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Morphology of pelagic fish eggs identified using mitochondrial DNA and their distribution in waters west of the Mariana Islands

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Abstract

Fish eggs collected in the West Mariana region of the western North Pacific (7°–18°N, 137°–144°E) were identified using mitochondrial 16S ribosomal RNA (16S rRNA) gene sequences, and their morphology and distribution were analyzed. Of the 5,321 eggs collected, 2,698 live eggs were morphologically divided into 108 types based on the character of shape, diameter, chorion, oil globule, pigmentation, yolk segmentation and perivitelline space. Excluding 20 types of formalin preserved eggs, partial sequences of 16S rRNA gene (1,019–1,190 base pairs) obtained for all remaining 88 types of ethanol preserved eggs were compared with sequences deposited in the DDBJ/EMBL/GenBank using Basic Local Alignment Search Tool. This resulted in 16 species being genetically identified and their morphological characters were observed including the first description of the eggs of three species, Ventrifossa garmani, Diodon hystrix, and Scopelogadus mizolepis. Distribution analysis showed that 52–100% eggs of eight species, Katsuwonus pelamis, D. hystrix, S. mizolepis, Thunnus spp., Xiphias gladius, Cepalopholis spp., Naso spp. and V. garmani were collected around seamounts of the West Mariana region, whereas the other eight species, Lampris guttatus, Oxyporhamphus micropterus, Ranzania laevis, Istiophorus platypterus, Exocoetidae spp., Lactoria diaphana, Tetrapturus angustirostris and Regalecus glesne showed no tendency to be concentrated around the seamounts and were widely distributed through the study area. These distributional patterns of eggs appeared to correspond well with the life histories of each species. The present study suggests that DNA species identification can provide a significant new tool for ecological studies on fish eggs.

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References

  • Aboussouan A, Leis JM (1984) Balistoidei: development. In: Moser HG, Richards WJ, Cohen DM, Fahay MP, A W Kendall J, Richardson SL (eds) Ontogeny and systematics of fishes. Am Soc Ichthyol Herpetol Spec Publ 1, pp 451–459

  • Ahlstrom EH, Moser HG (1980) Characters useful in identification of pelagic marine fish eggs. CalCOFI Rep 21:121–131

    Google Scholar 

  • Ahlstrom EH, Amaoka K, Hensley DA, Moser HG, Sumida BY (1984) Pleuronectiformes: development. In: Moser HG, Richards WJ, Cohen DM, Fahay MP, A W Kendall J, Richardson SL (eds) Ontogeny and systematics of fishes. Am Soc Ichthyol Herpetol Spec Publ 1, pp 640–670

  • Akimoto S, Kinoshita S, Sezaki K, Mitani I, Watabe S (2002) Identification of alfonsino and related fish species belonging to the genus Beryx with mitochondrial 16S rRNA gene and its application on their pelagic eggs. Fish Sci 68:1242–1249

    Article  CAS  Google Scholar 

  • Akimoto S, Itoi S, Sezaki K, Borsa P, Watabe S (2006) Identification of alfonsino, Beryx mollis and B-splendens collected in Japan, based on the mitochondrial cytochrome b gene, and their comparison with those collected in New Caledonia. Fish Sci 72:202–207

    Article  CAS  Google Scholar 

  • Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  PubMed  Google Scholar 

  • Aoyama J, Watanabe S, Nishida M, Tsukamoto K (2000) Discrimination of catadromous eels of genus Anguilla using polymerase chain reaction-restriction fragment length polymorphism analysis of the mitochondrial 16S ribosomal RNA domain. Trans Am Fish Soc 129:873–878

    Article  CAS  Google Scholar 

  • Aoyama J, Ishikawa S, Otake T, Mochioka N, Suzuki Y, Watanabe S, Shinoda A, Inoue J, Lokman PM, Inagaki T, Oya M, Hasumoto H, Kubokawa K, Lee TW, Fricke H, Tsukamoto K (2001) Molecular approach to species identification of eggs with respect to determination of the spawning site of the Japanese eel Anguilla japonica. Fish Sci 67:761–763

