Metazoan parasite species in cultured mussel Mytilus galloprovincialis in the Thermaikos Gulf (North Aegean Sea, Greece)

This is the first study on parasites of cultured Mytilus galloprovincialis L. in Greek waters, and is based on samples collected every 2 to 3 mo between September 2000 and November 2001 at 3 stations in the Thermaikos Gulf. Each sample comprised 40 mussels. We found 4 metazoan parasite species: hydroid Eugymnanthea inquilina, gill turbellarian Urastoma cyprinae, trematode Proctoces maculatus and gut copepod Mytilicola intestinalis. Of 840 mussels examined, 406 (48.3%) mussels were harbouring hydroids of E. inquilina, 278 (33.1%) were infested with U. cyprinae, 94 (11.2%) were infested with M. intestinalis, and only 7 (0.8%) were infested with P. maculatus. The prevalence and intensity of these parasites were related to temperature and pollution. Mussels infested with these parasites had significantly lower condition indices than non-infested mussels; larger mussels were more often infested than smaller ones.     

Ploidy levels in silverside fishes (Atherinidae, Menidia) on the Texas coast: flow-cytometric analysis of the occurrence of allotriploidy

Flow cytometry of nuclear DNA fluorescence in erythrocytes, coupled with gene dosage assessments derived from electrophoresis of proteins, reaffirmed that the Menidia clarkhubbsi complex of unisexual atherinid fishes is diploid. Non-recombinant hybrids between M. beryllina and M. peninsulae represented 18% (108 specimens) of the Menidia collected from three pools in the Copano Bay area and 9-6% (42 specimens) of those from a pool on Galveston Island. Of those hybrids, 35 and 5%, respectively, were triploids. Zymograms indicated that the triploids either had two doses of genes from M. beryllina and one from M. peninsulas or they had one from the former species and two from the latter. The hybrids seem to be maintained primarily, if not entirely, by ongoing hybridization and back-crossing of F₁ hybrids to the parental species. Triploids apparently result from the combination of unreduced, diploid gametes from F₁ hybrids with haploid gametes from either M. beryllina or M. peninsulae.     

Interspecific antagonism and virulence in hosts exposed to two parasite species

Co-infection of host organisms by multiple parasite species has evolutionary consequences for all participants in the symbiosis. In this study, we co-exposed aquatic-snails (Biomphalaria glabrata) to two of their trematode parasites, Schistosoma mansoni and Echinostoma caproni. In co-exposed snails, E. caproni prevalence was 63% compared to only 23% for S. mansoni. Co-exposed E. caproni-infected snails exhibited reduced fecundity, higher mortality, and higher parasite reproduction (higher virulence) compared to hosts exposed to echinostomes alone. Conversely, co-exposed S. mansoni-infected snails released fewer parasites and produced greater numbers of eggs compared to hosts exposed to S. mansoni alone. These results suggest that co-exposure not only influences the establishment (presence or absence) of particular parasite species, but also impacts host life history, parasite reproduction, and the virulence of the interaction.     

Migration highways and migration barriers created by host–parasite interactions

Co‐evolving parasites may play a key role in host migration and population structure. Using co‐evolving bacteria and viruses, we test general hypotheses as to how co‐evolving parasites affect the success of passive host migration between habitats that can support different intensities of host–parasite interactions. First, we show that parasites aid migration from areas of intense to weak co‐evolutionary interactions and impede migration in the opposite direction, as a result of intraspecific apparent competition mediated via parasites. Second, when habitats show qualitative difference such that some environments support parasite persistence while others do not, different population regulation forces (either parasitism or competitive exclusion) will reduce the success of migration in both directions. Our study shows that co‐evolution with parasites can predictably homogenises or isolates host populations, depending on heterogeneity of abiotic conditions, with the second scenario constituting a novel type of ‘isolation by adaptation’.     

