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

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.

The cause of global amphibian declines: a developmental endocrinologist's perspective

“…These pesticides also decreased eosinophils and increased encysted cercariae (Telorchis, Ribeiroia) in exposed amphibians (Kiesecker, 2002). Increased infections with parasites in pesticide-exposed amphibians have also been noted for R. ranae (Christin et al, 2003b;Gendron et al, 2003), Ribeiroia (Kiesecker, 2002) and trematode spp. (Rohr et al, 2008c), and Echinostoma trivolvis (Budischak et al, 2008;Rohr et al, 2008b).…”

“…Exposure to atrazine and sodium nitrate decreased peripheral leukocyte levels, and increased infections with Ambystoma tigrinum virus (ATV) in Ambystoma tigrinum nebulosum (Forson and Storfer, 2006a;Forson and Storfer, 2006b). Gendron and others (Gendron et al, 2003) showed that 21days exposure to atrazine, metribuzin, aldicarb, endosulfan, lindane and dieldrin accelerated the migration of parasites into the lungs and increased the number of parasites in the lungs when pesticideexposed R. pipiens were subsequently challenged with the parasite R. ranae. After 7 weeks of development in water with no malathion, tadpoles previously exposed as embryos for only 96h to 60 and 600gl -1 malathion suffered from an increased number of E. trivolvis cysts when compared with controls (Budischak et al, 2008).…”

Repeated and multiple stress (exposure to pesticides) on aquatic organisms

“…Although they identified changes in the cellularity and phagocytic activity of X. laevis and in the lymphocyte proliferation of R. pipiens, suggesting increased susceptibility to infections, it was not possible to determine the relative contributions of the component pesticides or the interactions between them. Similarly, Gendron et al (2003) identified increased migration of lungworm in Rana pipiens exposed to a mixture of atrazine, metribuzin, aldicarb, endosulfan, lindane and dieldrin. Hayes et al (2006) determined the toxicity of individual pesticides at 0.1 ppb (alachlor, atrazine, cyfluthrin, l-cyhalothrin, S metalochlor, metalaxyl, nicosulfuron, propiconazole and tebupirimphos), a mix of all nine pesticides each at 0.1ppb, and that of a combination of atrazine and S-metalochlor at 0.1ppb and 10 ppb to leopard frogs (Rana pipiens) by assessing effects on larval growth and development, sex differentiation and immune function.…”

Comparative Life Cycles and Life Histories of North American Rhabdias Spp. (Nematoda: Rhabdiasidae): Lungworms from Snakes and Anurans

“…Given their lack of study, global distribution, and varied hosts, lungworms appear to be an ideal place to search for life cycle variation. Furthermore, the increasing popularity of lungworms as ideal host-parasite models to test evolutionary principles and ecological interactions (e.g., Goater, 1992Goater, , 1994Goater and Ward, 1992;Christin et al, 2003;Gendron et al, 2003;Dare andForbes, 2008a, 2008b) warrants a greater understanding of the worms' life histories. Our goal is to elucidate and compare the life cycles and life history characteristics of several Rhabdias spp.…”