Alpine bullhead (Cottus poecilopus Heckel): a potential refuge for Gyrodactylus salaris Malmberg, 1957 (Monogenea).

The notifiable freshwater pathogen Gyrodactylus salaris Malmberg, 1957 tends to be a generalist in contrast to other monogeneans. Whilst it causes most damage to its primary host, the Atlantic salmon (Salmo salar Linnaeus), transport and reservoir hosts likely play a key role in maintaining the parasite in the environment. Here, we tested the ability of G. salaris (strain River Lierelva, southern Norway) to infect and reproduce on a population of wild caught alpine bullhead (Cottus poecilopus Heckel). Exposure of alpine bullhead yearlings (0+) to G. salaris for 24 h at low (6.5 °C) or high temperature (11.5 °C) resulted in the establishment of 1 to 104 parasites per fish. Eight to nine days post-infection at high temperature, the infection of G. salaris was eliminated, indicative of innate host immunity. In contrast, at low temperature G. salaris infections persisted for 47-48 days. The relative lengthy infection of alpine bullhead with G. salaris compared to other non-salmonids tested may be due to low temperature and high initial infection load in combination with an epibiont infection. The present results suggest that this non-salmonid may function as a temperature-dependent transport or reservoir host for G. salaris.

Population regulation in Gyrodactylus salaris - Atlantic salmon (Salmo salar L.) interactions: testing the paradigm.

BACKGROUND: Gyrodactylus salaris is a directly transmitted ectoparasite that reproduces in situ on its fish host. Wild Norwegian (East Atlantic) salmon stocks are thought to be especially susceptible to the parasite due to lack of co-adaptation, contrary to Baltic salmon stocks. This study i) identifies whether time- and density-dependent mechanisms in gyrodactylid population growth exist in G. salaris-Atlantic salmon interactions and ii) based on differences between Norwegian and Baltic stocks, determines whether the 'Atlantic susceptible, Baltic resistant' paradigm holds as an example of local adaptation. METHODS: A total of 18 datasets of G. salaris population growth on individually isolated Atlantic salmon (12 different stocks) infected with three parasite strains were re-analysed using a Bayesian approach. Datasets included over 2000 observations of 388 individual fish. RESULTS: The best fitting model of population growth was time-limited; parasite population growth rate declined consistently from the beginning of infection. We found no evidence of exponential population growth in any dataset. In some stocks, a density dependence in the size of the initial inoculum limited the maximum rate of parasite population growth. There is no evidence to support the hypothesis that all Norwegian and Scottish Atlantic salmon stocks are equally susceptible to G. salaris, while Baltic stocks control and limit infections due to co-evolution. Northern and Western Norwegian as well as the Scottish Shin stocks, support higher initial parasite population growth rates than Baltic, South-eastern Norwegian, or the Scottish Conon stocks, and several Norwegian stocks tested (Akerselva, Altaelva, Lierelva, Numedalslågen), and the Scottish stocks (i.e. Conon, Shin), were able to limit infections after 40-50 days. No significant differences in performance of the three parasite strains (Batnfjordselva, Figga, and Lierelva), or the two parasite mitochondrial haplotypes (A and F) were observed. CONCLUSIONS: Our study shows a spectrum of growth rates, with some fish of the South-eastern Norwegian stocks sustaining parasite population growth rates overlapping those seen on Baltic Neva and Indalsälv stocks. This observation is inconsistent with the 'Baltic-resistant, Atlantic-susceptible' hypothesis, but suggests heterogeneity, perhaps linked to other host resistance genes driven by selection for local disease syndromes.

Fauna europaea: helminths (animal parasitic).

