Laboratory Studies of Parasite Transmission Aspects between Hydrobia spp. (Gastropoda) and Corophium volutator (Amphipoda)

Aspects of parasite transmission between Hydrobia spp. and Corophium volutator, first and second intermediate host of digenetic trematodes, were investigated under laboratory conditions. H. ventrosa is used as an intermediate host by several trematode species. Under laboratory conditions the most frequently observed emergence from H. ventrosa was of cercariae of Maritrema subdolum. The number of cercariae shed per day varied considerably. It was observed that 30 cercariae on average and up to 450 cercariae at maximum can emerge from a single H. ventrosa per day. Cercarial production continued until the death of the snails. The life-span of cercariae of the species M. subdolum decreased as the water temperature increased. It can be concluded that under natural conditions the cercariae, after emerging, have a maximum period of 1 day in which to seek out their second intermediate host C. volutator. Almost all specimens of C. volutator exposed to cercariae of the species M. subdolum died within the test period of 6 days. High average cercarial densities caused short life-spans (<50 h), while at lower densities longer survival times were possible. For cercariae of other Trematoda species, we were unable to find any equally clear evidence of a reduction in the survival rate of C. volutator within the test period. Mortality of C volutator, and other effects of infestation, as observed in our experiment, can be assumed to be a result of the penetration process of the cercariae but they also can be attributed to the mesocercariae.     

Biogeographical patterns of marine larval trematode parasites in two intermediate snail hosts in Europe

Aim We used published inventories of trematodes in Littorina littorea (L.) and Hydrobia ulvae (Pennant) in European seas to search for two basic biogeographical patterns in the spatial occurrence of various trematode species: (1) do parasite distribution and richness patterns in the two host snails overlap with known ecoregions of free‐living organisms; and (2) does trematode species richness in the snails follow latitudinal or longitudinal gradients? Location North East Atlantic. Methods We used multidimensional scaling (MDS), analysis of similarity (ANOSIM) and analysis of variance (ANOVA) to test whether there were overlaps of parasite distribution and richness with known ecoregions of free‐living organisms. In addition, we used linear regression analyses to test whether trematode richness in snails (corrected for sampling effort) was correlated with the latitude or longitude of the sampling sites. Results When corrected for sampling effort, mean trematode species richness per site did not differ among the different ecoregions in L. littorea. In contrast, in H. ulvae, mean species richness was much lower for sites from the Celtic Sea compared with sites from the Baltic Sea and the North Sea. Based on the results of MDS analyses, trematode species composition was distinct among ecoregions; in particular, communities from the Baltic Sea differed markedly from communities in the Celtic Sea, for both snail species. Latitude and longitude were not significantly correlated with parasite species richness in either snail species. Most trematode species had restricted distributions, and only three species in L. littorea and five species in H. ulvae occurred at more than 50% of the sites. Main conclusions There is more structure in the large‐scale distribution of trematodes in gastropods than one would expect from the large‐scale dispersal capabilities of their bird and fish final hosts. We propose mechanisms based both on limited dispersal via fish and bird final hosts and on gradients in environmental factors to explain the observed patterns.     

Fouling of gastropods: a role for parasites?

A sample of mud snails Hydrobia ulvae (Prosobranchia) from an intertidal population revealed that the shells of trematode-infected specimens were especially likely to be fouled with epibionts. Experimentally trematode-infected Biomphalaria glabrata (Pulmonata) appeared to be especially prone to develop epigrowth in comparison with uninfected conspecifics as well. These findings suggest an interaction between trematode infections and epibiosis in aquatic gastropods. The two most likely explanations for this are (1) that trematode infections weakens the snails' natural defences against epibionts, or (2) that the defences against epibionts also are effective against invading trematodes, causing snail specimens with a particularly good fouling defence to be less likely to become infected.     

Predation of the shelduck Tadorna tadorna on the mud snail Hydrobia ulvae

Many waders and ducks rely exclusively on invertebrates for their food and can deplete populations of these invertebrates. The mudsnail Hydrobia ulvae and the shelduck Tadorna tadorna are both widespread and abundant and in previous studies H. ulvae has been identified as the main food source for shelduck. The objective of the study was to quantify the predation of shelduck of H. ulvae on an intertidal mud flat in north Wales in order to estimate the contribution of shelduck predation to H. ulvae mortality and to estimate the importance of H. ulvae in the diet of shelduck. The contribution of shelduck towards the observed mortality was estimated from the number of H. ulvae per dropping, the number of droppings produced per hour and the number of shelduck found at the study site. Shelduck predation hardly made a contribution to the observed mortality of H. ulvae. Examination of the energetic requirements of shelduck shows that H. ulvae cannot be a significant part of the diet. In conclusion, the predation of shelduck on H. ulvae was irrelevant for both the population dynamics of the mud snail and for the energy requirements of shelduck in the study area.     

