First record of Proliferative Kidney Disease in Iceland

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1 Bull. Eur. Ass. Fish Pathol., 30(1) 2010, 35 NOTE First record of Proliferative Kidney Disease in Iceland Á. Kristmundsson 1 *, T. Antonsson 2 and F. Árnason 2 1 Institute for Experimental Pathology, University of Iceland, Keldur v/vesturlandsveg, IS-112 Reykjavik, Iceland; 2 Institute of Freshwater Fisheries, Keldnaholti, IS-112, Reykjavík, Iceland Abstract Proliferative kidney disease caused by the myxozoan parasite Tetracapsuloides bryosalmonae is reported for the first time in Iceland. Infections were confirmed in both arctic charr and brown trout but only arctic charr showed clinical signs. The last two decades, populations of arctic charr in several lakes in Iceland have greatly declined. Possible relation of this decline with increasing water temperature has been speculated. It is hypothesized that PKD may play a significant role in this decline. Studies on the distribution of PKD and its effect on wild populations of arctic charr and brown trout in Iceland are presently in progress. For decades, Proliferative kidney disease (PKD) has been considered one of the most serious diseases of farmed salmonids in Europe and North America, causing mortality up to 90% (Cli on-hadley et al., 1984; Hedrick et al., 1993). The impact on wild fish populations is however poorly known. The causative agent is a myxozoan species Tetracapsuloides bryosalmonae whose life cycle involves different species of freshwater Bryozoa (Anderson et al., 1999; Canning et al., 1999; Longshaw et al., 1999). Most salmonid species are susceptible to infections and one non-salmonid, northern pike (Esox lucius L.), has been reported to show myxozoan forms resembling those observed in PKD infected salmonids (Bucke et al., 1991). Since the year 2007, a study investigating the prevalence of Renibacterium salmoninarum infections in the Ellidaár river system has been in progress with emphasis on Atlantic salmon, Salmo salar L. Part of the material was resident arctic charr, Salvelinus alpinus (L.), and brown trout, Salmo tru a L., from Lake Ellidavatn (64 06 N and W). Lake Ellidavatn is a shallow spring fed lake (mean depth 1.5m) with a surface area of 1.5 km 2 and a water volume approx. 2.7 million m 3. Two rivers flow into the lake and it is discharged into river Ellidaár (rate of flow approx. 5 m 3 /s). In addition to arctic charr and brown trout the lake harbours eel Anguilla anguilla (L.), three spined stickleback Gasterosteus aculeatus L. and migrating Atlantic salmon. * Corresponding author s arnik@hi.is

2 Bull. Eur. Ass. Fish Pathol., 30(1) 2010, 36 Fish were sampled on October 3 rd 2008, using a series of gillnets of monofilament nylon with mesh sizes mm (knot-to-knot). This combination of mesh sizes sampled arctic charr and brown trout in the length interval of cm. A total of 18 arctic charr and 60 brown trout were examined. During dissection, three of 18 charr showed clinical signs resembling proliferative kidney disease, i.e. extensive renal swelling (kidney 4 to 5 times normal size) with a pale mo led like appearance. None of the trout showed clinical signs. Kidney samples from these three charr were fixed in 10% buffered formalin for histological examination. No further examination was made on fish without clinical signs. Giemsa- and HE stained histological sections showed extensive numbers of forms resembling extrasporogonic stages of Tetracapsuloides bryosalmonae (Figure 1A). For confirmation, immunohistochemistry was applied using Mab against T. bryosalmonae (Aquatic Diagnostics Ltd) (Figure 1B). In light of these results, six arctic charr (length cm) and 41 brown trout (length cm) from a nearby lake, Lake Vifilsstadavatn, were sampled on November 21 st 2008, using the same mesh size combination of gillnet series as described before. Lake Vífilsstadavatn is a shallow spring fed lake (mean depth 0.5m) with a surface area of 0.27 km 2 and discharged into a small brook. Apart from arctic charr and brown trout, the lake is inhabited by eels and three spined sticklebacks. All fish sampled were screened for the presence of T. bryosalmonae; none of which had clinical signs of PKD. However, examination of stained histological slides (HE and immunostaining) showed all six charr and 5 of the 41 brown trout to be infected with T. bryosalmonae. Infections were very light, only few forms detected in each sample which in many cases seemed to be degenerating. This is the first report of PKD in Iceland and consequently extends its known geographic distribution which is wide; found in various species of salmonids in most European countries and North America (e.g. Cli on- Hadley et al., 1984; Hedrich et al., 1993). As mentioned before, the impact of PKD on wild salmonid populations is in general poorly known. However, PKD is thought to be an important factor in the extreme decline of wild populations of brown trout in Swiss rivers (Wahli et al., 2002). Furthermore, PKD is considered the main cause of mass mortality of Atlantic salmon fry in Norwegian rivers in the years and 2006, reducing the smolt production in River Åelva by 50-75% (Forseth et al., 2007; Sterud et al., 2007). In both these cases an increase in temperature due to global warming is mentioned as a potential factor intensifying the effect of PKD on salmonid populations. The last two decades, populations of arctic charr in several lakes in Iceland, including Lake Ellidavatn and Lake Vifilsstadavatn, have greatly declined. Populations of brown trout in these lakes have however remained steady during this same period (Einarsson and Árnason, 2001; Antonsson et al., 2007; Bjarnadó ir, 2007; Malmquist et al., 2009). Possible reasons for this decline have been studied in Lake Ellidavatn. The most likely

