Abstract
In this paper, we describe three morphotypes of large parasitic copepods identified as Pennella Oken, 1815 (Siphonostomatoida, Pennellidae), which are found on the commercial fish Pacific saury Cololabis saira (Brevoort, 1856) (Beloniformes, Scomberesocidae). Of three morphotypes (Pennella sp. (PSP), parasite A (PA), and indeterminate individuals (IDI)), PSP had feather-like abdominal brushes and egg sacs which were characters typical of Pennella, PA lacked abdominal brushes and egg sacs, and IDI had few abdominal brushes but no egg sacs. Nucleotide sequence differences of mitochondrial cytochrome oxidase subunit I (COI) and nuclear ribosomal internal transcribed spacer 1 (ITS1) regions between types were small and comparable with differences within a type, indicating that the three types were conspecific. Mean body length of PSP was significantly larger than those of PA and IDI, suggesting types PA and IDI were immature morphs of PSP or individuals that had ceased development prior to maturation.
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Bower JE, Dowton M, Cooper RD, Beebe NW (2008) Intraspecific concerted evolution of the rDNA ITS1 in Anopheles farauti sensu stricto (Diptera: Culicidae) reveals recent patterns of population structure. J Mol Evol 67:397–411
Bucklin A, Guarnieri M, Hill RS, Bentley AM, Kaartvedt S (1999) Taxonomic and systematic assessment of planktonic copepods using mitochondrial COI sequence variation and competitive, species-specific PCR. Hydrobiologia 401:239–254
Bucklin A, Frost BW, Bradford-Grieve J, Allen LD, Copley NJ (2003) Molecular systematic and phylogenetic assessment of 34 calanoid copepod species of the Calanidae and Clausocalanidae. Mar Biol 142:333–343
Chow S, Nakagawa T, Suzuki N, Takeyama H, Matsunaga T (2006) Phylogenetic relationships among Thunnus tuna species inferred from rDNA ITS1 sequence. Mar Biotechnol 8:260–267
Chow S, Ueno Y, Toyokawa M, Oohara I, Takeyama H (2009) Preliminary analysis of length and GC content variation in the ribosomal first internal transcribed spacer (ITS1) of marine animals. Mar Biotechnol 11:301–306
Eberhardt RL (1954) Observations on the saury (Cololabis saira) seen near the California coast during 1950–51. Calif Fish Game 40:39–46
Food and Agriculture Organization of the United Nations (2017) FAO Fisheries and Aquaculture—statistics. http://www.fao.org/fishery/statistics/en. Accessed 20 September 2017
Folmer O, Black M, Hoen W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299
Fukushima S (1979) Synoptic analysis of migration and fishing conditions of saury in the northwest Pacific Ocean. Tohoku Reg Fish Res Lab 41:1–70 (In Japanese, with English abstract)
Hogans WE (1986) Redescription of Pennella instructa Wilson, 1917 (Copepoda: Pennellidae) from the swordfish (Xiphias gladius L.). Can J Zool 64:727–730
Hogans WE (1987a) Description of Pennella filosa L. (Copepoda: Pennellidae) on the ocean sunfish (Mola mola L.) in the Bay of Fundy. Bull Mar Sci 40:59–62
Hogans WE (1987b) Morphological variation in Pennella balaenoptera and P. filosa (Copepoda Pennellidae) with a review of the genus Pennella Oken, 1816 parasitic on Cetacea. Bull Mar Sci 40:442–453
Hogans WE (1988a) Redescription of Pennella sagitta (Copepoda: Pennellidae) from Histrio histrio (Pisces) in the North-West Atlantic Ocean with a provisional review of the genus Pennella. J Zool 216:379–390
Hogans WE (1988b) Pennella makaira, new species (Copepoda: Pennellidae) from the Atlantic blue marlin, Makaira nigricans, in the Caribbean Sea. Proc Biol Soc Wash 101:15–19
Hubbs CL, Wisner RL (1980) Revision of the sauries (Pisces, Scombersocidae) with descriptions of two new genera and one new species. Fish Bull 77:521–566
Hughes SE (1973) Some metazoan parasites of the eastern Pacific saury, Cololabis saira. Fish Bull 71:943–953
Kabata Z (1979) Parasitic Copepoda of British fishes. Ray Soc, London, UK
Kirtisinghe P (1935) Parasitic copepods of fish from Ceylon. Parasitology 27:332–344
Kosaka S, Watanabe Y, Tanino Y, Takahashi S (1985) Ecology of the Pacific saury Cololabis saira Brevoort, determined by the distribution of its parasite Pennella sp. Bull Tohoku Reg Fish Res Lab 47:79–91 (In Japanese, with English abstract)
