1088 Ecophysiology and conservation: The contribution of energetics—introduction to the symposium Robert D. Stevenson1 Department of Biology, University of Massachusetts–Boston, Boston, MA 02125-3393, USA

Synopsis Animal physiologists have begun making contributions to conservation biology based on their knowledge of endocrinology, immunology, and sensory biology. Contributions to this symposium use the perspective of energy and mass balance to examine questions about habitat usage, activity times, competition, foraging, reproduction, and body condition. Physiological constraints or requirements sculpt the behavioral and life history choices of individuals and provide mechanistic linkages with population processes and conservation policies. Downloaded from https://academic.oup.com/icb/article/46/6/1088/719300 by guest on 27 September 2021

Introduction out of a pragmatic desire to stem the loss of our Preventing the loss of biodiversity is one of the great natural heritage. The Society for Conservation challenges facing humanity today (Wilson 2002). The Biology, now a worldwide organization with 10 000 earth is currently experiencing its sixth great mass members, was officially founded just 20 years ago. The extinction, but unlike the previous events this one is development of conservation science has focused at uniquely caused by human-related activities (Leakey the genetic, population, landscape, and ecosystem 1996). Overharvesting (Flannery 2002; Martin 2005) levels (Meffe and Carroll 1997; Hunter 2001; Soule was the initial driver, but today anthropogenic-induced and Orians 2001; Primack 2006). Curiously, con- climatic change, habitat loss, toxic substances, and servation practice has placed less emphasis on the invasive species (including novel diseases) all contribute individual organism and how it is affected by (Vitousek and others 1997; Lubchenco 1998; environmental change, despite the tools available McMichael and Kovats 2000; Wilson 2002). Cultures from decades of ecophysiological research. Recently, around the world have had complex relationships with however, physiologists, especially reproductive physi- nature, and no single cause is at the root of environ- ologists, have been making contributions (Clemmons mental degradation and loss (Diamond 2005). The and Buchholz 1997; Berger and others 1999; Gordon growth economy of present-day modern societies (Daly and Bartol 2004; Carey 2005; Stevenson and others 1996) shows that society as a whole does not value the 2005; Wikelski and Cooke 2006). For instance, in vital role of the environment, especially ecosystem the past 3 years the Society for Integrative and services (Daily 1997). However, across organizational Comparative Biology has sponsored 4 symposia that scales from the local to the global, individuals, NGOs, have related organismal level studies to conservation and governmental agencies are focusing on critical biology (2004—EcoPhysiology and Conservation: The environmental problems such as climatic change, Contribution of Endocrinology and Immunology; invasive species, habitat loss, water shortages, and 2005—Zoo-based Research and Conservation; 2006— pollution. Efforts by these organizations are underway Ecological Immunology: Recent Advances and to link scientific understanding to policy (Ludwig 2001; Applications for Conservation and Public Health; and Ludwig and others 2001; Folke and others 2005). this symposium) (for program listings see meetings link Scientists are key participants in these organizations and at the society Web site, www.sicb.org/). they have responded to the global environmental It is no surprise that an energetics perspective degradation with the creation of several new disciplines would be of help in conservation biology because including environmental toxicology, global change stud- energy is needed to sustain life and energetics is used ies, sustainable development, and conservation biology. as an organizing perspective in many areas of Conservation biology is a nascent, applied science, biological research. The study of energy flows, sources, born in the late 1960s (Carson 1962; Ehrenfeld 1970) and sinks, across levels of biological organization