    Article  CAS  Google Scholar 

  • Bayha KM, Graham WM, Hernandez FJ (2008) Multiplex assay to identify eggs of three fish species from the northern Gulf of Mexico, using locked nucleic acid Taqman real-time PCR probes. Aquat Biol 4:65–73

    Google Scholar 

  • Chow S, Kishino H (1995) Phylogenetic relationships between tuna species of the genus Thunnus (Scombridae: Teleostei): inconsistent implications from morphology, nuclear and mitochondrial genomes. J Mol Evol 41:741–748

    Article  CAS  PubMed  Google Scholar 

  • Collette BB, Nauen CE (1983) FAO species catalogue. Vol. 2. Scombrids of the world. An annotated and illustrated catalogue of tunas, mackerels, bonitos and related species known to date. FAO Fish Synop 2:137

    Google Scholar 

  • Daniel LB, Graves JE (1994) Morphometric and genetic identification of eggs of spring-spawning sciaenids in lower Chesapeake Bay. Fish Bull 92:254–261

    Google Scholar 

  • Dower JF, Perry RI (2001) High abundance of larval rockfish over Cobb Seamount, an isolated seamount in the Northeast Pacific. Fish Oceanogr 10:268–274

    Article  Google Scholar 

  • Fritzsche RA (1978) Chaetodontidae through Ophidiidae, vol V. Fish and Wildlife Service. U.S. Dept. of the Interior, Fort Collins

    Google Scholar 

  • Froese R, Pauly D (2009) FishBase. World Wide Web electronic publication. www.fishbase.org, version (06/2009)

  • Fujikura K, Tsuchida S, Ueno H, Ishibashi J, Gaze W, Maki Y (1998) Investigation of the deep-sea chemosynthetic ecosystem and submarine volcano at the Kasuga 2 and 3 seamounts in the Northern Mariana trough, Western Pacific. JAMSTEC J Deep Sea Res 14:127–138

    Google Scholar 

  • García-Vázquez E, Álvarez P, Lopes P, Karaiskou N, Pérez J, Teia A, Martínez JL, Gomes L, Triantaphyllidis C (2006) PCR-SSCP of the 16S rRNA gene, a simple methodology for species identification of fish eggs and larvae. Sci Mar 70(Suppl 2):13–21

    Google Scholar 

  • Graves JE, Curtis MJ, Oeth PA, Waples RS (1990) Biochemical genetics of southern california basses of the genus Paralabrax-Specific identification of fresh and ethanol-fixed individual eggs and early larvae. Fish Bull 88:59–66

    Google Scholar 

  • Hernández-Vázquez S (1994) Distribution of eggs and larvae from sardine and anchovy off California and Baja California, 1951–1989. CalCOFI Rep 35:94–107

    Google Scholar 

  • Humphreys RL (2000) Otolith-based assessment of recruitment variation in a North Pacific seamount population of armorhead Pseudopentaceros wheeleri. Mar Ecol Prog Ser 204:213–223

    Article  Google Scholar 

  • Hyde JR, Lynn E, Humphreys R, Musyl M, West AP, Vetter R (2005) Shipboard identification of fish eggs and larvae by multiplex PCR, and description of fertilized eggs of blue marlin, shortbill spearfish, and wahoo. Mar Ecol Prog Ser 286:269–277

    Article  CAS  Google Scholar 

  • Johns GC, Avise JC (1998) A comparative summary of genetic distances in the vertebrates from the mitochondrial cytochrome b gene. Mol Biol Evol 15:1481–1490

    Google Scholar 

  • Karaiskou N, Apostolidis AP, Triantafyllidis A, Kouvatsi A, Triantaphyllidis C (2003) Genetic identification and phylogeny of three species of the genus Trachurus based on mitochondrial DNA analysis. Mar Biotechnol 5:493–504

    Article  CAS  PubMed  Google Scholar 

  • Karaiskou N, Triantafyllidis A, Alvarez P, Lopes P, Garcia-Vazquez E, Triantaphyllidis C (2007) Horse mackerel egg identification using DNA methodology. Mar Ecol Evol Persp 28:429–434

