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.     

Positive interactions of the smooth cordgrass Spartina alterniflora on the mud snail Heleobia australis, in South Western Atlantic salt marshes

The role of positive interactions is often crucial in communities with intense abiotic stress such as intertidal environments. Grasses acting as ecosystem engineers, for example, may ameliorate intertidal harsh physical conditions and modify the community structure. The mud snails Heleobia australis d'Orbigny frequently inhabit the SW Atlantic marshes, mainly associated to intertidal marsh plants (mainly the smooth cordgrass Spartina alterniflora Loisel) probably due to the plant indirect effects. The purpose of this work was to investigate the magnitude of these association and the processes that generate the pattern. Samples of the snail abundance in six SW Atlantic coastal marshes show that H. australis is associated to coastal areas of low energy and low or none freshwater input. This result is important because this species is being used as bioindicator of coastal estuarine systems during the Holocene. Thus the paleontological interpretation based on this species should be revised. Within the studied areas, snails are associated to intertidal marsh plants. However, stable isotope analysis shows that neither plant nor their epiphytes are their main food sources. Field experiments show that snails actively select areas with plants, although tethering experiments show that plants do not provide shelter from predators. However, plants do buffer physical stress factors such as temperature, which generate important mortality outside plants covered areas. These positive interactions have large effects on H. australis distributions in marsh communities; increasing the habitats available for colonization and affecting their local distribution.     

The fishes associated with three intertidal salt marsh creeks in a temperate southern African estuary

This study compares the fish assemblages in a range of intertidal salt marsh creeks in the Kariega Estuary, South Africa, as well as highlighting any differences between the ichthyofaunal structure of the creeks and adjacent Zostera bed habitats. The superimposition of environmental variables on the creek biotic groupings (60% similarity level) indicated consistent relationships between both the creek water depth and mouth area with the major creek fish clusters. Water temperature, salinity and turbidity did not display any pattern which could explain the disparity between the ichthyofaunal groupings. The results also indicated that intertidal creeks form a unique littoral habitat within the Kariega Estuary, with ichthyofaunal compositions very different to those found in nearby eelgrass beds. Furthermore, intertidal creeks in the Kariega system appear to be similar to creeks found elsewhere in the world in that their fish assemblages are dominated by 0+ juveniles, have a conspicuous marine transient and estuarine resident component, and very few piscivorous representatives. These results also give weight to the hypothesis that southern African salt marsh creek habitats serve as temporary refuges to juvenile fishes, a role that has also been proposed in other parts of the world.     

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.     

The Ichthyofauna Associated with an Intertidal Creek and Adjacent Eelgrass Beds in the Kariega Estuary,South Africa

The structure and functioning of salt marsh fish communities in the overall ecology of southern African estuaries is poorly understood. This study compares the ichthyofauna associated with a salt marsh creek and eelgrass bed in an attempt to evaluate the relative importance of these habitats to fishes. Taylor's salt marsh creek and adjacent eelgrass bed in the Kariega Estuary were sampled twice per season between the winter of 1992 and the autumn of 1994. The average density and standing stock of fishes were found to be considerably higher in the eelgrass bed than in the intertidal creek. Both habitats had similar fish diversities but were dominated by different taxa, the most notable of which was the dominance of mugilids in the creek and their scarcity in the eelgrass. Taylor's intertidal creek and adjacent eelgrass beds were dominated by juvenile fish, with both habitats functioning as nursery areas for juvenile fish, albeit for totally different ichthyofaunal communities. The similar fish diversities but lower abundances in the intertidal creek compared to the eelgrass beds are in contrast to similar North American studies, and refute the hypothesis that intertidal salt marsh creeks have higher fish densities but lower diversities than eelgrass beds.The first author is also the senior author     

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.     

Esterases in natural populations of normal and Echinostoma revolutum-infected Helisoma trivolvis (Gastropoda)

Esterases of the digestive gland-gonad (DGG) complex of individual snails from a wild population of Helisoma trivolvis infected with the trematode Echinostoma revolutum were analyzed by vertical slab PAGE and compared to similar DGG homogenates of uninfected conspecifics from the same population. Our analysis indicated that: 1. Four classes of esterases, some atypical, could be resolved using diagnostic inhibitors. 2. Uninfected snails demonstrated polymorphism for two of these four esterase groups, including cholinesterases (CHE), in the 34 individual DGGs analyzed. 3. The rarer of the two ChE phenotypes in the uninfected sample (29.4%) was present in 100% of the 17 infected snails examined. However, no changes in esterase zymograms of infected DGGs due to the parasite were noted. 4. The possibility that the 'rare' ChE phenotype is somehow related to host susceptibility to Echinostoma revolutum is discussed in view of similar apparent linkages in other snail-trematode systems.     

