Synergism between trematode infection and pesticide exposure: A link to amphibian limb deformities in nature?

The apparently rapid increase in the prevalence of amphibian limb deformities has led to substantial interest from ecologists and public health professionals. Hypotheses proposed to explain the deformities fall into two broad categories: chemical contaminants and trematode infection. Although there are convincing experimental demonstrations that certain factors can lead to some deformities, the causes for recent increases in amphibian malformation remain controversial. Moreover, no experimental studies on amphibian deformities have been conducted in the field, and no studies have attempted to examine the synergistic effects of trematode infection and exposure to chemical contaminants. Here, I present the results of field and laboratory experiments that link increased trematode infection, and increased limb deformities, to pesticide exposure. Field experiments conclusively demonstrated that exposure to trematode infection was required for the development of limb deformities in wood frogs, Rana sylvatica. However, deformities were more common at sites adjacent to agricultural runoff. Laboratory experiments corroborated the association between pesticide exposure and increased infection with pesticide-mediated immunocompetency as the apparent mechanism. Given the conservative contaminant exposure levels used [Environmental Protection Agency (EPA) drinking water standards] and the widespread use of many pesticides, these negative impacts may help to explain pathogen-mediated amphibian declines in many regions.

[1]  C. Bridges ECOTOXICOLOGY OF AMPHIBIANS AND REPTILES , 2002, Copeia.

[2]  E. Michael Thurman,et al.  Parasite (Ribeiroia ondatrae) infection linked to amphibian malformations in the western United States , 2002 .

[3]  J. Kiesecker,et al.  Synergism between UV-B radiation and a pathogen magnifies amphibian embryo mortality in nature. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[4]  D. Molyneux,et al.  Vector-borne parasitic diseases--an overview of recent changes. , 1998, International journal for parasitology.

[5]  K. Gosner,et al.  A simplified table for staging anuran embryos and larvae with notes on identification , 1960 .

[6]  R. May,et al.  Infectious Diseases of Humans: Dynamics and Control , 1991, Annals of Internal Medicine.

[7]  Ross A. Alford,et al.  Global Amphibian Declines: A Problem in Applied Ecology , 1999 .

[8]  D. Wake,et al.  Amphibian Declines: Judging Stability, Persistence, and Susceptibility of Populations to Local and Global Extinctions , 1994 .

[9]  P. Epstein Climate and Health , 1999, Science.

[10]  D. Wake Declining Amphibian Populations , 1991, Science.

[11]  S. Sessions,et al.  Morphological clues from multilegged frogs: are retinoids to blame? , 1999, Science.

[12]  C. Scott Findlay,et al.  Quantitative evidence for global amphibian population declines , 2000, Nature.

[13]  Kevin B. Lunde,et al.  MORPHOLOGICAL ABNORMALITY PATTERNS IN A CALIFORNIA AMPHIBIAN COMMUNITY , 2001 .

[14]  P. Dixon,et al.  Ecology: Global amphibian population declines , 2001, Nature.

[15]  D. Stocum Frog limb deformities: an "eco-devo" riddle wrapped in multiple hypotheses surrounded by insufficient data. , 2000, Teratology.

[16]  S. Sessions,et al.  Explanation for naturally occurring supernumerary limbs in amphibians. , 1990, The Journal of experimental zoology.

[17]  D. Gardiner,et al.  Environmentally induced limb malformations in mink frogs (Rana septentrionalis). , 1999, The Journal of experimental zoology.

[18]  D Johnson,et al.  Strategies for assessing the implications of malformed frogs for environmental health. , 1999, Environmental health perspectives.

[19]  John H. Campbell,et al.  Biological response to climate change on a tropical mountain , 1999, Nature.

[20]  Kevin B. Lunde,et al.  The effect of trematode infection on amphibian limb development and survivorship. , 1999, Science.

[21]  P. Daszak,et al.  Emerging infectious diseases of wildlife--threats to biodiversity and human health. , 2000, Science.

[22]  D. Wake,et al.  Hermaphroditic, demasculinized frogs after exposure to the herbicide atrazine at low ecologically relevant doses , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[23]  J. Kiesecker,et al.  Complex causes of amphibian population declines , 2001, Nature.

[24]  D E Green,et al.  Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[25]  J. Kiesecker,et al.  EFFECTS OF DISEASE AND POND DRYING ON GRAY TREE FROG GROWTH, DEVELOPMENT, AND SURVIVAL , 2001 .

[26]  J. Bonin,et al.  HINDLIMB DEFORMITIES (ECTROMELIA, ECTRODACTYLY) IN FREE-LIVING ANURANS FROM AGRICULTURAL HABITATS , 1997, Journal of wildlife diseases.

[27]  D. Wake Action on amphibians. , 1998, Trends in ecology & evolution.

[28]  C. Dissous,et al.  Snail control strategies for reduction of schistosomiasis transmission. , 1998, Parasitology today.

[29]  S. Edwards Biochemistry and Physiology of the Neutrophil , 1994 .