Snail species diversity impacts the infection patterns of Echinostoma spp.: Examples from field collected data.

Rapid losses of biodiversity due to the changing landscape have spurred increased interest in the role of species diversity and disease risk. A leading hypothesis for the importance of biodiversity in disease reduction is the dilution effect, which suggests that increasing species diversity within a system decreases the risk of disease among the organisms inhabiting it. The role of species diversity in trematode infection was investigated using field studies from sites across the U.S. to examine the impact of snail diversity in the infection dynamics of both first and second intermediate larval stages of Echinostoma spp. parasites. The prevalence of Echinostoma spp. sporocysts/rediae infection was not affected by increases in snail diversity, but significant negative correlations in metacercariae prevalence and intensity with snail diversity were observed. Additionally, varying effectiveness of the diluting hosts was found, i.e., snail species that were incompatible first intermediate hosts for Echinostoma spp. were more successful at diluting the echinostome parasites in the focal species, while H. trivolvis, a snail species that can harbor the first intermediate larval stages, amplified infection. These findings have important implications not only on the role of species diversity in reducing disease risk, but the success of the parasites in completing their life cycles and maintaining their abundance within an aquatic system.

Tranmission pattern differences of miracidia and cercariae larval stages of digenetic trematode parasites.

Digenetic trematodes have complex life cycles involving multiple hosts and free-living larval stages. Some species have 2 lar-val stages that infect snails, with miracidia and cercariae using these molluscs as first and second intermediate hosts, respec-tively. Although both larval stages may infect the same snail species, this is accomplished using different chemical cues and may be influenced by different biotic and abiotic factors. Significant differences in the infection patterns of these parasitic stages regarding host size and density were observed in 2 separate field studies. The prevalence of sporocysts/rediae and mean abundance of Echinostoma spp. metacercariae infection were positively correlated with host size, while the prevalence of Echinostoma spp. cercariae infection was positively correlated with host density across 5 different pulmonate snail species. Larger snails within a given species tend to be older and the increased exposure time may be responsible for the positive correlations with host size. Additionally, infection by miracidia in more vagile snail hosts was influenced by trematode species richness at a sample site, which may be attributed to increased encounter rate as a result of increased movement by the snail hosts. Echinostoma spp. metacercariae prevalence was influenced by host density, possibly due to high abundances of larval clones and their response to more generalized chemical cues attributed to low host specificity by cercariae. Although they can infect the same gastropod hosts, miracidia and cercariae infection are dependent on different factors at both the individual and population level of their snail hosts.

Microhabitat Differences in the Benthic Substrata Affect Parasitism in a Pulmonate Snail Host, Helisoma anceps.

The microhabitats in which hosts live can potentially influence the ability and success of parasites in finding and infecting these hosts. The infection dynamics of both digenetic trematode parasites and a nematode parasite (Daubaylia potomaca) infecting a pulmonate snail, Helisoma anceps , were observed in a small North Carolina lake using 3 different classifications of substratum type based on percent coverage by leaves and debris. There were no differences in snail site occupancy or density between substratum types, but small-scale differences in microhabitat impacted parasite prevalence and intensity in their gastropod hosts. Snails inhabiting substrata covered in more leaf litter and debris had a lower prevalence and intensity of infection by all of the trematode species and life stages when compared to H. anceps inhabiting other substrata types, while only the intensity of infection was impacted in D. potomaca infections. These findings emphasize the importance of microhabitat, specifically its physical components, in influencing parasite infection in intermediate hosts and that small-scale differences may significantly affect the patterns of infection.

Auto-infection by Echinostoma spp. cercariae in Helisoma anceps.

Auto-infection is a life history strategy used by many parasitic organisms, including digenetic trematodes. The process of autoinfection most frequently involves the transfer of a life cycle stage of the parasite from one site to another inside the same host, usually accompanied by morphological transformation. Moreover, among trematodes, the stage being transferred may also move from one host to another in completing the life cycle, i.e., an indirect cycle. Echinostoma spp. parasites offer the opportunity to study auto-infection because they utilize gastropods as both first and second intermediate hosts. Rejection of a null model predicting independent infection of first and second intermediate larval stages coupled with the presence of rediae being the best predictor of metacercariae prevalence and intensity suggests that auto-infection by Echinostoma spp. cercariae is occurring in their molluscan hosts. Shell length was also found to be a significant predictor of metacercariae intensity in the snails hosts, but this is most likely attributed to larger snails being more commonly infected with Echinostoma spp. rediae as opposed to an increased likelihood of cercariae infection. Auto-infection as a life history strategy increases transmission success of the parasite, but may also have negative consequences for the parasite that necessitate auto-infection coupled with the release of cercariae to maximize transmission success and host survival.

