Parasites and phytoplankton, with special emphasis on dinoflagellate infections

Planktonic members of most algal groups are known to harbor intracellular symbionts, including viruses, bacteria, fungi, and protozoa. Among the dinoflagellates, viral and bacterial associations were recognized a quarter century ago, yet their impact on host populations remains largely unresolved. By contrast, fungal and protozoan infections of dinoflagellates are well documented and generally viewed as playing major roles in host population dynamics. Our understanding of fungal parasites is largely based on studies for freshwater diatoms and dinoflagellates, although fungal infections are known for some marine phytoplankton. In freshwater systems, fungal chytrids have been linked to mass mortalities of host organisms, suppression or retardation of phytoplankton blooms, and selective effects on species composition leading to successional changes in plankton communities. Parasitic dinoflagellates of the genus Amoebophrya and the newly described Perkinsozoa, Parvilucifera infectans, are widely distributed in coastal waters of the world where they commonly infect photosynthetic and heterotrophic dinoflagellates. Recent work indicates that these parasites can have significant impacts on host physiology, behavior, and bloom dynamics. Thus, parasitism needs to be carefully considered in developing concepts about plankton dynamics and the flow of material in marine food webs.     

Ontogenetic allometry of the bluemouth, <Emphasis Type="Italic">Helicolenus dactylopterus dactylopterus</Emphasis> (Teleostei: Scorpaenidae), in the Northeast Atlantic and Mediterranean based on geometric morphometrics

Since the emergence of the ‘microbial loop’ concept, heterotrophic flagellates have received particular attention as grazers in aquatic ecosystems. These microbes have historically been regarded incorrectly as a homogeneous group of bacterivorous protists in aquatic systems. More recently, environmental rDNA surveys of small heterotrophic flagellates in the pelagic zone of freshwater ecosystems have provided new insights. (i) The dominant phyla found by molecular studies differed significantly from those known from morphological studies with the light microscope, (ii) the retrieved phylotypes generally belong to well-established eukaryotic clades, but there is a very large diversity within these clades and (iii) a substantial part of the retrieved sequences cannot be assigned to bacterivorous but can be assigned instead to parasitic and saprophytic organisms, such as zoosporic true fungi (chytrids), fungus-like organisms (stramenopiles), or virulent alveolate parasites (Perkinsozoa and Amoebophrya sp.). All these microorganisms are able to produce small zoospores to assure dispersal in water during their life-cycles. Based on the existing literature on true fungi and fungus-like organisms, and on the more recently published eukaryotic rDNA environmental studies and morphological observations, we conclude that previously overlooked microbial diversity and related ecological potentials require intensive investigation (i) for an improved understanding of the roles of heterotrophic flagellates in pelagic ecosystems and (ii) to properly integrate the concept of ‘the microbial loop’ into modern pelagic microbial ecology.     

What has happened to the “aquatic phycomycetes” (sensu Sparrow)? Part II: Shared properties of zoosporic true fungi and fungus-like microorganisms

Many species of zoosporic heterotrophic parasites, saprotrophs and mutualists in the Phyla Perkinsozoa (dinoflagellates), Oomycota, Hyphochytriomycota, Labyrinthulomycota and Phyomyxea share morphological characteristics with zoosporic true fungi especially with some of the Chytridiomycota and with fungus-like organisms in the Phyla Mesomycetozoea, Chytridiomycota and Aphelidae. These characteristics include chemotactic motile zoospores, zoosporangia which produce zoospores, thick walled resistant cysts, rhizoid-like structures, hyphal-like structures and cell walls surrounding the cells in several phases of their life cycle. These assemblages also inhabit both marine and freshwater ecosystems in which aquatic fungi and fungus-like organisms are found, have similar life cycles, grow on similar substrates, use similar infection strategies and infect some of the same host plants and animals. Many of these species were once included in the aquatic phycomycetes, an ecological assemblage of microorganisms but not a valid taxonomic group. Some of the shared characteristics are discussed in this review.     