Ecological and developmental dynamics of a host-parasite system involving a sea anemone and two ctenophores

The lined sea anemone Edwardsiella lineata has evolved a derived parasitic life history that includes a novel body plan adapted for life inside its ctenophore hosts. Reputedly its sole host is the sea walnut, Mnemiopsis leidyi, a voracious planktivore and a seasonally abundant member of many pelagic ecosystems. However, we have observed substantially higher E. lineata prevalence in a second ctenophore species, the ctenophore predator Bero? ovata. The interplay among these 3 species has important conservation consequences as M. leidyi introductions are thought to be responsible for the severe depletion of numerous commercial fisheries in the Mediterranean basin, and both E. lineata and B. ovata have been proposed as biological controls for invasive M. leidyi. Over a 3-yr period (2004-2006), we collected 8,253 ctenophores from Woods Hole, Massachusetts, including M. leidyi, B. ovata, and a third ctenophore, Pleurobrachia pileus, and we recorded E. lineata infection frequencies, parasite load, and parasite location. We also conducted laboratory experiments to determine the likely mechanisms for parasite introduction and the effect of each host on parasite development. We observed peak E. lineata infection frequencies of 0% in P. pileus, 59% in M. leidyi, and 100% in B. ovata, suggesting that B. ovata could be an important natural host for E. lineata. However, in laboratory experiments, E. lineata larvae proved far more successful at infecting M. leidyi than B. ovata, and E. lineata parasites excised from M. leidyi exhibited greater developmental competence than parasites excised from B. ovata. Although we show that E. lineata is efficiently transferred from M. leidyi to B. ovata when the latter preys upon the former, we conclude that E. lineata larvae are not well adapted for parasitizing the latter species and that the E. lineata parasite is not well adapted for feeding in B. ovata; these developmental and ecological factors underlie the host specificity of this recently evolved parasite.     

Proximate factors affecting the larval life history of Acanthocephalus lucii (Acanthocephala)

The growth and eventual size of larval helminths in their intermediate hosts presumably has a variety of fitness consequences. Therefore, elucidating the proximate factors affecting parasite development within intermediate hosts should provide insight into the evolution of parasite life histories. An experimental infection that resulted in heavy intensities of an acanthocephalan (Acanthocephalus lucii) in its isopod intermediate host (Asellus aquaticus) permitted the examination of parasite developmental responses to variable levels of resource availability and intraspecific competition. Isopods were infected by exposure to egg-containing fish feces, and larval infrapopulations were monitored throughout the course of A. lucii development. The relative rate of parasite growth slowed over time, and indications of resource constraints on developing parasites, e.g., crowding effects, were only observed in late infections. Consequently, the factors likely representative of resource availability to larval parasites (host size and molting rate) primarily affected parasite size in late infections. Moreover, at this stage of infection, competitive interactions, gauged by variation in worm size, seemed to be alleviated by greater resources, i.e., larger hosts that molted more frequently. The relatively rapid, unconstrained growth of young parasites may be worse for host viability than the slower, resource-limited growth of larger parasites.     

High intensity and prevalence of two species of trematode metacercariae in the fathead minnow (Pimephales promelas) with no compromise of minnow anti-predator competence

Opportunity for parasites to manipulate host behavioral phenotype may be influenced by several factors, including the host ecology and the presence of cohabiting parasites in the same host. Metacercariae of Ornithodiplostomum ptychocheilus and "black spot" Crassiphiala bulboglossa have similar life cycles. Each parasite uses a littoral snail as a first intermediate host, fathead minnows as a second intermediate host, and a piscivorous bird as a final host. Metacercariae of black spot encyst in the dermal and epidermal tissues, while metacercariae of O. ptychocheilus encyst on the brain over a region that coordinates optomotor responses. Because of site differences within the host, we predicted that O. ptychocheilus metacercariae might manipulate the behavioral phenotype of minnows to facilitate transmission to the final host, but metacercariae of black spot would not. In our study population, prevalence was 100% for O. ptychocheilus , with an overall median intensity of 105 metacercariae per minnow. Prevalence of black spot was 60%, with a median abundance and intensity of 12 and 20 metacercariae per minnow for the overall sample and for infected fish, respectively. Minnows accumulated both parasites over time, producing significant correlations between intensity and minnow body length and between intensities of the 2 parasites. Minnows infected with black spot had on average twice as many O. ptychocheilus metacercariae as similar-sized minnows without any black spot cercariae. We found no correlation between body condition of minnows and intensity for either parasite. We measured 2 aspects of anti-predator competence to test for effects linked to parasite intensity. We found no correlation between intensity of either species of parasite and latency to behavioral response to attack from a mechanical model heron, nor was there any effect of parasite intensity on a measure of shoaling affinity. The absence of any detectable effect of metacercariae on anti-predator competence in minnows may reflect selection against parasite pathology from predation by non-hosts of the parasites and overwinter mortality due to low dissolved oxygen.     

