Trematode Species Richness Research Articles

The abundance of snail hosts mediates the effects of antagonist interactions between trematodes on the transmission of human schistosomes

BackgroundCombating infectious diseases and halting biodiversity loss are intertwined challenges crucial to ensure global health. Biodiversity can constrain the spread of vector-borne pathogens circulation, necessitating a deeper understanding of ecological mechanisms underlying this pattern. Our study evaluates the relative importance of biodiversity and the abundance of Bulinus truncatus, a major intermediate host for the trematode Schistosoma haematobium on the circulation of this human pathogen at aquatic transmission sites.MethodsWe combined mathematical modelling and a molecular based empirical study to specifically assess the effect of co-infections between S. haematobium and other trematodes within their B. truncatus snail hosts; and B. truncatus abundance at transmission sites, on the production of S. haematobium infective cercariae stages released into the aquatic environment.ResultsOur modelling approach shows that more competitive trematode species exploiting B. truncatus as an intermediate host at the transmission site level leads to higher co-infection rates within snail hosts, subsequently reducing the production of S. haematobium cercariae. Conversely, an increase in B. truncatus abundance results in lower co-infection rates, and a higher proportion of S. haematobium cercariae released into the environment. Our empirical data from the field support these findings, indicating a significant negative effect of local trematode species richness (P-value = 0.029; AIC = 14.9) and co-infection rates (P-value = 0.02, AIC = 17.4) on the dominance of S. haematobium based on our GLMM models, while B. truncatus abundance positively influences S. haematobium dominance (P-value = 0.047, AIC = 20.1).ConclusionsOur study highlights the importance of biodiversity in influencing the transmission of S. haematobium through the effect of antagonistic interactions between trematodes within bulinid snail hosts. This effect intensifies when B. truncatus populations are low, promoting co-infections within snails. In line with the One Health concept, our results suggest that maintaining high level of freshwater biodiversity to sustain global trematode diversity at transmission sites can help reducing the circulation of Schistosoma species locally.Graphical

Biogeography of larval trematodes in the freshwater snail, Semisulcospira libertina: a comparison of the morphological and molecular approaches

While biogeographic patterns of free-living organisms are well documented, the biogeography of parasitic fauna remains largely unclear. Due to morphological similarities, parasites are often difficult to identify without the aid of molecular genetics, further complicating the interpretation of their biogeographic patterns. We investigated trematode parasites infecting the East Asian freshwater snail Semisulcospira libertina to understand their biogeography and to evaluate how molecular approaches influence the interpretation of biogeographic patterns of the trematode fauna. We identified 46 genetically delimited species from 19 morphologically distinguishable trematodes infecting S. libertina and found that their species richness was negatively correlated to latitude. We also found that potential definitive host (fishes) richness and host body size were positively correlated with trematode species richness, suggesting that host attributes are essential factors shaping the biogeographic pattern in trematodes. These trends were observed irrespective of species identification methods, demonstrating that classical morphological identification can also effectively identify the latitudinal gradient pattern in trematodes. We further detected the distance decay of similarity in trematode communities, although this trend was only detectable in the biogeographic dataset based on molecular identification. Our study showed that morphological identification sufficiently reflects the latitudinal richness gradient while molecular identification is essential to estimate accurate local species richness and increase the resolution of the large-scale pattern of population similarities in the trematode communities.

Himasthla spp. (Trematoda) In The Edible Cockle Cerastoderma edule: Review, Long-Term Monitoring And New Molecular Insights.

AbstractTrematodes are the main macroparasites in coastal waters. The most abundant and widespread form of these parasites is metacercaria. Their impact on their host fitness is considered relatively low but metacercarial larvae of some species can have deleterious effects on individuals and/or populations. This review focused on the cockle Cerastoderma edule and four species of the genus Himasthla; a common host–parasite system in marine coastal environments. Our aims were (1) to review literature concerning Himasthla continua, Himasthla elongata, Himasthla interrupta and Himasthla quissetensis in cockles; (2) to provide molecular signatures of these parasites and (3) to analyse infection patterns using a 20-year monthly database of cockle monitoring from Banc d'Arguin (France). Due to identification uncertainties, the analysis of the database was restricted to H. interrupta and H. quissetensis, and it was revealed that these parasites infect cockles of the same size range. The intensity of parasites increased with cockle size/age. During the colder months, the mean parasite intensity of a cockle cohort decreased, while infection occurred in the warmest season. No inter-specific competition between trematode parasites was detected. Furthermore, even if the intensity of H. interrupta or H. quissetensis infection fluctuated in different years, this did not modify the trematode community structure in the cockles. The intensity of infection of both species was also positively correlated with trematode species richness and metacercarial abundance. This study highlighted the possible detrimental role of Himasthla spp. in cockle population dynamics. It also revealed the risks of misidentification, which should be resolved by further molecular approaches.

