Reservoir hosts for Gyrodactylus salaris may play a more significant role in epidemics than previously thought

Particle and Fibre Toxicology

Andrew P Shinn⁵  James E Bron²  Sigurd Hytterød²  Scott J Denholm⁴  Olga L Rubio-Mejía²  Nick GH Taylor³  Chris F Williams⁶  Haakon Hansen¹  Giuseppe Paladini² 

[1] Norwegian Veterinary Institute, Section for Parasitology, Sentrum NO-0106, Oslo, Norway;Institute of Aquaculture, School of Natural Sciences, University of Stirling, Stirling FK9 4LA, Scotland, UK;Centre for Environment, Fisheries & Aquaculture (Cefas), Weymouth Laboratory, Barrack Road, Weymouth DT4 8UB, UK;Animal Breeding and Genomics, Animal & Veterinary Sciences, SRUC, Roslin Institute Building, Easter Bush, Midlothian EH25 9RG, UK;Fish Vet Group Asia Ltd., 99/386, Chaengwattana Building, Chaengwattana Rd., Kwaeng Toongsonghong, Khet Laksi 10210, Bangkok, Thailand;Environment Agency, National Fisheries Laboratory, Bromholme Lane, Brampton PE28 4NE, UK

关键词: Pathogen;    Monogenea;    Susceptibility;    Grayling;    Thymallus thymallus;    Brown trout;    Salmo trutta;    Atlantic salmon;    Salmo salar;    Parasite;   

Others  :  1148323
DOI  :  10.1186/s13071-014-0576-5

 received in 2014-06-29, accepted in 2014-11-27,  发布年份 2014

【 摘 要 】

Background

Gyrodactylus salaris Malmberg, 1957 has had a devastating impact on wild Norwegian stocks of Atlantic salmon Salmo salar L., and it is the only Office International des Epizooties (OIE) listed parasitic pathogen of fish. The UK is presently recognised as G. salaris-free, and management plans for its containment and control are currently based on Scandinavian studies. The current study investigates the susceptibility of British salmonids to G. salaris, and determines whether, given the host isolation since the last glaciation and potential genetic differences, the populations under test would exhibit different levels of susceptibility, as illustrated by the parasite infection trajectory over time, from their Scandinavian counterparts.

Methods

Populations of S. salar, brown trout Salmo trutta L., and grayling Thymallus thymallus (L.), raised from wild stock in UK government hatcheries, were flown to Norway and experimentally challenged with a known pathogenic strain of G. salaris. Each fish was lightly anaesthetised and marked with a unique tattoo for individual parasite counting. A single Norwegian population of S. salar from the River Lærdalselva was used as a control. Parasite numbers were assessed every seven days until day 48 and then every 14 days.

Results

Gyrodactylus salaris regularly leads to high mortalities on infected juveniles S. salar. The number of G. salaris on British S. salar rose exponentially until the experiment was terminated at 33 days due to fish welfare concerns. The numbers of parasites on S. trutta and T. thymallus increased sharply, reaching a peak of infection on days 12 and 19 post-infection respectively, before declining to a constant low level of infection until the termination of the experiment at 110 days.

Conclusions

The ability of S. trutta and T. thymallus to carry an infection for long periods increases the window of exposure for these two hosts and the potential transfer of G. salaris to other susceptible hosts. This study demonstrates that G. salaris can persist on S. trutta for longer periods than previously thought, and that the role that S. trutta could play in disseminating G. salaris needs to be considered carefully and factored into management plans and epidemics across Europe.

