Predicting the similarity of parasite communities in freshwater fishes using the phylogeny,ecology and proximity of hosts

Parasite communities tend to be dissimilar in hosts that are geographically, phylogenetically, ecologically and developmentally distant from one another. The decay of community similarity is a powerful and increasingly common method of studying parasite beta diversity, but most studies have examined only a single type of distance. Here, we evaluate distances based on the phylogeny, ecology, spatial proximity and size of hosts, as predictors of the similarity of parasite communities in individual hosts, host populations and host species. We surveyed parasites in six species of fish collected simultaneously from six localities in the St. Lawrence River, Canada, and species in a common group of larval parasites were discriminated using DNA sequences from barcode region of cytochrome c oxidase I. Distances based on the habitat use patterns of host species were good predictors of short‐term, ecological similarity of parasite communities, such as that operating at the scale of the individual host. The genetic distance between host species was associated with almost all types of similarity at all scales, particularly qualitative and phylogenetic similarity of parasite communities at the level of populations and meta‐populations of hosts. The trophic level, diet, spatial proximity and size of hosts were poor predictors of parasite community similarity. The increased taxonomic resolution provided by molecular data increased the explanatory power of regression models, and different factors were implicated when parasite species were distinguished with DNA barcodes than when larval parasites were lumped into morphospecies, as is commonly practiced.     

Effect of the digenean parasites of fish on the fauna of Mediterranean lagoons

Attention is drawn to the effects of parasites on their hosts, taking as a model the digenean parasites of teleosts (hereafter: fish) from lagoons along the French Mediterranean coast. Because digeneans have a heteroxenic life cycle, their impact is not limited to the definitive host, which harbours the sexual adults, but is extended to the first host (mollusc) and to the second host ("invertebrate" or fish). Adult parasites, in order to ensure efficient sexual reproduction, never cause excessive damage to their definitive host, usually only exploiting the intestinal fluids; however, the host must intensify its search for prey, which results in a diminished fitness. Within the first host, 'larval' stages of digenean parasites invade the gonads, resulting in its castration, then exhaustion and eventually death. The diversion of energy from the second hosts towards the parasites forces them to intensify their search for food, resulting in decreased fitness and an increased risk of being eaten; in addition, manipulation of the host's behaviour by parasites drives this host into the food chain of the definitive host. In lagoons, many individuals of almost all species of fish and invertebrates act as first, second and/or definitive hosts for digeneans. Obviously, parasites have a severe impact on the population dynamics of key taxa, on the food web and therefore also on the functioning of the whole lagoon ecosystem. Yet this impact has been largely overlooked or underestimated in functioning models, by ecologists, who tend to prioritize more apparent trophic relationships.     

Differential sources of host species heterogeneity influence the transmission and control of multihost parasites

Controlling parasites that infect multiple host species often requires targeting single species that dominate transmission. Yet, it is rarely recognised that such ‘key hosts’ can arise through disparate mechanisms, potentially requiring different approaches for control. We identify three distinct, but not mutually exclusive, processes that underlie host species heterogeneity: infection prevalence, population abundance and infectiousness. We construct a theoretical framework to isolate the role of each process from ecological data and to explore the outcome of different control approaches. Applying this framework to data on 11 gastrointestinal parasites in small mammal communities across the eastern United States reveals variation not only in the magnitude of transmission asymmetries among host species but also in the processes driving heterogeneity. These differences influence the efficiency by which different control strategies reduce transmission. Identifying and tailoring interventions to a specific type of key host may therefore enable more effective management of multihost parasites.     

Differential diagnosis of the genera in the family Trichodinidae (Ciliophora: Peritrichida) with the description of a new genus ectoparasitic on freshwater fish from southern Africa

A trichodinid ectoparasite was collected from mormyrid fish in the Olifants River System, South Africa. A new genus, Hemitrichodina, is described to accomodate these trichodinid ciliophorans of which the blades are reduced and with an adoral spiral of more than 360°, but less than two full turns. A differential diagnosis of the genera within the family Trichodinidae is presented.     

