Turtles and global climate change

All animals with a shell and a backbone are turtles regardless of the various colloquial names, such as tortoise and terrapin, that people have given to them. There are approximately 270 species in the world occupying all continents except Antarctica. Of these, approximately half are in need of some form of conservation action to slow their inexorable decline toward extinction. Roughly the same percentage of turtles in the United States face significant challenges to their survival (Ernst et al., 1994; Lovich, 1995). Threats to turtles include a litany of familiar factors including habitat destruction, pollution, disease, and over-exploitation by an increasingly hungry world. In the face of this onslaught, turtles face a more insidious threat: predicted global increases in temperature caused by greenhouse gases.

Figure 1. The sex of hatchling turtles, like this Barbour's map turtle, is determined by incubation temperatures in the nest. Relatively warm incubation temperatures produce females, whereas cool temperatures produce males. Barbour's map turtle is only found in the Apalachicola River and its major tributaries in Alabama, Georgia, and Florida.

The majority of the world's turtles have environmental sex determination (ESD) and this was not discovered until the early 1970's. In contrast, most familiar animals have genetic sex determination in which the sex of the offspring is determined by the genetic contribution of the father. Offspring receiving an X chromosome from the father develop into female embryos, and offspring receiving a Y chromosome from the father develop into male embryos. Because the probability of receiving either chromosome is equal at conception, sex ratios of human babies tend to be 1:1.

With ESD, the incubation temperature of the eggs during the first trimester of development determines the sex of the hatchling. Eggs incubated above a pivotal temperature of about 30° C develop into females and those below about 30° C develop into males. Another group of turtles exhibit a pattern in which females are produced at relatively warm or cool incubation temperatures while males are produced at intermediate temperatures (Ewert and Nelson, 1991).

Strange as this system might appear to humans, it is not uncommon in the animal world, with the sex of alligators and crocodiles being similarly affected by incubation temperature (although males are produced at warm temperatures). Theoretical ecologists have speculated that such a system would be expected to evolve under conditions in which the fitness of offspring varies according to their sex. If female offspring grow faster and mature earlier under warmer conditions, then mothers of offspring in those environments would benefit by producing more females. Alternatively, if male offspring are more successful in cooler environmental conditions, then mothers of offspring in those environments would benefit from production of males. If the mother cannot predict the quality of the environment for her offspring, then conventional wisdom suggests that it is better to allow the environmental conditions to "choose" the sex of her offspring. A required extension of this scenario is that incubation temperatures will be a reflection of continuing environmental conditions, thus promoting the development and survival of one sex or the other.

Figure 2. Many turtles have restricted distributions. The Bolson tortoise is found only in a small portion of the Chihuahuan Desert in Mexico. Such species are especially at risk to a global climate change due to potentially narrow environmental tolerances.

ESD might be expected to cause wide variation in sex ratios of turtles and it is true that hatchling sex ratios can range from all male in some years to all females in others. Nests constructed under the shade of shrubs and trees often produce males while those deposited in the open typically produce all females. Intermediate nests can produce mixed sex ratios. However, over long periods of time, the hatchling sex ratios of most well-studied turtle populations averages 1:1. It is important to emphasize that a variety of factors including differential mortality, differences in timing of maturity, and differential emigration/immigration of the sexes can lead to strongly biased adult sex ratios (Lovich and Gibbons, 1990). In fact, many well studied turtle populations tend to show that male-biased sex ratios are the norm for adults.

Prior to recognition of ESD in turtles, conservation biologists routinely employed high incubation temperatures in sea turtle captive propagation programs because incubation time also decreases with increasing temperature. The result was production of all females (Morreale et al., 1982). A recent proposal to use ESD as a conservation tool to produce more females of endangered turtle species has been criticized because of potentially negative impacts on population structure and mating systems (Lovich, 1996).

Recently, some scientists have suggested that global climate change has the potential to eliminate the production of male turtle offspring if mean global temperatures increase 4° C, and increases of less than 2° C may dramatically skew sex ratios (Janzen, 1994). Thus, turtles appear to be good environmental sentinels for monitoring the biotic impacts of predicted global climate change. Although the scenario of turtle extinctions as a result of climate change may seem far-fetched, other scientists believe that the disappearance of dinosaurs may be linked to ESD and rapid climate change.

Even if turtles survive the possible effects of global climate change on sex ratios, they will still have to contend with other predicted changes. As "cold-blooded", or ectothermic, animals, digestion rate, growth, reproduction and activity are all closely related to temperature. In addition, changing water levels in lakes, rivers and wetlands could have major impacts on access to suitable nest sites and habitat. Their conservative evolutionary history suggests that they will not be able to "adapt" to rapid changes. Turtles may have outlived the dinosaurs, but it remains to be seen if turtles can survive in tomorrow's world.

References

Ewert, M. A., and C. E. Nelson. 1991. Sex determination in turtles: diverse patterns and some possible adaptive values. Copeia 1991:50-69.

Janzen, F. J. 1994. Climate change and temperature-dependent sex determination in reptiles. Proc. Nat. Acad. Sci. 91:7487-7490.

Lovich, J. E. 1995. Turtles. In, pp. 118-121. Our Living Resources: a report to the Nation on the Distribution, Abundance and Health of U.S. Plants, Animals and Ecosystems. Laroe, E. T., C. E. Puckett, P. D. Doran, and M. J. Mac (eds.). National Biological Service, Washington, D.C.

Lovich, J. E. and J. W. Gibbons. 1990. Age at maturity influences adult sex ratio in the turtle Malaclemys terrapin. Oikos 59:126-134.

Lovich, J. E. 1996. Possible demographic and ecologic consequences of sex ratio manipulation in turtles. Chelonian Conservation and Biology 2:114-117.

Morreale, S. J., G. J. Ruiz, J. R. Spotila, and E. A. Standora. 1982. Temperature-dependent sex determination: current practices threaten conservation of sea turtles. Science 216:1245-1247.

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