Ten polymorphic microsatellite loci for the trematode Gymnophallus sp.

Ten polymorphic loci were isolated and characterized from the intertidal New Zealand trematode Gymnophallus sp., a common parasite of the abundant local bivalve Austrovenus stutchburyi. Observed heterozygosities ranged from 0.17 to 0.96, and three to 23 alleles were detected in 24 trematode metacercariae. These loci are currently being used to investigate the molecular ecology of this species within the bivalve host.     

Host quality and spatial patterning in infections of the Eastern mudsnail (Ilyanassa obsoleta) by two trematodes (Himasthla quissetensis and Zoogonus rubellus)

Several studies have suggested that the fitness of a parasite can be directly impacted by the quality of its host. In such cases, selective pressures could act to funnel parasites towards the highest-quality hosts in a population. The results of this study demonstrate that snail host quality is strongly correlated with spatial patterning in trematode infections and that habitat type is the underlying driver for both of these variables. Two trematodes (Himasthla quissetensis and Zoogonus rubellus) with very different life cycles assume the same spatial infection pattern in populations of the first intermediate host (Ilyanassa obsoleta) in coastal marsh habitats. Infected snails are disproportionately recovered from intertidal panne habitats, which offer more hospitable environs for snails than do adjacent habitats (intertidal creeks, coastal flats, and subtidal creeks), in terms of protection from turbulence and wave action, as well as the availability of food stuffs. Snails in intertidal panne habitats are of higher quality when assessed in terms of average size-specific mass, growth rate, and fecundity. In mark-recapture experiments, snails frequently dispersed into intertidal pannes but were never observed leaving them. In addition, field experiments demonstrate that snails confined to intertidal panne habitats are disproportionately infected by both trematode species, relative to conspecifics confined to adjacent habitats. Laboratory experiments show that infected snails suffer significant energetic losses and consume more than uninfected conspecifics, suggesting that infected snails in intertidal pannes may survive better than in adjacent habitats. We speculate that 1 possible mechanism for the observed patterns is that the life cycles of both trematode species allows them to contact the highest-quality snails in this marsh ecosystem.     

Long-term variation in trematode (Trematoda, Digenea) component communities associated with intertidal gastropods is linked to abundance of final hosts

Trematodes are abundant parasites essential for maintaining stability of marine intertidal ecosystems. Despite the great ecological significance of trematodes, long-term dynamics of their communities remains practically unstudied. This study, based on 12-year-long seasonal monitoring of infection of Littorina and Hydrobia snails with 16 trematode species in the White Sea, aimed to reveal factors determining long-term variation in infection of intertidal snails by trematode parthenitae and larvae. Using the state-of-the-art method of singular spectrum analysis, we revealed trends in this variation and assessed their significance. Interestingly, these trends were not associated with oceanic and climatic parameters but were mostly determined by changes in abundance of the trematode final hosts. Moreover, the prevalence trends turned out to be connected with both large-scale events and local factors at the scale of the intertidal site. The main factors determining the long-term dynamics of the trematode component communities in the study area were the decreasing abundance of birds due to growing anthropogenic disturbance and the increasing abundance of the three-spined stickleback. The analysis of long-term trends of trematode prevalence in intertidal snails may be a sensitive indicator of the abundance dynamics of final hosts in the coastal areas of temperate and northern seas.     

Microsatellite loci for the New Zealand trematode Maritrema novaezealandensis

Seven polymorphic microsatellite loci were isolated and characterized from the coastal New Zealand trematode Maritrema novaezealandensis, an important driving force in the population dynamics of its snail and crustacean intermediate hosts. Observed heterozygosities ranged from 0.33 to 0.82, and three to 17 alleles were detected in 22 trematode sporocysts. These loci will be integral for identifying parasite genetic clones within hosts and addressing a range of questions concerning the molecular ecology of this species.     

Microsatellite loci for the progenetic trematode,Coitocaecum parvum (Opecoelidae)

Nine polymorphic microsatellite loci were characterized from the freshwater trematode Coitocaecum parvum. This parasite can either reproduce sexually in the definitive host or produce eggs by selfing inside its second intermediate host. Two to 11 alleles per locus were detected in 24 trematode sporocysts and observed heterozygosities ranged from 0.04 to 0.96. These loci will be useful for identifying parasite genetic clones within hosts and testing for effects of relatedness on parasite life history strategy.     