    CAS  Google Scholar 

  • Leis JM (1977) Development of the eggs and larvae of the slender mola, Ranzania laevis (Pisces, Molidae). Bull Mar Sci 27:448–466

    Google Scholar 

  • Leis JM, Moyer JT (1985) Development of eggs, larvae and pelagic juveniles of three Indo-Pacific Ostraciid fishes (Tetraodontiformes): Ostracion meleagris. Lactoria fornasini and L. diaphana. Jpn J Ichthol 32:189–202

    Google Scholar 

  • Manaresi S, Mantovani B, Zaccanti F (2001) Egg to adult identification of 13 freshwater fishes from Italy: a biochemical-genetic key. Aquat Sci 63:182–190

    Article  Google Scholar 

  • McDowell JR, Graves JE (2002) Nuclear and mitochondrial DNA markers for specific identification of istiophorid and xiphiid billfishes. Fish Bull 100:537–544

    Google Scholar 

  • Meyer A (1993) Evolution of mitochondrial DNA in fishes. In: Hochacka PW, Mommsen TP (eds) Molecular biology frontiers. Elsevier, Amsterdam, pp 1–38

    Google Scholar 

  • Mito S (1961) Pelagic fish eggs from Japanese waters-I. Clupeina, Chanina, Stomiatina, Myctophyda, Anguillida, Belonida and Syngnathida. Sci Bull Fac Agr Kyusyu Univ 18:285–310

    Google Scholar 

  • Miya M, Nishida M (1996) Molecular phylogenetic perspective in the evolution of the deep-sea fish genus Cyclothone (Stomiiformes: Gonostomatidae). Ichthyol Res 43:375–398

    Article  Google Scholar 

  • Mork J, Solemdal P, Sundnes G (1983) Identification of marine fish eggs: a biochemical genetics approach. Can J Fish Aquat Sci 40:361–369

    CAS  Google Scholar 

  • Naganuma A (1979) On spawning activities of skipjack tuna in the western Pacific Ocean. Bull Tohoku Reg Fish Res Lab 40:1–13

    Google Scholar 

  • Nakamura I (1985) FAO species catalogue. Vol. 5. Billfishes of the world. An annotated and illustrated catalogue of marlins, sailfishes, spearfishes and swordfishes known to date. FAO Fish Synop 125:65

    Google Scholar 

  • Olney JE (1984) Lampriformes: development and relationships. In: Moser HG, Richards WJ, Cohen DM, Fahay MP, A W Kendall J, Richardson SL (eds) Ontogeny and systematics of fishes. Am Soc Ichthyol Herpetol Spec Publ 1, pp 368–379

  • Onishi Y, Ikeda T, Hiroishi S, Okiyama M (2003) Identification of pelagic fish eggs using monoclonal antibody. Nippon Suisan Gakkaishi 69:170–177

    Google Scholar 

  • Orlowski SJ, Herman SS, Malsberger RG, Pritchard HN (1971) Distinguishing cunner and tautog eggs by immunodiffusion. J Fish Res Board Can 29:111–112

    Google Scholar 

  • Paine MA, McDowell JR, Graves JE (2007) Specific identification of western Atlantic Ocean scombrids using mitochondrial DNA cytochrome c oxidase subunit I (COI) gene region sequences. Bull Mar Sci 80:353–367

    Google Scholar 

  • Paine MA, McDowell JR, Graves JE (2008) Specific identification using COI sequence analysis of scombrid larvae collected off the Kona coast of Hawaii Island. Ichthyol Res 55:7–16

    Article  Google Scholar 

  • Ratnasingham S, Hebert PDN (2008) BOLD management and analysis system. www.barcodinglife.com. Accessed 4 Apr 2008

  • Rogers AD (1994) The biology of seamounts. Adv Mar Biol 30:304–350

    Google Scholar 

  • Sezaki K, Kuboshima Y, Mitani I, Fukui A, Watabe S (2001) Identification of chub and spotted mackerels with mitochondrial cytochrome b gene and its application to respective pelagic eggs fixed with formalin. Nippon Suisan Gakkaishi 67:17–22

