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Negative Effects of Kudoa Islandica N. Sp. (Myxosporea: Kudoidae) on Aquaculture and Wild fisheries in Iceland

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Negative Effects of Kudoa Islandica N. Sp. (Myxosporea: Kudoidae) on Aquaculture and Wild fisheries in Iceland IJPPAW 69 No. of Pages 12, Model 5G 20 June 2014 International Journal for Parasitology: Parasites and Wildlife xxx (2014) xxx–xxx 1 Contents lists available at ScienceDirect International Journal for Parasitology: Parasites and Wildlife journal homepage: www.elsevier.com/locate/ijppaw 5 6 3 Negative effects of Kudoa islandica n. sp. (Myxosporea: Kudoidae) 4 on aquaculture and wild fisheries in Iceland a,⇑ b 7 Q1 Árni Kristmundsson , Mark Andrew Freeman 8 a Institute for Experimental Pathology at Keldur, University of Iceland, Keldnavegur 1-3, IS-112, Reykjavik, Iceland 9 b Institute of Ocean and Earth Sciences, University of Malaya, Kuala Lumpur, Malaysia 1110 12 article info abstract 2714 15 Article history: In the early 2000s, experimental rearing of spotted wolffish, Anarhichas minor, was started in Iceland. 28 16 Received 14 February 2014 Health surveillance, carried out at regular intervals during the rearing period, revealed persistent and 29 17 Revised 5 June 2014 highly prevalent Kudoa infections of fish muscles which caused great financial losses due to post mortem 30 18 Accepted 5 June 2014 myoliquefaction. In addition, during the traditional process of drying and smoking wild Atlantic lumpfish, 31 19 Available online xxxx Cyclopterus lumpus, the muscles from some fish almost completely disappear and the fish have to be dis- 32 carded. 33 20 Keywords: To describe the etiological agent responsible for these conditions, spotted wolffish, Atlantic wolffish 34 21 Kudoa Anarhichas lupus, northern wolffish Anarhichas denticulatus and Atlantic lumpfish were caught off the 35 22 Myoliquefaction 23 Muscle Icelandic coast and examined for the presence of Kudoa. We describe a novel myxosporean, Kudoa islan- 36 24 Soft flesh syndrome Cyclopterus lumpus dica n. sp., using morphological and molecular data, and show with histopathology that it causes exten- 37 25 Anarhichas spp. sive myoliquefaction in three different wild fish hosts, which all are commercially valuable species in 38 26 Iceland. Although some spore dimensions varied significantly between fish species, the molecular anal- 39 yses showed that the same parasite was responsible for infection in all fish. The northern wolffish was 40 not found to be infected. Although robustly placed in the Kudoa clade in phylogenetic analyses, K. islan- 41 dica was phylogenetically distinct from other kudoids. 42 A single myxosporean, K. islandica, is responsible for the infections in the somatic muscles of lumpfish 43 and wolffish, causing extensive post mortem myoliquefaction. This myxosporean is likely to infect other 44 fish species and it is important to study its life cycle in order to evaluate any threat to salmonid culture 45 via the use of lumpfish as a biocontrol for sea lice. 46 Ó 2014 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license 47 (http://creativecommons.org/licenses/by-nc-nd/3.0/). 48 49 50 51 1. Introduction one Kudoa sp. has been found infecting the musculature of a non- 64 piscine host, the giant octopus Paroctopus dofleini (Yokoyama and 65 52 Myxosporeans are a diverse group of parasites commonly found Masuda, 2001). Although most Kudoa species are described from 66 53 infecting fish. Although the life cycles of many species are not a single host, several have been identified in numerous fish species 67 54 described, known life cycles require an alternate host which typi- from different families, such as Kudoa thyrsites (with at least 38 dif- 68 55 cally is an annelid worm. To date 95 nominal species of the ferent hosts), Kudoa nova (20 hosts) and Kudoa iwatai (19 hosts) 69 56 myxosporean genus Kudoa (Kudoidae) have been described, pres- (Burger and Adlard, 2011). While kudoids are generally not consid- 70 57 ently all with unknown life cycles. Most commonly kudoids are ered highly pathogenic to the host, some species have caused sig- 71 58 histozoic in skeletal muscles of fish (Moran et al., 1999a; Lom nificant detrimental effects on both commercial fisheries and 72 59 and Dykova, 2006; Eiras et al., 2014) but have also been found to aquaculture, due to the unsightly muscle cysts they form and more 73 60 infect other organs such as brain, heart, gills, kidney, gall bladder, importantly the post mortem myoliquefaction some species cause, 74 61 ovary and intestines (Egusa, 1986; Sandeep et al., 1986; Sarkar commonly known as ‘‘soft flesh’’, which greatly reduces the market 75 62 and Ghosh, 1991; Yurakhno, 1991; Blaylock et al., 2004; value of the fillets (Langdon, 1991; Moran et al., 1999a; 76 63 Yurakhno et al., 2007; Mansour et al., 2013). Furthermore, at least Alvarez-Pellitero and Sitjà-Bobadilla, 1993). In addition, cysts of Q3 77 Kudoa septempunctata from farmed fish in Japan and Korea have 78 been strongly linked with numerous