DAVID SAROKIN US.Environmental Protection Agency Washington, DC 20460
JAY SCHULKIN University of Pennsylvania Philadelphia, PA 19104
'
1
~
1
cientists at an International Herpetologists Congress in 1989 realized that many of their colleagues were observing a similar phenomenon: the rapid decline or complete disappearance of populations of frogs and other amphibians from diverse habitats. Subsequent symposia in April 1990 and August 1990 strengthened the consensus among scientists that such declines were indeed taking place at an accelerating pace. Amphibian declines have been reported in eastern and western Canada, the western United States, the Rocky Mountains, the southeastern United States, France, Italy, Costa Rica, Guatemala, the Amazon Basin, the cloud forests of the Andes, and Australia. Overt destruction of habitat such as rain forest is clearly an important factor in the decline of many amphibian populations. Habitat fragmentation can also diminish the capacity of an ecosystem to support a given population. But declines have also been noted in areas relatively untouched by developmental pressures. For instance, the gastric brooding frog of the Australian rain forests was plentiful in the 19709,but disappeared in 1981 and may, in fact, have become extinct. There is no apparent reason for the species' decline, although pollution is suspected as a contributing factor. Of roughly
200 frog species in Australia, about 10% show evidence of sienificant decline. esoeciallv in the southeast: most of t h i decline has occuked since the 1970s (54-571. Amphibians may be particularly vulnerable to pollution because of a suite of inherent characteristics, including a terrestrial and aquatic life history, developmental stages with particular and acute sensitivities to pH and pollutants, an epidermis that freely exchanges ions with the surroundings, and a propensity to biomagnify pollutants (58).A number of pollution-related factors may be contributing to amphibian decline. Climate change may be increasing the intensity and frequency of drought in some areas, threatening, in particular, amphibians living at the edges of their species' range. In many species, frog and salamander embryos are known to be acid-intolerant and may be heavily stressed by even transient episodes of habitat acidification. the The loss of high-elevation amphibian populations in the Andes, far removed from any overt habitat destruction or industrial sources of pollution, may be related to atmospheric inputs from the burning of
tropical forests and the resulting acidification (and other oollutionl in the Andes. Some hoe oooulations in Austrhia appear to have been decimzLd by mercury pollution associated with gold mining operations. Many amphibians bask in sunlight, and embryonic development may take place in shallow sunlit waters: increases in ultraviolet radiation caused by depletion of the ozone layer may be affecting these populations. Trees Unusual and extensive declines of forests have been noted since the 1960s (61).The effects on trees include rtality, thinning of crowns, leaf oloration, root damage, and diinished growth and regeneration. sts in what was West Germany rticularly broad impacts. y area of German forests ged in 1982; 34% in in 1984: and 52% in Of Illally and 1989 (figures cover levels ranked slight, modersevere]. Damage of more an 25% of foliage (moderate and evere damage levels) afflicted 159% of the trees (59,SO]. For the sil-
decline
Environ. Sci. Technol., Vol. 26. No. 9, 1992 1695
ver fir, the overall rate of damaged trees is 83%, with 61% showing leaf loss of more than 25%. In general, older trees of all types are strongly affected; in some areas of Germany virtually every tree more than 60 years old showed symptoms of damage in 1988,and the extent and severity of damage had increased rapidly over previous surveys. Other affected trees include the Norway spruce, Scotch pine, Douglas fir, beech, oak, maple ash, mountain ash, and birch. Damage to the German forest is distinguished from previous declines by several characteristics: the onset of symptoms was very rapid; symptoms are spread across different forest types and species; and decline covers the entire range of affected species and is of unusually long duration (more than 10 years). Forests in other European countries have been similarly surveyed, although the German