Trematode Community Research Articles

A review of indicators of estuarine tidal wetland condition

This review critically evaluates indicators of tidal wetland condition based on 36 indicator development studies and indicators developed as part of U.S. state tidal wetland monitoring programs. Individual metrics were evaluated based on relative scores on two sets of evaluation factors. A rigor score evaluated metric development based on conceptual relevance, indicator development method, degree of independent validation, and temporal and spatial extent tested. An applicability score evaluated metrics based on cost of data collection, probable spatial extent of applicability, technical complexity, and indicator responsiveness. The majority of indicators could be classified as biotic condition indicators (81%), with vegetation (37%) and macroinvertebrate (28%) metrics composing the largest proportion. Most metrics provided a conceptual model or scientific justification (97%), were developed by correlation to environmental gradients (46%), were tested over multiple seasons or years (49%) and at multiple sites (88%). Few were independently validated (18%). Average rigor score was 10 (on a scale of 0–25) and ranged between 1 and 21. Highest rigor scores were for trematode community metrics (community similarity index, species richness) and metrics of grass shrimp ( Palaemonetes pugio) individuals (gene expression, relative fecundity, embryo hatching success, larval survival). Most metrics had a high cost of data collection (63%), required field and laboratory processing (84%), would be applicable across the U.S. (72%), and were responsive to the variable of interest (44%). Mean applicability score was 4.9 (range: 2–8). Highest scores were found for metrics that only required field collection of data using simple or no instrumentation. Lowest scoring metrics required expensive equipment, specialized taxonomic knowledge, complex laboratory analysis, and/or culturing of organisms. Scores for individual metrics were grouped by indicator, then averaged and rescaled between 0 and 100 to provide a composite evaluation of the indicator they measured. Among major indicator types, biotic indicators had the highest rigor scores (mean = 44, range 20–79), followed by indicators of chemical/physical characteristics (mean = 36, range 16–56), landscape condition (mean = 31, range 24–37), and hydrology/geomorphology indicators (mean = 21, range 4–52). In contrast, biotic indicators scored lowest for applicability (mean = 58, range 25–100) and indicators of landscape condition scored highest. The results of this review suggest that the development and selection of tidal wetland indicators could be vastly improved by employing a standardized development methodology that provides uniform information about each indicator. In addition, tidal wetland indicator research should focus on the development of indicators of ecological processes and disturbance regimes.

Larval trematode communities in Radix auricularia and Lymnaea stagnalis in a reservoir system of the Ruhr River

BackgroundAnalysis of the data available from traditional faunistic approaches to mollusc-trematode systems covering large spatial and/or temporal scales in Europe convinced us that a parasite community approach in well-defined aquatic ecosystems is essential for the substantial advancement of our understanding of the parasite response to anthropogenic pressures in urbanised areas which are typical on a European scale. Here we describe communities of larval trematodes in two lymnaeid species, Radix auricularia and Lymnaea stagnalis in four man-made interconnected reservoirs of the Ruhr River (Germany) focusing on among- and within-reservoir variations in parasite prevalence and component community composition and structure.ResultsThe mature reservoir system on the Ruhr River provides an excellent environment for the development of species-rich and abundant trematode communities in Radix auricularia (12 species) and Lymnaea stagnalis (6 species). The lake-adapted R. auricularia dominated numerically over L. stagnalis and played a major role in the trematode transmission in the reservoir system. Both host-parasite systems were dominated by bird parasites (13 out of 15 species) characteristic for eutrophic water bodies. In addition to snail size, two environmental variables, the oxygen content and pH of the water, were identified as important determinants of the probability of infection. Between-reservoir comparisons indicated an advanced eutrophication at Baldeneysee and Hengsteysee and the small-scale within-reservoir variations of component communities provided evidence that larval trematodes may have reflected spatial bird aggregations (infection 'hot spots'). Two life history groupings of dominant species, the 'cyprinid' and 'anatid' parasites, that depict two aspects of progressive eutrophication in this mature reservoir system, were identified.ConclusionsWe conclude that trematode communities in the lake-adapted R. auricularia are better suited for monitoring the effect of environmental change on host-parasite associations in the reservoir system on the Ruhr River and other similar systems due to the important role of this host in trematode transmission in lakes. Whereas variations in trematode community diversity and abundance may indicate the degree of eutrophication on a larger scale (among reservoirs), the infection rates of the two life history groups of dominant species, the 'cyprinid' and 'anatid' assemblages, may be particularly useful in depicting environmental variability, eutrophication effects and infection 'hot spots' on smaller spatial scales.

