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"Animals as Environmental Sentinels of Human Pollution"

Leslie A. Dierauf, V.M.D.

PRESENTED AT: CURRENT TOPICS IN VETERINARY PUBLIC HEALTH
1999 AVMA Convention, New Orleans, Louisiana
TUESDAY, JULY 13, 1999

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Leslie Dierauf, V.M.D. is also the editor of The Marine Mammal Medicine textbook. Click below for CRC Press ordering information.
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INTRODUCTION
Animals, the silent sentinels, stand watch over the world's environmental health. Everyday, animals demonstrate intricate connections between them, us and our surroundings. In 1993, O'Brien(1) defined animals as indicators or sentinels. Sentinels are "organisms whose known characteristics can be measured to assess the extent of environmental...implications...and to provide early warning of those implications."

Pollution is defined as contamination of the earth's environment with materials that interfere with health, quality of life, or the natural functioning of ecosystems (living organisms and their physical surroundings). Although some environmental pollution is a result of natural causes like volcanic eruptions, most is caused by human activities.

Amphibians are vertebrates and include approximately 4,400 existing species. Amphibians are in most cases, small, diverse, and sensitive to environmental variability. They can be good indicators of habitat diversity, biological variety, and local stressors on the environment. They are bathed in both water and air. They live outdoors on land and water, and their skin, larvae, and unshelled eggs are constantly exposed and in contact with the substances in their surroundings.

The golden toad (Bufo periglenes) of Costa Rica within a 20-year period went from its initial discovery to extinction(2). Other species' populations have disappeared or are declining in numbers in Brazil, Mexico, Australia, India, Bangladesh, Portugal, Taiwan, the United States, and Norway. There is no one apparent cause for these declines.

POSSIBLE CAUSES OF AMPHIBIAN DECLINE

OBJECTIVE

To describe current hypotheses in the scientific literature as to causes of amphibian population declines and limb deformities world-wide.

Human population growth and its effects (Loss or modification of aquatic and terrestrial habitat; Predation &/or introduction of non-native competitors; Air and water quality impacts; Climate changes)

Habitat destruction is one of the most serious threats to amphibian populations. In 1988 on a West Michigan farm, frogs were nearly absent. When the farm switched from a conventional soy/corn rotation using traditional environmental herbicides and pesticides to an organic farm and nursery using composted materials and organically charged waters, frog populations and diversity of amphibian species exploded(3). A similar story exists on a ranch in Nutt, New Mexico. When the rancher went from heavily grazing cattle year round in a riparian area called Macho Creek to only grazing in the non-growing season, Macho Creek once again flowed and flourished, and previously unrecorded species of leopard frogs began to inhabit the creekbed(4).

In 1993, non-native crayfish (Orconectes virilis) were introduced into the stream habitat of the last known population of leopard frog (Rana chiricahuensis) in east-central Arizona. Where crayfish were abundant, leopard frogs were rare or absent, aquatic snails disappeared, and native aquatic plants and invertebrates were severely depleted. Staged encounters between crayfish and leopard frogs (adult, larvae and metamorphs) demonstrated predation by crayfish(5).

Acidification of habitat is also a possible cause for amphibian declines. The effects of anthropogenic acidification of waters and soils on amphibians in England and North America were exhibited as net loss of body sodium and embryonic curling defects(6).

Air quality effects (Greenhouse gases, such as carbon dioxide from burning of fossil fuels; Volatile organic compounds; Aerosolized pesticides/other chemicals; Particulate matter & silt/sedimentation)

Air has a great capacity for moving large amounts of pollutants over time and space. Fog and low clouds affect the inhalation exposure route(7) in humans and laboratory animals. Since frog skin is sensitive to moisture and is lipophilic, the diminishing of frog numbers and varieties in tropical rainforests could be due to climatic changes (such as less rainfall) or possibly aerosolized pollutants.