surveys may be the most comprehensive. Overall, 35% of Europe's total forested area shows symptoms of dying or damaged trees. Seventy-four percent of Czechoslovakia's forests are in decline (when all damage rankings are considered), as are 64% of forests in Greece and the United Kingdom. Forests i n Norway, Liechtenstein, Denmark, Poland, and parts of Italy and the former Soviet Union all have declined ahout 50% (Figure 1) (62, 63). Forest decline has also been documented in the United States. Some populations of red spruce in the northeast appear severely stressed, especially at higher elevations. Red spruces on Whiteface Mountain, NY,in the Adirondacks are experiencing a reduction in growth and increased mortality that began abruptly in the 1960s. Only 15% of the 1964 spruce population remains healthy. Similar damage to highelevation red spruce has been documented on Camels Hump (Green Mountains, VT) and Mount Mitchell (Appalachian Mountains, NC), and early stages of decline have been noted i n the Great Smoky Mountains. Damage in other types of trees has also been noted at these locations, though the impacts appear to be more localized than for red spruce (591. Sugar maples are i n decline throughout eastern Quebec, in scattered areas i n eastern Canadian provinces, and in New England states. Aerial surveys in parts of Quebec revealed damage to 50% of the trees. The bulk of the damage is 1696
Envimn. Sci. Technol.,
slight to moderate (11-25% canopy loss) and is occurring where acid deposition is the highest (62, 631. Sugar maples on Camels Hump peak in Vermont have shown a 25% reduction in overall mass in the past 25 years and a 50% reduction in the number of new trees ( 6 4 ) . Masson pines in the heavily polluted area of Chongqing, China, have been declining precipitously since the 1980s; 85% of the population shows injury symptoms similar to those produced by exposure to pollutants under controlled conditions (65).Although the area receives highly acidified rainfall, tree damage was more closely correlated with atmospheric levels of sulfur dioxide and hydrogen fluoride than with acidity. Ponderosa and Jeffery pine trees in southern and central California also appear to be in a state of decline ( 4 1 ) . Two pollutants, acid deposition
1
Vol. 26, No. 9, 1992
FIGURE 1
Estimated forest damage in Europe, 1988' Czechoslovakia Greece U.K.
Estonia tormer W. Germany Tuscany. Italy Liechtenstein Norway Denmark Poland Netherlands landers, Belgium mer E. Germany Bulgaria Switzerland Luxembourg
Finland Sweden Wallonia, Belgium Yugoslavia Spain Ireland Austria France Hungary Lithuania Boizano, Italy Portugal
1
t
and ozone, have been repeatedly implicated in damage to forests. Acidic cloud water, which can routinely reach pH levels of 2.8-3.8, is suspected as a key contributing factor to observed impacts on high-elevation spruce forests of the eastern United States. Ozone has been identified as a significant cause of damage to ponderosa and Jeffery pines in California. A third category of pollutants, chlorinated hydrocarbons, has received little attention as a possible contributing factor, yet these chemicals are readily transformed in the atmosphere to potent herbicide-like chemicals (e.g., trichloroacetic acid) and have been shown to be present at concentrations that can have a phytotoxic effect (66). A complex mix of pollutants, including those just mentioned, is thought to be a principal contributing factor to forest decline in Germany and in other European countries.
The precise mechanism of impact for air pollutants is not known, but it follows a general pattern of increasing stress, rendering trees more susceptible to damage from natural stresses-such as drought, insects, and freezes-and anthropogenic stresses such as changing patterns of land use. Current hypotheses include complex interactions of multiple effects: soil acidification liberates aluminum ions, which interferes with calcium and magnesium uptake by tree roots: excess nitrogen deposition overfertilizes trees, causing attempted growth at a time when the tree is depleted of essential metals; and reactive ozone and low-pH mists may directly damage leaves and destroy chlorophyll. Soil acidification may also lead to changes in microbial populations, decreasing the numbers of beneficial microbes andlor increasing those capable of adding to overall stress.