Rare inventory of trematode diversity in a protected natural reserve

In the face of ongoing habitat degradation and the biodiversity crisis, natural reserves are important refuges for wildlife. Since most free-living organisms serve as hosts to parasites, the diverse communities in protected areas can be expected to provide suitable habitats for a species-rich parasite fauna. However, to date, assessments of parasite diversity in protected nature reserves are rare. To expand our knowledge of parasite communities in natural habitats, we examined 1994 molluscs belonging to 15 species for trematode infections in a central European natural reserve. The parasitological examination revealed an overall prevalence of 17.3% and a total species richness of 40 trematode species. However, the parasite diversity and prevalence did not differ markedly from trematode communities in non-protected environments, which might be partly explained by a dilution effect caused by a high number of non-host organisms in our study system. The proportion of complex and long life cycles of parasites in the present study is high, indicating complex biotic interactions. We conclude that life cycle complexity, in addition to parasite diversity and trematode species richness, can provide valuable information on ecosystem health and should therefore be considered in future studies.

Emerging helminthiases of song thrush (Turdus philomelos) in Central Europe.

Turdus philomelos is a common Western Palearctic thrush species of forests and agricultural landscapes, where it relies on the presence of hedgerows, patches of trees, and shrubs. In the present study, we address long-term changes in component communities of trematodes in T. philomelos across the timespan of over half a century. Based on our preliminary observations, we hypothesized that component communities of trematodes in T. philomelos in the study area are more diverse and species-rich compared with several decades ago. In the 1961-2019, we performed full-body necropsies of T. philomelos, which originated from the southern Czech Republic, and examined them for the presence of trematodes. We compared the trematode species richness and diversity of the analyzed component communities. The number of trematode species per host steadily increased in time in adult females and males. In juveniles, the highest numbers of trematode species per host were reached already in 1961-1990, then dropped and slowly raised up again in the latter time periods. The newly accumulated evidence suggests that trematodes with intermediate hosts previously restricted to T. philomelos wintering grounds increased in abundance in the study area. Some of them (Morishitium polonicum, Psilotornus confertus) sporadically appeared in juveniles or first-year birds, from which they were previously completely absent. Some of the spreading species, such as Lutztrema attenuatum, are present in high prevalence and high intensities of infection. Yet unknown part of observed changes could be related to changes in food composition; however, direct evidence for changes in T. philomelos diet is lacking despite clear evidence for a decline in earthworms in agricultural landscapes.

Systemic collapse of a host-parasite trematode network associated with wetland birds in Europe.

As host community diversity decreases, parasite diversity may also decline. The life cycles of trematodes involve multiple hosts from different orders, with many trematodes displaying narrow host specialization. In the 1960s and 2010s, we performed full-body necropsies of juvenile or first-year birds of four wetland bird species, Anas platyrhynchos, Aythya fuligula, Fulica atra, and Chroicocephalus ridibundus which originated from the southern Czech Republic, and examined them for the presence of trematodes. We compared the trematode species richness and diversity of the analyzed component communities. We found complete disintegration of host-parasite networks, which led to declining populations and local extinctions of the majority of trematode species, particularly those with narrow host preferences. For example, in black-headed gulls, 67% of trematode species recorded in the 1960s were absent in gulls that were examined in the 2010s. In contrast, we did not identify any trematode species that were absent in the 1960s but present in the 2010s. This collapse provides new insight into the recent debate regarding whether human-caused extinctions should be considered a problem when locally extinct host species are replaced by an equal or even higher number of nonnative species, thus maintaining local alpha diversities but leading to biotic homogenization and consequently reducing beta diversity. By documenting the collapse of the host-parasite network, we provide a strong argument that biodiversity cannot be assessed by simple measures alone, as only local-scale conservation measures allow the preservation of host-pathogen interactions and nutrient cycles and thus prevent the loss of low-visibility species, such as helminths.

