Parasitism shaping host life-history evolution: adaptive responses in a marine gastropod to infection by trematodes

1. Variation in life-history strategies among conspecific populations indicates the action of local selective pressures; recently, parasitism has been suggested as one of these local forces. 2. Effects of trematode infections on reproductive effort, juvenile growth, size at maturity and susceptibility were investigated among different natural populations of the marine gastropod Zeacumantus subcarinatus, Sowerby 1855. 3. Reproductive effort was not higher in uninfected snails from populations experiencing a high trematode prevalence, but females from high prevalence populations produced significantly larger offspring compared with their conspecifics from other populations. 4. Juvenile growth rate was significantly higher in laboratory-raised snails originating from females in a high prevalence population compared with other populations. 5. Size at maturity, determined by the appearance of functional gonads, was significantly and negatively related to trematode prevalence, and positively related to mean snail size, across 10 populations in the study area. 6. There was no evidence of different host resistance against trematodes in sentinel snails from high and low prevalence populations exposed to the same infection pressure in the field. 7. Our results strongly indicate that Z. subcarinatus adapt to trematodes by reaching maturity early, thereby maximizing their chance of reproducing in populations experiencing a high prevalence of infection by castrating trematodes.     

Environmental factors influencing community composition of gastropods and their trematode parasites in southern Ontario

Agricultural activity and landscape features have previously been associated with diversity and prevalence of trematode species in amphibian second intermediate hosts. In this study, the density, diversity, and size of snail first intermediate hosts, and the diversity and prevalence of their trematode species, were assessed in 2 types of ponds, i.e., those adjacent to cornfields and those from the same region in southwestern Ontario that were adjacent to nonagricultural settings. Species of trematodes included, but were not restricted to, those that are known parasites of larval and adult frogs. We also assessed landscape factors likely to influence use by definitive hosts. Presence of the herbicide atrazine in ponds was measured to check that ponds adjacent to agriculture had potential to be affected by agricultural runoff. Both snail size and the proportion of snails releasing cercariae were greater in nonagricultural ponds, contrasting with a previous finding of lower trematode infection in tadpoles from nonagricultural ponds. Percentage of forest cover was associated with prevalence of certain trematode species, but not with estimates of combined prevalence. Absence of relations of trematode prevalence to measures of road density also contrasted with previous studies. We interpret our results in light of how agricultural activity might influence trematode viability, snail growth, and use by wildlife definitive hosts, independently of landscape factors.     

Opposing selective pressures decouple pattern and process of parasitic infection over small spatial scale

Species face multiple selective pressures that may require opposing responses to mitigate. On rocky shorelines, fitness of the intertidal snail Littorina littorea is determined by both parasitism and predation. We experimentally demonstrated that L. littorea was at greatest risk of infection from trematode parasites high in the intertidal zone where it was in closest proximity to abundant gull feces (the vector for the snail's parasites). However, because of extreme, size‐selective predation pressure at low tidal elevations, small snails often live high in the intertidal until they have grown sufficiently large. By prolonging their exposure to infection higher on the shore, ontogenetic responses to predation risk accentuate parasite risk. Counterintuitively, snails exhibited the highest trematode prevalence at the lowest tidal elevations where they had almost no risk of contracting infection. By carrying contracted infections into the lowest tidal zones, the larger, predation‐resistant snails invert hotspots of infection risk and prevalence, underscoring that size‐dependent selection pressures can decouple infection process and pattern even over small scales.     

Does habitat-specific variation in trematode infection risks influence habitat distribution of two closely related freshwater snails?