Character displacement in Hydrobia

Summary Fenchel's study of size variation in Hydrobiid snails in the Limfjord, Denmark, provides one of the most convincing cases of ecological character displacement available. In order to assess the generality of the phenomena within the Hydrobia genus, allopatric and sympatric Hydrobia ventrosa, H. neglecta and H. ulvae were collected from 24 coastal sites around Eastern England in July and October, 1982. Shell heights of 5,850 snails from 55 samples were recorded. These data were analysed for intraspecific allopatric-sympatric, and interspecific height differences. Such differences were not significant for H. ventrosa/H. neglecta, but the species exhibited parallel variation at sympatric sites. H. ventrosa/H. ulvae showed only significant interspecific differences, but in both allopatry and sympatry. The pattern of mean size variation for these species resembles that in the Limfjord. However the statistical analyses fail to provide support for character displacement. Differences in character states attributed to the process of character displacement may result from a number of other causes. Environmental conditions at sympatric and allopatric sites may act differentially on the heights of H. ulvae and H. ventrosa. The conditions that prevail at sympatric H. ulvae sites appear to lead to increased size in this species irrespective of the presence of H. ventrosa.     

The circatidal rhythm of the estuarine gastropod Hydrobia ulvae (Gastropoda: Hydrobiidae)

Intertidal animals display a suite of cyclic behaviours that evolved as adaptations to the predictable cycle of inundation and exposure. In estuarine habitats, mud snails from the genus Hydrobia are among the most abundant grazers, and have received considerable attention with respect to the behavioural mechanisms mediating locomotion, dispersal, and feeding, although the nature of the control of these processes has remained elusive. In particular, it is not clear whether endogenous activity patterns are related to periodic changes of microphytobenthos biomass at the sediment surface, or whether they are timed to the tidal cycle at all. In the present study, we address the crawling activity of Hydrobia ulvae under constant conditions, as well as the effects of individual size and previous short‐term exposure to tides of different range, by recording immersed individual snails under constant dark conditions. We show that the species displays an overt circatidal pattern of crawling, with activity peaks around high water, and that the start of inundation may act as an entrainment agent of the rhythm. Moreover, the results obtained indicate that smaller snails display higher levels of activity, although neither the size nor previous in situ influence of tidal range has an effect on the period and on the amplitude of the rhythm. These findings suggest that fluctuations of microphytobenthos biomass are not a sufficiently strong selective pressure to have shaped locomotor activity in H. ulvae. Moreover, feeding of H. ulvae should take place mostly during high water and be independent of periodic fluctuations of microphytobenthos biomass at the surface of the sediment. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 439–450.     

