First report of post-cyclic transmission in trematodes: Derogenes lacustris (Digenea: Hemiuroidea) in Patagonian freshwater fishes.

The transmission of adult parasites from prey to predatory hosts has been demonstrated for some acanthocephalan and one cestode species. Derogenes lacustris (Digenea: Hemiuroidea: Derogenidae) is a generalist parasite that infects, as an adult, the stomach of native and introduced freshwater fishes in Andean Patagonia. In the present work, the post-cyclic transmission of D. lacustris from native Galaxias maculatus (Galaxiidae) to introduced Oncorhynchus mykiss (Salmonidae) was proved experimentally. The observed transmission rate for this experimental infection was 19%. The body length of D. lacustris on day 14 post-infection was significantly greater than before transmission. The number of eggs also increased significantly after transmission, showing that D. lacustris can survive, grow and continue with egg production for at least 2 weeks in predatory salmonids. This study provides the first experimental evidence of post-cyclic transmission of trematodes and the results suggest that post-cyclic parasitism enables this species to broaden its range of hosts and distribution ranges in Argentinean Patagonia.

A New Species of Cryptocotyle (Digenea: Heterophyidae) Infecting Kelp Gull and a Galaxiid Fish in Patagonian Freshwater Environments: Morphological and Molecular Analyses.

Adults of a species of Cryptocotyle were found infecting the intestine of the kelp gull, Larus dominicanus Lichtenstein, 1823, and metacercariae were found in the fins and muscle of the galaxiid fish, Galaxias platei Steindachner, 1898 (local name "puyen grande"), in Nahuel Huapi National Park (Patagonia). Morphometrics and genetic markers of mitochondrial cytochrome oxidase (COI) and ribosomal internal transcribed spacer 1 (ITS1) confirmed that adults and metacercariae were conspecific and represent a new species, Cryptocotyle dominicana n. sp. The only congener known from South America (Cryptocotyle thapari McIntosh, 1953) matures in river otters (Lutra spp. and Pteronura spp.) in Brazil and Bolivia and differs from the new species in the arrangement of the testes, which are located in tandem in the species from otters. Adults of the new species resemble Cryptocotyle lingua (Creplin, 1825) Fischoeder, 1903 from marine environments of the Northern Hemisphere, both species being characterized by having a linguiform body, oblique testes, and vitelline follicles that extend posteriorly to the level of the ventral sucker. Considering the morphological findings that differentiate the new species from other Cryptocotyle, as well as the molecular analysis that shows significant differences from C. lingua, we conclude that these specimens represent a new species, the first of the genus Cryptocotyle to be described from birds in South America.

Gyrodactylus ginestrae n. sp. (Monogenea: Gyrodactylidae), a parasite of the big-scale sand smelt, Atherina boyeri Risso, 1810 (Actinopterygii: Atherinidae) from the Black Sea.

We describe a new species, Gyrodactylus ginestrae n. sp., a parasite of the big-scale sand smelt (Atherina boyeri) from the Black Sea. This is the third monogenean species known from this fish host, found at 70% prevalence, but at relatively low abundance (1.9), on fish gills and fins. The new species is, both morphologically and genetically, most similar to G. salinae, which parasitizes the killifish Aphanius fasciatus (Cyprinodontidae) in the Mediterranean region. These species differ in the size of the haptoral hard parts and the number of small spines of the male copulatory organ. For molecular characterization, the internal transcribed spacer 1 (ITS1), 5.8S rRNA gene, and the internal transcribed spacer 2 (ITS2) were sequenced, completed by a fragment of the COII gene, thereby representing the first molecularly characterized gyrodactylid species from the Black Sea. Phylogenetic reconstruction based on the ITS1-5.8S-ITS2 sequence data indicated the position of G. ginestrae n. sp. in the marine "rugiensis" group of G. (Paranephrotus) and G. (Neonephrotus) subgenera which is part of the monophyletic "long ITS1" group. Taking into account the similarity of G. ginestrae n. sp. to several monogeneans from the Atlantic and Mediterranean regions, we suggest the Boreal-Atlantic origin of this species.

