CASE STUDY:

-Declining and Malformed Amphibian Populations
-Emerging Infectious Diseases
-Emerging Infectious Agents
-Amphibian Handout
-Skin Cancer

Declining and Malformed Amphibian Populations

 The recently recognized phenomena of malformed amphibians and declining amphibian populations reveals both the sensitivity of some aquatic organisms to toxins and the complexity of identifying sources of aquatic toxicity (Wake, 1991; Kaiser, 1997). Amphibians had generally been considered unusually resilient species because: they were the first vertebrates to invade terrestrial environments during the Devonian Period, 400 million years ago; they survived the last two major extinction episodes, including the Great Cretaceous Extinction that wiped out the dinosaurs, which had evolved from amphibians; and they had radiated into diverse terrestrial habitats ranging from deserts to rain forests. Therefore, the realization in 1989-1990 that declines in amphibian populations were pandemic and subsequent press reports beginning in 1995 of numerous malformations in amphibians raised new concerns about the pervasive and subtle effects of aquatic toxins (Wake, 1990).

 Those concerns resulted in the establishment of the international Declining Amphibian Populations Task Force (DAPTF, 1998). It has listed the following reasons to justify concerns with the apparent decrease in amphibians:

  1. Declines in amphibian populations may provide a tangible measure of environmental degradation. This may be indicative of a global loss in biodiversity, the destruction of habitats and other species that lead to the loss of amphibians, the toxic effects of ozone depletion, and altered weather patterns associated with global warming.
  2. Declines in amphibian populations may disrupt the ecological balance, since they are both important prey and predators in many food chains.
  3. Extinction of amphibian species may preclude the development of new biomedicinal drugs, which have been derived from amphibian skins.
  4. Many people consider amphibians aesthetic.

 Preliminary findings indicate the complexity in quantifying the problem (Pechmann and Wilbur, 1994). There are large, natural fluctuations in amphibian populations that need to be established through long term monitoring programs to preclude the misinterpretation of preliminary data caused by variations in natural factors (e.g., temperature, rainfall) affecting fecundity (Reading and Clarke, 1995). Moreover, some species may be endangered and others may not within the same location (Blaustein et al., 1994).

 Similarly, there is no single "global" factor that accounts for the pandemic declines in amphibian populations (Table 1-3). Declines on different populations and species have been associated with the loss of aquatic habitats ( Bury et al., 1995) increased ionizing (UV-B) radiation from the depletion of the ozone layer (Blaustein et al., 1997), pesticides and other xenoestrogens (Reeder et al., 1998), acid precipitation, fertilizers, the introduction of exotic competitors and predators, and pathogens (Berger et al., 1998). Surprisingly, "road kills" was found to be a principal cause in one study (Cooke, 1995). Some of these factors are reviewed by Blaustein and Wake (1995).

 

 Table 1-3: Examples of endangered amphibian populations.

 

Species

Proposed Cause

Reference

numerous species

loss of wetlands

Bury et al., 1995

common toad (Bufo bufo)

"road kills"

Cooke, 1995

leopard frog (Rana spp.)

pesticides

Hine et al., 1981

natterjack toad (Bufo calamita)

acid rain

Beebee et al., 1990

cricket frogs (Acris crepitans)

PCBs and PCDFs

Reeder et al., 1998

not specified

fertilizers

USGS (pers. comm.)*

yellow-legged frog (Rana muscosa)

non-native predators

Bradford, 1991

19 species of anurans

chytrid fungus

Berger et al., 1998

Cascades frog (Rana cascadae)

UV-B damage to DNA

Blaustein et al., 1994

Pacific tree frog (Pseudacris regilla)

none**

Blaustein et al., 1994

*Listed in the USGS web site: An Outline of Issues Associated with Amphibian Declines (http://www.mp1-pwrc.usgs.gov/amphib/frogsum.html) in the section titled "Documented Factors Affecting Recent Declines in Amphibians" as (pers. comm. Jeremy Rouse).

 **There is no evidence of declining populations of P. regilla at locations where there are declining populations of R. cascadae (Blaustein et al., 1994).

Mass Deaths of Amphibian Populations from Chytridiomycosis

California    
1970's
Yosemite toad 1
Colorado    
1970's
leopard frog 1
1999
boreal toad 2
Central America    
1994-1999
golden toad 3-6
  Atelopus sp. 6
Arizona    
1996-1997
leopard frog 6
1999
leopard frog 7-8
Australia    
1993-1999
brooding frog 5-7,9
1998-1999
motorbike frog 6-7

1. Carey et al., 1999; 2. D.E. Green, unpublished; 3. Mahoney, 1996;
4. Pounds et al., 1997; 5. Berger et al., 1998; 6. Berger et al., 2000;
7. Morell, 1999; 8. Carey et al., 1999; Daszak et al., 1999;

