Comparison of parasite communities of yellow perch (Perca flavescens) from Otsego and Canadarago Lakes Maggie Doolin 1, Jill Darpino 2, Elise Iwanyckyj 2, Sisina Macchiarelli 2, Zach Piper 2, Sam Vandemark 2, Timothy Pokorny 3, and Florian Reyda 4 INTRODUCTION Yellow perch (Perca flavescens) are freshwater fish, widespread and ubiquitous in the lakes of central New York. As both predator and prey, these fish play important roles in lake ecosystems. Since they have an exceedingly generalist diet plant material, fish, insect larvae and other arthropods, and more they access prey at multiple trophic levels and interact with many aspects of their shallow-water lake environment (Wilkins et al. 2002). Then, as prey for fish, birds, and mammals that hunt in a lake environment, they serve as junctions between the lowest and highest trophic levels of the lake ecosystem. Because of the important trophic role that they have within their ecosystems, yellow perch serve as common hosts for parasites with complex life cycles that require movement through the food web. Parasites whose final destination is a fish host and parasites that need a bridge from a low trophic level to the top levelpredators of the ecosystem both use yellow perch for transport from one life stage to the next. Although some parasites can be harmful to their host organisms, they are an important component of a healthy ecosystem (Marcogliese 2005). Successful parasite life cycles can clue management professionals into environmental quality, and plant and animal community composition because they rely on several levels of an ecosystem to be functioning correctly to have lasting populations. This is true even for many of the parasites that yellow perch host. For example, the presence of the nematode Eustrongylides tubifex ( red worm ) that is found in the body cavity of yellow perch indicates the presence of piscivorous birds like kingfishers, the final host in the life cycle of that nematode, and the presence of the thorny-headed worm Leptorhynchoides thecatus in the intestine of the fish tells of the presence of a specific group of amphipods, the first hosts in the life cycle of that thorny-headed worm. In central New York, few of the parasites that affect yellow perch seriously decrease their fitness, and none are infective to humans. The benefits of having the parasites in our lake ecosystems outweigh the drawbacks. The goals of this study were to catalog the full complement of yellow perch parasites found in Otsego and Canadarago Lakes during the winter months, and then to compare the parasite communities found in the fish of each lake. This was the first study in the Otsego area in which full necropsies were performed, as all past work had focused on parasites of the digestive system, and did not examine the other parts of the fish. A total of 31 fish 13 from Otsego Lake and 18 from Canadarago Lake that had been caught via ice fishing in January and February 2016 were examined by the authors from January to March 2016. Each organ was thoroughly examined for parasitic infections, and representatives of eight major groups were recovered: Nematoda, Acanthocephala, Cestoda, Trematoda, Monogenea, Annelida, Ciliata and other protists, and Myxozoa. Several differences were discovered between the parasite communities in 1 SUNY Oneonta graduate student, Biology Department, SUNY Oneonta 2 SUNY Oneonta undergraduate student, Biology Department, SUNY Oneonta 3 Aquatic Biologist 1, Region 4, New York State Department of Environmental Conservation 4 Associate Professor and Researcher, Biology Department and Biological Field Station, SUNY Oneonta
the yellow perch of the two lakes. Given that this was the first effort to complete full necropsies of yellow perch from these two lakes, follow-up work is anticipated in the 2017-2018 academic year. The lakes are isolated from one another, but given their relative geographic proximity, fish stocking, and frequent movement of fishermen (and, therefore, the possibility of fish and water transportation) between the two water bodies, we expected to find great overlap in parasite communities of the two lakes. METHODS Yellow perch were collected from Canadarago Lake and Otsego Lake via ice fishing in January and February of 2016. Fish were kept, live, in aquaria at the Biological Field Station until the time of dissection. On the day of dissection, fish were anesthetized following the guidelines of SUNY Oneonta IACUC Protocol 201303 in a solution of Tricaine-S and tap water (ratio of 0.3g/L) for 10 minutes, measured to the nearest millimeter, photographed for the laboratory s host records, and then examined. Full necropsies were