Long-term spatiotemporal stability and dynamic changes in helminth infracommunities of bank voles (Myodes glareolus) in NE Poland.

Parasites are considered to be an important selective force in host evolution but ecological studies of host-parasite systems are usually short-term providing only snap-shots of what may be dynamic systems. We have conducted four surveys of helminths of bank voles at three ecologically similar woodland sites in NE Poland, spaced over a period of 11 years, to assess the relative importance of temporal and spatial effects on helminth infracommunities. Some measures of infracommunity structure maintained relative stability: the rank order of prevalence and abundance of Heligmosomum mixtum, Heligmosomoides glareoli and Mastophorus muris changed little between the four surveys. Other measures changed markedly: dynamic changes were evident in Syphacia petrusewiczi which declined to local extinction, while the capillariid Aonchotheca annulosa first appeared in 2002 and then increased in prevalence and abundance over the remaining three surveys. Some species are therefore dynamic and both introductions and extinctions can be expected in ecological time. At higher taxonomic levels and for derived measures, year and host-age effects and their interactions with site are important. Our surveys emphasize that the site of capture is the major determinant of the species contributing to helminth community structure, providing some predictability in these systems.

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.

On the systematic position of Collyricloides massanae Vaucher, 1969 (Platyhelminthes: Digenea) with notes on distribution of this trematode species.

The systematic position of the Collyricloides massanae, a rare cyst-dwelling parasite, located on intestinal wall of European birds and rodents, have always been controversial. Based on newly obtained sequences of the 28 sDNA of C. massanae from avian and rodent host from Central Europe, and on the previously published sequences of several genera and families among Microphalloidea, we evaluate its taxonomic position and the phylogenetic relationships within the genera Collyriclum Kossack, 1911 and Collyricloides Vaucher, 1969 which form the family Collyriclidae Ward, 1917. In the cladogram, C. massanae appears among the Pleurogenidae, forming a clade with Gyrabascus amphoraeformis (Modlinger, 1930) and Cortrema magnicaudata (Bykhovskaya-Pavlovskaya, 1950). We reject the commonly accepted placement of Collyricloides as the sister genus to Collyriclum within the Collyriclidae. Besides, we present and discuss the unusual records of C. massanae in the bank vole Myodes glareolus from northeastern Poland.

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.

Heligmosomoides neopolygyrus Asakawa & Ohbayashi, 1986, a cryptic Asian nematode infecting the striped field mouse Apodemus agrarius in Central Europe.

BACKGROUND: Heligmosomoides polygyrus is a widespread gastro-intestinal nematode infecting wild Apodemus (wood mice) throughout Europe. Using molecular and morphological evidence, we review the status of Heligmosomoides from Apodemus agrarius in Poland previously considered to be an outlying clade of H. polygyrus, to further resolve the status of the laboratory model species, H. bakeri. METHODS: Morphological analysis of the male bursa and the synlophe, and molecular analyses of concatenated nuclear (28S rDNA, ITS1 and ITS2) and mitochondrial (CO1 and cytb) genes, of Heligmosomoides collected from Apodemus agrarius from two sites in Poland and comparison with related heligmosomids from voles and mice in Eurasia. RESULTS: Heligmosomoides neopolygyrus, a heligmosomid nematode from Apodemus species from China and Japan, is recognised for the first time in western Europe infecting Apodemus agrarius in Poland. It can be distinguished from H. polygyrus by the filiform externo-dorsal rays of the male copulatory bursa and the small, equally distributed longitudinal crêtes on the body. Specimens from A. agrarius are 20% different at ribosomal (ITS1 and ITS2) nuclear loci, and 10% different at the mitochondrial cytb locus from H. polygyrus, and in phylogenetic analyses group with the vole-infecting genus Heligmosomum. CONCLUSIONS: Despite morphological similarity, H. neopolygyrus is only distantly related to H. polygyrus from western European Apodemus, and may be more closely related to vole-infecting taxa. It was brought into Europe by the recent rapid migration of the host mice. Inclusion of H. neopolygyrus in phylogenies makes it clear that Heligmosomoides is paraphyletic, with the pika-infecting Ohbayashinema and the vole-infecting Heligmosomum nesting within it. Clarification of the European status of H. neopolygyrus also allows H. bakeri, the laboratory model species, to be seen as a terminal sister clade to H. polygyrus, rather than as an internal clade of the latter taxon.

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.

PCR characterization suggests that an unusual range of Bartonella species infect the striped field mouse (Apodemus agrarius) in Central Europe.

Blood samples from Apodemus agrarius from Poland yielded PCR amplicons of Bartonella species. These included B. grahamii, B. taylorii, and B. birtlesii, as is typical of European Apodemus, as well as B. elizabethae-like forms and a recombinant strain of B. taylorii, most closely related to an American isolate from Tamiasciurus hudsonicus.