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. 1 E-mail: [email protected] Integrative and Comparative Biology, volume 46, number 6, pp. 1088–1092 doi:10.1093/icb/icl053 Advance Access publication October 18, 2006 Ó The Author 2006. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. All rights reserved. For permissions please email: [email protected]. Ecophysiology, energetics, and conservation 1089 provides useful insights into organization and func- extended droughts frogs could dehydrate even under tion. An energetics approach allows scientists to leaf litter. rank the quality of habitats or to ask how individual Harrison and colleagues presented an integrative time and energy budgets translate into population overview of the invasion of the European and African changes. Studies may be focused—such as asking honeybees, summarizing genetic, behavioral, and phy- if there is sufficient energy for reproduction—or may siological data. There are several ecotones between the be more expansive—such as examining coupled Africanized races (which now are dominant through- material and energy flows to assess tradeoffs between out the neotropics) and the European bees (which are reproduction and survival. This symposium provided dominant in the temperate zone). The authors ask a diverse and rich set of examples. The articles cover what individual genetic, behavioral, and physiological topics about reproductive energetics, migration, traits contribute to the success of each group. They feeding ecology, metabolic rates, thermoregulation, suggest that bees of strictly European origin have an and water loss. In addition, presentations covered advantage in cooler climates because of a behavioral Downloaded from https://academic.oup.com/icb/article/46/6/1088/719300 by guest on 27 September 2021 a diverse range of taxa including fence lizards, wood preference for honey over pollen that enhances their frogs, Atlantic bluefin tuna, honeybees, Monarch energy stores and increases the probability of survival butterflies, the Hawaiian po’ouli, and desert tortoises. over winter. They also suggest that increased winter Most are case studies providing linkages between survival is linked to the higher hemolymph vitel- physiology and population processes, while contribu- logenin levels found in European bees. In warmer tions from McNab and from Stevenson and climates Africanized bees are the better competitors Woods are more comparative and synthetic. because of (1) a preference for pollen over nectar, Techniques span many levels of biological organiza- which increases nutrient uptake and brood produc- tion from genetic analysis to biogeography. The tion, and (2) their larger and more energetically following section provides more detail about costly flight relative to body size, which makes them each article. better fliers and thereby increases their foraging intake, mating success and dispersal. Using distribu- tional patterns and climatic data from South America, Symposium articles Harrison and colleagues forecast that hybrid bees will In the first article, O’Conner and colleagues apply invade about 200 km further north to where biophysical models at the landscape level. The maximum January temperatures are 15–16C. approach of biophysical ecology combines microme- For many years Lincoln Brower and his colleagues terological data with thermal properties and physio- have documented one of nature’s greatest spectacles— logical data of organisms, linked by mass and thermal the migration of Monarch butterflies from Mexico to balance equations, to predict locations of animals or the United States and Canada and back. They have sources of water and food in the environment (Gates unraveled much of the behavior and ecology of these 1980). O’Conner and colleagues present 2 case studies. migratory populations, and documented several of the In the first they address questions about the impacts threats to their continued survival, especially the loss of climatic change on the canyon lizard (Sceloperous of the high elevation forests in 12 or so overwintering merriami). They use extensive field data to show that sites in the Sierra Madre Oriental Mountains of a site of intermediate elevation has the highest rate Mexico. We know that during their winter resting of reproductive success based on modeling balance period, butterflies do not feed but instead metabolize of thermal and chemical energy. The predicted fat reserves for their energy source. In this article, body temperatures of the lizards determine energy Brower and colleagues update the energetic aspects of expenditure and the thermal environment constrains migration and overwintering biology of the Monarchs, both the length of daily activity and foraging time and analyzing fat data from 17 published and unpublished thus access to food. Calculations suggest that the sources. They concluded that Monarchs are optimistic