Fauna Europaea provides a public web-service with an index of scientific names (including important synonyms) of all living European land and freshwater animals, their geographical distribution at country level (up to the Urals, excluding the Caucasus region), and some additional information. The Fauna Europaea project covers about 230,000 taxonomic names, including 130,000 accepted species and 14,000 accepted subspecies, which is much more than the originally projected number of 100,000 species. This represents a huge effort by more than 400 contributing specialists throughout Europe and is a unique (standard) reference suitable for many users in science, government, industry, nature conservation and education. Helminths parasitic in animals represent a large assemblage of worms, representing three phyla, with more than 200 families and almost 4,000 species of parasites from all major vertebrate and many invertebrate groups. A general introduction is given for each of the major groups of parasitic worms, i.e. the Acanthocephala, Monogenea, Trematoda (Aspidogastrea and Digenea), Cestoda and Nematoda. Basic information for each group includes its size, host-range, distribution, morphological features, life-cycle, classification, identification and recent key-works. Tabulations include a complete list of families dealt with, the number of species in each and the name of the specialist responsible for data acquisition, a list of additional specialists who helped with particular groups, and a list of higher taxa dealt with down to the family level. A compilation of useful references is appended.

Same barcode, different biology: differential patterns of infectivity, specificity and pathogenicity in two almost identical parasite strains.

Two Norwegian isolates of the monogenean Gyrodactylus salaris Malmberg, 1957 with identical cytochrome c oxidase subunit I barcodes from different hosts, show highly divergent biological and behavioural characteristics. The Lierelva parasite strain, typically infecting Atlantic salmon, Salmo salar L., grew exponentially on Atlantic salmon, but the Pålsbufjorden parasite strain, commonly infecting Arctic charr, Salvelinus alpinus L., grew slowly on both hosts and was non-pathogenic to Atlantic salmon. Both parasite strains reproduced successfully on Arctic charr, but the Atlantic salmon-infecting Lierelva strain grew faster on both hosts. Experiments with isolated worms revealed differences in reproductive rates which may account for the observed population differences. Atlantic salmon parasites consistently gave birth at an earlier age than the Arctic charr parasites, with the differential increasing from 1 day for the first birth up to 2-4 days for the third birth. Arctic charr-infecting parasites were more active on Atlantic salmon than salmon parasites on Arctic charr, a behavioural strategy leading to enhanced G. salaris mortality. Sequencing of 10 kb of nuclear genomic markers revealed only four single nucleotide polymorphisms, confirming that isolates of G. salaris with differences in fitness traits influencing establishment, fecundity and behaviour may be remarkably similar at a molecular level. The framework for reporting and control of G. salaris requires re-appraisal in light of the discovery of variants with such divergent biology.

An agent-based modelling approach to estimate error in gyrodactylid population growth.

Comparative studies of gyrodactylid monogeneans on different host species or strains rely upon the observation of growth on individual fish maintained within a common environment, summarised using maximum likelihood statistical approaches. Here we describe an agent-based model of gyrodactylid population growth, which we use to evaluate errors due to stochastic reproductive variation in such experimental studies. Parameters for the model use available fecundity and mortality data derived from previously published life tables of Gyrodactylus salaris, and use a new data set of fecundity and mortality statistics for this species on the Neva stock of Atlantic salmon, Salmo salar. Mortality data were analysed using a mark-recapture analysis software package, allowing maximum-likelihood estimation of daily survivorship and mortality. We consistently found that a constant age-specific mortality schedule was most appropriate for G. salaris in experimental datasets, with a daily survivorship of 0.84 at 13°C. This, however, gave unrealistically low population growth rates when used as parameters in the model, and a schedule of constantly increasing mortality was chosen as the best compromise for the model. The model also predicted a realistic age structure for the simulated populations, with 0.32 of the population not yet having given birth for the first time (pre-first birth). The model demonstrated that the population growth rate can be a useful parameter for comparing gyrodactylid populations when these are larger than 20-30 individuals, but that stochastic error rendered the parameter unusable in smaller populations. It also showed that the declining parasite population growth rate typically observed during the course of G. salaris infections cannot be explained through stochastic error and must therefore have a biological basis. Finally, the study showed that most gyrodactylid-host studies of this type are too small to detect subtle differences in local adaptation of gyrodactylid monogeneans between fish stocks.

Morphometric and molecular characterization of Gyrodactylus teuchis Lautraite, Blanc, Thiery, Daniel & Vigneulle, 1999 (Monogenea: Gyrodactylidae) from an Austrian brown trout population.

