Journal of Fish Biology (2009) 74, 961–966 doi:10.1111/j.1095-8649.2008.02166.x, available online at http://www.blackwell-synergy.com ‘Global worming’: first record of an epidemic of Triaenophorus crassus in a population of Arctic charr Salvelinus umbla D. A CHLEITNER *†, H. G ASSNER * AND R. S CHABETSBERGER ‡ *Federal Agency for Water Management, Institute of Water Ecology, Fisheries and Lake Research, Scharfling 18, 5310 Mondsee, Austria and ‡University of Salzburg, Department of Organismic Biology, Hellbrunnerstr. 34, 5020 Salzburg, Austria (Received 19 May 2008, Accepted 24 November 2008) In May 2005, an epidemic of the cestode Triaenophorus crassus occurred in the Salvelinus umbla population of Lake Grundlsee, an oligotrophic Austrian Alpine Lake. Based on catches with a standardized multi-mesh gillnet survey 53% of S. umbla were infected with up to 17 cysts of T. crassus per fish. This is the first documented record of an epidemic of this # 2009 The Authors tapeworm in S. umbla. Journal compilation # 2009 The Fisheries Society of the British Isles Key words: Alpine Lake; Cyclops abyssorum; Esox lucius; Salvelinus umbla; tapeworm; translocated fish. The Arctic charr Salvelinus umbla (L.) is a glacial relict species that was cut off from northern populations when glaciers retreated at the end of the last ice age. Landlocked stocks originally populated the lakes of the northern Alps, but the species was also transferred to water bodies south of the Alps as far as northern Italy (Doljan, 1920). Since medieval times S. umbla and whitefish Coregonus spp. have been the most important commercially exploited fish species in the Austrian lake district (Salzkammergut). Gassner et al. (2005) studied the fish communities of 43 lakes (>50 ha) in Austria and analysed all available historical documents recorded since the 13th century. Salvelinus umbla was classified as the sentinel (¼characteristic) species in 16 lakes. Among all those water bodies the cold, oligotrophic and dimictic Lake Grundlsee (47°389 N; 13°529 E) harboured one of the most important S. umbla fisheries in the country, and the first records are from 1280 AD. In the mid 18th century, the stock almost collapsed due to overexploitation, but catch restrictions allowed the population to recover (Wallner, 1911). During the 1970s, the average length of adult S. umbla decreased from c. 300 to 220 mm total length (LT), probably due to eutrophication and mismanagement (Jagsch, 1987). For >700 years, however, no parasites have been reported in the flesh of S. umbla. †Author to whom correspondence should be addressed. Tel.: þ43 6232/3847-35; fax: þ43 6232/3847-33; email: daniela.achleitner@baw.at 961 2009 The Authors Journal compilation # 2009 The Fisheries Society of the British Isles # 962 D. ACHLEITNER ET AL. In May 2005, a large outbreak of the cestode Triaenophorus crassus occurred in the Lake Grundlsee. The life cycle of T. crassus requires predaceous copepods and usually coregonid fishes as intermediate hosts and the pike Esox lucius L. as the definitive host (Williams & Jones, 1994). Although the parasite does not affect humans, the flesh of infected S. umbla is classified as ‘nauseous’ by Austrian food law and cannot be marketed. On 15 June 2005, the S. umbla fishery was closed and remains so. During the last century, the uncontrolled introduction of alien and translocated species increased throughout Europe, and natural fish communities were severely disturbed (Cowx, 1998; Zick et al., 2006). Originally, only eight fish species occurred in the Lake Grundlsee [S. umbla, lake trout Salmo trutta f. lacustris L., minnow Phoxinus phoxinus (L.), Danube bleak Chalcalburnus chalcoides (Güldenstädt), European chub Squalius cephalus (L.), bullhead Cottus gobio L., burbot Lota lota (L.) and stoneloach Barbatula barbatula (L.)]. Esox lucius were reported for the first time in Lake Grundlsee in 1966, although no records of stocking were available. They reproduced successfully and a viable population has established. In the 1980s perch Perca fluviatilis L. was introduced, probably by anglers releasing live baitfish. About 10 years ago, P. fluviatilis numbers started to increase. Based on a standardized gillnet survey in 2003 (EN 14757, 2005) P. fluviatilis dominated the catch (94% numbers and 66% mass). Coregonids (Coregonus spp.) were stocked for the first time in the 1920s and irregularly throughout the second half of the 20th century, but in contrast to the other two species they did not reproduce within this cold, oligotrophic Alpine lake. Large specimens (>2 kg) are caught infrequently, but the reason for failing to establish viable populations remains unknown. The fishery of the Lake Grundlsee is owned and managed by the Federal Forestry Agency. Besides one commercial licence, c. 60 angling licences are issued. Salvelinus umbla was the most important commercial species, and the yearly harvest was c. 1
4 kg ha1 (Total catch c. 600 kg). To determine the degree of infection of lake fish with plerocercoids of T. crassus, a survey was carried out from 26 to 28 June 2005. Multi-mesh gillnets were set randomly throughout the lake at 2–30 m (15 bottom-set nets, type Nordic, length 30 m, height 1
5 m and nine pelagic sets, type Nordic pelagic, length 27
5 m, height 6 m). In total, 2160 m2 of net were fished for 432 h. All fishes caught were determined to species level, weighed (M, g) and LT measured to the nearest mm. The fishes were examined for plerocercoid cysts by cutting the fillets transversally into c. 5 mm thick slices. Otoliths (sagittae) were removed and ground for age determination. Fulton’s condition factor (K) was calculated as: K ¼ 105  M L3 T : Two hundred and forty-four fishes, belonging to six different species, were caught (S. umbla, P. fluviatilis, C. chalcoides, L. lota, S. cephalus and Coregonus sp.). Salvelinus umbla dominated the catch by number (48
