Experimental exposure of juvenile snails (Potamopyrgus antipodarum ) to infection by trematode larvae (Microphallus sp.): infectivity, fecundity compensation and growth

Host-parasite interactions that result in host castration are evolutionarily similar to predator-prey interactions because both interactions terminate reproduction for the host or prey. Yet, host-parasite interactions differ from predator-prey interactions in that infected hosts remain alive and potentially can make adjustments to their life-history strategy before castration is complete. Here we exposed juvenile snails (Potamopyrgus antipodarum) to infection by a digenetic trematode (Microphallus sp.) in order to determine whether: (1) pre-reproductive individuals could be infected, (2) individuals that were exposed to infection shifted resources to early reproduction (fecundity compensation), and (3) infected individuals exhibit altered growth rates relative to uninfected individuals. We found that juveniles are susceptible to infection; hence P. antipodarum could be selected for earlier maturation in populations where the risk of infection is high. We also found that fecundity compensation does not occur in this snail. Finally, we found that Microphallus-infected snails exhibit altered growth rates; individuals infected as juveniles have lower growth rates and are smaller than uninfected snails. These results suggest that growth is altered by infection of a trematode parasite but reproduction in uninfected snails is not induced by exposure to trematode eggs. Received: 11 January 1998 / Accepted: 19 May 1998     

Parasite-induced changes in nitrogen isotope signatures of host tissues

To estimate isotopic changes caused by trematode parasites within a host, we investigated changes in the carbon and nitrogen isotope ratios of the freshwater snail Lymnaea stagnalis infected by trematode larvae. We measured carbon and nitrogen stable isotopes within the foot, gonad, and hepatopancreas of both infected and uninfected snails. There was no significant difference in the delta13C and delta15N values of foot and gonad between infected and uninfected snails; thus, trematode parasite infections may not cause changes in snail diets. However, in the hepatopancreas, delta15N values were significantly higher in infected than in uninfected snails. The 15N enrichment in the hepatopancreas of infected snails is caused by the higher 15N ratio in parasite tissues. Using an isotope-mixing model, we roughly estimated that the parasites in the hepatopancreas represented from 0.8 to 3.4% of the total snail biomass, including the shell.     

Parasite-induced change in host behavior of a freshwater snail: parasitic manipulation or byproduct of infection?

Host behavioral changes due to parasitism are often assumedto be adaptations of the parasite. However, behavioral effectsof parasites may be a generalized response to parasitism andonly coincidentally beneficial for parasite transmission. Forthis reason, alternatives to the manipulation hypothesis shouldbe tested. Previous work demonstrated that the trematode parasiteMicrophallus sp. influences the behavior of the snail Potamopyrgusantipodarum in a way that may increase the probability of transmission.Here I report work conducted to test alternatives to the manipulationhypothesis. In a field study, the effect of Microphallus onbehavior was compared to that of two other castrating parasitegroups to determine if the behavioral change is simply a byproductof parasitism. Also, the foraging behaviors of infected anduninfected snails were examined in the presence and absenceof food resources to determine if the hunger level of Microphallus-infectedsnails could account for the parasite-induced behavioral change.First, Microphallus-infected snails were found on top of rocksduring the day less often than the two other parasite groups. Thisevidence suggests that the behavioral change caused by Microphallusis specific to Microphallus-infected snails. Second, Microphallus-infectedsnails responded to the lack of food differently from uninfectedsnails. Uninfected snails retreated to safer positions underrocks when the food source was removed from the top of the rocks,while Microphallus-infected snails remained on top of the rockswhere the risk of consumption by the final host is greater.Taken together with previous studies, these results suggestthat infection by Microphallus results in behavior that enhancesparasite transmission.     