【 授权许可】

   
2014 Paladini et al.; licensee BioMed Central.

【 图 表 】

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【 参考文献 】

• [1]Harris PD, Shinn AP, Cable J, Bakke TA: Nominal species of the genus Gyrodactylus von Nordmann 1832 (Monogenea: Gyrodactylidae), with a list of principal host species. Syst Parasitol 2004, 59:1-27.
• [2]Johnsen BO, Møkkelgjerd PI, Jensen AJ: The parasite Gyrodactylus salaris on salmon parr in Norwegian rivers, status report at the beginning of year 2000. NINA Oppdragsmelding 1999, 617:1-129.
• [3]Bakke TA, Cable J, Harris PD: The biology of gyrodactylid monogeneans: the “Russian-doll killers”. Adv Parasitol 2007, 64:161-376.
• [4]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, 33:1471-1478.
• [5]Guttvik KT, Moen A, Skår K: Bekjempelse av lakseparasitten Gyrodactylus salaris ved bruk av plantegiften rotenon. Norsk Veterinærtidsskrift 2004, 3:172-174.
• [6]Rintamäki P: Gyrodactylus salaris at a fish farm in northern Finland. In Parasites of Freshwater Fishes in North-West Europe. Edited by Bauer ON. USSR: Institute of Biology, USSR Academy of Sciences, Karelian Branch, Petrozavodsk; 1989:123-130.
• [7]Ieshko E, Berland B, Shulman B, Bristow G, Shchurov I: On some parasites of salmon parr ( Salmo salar L., 1758) (Pisces, Salmonidae) from rivers of the Karelian White Sea Basin. In Proc IV Int Symp Ichthyoparasitology, 3rd-7thOct 1995. Munich, Germany; 1995:100.
• [8]Alenäs I: Gyrodactylus salaris på lax i Svenska vattendrag och laxproblematiken på Svenska västkysten. Vann 1998, 1:135-142.
• [9]Alenäs I, Malmberg G, Carlstrand H: Undersökningar av Gyrodactylus salaris på lax i Ätrans vattensystem, Falkenbergs kommun under fem år 1991–1995. Miljö og Hälsoskyddskontoret Falkenbergs Kommun 1998, 1:1-12.
• [10]Rokicka M, Lumme J, Ziętara MS: Identification of Gyrodactylus ectoparasites in Polish salmonid farms by PCR-RFLP of the nuclear ITS segment of ribosomal DNA (Monogenea, Gyrodactylidae). Acta Parasitol 2007, 52:185-195.
• [11]Paladini G, Gustinelli A, Fioravanti ML, Hansen H, Shinn AP: The first report of Gyrodactylus salaris Malmberg, 1957 (Platyhelminthes, Monogenea) on Italian cultured stocks of rainbow trout (Oncorhynchus mykiss Walbaum). Vet Parasitol 2009, 165:290-297.
• [12]Platten M, McLoughlin M, Shinn AP: Distribution and identification of gyrodactylid species in fish farms and rivers in Northern Ireland. Vet Rec 1994, 135:411-412.
• [13]Shinn AP, Sommerville C, Gibson DI: Distribution and characterization of species of Gyrodactylus Nordmann, 1832 (Monogenea) parasitizing salmonids in UK, and their discrimination from G. salaris Malmberg, 1957. J Nat Hist 1995, 29:1383-1402.
• [14]Mawle GW, Peirson G: Economic Evaluation of Inland Fisheries. Managers report from science project SC050026/SR2, Environment Agency, Bristol, UK; 2009.
• [15]Jansen PA, Bakke TA: Susceptibility of brown trout to Gyrodactylus salaris (Monogenea) under experimental conditions. J Fish Biol 1995, 46:415-422.
• [16]Soleng A, Bakke TA: The susceptibility of grayling (Thymallus thymallus) to experimental infections with the monogenean Gyrodactylus salaris. Int J Parasitol 2001, 31:793-797.
• [17]Bakke TA, Jansen PA, Kennedy CR: The host specificity of Gyrodactylus salaris Malmberg (Platyhelminthes, Monogenea): susceptibility of Oncorhynchus mykiss (Walbaum) under experimental conditions. J Fish Biol 1991, 39:45-57.
• [18]Bakke TA, Harris PD, Jansen PA: The susceptibility of Salvelinus fontinalis (Mitchill) to Gyrodactylus salaris Malmberg (Platyhelminthes; Monogenea) under experimental conditions. J Fish Biol 1992, 41:499-507.
