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Oecologia

, Volume 135, Issue 3, pp 469–476 | Cite as

Exposure of leopard frogs to a pesticide mixture affects life history characteristics of the lungworm Rhabdias ranae

  • A. D. Gendron
  • D. J. Marcogliese
  • S. Barbeau
  • M.-S. Christin
  • P. Brousseau
  • S. Ruby
  • D. Cyr
  • M. Fournier
Conservation Ecology

Abstract

We tested the hypothesis that exposure of leopard frogs (Rana pipiens) to agricultural pesticides can affect the infection dynamics of a common parasite of ranid frogs, the lungworm Rhabdias ranae. After a 21-day exposure to sublethal concentrations of a pesticide mixture composed of atrazine, metribuzin, aldicarb, endosulfan, lindane and dieldrin, or to control solutions (water, dimethyl sulfoxide), parasite-free juvenile frogs were challenged with 30 infective larvae of R. ranae. Approximately 75% of the larvae penetrated the skin and survived in both exposed and control animals, suggesting that pesticides did not influence host recognition or penetration components of the transmission process. Rather, we found that the migration of R. ranae was significantly accelerated in hosts exposed to the highest concentrations of pesticides, leading to the establishment of twice as many adult worms in the lungs of frogs 21 days post-infection. Pesticide treatment did not influence the growth of lungworms but our results indicate that they matured and reproduced earlier in pesticide-exposed frogs compared to control animals. Such alterations in life history characteristics that enhance parasite transmission may lead to an increase in virulence. Supporting evidence shows that certain components of the frog immune response were significantly suppressed after exposure to the pesticide mixture. This suggests that the immune system of anurans exerts a control over lungworm migration and maturation and that agricultural contaminants can interfere with these control mechanisms. Our results also contribute to the ongoing debate regarding the role that anthropogenic factors could play in the perplexing disease-related die-offs of amphibians observed in several parts of the world.

Keywords

Amphibian Contaminant Parasite infection Rana pipiens Virulence 

Notes

Acknowledgements

Lucie Ménard, Alain Branchaud and Stéphanie Gagné are acknowledged for their assistance in the laboratory and with frog rearing. We are also grateful to Dr Cameron Goater for sharing his expertise with culturing of lungworms and experimental infection of frogs. The image-analysing system of the Université de Montréal was used with permission from Bernadette Pinel-Aloul and technical assistance of Louise Pelletier. We thank Drs Cameron Goater and Robert Poulin, as well as two anonymous reviewers, for commenting on the manuscript. This project received the financial support of the Toxic Substances Research Initiative program (grant no. 46).

