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Infection of Diplostomum spp. in invasive round gobies in the St Lawrence River, Canada

Published online by Cambridge University Press:  10 November 2021

D.J. Marcogliese Open the ORCID record for D.J. Marcogliese [Opens in a new window]  and
S.A. Locke
D.J. Marcogliese*
Affiliation:
Aquatic Contaminants Research Division, Water Science and Technology Directorate, Science and Technology Branch, Environment and Climate Change Canada, St Lawrence Centre, 105 McGill Street, 7th floor, Montreal, Quebec, H2Y 2E7, Canada St Andrews Biological Station, 125 Marine Science Drive, St Andrews, New Brunswick, E5B 0E4, Canada
S.A. Locke
Affiliation:
Department of Biology, University of Puerto Rico at Mayagüez, Box 9000, Mayagüez, Puerto Rico00681-9000, USA
*
Author for correspondence: D.J. Marcogliese, E-mail: david.marcogliese@ec.gc.ca
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Abstract

The round goby (Neogobius melanostomus) is a successful invader of the Great Lakes–St Lawrence River basin that harbours a number of local parasites. The most common are metacercariae of the genus Diplostomum. Species of Diplostomum are morphologically difficult to distinguish but can be separated using molecular techniques. While a few species have been sequenced from invasive round gobies in this study system, their relative abundance has not been documented. The purpose of this study was to determine the species composition of Diplostomum spp. and their relative abundance in round gobies in the St Lawrence River by sequencing the barcode region of cytochrome c oxidase I. In 2007–2011, Diplostomum huronense (=Diplostomum sp. 1) was the most common, followed in order by Diplostomum indistinctum (=Diplostomum sp. 4) and Diplostomum indistinctum sensu Galazzo, Dayanandan, Marcogliese & McLaughlin (2002). In 2012, the most common species infecting the round goby in the St Lawrence River was D. huronense, followed by D. indistinctum and Diplostomum gavium (=Diplostomum sp. 3). The invasion of the round goby in the St Lawrence River was followed by a decline of Diplostomum spp. in native fishes to low levels, leading to the previously published hypothesis that the presence of the round goby has led to a dilution effect. Herein, it is suggested that despite the low infection levels in the round goby, infections still may lead to spillback, helping to maintain Diplostomum spp. in native fishes, albeit at low levels.

