© 2002 by The Society for Integrative and Comparative Biology
Taking Physiology to the Field: An Introduction to the Symposium1
1 Department of Biological Sciences, Wright State University, Dayton, Ohio 45435
2 Mitrani Department of Desert Ecology, Blaustein Institute for Desert Research, Ben-Gurion University of the Negev, Midreshet Ben-Gurion, 84990 Israel
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INTRODUCTION |
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Over the past decades, comparative and ecological physiologists have successfully described many wondrous ways in which organisms are specialized for life in a variety of habitats. However, most of these investigations were done in the laboratory, where both animals and their environments are under control and manipulable.
An important focus of contemporary comparative and ecological physiology is to explore physiological function under natural conditions with ecological context in mind. The impetus for this has come from two directions. First, advances in technology and methodology have provided opportunities for addressing an ever-expanding array of physiological questions in wild animals. Second, conceptual advances have inspired new sorts of questions, and an understanding of physiology in the field continues to contribute to the deepening interplay between physiologists, ecologists, and evolutionary biologists.
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METHODOLOGICAL ADVANCES |
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Methodological advances include both the development of new technologies and the application of existing approaches to new questions. Implanted transmitters that relay information about body temperature and heart rate have been used for many years in free-living animals. However, these approaches continue to be refined (e.g., Froget et al., 2001
) and to offer fresh insights and applications, such as documentation of regional heterothermy (Bevan et al., 1997). The increasing sophistication of data storage and transmission systems has contributed importantly to these advances. In some cases, animals can carry with them physiological sensors that record to on-board data storage modules. Thus, for example, it has been possible to record data on cardiovascular performance, respiration, and body temperature during diving in free-ranging pinnipeds (Andrews, 1998). Furthermore, data can now be transmitted from an animal to an orbiting satellite, thereby allowing data capture over periods of months while the animals traverse thousands of miles (see Fedak, in this symposium for a discussion of the opportunities and constraints of such systems). Miniaturization of transmitters and data loggers also permits investigation of previously unexplored variables, such as the patterns of exhaled temperature and respiratory and cutaneous evaporative water loss in free-flying pigeons (Michaeli and Pinshow, 2001). These measures can be integrated with more "traditional" methodologies such as careful mass balance studies (Giladi and Pinshow, 1999) to provide a detailed evaluation of homeostatic regulation in the field.
The development of miniature, implantable chemical delivery systems has contributed to the evaluation of a number of regulatory systems in free-living animals. On the one hand, such systems can be used to evaluate normal physiology under natural conditions. For example, Goldstein and Rothschild (1993) were able to measure urine flow rate and glomerular filtration rate in free-living song sparrows, using osmotic minipumps to infuse a marker of renal function. On the other hand, implants may be used to accomplish "phenotypic engineering," in which physiological condition is manipulated as a means to evaluate the consequences for physiology and behavior. For example, studies using Silastic® implants to introduce sex steroids into birds during various phases of their annual cycle (see Casto et al., 2001; Wingfield and Soma, this symposium) provide insight into the relation between endocrine status, social role, and reproductive output.
Botanists have made extensive use of stable isotopes to trace material fluxes through plants. Although animal physiological ecologists have made use of the doubly labeled water technique in the field for 30 years, only recently have other uses of stable isotopes been gaining in application (see Hatch et al., in this symposium, and Gannes et al., 1997). By tracing the abundance of naturally occurring isotopes of carbon, nitrogen, and hydrogen, and potentially by manipulating these abundances to create a traceable marker, one can track a variety of materials, including water, metabolic fuels and other nutrients, through ecosystems (Wolf and Martinez del Rio, 2000). Moreover, the transfer of these materials between trophic levels can potentially be evaluated over time spans ranging from hours to months. These data can be coupled with improved methods for assessing "physiological status," including such variables as lean mass, fat content, bone mass, and immune competence (for examples, see papers in this symposium by Grasman, Henen, and Piersma). Together, these approaches are beginning to add both qualitatively and quantitatively to the integration of physiological processes, such as digestion and water loss, with ecological processes, such as foraging strategies and energy flow.
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In addition to technological advances, conceptual strides also contribute to an expanding interest in exploring physiology in the field. We note two of these in particular. The first is the recognition in recent years that physiological processes can be, indeed need be, explored within a framework of phylogenetic history. That is, species may not just be independent data points, but rather they share traits through their evolutionary heritage (Garland and Adolph, 1994
). The statistical methods to account for these patterns of evolutionary relationship have been applied to a variety of sorts of physiological data, and can enhance our interpretation of those data. Thus, conventional statistical analysis based on analysis of variance models suggests that birds from arid environments have lower water fluxes in the field than do birds from mesic environments, but analysis using phylogenetically independent contrasts questions whether this is truly the case (Tieleman and Williams, 2000).