Intestinal fluke Metagonimus yokogawai infection increases probiotic Lactobacillus in mouse cecum.

Helminth infection can alleviate immune-mediated disorders such as allergies and autoimmune diseases, by altering the gut microbiome. However, changes in gut microbiome due to intestinal trematodes remain unelucidated. Here, we evaluated the changes in the gut microbiome of ICR mice infected with Metagonimus yokogawai, a hypo-virulent intestinal trematode. Four weeks after infection, mouse cecal content was analyzed by 16S rRNA amplicon analysis. Although there was no apparent difference in species richness and diversity, the microbiome composition was different in the infected and control groups. Furthermore, several Lactobacillus species with known immunomodulatory role in immune-mediated diseases were increased in the infected group.

Helminths of European smelt Osmerus eperlanus (Linnaeus, 1758) in Lake Hancza and the Vistula Lagoon, with special regard to their zoonotic threats.

Reports published in recent years on the increased risk in the Baltic Sea of fish infection with larvae of nematodes potentially pathogenic to humans have prompted a study of European smelt Osmerus eperlanus with respect to the presence of these parasites in the Vistula Lagoon. Additionally, samples of this fish from Lake Hancza were comparatively considered. The body cavity, the surface of internal organs, the alimentary tract and the swimbladder of fish from two environmentally different water bodies were taken into account in the analysis. Only the tapeworm Proteocephalus longicollis was found in the alimentary tract of the fish from Lake Hancza. Depending on the period of study, the prevalence ranged from 60% to 100%, and the mean intensity from 11.5 to 42.0. The helminth fauna of smelt from the Vistula Lagoon was more diverse: Cystidicola farionis occurred with a prevalence from 25.9 to 75.0% and a mean intensity of infection from 2.7 to 66.0%, Proteocephalus longicollis and cystacanths of Corynosoma with a prevalence ranging in different years from 12.0 to 44.0% and from 14.8 to 50.0%, respectively. Zoonotic parasites, such as nematode larvae of the Anisakidae family (Contracaecum sp., Anisakis simplex), occurred in the intestine with a prevalence of 31%, 72% and 22% in consecutive years of the study.

Species composition and infection dynamics of ascaridoid nematodes in Barents Sea capelin (Mallotus villosus) reflecting trophic position of fish host.

Capelin (Mallotus villosus) is among the most abundant fish species in the Barents Sea, and represents a critical food source for many predators in the area including Atlantic cod and harp seal. In Norway, the fish is of economic importance since whole capelin and roe are valuable export products. Despite its economic and ecological importance, the parasites of Barents Sea capelin are poorly known. However, the presence of parasites in the edible parts may adversely affect product quality and consumer safety. During the main annual catching seasons of 2009-2012, we investigated the diversity and infection dynamics of ascaridoid nematodes in capelin (n = 620) from the southern Barents Sea. Three anisakid species were identified by genetic or molecular methods; Anisakis simplex (s.s.), Contracaecum osculatum sp. B, and Hysterothylacium aduncum, with C. osculatum sp. B as the most prevalent and abundant species. The present findings suggest that the ascaridoid species composition in capelin reflects its trophic position in the Barents Sea ecosystem. There appears to be a link between infection level of the nematode species and the preferred prey organisms of the different developmental phases of capelin. Thus, the higher abundance of C. osculatum sp. B compared to A. simplex (s.s.) and H. aduncum may be related to more extensive feeding on calanoid copepods over a wider ontogenetic size range including adolescence, while the main intermediate hosts of the latter nematode species, i.e. euphausiids and amphipods, appear to be the preferred prey of larger capelin.

[NUMBER DISTRIBUTION AND POPULATION STRUCTURE OF PROTEOCEPHALUS LONGICOLLIS (ZEDER, 1800) (CESTODA: PROTEOCEPHALIDEA), A PARASITE OF SMELT AND COREGONIDS].