completed, including scale scrapes that were examined under a compound light microscope, and examination of external surfaces and all organs under a stereoscope. Workers used saline solution (7.5g NaCl/1L H 2 O) to bathe organs, limiting desiccation. Any parasites found upon examination were moved to a clean dish filled with saline solution. For preservation, parasites were separated by taxon and by host organ. Parasites were preserved in 17 x 60 mm screw thread glass vials in preservative fluids that varied by taxon and purpose of preservation. Specimens that were to be used for morphological examination went in 70% ethanol (leeches, large nematodes, and arthropods), hot formalin (cestodes, trematodes, monogenes, and small nematodes), or tap water for 24 hours, then formalin (acanthocephalans). Specimens of difficult to preserve taxa such as Ciliata were not saved but were photographed using a Leica DSC295 digital camera on a Leica DM2500 compound microscope. Any specimens that were to be used for DNA sequence analysis were preserved in 100% moleculargrade ethanol and then kept in a cold room at 4 C. Permanent whole mount slides of parasites were prepared by hydrating specimens with a graded ethanol/water treatment, staining in Delafield s hematoxylin, and then dehydrating with a graded ethanol/water treatment. Specimens were then cleared with methyl salicylate and mounted in Canada balsam on 25x75mm glass slides with glass coverslips (22x22mm or 22x50mm). RESULTS The authors dissected thirty-one yellow perch 13 from Otsego Lake and 18 from Canadarago Lake for this study, attempting to gain perspective on the parasite communities from this species of fish in the two lakes. In total, there were 21 species of parasites representing six major parasitic groups recorded from both lakes (Table 1). The intestine was the organ both most often parasitized and also the organ with the highest species diversity. Although the majority of taxa were found in both lakes, there were some interesting differences. Ichthyophthirius multifiliis (a ciliate), Bunodera sacculata (a trematode), and an unidentified
amoeba were only found in fish from Otsego Lake, while Traenophorus crassus (a tapeworm), Dichelyne cotylophora (a nematode), Clinostomum marginatum and Crepidostomum cornutum (both trematodes), and an unidentified myxozoan were only found in Canadarago Lake. This study is the first record of Otsego Lake fishes carrying Ichthyophthirius multifiliis. Canadarago Lake fishes had highest prevalences of Clinostomum marginatum (10/18 fish), Eustrongylides tubifex (9/18), and unknown species of trematode metacercaria (9/18 fish). In contrast, Otsego Lake fishes had highest prevalences of Proteocephalus sp. (11/13 fish) and the ectocommensal protist Trichodina sp. (10/13 fish). Table 1. Records of parasite prevalence from 18 Canadarago Lake yellow perch and 13 Otsego Lake yellow perch. Parasites encountered are separated according to taxonomy and identified to as specific of a taxon as possible. Percentages listed represent prevalence of the parasite in the fishes examined from each lake (# of fish infected / # of fish examined). Canadarago n=18 Otsego n=13 Acanthocephala (thorny-headed worms) Neoechinorhynchus tenellus 28% 23% Leptorhynchoides thecatus 11% 15% Cestoda (tapeworms) Bothriocephalus sp. (adult) 6% 38% Proteocephalus sp. (adult) 17% 85% Traenophorus crassus 6% 0% Unknown (larval) 22% 23% Annelida (leeches) Piscicolaria sp. 11% 62% Monogenea Unknown 22% 38% Myxoza Unknown 6% 0% Nematoda (round worms) Dichelyne cotylophora 6% 0% Eustrongylides tubifex 50% 38% Unknown 11% 8% Ciliata/Protista Amoeba 0% 8% Ichthyophthirius multifiliis 0% 54% Trichodina sp. 33% 77% Unknown 22% 23% Trematoda (flukes) Azygia sp. 33% 46% Bunodera sacculata 0% 15% Clinostomum marginatum 56% 0% Crepidostomum cornutum 6% 0% Other metacercaria 50% 23%
DISCUSSION Prior to this study, several parasites had been recorded from yellow perch from both Otsego Lake and Canadarago Lake through examination efforts at the Biological Field Station. Since 2008, Dr. Florian Reyda has led a laboratory of undergraduate research students with a focus on recording parasites from local water bodies (e.g., Reyda 2010). Through these years of dedicated research, there had been a heavy emphasis on parasites of the digestive tract of these fish and relatively little investigation of other organs and external surfaces, resulting in incongruent records of parasite prevalence based on their site of infection. This study serves to establish a baseline of relative frequency of a larger range of parasite fauna than has been emphasized in past work in Dr. Reyda s laboratory, in Otsego