Host species,and not environment,predicts variation in blood parasite prevalence,distribution, and diversity along a humidity gradient in northern South America

Environmental factors strongly influence the ecology and evolution of vector‐borne infectious diseases. However, our understanding of the influence of climatic variation on host–parasite interactions in tropical systems is rudimentary. We studied five species of birds and their haemosporidian parasites (Plasmodium and Haemoproteus) at 16 sampling sites to understand how environmental heterogeneity influences patterns of parasite prevalence, distribution, and diversity across a marked gradient in water availability in northern South America. We used molecular methods to screen for parasite infections and to identify parasite lineages. To characterize spatial heterogeneity in water availability, we used weather‐station and remotely sensed climate data. We estimated parasite prevalence while accounting for spatial autocorrelation, and used a model selection approach to determine the effect of variables related to water availability and host species on prevalence. The prevalence, distribution, and lineage diversity of haemosporidian parasites varied among localities and host species, but we found no support for the hypothesis that the prevalence and diversity of parasites increase with increasing water availability. Host species and host × climate interactions had stronger effects on infection prevalence, and parasite lineages were strongly associated with particular host species. Because climatic variables had little effect on the overall prevalence and lineage diversity of haemosporidian parasites across study sites, our results suggest that independent host–parasite dynamics may influence patterns in parasitism in environmentally heterogeneous landscapes.     

Bottom–up regulation of parasite population densities in freshwater ecosystems

Theory predicts the bottom–up coupling of resource and consumer densities, and epidemiological models make the same prediction for host–parasite interactions. Empirical evidence that spatial variation in local host density drives parasite population density remains scarce, however. We test the coupling of consumer (parasite) and resource (host) populations using data from 310 populations of metazoan parasites infecting invertebrates and fish in New Zealand lakes, spanning a range of transmission modes. Both parasite density (no. parasites per m²) and intensity of infection (no. parasites per infected hosts) were quantified for each parasite population, and related to host density, spatial variability in host density and transmission mode (egg ingestion, contact transmission or trophic transmission). The results show that dense and temporally stable host populations are exploited by denser and more stable parasite populations. For parasites with multi‐host cycles, density of the ‘source’ host did not matter: only density of the current host affected parasite density at a given life stage. For contact‐transmitted parasites, intensity of infection decreased with increasing host density. Our results support the strong bottom–up coupling of consumer and resource densities, but also suggest that intraspecific competition among parasites may be weaker when hosts are abundant: high host density promotes greater parasite population density, but also reduces the number of conspecific parasites per individual host.     

Aggregation and species coexistence of ectoparasites of marine fishes.

Interspecific interaction may lead to species exclusion but there are several ways in which species can coexist. One way is by reducing the overall intensity of competition via aggregated utilisation of fragmented resources. Known as the 'aggregation model of coexistence', this system assumes saturation and an equilibrium number of species per community. In this study we tested the effects of interspecific aggregation on the level of intraspecific aggregation among ectoparasites of marine fishes (36 communities of gill and head ectoparasite species). If parasite species are distributed in a way that interspecific aggregation is reduced relative to intraspecific aggregation then species coexistence is facilitated. We found a positive relationship between parasite species richness and fish body size, controlling for host phylogeny. A positive relationship between infracommunity species richness and total parasite species richness was also found, providing no evidence for saturation. This result supports the view that infracommunities of parasites are not saturated by local parasite residents. The observed lack of saturation implies that we are far from a full exploitation of the fish resource by parasites. Ectoparasites were aggregated at both population and species levels. However, only half of the ectoparasite communities were dominated by negative interspecific aggregation. We found that infracommunity parasite species richness was positively correlated with the level of intraspecific aggregation versus interspecific aggregation. This means that intraspecific aggregation increases compared with interspecific aggregation when total parasite species richness increases, controlling fish size and phylogeny. This supports one assumption of the 'aggregation model of coexistence', which predicts that interspecific interactions are reduced relative to intraspecific interactions, facilitating species coexistence.     

