The Society for Integrative and Comparative Biology
EcoPhysiology and Conservation: The Contribution of Endocrinology and Immunology– Introduction to the Symposium1
1 Department of Biology, University of Massachusetts Boston, Boston, Massachusetts 02125-3393
2 Department of Biology, Appalachian State University, 572 Rivers Street, Boone, North Carolina 28608
3 Environmental Stewardship Concepts, Inc. Affiliate Associate Professor, Virginia Commonwealth University, Center for Environmental Studies, 1000 West Cary Street, P.O. Box 843050, Richmond, Virginia 23284-3050
4 Department of Zoology, University of Washington, Box 351800, Seattle, Washington 98195-1800
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Climate change (Karieva et al., 1992
), habitat loss (Hughes et al., 1997) and the release of toxic chemicals (deFur et al., 1999; McLachlan, 2001) are among many factors that threaten the health of our environment and directly or indirectly contribute to biodiversity loss. The scientific disciplines of environmental toxicology and conservation biology share a common goal that may be summarized as attempting to identify, characterize and ameliorate problems or stressors that are acting to harm or destroy a species, community or ecosystem. Physiologists from both these disciplines have applied a diversity of established tools towards development of sensitive assays that recognize and quantify problems ranging from the environmental toxicity on wildlife of estrogenic agents to chronic stress on plants and animals from global warming. Now, scientists are developing new tools that identify stressed and unhealthy animals in the field based on immunological and endocrine signals. They are also using physiological methods to investigate the mechanistic underpinnings of behavioral choices that determine source and sink populations and the carrying capacity of specific habitats.
Practitioners of these two disciplines have much to offer one another and the synergy born from these interactions will undoubtedly prove fruitful in the years to come. As the scientific community continues to embrace and build upon the ideal of interdisciplinary science, increasingly sophisticated methods will be used to aid the fight against the loss of biodiversity. In the year leading up to the SICB symposium "Ecophysiology and Conservation: The Contribution of Endocrinology and Immunology" the organizers spoke at length about the need to understand population declines and to uncover the often unseen roots of the problem by examining the physiology of individuals. The goal of our symposium is to initiate a new field the organizers have termed Conservation Physiology (see Berger et al. [1999] and Clemmons and Buchholz [1997] for some earlier examples).
Conservation physiology will help establish better mechanistic and theoretical linkages across levels of biological organization and between the ecological, behavioral, and genetic studies currently of focus in conservation biology (Hunter and Sulzer, 2001; Meffe and Carroll, 1997; Primack, 2004). We commonly see environmental physiology and conservation biology used in close proximity with one another. Furthermore, reproductive physiology has enjoyed a close relationship with conservation biologists for some time, but only rarely do we think of ourselves as conservation physiologists.
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There are 26 symposium papers included in this volume. The papers illustrate a diversity of scientific approaches from a variety of species and habitats. There are examples of vertebrates and terrestrial environments, but a preponderance of the papers focus on endocrine disrupters of aquatic and marine invertebrates. The ordering of papers is somewhat arbitrary and we are sure that consumers of this volume will pick and choose as they please and make connections we have not identified. We have also included a brief synopsis of the five presentations that were not submitted for inclusion in the published record as they give the reader additional entry points into the emerging literature of conservation physiology.
In the first paper, Carey gives an overview of several subdisciplines of physiology and provides examples, mainly from studies on amphibians and coral reefs, of how these subdisciplines are being used to address conservation issues. Next, Walker et al. discuss endocrine assays of blood, urine, feces, and tissue sampled in the field to determine the physiological status of free-living animals, especially birds. Guillette provides a third example of work on vertebrates as he reviews the effects of nitrate-rich freshwater on reproduction of fish, amphibians, and alligators, and postulates mechanisms by which nitrates could alter steroidogenesis.
The next group of nine papers focuses on invertebrates. By and large, studies in conservation biology have focused on large vertebrate animals because they have large home ranges and are known to the public, making them ideal as umbrella species. Clearly charismatic megafauna play an important role in the practice of conservation. Nonetheless, invertebrate species are orders of magnitude more numerous and they hold critical positions in food webs of aquatic, marine and terrestrial ecosystems. If we wish to protect biodiversity across the planet, we must not forget the invertebrates, microbes and plants because they are all part of the infrastructure of our ecosystems.