The World Health Organization estimates that mercury is released into the air in large amounts worldwide from natural and anthropogenic sources. If carried to water sources, methylmercury binds to aquatic biota, accumulating as it moves up the aquatic food chain,(8) bathing the gill systems of the amphibians inhabiting the tainted water, causing neurotoxic effects.

In Costa Rica, Karen Lips from St. Lawrence University, conducted numerous site specific surveys. In the 1994-5 survey season, she encountered 55 species of amphibians; in the 1996-7 season, only 24 species could be found; five of seven streams she had checked regularly since 1990, were essentially "frogless". During this same survey, she found 54 dead or dying frogs from 10 different species. Her field notes are: "Many of the casualties still had very life-like appearances; most were found during morning surveys, still sitting in a perched position. Dying individuals were lethargic, had no righting response and exhibited convulsions and trembling of the limbs and head. Sever dying adults were somewhat thin, but not had any obvious lesions or wounds. Two tadpoles were found swimming in an uncoordinated fashion. Several of these symptoms are similar to those described for dying frogs from an Australian site, and from which viruses were isolated"(9,10).

Water quality and quantity effects (Herbicides; Pesticides; Heavy metals; Other run-off materials; Decreased pH/Increased salinity; Lowering of water tables; Loss of freshwater spring flows)

There is increasing evidence that rain water, well water, lakes, freshwater, saltwater and terrestrial foods can carry endocrine-disrupting chemicals(11). Amphibians appear vulnerable to the reproductive effects of these chemicals.

A high prevalence of hindlimb deformities were found in wild-caught green frogs, American toads, and bullfrogs from agricultural sites exposed to pesticide run-off in the St. Lawrence River Valley of Quebec, Canada(12). In southern Quebec, pesticides contaminate watercourses and underground water sources in agricultural regions where intense sweet corn and potato farming are common. In this area, of 853 metamorphosing amphibians from 14 farmland habitats, 106 had severe ectromelia (limb absence) and ectrodactyly (digit absence), compared to only 2 of 271 in control sites. Similar malformations have been induced in the laboratory with water sources from ponds in Minnesota with high percentages of wild frog deformities(13).

The Australian government in late 1996 took an unprecedented step banning 84 herbicides (each containing glyphosate as the active ingredient and a detergent additive used as a dispersant/wetting agent) from use near streams or waters because of their apparent effects on frogs and tadpoles. The dispersant may be the culprit, since the purpose of this agent is to break down surface tension on the leaf surface allowing spray droplets to completely cover the leaf. Unfortunately, this same dispersant interferes with cutaneous and gill respiration in frogs and tadpoles(14).

Climate change effects (Increased ultraviolet light from ozone depletion; Acid rain; Global warming; Disease (fungal, parasitic, viral))

In 1995, Blaustein and Wake observed that many threatened amphibian species lay their jelly-like egg masses in open, shallow waters at high altitudes. They proposed that increased UVB radiation coming through a thinning stratospheric ozone layer was making the amphibians' eggs more susceptible to fungal infection(15). The long-toed salamander species these researchers studied were from the mountain lakes of Oregon's Cascade Mountains, and if the eggs were shielded from UVB light, they hatched normally.

Similarly, Dr. Joyce Longcore at the University of Maine working with the National Zoo has discovered a chytrid fungus, previously only found in decaying matter and insects, as a causative agent in frog deaths (possibly by suffocating them) in large numbers over wide areas of Central America and Australia. Dr. Earl Green, a veterinary pathologist at the University of Maryland Animal Health Laboratory has found the fungus in healthy frogs from Maryland to Illinois(16). Epidemiologically, we must ask, was this fungus brought in from elsewhere mistakenly, or is it now only revealing itself in amphibian populations weakened by other factors?

In England, certain species of frogs, toads and newts in a long-term study between 1977 and 1994 spawned earlier, with these changes closely correlated to increased average temperature during the study period(17).

