Controls of Spatial Variation in the Prevalence of Trematode Parasites Infecting a Marine Snail (original) (raw)

Relating bird host distribution and spatial heterogeneity in trematode infections in an intertidal snail—from small to large scale

Marine Biology, 2006

Shorebird abundance and spatial distribution of larval trematodes in the New Zealand mudsnail, Zeacumantus subcarinatus, were investigated in soft-sediment intertidal bays within Otago Harbour, South Island, New Zealand. In a small-scale study, recruitment of trematodes to caged sentinel snails and the prevalence of infection in free-living snails were examined across a grid of fifteen 50·25 m plots arranged in a representative area of an intertidal bay, in relation to within-plot shorebird abundance (definitive hosts) and tidal height. In a large-scale study, natural spatial variation of larval trematodes in Z. subcarinatus was examined across 12 bays in relation to local abundance of shorebirds. Our results revealed that trematode prevalence in snails was positively correlated with bird abundance across bays (R 2 =0.503, P=0.006). In contrast, despite a difference in bird abundance between tidal heights, there was no evidence that trematode prevalence reflected the spatial distribution of birds in the small-scale study, suggesting that factors related to differences in submersion time may override the differential input of trematode eggs from birds.

Trematode prevalence-occupancy relationships on regional and continental spatial scales in marine gastropod hosts

Marine Ecology Progress Series, 2013

The positive inter-specific relationship between local abundance and large-scale spatial occupancy is one of the most universal patterns in the distribution of species. However, evidence for the validity of this relationship in the marine realm is still scarce, especially for parasites. Using data from published studies, we investigated this relationship in trematode parasites infecting several marine gastropod species. On a regional spatial scale (<100 km between any pair of sites), we found a positive relationship between mean local prevalence (percentage of infected individuals in a population) and large-scale site occupancy among trematode species in all 4 gastropod host species investigated (Littorina obtusata, L. saxatilis, Hydrobia ventrosa, Ilyanassa obsoleta), although this was not significant in the case of L. saxatilis. Similar positive relationships were observed on a continental scale (>1000 km between the most distant sites) in 2 host species (L. littorea, H. ulvae). Further analyses pointed to the role of dispersal by the definitive hosts in shaping these prevalence−occupancy relationships as we found a significant interaction between definitive host type and mean local prevalence affecting the spatial occupancy of the trematodes infecting H. ulvae. While trematode species that use highly dispersive birds as definitive hosts exhibited a significant positive relationship, the ones that use less dispersive fish did not. Our results indicate that a positive relationship between local abundance and large-scale distribution also holds true for marine parasites, and they suggest a strong role of definitive host dispersal in linking local epidemiological infection patterns of parasites with their large-scale biogeographic distributions.

Habitat influences snail community structure and trematode infection levels in a spring-fed river, Texas, USA

Hydrobiologia, 2008

The spring-fed Comal River in Texas, USA, has been impounded and channelized resulting mainly in a lentic environment with four headwater spring runs. We sampled two spring runs (lotic sites) and two lentic sites seasonally from April 2001 through April 2002 to assess (1) co-occurrence of native and exotic snail species (as determined by interspecific association), (2) the importance of habitat conditions in structuring relationships among these species, and (3) the distribution of snails infected with exotic trematode parasites. Three exotic and four endemic species of aquatic snails were collected, but only Elimia comalensis (Prosobranchia: Pleuroceridae, native), Melanoides tuberculatus, and Tarebia granifera (Prosobranchia: Thiaridae, exotic) were in sufficient densities for further analyses. Tarebia granifera was positively associated with both M. tuberculatus (χ2 = 18.5, P < 0.001) and E. comalensis (χ2 = 7.3, P < 0.01), although the co-occurrence between the two exotics was much stronger. Melanoides tuberculatus and E. comalensis exhibited a strong, negative association (χ2 = 10.9, P < 0.001). The weaker co-occurrence between E. comalensis with the thiarids appeared to be driven by differences in habitat use by the thiarids and native E. comalensis. In lentic habitats, densities of M. tuberculatus and T. granifera were similar but differed significantly from E. comalensis whose densities were 200 times less than the exotic snails. In lotic spring runs, densities of T. granifera and E. comalensis were similar, but differed significantly from M. tuberculatus whose densities were 10 times fewer. Lower densities of M. tuberculatus and T. granifera in habitat conditions common to the spring runs may explain why exotic snail interactions were less with the native E. comalensis than with each other. The native snail, E. comalensis, was not infected with any trematodes, while 6.1% of M. tuberculatus and 4.8% of T. granifera were infected with exotic trematodes. Distributions of infected snails were aggregated; such that most infected snails were found in lentic habitats with silt substrates and moderate to high levels of detritus. Continued declines in spring-flows due to aquifer withdrawals and droughts will increase lentic habitats that may lead to increased densities of T. granifera and M. tuberculatus and their concomitant parasites.