Large-scale patterns of host use by parasites of freshwater fishes

Organisms that are abundant locally in a habitat patch are commonly observed to be frequent regionally, or among patches. In parasites, species present in high numbers in host individuals are also present in many individuals in the host population. On a larger scale, however, when host species are considered as patches, we may expect the opposite pattern because of the cost of producing mechanisms to evade the immune responses of several host species. Thus parasite species exploiting many host species may achieve lower average abundance in their hosts than parasite species exploiting fewer host species. This prediction was tested with data from 188 species of metazoan parasites of freshwater fish, using a comparative approach that controlled for study effort and phylogenetic influences. A negative correlation was found between the number of host species used by parasites and their average abundance in hosts, measured as either prevalence or intensity of infection. There was no evidence that parasite species fall into distinct categories based on abundance patterns, but rather that they fall along a continuum ranging from a generally low abundance in many host species, to a generally high abundance in few host species. These results applied to both ecto- and endoparasites. The pattern observed suggests the existence of a trade-off between how many host species a parasite can exploit and how well it does on average in those hosts.     

Speciation by host switch and adaptive radiation in a fish parasite genus Gyrodactylus (Monogenea,Gyrodactylidae)

Four hundred Gyrodactylus species have been formally described, but the estimated number of species in this fish ectoparasite genus of Monogenean Platyhelminthes is more than 20,000. The unusually high species richness has lead to the hypotheses of speciation and adaptive radiation via host switching. These hypotheses were tested by reconstructing a molecular phylogeny for the subgenus G. (Limnonephrotus) which is a group of freshwater parasites, including five species infecting wild and farmed salmonids. The highly variable ITS1 and ITS2 segments and the conservative 5.8S ribosomal gene were sequenced in 22 species plus two species representing the subgenus G. (Paranephrotus) as an outgroup. The phylogeny was compared with host systematics: the species were collected from six fish families (Cyprinidae, Salmonidae, Percidae, Esocidae, Gasterosteidae, and Gobitidae). The phylogenetic analysis demonstrated that G. (Limnonephrotus) is a monophyletic group that was originally hosted by cyprinids. The speciation has occurred in two episodes, the older one manifested in genetic distances 25-33% (4-6 Myr BP). The latter speciation burst occurred in one clade only, perhaps one million years ago. This clade has been morphologically identified as a wageneri species group. It is a monophyletic group of 18 species [studied here] and contains all five salmonid parasites, but also parasites, on cyprinids, percids, esocids, and gasterosteids. In G. (Limnonephrotus), eight host switches crossing the host family barrier were observed, and at least three of them were followed by repetitive speciation. Seven host-switch events were statistically confirmed by bootstrapping. The suggested model of speciation by host switch was accepted, and interestingly the adaptive radiation seems to be a consequence of host switch to a new family (key innovation model). The molecular and ecological evolution rate of Gyrodactylus parasites is manyfold in comparison to host species, and the phylogenies are largely independent and disconnected.     

The underrated importance of predation in transmission ecology of direct lifecycle parasites

Most parasites with complex life cycles exploit trophic webs to pass from host to host in order to develop and, eventually, reproduce. Thus predation constitutes the necessary route for transmission. Conversely, the transmission of parasites that use a single host to develop and reproduce should be, in principle, not particularly affected by host trophic ecology. Here I challenge this view, showing that predation may be relevant also for direct lifecycle parasites. I used a large dataset of fish trophic interactions to investigate if the degree of monogenean species overlap in predators and prey deviated from randomness. I demonstrated that predators and prey often share more monogenean parasite genera than explained by host habitat ecology, geographical distribution and phylogeny. This suggests that predation may play an important role in promoting monogenean host range expansion. In addition, a non‐negligible proportion of considered prey–predator pairs showed a significantly high overlap in their monogenean parasites at the species level. This may indicate a tendency of some monogenean parasites to evolve transmission strategies targeted towards host interactions. If this hypothesis is true, these monogenean parasites would be much more vulnerable to co‐extinction than previously thought. Synthesis Predation is not expected to play an important role in the ecology and evolution of simple life cycle parasites. Yet, several predator fish tend to share with their prey more monogenean parasites than one would expect predicted from their geographical distribution, habitat preference, and or phylogenetic relationships. This suggests that some monogenean parasites have evolved transmission strategies more targeted towards host interactions than towards species‐specific traits. If this hypothesis is supported, it would have strong implications on host–parasite evolutionary ecology, primarily, suggesting the existence of peculiar situations where some parasites have evolved high specialized host finding behaviors to expand their host range.     

