Population regulation in Gyrodactylus salaris – Atlantic salmon (Salmo salar L.) interactions: testing the paradigm
© Ramírez et al. 2015
Received: 3 December 2014
Accepted: 1 July 2015
Published: 25 July 2015
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.
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.
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.
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.
The monogenean Gyrodactylus salaris Malmberg, 1957 has been an important pathogen of juvenile freshwater stages of Atlantic salmon, Salmo salar L. in Norway since the 1970s, when it is thought to have been introduced from the Baltic region . An early conclusion was that, following the introduction of this parasite, Norwegian (Eastern Atlantic) salmon stocks were especially susceptible due to a lack of co-adaptative evolutionary experience of G. salaris, contrary to Baltic salmon stocks . This hypothesis has been repeated, with numerous studies comparing parasite performance on different salmon stocks and other salmonids, generating one of the largest available data sets using a common garden experimental approach to examine host specificity of a metazoan parasite infecting vertebrates. Studies with other gyrodactylid-host systems have shown that parasite infra-populations grow rapidly to a peak, followed by decline and eventual elimination [3–14], a pattern interpreted as exponential increase before induction of immunity after a short period of recognition and activation [15–19]. The continuous growth of G. salaris on susceptible Norwegian salmon was therefore interpreted as evidence of impaired immunity , despite earlier suggestions that even on these fish, parasite population growth rates could decline throughout infection . The resulting ‘Atlantic susceptible, Baltic resistant’ paradigm has become firmly entrenched. Resistance to G. salaris has been described as the ‘most convincing example of adaptive variation leading to local adaptation in Atlantic salmon’ , while Peeler et al.  consider this parasite to be the greatest threat posed to susceptible Eastern Atlantic salmon stocks in the UK. At a practical level, the paradigm has driven the rotenone eradication campaign in Norway, which has been applied to both infected rivers and large lake systems, and the costly surveillance and public education programmes implemented in many other northern European nations such as Scotland .
An assumption of all previous experimental work has been that differences between fish and fish stocks have an underlying genetic cause [2, 5, 7, 11, 25–27] and that the common garden methodology with isolated hosts can detect this . Indeed, this assumption of a genetic basis to susceptibility/resistance is fundamental to the concept of local adaptation to parasites . Studies with gyrodactylids have, however, all used a frequentist (mean variance) statistical framework in which it is difficult to identify phenotypic differences in host susceptibility between individuals, which may correlate with genotype. In particular, the auto-correlative nature of gyrodactylid population growth, and small differences between hosts in the timing of parasite population growth have major effects on the outcome of infections , which cannot be captured by frequentist methodologies. At the same time, a key issue with the common garden approach is the nature of experimental replication . In the case of Gyrodactylus, most published studies consist of single studies with fish infected simultaneously in a single laboratory. There are no published studies replicating susceptibility trials in space and time, which could allow realistic estimation of genuine genetic stock effects as opposed to experimental, environmental replicate effects. In this paper we therefore set out to re-evaluate the corpus of data on common garden experiments, some unpublished, using G. salaris on different Atlantic salmon stocks performed since the late 1980s, carried out by researchers from the Natural History Museum Oslo (NHMO). We applied a Bayesian statistical methodology to avoid the pitfalls of the frequentist analytical approach used in the original papers, and we included datasets featuring the same salmon stock infected at different times under different conditions to allow appraisal of stock replicability. We were especially interested in establishing (a) whether there is any time-dependent limitation of gyrodactylid population growth consistent with an immune response; and (b), whether any density-dependent regulation of parasite population growth can be detected. In particular, we focused on the differences between salmon stocks from Scotland and Fennoscandia to determine whether the ‘Atlantic susceptible, Baltic resistant’ paradigm of resistance to G. salaris can be sustained as the ‘most convincing example of adaptive variation leading to local adaptation in Atlantic salmon’.