cases of food poisoning in 79 ⇑ Corresponding author. Tel.: +354 5855100, mobile: +354 8664404. E-mail addresses: [email protected] (Á. Kristmundsson), [email protected] humans (Matsukane et al. 2010; Kawai et al. 2012; Iwashita 80 (M.A. Freeman). http://dx.doi.org/10.1016/j.ijppaw.2014.06.001 2213-2244/Ó 2014 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/3.0/). Please cite this article in press as: Kristmundsson, Á., Freeman, M.A. Negative effects of Kudoa islandica n. sp. (Myxosporea: Kudoidae) on aquaculture and wild fisheries in Iceland. International Journal for Parasitology: Parasites and Wildlife (2014), http://dx.doi.org/10.1016/j.ijppaw.2014.06.001 IJPPAW 69 No. of Pages 12, Model 5G 20 June 2014 2 Á. Kristmundsson, M.A. Freeman / International Journal for Parasitology: Parasites and Wildlife xxx (2014) xxx–xxx 81 et al., 2013). Therefore, the production of Kudoa-free fish products In February 2013, wild spotted wolffish (length 65–103 cm), 144 82 from aquaculture ventures has become a priority. Atlantic wolffish (62–89 cm) and Atlantic lumpfish (41–48 cm), 5 145 83 Atlantic wolffish Anarhichas lupus L. 1758, spotted wolffish Ana- fish of each species, were caught in Bay Faxaflói off the west coast 146 84 rhichas minor Olafsen, 1772 and Atlantic lumpfish Cyclopterus lum- of Iceland and examined for the presence of Kudoa spp. In addition, 147 85 pus L. 1758 are all commercially important species in Iceland, the in July 2013, ten northern wolffish (length, 65–105 cm), were 148 86 mean annual catch over the last 10 years being around 14,000 tn, caught off the NW coast of Iceland and examined for Kudoa 149 87 2500 tn and 5500 tn, respectively (Anonymous, 2012). The wolffish infections. 150 88 species are considered desirable products because of their rich and 89 tasty fillet but also their unusual and popular skin, which is used 2.2. Examination of fresh fish and sampling methods 151 90 for making designer wear. The northern wolffish Anarhichas denti- 91 culatus is common in sea water around Iceland, especially off the Skeletal muscles of all fish, farmed and wild, were examined for 152 92 NW coast, but is not considered a commercially valuable species the presence of Kudoa sp. Three slices of muscles, approximately 153 93 due to the unusual texture of its flesh. Lumpfish are targeted dur- 4 cm wide and 8 cm long, from the anterior-, mid- and posterior 154 94 ing a coastal spring fisheries as their valuable eggs are harvested parts of the fish fillets, were thoroughly searched under a stereomi- 155 95 for use as a caviar substitute. Traditionally, female lumpfish are croscope for the presence of plasmodia/pseudocysts. If detected, 156 96 dried and the fillets of male fish are smoked, and processed for they were removed from the fillet and placed on a microscope slide 157 97 human consumption. Recently, new markets have opened for and examined at 400Â magnification, to confirm the presence of 158 98 lumpfish muscle and presently most of it is exported to Asia. Kudoa spores. If no plasmodia were detected, the muscle slices 159 99 Knowledge of Kudoa infections in wild Icelandic fish are very were homogenised in PBS using a pestle and mortar. The homoge- 160 100 scarce. The only report of such infections are in a local fisheries nised muscle was sieved (500 lm) and the fluid centrifuged at 161 101 magazine from 1986, where infections in lumpfish muscle are 1500 g for 5 min and the pellet microscopically screened for the 162 102 mentioned (Thorsteinsson, 1986) and a report on the healthiness presence of Kudoa spores. Infection intensity was determined as 163 103 of seafood from 1999 where Kudoa sp. is briefly mentioned causing follows: very light = no pseudocysts seen but spores detected from 164 104 spoilage of fillets of lumpfish and Atlantic wolffish (Bjarnason et al., centrifuged muscle homogenate; light = 1–20 pseudocysts 165 105 1999). No data existed on Kudoa in the spotted wolffish until 2003 detected in any of the muscle slices; moderate = pseudocysts 166 106 when an experimental rearing of this fish species was carried out detected in all muscle slices, total number 20–50; severe = pseud- 167 107 in land based tanks in Iceland. The major problems experienced ocysts detected in all muscle slices, total number >50. 168 108 during culture and harvest were persistent Kudoa infections in The size of 10 pseudocysts from each fish species (except the 169 109 muscles of the spotted wolffish. No data exists on Kudoa infections wild spotted wolfish) were measured and photographed using a 170 110 in northern wolffish. stereomicroscope. Morphological characteristics of 50 fresh spores 171 111 The aim of the present study was to identify and describe the from each fish species (except for spore length: n = 30 and length of 172 112 kudoid myxosporean responsible for the problems experienced polar filaments: n = 10) were measured following the recommen- 173 113 during the rearing of the spotted wolffish and to analyse the detri- dations of Lom and Arthur (1989) and Adlard et al.
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