged (Dawson and others 1987
; Doak 1989; Dunbar and others 1991). Mature stands of pines in the southeastern US were widely cut resulting in the endangerment of the red-cockaded woodpecker (Dendrocopus borealis), which requires large live pines in which to construct nesting holes that stimulate the production of resins to reduce snake predation (Connor and others 1998). The destruction of the extended swamp forests in the southeastern US apparently was responsible for the extinction of the ivory-billed woodpecker (Campephilus principalis). (A recent reported observation of this species in Arkansas increasingly appears doubtful given the inability to confirm the original observation in spite of a great effort.) More generally, humans have been claimed to be responsible for much, or most, of the Pleistocene die-off of large mammals in North America (Martin 1984; Steadman and others 2005), and evidence clearly indicates that most of the over-kill of birds on oceanic islands coincided with the arrival of humans (Steadman and Martin 2003; Steadman 2006).
Another round of mass extinctions is anticipated from a human-based increase in the carbon-dioxide content of the atmosphere with the consequent increase in the earth's mean temperature, evidence of which is that glaciers throughout the world are retreating, sea ice diminishing, mountain temperatures rising, and tundra melting and subsiding (Diaz and Bradley 1997; Serreze and others 2000). Therefore, polar and mountaintop environments, as we know them, are likely to disappear with the loss of many species adapted to these conditions. At the present time, polar bears (Ursus maritimus) are facing a serious problem in Hudson's Bay, Canada, and in the Arctic because of the loss of sea ice, which is used by the bears as a platform for hunting and dispersal in winter (Stirling and others 1999; Derocher and others 2004). As a result, the IUCN has recently reclassified the polar bear as being vulnerable. If the warming continues, the melting of continental glaciers on Greenland and Antarctica will dump massive amounts of fresh water into polar oceans, which may redirect ocean currents and will raise sea level with the loss of many low islands (and archipelagos) along with their endemic faunas (and the forced movement of their resident human populations). Furthermore, continental desertification may increase with the destruction of many mesic environments and communities.
If mortality in a species increases as a result of climatic change, the invasion of competitors, or human activity, can it compensate through an increase in its fecundity? That is, to what extent does the propensity of a species to become endangered, or even threatened with extinction, depend on the characteristics of that species?
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Factors that influence fecundity |
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Many factors influence fecundity, including body mass, resource availability, and rate of metabolism.
Body mass
The principal factor influencing fecundity in endotherms is body size, as measured by body mass (McNab 1980a,b; Calder 1984). As with many factors that vary quantitatively with body mass, fecundity and its components take the form of a power function and therefore are generally illustrated as a linear curve on a log–log graph, the slope of the curve being the power of the function. Some relevant components of reproduction are gestation period, post-natal growth rate, and the time from conception to weaning. In eutherian mammals gestation period increases with body mass: P = a·mb, where the period (P) is longer in precocial than altricial species (Fig. 1). The post-natal growth constant k is the exponent that describes the growth of body mass in the relationship: m2 = m1·ekt, where m2 is the mass at time 2, m1 is mass at time 1, and t is the time interval. The constant k varies inversely with body mass (Fig. 2). The time from conception to weaning (t) increases with body mass: t = c·md (Fig. 3). These parameters contribute to the fecundity of mammals, the growth rate positively and the time periods inversely. In small species the gestation period and the time from conception to weaning may be so short that under appropriate environmental conditions they can have more than 1 litter in a year, so that fecundity in mammals, which is the product of litter size and litter frequency, is inversely related to body mass (Fig. 4). Notice that an appreciable residual variation exists around all these curves. What is responsible for the residual variation in these relationships?
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Resource availability
An "external" factor influencing fecundity is resource availability. Species that show remarkable population fluctuations, such as arvicoline rodents, including lemmings, and snowshoe hares, depend on an abundance of resources for their populations to recover from a population crash. The recovery may be delayed for several years in these herbivores either because the plants themselves have not recovered from a period of heavy cropping at the cropper's population high (Lack 1954
; Pitelka 1957; but see Krebs 1963) or because the plants have responded to cropping by the synthesis of secondary compounds that inhibit additional cropping (Haukioja and others 1983; Bryant and others 1989). Equally, predators, such as snowy owls (Nyctea scandiaca), short-eared owls (Asio flammeus), great horned owls (Bubo virginianus), jaegers (Stercorarius spp.), Arctic foxes (Alopex lagopus), and lynx (Lynx lynx), delay or diminish reproduction when their prey is uncommon or rare (for example, Pitelka and others 1955; Nellis and others 1972; Rusch and others 1972; Maher 1974; Chesemore 1975; Brand and others 1976).