References

  1. Alford RA, Richards SJ (1999) Global amphibian declines: a problem in applied ecology. Annu Rev Ecol Syst 30:133–165CrossRefGoogle Scholar
  2. Baker MR (1979a) Seasonal population changes in Rhabdias ranae Walton, 1929 (Nematoda:Rhabdiasidae) in Rana sylvatica of Ontario. Can J Zool 57:179–183Google Scholar
  3. Baker MR (1979b) The free-living and parasitic development of Rhabdias spp. (Nematoda:Rhabdiasidae) in amphibians. Can J Zool 57:161–178Google Scholar
  4. Bollinger TK, Mao J, Shock D, Brigham RM, Chinchar VG (1999) Pathology, isolation and molecular characterization of an iridovirus from tiger salamanders in Saskatchewan. J Wildl Dis 35:413–429PubMedGoogle Scholar
  5. Boroskova Z, Soltys J, Benkova M (1995) Effect of mercury on the immune response and mean intensity of Ascaris suum infection in guinea pigs. J Helminthol 69:187–194PubMedGoogle Scholar
  6. Boroskova Z, Dvoroznakova E (1997) The effect of cadmium on the immune behaviour of guinea pigs with experimental ascariasis. J Helminthol 71:139–146PubMedGoogle Scholar
  7. Bull JJ (1994) Virulence. Evolution 48:1423–1437Google Scholar
  8. Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–593PubMedGoogle Scholar
  9. Carey C, Cohen N, Rollins-Smith L (1999) Amphibian declines: an immunological perspective. Dev Comp Immunol 23:459–472PubMedGoogle Scholar
  10. Carlson EA, Li Y, Zelikoff JT (2002) Exposure of Japanese medaka (Orzias latipes) to benzo-a-pyrene. Aquat Toxicol 56:289–301CrossRefPubMedGoogle Scholar
  11. Christin M-S, Gendron AD, Brousseau P, Ménard L, Marcogliese DJ, Cyr D, Ruby S, Fournier M (in press) Effects of agricultural pesticides on the immune system of Rana pipiens and on its resistance to parasitic infection. Environ Toxicol ChemGoogle Scholar
  12. Cunningham AA, Langton EES, Bennett PM, Lewin JF, Drury SEN, Gough RE, MacGregor SK (1996) Pathological and microbiological findings from incidents of unusual mortality of the common frog (Rana temporaria). Phil Trans R Soc Lond B 351:1539–1557Google Scholar
  13. Daszak P, Berger PL, Cunningham AA, Hyatt AD, Green DE, Speare R (1999) Emerging infectious diseases and amphibian population declines. Emerg Infect Dis 5:1–14PubMedGoogle Scholar
  14. Day T (2001) Parasite transmission modes and the evolution of virulence. Evolution 55:2389–2400PubMedGoogle Scholar
  15. Ebert D, Herre EA (1996) The evolution of parasitic diseases. Parasitol Today 12:96–101CrossRefGoogle Scholar
  16. Esch GW, Fernández JC (1993) A functional biology of parasitism. Ecological and evolutionary implications. Chapman and Hall, New YorkGoogle Scholar
  17. Ewald P (1994) Evolution of infectious disease. Oxford University Press, OxfordGoogle Scholar
  18. Frank SA (1996) Models of parasite virulence. Q Rev Biol 71:37–38Google Scholar
  19. Garnick E (1992) Parasite virulence and parasite-host coevolution: a reappraisal. J Parasitol 78:381–386PubMedGoogle Scholar
  20. Gendron AD, Bishop CA, Fortin R, Hontela A (1997) In vivo testing of the functional integrity of the corticosterone-producing axis in mudpuppy (Amphibia) exposed to chlorinated hydrocarbons in the wild. Environ Toxicol Chem 16:1694–1706Google Scholar
  21. Gilbert M, Leclair RJ, Fortin R (1994) Reproduction of the northern leopard frog (Rana pipiens) in floodplain habitat in the Richelieu River, P. Quebec, Canada. J Herpetol 28:465–470Google Scholar
  22. Giroux I (1999) Contamination de l'eau par les pesticides dans les régions de culture de maïs et de soya au Québec, Campagnes d'échantillonnage de 1996, 1997 et 1998. Ministère de l'Environnement, Direction des écosystèmes aquatiques, QuébecGoogle Scholar
  23. Goater CP (1992) Experimental population dynamics of Rhabdias bufonis (Nematoda) in toads (Bufo bufo): density dependence in the primary infection. Parasitology 104:179–187PubMedGoogle Scholar
  24. Goater CP (1994) Growth and survival of postmetamorphic toads: interactions among larval history, density, and parasitism. Ecology 75:2264–2274Google Scholar
  25. Goater CP, Vandenbos RE (1997) Effects of larval history and lungworm infection on the growth and survival of juvenile wood frog (Rana sylvatica). Herpetologica 53:331–338Google Scholar
  26. Goater CP, Ward PI (1992) Negative effects of Rhabdias bufonis (Nematoda) on the growth and survival of toads (Bufo bufo). Oecologia 89:161–165Google Scholar
  27. Goater CP, Semlitsch RD, Bernasconi MV (1993) Effects of body size and parasite infection on the locomotory performance of juvenile toads, Bufo bufo. Oikos 66:129–136Google Scholar
  28. Gosner VA (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:203–210Google Scholar
  29. Hoole D (1997) The effects of pollutants on the immune response of fish: implications for helminth parasites. Parassitologia 39:219–225PubMedGoogle Scholar