Latitudinal gradients of parasite richness: a review and new insights from helminths of cricetid rodents

The latitudinal diversity gradient (LDG), or the trend of higher species richness at lower latitudes, has been well documented in multiple groups of free‐living organisms. Investigations of the LDG in parasitic organisms are comparatively scarce. Here, I investigated latitudinal patterns of parasite diversity by reviewing published studies and by conducting a novel investigation of the LDG of helminths (parasitic nematodes, trematodes and cestodes) of cricetid rodents (Rodentia: Cricetidae). Using host–parasite records from 175 parasite communities and 60 host species, I tested for the presence and direction of a latitudinal pattern of helminth richness. Additionally, I examined four abiotic factors (mean annual temperature, annual precipitation, annual temperature range and annual precipitation range) and two biotic variables (host body mass and host diet) as potential correlates of parasite richness. The analyses were performed with and without phylogenetic comparative methods, as necessary. In this system, helminths followed the traditional LDG, with increasing species richness with decreasing latitude. Nematode richness appeared to drive this pattern, as cestodes and trematodes exhibited a reverse LDG and no latitudinal pattern, respectively. Overall helminth richness and nematode richness were higher in areas with higher mean annual temperatures, annual precipitation and annual precipitation ranges and lower annual temperature ranges, characteristics that often typify lower latitudes. Cestode richness was higher in areas of lower mean annual temperatures, annual precipitation and annual precipitation ranges and higher annual temperature ranges, while trematode richness showed no relationship with climate variables when phylogenetic comparative methods were used. Host diet was significantly correlated with cestode and trematode species richness, while host body mass was significantly correlated with nematode species richness. Results of this study support a complex association between parasite richness and latitude, and indicate that researchers should carefully consider other factors when trying to understand diversity gradients in parasitic organisms.

Phylogeography and genetics of the globally invasive snail Physa acuta Draparnaud 1805, and its potential to serve as an intermediate host to larval digenetic trematodes

BackgroundPhysa acuta is a globally invasive freshwater snail native to North America. Prior studies have led to conflicting views of how P. acuta populations are connected and genetic diversity is partitioned globally. This study aims to characterize phylogeographic and population genetic structure within the native range of P. acuta, elucidate its invasion history and assess global patterns of genetic diversity. Further, using meta-analytic methods, we test the ‘Enemy-Release hypothesis’ within the P. acuta – digenetic trematode system. The ‘Enemy-Release hypothesis’ refers to the loss of native parasites following establishment of their host within an invasive range. Population genetic data is combined with surveys of trematode infections to map range-wide trematode species richness associated with P. acuta, and to identify relevant host-population parameters important in modeling host-parasite invasion.ResultsPhylogenetic analyses using mtDNA uncovered two major clades (A & B). Clade A occurs globally while clade B was only recovered from the Western USA. All invasive populations sampled grouped within Clade A, where multiple independent source populations were identified from across North America. Significant population genetic structure was found within the native range of P. acuta, with some evidence for contemporary geographic barriers between western and eastern populations. Mito-nuclear discordance was found suggesting historical isolation with secondary contact between the two mitochondrial clades. Trematode species richness was found to differ significantly between native and invasive populations, in concordance with the ‘Enemy-Release hypothesis’. Further, our data suggests a positive relationship between nucleotide diversity of invasive populations and trematode prevalence and richness.ConclusionsThis study includes a wider geographic sampling of P. acuta within its native range that provides insight into phylogeographic and population genetic structure, range-wide genetic diversity and estimation of the invasion history. Meta-analysis of P. acuta – trematode surveys globally is consistent with the ‘Enemy-Release hypothesis’. Additionally, results from this study suggest that host demographic parameters, namely genetic diversity as a proxy for population size, may play an essential role in how parasite communities assemble within invasive host populations. This knowledge can be used to begin to construct a framework to model host-parasite invasion dynamics over time.

Parasites and invasions: a biogeographic examination of parasites and hosts in native and introduced ranges

AbstractAim To use a comparative approach to understand parasite demographic patterns in native versus introduced populations, evaluating the potential roles of host invasion history and parasite life history.Location North American east and west coasts with a focus on San Francisco Bay (SFB).Methods Species richness and prevalence of trematode parasites were examined in the native and introduced ranges of two gastropod host species, Ilyanassa obsoleta and Littorina saxatilis. We divided the native range into the putative source area for introduction and areas to the north and south; we also sampled the overlapping introduced range in SFB. We dissected 14,781 snails from 103 populations and recorded the prevalence and identity of trematode parasites. We compared trematode species richness and prevalence across the hosts’ introduced and native ranges, and evaluated the influence of host availability on observed patterns.Results Relative to the native range, both I. obsoleta and L. saxatilis have escaped (lost) parasites in SFB, and L. saxatilis demonstrated a greater reduction of trematode diversity and infection prevalence than I. obsoleta. This was not due to sampling inequalities between the hosts. Instead, rarefaction curves suggested complete capture of trematode species in native source and SFB subregions, except for L. saxatilis in SFB, where infection was extremely rare. For I. obsoleta, infection prevalence of trematodes using fish definitive hosts was significantly lower in SFB compared to the native range, unlike those using bird hosts. Host availability partly explained the presence of introduced trematodes in SFB.Main conclusions Differential losses of parasite richness and prevalence for the two gastropod host species in their introduced range is probably the result of several mechanistic factors: time since introduction, propagule pressure, vector of introduction, and host availability. Moreover, the recent occurrence of L. saxatilis’ invasion and its active introduction vector suggest that its parasite diversity and distribution will probably increase over time. Our study suggests that host invasion history and parasite life history play key roles in the extent and diversity of trematodes transferred to introduced populations. Our results also provide vital information for understanding community‐level influences of parasite introductions, as well as for disease ecology in general.