    CAS  Google Scholar 

  • Shao KT, Chen KC, Wu JH (2002) Identification of marine fish eggs in Taiwan using light microscopy, scanning electric microscopy and mtDNA sequencing. Mar Freshwater Res 53:355–365

    Article  Google Scholar 

  • Song LS, Liu BZ, Xiang JH, Qian PY (2001) Molecular phylogeny and species identification of pufferfish of the genus Takifugu (Tetraodontiformes, Tetraodontidae). Mar Biotechnol 3:398–406

    Article  CAS  PubMed  Google Scholar 

  • Teletchea F (2009) Molecular identification methods of fish species: reassessment and possible applications. Rev Fish Biol Fisheries 19:265–293

    Article  Google Scholar 

  • Tringali MD, Bert TM, Seyoum S, Bermingham E, Bartolacci D (1999) Molecular phylogenetics and ecological diversification of the transisthmian fish genus Centropomus (Perciformes: Centropomidae). Mol Phylogenet Evol 13:193–207

    Article  CAS  PubMed  Google Scholar 

  • Tsukamoto K, Otake T, Mochioka N, Lee TW, Fricke H, Inagaki T, Aoyama J, Ishikawa S, Kimura S, Miller MJ, Hasumoto H, Oya M, Suzuki Y (2003) Seamounts, newmoon and eel spawning: the search for the spawning site of Japanese eel. Env Biol Fish 66:221–229

    Article  Google Scholar 

  • Ueyanagi S (1969) Observations on the distribution of tuna larvae in the Indo-Pacific ocean with emphasis on the delineation of the spawning areas of albacore, Thunnus alalunga. Bull Far Seas Fish Res Lab 2:177–256

    Google Scholar 

  • Ueyanagi S, Nishikawa Y, Matsuoka T (1974) Artificial fertilization and larval development of skipjack tuna, Katsuwonus pelamis. Bull Far Seas Fish Res Lab 10:179–188

    Google Scholar 

  • Ward RD, Zemlak TS, Innes BH, Last PR, Hebert PDN (2005) DNA barcoding Australia’s fish species. Philos T R Soc B 360:1847–1857

    Article  CAS  Google Scholar 

  • White BN, Lavenberg RJ, McGowen GE (1984) Atheriniformes: development and relationships. In: Moser HG, Richards WJ, Cohen DM, Fahay MP, Kendall AW, Richardson SL (eds) Ontogeny and systematics of fishes. Am Soc Ichthyol Herpetol Spec Publ 1, pp 355–362

  • Wilson RR, Kaufmann RS (1987) Seamount biota and biogeography. In: Keating BH, Fryer P, Batiza R, Bohlert GW (eds) Seamounts, islands, and atolls, vol 43. American Geophysical Union, Washington, DC, pp 355–377

    Google Scholar 

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Acknowledgements

We are grateful to the captain and his crew of the R/V Hakuho Maru for their assistance during the sampling survey and to all the other scientists who helped sort the eggs out of the plankton samples on board during the KH-02-2 cruise. We are sincerely grateful to M.J. Miller for improving this manuscript. This study was partly supported by a Grant-in-Aid No. 1611626 and for Creative Scientific Research No. 12NP0201 (DOBIS) Numbers 12NP0201 from the Ministry of Education, Science and Culture of Japan. T.K. was supported by Research Fellowships of the Japan Society for the Promotion of Science for Young Scientists. K.T. was partly supported by the Research Foundation Touwa Shokuhin Shinkoukai and the Eel Research Foundation Nobori-kai.

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  1. Ocean Research Institute, University of Tokyo, 1-15-1 Minamidai, Nakano, Tokyo, 164-8639, Japan

    Tatsuya Kawakami, Jun Aoyama & Katsumi Tsukamoto

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  1. Tatsuya Kawakami
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  2. Jun Aoyama
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  3. Katsumi Tsukamoto
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Correspondence to Tatsuya Kawakami.

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Kawakami, T., Aoyama, J. & Tsukamoto, K. Morphology of pelagic fish eggs identified using mitochondrial DNA and their distribution in waters west of the Mariana Islands. Environ Biol Fish 87, 221–235 (2010). https://doi.org/10.1007/s10641-010-9592-2

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