Associations between shorebird abundance and parasites in the sand crab, Emerita analoga, along the California coast

I investigated spatial variation in the prevalence and abundance of 4 species of parasites in the sand crab, Emerita analoga, on 8 sandy beaches along 800 km of the California coast, to assess the importance of bird abundance for the distribution of parasites among sand crab populations. I collected sand crabs and counted shorebirds and gulls at each beach during June and November 1994. Sand crabs served as intermediate hosts for 4 species of parasites, including a trematode, Spelotrema nicolli (Cable and Hunnienen, 1938); an acanthocephalan, Polymorphus kenti (Van Cleave, 1947); a nematode, Proleptus sp., and an unidentified trypanorhynch tapeworm. Among sand crab populations, there was substantial spatial variation in the prevalence and abundance of each parasite species. No latitudinal pattern was apparent for any of the 4 species observed. Temporally, parasite prevalence and abundance was significantly different between dates for all 4 parasites. Specifically, sand crab populations experienced higher trematode, nematode, and trypanorhynch prevalence and abundance in November than in June. In contrast, prevalence and abundance of acanthocephalans were higher in June than in November. There were strong positive associations between bird abundance and prevalence of parasitic infection for trematodes and acanthocephalans for some dates but not for nematodes or trypanorhynchs, which use elasmobranchs as definitive hosts. The spatial variation in prevalence and abundance of trematodes and acanthocephalans observed among sand crab populations may be attributed to the distribution and abundance of shorebirds and gulls that serve as definitive hosts.     

Land Use and Wetland Spatial Position Jointly Determine Amphibian Parasite Communities

Land use change is one of the most commonly cited contributing factors to infectious disease emergence, yet the mechanisms responsible for such changes and the spatial scales at which they operate are rarely identified. The distributions of parasites with complex life cycles depend on interactions between multiple host species, suggesting the net effects of land use on infection patterns may be difficult to predict a priori. Here, we used an information-theoretic approach to evaluate the importance of land use and spatial scale (local, watershed, and regional) in determining the presence and abundance of multi-host trematodes of amphibians. Among 40 wetlands and 160 hosts sampled, trematode abundance, species richness, and the presence and abundance of pathogenic species were strongly influenced by variables at the watershed and regional scales. Based on model averaging results, overall parasite richness and abundance were higher in forested wetlands than in agricultural areas; however, this pattern was influenced by a wetland's proximity to the Mississippi Flyway at the regional scale. These patterns likely reflect the activity of trematode definitive hosts, such as mammals and especially birds, such that infections decreased with increasing distance from the Mississippi River. Interestingly, despite lower mean infections, agricultural wetlands had higher variances and maximum infections. At the wetland scale, phosphorus concentrations and the abundances of intermediate hosts, such as snails and larval amphibians, positively affected parasite distributions. Taken together, these results contribute to our understanding of how altered landscapes affect parasite communities and inform further research on the environmental drivers of amphibian parasite infections.     

Larval trematodes (Digenea) of the great pond snail, Lymnaea stagnalis (L.), (Gastropoda, Pulmonata) in Central Europe: a survey of species and key to their identification

A survey of cercariae and metacercariae (Trematoda, Digenea) from the great pond snail (Lymnaea stagnalis) in Central Europe (Austria, Czech Republic, South-East Germany, Poland and Slovak Republic) is presented, based on a study of 3,628 snails examined from 1998 to 2005. A total of 953 (26.3%) L. stagnalis were infected with 24 trematode species comprising 19 species of cercariae and 11 species of metacercariae (six species occurred both as cercarie and metacercarie) of eight families. The dominant cercariae were those of Opisthioglyphe ranae (159 hosts infected), Plagiorchis elegans (141) (both family Plagiorchiidae) and Echinoparyphium aconiatum (153) (Echinostomatidae); 14 double infections were found. The most frequent metacercariae were those of Neoglyphe locellus (71) (Omphalometridae), E. aconiatum (66), Echinostoma sp. (59) and Moliniella anceps (48) (Echinostomatidae). In the previous studies carried out in Central Europe, a very similar spectrum of nine trematode families of 22 cercariae determined to species level and 43 types of cercariae reported under generic or provisional names, which can be in many cases conspecific with the previous taxa, were found. A simple key to identification of cercariae and metacercariae, together with their illustrations, is provided.     