Disturbance and recovery of salt marsh arthropod communities following BP Deepwater Horizon oil spill

Oil spills represent a major environmental threat to coastal wetlands, which provide a variety of critical ecosystem services to humanity. The U.S. Gulf of Mexico is a hub of oil and gas exploration activities that historically have impacted intertidal habitats such as salt marsh. Following the BP Deepwater Horizon oil spill, we sampled the terrestrial arthropod community and marine invertebrates found in stands of Spartina alterniflora, the most abundant plant in coastal salt marshes. Sampling occurred in 2010 as oil was washing ashore and a year later in 2011. In 2010, intertidal crabs and terrestrial arthropods (insects and spiders) were suppressed by oil exposure even in seemingly unaffected stands of plants; however, Littoraria snails were unaffected. One year later, crab and arthropods had largely recovered. Our work is the first attempt that we know of assessing vulnerability of the salt marsh arthropod community to oil exposure, and it suggests that arthropods are both quite vulnerable to oil exposure and quite resilient, able to recover from exposure within a year if host plants remain healthy.     

Estuarine and habitat-related differences in growth rates of young-of-the-year winter flounder (Pseudopleuronectes americanus) and tautog (Tautoga onitis) in three northeastern US estuaries

Instantaneous growth rates of young-of-the-year winter flounder Pseudopleuronectes americanus (Walbaum) (12.0-60.4 mm standard length, SL) and tautog Tautoga onitis (Linnaeus) (21.4-73.8 mm total length, TL) from three estuarine systems in New Jersey (Great Bay-Little Egg Harbor and Navesink River) and Connecticut (Hammonasset River) were used in an attempt to assess the relative quality of selected nominal habitats. A series of short-term field caging experiments were conducted during 1994 and 1995 in: macroalgae (primarily, Ulva lactuca), eelgrass (Zostera marina), unvegetated areas adjacent to macroalgae and eelgrass and tidal creeks in Spartina dominated marsh. Growth rates varied with habitat, estuary and year. Comparisons across nominal habitats within and among estuaries did not show any one habitat with consistently higher growth, and growth was relatively independent of whether a habitat was vegetated or adjacent to vegetation. The growth rates of winter flounder and tautog from the Hammonasset River were not different among habitats in either year of the study. In the Great Bay-Little Egg Harbor, both winter flounder and tautog had higher growth rates in macroalgae with growth in eelgrass varying significantly between years. Conversely, in the Navesink River both species had higher growth rates in eelgrass. Environmental changes associated with temperature and dissolved oxygen appeared to influence growth rates. Winter flounder growth rate and survival was depressed in tidal marsh creeks in the three estuaries and in vegetated macroalgae habitats in the Navesink River where dissolved oxygen levels were often very low (<2 mgl(-1)) for extended periods. In summary, the growth rates of the young-of-the-year of these two species varied temporally and were dependent on the interaction of both the specific estuary and habitat in which the experiments took place. Further, habitat quality, as defined by relative growth rate, was difficult to evaluate because it can be variable and nominal habitat designations are often not sufficient to define the boundaries of a species habitat requirements.     

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.     

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

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

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.     

Larval trematode infections and spatial distributions of snails

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

Composition and abundance of resident marsh-surface nekton: comparison between tidal freshwater and salt marshes in Virginia,USA