Catastrophic collapse of the larval trematode component community in Charlie's Pond (North Carolina).

In 1984, work on the parasite population and community ecology in the pulmonate snail, Helisoma anceps , was initiated in Charlie's Pond (North Carolina). Similar research on Physa gyrina was started in 1986. When study in the pond began in 1984, 8 species of larval trematodes were being shed from Hel. anceps. By far, the dominant species was Halipegus occidualis , with prevalences generally ∼60%, except during midsummer, when older snails were dying. For the other 7 trematode species being shed, prevalences were consistently less than 4%. By 2006, 18 species had been identified in Hel. anceps at one time or another. In 1986, Hal. eccentricus was discovered in P. gyrina , with a prevalence of ∼49%. Through 2006, 7 trematodes were found to be shedding cercariae from P. gyrina . Halipegus eccentricus disappeared from the pond in 1998. From March through November of 2012 and 2013, 1,292 Hel. anceps and 716 P. gyrina were collected, using collection protocols that were identical to those used from 1984 through 2006. In 2012, 5 trematode species, including Hal. occidualis, were present in Hel. anceps at one time or another. During the last part of the 2012 collecting season cercariae of just 2 species were being shed from Hel. anceps (and 1 from P. gyrina ). In 2013, only cercariae of Haematoloechus longiplexus and Uvulifer ambloplitis were observed from Hel. anceps. The latter species was lost by 2014, and an echinostome was present (2.1%); a single snail was infected with Haem. longiplexus. Four species were being shed from P. gyrina , i.e., Echinoparyphium sp. (7.9%), Glypthelmins sp. (1.5%), Plagiorchis sp. (4.9%), and Posthodiplostomum sp. (7.4%). Rarefaction curves were generated for Hel. anceps shedding in 1984, 1988, 1989, 2002, 2006, and August of 2014. The data clearly indicate that species diversity was constantly declining over the 31-yr period. We did not include P. gyrina in the analysis since data for this snail species were not acquired until 1991-1992. At present, we have no definitive explanation for the decrease in diversity, although circumstantial evidence suggests that it might be related to periodic declines in water level that negatively affected the colonization and maintenance of emergent vegetation within the pond.

Differences in snail ecology lead to infection pattern variation of Echinostoma spp. larval stages.

The infection patterns of parasites are often tied to host behavior. Although most studies have investigated definitive hosts and their parasites, intermediate host behavior may play a role in shaping the distribution and accumulation of parasites, particularly the larval stages. In an attempt to answer this question, more than 4,500 pulmonate snails were collected from 11 states in the mid-Atlantic and Midwestern United States in the summer of 2012. These snails were necropsied and echinostome metecercariae were commonly observed infecting the snails as 2(nd) intermediate hosts (20.0%). The snails included species of 3 genera with distinct differences in the infection patterns of Echinostoma spp. metacercariae among them. Physa spp. (comprising of P. acuta and P. gyrina) snails exhibited a significantly higher prevalence of infection (23.5%) than both Lymnaea columella (11.6%) and Helisoma spp. (comprising of H. anceps and H. trivolvis) (14.2%; P < 0.05), with no difference in prevalence observed between the latter 2 genera (P > 0.05). The intensity of metacercariae within the snail hosts was significantly different between the 3 genera (P < 0.05), with L. columella having the highest intensity (24.3 ± 5.6), followed by Physa spp. (15.2 ± 1.5) and Helisoma spp. (5.0 ± 0.9). Differences in prevalence and intensity were also observed when the different snail families co-habited the same body of water. The disparities in infection patterns are likely due to distinct differences in the behavioral and feeding ecology of the snail hosts.

Shedding patterns of Daubaylia potomaca (Nematoda: Rhabditida).