Relationships between trematode infection and habitat depth in a freshwater snail, Semisulcospira libertina (Gould)

1999

We found that in natural conditions, the freshwater snail Semisulcospira libertina was distributed in deeper sites when infected with trematode larvae than when uninfected, and examined whether water-depth selection was different between infected and uninfected snails in the laboratory. We compared the mean size of infected and uninfected snails, and the correlation between mean water depth and shell size in uninfected snails. Small uninfected snails (up to 11 mm in shell width) showed a correlation between shell width and water depth, while large snails (larger than 11 mm) did not, but used deeper sites on average than smaller snails. In the small-size class, snails infected with mature cercariae used significantly deeper sites than uninfected snails. On the other hand, in the large-size class, snails infected with immature cercariae used significantly shallower sites than uninfected snails. In each size class, snails infected with mature cercariae used deeper sites than snails infected with immature cercariae or parthenitae. Thus, the influence of trematode infection to host behavior varies according to the development stage of trematodes. In the field, snails infected with mature and immature cercariae had a tendency to occur in deeper sites than uninfected snails of both small and large size classes. These results suggest that some factor other than active selection of water depth by snails determined the distribution pattern of infected snails in natural conditions.

The Role of Spatial and Temporal Heterogeneity and Competition In Structuring Trematode Communities In the Great Pond Snail, Lymnaea stagnalis (L.)

Journal of Parasitology, 2012

We assessed how spatial and temporal heterogeneity and competition structure larval trematode communities in the pulmonate snail Lymnaea stagnalis. To postulate a dominance hierarchy, mark-release-recapture was used to monitor replacements of trematode species within snails over time. In addition, we sampled the trematode community in snails in different ponds in 3 consecutive years. A total of 7,623 snails (10,382 capture events) was sampled in 7 fishponds in the Jindřichů v Hradec and Třeboň areas in South Bohemia (Czech Republic) from August 2006 to October 2008. Overall, 39% of snails were infected by a community of 14 trematode species; 7% of snails were infected with more than 1 trematode species (constituting 16 double-and 4 triple-species combinations). Results of the null-model analyses suggested that spatial heterogeneity in recruitment among ponds isolated trematode species from each other, whereas seasonal pulses in recruitment increased species interactions in some ponds. Competitive exclusion among trematodes led to a rarity of multiple infections compared to null-model expectations. Competitive relationships among trematode species were hypothesized as a dominance hierarchy based on direct evidence of replacement and invasion and on indirect evidence. Seven top dominant species with putatively similar competitive abilities (6 rediae and 1 sporocyst species) reduced the prevalence of the other trematode species developing in sporocysts only.

Spatial covariation between infection levels and intermediate host densities in two trematode species

2006

Both theoretical arguments and empirical evidence suggest that parasite transmission depends on host density. In helminths with complex life cycles, however, it is not clear which host, if any, is the most important. Here, the relationships between the abundance of metacercariae in second intermediate hosts, and the local density of both the first and second intermediate hosts of two trematode species, are investigated. Samples of the snail Potamopyrgus antipodarum, the amphipod Paracalliope fluviatilis and the isopod Austridotea annectens were collected from ten stations in a New Zealand lake. In the trematode Coitocaecum parvum, neither the density of the snail first intermediate host nor that of the amphipod second intermediate host correlated with infection levels in amphipods. In contrast, in the trematode Microphallus, infection levels in isopod second intermediate hosts were positively associated with isopod density and negatively associated with the density of snail first intermediate hosts. These relationships are explained by a negative correlation between snail and isopod densities, mediated in part by their different use of macrophyte beds in the lake. Overall, the results suggest that, at least for Microphallus, local infection levels depend on local intermediate host densities.