and Canadarago Lakes. The study focused on yellow perch because of this species ecological habits and its position as both a predatory and prey animal in the shallow water lake ecosystem. In this study, fish from Canadarago Lake were, on average, smaller than those from Otsego Lake, and had fewer parasites. This finding could be a result of a couple of different factors. First, it could represent the inherent differences between lakes, including nutrient levels, fish growth parameters and general abundance of parasites in the ecosystems. Alternatively, it could be preliminary evidence that parasite communities in central New York yellow perch follow similar trends to those found by Johnson et al. (2004) in which parasite abundance and the rate at which perch acquire parasites increase with fish age and size. It will be interesting to follow up on these possibilities when there are more data available from next year s study. Hopefully future researchers will be able to shed light on the differences between fish size and parasite community assemblage, if such differences truly exist. In general, there were several interesting observations about the parasitic communities of these fish. First, Otsego Lake fishes, collected in February, had many fresh infections with juvenile tapeworms (sometimes up to 50 in one fish s intestine) of the genus Proteocephalus. Observations of this phenomenon had not been previously recorded, and authors hypothesize that this could be related to the Proteocephalus life cycle or to yellow perch feeding ecology, involving a fish s ingestion of the parasite larval stage in copepods at this time of year, and subsequent parasitic survival in the host gut. Canadarago Lake fish that were collected about one month earlier, in January 2016, did play host to these worms, but there was not the abundance of juveniles in these fish that there was in Otsego Lake fish. Another interesting observation was that researchers encountered the ciliate parasite Ichthyopthirius multifiliis (a.k.a. Ick ) in Otsego Lake fish. Although the relatively low density of fish in the wild restricts the spread of this organism, it can be an aquarium pest and did spread to all remaining fish in the holding aquarium in the laboratory within a few weeks of the fish being caught. If allowed to fester in a restricted amount of water, infections of Ick can proliferate and result in fish death. It is important to be aware of the presence of highly infective parasites like Ick so that they are not spread to water bodies or to people s home aquaria. This work has established baseline knowledge of parasite assemblages in both lakes, and the data gained will serve as important comparison points for future work by the Reyda Lab and others in the Northeastern USA. The authors did find differences in the parasite communities of the two lakes. Parasites unique to Otsego Lake include Ick and Bunodera sacculata, and those unique to Canadarago Lake include Dichelyne cotylophora, Clinostomum marginatum, and
Traenophorus crassus. Next steps include gathering more data to increase confidence that all parasites, even rare ones, that are infecting yellow perch in both lakes are recorded, and then trying to establish a better understanding of what governs the differences in parasite communities between lakes. REFERENCES Ecology and Natural Resources Collection. UW-Madison Libraries Digital Collection. 2015. Web. <http://digital.library.wisc.edu/1711.dl/econatres> Great Lakes Fishery Commission. Heterosporis sp. Yellow perch parasite. 2015. Web. <http://www.glfc.org/research/reports/marcquenski.pdf> Johnson, M.W., and Dick, T.A. 2001. Parasite effects on the survival, growth, and reproductive potential of yellow perch (Perca flavescens Mitchill) in Canadian Shield lakes. Can. J. Zool. 79: 1980-1992. Johnson, M.W., Nelson, P.A., and Dick, T.A. 2004. Structuring mechanisms of yellow perch (Perca flavescens) parasite communities: host age, diet, and local factors. Can. J. Zool., 82: 1291-1301. Marcogliese, D. 2005. Parasites of the superorganism: Are they indicators of ecosystem health? International Journal for Parasitology 35(7): 705-716. Reyda, F.B. 2010. Parasitic worms of fishes of Otsego Lake and nearby water bodies, 2009. In 42 nd Annual Report of the SUNY Oneonta Biological Field Station. Pp. 276 281. Spear, M. 2013. Infection of yellow perch (Perca flavescens) by black-spot parasites in a public and private lake. Student Project: University of Notre Dame. Wilkins, J.L., T.J. DeBates, and D.W. Willis. 2002. Food habits of yellow perch, Perca flavescens, in West Long Lake, Nebraska. Transactions of the Nebraska Academy of Sciences 28: 49-56.