Distribution of parasites in their second ­intermediate host, the cockle Cerastoderma edule: community heterogeneity and spatial scale

We studied the spatial heterogeneity of infection of the marine bivalve Cerastoderma edule (cockle) by trematode parasites at 5 different scales in Banc d'Arguin, France. At the km-scale, the communities of trematodes differed among stations in terms of species composition and specific abundance. Infection heterogeneity was likely due to the occurrence of the definitive host and the conditions of transmission (water parameters). At the 100 m scale, trematode species richness was similar among stations, but specific trematode abundances differed. The most significant variable in terms of explaining trematode infection heterogeneity was the presence of the first intermediate host. At the 10 m scale, the distance at which parasite abundance diminished varied according to trema- tode species. When an intense source of trematode larvae (cercariae) emission was suspected, this abundance was maintained within ca. 20 m. Outside this area, parasite abundance progressively dropped. We found a higher aggregation in parasite distribution at the 100 m scale than at the 10 m scale using a community aggregation measure. At the cm-scale, the parasite species richness was similar in all cockles but parasite abundance differed in relation to distance when the parasites were shed by a sedentary host compared to a motile host. Observed differences of infection could also be due to intrinsic factors (life history, immune system) as suggested by an experimental infestation where cockles challenged in similar conditions displayed different parasite loads. We demonstrated that high heterogeneity of parasite infection in cockles should be taken into account in studies con- cerning the role of parasites in ecosystems.

Large-scale patterns in trematode richness and infection levels in marine crustacean hosts

Little is known about the patterns of variation in parasitism in marine hosts. Trematodes, the dominant parasites in intertidal systems, are transmitted from their first intermediate hosts (snails) to a range of second intermediate hosts, including crustaceans. Using published studies of trematode infections in crustacean hosts, we investigated general patterns of variation in trematode species richness and infection levels (i.e. percentage of hosts infected and mean number of individ- ual parasites per host). Since the production and release of infective stages in snails is strongly tem- perature dependent, we also investigated a potential decrease in trematode infection levels with increasing latitude (as a proxy for decreasing temperature). Trematode species richness in the crus- tacean hosts was generally low (mostly 1 or 2), and infection levels were moderate. However, there were differences among taxa in some groups, particularly among brachyuran crabs, which showed significantly higher values than in other groups. For amphipods, which were the only well-studied group across a large range of latitudes, we found negative correlations between latitude and the trematode species richness or measures of infection level considered here. These relationships per- sisted after correction of the potentially confounding effects of sampling effort, host body size and host generic identity (as a control for phylogenetic influences). We discuss these findings in light of environmental mediation of parasite transmission, in particular with respect to the probably funda- mental role of temperature in driving the output of trematode infective stages in marine systems.

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

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

Large-scale determinants of trematode infections in intertidal gastropods

The influence of latitude, substrate type, tidal level, and host shell size on trematode species-richness and prevalence were assessed using published data on 255 samples from 54 species of marine intertidal gastropods. The analyses were performed at different levels of statistical inde- pendence: among all samples, across snail species, and using phylogenetically independent con- trasts. Repeatability analysis showed that both trematode species richness and prevalence could be considered as snail species traits. Although there was much within-species variation among values obtained from different samples, the among-species variation was much higher. After removing the confounding effect of sample size, positive relationships between trematode prevalence and species richness were observed at all levels of analysis, highlighting the additive nature of trematode infec- tions in snails. The latitude at which samples were collected had a significant effect on trematode species richness across all samples, but this influence disappeared at higher levels of analyses. There was no evidence that host shell size (as well as life-span and population density) was associated with either trematode species richness or prevalence. Tidal level and substrate type (rocky versus soft- sediment) where samples were collected had significant effects on trematode species richness across all samples. These effects could not be verified at higher levels of analyses. Overall, the results point toward an important role of local, small-scale factors in determining the number of trematode species infecting snails and the proportion of infected snails in a population.