The role of trematode parasites in larval anuran communities: an aquatic ecologist’s guide to the major players

Conservation strategies depend on our understanding of the ecosystem and community dynamics. To date, such understanding has focused mostly on predator–prey and competitor interactions. It is increasingly clear, however, that parasite–host interactions may represent a large, and important, component of natural communities. The need to consider multiple factors and their synergistic interactions if we are to elucidate the contribution of anthropogenic factors to loss in biodiversity is exemplified by research into present-day amphibian declines. Only recently has the role of factors such as trematode parasite infections been incorporated into studies of the population and community dynamics of aquatic systems. We argue that this is due, at least in part, to difficulties faced by aquatic ecologists in sifting through the complex systematics that pervade the parasite literature. We note that two trematode species are of dominant importance with regard to North American larval anuran communities, and provide in this review a clear explanation of how to distinguish between the infective stages of these two parasites. We describe the general biology and life history of these parasites, as well as what is known about their effect on larval anurans, and the interactive effects of environmental stressors (typically anthropogenic in nature) and parasites on larval anurans. We hope that this review will convince the reader of the potential importance of these parasites to aquatic communities in general, and to amphibian communities specifically, and will also provide the information necessary for aquatic ecologists to more frequently consider the role of these parasites in their studies of aquatic ecology.     

Phytoplankton chytridiomycosis: community structure and infectivity of fungal parasites in aquatic ecosystems

Fungal parasitism is recurrent in plankton communities, especially in the form of parasitic chytrids. However, few attempts have been made to study the community structure and activity of parasites at the natural community level. To analyse the dynamics of zoosporic fungal parasites (i.e. chytrids) of phytoplankton, samples were collected from February to December 2007 in two freshwater lakes. Infective chytrids were omnipresent in lakes, with higher diversity of parasites and infected phytoplankton than in previous studies. The abundance and biomass of parasites were significantly higher in the productive Lake Aydat than in the oligomesotrophic Lake Pavin, while the infection prevalence in both lakes were similar and averaged about 20%. The host species composition and their size appeared as critical for chytrid infectivity, the larger hosts being more vulnerable, including pennate diatoms and desmids in both lakes. The highest prevalence (98%) was noted for the autumn bloom of the cyanobacterium Anabaena flosaquae facing the parasite Rhizosiphon crassum in Lake Aydat. Because parasites killed their hosts, this implies that cyanobacterial blooms, and other large size inedible phytoplankton blooms as well, may not totally represent trophic bottlenecks because their zoosporic parasites can release dissolved substrates for microbial processes through host destruction, and provide energetic particles as zoospores for grazers. Overall, we conclude that the parasitism by zoosporic fungi represents an important ecological driving force in the food web dynamics of aquatic ecosystems, and infer general empirical models on chytrid seasonality and trophodynamics in lakes.     

Ecological impacts of parasitic chytrids,syndiniales and perkinsids on populations of marine photosynthetic dinoflagellates

Parasitism is a widespread interaction that plays significant roles in ecosystem balance and evolution. Historically the biology of zoosporic parasites is often a neglected field when studying aquatic ecological dynamics, especially in marine ecosystems. In the marine environment, dinoflagellates represent a significantly large component of primary production, and may be infected by a variety of fungal and fungus-like parasites including chytrids, syndiniales, and perkinsids as well as other microorganisms. The relationship between these organisms and their dinoflagellate hosts constitutes a highly significant pathosystem given the increasing importance of aquaculture. Because of their small size and lack of morphological characteristics these organisms are difficult to identify. This review compares the taxonomy, life cycle, host range, infection strategies, and ecological roles of species of Parvilucifera, Amoebophrya and Dinomyces which are parasites of dinoflagellates. Most of these species have only been described recently. Implications for environmental management are discussed.     