Infection experiments and parasite strains
Overview of the experimental data-sets analysed
Date of experiments
Parasite strain and haplotype [ ]
Length of experiment (days)
Number of fish used
Initial parasite load
Max parasite load
Loneelva single worm
Neva single worm
Three approaches to infection were followed. In the earliest experiments fish were infected by allowing them to swim with infected donor fish before separation into the individual enclosures, after which fish were anaesthetised once per week using 0.04 % chlorbutanol and all parasites were counted. This approach resulted in considerable variation in the initial parasite inoculum, and so in later experiments fish were allowed to swim for 24 hours amongst heavily infected fins clipped from previously killed donors. With experience, manipulation of the number of parasites added resulted in relatively consistent initial inocula. Finally, for experiments with specified starting inocula (e.g. single worm infections), individual worms were manipulated from a donor onto insect pins and then transferred onto a fin of an anaesthetised experimental host. When the appropriate number of worms had been added, the experimental fish was returned to the individual enclosure, and was checked after 24 hours to ensure that the worm or worms had attached and not been lost. Infections were continued for variable periods (determined pragmatically depending on the initial burden and the extent of pathogenicity observed), and infection levels were examined at 7 day intervals. These methods have been reported more fully in the accounts of the individual experiments [2, 26, 27, 32, 33], and are summarised in Table 1.
Statistical analyses and Bayesian models of gyrodactylid population growth
Fit of Bayesian models for exponential, time-dependent and density-dependent gyrodactylid population growth to experimental data-sets
Time- dependent model
Loneelva single worm
DIC – 4.452
Failed to converge
Failed to converge
Failed to converge
Failed to converge
Failed to converge
Failed to converge
Failed to converge
Failed to converge
Failed to converge
Neva single worm
Failed to converge
Failed to converge
Failed to converge
Failed to converge
Population growth rate~age of infection (Days) * stock * lon(initial population size)
The model was simplified with the step function in R, using comparisons of the Akaike Information Criterion (AIC) provided to establish minimum sufficient models.
Rates of parasite population growth rate were calculated for all twelve stocks using the time-dependent model of population growth, whereby the rate of growth (r) declines by a constant daily increment from the maximum achieved at the beginning of the experiment. Comparison of replicated stocks (Additional file 1), and of different stocks analysed under identical conditions in the same aquarium at the same time (datasets F, G and L at Vikan VESO; datasets Bi and Bii at NHMO; datasets D and K, NHMO; datasets M and O, NHMO, see Table 1) give confidence that the initial (maximal) population growth rates of G. salaris are a valid measure of genetic differences between the fish stocks used, and make possible comparisons between stocks even when these were carried out at different times. The remaining variation observed was environmental, due to stochasticity in growth rates in small populations and to a significant effect of parasite inoculum on the initial population growth rate.
Within stock effects
Stochasticity in small parasite populations
Density-dependence at the beginning of the infection
Factors influencing gyrodactylid population growth
Sum of squares
% variance accounted for
Age of infection
2 × 10-16
2 × 10-16
2 × 10-10
First order interactions
Age of infection: stock
2 × 10-16
Age of infection: initial inoculum
Stock: initial inoculum
1.8 × 10-6
Second order interactions
Age of infection: stock: initial inoculum
Residual (Unaccounted) variance
For each host stock, a frequency distribution of parasite population growth rates were observed following fitting of the Bayesian time-dependent model. These frequency distributions contribute to a spectrum, with the fishes supporting the lowest parasite population growth rates observed in the Norwegian Akerselva stock, while the Baltic Indalsälv stock included fishes supporting growth rates overlapping those seen in Norwegian stocks. The frequency distribution of parasite population growth rates in the Akerselva salmon stock (Fig. 4b) has a wider range than that of other fish stocks, and shows some tendency to be polymodal.
This study represents the largest re-analysis of the growth dynamics of Gyrodactylus salaris on different Atlantic salmon stocks since the beginning of the epidemic in Norway in the mid-1970s. Prior to this study, the susceptibility of only six wild Norwegian [2, 21, 25–27, 32], two Baltic [2, 33] and two Scottish  salmon stocks had been published using the isolated, single fish, common garden methodology, a number of other Baltic and eastern Atlantic stocks have also been compared in complex multi-host arenas [38–40], and other stocks have been tested but the results remain unpublished. To place this in context, the epidemic in Norway has affected 44 rivers  out of 200+ rivers which support commercially and conservationally important salmon stocks, and so less than 10 % of Norwegian salmon stocks have been tested for their response to G. salaris; even with this re-analysis, the majority of stocks, in Norway and elsewhere, remain untested.
