The BIOLOGY of SEA TURTLES (Volume II) - CHAPTER 6

6 Physiological and Genetic Responses to Environmental Stress Sarah L. Milton and Peter L. Lutz CONTENTS 6.1 What Is Stress? ...........................................................................................163 6.2 Why Sea Turtles Are at Special Risk .........................................................164 6.3 Stressors ......................................................................................................166 6.3.1 Temperature .....................................................................................166 6.3.1.1 Hypothermia ....................................................................166 6.3.1.2 Hyperthermia ...................................................................169 6.3.2 Chemical Pollutants ........................................................................169 6.3.2.1 Bioaccumulation ..............................................................170 6.3.2.2 Effects ..............................................................................171 6.3.3 Eutrophication and Algal Blooms ..................................................173 6.3.4 Disease ............................................................................................175 6.3.4.1 Trematodes .......................................................................175 6.3.4.2 GTFP ................................................................................176 6.3.5 Effects of Environmental Stressors on Hatchlings ........................177 6.3.5.1 Emergence Stress and Lactate .........................................178 6.3.5.2 Temperature .....................................................................180 6.3.5.3 Frenzy Swimming ...........................................................180 6.4 Responses to Stress .....................................................................................182 6.4.1 Neuroendocrine Responses (Stress Hormones) .............................182 6.4.2 Immunological Responses ..............................................................184 6.4.3 Gene Response, Molecular Biomarkers, and the Measurement of Stress: Potential Tools for the Future ........................................185 References ............................................................................................................187 6.1 WHAT IS STRESS? Many people are uncomfortable with the term stress in animal biology. The root of the difficulty lies in the common usage of the word and its richness of meanings 163 © 2003 CRC Press LLC 164 The Biology of Sea Turtles, Vol. II that bedevil an exact scientific definition. In biology, the term embraces psychology to biomechanics, and it is only in the latter that it is used in the precise and quantitative terms of Hooke’s law, where stress (the deforming force) is proportional to strain (the deformation). For the rest there is no agreement about whether stress refers to external or internal factors, what it consists of, or how it can be measured. Nevertheless, the fact that the concept is still widely used in biology, from the molecular to ecosystem level, indicates its utility and its necessity (Bonga, 1997). Perhaps the term should be used only in combination with the causal factor (i.e., crowding stress, temperature stress), with the concept that there is an (identified) tolerance range for the external factor within which the individual or community copes by means of adaptive responses, but that outside this range there is a quanti-tative or qualitative break in the (described) response. The adaptive function of the stress response is to accommodate changes in the environment (stressors) by adjustments in behavior and/or changes in physiology. How-ever, an excessive exposure to the stressor, in either intensity or duration, will result in dysfunctional debilitating responses. Environmental conditions to which an animal cannot adapt lead to both transient and relatively long-term physiological changes. Such changes often contribute to the development of disease, especially if the organism is exposed at the same time to potentially pathogenic stimuli. Various stressors, however, do not all produce the same outcomes; effects will depend on the quality, quantity, and duration of the stressor; the temporal relationship between the exposure to a stressor and the introduction of pathogenic stimuli; environmental conditions; and a variety of host factors (age, species, gender, etc.) (Ader and Cohen, 1993). This chapter presents an overview of the relationship between sea turtles and some of the more important stressful aspects of their environment. Because stress is such a broad topic, many aspects of stress have been treated in previous chapters and elsewhere in this volume (see Lutcavage et al., 1997; George, 1997; Epperly, Chapter 13; and Herbst and Jacobson, Chapter 15, this volume). This chapter reviews a few environmental stressors of particular significance to sea turtles: temperature, chemical pollutants (organic and inorganic) and habitat degradation, and the sea turtle’s physiological and potential genetic responses are discussed. Distinct envi- ronmental stressors affect the terrestrial nest and hatchlings, and are discussed separately from the other (oceanic) life stages. 