thermal sensitivity of digestive rates may be very fuelers during migration (fat levels between 0 and important. In the second example, O’Conner and 150 mg) and that they do not gain large amounts of colleagues studied the impacts of habitat alterations fat (150–250 mg) until they spend more time feeding on activity and population dynamics of the wood frog on nectar in Texas or northern Mexico, just before (Rana sylvatica). Here, biophysical models show that reaching the overwintering sites. Brower and frogs can be active in rainy periods but under drier colleagues worry that changes in nectar-producing conditions leaf litter provides a refuge from dehy- plants across the landscape will reduce migrational dration. Frogs cannot be active but they maintain success. Specifically, in the Great Plains farmers have water balance. Calculations show that during been actively reducing weeds that provide nectar. 1090 R. D. Stevenson

The analysis by Brower and colleagues implies that Comparisons of the outcome of competition between conservation of this long-distance migratory species species with high and low fecundity support his requires more emphasis on energetics and stopover conclusions. McNab used his fecundity rule to make ecology. some useful predictions for conservation biologists. Porter and colleagues apply the same biophysical Marsupial and island species generally are at a modeling approach as O’Connor and colleagues to competitive disadvantage and need isolation, whether investigate the potential distribution of the Hawaiian on islands or in otherwise protected habitats, if they po’ouli (Melamprosops phaeosoma), a bird that are to survive. inhabited Maui. This species was only discovered in Stevenson and Woods reviewed approaches to 1974 and is now thought to be extinct. Archeological judging the health of individuals, especially their records indicate that po’ouli historically lived at sea energetic status. They provided an introduction to a level but that the most recent distribution was limited very large literature (over 200 citations) on condition to elevations close to 2100 m. The thermal balance indices that have been widely used in studies of Downloaded from https://academic.oup.com/icb/article/46/6/1088/719300 by guest on 27 September 2021 model predicts that at sea level the required foraging humans, agricultural and zoo animals, and other rates (grams wet weight) are 3–4 times greater for vertebrates in the contexts of resource management, snails, the po’ouli’s historical prey, than for insects, ecology, and conservation biology. The review suggests their most recent prey. Foraging rates on both diets that specific condition indices are used because of were higher at 2100 m but the ratio remained about historical precedent rather than having been proven to the same. There was little seasonal effect in the model be a good measure for animal health. The human and calculations because the climate is relatively constant, fisheries biologists have had the most active discus- but in April and May, during the reproductive season, sions, and it would appear that more effort to foraging rates need to increase to meet reproductive standardize approaches would be prudent for the energy requirements. Porter and colleagues also scientific community. Stevenson and Woods also predicted discretionary energy for the birds. The reviewed the variety of advanced technologies used to calculations suggest that low metabolic costs at low measure body composition directly and nondestruc- elevations increase discretionary energy, and that tively. These methods are diverse and often require when the gut cannot process bulky food fast enough specialized machinery, but several hold promise for to meet the reproductive demand for energy, a diet of becoming more usable in the field and for validating snails reduces discretionary energy. These models traditional morphological metrics. Finally, Stevenson demonstrate the interrelationships of metabolism and and Woods identified 2 common views of how body water balance on activity times, diet, and the potential mass changes among animals. The cargo model for growth and reproduction. assumes that structural components of the body are McNab used allometric and comparative analyses of fixed and that changes result from taking on loads. metabolic data to make inferences about populational The dynamic models meet the more complex biologi- processes in birds and mammals. He summarized the cal reality in which “structural materials” including basic pattern that small