Anthropogenic factors can have simultaneous positive and negative effects on parasite transmission, and thus it is important to quantify their net effects on disease risk. Net effects will be a product of changes in the survival and traits (e.g., susceptibility, infectivity) of both hosts and parasites. In separate laboratory experiments, we exposed cercariae of the trematode Echinostoma trivolvis, and its first and second intermediate hosts, snails (Planorbella trivolvis) and green frog tadpoles (Rana clamitans), respectively, to one of four common pesticides (atrazine, glyphosate, carbaryl, and malathion) at standardized, ecologically relevant concentrations (201.0, 3700.0, 33.5, and 9.6 microg/L, respectively). We measured effects of pesticide exposure on six mechanisms important to this host-parasite interaction: (1) survival of E. trivolvis cercariae over 26 hours, (2) tadpole survival over two weeks, (3) snail survival over four weeks, (4) snail growth and fecundity, (5) cercarial infectivity, and (6) tadpole susceptibility to a fixed number of cercariae. Pesticides, in general, caused significantly greater mortality of E. trivolvis cercariae than did control treatments, but atrazine was the lone chemical to significantly reduce cercarial survival (LC50 value = 267 mg/L) and then only at concentrations greater than commonly found in aquatic ecosystems (> or =200 microg/L). None of the pesticides significantly enhanced E. trivolvis virulence, decreased tadpole survival, or reduced snail survival, growth, or fecundity. Sublethal exposure of the cercariae to the pesticides (4 h) did not significantly affect trematode encystment in R. clamitans. In contrast, sublethal exposure of R. clamitans to each of the four pesticides increased their susceptibility as measured by the percentage of cercariae that encysted. The reduction in exposure to trematodes due to pesticide-induced cercarial mortality (a density-mediated effect) was smaller than the pesticide-induced increase in amphibian susceptibility (a trait-mediated effect), suggesting that the net effect of exposure to environmentally realistic levels of pesticides will be to elevate amphibian trematode infections. These findings highlight the importance of elucidating the lethal and sublethal effects of anthropogenic factors on both hosts and parasites to understand the mechanisms underlying changes in parasite transmission and virulence, an approach that is especially needed for amphibians, a taxon experiencing global disease-related declines.

https://shell.cas.usf.edu/rohrlab/data/2008%20Rohr%20et%20al.%20Ecol.%20Appl..pdf

Understanding the net effects of pesticides on amphibian trematode infections

Trematodes in the genus Ribeiroia have an indirect life cycle involving planorbid snails as first intermediate hosts, fishes or amphibians as second intermediate hosts and birds or mammals as definitive hosts. Although rarely pathogenic in definitive hosts, Ribeiroia infection can cause severe pathology and mortality in snails and amphibians. This group of parasites has gained notoriety for its prominent rol in the recent rash of amphibian deformities in North America. Under some circumstances, these malformations may enhance parasite transmission by rendering infected amphibian hosts more susceptible to definitive host predators. However, increasing reports of malformations in North American amphibian populations emphasize the importance of understanding infection patterns. Here we review important aspects of the biology, ecology, life cycle and pathogenesis of parasites in the genus Ribeiroia and identify priorities for future research. Based on available morphological descriptions and preliminary molecular data, three species of Ribeiroia are recognized: R. ondatrae in the Americas, R. marini in the Caribbean and R. congolensis/C. lileta in Africa. We further evaluate the influence of abiotic and biotic factors in determining the intensity and prevalence of Ribeiroia infection and malformations in amphibians, highlighting the importance of habitat alteration and secondary factors (e.g. aquatic eutrophication, contaminants) in promoting infection. Although not a "new" parasite, Ribeiroia may have increased in range, prevalence, or intensity in recent years, particularly within amphibian hosts. Nevertheless, while much is known about this intriguing group of parasites, there remains much that we do not know. Particular importance for future research is placed on the following areas: evaluating the phylogenetic position of the genus, establishing the molecular mechanism of parasite-induced malformations in amphibians, isolating the drivers of parasite transmission under field conditions and studying the consequences of malformations for parasite and host populations. Investigation of these questions will benefit enormously from a multidisciplinary approach that effectively integrates parasitology, developmental biology, immunology, herpetology and aquatic ecology.