The spatial structure and seasonal aspects in the number distribution of the cestode Proteocephalus longicollis population, maintained by trophic connections of specialized plankton-feeders (the vendace Coregonus albula L. and the smelt Osmerus eperlanus L.) in the Lake Onego were studied. Differences in the distribution of number of cestode population in host population, size-age structure, and pre-reproductive/reproductive stages ratio of the studied parasites were revealed. It was demonstrated that the spatial structure of P. longicollis was shaped by the specific characteristics of vendace and smelt populations in the Lake Onego. These species possess partially overlapping ecological niches and differences in the use of food resources, significantly determining the infection dynamics of the examined fish species.

Metagonimus yokogawai (Trematoda: Heterophyidae): From Discovery to Designation of a Neotype.

Metagonimus yokogawai (Katsurada, 1912) Katsurada, 1912 (Trematoda: Heterophyidae) is parasitic in the small intestine of mammals including man and birds in Far Eastern Russia, Korea, Japan, China, and Taiwan. In the present study, the metacercariae and adults of M. yokogawai were redescribed to designate a neotype of this fluke together with reviews of previous studies including study histories from the first discovery to now. We particularly, attempted to review the study histories and morphological descriptions of M. yokogawai for the species validity, and compared with the morphological characteristics and life cycles of the closely related species, Metagonimus takahashii and Metagonimus miyatai. Finally, we proposed a differential key for the 8 known Metagonimus species distributed in East Asia. Metacercariae were obtained from the body muscles of sweetfish (Plecoglossus altivelis) collected in the Asahi River at Takebe-cho, Kita-ku, Okayama City, Okayama Prefecture, Japan. Adults were recovered from the small intestine of Syrian golden hamsters, to which the metacercariae had been fed 14 days before. A neotype was selected out of the present adult specimens. The Asahi River at Takebo-cho became the type locality of M. yokogawai. In conclusion, the present review shows that M. yokogawai, M. takahashii, and M. miyatai are valid and discriminated by means of morphological characteristics.

Metagonimus yokogawai (Trematoda: Heterophyidae): From Discovery to Designation of a Neotype

Metagonimus yokogawai (Katsurada, 1912) Katsurada, 1912 (Trematoda: Heterophyidae) is parasitic in the small intestine of mammals including man and birds in Far Eastern Russia, Korea, Japan, China, and Taiwan. In the present study, the metacercariae and adults of M. yokogawai were redescribed to designate a neotype of this fluke together with reviews of previous studies including study histories from the first discovery to now. We particularly, attempted to review the study histories and morphological descriptions of M. yokogawai for the species validity, and compared with the morphological characteristics and life cycles of the closely related species, Metagonimus takahashii and Metagonimus miyatai. Finally, we proposed a differential key for the 8 known Metagonimus species distributed in East Asia. Metacercariae were obtained from the body muscles of sweetfish (Plecoglossus altivelis) collected in the Asahi River at Takebe-cho, Kita-ku, Okayama City, Okayama Prefecture, Japan. Adults were recovered from the small intestine of Syrian golden hamsters, to which the metacercariae had been fed 14 days before. A neotype was selected out of the present adult specimens. The Asahi River at Takebo-cho became the type locality of M. yokogawai. In conclusion, the present review shows that M. yokogawai, M. takahashii, and M. miyatai are valid and discriminated by means of morphological characteristics.

Life-cycle stages of a Posthodiplostomum species (Digenea: Diplostomidae) from Patagonia, Argentina.

In Patagonia, populations of the galaxiid fish Galaxias maculatus are parasitized by metacercariae of a species of Posthodiplostomum (Digenea: Diplostomidae). The aim of this work was to describe larval and adult stages of this species in experimental and natural hosts from an Andean Patagonian lake. Specimens of G. maculatus and the pulmonate snail, Anisancylus obliquus, were collected in Patagua Lake. The snails were isolated in individual containers to observe emergence of cercariae, dissected, and examined under a stereoscopic microscope to record sporocysts and cercariae. Fish were examined to obtain metacercariae, and uninfected fish from Gutiérrez Lake were exposed to cercariae from A. obliquus to obtain experimental metacercariae. Chicks and mice were infected with metacercariae from naturally infected G. maculatus to obtain experimental adults. Specimens recovered belong to Posthodiplostomum sp. on the basis of morphological features. This is the first description of sporocysts, cercariae, metacercariae, and adults stages of a Posthodiplostomum species in Patagonia, including data about its natural intermediate hosts.

