I should like to thank the editor of the Endangered Species UPDATE for the opportunity to comment on the article "Endocrine Disruption: Hidden Threats to Wildlife" by Michael Smolen and Theo Colborn of the World Wildlife Fund in the September/October 1997 issue. The conclusion of this article is that a very wide range of wildlife species is now threatened by a diverse assortment of synthetic chemicals in the environment. Their effects are initially hidden but in the longer term reproductive abnormalities and disruptions in other essential life processes result from the "stealth damage caused by interference with endogenous messengers" (Smolen and Colborn 1997:10).
Thirty years ago, this statement would have been at least partly true, with an important qualification: the effects at that time were hardly hidden. Peregrine falcons (Falco peregrinus) had become extinct as a breeding species over half of the country. Bald eagle (Haliaeetus leucocephalus) populations were rapidly declining. The state bird of Louisiana, the brown pelican (Pelecanus occidentalis), once numerous, was no longer breeding in the delta of the Mississippi. Everywhere, fish-eating birds were in trouble. A process of extinction, without precedent in evolutionary history, was threatening the integrity of ecosystems.
In 1968, six years after Silent Spring (Carson 1962), there was as yet little control over the application of vast quantities of the chlorinated hydrocarbon pesticides then still in widespread use; polychlorinated biphenyls (PCBs), not yet known to be environmental contaminants of greater significance than the biocides, could be purchased in railway-car amounts for incorporation into a diversity of industrial products.
In that year, the spraying programs to "eradicate" Dutch elm disease in Milwaukee were continuing to kill countless numbers of songbirds, prompting a group of citizens to petition the Wisconsin Department of Natural Resources. The Hearing Examiner ruled that he had no legal authority to stop the spraying program, but pointed out that a law on the Wisconsin books prohibited the use in that state of any substance that, as a consequence of its use, entered the waters of the state and caused harm to wildlife. The stage was set for a confrontation between the environmentalists, represented by the Environmental Defense Fund, and the pesticide industry. In less than a decade the uses of the major chlorinated hydrocarbon pesticides had ended in the USA and most of the other industrialized countries; PCBs were no longer manufactured in North America and a process, inevitably imperfect, to prevent future 'PCBs' (chemicals that are persistent, mobile in the environment, with unpredictable biological activity) was implemented by the Toxic Substances Control Act.
Recovery of the wildlife populations affected by these contaminants, although dramatic for peregrine falcons and most populations of the bald eagle, has not happened overnight, and is not yet complete. Environmental contamination by the persistent biocides, although declining, continues to affect populations of sensitive species. How then are the remnant 'old' effects, those caused by the chemicals whose uses ended a generation or more ago, to be distinguished from the 'new' "hidden threats" that are the subject of the article by Smolen and Colborn
The example of a 'new' threat that is discussed in greatest detail is the continuing lower productivity of bald eagles nesting on the shores of the Great Lakes, even though "Eggshell thinning and outright mortality are no longer visible" (Smolen and Colborn 1997:6). The balance of the scientific evidence, however, indicates that this is a remnant 'old' effect; in part, the evidence comes from a population of bald eagles reintroduced to Santa Catalina Island in southern California that continues to suffer from severe effects of contamination by DDE, the environmental derivative of DDT that has been responsible for all, or almost all, of the eggshell thinning documented since 1946. The argument derives from multiple sources.
1) The bald eagle was the first species for which an effect at the population level induced by an environmental contaminant was documented. A retired Canadian banker, Charles Broley from Winnipeg, began to band nestling bald eagles in Florida in 1939. By 1946, he had reached 150 young eagles a year. But in 1947 the number of young eagles dropped sharply and continued to drop in the following years (Broley 1958).
2) Beginning abruptly in 1947, the weights of eggshells and the eggshell thickness of Florida bald eagles dropped by 15-19 % (Hickey and Anderson 1968; Anderson and Hickey 1972), coinciding with the sudden depression of productivity observed by Broley.
3) The eggshell weight and the shell thicknesses of other species of raptorial birds also declined abruptly in 1947 in other areas of North America (Hickey and Anderson 1968; Anderson and Hickey 1972) and in Britain (Ratcliffe 1967).
