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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.

Age Factors↗

Life history constraints on the evolution of abbreviated life cycles in parasitic trematodes.

Abbreviations of the complex life cycle of trematodes, from three to two hosts, have occurred repeatedly and independently among trematode lineages. This is usually facultative and achieved via progenesis: following encystment in the second intermediate host, the metacercaria develops precociously into an egg-producing adult, bypassing the need to reach a definitive host. Given that it provides relatively cheap insurance against a shortage of definitive hosts, it is not clear why facultative progenesis has only evolved in a few taxa. Here a comparative approach is used to test whether progenetic trematodes are characterized by larger body size and egg volumes, two traits that correlate with other key life history features, than other trematodes. These traits may constrain the evolution of progenesis, because precocious maturation might be impossible when the size difference between the metacercaria and a reproductive adult is too large. First, trematode species belonging to genera in which progenesis has been documented were found not to differ significantly from other trematode species. Second, using within-genus paired comparisons across 19 genera in which progenesis has been reported, progenetic species did not differ, with respect to body size or egg size, from their non-progenetic congeners. Third, using intraspecific paired comparisons in species where progenesis is facultative, no difference was observed in the sizes of eggs produced by worms in both the intermediate and definitive host, suggesting that opting for progenesis does not influence the size of a worm's eggs. Overall, the lack of obvious differences in body or egg size between trematodes with truncated life cycles and those with the normal three-host cycle indicates that basic life history characteristics are not acting as constraints on the evolution of progenesis; trematodes of all sizes can do it. Why facultative progenesis is not more widespread remains a mystery.

Animals↗

Analysis of 16S rRNA and 51-kilodalton antigen gene and transmission in mice of Ehrlichia risticii in virgulate trematodes from Elimia livescens snails in Ohio.

Operculate snails (the family Pleuroceridae: Elimia livescens) were collected between June and October 1998 from a river in central Ohio where repeated cases of Potomac horse fever (PHF) have occurred. Of collected snails, consistently 50 to 80% carried a combination of cercariae and sporocysts of digenetic virgulate trematodes. The trematodes obtained from each snail were pooled and tested for Ehrlichia risticii, the agent of PHF, by nested PCR using primers specific to the 16S rRNA gene. Out of a total of 209 trematode pools, 50 pools were found to be positive by PCR. The DNA sequence of the 16S rRNA gene identified in one trematode pool was identical to that of the type strain of E. risticii, and the sequence of the gene identified in another pool differed from that of the type strain by 1 nucleotide. Comparison of the deduced amino acid sequence of the partial 51-kDa antigen gene from various sources revealed that Maryland, Ohio (except Ohio 081), and Kentucky strains are in a cluster distinct from the sequences obtained from sources in California and Oregon. Ohio 081 was shown previously by antigenic composition analysis to be distinct from other groups. However, all sequences examined were not segregated according to their sources: horse blood or infected trematodes. E. risticii was found to be transmittable from trematodes to mice and was subsequently passaged from infected mice to additional mice, as determined by PCR analysis. Our findings suggest the evolution of E. risticii in the natural reservoir in separate geographic regions and persistent infection of trematode populations with E. risticii during summer and early fall. The study also suggests that the mouse can be used to isolate E. risticii from the infected trematode.

Amino Acid Sequence↗

A perspective on the ecology of trematode communities in snails.

This paper presents a perspective on the ecology of trematodes in snail hosts based on recent evidence. Because flukes use snails almost obligatorily as first intermediate hosts, we highlight the role of gastropods as keystone species for trematodes and their communities. After reviewing recent developments in the transmission of trematodes to and from snails, we discuss trematode communities within individual snails (infracommunities) and in snail populations (component communities). Results garnered using various protocols at the infracommunity level are reviewed. The few data available, all from marine systems, indicate that low colonization rates characterize infracommunities, suggesting that trematode infracommunities tend to be isolationist in character rather than interactive. The variety of trematode species present in a component community seems to be determined by spatial overlap of definitive hosts. Relative abundance of species in a component community shows little dependence on negative interspecific interactions at the level of the infracommunity. Temporal aspects of trematode communities are related to the life history of the host snail. The component communities of long-lived snails (mostly marine) integrate many infection episodes whereas shorter-lived snails (mostly freshwater) acquire new component communities each time host cohorts turnover.