Review of the trematode genus Ribeiroia (Psilostomidae): ecology, life history and pathogenesis with special emphasis on the amphibian malformation problem.

The effect of echinostome infections on the survival of Rana pipiens tadpoles was examined in relation to developmental stage of tadpoles. Individual tadpoles of Gosner stages 25, 27, 32–33, and 37–39 were exposed to 1 of 4 levels of cercariae (0, 20, 50, or 100). Only tadpoles at stage 25, the earliest stage infected, died within a 5-day experimental period. This stage-specific mortality rate could be explained, in part, by the stage-specific location of encystment of cercariae, which was documented in a separate experiment. In accordance with kidney development, cercariae predominately encysted in the pronephroi during early stages of tadpole development (stages 25 through 31–32) and only in the mesonephroi and associated ducts at later stages (stages 37 through 46). As the mesonephros develops, renal capacity presumably increases. Thus, tadpoles died only when metacercariae concentrated in the functional portion of the kidney with the most limited renal capacity. As tadpoles aged, they also became less...

Relationship of tadpole stage to location of echinostome cercariae encystment and the consequences for tadpole survival.

Using field surveys and experimental infections, we investigated the influence of a trematode parasite on life history traits of adult Lymnaea elodes snails. We found that parasitism significantly affected the growth, fecundity, and survival of host snails. Within five of the six natural L. elodes populations we sampled, shell length of echinostome-infected hosts was significantly greater than for uninfected conspecifics. Furthermore, we show that gigantism occurs among experimentally infected snails due to an accelerated growth rate and size-selective mortality following an Echinostoma revolutum infection. The fecundity of infected snails sharply decreased beginning at 3 weeks post exposure (PE) and all egg production eventually ceased for most hosts by 5–6 weeks PE. Energy constraints, imposed by parasite development, alter the host energy budget. Early in the infection, parasite depletion of host energy reserves reduces host reproduction, but sufficient resources remain to allow accelerated host growth. Mortality was increased among host snails at two distinct stages: shortly after exposure and several weeks after cercariae were first released. We did not observe tissue degradation in snails during the first 4 weeks after exposure to the parasite, but destruction of host tissues was noted among snails dying later in the infection.

Parasite influences on host life history: Echinostoma revolutum parasitism of Lymnaea elodes snails

The increasing threat of emerging infectious diseases in both wildlife and humans has spurred interest in the causes of disease emergence, including the role of anthropogenic change. A prior field study of infection patterns in amphibians suggests that echinostome infection may be an emerging disease of green frogs Rana clamitans living in urbanized environments. We examined the impact of echinostome infection on green frog tadpoles at a wide range of developmental stages (Gosner stage 25–39). Echinostome infection was associated with green frog mortality rates of up to 40% in an early developmental stage, and none in later developmental stages. Tadpoles exposed to higher echinostome doses exhibited higher edema rates, a potential sign of compromised renal function. Histopathological analysis further supported the hypothesis that echinostome-induced tadpole mortality resulted from compromised renal function. Given that the timing of highest cercarial shedding can coincide with the most vulnerable stages of green frog tadpole development, echinostomes could significantly impact green frog survival in nature.

Echinostome infection in green frogs (Rana clamitans) is stage and age dependent

Prevalence of larval trematodes in Helisoma trivolvis (Gastropoda) from a farm pond in Northampton County, Pennsylvania with special emphasis on Echinostoma trivolvis (Trematoda) cercariae

K. A. Schmidt

Papers

Prevalence of larval trematodes in Helisoma trivolvis (Gastropoda) from a farm pond in Northampton County, Pennsylvania with special emphasis on Echinostoma trivolvis (Trematoda) cercariae