Environmental factors influencing community composition of gastropods and their trematode parasites in southern Ontario

Agricultural activity and landscape features have previously been associated with diversity and prevalence of trematode species in amphibian second intermediate hosts. In this study, the density, diversity, and size of snail first intermediate hosts, and the diversity and prevalence of their trematode species, were assessed in 2 types of ponds, i.e., those adjacent to cornfields and those from the same region in southwestern Ontario that were adjacent to nonagricultural settings. Species of trematodes included, but were not restricted to, those that are known parasites of larval and adult frogs. We also assessed landscape factors likely to influence use by definitive hosts. Presence of the herbicide atrazine in ponds was measured to check that ponds adjacent to agriculture had potential to be affected by agricultural runoff. Both snail size and the proportion of snails releasing cercariae were greater in nonagricultural ponds, contrasting with a previous finding of lower trematode infection in tadpoles from nonagricultural ponds. Percentage of forest cover was associated with prevalence of certain trematode species, but not with estimates of combined prevalence. Absence of relations of trematode prevalence to measures of road density also contrasted with previous studies. We interpret our results in light of how agricultural activity might influence trematode viability, snail growth, and use by wildlife definitive hosts, independently of landscape factors.     

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.     

Host-parasite interactions and global climate oscillations

It is suspected that host-parasite interactions are influenced by climatic oscillations such as the North Atlantic Oscillation (NAO). However, the effects of climatic oscillations on host-parasite interactions have never been investigated. A long-term (1982-1999) dataset of the host snail Lymnaea stagnalis and trematode metacercariae infection has been collected for Lake Chany in Western Siberia. Using this dataset, we estimated the impact of the NAO on the population dynamics of hosts and parasites as well as their interactions. The results of general linear models showed that the abundance of dominant parasite species and the total parasite abundance significantly increased with NAO, with the exception of Moliniella anceps. Other climatic and biological factors were relatively weak to explain the abundance. There was no significant relationship between NAO and the population density of host snails. The prevalence of infection was related to the total abundance of parasites, but not to the NAO. Thus, the responses to the NAO differed between the host and parasites, indicating mismatching in host-parasite interactions. Therefore, climatic oscillations, such as the NAO, influence common parasitism.     

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.     

Guild structure of larval trematodes in the snail Helisoma anceps: patterns and processes at the individual host level

Factors that influenced the infracommunity structure of trematodes parasitizing the pulmonate snail Helisoma anceps were studied over a 15-mo period; the guild included 8 species of parasites. Infracommunities were depauperate, with double patent infections observed in only 7 of 1,485 infected snails; a total of 4,899 was examined. Halipegus occidualis-Haematoloechus longiplexus was the most common dual infection. Both species share the same definitive host and, in both cases, eggs are the infective stage for the snail. Switches and losses of infections in individual snails were observed, suggesting the occurrence of dynamic interactions within the guild. A dominance hierarchy was constructed based on field observations and experimental infections. Echinostomatids were dominant; species without rediae in their life cycles were subordinates. Halipegus occidualis (which has rediae) was intermediate in dominance. Spatial and temporal heterogeneity in the distribution and abundance of trematode infective stages indicate that not all the snails have the same probability of becoming infected. Habitat structure, behavior of the definitive host, the nature of the infective stages, and snail population dynamics (mortality, recruitment, and size structure) generated spatial and temporal heterogeneity in this system. As a consequence, predictions of the probabilities of interspecific interactions based on an analysis of observed and expected frequencies of multiple infections could be inappropriate unless the potential sources of heterogeneity are considered.     

Host, macrohabitat, and microhabitat specificity in the gill parasite Afrodiplozoon polycotyleus (Monogenea)

Studies on species of Monogenea have shown that these parasites often infect only a specific host species, genus, or family, and that they attach only to specific sites within hosts. Few studies, however, examine habitat specificity across host and habitat scales. In this study, we focused on host, macrohabitat, and microhabitat specificity in the monogenean diplozoon Afrodiplozoon polycotyleus, a gill parasite of African cyprinid fishes, Barbus spp. We first compared the occurrence of A. polycotyleus among 4 species of Barbus from a single location in the Mpanga River of western Uganda; Barbus neumayeri was the only species infected with the parasite. We then quantified parasite prevalence and mean abundance in B. neumayeri from a series of river and swamp sites in the same drainage, looking for environmental predictors of diplozoon prevalence and abundance over a broad habitat scale. The prevalence and mean abundance of A. polycotyleus on gills of B. neumayeri was highest in the hypoxic swamp habitat, followed by the intermittent stream sites, and faster flowing river sites. Parasite prevalence and mean abundance across habitats were negatively related to both water current and dissolved oxygen concentration. Within hosts, A. polycotyleus was strongly specific among hemibranchs in poorly oxygenated water and was found on arch 2, hemibranch 4 most frequently.     

