3.2. Sustainable production of healthy fish tackling parasitic threats with knowledge on their ecology

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1 ISBN (pdf) ISSN Sustainable production of healthy fish tackling parasitic threats with knowledge on their ecology Anssi Karvonen, Teija Hakalahti, Otto Seppälä, E. Tellervo Valtonen* Department of Biological and Environmental Science, P.O. Box 35, FI University of Jyväskylä * ( ) Tel: , Fax: INTRODUCTION Modern fish farming conditions with high fish densities and intensive production units provide ideal conditions for the invasion and persistence of a range of pathogens and parasites (bacteria, viruses, protozoan and metazoan parasites). Infections by these disease-causing agents reduce the condition and survival of fish causing economical losses to farmers. This is a large-scale problem in countries such as Finland, where, for instance, most natural salmonid populations are maintained by frequent stocking of farmed fish. Parasitic diseases have traditionally been treated with chemicals and drugs, which in many cases has produced effective results (Rintamäki-Kinnunen 1997; Rintamäki-Kinnunen and Valtonen 1997). However, treatments unavoidably cause problems related to environmental pollution, drug resistance and health issues, which is why environmentally and ecologically sustainable solutions are now being sought in fish farming. Reaching this long-term objective will depend on the detailed information and knowledge on the ecology of main disease threats. In this article, we focus on two metazoan parasite species, Diplostomum eye flukes and Argulus ectoparasites, which are frequently found at fish farms and cause severe losses to farmers. Our purpose is to present results from long-term studies on the life histories and life cycle biology of these parasites. We will also discuss how these results could be applied when designing 1) prevention protocols and 2) epidemiological models to seek ecological and environmentally friendly solutions to these parasite problems. EYE FLUKE INFECTIONS IN CULTURED FISH The digenean parasite Diplostomum spathaceum is a common parasite in the eyes of wild fish species (Valtonen and Gibson 1997). The parasite uses three hosts in its life cycle, which begins with sexual reproduction in the definitive host, a fish-eating bird (Fig. 1). Eggs are released from birds to water where they hatch to miracidia larvae to infect the first intermediate host, a freshwater snail. Infected snails produce cercariae, which penetrate the nearby fish, migrate to the lens of the fish eye and develop to metacercariae. While in the lens, metacercariae cause cataracts (Shariff et al. 1980; Anneli Jalkanen & Pekka Nygren (eds.) Sustainable use of renewable natural resources from principles to practices. University of Helsinki Department of Forest Ecology Publications 34.

2 Karvonen et al. Fig. 1. Life cycle of Diplostomum spathaceum. Karvonen et al. 2004a), which reduces the vision of fish and leads to impaired feeding ability and growth (Crowden and Broom 1980; Owen et al. 1993; Buchmann and Uldal 1994). The life cycle is completed when an infected fish is eaten by the definitive host. Outbreaks of D. spathaceum have also been reported at fish farms (Ferguson and Hayford 1941; Stables and Chappell 1986a; Field and Irwin 1994), where infections cause considerable financial losses. Fish farms provide favourable conditions for the parasite for several reasons. First, outdoor ponds with high nutrient load and primary production maintain high numbers of intermediate snail hosts. Second, constantly high fish densities ensure high cercarial infection rate. Third, easy prey attracts bird hosts to feed on infected fish, which effectively completes the parasite life cycle. Several workers have attempted to find solutions to Diplostomum infections in fish culture. These have included removal of the snail hosts by applying chemicals (Stables and Chappell 1986a) or changing the structure of the farm (Field and Irwin 1994). However, methods have in many cases proven expensive and ineffective. We propose a cost-effective and ecologically friendly method, which utilizes data from detailed experiments and empirical field observations on parasite transmission biology in combination with modern epidemiological modelling. Our purpose is first to quantify the parasite life cycle in detail and then construct a population model that will capture the dynamics of the parasite-host system. This model is to be used in determining optimal ways to control Diplostomum infections at farms in an environmentally and economically viable manner. The following sections present some of the results obtained so far and discuss these results in relation to parasite life cycle and prevention at fish farms. These results, together with results from subsequent experiments, will also form the basis for the model parameter estimation. 2