Gyrodactylus teuchis is a widespread parasite of wild and farmed salmonids throughout Europe. It has been frequently confused with the notifiable pathogen G. salaris, to which it bears a striking morphological similarity. The species is frequently referred to as 'cryptic', and diagnoses are primarily based on molecular evidence. We provide the first comprehensive re-description of G. teuchis from a natural wild brown trout population in the Danube watershed, based on the state of the art morphometrics in addition to standard molecular markers. We demonstrate that despite the lack of uni-variate diagnostic character measurements, G. teuchis can be reliably distinguished from G. salaris using multivariate morphological approaches such as Principal Component Analysis or Canonical Variate Analysis, suggesting that automated diagnostic approaches for G. salaris can be modified to take account of potential G. teuchis in samples. This is the first record of G. teuchis from a host population unlikely to have been modified by human stocking efforts. The morphological variability observed in the samples collected from one site on 1 day reflects the overall level of variation reported for European G. teuchis. We also report new sequence variants of the internal transcribed spacer (ITS-1) of the nuclear ribosomal gene cluster with evidence for intra-individual heterogeneity of ITS-1 within this population of G. teuchis.

Mitochondrial DNA variation of a natural population of Gyrodactylus thymalli (Monogenea) from the type locality River Hnilec, Slovakia.

The monogenean flatworm Gyrodactylus thymalli (Zitnan, Helminthologia, 2:266-269, 1960) is considered a harmless ectoparasite on grayling (Thymallus thymallus). The species is closely related to G. salaris Malmberg, 1957 that causes severe gyrodactylosis on Atlantic salmon (Salmo salar) in many Norwegian rivers. In this paper, we study the mitochondrial diversity of a G. thymalli population from one of the type localities Hrable on River Hnilec, Slovakia. By sequencing parts of the mitochondrial NADH dehydrogenase subunit 5 gene, we detected three haplotypes that differ from each other by 2.1-4.1%. The haplotype HnilecI was found most common. Our data suggest that River Hnilec has been colonized independently at least three times with G. thymalli.

DNA taxonomy and barcoding of monogenean parasites: lessons from Gyrodactylus.

DNA taxonomy and barcoding use nucleotide sequence data to achieve comprehensive species descriptions that facilitate reliable species diagnostics and rapid assessment of biodiversity, both of which are of great importance for parasitologists. Such molecular approaches have been applied to the monogenean genus Gyrodactylus, in particular to G. salaris, the cause of serious gyrodactylosis on Atlantic salmon. Here, we discuss, using the example of G. salaris and related species, why DNA barcodes, although powerful for biodiversity assessment, are insufficient to appropriately characterize parasite species--from a parasitological point of view--in the absence of additional data on and infection biology and morphology.

The complete mitochondrial DNA sequence of the monogenean Gyrodactylus thymalli (Platyhelminthes: Monogenea), a parasite of grayling (Thymallus thymallus).

We present the complete mitochondrial (mt) genome of Gyrodactylus thymalli, a monogenean ectoparasite on grayling (Thymallus thymallus). The circular genome is 14788 bp in size and includes all 35 genes recognized from other flatworm mt genomes. The overall A+T content of the mt genome is 62.8%. Twenty regions of non-coding DNA ranging from 1 to 111 bp in length were identified in addition to 2 highly conserved large non-coding regions 799 bp and 767 bp in size. Compared to the recently described mt DNA of the closely related G. salaris from Atlantic salmon from Signaldalselva, Norway, the mitochondrial genome of G. thymalli from Hnilec, Slovakia, differs on average by 2.2%.

Mitochondrial haplotype diversity of Gyrodactylus thymalli (Platyhelminthes; Monogenea): extended geographic sampling in United Kingdom, Poland, and Norway reveals further lineages.