Remarkably, all but one dataset reanalysed here with Bayesian growth models showed strong support for time-limitation of parasite population growth rate, implying immunological response, and none, even amongst the Norwegian datasets, support prolonged exponential population growth by G. salaris. This is a similar conclusion to that reached by a smaller, non-Bayesian comparison of salmon stocks . We can say unequivocally that unlimited population growth of G. salaris does not occur on Norwegian Atlantic salmon stocks, contrary to the widely held view of this interaction . Instead, parasite population growth is limited by a complex interaction of declining population growth rates as the infection progresses, a density-dependent effect of parasite inoculum on initial (maximal) population growth rates, and stochastic effects limiting growth in small parasite populations . The dependence of growth rate on infection age implies a common mechanism of parasite population regulation in Baltic and East Atlantic salmon stocks, contrary to the paradigm that ‘severe disease represents a lack of co-adaptation between the host and parasite’ . In fact both Norwegian and Baltic salmon seem equally able to limit G. salaris population growth, as the rate of decline in the parasite growth rate is similar in fish stocks from both regions. The key difference is that initial parasite population growth rate is much higher on highly susceptible stocks. Nevertheless, even this statement must be interpreted with caution; to some extent, all salmon stocks show overlap in parasite population growth rates (Fig. 4), and the lowest initial rates were observed on individuals of the Norwegian Akerselva stock.
Previous interpretations of gyrodactylid population biology recognise exponential increase before an immune response eliminates parasites [15–19], and it is usually assumed that sterile immunity results , although this runs counter to observation, and has led various authors to postulate a ‘refractory period’, after which the fish once more becomes susceptible in the absence of further challenge [3, 9, 41]. The growth of G. salaris on Norwegian salmon stocks, is considered evidence of an impaired immune response . The current work, however, suggests that G. salaris - Atlantic salmon interactions can be modelled conceptually in a different way. We envisage a maximum initial growth rate, set by host phenotype (including genetic and environmental components), which is reduced by a daily increment and will eventually become negative, leading to a decline in parasite population size. If the initial inoculum is large, initial parasite population growth rate may be limited in a density-dependent manner. On Neva fish, the initial growth rate is sufficiently low that population growth becomes negative after 10–30 days, and stochastic effects may dominate the interaction and maintain parasite populations at a very small size for considerable periods. Indeed, demographic stochasticity may play an important part in regulating gyrodactylid population growth when growth rates are very low; it is certainly likely to be important for example in maintaining prevalence and intensity of the Pålsbufjorden strain of G. salaris at very low levels on Arctic Charr [25, 32], and could represent a dominant form of population regulation in natural gyrodactylid populations. On Norwegian stocks supporting a higher initial growth rate, population growth remains positive for 40–50 days, and a decline in the infrapopulations is not often seen because fish death intervenes; on intermediate stocks such as the Norwegian Lierelva or the Scottish Conon stocks, host survival is such that parasite population growth rate does become negative, and the parasite population begins to decline, a fact noted in the original study by Bakke and Mackenzie .
In natural populations, the response to gyrodactylids is complex; most fish remain infected even though, given their age and history of exposure, they should have responded to infection [8, 14, 42, 43]. This is actually the case for G. salaris, at least in Southern Norway, where in the Lierelva River most infected fish carried declining parasite populations by midsummer [44, 45], in line with predictions of a 50 day threshold before parasite population growth rates become negative in this stock. Non-sterile immunity is characteristic of gyrodactylids, and a model of the immune response, which limits parasite population growth, but does not necessarily eliminate the Gyrodactylus population entirely, is more realistic than the rather crude search for ‘resistance genes’ which has been undertaken to date [46, 47]. The reanalyses presented here suggest that immune activation after a lag phase does not take place, and that the response is apparent from the earliest stages of the infection. This strongly argues against a specific response in favour of expression of a non-specific effector, capable of pattern recognition and response, similar perhaps (but not exclusive to) to alternate pathway complement activation against gyrodactylids [48, 49]. When parasite challenge is low, expression of the response declines and the fish become phenotypically more susceptible; when the parasite challenge is high, expression increases, reducing susceptibility, but at no point does the fish become entirely refractory, and neither does it lose all resistance if challenge ends. This owes much more to the model of the gyrodactylid host interaction of Lester and Adams  than it does to the compartmentalisation of fish as naïve, infected or refractory , based on immune processes in tetrapods, or to the unrealistic expectations of sterile immunity seen in the veterinary and fish health literature [15, 17–19, 47].