3 Sustainable production of healthy fish 3 Log (Number alive +1 ) Age of cercariae (hours) 40 Fig. 2. Survival of Diplostomum spathaceum cercariae at constant temperature (20ºC) as a function of the age of the cercariae. Redrawn using data from Karvonen et al. (2003). Log (Number infecting +1) Age of cercariae (hours) Fig. 3. Infectivity of Diplostomum spathaceum cercariae to rainbow trout as a function of the age of the cercariae. Redrawn using data from Karvonen et al. (2003). Transmission to fish Development of cercariae within the snail host takes 4-10 weeks depending on the water temperature (Chappell et al. 1994), after which they are released to water. In natural conditions, cercariae face highly unpredictable environment in terms of host contact probability. This is because the infection is determined principally by movements of the fish hosts (Höglund 1995; Karvonen et al. 2003) i.e. cercariae do not seek out the host. Cercariae are also diluted to large water volume decreasing the contact rate with the host. Cercarial survival rate is also low; in 20 ºC they die within 36 hours (Karvonen et al. 2003; Fig. 2). Infectivity is lost even faster (Karvonen et al. 2003; Fig. 3), probably because of the utilisation of limited glycogen energy reserves. However, to counterbalance the uncertainty of transmission, tens of thousands of cercariae are released from a single snail per day for several weeks, although this is characterised by great variation between individual snails (Karvonen et al. 2004b; Fig. 4). This is likely to increase contacts with the fish host in nature, but also to cause problems at fish farms, where the contact rate becomes unnaturally high because of high fish density. Responses in fish Vertebrates such as fish generally have two lines of immunological defence: innate, unspecific immunity, which attacks all invading pathogens and acquired, specific 3

4 Karvonen et al. Cercariae per day Days before host death Fig. 4. Daily cercariae production of Diplostomum spathaceum from two individual snails kept at constant room temperature until the death of the snails. Drawn using data from Karvonen et al. (2004b). immunity, which is activated after the first encounter with a particular pathogen (Manning 1994). Uncertainty of the cercarial transmission process (see above) suggests that cercariae in natural conditions should be highly infectious once they become in contact with a fish. Indeed, immunologically naïve rainbow trout (i.e. fish without previous experience of D. spathaceum) are highly susceptible to infection (Karvonen et al. 2005). This confirms the high infectivity of the cercariae but also suggest that innate immunity has a minor role in protecting the fish against D. spathaceum. However, fish acquire resistance following an exposure to the parasite both in laboratory and natural conditions (Bortz et al. 1984; Stables and Chappell 1986b; Whyte et al. 1987, 1989, 1990; Höglund and Thuvander 1990; Karvonen et al. 2004c). This acquired immunity reduces the number of establishing parasites by almost 90 % in subsequent exposures (Karvonen et al. 2005). However, some parasites are still able to establish and the effect of these parasites on the host ultimately determines the general efficiency of immune system in protecting the fish against the parasite. Our experiments in natural exposure conditions have shown that acquired resistance does not provide sufficient protection (Karvonen et al. 2004d). However, fish also avoid the cercariae by escaping, which suggests that fish use a combination of physiological and behavioural defences against the parasite. Effects on fish Once cercariae become established in the lens and develop to metacercariae, they excrete metabolites to the lens, which leads to the formation of parasite-induced cataracts in an intensity-dependent manner (Karvonen et al. 2004a). This affects the vision of fish impairing the feeding ability and growth (Crowden and Broom 1980; Owen et al. 1993; Buchmann and Uldal 1994). It has also been assumed that the parasite increases the vulnerability of fish to predation, especially by the definitive avian host, but this has not yet been experimentally verified. Studies have shown that infected fish are located closer to the water surface (Crowden and Broom 1980), which might increase their susceptibility to bird predation. However, in our studies, no difference in swimming depth was found between infected and uninfected fish (Seppälä et al. 2004; Fig. 5). Instead, we found that infected fish had impaired ability to respond to approaching predators (Seppälä et al. 2004; Fig. 6). Predation experiments using simulated bird predation indicated that infected fish were significantly more susceptible to predation (Seppälä et al. 2004) suggesting that the parasite infection may have 4