In recent years, the mitochondrial haplotype diversity of the monogenean ectoparasites Gyrodactylus salaris Malmberg, 1957 on Atlantic salmon and G. thymalli Zitnan, 1960 on grayling has been studied intensively to understand the taxonomy and phylogeography of the two species. According to these studies, neither species can be considered monophyletic, but unfortunately, the geographic sampling has mostly been restricted to Fennoscandia. Only few samples from continental Europe have been analysed, and samples from the United Kingdom have not been included at all. Gyrodactylosis is a notifiable disease in Europe and is in the UK considered the most important exotic disease threat to wild Atlantic salmon populations. In this study, we report six new mitochondrial haplotypes of G. thymalli from England, Poland, and Norway detected by sequencing 745 bp of the cytochrome oxidase I gene. The six new haplotypes add five new clades to a neighbor-joining dendrogram deduced on the basis of the currently known 44 mitochondrial haplotypes for G. thymalli and G. salaris. We conclude that G. thymalli established in the UK along with the immigration of grayling. There is currently no reason to suspect that this parasite is a threat to Atlantic salmon in the UK, although its infectivity to salmon stocks in the UK has not been tested.

The use of morphometric characters to discriminate specimens of laboratory-reared and wild populations of Gyrodactylus salaris and G. thymalli (Monogenea).

Gyrodactylus thymalli Zitnan, 1960 and G. salaris Malmberg, 1957 have an indistinguishable ribosomal internal transcribed spacer (ITS) DNA sequence, but exhibit surprisingly high levels of intra- and interspecific sequence variation of the mitochondrial cytochrome oxidase I (CO1) gene. To test whether different populations of these reportedly very similar species could be discriminated using morphometric methods, we examined the morphometry of four different populations representing different mitochondrial clades. Twenty five point-to-point measurements, including five new characters of the attachment hooks, were recorded from three Norwegian laboratory populations (G. salaris from the Rivers Lierelva and Rauma, and G. thymalli from the River Rena), and from one wild population of G. thymalli from the River Test, UK. The Norwegian populations were kept under identical environmental conditions to control for the influence of temperature on the haptoral attachment hooks. Data were subsequently subjected to univariate and linear stepwise discriminant analyses. The model generated by the linear stepwise discriminant analysis used 18 of the 25 original variables, the first two roots accounting for 96.6% of the total variation between specimens. The hamulus shaft length accounts for 66.7% of the overall correct classification efficiency. Based on morphometry, all specimens were assigned to the correct species. Apart from three specimens of G. salaris from the River Lierelva population which were misclassified as belonging to the G. salaris Rauma population, all specimens were assigned to the correct population. Thus, populations of Gyrodactylus identified by mtDNA can also be discriminated using morphometric landmark distances.

Chaetotaxy applied to Norwegian Gyrodactylus salaris Malmberg, 1957 (Monogenea) clades and related species from salmonids.

Gyrodactylus salaris Malmberg, 1957 is a major pathogen of wild Salmo salar L. parr populations in Norway, and its delimitation from non-pathogenic species is important. The present study was undertaken to test the power of chaetotaxy to differentiate between three populations belonging to both the same and different clades (as stated by mtDNA) of G. salaris, in addition to three different species of gyrodactylids (G. salaris, G. thymalli and G. caledoniensis). The gyrodactylids were processed for chaetotaxy in situ and a maximum of 50 specimens per collection site were used to construct a generalised map over the sensilla. The sensilla were found in all populations to be symmetrically distributed around the median longitudinal axis, according to a formula of 7 dorsal (34 sensilla) and 8 ventral (44 sensilla) clusters on each side of the median line. The three Norwegian populations of G. salaris were found identical, as were the population of G. thymalli. The specimens of G. caledoniensis from Scotland, however, were found to differ from the Norwegian species G. salaris and G. thymalli by the position of one sensillum in two of the clusters. A comparison of the sensillum pattern of laboratory maintained G. salaris (River Lierelva) with results obtained ten years earlier, questions the temporal stability of the chaetotaxy pattern. The present results indicate that chaetotaxy can be used to discriminate between certain Gyrodactylus spp. but not generally.

Mitochondrial DNA variation of Gyrodactylus spp (Monogenea, Gyrodactylidae) populations infecting Atlantic salmon, grayling, and rainbow trout in Norway and Sweden.