Fish introduction and parasites in marine ecosystems: a need for information

Invasive species provide unique and useful systems by which to examine various ecological and evolutionary issues, both in terms of the effects on native environments and the subsequent evolutionary impacts. While biological invasions are an increasing agent of change in aquatic systems, alien species also act as vectors for new parasites and diseases. To date, colonizations by hosts and parasites have not been treated and reviewed together, although both are usually interwoven in various ways and may have unpredictable negative consequences. Fish are widely introduced worldwide and are convenient organisms to study parasites and diseases. We report a global overview of fish invasions with associated parasitological data. Data available on marine and freshwater are in sharp contrast. While parasites and diseases of inland freshwater fish, ornamental, reared and anadromous fish species are well documented, leading to the emergence of several evolutionary hypotheses in freshwater ecosystems during the last decade, the transfer of such organisms are virtually unexplored in marine ecosystems. The paucity of information available on the parasites of introduced marine fish reflects the paucity of information currently available on parasites of non-indigenous species in marine ecosystems. However, such information is crucial as it can allow estimations of the extent to which freshwater epidemiology/evolution can be directly transferred to marine systems, providing guidelines for adapting freshwater control to the marine environment.     

More than meets the eye: detecting cryptic microgeographic population structure in a parasite with a complex life cycle

Nonrandom recruitment of parasites among hosts can lead to genetic differentiation among hosts and mating dynamics that promote inbreeding. It has been hypothesized that strictly aquatic parasites with intermediate hosts will behave as panmictic populations among hosts because ample opportunity exists for random mixing of unrelated individuals during transmission to the definitive host. A previous allozyme study on the marine trematode Lecithochirium fusiforme did not support this hypothesis; in that, there was genetic differentiation among, and significant heterozygote deficiencies within, definitive hosts. We revisit this system and use microsatellites to obtain multilocus genotypes. Our goal was to determine whether cryptic subgroups and/or the presence of clones could account for the apparent deviation from 'panmixia'. We find strong evidence for cryptic subdivision (three genetic clusters) that causes the Wahlund effect and differentiation among definitive hosts. After accounting for these cryptic groups, we see panmictic genetic structure among definitive hosts that is consistent with the 'high mixing in aquatic habitats' hypothesis. We see evidence for cotransmission of clones in all three clusters, but this level of clonal structure did not have a major impact in causing deviations from Hardy-Weinberg equilibrium, and only affected genetic differentiation among hosts in one cluster. A cursory examination of the data may have led to incorrect conclusions about nonrandom transmission. However, it is obvious in this system that there is more than meets the eye in relation to the actual make-up of parasite populations. In general, the methods we employ will be useful for elucidating hidden patterns in other organisms where cryptic structure may be common (e.g. those with limited morphology or complex life histories).     

The fascinating biology behind phage display: filamentous phage assembly

With the recently awarded Nobel Prize to the inventor of Phage Display, George Smith, the technique has once more gained attention. However, one should not forget about the biology behind the method. Almost always ignored is how the structure of this bacterial virus is assembled. In contrast to lytic phages, filamentous phages are constantly being extruded through the bacterial membranes without lysis. Such filamentous phages are found in all aquatic environments, such as rivers and lakes, in the deep sea, in arctic ice, in hot springs and, associated with their hosts, in plants and animals including humans. While most filamentous phages infect Gram‐negative hosts, inoviruses of Gram‐positive hosts have also been described. Despite being among the minority within the phage family with an estimate of less than 5%, filamentous phages are real parasites as they exist at the expense of the host, but do not kill it. In contrast to lytic bacteriophages, filamentous phages are assembled in the host’s membrane and extruded across the cellular envelope while the bacterium continues to grow. In this review, we focus on this complex and yet poorly understood process of assembly and secretion of filamentous phages.     