Impact of trematode parasitism on the fauna of a North Sea tidal flat

The impact of larval trematodes on the fauna of a North Sea tidal flat is considered at the individual and at the population level, depicting the digenean parasites of the common periwinkle,Littorina littorea, and their life cycles, as an example. On the German North Sea coast,L. littorea is first intermediate host for 6 larval trematodes representing 6 digenean families —Cryptocotyle lingua (Heterophyidae),Himasthla elongata (Echinostomatidae),Renicola roscovita (Renicolidae),Microphallus pygmaeus (Microphallidae),Podocotyle atomon (Opecoelidae) andCercaria lebouri (Notocotylidae). All exceptP. atomon utilize shore birds as final hosts; adultP. atomon parasitize in the intestine of teleosts, mainly pleuronectid flatfish. Second intermediate hosts ofC. lingua are various species of fish; the cercariae ofH. elongata encyst in molluscs and polychaetes, those ofR. roscovita in molluscs;M. pygmaeus has an abbreviated life cycle;C. lebouri encysts free on solid surfaces; and the fish trematodeP. atomon utilizes benthic crustaceans, mainly amphipods, as second intermediate hosts. On the tidal flats of the Königshafen (Sylt), up to 77% of the periwinkles have been found to be infested by larval trematodes. Maximum infestations in individual samples were 23% forC. lingua, 47% forH. elongata and 44% forR. roscovita. The digeneans cause complete parasitic castration of their carriers and hence exclude a considerable proportion of the snails from the breeding population. Infestation reduces the longevity of affected hosts, and size-related, trematode-induced differential mortality causes changes in the normal size-frequency distribution of individual snail-age classes. Young flatfishPleuronectes platessa from the Königshafen are 100% infested with metacercariae ofC. lingua. Heavy infestation of the gills causes obstruction of blood vessels and respiratory impairment; metacercariae in the eyes and optic nerves cause visual and neurological disturbances. A single metacercaria is sufficient to kill a larval fish.Mytilus edulis andCardium (Cerastoderma) edule are 100% infested with metacercariae ofH. elongata. Heavy infestation impairs the byssus-thread production in mussels and affects the burrowing ability of cockles. Longevity and resistance to environmental — particularly thermal — stress are reduced in bivalves infested withH. elongata andR. roscovita. There is evidence that, in the study area, population size and age composition of the molluscs discussed are (indirectly) controlled by trematode parasites employing sea birds as final hosts, rather than directly by the predatory activities of these birds.     

Effect of the snail Ilyanassa obsoleta (Say) on dynamics of the amphipod Corophium volutator (Pallas) on an intertidal mudflat

We investigated interactions between two dominant invertebrate species of intertidal soft-sediment environments of the northwest Atlantic, the mud snail Ilyanassa obsoleta and the burrowing amphipod Corophium volutator, on a mudflat of the upper Bay of Fundy, Canada. Distribution of I. obsoleta on the mudflat was highly patchy and negatively correlated with density of C. volutator. Manipulation of snail density in cages showed that I. obsoleta influences C. volutator; specifically, increasing density of snails reduced density, increased patchiness in distribution, decreased recapture rates and decreased immigration of C. volutator. Ilyanassa obsoleta seems to be affecting C. volutator through an influence on survival rate and emigration rate, although temporal variation in these effects was observed. Given that both I. obsoleta and C. volutator show a preference for tide pools, an important microhabitat on mudflats, snails might have a profound impact on C. volutator population dynamics.     

Macroparasite community in molluscs of a tidal basin in the Wadden Sea

We provide a quantitative inventory of macroparasites in intertidal molluscs from a tidal basin in the Wadden Sea (eastern North Sea). Gastropods and bivalves contained a species rich macroparasite community consisting of trematodes (26 species), turbellarians (1), nematodes (1), copepods (2) and polychaetes (1) in 3,800 host individuals from 10 host species. Highest parasite burdens were observed in the gastropods Hydrobia ulvae and Littorina littorea and in the bivalves Cerastoderma edule and Mytilus edulis. In contrast, only one parasite species and no trematodes were found in Crepidula fornicata. The parasite community in the molluscs was similar to other Western European localities but some parasite species showed obvious differences, related to the large-scale distribution of intermediate and final hosts. Parasitism seems to be a common phenomenon in molluscs of the Wadden Sea and hence the detrimental effects observed in experiments can be expected to frequently happen in the field.     

The effect of larval trematodes on the survival rates of two species of mud snails (hydrobiidae) experimentally exposed to desiccation,freezing and anoxia

Digenetic trematodes are widespread among mud snails (Hydrobiidae) living in coastal lagoons and estuaries, but knowledge is generally lacking on their impact on these host organisms. We examined the survival rates of infected and non-infected experimental populations of two mud snail species,Hydrobia ventrosa (Montagu) andHydrobia neglecta Muus, exposed to desiccation, freezing and anoxia in the laboratory. Our experiments indicated that non-infected groups of both species had similar survival rates after being subjected to desiccation and anoxia, whereasH. ventrosa survived freezing better thanH. neglecta. However, infected groups ofH. neglecta specimens subjected to desiccation showed significantly lower survival rates than non-infected groups. Infected and non-infected snails of both species exposed to freezing and anoxia exhibited similar survival rates. The possible mechanisms by which parasites influence their hosts are discussed. It is unlikely that the parasites in the present case mediate the coexistence of the twoHydrobia-species, because the snail with the highest reproductive effort-H. neglecta-showed lower infection rates in situ than its congenerH. ventrosa.     