Birds Some bird populations of North America have been declining fairly rapidly. A comparison of historical radar records capable of imaging migrating bird populations across the Gulf of Mexico suggests a 50% drop in migration during 1987-89, compared to records from 1965-67 (67, 68). A survey of 251 species documented population declines in 60% of the species between 1988 and 1989, and similar numbers of declines appear to have occurred over a 20-year period. For survey years 1986-89, reduced populations were particularly pronounced in the central part of North America (69). Migrating birds that winter in the tropics also show sharp drops in population. Of the 62 species surveyed, 15 showed declines (six of which were considered significant) in the period 1966-78. For the period 1978-1987,44 species showed declines, 20 of which were considered significant (70). Migrant bird populations in Europe appear to be experiencing similar declines. From one third to one half of all European bird populations monitored are declining in number; of the 15 species with the most serious declines, 14 are migrant populations that winter in Africa (71). Only a few of the population reductions have been linked in any way to the possible impact of pollutants. Populations of black ducks have shrunk by 50% since the mid1950s (72)in eastern Canada an
the northeastern United States, areas affected by acid precipitation (Figure 2). Populations of ringnecked ducks have similarly declined ( 4 1 ) . In one study, black duck ducklings reared in acidified waters had a lower survival rate and less weight gain than ducks in nonacidified waters: a diminished food supply as a result of acidification may have been the cause. However, other studies have come to the opposite conclusion that acid-induced reductions in fish populations led to increased insect populations that served as food for ducklings (41). Metals and organic pollutants may also be causing direct toxic effects on some populations. The near-decimation of populations of bald eagles and ospreys from eggshell thinning caused by DDT contamination led to a ban in the 1970s on use of this pesticide in the United States. Although populations have rebounded since then, DDT breakdown products are still found in some Chesapeake Bay bird populations in concentrations great enough to jeopardize reproductive success. Lead concentrations in bird tissues (chiefly as a result of ingestion of lead shot) were high enough to have adverse effects in 14 out of 15 Chesapeake Bay bird species studied. Lead contamination
was particularly widespread among black ducks (73).
Other populations O t h e r p o p u l a t i o n s may b e broadly threatened by pollution, hut there is little information with which to gauge whether a population decline is occurring and, if it is, the causes of the decline. We mention these briefly here. Mangrove swamps appear to be heavily damaged by coastal pollution in Southeast Asia (741, the Caribbean (21,the South Pacific (301,and South America: mangrove-dwelling species of manatee are particularly threatened (75).Various populations of turtles are affected by pollution: Marine turtles of the Mediterranean are threatened by human disturbances to nesting sites and general pollution (76):marine turtles in the Caribbean and the Pacific have unusual numbers of tumors that were quite rare until 10 years ago, but are now affecting up to one half of all turtles examined in some areas of the world (27). Freshwater molluscs, chiefly river snails and mussels, seem to be disappearing rapidly as a result of habitat alteration and pollution; more than 130 species in the United States are presumed extinct (77). Earthworms exposed to organochlorines develop lesions and abnormal
Total United States
........ .\ .......u.. ..... \J..t....I................................
.........
..,
1Y34
1 Ybd
lYlL
IYUI
Tne declining populations mirror those Of some Other wateflowl I" the eastern hall 01 the United Slates l Y l7q YU
I
Envimn. Sci. Technol., Vol. 26. No. 9, 1992 16W
swellings (78). Acidification of freshwater systems shifts microbial populations from bacteria to fungal species and reduces species richness of both zooplankton a n d benthic invertebrate populations (42). Leeches appear to be among the most acid-sensitive of freshwater organisms and are greatly reduced in both numbers and diversity in acidified fresh waters (79). Eelgrass populations may be succumbing to a disease-related decline that is exacerbated by coastal p o l l u t i o n ( 8 0 ) . Williams a n d Bunklev-Williams 12) . _noted lareescale marine disturbances affecting crustaceans, shellfish, sponges, sea stars, sea cucumbers, turtlegrass, and pelicans, among others. Pollution in the Black Sea is considered responsible for increased zooplankton mass, reduced diversity, and a 500-fold increase in biomass of jellyfish in a 20-year period (811. Saguaro cactuses in the deserts of the southwestern United States and northern Mexico are in serious decline, with up to 50% of the population lost in some areas and many others showing browning and loss of spines, especially on the south side of the plants. Pollution borne by prevailing winds from the south and excess ultraviolet radiation are suspected as causes (90).