Acceptance of the 2009 Henry Baldwin Ward Medal: The Accidental Parasitologist

Acceptance of the 2009 Henry Baldwin Ward Medal: The Accidental Parasitologist

LONG-TERM ANALYSIS OF CHARLIE'S POND: FECUNDITY AND TREMATODE COMMUNITIES OF HELISOMA ANCEPS

Charlie's Pond (North Carolina) harbors a diverse community of trematodes that infect the planorbid snail Helisoma anceps. Research at the Pond began in 1984 and serves as a foundation on which to investigate long-term changes in trematode communities. In 2002, 2005, and 2006 average size and fecundity of H. anceps were calculated each month, and seasonal trends analyzed with randomization tests. Concomitantly, trematode infections were recorded, and the community composition compared to those from previous studies. Helisoma anceps in 2002, 2005, and 2006 were smaller and less fecund than snails in 1984. The trematode community was consistently diverse, with 11 species recovered in 2006 versus 7 in 1984. However, the prevalence of Halipegus occidualis was much lower than previously observed (60% in 1984) and never exceeded 20% during the latter years. The decline of emergent vegetation is likely contributing to these changes. Aquatic macrophytes increase the surface area for growth of periphyton, the food source of these snails. Limited food supplies result in lower snail growth rates and fecundity. Similarly, emergent vegetation creates foci of transmission for H. occidualis between the frog definitive host and the snail intermediate host. When these areas are lost from the Pond, probability of transmission is reduced, and prevalence in the snail declines.

ENDANGERED LIGHT‐FOOTED CLAPPER RAIL AFFECTS PARASITE COMMUNITY STRUCTURE IN COASTAL WETLANDS

An extinction necessarily affects community members that have obligate relationships with the extinct species. Indirect or cascading effects can lead to even broader changes at the community or ecosystem level. However, it is not clear whether generalist parasites should be affected by the extinction of one of their hosts. We tested the prediction that loss of a host species could affect the structure of a generalist parasite community by investigating the role of endangered Light-footed Clapper Rails (Rallus longirostris levipes) in structuring trematode communities in four tidal wetlands in southern California, U.S.A. (Carpinteria Salt Marsh, Mugu Lagoon) and Mexico (Estero de Punta Banda, Bahia Falsa-San Quintin). We used larval trematode parasites in first intermediate host snails (Cerithidea californica) as windows into the adult trematodes that parasitize Clapper Rails. Within and among wetlands, we found positive associations between Clapper Rails and four trematode species, particularly in the vegetated marsh habitat where Clapper Rails typically occur. This suggests that further loss of Clapper Rails is likely to affect the abundance of several competitively dominant trematode species in wetlands with California horn snails, with possible indirect effects on the trematode community and changes in the impacts of these parasites on fishes and invertebrates.

Population dynamics of Chaetogaster limnaei (Oligochaeta: Naididae) in the field populations of freshwater snails and its implications as a potential regulator of trematode larvae community

The objectives of this work were to study (1) the population dynamics of Chaetogaster limnaei in the field populations of freshwater snails and the implications for the species as a potential regulator of the trematode larvae community and (2) prevalence and intensity of C. limnaei in relation to host species, host size, and season. This study was conducted at Al-Salam Canal and Al-Abtal village (new cultivated area in north Sinai). The samples were collected from March 2004 to February 2005. The natural infection rate by trematodes and C. limnaei was assessed monthly. Thirteen species of snails were examined for C. limnaei infection, five species were found infected. There were positive correlations between host size and both combined prevalence and mean intensity in all hosts. The data demonstrated that prevalence in Bulinus truncatus was higher when compared with other hosts. Bellamya unicolor has higher mean intensity when compared with other host species. A significant difference was found between host species and both prevalence and intensity. There were spatial and temporal variations in prevalence and mean intensity in most hosts, and the data suggest some seasonality. A negative correlation was found between prevalence of C. limnaei and trematode infection. C. limnaei did not co-occur with trematode larvae in infected hosts indicating that the oligochaete may protect the hosts from trematode infection. B. unicolor was recorded for the first time as a host for C. limnaei. C. limnaei may be a potential regulator of the trematode community in freshwater snails. In conclusion, this study demonstrated that C. limnaei, symbiotically associated with snail vector of parasitic diseases, may have important implications with respect to biological control and/or changes in the epizootiology of native parasites in the study area.