These nine papers offer examples of endocrine and immunological disruption from four major lineages (nematodes, annelids, mollusks, crustaceans) including species that are ecologically and economically important. Oberdörster et al. investigate the neuropeptide hormone basis of the tributyltin (TBT)-induced gynopenus (imposex induction) in female snails. Zou shows how chemical pollutants disrupt hormones used by crabs for molting. Ayaki and colleagues report that in samples of male crabs from mountain streams, which are assumed to be relatively clean, 8 to 30% of the males showed evidence of female sexual morphology. Based on the hyperglycemic hormone, Chang describes the development of an enzyme-linked immunosorbent assay (ELISA) to quantify hypoxic, thermal, and salinity stresses in American and Norwegian lobsters. Sanders et al. investigate hormones involved in the development and reproduction of barnacles also using the ELISA technique. There are two papers from the Callard lab. The first by Novillo et al. describes the effects of steroids and heavy metals on gene expression in the roundworm, Caenorhabditis elegans. In the second, Won et al. study the impacts of foreign compounds on reproductive hormone receptors in freshwater mussels with the goal of finding a sensitive biomarker to document the impacts of pollution coming from a superfund site. Leblanc et al. report on the esterification of testosterone as a possible pathway by which tributyltin induces imposex in snails. Finally Krajniak reviews the large number of FMRFamide-related peptides that have been found in invertebrates and then briefly discusses possible routes of endocrine disruption in annelids.
The next six papers discuss the role of insecticides acting as endocrine disruptors because they impede the proper functioning of juvenile hormone (JH). McKenney documents the impacts of the juvenile hormone agonist (JHA) insecticide, fenoxycarb, on the growth and reproduction of estuarine shrimp, crabs and mysids. He shows that certain life stages are orders of magnitude more sensitive and the effects can be trans-generational. Tuberty and McKenney then describe experiments to elucidate the mechanism of JHA toxicity. Grass shrimp and mud crab exposed to insecticides have altered ecdysteriod levels suggesting that both ecdysteriod signaling has been interrupted, and that cross-signaling between JH and ecdysteroids occurs in these animals. In concentrations as low as 1 ppb, the insecticide methoprene is shown to be toxic to stage II lobster larvae in the paper by Walker et al. Raimondo and McKenney conducted life table response experiments to quantify the effects of methoprene concentrations on mysid survival and reproduction. These data were used to parameterize a life stage matrix model that demonstrate that the population is viable for all environmentally relevant concentrations of methoprene tested (
> 1) but population growth () decreased as the concentration of methoprene increased. Using the model species Drosophila melanogaster, Wilson details the advantages to understanding the evolution of resistance to JHA pesticides. Leight et al. report 10 years of grass shrimp population data from four sites in South Carolina. Adjacent golf courses and agricultural lands reduced population densities, shrimp size and percentage of gravid females. These impacts were ameliorated when best management practices were instituted.
The next three papers have policy implications. On several continents the declines of amphibians have been linked to a skin disease caused by chytrid fungus (see Stuart et al., 2004 for the most recent assessment). Rollins-Smith et al. examine skin secretions and find a potent set of antimicrobial peptide defenses suggesting that it is not a lack of chemical defense but some other combination of factors that is likely to be contributing to the infections.
The paper by Powell et al. demonstrates that hagfish have a seasonal reproductive cycle which provides basic life history data to manage the fishery for a species that is at risk of being overfished. Likewise, Tamone and Dutton demonstrate the utility of measuring and understanding molting hormone levels of an Alaskan crab for managing an important resource of the state's fisheries.
Baker discusses the evolution of nuclear receptors and enzymes that metabolize the associated lipophilic molecules. His perspective provides a framework for understanding the impact of xenobiotic substances on development and reproduction.
Propper surveys the literature and finds that most studies of endocrine disruptors examine estrogens that provide signals for development and reproduction. She argues that scientists should also be looking for signal disruption at the level of the pituitary and hypothalamus. She reports a new example by demonstrating that pheromone communication in red spotted newts is disrupted by pesticides.
Müller et al. document that a water soluble fraction of crude oil can disrupt pheromone communication and thus the mating swarms of annelid worms in marine environments.
The final two papers explore the role of estrogen in systems where scientists have little information. Tarrant describes what progress has been made understanding the role of estrogens in corals, where the molecule is known to be released during spawning and can affect growth and development. In an exciting paper, Fox describes how estrogen signals between plants and their symbiotic rhizobium soil bacteria can be disrupted by agricultural chemicals.
Five presenters at the symposium chose not to submit papers for publication, but their contributions to our sessions were nonetheless quite important. John Wingfield read a paper by Prof. Susumu Ishii (Waseda University) that recapped his laboratory's application of standard and original endocrine techniques towards understanding the reproduction of the Japanese Crested Ibis or Toki, a highly endangered bird. Milton Fingerman (Tulane University) reviewed the development of environmental toxicology beginning with the publication of Rachel Carson's book "Silent Spring." Peter deFur (Virginia Commonwealth University) provided an overview of the use of invertebrates to monitor the impacts of endocrine disruptors in the field. Sam Wasser (University of Washington) presented a summary of his work using non invasive techniques to monitor populations of large carnivores at the landscape scale. His novel use of dogs to locate fecal matter upon which endocrine and DNA analyses could be completed, attracted much attention (Wasser et al., 2004). Following up on his highly cited work that has caused great controversy at the EPA (Hayes et al., 2003), Tyrone Hayes (UC Berkeley) used a mixture of nine compounds, modeled after chemical use on cornfields in Nebraska, to study pesticide impacts on amphibians. While none of the chemicals except the herbicide atrazine had measurable impacts by themselves, in combination, as these chemicals are applied in agro-systems across America, they negatively affected the development, growth and metamorphosis of larval frogs.