Interspecific associations among larval helminths in fish

Various processes can generate associations between the larvae of different helminth species in their fish intermediate or paratenic host. We investigated the pairwise associations among larval helminth species in eight different fish populations, using two different coefficients of associations, in order to determine in what situations they are strongest. All helminth species included use the fish studied as either their second intermediate host or their paratenic host, and are acquired by the fish when it ingests an infected first intermediate host. The intensity of infection correlated positively with fish length for most helminth species. Pairs of species which both exhibited positive correlations with fish length tended to be more strongly associated with one another, although this tendency was not pronounced. Similarity in life cycle had a more important influence on pairwise associations. Among the 62 pairwise associations that could be computed, pairs of helminth species that shared both first intermediate hosts and definitive hosts were the most strongly associated, followed by pairs that shared only one other host, and finally by pairs that did not share other hosts. The results suggest that assemblages of larval helminth parasites in fish are not random collections of locally available species, but rather structured packets of larval parasites that travel together along common transmission routes.     

Body size,trophic level,and the use of fish as transmission routes by parasites

Within food webs, trophically transmitted helminth parasites use predator–prey links for their own transfer from intermediate prey hosts, in which they occur as larval or juvenile stages, to predatory definitive hosts, in which they reach maturity. In large taxa that can be used as intermediate and/or definitive hosts, such as fish, a host species’ position within a trophic network should determine whether its parasite fauna consists mostly of adult or larval helminths, since vulnerability to predation determines an animal’s role in predator–prey links. Using a large database on the helminth parasites of 303 fish species, we tested whether the proportion of parasite species in a host that occur as larval or juvenile stages is best explained by their trophic level or by their body size. Independent of fish phylogeny or habitat, only fish body length emerged as a significant predictor of the proportion of parasites in a host that occur as larval stages from our multivariate analyses. On average, the proportion of larval helminth taxa in fish shorter than 20 cm was twice as high as that for fish over 100 cm in length. This is consistent with the prediction that small fishes, being more vulnerable to predation, make better hosts for larval parasites. However, trophic level and body length are strongly correlated among fish species, and they may have separate though confounded effects on the parasite fauna exploiting a given species. Helminths show varying levels of host specificity toward their intermediate host when the latter is the downstream host involved in trophic transmission toward an upstream definitive host. Given this broad physiological compatibility of many helminths with fish hosts, our results indicate that fish body length, as a proxy for vulnerability to predators, is a better predictor of their use by helminth larvae than their trophic level based on diet content.     

南极鱼类后生动物寄生虫研究进展: 线虫、绦虫与桡足类

极端的环境造就了南极独特的生物群体, 其中鱼类是南大洋生态系统中最具多样性的脊椎动物, 也是许多寄生虫的中间或终末宿主。南极鱼类寄生虫种类丰富, 是南大洋海洋生物多样性的重要组成部分。探究南极鱼类及其寄生虫的营养关系可为阐释南极海洋生态系统功能及其变动提供重要的生态数据。虽然关于南极鱼类寄生虫的研究已有一百多年的历史, 但这些研究主要集中在寄生虫的种类鉴定、区系调查和组织病理等方面。由于南极鱼类寄生虫研究跨度时间长、地域范围广, 相关研究较为零散。文章综述了南极鱼类寄生线虫、绦虫以及桡足类的种类组成、宿主范围和地理分布等方面的研究, 并对今后开展南极鱼类寄生虫研究工作提出了展望。     

The Thrombospondin-related Protein Family of Apicomplexan Parasites: The Gears of the Cell Invasion Machinery

A number of severe diseases of medical and veterinary importance are caused by parasites of the phylum Apicomplexa. These parasites invade host cells using similar subcellular structures, organelles and molecular species. Proteins containing one or more copies of the type I repeat of human platelet thrombospondin (TSP1), are crucial components of both locomotion and invasion machinery. Members of this family have been identified in Eimeria tenella, E. maxima, Toxoplasma gondii, Cryptosporidium parvum and in all Plasmodium species so far analysed. Here, Andrea Crisanti and colleagues discuss the structure, localization and current understanding of the function of TSP family members in the invasion of target cells by apicomplexan parasites.     