In all stocks tested, a spectrum of initial parasite population growth rates was observed. Trials using the same fish stock conducted several years apart showed sufficient repeatability, while results with different stocks at the same time in the same facility were sufficiently different to consider that observed stock differences were not artefacts. This also strongly argues the case for a host genetic component influencing parasite population growth characteristics, and allows a quantitative genetic approach to be adopted. In most cases, initial parasite population growth rates follow a unimodal distribution (Fig. 4), suggesting complex polygenic control of susceptibility, but in the Akerselva stock, and to some degree in the Indalsälv stock, initial growth rates were polymodal and suggestive of an additive genetic basis for parasite population growth, similar to that noted by Madhavi and Anderson  for guppies infected with G. turnbulli. The Akerselva dataset is most striking; this included two fish which sustained parasite population growth rates similar to those seen in the most susceptible northern and western Norwegian stocks, but it also included fishes supporting the lowest growth rates ever noted, lower even than those seen in Baltic stocks. It is not clear why these extreme individuals were not observed in other fish stocks, and it may be relevant that the Akerselva study was composed of fry and alevins rather than parr, or that the Akerselva has a history of introduction, including Baltic Neva fishes . Equally however, the Akerselva study represented the largest group of fish analysed in the present work (100 fish), and it may simply require samples of this size to reveal the full range of phenotypes present in a fish stock.
The original host phylogeographic hypothesis, based on protein allozyme electrophoresis  and RFLP analysis of mitochondrial DNA , suggested that the Atlantic salmon is broadly distributed into three major races (West Atlantic, East Atlantic and Baltic), and the first experimental study of G. salaris population growth on individually isolated fish included the Norwegian Loneelva stock and a Baltic salmon stock from the Russian river Neva . The ability of the Neva stock to control their infections supported the paradigm of a resistant Baltic salmon race, which have long prior evolutionary experience of the parasite, and of a susceptible, previously unexposed East Atlantic race (see [1, 21]). We found no evidence supporting the partitioning of resistance / susceptibility between salmon stocks according to phylogeographic hypotheses. Differences in G. salaris population growth rate cannot be predicted based on a partitioning of stocks between East Atlantic and Baltic salmon races (the Bakke et al.  hypothesis), or between the three geographical areas considered in this work, Norway, Scotland and the Baltic. The diversity of G. salaris growth rates on different stocks most strongly support the view central to conservation of the species, that the Atlantic salmon comprises multiple, genetically differentiated and reproductively isolated, populations within, as well as between, major river systems [51, 53–55]. At the same time, the results reject local adaptation in response to parasite selective pressure; the heterogeneity of parasite growth rates on Norwegian and Scottish salmon stocks, and especially the relatively low growth rates supported by South-eastern Norwegian stocks, which according to the paradigm have no prior experience of the parasite, argues strongly against local adaptation specifically to G. salaris. It could be that local adaptation takes place in response to locally distributed disease syndromes, and that for example the Scottish Conon stock supports low growth of G. salaris because of prior evolutionary experience of other pathogens. In fact, most Atlantic salmon stocks have evolutionary experience of gyrodactylids; Gyrodactyloides bychowskii Albova, 1948 is present in the marine phase , infections with Gyrodactylus derjavinoides Malmberg et al., 2007 or G. teuchis Cunningham et al., 2001 are frequent in rivers containing brown trout [57, 58] and when surveyed, 50 % of Scottish salmon populations were infected with either G. derjavinoides or G. caledoniensis Shinn et al., 1995 . The poor performance on Norwegian South-eastern stocks may reflect past experience of G. salaris, as this region is relatively close to the current northern limit of the natural range, or genetic exchange with salmon stocks from rivers historically infected with G. salaris along the Swedish west coast. This may therefore have conferred some degree of resistance into salmon from the South-eastern Norwegian rivers.