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

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. Received: 5 September 1997 / Accepted: 19 November 1997     

Save your host,save yourself? Caste‐ratio adjustment in a parasite with division of labor and snail host survival following shell damage

Shell damage and parasitic infections are frequent in gastropods, influencing key snail host life‐history traits such as survival, growth, and reproduction. However, their interactions and potential effects on hosts and parasites have never been tested. Host–parasite interactions are particularly interesting in the context of the recently discovered division of labor in trematodes infecting marine snails. Some species have colonies consisting of two different castes present at varying ratios; reproductive members and nonreproductive soldiers specialized in defending the colony. We assessed snail host survival, growth, and shell regeneration in interaction with infections by two trematode species, Philophthalmus sp. and Maritrema novaezealandense, following damage to the shell in the New Zealand mud snail Zeacumantus subcarinatus. We concomitantly assessed caste‐ratio adjustment between nonreproductive soldiers and reproductive members in colonies of the trematode Philophthalmus sp. in response to interspecific competition and shell damage to its snail host. Shell damage, but not parasitic infection, significantly increased snail mortality, likely due to secondary infections by pathogens. However, trematode infection and shell damage did not negatively affect shell regeneration or growth in Z. subcarinatus; infected snails actually produced more new shell than their uninfected counterparts. Both interspecific competition and shell damage to the snail host induced caste‐ratio adjustment in Philophthalmus sp. colonies. The proportion of nonreproductive soldiers increased in response to interspecific competition and host shell damage, likely to defend the parasite colony and potentially the snail host against increasing threats. These results indicate that secondary infections by pathogens following shell damage to snails both significantly increased snail mortality and induced caste‐ratio adjustments in parasites. This is the first evidence that parasites with a division of labor may be able to produce nonreproductive soldiers according to environmental factors other than interspecific competition with other parasites.     

ADAPTATION BY A PARASITIC TREMATODE TO LOCAL POPULATIONS OF ITS SNAIL HOST

In each of two reciprocal cross-infection experiments, a digenetic trematode (Microphallus sp.) was found to be significantly more infective to snails (Potamopyrgus antipodarum) from its local host populations. This gives strong evidence for local adaptation by the parasite and indicates that there is a genetic basis to the host–parasite interaction. It is suggested that the parasite should be able to track common snail genotypes within populations and, therefore, that it could be at least partially responsible for the persistence of sexual subpopulations of the snail in those populations that have both obligately sexual and obligately parthenogenetic females.     

Effects of UVB on interactions between Schistosoma mansoni and Biomphalaria glabrata

Ultraviolet B (UVB, 280-315 nm) radiation is detrimental to both of larvae of the digenetic trematode Schistosoma mansoni and its snail intermediate host, Biomphalaria glabrata. We explored effects of UVB on three aspects of the interaction between host and parasite: survival of infected snails, innate susceptibility and resistance of snails to infection, and acquired resistance induced by irradiated miracidia. Snails infected for 1 week showed significantly lower survival than uninfected snails following irradiation with a range of UVB intensities. In contrast to known immunomodulatory effects in vertebrates, an effect of UVB on susceptibility or resistance of snails to infection could not be conclusively demonstrated. Finally, exposure of susceptible snails to UVB-irradiated miracidia failed to induce resistance to a subsequent challenge with nonirradiated miracidia, a result similar to that reported previously with ionizing radiation.     

Genomic evidence for population‐specific responses to co‐evolving parasites in a New Zealand freshwater snail

Reciprocal co‐evolving interactions between hosts and parasites are a primary source of strong selection that can promote rapid and often population‐ or genotype‐specific evolutionary change. These host–parasite interactions are also a major source of disease. Despite their importance, very little is known about the genomic basis of co‐evolving host–parasite interactions in natural populations, especially in animals. Here, we use gene expression and sequence evolution approaches to take critical steps towards characterizing the genomic basis of interactions between the freshwater snail Potamopyrgus antipodarum and its co‐evolving sterilizing trematode parasite, Microphallus sp., a textbook example of natural coevolution. We found that Microphallus‐infected P. antipodarum exhibit systematic downregulation of genes relative to uninfected P. antipodarum. The specific genes involved in parasite response differ markedly across lakes, consistent with a scenario where population‐level co‐evolution is leading to population‐specific host–parasite interactions and evolutionary trajectories. We also used an F_ST‐based approach to identify a set of loci that represent promising candidates for targets of parasite‐mediated selection across lakes as well as within each lake population. These results constitute the first genomic evidence for population‐specific responses to co‐evolving infection in the P. antipodarum‐Microphallus interaction and provide new insights into the genomic basis of co‐evolutionary interactions in nature.     

