Abstract
Eggs of the Japanese eel Anguilla japonica collected in the western North Pacific were identified by onboard species-specific polymerase chain reaction (PCR) and DNA nucleotide sequencing after the cruise. Fish eggs of various species were collected by large plankton net tows at 12 stations along the southern part of the West Mariana Ridge on 19–25 May 2009. A total of 43 fish eggs were distinguished morphologically as possibly being of A. japonica. Thirty-one of those were analyzed by PCR, which included 15 eggs collected at 12°50–55′N, 141°15–20′E (in 5 tows) that showed positive results. The 16S ribosomal RNA (rRNA) gene sequences of eggs determined after the cruise indicated that 31 A. japonica eggs had been collected. The remaining eggs were of mesopelagic eel species (Serrivomeridae and Derichthyidae), or unidentified species. The morphological characteristics of the A. japonica eggs were consistent with those of artificially spawned eggs, except they had a slightly larger diameter. The egg diameter range did not overlap with those of mesopelagic eels of the Serrivomeridae, which often spawn in the same area as A. japonica. These results suggest that egg diameter and embryo shape can be used to morphologically identify naturally spawned A. japonica eggs.
Similar content being viewed by others
References
Aoyama J (2009) Life history and evolution of migration in catadromous eels (genus Anguilla). Aqua BioSci Monogr 2(1):1–42
Tatsukawa K (2003) Eel resources in East Asia. In: Aida K et al (eds) Eel biology. Springer, Tokyo, pp 293–298
Tsukamoto K (1992) Discovery of the spawning area for Japanese eel. Nature 356:789–791
Tsukamoto K (2006) Spawning of eels near a seamount. Nature 439:929
Ishikawa S, Aoyama J, Tsukamoto K, Nishida M (2001) Population structure of the Japanese eel Anguilla japonica as examined by mitochondrial DNA sequencing. Fish Sci 67:246–253
Han YS, Hung CL, Liao YF, Tzeng WN (2010) Population genetic structure of the Japanese eel Anguilla japonica: panmixia at spatial and temporal scales. Mar Ecol Prog Ser 401:221–232
Tsukamoto K, Chow S, Otake T, Kurogi H, Mochioka N, Miller MJ, Aoyama J, Kimura S, Watanabe S, Yoshinaga T, Shinoda A, Kuroki M, Oya M, Watanabe T, Hata K, Ijiri S, Kazeto Y, Nomura K, Tanaka H (2011) Oceanic spawning ecology of freshwater eels in the western North Pacific. Nat Commun. doi:10.1038/ncomms1174
Watanabe S, Aoyama J, Tsukamoto K (2009) A new species of freshwater eel Anguilla luzonensis (Teleostei: Anguillidae) from Luzon Island of the Philippines. Fish Sci 75:387–392
Fish MP (1927) Contributions to the embryology of the American eel (Anguilla rostorata Le Sueur). Zool NY 8:289–324
Yamamoto K, Yamauchi K, Kasuga S (1975) On the development of the Japanese eel, Anguilla japonica. Bull Jpn Soc Sci Fish 41:21–28
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 (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
Yamamoto K, Yamauchi K (1974) Sexual maturation of Japanese eel and production of eel larvae in the aquarium. Nature 251:220–221
Yamauchi K, Nakamura M, Takahashi H, Takano K (1976) Cultivation of larvae of Japanese eel. Nature 263:412
Tanaka H, Kagawa H, Ohta H (2001) Production of leptocephali of Japanese eel (Anguilla japonica) in captivity. Aquaculture 201:51–60
Tanaka H, Kagawa H, Ohta H, Unuma T, Nomura K (2003) The first production of glass eel in captivity: fish reproductive physiology facilitates great progress in aquaculture. Fish Physiol Biochem 28:493–497
Unuma T, Kondo S, Tanaka H, Kagawa H, Nomura K, Ohta H (2004) Determination of the rates of fertilization, hatching and larval survival in the Japanese eel, Anguilla japonica, using tissue culture microplates. Aquaculture 241:345–356
Okamura A, Yamada Y, Horie N, Utoh T, Mikawa N, Tanaka S, Tsukamoto K (2007) Effects of water temperature on early development of Japanese eel Anguilla japonica. Fish Sci 73:1241–1248
Kurokawa T, Okamoto T, Gen K, Uji S, Murasita K, Unuma T, Nomura K, Matsubara H, Kim S-K, Ohta H, Tanaka H (2008) Influence of water temperature on morphological deformities in cultured larvae of Japanese eel, Anguilla japonica, at completion of yolk resorption. J World Aquac Soc 39:729–735
Watanabe S, Minegishi Y, Yoshinaga T, Aoyama J, Tsukamoto K (2004) A quick method for species identification of the Japanese eel Anguilla japonica using real-time PCR: an onboard application for use during sampling surveys. Mar Biotechnol 6:566–574