Between 1974 and 1982, 11 populations of boreal toads (Bufo boreas boreas) in the West Elk Mountains of Colorado totally disappeared. The apparent cause of extinction was Aeromonas hydrophila(18). Environmental effects on amphibian immune function were a part of this study; leopard frogs (Rana pipiens) and cane toads (Bufo marinus) were exposed to prolonged acidic environs (pH=3.8), as well as cold body temperatures. Results suggest both low pH and cold temperature situations caused immunosuppression, manifested by significantly depressed proliferative responses of lymphocytes to mitogens and lowered serum complement levels(19,20).

A previously undescribed iridovirus (Ambystoma tigrinum virus-ATV) has been isolated from the Sonoran tiger salamander (Ambystoma tigrinum stebbinsi). Researchers believe non-native bullfrogs may play a major role in the spread of this virus to native amphibian species(21).

Effects on changes in biological diversity

Threats to biological diversity include many of the topics discussed above, from habitat fragmentation and modification/destruction to harvesting of native species for food or research, to introduction of non-native species, to pollution of air, water or soil, to increased ultraviolet radiation and global warming. Unrestrained human population growth and the inability of humans to fully comprehend the economic value of biological diversity are serious challenges that must through education, be overcome(22).

The poison dart frogs occupy at least 100 rare and minute niches in the rainforests of Central and South America. Not only do they exhibit extraordinary colors and color patterns, they also are of great medical and scientific interest. These frogs produce deadly natural toxins composed of alkaloids. Physiologically, these alkaloids paralyze through biochemical actions on sodium and potassium channels, calcium pumps and acetylcholine receptors. Yet, as the habitat these tropical frogs depend upon disappears, so does the knowledge we could gain by studying these unique medical models and the substances they are capable of producing.

DISCUSSION

As these examples indicate, the scientific literature is full of animal warnings. Amphibians, a unique group of animals found world-wide, are apparently being affected by direct and indirect human activities. No single cause for the declines and disappearances can be identified. Scientists are not certain whether these signals are part of an evolutionary trend or an indication of a more serious ecological crisis.

At the September, 1995 "Conference on Human Health and Global Climate Change", sponsored by the White House National Science & Technology Council, the Institute of Medicine and the National Academy of Sciences, one speaker commented that "new styles of science" are warranted that go beyond the traditional demand for "precise, empirically-grounded answers" from scientists to a science that deals with complexity, uncertainty, and future-oriented questions. The discussion that follows is meant to peak that type of "science out-of-the-box thinking". There are fewer answers than suggestions as to the future direction of veterinary medicine/public health research.

We must scrutinize individual cases with regard to these amphibian population declines and deformities in an attempt to explain whether any particular population is changing, and if so try to explain how, while working these identified mechanisms into systematic models. Researchers must commit to providing long-term monitoring and rigorous investigation of the causes of declines in the especially sensitive amphibian component of the aquatic and terrestrial ecosystems worldwide. Following are five sets of examples of the effects of human activities ("pollution") on amphibian species.

Humans tend to be unconcerned/unimpressed unless our own health is threatened or unless scientific evidence shows direct cause and effect. Yet the first step in addressing environmental/ecosystem health is admitting that animals are indicating problems. We need to move forward with multi-disciplinary research that recognizes the value of animals as sentinels of environmental health. We also need to recognize that environmental protection measures which protect animal health often directly and indirectly protect our health as well.

For more information on amphibian declines, check the following websites:
www.npsc.nbs.gov/narcam [North American Reporting Center on Amphibian Malformations]
acs-info.open.ac.uk/info/newsletters/FROGLOG.html [Declining Amphibians Population Task Force]

"When you were a little child", said the hawk, "all kinds of things seemed possible.
As you got older and wiser, you learned more and more about the boundaries of your world, and you got more and more used to thinking within those boundaries.
The unknown is simply the not-yet-known. Most people look for solutions within the known.
If there is something you want to do, and you think it impossible, I want you to look outside the known, not within it.
I want you to learn to think beyond your thoughts."
[from Matthew's Meadow by Corrine Demes Bliss]