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Since the first Earth Day in 1971, there has been a growing awareness that the trajectory of industrialized society, with all the easy living and luxuries it brings, is, nonetheless fouling our planetary nest. As this view makes its way into scientific cultures, more and more research will be devoted to environmental issues.
The papers presented here demonstrate that undertaking conservation physiological studies can be intellectually rewarding and directly impact current policy decisions—the underlying message being that there is no onus or penalty for doing applied work. We hope these papers will be the focus of graduate seminars, provide material that can be incorporated into courses and textbooks, and serve as inspiration for physiologists and others concerned about human, animal and environmental health. Indeed, the upcoming generation of environmental, evolutionary and ecological physiologists, those born after the first Earth Day, seems especially aware of conservation issues.
The perspective and examples offered here, are, of course, only one small piece of the much larger sustainability puzzle. For those wanting an entry point into the wider conservation literature, the textbooks cited above are a good starting point and "Our Stolen Future" by Colburn et al. (1996) sounds the alarm for endocrine disruptors. In addition, we can recommend the popular books "Guns, Germs and Steel" and "Collapse" by Jared Diamond. As physiologists and environmentalists, we can all take inspiration from Diamond, who as one of the most accomplished physiologists and ecologists of his generation, has now turned his attention to providing a broad historical overview of the relationship between humans and their environment.
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ACKNOWLEDGMENTS |
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The organizers would like to thank SICB for logistical support and funding, especially the Divisions of Comparative Endocrinology, Invertebrate Zoology, and Developmental and Cell Biology. Miles Orchinik, program officer for DCE, provided early support for our symposium and Stacia Sower, SICB Program Officer, guided us through the process for what turned out to be an unusually large symposium. Financial support from the National Science Foundation (IBN-0344822), the U.S. Environmental Protection Agency, and the Crustacean Society covered the costs of the symposium. A CD-ROM containing all symposium abstracts, author contact information, and PowerpointTM presentations is available from SICB (webmaster@sicb.org).
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1 From the Symposium EcoPhysiology and Conservation: The Contribution of Endocrinology and Immunology presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 5–9 January 2004, at New Orleans, Louisiana.
2 E-mail: robert.stevenson{at}umb.edu
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References |
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Berger, J., J. W. Testa, T. Roffe, and S. L. Monfort. 1999. Conservation endocrinology: A noninvasive tool to understand relationships between carnivore colonization and ecological carrying capacity. Conserv. Biol, 13:980-989.[CrossRef]
Clemmons, J. R., and R. Buchholz. 1997. Behavioral approaches to conservation in the wild. Cambridge University Press, Cambridge.
Colborn, T., D. Dumanoski, and J. P. Myers. 1996. Our stolen future: are we threatening our fertility, intelligence, and survival?—a scientific detective story. Dutton, NY.
deFur, P., M. Crane, C. Ingersoll, and L. Tattersfield. 1999. Endocrine Disruption in Invertebrates: Endocrinology, Testing, and Assessment. Workshop Dec 2–15 1998; Noordwijkerhout, The Netherlands. Society of Environmental Toxicology and Chemistry (SETAC), Pensacola, Florida.
Hayes, T., K. Haston, M. Tsui, A. Hoang, C. Haeffele, and A. Vonk. 2003. Atrazine-induced hermaphroditism at 0.1 ppb in American leopard frogs (Rana pipiens): laboratory and field evidence. Environ. Health Perspect, 111:568-75.[Web of Science][Medline]
Hughes, J., B. G. C. Daily, and P. R. Ehrlich. 1997. Population diversity: Its extent and extinction. Science, 278:689-692.
Hunter, M. L., and A. Sulzer. 2001. Fundamentals of conservation biology, 2nd ed. Blackwell Science, Malden, MA.
Kareiva, P. M., J. G. Kingsolver, and R. B. Huey. 1992. Biotic interactions and global change. Sinauer Associates, Sunderland, MA.
McLachlan, J. 2001. Environmental signaling: What embryos and evolution teach us about endocrine disrupting chemicals. Endocrine Rev, 22:319-341.
Meffe, G. K., and C. R. Carroll. 1997. Principles of conservation biology, 2nd ed. Sinauer Associates, Sunderland, MA.
Primack, R. B. 2004. Essentials of conservation biology, 3rd ed. Sinauer Associates, Sunderland, MA.
Stuart, S. N., J. S. Chanson, N. A. Cox, B. E. Young, A S. L. Rodrigues, D. L. Fischman, and R. W. Waller. 2004. Status and trends of amphibian declines and extinctions worldwide. Science, 306:1783-1786.
Wasser, S. K., B. Davenport, E. R. Ramage, K. E. Hunt, M. Parker, C. Clarke, and G. Stenhouse. 2004. Scat detection dogs in wildlife research and management: Applications to grizzly and black bears in the Yellowhead Ecosystem, Alberta, Canada. Can. J. Zool, 82:475-492.[CrossRef]
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