  30. Houlahan JE, Findlay CS, Schmidt BR, Meyer AH, Kuzmin SL (2000) Quantitative evidence for global amphibian population declines. Nature 404:752–755Google Scholar
  31. Institute of Laboratory Animal Resources (1974) Amphibians: guidelines for the breeding, care and management of laboratory animals. National Research Council, Subcommittee on Amphibian Standards, National Academy of Sciences, Washington, D.C.Google Scholar
  32. Kiesecker JM (2002) Synergism between trematode infection and pesticide exposure: a link to amphibian limb deformities in nature? Proc Natl Acad Sci 99:9900–9904CrossRefPubMedGoogle Scholar
  33. Laurance WF, McDonald KR, Speare R (1996) Epidemic disease and the catastrophic decline of Australian rain forest frogs. Conserv Biol 10:406–413CrossRefGoogle Scholar
  34. Luebke RW, Hodson PV, Faisal M, Ross PS, Grasman KA, Zelikoff J (1997) Aquatic pollution-induced immunotoxicity in wildlife species. Fundam Appl Toxicol 37:1–15CrossRefPubMedGoogle Scholar
  35. Maloy WL, Kari UP (1995) Structure-activity studies on magainins and other host defense peptides. Biopolymers 37:105–122PubMedGoogle Scholar
  36. Marcogliese DJ (1997) Fecundity of sealworm (Pseudoterranova decipiens) infecting grey seals (Halichoerus grypus) in the Gulf of St. Lawrence, Canada: lack of density-dependent effects. Int J Parasitol 27:1401–1409CrossRefPubMedGoogle Scholar
  37. Morand S (1996) Life-history traits in parasitic nematodes: a comparative approach for the search of invariants. Funct Ecol 10:210–218Google Scholar
  38. Poulin R, Combes C (1999) The concept of virulence: interpretations and implications. Parasitol Today 15:474–475CrossRefPubMedGoogle Scholar
  39. Read AF, Skorping A (1995) The evolution of tissue migration by parasitic nematode larvae. Parasitology 111:359–371PubMedGoogle Scholar
  40. Riffkin M, Seow H-F, Jackson D, Brown L, Wood P (1996) Defence against the immune barrage: helminth survival strategies. Immunol Cell Biol 74:564–574PubMedGoogle Scholar
  41. Rondeau B (1996) Pesticides dans les tributaires du fleuve Saint-Laurent 1989–1991. Environnement Canada-Région du Québec, Conservation de l'Environnement, Centre Saint-Laurent, MontrealGoogle Scholar
  42. Schallig HDFH (2000) Immunological responses of sheep to Haemonchus contortus. Parasitology 120:S63–S72CrossRefPubMedGoogle Scholar
  43. Soltys J, Boroskova Z, Dvoroznakova E (1997) Effect of concurrently administered copper and mercury on phagocytic cell activity and antibody levels in guinea pigs with experimental ascariasis. J Helminthol 71:339–344PubMedGoogle Scholar
  44. Taylor SK, Williams ES, Mills KW (1999) Effects of malathion on disease susceptibility in Woudhouse's toads. J Wildl Dis 35:635–541Google Scholar
  45. Tinsley RC (1995) Parasitic disease in amphibians: control by regulation of worm burdens. Parasitology 111:S153–S178PubMedGoogle Scholar
  46. Torgensen PR, Llyod S (1992) The B-cells dependence of Haemonchus contortus antigen-induced lymphocyte proliferation. Int J Parasitol 54:244–246Google Scholar
  47. Torgerson PR, Llyod S (1993) The same fractions of Haemonchus contortus soluble antigen induce lymphocyte responses in naive lambs and immune sheep. Res Vet Sci 54:244–246PubMedGoogle Scholar
  48. Vermeer BJ, Hurks M (1996) The clinical immunotoxicity of pesticides. J Toxicol Environ Health 24:149–154Google Scholar
  49. Viney M (2002a) How do host immune responses affect nematode infections? Trends Parasitol 18:63–66CrossRefPubMedGoogle Scholar
  50. Viney M (2002b) Developing worms need the host immune system. Trends Parasitol 18:57CrossRefPubMedGoogle Scholar
  51. Wagner G (1997) Status of the Northern leopard frog (Rana pipiens) in Alberta. Alberta Environmental Protection, Wildlife Management Division, EdmontonGoogle Scholar
  52. Waye HL, Cooper JM (2001) Status of the Northern leopard frog (Rana pipiens) in the Creston valley wildlife management area. Columbia Basin Fish and Wildlife Compensation Program, NelsonGoogle Scholar
  53. Weyts FAA, Cohen N, Flik G, Verburg-van Kemenade BML (1999) Interactions between the immune system and the hypothalmo-pituitary-interrenal axis in fish. Fish Shellfish Immunol 9:1–20CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  • A. D. Gendron
    • 1
  • D. J. Marcogliese
    • 1
  • S. Barbeau
    • 1
  • M.-S. Christin
    • 2
  • P. Brousseau
    • 2
  • S. Ruby
    • 3
  • D. Cyr
    • 2
  • M. Fournier
    • 2
  1. 1.St. Lawrence CentreEnvironment CanadaMontrealCanada
  2. 2.INRS-Institut Armand-FrappierPointe-ClaireCanada
  3. 3.Department of BiologyConcordia UniversityMontrealCanada

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