Animals↗

Snail-trematode life history interactions: past trends and future directions.

Life history traits expressed by organisms vary due to ecological and evolutionary constraints imposed by their current environmental conditions and genetic heritage. Trematodes often alter the life history of their host snails by inducing parasitic castration. Our understanding of the variables that influence the resulting changes in host growth, fecundity and survivorship is insufficient to confidently predict specific outcomes of novel snail-trematode combinations. In a literature review of the last 30 years, we found 41 publications examining various life history characteristics of trematode-infected snails. These publications reported 113 different field and laboratory experiments involving 30 snail species and 39 trematode species and provided a data set for assessing factors that potentially affect life history outcomes. Analysis of the diverse responses across various snail-trematode systems and experimental conditions teased out general patterns for the expression of host growth, fecundity and survival. These were used to address existing hypotheses and develop several new ones relating the response of snail-trematode interactions to environmental and genetic factors. Finally, we propose directions for future experiments that will better assess the ecological and evolutionary factors influencing snail life history responses to trematode parasitism.

Animals↗

Can parasites be indicators of free-living diversity? Relationships between species richness and the abundance of larval trematodes and of local benthos and fishes.

Measuring biodiversity is difficult. This has led to efforts to seek taxa whose species richness correlates with the species richness of other taxa. Such indicator taxa could then reduce the time and cost of assessing the biodiversity of the more extensive community. The search for species richness correlations has yielded mixed results, however. This may be primarily because of the lack of functional relationships between the taxa studied. Trematode parasites are highly promising bioindicators. Diverse assemblages of larval trematode parasites are easily sampled in intermediate host snails. Through their life cycles these parasites are functionally coupled with the surrounding free-living diversity of vertebrate and invertebrate animals. It has been shown that larval trematodes in snails correlate positively with bird diversity and abundance. Here, we explore whether trematodes also correlate with standard measures of fishes, and large and small benthos, for 32 sites in three wetlands. We found associations between trematodes and benthic communities that were not consistent across wetlands. The associations were, however, consistently positive for large benthic species richness and density. Some of the contrasting associations between trematode and benthos may be explained by negative associations between large and small benthos. We found no associations with fish communities (probably because of the inadequacy of standard "snapshot" sampling methods for highly mobile fishes). The results support further exploration of trematodes as bioindicators of diversity and abundance of animal communities.

Animals↗

The trematodes of groupers (Serranidae: Epinephelinae): knowledge, nature and evolution.

Groupers (Epinephelinae) are prominent marine fishes distributed in the warmer waters of the world. Review of the literature suggests that trematodes are known from only 62 of the 159 species and only 9 of 15 genera; nearly 90% of host-parasite combinations have been reported only once or twice. All 20 families and all but 7 of 76 genera of trematodes found in epinephelines also occur in non-epinephelines. Only 12 genera of trematodes are reported from both the Atlantic-Eastern Pacific and the Indo-West Pacific. Few (perhaps no) species are credibly cosmopolitan but some have wide distributions across the Indo-West Pacific. The hierarchical 'relatedness' of epinephelines as suggested by how they share trematode taxa (families, genera, species) shows little congruence with what is known of their phylogeny. The major determinant of relatedness appears to be geographical proximity. Together these attributes suggest that host-parasite co-evolution has contributed little to the evolution of trematode communities of epinephelines. Instead, they appear to have arisen through localized episodes of host-switching, presumably both into and out of the epinephelines. The Epinephelinae may well be typical of most groups of marine fishes both in the extent to which their trematode parasites are known and in that, apparently, co-evolution has contributed little to the evolution of their communities of trematodes.

Adaptation, Physiological↗

Digenetic trematodes, Acanthatrium sp. and Lecithodendrium sp., as vectors of Neorickettsia risticii, the agent of Potomac horse fever.