4) Like the brown pelican and the prairie falcon (Falco mexicanus), the bald eagle is very sensitive to DDE. Reproduction invariably fails whenever concentrations in the eggs exceed a few parts per million, whether the relationship is expressed logarithmically with a pronounced effect even at the lowest levels of DDE (Wiemeyer et al. 1984, 1993) or by a model that assumes a minimum effect at the lowest levels with a sharp decrease above a threshold (Nisbet 1989).
5) Unlike species such as the brown pelican, whose eggs break above a critical level of thinning thereby accounting for a major portion if not all of the reproductive failures, productivity of bald eagles is, unexpectedly, not related to shell thinning, but is nevertheless strongly related to DDE concentrations (Nisbet 1989). This DDE effect on reproduction is therefore distinct from eggshell thinning.
6) Bald eagles disappeared from the southern California islands during the 1950s (Kiff 1980) when wastes from a DDT factory in Los Angeles, containing many tons of DDT, were taken in barges to sea throughout the 1950s for offshore dumping. Following recovery of the brown pelicans in the mid-1970s, they were reintroduced to Santa Catalina Island beginning in 1980 by David Garcelon of the Institute for Wildlife Studies. The first egg appeared in 1987, but it broke shortly after being laid. Shell fragments with portions of the yolk were retrieved for analysis in my laboratory. The California Bald Eagle Working Team was to meet the following week on Santa Catalina Island; there was a certain urgency to report both the contaminant levels and the degree of shell thinning. On a lipid basis DDE concentrations were five times higher than the threshold level of reproduction effects. On the day of the meeting, Sam Sumida of the Western Foundation of Vertebrate Zoology, measured shell thickness. It was almost normal. We had no explanation why the egg had broken. In 1988 a second female produced an egg which also broke in the nest almost immediately after being laid. Its shell thickness was also almost normal, and the DDE levels were high (Garcelon et al. 1989; Jenkins et al. 1994).
7) Thereafter eggs have been collected as soon as possible for artificial incubation, initially at the Santa Cruz Predatory Bird Group and currently at the San Francisco Zoo. Only if exhaustive measures are taken to control the rate of water loss from the egg is the embryo able to survive. David Garcelon reports that one of this year's breeding males was hatched in 1992 from a deformed egg artificially incubated by the Santa Cruz Predatory Bird Group in 1992 while his parents incubated a dummy egg on Santa Catalina Island. Like his parents before him, he and his mate incubated dummy eggs after their own deformed eggs were removed. This year's chicks, however, died at the pipping stage, despite all the efforts of the zoo personnel to nurse them through the hatching process (D.K. Garcelon, personal communication).
8) Scanning electron microscopy detected small areas of gross structural abnormalities of the eggshell (Figures 1 and 2), associated with gross changes of the organic crystallization sites on the eggshell membrane (Bland 1990; Risebrough 1993). The rapid rate of water loss and the embryonic deaths were thereby explained; these structural abnormalities could also have produced a weakening of the eggshell that resulted in breakage in the absence of any significant thinning.
9) There are no DDE effects on the structure and thickness of eggshells of many bird species. Particularly if the primary effect of DDE is on the organic crystallization matrices, a 'disruption' if any of an endocrine function could be a secondary effect. Moreover, virtually any metabolic function is related one way or another to an endocrine activity. In this context therefore, the use of the term 'endocrine disruption' in the absence of any definitive demonstration of the cause(s) of eggshell thinning and structural abnormalities would not appear to be justified.
10) The number of young bald eagles fledged per breeding pair in the Great Lakes and along rivers supporting runs of anadromous fish increased from 0.23 in 1977 to 0.87 in 1993 (Bowerman 1993). A goal of 1.0 young fledged/occupied nest has been established by the Northern States Bald Eagle Recovery Plan (Grier et al. 1983). This recovery is remarkable, particularly to those of us who were bird-watching on the shores of the Great Lakes in the 1950s and who followed the later population declines of bald eagles with dismay and alarm. Smolen and Colborn, however, look at the remaining 13% of the unfilled glass and predict catastrophe.