scrutiny, and put forward by scientists whose agendas may include policy making and fund raising in addition to research. This is partially evidenced by the fact that so much of the information generated on these disturbances is in the “gray literature” of congressional hearings, draft government agency reports, and science reporting in the general press. This paper attempts to accomplish two distinct objectives. One, it summarizes available literature (technical and lay) on large-scale disturbances and Dossi.DoDulation I
-
The degree of certainty Many human activities can damage or decimate a population: habitat destruction, hunting, domestication, and introduction of competing populations. We have presented in this paper information on large-scale perturbations to aquatic and terrestrial populations that are known or suspected to be related to pollution. The nonpollution-related impacts are not included here, except where they shed light on possible pollution-related effects. We have presented available information in a fairly uncritical manner. Where publications could be found relating population disturbances to pollution, we have tried to summarize these materials without undue evaluation of the adequacy of scientific investigation or the possible motivations for assigning one cause or another to an event. It is clear, however, that a great deal of the information surrounding these events is generated in an atmosphere of public concern, occasionally heightened by intense media
i
paleontology lie many of the large-scale population disturbances that we have summarized in thisarticle.
1WE Environ. Sd. Technol., Vol. 26. No. 9. 1992
ble relations to pollution. Two, we evaluate the degree of confidence in findings that a population disturbance has indeed taken place, and that pollution is a primary or contributing cause of the disturbance. How real are these phenomena that have been reviewed? By this, we mean several things: Is it clear that a large-scale disturbance of some sort has actually occurred? If so, how well are the causes of the disturbance understood and, in particular, how clear is it that pollution is a contributing factor?
Is the disturbance a novel event? That is, is it truly without precedent, rather than an event that has occurred before (possibly many times) but is being noted by the scientific community for the first time? The population disturbances reviewed here are summarized in Table l. Table 2 is the authors’ attempt to answer the above questions. We have not only summarized reported events, but included our informed judgment of the degree of certainty and consensus in the scientific communitv reeardine these lareescale pe&rb&ions. Of all the events listed, the epizootic of fish tumors strikes us as ”le most “real” phenomenon in ~rmsof addressing the questions 1st outlined. [See Part 1 in last lonth’s ESSbT for a discussion of p a t i c disturbances.] Several nes of evidence from the field, cperimental work, historical observation, and theory of tumorigenesis all converge to create a Impelling picture of pollutioniduced liver tumors in fish occurring over a broad geographic area in North America in a num%r of different species. The full 3ographical extent of such tuiors is not clear, however. Outde of North America, it is not nown whether such tumors are ot occurring or are occurring but ot being reported, in the many :Bas of the world where polluon might be supposed to have similar impacts on fish populations. The bleaching of coral reefs is somewhat the reverse of the fish tumors epizootic. The bleaching events stand out as the one truly global-scale perturbation, having 3en documented in virtually all F the world’s tropical waters; although bleaching itself is a familiar event, the scale and severity of recent episodes do appear to be without precedent. The documentation remains “soft,” however, relying as much on casual observation as on formal research. Little formal research on coral reefs was carried out prior to the 1960s (29). The evidence linking bleaching to a general warming of coastal waters is, as yet, inconclusive, and the relationship of any such warming trends to global warming can only be labeled speculative. The complex interactions among phytoplankton, sea urchins, starfish, and other organisms that may also be affected by pollutants also need to be considered as I
c I
I
potential stresses affecting coral reefs across a broad scale. For several of the population perturbations, there is a legitimate question whether anything out of the ordinary has taken place. Although large-scale die-offs of dolphins are not thought to be common, there is not much historical record on which to base a comparison. A review of seal die-offs documented several in the 1800s involving thousands of animals; because seals "haul out" and congregate closely on rocks, there is thought to be more of an opportunity for transmitting disease in seals than in animals that spend all their lives in water (82). Perhaps what emerges as a novel perturbation is not so much any one incidence of mass mortality or decline, but the onslaught of events in rapid succession, all possibly related to anthropogenic causes such as toxic blooms of algae or other microorganisms spurred by excess nutrients, pollution-induced immunosuppression, behavioral responses to warmer waters, or a combination of factors influencing the marine environment. However, it is difficult to confirm the widely held suspicion that many of these episodes are without precedent or are ultimately related to human activities. The status of amphibian populations is not well known, although steps are being taken to coordinate scattered reports and provide common methodologies for future data gathering. Reports of disappearing frog populations, although convincing, are thus far mostly anecdotal. Pechmann et al. (83) have detailed some of the difficulties in distinguishing human impacts from natural fluctuation. Forest die-back in Germany is clearly occurring and seems to be without historical precedent. The situation in the rest of Europe is incompletely documented, although even casual observation is enough to confirm severe problems in some areas. The combined impact of a number of pollutants clearly seems to be negatively affecting forest health and is likely the primary cause of the observed declines. Several researchers have suggested that spruce and maple declines in the eastern United States may be due merely to the aging of populations stressed by unusually cold or dry conditions (841. However, the preponderance of evidence strongly suggests a negative role of acid precipitation and other pollutants.