Minimal selfing, few clones, and no among-host genetic structure in a hermaphroditic parasite with asexual larval propagation

Little is known about actual mating systems in natural populations of parasites or about what constitutes the limits of a parasite deme. These parameters are interesting because they affect levels of genetic diversity, opportunities for local adaptation, and other evolutionary processes. We expect that transmission dynamics and the distribution of parasites among hosts should have a large effect on mating systems and demic structure, but currently we have mostly speculation and very few data. For example, infrapopulations (all the parasites in a single host) should behave as demes if parasite offspring are transmitted as a clump from host to host over several generations. However, if offspring are well mixed, then the parasite component population (all the parasites among a host population) would function as the deme. Similarly, low mean intensities or a high proportion of worms in single infections should increase the selfing rate. For species having an asexual amplification stage, transmission between intermediate and definitive (final) hosts will control the variance in clonal reproductive success, which in turn could have a large influence on effective sizes and rates of inbreeding. We examined demic structure, selfing rates, and the variance in clonal reproductive success in natural populations of Plagioporus shawi, a hermaphroditic trematode that parasitizes salmon. Overall levels of genetic diversity were very high. An a posteriori inference of population structure overwhelmingly supports the component population as the deme, rather than individual infrapopulations. Only a single pair of 597 adult individuals was identified as clones. Thus, the variance in clonal reproductive success was almost zero. Despite being hermaphroditic, P. shawi appears to be almost entirely outcrossing. Genetic estimates of selfing (<5%) were in accordance with the proportion of parasites from single infections. Thus, it appears that individual flukes outcross whenever possible and only resort to selfing when alone. Finally, our data support the hypothesis that aquatic transmission and the use of several intermediate hosts promotes high genetic diversity and well-mixed infrapopulations.     

The parasitic chytrid, Zygorhizidium, facilitates the growth of the cladoceran zooplankter, Daphnia, in cultures of the inedible alga, Asterionella

In food-web studies, parasites are often ignored owing to their insignificant biomass. We provide evidence that parasites may affect trophic transfer in aquatic food webs. Many phytoplankton species are susceptible to parasitic fungi (chytrids). Chytrid infections of diatoms in lakes may reach epidemic proportions during diatom spring blooms, so that numerous free-swimming fungal zoospores (2-3 microm in diameter) are produced. Analysis shows that these zoospores are rich in polyunsaturated fatty acids and sterols (particularly cholesterol), which indicates that they provide excellent food for zooplankters such as Daphnia. In life-table experiments using the large diatom Asterionella formosa as food, Daphnia growth increased significantly in treatments where a parasite was present. By grazing on the zoospores, Daphnia acquired important supplementary nutrients and were able to grow. When large inedible algae are infected by parasites, nutrients within the algal cells are consumed by these chytrids, some of which, in turn, are grazed by Daphnia. Thus, chytrids transfer energy and nutrients from their hosts to zooplankton. This study suggests that parasitic fungi alter trophic relationships in freshwater ecosystems and may be the important components in shaping the community and the food-web dynamics of lakes.     

Different thermal conditions of lakes affect host–parasite systems: A case study of Viviparus contectus (Millet, 1813) and digenean trematodes

1. Thermal disturbance of aquatic ecosystems directly and/or indirectly affects interspecific interactions, including parasitism. Both hosts and parasites respond differently to environmental changes, thus, predicting how host–parasite systems behave under the influence of disturbance remains a challenge. The aim of the study was to check how the differences in thermal conditions of lakes affect life-history traits of hosts and the level of parasitism, using a Viviparus contectus–digenean trematodes model.
2. Overall, we examined 480 individuals of V. contectus collected from a thermally polluted lake (TPL) and a natural lake (NL). Host features, including body size and fecundity, as well as the prevalence and species richness of digenean trematodes in snail populations were investigated.
3. We found that V. contectus from the TPL were significantly larger, heavier, and females were more fertile than snails collected from the NL. A total of 20.4% of the collected snails were infected with digenean larvae. The species richness of parasites was twice as high in the NL compared to the TPL (six and three species, respectively). A significant difference in the percentage of snails infected with parasites was identified between both types of lakes, with a higher prevalence of V. contectus in the NL (31.3%) compared to the TPL (7.3%).
4. These results indicate that host–parasite systems follow the environmental changes in lakes due to thermal pollution by increasing fertility and metabolism rate of viviparid hosts and by decreasing the prevalence and diversity of digenean trematodes.