0%) and mass (67
0%). The translocated P. fluviatilis were almost as abundant (41
8%). The remaining species constituted only 10
2% by number and 16
4% by mass. Cysts with T. crassus plerocercoids were found only in the flesh of S. umbla and were externally visible as 10–15 mm diameter masses on the flanks of the fish (Fig. 1). Salvelinus umbla 130–390 mm LT were caught and the dominant Journal compilation # # 2009 The Authors 2009 The Fisheries Society of the British Isles, Journal of Fish Biology 2009, 74, 961–966 E P I D E M I C O F T. C R A S S U S I N S A LV E L I N U S U M B L A 963 LT class was 240 mm. Fifty-three per cent S. umbla sampled were infected with T. crassus, with one to 17 cysts per fish (Fig. 2). The proportion of infected fish increased with LT up to 350 mm. The few larger fish (>350 mm; n ¼ 2) in the catch carried no plerocercoids (Fig. 3). No significant difference was found between the K of infected and uninfected fish (Mann–Whitney U-test; median ¼ 0
78 both groups). Seventy-five per cent of fish of the age classes 5þ years were infected with T. crassus (Fig. 4). Young fish (<130 mm) were missing from the catch. Previous results show their catchability was low, because young S. umbla stay hidden in gravel (Zick et al., 2007). Preliminary data collected during 2007 indicate that infection rate had increased to >90%, and the maximum number of cysts per fish had risen to 29 (unpubl. obs.). Triaenophorus crassus, for which Coregonus spp. are normally intermediate hosts (Miller, 1952; Dick & Rosen, 1982; Rosen & Dick, 1984; Pulkkinen & Valtonen, 1999), has occurred as an epidemic for the first time in S. umbla. So far, T. crassus plerocercoids were found only occasionally in S. umbla (Lawler & Scott, 1954). Both, E. lucius and translocated Coregonus spp. could have been the vectors introducing the parasite into Lake Grundlsee. Coregonus spp. may have consistently contaminated the lake with parasites until 1998, when stocking was finally abandoned. Infected S. umbla had a remarkable appearance: clearly visible, large cysts were spread over their body (Fig. 1). Infected Coregonus spp. do not show these lumps, supposedly because their large scales cover the plerocercoids (Ulmer, 1971). In Coregonus spp., T. crassus plerocercoids have a live span of several years (Miller, 1952; Rosen & Dick, 1984) and they accumulate with age (Pulkkinen & Valtonen, 1999). Consequently, older (>5 years) and longer (>210 mm) S. umbla carried more plerocercoids. The largest S. umbla caught contained no plerocercoids, but sample size was too low to conclude that large fish are not infected. Infections with T. crassus are known to impair the growth of Coregonus spp. (Pulkkinen & Valtonen, 1999), and to cause serious damage in the muscles of FIG. 1. Typical cysts with plerocercoids of Triaenophorus crassus ( umbla. ) in the muscle tissue of Salvelinus 2009 The Authors Journal compilation # 2009 The Fisheries Society of the British Isles, Journal of Fish Biology 2009, 74, 961–966 # 964 D. ACHLEITNER ET AL. FIG. 2. Frequency of occurrence of Triaenophorus crassus cysts in Salvelinus umbla (n ¼ 117). experimentally infected fry (Dick & Rosen, 1982; Rosen & Dick, 1984). The growth and condition of S. umbla in Grundlsee may also have been affected, but a thorough analysis of glycogen or lipid contents of muscle tissue will be required to test for differences between healthy and infected fish. Given the long tradition and the high value of the local S. umbla fishery, this epidemic has severe socio-economic consequences in the area. Not only had the commercial S. umbla fishery to be closed but also valued angling licences are no longer issued for this species. The debate about health risks for humans caused anxiety in the local community. FIG. 3. Infection with plerocercoids of Triaenophorus crassus (n ¼ 117) in relation to total length (LT) of Salvelinus umbla ( , infected and , uninfected). Journal compilation # # 2009 The Authors 2009 The Fisheries Society of the British Isles, Journal of Fish Biology 2009, 74, 961–966 E P I D E M I C O F T. C R A S S U S I N S A LV E L I N U S U M B L A 965 FIG. 4. Infection with plerocercoids of Triaenophorus crassus (n ¼ 109) in relation to age of Salvelinus umbla ( , infected and , uninfected). The eradication of E. lucius will be a straightforward strategy to reduce the parasite populations, and it is already promoted by paying anglers for each fish. Nevertheless, as one adult cestode can release more than a million eggs (Bohl, 1966), it will take many years of intensive fishing to contain the epidemic. The ecosystem has been severely changed and may not return to the pristine conditions before the introduction of translocated fish species. We thank two anonymous referees for numerous suggestions that improved the manuscript. Funding for this study was provided by the Austrian Academy of Sciences and the Federal Forestry Agency. References Bohl, M. (1966). Über das Vorkommen des Bandwurmes Triaenophorus (Forel 1868) in oberbayerischen Seen. Allgemeine Fischereizeitung 19, 91. Cowx, I. G. (Ed.) (1998). Stocking and Introduction of Fish. Oxford: Blackwell Science. Dick, T. A. & Rosen, R. (1982). Experimental infections of whitefish, Coregonus clupeaformis (Mitchill), with Triaenophorus crassus Forel. Journal of Fish Diseases 5, 83–86. Doljan, E. (1920). Der Seesaibling (Salmo salvelinus) und seine wirtschaftliche Bedeutung. Österreichische Fischerei Zeitung 17, 86–104. EN 14757 (2005). Wasserbeschaffenheit – Probenahme von Fisch mittels Multi-MaschenKiemennetzen. Berlin: Beuth Verlag. 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