Effects of host condition on susceptibility to infection, parasite developmental rate, and parasite transmission in a snail-trematode interaction

Whether or not organisms become infected by parasites is likely to be a complex interplay between host and parasite genotypes, as well as the physiological condition of both species. Details of this interplay are very important because physiology‐driven susceptibility has the potential to confound genetic coevolutionary responses. Here we concentrate on how physiological aspects of infection may interfere with genetic‐based infectivity in a snail–trematode (Potamopyrgus antipodarum/Microphallus sp.) interaction by asking: (1) how does host condition affect susceptibility to infection? and (2) how does host condition affect the survival of infected individuals? We manipulated host condition by experimentally varying resources. Contrary to our expectation, host condition did not affect susceptibility to infection, suggesting that genetics are more important than physiology in this regard. However, hosts in poor condition had higher parasite‐induced mortality than hosts in good condition. Taken together, these results suggest that coevolutionary interactions with parasites may depend on host condition, not by altering susceptibility, but rather by affecting the likelihood of parasite transmission.     

Co-occurrences of parasite clones and altered host phenotype in a snail-trematode system

The frequent co-occurrence of two or more genotypes of the same parasite species in the same individual hosts has often been predicted to select for higher levels of virulence. Thus, if parasites can adjust their level of host exploitation in response to competition for resources, mixed-clone infections should have more profound impacts on the host. Trematode parasites are known to induce a wide range of modifications in the morphology (size, shell shape or ornamentation) of their snail intermediate host. Still, whether mixed-clone trematode infections have additive effects on the phenotypic alterations of the host remains to be tested. Here, we used the snail Potamopyrgus antipodarum-infected by the trematode Coitocaecum parvum to test for both the general effect of the parasite on host phenotype and possible increased host exploitation in multi-clone infections. Significant differences in size, shell shape and spinosity were found between infected and uninfected snails, and we determined that one quarter of naturally infected snails supported mixed-clone infections of C. parvum. From the parasite perspective, this meant that almost half of the clones identified in this study shared their snail host with at least one other clone. Intra-host competition may be intense, with each clone in a mixed-clone infection experiencing major reductions in volume and number of sporocysts (and consequently multiplication rate and cercarial production) compared with single-clone infections. However, there was no significant difference in the intensity of host phenotype modifications between single and multiple-clone infections. These results demonstrate that competition between parasite genotypes may be strong, and suggest that the frequency of mixed-clone infections in this system may have selected for an increased level of host exploitation in the parasite population, such that a single-clone is associated with a high degree of host phenotypic alteration.     

Effects of diet and<Emphasis Type="Italic"> Echinostoma revolutum</Emphasis> infection on energy allocation patterns in juvenile<Emphasis Type="Italic"> Lymnaea elodes</Emphasis> snails

Resource allocation strategies may be influenced by both biotic and abiotic factors. The purpose of this study was to investigate the effects of both parasitism and diet quality on the growth, reproduction, and survival of the pond snail, Lymnaea elodes. In addition, we assessed parasite growth and reproduction. High-protein (high diet) or low-protein diets (low diet) were fed to juvenile L. elodes snails that were either exposed or sham-exposed to the castrating trematode, Echinostoma revolutum. Host growth was assessed weekly; reproduction and survival were recorded every 2-3 days. We estimated parasite development as the time to parasite release from the host (patency), and parasite reproduction as the number of larvae shed from infected snails at two time points. Diet and infection status had significant effects on snail growth. Infected snails produced few eggs and tended to grow to larger sizes than uninfected snails regardless of diet. In contrast, exposed-uninfected individuals displayed diet-dependent patterns of growth and reproduction. On the high-protein diet, uninfected and exposed-uninfected snails exhibited similar patterns of growth and reproduction, whereas in the low-diet treatment, exposed-uninfected snails exhibited reduced growth and delayed reproduction relative to uninfected individuals. Survival differed among treatments in the latter stages of the study with infected snails exhibiting reduced survival relative to snails from other treatments. Moreover, infected low-diet snails exhibited lower survival than infected high-diet snails. Parasite development and reproduction did not appear to be directly influenced by the quality of host diet. Results from this study suggest that energy allocation patterns are context-dependent in juvenile snails, influenced by parasite exposure and diet quality. Furthermore, parasite reproduction appears to depend more on host size than on the quality of host diet.     