Range limits and parasite prevalence in a freshwater snail

Proceedings. Biological sciences / The Royal Society, 2003

Geographical range limits are thought to be set by species' physiological or ecological adaptation to abiotic factors, but the importance of biotic factors such as parasitism in determining range limits has not been well explored. In this study the prevalence of trematode parasitism in populations of a freshwater gastropod snail, Lymnaea stagnalis, increased sharply as this species approached its western UK range limit. The likelihood of trematode infection increased with snail size, but high prevalence at the range edge was not a result of interpopulation variation in snail size. Changes in population growth rates resulting from high rates of parasitism at the range edge could contribute to range limitation. The mechanism driving high rates of parasitism at the range edge is not clear, but changes in abiotic factors towards the range limit may influence snail life history and immune response to trematode infection, indirectly altering the prevalence of parasites in marginal host populations.

Spatial heterogeneity in parasite infections at different spatial scales in an intertidal bivalve

Oecologia, 2006

Spatial heterogeneities in the abundance of free-living organisms as well as in infection levels of their parasites are a common phenomenon, but knowledge on parasitism in invertebrate intermediate hosts in this respect is scarce. We investigated the spatial pattern of four dominant trematode species which utilize a common intertidal bivalve, the cockle Cerastoderma edule, as second intermediate host in their life cycles. Sampling of cockles from the same cohort at 15 sites in the northern Wadden Sea (North Sea) over a distance of 50 km revealed a conspicuous spatial heterogeneity in infection levels in all four species over the total sample as well as among and within sampling sites. Whereas multiple regression analyses indicated the density of first intermediate upstream hosts to be the strongest determinant of infection levels in cockles, the situation within sites was more complex with no single strong predictor variable. However, host size was positively and host density negatively correlated with infection levels and there was an indication of differential susceptibility of cockle hosts. Small-scale differences in physical properties of the habitat in the form of residual water at low tide resulted in increased infection levels of cockles which we experimentally transferred into pools. A complex interplay of these factors may be responsible for within-site heterogeneities. At larger spatial scales, these factors may be overridden by the strong effect of upstream hosts. In contrast to first intermediate trematode hosts, there was no indication for inter-specific interactions. In other terms, the recruitment of trematodes in second intermediate hosts seems to be largely controlled by pre-settlement processes both among and within host populations.

Spatial distribution of the intertidal snail Ilyanassa obsoleta in relation to parasitism by two species of trematodes

Canadian Journal of Zoology, 2000

We studied the spatial distributions of mud snails (Ilyanassa obsoleta) infected by two trematodes, Lepocreadium setiferoides and Gynaecotyla adunca, on a macrotidal mudflat in the Minas Basin, Bay of Fundy. Snails, as first intermediate hosts, were castrated by both parasites, and we found no evidence of sex differences in parasitism. Similar to previous work, prevalence of L. setiferoides in I. obsoleta increased exponentially with host size (and age). Unexpectedly, prevalence of G. adunca decreased over the largest size classes of snails, a result that may be due to several causes. Distributions of both parasites across the intertidal zone differed from previous accounts in that snails infected with L. setiferoides were found only in the middle of the intertidal zone, whereas prevalence of G. adunca increased exponentially moving seaward. Several species of polychaetes could be infected by L. setiferoides in the laboratory and may act as appropriate second intermediate hosts, whereas only the amphipod Corophium volutator served as a second intermediate host for G. adunca. Finally, the vertical distributions of I. obsoleta infected by either species of trematode overlap with distributions of apparent or known second intermediate hosts.