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.     

Diversity of trematode genetic clones within amphipods and the timing of same-clone infections

The genetic diversity of trematodes within second intermediate hosts has important implications for the evolution of trematode populations as these hosts are utilized after the parasites reproduce asexually within first intermediate hosts and before sexual reproduction within definitive hosts. We characterised the genetic clonal diversity of the marine trematode Maritrema novaezealandensis within amphipod (Paracalliope novizealandiae) second intermediate hosts using four to six microsatellite loci to determine if multiple copies of identical trematode clones existed within naturally infected amphipods. To determine the relative timing of infections by identical clones within hosts, trematode metacercariae were assigned to six developmental stages and the stages of identical clones were compared. The genotypes of 306 trematodes were determined from 44 amphipods each containing more than one trematode. Six pairs of identical trematode clones were recovered in total (representing five amphipods: 11% of amphipods with greater than one trematode) and all pairs of clones belonged to the same developmental stage. This suggests that identical clone infections are effectively synchronous. A general decrease in the number of metacercariae recovered, prevalence, and mean intensity of infection for each subsequent developmental stage coupled with large numbers of metacercariae (>9) only being recovered from recent infections, supports the occurrence of post-infection amphipod mortality and/or within-host trematode mortality. Taken together, our results indicate that natural infections are characterised by high genetic diversity, but that amphipods also periodically encounter "batches" of genetically identical clones, potentially setting the stage for interactions within and between clonal groups inside the host.     

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.     

Spatial heterogeneity in recruitment of larval trematodes to snail intermediate hosts

Spatial variation in parasitism is commonly observed in intermediate host populations. However, the factors that determine the causes of this variation remain unclear. Increasing evidence has suggested that spatial heterogeneity in parasitism among intermediate hosts may result from variation in recruitment processes initiated by definitive hosts. I studied the perching and habitat use patterns of wading birds, the definitive hosts in this system, and its consequences for the recruitment of parasites in snail intermediate hosts. Populations of the mangrove snail, Cerithidea scalariformis, collected from mangrove swamps on the east coast of central Florida are parasitized by a diverse community of trematode parasites. These parasites are transmitted from wading birds, which frequently perch on dead mangrove trees. I tested the hypothesis that mangrove perches act as transmission foci for trematode infections of C. scalariformis and that the spatial variation of parasitism frequently observed in this system is likely to emanate from the distribution of wading birds. On this fine spatial scale, definitive host behaviors, responding to a habitat variable, influenced the distribution, abundance and species composition of parasite recruitment to snails. This causal chain of events is supported by regressions between perch density, bird abundance, bird dropping density and ultimately parasite prevalence in snails. Variation between prevalence of parasites in free-ranging snails versus caged snails shows that while avian definitive hosts initiate spatial patterns of parasitism in snails through their perching behaviors, these patterns may be modified by the movement of snail hosts. Snail movement could disperse their associated parasite populations within the marsh, which may potentially homogenize or further increase parasite patchiness initiated by definitive hosts.     

The component community structure of larval trematodes in the pulmonate snail Helisoma anceps

Factors that affected the component community structure of larval trematodes in the pulmonate snail Helisoma anceps in Charlie's Pond, North Carolina, were studied over a 15-mo period using a multiple mark-recapture protocol. Patent infections of 8 species were observed in 1,485 of 4,899 snails examined. Reproductive activity, population size, and survival rate of the snail population were estimated to evaluate the extent of resource availability for the parasites. Antagonistic interactions between trematode species that occurred at the infracommunity level had a neglible effect on the composition and structure of the component community. The patterns observed at this level were related to temporal heterogeneity in the abundance of infective stages (mostly miracidia), differential responses of trematode species to the diverse and constantly changing distribution of snail size and abundance, differential mortality of snails infected with certain trematode species, constant recruitment of 1 trematode species over time, and the existence of predictable disturbances such as the complete mortality of the host population and recruitment of a replacement population during a 6-8 wk period. The last factor operated as a reset mechanism for this snail-trematode system once each year. A model of patch dynamics, with snails as patch resources, best explains the organization and dynamics of this system.     

Relationships between nutrient enrichment,pleurocerid snail density and trematode infection rate in streams

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Changes in the sulfhydryl group content in the hemolymph of freshwater gastropods infected with trematode parthenitae and larvae

A study was conducted on the changes in sulphhydryl groups in the haemolymph of Lymnaea stagnalis infected with partenites of Opisthioglyphe ranae, Planorbis corneus infected with partenites of Cotylurus cornutus and females of Viviparus viviparus infected with partenites and larvae of Echinoparyphium petrowi. At the infection in the haemolymph of hosts were recorded statystically reliable changes in the protein sulphhydryl groups which are blocked by toxines excreted by the parasites. The reduction rate in the content of these substances depends on the localization of the parasites and infection intensity of the hosts.     