Parasitism may be an important factor determining the geographic distribution of closely related species. A habitat-specific risk of parasitism may lead to exclusion of susceptible host types from parasite-rich environments, and promote speciation if it leads to reproductive isolation between susceptible and resistant types. We surveyed populations of the freshwater snail Lymnaea peregra for differences in habitat distribution and trematode parasitism between its two distinct shell morphs, L. ovata and L. peregra. We surveyed 58 populations (43 L. ovata, 15 L. peregra). At each location we recorded an array of habitat characteristics that were summarized using a nonlinear principal components analysis. This yielded two orthogonal habitat score variables. Discriminant analysis with these habitat dimensions indicated that the snail morphs differed in their habitat distribution. L. ovata preferred larger, more permanent natural habitats surrounded by forests, while L. peregra was found more often at a higher altitude, in nonpermanent habitats, often surrounded by meadows. The snails were parasitized by four cercarial types of castrating trematodes. The morphs had a similar prevalence of infection by each of the parasite types, with one exception: monostomid cercariae were found at a higher prevalence in L. ovata than in L. peregra. However, monostomes were rare parasites, and the difference in prevalence of infection was not significant when only populations with monostomes were compared. Our results indicate that variation in the overall prevalence of infection seems to be independent of snail morph, and do not support the idea that a difference in the rate of parasitism might explain differences in the habitat distribution of these snail morphs. Received: 4 January 1999 / Accepted: 30 June 1999     

How Temperature,Pond-Drying,and Nutrients Influence Parasite Infection and Pathology

The rapid pace of environmental change is driving multi-faceted shifts in abiotic factors that influence parasite transmission. However, cumulative effects of these factors on wildlife diseases remain poorly understood. Here we used an information-theoretic approach to compare the relative influence of abiotic factors (temperature, diurnal temperature range, nutrients and pond-drying), on infection of snail and amphibian hosts by two trematode parasites (Ribeiroia ondatrae and Echinostoma spp.). A temperature shift from 20 to 25 °C was associated with an increase in infected snail prevalence of 10–20%, while overall snail densities declined by a factor of 6. Trematode infection abundance in frogs was best predicted by infected snail density, while Ribeiroia infection specifically also declined by half for each 10% reduction in pond perimeter, despite no effect of perimeter on the per snail release rate of cercariae. Both nutrient concentrations and Ribeiroia infection positively predicted amphibian deformities, potentially owing to reduced host tolerance or increased parasite virulence in more productive environments. For both parasites, temperature, pond-drying, and nutrients were influential at different points in the transmission cycle, highlighting the importance of detailed seasonal field studies that capture the importance of multiple drivers of infection dynamics and the mechanisms through which they operate.     

Habitat-specific variation in life-history traits,clonal population structure and parasitism in a freshwater snail (Potamopyrgus antipodarum)

High risk of infection by parasites may select for early reproduction in natural host populations. In a previous study of a freshwater snail (Potamopyrgus antipodarum) we found (1) that different clones of the snail are associated with different depth-structured vegetation zones and (2) that snails in shallow water, where the age-specific risk of infection is highest, mature at a smaller size than snails in deeper habitats. This result suggests that there has been selection for early reproduction in these snails, and that different clonal genotypes have different life-history strategies. Alternatively, the observed life-history variation in the snails might be due to ecological factors that are independent of parasites, but correlated with depth. In the present study, we decoupled parasitism and depth by examining life histories and clonal population structure in a second lake (Lake Tennyson) where the mean prevalence of trematode parasites was low and unrelated to depth. Consistent with the previous results, clones were structured according to vegetation zones in Lake Tennyson. However, we found no relationship between depth and life-history traits, which is inconsistent with the idea that depth-associated factors other than parasites affect snail life histories. Taken together, these results suggest that life-history variation is more likely to result from a depth-specific risk of infection than from depth per se, and that partitioning of habitat zones by different groups of clones may be a general phenomenon in P. antipodarum populations.     

Spatial and temporal structure of the trematode component community in Valvata macrostoma (Gastropoda, Prosobranchia)

We conducted the first comprehensive study on the spatiotemporal structure of trematode communities in the large-mouthed valve snail, Valvata macrostoma. A total of 1103 snails were examined monthly between May and October 2007 from Lake Konnevesi, Central Finland, from a shallow (1-2 m deep) and an offshore site (5-6 m deep), located ca. 50-70 m apart. Snails were infected by 10 trematode species. The species composition and prevalence were strikingly different between the sites with high species diversity in the shallow site (all 10 species; total prevalence of sporocysts/rediae 12.1%, metacercariae 55.4%) compared to the deeper site (3 species; prevalence 15.0% and 1.9%, respectively). This difference persisted throughout our study and is probably related to the spatial distribution of bird definitive hosts, whereas the seasonal parasite dynamics are likely to be affected by changes in the age-structure of the snail population. The probability of sporocyst infections increased with snail size, but no such trend was observed in redial or metacercarial infections which decreased with host size. Our results show that generally well-described spatiotemporal differences in trematode infection of molluscs can emerge in very narrow spatial and temporal scales, which emphasizes the importance of these factors in community studies.     

