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Ligulosis Associated with Mortality in Largescale Suckers

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Ligulosis Associated with Mortality in Largescale Suckers Journal of Fish Biology (2002) 61, 448–455 doi:10.1006/jfbi.2002.2051, available online at http://www.idealibrary.com on Ligulosis associated with mortality in largescale suckers B. A. S*‡, K. L. G†, C. R* R. B* *Department of Fisheries and Wildlife, Oregon State University, 104 Nash Hall, Corvallis, OR 97331, U.S.A. and †USDA Forest Service, NFJD Ranger District, Highway 244, Ukiah, OR 97880, U.S.A. (Received 4 December 2001, Accepted 27 June 2002) Investigations of a fish kill at an irrigation reservoir in the Deschutes River basin, Oregon, documented at least 153 dead largescale suckers Catostomus macrocheilus, all heavily infected with large Ligula intestinalis (Cestoda). Moribund fish nearshore were similarly infected, with no evidence of secondary disease or infection. Morbidity and mortality in all cases was probably due to severe mechanical damage to internal host organs resulting from infection with multiple, large L. intestinalis. The pathology of L. intestinalis documented in largescale sucker in this study contrasts sharply with previous accounts and may represent a new and emerging disease for largescale suckers. 2002 The Fisheries Society of the British Isles Published by Elsevier Science Ltd. All rights reserved. Key words: Ligula intestinalis; largescale sucker; Catostomus macrocheilus; plerocercoid; wildlife infection. INTRODUCTION Several species of cestode have been implicated in mass fish kills, including Ligula intestinalis (Bloch). The pathogenic nature of L. intestinalis in cyprinids in Europe has been discussed in detail (Arme & Owen, 1968; Bauer et al., 1973; VanDuijn, 1973; Sweeting, 1977; Dubinina, 1980; Scha¨perclaus, 1991; Arme 1997b), but infections reported in North American populations of catostomids have not been extensive (Lawler, 1964; Dauble, 1985). Pathogenesis was noted recently in bridgelip sucker Catostomus columbianus (Eigenmann & Eigenmann) in the Crooked River of central Oregon after infection with unusually large L. intestinalis (Groves & Shields, 2001), but prevalence was low and mortality was not documented. In the present study an apparent L. intestinalis-induced mortality of largescale suckers Catostomus macrocheilus Girard in Haystack Reservoir was investigated. MATERIALS AND METHODS STUDY AREA Filled in 1957, Haystack Reservoir is part of the North Unit Irrigation District of Central Oregon, and is supplied with water diverted from the Deschutes River just north of the city of Bend. It is located in Jefferson County, Oregon at 443001 N; 121912 W. The reservoir is managed for recreational fisheries for rainbow trout Oncorhynchus mykiss (Walbaum), brown trout Salmo trutta L., kokanee Oncorhynchus nerka ‡Author to whom correspondence should be addressed. Tel.: +1 541 737 1939; fax: +1 541 737 3590; email: [email protected] 448 0022–1112/02/080448+08 $35.00/0 2002 The Fisheries Society of the British Isles. Published by Elsevier Science Ltd. All rights reserved. 449 (Walbaum), brown bullhead Ameiurus nebulosus (Lesueur) and centrarchids, including largemouth bass Micropterus salmoides (Lecepe´de), bluegill Lepomis macrochirus Rafinesque and black crappie Pomoxis nigromaculatus (Lesueur). Surface area and depth of the reservoir varies with seasonal and daily water use, with a useable storage of 2280 ha, maximum capacity of 3116 ha, a maximum depth of 24 m and an average depth of 8·1 m. Water clarity in the reservoir at the time of the study was very good, with snorkelling visibility of up to 3 m. No algal blooms were noted, and no other affected or dead fish species were observed. Input of water from the supply canal increased water level by nearly 1·5 m during the 5 h collection and observation period on 7 April 2001. Water temperature was c. 5 C and air temperature fluctuated between 0–8 C. DATA COLLECTION AND ANALYSIS Observations of fish were made from shore as well as underwater with SCUBA gear, but dead suckers observed by SCUBA were not included in total mortality counts. Fish and bird mortalities were counted through a survey on foot around the perimeter of the reservoir, during which all wildlife species observed (and their feeding activity) were noted. Plerocercoid ingestion by wildlife was confirmed from direct observation of feeding and inferred from the presence of plerocercoids in faeces. Body cavities of dead fish were opened to determine presence or absence of L. intestinalis and associated tissue damage, but were not studied further due to the advanced state of specimen decay. Live fish were captured by angling with bait, hand nets, jigging, spear and snagging. All fish were euthanized with clove oil (Cho & Heath, 2000) immediately after capture. Total length (LT) and mass (M) were measured for each fish before the body cavity was opened. All plerocercoids were removed, measured, and weighed. Host gonad development, as well as tissue and organ damage, was documented. Plerocercoids were identified according to Hoffman (1998). A modified Fulton’s condition factor KF (Simpkins & Hubert, 1996) was calculated for 5 3 each fish from KF=10 MLT , where M is in g and LT is in mm. The parasite index (IP) 1 was calculated from IP=100 (total mass of parasites) (total mass of host plus parasites) (Arme & Owen, 1968), where IP=50 would indicate a mass of L. intestinalis equal to M, the mass of the host’s body. Regression analysis of data was performed with StatGraphics Plus (StatGraphics, 1998). RESULTS A total of 153 dead largescale suckers (all heavily infected with L. intestinalis) as well as abundant L. intestinalis-infected wildlife faeces were documented during the shoreline survey. Heavily infected fish were slow swimming and ‘ docile ’ to the approach of observers, yet two live fish with plerocercoids protruding from abscesses in the host body wall, as observed elsewhere in the basin (Groves & Shields, 2001), evaded capture. ‘ Free-living ’ L. intestinalis plerocercoids (Barus et al., 1997) were observed moving actively on the sub- stratum in shallow waters after emerging from the body walls of fish hosts. Animals ingesting plerocercoids included ducks Anas sp. L. and Mergus sp. L., geese Branta canadensis L., gulls Larus sp. L., great blue heron Ardea herodias L., Brewer’s blackbird Euphagus cyanocephalus Wagler, osprey Pandion haliaetus L., river otter Lutra canadensis Schreber and mink Mustella vison Schreber. Other wildlife observed in the area, but for which there was no direct or indirect evidence of L. intestinalis ingestion included scrub jay Aphelocoma coerulescens Bosc, raven Corvus corax L., belted kingfisher Megaceryle alcyon L., raccoon Procyon lotor L. and coyote Canis latrans Say. A great blue heron and Brewer’s blackbird, both recently dead and in emaciated condition, were found near the 450 . . reservoir, but necropsies could not be performed to confirm L. intestinalis infection due to a lack of scientific permits. Only one of 18 live largescale suckers collected was uninfected, indicating a prevalence of 94%. Infected fish were characterized by a firm, distended abdomen, with discrete ‘ lumps ’ externally visible and palpable. Most of the fish examined contained multiple plerocercoids with up to 12 in the body cavity of a single host (Table I). The sex of heavily infected fish with vestigial gonads could be readily determined from external secondary sexual characteristics, with intense spawn- ing colours, pearl organs and elongated anal fins in males compared to uninfected fish observed elsewhere. This is an indication that L. intestinalis- induced castration may not inhibit spawning activity completely in largescale suckers, consistent with reports from European populations of large cyprinids (Sweeting, 1977; Scha¨perclaus, 1991). Pathology observed in largescale suckers from the current study was comparable with reports from other species. This included liver degeneration and necrosis (Arme & Owen, 1968), internal haem- orrhages and adhesions (Sweeting, 1977), organ compression and displacement (Bauer & Stolyarov, 1961), parasitic castration (Orr, 1966; Arme, 1997a) and emaciation (Bauer & Stolyarov, 1961). Fish with severely reduced livers also had greatly enlarged gall bladders, symptomatic of anorexia. Plerocercoids were interwoven among the mesenteries and organs of the fish, and were constricted at several points along their bodies by adhesions, consistent with larval migrans exhibited by L. intestinalis plerocercoids infecting an ‘ unpreferred ’ fish host (Orr, 1968). Variation in the size, colour and dimensions of the plerocercoids was consider- able. Plerocercoid length-mass-width relationships were all positive but not well correlated with prevalence or host size or condition. Plerocercoids stored in plastic bags on ice for up to 1 week after removal from fish hosts subsequently matured and produced fertile eggs when cultured in vitro, evidence of the duration of viability of ‘ free-living ’ plerocercoids in the cold water of the reservoir. Host condition declined with level of infection (Fig. 1). Although intensity of infection increased with host LT (indicating cumulative lifetime burdens of L. intestinalis), IP values were negatively correlated with host size (Fig. 2). Higher IP values in smaller hosts suggest a lack of compensatory inhibition of parasite growth within the physical constraints imposed by a smaller host body. Such proportionally large masses of parasites may be incompatible with host survival, especially of smaller hosts. DISCUSSION Despite anecdotal accounts, there is no mention of L. intestinalis infection in the Crooked River Basin
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