Bartonella infections in deer keds (Lipoptena cervi) and moose (Alces alces) in Norway.

Infections with Bartonella spp. have been recognized as emerging zoonotic diseases in humans. Large knowledge gaps exist, however, relating to reservoirs, vectors, and transmission of these bacteria. We describe identification by culture, PCR, and housekeeping gene sequencing of Bartonella spp. in fed, wingless deer keds (Lipoptena cervi), deer ked pupae, and blood samples collected from moose, Alces alces, sampled within the deer ked distribution range in Norway. Direct sequencing from moose blood sampled in a deer ked-free area also indicated Bartonella infection but at a much lower prevalence. The sequencing data suggested the presence of mixed infections involving two species of Bartonella within the deer ked range, while moose outside the range appeared to be infected with a single species. Bartonella were not detected or cultured from unfed winged deer keds. The results may indicate that long-term bacteremia in the moose represents a reservoir of infection and that L. cervi acts as a vector for the spread of infection of Bartonella spp. Further research is needed to evaluate the role of L. cervi in the transmission of Bartonella to animals and humans and the possible pathogenicity of these bacteria for humans and animals.

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.

Recombination, diversity and allele sharing of infectivity proteins between Bartonella species from rodents.

The alpha-Proteobacterium Bartonella is a common parasite of voles and mice, giving rise to short-lived (4 weeks to 2 months) infections. Here, we report high sequence diversity in genes of the VirB/VirD type IV secretion system (T4SS), amongst Bartonella from natural rodent populations in NE Poland. The VirB5 protein is predicted to consist of three conserved alpha helices separated by loops of variable length which include numerous indels. The C-terminal domain includes repeat stretches of KEK residues, reflecting underlying homopolymeric stretches of adenine residues. A total of 16 variants of VirB5, associated with host identity, but not bacterial taxon, were identified from 22 Bartonella isolates. One was clearly a recombinant from two others, another included an insertion of two KEK repeats. The virB5 gene appears to evolve via both mutation and recombination, as well as slippage mediated insertion/deletion events. The recombinational units are thought to be relatively short, as there was no evidence of linkage disequilibrium between virB5 and the bepA locus only 5.5 kb distant. The diversity of virB5 is assumed to be related to immunological role of this protein in Bartonella infections; diversity of virB5 may assist persistence of Bartonella in the rodent population, despite the relatively short (3-4 weeks) duration of individual infections. It is clear from the distribution of virB5 and bepA alleles that recombination within and between clades is widespread, and frequently crosses the boundaries of conventionally recognised Bartonella species.

Recombination within and between species of the alpha proteobacterium Bartonella infecting rodents.

Bartonella infections from wild mice and voles (Apodemus flavicollis, Mi. oeconomus, Microtus arvalis and Myodes glareolus) were sampled from a forest and old-field habitats of eastern Poland; a complex network of Bartonella isolates, referrable to B. taylorii, B. grahamii, B. birtlesii and B. doshiae, was identified by the sequencing of a gltA fragment, comparable to previous studies of Bartonella diversity in rodents. Nested clade analysis showed that isolates could be assigned to zero- and one-step clades which correlated with host identity and were probably the result of clonal expansion; however, sequencing of other housekeeping genes (rpoB, ribC, ftsZ, groEl) and the 16S RNA gene revealed a more complex situation with clear evidence of numerous recombinant events in which one or both Bartonella parents could be identified. Recombination within gltA was found to have generated two distinct variant clades, one a hybrid between B. taylorii and B. doshiae, the other between B. taylorii and B. grahamii. These recombinant events characterised the differences between the two-step and higher clades within the total nested cladogram, involved all four species of Bartonella identified in this work and appear to have played a dominant role in the evolution of Bartonella diversity. It is clear, therefore, that housekeeping gene phylogenies are not robust indicators of Bartonella diversity, especially when only a single gene (gltA or 16S RNA) is used. Bartonella clades infecting Microtus were most frequently involved in recombination and were most frequently tip clades within the cladogram. The role of Microtus in influencing the frequency of Bartonella recombination remains unknown.

Utilisation of rodent species by larvae and nymphs of hard ticks (Ixodidae) in two habitats in NE Poland.

The impact of host identity and habitat type on the density of hard ticks (Ixodes ricinus and Dermacentor reticulatus) infections on rodents in forest and abandoned field habitats in NE Poland was investigated. Ixodes ricinus was most abundant in the forest system, but D. reticulatus, although rarer, was most abundant in the field system. Environmental humidity and the much lower density of rodents probably limited the abundance of I. ricinus larvae in the field system, although this tick was still common on Microtus oeconomus from around small ponds. Nymphs of I. ricinus were comparatively rare in the forest, probably because of infection of non-rodent hosts. Dermacentor reticulatus nymphs on the other hand were very much more common in the ears of Microtus species than would have been predicted based on larval densities. The impact of habitat change (in this case successional change following field abandonment) on tick densities is emphasised, and the role of Apodemus as an epidemiological bridge, linking woodland and field habitats, is highlighted.