Structure and temporal variation of trematode and gastropod communities in a freshwater ecosystem.

The infro- and component community dynamics of digenetic trematodes in a freshwater gastropod community were examined over a 33-month period. The gastropod and trematode communities were composed of 17 and 10 species respectively. A total of 9,831 snails was collected; among them, 192 belonging to 14 species were infected by larval trematodes. The size of infected snails was significantly greater than that of healthy ones, and the increase of prevalence with size/age was interpreted as related to the increased probability of ultimately becoming parasitized. The trematode community was rich in allogenic species, but the most frequent trematode (cercariaeum) was autogenic and generalist (a range of 12 snail host species). There was a significantly positive relationship between the frequency of trematode species in the community and the number of first intermediate host species. A great temporal heterogeneity occurred in the prevalence of the snails, mainly attributed to the great temporal fluctuations of snail host populations and the variability of freshwater ecological conditions. The data on the occurrence of larval trematodes in 14 host species over the 33-month study allowed indicate a significant negative correlation between the abundance of gastropods and the prevalence of trematodes.     

Community regulation by herbivore parasitism and density: Trait-mediated indirect interactions in the intertidal

The abundant herbivorous mud-snail Hydrobia ulvae is an ecosystem engineer in soft-bottom intertidal habitats due to its grazing and bioturbation activity. However, mud snails are commonly infected by trematodes that reduce their overall activity, which in turn may affect their impact on the surrounding benthic community. To test this hypothesis, we performed field experiments manipulating both the abundance of uninfected snails (0, 7500 and 15.000 ind. m^- 2) and the level of snail parasitism (0, 33 and 100% trematode prevalence) on a Danish mud-flat. The results showed that increasing snail abundance and parasitism generally had opposite effects on the community of microphytobenthos and zoobenthos. Increasing snail density increased the chlorophyll-a concentration in the substrate (enhancement), whereas increasing parasitism decreased it. In accordance, the benthic primary producers were generally less nutrient limited at high snail density and mostly so at high levels of snail parasitism. Moreover, epipsammic diatoms were favoured over epipelic diatoms at increasing snail density, whereas the opposite was evident at increasing snail parasitism. At the community level, increasing snail density increased evenness among epipelic diatoms, whereas increasing snail parasitism decreased evenness and species diversity. Probably through the action of trophic cascades and varying levels of disturbance, the zoobenthic community was influenced by experimental treatments as well. The indirect effects of snail parasitism influenced significantly the abundance of more faunal species (seven) than did snail density (two). At the community level, increasing snail density decreased evenness and lowest species richness coincided with intermediate snail density. In contrast, increasing snail parasitism resulted in increasing evenness and peaking species richness at intermediate level of parasitism. Together, the results show that parasites solely through their impact on the behaviour of a single community member can be significant indirect determinants of community organisation and function.     

Component community dynamics of larval trematodes in the freshwater snail Semisulcospira nakasekoae in the Uji River, central Japan

The component community of larval trematodes in the freshwater snail Semisulcospira nakasekoae (Caenogastropoda: Sorbeoconcha: Pleuroceridae) was surveyed over 13 months from April 1996 to April 1997 inclusive. Temporal and spatial fluctuation of trematode prevalence, the frequency of multiple infections, and the duration of cercarial shedding were examined as factors that might affect trematode community structure. The spatial prevalence of some species varied significantly, but the dynamics were too small to allow an explanation of the overall pattern. The prevalence of sanguinicolids fluctuated temporally, despite a stable size distribution in the host populations (> 6.0 mm shell width), suggesting the life-cycle phenology of this species. Some pairs of species had statistically positive associations, but no pairs had negative associations. This shows the importance of positive association possibly as a result of suppression of the host defensive response on trematode community structures in molluscan hosts. The length of the patent period, which is part of the persistent period, varied among trematode species, suggesting it to be one of the factors determining prevalence in the host population.     