Keywords

EyeflukesNeogobius melanostomusGreat Lakesriversinvasive speciesspillback
Type
Research Paper
Information
Journal of Helminthology , Volume 95 , 2021 , e64
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Achatz, TJ, Martensa, JR, Kostadinova, A, et al. (2021) Molecular phylogeny of Diplostomum, Tylodelphys, Austrodiplostomum and Paralaria (Digenea: Diplostomidae) necessitates systematic changes and reveals a history of evolutionary host switching events. International Journal for Parasitology (in press). doi: 10.1016/j.ijpara.2021.06.002.CrossRefGoogle ScholarPubMed
Camp, JW, Blaney, LM and Barnes, DK (1999) Helminths of the round goby, Neogobius melanostomus (Perciformes: Gobiidae), from southern Lake Michigan, Indiana. Journal of the Helminthological Society of Washington 66, 70–72.Google Scholar
Chappell, LH, Hardie, LJ and Secombes, CJ (1994) Diplostomiasis: the disease and host-parasite interactions. pp. 59–86 in Pike, AW and Lewis, JW (Eds) Parasitic diseases of fish. Dyfed, Samara Publishing Limited.Google Scholar
Désilets, HD, Locke, SA, McLaughlin, JD and Marcogliese, DJ (2013) Community structure of Diplostomum spp. (Digenea: Diplostomidae) in eyes of fish: main determinants and potential interspecific interactions. International Journal for Parasitology 43, 929–939.10.1016/j.ijpara.2013.07.002CrossRefGoogle ScholarPubMed
Dunn, AM and Hatcher, MJ (2015) Parasites and biological invasions: parallels, interactions, and control. Trends in Parasitology 31, 189–199.10.1016/j.pt.2014.12.003CrossRefGoogle ScholarPubMed
Essian, DA, Chipault, JG, Lafrancois, BM and Leonarda, JBK (2016) Gut content analysis of Lake Michigan waterbirds in years with avian botulism type E mortality, 2010–2012. Journal of Great Lakes Research 42, 1118–1128.10.1016/j.jglr.2016.07.027CrossRefGoogle Scholar
Galazzo, DE, Dayanandan, S, Marcogliese, DJ and McLaughlin, JD (2002) Molecular systematics of some North American species of Diplostomum (Digenea) based on rDNA sequence data and comparisons with European congeners. Canadian Journal of Zoology 80, 2207–2217.10.1139/z02-198CrossRefGoogle Scholar
Gendron, AD and Marcogliese, DJ (2017) Enigmatic decline of a common fish parasite (Diplostomum spp.) in the St. Lawrence River: evidence for a dilution effect induced by the invasive round goby. International Journal for Parasitology-Parasites and Wildlife 6, 402–411.10.1016/j.ijppaw.2017.04.002CrossRefGoogle Scholar
Gendron, AD, Marcogliese, DJ and Thomas, M (2012) Invasive species are less parasitized than native competitors, but for how long? The case of the round goby in the Great Lakes-St. Lawrence Basin. Biological Invasions 14, 367–384.10.1007/s10530-011-0083-yCrossRefGoogle Scholar
Hatcher, MJ, Dick, JTA and Dunn, AM (2012) Disease emergence and invasions. Functional Ecology 26, 1275–1287.10.1111/j.1365-2435.2012.02031.xCrossRefGoogle ScholarPubMed
Johnson, TB, Bunnell, DB and Knight, CT (2005) A potential new energy pathway in Central Lake Erie: the round goby connection. Journal of Great Lakes Research 31(Suppl. 2), 238–251.10.1016/S0380-1330(05)70317-8CrossRefGoogle Scholar
Kelly, DW, Paterson, RA, Townsend, CR, Poulin, R and Tompkins, DM (2009) Parasite spillback: a neglected concept in invasion ecology? Ecology 90, 2047–2056.10.1890/08-1085.1CrossRefGoogle ScholarPubMed
Kornis, MS, Mercado-Silva, N and Vander Zanden, MJ (2012) Twenty years of invasion: a review of round goby Neogobius melanostomus biology, spread and ecological implications. Journal of Fish Biology 80, 235–285.10.1111/j.1095-8649.2011.03157.xCrossRefGoogle ScholarPubMed
Kvach, Y and Stepien, CA (2008) Metazoan parasites of introduced round and tubenose gobies in the Great Lakes: support of the “enemy release hypothesis”. Journal of Great Lakes Research 34, 23–35.10.3394/0380-1330(2008)34[23:MPOIRA]2.0.CO;2CrossRefGoogle Scholar
Locke, SA, McLaughlin, JD, Dayanandan, S and Marcogliese, DJ (2010a) Diversity and specificity in Diplostomum spp. metacercariae in freshwater fishes revealed by cytochrome c oxidase I and internal transcribed spacer sequences. International Journal for Parasitology 40, 333–343.10.1016/j.ijpara.2009.08.012CrossRefGoogle Scholar
