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Black sea bass are a host in the developmental cycle of Lernaeenicus radiatus (Copepoda: Pennellidae): insights into parasite morphology, gill pathology and genetics

Published online by Cambridge University Press:  19 December 2019

J. Lovy Open the ORCID record for J. Lovy [Opens in a new window]  and
S. E. Friend
J. Lovy*
Affiliation:
Office of Fish and Wildlife Health and Forensics, N.J. Division of Fish and Wildlife, 605 Pequest Road, Oxford, NJ07863, USA
S. E. Friend
Affiliation:
Office of Fish and Wildlife Health and Forensics, N.J. Division of Fish and Wildlife, 605 Pequest Road, Oxford, NJ07863, USA
*
Author for correspondence: J. Lovy, E-mail: Jan.Lovy@dep.nj.gov
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Abstract

Lernaeenicus radiatus, a mesoparasitic pennellid copepod, has long been known in the northwest Atlantic with metamorphosed females infecting the muscle of marine fish. The study herein is the first to identify a definitive first host, black sea bass Centropristis striata, for L. radiatus supporting larval development to adults and sexual reproduction in the gills. This finding suggests a two-host life cycle for L. radiatus, with black sea bass as the first host. Heavy infections in the gill were associated with considerable pathology related to a unique and invasive attachment process that penetrated the gill and selectively attached to the gill filament cartilage. The morphology of the developing copepod was highly conserved with that of a related pennellid copepod, Lernaeocera branchialis, though was distinguished by the attachment process, unique pigmentation and other morphologic features described herein. Sequencing the small and large subunits of the ribosomal RNA and mitochondrial cytochrome c oxidase subunit I genes demonstrated L. radiatus to share closer identities with Lernaeocera and Haemobaphes spp. pennellid copepods rather than other Lernaeenicus spp. available in GenBank to date. Taxonomy of L. radiatus is discussed in relation to life cycles, tissue tropism, morphology and genetics of other closely related pennellid copepods.

Keywords

Black sea bassgeneticsgill pathologyLernaeenicus radiatuslife cyclePennellidae.
Type
Research Article
Information
Parasitology , Volume 147 , Issue 4 , April 2020 , pp. 478 - 490
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Copyright
Copyright © Cambridge University Press 2019