• [19]Bakke TA, Jansen PA, Grande M: The susceptibility of Salvelinus namaycush (Walbaum) to Gyrodactylus salaris Malmberg (Platyhelminthes; Monogenea) under experimental conditions. Fauna Nor (Ser A) 1992, 13:1-7.
• [20]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, 49:341-351.
• [21]Soleng A, Bakke TA: The susceptibility of whitefish (Coregonus lavaretus L.) to experimental infections with the monogenean Gyrodactylus salaris Malmberg, 1957. Bull Scand Soc Parasitol 2001, 11:32-36.
• [22]Bakke TA, Sharp LA: Susceptibility and resistance of minnows, Phoxinus phoxinus (L.) to Gyrodactylus salaris Malmberg, 1957 (Monogenea) under laboratory conditions. Fauna Nor (Ser A) 1990, 11:51-55.
• [23]Soleng A, Bakke TA: The susceptibility of three-spined stickleback (Gasterosteus aculeatus), nine-spined stickleback (Pungitius pungitius) and flounder (Platichthys flesus) to the monogenean Gyrodactylus salaris. Parasitol Int 1998, 47:319.
• [24]Bakke TA, Jansen PA, Hansen LP: Experimental transmission of Gyrodactylus salaris Malmberg, 1957 (Platyhelminthes, Monogenea) from the Atlantic salmon (Salmo salar) to the European eel (Anguilla anguilla). Can J Zool 1991, 69:733-737.
• [25]Bakke TA, Jansen PA, Brabrand A: Susceptibility and resistance of brook lamprey, Lampetra planeri (Bloch), roach, Rutilus rutilus (L.) and perch, Perca fluviatilis L. to Gyrodactylus salaris Malmberg (Monogenea). Fauna Nor (Ser A) 1990, 11:23-26.
• [26]Bakke TA, Harris PD, Cable J: Host specificity dynamics: observations on gyrodactylid monogeneans. Int J Parasitol 2002, 32:281-308.
• [27]Peeler EJ, Thrush MA: Qualitative analysis of the risk of introducing Gyrodactylus salaris into the United Kingdom. Dis Aquat Organ 2004, 62:103-113.
• [28]Peeler EJ, Oidtmann BC: Demonstrating freedom from Gyrodactylus salaris (Monogenea: Gyrodactylidae) in farmed rainbow trout Oncorhynchus mykiss. Dis Aquat Organ 2008, 79:47-56.
• [29]Thrush MA, Peeler EJ: Stochastic simulation of live salmonid movement in England and Wales to predict potential spread of exotic pathogens. Dis Aquat Organ 2006, 72:115-123.
• [30]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, 37:577-587.
• [31]Bakke T, 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.
• [32]Bakke TA, Soleng A, Harris PD: The susceptibility of Atlantic salmon (Salmo salar L.) × brown trout (Salmo trutta L.) hybrids to Gyrodactylus salaris Malmberg and Gyrodactylus derjavini Mikailov. Parasitology 1999, 119:467-481.
• [33]Harris PD, Soleng A, Bakke TA: Increased susceptibility of salmonids to the monogenean Gyrodactylus salaris following administration of hydrocortisone acetate. Parasitology 2000, 120:57-64.
• [34]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 G. thymalli Žitňan, 1960 (Monogenea: Gyrodactylidae). Parasitology 2002, 124:203-213.
• [35]Ståhl G: Genetic population structure of Atlantic salmon. In Population Genetics and Fishery Management. Edited by Ryman N, Utter F. University of Washington Press, Seattle; 1987:121-140.
• [36]Halvorsen O, Hartvigsen R: A review of the biogeography and epidemiology of Gyrodactylus salaris. NINA Utred 1989, 2:1-41.
• [37]Gupta S, Collier JS, Palmer-Felgate A, Potter G: Catastrophic flooding origin of shelf valley systems in the English Channel. Nature 2007, 448:342-345.
• [38]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 Organ 2003, 53:173-176.
• [39]Dalgaard MB, Larsen TB, Jørndrup S, Buchmann K: Differing resistance of Atlantic salmon strains and rainbow trout to Gyrodactylus salaris infection. J Aquat Anim Health 2004, 16:109-115.