The helminth community of the sand smelt (Atherina boyeri Risso, 1810) from Lake Iznik, Turkey.

Metazoan parasites of the sand smelt Atherina boyeri Risso, 1810 in Lake Iznik were studied. A total of 271 specimens of A. boyeri, 208 female and 63 male, mean ( ± SD) total length 8.4 ± 2.2 cm (range 3.1-12.2 cm) and mean total weight 4.7 ± 3.5 g (range 0.1-11.7 g) were examined between June 2008 and May 2009 at monthly intervals. In 33 fish no parasites were found. In the other fish, four parasite species were recorded: Diplostomum sp. (prevalence 39.13%, mean intensity 3.50 ± 3.03); Tylodelphys clavata (prevalence 74.16%, mean intensity 10.41 ± 14.89); Bothriocephalus cf. acheilognathi (prevalence 40.59%, mean intensity 31.83 ± 57.74); and Eustrongylides excisus (prevalence 6.64%, mean intensity 1.16 ± 0.39). The mean abundance of Diplostomum sp., T. clavata and E. excisus was higher during the winter and early spring months. In contrast, the mean abundance of B. cf. acheilognathi was higher in the summer and autumn months. This distribution of the parasites was related to a change in the environment of A. boyeri from the pelagic zone to deeper water at the end of autumn and a change in food supply.

Migration as an escape from parasitism in New Zealand galaxiid fishes.

Parasite avoidance is increasingly considered to be a potential driving factor in animal migrations. In many marine and freshwater benthic fish, migration into a pelagic environment by developing larvae is a common life history trait that could reduce exposure to parasites during a critical window of developmental susceptibility. We tested this hypothesis on congeneric fish (family Galaxiidae, genus Galaxias) belonging to a closely related species complex sampled from coastal streams in southeastern New Zealand. Migratory Galaxias have larvae that migrate to pelagic marine environments, whereas the larvae of non-migratory species rear close to adult habitats with no pelagic larval phase. Both migratory and non-migratory fish are hosts to two species of skin-penetrating trematodes that cause spinal malformations and high mortality in young fish. Using generalized linear models within an Akaike information criterion and model averaging framework, we compared infection levels between migratory and non-migratory fish while taking into account body size and several other local factors likely to influence infection levels. For one trematode species, we found a significant effect of migration: for any given body length, migratory fish harboured fewer parasites than non-migratory fish. Also, no parasites of any kind were found in juvenile migratory fish sampled in spring shortly after their return to stream habitats. Our results demonstrate that migration spares juvenile fish from the debilitating parasites to which they would be exposed in adult stream habitats. Therefore, either the historical adoption of a migratory strategy in some Galaxias was an adaptation against parasitism, or it evolved for other reasons and now provides protection from infection as a coincidental side-effect.

Prevalence of Metagonimus metacercariae in sweetfish, Plecoglossus altivelis, from eastern and southern coastal areas in Korea.

The present study was performed to determine the current infecion status of Metagonimus yokogawai metacercariae in sweetfish, Plecoglossus altivelis, collected from several streams in eastern and southern coastal areas of Korea. The sweetfish collected were artificially digested with pepsin-HCl solution and examined under a stereomicroscope in August and September, 2007. Out of 145 sweetfish collected from 10 streams in eastern coasts (Gangwon-do and Gye-ongsangbuk-do), 88 (60.7%) were infected with Metagonimus metacercariae. The average metacercarial density was 61 per infected fish. Among 141 sweetfish collected from 10 streams in southern coasts (Gyeongsangnam-do, Ulsan Metropolitan city, and Jeollanam-do), 140 (99.3%) were infected with Metagonimus metacercariae, and their average density was 949 per infected fish. The present study confirmed that M. yokogawai metacercariae are still prevalent in the sweetfish from several eastern and southern coastal localities. The prevalence and metacercarial density were much higher in the sweetfish from streams of southern coasts than in those of eastern coasts. Therefore, attention should be paid to this small fluke infection, and consumption of raw sweetfish naturally produced in these areas should be prohibited.