Leaf litter transport and retention in a tropical Rift Valley stream: an experimental approach

The impact of a drought on freshwater snail and trematode communities was investigated in a lake. Before the drought, 15 gastropod species (Valvatidae, Planorbidae, Lymnaeidae, Ancylidae, Physidae) and 10 trematode species (cercariaeum, xiphidiocercariae, echinostome, furcocercariae, notocotyle, lophocercous) were recorded. The rate of parasitism was 5.13% and there were 11 host species. The 2 major consequences of desiccation were the disappearance of snails, except Valvata piscinalis and Lymnaea peregra, and the absence of trematodes infecting the surviving snails. As soon as favourable conditions were restored, the littoral area was recolonized, first by hygrophilic and amphibious species, second by aquatic species. Nine months after the drought, the gastropod community was restored. Recolonization by the trematodes was delayed compared with that of gastropods. During the study, the overall prevalence was equal to 0.36% and only 4 trematode species and 5 host species were recorded. Because of the great variability of freshwater ecosystems, long-term studies are necessary to understand the dynamics of snail and trematode populations and determine the regulatory effect of parasitism in the field.     

Rapid colonisation of Lymnaea stagnalis by larval trematodes in eutrophic ponds in central Europe

High recruitment rates of multiple species and hierarchical competition are the keys to a competitive exclusion model of community assembly in larval trematode communities in molluscs. Eutrophic environments provide conditions for accelerating trematode transmission and this would increase the strength of interspecific interactions. To test these predictions, we provide the first known assessment for a pulmonate snail host, and for highly productive aquatic environments, of the rates of colonisation and extinction at the level of individual snail host patches, of a large guild of trematode species. Using a uniquely large dataset from a relatively long-term mark-recapture study of Lymnaea stagnalis in six eutrophic fishponds in central Europe, we demonstrate extraordinarily rapid colonisation by trematodes of a snail host, thus meeting the assumptions of the competitive exclusion model. Overall annual colonisation rates ranged from 243% to 503% year⁻¹ so that the odds of trematode establishment in an individual snail in these ponds are two to five times per year. Extinction rates were substantially lower than colonisation rates and, therefore, would not result in turnover rates high enough to significantly affect prevalence patterns in the snail populations. At the species level, analyses of sample-based estimates of probabilities of colonisation revealed that shared species traits associated with transmission and competitive abilities determined the limits of colonisation abilities. Colonisation rates were exceedingly high for the species transmitted to the snails passively via eggs. There was a significant effect of species competitive abilities on colonisation rates due to subordinate species being substantially better colonisers than both strong and weak dominants, a pattern consistent with the predictions of the competition-colonisation trade-off hypothesis. Our results suggest that, with the extraordinarily high trematode colonisation potential in the area studied, the spatial and temporal patterns of intraspecific heterogeneity in recruitment may provide conditions for intensification of interspecific interactions so that complex community assembly rules may be involved.     

Spatial heterogeneity in recruitment of larval trematodes to snail intermediate hosts