Locke, SA, McLaughlin, JD and Marcogliese, DJ (2010b) DNA barcodes show cryptic diversity and a potential physiological basis for host specificity among Diplostomoidea (Platyhelminthes: Digenea) parasitizing freshwater fishes in the St. Lawrence River, Canada. Molecular Ecology 19, 2813–2827.10.1111/j.1365-294X.2010.04713.xCrossRefGoogle Scholar
Locke, SA, McLaughlin, JD and Marcogliese, DJ (2013) Predicting the similarity of parasite communities in freshwater fishes using the phylogeny, ecology and proximity of hosts. Oikos 122, 73–83.10.1111/j.1600-0706.2012.20211.xCrossRefGoogle Scholar
Locke, SA, Al-Nasiri, FS, Caffara, M, et al. (2015) Diversity, specificity and speciation in larval Diplostomidae (Platyhelminthes: Digenea) in the eyes of freshwater fish, as revealed by DNA barcodes. International Journal for Parasitology 45, 841–855.10.1016/j.ijpara.2015.07.001CrossRefGoogle ScholarPubMed
Marcogliese, DJ and Compagna, S (1999) Diplostomatid eyeflukes in young-of-the-year and forage fishes in the St. Lawrence River, Quebec. Journal of Aquatic Animal Health 11, 275–282.10.1577/1548-8667(1999)011<0275:DEFIYO>2.0.CO;22.0.CO;2>CrossRefGoogle Scholar
Marcogliese, DJ, Dumont, P, Gendron, AD, Mailhot, Y, Bergeron, E and McLaughlin, JD (2001) Spatial and temporal variations in abundance of Diplostomum sp. in walleye (Stizostedion vitreum) and white sucker (Catostomus commersoni) from the St. Lawrence River. Canadian Journal of Zoology 79, 355–369.10.1139/z00-209CrossRefGoogle Scholar
Morissette, O, Paradis, Y, Pouliot, R and Lecomte, F (2018) Spatio-temporal changes in littoral fish community structure along the St. Lawrence River (Québec, Canada) following round goby (Neogobius melanostomus) invasion. Aquatic Invasions 13, 501–512.10.3391/ai.2018.13.4.08CrossRefGoogle Scholar
Moszczynska, A, Locke, SA, McLaughlin, JD, Marcogliese, DJ and Crease, TJ (2009) Development of primers for the mitochondrial cytochrome c oxidase I gene in digenetic trematodes (Platyhelminthes) illustrates the challenge of barcoding parasitic helminths. Molecular Ecology Resources 9, 75–82.10.1111/j.1755-0998.2009.02634.xCrossRefGoogle ScholarPubMed
Muzzall, PM, Peebles, R and Thomas, MV (1995) Parasites of the round goby, Neogobius melanostomus, and tubenose goby, Proterohinus marmoratus (Perciformes: Gobiidae), from the St. Clair River and Lake St. Clair, Michigan. Journal of the Helminthological. Society of Washington 62, 226–228.Google Scholar
Paterson, RA, Townsend, CR, Tompkins, DM and Poulin, R (2012) Ecological determinants of parasite acquisition by exotic fish species. Oikos 121, 1889–1895.10.1111/j.1600-0706.2012.20143.xCrossRefGoogle Scholar
Paterson, RA, Rauque, CA, Fernandez, MV, Townsend, CR, Poulin, R and Tompkins, DM (2013) Native fish avoid parasite spillback from multiple exotic hosts: consequences of host density and parasite competency. Biological Invasions 15, 2205–2218.10.1007/s10530-013-0445-8CrossRefGoogle Scholar
Poulin, R, Paterson, RA, Townsend, CR, Tompkins, DM and Kelly, DW (2011) Biological invasions and the dynamics of endemic diseases in freshwater ecosystems. Freshwater Biology 56, 676–688.10.1111/j.1365-2427.2010.02425.xCrossRefGoogle Scholar
Pronin, NM, Fleischer, GW, Baldahova, DR and Pronina, SV (1997) Parasites of the round goby (Neogobius melanostomus) and tubenose goby (Proterohinus marmoratus) (Cottidae) from the St. Clair River and Lake St. Clair, Michigan, USA. Folia Parasitologica 44, 1–6.Google Scholar
Reyjol, Y, Brodeur, P, Mailhot, Y, Mingelbier, M and Dumont, P (2010) Do native predators feed on non-native prey? The case of round goby in a fluvial piscivorous fish assemblage. Journal of Great Lakes Research 36, 618–624.10.1016/j.jglr.2010.09.006CrossRefGoogle Scholar
Rohr, JR, Civitello, DJ, Halliday, FW, Hudson, PJ, Lafferty, KD, Wood, CL and Mordecai, EA (2020) Towards common ground in the biodiversity-disease debate. Nature Ecology & Evolution 4, 24–33.10.1038/s41559-019-1060-6CrossRefGoogle ScholarPubMed
Stewart Merrill, TE and Johnson, PTJ (2020) Towards a mechanistic understanding of competence: a missing link in diversity-disease research. Parasitology 147, 1159–1170.10.1017/S0031182020000943CrossRefGoogle ScholarPubMed