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References

Atlantic States Marine Fisheries Commission (ASMFC) (2018) Black Sea Bass. http://www.asmfc.org/species/black-sea-bass (Accessed 3 September 2019).Google Scholar
Barta, JR, Martin, DS, Liberator, PA, Dashkevicz, M, Anderson, JW, Feighner, SD, Elbrecht, A, Perkins-Barrow, A, Jenkins, MC, Danforth, HD, Ruff, MD and Profous-Juchelka, H (1997) Phylogenetic relationships among eight Eimeria species infecting domestic fowl inferred using complete small subunit ribosomal DNA sequences. Journal of Parasitology 83, 262–271.CrossRefGoogle ScholarPubMed
Brooker, AJ, Shinn, AP and Bron, JE (2007) A review of the biology of the parasitic copepod Lernaeocera branchialis (L., 1767) (Copepoda: Pennellidae). Advances in Parasitology 65, 297–341.CrossRefGoogle Scholar
Castro-Romero, R, Montes, MM, Martorelli, SR, Sepulveda, D, Tapia, S and Martínez-aquino, A (2016) Integrative taxonomy of Penuculus, Metapeniculus, and Trifur (Siphonostomatoida: Pennellidae), copepod parasites of marine fishes from Chile: species delimitation analyses using DNA barcoding and morphological evidence. Systematics and Biodiversity 14, 466–483.CrossRefGoogle Scholar
Folmer, O, Black, M, Hoeh, W, Lutz, R and Vrijenhoek, R (1994) DNA Primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.Google ScholarPubMed
Hales, LS, Able, KW (1995) Effects of oxygen concentration on somatic and otolith growth rates of juvenile black sea bass, Centropristis striata. In Secor, DH, Dean, JM and Campana, SE (eds), Recent Developments in Fish Otolith Research. Belle W. Baruch Library in Marine Science 19. University of South Carolina Press, pp. 135–153.Google Scholar
Hasegawa, M, Kishino, H and Yano, T (1985) Dating the human-ape split by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution 22, 160–174.CrossRefGoogle Scholar
Hogans, WE (2018) Functional morphology and structural variability in Lernaeenicus (Copepoda: Pennellidae) parasitic on teleost fishes from the northwest Atlantic Ocean. Comparative Parasitology 85, 13–26.CrossRefGoogle Scholar
Hvas, M, Karlsbakk, E, Mæhle, S, Wright, DW and Oppedal, F (2017) The gill parasite Paramoeba perurans compromises aerobic scope, swimming capacity and ion balance in Atlantic salmon. Conservation Physiology 5, 1–12.CrossRefGoogle Scholar
Ismail, N, Ohtsuka, S, Maran, BAV, Tasumi, S, Zaleha, K and Yamashita, H (2013) Complete life cycle of a pennellid Peniculus Minuticaudae Shiino, 1956 (Copepoda: Siphonostomatoida) infecting cultured threadsail filefish, Stephanolepis cirrhifer. Parasite 20, 42.CrossRefGoogle ScholarPubMed
Izawa, K (2019) Redescription of Lernaeenicus ramosus Kirtisinghe, 1956 (Copepoda, Siphonostomatoida, Pennellidae), with description of its male and the postnaupliar developmental stages. Crustaceana 92, 119–128.CrossRefGoogle Scholar
Jones, MEB and Taggart, CT (1998) Distribution of gill parasite (Lernaeocera branchialis) infection in northwest Atlantic cod (Gadus morhua) and parasite-induced host mortality: inferences from tagging data. Canadian Journal of Fisheries and Aquatic Sciences 55, 364–375.CrossRefGoogle Scholar
Kabata, Z (1961) Lernaeocera branchialis (L.) a parasitic copepod from the European and the American shores of the Atlantic. Crustaceana 2, 243–249.CrossRefGoogle Scholar
Kabata, Z (1965) Systematic position of the copepod Lernaeocera centropristi. Proceedings of the Zoological Society of London 144, 351–360.CrossRefGoogle Scholar
Kabata, Z (1970) Book I: Crustacea as enemies of fish. In Snieszko, SF and Axelrod, HR (eds), Diseases of Fish. Jersey City, NJ, USA: T.F.H Publications, pp. 1–171.Google Scholar
Kabata, Z (1979) Parasitic Copepoda of British Fishes. London, UK: Ray Society.Google Scholar
Khan, RA (1988) Experimental transmission, development, and effects of a parasitic copepod, Lernaeocera branchialis, on Atlantic cod, Gadus morhua. Journal of Parasitology 74, 586–599.CrossRefGoogle ScholarPubMed
Khan, RA, Lee, EM and Barker, D (1990) Lernaeocera branchialis: a potential pathogen to cod ranching. Journal of Parasitology 76, 913–917.CrossRefGoogle ScholarPubMed
Khodami, S, McArthur, JV, Blanco-Bercial, L and Arbizu, PM (2017) Molecular phylogeny and revision of copepod orders (Crustacea: Copepoda). Scientific Reports 7, 9164.CrossRefGoogle Scholar
Kumar, S, Stecher, G, Li, M, Knyaz, C and Tamura, K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35, 1547–1549.CrossRefGoogle ScholarPubMed