The current Bayesian analysis shows that the control of G. salaris infrapopulation growth is complex, involving stochasticity, time-dependence, and density-dependence limiting population growth on fish receiving the largest inocula. These features are present even in fish stocks with no recent evolutionary experience of the parasite, suggesting that they are common to all S. salar stocks. A spectrum of phenotypes is present, and is shaped by natural selection, either in response to Gyrodactylus infection, or to proxy infections. However, we find no evidence to support the ‘Baltic resistant, Norwegian susceptible’ paradigm which has come to dominate this topic, and rather note that some South-eastern Norwegian salmon stocks, with no evolutionary experience of the parasite, are at least as resistant as some Baltic salmon stocks which are thought to have co-evolved with G. salaris.
This work was supported by the Research Council of Norway’s “Miljø2015 Vann” grant 196420/S30. The experimental laboratory research at “Avdeling for Forsøksdyr” nr. 166, UiO, Natural History Museum, using live fish was performed in accordance with “Lov om dyrevelferd”, Norwegian Ministry of Agriculture and Food. The experiments related to the “Miljø2015 Vann” grant were approved by the Norwegian Animal Research Authority (Forsøksdyrutvalget, FDU), licence ID Saksnr. 2012/279509.
- Bakke TA, Cable J, Harris PD. The biology of gyrodactylid monogeneans: the “Russian doll-killers”. Adv Parasitol. 2007;64:278–9.Google Scholar
- Bakke TA, Jansen PA, Hansen LP. Differences in the host resistance of Atlantic salmon, Salmo salar L., stocks to the monogenean Gyrodactylus salaris Malmberg, 1957. J Fish Biol. 1990;37:577–87.View ArticleGoogle Scholar
- Lester RJG, Adams JR. A simple model of a Gyrodactylus population. Int J Parasitol. 1974;4:497–506.PubMedView ArticleGoogle Scholar
- Cusack R. Development of infections of Gyrodactylus colemanensis Mizelle and Kritsky, 1967 (Monogenea) and the effect on fry of Salmo gairdneri Richardson. J Parasitol. 1986;72:663–8.PubMedView ArticleGoogle Scholar
- Bakke TA, Jansen PA, Harris PD. Differences in susceptibility of anadromous and resident stocks of Arctic charr to infections of Gyrodactylus salaris under experimental conditions. J Fish Biol. 1996;49:341–51.Google Scholar
- Sterud E, Mo TA, Collins CM, Cunningham CO. The use of host specificity, pathogenicity and molecular markers to differentiate between Gyrodactylus salaris Malmberg, 1957 and Gyrodactylus thymalli Zitnan, 1960 (Monogenea, Gyrodactylidae). Parasitology. 2002;124:203–13.PubMedView ArticleGoogle Scholar
- Bakke TA, Jansen PA, Kennedy CR. The host specificity of Gyrodactylus salaris Malmberg (Platyhelminthes, Monogenea): the susceptibility of Oncorhynchus mykiss (Walbaum) under experimental conditions. J Fish Biol. 1991;39:45–57.View ArticleGoogle Scholar
- Scott ME, Robinson MA. Challenge infections of Gyrodactylus bullatarudis (Monogenea) on guppies, Poecilia reticulata (Peters), following treatment. J Fish Biol. 1984;24:581–6.View ArticleGoogle Scholar
- Madhavi R, Anderson RM. Variability in the susceptibility of the fish host, Poecilia reticulata, to infection with Gyrodactylus bullatarudis (Monogenea). Parasitology. 1985;91:531–44.View ArticleGoogle Scholar
- Scott ME. Dynamics of challenge infections of Gyrodactylus bullatarudis Turnbull (Monogenea) on guppies, Poecilia reticulata (Peters). J Fish Dis. 1985;8:495–503.View ArticleGoogle Scholar