It is not therefore necessary to evoke a hypothesis that new, even more insidious, chemicals with "hidden" effects will threaten the future survival of the national emblem. The low production of young eagles in Florida beginning in 1947, the continuing lower production on the shores of the Great Lakes, and the absence of any natural reproduction in the marine environment of southern California can all be considered as 'old' effects. Until DDE contamination drops further in the Great Lakes, depression of bald eagle reproduction will continue. As long as the Institute for Wildlife Studies is able to continue its program in southern California, the bald eagle population will be maintainedand continue to fly free in the Channel Islandsuntil the DDE contamination finally clears. Meanwhile, the defective eggshells will continue to provide a living example of an unpredictable deleterious effect of an environmental contaminant.
Each of the other 'new' effects cited by Smolen and Colborn deserves a comparable, detailed comment for which there is no space in this issue of the Endangered Species UPDATE. Certainly, something happened to the sexuality of the alligators of Lake Apopka in Florida; was this, however, an 'early warning' of a new universal environmental threat or a unique, local event? A possibility that the effects were local only comes from a recent report (Semenza et al. 1997) that the nematicide DBCP had been manufactured at a nearby pesticide manufacturing facility. Like the dieldrin and related biocides from a factory on the Rhine that killed seabirds along the Netherlands coast, and like DDT in factory wastes in Los Angeles and Alabama that grossly contaminated local environments, DBCP from factory waste could have entered the waters of Lake Apopka. This pesticide was banned in the US when it was found to cause sterility among male workers in California (unused supplies were then sent, shamefully, to Costa Rica). Hopefully, experiments to resolve this question are currently underway.
Smolen and Colborn mention the "feminization and de-masculinization of male birds", referring to a study by Ian Nisbet and his colleagues of common terns of a colony in New Bedford Harbor that is highly contaminated by PCBs (Nisbet et al. 1996). The "feminization" refers to the appearance of female-type cells in the testes of male embryos. Not mentioned is that the degree of feminization could not be correlated with the concentrations of contaminants, and that so far at least it has been reported only in embryos; whether or not the phenomenon in this colony is related to contaminants is yet to be demonstrated. For the layman it is reasonable to believe that "reproductivity and survivorship are compromised" in this population of terns, but a scientist can hardly make such a statement in the absence of any supporting information. The production of young is high, and the colony has survived many years of high contamination.
Documentation of the existence of feminized adult male common terns, or of any other species of birds for which "feminization" has been claimed, would be the critical first step in the establishment of credibility.
The argument for simplified technologies with fewer, or no, synthetic chemicals has its own, defensible, rationale. It is not, however, the same argument that prompted the DDT hearings in Madison thirty years ago, - that persistent, mobile, bioaccumulating and biologically active chemicals such as DDT and the PCBs have no place in the longer-term technology. This technology does have room for any combination of synthetic chemicals that does not threaten either human health or wildlife. The public interest requires that all participants in the continuing debates about synthetic chemicals distinguish between these two separate and distinct arguments.
The chemical analysis of environmental samples, however, continues to detect unidentified contaminants of undetermined significance. Chromatograms frequently contain many more peaks representing unidentified organic contaminants than peaks that have been identified in previous programs. Older chemists remember the first electron capture chromatograms in the 1960s with the unidentified peaks that turned out to be the PCBs. Vigilance to protect both wildlife and human health from any unanticipated effect of chemical technologies is required now more than ever. But the most significant of the "new threats" to wildlife proposed by Smolen and Colborn are already a half-century old and should not be confused with unanticipated effects of newer chemicals.
Serious and important issues therefore remain. The argument, for example, that genetic defects alone can not account for the abnormalities in the Florida panther population, and that one or more contaminants might be involved, deserves to be expanded. Meanwhile, however, in the absence of supporting data, the central thesis of Smolen and Colborn-that many wildlife species, including populations of endangered species, are now threatened by new 'hidden' factors-lacks credibility.
Studies of the structure of bald eagle eggshells by scanning electron microscopy were supported by the U.S. Fish & Wildlife Service and the Bodega Bay Institute.
Anderson, D. W., and J. J. Hickey. 1972. Eggshell changes in certain North American birds. Proc. 15th Intern. Ornithol. Congress:514-540.
Bland, D.C. 1990. The relationship of organic and inorganic components of eggshells to DDE content in eggs of California brown pelicans and bald eagles. M.Sc. thesis. University of California, Santa Cruz. 43 pp.