Transmission and burden and the impact of temperature on two species of vertically transmitted microsporidia

Microsporidia are unusual amongst eukaryotic parasites in that they utilize both vertical and horizontal transmission and vertically transmitted species can cause sex ratio distortion in their host. Here we study vertical transmission in two species of feminising microsporidia, Nosema granulosis and Dictyocoela duebenum, infecting a single population of the crustacean host Gammarus duebeni and measure the effect of temperature on parasite transmission and replication. N. granulosis was vertically transmitted to 82% of the host embryos and D. duebenum was transmitted to 72% of host embryos. For both parasites, we report relatively low parasite burdens in developing host embryos. However, the parasites differ in their pattern of replication and burden within developing embryos. Whilst N. granulosis undergoes replication during host development, the burden of D. duebenum declines, leading us to propose that parasite dosage and feminisation efficiency underlie the different parasite frequencies in the field. We also examine the effect of temperature on parasite transmission and replication. Temperature does not affect the percentage of young that inherit the infection. However, low temperatures inhibit parasite replication relative to host cell division, resulting in a reduction in parasite burden in infected embryos. The reduced parasite burden at low temperatures may underpin reduced feminization at low temperatures and so limit the spread of sex ratio distorters through the host population.     

Spatiotemporal and gender‐specific parasitism in two species of gobiid fish

Parasitism is considered a major selective force in natural host populations. Infections can decrease host condition and vigour, and potentially influence, for example, host population dynamics and behavior such as mate choice. We studied parasite infections of two common marine fish species, the sand goby (Pomatoschistus minutus) and the common goby (Pomatoschistus microps), in the brackish water Northern Baltic Sea. We were particularly interested in the occurrence of parasite taxa located in central sensory organs, such as eyes, potentially affecting fish behavior and mate choice. We found that both fish species harbored parasite communities dominated by taxa transmitted to fish through aquatic invertebrates. Infections also showed significant spatiotemporal variation. Trematodes in the eyes were very few in some locations, but infection levels were higher among females than males, suggesting differences in exposure or resistance between the sexes. To test between these hypotheses, we experimentally exposed male and female sand gobies to infection with the eye fluke Diplostomum pseudospathaceum. These trials showed that the fish became readily infected and females had higher parasite numbers, supporting higher susceptibility of females. Eye fluke infections also caused high cataract intensities among the fish in the wild. Our results demonstrate the potential of these parasites to influence host condition and visual abilities, which may have significant implications for survival and mate choice in goby populations.     

Performance of Myrmica ant colonies is correlated with the presence of social parasites

1. The performance of ant colonies depends on different factors such as nest site, colony structure or the presence of pathogens and social parasites. Myrmica ants host various types of social parasites, including the larvae of Maculinea butterflies and Microdonmyrmicae (Schönrogge) hoverfly. How these social parasites affect host colony performance is still unexplored. 2. It was examined how the presence of Maculinea teleius Bergsträsser, Maculinea alcon (Denis & Schiffermüller), and M. myrmicae larvae, representing different feeding and growth strategies inside host colonies, is associated with worker survival, the number of foragers, and colony productivity parameters such as growth and reproduction. 3. It was found that the presence of social parasites is negatively associated with total colony production and the production of ant larvae and gynes. Male production was lower only in nests infested by M. teleius, whereas the number of worker pupae was significantly higher in all types of infested colonies than in uninfested colonies. Laboratory observations indicated that nests infested by Maculinea larvae are characterised by a higher number of foragers compared to uninfested nests but we did not find differences in worker survival among nest types. 4. The observed pattern of social parasite influence on colony productivity can be explained by the feeding strategies of parasitic larvae. The most negative effect was found for M. teleius, which feeds on the largest host brood and eliminates a high number of sexual forms. The strong, adverse influence of all studied parasite species on gyne production may result in low queen production in Myrmica populations exposed to these social parasites.     