- Bakke TA, Harris PD, Jansen PA. The susceptibility of Salvelinus fontinalis (Mitchell) to Gyrodactylus salaris Malmberg (Platyhelminthes; Monogenea) under experimental conditions. J Fish Biol. 1992;41:499–507.View ArticleGoogle Scholar
- Richards GR, Chubb JC. Host response to initial and challenge infections, following treatment, of Gyrodactylus bullatarudis and G. turnbulli (Monogenea) on the guppy (Poecilia reticulata). Parasitol Res. 1996;82:242–7.PubMedView ArticleGoogle Scholar
- De Roij J, Harris PD, MacColl ADC. Divergent resistance to a monogenean flatworm amongst three-spined stickleback populations. Funct Ecol. 2011;25:217–26.View ArticleGoogle Scholar
- Raeymaekers JAM, Wegner M, Huyse T, Volkaert FAM. Infection dynamics of the monogenean parasite Gyrodactylus gasterostei on sympatric and allopatric populations of the three spined stickleback Gasterosteus aculeatus. Folia Parasitol. 2011;58:27–34.PubMedView ArticleGoogle Scholar
- Buchmann K. Immune mechanisms in fish skin against monogeneans – a model. Folia Parasit. 1999;46:1–9.Google Scholar
- Buchmann K, Lindenstrøm T. Interactions between monogenean parasites and their fish hosts. Int J Parasitol. 2002;32:309–19.PubMedView ArticleGoogle Scholar
- Lindenstrøm T, Buchmann K, Secombes CJ. Gyrodactylus derjavini infection elicits IL-1ß expression in rainbow trout skin. Fish Shellfish Immun. 2003;15:107–15.View ArticleGoogle Scholar
- Lindenstrøm T, Secombes CJ, Buchmann K. Expression of immune response genes in rainbow trout skin induced by Gyrodactylus derjavini infections. Vet Immunol Immunop. 2004;97:137–48.View ArticleGoogle Scholar
- Lindenstrøm T, Sigh J, Dalgaard MB, Buchmann K. Skin expression of IL-1 beta in East Atlantic salmon, Salmo salar L., highly susceptible to Gyrodactylus salaris infection enhanced compared to low susceptibility Baltic stock. J Fish Dis. 2006;29:123–8.PubMedView ArticleGoogle Scholar
- Johnsen BO, Jensen AJ. Infestations of Atlantic salmon, Salmo salar, by Gyrodactylus salaris in Norwegian rivers. J Fish Biol. 1986;29:233–41.View ArticleGoogle Scholar
- Bakke TA, Harris PD, Cable J. Host-specificity dynamics: observations on gyrodactylid monogeneans. Int J Parasitol. 2002;32:281–308.PubMedView ArticleGoogle Scholar
- Garcia De Leaniz C, Fleming IA, Einum S, Verspoor E, Jordan WC, Consuegra S, et al. A critical review of adaptive genetic variation in Atlantic salmon: implications for conservation. Biol Rev. 2007;82:173–211.PubMedView ArticleGoogle Scholar
- Peeler EJ, Gardiner R, Thrush MA. Qualitative risk assessment of routes of transmission of the exotic fish parasite Gyrodactylus salaris between river catchments in England and Wales. Prev Vet Med. 2004;64:175–89.PubMedView ArticleGoogle Scholar
- Riddington G, Radford A, Paffrath S, Bostock J, Shinn A. An economic evaluation of the impact of the salmon parasite Gyrodactylus salaris (Gs) should it be introduced into Scotland. In: Summary Report. Edinburgh: Scottish Executive Environment and Rural Affairs Department, St Andrew’s House; 2006.Google Scholar
- Olstad K, Robertsen G, Bachmann L, Bakke TA. Variation in host preference within Gyrodactylus salaris (Monogenea): an experimental approach. Parasitology. 2007;134:589–97.PubMedView ArticleGoogle Scholar
- Bakke TA, MacKenzie K. Comparative susceptibility of native Scottish and Norwegian stocks of Atlantic salmon, Salmo salar L., to Gyrodactylus salaris Malmberg: Laboratory experiments. Fish Res. 1993;17:69–85.View ArticleGoogle Scholar