Table 1. Mass deaths caused by Chytridomycosis in wild populations of amphibians

Table 2. Iridoviruses in amphibians
Figure 2. Electron micrograph of chytridiomycosis
Figure 1a. Acute infection by Batrachochytrium

 Malformed Amphibians

 While reports of malformations in amphibians date back to 1740, concerns over environmental causes of those malformations are much more recent (Sessions, 1998). Those concerns were catalyzed by press accounts of the discovery of a high school science class in 1995 that about 50% of the northern leopard frogs that they collected on a field trip were deformed. Since then, there has been a dramatic increase in the number of reports of deformed amphibians. This has resulted in the establishment of the North American Reporting Center for Amphibian Malformations (NARCAM, 1998).

 

 The concerns were partially allayed by a study indicating high frequencies of limb abnormalities in some amphibians in Aptos, California (Table 1-3) are caused by a parasitic flatworm (Sessions and Ruth, 1990). That trematode uses amphibians as intermediate hosts in its life cycle. The cerearial larval stage of the parasite penetrates the skin of larval frogs (Hyla regilla) and salamanders (Ambystoma macrodactylum), and forms cysts (metaceracarie) that are localized in the cloacal area of the amphibians. There, the cysts mechanically disrupt the amphibian's developing and regenerating limb tissues, resulting in diverse limb abnormalities (including extra digits and limbs). This mechanical disruption has been substantiated in laboratory studies, where similar supernumerary structures were formed in frogs and salamanders after inert resin beads were implanted into their developing limb buds.

 Still, concerns about anthropogenic causes of amphibian malformations persist (Kaiser, 1997). These are supported by field observations of malformations in amphibians in water bodies receiving chemical runoff and by laboratory studies which show that ultraviolet radiation and some chemicals can induce malformations in amphibians. Other studies indicate that some chemicals can reduce the resistance of amphibians to pathogens. Therefore, the relative importance of natural and anthropogenic factors on amphibian malformations remains unresolved.

 Table 1-4. Incidence of amphibian malformations in an Aptos,
California pond in 1986 (from Sessions and Ruth, 1990).

Species

Normal

Malformed

Malformed

Malformations

(n)

(n)

(%)

(types)

Pacific treefrog
(Hyla regilla)

78

202

72

various hind limb abnormalities, extra hind limbs, missing hind and fore limbs

Long-toed salamander
(Ambystoma macrodactylum)

4240

1686

28

various hind and fore limb abnormalities, extra hind and fore limbs, missing digits, extra digits

 

 

Figure 9. Deformed axolotl larva.

Links:

Declining Amphibian Populations Task Force

North American Reporting Center for Amphibian Malformations

USGS Amphibian Declines and Deformities

References:

 Beebee, T.J.C., R.J. Flower, A.C. Stevenson, S.T. Patrick, P.G. Appleby, C. Fletcher, C. Marsh, I. Natkanski, B. Rippet, and R.W. Battarbee. 1990. Decline of the natterjack toad Bufo calamita in Britain: palaeoecological, documentary, and experimental evidence for breeding site acidification. Biological Conservation 53: 1-20.

 Berger, L. et al. 1998. Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proceedings of the national Academy of Sciences 95: 9031-9036.

 Blaustein, A.R., P.D. Hoffman, D.G. Hokit, J.M. Kiesecker, S.C. Wells, and J.B. Wells. 1994. UV repair and resistance to solar UV-B in amphibian eggs: a link to population declines? Proceedings of the National Academy of Sciences 91: 1791-1795.

 Blaustein, A.R. and D.B. Wake. 1995. The puzzle of declining amphibian populations. Scientific American 272: 52-57.

 Blaustein, A.R., J.M. Kiesecker, D.P. Chivers, and R.G. Anthony. 1997. Ambient UV-B radiation causes deformities in amphibian embryos. Proceedings of the National Academy of Sciences 94: 13735-13737.

 Bury, R.B., P. S. Corn, C.K. Dodd, Jr., R.W. McDonald, and N. J. Scott, Jr. 1995. Amphibians. In: our Living Resources, U.S. Department of Interior, Washington, D.C., pp. 124-126.

 Cooke, A.S. 1995. Road mortality of common toads (Bufo bufo) near a breeding site, 1974-1994. Amphibia-Reptilia 16: 87-90.

 DAPTF. 1998. Declining Amphibian Populations Task Force. (http://www.open.ac.uk/daptf/).

 Hine, R.L., B.L. Les, and B.F. Hellmich. 1981. Leopard frog populations and mortality in Wisconsin, 1974-1976. Wisconsin Department of Natural Resources Technical Bulletin 122: 1-39.

 Kaiser, J. 1997. Deformed frogs leap into spotlight at health workshop. Science 278: 2051-2052.

