Vicariance in a generalist fish parasite driven by climate and salinity tolerance of hosts.

Acanthocephalans are parasites with complex lifecycles that are important components of aquatic systems and are often model species for parasite-mediated host manipulation. Genetic characterization has recently resurrected Pomphorhynchus tereticollis as a distinct species from Pomphorhynchus laevis, with potential implications for fisheries management and host manipulation research. Morphological and molecular examinations of parasites from 7 English rivers across 9 fish species revealed that P. tereticollis was the only Pomphorhynchus parasite present in Britain, rather than P. laevis as previously recorded. Molecular analyses included two non-overlapping regions of the mitochondrial gene - cytochrome oxidase and generated 62 sequences for the shorter fragment (295 bp) and 74 for the larger fragment (583 bp). These were combined with 61 and 13 sequences respectively, from Genbank. A phylogenetic analysis using the two genetic regions and all the DNA sequences available for P. tereticollis identified two distinct genetic lineages in Britain. One lineage, possibly associated with cold water tolerant fish, potentially spread to the northern parts of Britain from the Baltic region via a northern route across the estuarine area of what is now the North Sea during the last Glaciation. The other lineage, associated with temperate freshwater fish, may have arrived later via the Rhine/Thames fluvial connection during the last glaciation or early Holocene when sea levels were low. These results raise important questions on this generalist parasite and its variously environmentally adapted hosts, and especially in relation to the consequences for parasite vicariance.

Inter-population variation in the intensity of host manipulation by the fish acanthocephalan Pomphorhynchus tereticollis: are differences driven by predation risk?

Many trophically-transmitted parasites induce behavioural alteration in their intermediate hosts that tend to increase host vulnerability to predation. Inter-population variability in parasite-induced alterations is expected to arise from variable local opportunities for trophic transmission. Yet, this hypothesis has not been investigated so far. We addressed the issue in four populations of the fish parasite Pomphorhynchus tereticollis (Acanthocephala), using variable fish biomass density as a proxy for transmission opportunities. We found variation in the intensity of parasite-induced changes in phototaxis and refuge use among populations. Two of the populations with the lowest predator biomass exhibited the highest levels of behavioural manipulation and prevalence, as expected at low transmission opportunities. They also exhibited micro-habitat segregation between infected and uninfected gammarids in the field. In addition, infection had variable effects on two physiological defence systems, immunity and antioxidant capacity, and on total protein content. Overall, our study brings partial support to the prediction that host manipulation and prevalence should be higher at low predator biomass. Although stronger evidence should be sought by increasing population replicates, our study points to the importance of the ecological context, specifically transmission opportunities brought about by predation pressure, for the evolution of parasite manipulation in trophically-transmitted parasites.

Egg fibrils and transmission in the acanthocephalan Acanthocephalus dirus.

Acanthocephalans have multi-host life cycles that include arthropods as intermediate hosts and vertebrates as definitive hosts. Eggs are dispersed into the habitat from definitive hosts and in some species eggs possess fibrils, which have been proposed to facilitate transmission to intermediate hosts. We examined the potential role of fibrils in transmission of the acanthocephalan Acanthocephalus dirus to its intermediate host Caecidotea intermedius, a stream-dwelling isopod. We identify three properties of fibrils that could favor transmission. First, there was a slow rate of fibril release, which was dependent on the actions of stream microorganisms. Second, eggs with fibrils were more likely to adhere to the substrate than those without fibrils. Third, in feeding trials, isopods exposed to eggs with fibrils had a higher infection prevalence than isopods exposed to eggs without fibrils. These properties could favor transmission by increasing the likelihood that eggs sink to the sediment occupied by their target hosts before adhering to items on the substrate (e.g., leaves) and by increasing recruitment after the eggs have been consumed.

How Ponto-Caspian invaders affect local parasite communities of native fish.