Spatial variation in parasitism is commonly observed in intermediate host populations. However, the factors that determine the causes of this variation remain unclear. Increasing evidence has suggested that spatial heterogeneity in parasitism among intermediate hosts may result from variation in recruitment processes initiated by definitive hosts. I studied the perching and habitat use patterns of wading birds, the definitive hosts in this system, and its consequences for the recruitment of parasites in snail intermediate hosts. Populations of the mangrove snail, Cerithidea scalariformis, collected from mangrove swamps on the east coast of central Florida are parasitized by a diverse community of trematode parasites. These parasites are transmitted from wading birds, which frequently perch on dead mangrove trees. I tested the hypothesis that mangrove perches act as transmission foci for trematode infections of C. scalariformis and that the spatial variation of parasitism frequently observed in this system is likely to emanate from the distribution of wading birds. On this fine spatial scale, definitive host behaviors, responding to a habitat variable, influenced the distribution, abundance and species composition of parasite recruitment to snails. This causal chain of events is supported by regressions between perch density, bird abundance, bird dropping density and ultimately parasite prevalence in snails. Variation between prevalence of parasites in free-ranging snails versus caged snails shows that while avian definitive hosts initiate spatial patterns of parasitism in snails through their perching behaviors, these patterns may be modified by the movement of snail hosts. Snail movement could disperse their associated parasite populations within the marsh, which may potentially homogenize or further increase parasite patchiness initiated by definitive hosts.     

Life history cost of trematode infection in Helisoma anceps using mark-recapture in Charlie's Pond

Parasitism has the potential to affect key life history traits of an infected host. Perhaps the most studied interactions are in snail-trematode systems, where infection can result in altered growth rates, survival, and/or fecundity of the individual. Positive correlations between host size and parasite prevalence are often attributed to changes in growth rates or mortality, which have been observed in the laboratory. Extending lab-based conclusions to the natural setting is problematic, especially when environmental conditions differ between the laboratory and the field. The present study uses reproduction experiments and mark-recapture methods to directly measure key life history traits of the pulmonate snail Helisoma anceps in Charlie's Pond. Based on previous laboratory and field experiments on H. anceps, we predict a significant reduction in fecundity, but not growth rate or survival, of infected snails. Individual capture histories were analyzed with multistate models to obtain estimates of survival and infection probabilities throughout the year. Recaptured individuals were used to calculate specific growth rates. Trematode infection resulted in complete castration of the host. However, neither survival nor growth rates were found to differ between infected and uninfected individuals. The probability of infection exhibited seasonal variation, but it did not vary with size of the snail. These results suggest that the correlation between host size and trematode prevalence is not due to differential mortality or changes in growth rates. Instead, the infection accumulates in large snails via the growth of smaller, infected individuals.     

Differential Parasitism of Native and Introduced Snails: Replacement of a Parasite Fauna

The role of parasites in a marine invasion was assessed by first examining regional patterns of trematode parasitism in the introduced Japanese mud snail, Batillaria cumingi (= B. attramentaria), in nearly all of its introduced range along the Pacific Coast of North America. Only one parasite species, which was itself a non-native species, Cercaria batillariae was recovered. Its prevalence ranged from 3 to 86%. Trematode diversity and prevalence in B. cumingi and a native sympatric mud snail, Cerithidea californica, were also compared in Bolinas Lagoon, California. Prevalence of larval trematodes infecting snails as first intermediate hosts was not significantly different (14% in B. cumingi vs 15% in C. californica). However, while the non-native snail was parasitized only by one introduced trematode species, the native snail was parasitized by 10 native trematode species. Furthermore, only the native, C. californica, was infected as a second intermediate host, by Acanthoparyphium spinulosum(78% prevalence). Given the high host specificity of trematodes for first intermediate hosts, in marshes where B. cumingi is competitively excluding C. californica, 10 or more native trematodes will also become locally extinct.     

Indirect effects of a parasite on a benthic community: an experiment with trematodes, snails and periphyton

1. Few studies have directly addressed the role played by parasites in the structure and function of ecosystems. Parasites influence the behaviour, reproduction and overall fitness of their hosts, but have been usually overlooked in community and ecosystem‐level studies. We investigated the effects of trematode parasites on snail–periphyton interactions. 2. Physa  acuta (Gastropoda: Pulmonata) snails infected with the trematode Posthodiplostomum minimum (often >30% of within‐shell biomass) grazed more rapidly than uninfected snails. Trematode effects on snail grazing indirectly affected the standing stock and community structure of periphyton. Populations of snails with 50% infected individuals reduced algal biomass by 20% more than populations with lesser (10% or 0%) infection rates. 3. The alga Cladophora glomerata dominated periphyton communities grazed by snail populations with 50% infection rates, whereas diatoms and blue–green algal taxa dominated when grazed by snail populations with lower infection rates. 4. Thus, trematodes indirectly affected periphyton communities by altering host snail behaviour, a trait‐mediated indirect effect. These results indicate that trematodes can indirectly influence benthic community structure beyond simple population fitness, with possible related effects on ecosystem function.     