5 Sustainable production of healthy fish Fig. 5. Average movements of infected ( ; N = 4) and control fish ( ; N = 8) into the water column of two meters + SE. Redrawn using data from Seppälä et al. (2004). Fig. 6. Average movements of infected and control fish into deeper water layers ± SE following disturbances made above them by an artificial surface predator. Redrawn using data from Seppälä et al. (2004). important implications for the survival of fish at farms and after stocking to natural conditions. The model One of the most important concepts in epidemiology is the basic reproductive ratio of a parasite, R 0, which is defined for macroparasites as the number of new female parasites produced by a single female in a completely susceptible host population where density dependent constraints are not operating (Anderson and May 1991; Hudson et al. 2002). Clearly, parasite can only persist if R 0 > 1 and the purpose of the D. spathaceum population model is to identify the key steps in the parasite life cycle that could be manipulated to suppress R 0 below 1. In practice this could mean that by removing some specific proportion of the host population, estimated from the model dynamics, the control of the parasite could be achieved with lower costs. A preliminary working model has already been produced, based on the models of Anderson and May (1991) and extended to multiple host life cycles by Dobson (1988). In essence, the results described in previous sections and those obtained from further experiments allow an estimation of the important and tangible variables for such a model, and thus can ultimately produce a functional and effective model for the purposes of parasite control in fish culture. 5

6 Karvonen et al. The model is still under construction and this is why no clear, detailed conclusions or suggestions of the preventative actions applicable in fish farming can yet be presented. However, our present results on the intensity-dependent cataract formation suggest that the parasite numbers in fish should be reduced to a known average level to prevent the effects on fish. Our experiments with immunologically naïve and immunised fish indicate that immunised fish are significantly less susceptible to infection and can effectively avoid the parasite if given an opportunity. This could provide one direction for future studies e.g. on the relationships between rearing densities and immunological background of fish. High, long-lasting cercarial output from the snails, however, suggests that solving this parasite problem ultimately requires manipulation of the snail population for which the predictions of the population model become important. THE CASE OF ARGULOSIS Two species of ectoparasitic fish lice cause problems at Finnish fish farms. Argulus coregoni is a specialist species found mainly on salmonids (Shimura 1983), whereas A. foliaceus has been recorded from several species of freshwater fish (e.g. Valtonen et al. 1997). Argulids attach themselves on fish and pierce the skin of the fish using their modified mouthparts. After this, they feed on the fish blood simultaneously releasing toxic anticoagulant substances (Stammer 1959; LaMarre and Cochran 1992). Secondary bacterial and fungal infections invading the puncture sites further weaken the fish and may lead to the death of the fish (Lester and Roubal 1995). Severe Argulus infestations and associated mass mortalities of fish have been reported around the world (Cross and Stott 1974; Shimura 1983; Menezes et al. 1990; Gault et al. 2002; Hakalahti and Valtonen 2003). Traditionally, control measures against argulids have relied on chemical baths, which are laborious and ineffective procedures (Kabata 1970). Surprisingly little effort has been put in developing novel control practices based on the ecology and life cycle biology of the parasite. The aim of this study project has been to develop an ecological control method to counteract Argulus epizootics at fish farms. The seasonal cycle of an Argulus coregoni population on a commercial fish farm Strategic life cycle decisions of parasites in northern latitudes are largely constrained by seasonal variations in temperature. We studied the seasonal cycle of A. coregoni at a fish farm by collecting weekly samples of lice attached to rainbow trout (Oncorhynchus mykiss) (Hakalahti and Valtonen 2003). The results revealed strong seasonality in the life cycle of the parasite. The first newly-hatched A. coregoni were observed on fish in spring, when water temperature exceeded 10 ºC by the end of May (Hakalahti and Valtonen 2003). At this time, adult specimens were not recorded on fish, indicating that A. coregoni survives the winter only as eggs. In contrast, the other species, A. foliaceus, can live through the winter as an inactive juvenile stage, or as an adult on fish (Pasternak et al. 2000; Gault et al. 2002). Interestingly, we found that the recruitment of A. coregoni juveniles from eggs extended until September. However, the population size decreased substantially after the females started to lay their eggs from early July onwards and no peak in recruitment 6