Determinants of host-specificity in parasites of freshwater fishes.

Factors responsible for interspecific variability in host-specificity were investigated within 15 genera (including 176 species) of metazoan parasites found in Canadian freshwater fish. For each species in a genus, the parasite's number of known hosts was determined from published host-parasite records. The effects of the total number and mean size of potential hosts (i.e. all fish species belonging to the family or families that include a parasite's known hosts) on number of hosts of congeneric species were evaluated using multiple regressions. Since parasite species that have been recorded often tend to have greater numbers of known hosts than do seldom-recorded parasites, it was necessary to control for the confounding effect of study intensity. In all parasite genera, whether from highly specific taxa such as monogeneans or from less host-specific ones, there was a positive relationship between the number of potential hosts and the number of known hosts. However, no consistent relationships were observed between the mean size of potential hosts and number of known hosts. These results suggest that the availability of suitable host species may have been a key factor limiting the colonization of new hosts by fish parasites.     

Diversity, distribution and exchange of blood parasites meeting at an avian moving contact zone

Research on contact zones has paid relatively little attention to host-parasite interactions, although these situations have important but different implications depending on whether one considers the host or the parasite's perspective. We investigated both the role of a host contact zone in parasite expansion and whether parasites could influence contact zone dynamics. We studied the diversity and the patterns of parasite exchange (genera Haemoproteus and Plasmodium) infecting two parapatric sibling passerines meeting at a moving contact zone in western Europe. We amplified and sequenced a fragment of the parasite cytochrome b gene. The expanding host harboured more diverse parasites, which might indicate a superior ability to face a diverse parasite fauna than the receding host. Prevalence was very high in both hosts, due to the frequent occurrence of two sister Haemoproteus lineages. Despite the recent movement of the contact zone, these two parasites fitted almost perfectly to the geographic range of their main host species. Yet, we found several cases of cross-species infection in sympatric areas and evidences of asymmetrical spreading of parasites from the expanding host towards the receding host. Altogether, our results suggest that the host contact zone mainly acts as a barrier to parasite expansion even if recurrent host shifts are observed. Besides, they also support the idea that parasite-mediated competition might contribute to the displacement of hosts' contact zones, thereby emphasizing the role of parasitism on the population dynamics of sympatric species.     

In vitro leukocyte response of three-spined sticklebacks (Gasterosteus aculeatus) to helminth parasite antigens

Helminth parasites of teleost fish have evolved strategies to evade and manipulate the immune responses of their hosts. Responsiveness of fish host immunity to helminth antigens may therefore vary depending on the degree of host-parasite counter-adaptation. Generalist parasites, infective for a number of host species, might be unable to adapt optimally to the immune system of a certain host species, while specialist parasites might display high levels of adaptation to a particular host species. The degree of adaptations may further differ between sympatric and allopatric host-parasite combinations. Here, we test these hypotheses by in vitro exposure of head kidney leukocytes from three-spined sticklebacks (Gasterosteus aculeatus) to antigens from parasites with a broad fish host range (Diplostomum pseudospathaceum, Triaenophorus nodulosus), a specific fish parasite of cyprinids (Ligula intestinalis) and parasites highly specific only to a single fish species as second intermediate host (Schistocephalus pungitii, which does not infect G. aculeatus, and Schistocephalus solidus, infecting G. aculeatus). In vitro responses of stickleback leukocytes to S. solidus antigens from six European populations, with S. solidus prevalence from <1% to 66% were tested in a fully crossed experimental design. Leukocyte cultures were analysed by means of flow cytometry and a chemiluminescence assay to quantify respiratory burst activity. We detected decreasing magnitudes of in vitro responses to antigens from generalist to specialist parasites and among specialists, from parasites that do not infect G. aculeatus to a G. aculeatus-infecting species. Generalist parasites seem to maintain their ability to infect different host species at the costs of relatively higher immunogenicity compared to specialist parasites. In a comparison of sympatric and allopatric combinations of stickleback leukocytes and antigens from S. solidus, magnitudes of in vitro responses were dependent on the prevalence of the parasite in the population of origin, rather than on sympatry. Antigens from Norwegian (prevalence 30–50%) and Spanish (40–66%) S. solidus induced generally higher in vitro responses compared to S. solidus from two German (<1%) populations. Likewise, leukocytes from stickleback populations with a high S. solidus prevalence showed higher in vitro responses to S. solidus antigens compared to populations with low S. solidus prevalence. This suggests a rather low degree of local adaptation in S. solidus populations, which might be due to high gene flow among populations because of their extremely mobile final hosts, fish-eating birds.     