Invasive species are a major threat to ecosystems worldwide. Their effects are versatile and mostly well studied. However, not much is known about the impact of invasion on native parasite communities, although parasites are usually important response variables for ecosystem health. To improve the knowledge on how native fish parasite communities and their dynamics are affected by invasive species and how these processes change local host-parasite interactions over time, we studied different host-parasite systems in four German rivers. Three of these rivers (Rhine, Ems, and Elbe) are heavily invaded by different Ponto-Caspian species such as the amphipod Dikerogammarus villosus and various gobiids such as Neogobius melanostomus and Ponticola kessleri that serve as potential hosts for different local parasite species, while the fourth river (Schwentine) was free of any Ponto-Caspian invaders. Due to the lack of additional uninvaded river systems, literature data on parasite communities before invasion were compared with the post invasion status for the rivers Rhine and Elbe. The results showed differences among the parasite communities of different host species from the three invaded rivers when compared to the Schwentine River. Among the local internal parasite communities, especially the acanthocephalan Pomphorhynchus laevis and the nematode Raphidascaris acus have to be considered as key species associated with invasions from the Ponto-Caspian region. As the examined invasive Ponto-Caspian fish species serves as suitable host for both parasite species, the increases in their infection rates in native fish species are examples of parasite spill back (R. acus) and spill over (P. laevis, at least in the river Rhine). These results were further supported by the analysis of literature data on parasite communities of the past 20 years. Consequences for local parasite communities range from decreased prevalence of native parasites towards an extinction of entire parasite species.

Distribution patterns of two species of Corynosoma (Acanthocephala: Polymorphidae) in fishes from Southwestern Atlantic.

Corynosoma australe and C. cetaceum are the most frequently reported acanthocephalans in fish from the Argentine Sea, particularly in central and northern areas. Their definitive hosts are otariids and odontocete cetaceans, respectively. The low specificity of these larvae, in combination with high infective capability and long survival periods in fish, make them potentially good biological markers for stocks and other biological features of their fish hosts. In order to determine the distribution patterns of these species and their determining factors, a large dataset composed by newly collected fish samples, published and unpublished data from previous studies by the authors in the region were analysed in relation to host and environmental variables. The complete dataset comprised a total of 5084 fish, belonging to 29 species distributed in 21 families and 9 orders. Host size and trophic habits arose as the main determinants of abundance for both species of Corynosoma, showing higher abundances on larger fish and on higher trophic levels, as it is usual for trophically transmitted parasites. Biogeographic province and depth (indirectly representing the temperature of water) were the main drivers of the spatial distribution, displaying a latitudinal pattern associated to the temperature clines created by the interaction of Malvinas and Brazil currents, determining a decrease in abundance southwards and towards the deeper areas. No patterns were found regarding the distribution of definitive hosts. The knowledge of these distribution patterns of Corynosoma spp. in fish at regional scale, as well as of their causes, provides useful information to design management and conservation policies thus contributing to maintain the full and sustainable productivity of fisheries.

A closer look at the morphological and molecular diversity of Neoechinorhynchus (Acanthocephala) in Middle American cichlids (Osteichthyes: Cichlidae), with the description of a new species from Costa Rica.

Neoechinorhynchus is one of the most speciose genera of acanthocephalans, with approximately 116 described species. A recent study, aimed at establishing the genetic diversity of Neoechinorhynchus in Middle American freshwater fishes, validated nine species molecularly and morphologically and revealed the existence of 10 putative candidate species. Neoechinorhynchus golvani, a parasite commonly found in cichlids throughout Middle America with an allegedly large intraspecific morphological variability, was found to represent a species complex; species delimitation methods uncovered three additional genetic lineages. Here, we re-analyse the morphological and molecular data for N. golvani species complex infecting cichlids in that geographical area. A multivariate analysis of variance (MANOVA) was conducted particularly for the length of apical, middle and posterior hooks of the species/lineages of Neoechinorhynchus in cichlids, revealing morphological variation in the length of apical hooks for Lineage 8, although no morphological distinction was observed for Lineages 9 and 10. A new concatenated phylogenetic analysis of one mitochondrial and two ribosomal DNA genes was used to further corroborate the species delimitation among lineages; Neoechinorhynchus Lineage 8 was found to be morphologically and genetically distinct from its sister taxa, N. golvani and other two undescribed genetic lineages, and is formally described as a new species. Neoechinorhynchus costarricense n. sp. is described from the intestines of eight species of cichlids in Costa Rica. The new species is distinguished from the other species/lineages of Neoechinorhynchus in cichlids mainly by the size of the apical hooks of the proboscis.