7 Sustainable production of healthy fish Fig. 7. The hatching dynamics of Argulus coregoni eggs in the laboratory. The eggs in group A were kept at constant room temperature; while the eggs in group B were treated 6 times with cooling (2 weeks at 1 o C). The arrows indicate the beginning of each cold treatment. All egg clutches within a treatment are pooled together (Hakalahti et al. 2004a). was observed in autumn, which suggests that only one annual generation thrived (Hakalahti and Valtonen 2003). Extended hatching at the population level may imply that each individual female produces eggs that hatch over an extended period. However, the extended pattern could also arise from genetic variability between females, or from phenotypic plasticity. Fecundity of Argulus coregoni females and hatching dynamics of individual egg clutches Since fish hosts are highly mobile, the availability of hosts is likely to be unpredictable for newly-hatched argulid metanauplii carrying limited sets of resources. High mortality may be compensated by high reproductive effort (Poulin 1988), but natural selection may also favour the development of alternative transmission strategies to reduce the effects of unpredictability in transmission. For instance, individual parasites may hedge their bets by producing offspring with different hatching patterns (Fenton and Hudson 2002). A. coregoni females were bred in the laboratory, individual egg clutches were collected, and their hatching was monitored. The mean reproductive output of A. coregoni females was 317 eggs, and 85% of females laid just a single clutch of eggs before dying. Each female produced offspring that hatched over an extended period, with the mean hatching period of each clutch being 7 months (Hakalahti et al. 2004a). A cold treatment (2 weeks at 1 ºC) triggered the hatching of the eggs, but the extended hatching pattern remained (Hakalahti et al. 2004a; Fig. 7). The results of this study support the predictions of the adaptive bet-hedging strategy in relation to hatching dynamics (Seger and Brockmann 1987; Philippi and Seger 1989). Extended hatching dynamics coupled with the long-term survival (> 2 years) of diapausing A. coregoni eggs (Mikheev et al. 2001) suggest that the development of control methods against argulids should focus on removal and destroying the parasite eggs. 7

8 Karvonen et al. 0.5 m Floats 1.7 m 1.5 m Anchors 0.2 m Fig. 8. Scheme for the positioning of the egg trap in the farming canal. Traps were anchored to the bottom of the canal with bricks, and their positions were marked using floats and ropes attached to bridges dividing the canal in such a way that one of the upper flat surfaces directly faced the direction of the current. Each of the surfaces of the trap was divided into 12 rectangular sections (3 4) of equal size. Redrawn using data from Hakalahti et al. (2004b). Egg laying behaviour - the key to control argulids? Due to harsh over-wintering conditions, the survival of eggs through the winter and subsequent transmission are likely to be key factors limiting the growth of Argulus populations in northern latitudes. As such, the development of control methods to reduce future recruitment and survival rates could be an effective and novel approach to counteract parasite epizootics at fish farms (Gault et al. 2002). This hypothesis was tested by constructing artificial egg laying boards to capture and remove the overwintering eggs from the lice population (Fig. 8). Eight boards were kept in a farming canal for 3.5 months during the reproductive season of the lice (Hakalahti et al. 2004b). These experiments showed that A. coregoni females choose specific type of substrates and microhabitat for egg laying. The spatial distribution of A. coregoni eggs was aggregated, with most eggs collected from deeper habitats within the 2-m-deep farming canal (Hakalahti et al. 2004b; Fig. 9). Moreover, significantly more A. coregoni eggs were laid on dark than on light substrates, suggesting the use of visual cues (Hakalahti et al. 2004b). Although approximately 1.5 million eggs were successfully harvested from the A. coregoni population, marked stones kept as controls near the traps were also covered with egg clutches (Hakalahti et al. 2004b). The results indicate that artificial egg laying boards can be used as an ecological control method against argulids at fish farms. For such traps to be effective, ponds should not contain stones or any other substrate that would attract the parasite females. Boards should also be positioned so that they take account the egg laying strategy of the parasite. CONCLUSIONS Detailed knowledge on the ecology of disease-causing agents forms the basis for sustainable prevention. We have investigated the life cycles of two important parasite species found in the fish culture, Diplostomum spathaceum and Argulus coregoni. 8