Neorickettsia (formerly Ehrlichia) risticii, the agent of Potomac horse fever (PHF), has been recently detected in trematode stages found in the secretions of freshwater snails and in aquatic insects. Insectivores, such as bats and birds, may serve as the definitive host of the trematode vector. To determine the definitive helminth vector, five bats (Myotis yumanensis) and three swallows (Hirundo rustica, Tachycineta bicolor) were collected from a PHF endemic location in northern California. Bats and swallows were dissected and their major organs examined for trematodes and for N. risticii DNA using a nested polymerase chain reaction (PCR) assay. Adult digenetic trematodes, Acanthatrium sp. and/or Lecithodendrium sp., were recovered from the gastrointestinal tract of all bats and from one swallow. The intestine of three bats, the spleen of two bats and one swallow as well as the liver of one swallow tested PCR positive for N. risticii. From a total of seven pools of identical digenetic trematodes collected from single hosts, two pools of Acanthatrium sp. and one pool of Lecithodendrium sp. tested PCR positive. The results of this investigation provide preliminary evidence that at least two trematodes in the family Lecithodendriidae are vectors of N. risticii. The data also suggest that bats and swallows not only act as a host for trematodes but also as a possible natural reservoir for N. risticii.

Anaplasmataceae Infections↗

Component community of larval trematodes in the mudsnail Hydrobia ventrosa: temporal variations in prevalence in relation to host life history.

Temporal variations in the prevalence of larval trematodes in the short-lived prosobranch mudsnail Hydrobia ventrosa (Montagu) were investigated in relation to host life history and season for 4 successive years in temperate windflats of the southern Baltic Sea. The component community of trematode larvae in H. ventrosa comprises at least 10 species; families (and species) represented include Notocotylidae (1), Echinostomatidae (1 or 2), Heterophyidae (2), Monorchidae (1), Microphallidae (3 or 4), Psilostomatidae (1), and Hemiuridae (1). The notocotylid Paramonostomum alveatum was the most prevalent species, followed by the microphallids Maritrema subdolum and Microphallus sp. Trematode prevalence in H. ventrosa fluctuated seasonally. Prevalence usually peaked in summer between July and September-October and decreased in late winter-early spring. This seasonal change is chiefly explained by the life history patterns of the semelparous snail host. Hydrobia ventrosa has a maximum life span of about 2 yr and reproduces between June and November of its second calendar year. The first trematode infections appeared annually in May when the most abundant cohort of H. ventrosa, the second-calendar-year snails, mature. The prevalence continued to increase until August-September, throughout the reproductive period of the second-calendar-year snails, Prevalence decreased during winter, when most of the second-calendar-year snails died after reproduction. On the basis of longterm laboratory experiments, it has been shown that the late autumn-winter mortality was not the result of trematode infections. Seasonal patterns of prevalence were similar among the trematode species except for the monorchid Asymphylodora demeli, the only one using fish definitive hosts. Species-specific differences in the seasonal occurrence of prepatent infections and the predominance of certain larval stages in winter are interpreted as different strategies of the trematode species to survive the harsh winter conditions, or to survive the death of the first intermediate host in autumn-winter, or both.

Animals↗

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.

Animals↗

Egg production in adult trematodes: adaptation or constraint?

Parasite life-history traits should reflect past environmental and host-related selective pressures acting to produce strategies that maximize transmission success. The evolution of adult body size and egg production in 804 species of trematode parasites was investigated using independent contrasts derived from a phylogeny of trematodes. Contrasts in trematode body size were positively correlated with contrasts in egg size, and almost significantly correlated with contrasts in numbers of uterine eggs. After controlling for body size, no relationship existed between egg size and egg numbers, suggesting that there is no trade-off between the two components of egg production. Average host body mass and latitude of the sampling site did not correlate with either trematode body size or egg size. Contrasts between trematode taxa exploiting ectotherm hosts and their sister taxa exploiting endotherms showed no consistent difference in either body size or egg size. The effect of other variables on trematode life-histories, such as the nature of the habitat in which eggs are released, the site of attachment within the host's body, or the number of hosts involved in the life-cycle, could not be evaluated statistically. The similarity in life-history traits among members of given clades suggests that phylogenetic constraints may have acted to limit or mask any adaptive changes expected from changes in host-related or environmental conditions.