Parasites alter host phenotype and may create a new ecological niche for snail hosts

By modifying the behaviour and morphology of hosts, parasites may strongly impact host individuals, populations and communities. We examined the effects of a common trematode parasite on its snail host, Batillaria cumingi (Batillariidae). This widespread snail is usually the most abundant invertebrate in salt marshes and mudflats of the northeastern coast of Asia. More than half (52.6%, n=1360) of the snails in our study were infected. We found that snails living in the lower intertidal zone were markedly larger and exhibited different shell morphology than those in the upper intertidal zone. The large morphotypes in the lower tidal zone were all infected by the trematode, Cercaria batillariae (Heterophyidae). We used a transplant experiment, a mark-and-recapture experiment and stable carbon isotope ratios to reveal that snails infected by the trematode move to the lower intertidal zone, resume growth after maturation and consume different resources. By simultaneously changing the morphology and behaviour of individual hosts, this parasite alters the demographics and potentially modifies resource use of the snail population. Since trematodes are common and often abundant in marine and freshwater habitats throughout the world, their effects potentially alter food webs in many systems.     

Effects of trematode double infection on the shell size and distribution of snail hosts

Infection with larval trematodes sometimes alters the phenotypes of their snail hosts. While some trematode species have distinct effects on host phenotypes, it is still unclear how snail phenotypes are altered when they are parasitized with multiple trematode species. Here, we report that double infection with trematode species averages the effects of parasitic alteration on host phenotype. We found that snail hosts Batillaria attramentaria (Batillariidae) infected with Cercaria batillariae (Heterophyidae) have abnormally large shells and distribute in lower areas of the intertidal zone. Snails with another dominant trematode species, the renicolid cercaria I (Renicolidae), have slightly larger shells and distribute in upper areas of the intertidal zone. A number of double infections with both trematodes was observed in this study. Snails infected with both trematode species exhibited an intermediate size and inhabited a depth between those of snails solely infected with either trematode species, suggesting that the two trematodes simultaneously affected the snail phenotypes. Because altered host phenotypes are frequently beneficial to parasites, two trematode species may compete for successful transmission through alteration of host phenotypes.     

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.     

From first to second and back to first intermediate host: the unusual transmission route of Curtuteria australis (Digenea: Echinostomatidae)

The trematode Curtuteria australis uses the whelk Cominella glandiformis as first intermediate host and the cockle Austrovenus stutchburyi as second intermediate host before maturing in shorebirds. The whelk also happen to be an important predator of cockles on intertidal mudflats. In this study we show that whelks can act as temporary paratenic hosts for the trematode. A single whelk feeding on 1 cockle can ingest large numbers of metacercariae, which remain within the whelk for 1-3 days before passing out in feces. The viability of these metacercariae assessed as the percentage capable of successfully excysting under conditions simulating those inside a bird's digestive tract, is lower after passage through a whelk (48%) than before (59%). Still, given that shorebird definitive hosts prey on whelks as well as cockles, survival inside the whelk allows C. australis to complete its life cycle: overall, though, whelk predation is likely to be an important sink for the trematode population. To our knowledge, this is the first report of a trematode using a snail as both first intermediate host and paratenic host, offering an alternative transmission route for the parasite as a result of the unusual trophic relationships of its hosts.     

Evidence of plasticity in the reproduction of a trematode parasite: the effect of host removal

The parasitic trematode Proctoeces lintoni requires 3 hosts (intertidal mussels, keyhole limpets, and clingfish) to complete its life cycle. The densities and size structure of host communities are modified by selective human harvesting. This study examined clutch and egg size of P. lintoni in 3 adjacent sites in rocky intertidal areas of central Chile presenting differences in the levels of human disturbance (i.e., from a fully protected marine reserve to free open-access areas). We found significant differences in parasite fecundity among sites. An increase in number of eggs was observed inside protected marine areas compared with open-access areas, suggesting a plastic response of the parasite reproductive strategies to the host community modification. These results show that host removal by humans in coastal ecosystems can strongly influence parasite life history traits.     

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.     