The status of large-scale perturbations in populations of phytoplankton is difficult to assess. Many phytoplankton researchers have concluded that blooms are indeed increasing in numbers, that many novel blooms are occurring, and that well-known bloom organisms are displaying unusual characteristics such as sudden toxicity. However, these observations are based chiefly on professional judgment stemming from years or decades of familiarity with phytoplankton: there are only scattered collections of concrete data beyond personal observation. There are, however, considerable data on the changing chemical regimes of coastal waters caused by pollution and eutrophication, and there is little reason to
suppose that such changes would not affect phytoplankton.
Discussion Lessios (31)has noted that population disturbances are usually studied on two very different scales. Ecologists, for practical reasons, limit their observations to short-lived, local perturbations, especially ones subject to experimental manipulation. Paleontologists, on the other hand, concern themselves with long-term, widespread, irreversible events as preserved in the geological record. Ecologists are thus limited in their scope, paleontologists in their spatial and temporal resolution. In the scientific no man's land between ecology and paleontology lie many of the large-scale population
?r SC1l)"tltlE name
Tuniops truncatus Phocoenaphocoena Megaptera novaeangiliae Stenella coeruleoalba Phocoena sinus Phoca sibirica Phoca vitulina Halichoerus grypus Monachus sp. Acoropora spp. Millepora sp. nov. prychodiscus brevis Acompora spp. Aureocmcus anophagefferens Chrysochromulina polylepis Acanthaster planci Diadema antillarum Strongylmntrotus drobachiensis Zostera manna Poecilia reticulata Salvelinus fontlnalis timagiensis Mugil cephalus Micmpogon undulatus Parophrys vetulus Rheobatrachus silus Pima rubens Sarg. Pinus jeffreyi Acer saccharum Pinus massoniana Lamb Anas rubripes Ayihya collaris Haliaeefus leucocephalus Pandion haiiaetus
Envimn. Sci. Technol., Vol. 26, No. 9. 1892 1688
disturbances that we have summarized in this article. For all the literature these events generate, much of it is journalistic or in nonrefereed “gray literature.” Many of the incidents have a single champion in the scientific community without whom there would be little or no careful documentation of a given perturbation. The efforts of the scientific community to provide information on population baselines and trends, historical perspective on perturbations, and natural and anthropogenic mechanisms of disturbance are sporadic at best. It has become clear in recent decades that the scale of human activity on Earth has grown large enough to have global environmental consequences. Increased levels of potentially toxic pollutants are ubiquitous, even in isolated regions such as the Arctic (85).Increases in atmospheric concentrations of carbon dioxide as a result of anthropogenic activity are well known; levels of carbon monoxide, methane, NO,, SO,, nitrous oxide, and chlorofluorocarbons have increased as well (86). Atmospheric levels of hydrogen are estimated to have increased as a result of human activity from a pre-industrial level of 200 ppb to 500 ppb at present (87). Human activity now exceeds natural inputs as an atmospheric source of lead, cadmium, vanadium, zinc, arsenic, copper, mercury, nickel, and antimony; anthropogenic inputs to aquatic systems are similarly dominant over natural inputs (88). In most cases, the large-scale effects of such pollution on the biosphere are little understood, and our ignorance has added to the difficulty of creating responsible environmental policy. This situation needs to be remedied if we are to allow ourselves the option of preventing population perturbations when we can and responding sooner, and in a more informed manner, to such perturbations when they do occur. We have several observations that would bear on any efforts to improve the current quality of scientific information: Populations that are fixed in place-coral reefs and forestslend themselves to field monitoring of readily identifiable individuals as well as broad and clearly definable areal sampling. Fish populations, although not fixed in the same sense, can often be easily enough sampled to allow for continual, broad-scale documentation. Marine mammals pose particular problem fmm a sampling point of 1700 Envimn. Sei. Technol.. Vol. 26, No. 9, 1992