Trichodinid ectoparasites (Ciliophora: Peritrichida) of freshwater fishes of the Zambesi River System,with a reappraisal of host specificity

Over a period of five years parasitological surveys were carried out on the freshwater fish fauna in the eastern Caprivi which included the upper Zambesi River, a section of the Chobe and Kwando Rivers, and vast swampy areas. This area is well known for its wide variety of indigenous fish and has so far not been influenced in any way by introduced alien fish species. In these surveys 45 different fish species of 12 families were examined. This paper reports on the parasites of the generaTrichodina andHemitrichodina of the eastern Caprivi. A total of 15 species of parasites were recorded of which nine are new species described here-in. The list of host records of known species are expanded and an evaluation of host specificity based on information recorded in this survey as well as previously published data from southern Africa is provided.     

Has the introduction of brown trout altered disease patterns in native New Zealand fish?

1. It is well recognised that non-indigenous species (NIS) can affect native communities via the 'spillover' of introduced parasites. However, two other potentially important processes, the 'spillback' of native parasites from a competent NIS host, where the latter acts as a reservoir leading to amplified infection in native hosts, and the 'dilution' of parasitism by a NIS host acting as a sink for native parasites, have either not been tested or largely overlooked.
2. We surveyed the helminth parasite fauna of native New Zealand fish in Otago streams that varied in the abundance of introduced brown trout Salmo trutta , to look for evidence of spillback and/or dilution. Spillover is not an issue in this system, with trout introduced as parasite-free eggs.
3. Seven native parasite species were present across 12 sites; significant inverse relationships with an index of trout abundance (i.e. dilution) were documented for three species infecting the native upland bully Gobiomorphus breviceps , and one species infecting the native roundhead galaxias Galaxias anomalus .
4. An inverse relationship between bully energy status and infection intensity of one parasite species suggests that parasite dilution could have positive effects on bully populations. Our failure to detect similar relationships for the other parasites does not preclude the possibility that dilution is beneficial to native fish, since parasites may have subtle or unmeasured impacts.
5. The parasite dilution patterns reported are compelling in that they occurred across several native host and parasite species; as such they have important implications for invasion ecology, providing an interesting contrast to the largely negative impacts reported for NIS. Mechanisms potentially responsible for the patterns observed are discussed.     

指环虫属的早期辐射及其与宿主鲤科鱼类的协同进化关系

本研究利用28SrDNAC1-D2区序列分析采自鲤科鱼类中6亚科宿主和寄生在花鲈、梅花鲈上的共17种指环虫的系统发育关系。同时,通过比较宿主鲤科鱼类与指环虫的系统发育树,检验指环虫与其宿主是否存在协同进化关系。结果表明:17种指环虫形成5个进化支(Clade),其中寄生在团头鲂(亚科)和鲢、鳙(鲢亚科)上的6种指环虫聚为一支(Clade1),而它们的宿主鱼类在系统发育分析中也表现为近缘关系;寄生在鲮鱼(野鲮亚科)上的D.quanfami(Clade5)位于系统树最基部,鲫鱼和鲤鱼(鲤亚科)的寄生指环虫处在系统树的次基部位置,而鲤亚科与野鲮亚科组成的姐妹群在宿主系统树上同样处在基部位置,寄生虫和宿主在进化上较为原始的地位得到了很好地相互印证。因而,本研究首次利用分子系统学手段分析指环虫属远缘物种间的系统关系,揭示了指环虫属与宿主鱼类之间存在协同进化关系。另外,本研究首次发现,野鲮亚科鱼类也可能是指环虫类的早期宿主,这与先前认为鲤亚科鱼类为指环虫类的祖先宿主的推测有所不同。     

Parasite fauna of seabass (Lates calcarifer) under mariculture conditions in Lampung Bay, Indonesia