Rate of metabolism
Rate of metabolism, through its impact on the residual variation in gestation period, post-natal growth rate, and time from conception to weaning, has an important effect on fecundity (McNab 1980). Note that these variables must be corrected for the influence of body mass because otherwise they will correlate with basal rate through their correlations with mass. However, these variables also correlate with basal rate independently of the influence of body mass. Thus, the mass-independent gestation period decreases with an increase in mass-independent basal rate of metabolism, especially in species with a precocial form of reproduction (Fig. 5). The mass-independent post-natal growth constant increases with mass-independent basal rate (Fig. 6), whereas the mass-independent time from conception to weaning decreases with an increase in mass-independent basal rate (Fig. 7). That is, eutherians with high basal rates of metabolism, a standard measure of metabolism, grow more rapidly, have shorter gestation periods, and have a shorter time from conception to weaning than eutherians of the same mass with low basal rates. As a result, species with high basal rates have shorter periods between birth and the time of first reproduction.
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Fecundity in eutherians, expressed relative to the value expected from mass, correlates with basal rate of metabolism, expressed relative to mass expectations (Fig. 8): eutherians with high basal rates, and by implication high field energy expenditures (Speakman 2000
; McNab 2002), have higher fecundities than species of the same mass with low basal rates. Harvey and others (1991) argued that the correlation seen by McNab (1980) between fecundity and basal rate of metabolism actually represented a correlation of reproduction with taxonomy, that is, phylogeny. However, phylogeny and ecology cannot be easily separated because most taxonomic units are behaviorally and ecologically distinctive and doubt exists whether species can maintain character states derived from phylogeny that are ecologically unacceptable.
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One expectation of these correlations is that eutherians with high basal rates have higher exponential population growth constants because this constant is defined by r = ln R0/T, where R0 is fecundity per generation, which increases with mass-independent basal rate, and T is generation time, which decreases with mass-independent basal rate. The equation N2 = N1ert describes population growth where N2 is the number of individuals in a population after a time interval t, and N1 is the original number of individuals in the population. So, it is not surprising that eutherians characterized by high basal rates of metabolism have higher population amplitudes than eutherians of the same mass with low basal rates under the same environmental conditions (Fig. 9). Population fluctuations among small herbivores are greatest in arvicolines and some hares, intermediate in cricetines, and lowest in heteromyids, and that is the sequence in their mass-independent basal rates (Fig. 9). This dichotomy between species with high basal rates and high rates of reproduction and species with low basal rates and low rates of reproduction is equivalent to the dichotomy between r- and K-selected species, respectively.
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The correlation of reproduction with rate of metabolism is not found in marsupials because an increase in rate of metabolism cannot be translated into higher fetal growth rates (McNab 1986b
, 2005). This does not occur because marsupials do not have placentae that permit high rates of material, gas, and waste exchange between mother and fetus due to the threat of immunological rejection before birth, which is avoided by the presence of a nearly impermeable shell membrane (Lillegraven 1976; Lillegraven and others 1987). Thus, marsupial fetal development in utero, as modest as it is, depends principally on the metabolism of egg yolk, and not on uterine exchange. Furthermore, the intestinal tract in a neonatal marsupial develops slowly (Parker 1977) and therefore a high rate of milk production by its mother could not increase the young's rate of development. Although an appreciable residual variation in post-natal growth rate and time from conception to weaning exists in marsupials, they do not correlate with variation in basal rate of metabolism (McNab 1986b). Marsupials also differ from eutherians by having only 6 out of 70 species (9%) with standard to high basal rates compared with a general mammalian standard (for example, BMR [mL O2/h] = 3.42 m0.713 [McNab 1988]), the greatest being 110%, whereas 152 out of 272 of eutherians (56%) have high basal rates by the same standard, 40 greater than 150% (McNab 2005). This observation led to the suggestion that the high basal rates of eutherians stem from their importance in maximizing the rate of reproduction, not reflecting the cost of thermoregulation (McNab 1980, 1986b, 2005), and that is why there is more residual variation in the basal rate of eutherians: body mass alone accounts for 98.8% of the variation in total basal rate in marsupials and 95.6% in eutherians (McNab 2005).