Lester, RJG and Hayward, CJ (2006) Phylum Arthropoda. In Woo, PTK (ed.), Fish Diseases and Disorders. Volume 1 Protozoan and Metazoan Infections, 2nd Edn. Oxfordshire, UK: CAB International, pp. 466–565.CrossRefGoogle Scholar
Luna, LG (1968) Manual of Histologic Staining Methods of the Armed Forces Institute of Pathology, 3rd Edn. NY, USA: Blakiston Division, McGraw-Hill Inc.Google Scholar
Pearse, AS (1947) Parasitic copepods from Beaufort, North Carolina. Journal of the Elisha Mitchell Scientific Society 63, 1–16.Google Scholar
Powell, MD and Gamperl, AK (2016) Effects of Loma morhua (Microsporidia) infection on the cardiorespiratory performance of Atlantic cod Gadus morhua (L). Journal of Fish Diseases 39, 189–204.CrossRefGoogle Scholar
Raja, K, Saravanakumar, A, Gopalakrishnan, A, Vijayakumar, R, Hwang, UW and Maran, BAV (2016) The genus Lernaeenicus Lesuer (Copepoda, Siphonostomatoida, Pennellidae) in India: a checklist with notes on its taxonomy and ecology. Zootaxa 4174, 192–211.CrossRefGoogle Scholar
Raupach, MJ, Barco, A, Steinke, D, Beermann, J, Laakmann, S, Mohrbeck, I, Neumann, H, Kihara, TC, Pointner, K, Radulovici, A, Segelken-Voigt, A, Wesse, C and Knebelsberger, T (2015) The application of DNA barcodes for the identification of marine crustaceans from the North Sea and adjacent regions. PLOS ONE 10, e0139421.CrossRefGoogle ScholarPubMed
Schram, TA (1979) The life history of the eye-maggot of the sprat Lernaeenicus sprattae (Sowerby) (Copepoda, Lernaeoceridae). Sarsia 64, 279–316.CrossRefGoogle Scholar
Sherman, K and Wise, JP (1961) Incidence of the cod parasite Lernaeocera branchialis L. in the New England area, and its possible use as an indicator of cod populations. Limnology and Oceanography 6, 61–67.CrossRefGoogle Scholar
Song, Y, Wang, GT, Yao, WJ, Gao, Q and Nie, P (2008) Phylogeny of freshwater parasitic copepods in the Ergasilidae (Copepoda: Poecilostomatoida) based on 18S and 28S rDNA sequences. Parasitology Research 102, 299–306.CrossRefGoogle ScholarPubMed
Speare, DJ and Ferguson, HW (2006) Gills and Pseudobranchs. In Ferguson, HW (ed.), Systemic Pathology of Fish: A Test and Atlas of Normal Tissues in Teleosts and Their Responses in Disease. London, UK: Scotian Press, pp. 24–63.Google Scholar
Sproston, NG (1942) The developmental stages of Lernaeocera branchialis (Linn.). Journal of the Marine Biological Association of the United Kingdom 25, 441–466.CrossRefGoogle Scholar
Templeman, W, Hodder, VM and Fleming, AM (1976) Infection of lumpfish (Cyclopterus lumpus) with larvae and of Atlantic cod (Gadus morhua) with adults of the copepod, Lernaeocera branchialis, in and adjacent to the Newfoundland area, and inferences therefrom on inshore-offshore migrations of cod. Journal of the Fisheries Research Board of Canada 33, 711–731.CrossRefGoogle Scholar
Van Damme, PA and Ollevier, F (1995) Morphological and morphometric study of crustacean parasites within the genus Lernaeocera. International Journal for Parasitology 25, 1401–1411.CrossRefGoogle ScholarPubMed
Voorhees, JT and Schwartz, FJ (1979) Attachment site, seasonality, and effects of the parasitic copepod Lernaeenicus radiatus on two estuarine fishes in the Cape Fear River, North Carolina. Transactions of the American Fisheries Society 108, 191–196.2.0.CO;2>CrossRefGoogle Scholar
Walter, TC and Boxshall, G (2018) World of copepods database. Lernaeenicus Lesueur, 1824. Accessed at: http://www.marinespecies.org/copepoda/aphia.php?p=taxdetails&id=135644 on 2019-12-02.Google Scholar
Watanabe, WO (2011) Species profile: black sea bass. Southern Regional Aquaculture Center 7207, https://agrilifecdn.tamu.edu/fisheries/files/2013/09/SRAC-Publication-No.-7207-Species-Profile-Black-Sea-Bass.pdf (Accessed 3 September 2019).Google Scholar
Whipps, CM, Fournie, JW, Morrison, DA, Azevedo, C, Matos, E, Thebo, P and Kent, ML (2012) Phylogeny of fish-infecting Calyptospora species (Apicomplexa: Eimeriorina). Parasitology Research 111, 1331–1342.CrossRefGoogle Scholar
Whitfield, PJ, Pilcher, MW, Grant, HJ and Riley, J (1988) Experimental studies on the development of Lernaeocera branchialis (Copepoda: Pennellidae): population processes from egg production to maturation on the flatfish host. Hydrobiologia 167/168, 579–586.CrossRefGoogle Scholar
Wilson, CB (1917) North American Parasitic copepods belonging to Lernaeidae, with a revision of the entire family. Proceedings US National Museum 53, 2194.CrossRefGoogle Scholar
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