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Baseline Histopathological Survey of a Recently Invading Island Population of ‘Killer Shrimp’, Dikerogammarus Villosus

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Baseline Histopathological Survey of a Recently Invading Island Population of ‘Killer Shrimp’, Dikerogammarus Villosus Vol. 106: 241–253, 2013 DISEASES OF AQUATIC ORGANISMS Published November 6 doi: 10.3354/dao02658 Dis Aquat Org FREEREE ACCESSCCESS Baseline histopathological survey of a recently invading island population of ‘killer shrimp’, Dikerogammarus villosus J. Bojko1,2, P. D. Stebbing1, K. S. Bateman1,3, J. E. Meatyard4, K. Bacela-Spychalska5, A. M. Dunn2, G. D. Stentiford1,3,* 1Centre for Environment, Fisheries and Aquaculture Science, Weymouth Laboratory, The Nothe, Barrack Road, Weymouth, Dorset, DT4 8UB, UK 2Faculty of Biological Sciences, University of Leeds, Clarendon Way, Leeds, LS2 9JT, UK 3European Union Reference Laboratory for Crustacean Diseases, Centre for Environment, Fisheries and Aquaculture Science (Cefas), Weymouth Laboratory, The Nothe, Barrack Road, Weymouth, Dorset, DT4 8UB, UK 4Biology Department, Anglian Water Central Laboratory, Kingfisher Way, Hinchinbrook Business Park, Huntingdon, PE29 6FL, UK 5Department of Invertebrate Zoology & Hydrobiology, University of Lodz, Banacha 12/16 90-237 Lodz, Poland ABSTRACT: Dikerogammarus villosus, an invasive amphipod, has recently been detected in UK freshwaters. To assess the potential for pathogen introduction with the invader, a year-long histopathology survey of the D. villosus population inhabiting the initial site of detection (Grafham Water, Cambridgeshire, UK) was conducted. Additional samples were collected from 2 other subse- quently identified populations within the UK (Cardiff Bay and Norfolk Broads), and from established populations in France (River Rhine) and Poland (River Vistula). The data revealed a range of pathogens and commensals. Several pathogens occurring within continental populations were not present within the UK populations. Microsporidian parasites and a novel viral pathogen were amongst those not observed in the UK. The absence of these pathogens at UK sites may there- fore impart significant survival advantages to D. villosus over native fauna, thereby increasing its success as an invader. The contrast in pathogen profile between UK and continental-invasive popu- lations of D. villosus provides preliminary evidence for so-called ‘enemy release’ in UK populations of D. villosus and is suggestive of single-point introductions, rather than continual incursion events as previously observed throughout its continental invasive range. This baseline survey provides im- portant data on the pathogen and commensal profile of a high-impact, invasive species early in its invasion history of the UK. It can be utilised to assess potential for temporal pathogen acquisition by non-native invasive aquatic species and to investigate competitive advantages placed upon this in- vader due to absence of important pathogens experienced within its native range. KEY WORDS: Amphipod · Non-native invasive species · Biodiversity · Virus · Microsporidia · Parasite · Commensal Resale or republication not permitted without written consent of the publisher INTRODUCTION Perkins 2012). Invasive species may introduce novel parasites and pathogens to their new range (Steb- Biological invasions often lead to altered host−par- bing et al. 2012, Strauss et al. 2012). Some acquire asite relationships that in turn influence their impact parasites previously unreported in the invasive spe- on the recipient community (Dunn 2009, Dunn & cies from the new environment, or benefit from a loss *Corresponding author. Email: [email protected] © The Crown 2013 Publisher: Inter-Research · www.int-res.com 242 Dis Aquat Org 106: 241–253, 2013 of natural enemies, including parasites, freeing re - gorenko et al. 1978). Several microsporidians have sour ces that would otherwise be devoted to immune been reported to infect D. villosus, including Cucu - responses, allowing increased investment in growth mispora dikerogammari (= Nosema dikerogammari and reproduction (Mitchell & Power 2003, Torchin et Ovcharenko and Kurandina, 1987) (Ovcharenko et al. 2003, Roy & Handley 2012). al. 2010), Nosema granulosis, Dictyocoela roeselum, Dikerogammarus villosus (Sowinsky, 1894) is a Dictyocoela muelleri and Dictyocoela berillonum freshwater amphipod native to the Ponto-Caspian re- (Wattier et al. 2007). Despite these descriptions, to gion of Eastern Europe. Several life history character- date, there have been no published reports which istics of D. villosus are important for its success as an provide comprehensive data on the pathogen profile invader; these include a high salinity tolerance (Bruijs of D. villosus within its native range. et al. 2001, Piscart et al. 2011), an ability to survive Wattier et al. (2007) surveyed 34 Dikerogammarus and grow