Diversity of trematode genetic clones within amphipods and the timing of same-clone infections

The genetic diversity of trematodes within second intermediate hosts has important implications for the evolution of trematode populations as these hosts are utilized after the parasites reproduce asexually within first intermediate hosts and before sexual reproduction within definitive hosts. We characterised the genetic clonal diversity of the marine trematode Maritrema novaezealandensis within amphipod (Paracalliope novizealandiae) second intermediate hosts using four to six microsatellite loci to determine if multiple copies of identical trematode clones existed within naturally infected amphipods. To determine the relative timing of infections by identical clones within hosts, trematode metacercariae were assigned to six developmental stages and the stages of identical clones were compared. The genotypes of 306 trematodes were determined from 44 amphipods each containing more than one trematode. Six pairs of identical trematode clones were recovered in total (representing five amphipods: 11% of amphipods with greater than one trematode) and all pairs of clones belonged to the same developmental stage. This suggests that identical clone infections are effectively synchronous. A general decrease in the number of metacercariae recovered, prevalence, and mean intensity of infection for each subsequent developmental stage coupled with large numbers of metacercariae (>9) only being recovered from recent infections, supports the occurrence of post-infection amphipod mortality and/or within-host trematode mortality. Taken together, our results indicate that natural infections are characterised by high genetic diversity, but that amphipods also periodically encounter "batches" of genetically identical clones, potentially setting the stage for interactions within and between clonal groups inside the host.     

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.     

Local site differences in survival and parasitism of periwinkles (Littorina sitkana Philippi, 1846)

The periwinkle, Littorina sitkana, is found throughout the intertidal zone, often in isolated subpopulations. The majority of trematode parasites use snails as intermediate hosts, and decreased survivorship is often observed in snails infected with trematodes. Sampling L. sitkana from four sites in Barkley Sound, British Columbia, Canada, we test the effects of parasitic infection on snail survival using maximum likelihood and Bayesian approaches using the software MARK and WinBUGS. We found that survival of periwinkles and trematode community composition differed among sites, but survival and trematode prevalence were uncorrelated. WinBUGS performed better than MARK in two ways: (1) by allowing the use of information on known mortality, thus preventing survival overestimation; and (2) by giving more stable estimates while testing the effect of body size on snail survival. Our results suggest that snail survival depends heavily on local environmental factors that may vary greatly within a small geographical region. These findings are important because the majority of experimental studies on survival are done on snails from a single location.     

Effects of ultraviolet radiation on the transmission process of an intertidal trematode parasite

The transmission of parasites takes place under exposure to a range of fluctuating environmental factors, one being the changing levels of solar ultraviolet radiation (UVR). Here, we investigated the effects of ecologically relevant levels of UVR on the transmission of the intertidal trematode Maritrema novaezealandensis from its first intermediate snail host (Zeacumantus subcarinatus) to its second intermediate amphipod host (Paracalliope novizealandiae). We assessed the output of parasite transmission stages (cercariae) from infected snail hosts, the survival and infectivity of cercariae, the susceptibility of amphipod hosts to infection (laboratory experiments) and the survival of infected and uninfected amphipod hosts (outdoor experiment) when exposed to photo-synthetically active radiation only (PAR, 400-700 nm; no UV), PAR+UVA (320-700 nm) or PAR+UVA+UVB (280-700 nm). Survival of cercariae and susceptibility of amphipods to infection were the only two steps significantly affected by UVR. Survival of cercariae decreased strongly in a dose-dependent manner, while susceptibility of amphipods increased after exposure to UVR for a prolonged period. Exposure to UVR thus negatively affects both the parasite and its amphipod host, and should therefore be considered an influential component in parasite transmission and host-parasite interactions in intertidal ecosystems.     

Characterization of microsatellite loci for the littorine snail Bembicium vittatum

We describe the isolation and development of 17 polymorphic microsatellite loci for the intertidal snail Bembicium vittatum (Gastropoda: Littorinidae). The loci were tested in 46 individuals from a single population situated near the centre of the species distribution. No evidence of linkage disequilibrium was detected between any pair of loci. However, two loci showed significant departures from Hardy-Weinberg expectations. The number of alleles per locus ranged from two to 15.     