- Bakke TA, Soleng A, Harris PD. The susceptibility of Atlantic salmon (Salmo salar L.) x brown trout (Salmo trutta L.) hybrids to Gyrodactylus salaris Malmberg and Gyrodactylus derjavini Mikailov. Parasitology. 1999;119:467–81.PubMedView ArticleGoogle Scholar
- Kawecki TJ, Ebert D. Conceptual issues in local adaptation. Ecol letters. 2004;7:1225–41.View ArticleGoogle Scholar
- Ramírez R, Harris PD, Bakke TA. An agent-based modelling approach to estimate error in gyrodactylid population growth. Int J Parasitol. 2012;42:809–17.PubMedView ArticleGoogle Scholar
- Crabbe JC, Wahlsten D, Dudek BC. Environment Genetics of Mouse Behavior: Interactions with Laboratory. Science. 1999;284:1670.PubMedView ArticleGoogle Scholar
- Hansen H, Bachmann L, Bakke TA. Mitochondrial DNA variation of Gyrodactylus spp. (Monogenea, Gyrodactylidae) populations infecting Atlantic salmon, grayling and rainbow trout in Norway and Sweden. Int J Parasitol. 2003;33:1471–8.PubMedView ArticleGoogle Scholar
- Ramírez R, Harris PD, Bakke TA. Same barcode, different biology: differential patterns of infectivity, specificity and pathogenicity in two almost identical parasite strains. Int J Parasitol. 2014;44:543–9.PubMedView ArticleGoogle Scholar
- Bakke TA, Harris PD, Hansen H, Cable J, Hansen LP. Susceptibility of Baltic and East Atlantic salmon Salmo salar stocks to Gyrodactylus salaris (Monogenea). Dis Aquat Org. 2004;58:171–7.PubMedView ArticleGoogle Scholar
- Gelfand AE, Hills SE, Racine-Poon A, Smith AFM. Illustration of Bayesian inference in Normal data models using Gibbs sampling. J Am Stat Assoc. 1990;85:972–85.View ArticleGoogle Scholar
- Lunn DJ, Thomas A, Best N, Spiegelhalter D. WinBUGS- A Bayesian modelling framework: Concepts, structure and extensibility. Stat Comput. 2000;10:325–37.View ArticleGoogle Scholar
- Lunn D, Jackson C, Best N, Thomas A, Spiegelhalter D. The BUGS book: a practical introduction to Bayesian analysis. Boca Raton, FL: CRC press; 2012.Google Scholar
- R Development Core Team: R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria 2011. ISBN 3-900051-07-0, URL http://www.R-project.org.
- Dalgaard MB, Nielsen CV, Buchmann K. Comparative susceptibility of two races of Salmo salar (Baltic Lule river and Atlantic Conon river strains) to infection with Gyrodactylus salaris. Dis Aquat Org. 2003;53:173–6.PubMedView ArticleGoogle Scholar
- Heinecke RD, Martinussen T, Buchmann K. Microhabitat selection of Gyrodactylus salaris Malmberg on different salmonids. J Fish Dis. 2007;30:733–43.PubMedView ArticleGoogle Scholar
- Jørgensen TR, Larsen TB, Jørgensen LG, Bresciani J, Kania PW, Buchmann K. Characterisation of a low pathogenic form of Gyrodactylus salaris from rainbow trout. Dis Aquat Org. 2007;73:235–44.PubMedView ArticleGoogle Scholar
- Scott ME, Anderson RM. The population dynamics of Gyrodactylus bullatarudis (Monogenea) within laboratory populations of the fish host Poecilia reticulata. Parasitology. 1984;89:159–94.PubMedView ArticleGoogle Scholar
- Harris PD, Lyles AM. Infections of Gyrodactylus bullatarudis and Gyrodactylus turnbulli on Guppies (Poecilia reticulata) in Trinidad. J Parasitol. 1992;78:912–4.PubMedView ArticleGoogle Scholar
- Cable J, van Oosterhout C. The role of innate and acquired resistance in two natural populations of guppies (Poecilia reticulata) infected with the ectoparasite Gyrodactylus turnbulli. Biol J Linn Soc. 2007;90:647–55.View ArticleGoogle Scholar
- Jansen PA, Bakke TA. Regulatory processes in the monogenean Gyrodactylus salaris Malmberg - Atlantic salmon (Salmo salar L.) association: I. Field studies in South-east Norway. Fish Res. 1993;17:87–101.View ArticleGoogle Scholar