Introduced brown trout alter native acanthocephalan infections in native fish.

1. Native parasite acquisition provides introduced species with the potential to modify native host-parasite dynamics by acting as parasite reservoirs (with the 'spillback' of infection increasing the parasite burdens of native hosts) or sinks (with the 'dilution' of infection decreasing the parasite burdens of native hosts) of infection. 2. In New Zealand, negative correlations between the presence of introduced brown trout (Salmo trutta) and native parasite burdens of the native roundhead galaxias (Galaxias anomalus) have been observed, suggesting that parasite dilution is occurring. 3. We used a multiple-scale approach combining field observations, experimental infections and dynamic population modelling to investigate whether native Acanthocephalus galaxii acquisition by brown trout alters host-parasite dynamics in native roundhead galaxias. 4. Field observations demonstrated higher infection intensity in introduced trout than in native galaxias, but only small, immature A. galaxii were present in trout. Experimental infections also demonstrated that A. galaxii does not mature in trout, although parasite establishment and initial growth were similar in the two hosts. Taken together, these results support the hypothesis that trout may serve as an infection sink for the native parasite. 5. However, dynamic population modelling predicts that A. galaxii infections in native galaxias should at most only be slightly reduced by dilution in the presence of trout. Rather, model exploration indicates parasite densities in galaxias are highly sensitive to galaxias predation on infected amphipods, and to relative abundances of galaxias and trout. Hence, trout presence may instead reduce parasite burdens in galaxias by either reducing galaxias density or by altering galaxias foraging behaviour.

Structure of capsule surrounding acanthocephalans Corynosoma strumosum in paratenic hosts of three species.

Morphology of capsules surrounding acanthocephalan Corynosoma strumosum in paratenic hosts (sea fishes of three species from the northern part of the Sea of Okhotsk) was studied. A thick layer of glycocalyx is formed on the surface of acanthocephalan's tegument in smelts Osmerus mordax dentex and Hypomesus olidus; the surrounding capsule is formed by fibroblasts and collagen fibers and do not include inflammatory cells. Besides fibroblasts, capsule of the sole Limanda aspera consists also of macrophages, granulocytes, "dark" cells, and once of erythrocytes that indicate obvious inflammatory response of the host's organism to invasion; glycocalyx on the surface of acanthocephalans from the sole is weakly developed. The obtained results allow considering the smelts as the most suitable paratenic hosts and the yellow-finned sole as unsuitable paratenic host for the studied acanthocephalans.

Prevalence of Metagonimus Metacercariae in Sweetfish, Plecoglossus altivelis, from Eastern and Southern Coastal Areas in Korea

The present study was performed to determine the current infecion status of Metagonimus yokogawai metacercariae in sweetfish, Plecoglossus altivelis, collected from several streams in eastern and southern coastal areas of Korea. The sweetfish collected were artificially digested with pepsin-HCl solution and examined under a stereomicroscope in August and September, 2007. Out of 145 sweetfish collected from 10 streams in eastern coasts (Gangwon-do and Gye-ongsangbuk-do), 88 (60.7%) were infected with Metagonimus metacercariae. The average metacercarial density was 61 per infected fish. Among 141 sweetfish collected from 10 streams in southern coasts (Gyeongsangnam-do, Ulsan Metropolitan city, and Jeollanam-do), 140 (99.3%) were infected with Metagonimus metacercariae, and their average density was 949 per infected fish. The present study confirmed that M. yokogawai metacercariae are still prevalent in the sweetfish from several eastern and southern coastal localities. The prevalence and metacercarial density were much higher in the sweetfish from streams of southern coasts than in those of eastern coasts. Therefore, attention should be paid to this small fluke infection, and consumption of raw sweetfish naturally produced in these areas should be prohibited.

The relationship between fish assemblages and the helminth communities of a prey fish, in a group of small shallow lakes.