Contrasting mtDNA diversity and population structure in a direct-developing marine gastropod and its trematode parasites

The comparative genetic structure of hosts and their parasites has important implications for their coevolution, but has been investigated in relatively few systems. In this study, we analysed the genetic structure and diversity of the New Zealand intertidal snail Zeacumantus subcarinatus ( n  =   330) and two of its trematode parasites, Maritrema novaezealandensis ( n  =   269) and Philophthalmus sp. ( n  =   246), using cytochrome c oxidase subunit I gene ( COI ) sequences. Snails and trematodes were examined from 11 collection sites representing three regions on the South Island of New Zealand. Zeacumantus subcarinatus displayed low genetic diversity per geographic locality, strong genetic structure following an isolation by distance pattern, and low migration rates at the scale of the study. In contrast, M. novaezealandensis possessed high genetic diversity, genetic homogeneity among collection sites and high migration rates. Genetic diversity and migration rates were typically lower for Philophthalmus sp. compared to M. novaezealandensis and it displayed weak to moderate genetic structure. The observed patterns likely result from the limited dispersal ability of the direct developing snail and the utilization of bird definitive hosts by the trematodes. In addition, snails may occasionally experience long-distance dispersal. Discrepancies between trematode species may result from differences in their effective population sizes and/or life history traits.     

Local effects of a global problem: modelling the risk of parasite-induced mortality in an intertidal trematode–amphipod system

The interactive effects of climate change and parasitism are of concern because of potentially important consequences for host populations, communities and entire ecosystems. In marine environments, the absence of historic baseline data on parasitism and disease limits our ability to make realistic predictions about these consequences. Here, we adapt a simulation model developed for a Northern Hemisphere intertidal host–parasite system to a comparable system in the Southern Hemisphere. The entire life cycle of the intertidal trematode parasite Maritrema novaezealandensis was modelled in order to investigate the interactive effects of parasitic infections and increasing temperatures on the population dynamics of the amphipod host Paracalliope novizealandiae. Despite uncertainties associated with the model and its parameterisation, most temperature increases that were predicted to cause the collapse of the modelled amphipod population in the long term lay within the range of predicted warming for the study area. The high vulnerability of the amphipods in the modelled system illustrates a potentially important ecological mechanism by which consequences of a global problem might manifest on the local scale.     

Infection patterns in white sea blue mussels Mytilus edulis of different age and size with metacercariae of Himasthla elongata (Echinostomatidae) and Cercaria parvicaudata (Renicolidae)

Infection of mussels Mytilus edulis L. by 2 trematode species was studied in a natural intertidal population in the Chupa inlet of the White Sea. The prevalence of metacercariae of Himasthla elongata (Mehlis, 1831) and Cercaria parvicaudata (Stunkard & Shaw, 1931) in mussels reached 100% in 3 to 4 yr old molluscs and remained at this level in older individuals. Infection intensity increased evenly with the age of the molluscan host, showing a tendency to decrease only in the oldest (9 yr old) mussels. These patterns of age dynamics of prevalence and infection intensity were associated with accumulation of trematode larvae in the course of the molluscs' lives. Ability of metacercariae to exist in mussels for long periods (at least 2.5 yr) was verified in the course of an experiment, during which infected molluscs were kept in a subtidal net cage. Decrease of infection intensity in the oldest individuals may reflect selective mortality of the most severely infected molluscs. Among mussels of the same age, higher infection intensity values occurred in larger individuals. This may be due to an enhanced pumping rate in large molluscs, which increases the probability of cercariae, free-living trematode larvae, infecting them via water currents.     

Ambient fauna impairs parasite transmission in a marine parasite-host system

To understand possible factors controlling transmission of trematode larvae between first and second intermediate hosts we examined the impact of ambient fauna on parasite transmission in a marine intertidal parasite-host association. Cockle hosts (Cerastoderma edule) kept together with selected co-occurring macrozoobenthic species in mesocosms acquired a lower parasite load compared to cockles kept alone, when targeted by cercariae of the trematode Himasthla elongata. The reduction of parasite load in the cockles differed between the 7 macrozoobenthic species tested and was between 35 and 91%. Three different types of reduction could be distinguished: (1) predators (Carcinus maenas, Crangon crangon) actively preying upon cercariae, (2) non-host filter feeders (Crepidula fornicata, Mya arenaria, Crassostrea gigas) filtering cercariae but not becoming infected and (3) alternative hosts (Mytilus edulis, Macoma balthica) becoming infected by the cercariae and thus distracting cercariae from the target hosts. In addition, interference competition may occur in the form of disturbance of cockles by ambient organisms resulting in lower filtration rates and subsequently lower parasite loads. Our results suggest that the species composition and relative abundance of the ambient fauna of parasite-host systems play an important role in controlling trematode transmission rates in benthic marine systems.