view because many populations are difficult to locate, and destructive sampling of dolphins or seals is much more likely to raise a public outcry than would sampling of trees, fish, or frogs. Examination of dead animals after a die-off seems to provide frustratinglylittle information as to the overall health of, or the extent of threats to, marine mammal populations. The use of historical records-either naturally stored in biological systems or maintained in scientific archives--seems largely unexplored. Tree ring data have been used to shed light on patterns of forest growth and stress (84);radar records dating back to the 1950s have been used to document historical trends in numbers of migrating birds (67);and examinations of historical collections of bones have documented
structural impacts of pollution on seals (21). Useful historical perspectives might also be gleaned through such “retroactive monitoring” as cores taken from coral reefs, high-altitude photography of phytoplankton blooms, and examination of preserved tissues for evidence of carcinogenicity or pollutant loadings. We know of no truly global-scale biological sampling scheme in place for any population, despite the growing concern about global-scale impacts from pollution. It would not seem to be inordinately difficult or expensive to institute, for instance, a fish tumor sampling program for commercial fish catches around the world, or even for fish caught explicitly for research purposes. The use of biological monitor organisms from a host of taxa has a
TABLE 2
The degree of certainty for novel population disturbances and the role of pollution’ Population
Type ot dlatutbnnm
Bonlenose dolphins
Mass mortality, U.S. east coast
Bonlenose dolphins
Mass mortality, Gulf coast of Texas Mass mortality,
Striped dolphins
Vaquita
(harbor porpoise) Harbor seals
Lake Baikal seals Baltic grey seals Mediterranean monk seals Coral reefs
Mediterranean Diminished population, Gulf of California Mass mortality, North Sea Mass mortality, Lake Baikal
Skeletal deformations, Baltic Sea Endangered po dation, Mediterranean gaa ~~~~
~~
~~
~~~
Worldwide bleaching White band disease Crown-of-thornsstarfish Black sea urchins Mass mortality Fish, multiple populations Outbreak of liver tumors, North America Extinct populations Endangered, threatened, or diseased populations Phytoplankton Unusual blooms Abrupt scarcity of certai~ Amphibians populations Mixed forests, Germany Mixed forests, Disease throughout Europe symptoms High-altitude red spruce and mortality Sugar maple Masson pines Migrant birds Declining Black ducks populations a
... If..
’* * 0
As anributed by Me authors High confdence.
Fleacanable confidence. tirnited conliience. Low confidence.
Unsupparted by available information.
Dlstutbnnm I. a now1 event
Pollutbn is a contributing E.UI
*. 0
demonstrated value in local monitoring of pollution (78)and could conceivably be expanded to broader geographical scales. Similarly, in large areas of the world, we have virtually no information whatsoever of a historical, baseline, or etiological nature. Without such data there can be no truly global perspective for MY pollution-related concern. The general phenomenon of pollution increasing stress, thereby lowering resistance t o other threats such as disease, temperature extremes, or drought, is commonly hypothesized but little explored. The extent to which pollution can act synergistically with other factors to affect organisms or entire systems is, at present, largely unknown. If the Earth were to pay a visit to its doctor, it would likely hear advice like this: You have a number of troubling symptoms, but I don't quite know what they mean, bow serious an illness you have, or what the prognosis is. More intensive testing and observation are definitely called for. The better our understanding, the better the chances for returning the patient to full health.
A call for information The authors would appreciate receiving any infomation relevant to the population perturbations covered in this article, or on other perturbations not covered hut meeting the criteria laid out in the introduction. Send information to David Sarokin. USEPA TS792a. Washington, DC 20460. The views in this article are those of the authors and not necessarily of the institutions with which they are affiliated.