The combined influence of trematode parasites and predatory salamanders on wood frog (<Emphasis Type="Italic">Rana sylvatica</Emphasis>) tadpoles

Predators can have important impacts on host–parasite dynamics. For many directly transmitted parasites, predators can reduce transmission by removing the most heavily infected individuals from the population. Less is known about how predators might influence parasite dynamics in systems where the parasite relies on vectors or multiple host species to complete their life cycles. Digenetic trematodes are parasitic flatworms with complex life cycles typically involving three host species. They are common parasites in freshwater systems containing aquatic snails, which serve as obligate first intermediate hosts, and multiple trematode species use amphibians as second intermediate hosts. We experimentally examined the impact of predatory salamanders (Ambystoma jeffersonianum) and trematode parasites (Echinostoma trivolvis and Ribeiroia ondatrae) on short-term survival of wood frog tadpoles (Rana sylvatica) in 150-L outdoor pools. Two trematode species were used in experiments because field surveys indicated the presence of both species at our primary study site. Parasites and predators both significantly reduced tadpole survival in outdoor pools; after 6 days, tadpole survival was reduced from 100% in control pools to a mean of 46% in pools containing just parasites and a mean of 49% in pools containing just predators. In pools containing both infected snails and predators, tadpole survival was further reduced to a mean of 5%, a clear risk-enhancement or synergism. These dramatic results suggest that predators may alter transmission dynamics of trematodes in natural systems, and that a complete understanding of host–parasite interactions requires studying these interactions within the ecological framework of community interactions.     

How large is the hand in the puppet? Ecological and evolutionary factors affecting body mass of 15 trematode parasitic castrators in their snail host

Parasitic castration is an adaptive strategy where the parasite usurps its host’s phenotype, most notably the host’s reproductive effort. Though castrators are loosely known to be large relative to their hosts (compared to typical parasites), their mass has rarely been quantified and little is known about size variation, even if such variation exists. By cross-sectioning snails, we examined intra- and inter-specific variation in the parasite/host mass of 15 trematode species that castrate the California horn snail, Cerithidea californica. Trematode species occupied 14–39% (mean = 20.3%) of an infected snail’s soft tissue mass. Intraspecific variation in castrator mass fluctuated with variables that covary with energy available for host reproduction. Specifically, trematode mass was 24% higher in summer than in winter, 15% greater in snails from intertidal flats than from tidal channels, and increased with host mass to the 1.37 power (a finding contrary to that previously documented for other types of parasites). Relative body mass differed across trematode species, varying interspecifically with: (1) taxonomic family, (2) host tissue use (larger species used more types of host-tissue), (3) position in the trematode interspecific competitive dominance hierarchy (the two most subordinate species were the largest, otherwise size tended to increase with dominance), and (4) type of host used by offspring (species whose offspring infect relatively predictably occurring benthic invertebrates were larger than those infecting transient vertebrates). Our findings suggest that ecological constraints and life history trade-offs between reproduction and survival influence the mass of these very large parasites.     