Recent information indicates that the reproduction of birds is similar to that in eutherian mammals in correlating with their basal rate of metabolism. For example, pursuing, bird-eating raptors of the genera Falco and Accipiter have higher basal rates, corrected for body size, than raptors, such as Daptrius, Buteo, Parabuteo, Aquila, and Ictinia, with other food habits and hunting strategies (Wasser 1986): these pursing raptors also have larger clutch sizes (del Hoyo and others 1994). Flightless rails endemic to oceanic islands have smaller clutches and lower basal rates of metabolism than volant rails on continents and islands (McNab and Ellis 2006) (Fig. 10). Furthermore, some (many?) volant birds endemic to oceanic islands are characterized both by low basal rates (McNab 2000) and reduced rates of reproduction (Cody 1966). However, Cody (1966), referring to the suggestion that fecundity in birds might be adjusted to balance mortality, was concerned that " it has been pointed out by Lack (1947, 1948, 1954) that there is no proven mechanism to carry out this adjustment...." If, however, fecundity in birds is correlated with rate of energy expenditure, as proposed here, and if energy expenditure and mortality are correlated with conditions in the environment, this might explain how, by adjusting rate of energy expenditure, fecundity can be adjusted to match mortality. In fact, basal rate of metabolism (Weathers 1979; Hails 1983; Ellis 1985) and clutch size in birds (Cody 1966) increase with latitude. So, it appears that in environments where mortality is high, as in cold-temperate and polar climates, rate of metabolism and rate of reproduction are high, whereas in tropical climates and on oceanic islands, where mortality is low, these rates are low. Indeed, Gavrilov (1995) argued that the acquisition of high basal rates of metabolism, along with their correlates of high productive and potential energy expenditures, permitted passerines to dominate temperate, terrestrial environments.
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Consequences |
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Many are the consequences of a correlation of reproductive output with the rate of energy expenditure. (1) As we have seen, eutherians that have high basal rates of metabolism often show marked population fluctuations (McNab 1980
). This is most clear in arvicoline rodents, some murid rodents, hares, and some predators. (2) Marsupials can coexist with ecologically equivalent eutherians only if marsupials eat foods that are associated with low rates of metabolism in eutherians, thereby denying eutherians a reproductive advantage over marsupials (McNab 1986b, 2005). Almost all marsupials found in the Neotropics, in spite of their taxonomic diversity, feed on insects, fruit, or a mixture of fruit and insects, food habits that are associated with low basal rates in eutherians (McNab 1986a, 2005). The 2 principal food habits that are correlated with high basal rates in eutherians are carnivory and grazing (McNab 1986a), and these food habits are found in marsupials only in Australia, Tasmania, and New Guinea, where eutherians with these habits are not found. When the wolf (Canis lupus) was brought into Australia in the form of dingos, equivalent marsupial carnivores became extinct, except in Tasmania, where dingos never occurred (McNab 1986b, 2005). (3) Rails that are found on oceanic islands have smaller clutches than rails found on continents, and this reduction in clutch size is most marked in flightless species, which have the lowest basal rates of metabolism, independent of body mass (McNab and Ellis 2006). These differences between island and continental rails are correlated with the absence or presence of eutherian carnivores, respectively, that is, with the level of predation. (4) The pattern found in island rails, that is, being characterized by low basal rates and small clutches in the absence of eutherian predators (McNab and Ellis 2006), may occur generally in flighted birds endemic to oceanic islands (McNab 2002). Another distinctive geographic pattern in energy expenditure is that some species of birds in the South Pacific, such as the island thrush (Turdus poliocephalus), are generally limited in distribution to low altitudes on small oceanic islands, but occur on large island/continents such as New Guinea only at altitudes >2500 m. Those species with this distribution that have been examined are characterized by low basal rates of metabolism, which raises the question: what, if anything, is common to life in these 2 radically different environments? The 1 factor that appears to be present is a low species diversity, which suggests that the low basal rates of island endemics may reflect low levels of predation and competition, as well as a limited resource base, and results in a low fecundity. Maybe we should abandon our continental bias and realize that island endemics do not have low basal rates, but that continental endotherms have high basal rates to increase rate of reproduction in the face of high levels of predation and competition, which may explain why continental species are often more resilient than island endemics in the face of a human presence.