References Rejerences 1-53 appeor at the end of Part 1 of this article (August issue. pp. 1483-84) (54) Wyman. R. Conserv. Biol. 1990. 4 ,
(60) Facts and Figures on the Environment of Germany: 1988-89: Federal Envi-
ronmental Agency of West Germany: Bonn. 1990. (61) French. H. Clearing the Air: A Global Agendo: Worldwatch Institute: Washington. DC. 1990; paper 94. ( 6 2 ) The State of the Environment: Organization for Economic Cooperation and Development: Paris, 1991. 1631 United Nations Environment Programme. Environmental Data Reporl prepared by GEMS Monitoring and Assessment Research Centre: London. 1991. (641 The New York Times. May 15, 1991. p. A18. (65) Yu Shu-Wen et al. Environ. Monit. Assess. 1990,23946. (66) Frank. H. Ambio 1991.20, 13-18. (67) Gauthreaux, S. A. The use of weather radar to monitor long-term patterns of trans-Gulf 1990 migration in spring (in press). (68) Wille, C. Audubon 1990, May, 8 W 5 . (691 "North American Breeding Bird Survey Annual Summary, 1989": US. Fish and Wildlife Service: Washington. DC. 1990: biological report 90(81.
Robhins. C. S. et al. Proc. Natl. Acad. Sci. USA. 1989.86.7658-62. (71) Berthold,'P.; Terrill. S. B. Ann. Rev. Ecol. Syst. 1991,22,357-78. (72) Rusch, D. H. et al Wildlife SOC. Bull. (70)
Duhois, A. "Declining Amphibian Populations-A Global Phenomenon: Some Preliminary Comments": manuscript, Musee National $Histoire Naturelle: Paris, 1990. (57) Tyler, M. J. "Declining Amphibian Populations: A Global Phenomenon-An Australian Perspective"; manuscript. University of Adelaide: Australia, 1991. (58) Vitt, L. et a]. BioScience 1990, 40,
(561
418. (59)
Krahl-Urban, B.: Peters. H. E.; Schimansky. C. Forest Decline: US. Environmental Protection Agency and German Ministry of Research and Technology: Washington, DC. 1988.
behovioml neuroscience a t the University of Pennsylvania. His Ph.D. is from the University of Pennsylvania.
1989.17.379406.
Ohlendorf. H. M.; Fleming, W. J. Mar. Pollut. Bull. 1988, 19,487-95. (74) Fortes, M. D.Ambio1988,17.207-13. (75) Annual Report to Congress of the Marine Mammal Commission, Calendar Year 7990; Marine Mammal Commission: Washington. DC, 1991. (76) Venizelos. L. E. Mar. Pollut. Bull. 1991,23,613-16.
Palmer, S. Atala 1985. 13, 1-7. Root. M. BioScience 1990. 40, 83-86. Bendell, B. E.; McNicol. D.K. Can. I. Zoo/. 1991. 69.13W33. (80) Short, F. T.; h l i n g s , 8. W.; den Hartog. C. Aquaf. Bot. 1988.30.295-304. (81) Balkas. T. et al. "State of the Marine Environment in the Black Sea Region"; United Nations Environment Programme: New York. 1990: Regional Seas Reports and Studies No. (77) (78) (79)
124.
1.: Grenfell. B. Mar. Pollut. Bull. 1990, 21. 284-87. (83) Pechman. J.H.K. et al. Science 1991,
(82) Hamood.
253.892-95.
Wildlife
L
Jay Schulkin is an assistant professor of
(73)
350-52.
(55) Phillips. K. International 1990, Nov.-Dec., 610.
David Sarokin is a biologist with the US. Environmental Protection Agency. Hish4.S. degree is from the State University of New York a t Stonybrook.
(84)
Johnson, A. H.:Cook E. R.; Siccama, T. G. Proc. Nail. Acad. Sci. USA 1988, 85,536%73.
(85) Travis. C. C.: Hester. S. T. Environ. Sci. Technol. 1991,25.815-19. (86) Graedel, T. E.; Crutzen, P. J. Sci. Am. 1989. 261(3). 58-68. (87) .Monastersky, R. Sci. News. 1990. 138. 261. (88) Nriagu, J. 0. Environment 1990,32(7), 7-11.28-33. I891 Smith, R. Written testimony to the
U.S.House of Representatives Committee on Merchant Marine and Fisheries Hearing on Fish Cancer Epidemic Oversight, September 21.1983, pp. 87-91. (90) The New York Times. August 11. 1991, p. 23.
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