Lazarus S, Sreenivasan PV (1977) On a copepod parasite, Pennella diodontis Oken, with epizoic cirrepede [sic.] Conchoderma virgatum Spengler on a new host Zanclus canascens (Linnaeus). Indian J Fish 24:204–206
Machida RJ, Miya MU, Nishida M, Nishida S (2006) Molecular phylogeny and evolution of the pelagic copepod genus Neocalanus (Crustacea: Copepoda). Mar Biol 148:1071–1079
Machida RJ, Tsuda A (2010) Dissimilarity of species and forms of planktonic Neocalanus copepods using mitochondrial COI, 12S, nuclear ITS, and 28S gene sequences. PLoS One 5:e10278
Nagasawa K (1984) The finding of Pennella sp. (Copepoda: Pennellidae) on the saury, Cololabis saira, in the western and central North Pacific Ocean and the Okhotsk Sea. Fish Pathol 18:205–208
Nagasawa K, Ishida K, Nakamura S (1984) Occurrence of Pennella sp. (Copepoda: Pennellidae) on the saury, Cololabis saira, in Japanese and central North Pacific waters in 1983. J Hokkaido Fish Exp Stat (Hokusuishi Geppo) 41:221–236 (In Japanese)
Nagasawa K, Imai Y, Ishida K (1985) Distribution, abundance, and effects of Pennella sp. (Copepoda: Pennellidae), parasitic on the saury, Cololabis saira (Brevoort), in the western North Pacific Ocean and adjacent seas, 1984. Bull Biogeogr Soc Jpn 40:35–42
Nagasawa K, Imai Y, Ishida K (1988) Long-term changes in the population size and geographical distribution of Pennella sp.(Copepoda) on the saury, Cololabis saira, in the western North Pacific Ocean and adjacent seas. Hydrobiologia 167:571–577
Øines Ø, Heuch PA (2005) Identification of sea louse species of the genus Caligus using mtDNA. J Mar Biol Assoc UK 85:73–79
Pascual S, Gestal C, Abollo E (1997) Effect of Pennella sp. (Copepoda, Pennellidae) on the condition of Illex coindetii and Todaropsis eblanae (Cephalopoda, Ommastrephidae). Bull. Eur. Ass. Fish Pathol 17:1–95
Presa P, Pardo BG, Martinez P, Bernatchez L (2002) Phylogeographic congruence between mtDNA and rDNA ITS markers in brown trout. Mol Biol Evol 19:2161–2175
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, 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
Sebastian MJ (1966) Observations on a few parasitic copepods from South India. Bull. Dep Mar Biol Ocean Univ Kerala 2:19–25
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729
Watanabe Y, Kosaka S, Tanino Y, Takahashi S (1985) Occurrence of parasitic copepod Pennella sp. on the Pacific saury Cololabis saira in 1983. Bull Tohoku Reg Fish Res Lab 47:37–46 (In Japanese, with English abstract)
Wilson CB (1917) North American parasitic copepods belonging to the Lernaeidae with a revision of the entire family. Proc US Nat Mus 47:568–729
Yamaguchi M, Honma T (1992) Parasitological study of the migration route of the Pacific saury, Cololabis saira, to the Okhotsk Sea. Sci Re Hokkaido Fish Exp Sn 39:35–44 (In Japanese, with English abstract)
Yasuike M, Leong J, Jantzen SG, von Schalburg KR, Nilsen F, Jones SR Koop BF (2012) Genomic resources for sea lice: analysis of ESTs and mitochondrial genomes. Mar Biotechnol 14:155–166
Acknowledgments
We thank the crews of the T/S Hokuho-maru from the Hokkaido Board of Education and the R/V Hokko-maru from Hokkaido National Fisheries Research Institute. We thank Dr. Dharmamony Vijai, Hachinohe Station, Tohoku National Fisheries Research Institute, for reviewing the manuscript. We also thank Dr. Kazuo Ogawa, Meguro Parasitological Museum, for access to closed-storage specimens of Pennella sp., and Dr. Masayasu Nakagami, Japan Fisheries Research and Education Agency, for assistance with collection of Pennella sp. We thank Ms. Junko Momosawa, Ms. Naoko Kubo, and Ms. Kanae Okabori of the Hachinohe station of the Tohoku National Fisheries Research Institute, for measuring Pacific saury and counting of Pennella sp.
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This work was partially supported by the Fisheries Agency of Japan.
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Suyama, S., Masuda, Y., Yanagimoto, T. et al. Genetic and morphological variation in Pennella sp. (Copepoda: Siphonostomatoida) collected from Pacific saury, Cololabis saira. Mar Biodiv 49, 1233–1245 (2019). https://doi.org/10.1007/s12526-018-0901-x
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DOI: https://doi.org/10.1007/s12526-018-0901-x