Morphological and histochemical changes associated with massive infection by Neoechinorhynchus buttnerae (Acanthocephala: Neoechinorhynchidae) in the farmed freshwater fish Colossoma macropomum Cuvier, 1818 from the Amazon State, Brazil.

The study describes the morphological changes associated with parasitism by the intestinal acanthocephalan Neoechinorhynchus buttnerae in tambaqui juveniles Colossoma macropomum farmed in an excavated nursery, in Manaus (Amazon) in September 2013. After fish biometrics, analysis of macroscopic changes in morphology and counting of parasites, bowel fragments were fixed and submitted to histological and histochemical processing. All fish analyzed had acanthocephalans in the intestine; intestinal loops were milky white in color, with the presence of nodules with heavy parasitism. The changes in tissues that form the intestine varied according to the arrangement of the parasites: either free in the intestinal lumen or fixed by the proboscis on the organ wall. In the first case, the changes found were flaking, abrasion, compression, hypertrophy of goblet cells and disappearance of the villi on the mucosa, leukocytic cell infiltration in the submucosa, and muscle layer thickening. In the second case, in addition to these, other changes were observed as metaplasia in muscle tissue with its replacement by a loose connective tissue with severe leukocytic infiltration, edema in blood vessels, and necrotic foci. The histochemical analysis revealed that positive Alcian Blue mucosal cells (pH 2.5) were more expressive in parasitized intestines than in intestines not parasitized by N. buttnerae.

Pan-American marine coastal distribution of the acanthocephalan Profilicollis altmani based on morphometric and phylogenetic analyses of cystacanths from the mole crab Emerita brasiliensis.

Thorny-headed acanthocephalan worms of the genus Profilicollis are widely distributed in the oceans of the world and present complex life cycles with intermediate and definitive hosts. The genus is still poorly known, with an unstable taxonomy and, for most species, incompletely characterized geographical distributions. In this study, based on molecular and morphological evidence, we report that the species Profilicollis altmani is also distributed along the South American Atlantic coast, using the mole crab Emerita brasiliensis as an intermediate host. As such, our record shows that P. altmani has a Pan-American distribution where five species of Emerita are utilized as intermediate hosts.

ACANTHOCEPHALANS PROSTHENORCHIS CF. ELEGANS (ARCHIACANTHOCEPHALA: OLIGACANTHORHYNCHIDAE), PARASITES OF PRIMATES IN THE MOSCOW ZOO.

Acanthocephalans Prosthenorchis cf. elegans were found in primates in the Moscow Zoo. The larvae of these parasites (cistacanths) were found in cockroaches Blattella germanica that had been captured near aviaries of infected animals. Descriptions and drawings of adult parasites and their larvae are given. Analysis of Prosthenorchis cf. elegans genes ITS 1 rDNA and CO 1 mtDNA shows phylogenetic relations of these parasites with several representatives of the class Archiacanthocephala. The obtained molecular data, however, do not support the monophyly of the family Oligacanthorhynchidae and the order Oligacanthorhynchida.

Host-parasite relationships as determinants of heavy metal concentrations in perch (Perca fluviatilis) and its intestinal parasite infection.

The concentrations of As, Cd, Cr, Cu, Hg, Mn, Ni, Pb, and Zn and their bioconcentration factors (BCFs) were determined in two intestinal parasites, an acanthocephalan, Acanthocephalus lucii, a tapeworm, Proteocephalus percae, present in the same host, the European perch (Perca fluviatilis, L.), in the heavily polluted Ruzín reservoir in eastern Slovakia. The bioaccumulation of heavy metals in the fish organs and parasites was studied for acanthocephalan and tapeworm monoinfections or mixed infections by the two parasites and for the size of their parasitic infrapopulations. Bioconcentration factors (c[parasite]/c[muscle tissue]) showed that the concentrations of As, Ni, Pb and Zn were higher in mixed infections than in monoinfections. Negative correlations between heavy metal concentrations in perch organs and the parasites were found. For example, higher concentrations of Ni and Zn in both parasite species corresponded with lower metal concentrations in perch and hard roe. Likewise, significant negative relationships between metal concentrations in fish organs and number of parasites were noticed with lower levels of Pb in fish harbouring higher numbers of tapeworms. Similarly, in both parasite species the concentrations of some essential elements (Cr, Mn) were lower at high infection intensities compared to low intensities. Our study revealed that the differential concentration of heavy metals in perch organs was affected by the type of infection (mono- or mixed-infection), and needs to be considered in field ecotoxicological and parasitological studies as a potentially important factor influencing the pollutant concentrations in fish.