- Jansen PA, Bakke TA. Regulatory processes in the monogenean Gyrodactylus salaris Malmberg - Atlantic salmon (Salmo salar L.) association: II. Experimental studies. Fish Res. 1993;17:103–14.View ArticleGoogle Scholar
- Gilbey J, Verspoor E, Mo TA, Sterud E, Olstad K, Hytterød S, et al. Identification of genetic markers associated with Gyrodactylus salaris resistance in Atlantic salmon Salmo salar. Dis Aquat Org. 2006;71:119–29.PubMedView ArticleGoogle Scholar
- Matejusová I, Felix B, Sorsa-Leslie T, Gilbey J, Noble LR, Jones CS, et al. Gene expression profiles of some immune relevant genes from skin of susceptible and responding Atlantic salmon (Salmo salar L.) infected with Gyrodactylus salaris (Monogenea) revealed by suppressive subtractive hybridisation. Int J Parasitol. 2006;36:1175–83.PubMedView ArticleGoogle Scholar
- Buchmann K. Binding and lethal effect of complement from Oncorhynchus mykiss on Gyrodactylus derjavini (Platyhelminthes: Monogenea). Dis Aquat Org. 1998;32:195–200.PubMedView ArticleGoogle Scholar
- Harris PD, Soleng A, Bakke TA. Killing of Gyrodactylus salaris (Platyhelminthes, Monogenea) mediated by host compliment. Parasitology. 1998;117:137–43.PubMedView ArticleGoogle Scholar
- Hansen LP, Jonsson B. Restocking the river Akerselv, Oslo with Atlantic salmon smolts Salmo salar L. of different stocks. Fauna norv Ser A. 1990;11:9–15.Google Scholar
- Ståhl G. Genetic population structure of Atlantic salmon. In: Ryman N, Utter F, editors. Population genetics and fishery management. Seattle: University of Washington Press; 1987. p. 121–40.Google Scholar
- Verspoor E, McCarthy EM, Knox D, Bourke EA, Cross TF. The phylogeography of European Atlantic salmon (Salmo salar L.) based on RFLP analysis of the ND1/16S RNA region of the mtDNA. Biol J Linn Soc. 1999;68:129–46.View ArticleGoogle Scholar
- Verspoor E. Genetic Diversity among Atlantic salmon (Salmo salar L.) populations. ICES J Mar Sci. 1997;54:965–73.Google Scholar
- Verspoor E, Stradmeyer L, Nielsen JL. The Atlantic Salmon: Genetics, Conservation and Management. Oxford: Blackwell Publishing Ltd; 2007.View ArticleGoogle Scholar
- Hindar K, Hutchings J, Diserud O, Fiske P, Aas O, Einum S, et al. Stock, Recruitment and Exploitation. In: Atlantic salmon ecology. Oxford: Blackwell Publishing; 2011. p. 221–52.Google Scholar
- Bruno DW, Collins CM, Cunningham CO, MacKenzie K. Gyrodactyloides bychowskii (Monogenea: Gyrodactylidae) from sea-caged Atlantic salmon Salmo salar in Scotland: occurrence and ribosomal RNA sequence analysis. Dis Aquat Org. 2001;45:191–6.PubMedView ArticleGoogle Scholar
- Mo TA. Seasonal occurrence of Gyrodactylus derjavini (Monogenea) on brown trout, Salmo trutta, and Atlantic salmon, S. salar, in the Sandvikselva river, Norway. J Parasitol. 1997;83:1025–9.PubMedView ArticleGoogle Scholar
- Cunningham CO, Mo TA, Collins CM, Buchmann K, Thiery R, Blanc G, et al. Redescription of Gyrodactylus teuchis Lautraite, Blanc, Thiery, Daniel & Vigneulle, 1999 (Monogenea, Gyrodactylidae); a species identified by ribosomal RNA sequence. Sys Parasitol. 2001;48:141–50.View ArticleGoogle Scholar
- Shinn AP, Sommerville C, Gibson DI. Distribution and characterization of species of Gyrodactylus Nordmann, 1832 (Monogenea) parasitising salmonids in the UK, and their discrimination from G. salaris Malmberg, 1957. Sys Parasitol. 1995;29:1383–402.Google Scholar
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