Previous research on intertidal nekton communities has identifiedimportant determinants of community structure and distribution; however, fewstudies have compared nekton utilization of disparate marsh habitats. Inthis study, abundance and distribution patterns of resident nekton werecompared between tidal freshwater marsh and salt marsh surfaces varying inflooding depth and duration. Nekton were collected in pit traps installedalong elevational transects at four marshes in coastal Virginia (twofreshwater, two saline) from April through November 1992–1993. Thedominant fish collected at all sites was the mummichog Fundulusheteroclitus. The daggerblade grass shrimp Palaemonetes pugio was thedominant nekton species collected at salt marsh sites, and was seasonallyabundant on tidal freshwater marshes. A positive correlation betweenflooding depth and nekton abundance was observed on salt marshes; anopposite pattern was observed on tidal freshwater marshes. Tidal floodingregime influences the abundance of resident nekton, however, the effect maybe confounded by other environmental variables, including variation insurface topography and seasonal presence or absence of submerged aquaticvegetation (SAV) in adjacent subtidal areas. In mid-Atlantic tidalfreshwater wetlands, SAV provides a predation refuge and forage site forearly life stages of marsh-dependent nekton, and several species utilizethis environment extensively. Salt marshes in this region generally lackdense SAV in adjacent subtidal creeks. Consequently, between-sitedifferences in species and size-specific marsh surface utilization byresident nekton were observed. Larvae and juveniles represented 79%and 59% of total fish collected at tidal freshwater and salt marshsites, respectively. The resident nekton communities of tidal freshwater andsalt marsh surfaces are characterized by a few ubiquitous species with broadenvironmental tolerances. This revised version was published online in July 2006 with corrections to the Cover Date.     

Experimental warming causes rapid loss of plant diversity in New England salt marshes

Anthropogenic climate change is predicted to cause widespread biodiversity loss due to shifts in species' distributions, but these predictions rarely incorporate ecological associations such as zonation. Here, we predict the decline of a diverse assemblage of mid-latitude salt marsh plants, based on an ecosystem warming experiment. In New England salt marshes, a guild of halophytic forbs occupies stressful, waterlogged pannes. At three sites, experimental warming of < 4 °C led to diversity declines in pannes and rapid takeover by a competitive dominant, Spartina patens . In Rhode Island, near their southern range limit, pannes were more sensitive to warming than farther north, and panne area also declined in control plots over the three-season experiment. These results suggest that warming will rapidly reduce plant diversity in New England salt marshes by eliminating a high diversity zone. Biodiversity in zoned ecosystems may be more affected by climate-driven shifts in zonation than by individual species' distribution shifts.     

Effect of starvation on parasite-induced mortality in a freshwater snail (Potamopyrgus antipodarum)

The level of host exploitation is expected, under theory, to be selected to maximise (subject to constraints) the lifetime reproductive success of the parasite. Here we studied the effect of two castrating trematode species on their intermediate snail host, Potamopyrgus antipodarum. One of the trematode species, Microphallus sp., encysts in the snail host and the encysted larvae “hatch” following ingestion of infected snails by birds. The other species, Notocotylus gippyensis, by contrast, releases swimming larvae; ingestion of the snail host is not required for, and does not aid, transmission to the final host. We isolated field-collected snails for 3 months in the laboratory, and followed the survival of infected and uninfected snails under two conditions: not fed and fed ad libitum. Mortality of the infected hosts was higher than mortality of the uninfected ones, but the response to starvation treatment was parasite species specific. N. gippyensis induced significantly higher mortality in starved snails than did Microphallus. Based on these results, we suggest that host exploitation by different species of trematodes may depend on the type of transmission. Encysting in the snail host may select for a reduced rate of host exploitation so as to increase the probability of transmission to the final host. Received: 29 July 1998 / Accepted: 1 February 1999     

Spatial and temporal habitat use patterns for salt marsh nekton: implications for ecological functions

We synthesized information on temporal and spatial patterns of salt marsh habitat use by nekton in order to infer the importance of five main types of marsh function: reproduction, foraging, refuge from predation, refuge from stressful environmental conditions and environmental enhancement of physiology. We then extended the concept that intertidal gradients regulate habitat use patterns of nekton to a more universal concept that applies to all salt marsh habitats. We contend that all marsh habitats are linked to each other and to adjacent estuarine habitats along a depth gradient that mediates gradients in abiotic and biotic conditions. Tidal, diel and seasonal shifts in the magnitude and direction of these gradients result in gradients in tidal, diel and seasonal variation in biotic and abiotic conditions within the salt marsh. Collectively these gradients form the `marsh gradient'. We propose that patterns of marsh use and ecological function for nekton result primarily from physiological and behavioral responses to this marsh gradient. A comparison of habitat use patterns in the context of the marsh gradient is an important – and underutilized – method to study marsh function and essential fish habitat. We note that our limited insight into the function of the marsh habitat results from a significant lack of information on the occurrence and causes of tidal, diel and ontogenetic marsh use patterns by nekton; this is particularly relevant with respect to data on the variation in environmental conditions along marsh gradients over tidal, diel and seasonal cycles and on how environmental variation on these scales influences nekton behavior, growth and survival.     