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

Aim 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.     

Distance decay of similarity among parasite communities of three marine invertebrate hosts

The similarity in species composition between two communities generally decays as a function of increasing distance between them. Parasite communities in vertebrate definitive hosts follow this pattern but the respective relationship in intermediate invertebrate hosts of parasites with complex life cycles is unknown. In intermediate hosts, parasite communities are affected not only by the varying vagility of their definitive hosts (dispersing infective propagules) but also by the necessary coincidence of all their hosts in environmentally suitable localities. As intermediate hosts often hardly move they do not contribute to parasite dispersal. Hence, their parasite assemblages may decrease faster in similarity with increasing distance than those in highly mobile vertebrate definitive hosts. We use published field survey data to investigate distance decay of similarity in trematode communities from three prominent coastal molluscs of the Eastern North-Atlantic: the gastropods Littorina littorea and Hydrobia ulvae, and the bivalve Cerastoderma edule. We found that the similarity of trematode communities in all three hosts decayed with distance, independently of local sampling effort, and whether or not the parasites used the mollusc as first or second intermediate host in their life cycle. In H. ulvae, the halving distance (i.e. the distance that halves the similarity from its initial similarity at 1 km distance) for the trematode species using birds as definitive hosts was approximately two to three times larger than for species using fish. The initial similarities (estimated at 1 km distance) among trematode communities were relatively higher, whereas mean halving distances were lower, compared to published values for parasite communities in vertebrate hosts. We conclude that the vagility of definitive hosts accounts for a high similarity at the local scale, while the strong decay of similarity across regions is a consequence of the low probability that all necessary hosts and suitable environmental conditions coincide on a large scale.     

Spatial and temporal structure of the trematode component community in Valvata macrostoma (Gastropoda, Prosobranchia)

We conducted the first comprehensive study on the spatiotemporal structure of trematode communities in the large-mouthed valve snail, Valvata macrostoma. A total of 1103 snails were examined monthly between May and October 2007 from Lake Konnevesi, Central Finland, from a shallow (1-2 m deep) and an offshore site (5-6 m deep), located ca. 50-70 m apart. Snails were infected by 10 trematode species. The species composition and prevalence were strikingly different between the sites with high species diversity in the shallow site (all 10 species; total prevalence of sporocysts/rediae 12.1%, metacercariae 55.4%) compared to the deeper site (3 species; prevalence 15.0% and 1.9%, respectively). This difference persisted throughout our study and is probably related to the spatial distribution of bird definitive hosts, whereas the seasonal parasite dynamics are likely to be affected by changes in the age-structure of the snail population. The probability of sporocyst infections increased with snail size, but no such trend was observed in redial or metacercarial infections which decreased with host size. Our results show that generally well-described spatiotemporal differences in trematode infection of molluscs can emerge in very narrow spatial and temporal scales, which emphasizes the importance of these factors in community studies.     

Acanthocephala from lake fishes in Wisconsin: ecology and host relationships of Pomphorhynchus bulbocolli (Pomphorhynchidae)

Pomphorhynchus bulbocolli Linkins in Van Cleave, 1919, was considerably more common in fishes of the river-connected Tichigan Lake than of the landlocked Silver Lake, southeastern Wisconsin. It is reported from 17 species of principal, accessory, and occasional definitive hosts (new record in Moxostoma carinatum) and from 13 species of paratenic hosts (new records in Amia calva, Ictalurus punctatus, Lepomis cyanellus, and Pomoxis nigromaculatus). Infection patterns were influenced by fish species, feeding behavior, temperature, availability of intermediate host, type of water body, fish movement, and changes in fish host community. Host roles are not fixed but are often interchangeable. A seasonal cycle in prevalence, intensity, and maturation was evident, with greatest abundance and maturation during summer and recruitment during summer and autumn. Recruitment of new infections, development, and release of eggs, however, occurred all year. Sex ratio changed from near equal in new infections to one more highly in favor of females in older adults. Female fish were considerably more frequently and heavily infected than males. No relationship with fish age (size) was evident. Worms were mostly attached in posterior intestinal locations but initial establishment sites correlated with temperature. Translocation of P. bulbocolli due to competitive exclusion in concurrent infections was not observed. The significance of extraintestinal larval forms in the cycle of transmission was noted.