Anthropogenic Pressure on a Molluscan–Trematode Community over a Long-term Period in the Basingstoke Canal, UK, and Its Implications for Ecosystem Health

A long-term study of a molluscan–trematode community in the Basingstoke Canal, UK, was undertaken over the period 1970–2003 which coincided with a significant restoration program involving substantial anthropogenic changes to the canal’s ecosystem. The aim of this study was to correlate these changes with alterations in the molluscan–trematode community, focusing on fluctuations in the prevalence and species richness of the trematode population as a good indicator, in terms of biodiversity, of ecosystem health. Molluscs were sampled at four time periods (1970, 1982, 1983, 2003) and examined for trematode parasites. The molluscan population over the sampling period demonstrated a limited stability with few species being present during all time periods. During 1982 and 1983, when restoration of the sampling site was being undertaken, Lymnaea stagnalis dominated the molluscan fauna, possibly because it was best able to take advantage of the disturbed conditions, while other species such as Bithynia tentaculata were absent. In the trematode population, the prevalence and diversity of both cercarial and metacercarial infections was high in 1970 prior to the period of restoration work. However, during 1982 and 1983, the trematode community was significantly reduced with cercarial prevalence declining to less than 1%. By 2003, more than 12 years after restoration had been completed, the trematode population had shown only a modest recovery. Trematodes use a wide range of different host species for completing their life-cycles and may be used as bioindicators of ecosystem diversity and health. An interpretation of the structure of the molluscan–trematode community over the sampling period suggests that the restoration project had an initial negative effect on ecosystem health, in terms of biodiversity, but this has subsequently only shown modest signs of recovery suggesting continuing problems in ecological functioning and stability.

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

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

Spatial and temporal variations in the trematode component community of the mudsnail Hydrobia ventrosa in relation to the occurrence of waterfowl as definitive hosts.

The component community of larval trematodes infecting the mudsnail Hydrobia ventrosa (Montagu) was examined in coastal lagoons of the southern Baltic Sea among different host subpopulations in relation to the structure of the waterfowl community. The 10 trematode species observed represent the families Notocotylidae (1), Echinostomatidae (1 or 2), Heterophyidae (2). Monorchidae (1). Microphallidae (3 or 4), Psilostomatidae (1), and Hemiuridae (1). Eight of these species infect waterfowl as adults. The structure of the trematode communities was similar between sampling sites. Seven trematode taxa were commonly found at all sampling sites. Prevalence values of the 6 most abundant taxa, which infect birds as final hosts, were significantly different between neither sampling sites nor across year. Overall trematode prevalence in H. ventrosa fluctuated seasonally. Prevalence usually peaked in summer between July and September or October. Low prevalences were observed in late winter and early spring. In contrast, the seasonal maximum in waterfowl numbers differed between areas because of significant spatial differences in the bird community structure. The species composition of the component trematode community of H. ventrosa in the coastal lagoons of the southern Baltic Sea is more or less independent of the species composition of the waterfowl community. This independence presumably results from the lack of host specificity in most of the observed trematode species. Otherwise, the low host specificity in combination with the enormous waterfowl diversity in the coastal lagoons might explain the stability of the prevalence pattern of the component trematode community.

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

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

Larval Trematode Assemblages in the Snail Lymnaea stagnalis from Southeastern Wisconsin

From May through November 1993 and 1994, Lymnaea stagnalis appressa were collected from a stream adjacent to Cedarburg Bog, Ozaukee County, Wisconsin. Observations of cercarial shedding and subsequent dissection of snails revealed a relatively depauperate digenean component community consisting primarily of 3 common species. The most frequently occurring form was the metacercaria of Cotylurus flabelliformis. Sporocysts and cercariae of this species were rarely observed. Snails also harbored sporocysts and shed cercariae of Schistosomatium douthitti and a plagiorchid. Seasonal and yearly dynamics of the component trematode community reflect the apparent inability of sporocysts to overwinter in snails at this location. They also seem to be associated closely with snail life histories in terms of the availability of large snails, most often infected by the sporocysts of S. douthitti and the plagiorchid. Analyses of double infections revealed the occurrence of a negative interspecific interaction between the tetracotyles of C. flabelliformis and sporocysts of S. douthitti. Other combinations of trematode species did not reveal negative interactions. Competition does not seem to play a major role in the structure of the component community at this location.