mammals have higher digestive tissue and flight muscle mass can be metabolic rates per unit body mass and faster growth regulated to accommodate the immediate ecological rates than do large mammals. Based on analyses of the needs of an animal. residuals of metabolic rate, he suggested that animals Tracy and colleagues discussed basic feeding biology of the same body mass but with higher metabolic rate and the relationship between stress, disease, and have higher reproductive rates. When comparing population ecology of an endangered species, the eutherian with marsupial mammals, McNab argues desert tortoise, a species originally listed as threatened that basic limits of reproductive physiology in because of die-off from respiratory illness. Desert marsupials limit growth rates of young, implying tortoises occur mainly in Nevada and California where that selection for high reproductivity drives selection a variety of anthropogenic factors including habitat for increasing relative basal metabolic rate of loss from agriculture and military maneuvers, off-road eutherian mammals. Recent analyses among birds vehicles, and grazing competition from burros and suggest that they might show a similar pattern. His horses negatively impact them (Berry 1997). Four conclusion is that the species with relatively low resource acquisition hypotheses (the nutritional fecundity (large size and relatively low metabolic wisdom hypothesis, the optimal diet hypothesis, rates) are more prone to extinction. High-energy the optical digestion hypothesis, and the cost of species have flexibility in their reproductive outputs, switching hypothesis) have been used to explain whereas low-energy species are inflexible in tortoise foraging patterns. Foraging observations and theirs, making low-energy species more vulnerable. plant nutritional data are consistent with the last Ecophysiology, energetics, and conservation 1091

3 hypotheses, but the authors find no support for the helped to organize the symposium. William A. Woods nutritional wisdom hypothesis that was based on and Susan Speak provided comments on the intro- (1) balancing the calcium, phosphorus, and magne- duction. Financial support was provided by the sium acquisition for bone and shell growth or National Science Foundation (IBN-0344822). (2) avoiding excessive phosphorus because of the Conflict of interest: None declared. lack of extrarenal salt glands and the potential negative consequences of storing high concentrations in the References urine. Tracy and colleagues also discuss the immune system function of tortoises. They make the novel Berger J, Testa JW, Roffe T, Monfort SL. 1999. Conservation suggestion that at high densities (as many as 200–250 endocrinology: a noninvasive tool to understand relation- animals per hectare) aggressive behaviors can lead to ships between carnivore colonization and ecological carrying increased testosterone levels. Higher levels of testos- capacity. Conserv Biol 13(5):980–9. terone imply increased levels of corticosterone, Berry KH. 1997. The desert tortoise recovery plan: an ambitious Downloaded from https://academic.oup.com/icb/article/46/6/1088/719300 by guest on 27 September 2021 because both are regulated by the same globulins, effort to conserve biodiversity in the Mojave and Colorado deserts of the United States. Proceedings: Conservation, and increased plasma titers of corticosterone would Restoration, and Management of Tortoises and Turtles—An reduce the effectiveness of the immune system. Their International Conference. p 430–40. Available at http://www. hypothesis is that this linkage could lead to the tortoise-tracks.org/publications/berry2.html. outbreak of disease and become the driving mecha- Brown JH, Gillooly JF, Allen AP, Savage VM, West GB. 2004. nism for population cycles on the scale of decades. Toward a metabolic theory of ecology. Ecology 85(7):1771–89. Final comments Carey C. 2005. How physiological methods and concepts can be Hopefully this collection of articles, along with others useful in conservation biology. Integr Comp Biol 45:4–11. such as those by Jones and colleagues (2004) and Carson R. 1962. Silent spring. Boston: Houghton Mifflin. Wallace and colleagues (2005), will serve to stimulate Clemmons JR, Buchholz R. 1997. Behavioral approaches to conversations about the role of physiological energet- conservation in the wild. Cambridge: Cambridge University ics in conservation biology. For environmental Press. p 396. physiologists, I believe they demonstrate how their Daily GC, editor. 