Galaxias maculatus (small puyen) is an abundant native fish distributed in lakes and rivers of the Patagonia, and it is the frequent prey of other fishes, fish-eating birds, and mammals. Previous studies have shown that it is parasitized by 33 metazoan species and that the richness and composition of the parasite communities vary between lakes. The aim of the present work was to analyze the relationship between the composition of fish assemblages and the helminth component community structure of G. maculatus . Ten environmentally similar, small, shallow lakes, belonging to the Nahuel Huapi Lake basin, were chosen because of the differences in the native fish assemblages. Parasite community structure in G. maculatus varied according to the fish assemblage of each lake. The presence of the piscivorous fish Percichthys trucha regularly produced variations in the composition and richness at the component and infracommunity levels, as well as the percentage of autogenic parasite species in G. maculatus .

[Microevolutionary aspects of morphological variability and specificity of cestodes by the example of Proteocephalus longicollis (Zeder, 1800) (Proteocephalidae), a parasite of Coregonids].

Morphological variability of the cestode Proteocephalus longicollis from the smelt Osmerus eperlanus L., which was spontaneously introduced into the Syamozero Lake, has been studied. It was established that P. longicollis became an abundant element of the smelt parasite fauna during last 20 years, thereby showing the absence of host specificity. It was revealed that morphological polymorphism of P. longicollis from smelt combines features of ecological forms characteristic for aboriginal host species, namely whitefish Coregonus lavaretus L. and vendace Coregonus albula L. Cestodes from smelt are more similar to ecological forms from whitefish by the characteristics of variability. It is concluded that colonization of a host species, which is new for a given water body, is accompanied by the forming of a new group of host, which contributes to the maintenance of the parasite number and to its population stability under changing conditions of freshwater ecosystems.

A new hedrurid species (Nematoda) from galaxiid fishes in Patagonia (Argentina) and infection of amphipods as intermediate host.

During a parasite survey of galaxiid fishes (Galaxiidae) from Patagonian Andean lakes, a new species of nematode, Hedruris suttonae n. sp. was collected from the stomach of the native Galaxias maculatus (Jenyns) and G. platei (Steindachner). Specimens were examined by light and scanning electron microscopy, especially head morphology, female caudal prehensile structure, and distribution of spines. The new species is distinguished by body and tail size, morphology and size of spicules, the arrangement of caudal papillae in the male, the female caudal hook, and size of eggs. Hyalella patagonica (Ortmann), a Neotropical species of Amphipoda, is reported as its natural intermediate host. Data regarding prevalence and mean intensity in the intermediate and definitive hosts are included. The diet and habitat of the hosts, the percentage of gravid females, the high values of prevalence, and mean intensity in galaxiid fishes, as well as the wide distribution of H. suttonae , collectively indicate that, in these oligotrophic Andean lakes, G. maculatus and G. platei are true definitive hosts of this nematode.

Trematode infection causes malformations and population effects in a declining New Zealand fish.

1. Animal malformations engender wide public and scientific concern because of associated environmental health risks. This is highlighted by increased incidence of limb malformations in amphibians associated with trematode infections and disturbance. Malformations may signal new emerging disease threats, but whether the phenomenon is broadly applicable across taxa, or has population-scale impacts, is unknown. 2. Malformations are widely reported in fish and, until now, have been attributed mainly to contaminants. We tested whether the trematode Telogaster opisthorchis caused severe malformations, leading to population effects, in Galaxias anomalus, a threatened New Zealand freshwater fish. 3. Experimental infection of larval fish caused increasing spinal malformation and mortality with infection intensity that closely matched field patterns. Field malformation frequency peaked in January (65%), before declining sharply in February (25%) and remaining low thereafter. 4. The peak occurred during a 'critical window' of larval development, with the decline coincident with a population crash, indicating that malformation was causing mortality in the field. 5. The occurrence of such critical developmental windows may explain why this mechanism of population impact has been overlooked. With global environmental stressors predicted to enhance trematode infections, our results show that parasite-induced malformation, and its population-scale impacts, could be more widespread than previously considered.