Minegishi Y, Yoshinaga T, Aoyama J, Tsukamoto K (2009) Species identification of Anguilla japonica by real-time PCR based on sequence detection system: a practical application to egg and larva. ICES J Mar Sci 66:1915–1918
Shinoda A, Aoyama J, Miller MJ, Otake T, Mochioka N, Watanabe S, Minegishi Y, Kuroki M, Yoshinaga T, Yokouchi K, Fukuda N, Sudo R, Hagihara S, Zenimoto K, Suzuki Y, Oya M, Inagaki T, Kimura S, Fukui A, Lee TW, Tsukamoto K (2011) Evaluation of the larval distribution and migration route of the Japanese eel in the western North Pacific. Rev Fish Biol Fish. doi:10.1007/s11160-010-9195-1
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
Kuroki M, Aoyama J, Miller MJ, Yoshinaga T, Shinoda A, Hagihara S, Tsukamoto K (2009) Sympatric spawning of Anguilla marmorata and Anguilla japonica in the western North Pacific Ocean. J Fish Biol 74:1853–1865
ICES (2006) Report of the ICES/EIFAC working group on eels, Rome, 23–27 January 2006. ICES Doc ICES CM 2006/ACFM 16
CITES (2007) Append I, II and III valid from 13 September 2007
Virta VC, Cooper MS (2009) Ontogeny and phylogeny of the yolk extension in embryonic cypriniform fishes. J Exp Zool (Mol Dev Evol) 312B:196–223
Oliveria K, Hable WE (2010) Artificial maturation, fertilization, and early development of the American eel (Anguilla rostrata). Can J Zool 88:1121–1128
Pedersen BH (2004) Fertilisation of eggs, rate of embryonic development and hatching following induced maturation of the European eel Anguilla anguilla. Aquaculture 237:461–473
Lokman PM, Young G (2000) Induced spawning and early ontogeny of New Zealand freshwater eels (Anguilla dieffenbachii and A. australis). N Z J Mar Freshw Res 34:135–145
Castle PHJ (1984) Notacanthiformes and Anguilliformes: development. In: Moser HG, Richards WJ (eds) Ontogeny and systematics of fishes. Am Soc Ichthyol Herpetol Sp Publ 1. Am Soc Ichthyol Hepetol, New York pp 62–93
Mito S (1961) Pelagic fish eggs from Japanese waters—I. Clupeina, Chanina, Stomiatina, Myctophida, Anguillida, Belonida and Syngnathida. Sci Bull Fac Agric Kyushu Univ 18:285–310
Kawakami T, Aoyama J, Tsukamoto K (2011) Morphology of pelagic fish eggs identified using mitochondrial DNA and their distribution in waters west of the Mariana Islands. Environ Biol Fishes 87:221–235
Miller MJ (2009) Ecology of anguilliform leptocephali: remarkable transparent fish larvae of the ocean surface layer. Aqua BioSci Monogr 2(4):1–94
Chow S, Kurogi H, Mochioka N, Kaji S, Okazaki M, Tsukamoto K (2009) Discovery of mature freshwater eels in the open ocean. Fish Sci 75:257–259
Kurogi H, Okazaki M, Mochioka N, Jinbo T, Hashimoto H, Takahashi M, Tawa A, Aoyama J, Shinoda A, Tsukamoto K, Tanaka H, Gen K, Kazeto Y, Chow S (2011) First capture of post-spawning female of the Japanese eel Anguilla japonica at the southern West Mariana Ridge. Fish Sci 77:199–205
Inoue JG, Miya M, Miller MJ, Sado T, Hanel R, Hatooka K, Aoyama J, Minegishi M, Nishida M, Tsukamoto K (2010) Deep-ocean origin of the freshwater eels. Biol Lett 6:363–366
Miller MJ, Yoshinaga T, Aoyama J, Otake T, Mochioka N, Kurogi H, Tsukamoto K (2011) Offshore spawning of Conger myriaster in the western North Pacific: evidence for convergent migration strategies of anguilliform eels in the Atlantic and Pacific. Naturewissenshaften 98:537–554
Burgerhout E, Brittijn SA, Kurwie T, Decker P, Dirks RP, Palstra AP, Spaink HP, Van den Thillart GEEJM (2011) First artificial hybrid of the eel species Anguilla australis and Anguilla anguilla. BMC Dev Biol 11:16
Acknowledgments
We thank the captain and crew of the R/V Hakuho Maru for their support during the 2009 sampling surveys that made this study possible. The IRAGO Institute kindly provided the photos of their artificially produced eggs. We also thank Dr. Hiroaki Kasai and Ms. Yukie Inomata of Kamaishi Biotechnology Research Institute of Kitasato University, who kindly provided us an opportunity to use their genetic analyzer. Thanks are also due to two anonymous reviewers for their critical comments on the manuscript. This study was partly supported by a grant-in-aid for scientific research (S) (21228005) from the Japan Society for the Promotion of Science to K.T.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Yoshinaga, T., Miller, M.J., Yokouchi, K. et al. Genetic identification and morphology of naturally spawned eggs of the Japanese eel Anguilla japonica collected in the western North Pacific. Fish Sci 77, 983–992 (2011). https://doi.org/10.1007/s12562-011-0418-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12562-011-0418-8