1997. Nature’s services: societal dependence own cutting-edge science can simultaneously inform on natural ecosystems. Washington, DC: Island Press. p 416. conservation biology. For nonphysiologists, I believe Daly HE. 1996. Beyond growth: the economics of sustainable these articles specifically demonstrate how physiolo- development. Boston: Beacon Press. p 253. gists can help explain the mechanical underpinnings Diamond J. 2005. Collapse: how societies choose to fail or of changes at the population level. The role of succeed. NY: Viking Press. p 575. energetics at the individual level and its application in Ehrenfeld D. 1970. Biological conservation. New York: Holt, ecology is currently undergoing a transformation led Rinehart and Winston. p 226. by the efforts of Brown and colleagues (2004). Their Flannery TS. 2002. The future eaters: an ecological history of the scaling relations (also see Marquet and others 2005) Australian lands and people. New York: Grove Press. p 423. provide a big-picture perspective such as the specific Folke C, Hahn T, Olsson P, Norberg J. 2005. Adaptive examples McNab presents here. These observations governance of social-ecological systems. Annu Rev Environ suggest that energetics, as a branch of conservation Resour 30:441–73 (doi: 10.1146/annurev.energy. physiology, will continue to make fruitful contribu- 30.050504.144511). tions to an understanding of how to preserve Gates DM. 1980. Biophysical ecology. New York, Heidelberg, biodiversity. Berlin: Springer-Verlag. p xxiii þ 611. Gordon M, Bartol S. 2004. Experimental approaches to Acknowledgments conservation biology. Berkeley and Los Angeles: University of California Press. p 343. I would like to thank all the participants for agreeing Hunter ML. 2001. Fundamentals of conservation biology. to apply their physiological wisdom to conservation Cambridge: Blackwell Science. 2nd edition. p 496. problems and to SICB for logistical support and Jones DR, Southwood AL, Andrews RD. 2004. Energetics of funding, especially the Division of Comparative leatherback sea turtles: a step toward conservation. In: Biochemistry and Physiology. Michael Dickinson, Gordon MS, Bartol SM, editors. Experimental approaches to the former program officer for DBP; John Wingfield, conservation biology. Berkeley: University of California SICB past president; and Catherine Loudon, former Press. p 66–82. SICB program officer, all provided guidance and Leakey R. 1996. The sixth extinction. London: Weidenfeld and encouragement for the symposium. William A. Woods Nicolson. 1092 R. D. Stevenson

Lubchenco J. 1998. Entering the century of the environment: a Soule ME, Orians GH, editors. 2001. Conservation biology: new social contract for science. Science 279:491–7. research priorities for the next decade. Washington, DC: Ludwig D. 2001. Crisis and transformation. Conserv Ecol Island Press. p 288. 5(1):11 Available at http://www.consecol.org/vol5/iss1/art11/. Stevenson RD, Tuberty SR, deFur PL, Wingfield JC. 2005. Ludwig D, Mangel M, Haddad B. 2001. Ecology, conservation, Ecophysiology and conservation: the contribution of and public policy. Annu Rev Ecol Syst 32:481–517 (doi: endocrinology and immunology—introduction to the sym- 10.1146/annurev.ecolsys.32.081501.114116). posium. Integr Comp Biol 45:1–3. Marquet PA, Quin˜ones RA, Abades S, Labra F, Tognelli M, Vitousek PM, Mooney HA, Lubchenco J, Melillo JM. 1997. Arim M, Rivadeneira M. 2005. Scaling and power-laws in Human domination of earth’s ecosystems. Science 25: ecological systems. J Exp Biol 208:1749–69. 494–9. Martin PS. 2005. Twilight of the mammoths: ice age extinctions Wallace BP, Williams CL, Paladino FV, Morreale SJ, and the rewilding of America. Berkeley and Los Angeles: Lindstrom RT, Spotila JR. 2005. Bioenergetics and diving

University of California Press. p 250. Downloaded from https://academic.oup.com/icb/article/46/6/1088/719300 by guest on 27 September 2021 activity of interesting leatherback turtles Dermochelys McMichael AJ, Kovats RS. 2000. Global environmental changes and health: approaches to assessing risks. Ecosyst Health coriacea at Parque Nacional Marino Las Baulas, Costa Rica. 6(1):59–66. J Exp Biol 208:3873–84. Meffe GK, Carroll RC. 1997. Principles of conservation biology. Wikelski M, Cooke SJ. 2006. Conservation physiology. TREE 2nd edition. Sunderland, MA: Sinauer Association. p 673. 21:38–46. Primack RB. 2006. Essentials of conservation biology. 4th Wilson EO. 2002. The future of life. New York: Alfred A. edition. Sunderland, MA: Sinauer Associates, Inc. p 530. Knopf. p 229.