Movements and growth of tagged young-of-the-year Atlantic croaker (Micropogonias undulatus L.) in restored and reference marsh creeks in Delaware Bay, USA

The residence time, movements, and growth of tagged young-of-the-year Atlantic croaker, Micropogonias undulatus L., were studied from July to October 1998 as measures of the success of a marsh restoration project adjacent to Delaware Bay. A total of 8173 croaker (41-121 mm SL) were tagged from each of two creeks in both marshes during July and August with internal sequential coded wire microtags. A prior tag-retention study in the laboratory found a 95% tag retention rate. Of those tagged, 3.6% were recaptured within and nearby the study creeks using seines, otter trawls, and weirs during a 105-day period. Recapture percentages ranged from 1.5% to 6.1% in individual creeks in the restored marsh. There was some movement of tagged fish between creeks in the restored marsh and out into the main creek, but 95% of the recaptures were made in the subtidal and intertidal portions of the same creek in which they were tagged. Fewer fish were recaptured at the reference marsh (1.6% recapture; n=1489 tagged) up to 50 days after tagging, with no evidence of movement between creeks. The average individual growth rates for recaptured croaker was the same in both restored (0.69 mm/day) and reference (0.63 mm/day) marshes before egress from the creeks in September and October. As a result, both created creeks in a restored marsh and natural creeks in a reference marsh appeared to be utilized as young-of-the-year habitat in a similar way during the summer and until egress out of the marshes during the fall, thus this restoration effort has been successful in creating suitable habitat for Atlantic croaker.     

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

Using field surveys and experimental infections, we investigated the influence of a trematode parasite on life history traits of adult Lymnaea elodes snails. We found that parasitism significantly affected the growth, fecundity, and survival of host snails. Within five of the six natural L. elodes populations we sampled, shell length of echinostome-infected hosts was significantly greater than for uninfected conspecifics. Furthermore, we show that gigantism occurs among experimentally infected snails due to an accelerated growth rate and size-selective mortality following an Echinostoma revolutum infection. The fecundity of infected snails sharply decreased beginning at 3 weeks post exposure (PE) and all egg production eventually ceased for most hosts by 5–6 weeks PE. Energy constraints, imposed by parasite development, alter the host energy budget. Early in the infection, parasite depletion of host energy reserves reduces host reproduction, but sufficient resources remain to allow accelerated host growth. Mortality was increased among host snails at two distinct stages: shortly after exposure and several weeks after cercariae were first released. We did not observe tissue degradation in snails during the first 4 weeks after exposure to the parasite, but destruction of host tissues was noted among snails dying later in the infection. Received: 5 September 1997 / Accepted: 19 November 1997     

Trematode fauna of prosobranch snails of the genus Semisulcospira in Lake Biwa and the connected drainage system

The parasite fauna of prosobranch snails of the genus Semisulcospira was surveyed in Lake Biwa and the adjacent water system. One aspidogastrean and 28 digenetic trematode taxa were detected in 19209 snails consisting of 10 morphological species. There was no trematode species peculiar to members of the subgenus Biwamelania that is endemic to the Lake Biwa water system. However, one species, Notocotylus magniovatus, was found only in the non-endemic subgenus Semisulcospira. Of 23 digenean taxa detected in more than one host, 13 were distributed in both the lake and the tributaries. Seven of these had host taxa, more than 1% of which were infected with the parasite in both the lake and the tributaries, four had such hosts only in the tributaries, and two had no such hosts. Three species detected only in Lake Biwa were previously reported from other rivers in Japan. In the seven species detected only in the tributaries, two species had life cycles that could be maintained only in rivers. These results indicate that the core areas for the distribution of parasites of Semisulcospira are tributaries, and the lake is a sink for these species. These results contradict the expectation that the parasite fauna should be richer in the lake than in tributaries because the lake is a stable habitat over a geological time scale and has more divergent freshwater animals than the adjacent water system.