Daubaylia potomaca is a nematode parasite that exhibits an unusual direct life cycle in planorbid snails in which adult females are the infective stage, after being shed from a definitive host. The present study examined the shedding patterns of this nematode to determine what cues or mechanisms might lead to the parasite leaving its host. A correlation was found between host death and the frequency and number of D. potomaca shed, suggesting that the nematodes can detect that the host is dying and may leave in search of a new host. Furthermore, elevated intensities of D. potomaca in the snail induce shedding earlier, suggesting that competition for space and resources may also play a role in the shedding patterns of the nematode, but not when time to death is controlled. Finally, nematodes shed a longer time before host death were significantly longer and more likely to be gravid than those shed as time to snail death approached, implying that the nematode reaching maturity or being inseminated might also be cues for D. potomaca to leave its snail host. In summary, the shedding patterns of D. potomaca appear to be a complex mix of host death detection, competition, and nematode maturation.

Population and infection dynamics of Daubaylia potomaca (Nematoda: Rhabditida) in Helisoma anceps.

Daubaylia potomaca is an unusual parasite for several reasons. Specifically, it has a direct life cycle in which it uses a planorbid snail, Helisoma anceps , as the definitive host. In addition, adult females have been shown to be both the infective stage and the only stage documented to be shed from a live, infected host. Finally, adults, juveniles, and eggs have been observed in all tissues and blood spaces of the host, suggesting the parasite consumes and actively migrates through host tissue. The present study examined the population and infection dynamics of D. potomaca in Mallard Lake, a 4.9-ha public access pond in the Piedmont region of North Carolina. In particular, the study examined the role of seasonality on the prevalence and mean intensity of infection of D. potomaca in the snail host. Data collected from August 2008 to October 2009 suggest that prevalence and mean intensity were inversely related in the spring and fall. Prevalence in fall 2008 was 10.3% but increased to 47.3% in spring 2009. Conversely, intensity was high in fall 2008 at 52.4 ± 8.9 worms/infected host but dropped to 3.1 ± 0.3 worms/infected host in spring 2009. During the same time, the parasites within the snails went from highly aggregated populations in the fall to a less aggregated distribution in the spring. It is hypothesized that D. potomaca induces mortality of the snail hosts during the winter, followed by a rapid recruitment event of the nematodes by the snail population after torpor.

Complex interactions among a nematode parasite (Daubaylia potomaca), a commensalistic annelid (Chaetogaster limnaei limnaei), and trematode parasites in a snail host (Helisoma anceps).

Many biotic interactions can affect the prevalence and intensity of parasite infections in aquatic snails. Historically, these studies have centered on interactions between trematode parasites or between trematodes and other organisms. The present investigation focuses on the nematode parasite Daubaylia potomaca and its interactions with a commensal, Chaetogaster limnaei limnaei , and a variety of trematode species. It was found that the presence of C. l. limnaei indirectly increased the mean intensity of D. potomaca infections, apparently by acting as a restraint for various trematode parasites, particularly the rediae of Echinostoma sp. In turn, Echinostoma sp. rediae adversely affected the mean intensity of D. potomaca by their consumption of both juvenile and adult nematodes present in tissues of the snail. These organisms not only belong to 3 different phyla but occupy distinct trophic levels as well. The complex interactions among these 3 organisms in the snail host provide an excellent example of biotic interactions influencing the infection dynamics of parasites in aquatic snails.

The unusual life cycle of Daubaylia potomaca, a nematode parasite of Helisoma anceps.

Daubaylia potomaca is a parasitic nematode that exhibits a direct life cycle using planorbid snails as their only host. Within the snail host Helisoma anceps , all developmental stages of the parasite are present at any given time. The nematode has an unusual life cycle, with the adult female being the infective stage rather than the third-stage larvae (L(3)), as is commonly the case in many other parasitic nematode life cycles. In addition, length analysis showed that L(1) and L(2) were not present in tissues, suggesting that larvae hatch from eggs as the L(3). Previous studies by other investigators show that adult females abandon Biomphalaria glabrata at some point between 3 and 9 days of host death; in the present study, adult female D. potomaca leave H. anceps up to 59 days (and a mean of 14.8 days) before host death. This observation indicates a striking physiological difference between an experimental and a natural host for the parasite.