Host tolerance and resistance to parasitic nest flies differs between two wild bird species

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Variations in the parasite fauna of the Patagonian toothfish (Dissostichus eleginoides Smitt, 1898), with length, season, and depth of habitat around the Falkland Islands

The parasite fauna of Dissostichus eleginoides was examined from locations around the Falkland Islands. In total, of 11,362 individual parasites of 27 taxa were recovered from 105 fish. Two species, Ceratomyxa dissostichi and Sphaerospora dissostichi, represent new host records. The nematode Ascarophis nototheniae and the larval acanothocephalan Corynosoma bullosum were found to be new locality records and add to the knowledge of the biogeography and host specificity of parasites on the Patagonian Shelf. There were no significant differences in the mean abundance and prevalence of parasites recovered between sexes. Therefore, sex was not considered in further analysis and the data were pooled. Cysts of unknown etiology (CUE), the monogenean Neopavlovskioides georgianus, the larval acanthocephalan Corynosoma bullosum, and the digenean Neolepidapedon magnatestis had significant positive correlations with increasing host length. The larval Trypanorhynch cestode Grillotia erinaceus and the digenean Elytrophalloides oatesi showed significant negative correlations with increasing host length. CUEs, N. georgianus, the digenean Gonocerca physidis and E. oatesi showed statistically significant prevalence between summer, winter, and spring. The effect of depth on parasite communities was also examined, initially using a linear discriminant function analysis. The prevalence of individual parasites was then compared between depth strata using the chi-square test. The parasite communities on the shelf and deep water (> 1,000 m) were found to be different, whereas those caught at intermediate depths on the shelf slope were found to have parasite communities that were intermediate, containing a mixture of shelf and deeper-water parasites. The causes of the variations in parasite faunas in association with these intrinsic and extrinsic factors are discussed.     

Co‐evolutionary patterns in congeneric monogeneans: a review of Dactylogyrus species and their cyprinid hosts

Patterns associated with the evolution of parasite diversity, speciation and diversification were analysed using Dactylogyrus species (gill monogeneans) and their cyprinid hosts as a model. The aim of this study was to use this highly specific host–parasite systems to review: (1) the diversity and distribution of Dactylogyrus species, (2) the patterns of organization and structure of Dactylogyrus communities, (3) the evolution and determinants of host specificity and (4) the mode of Dactylogyrus speciation and co‐evolutionary patterns in this Dactylogyrus–cyprinid systems. Dactylogyrus are a highly diverse group of parasites, with their biogeography and distribution clearly linked to the evolutionary history of their cyprinid hosts. The coexistence of several Dactylogyrus species on one host is facilitated by increasing niche distances and the differing morphology of their reproductive organs. The positive interspecific and intraspecific interactions seem to be the most important factors determining the structure of Dactylogyrus communities. Host specificity is partially constrained by parasite phylogeny. Being a strict specialist is an ancestral character for Dactylogyrus, being the intermediate specialists or generalists are the derived characters. The evolution of attachment organ morphology is associated with both parasite phylogeny and host specificity. Considering larger and long‐lived hosts or hosts with several ecological characters as the measures of resource predictability, specialists with larger anchors occurred on larger or longer‐living fish species. Intra‐host speciation, a mode of speciation not often recorded in parasites, was observed in Dactylogyrus infecting sympatric cyprinids. Sister parasite species coexisting on the same host occupied niches that differed in at least one niche variable. Intra‐host speciation, however, was not observed in Dactylogyrus species of congeneric hosts from geographically isolated areas, which suggested association by descent and host‐switching events.     

Host defence versus intraspecific competition in the regulation of infrapopulations of the flea Xenopsylla conformis on its rodent host Meriones crassus

Mechanisms that regulate parasite populations may influence the evolution of hosts and parasites, as well as the stability of host-parasite dynamics but are still poorly understood. A manipulation experiment on the grooming ability of rodent hosts (Meriones crassus) and flea (Xenopsylla conformis) densities on these hosts successfully disentangled two possible regulating mechanisms: (i) behavioural defence of the host and (ii) intraspecific competition among parasites, and revealed their importance in suppressing the feeding of fleas. Moreover, the results suggest that flea competition is direct and is not mediated by host grooming, immune response, or parasite-induced damage to the host. These mechanisms, together with interspecific competition and density-dependent parasite-induced host damage, may limit the parasite burden on an individual host and may prevent parasites from overexploiting their host population.     