     

Methylmercury levels in a parasite (<Emphasis Type="Italic">Apophallus brevis</Emphasis> metacercariae) and its host,yellow perch (<Emphasis Type="Italic">Perca flavescens</Emphasis>)

The biomagnification of methylmercury (MeHg) amongst trophic levels results in high levels of this compound in many freshwater fish species. The role of parasites in MeHg cycling and trophic transfer in freshwater systems is largely unknown. This study examined the potential for metacercariae of Apophallus brevis to accumulate and biomagnify MeHg from their second intermediate host, yellow perch, Perca flavescens. Contrary to our prediction that MeHg levels would be higher in parasites than in the host muscle tissue in which they are embedded, we found that concentrations were similar. The lack of increase in MeHg levels from host to parasite may be due to limited assimilation of host muscle tissue or, in part, to low parasite metabolism. Parasite load did not reduce fish growth and subsequently alter MeHg concentrations. This study suggests that relationships between larval parasites and their hosts do not conform to typical patterns of MeHg biomagnification seen in aquatic systems.     

Spread of parasites and diseases of aquatic organisms by acclimatization: a short review

The influence of transportation and acclimatization of fishes and shellfishes on their parasites and pathogens is discussed. It has been shown that aquatic organisms lose most of their parasites during the period of establishment, but some species may remain. In most instances these are parasites with direct development (Myxosporea, Monogenea, Crustacea). Species with intermediate hosts, but which utilize many species of invertebrates, establish more easily than those which have specific invertebrate intermediate hosts. If there are closely related host species to those introduced into the water body, parasites brought to it can transfer to these related species. This may result in a high infection of the native species and significant mortality.     

Do basophils play a role in immunity against parasites?

The link between parasites and eosinophilia has been known for more than a century, although the role of eosinophils in host protection is still an open issue. Much less appreciated, however, is the concurrent systemic induction of a related cell type, the basophil, in parasitized hosts. To date, little is known about the role of basophils in immunity against parasites, but recent evidence points to a possible crucial role in the initiation of T-helper type 2 responses in the host. In this article, we review the current understanding of parasitic infections and basophils and discuss their putative role in immunity.     

Impact of forest size on parasite biodiversity: implications for conservation of hosts and parasites

Studies of biodiversity traditionally focus on charismatic megafauna. By comparison, little is known about parasite biodiversity. Recent studies suggest that co-extinction of host specific parasites with their hosts should be common and that parasites may even go extinct before their hosts. The few studies examining the relationship between parasite diversity and habitat quality have focused on parasites that require intermediate hosts and pathogens that require vectors to complete their life-cycles. Declines in parasite and pathogen richness in these systems could be due to the decline of any of the definitive hosts, intermediate hosts, or vectors. Here we focus on avian ectoparasites, primarily lice, which are host specific parasites with simple, direct, life-cycles. By focusing on these parasites we gain a clearer understanding of how parasites are linked to their hosts and their hosts’ environment. We compare parasite richness on birds from fragmented forests in southern China. We show that parasite richness correlates with forest size, even among birds that are locally common. The absence of some ectoparasite genera in small forests suggests that parasites can go locally extinct even if their hosts persist. Our data suggest that the conservation of parasite biodiversity may require preservation of habitat fragments that are sufficiently large to maintain parasite populations, not just their host populations.     

Assessing the diversity and specificity of two freshwater viral communities through metagenomics