A second direction for conceptual progress has been an increased focus on individual variation in physiology. What Bennett (1987) called "the tyranny of the golden mean," in which we focus on average performance and ignore variability, has been applied equally to field and laboratory studies. Yet individuals undoubtedly differ in their physiological capacities and in the priorities with which various physiological responses are initiated. Moreover, a physiological response is only one means by which an animal may react to its environment, and studies in the laboratory may substantially constrain the complementary repertoire of behavioral options (Bartholomew, 1966). Careful observation of individual animals, and correlation of physiological condition with behavior (see Vleck and Vleck, this symposium), can provide great insight into the interplay between physiology and ecology under natural conditions. Individual variability is also, of course, the stuff of natural selection. The demonstration that variation in physiological capacity is a determinant of fitness in wild populations represents a significant challenge (see, e.g., Clobert et al., 2000), but one that can provide a fruitful joint objective of physiologists and evolutionary biologists.
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The research reported in this symposium demonstrates our increasing ability to monitor physiology within the context of both natural environmental variability and variability among individual organisms, amidst the full suite of behavioral options available to the organism in question (e.g. Thomas et al., 2001
). In so doing, measures of physiological variables continue to offer fresh insights into other fields of zoological research, and so bring about new intercourse between physiological-ecology and other disciplines.
Integrative physiological studies using modern techniques and approaches improve our basic understanding of physiology, including mechanisms of response and prioritization of interacting homeostatic systems. Such studies enhance our interpretation of ecological relationships, providing a quantitative basis for understanding an animal's decisions about foraging, migration, reproduction, and other life history characteristics and furthermore offer insights into pathways of adaptation and determinants of fitness to evolutionary biologists. It seems likely that as concerns continue over potential impacts of changing global climate on ecological and evolutionary processes (e.g., Lovegrove, 2000), the understanding of physiological responses under field conditions will contribute importantly to both theoretical discussion and practical application.
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FOOTNOTES |
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1 From the Symposium Taking Physiology to the Field: Advances in Investigating Physiological Function in Free-Living Vertebrates presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 3–7 January 2001, at Chicago, Illinois.
2 E-mail: david.goldstein{at}wright.edu
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Bartholomew, G. A. 1966. Interaction of physiology and behavior under natural conditions. In R. I. Bowman (ed.), The Galapagos, pp. 39–45. University of California Press, city??
Bennett, A. F. 1987. Interindividual variability: An underutilized resource. In M. Feder et al. (eds.), New directions in ecological physiology, pp. 147–169. Cambridge University Press, Cambridge.
Bevan, R., I. Boyd, P. Butler, K. Reid, A Woakes, and J Croxall. 1997. Heart rates and abdominal temperatures of free-ranging South Georgian shags, Phalacrocorax georgianus. J. Exp. Biol, 200:661-675.[Abstract]
Casto, J. M., V. Nolan, Jr., and E. D. Ketterson. 2001. Steroid hormones and immune function: Experimental studies in wild and captive dark-eyed juncos (Junco hyemalis). Am. Nat, 157:408-420.[CrossRef]
Clobert, J., A. Oppliger, G. Sorci, B. Ernande, J. G. Swallow, and T. Garland, Jr. 2000. Trade-offs in phenotypic traits: Endurance at birth, growth, survival, predation and susceptibility to parasitism in a lizard, Lacerta vivipara. Funct. Ecol, 14:675-684.[CrossRef]
Froget, G., P. J. Butler, Y. Handrich, and A. J. Woakes. 2001. Heart rate as an indicator of oxygen consumption: Influence of body condition in the king penguin. J. Exp. Biol, 204:2133-2144.
Gannes, L. Z., D. M. O'Brien, and C. Martínez del Rio. 1997. Stable isotopes in animal ecology: Assumptions, caveats, and a call for more laboratory experiments. Ecology, 78:(4)1271-1276.[CrossRef]
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Goldstein, D. L., and E. L. Rothschild. 1993. Daily rhythms in rates of glomerular filtration and cloacal excretion in captive and wild song sparrows (Melospiza melodia). Physiol. Zool, 66:708-719.
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Thomas, D. W., J. Blondel, P. Perret, M. M. Lambrechts, and J. R. Speakman. 2001. Energetic and fitness costs of mismatching resource supply and demand in seasonally breeding birds. Science, 291:2598-2600.
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