Water temperature,not fish morph,determines parasite infections of sympatric Icelandic threespine sticklebacks (Gasterosteus aculeatus)

Parasite communities of fishes are known to respond directly to the abiotic environment of the host, for example, to water quality and water temperature. Biotic factors are also important as they affect the exposure profile through heterogeneities in parasite distribution in the environment. Parasites in a particular environment may pose a strong selection on fish. For example, ecological differences in selection by parasites have been hypothesized to facilitate evolutionary differentiation of freshwater fish morphs specializing on different food types. However, as parasites may also respond directly to abiotic environment the parasite risk does not depend only on biotic features of the host environment. It is possible that different morphs experience specific selection gradients by parasites but it is not clear how consistent the selection is when abiotic factors change. We examined parasite pressure in sympatric morphs of threespine stickleback (Gasterosteus aculeatus) across a temperature gradient in two large Icelandic lakes, Myvatn and Thingvallavatn. Habitat‐specific temperature gradients in these lakes are opposite. Myvatn lava rock morph lives in a warm environment, while the mud morph lives in the cold. In Thingvallavatn, the lava rock morph lives in a cold environment and the mud morph in a warm habitat. We found more parasites in fish living in higher temperature in both lakes, independent of the fish morph, and this pattern was similar for the two dominating parasite taxa, trematodes and cestodes. However, at the same time, we also found higher parasite abundance in a third morph living in deep cold–water habitat in Thingvallavatn compared to the cold‐water lava morph, indicating strong effect of habitat‐specific biotic factors. Our results suggest complex interactions between water temperature and biotic factors in determining the parasite community structure, a pattern that may have implications for differentiation of stickleback morphs.     

Entobdella soleae--pointers to the future

The biology of the monogenean skin parasite Entobdella soleae and its relationship with its host, the common sole (Solea solea), are probably better known than those of any other monogeneans. The author describes his early involvement with this parasite and the special features of parasite and host that make this relationship so suitable for parasitological studies. Aspects of the biology of E. soleae that have been investigated are briefly mentioned, but most of the paper is concerned with areas of the parasite's biology that remain a challenge to determine. Unresolved areas are as follows: (1) the identity of the factor (or factors) in host skin mucus that stimulates hatching of the parasite's eggs; (2) whether or not the larvae of the parasite are attracted to their host; (3) the nature of factors controlling the contrasting behaviour of adult parasites on the upper and lower surfaces of the host; (4) how nutrients are supplied to the remote regions of the haptor; (5) whether the host has any control via its immune system over parasite invasion success and survival; (6) how the parasite copes with the migratory habits of some sole populations, assuming that such populations are infested with the parasite. The intimacy of this parasite/host relationship is its most remarkable feature, the reflection of which, not surprisingly, is the greatly restricted host range of the parasite. E. soleae has been reported from only three host species, all highly specialised bottom-dwelling members of Solea. It is all the more surprising that relatives of E. soleae, such as Neobenedenia melleni, retain the ability to parasitise an enormous range of hosts. How this versatility is achieved remains to be seen.     

Multiple choice: hemiparasite performance in multi‐species mixtures

Hemiparasitic plants have green leaves, but extract water and solutes from neighbouring plants. It is still poorly understood how different host plants in communities contribute to parasite performance, as species that are good hosts in single‐host experiments may not necessarily be preferred hosts in mixtures. We grew the root hemiparasite Rhinanthus alectorolophus (Orobanchaceae) together with each of 13 host species (experiment 1) and with 15 different four‐species mixtures of these hosts (experiment 2) that differed in the number of legumes and of host functional groups. Parasites profited from mixtures including more legumes and from mixtures including different host functional groups. Some host species and mixtures were very tolerant of parasitism and supported large parasites without being strongly suppressed in their own growth, but the suppression of a species in the single‐host experiment did not explain the suppression of a species in a host mixture. We thus calculated for each host species an index of the difference in suppression between the two experiments which may be related to host use in a mixture. Host quality (mean parasite biomass with a host species) in the single‐host experiment could explain 64% of the variation in parasite biomass with a host mixture when it was weighted by the proportion of the host species in the mixture without the parasite and by the suppression difference index. Our results suggest that plant species which are the best hosts in single‐host experiments are not always those used most strongly by a parasite growing with a mixture. Together with the finding that hemiparasites benefit from a mixed diet based on hosts from different functional groups this suggests that parasites prefer certain host species to obtain a mixed diet.