Animals↗

Environmental factors influencing trematode prevalence in grey tree frog (Hyla versicolor) tadpoles in southern Ontario.

The emergence or increased prevalence of various parasites may be linked to alterations in host-parasite interactions caused by environmental changes. We investigated prevalence of trematode infections in grey tree frog (Hyla versicolor) tadpoles from ponds in nonagricultural settings versus ponds adjacent to cornfields in southern Ontario. We found that agricultural activity was a significant factor in determining the percentage of tadpoles infected by 1 or more trematodes from 1 or more species (combined trematode infection). However, we found no associations between combined trematode infection and forest cover; pond size; road density; and measures of water quality, such as nitrate level and the presence of the herbicide atrazine. Although combined trematode prevalence was associated only with agricultural activity, prevalence of Alaria species showed a positive association with forest cover. This latter result probably reflects the importance of habitat suitability for the canid definitive hosts of this trematode species.

Analysis of Variance↗

Trematode hemoglobins show exceptionally high oxygen affinity.

Ligand binding studies were made with hemoglobin (Hb) isolated from trematode species Gastrothylax crumenifer (Gc), Paramphistomum epiclitum (Pe), Explanatum explanatum (Ee), parasitic worms of water buffalo Bubalus bubalis, and Isoparorchis hypselobagri (Ih) parasitic in the catfish Wallago attu. The kinetics of oxygen and carbon monoxide binding show very fast association rates. Whereas oxygen can be displaced on a millisecond time scale from human Hb at 25 degrees C, the dissociation of oxygen from trematode Hb may require a few seconds to over 20 s (for Hb Pe). Carbon monoxide dissociation is faster, however, than for other monomeric hemoglobins or myoglobins. Trematode hemoglobins also show a reduced rate of autoxidation; the oxy form is not readily oxidized by potassium ferricyanide, indicating that only the deoxy form reacts rapidly with this oxidizing agent. Unlike most vertebrate Hbs, the trematodes have a tyrosine residue at position E7 instead of the usual distal histidine. As for Hb Ascaris, which also displays a high oxygen affinity, the trematodes have a tyrosine in position B10; two H-bonds to the oxygen molecule are thought to be responsible for the very high oxygen affinity. The trematode hemoglobins display a combination of high association rates and very low dissociation rates, resulting in some of the highest oxygen affinities ever observed.

Animals↗

Trematode life cycles: short is sweet?

Complex life cycles are a hallmark of parasitic trematodes. In several trematode taxa, however, the life cycle is truncated: fewer hosts are used than in a typical three-host cycle, with fewer transmission events. Eliminating one host from the life cycle can be achieved in at least three different ways. Some trematodes show even more extreme forms of life cycle abbreviations, using only a mollusc to complete their cycle, with or without sexual reproduction. The occurrence of these phenomena among trematode families are reviewed here and show that life cycle truncation has evolved independently many times in the phylogeny of trematodes. The hypotheses proposed to account for life-cycle truncation, in addition to the factors preventing the adoption of shorter cycles by all trematodes are also discussed. The study of shorter life cycles offers an opportunity to understand the forces shaping the evolution of life cycles in general.

Adaptation, Physiological↗

A loss of fecundity in a population of mudsnails Hydrobia ventrosa caused by larval trematodes does not measurably affect host population equilibrium level.

Host snail demography and trematode parasitism were followed for one host generation in a shallow brackish lagoon of the western Baltic Sea. In addition, a laboratory experiment was simultaneously conducted to quantify the effects of parasitic infection on host fecundity. Hydrobia ventrosa of the cohort of 1996 had a maximum life-span of up to 2 years and reproduced between May and November of their second calendar year in 1997. Snails died after reproduction. The first trematode infections appeared in May 1997 when the snails started to mature. Total trematode prevalence peaked in summer and declined during winter to the lowest level in early spring 1998. Eight taxa of larval trematodes were found. Egg production of females with trematode infections was significantly reduced. Among females with pre-patent infections, about 20% were still able to produce eggs. Among females with patent infections merely 9% could lay eggs, compared to an average of about 51% in uninfected females. Taking into account a summer prevalence of about 25%, parasitic infections caused an overall reduction in egg production of the snail host population of about 15%. The reduction in host fecundity as a result of larval trematode infection did not measurably affect the population dynamics of H. ventrosa, because other environmental factors, especially winter severity and available food supply, were concluded to be much more relevant.