Spatial variation in infection by digenetic trematodes in a population of freshwater snails (Potamopyrgus antipodarum)

Larval digenetic trematodes commonly castrate their first intermediate hosts, and should therefore impose strong selection on the timing and mode of host reproduction. Here we examine spatial variation in infection by trematodes in the freshwater snail Potamopyrgus antipodarum. Snails were collected at 11 different sites at Lake Alexandrina on the South Island of New Zealand from transects that ran perpendicular to the shore and across several different habitat types (from 0 to 8 m deep). Logistic regression was used to analyze the relationships between the frequency of trematode infection and snail size, habitat type, and transect location. On average, the probability of infection increased 3.3 times with each 1 mm increase in shell length. Prevalence of infection by the most common species of trematode, Microphallus sp., was highest in the shallow-water habitats where its final hosts (waterflow) spend most of their time. Prevalence of infection by another parasite, Telogaster ophistorchis (final host: eels) increased with depth, but because Microphallus was much more common, total infection by all trematodes decreased with depth. The effects of transect location were minor for Telogaster, but there was significant variation in Microphallus prevalence among transects, especially in the shore-bank habitat. Taken together, these results suggest that the risk of infection is spatially variable, but generally higher in shallow-water habitats, which may explain the greater frequency of sexual individuals as well as earlier reproduction among individuals near shore.     

A trematode parasite alters growth,feeding behavior,and demographic success of invasive rusty crayfish (Orconectes rusticus)

Nonindigenous species can cause major changes to community interactions and ecosystem processes. The strong impacts of these species are often attributed to their high demographic success. While the importance of enemy release in facilitating invasions has often been emphasized, few studies have addressed the role of parasites in the invasive range in controlling demographic success of potential invaders. Here we examine whether a trematode parasite (Microphallus spp.) can contribute to previously documented alternate states in the abundance of invasive rusty crayfish (Orconectes rusticus) in north temperate lakes in Wisconsin, USA. Microphallus infect O. rusticus after emerging from their first intermediate host, a hydrobiid snail. As previously documented, O. rusticus reduce densities of hydrobiid snails through direct predation and destruction of macrophyte habitat. Therefore, if Microphallus substantially reduce O. rusticus fitness, these parasites may reinforce a state of low crayfish abundance, and, at the other extreme, abundant crayfish may repress these parasites, reinforcing a state of high crayfish abundance. From samples collected from 109 sites in 16 lakes, we discovered (1) a positive relationship between crayfish infection intensity and hydrobiid snail abundance, (2) a negative relationship between parasite prevalence and crayfish abundance, and (3) a negative relationship between parasite prevalence and crayfish population growth. With experiments, we found that infection with Microphallus reduced foraging behavior and growth in O. rusticus, which may be the mechanisms responsible for the population reductions we observed. Overall results are consistent with the hypothesis that Microphallus contributes to alternate states in the abundance and impacts of O. rusticus.     

Population dynamics of two snail species,Planaxis sulcatus and Cerithium moniliferum,and their trematode species at Heron Island,Great Barrier Reef

Summary The population dynamics of the prosobranch snail Planaxis sulcatus and its trematode parasites on 600 m of beachrock on the southern side of Heron Island, Great Barrier Reef, were studied. Populations of Planaxis show little mixing, due to lack of long-distance movements. From March 1973 to June 1975, an increase in the numbers of small and medium-sized snails occurred, but the biomass (dry tissue weight) of the snail population did not change. Snails were infected with one species of Aspidogastrea and six species of cerariae. Infections with cercariae did not significantly affect the relative weight of the snails. Multiple infections were random, i.e. neither negative nor positive interactions between trematode species could be demonstrated. Proportions of uninfected snails and snails infected with various trematode species remained more or less constant from July 1973 to February 1975.The population dynamics of the prosobranch snail Cerithium moniliferum and its 11 species of cercariae and one species of Aspidogastrea in a small area at Heron Island were studied. Numbers of large snails decreased and numbers of small snails increased from August 1973 to June 1975. The biomass of the Cerithium population increased only slightly. Prevalence of infection changed significantly only in large snails.Infections of Cerithium moniliferum and Peristernia australiensis with an aspidogastrid species decreased strongly from January 1971 to March/April 1972 and had not recovered by mid 1975.Seasonal fluctuations could not be demonstrated for any of the snails or parasites.The data for Planaxis suggest equilibrium conditions and saturation of the habitat.     