A description of Neoechinorhynchus (Neoechinorhynchus) veropesoi n. sp. (Acanthocephala: Neoechinorhynchidae) from the intestine of the silver croaker fish Plagioscion squamosissimus (Heckel, 1840) (Osteichthyes: Sciaenidae) off the east coast of Brazil.

Plagioscion squamosissimus (Heckel, 1840) (Osteichthyes: Sciaenidae) is considered piscivorous and is a generalist species endemic to the Amazon region. This fish is an important part of the natural ecosystems in which it occurs and provides basic functional components in the food web. The genus Neoechinorhynchus Stiles & Hassall, 1905 is distributed worldwide and parasitizes fish and turtles, but there are few reports of parasites of this genus in South America, due to the high diversity of fish that can be found in this region. A new species of thorny-headed worm (Acanthocephala: Neoechinorhynchidae) is described from P. squamosissimus from Guajará Bay, Belém, Pará, Brazil. In general, the unique characteristics of the hooks on the anterior end of the proboscis and the length-to-width ratio relationship separate this new species from other described species in the genus Neoechinorhynchus. Although the species in this genus are mostly found in North America, the dearth of species known from the neotropics may be due to the lack of studies in this region.

An annotated checklist of Acanthocephala from Australian fish.

Thirty one genera, comprising 58 named species, 15 undetermined species and nine species known only as cystacanths from paratenic fish hosts were found infesting 144 marine, esturine and freshwater species of fish from Australian and Australian Antarctic waters. Host habitats are given and the distribution and records of the acanthocephalans are given. A key to these parasites at the generic level is provided.

Checklist of the species of Neoechinorhynchus (Acanthocephala: Neoechinorhynchidae) in fishes and turtles in Middle-America, and their delimitation based on sequences of the 28S rDNA.

Among the acanthocephalans, Neoechinorhynchus is one of the most speciose genera, with 116 described species distributed worldwide. The adults of Neoechinorhynchus are found in the intestine of freshwater and brackish water fish, as well as in freshwater turtles. In this study, a checklist of the congeneric species of Neoechinorhynchus occurring in Middle-American fish and turtles is presented. The checklist contains the records established in all published accounts, as well as novel data from survey work conducted in the region comprising Neotropical areas of Mexico, as well as some localities in Central America. The species delimitation criteria used to discriminate among species is based on molecular data. In the last years, a large database derived from sequences of the D2 + D3 domains of the large subunit of rDNA (28S) was generated for 262 specimens corresponding to nine species of Neoechinorhynchus. This molecular marker has shown to be useful in establishing species limits within Neoechinorhynchus and in resolving phylogenetic relationships at species level. Based on our results, the domains D2 + D3 of the 28S rDNA could be considered as potential DNA barcodes to complement mitochondrial DNA to discriminate among acanthocephalan species.

Origination of a separate form of Neoechinorhynchus salmonis Ching, 1984 (Acanthocephales: Neoechinorhynchidae) in severe environment of the Asian Arctic.

Previous morphological research has shown that the species Neoechinorhynchus salmonis, first described from Canada, is also widespread in the northern Asia, in different climatic zones. Analysis of data from samples collected in various parts of its area of distribution leads to a conclusion about the existing two life forms of this species, namely temperate and polar ones. The specimens of the latter at the adult stage develop at far greater rate and reach maturity being smaller in size. It results in morphological difference: in the temperate form, the maximal body length of males is 7.8 mm; of females-15.0 mm, while in the polar form corresponding values are 4.5 and 7.8 mm (irrespective of host species). In the temperate form, in the course of maturing and growth of the adult worms, no seasonality was found which means a continuous replenishment of infection in the definitive hosts throughout a year. In the polar form, seasonal behavior of the intermediate hosts, the ostracods Cypria kolymensis, secures a heavy infection of the definitive hosts at the very beginning of the warm period (late June). In late August, the majority of parasites reach maturity and there are solid grounds to believe that adult worms are eliminated during the nearing wintering. In our opinion, the traits of the polar form are an adaptation to severe climatic conditions.