Are Sick Individuals Weak Competitors? Competitive Ability of Snails Parasitized by a Gigantism-Inducing Trematode

Parasitized individuals are often expected to be poor competitors because they are weakened by infections. Many trematode species, however, although extensively exploiting their mollusc hosts, also induce gigantism (increased host size) by diverting host resources towards growth instead of reproduction. In such systems, alternatively to reduced competitive ability due to negative effects of parasitism on host performance, larger size could allow more efficient resource acquisition and thus increase the relative competitive ability of host individuals. We addressed this hypothesis by testing the effect of a trematode parasite Diplostomum pseudospathaceum on the competitive ability of its snail host Lymnaea stagnalis. We experimentally examined the growth of snails kept in pairs in relation to their infection status and intensity of resource competition (i.e. food availability). We found that parasitized snails grew faster and their reproduction was reduced compared to unparasitized individuals indicating parasite-induced gigantism. However, growth of the snails was faster when competing with parasitized individuals compared to unparasitized snails indicating reduced competitive ability due to parasitism. The latter effect, however, was relatively weak suggesting that the effects of the parasite on snail physiology may partly override each other in determining competitive ability.     

Factors influencing the distribution of digenetic trematode infections in a mudsnail (Hydrobia ventrosa) population inhabiting salt marsh ponds in Iceland

This study analyzed the influence of several abiotic and biotic variables on the distribution of digenetic trematode infections in a mudsnail, Hydrobia ventrosa, population inhabiting 12 ponds on the Melabakkar salt marsh in Iceland, the northwestern limits of the geographical distribution. Nine trematode species were found to infect the snail population, which included Microphallus pirum, Microphallus breviatus, Microphallus claviformis, Maritrema subdolum (Microphallidae), Cercaria Notocotylidae sp. 11 Deblock, 1980, C. Notocotylidae sp. 12 Deblock, 1980, C. Notocotylidae sp. 13 Deblock, 1980 (Notocotylidae), Cryptocotyle concavum (Heterophyidae), and Psilostomum brevicolle (Psilostomatidae). Correlations between biotic variables (snail density in the ponds and vegetation cover), abiotic variables (distance of each pond from the sea, pond elevation above chart datum, size, average depth, salinity, and some characters of the littoral zone and sediments), and trematode infections were analyzed. These variables indirectly affected the trematode infections because some determined how attractive the ponds were for the final hosts, which were various species of marine and shore birds. We propose that their habitat use and defecating habits are the main determinants of the trematode distribution in the area.     

Pollinator Abundance and Pollen Limitation of a Solanaceous Shrub at Premontane and Lower Montane Sites

Populations at geographic range limits may frequently encounter changing biotic interactions as well as abiotic constraints. A conundrum in plant population biology, the frequent apparent overproduction of flowers, is thought to be a response by plant populations to unpredictable pollinator environments, such as those that may be expected at the range limit. We studied pollinator visitation rates and pollen limitation of fruit set in populations of Witheringia solanacea , a widespread bee-pollinated species. We compared two populations in the south and two in the north of Costa Rica, with each region encompassing a lower montane site at the upper elevational limit of the species range with small plant populations, and a premontane site where population densities were high. Populations in the south, where the climate was favorable, had higher pollinator visitation and higher natural fruit set, and showed only minor pollen limitation as compared with northern populations at windy sites near the Continental Divide. Lower montane populations had lower pollinator visitation rates than premontane populations but did not show more pollen limitation of fruit set. In general, pollen limitation was not inversely proportional to pollinator abundance but was higher where the climate is unpredictable.     

Relationships between nutrient enrichment,pleurocerid snail density and trematode infection rate in streams

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