Transitions between saline and fresh waters have been shown to be infrequent for microorganisms. Based on host-specific interactions, the presence of specific clades among hosts suggests the existence of freshwater-specific viral clades. Yet, little is known about the composition and diversity of the temperate freshwater viral communities, and even if freshwater lakes and marine waters harbor distinct clades for particular viral sub-families, this distinction remains to be demonstrated on a community scale.To help identify the characteristics and potential specificities of freshwater viral communities, such communities from two lakes differing by their ecological parameters were studied through metagenomics. Both the cluster richness and the species richness of the Lake Bourget virome were significantly higher that those of the Lake Pavin, highlighting a trend similar to the one observed for microorganisms (i.e. the specie richness observed in mesotrophic lakes is greater than the one observed in oligotrophic lakes). Using 29 previously published viromes, the cluster richness was shown to vary between different environment types and appeared significantly higher in marine ecosystems than in other biomes. Furthermore, significant genetic similarity between viral communities of related environments was highlighted as freshwater, marine and hypersaline environments were separated from each other despite the vast geographical distances between sample locations within each of these biomes. An automated phylogeny procedure was then applied to marker genes of the major families of single-stranded (Microviridae, Circoviridae, Nanoviridae) and double-stranded (Caudovirales) DNA viruses. These phylogenetic analyses all spotlighted a very broad diversity and previously unknown clades undetectable by PCR analysis, clades that gathered sequences from the two lakes. Thus, the two freshwater viromes appear closely related, despite the significant ecological differences between the two lakes. Furthermore, freshwater viral communities appear genetically distinct from other aquatic ecosystems, demonstrating the specificity of freshwater viruses at a community scale for the first time.     

Spatial heterogeneity of daphniid parasitism within lakes

Spatially explicit models show that local interactions of hosts and parasites can strongly influence invasion and persistence of parasites and can create lasting spatial patchiness of parasite distributions. These predictions have been supported by experiments conducted in two-dimensional landscapes. Yet, three-dimensional systems, such as lakes, ponds, and oceans, have received comparatively little attention from epidemiologists. Freshwater zooplankton hosts often aggregate horizontally and vertically in lakes, potentially leading to local host–parasite interactions in one-, two-, or three-dimensions. To evaluate the potential spatial component of daphniid parasitism driven by these local interactions (patchiness), we surveyed vertical and horizontal heterogeneity of pelagic Daphnia infected with multiple microparasites in several north temperate lakes. These surveys uncovered little evidence for persistent vertical patchiness of parasitism, since the prevalence of two parasites showed little consistent trend with depth in four lakes (but more heterogeneity during day than at night). On a horizontal scale of tens of meters, we found little systematic evidence of strong aggregation and spatial patterning of daphniid hosts and parasites. Yet, we observed broad-scale, basin-wide patterns of parasite prevalence. These patterns suggest that nearshore offshore gradients, rather than local-scale interactions, could play a role in governing epidemiology of this open water host–parasite system. Electronic Supplementary Material Supplementary material is available for this article at     

Pollution and parasitism in the aquatic environment

The studies of aquatic parasitology and of aquatic pollution effects both have experienced increasing interest during the recent fifteen years. Although considerable effort has been spent on studying the role of pollution as a cause or a trigger of anomalies, tumors and infectious diseases in aquatic organisms, the interactions between pollution and parasitism have been largely neglected by scientists.Pollution and other man-made alterations of the aquatic environment may affect a parasite community directly by acting on free-living parasite stages or on ectoparasites, or indirectly by acting on the intermediate or the definitive host population. Certain pollution conditions favour the propagation of parasites by excluding their natural predators, by reducing the resistance of their hosts or by providing improved living conditions for their intermediate hosts. In a number of experimental studies parasitized organisms have been shown to suffer from greater mortalities when exposed to high temperature, to low oxygen stress or to high levels of dissolved heavy metal salts, when compared to nonparasitized control animals. Unfortunately, field studies on synergistic effects of pollution and parasites on host populations are still scarce and seldom offer more than qualitative observations and theoretical evaluations.The complexity of the pollution-parasite-host system complicates the use of parasites as indicators of pollution effects. However, experience from aquaculture practice teaches that a number of (mostly ecto-) parasites are more susceptible to certain chemicals (used as parasiticides) and to artificial alterations of salinity, temperature or oxygen content of the water than their hosts. Accordingly, it is postulated that during future studies the composition of ectoparasitic faunas of aquatic organisms might turn out to become a useful and quickly reacting indicator for effects of certain pollution conditions, such as anthropogene oxygen deficiency, salt introduction from salines into freshwater ecosystems, and introduction of certain heavy metal salts.