Differential emigration causes aggregation of the amphipod Corophium volutator (Pallas) in tide pools on mudflats of the upper Bay of Fundy, Canada

We investigated mechanisms responsible for the formation of spatial patterns in a dominant macro-invertebrate, the burrowing amphipod Corophium volutator, in relation to tide pools on intertidal mudflats of the upper Bay of Fundy, Canada. A field survey of 3 different mudflats showed that density of C. volutator at low tide was consistently higher inside than outside tide pools, and a manipulative field experiment indicated that C. volutator selected tide pools over the adjacent emerged areas. Differential survival in immersed and emerged areas at low tide did not explain the observed pattern, because short-term survival of amphipods was not affected by immersion at low tide. As well, immigration rates of C. volutator into immersed and emerged areas at low tide were similar after one day, so preferential settlement did not explain aggregation of amphipods. However, marked C. volutator departed from experimental areas that were immersed at low tide at a slower rate compared to emerged experimental areas. Thus, formation of the spatial pattern observed in the field (higher densities inside tide pools) is likely the result of an effect of immersion at low tide on proportion of individuals emigrating from an area every day.     

Tolerance and Resistance in Gastropod Mollusks Hydrobia ulvaeand H. ventrosafrom the White Sea to Abiotic Environmental Factors

Tolerance to salinity changes and resistance to desiccation, fresh water, and freezing were studied in two hydrobiid species from the White Sea, Hydrobia ulvae(Pennant) and H. ventrosaMontagu. It was shown that H. ventrosahas a greater tolerance to low salinities in the range of 6–10 but is less tolerant to high salinities (35–45). The interspecies differences in low salinity tolerance persisted after the acclimation of snails to 20, 16, and 12. A comparison of survival in fresh water and under desiccation conditions suggests that H. ulvaeis more resistant to these factors. In fresh water, LT₅₀was 30 and 60 days for H. ventrosaand H. ulvae, respectively. Under desiccation conditions, LT₅₀was 6 and 25 days for H. ventrosaand H. ulvae, respectively. At subzero temperatures, H. ventrosawas shown to be a superior survivor. Within the same species of mud snail, the detrimental effect of freezing depended on the salinity: survival decreased with decreasing salinity. These data suggest significant differences in the mechanisms of resistance and tolerance to abiotic environmental factors between the two species. Despite the partial overlapping of their ecological niches, the interspecies differences may play an important role in the distribution and spatial structure dynamics of coexisting populations of these species in the White Sea region.     

Parasites and salinity: costly tradeoffs in a threatened species

Parasites and environmental conditions can have direct and indirect effects on individuals. We explore the relationship between salinity and parasites in an endemic New Mexico State threatened fish, the White Sands pupfish (Cyprinodon tularosa). Spatial variation in salinity limits the distribution of the endemic springsnail (Juturnia tularosae) within Salt Creek, a small desert stream. The springsnail is the presumed intermediate host for trematodes that infect the White Sands pupfish, and trematode prevalence and intensity in pupfish are positively associated with the springsnail. Salinity and parasites both have negative impacts on pupfish, but in areas of high salinity, pupfish can effectively escape parasites. Pupfish trematodes were absent from sites lacking snails. At the upstream site, the absence of parasites and lower variance in salinity were correlated with larger pupfish that were in better condition than pupfish at either the middle or lower sites. Springsnails were present in the middle section, an area with moderate salinity, and all pupfish had trematodes (median abundance 847 trematodes/fish). Lipid levels and condition were lowest in fish from the middle site. Additionally, fewer older fish indicated an increased mortality rate. At the lower site, springsnails were absent due to high salinity; pupfish trematode abundance was much lower (six trematodes/fish), and fish condition was intermediate. An additional experiment revealed that snail activity and survival were significantly reduced at high salinities commonly present at the lower site. Although both high salinity and parasites significantly affect pupfish, parasites might be more detrimental.     

Climate warming may cause a parasite-induced collapse in coastal amphipod populations

Besides the direct impact on the general performance of individual organisms, the ecological consequences of climate change in terrestrial and marine ecosystems are expected to be determined by complex cascading effects arising from modified trophic interactions and competitive relationships. Recently, the synergistic effect of parasitism and climate change has been emphasised as potentially important to host population dynamics and community structure, but robust empirical evidence is generally lacking. The amphipod Corophium volutator is an ecologically important species in coastal soft-bottom habitats of the temperate North Atlantic, and commonly serves as host to microphallid trematodes that cause intensity-dependent and temperature-dependent mortality in the amphipod population. Using a simulation model parameterised with experimental and field data, we demonstrate that a 3.8°C increase in ambient temperature will likely result in a parasite-induced collapse of the amphipod population. This temperature increase is well within the range predicted to prevail by the year 2075 in the International Wadden Sea region from where the model data are obtained. Due to the amphipods’ ecological importance, their population decline may impact the coastal ecosystem as a whole.     