1. O'Brien, D. J., Kaneene, J. B. and Poppenga, R. H., The Use of Mammals as Sentinels for Human Exposure to Toxic Contaminants in the Environment, Environ. Health Perspect. 99:351-369, 1993.
2. Sarkar, S., Ecological Theory and Anuran Declines, BioScience 46(3): 199-207, 1996.
3. McKown, P.D. and DeFazio, S.M., Froglog Shorts, Froglog 21, 1997.
4. Shiner, J., personal communication, rancher, Nutt, NM, 1996.
5. Fernandez, P.J., and Rosen, P.C., Effects of Introduced Crayfish on the Chiricahuan Leopard Frog and its stream habitat in the White Mountains, Arizona, Declining Amphibian Populations Task Force Southwestern U.S. Working Group, Abstract, January, 1998.
6. Dunson, W.A., Wyman, R.L., and Corbett, E.S., A Symposium on Amphibian Declines and Habitat Acidification, J. Herp 26(4): 349-352, 1992.
7. Oehme, F.W., Coppock, R.W., Mostrom, M.S., and Khan, A.A., A Review of the Toxicology of Air Pollutants: Toxicology of Chemical Mixtures, Vet Human Toxicol 38(5):371-377, 1996.
8. Wheeler, M., Measuring Mercury, Environ. Health Perspect. 104:826-830, 1996.
9. Speare, R., Field, K., Koehler, J. and MacDonald, K., Review of the Presentation: Disappearing Australian Rainforest Frogs: Have We Found The Answer? Froglog 9, 1994.
10. Lips, K.R., Decline of a tropical montane amphibian fauna. Conservation Biology 12:1-13, 1998.
11. The Keystone Center, Convening Report of the Endocrine Disrupter Screening and Testing Advisory Committee, U.S. Environmental Protection Agency, October, 1996.
12. Ouellet, M., Bonin, J., Rodregue, J., DesGranges, J-L, Lair, S., Hindlimb Deformities (ectromelia, ectrodactyly) in Free-Living Anurans from Agricultural Habitats, J. Wildl. Dis. 33(1):95-104, 1997.
13. Burkhart, J.G., Helgen, J.C., Fort, D.J., et. al, Induction of Mortality and Malformation in Xenopus laevis Embryos by Water Sources Associated with Field Frog Deformities, Env. Health Persp. 106:841-848, 1998.
14. Tyler, M.J., Herbicides Kill Frogs, University of Adelaide, South Australia, Froglog 21, 1997.
15. Blaustein, A.R. and Wake, D.B., The Puzzle of Declining Amphibian Populations, Sci. Am. 272(4):52-57, 1995.
16. New York Times, Newly Found Fungus is Tied to Vanishing Species of Frogs,Sunday, June 28, 1998, p. A12.
17. Beebee, T.J., Amphibian Breeding and Climate, Nature 374:29-220,1995.
18. Carey, C., Hypothesis Concerning the Causes of the Disappearance of Boreal Toads from the Mountains of Colorado, Conservation Biology 7:355-362, 1993.
19. Carey, C., Maniero, G.D., Harper, C.W., and Snyder, G.K., Measurements of Several Aspects of Immune Function in Toads After Exposure to Low pH, in Modulators of immune responses: the evolutionary trail, Stolen, J.S. et al (eds), Fair Haven, NJ, SOS Publications, 1996.
20. Carey, C., Maniero, G.D. and Stinn, J.F., Effect of Cold on Immune Function and Susceptibility to Bacterial Infection in Toads, in Life in the cold, 10th hibernation symposium, University of New England Press, New South Wales, Australia, 1996.
21. Jancovish, J.D., Davidson E.W., Morado, J.F., Jacobs, B. L., and Collins, J.P., Isolation of a Lethal Virus from the Endangered Tiger Salamander, Ambystoma tigrinum stebbinsi Lowe, Declining Amphibian Populations Task Force Southwestern U.S. Working Group, Abstract, January, 1998.
22. Grifo, F. and Rosenthal, J. (eds.), Biodiversity and human health, Washington, D.C., Island Press, 1997.


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