in a wide range of temperatures (Maazouzi villosus populations in Europe and found no evi- et al. 2011), rapid growth and early maturation, with dence for reduced genetic diversity or for loss of short interbrood periods (Piscart et al. 2003, Devin et microsporidian parasites in the continental-invasive al. 2004), high fecundity (Kley & Maier 2003, Pöckl range of the host. This led to the conclusion that the 2007), an omnivorous diet (Krisp & Maier 2005) and a invasion within continental Europe was either mas- capability to compete with, and prey upon, a range of sive, recurrent or both and led to a concurrent estab- cohabiting taxa, including those se veral trophic lishment of a pathogen fauna, across the continental levels above itself (Dick et al. 2002, Krisp & Maier invasive range of D. villosus. In contrast, the estab- 2005, MacNeil et al. 2013). These attributes have re- lishment of the recently identified UK D. villosus sulted in D. villosus out-competing other gammarids populations is likely to be the result of isolated intro- within Europe, including Gamma rus pulex (Boets et ductions. This different introduction pathway poses al. 2010), G. tigrinus and G. due beni (Dick & Platvoet the question of whether the pathogen fauna in UK 2000). The invasion of con ti nen tal Europe by D. villo- populations may be depleted when compared to that sus began with the construction of the Danube-Main- found within native or continental-invasive range Rhine canal in 1992 which linked waterways of the populations of this species. This is hinted at by a sur- Ponto-Caspian region to those of northwest mainland vey which included a small number of samples of Europe, creating ‘invasion corridors’ along which D. villosus obtained from Grafham Water in which no D. villosus rapidly spread (Bij de Vaate et al. 2002). evidence was found for microsporidia within the Ponto-Caspian populations of D. villosus are expected genus Dictyocoela (Wilkinson et al. 2011). to have further colonised adjoining river systems and have invaded larger areas of continental Europe via shipping and natural upstream migration using MATERIALS AND METHODS the Danube- Main-Rhine canal (Bij de Vaate et al. 2002, Grigorovich et al. 2003, Casellato et al. 2006). In Field sampling 2010, populations of D. villosus were detected for the first time in the UK, at Grafham Water, Cambridge - Dikerogammarus villosus were sampled monthly shire, and subsequently at Cardiff Bay and Eglwys (n = ~150 mo−1) from Grafham Water, Cambridge - Nunydd reservoir in South Wales. By 2012, the shire, between September 2011 and August 2012. invasion reached The River Ant and Barton Broad in Since D. villosus inhabit gaps within rocky sub- Norfolk. strates, unbaited ‘colonisation samplers’ constructed Previous studies on pathogens of Dikerogammarus from air bricks were deployed on the shoreline of the villosus are restricted to samples collected from con- reservoir. During colder months, D. villosus were less tinental Europe. Four species of gregarines (Apicom- frequently found within colonisation samplers. At plexa) were described in populations from Poland: these times, D. villosus were collected from within Cephaloidophora similis, C. mucronata, Uradiophora rope-growing populations of zebra mussels Dreis- longissima and U. ramosa (Ovcharenko et al. 2009). sena polymorpha, a co-existing invasive species at The peritrich ciliate Lagenophrys pontocaspica was this site. In addition to the seasonal survey of D. villo- reported attached to the gills and oostegites of sus from Grafham Water, animals were also collected amphipods in the Ukraine, including D. villosus, at a from other UK populations at Cardiff Bay and the prevalence of up to 80% (Boshko 1996). The trema- Norfolk Broads, and from sites within its continental- tode Plagioporus skrjabini was reported in D. villosus invasive range in France (Chalampé, Rhine River) from the Volga River in central Russia (Cherno- and Poland (Vistula River) (Table 1). Bojko et al.: Histopathology of Dikerogammarus villosus 243 Histopathology Individual specimens (n = 2899) were euthanised by initially being placed on ice following fixation for histology by direct injection with and submersion in Davidson’s freshwater fixative (Hopwood 1996) over the study period. Of these, 2310 animals were sampled from sites within the UK, 291 were sampled from France, and 298 were sampled bacilliform virus from Poland (Table 1). After 24 h, samples were transferred to 70% industrial methylated spirit (IMS). Whole-animal histological preparations of Dikerogammarus villosus were created by initial placement of fixed specimens in ‘Rapid Decalcifier II’ for 30 min with frequent agitation. Paraffin wax infiltration was com- Dikerogammarus villosus pleted using a vacuum infiltrating automated tissue processor (Poloris, Leica Microsys- tems) before specimens were embedded long - itudinally into paraffin
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