6.2 WHY SEA TURTLES ARE AT SPECIAL RISK Sea turtles naturally encounter a wide variety of stressors, both natural and anthropo-genic, including environmental factors (salinity, pollution, temperature), physiological factors (hypoxia, acid–base imbalance, nutritional status), physical factors (trauma), and biological factors (toxic blooms, parasite burden, disease). Although they are physically robust and able to accommodate severe physical damage, sea turtles appear to be surprisingly susceptible to biological and chemical insults (Lutcavage and Lutz, 1997). For example, in the green sea turtle even a short exposure to crude oil shuts down the salt gland, produces dysplasia of the epidermal epithelium, and destroys the cellular organization of the skin layers, thus opening routes for infection (Lutcavage et al., 1995). The effects of many stressors, however, are likely to be less obvious, as in the (unknown) long-term effects of toxin exposure and bioaccumulation. © 2003 CRC Press LLC Physiological and Genetic Responses to Environmental Stress 165 Because sea turtles are long-lived animals, the cumulative effect of various stressors is likely to be great. Because sea turtles spend discrete portions of their life in a variety of marine habitats, they are vulnerable at multiple life stages: as eggs on the beach, in the open ocean gyres, as juveniles in nearshore waters, and as adults migrating between feeding and nesting grounds. Thus, turtles may be exposed to a greater variety of environmental stressors than less migratory animals, with presumably different vulnerabilities at each stage. However, their exposure to a particular stressor may be limited by the length of that life history stage. For example, fibropapilloma disease appears to affect primarily juvenile green turtles of 40–90 cm carapace length (Ehrhart, 1991), but is rare in nesting adults. Exposure to weathered oil has significant health effects on swimming turtles (Lutcavage et al., 1995), but in one study demonstrated little impact on egg survival. Fresh oil, on the other hand, significantly affected egg survival (Fritts and McGehee, 1981). Vulnerability to certain stressors will also vary by ecological niche, i.e., polychlorobiphenyl (PCB) and dichlorodiphenyldichloroethylene (DDE) accumu-lations are consistently higher in loggerhead turtle tissues and eggs than in those of green turtles (George, 1997; Clark and Krynitsky, 1980), presumably because of dietary differences. Clark and Krynitsky (1980) also reported that DDE and PCB loads in both loggerhead and green turtle eggs were significantly lower than in bird eggs taken from the same location (Merritt Island, FL) and lower than contaminant levels in eggs from Everglades (FL) crocodiles. They speculated that adult turtles nesting on Merritt Island lived and fed in areas less contaminated than did the residential bird and Everglades crocodile populations. Natural stressors include thermal stress (heat stress, cold stunning), seasonal or temperature-related changes in immune function, and the presence of disease, par-asites, or epiphytes. Even these natural physiological stressors may, of course, be impacted or exaggerated by anthropogenic factors. For example, physiological responses to natural diving are significantly different from those produced by the forced submergence of trawl entanglement (Lutcavage et al., 1997), and animals with a depressed immune system related to pollutant levels would be more vulnerable to parasites and disease. Anthropogenic stressors may have either direct or indirect impacts on sea turtle health. Direct impacts include such problems as oil spills, latex or plastic ingestion, fishing line entanglement, and the presence of persistent pesticides, hormone dis-rupting pollutants, and heavy metals. Indirect effects occur primarily through habitat degradation: eutrophication, the contribution of pollutants to toxic algal blooms, and collapse of the food web. Inappropriate sea turtle behavior can put them at particular risk. For example, it appears that unlike marine mammals, adult sea turtles show no avoidance behavior when they encounter an oil slick (Odell and MacMurray, 1986); they also indiscrim-inately ingest tar balls and plastics (Lutz, 1990), and hatchlings congregate in ocean rift zones where floating debris concentrate. Their breathing pattern of large tidal volumes and rapid inhalation before diving will result in the most direct and effective exposure to petroleum vapors (the most toxic part of oil spills), as well as biotoxin aerosols resulting from dinoflagellate blooms. © 2003 CRC Press LLC 166 The Biology of Sea Turtles, Vol. II Sea turtles are at particular risk from the stresses presented by degraded tropical coastal marine environments. Indeed, the high public awareness of sea turtles is such that they can serve as effective sentinels of tropical coastal marine ecosystem health (Aguirre and Lutz, in press). 6.3 STRESSORS This review selects some of the most critical identified natural and anthropogenic stressors of sea turtle physiology, while omitting some (oil, nesting, capture stress) that have been previously reviewed (see Lutz and Musick, 1997). 6.3.1 TEMPERATURE Both high and low temperatures are known to negatively impact sea turtle physiology, affecting feeding behavior, acid–base and ion balance, and stress hormone levels. 