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Implications for conservation |
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As implied, the correlation of reproductive output with rate of energy expenditure may have serious consequences for conservation. If some species respond to environmental conditions by reducing energy expenditure, as is the case when consuming certain foods or living on islands or in deserts, the reduction in energy expenditure may inflexibly lock a species into a low fecundity. Therefore such species may be denied the capacity to respond to an externally driven increase in mortality by an increase in fecundity. For example,
98% of the species of flightless rails endemic to oceanic islands became extinct after the arrival of humans during the past 30 000 to 1000 years (Steadman 2006). This may have been the product not only of hunting, the burning and cutting of the forests, and the importation of rats, dogs, and pigs, but also of the inability of these rails to respond to a dramatic increase in mortality by increasing their rates of reproduction. This pattern may have also accounted for the great loss of volant birds endemic to predator-free oceanic islands after the arrival of humans.
A recent examination of the extinction-prone characteristics of terrestrial mammals in China (Lui and Li 2005) indicated that their threatened status increases with (1) body size and (2) a decrease in fecundity. From the analysis given here, fecundity decreases both with an increase in body mass and with a decrease in rate of metabolism. So, depending on the characteristics of a particular species and the adjustments that it has made to the environment in which it lives, these characteristics may make them prone to an endangered status and ultimately to extinction.
High-energy species have a reproductive flexibility that is not found in low-energy species; they may have facultatively low reproductive rates when resources are limited, but if resource abundance increases, their high rates of energy expenditure will permit them to increase, often dramatically, their rate of reproduction, as has been repeated observed (see Resource availability above). This response is most notable in species known to have large population fluctuations. Species with high rates of metabolism are also vulnerable to extinction as a result of an environmental calamity or the presence of an overwhelming predator, such as Homo sapiens. Nevertheless, the endotherms that are most vulnerable to a change in environmental conditions are those that have inflexibly low rates of reproduction and most of those will be characterized by low basal rates of metabolism.
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Solutions? |
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Given this analysis of the vulnerability of some species, those with the lowest rates of metabolism must be given an environment where the level of mortality is acceptably low, if they are to survive. Some of the most vulnerable species are island endemics, many or most of which are characterized by low rates of energy expenditure and investment. Such species survive well when isolated on islands free of eutherian predators. The Department of Conservation in New Zealand has transported endangered species, including the little spotted kiwi (Apteryx owenii), takahe (Porphyrio hochstetteri), kakapo (Strigops habroptilus), stitchbird (Notiomystis cincta), and saddleback (Philesturnus carunculatus), from the main islands to small offshore islands. In part, this program has been successful by preventing predators from occupying these islands or, as in the case of Kapiti (Empson and Miskelly 1999
) and Campbell Islands (Seddon and Maloney 2003), of eliminating rats that had been brought onto the islands by earlier human activity. This extermination has extended protection to small-island endemics, including Auckland Island teal (Anas aucklandica), Campbell Island teal (Anas nesiotis), Auckland Island rail (Lewinia pectoralis), New Zealand snipe (Coenocorypha spp.), and black robin (Petroica traversi). Such isolation decreased mortality so that species with low rates of reproduction and, in the case of all of these species that have been studied, low basal rates of metabolism (McNab 1996, 2003; McNab and Ellis 2006) could survive in spite of their inheritantly low fecundities. A continental solution might also be possible, but that would occur only if large land areas were rigorously protected. However, given the naturally high predation rates typical of continents, such areas are unlikely to be effective in protecting species characterized by low rates of energy expenditure, except as they are protected by habits that isolate them from all but the most specialized predators. Such habits include life in deserts, burrows, caves, and trees, or by having unusual food habits.
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Acknowledgements |
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I thank Robert D. Stevenson, Department of Biology, University of Massachusetts at Boston, for the invitation to be part of the symposium that led to this article. David Whitacre, The Perigrine Fund, Boise, Idaho, pointed out to me that bird-eating raptors have larger clutches than other raptors. I also appreciate editorial suggestions by Harold Heatwole and comments made by Hugh Ellis and an anonymous reviewer.
Conflict of interest: None declared.
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Footnotes |
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From the symposium "Ecophysiology and Conservation: The Contributions of Energetics" presented at the annual meeting of the Society for Integrative and Comparative Biology, January 4–8, 2006, at Orlando, Florida.
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