Hemocytes from neonates of Biomphalaria glabrata are functionally less mature than those from adult snails

Gastropod molluscs, which serve as obligatory intermediate hosts for digenetic trematodes, possess an internal defense system (IDS) consisting of phagocytic hemocytes and plasma factors. This IDS is responsible for resistance to infection with larval trematodes, which are encapsulated and killed by hemocytes in incompatible snails. Like other physiological systems, the IDS probably undergoes maturation during early stages of life, and the relatively undeveloped state of the IDS in young snails has been hypothesized to be a factor in their increased susceptibility to infection with larval trematodes. In this study, hemocytes were examined in the BS-90 laboratory strain of Biomphalaria glabrata that is resistant to infection with Schistosoma mansoni as adults but susceptible to infection as neonates. Compared with hemocytes from adults, hemocytes from neonates had a smaller perimeter and lower intrinsic directional motility on glass microscope slides. Additionally, in vitro assays showed a lower association with fucoidan-linked polystyrene beads and less ability to produce superoxide anion in hemocytes from neonates compared to hemocytes from adults. These results support the hypothesis that the gastropod IDS undergoes maturation during growth. However, whether the observed differences between hemocytes of neonatal and adult BS-90 snails play a role in the susceptibility of the former and resistance of the latter to infection with S. mansoni is not known.     

The effects of Relic fauna on initial patch colonisation in a British saltmarsh

When a disturbance impacts an area it rarely leads to a complete defaunation, some individuals survive forming a relic fauna. Relic fauna in azoic patches in an intertidal soft-bottom habitat were simulated by the separate introduction of individuals ofNereis diversicolor, Hydrobia ulvae andLittorina littorea into defaunated cores. These were exposed in the field for 24 hours and the effects of relics on colonisation were assessed separately for colonisation via the sediment surface and colonisation via the surface and laterally through the sediment. After 24 hours all the species in the ambient community were recorded from at least some experimental cores. Densities of the most abundant infaunal taxa,Corophium volutator, Enchytraeus buchholzi, Manayunkia aestuarina, Tubificoides benedeni and nematodes, varied between 1% and 279% of ambient. MDS ordinations showed significant differences in the fauna of experimental cores, a result of the lack of full colonisation by some species and the presence of other species at densities in excess of ambient. Comparisons (ANOSIM and ANOVA) of the fauna of the relic addition cores vs. no-addition cores showed an influence ofN. diversicolor on colonisation. However, this relic effect appeared to be masked by the high degree of variation in colonisation. Densities ofL. littorina andH. ulvae were not maintained in all of the experimental cores and there was no significant difference in the fauna of cores in which the treatments were maintained. It therefore seems that initial colonisation of patches in the emergent saltmarsh is controlled by the (i) supply of colonists and (ii) attraction to under-exploited organic matter and that any relic fauna exerts little influence on the early stages of the colonisation process.     

Different thermal conditions of lakes affect host–parasite systems: A case study of Viviparus contectus (Millet, 1813) and digenean trematodes

1. Thermal disturbance of aquatic ecosystems directly and/or indirectly affects interspecific interactions, including parasitism. Both hosts and parasites respond differently to environmental changes, thus, predicting how host–parasite systems behave under the influence of disturbance remains a challenge. The aim of the study was to check how the differences in thermal conditions of lakes affect life-history traits of hosts and the level of parasitism, using a Viviparus contectus–digenean trematodes model.
2. Overall, we examined 480 individuals of V. contectus collected from a thermally polluted lake (TPL) and a natural lake (NL). Host features, including body size and fecundity, as well as the prevalence and species richness of digenean trematodes in snail populations were investigated.
3. We found that V. contectus from the TPL were significantly larger, heavier, and females were more fertile than snails collected from the NL. A total of 20.4% of the collected snails were infected with digenean larvae. The species richness of parasites was twice as high in the NL compared to the TPL (six and three species, respectively). A significant difference in the percentage of snails infected with parasites was identified between both types of lakes, with a higher prevalence of V. contectus in the NL (31.3%) compared to the TPL (7.3%).
4. These results indicate that host–parasite systems follow the environmental changes in lakes due to thermal pollution by increasing fertility and metabolism rate of viviparid hosts and by decreasing the prevalence and diversity of digenean trematodes.