Infection with a trematode parasite differentially alters competitive interactions and antipredator behaviour in native and invasive crayfish

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Larval trematode infections and spatial distributions of snails

Abstract. The hypothesis that infecting trematodes influence the spatial distribution of the estuarine snail Ilyanassa obsoleta was tested. This work was conducted in the Savages Ditch habitat, Rehoboth Bay, DE, USA, which has an essentially flat, sandy-mud bottom bordered by saltmarsh shorelines and many infected snails. In 1996, two groups of snails were individually marked and released from one location after being screened for trematode infections. One group, transplanted from sites where snails tended not to be infected, consisted of snails that tested as uninfected. The other group consisted of snails native to Savages Ditch. Species of trematode carried by each snail was recorded. Marked snails were found and their positions were recorded until 2001. Snails were in five infection categories: (1) not infected, and infected with (2) Himasthla quissetensis , or (3) Lepocreadium setiferoides or (4) Zoogonus rubellus , or (5) with both H. quissetensis and Z. rubellus . The results show that the spatial distributions of snails depended on whether or not they were infected and, if infected, on which trematode species they carried. To complete life cycles, these parasites must accomplish transmission from the first (the snail) to the second intermediate hosts by short-lived, swimming cercariae. These data do not allow resolution of why snails distributed as they did, but sighting distributions of infected snails can be related to distributions of second hosts and it is proposed that parasites engender host snail distributions that improve chances of transmission.     

Parasite prevalence in an intermediate snail host is subject to multiple anthropogenic stressors in a New Zealand river system

Most ecosystems are exposed to multiple stressors acting in concert and their combined effects on parasite prevalence in freshwater, marine and terrestrial habitats are largely unknown. We investigated the relationships between farming intensity, water abstraction intensity and parasite prevalence in the mud snail Potamopyrgus antipodarum from 20 stream sites within the Manuherikia River catchment (New Zealand) by using generalized linear models and an information-theoretic model-selection approach. Three trematode taxa that use water birds as definitive hosts were found in the snail host. The average prevalence of all parasites infecting Potamopyrgus in the catchment was 5%. Microphallus sp. “lively”, the most common parasite, was most prevalent at high farming intensity and low water abstraction, besides showing an antagonistic interaction between the two agricultural stressors. These findings highlight the importance of considering multiple stressors and their potential interactions when studying host–parasite systems. Because snails often play key roles in aquatic communities, providing an important link between primary producers and higher trophic levels, and are a common intermediate host to a high diversity of trematode parasites, this host–parasite model system may represent a promising bioassessment tool for detecting anthropogenic disturbances in freshwater systems.     

THE GEOGRAPHY OF COEVOLUTION: COMPARATIVE POPULATION STRUCTURES FOR A SNAIL AND ITS TREMATODE PARASITE

Gene flow and the genetic structure of host and parasite populations are critical to the coevolutionary process, including the conditions under which antagonistic coevolution favors sexual reproduction. Here we compare the genetic structures of different populations of a freshwater New Zealand snail (Potamopyrgus antipodarum) with its trematode parasite (Microphallus sp.) using allozyme frequency data. Allozyme variation among snail populations was found to be highly structured among lakes; but for the parasite there was little allozyme structure among lake populations, suggesting much higher levels of parasite gene flow. The overall pattern of variation was confirmed with principal component analysis, which also showed that the organization of genetic differentiation for the snail (but not the parasite) was strongly related to the geographic arrangement of lakes. Some snail populations from different sides of the Alps near mountain passes were more similar to each other than to other snail populations on the same side of the Alps. Furthermore, genetic distances among parasite populations were correlated with the genetic distances among host populations, and genetic distances among both host and parasite populations were correlated with “stepping-stone” distances among lakes. Hence, the host snail and its trematode parasite seem to be dispersing to adjacent lakes in a stepping-stone fashion, although parasite dispersal among lakes is clearly greater. High parasite gene flow should help to continuously reintroduce genetic diversity within local populations where strong selection might otherwise isolate “host races.” Parasite gene flow can thereby facilitate the coevolutionary (Red Queen) dynamics that confer an advantage to sexual reproduction by restoring lost genetic variation.