 NARCAM. 1998. North American Reporting Center for Amphibian Malformations http://www.npwrc.usgs.gov/narcam/

 Pechmann, J.H.K. and H.M. Wilbur. 1994. Putting declining amphibian populations in perspective: natural fluctuations and human impacts. Herpetologica 50: 65-84.

 Reeder, A.L., G.L. Foley, D.K. Nichols, L.G. Hansen, B. Wikoff, S. Faeh, J. Eisold, M.B. Wheeler, R. Warner, J.E. Murphy, and V.R. Beasley. 1998. Forms and prevalence of intersexuality and effects of environmental contaminants on sexuality in cricket frogs (Acris crepitans). Environmental Health Perspectives 106: 261-266.

 Sessions, S.K. 1998. Frog deformities. Science 23: 279.

 Sessions, S.K. and S.B. Ruth. 1990. Explanations for naturally occurring supernumerary limbs in amphibians. The Journal of Experimental Zoology 254: 38-47.

 Wake, D.B. 1991. Declining amphibian populations. Science 253: 860.

Emerging Infectious Diseases

The past two decades have seen the emergence of pathogenic infectious diseases which represent a substantial global threat to human health (Lederberg et al., 1992). Clear cut pandemics in wildlife populations are probably rare, but are almost certainly under reported due to a lack of awareness. Historically, wildlife diseases have only been considered important when agriculture or human health have been threatened. Disease emergence most frequently results from a change in ecology of host, pathogen, or both (Schrag and Wiener, 1995). Human encroachment into wildlife habitat in Africa may have been a key factor towards the global emergence of HIV and the Ebola virus (Krause, 1994). EID in wildlife populations is mainly a result of "spill over" from domestic populations. This is especially critical to endangered species with localized populations. The canine distemper virus has been identified in Antarctic and Lake Baikal seals, most likely introduced by infected domistic dogs (sled dogs and local pets, respectively)(Bengston, 1991). Similar strains of morbilliviruses have been identified in dolphin and porpoise die offs around the world (Domingo, 1990).

Introduction of animals and humans to new geographic regons can facillitate the emergence of infectious disease: the translocation of fish and amphibians may have driven the emergence of ranavirus as threats to freshwater fish (Cunningham et al., 1996). Wild mountain gorillas are contracting measles from infected tourists, and poliovirus has killed chimpanzees in the Gombe National Park in Tanzania (Butynski et al., 1998). Normally relatively benign pathogens can be extremely lethal to introduced species. External enironmental changes can also have profound affects. El Nino weather patterns (El Nino Southern Oscillation) have be associated with parasite prevalence and host mortality rates (Grenfell et al., 1998). A newly discovered fungal disease, cutaneous chytridiomycosis, has recently been identified as the cause of amphibian mortality linked to declines in Central American and Australian rain forests. This is the first such disease known to emerge in "pristine" sites, to infect a wide range of hosts, and to cause declinces and possibly extinctions in disparate regions (Morrell, 1999).

This anthropogenic form of invasion, sometimes termed "biological pollution," has caused a loss of biodiversity globally, particularly on oceanic islands (Steadman, 1995). These pathogens have the potential to cause catastrophic depopulation of the new host population. In the first known case of extinction by infection, a microsporidian parasite eliminated the captive remnant population of the Polynesian tree snail, Partula turgida (Cunningham et al., 1998). In addition to diseases, there has been an increase in the reports of toxic algal blooms in the last decade. Cetacean, pinniped, and fish populations have been affected by algal toxins or viral epidemics (Epstein, 1998).

see also: Invasive Species

Bengston, J.L., et al. Marine Mammal Science., 7, 85 (1991)

Butynski, T. M., and J. Kalina. Conservation of Biological Resources, E.J. Milner-Gulland and R. Mace, Eds. (Blackwell Science, Oxford, 1998)

Cunningham, A.A., et al. Philos. Trans. R. Soc. London Ser. B. 351, 1529 (1996)

Cunningham, A.A., and P. Daszak, Conserv. Biol. 12, 1139 (1998)

Domingo, M., et al. Nature 348, 21 (1990)

Epstein, P.R., et al. Marine Ecosystems: Emerging Diseases as Indicators of Change (Harvard Medical School, Boston, MA, 1998). p.85.

Grenfell, B.T. et al. Nature 394, 674 (1998)

Krause, R.M. Journal of Infectious Diseases. 170, 265 (1994)

Lederberg, J., R.E. Shope, S.C. Oakes Jr., Eds. Emerging Infections: Microbial Threats to Health in the United States (Institute of Medicine, National Academy Press, Washington, DC, 1992)

Morrell, V. Science 284, 728 (1999)

Schrag, S.J., and P. Wiener. Trends Ecol. Evol. 10, (1995)

Steadman, D.W. Science. 267, 1123 (1995)

 

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