Bowerman, W.W. 1993. Regulation of bald eagle (Haliaeetus leucocephalus) productivity in the Great Lakes Basin: an ecological and toxicological approach. Ph.D. thesis. Michigan State University, East Lansing, MI.
Broley, C.E. 1958. The plight of the American bald eagle. Audubon Magazine 60:162-163;171.
Carson, R. 1962. Silent Spring. Houghton Mifflin Co., Boston.
Garcelon, D.K., R.W. Risebrough, W.M. Jarman, A.B. Chartrand, and E.E. Littrell. 1989. Accumulation of DDE by bald eagles Haliaeetus leucocephalus reintroduced to Santa Catalina Island in southern California. Pages 491-494 in B.-U. Meyburg and R.D. Chancellor, eds. Raptors in the Modern World. World Working Group on Birds of Prey and Owls. Berlin, London and Paris.
Grier, J.W., J.B. Elder, F.J. Gramlich, N.F. Green, J.V. Kussman, J.E. Mathisen, and J.P. Mattsson. 1983. Northern states bald eagle recovery plan. U.S. Department of the Interior, Fish & Wildlife Service, Washington, D.C.
Hickey, J. J., and D. W. Anderson. 1968. Chlorinated hydrocarbons and eggshell changes in raptorial and fish-eating birds. Science 162:271-273.
Jenkins, J.M., R. M. Jurek, D. K. Garcelon, R. Mesta, W. G. Hunt, R. E. Jackman, D. E. Driscoll and R. W. Risebrough. 1994. DDE contamination and population parameters of Bald Eagles Haliaeetus leucocephalus in California and Arizona, USA. Pages 751-756 in B.-U. Meyburg & R.D. Chancellor, eds. Raptor Conservation Today. The Pica Press, Buteo Books, Shipman, VA.
Kiff, L.F. 1980. Historical changes in resident populations of California Islands raptors. Pages 651-673 in D.M. Power, ed. The California Islands: Proceedings of a Multidisciplinary Symposium. Santa Barbara Museum of Natural History. Santa Barbara.
Nisbet, I.C.T. 1989. Organochlorines, reproductive impairment, and declines in Bald Eagle Haliaeetus leucocephalus populations: Mechanisms and dose-response relationships. Pp. 483-489 in B.-U. Meyburg & R. D. Chancellor, eds. Raptors in the Modern World. World Working Group on Birds of Prey and Owls. Berlin, London, and Paris.
Nisbet, I. C. T., D. M. Fry, J. J. Hatch, and B. Lynn. 1996. Feminization of male common tern embryos is not correlated with exposure to specific PCB congeners. Bull. Environ. Contam. Toxicol. 57:895-901.
Ratcliffe, D. A. 1967. Decrease in eggshell weight in certain birds of prey. Nature 215:208-210.
Risebrough, R.W. 1993. Scanning electron microscopy studies of eggshells of bald eagles from Santa Catalina Island, 1992, and of Southern California peregrine falcons. A Report to the U.S. Fish & Wildlife Service. The Bodega Bay Institute, Berkeley.
Semenza, J. C., P. E. Tolbert, C. H. Rubin, L. J. Guillette, Jr., and R. J. Jackson. 1997. Reproductive toxins and alligator abnormalities at Lake Apopka, Florida. Environ. Health Perspectives 105:1030-1032.
Smolen, M., and T. Colborn. 1997. Endocrine disruption: hidden threats to wildlife. Endangered Species UPDATE 14:6-10.
Wiemeyer, S.N., T.G. Lamont, C.M. Bunck, C.R. Sindelar, F.J. Gramlich, J.D. Fraser, and M.A. Byrd. 1984. Organochlorine pesticide, polychlorobiphenyl, and mercury residues in bald eagle eggs - 1969-79 - and their relationships to shell thinning and reproduction. Archives of Environmental Contamination and Toxicology 13:529-549.
Wiemeyer, S. N., C. M. Bunck, and C. J. Stafford. 1993.
Environmental contaminants in Bald Eagle eggs - 1980-84 - and further interpretations
of relationships to productivity and shell thickness. Archives Environmental
Contamination and Toxicology 24: 213-227.
Robert W. Risebrough is an employee of The Bodega Bay Institute and can be reach at 2711 Piedmont Avenue, Berkeley, CA 94705 or pelecanus@igc.org.
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