Approximately 800 bp of the mitochondrial cytochrome oxidase I (COI) gene were sequenced from 76 Gyrodactylus specimens of 32 salmonid host populations, i.e. from Salmo salar, Thymallus thymallus, and Oncorhynchus mykiss in Norway, Sweden and Latvia. The COI sequences indicated a substantial intraspecific differentiation of Gyrodactylus salaris and Gyrodactylus thymalli. In total, 12 haplotypes were identified which group into five well supported clades, three clades with parasites from Atlantic salmon and two clades with parasites from grayling. The basal nodes linking the five clades together are only weakly supported. Thus, there is no support for the monophyly of all G. salaris haplotypes and the monophyly of all G. thymalli haplotypes. The lack of monophyly of the mitochondrial haplotypes of G. salaris and G. thymalli may indicate that G. salaris and G. thymalli represent (i). two polytypic species or (ii). one polytypic species, or (iii). refer to a complex of more than two sibling species. The mtDNA data indicate multiple introductions of G. salaris and G. thymalli into Norway. A minimum of three independent introductions of G. salaris and two independent introductions of G. thymalli are supported. This is congruent with earlier hypotheses on the introduction of G. salaris and G. thymalli into Norway.

Host specificity dynamics: observations on gyrodactylid monogeneans.

The directly transmitted viviparous gyrodactylids have high species richness but low morphological and biological diversity, and many species are recorded from only a single host. They therefore constitute a guild of species ideal for studies of the evolutionary significance of host specificity. The group has the widest host range of any monogenean family, being found on 19 orders of bony fish. However, individual species range from narrowly specific (71% of 402 described species recorded from a single host) to extremely catholic (Gyrodactylus alviga recorded from 16 hosts). Gyrodactylid-host interactions extend from 60 mya (G. lotae, G. lucii) down to 150 years (G. derjavini on Oncorhynchus mykiss). Co-evolution with the host is comparatively rare within the gyrodactylids, but host switching or ecological transfer is common, and has been facilitated by the mixing of fish strains that followed glaciation. In this review, we consider the factors responsible for gyrodactylid specificity patterns, using examples from our work on salmonid gyrodactylids including G. salaris, responsible for major epidemics on wild Atlantic salmon (Salmo salar) in Norway since 1975, and G. thymalli from grayling and G. derjavini from trout.G. salaris has a wide host range with highest population growth rates on Norwegian salmon strains. However, growth rates are variable on both host strains and species, because of the multitude of micro- and macro-environmental factors influencing parasite mortality and fecundity. A better predictor of performance is the proportion of fishes of a strain which are innately resistant to the parasite, a measure which is negatively correlated with the time to peak infection in a host strain. Population growth rate is also negatively correlated with age of infection; the initial rate, therefore, predicts best the suitability of a fish as host for G. salaris. The host response to gyrodactylids appears to be the same mechanism in all salmonids with innate resistance as one end of a spectrum, but influenced by stress and probably under polygenic control. Hybrid experiments show that performance of G. salaris on a host is heritable, and usually intermediate between that of the parents. This host response mechanism, coupled with the initial parasite population growth on a fish, determines the host specificity, i.e. whether the fish will be susceptible, a responder or innately resistant. The use of population growth rate parameters allows comparison of different hosts as a resource for a gyrodactylid. In the case of G. salaris, East Atlantic and Baltic strains of Atlantic salmon are core hosts, but other salmonids can physiologically sustain infections for considerable periods, and may be important in parasite dispersal and transmission. A further group of non-salmonid fishes are unable to sustain G. salaris reproduction, but can act as transport hosts.Population growth parameters are very labile to stressors and environmental factors, particularly temperature and salinity, and also other aspects of host ecology and water quality. These factors may also influence the spectrum of hosts that can be infected under particular conditions, and probably favoured ecological transfer of gyrodactylids between host species in periglacial conditions. G. salaris may still be undergoing post-glacial range expansion (aided by anthropogenic spread) as shown by the increase in the species range over the last 25 years. The origin of G. salaris, G. teuchis and G. thymalli is discussed in relation to glacial refugiums during the last ice age.