Journal of Great Lakes Research 36 (2010) 18–28 Contents lists available at ScienceDirect Journal of Great Lakes Research journal homepage: www.elsevier.com/locate/jglr Widespread infection of lake whitefish Coregonus clupeaformis with the swimbladder nematode Cystidicola farionis in northern lakes Michigan and Huron Mohamed Faisal a,b,⁎, Walied Fayed a,c, Travis O. Brenden a,d, Abdelaziz Noor c, Mark P. Ebener e, Gregory M. Wright f, Michael L. Jones a,d a Department of Fisheries and Wildlife, Michigan State University, East Lansing, MI 48824, USA b Department of Pathobiology and Diagnostic Investigation, Michigan State University, East Lansing, MI 48824, USA c Faculty of Agriculture, Alexandria University, Alexandria, Egypt d Quantitative Fisheries Center, Department of Fisheries and Wildlife, Michigan State University, 153 Giltner Hall, East Lansing, MI 48824–1101, USA e Chippewa Ottawa Resource Authority, 179 East Three Mile Road, Sault Ste. Marie, MI 49783, USA f Nunns Creek Fishery Enhancement Facility, HC 47, Box 8100, Hessel, MI 49745, USA article info abstract Article history: We estimated the prevalence, intensity, and abundance of swimbladder nematode infection in 1281 lake Received 3 August 2009 whitefish (Coregonus clupeaformis) collected from four sites in northern lakes Huron (Cheboygan and DeTour Accepted 11 January 2010 Village) and Michigan (Big Bay de Noc and Naubinway) from fall 2003 through summer 2006. Morphological examination of nematode egg, larval, and mature stages through light and scanning electron microscopy Communicated by Trent M. Sutton revealed characteristics consistent with that of Cystidicola farionis Fischer 1798. Total C. farionis prevalence was 26.94%, while the mean intensity and abundance of infection was 26.72 and 7.21 nematodes/fish, Index words: Lake whitefish respectively. Although we detected C. farionis in all four stocks that were examined, Lake Huron stocks Cystidicola farionis generally had higher prevalence, intensity, and abundance of infection than Lake Michigan stocks. A distinct Swimbladder pathology seasonal fluctuation in prevalence, abundance, and intensity of C. farionis was observed, which does not Lake Michigan coincide with reported C. farionis development in other fish species. Lake whitefish that were heavily Lake Huron infected with C. farionis were found to have thickened swimbladder walls with deteriorated mucosa lining, which could affect swimbladder function. Whether C. farionis infection may be negatively impacting lake whitefish stocks in the Great Lakes is unclear; continued monitoring of C. farionis infection should be conducted to measure responses of lake whitefish stocks to infection levels. © 2010 Elsevier B.V. All rights reserved. Introduction depends on several factors, including fish age, parasite and intermediate host abundance, and water temperature (Knudsen et al., 2002, 2004). Nematodes of the genus Cystidicola Fischer 1798 (Habronematoidea: Lake whitefish (Coregonus clupeaformis) in North America have Cysticolidae) are parasitic in the swimbladders of physostomus fishes in been found to be susceptible to infection with C. farionis (Lankester the Northern hemisphere. Presently, two species of Cystidicola are and Smith, 1980). However, maturation of C. farionis in lake whitefish recognized: C. farionis and C. stigmatura. C. farionis Fischer 1798 in North America is regarded as atypical, which has led some parasitizes the swimbladders of rainbow smelt (Osmerus mordax)and researchers to theorize that it is a new Cystidicola sp. infecting lake Coregonus, Oncorhynchus,andSalvelinus spp. from Eurasia and North whitefish and not C. farionis (Lankester and Smith, 1980; Dextrase, America, while C. stigmatura Leidy 1886 parasitizes Salvelinus spp. from 1987). In Lake Nipigon, Canada, lake whitefish have been found to be North America (Black, 1983). Through their physical movements and routinely infected with large numbers of immature C. farionis, but no production of toxic metabolites, Cystidicola spp. cause destruction of the mature nematodes have been found in infected individuals (Lankester highly vascularized swimbladder walls, which can affect swimming and Smith, 1980). Immature nematodes are also common in Lake performance and buoyancy control of infected individuals (Lankester Superior lake whitefish, but only small numbers of mature nematodes and Smith, 1980; Black, 1984; Willers et al., 1991; Dzeikonska-Rynko have been found (Lankester and Smith, 1980). Buccal cavity structure et al., 2003). The infection rate of Cystidicola spp. in fish populations and eggs from C. farionis found in lake whitefish exhibit morphol- ogical characteristics that are slightly different when compared to eggs collected from other susceptible species in the same environ- ment (Dextrase, 1987; Miscampbell et al., 2004). Despite these ⁎ Corresponding author. S-110 Plant Biology Building, Michigan State University, East Lansing, Michigan 48824, USA. atypical characteristics, extensive genetic studies using samples from E-mail address: [email protected] (M. Faisal). both Canada and Finland have failed to find sequence differences in 0380-1330/$ – see front matter © 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.jglr.2010.01.008 M. Faisal et al. / Journal of Great Lakes Research 36 (2010) 18–28 19 ribosomal DNA among mature C. farionis nematodes in lake white- (BBN), Naubinway (NAB), Cheboygan (CHB), and DeTour Village fish and other susceptible species, which has led researchers to (DET). The BBN and NAB stocks are located in northern Lake Michigan, conclude that it is indeed C. farionis that is infecting lake whitefish while the CHB and DET stocks are located in northern Lake Huron (Miscampbell et al., 2004). (Fig. 1). Each of these areas has large spawning aggregations of lake In the Laurentian Great Lakes of North America, lake whitefish whitefish, and although b50 km separates some of these locations, is a commercially, ecologically, and culturally important species individuals have been found to display strong fidelity to these areas (Fleischer, 1992; Ebener et al., 2008). The invasion and spread of zebra during the spawning season (Ebener and Copes, 1985; Ebener et al., (Dreissena polymorpha) and quagga mussels (D. bugensis) in the Great 2010). Lakes have been associated with significant declines in lake whitefish Collection of lake whitefish from each of the stocks began in condition, growth, and recruitment (Hoyle et al., 1999; Pothoven fall 2003, and continued seasonally through summer 2006. For the et al., 2001; Mohr and Ebener, 2005). These declines are believed purpose of this study, fall is considered to encompass the months to have been caused primarily from declines in indigenous benthic of October through December, winter encompasses the months of macroinvertebrates, Diporeia spp. in particular, as a result of January through March, spring encompasses the months of April dreissenid invasion in the Great Lakes (Pothoven et al., 2001; Mills through June, and summer encompasses the months of July through et al., 2005; Nalepa et al., 2005). The absence of Diporeia spp. in large September. Additionally, for the purpose of this study, fall 2003 areas of the Great Lakes has resulted in lake whitefish increasing through summer 2004 is identified as the 2004 sampling year; fall consumption of other benthic macroinvertebrates, including dreisse- 2004 through summer 2005 is identified as the 2005 sampling year; nid mussels, gastropods, opossum shrimp (Mysis relicta), ostracods, and fall 2005 through summer 2006 is identified as the 2006 sampling oligochaetes, and zooplankton (Hoyle et al., 1999; Pothoven et al., year. Because of inclement weather conditions, no lake whitefish were 2001; Pothoven, 2005; Hoyle, 2005). Because benthic macroinverte- collected from the CHB stock in fall 2006 or from the NAB stock in brates are known to be immediate hosts for C. farionis, a question has winter 2004. Total numbers of lake whitefish collected and examined been raised whether changes in feeding habits of lake whitefish may for swimbladder nematodes during each sampling period ranged have led to changes in the extent of swimbladder nematode infection from 15 to 35 fish/stock (Table 1). or exacerbated its pathologic impacts. The objectives of this study Sampling locations were typically chosen by contract fishermen were to: (1) identify the species of swimbladder nematodes in lake based on prior commercial catches. Lake whitefish were collected whitefish collected from four lake whitefish stocks in northern lakes using a combination of commercial traps and gill nets. Captured lake Huron and Michigan; (2) measure the prevalence, abundance, and whitefish were transferred (alive or recently dead and shipped on ice) intensity of the swimbladder nematodes in these stocks; (3) evaluate to the Michigan State University-Aquatic Animal Health Laboratory in variations in larval stage development and maturation among the East Lansing, MI for immediate processing. Once at the laboratory, live stocks; and (4) assess the damage to lake whitefish swimbladders fish were sacrificed with an overdose (300 mg/liter) of Tricaine caused by the nematode infection. Methanesulfonate (MS-222, Argent Chemicals, Redmond, WA). Methods Parasite identification and swimbladder pathology Study area and fish sampling The swimbladder from each lake whitefish was removed intact, dissected, and swimbladder walls examined for the presence of mac- We studied four lake whitefish stocks, two in northern Lake Huron roscopic lesions. Swimbladder nematodes