Animals↗

Agricultural land use and ensuing eutrophication both shape parasitic trematode communities in rural African lakes.

Land use is a major driver of biodiversity loss, but how it impacts parasite communities is scarcely documented. Crater lakes and their catchments in rural western Uganda greatly vary in their intensity of anthropogenic disturbance, thus providing an opportunity to assess the effects of land use on snail-borne parasitic trematodes. We applied state-of-the-art molecular biomonitoring to 2385 Bulinus tropicus snails from 34 lakes to detect and genotype trematode infections. The 45 trematode taxa recovered infect a wide range of final vertebrate hosts, and some can cause health burdens of significant public importance. Using constrained ordinations and generalized additive models, we found that B. tropicus reaches peak abundance in lakes with catchments partly under agriculture, whereas trematode infections increase with B. tropicus abundance and peak at intermediate aquatic productivity. Trematode diversity also increases with aquatic productivity, levelling off only in the most productive lakes. These relationships likely reflect the higher abundance and variety of final hosts sustained by more productive lakes. Finally, we found that land use affects trematode community composition, with more livestock parasites and less bird parasites occurring in agricultural catchments. Our results indicate that both land use and lake eutrophication affect the distribution of hotspots for parasitic disease transmission.

Lakes↗

Parasitism shaping host life-history evolution: adaptive responses in a marine gastropod to infection by trematodes.

1. Variation in life-history strategies among conspecific populations indicates the action of local selective pressures; recently, parasitism has been suggested as one of these local forces. 2. Effects of trematode infections on reproductive effort, juvenile growth, size at maturity and susceptibility were investigated among different natural populations of the marine gastropod Zeacumantus subcarinatus, Sowerby 1855. 3. Reproductive effort was not higher in uninfected snails from populations experiencing a high trematode prevalence, but females from high prevalence populations produced significantly larger offspring compared with their conspecifics from other populations. 4. Juvenile growth rate was significantly higher in laboratory-raised snails originating from females in a high prevalence population compared with other populations. 5. Size at maturity, determined by the appearance of functional gonads, was significantly and negatively related to trematode prevalence, and positively related to mean snail size, across 10 populations in the study area. 6. There was no evidence of different host resistance against trematodes in sentinel snails from high and low prevalence populations exposed to the same infection pressure in the field. 7. Our results strongly indicate that Z. subcarinatus adapt to trematodes by reaching maturity early, thereby maximizing their chance of reproducing in populations experiencing a high prevalence of infection by castrating trematodes.

Adaptation, Physiological↗

Neorickettsia risticii is vertically transmitted in the trematode Acanthatrium oregonense and horizontally transmitted to bats.

Potomac horse fever is known to be transmitted through the ingestion of caddisflies parasitized with Neorickettsia (formerly Ehrlichia) risticii-infected metacercaria. However, the species of trematode involved and how N. risticii is maintained in nature are unknown. In this study, gravid trematodes were recovered from the intestines of 12 out of 15 Eptesicus fuscus big brown bats and eight out of nine Myotis lucifugus little brown bats from various sites in Pennsylvania, USA. Trematode specimens isolated from six E. fuscus bats contained N. risticii DNA. The trematode was identified as Acanthatrium oregonense. N. risticii was detected within individual trematode eggs by polymerase chain reaction as well as by immunofluorescence labelling with an anti-N. risticii antibody, indicating that N. risticii is vertically transmitted (from adult to egg) in A. oregonense. Furthermore, N. risticii DNA was detected in the blood, liver or spleen of 23 out of 53 E. fuscus and M. lucifugus bats, suggesting that N. risticii can also be transmitted horizontally from trematode to bat. These results indicate that A. oregonense is a natural reservoir and probably a vector of N. risticii.

Anaplasmataceae Infections↗