Fish parasites have been repeatedly reported to be a major threat to the developing industry of finfish mariculture in Indonesia, due to severe parasite and disease outbreaks. The aim of this study was to identify the metazoan parasite fauna and trichodinid ciliates that infect Lates calcarifer in a representative mariculture farm in Indonesia. Examined were 105 L. calcarifer (seabass) for the metazoan parasite fauna and trichodinid ciliates. Thirty‐five specimens each from the net cages of the National Sea Farming Development Centre (Balai Budidaya Laut, BBL) in Lampung Bay, South Sumatra, Indonesia were investigated in three consecutive seasons (two dry and one rainy season from 2002 to 2003). Nineteen parasite species were identified; all fish specimens were infected with two to 10 parasite species, demonstrating a species‐rich parasite fauna. Protozoans (1 species), myxozoans (1), digeneans (3), monogeneans (5), cestodes (3), nematodes (5) and acanthocephalans (1) were found, including 11 new host records in cultured L. calcarifer from Indonesia. Larval and adult parasite stages were isolated, demonstrating that this fish species, although kept inside the net cages, still functions as an intermediate and final host for marine fish parasites. During all seasons, the six detected monoxenous (single host life cycle) parasite species showed a higher prevalence than the 13 heteroxenous (multiple hosts) species. Most abundant were the fish pathogenic monogeneans Pseudorhabdosynochus epinepheli, Pseudorhabdosynochus lantauensis, Benedenia epinepheli and Neobenedenia melleni with a high prevalence. Most heteroxenous parasites (Digenea, Cestoda, Nematoda and Acanthocephala) occurred with a low prevalence below 26%, caused by the specific culture conditions. Diversity of the heteroxenous parasites was higher in the dry seasons than in the rainy season. Though some seasonality could be observed for the fish pathogenic monogeneans, severe disease outbreaks of these ectoparasites cannot be excluded in either the dry or rainy season.     

Sexual differences in the incidence and severity of ectoparasitic infestation of the brown trout, Salmo trutta L.

Hatchery-reared and wild brown trout, Salmo trutta L., were examined for skin ectoparasites during their spawning period in 1977 and 1978. A total of eight genera of parasites, comprising five ciliates, one flagellate, one monogenean and one parasitic fungus, were identified with as many as five different genera occurring on a single fish. Sexually mature male fish were more frequently or more severely infested by species of Ichthyophthirius, Scyphidia, Gyrodactylus and Saprolegnia than were immature fish of either sex or mature female fish. The differences in ectoparasitic loading could not be correlated with known, seasonal changes in the mucus-producing potential of the epidermis. These findings are discussed in relation to the defence mechanisms of teleost fish and to some of the endocrinological changes that occur in salmonid fish during the spawning season.     

Temperature and multiple parasites combine to alter host community structure

Predicting the effects of climate change requires understanding complex interactions among multiple abiotic and biotic factors. By influencing key interactions among host species, parasites can affect community and ecosystem structuring. Yet, our understanding of how multiple parasites and abiotic factors interact to alter ecosystem structure remains limited. To empirically test the role of temperature variation and parasites in shaping communities, we used a multigenerational mesocosm experiment composed of four sympatric freshwater crustacean species (isopods and amphipods) that share up to four parasite species. Mesocosms were assigned to one of four different treatments with contrasting seasonal temperatures (normal and elevated) and parasite exposure levels (continuous and arrested (presence or absence of parasite larvae in mesocosm)). We found that parasite exposure and water temperature had interactive effects on the host community. Continuous exposure to parasites altered the community structure and differences in water temperature altered species abundance. The abundance of the amphipod Paracalliope fluviatilis decreased substantially when experiencing continuous parasite exposure and elevated water temperatures. Elevated temperatures also led to parasite-induced mortality in another amphipod host, Paracorophium excavatum. Contrastingly, isopod hosts were affected much less, suggesting increasing temperatures in conjunction with higher parasite exposure might increase their relative abundance in the community. Changes in invertebrate host populations have implications for other species such as fish and birds that consume crustaceans as well as having impacts on ecosystem processes, such as aquatic primary production and nutrient cycling. In light of climate change predictions, parasite exposure and rise in average temperatures may have substantial impacts on communities and ecosystems, altering ecosystem structure and dynamics.