9 Sustainable production of healthy fish Fig. 9. Proportion of Argulus coregoni egg clutches collected within each distance measured from the bottom of about 2- m-deep farming canal. Redrawn using data from Hakalahti et al. (2004b). Based on the results on parasite reproduction in snails, patterns of resistance in fish and effects on fish in terms of increased transmission to the definitive hosts, we are currently constructing a population model of the life cycle of D. spathaceum. This model is to be used in estimating optimal solutions to this parasite problem at fish farms. Studies on A. coregoni have determined the population dynamics of the parasite at fish farms and indicated when the use of prevention protocols, such as artificial egg laying substrates, would be most effective. REFERENCES Anderson, R. M. & May, R. M Infectious Diseases of Humans: Dynamics and Control. Oxford University Press, Oxford. Bortz, B. M., Kenny, G. E., Pauley, G. B., Garcia-Ortigoza, E. & Anderson, D. P The immune response in immunized and naturally infected rainbow trout (Salmo gairdneri) to Diplostomum spathaceum as detected by enzyme-linked immunosorbent assay (ELISA). Developmental and Comparative Immunology 8: Buchmann, K. & Uldal, A., Effects of eyefluke infections on the growth of rainbow trout (Oncorhynchus mykiss) in a mariculture system. Bulletin of the European Association of Fish Pathologists 14: Chappell, L. H., Hardie, L. J. & Secombes, C. J Diplostomiasis: the disease and host-parasite interactions. In: Parasitic Diseases of Fish (ed. Pike, A. W. & Lewis, J. W.). Samara Publishing Limited, Dyfed. pp Cross, D. G. & Stott, B The effect of Argulus foliaceus L. on the growth and mortality of a grass carp population. Journal of Institutional Fisheries Management 5: Crowden, A. E. & Broom, D. M Effects of eyefluke, Diplostomum spathaceum, on the behaviour of dace (Leuciscus leuciscus). Animal Behaviour 28:

10 Karvonen et al. Dobson, A The population biology of parasite-induced changes in host behaviour. The Quarterly Review of Biology 63: Fenton, A. & Hudson, P. J Optimal infection strategies: should macroparasites hedge their bets? Oikos 9: Ferguson, M. S. & Hayford, R. A The life history and control of an eye fluke. An account of a serious hatchery disease caused by a parasitic worm. Prog. Fish Cult. 54: Field, J. S. & Irwin, S. W. B The epidemiology, treatment and control of diplostomiasis on a fish farm in Northern Ireland. In: Parasitic diseases of fish. (ed. Pike, A. W. & Lewis, J. W.). Samara Publishing Limited, Dyfed. pp Gault, N. F. S., Kilpatric, D. J. & Steward, M. T Biological control of the fish louse in a rainbow trout fishery. Journal of Fish Biology 60: Hakalahti, T. & Valtonen, E. T Population structure and recruitment of the ectoparasite Argulus coregoni Thorell (Crustacea: Branchiura) on a fish farm. Parasitology 127: , Häkkinen, H. & Valtonen, E. T. 2004a. Ectoparasitic Argulus coregoni (Crustacea: Branchiura) hedge their bets studies on egg hatching dynamics. Oikos 107: , Pasternak, A. F. & Valtonen, E. T. 2004b. Seasonal dynamics of egg laying and egg-laying strategy of the ectoparasite Argulus coregoni (Crustacea: Branchiura). Parasitology 128: Hudson, P. J., Rizzoli, A., Grenfell, B.T., Heesterbeek, H. & Dobson, A. P The Ecology of Wildlife Diseases. Oxford University Press, Oxford. Höglund, J Experiments on second intermediate fish host related cercarial transmission of the eyefluke (Diplostomum spathaceum) into rainbow trout (Oncorhynchus mykiss). Folia Parasitologica 42: & Thuvander, A., Indications of non-specific protective mechanisms in rainbow trout Oncorhynchus mykiss with diplostomosis. Diseases of Aquatic Organisms 8: Kabata, Z. 1970: Diseases of fishes: Book I. Crustacea as enemies of fishes. T.H.F. Publications, New Jersey. Karvonen, A., Paukku, S., Valtonen, E. T. & Hudson, P. J Transmission, infectivity and survival of Diplostomum spathaceum cercariae. Parasitology 127: , Seppälä, O. & Valtonen, E. T. 2004a. Eye fluke-induced cataract formation in fish: quantitative analysis using an opthalmological microscope. Parasitology 129: , Kirsi, S., Hudson, P. J. & Valtonen, E. T. 2004b. Patterns of cercarial production from Diplostomum spathaceum: terminal investment or bet hedging? Parasitology 129: , Hudson, P. J., Seppälä, O. & Valtonen, E. T. 2004c. Transmission dynamics of a trematode parasite: exposure, acquired resistance and parasite aggregation. Parasitology Research 92: , Seppälä, O. & Valtonen, E. T. 2004d. Parasite resistance and avoidance behaviour in preventing eye fluke infections in fish. Parasitology 129: , Paukku, S., Seppälä, O. & Valtonen, E. T Resistance against eye flukes: naïve versus previously infected fish. Parasitology Research 95: LaMarre, E. & Cochran, P. A Lack of host species selection by exotic parasitic crustacean, Argulus japonicus. Journal of Freshwater Ecology 7:

11 Sustainable production of healthy fish Lester, R. J. G. & Roubal, F. R Phylum Arthropoda. In: Fish diseases and disorders (1). Protozoan and Metazoan Infection (ed. Woo, P. T. K.). Cab International, Wallingford, U.K. pp Manning, M. J Fishes. In: Immunology. A Comparative approach. (ed. Turner, R. J.). John Wiley and Sons, Chichester, UK, pp Menezes, J. Ramos, M. A., Pereira, T. G. & da Silva, A. M Rainbow trout culture failure in small lake as a result of massive parasitosis related to careless fish introductions. Aquaculture 89: Mikheev, V. N., Pasternak, A. F., Valtonen, E. T. & Lankinen, Y Spatial distribution and hatching of overwintered eggs in a fish ectoparasite Argulus coregoni Thorell (Crustacea: Branchiura). Diseases of Aquatic Organisms 46: Owen, S. F., Barber, I. & Hart, P. J. B Low level infection by eye fluke, Diplostomum spp., affects the vision of three-spined sticklebacks, Gasterosteus aculeatus. Journal of Fish Biology 42: Pasternak, A. F., Mikheev, V. N. & Valtonen, E. T Life history characteristics of Argulus foliaceus L (Crustacea: Branchiura) populations in Central Finland. Annales Zoologici Fennici 37: Philippi, T. & Seger J Hedging One's Evolutionary Bets, Revisited. Trends in Ecology and Evolution 2: Poulin, R Evolutionary Ecology of Parasites. From Individuals to Communities. Chapman and Hall, London. Rintamäki-Kinnunen, P Parasitic and bacterial diseases at salmonid fish farms in Northern Finland. Acta Universitatis Ouluensis, Scientiae Rerum Naturalium A 294: & Valtonen, E.T Epizootiology of protozoans in farmed salmonids at northern latitudes. International Journal for Parasitology 27: Seger, J. & Brockmann, H. J What is bet-hedging? Oxford Surveys in Evolutionary Biology 4: Seppälä, O., Karvonen, A. & Valtonen, E. T Parasite-induced change in host behaviour and susceptibility to predation in an eye fluke fish interaction. Animal Behaviour 68: Shariff, M., Richards, R. H. & Sommerville, C The histopathology of acute and chronic infections of rainbow trout Salmo gairdneri Richardson with eye flukes, Diplostomum spp. Journal of Fish Diseases 3: Shimura, S Seasonal occurrence, sex ratio and site preference of Argulus coregoni (Crustacea: Branchiura). Parasitology 86: Stables, J. N. & Chappell, L. H. 1986a. The epidemiology of diplostomiasis in farmed rainbow trout from Northeast Scotland. Parasitology 92: & Chappell, L. H. 1986b. Putative immune response of rainbow trout, Salmo gairdneri, to Diplostomum spathaceum infections. Journal of Fish Biology 29: Stammer, J Beiträge zur Morphologie, Biologie und Bekämpfung se Karpfenläuse. Z. Parasitenk. 19: Valtonen, E. T. & Gibson, D. I Aspects of the biology of diplostomid metacercarial (Digenea) populations occurring in fishes in different localities of northern Finland. Annales Zoologici Fennici 34: , Holmes, J. C. & Koskivaara, M Eutrophication, pollution and fragmentation: effects on parasite communities in roach (Rutilus rutilus) and perch (Perca fluviatilis) in four lakes in Central Finland. Can. J. Fish Aq. Sci. 54:

12 Karvonen et al. Whyte, S. K., Allan, J. C., Secombes, C. J. & Chappell, L. H Cercariae and diplostomules of Diplostomum spathaceum (Digenea) elicit an immune response in rainbow trout, Salmo gairdneri Richardson. Journal of Fish Biology 31: , Chappell, L. H. & Secombes, C. J Cytotoxic reactions of rainbow trout, Salmo gairdneri Richardson, macrophages for larvae of the eye fluke Diplostomum spathaceum (Digenea). Journal of Fish Biology 35: , Chappell, L. H. & Secombes, C. J Protection of rainbow trout, Oncorhynchus mykiss (Richardson), against Diplostomum spathaceum (Digenea): the role of specific antibody and activated macrophages. Journal of Fish Diseases 13:

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