• [40]Hytterød S, Adolfsen P, Aune S, Hansen H: Gyrodactylus salaris funnet på røye (Salvelinus alpinus) i Fustvatnet (Nordland); patogen for laks (Salmo salar)? Rapp 2011, 11:1-15.
• [41]Yates DS, Moore DS, Starnes DS: The Practice of Statistics. Third edition. Freeman WH, New York, USA; 2008.
• [42]Cable J, Harris PD, Bakke TA: Population growth of Gyrodactylus salaris (Monogenea) on Norwegian and Baltic Atlantic salmon (Salmo salar) stocks. Parasitology 2000, 121:621-629.
• [43]Gheorghiu C, Cable J, Marcogliese DJ, Scott ME: Effects of waterborne zinc on reproduction, survival and morphometrics of Gyrodactylus turnbulli (Monogenea) on guppies (Poecilia reticulata). Int J Parasitol 2007, 37:375-381.
• [44]Gheorghiu C, Marcogliese DJ, Scott ME: Waterborne zinc alters temporal dynamics of guppy Poecilia reticulata epidermal response to Gyrodactylus turnbulli (Monogenea). Dis Aquat Organ 2012, 98:143-153.
• [45]Bridcut EE: A coded alcian blue marking technique for the identification of individual brown trout, Salmo trutta L.: an evaluation of its use in fish biology. Biol Environ Proc R Irish Acad 1993, 93B:107-110.
• [46]Barber I, Crompton DWT: The distribution of the metacercariae of Diplostomum phoxini in the brain of minnows, Phoxinus phoxinus. Folia Parasitol 1997, 44:19-25.
• [47]Otranto D, Eberhard ML: Zoonotic helminths affecting the human eye. Parasit Vectors 2011, 4:41. BioMed Central Full Text
• [48]Cox FEG: Immunology. In Modern Parasitology. Third edition. Edited by Cox FEG. Blackwell Scientific Publications, Oxford, UK; 1994:193-218.
• [49]Price PW: Evolution in parasite communities. Int J Parasitol 1987, 17:209-214.
• [50]Sukhdeo MVK, Mettrick DF: Parasite behaviour: understanding platyhelminth responses. Adv Parasitol 1987, 26:73-144.
• [51]Buchmann K, Lindenstrøm T: Interactions between monogenean parasites and their fish hosts. Int J Parasitol 2002, 32:309-319.
• [52]Van Oosterhout C, Mohammed RS, Hansen H, Archard GA, McMullan M, Weese DJ, Cable J: Selection by parasites in spate conditions in wild Trinidadian guppies (Poecilia reticulata). Int J Parasitol 2007, 37:805-812.
• [53]Hockley FA, Wilson CAME, Graham N, Cable J: Combined effects of flow condition and parasitism on shoaling behaviour of female guppies Poecilia reticulata. Behav Ecol Sociobiol 2014, 68:1513-1520.
• [54]Bakke TA: A review of the inter- and intraspecific variability in salmonid hosts to laboratory infections with Gyrodactylus salaris Malmberg. Aquaculture 1991, 98:303-310.
• [55]Titus RG: Territorial behavior and its role in population regulation of young brown trout (Salmo trutta): new perspectives. Ann Zool Fennici 1990, 27:119-130.
• [56]Buchmann K, Uldal A: Gyrodactylus derjavini infections in four salmonids: comparative host susceptibility and site selection of parasites. Dis Aquat Organ 1997, 28:201-209.
• [57]Olstad K, Cable J, Robertsen G, Bakke TA: Unpredicted transmission strategy of Gyrodactylus salaris (Monogenea: Gyrodactylidae): survival and infectivity of parasites on dead hosts. Parasitology 2006, 133:33-41.
• [58]Hansen H, Bakke TA, Bachmann L: DNA taxonomy and barcoding of monogenean parasites: lessons from Gyrodactylus. Trends Parasitol 2007, 23:363-367.
• [59]Hansen H, Bakke TA, Bachmann L: Mitochondrial haplotype diversity of Gyrodactylus thymalli (Platyhelminthes; Monogenea): extended geographic sampling in United Kingdom, Poland, and Norway reveals further lineages. Parasitol Res 2007, 100:1389-1394.