Patterns of trunk spine growth in two congeneric species of acanthocephalan: investment in attachment may differ between sexes and species.

Acanthocephalans have evolved a hooked proboscis and some taxa have trunk spines to attach to their definitive hosts. These structures are generated before being used, thus a key question is how investment in attachment could optimally be allocated through the ontogeny. The number and arrangement of hooks and spines are never modified in the definitive host, but it is unclear whether these structures grow during adult development. A comparison of the size of trunk spines between cystacanths and adults of Corynosoma cetaceum and C. australe indicated that spines grow in both species, but only in females, which also had significantly larger spines than males. This sexual dimorphism did not result from pure allometry because the body of females was smaller, and did not grow more than that of males. However, having a longer lifespan, females would need to withstand the extreme flow conditions prevailing in marine mammals for longer, inducing different investment and development schedules for spines. Patterns of spine growth also differed between species: fore-trunk spines grew in both species, but hind-trunk spines did only in C. cetaceum. In conclusion, investment strategies on attachment may differ, not only between congeneric species of acanthocephalan, but also between sexes of the same species.

Genetic and morphological variation in Echinorhynchus gadi Zoega in Müller, 1776 (Acanthocephala: Echinorhynchidae) from Atlantic cod Gadus morhua L.

Previous studies have shown considerable variability in morphological features and the existence of genetically distinct sibling species in the acanthocephalan Echinorhynchus gadi Zoega in Müller, 1776. The aim of the present study was to follow up and extend those earlier studies by using a combination of DNA analysis and morphometrics to investigate differences between samples of E. gadi from Atlantic cod Gadus morhua L. caught at five fishing grounds in the Baltic Sea and three in different parts of the North Atlantic. Twelve morphological features were measured in 431 specimens of E. gadi, 99 individuals were studied by polymerase chain reaction-restriction fragment length polymorphosm (PCR-RFLP), and selected PCR products were sequenced. The molecular analyses showed the nucleotide sequences of E. gadi rDNA from cod caught at all the sampling sites to be identical. The comparative morphological study, in contrast, revealed significant differences between samples of E. gadi from different sampling sites and showed the separation of E. gadi into two groups corresponding approximately to the systematic classification of cod into the two subspecies, Atlantic G. morhua morhua and Baltic G. morhua callarias. The E. gadi infrapopulation size had a significant effect on some of the morphological features. The results are discussed in relation to cod population biology, the hydrography of the study area and the history of the Baltic Sea formation.

[Convergence of the cyst in cysticercoids (Cestoda, Hymenolepidata) and the tegument in cystacanths (Acanthocephala)].

It was shown that despite fundamental differences in the organization of the tegument of cystacanths and the cyst wall of cysticeroids, they have a number of features similar in localization, morphology, terms of formation, and functional value. These include a powerful outer layer of glycocalyx on the surface of the tegument, filling of the distal department with dense substance, and the presence of complicated fibrillar systems. It is supposed that the nature of these particularities is convergent and is determined by the similarity of the life cycles of Hymenolepidata and Acanthocephala.

Genetic diversity and phylogeography of Corynosoma australe Johnston, 1937 (Acanthocephala: Polymorphidae), an endoparasite of otariids from the Americas in the northern and southern hemispheres.