Ilyanassa obsoleta (Gastropoda) as a Host for Trematodes in Delaware Estuaries

Extensive data characterizing larval trematode communities in marine gastropods do not exist for many systems. The purpose here is to report on the infections encountered in Delaware Ilyanassa obsoleta and to compare this trematode community with certain others that have been well studied. Over 15 yr, 11,774 I. obsoleta from 9 different estuarine habitats were examined. Trematode parasitism, sex, and size were determined for each snail. In the total collection, 9 trematode species were encountered; 51.04% of snails were infected with 1 or more species. The sexes were equally susceptible to being parasitized. Smaller snails were less likely to be infected than larger ones. Juvenile snails can be infected, but few have been colonized because of the short time they have been exposed to infective stages. Other studies of trematodes in this snail have revealed few multispecies infections. In contrast, they were strikingly common in this study (12.57% of all snails). Himasthla quissetensis seldom infects the same snail with Lepocreadium setiferoides or Austrobilharzia variglandis, but other species combinations can coexist. The important element in this trematode community seems to be time. The observed frequencies of different infracommunities (single and multispecies combinations) in samples of snails are considered to result from a variety of causes. These include commonness of the trematode species in the system, where and how the sample was collected, definitive host behavior, the low probability of a snail becoming infected, the long life of the snail and its infections, the vagility of the snail, and the incompatibility of certain species in terms of infecting the same snail.

The Prevalence of Cercariae from Stagnicola emarginata (Lymnaeidae) over 50 Years in Northern Michigan

Stagnicola emarginata were collected from 3 northern Michigan lakes and examined for larval trematode infections. The structure of the trematode community was then compared with 2 previous studies conducted on Douglas Lake in order to determine what changes had taken place over a period of more than 50 yr and to examine the possibility of using trematodes as bioindicators of environmental quality. Species richness was reduced by half (from 16 to 8 species) from the first study conducted in 1936, along with a decrease in the overall prevalence from 61% to 13%. No new species had colonized the lake, and the same 8 trematodes were also the only species found in 2 other lakes. The decline in prevalence was most severe in trematodes that used gulls as definitive hosts, whereas species that used ducks as hosts increased slightly. The decrease in species richness and prevalence of infection over time may reflect increasing human impacts on lakes. However, because of patchy host distributions, the use of larval trematodes as bioindicators of environmental change requires further investigation.

Trematode Community Structure in the Pulmonate Snail Physa gyrina

Trematode community structure was examined in the pulmonate snail Physa gyrina over a 12-mo period. A total of 1,181 snails was collected from Charlie's Pond, North Carolina, and was found to be parasitized by 6 trematode species. Infracommunities were relatively species rich when compared to previous studies, with 18.4% of infected snails having multi-species infections. Halipegus eccentricus was found in 88.4% of multiple infections, usually with 1 of 2 other autogenic, egg-transmitted species (Haematoloechus complexus and Glypthelmins quieta). Neither negative interspecific interactions nor a dominance hierarchy were apparent among the trematodes. These factors, along with high snail vagility and the temporal heterogeneity of infective stages in the environment, are suggested to have contributed to the high number of multiple infections. Halipegus eccentricus was also the most prevalent parasite throughout the study, occurring in nearly 50% of all snails during May, June, and July. Apparent parasite-induced host mortality caused by this trematode species contributed to increasing species diversity in larger snails. The component community was also affected by the continuous recruitment of new snails into the host population and by changes in the number of infective stages present over time.

Abundance/host size relationship in a fish trematode community.

The abundance of six species of trematodes: Aphanurus stossichi, Bacciger israelensis, Diphterostomum israelense, Plagioporus idoneus, Leprocreadium album and L. pegorchis, parasitic in the digestive tract of marine teleostei (Sparidae) collected near Jounieh (east Mediterranean), was analysed as a function of the host-size. In two parasite/host systems, infections were observed from the lowest size classes of the sample, with a clear tendency to an increase of abundance in older fish. In four others, parasites appear only above a rather high threshold class, young individuals never being infected. In the last three parasite/host systems, host invasion may occur early or late, but infection decreases above a well defined size class, old fishes rarely or never being infected. A given trematode species, when parasitizing several host species, shows similar abundance/host size relationships, e.g., P. idoneus in Diplodus vulgaris and Oblada melanura. When more than one species of trematode infects a single host species, curves can be markedly distinct; for instance, L. pegorchis was collected from Pagellus erythrinus below 15 cm. whereas D. israelense parasitized the same fish approximately above the same size. There is no evidence that such a replacement of one trematode by another in the course of host growth is a result of inter-specific competition.