• [60]Hansen H, Martinsen L, Bakke TA, Bachmann L: The incongruence of nuclear and mitochondrial DNA variation supports conspecificity of the monogenean parasites Gyrodactylus salaris and G. thymalli. Parasitology 2006, 133:639-650.
• [61]Meinilä M, Kuusela J, Ziętara MS, Lumme J: Initial steps of speciation by geographic isolation and host switch in salmonid pathogen Gyrodactylus salaris (Monogenea: Gyrodactylidae). Int J Parasitol 2004, 34:515-526.
• [62]Kuusela J, Holopainen R, Meinilä M, Veselov A, Shchurov IL, Ieshko EP, Lumme J: Potentially dangerous Gyrodactylus salaris in Russian Karelia: harmless and harmful combinations of host species and parasite strains. In Salmonid Fishes of Eastern Fennoscandia. KarRC RAS, Petrozavodsk; 2005:47-55.
• [63]Kuusela J, Ziętara MS, Lumme J: Hybrid origin of Baltic salmon-specific parasite Gyrodactylus salaris: a model for speciation by host switch for hemiclonal organisms. Mol Ecol 2007, 16:5234-5245.
• [64]Robertsen G, Hansen H, Bachmann L, Bakke TA: Arctic charr (Salvelinus alpinus) is a suitable host for Gyrodactylus salaris (Monogenea, Gyrodactylidae) in Norway. Parasitology 2007, 134:257-267.
• [65]Bakke TA, Jansen PA, Saltveit S: Early life survival of wild Atlantic salmon (Salmo salar) experimentally exposed to Gyrodactylus salaris (Monogenea). Parasitol Int 1998, 47:318.
• [66]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 Organ 2004, 58:171-177.
• [67]Jansen PA, Bakke TA, Hansen LP: Resistance to Gyrodactylus salaris Malmberg, 1957 (Monogenea) in Salmo salar : a genetic component. Bull Scand Soc Parasitol 1991, 1:50.
• [68]Tanum K: Studier av taksonomi og vertsforhold hos Gyrodactylus-arter på laksefisk av slektene Salmo og Salvelinus i Norge. In M.Sc. thesis. University of Oslo, Norway; 1983:1-99.
• [69]Mo TA: Gyrodactylus-undersokelsene av fisk i forbindelse med rotenon-behandlingen av Skibotnelva i August 1988. Gyrodactylus-undersøkelsene ved Zool Museum Univ i Oslo 1988, 5:1-14.
• [70]Malmberg G, Malmberg M: Undersökningar angående Gyrodactylus på laxfisk i fria vatten och odlingar under åren 1951–72 Och 1986 - Maj 1991. Inf från Sötvattenlaboratoriet Drottningholm 1991, 2:1-30.
• [71]Johnsen BO, Jensen AJ: Infection of Atlantic salmon, Salmo salar L., by Gyrodactylus salaris Malmberg 1957, in the River Lakselva, Misvaer in northern Norway. J Fish Biol 1992, 40:433-444.
• [72]De Roij J, Harris PD, MacColl ADC: Divergent resistance to a monogenean flatworm among three-spined stickleback populations. Funct Ecol 2011, 1:217-226.
• [73]McHugh ES, Shinn AP, Kay JW: Discrimination of the notifiable pathogen Gyrodactylus salaris from G. thymalli (Monogenea) using statistical classifiers applied to morphometric data. Parasitology 2000, 121:315-323.
• [74]Shinn AP, Hansen H, Olstad K, Bachmann L, Bakke TA: The use of morphometric characters to discriminate specimens of laboratory-reared and wild populations of Gyrodactylus salaris and G. thymalli (Monogenea). Folia Parasitol 2004, 51:239-252.
• [75]Fromm B, Burow S, Hahn C, Bachmann L: MicroRNA loci support conspecificity of Gyrodactylus salaris and Gyrodactylus thymalli (Platyhelminthes: Monogenea). Int J Parasitol 2014, 44:787-793.
• [76]Shinn AP, Collins C, García-Vásquez A, Snow M, Matejusová I, Paladini G, Longshaw M, Lindenstrøm T, Stone DM, Turnbull JF, Picon-Camacho SM, Vázquez Rivera C, Duguid RA, Mo TA, Hansen H, Olstad K, Cable J, Harris PD, Kerr R, Graham D, Monaghan SJ, Yoon GH, Buchmann K, Taylor NGH, Bakke TA, Raynard R, Irving S, Bron JE: Multi-centre testing and validation of current protocols for the identification of Gyrodactylus salaris (Monogenea). Int J Parasitol 2010, 40:1455-1467.