Adult specimens of Corynosoma australe Johnston, 1937 were recorded from the intestines of California sea lions, Zalophus californianus (Lesson), from Baja California Peninsula, Mexico, whereas larval forms were collected from two fish species on the Argentinian coast. Adult specimens of C. australe were morphologically characterized by having a cylindrical proboscis with 18-20 rows of 12-14 hooks per row and a cylindrical trunk expanded anteriorly into a disk with tiny, triangular spines spreading almost to three quarters of the hind-trunk in males and to the posterior body end in females. The aim of this study was to explore the genetic diversity and systematic position of C. australe distributed in the Americas. Newly generated sequences of the mitochondrial cytochrome c oxidase subunit 1 (cox 1) gene were compared with sequences available from GenBank. Phylogenetic analyses performed with the cox 1 dataset using maximum likelihood and Bayesian inference showed that the 11 new sequences of C. australe recovered from the California sea lion in northern Mexico plus the six sequences from Argentinian seashores formed a clade with other sequences of specimens previously identified as C. australe. The intraspecific genetic divergence among the isolates was very low, ranging from 1 to 1.7%, and in combination with the phylogenetic trees confirmed that the isolates belonged to the same species. The cox 1 haplotype network inferred with 27 sequences revealed 18 haplotypes divided into two clusters clearly separated from each other by 5 substitutions. The first cluster corresponded to specimens from the Northern Hemisphere (United States of America and Mexico), and the second corresponded to specimens from the Southern Hemisphere (Argentina and Brazil). The current evidence suggests that C. australe has an amphitemperate distribution and is associated mainly with otariids with secondary and independent colonization events to other mammals and the Magellanic penguin in the Southern Hemisphere.

MORPHOLOGY OF ADULTS AND IMMATURES OF THE ACANTHOCEPHALAN, POMPHORHYNCHUS FUHAIENSIS YUE, 1998 (ACANTHOCEPHALA: POMPHORHYNCHIDAE) FROM CYPRINID FISH IN NORTHWEST CHINA.

Adult specimens of Pomphorhynchus fuhaiensis were identified from common carp (Cyprinus carpio L.) in Ulungur Lake of northwest China, and acanthors, acanthellae, cystacanths dissected from Gammarus lacustris in a small tributary of Ulungur River for the first time. The acanthocephalans were also found in crucian carp (Carassius carassius L.), tench (Tinca tinca L.), oriental bream (Abramis brama orientalis Berg), and ide (Leuciscus idus L.) in the lake. This species is distinguished from other species in Pomphorhynchus by its large, spherical bulb and very long neck as well as by a cylindrical proboscis armed with 15-17 longitudinal rows of 9-12 hooks each. The anterior proboscis hooks are almost uniform in size and shape, the sixth hook in a short row and the seventh hook in long row decrease abruptly in size posteriorly with the last end hook being a little larger than the prebasal hook, and in a ring; posterior proboscis hooks much more widely spaced. Furthermore, the lemnisci are claviform. The mean neck:trunk ratio is about 0.5, which is larger than most other species in Pomphorhynchus. Females are larger than males. In males, the testes are in one-third to one-half of the trunk, equal, ovoid-spheroid, usually contiguous, and small relative to the body size, and there are 6 ovoid cement glands. Pomphorhynchus fuhaiensis is similar to Pomphorhynchus laevis but can be distinguished by the number of longitudinal rows of hooks. Pomphorhynchus laevis is armed with 18-20 longitudinal rows of 11-13 hooks, P. fuhaiensis is armed with 15-17 longitudinal rows of 9-12 hooks.

Co-variation between the intensity of behavioural manipulation and parasite development time in an acanthocephalan-amphipod system.

Pomphorhynchus laevis, a fish acanthocephalan parasite, manipulates the behaviour of its gammarid intermediate host to increase its trophic transmission to the definitive host. However, the intensity of behavioural manipulation is variable between individual gammarids and between parasite populations. To elucidate causes of this variability, we compared the level of phototaxis alteration induced by different parasite sibships from one population, using experimental infections of Gammarus pulex by P. laevis. We used a naive gammarid population, and we carried out our experiments in two steps, during spring and winter. Moreover, we also investigated co-variation between phototaxis (at different stages of infection, 'young' and 'old cystacanth stage') and two other fitness-related traits, infectivity and development time. Three main parameters could explain the parasite intra-population variation in behavioural manipulation. The genetic variation, suggested by the differences between parasite families, was lower than the variation owing to an (unidentified) environmental factor. Moreover, a correlation was found between development rate and the intensity of behavioural change, the fastest growing parasites being unable to induce rapid phototaxis reversal. This suggests that parasites cannot optimize at the same time these two important parameters of their fitness, and this could explain a part of the variation observed in the wild.