     

Character displacement and coexistence in mud snails (Hydrobiidae)

Summary Populations of coexisting and of allopatrically occurring species of hydrobiid snails (Hydrobia ulvae, H. neglecta, H. ventrosa and Potamopyrgus jenkinsi) have been studied in 90 localities within three different areas. When H. ventrosa coexists with H. ulvae they show character displacement, i.e., the average body size of the former is smaller and that of the latter is larger. When these species live alone they are of approximately the same size. It is shown here that the size ratio between the coexisting species usually found (1.3–1.5) allows stable coexistence based on food praticles size selectivity alone. Variation in the degree of character displacement from locality to locality is explained by different degrees of genetical isolation of the populations. Coexisting H. ventrosa and H. ulvae have shorter, more well-defined periods of reproduction than they do when they occur alone. H. neglecta is larger than coexisting H. ventrosa and smaller than coexisting H. ulvae. Due to the patchy distribution and the fluctuating populations of this species, and due to the fact that pure H. neglecta populations are rare, data on this species are difficult to interpret. Potamopyrgus jenkinsi shows a different food particle size selection than the Hydrobia spp. of identical sizes. Competitive interactions between P. jenkinsi and coexisting Hydrobia spp. are therefore probably weak. In accordance with this, P. jenkinsi does not show character displacement when coexisting with, e.g., H. ventrosa.The fact that the major study area, the Limfjord, is only 150 years old as a marine habitat as well as various more recent man-made changes of the coast line allow estimates of the time scale of the microevolutionary changes which lead to character displacement.     

Does parasitic infection compromise host survival under extreme environmental conditions? The case for Cerithidea californica (Gastropoda: Prosobranchia)

Summary This laboratory study examined the influence of parasitic infection by larval trematodes on the survival of extreme environmental conditions by the salt marsh snail, Cerithidea californica. Experimental treatments simulated the durations, combinations, and levels of potentially lethal environmental extremes to which the snail is exposed in its natural habitat, as determined from long-term field measurements. No significant difference was found in the rates of mortality suffered by infected and uninfected snails when exposed to simulated natural extremes of water temperature, water salinity, or exposure in air. Exposure to low levels of dissolved oxygen was the only treatment that caused differential mortality: infected snails died at higher rates than uninfected. This differential mortality was accentuated by high water temperature, and varied with the species of infecting parasite. The potential impact of this interaction between parasitism and anoxia on snail survival and population dynamics is discussed.     

Parasitized snails take the heat: a case of host manipulation?

Infection-induced changes in a host’s thermal physiology can represent (1) a generalized host response to infection, (2) a pathological side-effect of infection, or (3), provided the parasite’s development is temperature-dependent, a subtle case of host manipulation. This study investigates parasite-induced changes in the thermal biology of a first intermediate host infected by two castrating trematodes (genera Maritrema and Philophthalmus) using laboratory experiments and field surveys. The heat tolerance and temperatures selected by the snail, Zeacumantus subcarinatus, displayed alterations upon infection that differed between the two trematodes. Upon heating, snails infected by Maritrema sustained activity for longer durations than uninfected snails, followed by a more rapid recovery, and selected higher temperatures in a thermal gradient. These snails were also relatively abundant in high shore localities in the summer only, corresponding with seasonal elevated microhabitat temperatures. By contrast, Philophthalmus-infected snails fell rapidly into a coma upon heating and did not display altered thermal preferences. The respective heat tolerance of each trematode corresponded with the thermal responses induced in the snail: Maritrema survived exposure to 40°C, while Philophthalmus was less heat tolerant. Although both trematodes infect the same tissues, Philophthalmus leads to a reduction in the host’s thermal tolerance, a response consistent with a pathological side effect. By contrast, Maritrema induces heat tolerance in the snail and withstood exposure to high heat. As the developmental rate and infectivity of Maritrema increase with temperature up to 25°C, one adaptive explanation for our findings is that Maritrema manipulates the snail’s thermal responses to exploit warm microhabitats.