6.3.1.1 Hypothermia Temperature has a marked effect on the feeding rates of sea turtles. At 20C Kemp’s ridley turtles decreased food consumption to 50% of control levels (at 26°C), and a similar reduction in food intake was found in green turtles at 15°C (Moon et al., 1997). Below 15C both species ceased feeding. Interestingly, Moon et al. (1997) found that green and Kemp’s ridley turtles’ swimming behavior differed as temper-atures decreased. When temperatures dropped below 20°C green turtles reduced swimming activity, but at these temperatures the ridleys became very agitated. Below 15°C both species became semidormant, hardly moving and only coming to the surface at intervals of up to 3 h to breathe. Field evidence supports these findings. During cold temperatures in winter, loggerhead turtles in Tunisian waters reduce overall activity even though they continue to forage (Laurent and Lescure, 1994). Temperature also profoundly influences the physiology of sea turtles. In ridleys and greens, both venous blood partial pressure of oxygen (pO2) and partial pressure of carbon dioxide (pCO2) decreased with temperature (Moon et al., 1997), whereas venous blood pH increased. Similar temperature-dependent changes in blood pH, pCO2, and pO2 have been widely found in other reptiles, including loggerhead sea turtles (Lutz et al., 1989). Temperature-related adjustments of blood pH in the loggerhead appeared to be managed at both the lung and tissue (ion exchange) levels (Lutz et al., 1989). In both wild (Lutz and Dunbar-Cooper, 1987) and captive (Lutz et al., 1989) loggerheads, plasma potassium increased with temperature, which may be related to cellular-mediated adjustments in blood pH. Excessively low tempera-tures can also interfere with physiological functioning. For example, there was an abrupt failure in pH homeostasis and a sharp increase in blood lactate at temperatures below 15°C in the loggerhead (Lutz et al., 1989). At 10°C the loggerheads were lethargic and “floated” (Lutz, personal observation). Such positive buoyancy is probably due to cessation of intestinal mobility and the collection of ferment gases and is commonly observed in cold stunning. © 2003 CRC Press LLC Physiological and Genetic Responses to Environmental Stress 167 Unlike certain freshwater turtles, which overwinter in frozen ponds and thus withstand months submerged in near-freezing water (Jackson, 2000), sea turtles (with the exception of leatherbacks) trapped in cold waters (below 8–10C) may become lethargic and buoyant, floating at the surface. This condition is defined as cold stunning (Schwartz, 1978). Salt gland function may be impaired in cold-stunned animals, as evidenced by increased blood concentrations of sodium, potassium, chlorine, calcium, magnesium, and phosphorus (George, 1997; Carminati et al., 1994). Affected animals may not eat for days or even weeks prior to cold stunning, increasing overall physiological stress (Morreale et al., 1992). However, it is likely that it is the rate of cooling below 15C that evokes cold stunning rather than the temperature per se. Satellite tracking studies of ocean migrating Kemp’s ridley and loggerhead turtles indicate that they remain active in water temperatures as low as 6C (Keinath, 1993). Sea turtles that overwinter in inshore waters are most suscep-tible to cold-stunning because temperature changes are most rapid in shallow water, especially in semienclosed areas such as lagoons (Witherington and Ehrhart, 1989). As temperatures drop below 5–6C, death rates become significant, because the animals can no longer swim or dive, become vulnerable to predators, and may wash up onshore, where they are exposed to even colder temperatures. As with other physiological stressors, cold stunning can affect specific popula-tions of sea turtles more than others. For example, although cold-stunning events occur in Florida as well as in northern waters, the extended exposure to frigid waters experienced by turtles off New England or New York results in much higher mortality rates. Morreale et al. (1992) reported overall mortality rates as high as 94% over three winters in New York, whereas Witherington and Ehrhart (1989) reported only 10% mortality for cold-stunned turtles in a Florida estuary. Habitat utilization is also a significant factor in differential mortality during cold-stun events. The waters off New York and New England appear to be an important habitat for juvenile Kemp’s ridley turtles, with the result that a large percentage of identified cold-stunned animals are of this species (Figure 6.1). Of the 277 total sea turtles found on Cape Cod, MA, during the 1999–2000 winter season, 79% were Kemp’s ridley turtles, 19% loggerheads, and 2% greens (Still et al., in press). During the 1985–1986 winter, 79% of the turtles retrieved on Long Island (NY) were Kemp’s ridleys (Meylan and Sadove, 1986). Indeed, Kemp’s ridleys have consistently made up more than 50% of the cold-stunned turtles found along Cape Cod for the past 20 winters, and 67–80% of cold-stunned turtles found off Long Island over a 3-year period were Kemp’s ridleys (Morreale et al., 1992). By contrast, in five significant stunning events over a 9-year period in the Indian River Lagoon (FL), 73% of 467 recovered turtles were greens (Figure 6.1), 26% were loggerheads, but less than 1% (2 animals) were Kemp’s ridleys (Witherington and Ehrhart, 1989). Size is also an important factor in susceptibility to cold-stun events, because juveniles are the primary life history stage affected. The majority of Kemp’s ridleys retrieved off Cape Cod in the 1999–2000 season were in the 25.0–29.9 cm curved carapace length (CCL) size class, as were many greens. Similarly, Morreale et al. (1992) reported a mean straight carapace length (SCL) of 29.4 cm for Lepidochelys kempii and 32.7 cm for Chelonia mydas for cold-stunned turtles collected off Long © 2003 CRC Press LLC ... - tailieumienphi.vn