3 Bull. Eur. Ass. Fish Pathol., 30(1) 2010, 37 Figure 1. Histological sections of kidney of arctic charr from Lake Ellidavatn showing numerous exstrasporogonic stages of Tetracapsuloides bryosalmonae. (A) HE staining, (B) immunostaining.

4 Bull. Eur. Ass. Fish Pathol., 30(1) 2010, 38 factor of influence is thought to be the water temperature which significantly increased in all summer months from 1988 to 2006, e.g. the mean temperature in August ( 14 C in 2006) increasing of 2.3 C over the period (Antonsson et al., 2007, Malmquist et al., 2009).. However, the nature of this relationship remains to be explained. PKD is associated with rising temperature, symptoms most frequently occurring when temperature reaches 12 to 15 C and above (Morris et al., 2005; Tops et al., 2006). Given that T. bryosalmonae is widespread in the lakes examined, one could assume that many of the older fish in these lakes have previously been exposed to the pathogen and acquired resistance. The great majority of the fish examined in present study ranged from 20 to 45 cm in length (age 2 to 8 years). Of the three fish showing clinical sign of PKD, two were of age group 1+ and one 2+. This leads to speculations regarding the effect on the younger fish in the lakes being exposed to the pathogen for the first time. Previous studies have shown that infected fish that recover from the disease are resistant to further infection (Foott and Hedrick, 1987). Consequently, juvenile fish (fry and fingerlings) are generally more susceptible to infections than older fish. Our results demonstrate the presence of T. bryosalmonae in the lakes Ellidavatn and Vífilsstadavatn. Furthermore, the results indicate that arctic charr is more susceptible to PKD than brown trout; three of 18 arctic charr from Lake Ellidavatn showed clinical signs of PKD but none of the 40 trout examined. The prevalence in arctic charr from Lake Vífilsstadavatn was also much higher than in brown trout, i.e. 100% and 12%, respectively. The limited studies made on PKD in arctic charr have shown this species to be extremely susceptible to PKD (Brown et al., 1991; Kent et al., 2000). According to these studies, arctic charr seem to develop PKD at a lower temperature than other salmonid species (Brown et al., 1991; Kent et al., 2000). This could possibly be the case for brown trout and arctic charr in Iceland. Tetracapsuloides bryosalmonae occurs in a broad range of bryozoan hosts (Anderson et al., 1999; Longshaw et al., 1999; Okamura and Wood, 2002) but species of the genera Plumatella and Fredericella are considered the most important hosts (Okamura and Wood, 2002). Five bryozoan species, i.e. Plumatella fungosa, P. repens, Fredericella sultana, Hyalinella punctata and Christatella mucedo, have been found in Icelandic lakes (Steingrimsson, 1985). Two of them, F. sultana and P. repens, have been studied in the Lake Urridakotsvatn which is about 5 km away from Lake Ellidavatn and 2 km from Lake Vífilsstadavatn. Even though the existence of bryozoans has not been confirmed in Lake Ellidavatn and Lake Vífilsstadavatn, in light of our results one must assume they do. We hypothesize that PKD, as a consequence of increased temperature in Lake Ellidavatn, could be a considerable factor of significance in the declining population of arctic charr in the lake. Extensive studies on the distribution of PKD and its effect on wild populations of arctic charr and brown trout in Iceland are presently in progress.