A new gyrodactylid (Monogenea) genus on gray bichir, Polypterus senegalus (Polypteridae) from Senegal (West Africa).

Diplogyrodactylus martini n. g. et sp., a viviparous monogenean, is described from the gills of gray bichir Polypterus senegalus Cuvier, 1829, in Senegal. This new genus can be readily distinguished from the other described viviparous genera based on the morphology of the attachment apparatus. The haptor is equipped with a pair of centrally positioned hamuli, a simple ventral bar without membrane and 8 pairs of marginal hooks of 2 types, 5 pairs of hooks with well-defined large falculate sickles, and 3 pairs of smaller hooks with well-articulated sickles. The new genus is unique in having a teardrop-shaped muscular tubular male copulatory organ which lacks spines. A partial sequence of the internal transcribed spacer (ITS rDNA) was obtained from 4 specimens of D. martini. The relationship among D. martini and other genera of the Gyrodactylidae is discussed based on the similarities of the attachment apparatus.

Immunomodulatory parasites and toll-like receptor-mediated tumour necrosis factor alpha responsiveness in wild mammals.

BACKGROUND: Immunological analyses of wild populations can increase our understanding of how vertebrate immune systems respond to 'natural' levels of exposure to diverse infections. A major recent advance in immunology has been the recognition of the central role of phylogenetically conserved toll-like receptors in triggering innate immunity and the subsequent recruitment of adaptive response programmes. We studied the cross-sectional associations between individual levels of systemic toll-like receptor-mediated tumour necrosis factor alpha responsiveness and macro- and microparasite infections in a natural wood mouse (Apodemus sylvaticus) population. RESULTS: Amongst a diverse group of macroparasites, only levels of the nematode Heligmosomoides polygyrus and the louse Polyplax serrata were correlated (negatively) with innate immune responsiveness (measured by splenocyte tumour necrosis factor alpha responses to a panel of toll-like receptor agonists). Polyplax serrata infection explained a strikingly high proportion of the total variation in innate responses. Contrastingly, faecal oocyst count in microparasitic Eimeria spp. was positively associated with innate immune responsiveness, most significantly for the endosomal receptors TLR7 and TLR9. CONCLUSION: Analogy with relevant laboratory models suggests the underlying causality for the observed patterns may be parasite-driven immunomodulatory effects on the host. A subset of immunomodulatory parasite species could thus have a key role in structuring other infections in natural vertebrate populations by affecting the 'upstream' innate mediators, like toll-like receptors, that are important in initiating immunity. Furthermore, the magnitude of the present result suggests that populations free from immunosuppressive parasites may exist at 'unnaturally' elevated levels of innate immune activation, perhaps leading to an increased risk of immunopathology.

Seasonality of the ectoparasite community of woodland rodents in a Mazurian Forest, Poland.

Myodes glareolus and Apodemus flavicollis support a large and diverse community of arthropod ectoparasites. This study of rodents in a Mazurian woodland sampled at monthly intervals between 2007 and 2009 revealed an ectoparasite community composed of 2 species of tick, 1 louse, 9 flea species, 7 species of gamasid mites, 4 fur mites and one trombiculid mite. A strong seasonality was noted in the dynamics of the ectoparasite community, with the fur mite Listrophorus sp. and the hypopus larva of a glycyphagid mite especially common in winter. Several of the ectoparasites have the potential to be pathogenic; the impact of these organisms on the population dynamics of their hosts remains to be investigated.

The evolution of fish ectoparasite communities--the role of the ice ages.

The monogenean ectoparasite genera Dactylogyrus and Gyrodactylus are hyperdiverse, and yet monogenean communities infecting freshwater fish in the northern Holarctic are variable and often impoverished. This is a result of extinctions during periods of glaciation when the host fishes experienced range contraction. Fish species recolonised northern Europe by one of three routes; stenohaline fishes recolonised from the Black Sea basin via Danube-Rhine or Dnieper-Dniester-Vistula connections. These fish retain complex rich monogenean faunas with numerous species of Dactylogyrus and Paradiplozoon. Anadromous fishes, recolonising via marine migrations along the coast, and cold-water fishes surviving in refugia close to the ice sheets, have impoverished monogenean faunas, characterised by gyrodactylid and ancyrocephalid species. However, there may be great complexity, due to the evolution of new host-parasite interactions within specific watersheds before, during and after the Last Glacial Maximum (LGM). This is demonstrated using examples from the sticklebacks (Gasterosteus aculeatus) and the bullheads (Cottus gobio). Finally, the evolution of Gyrodactylus salaris from a clade of G. thymalli is described, and the role of glaciation in stimulating the evolution of numerous clades of the latter is discussed. This latter example represents a unique opportunity to study speciation by host shift in real time.