5 Bull. Eur. Ass. Fish Pathol., 30(1) 2010, 39 References Anderson CL, Canning EU and Okamura B (1999). Molecular data implicate bryozoans as hosts for PKX (Phylum Myxozoa) and identify clade of bryozoan parasites within the Myxozoa. Parasitology 119, Antonsson Th, Árnason F and Guðjónsson S (2007). [A survey on the fish populations in the water catchment area of the Ellidaár-river system in 2006]. Report no. VMST-R/07011, 34 pp. Institute of Freshwater Fisheries, Reykjavík. (In Icelandic.) Bjarnadó ir KS (2007). [The ecology of arctic charr Salvelinus alpinus (L.) and brown trout Salmo tru a L. in lakes Ellidavatn, Hafravatn and Vífilsstadavatn]. B.Sc. honours thesis, 39 pp. University of Iceland, Reykjavik. (In Icelandic.) Brown JA, Thonney J-P, Holwell D and Wilson WR (1991). A comparison of the susceptibility of Salvelinus alpinus and Salmo salar ouananiche to proliferative kidney disease. Aquaculture 96, 1-6. Bucke, D, Feist, SW and Cli on-hadley, RS (1991). The occurrence of proliferative kidney disease (PKD) in cultured and wild fish: further investigations. Journal of Fish Diseases 14, Canning EU, Curry A, Feist SW, Longshaw M and Okamura B (1999) Tetracapsula bryosalmonae n.sp. for PKX organism, the cause of PKD in salmonid fish. Bulletin of the European Association of Fish Pathologists 19, Cli on-hadley RS, Bucke D and Richards RH (1984). Proliferative kidney disease of salmonid fish: a review. Journal of Fish Diseases 7, Einarsson SM and Árnason F (2001). [A survey on fish populations in lakes in Svínadal]. Report no. VMST-R/01004, 17 pp. Institute of Freshwater Fisheries, Reykjavík,. (In Icelandic.) Foo JS and Hedrick RP (1987). Seasonal occurrence of the infectious stage of proliferative kidney disease (PKD) and resistance of rainbow trout, Salmo gairdneri Richardson, to reinfection. Journal of Fish Biology 30, Forseth T, Jørgensen A. and Mo TA (2007). [Mapping of PKD in Norwegian salmon rivers]. NINA rapport 259, 12pp. National Veterinary Institute, Trondheim. (In Norwegian.) Hedrich RP, MacConell E and de Kinkilin P (1993). Proliferative kidney disease of salmonid fish. Annual review of Fish diseases 3, Kent ML, Kha ra J, Hedrick RP and Devlin RH (2000). Tetracapsula renicola n. sp. (Myxozoa: Saccosporidae); The PKX myxozoan The cause of proliferative kidney disease of salmonid fishes. Journal of Parasitology 86, Longshaw M, Feist SW, Canning EU and Okamura B (1999) First identification of PKX in bryozoans from the United Kingdom - molecular evidence. Bulletin of the European Association of Fish Pathologists 19, Malmquist HJ, Antonsson Th, Ingvason HR, Ingimarsson F and Árnason F (2009). Salmonid fish and warming of shallow Lake Ellidavatn in SW-Iceland. Verhandlungen der Internationalen Vereinigung für Limnologie 30, Morris DJ, Ferguson HW and Adams A (2005). Severe, chronic proliferative kidney disease (PKD) induced in rainbow trout Onchorhynchus mykiss held at a constant 18 C. Diseases of Aquatic Organisms 66, Okamura B and Wood TS (2002). Bryozoans as hosts for Tetracapsula bryosalmonae, the PKX organism. Journal of Fish Diseases 25, Steingrimsson SA (1985). [Bryozoans in Lake

6 Bull. Eur. Ass. Fish Pathol., 30(1) 2010, 40 Urriðakotsvatn]. Ná úrufræðingurinn 55, (In Icelandic.) Sterud E, Forseth T, Ugedal O, Poppe TT, Jorgensen A, Bruheim T, Fjeldstad HP and Mo TA (2007). Severe mortality in wild Atlantic salmon Salmo salar due to proliferative kidney disease (PKD) caused by Tetracapsuloides bryosalmonae (Myxozoa). Diseases of Aquatic Organisms 77, Tops S, Lockwood W and Okamura B (2006). Temperature-driven proliferation of Tetracapsuloides bryosalmonae in bryozoan hosts portend salmonid decline. Diseases of Aquatic Organisms 70, Wahli T, Knuesel R, Bernet D, Segner H, Pugovkin D, Burkhardt-Holm P, Escher M and Scmidt-Posthaus H (2002). Proliferative kidney disease in Switzerland: current state of knowledge. Journal of Fish Diseases 25,

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