Abstract
Age, growth, and gonadal condition of the Giant mottled eel, Anguilla marmorata, were estimated from 303 specimens collected at Okinawa-jima Island, Japan. Otolith opaque zones that formed every year correlated with high water temperature and were thought to be annual rings. The growth of this species differed between males and females, and females were longer lived and larger than males. The mean gonadosomatic index (GSI) and the appearance of silver eels showed no clear seasonality. Comparing life history characteristics of this species between natural (northern specimens) and urban rivers (southern specimens), the growth of southern specimens was faster than that of the northern specimens, leading to the development of gonads and their downstream migration at younger ages. Therefore, we conclude that the life history characteristics of A. marmorata strongly influence by the river environments.
This is a preview of subscription content, log in via an institution to check access.
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. https://doi.org/10.5047/absm.2009.00201.0001
Arai T, Marui M, Miller MJ, Tsukamoto K (2002a) Growth history and inshore migration of the tropical eel, Anguilla marmorata, in the Pacific. Mar Biol 140(2):309–316. https://doi.org/10.1007/s002270100699
Arai T, Marui M, Otake T, Tsukamoto K (2002b) Inshore migration of a tropical eel, Anguilla marmorata, from Taiwanese and Japanese coasts. Fish Sci 68(1):152–157. https://doi.org/10.1046/j.1444-2906.2002.00401.x
Arai T, Limbong D, Otake T, Tsukamoto K (2001) Recruitment mechanisms of tropical eels Anguilla spp. and implications for the evolution of oceanic migration in the genus Anguilla. Mar Ecol Prog Ser 216:253–264. https://doi.org/10.3354/meps216253
Arai T, Kotake A, Ohji M, Miyazaki N, Tsukamoto K (2003) Migratory history and habitat use of Japanese eel Anguilla japonica in the Sanriku coast of Japan. Fish Sci 69:813–818. https://doi.org/10.1046/j.1444-2906.2003.00691.x
Arai T, Kotake A, Lokman PM, Miller MJ, Tsukamoto K (2004) Evidence of different habitat use by New Zealand freshwater eels Anguilla australis and A. dieffenbachii, as revealed by otolith microchemistry. Mar Ecol Prog Ser 266:213–225. https://doi.org/10.3354/meps266213
Castle PHJ, Williamson GR (1974) On the validity of the freshwater eel species Anguilla ancestralis Ege from Celebes. Copeia 1974:569–570
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(1):257–259. https://doi.org/10.1007/s12562-008-0017-5
Davey AJ, Jellyman DJ (2005) Sex determination in freshwater eels and management options for manipulation of sex. Rev Fish Biol Fish 15(1–2):37–52
Ege V (1939) A revision of the genus Anguilla Shaw: a systematic, phylogenetic and geographical study. Dana-Report 16:1–256. https://doi.org/10.1007/s11160-005-7431-x
Hagihara S, Aoyama J, Limbong D, Tsukamoto K (2018) Age and growth of migrating tropical eels, Anguilla celebesensis and Anguilla marmorata. J Fish Biol 92(5):1526–1544. https://doi.org/10.1111/jfb.13608
Han YS, Yambot AV, Zhang H, Hung CL (2012) Sympatric spawning but allopatric distribution of Anguilla japonica and Anguilla marmorata: temperature and oceanic current-dependent sieving. PLoS One 7(6) https://dx.doi.org/10.1371%2Fjournal.pone.0037484
Helms BS, Bickford NA, Tubbs NW, Feminella JW (2018) Feeding, growth, and trophic position of redbreast sunfish (Lepomis auritus) in watersheds of differing land cover in the lower Piedmont, USA. Urban Ecosyst 21(1):107–117. https://doi.org/10.1007/s11252-017-0696-8
Ichthyological Society of Japan (2003) Guidelines for the use of fishes in research. The Ichthyological Society of Japan, Japan, http://www.fish-isj.jp/english/guidelines.html
Ishikawa S, Tsukamoto K, Nishida M (2004) Genetic evidence for multiple geographic populations of the giant mottled eel Anguilla marmorata in the Pacific and Indian oceans. Ichthyol Res 51(4):343–353. https://doi.org/10.1007/s10228-004-0241-7
Itakura H, Kitagawa T, Miller MJ, Kimura S (2015a) Declines in catches of Japanese eels in rivers and lakes across Japan: have river and lake modifications reduced fishery catches? Landsc Ecol Eng 11(1):147–160. https://doi.org/10.1007/s11355-014-0252-0
Itakura H, Kaino T, Miyake Y, Kitagawa T, Kimura S (2015b) Feeding, condition, and abundance of Japanese eels from natural and revetment habitats in the Tone River, Japan. Environmental Biology Fish 98:1871–1888. https://doi.org/10.1007/s10641-015-0404-6
Jessop BM, Shiao JC, Iizuka Y, Tzeng WN (2004) Variation in the annual growth, by sex and migration history, of silver American eels Anguilla rostrata. Mar Ecol Prog Ser 272:231–244. https://doi.org/10.3354/meps272231
Koda M (2003) Strange fertilization system of Corydoras with small male. Nakajima H, Kano K (eds) fish Socioethology 2. Kaiyusha, Tokyo, p 136 (in Japanese)
Krueger WH, Oliveira K (1999) Evidence for environmental sex determination in the American eel, Anguilla rostrata. Environ Biol Fish 55(4):381–389. https://doi.org/10.1023/A:1007575600789
Kuroki M (2018) Early life history of anguillid eels. Nippon Suisan Gakkaishi 84(4):614–617
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(9):1853–1865. https://doi.org/10.1111/j.1095-8649.2009.02299.x
Kuroki M, Miller MJ, Feunteun E, Sasal P, Pikering T, Han YS, Faliex E, Acou A, Dessier A, Schabetsberger R, Watanabe S, Kawakami T, Onda H, Higuchi T, Takeuchi A, Shimizu M, Hewavitharane S, Taka T, Kimura S, Mochioka N, Otake T, Tsukamoto K (2020) Distribution of anguillid leptocephali and possible spawning areas in the South Pacific Ocean. Prog Oceanogr 180:102234. https://doi.org/10.1016/j.pocean.2019.102234
Lin YJ, Tzeng WN (2009) Modelling the growth of Japanese eel Anguilla japonica in the lower reach of the Kao-Ping River, southern Taiwan: an information theory approach. J Fish Biol 75(1):100–112. https://doi.org/10.1111/j.1095-8649.2009.02268.x
Leander NJ, Shen KN, Chen RT, Tzeng WN (2012) Species composition and seasonal occurrence of recruiting glass eels (Anguilla spp.) in the Hsiukuluan River, eastern Taiwan. Zool Stud 51(1):59–71
Luo M, Guan R, Li Z, Jin H (2013) The effects of water temperature on the survival, feeding, and growth of the juveniles of Anguilla marmorata and A. bicolor pacifica. Aquaculture 400:61–64. https://doi.org/10.1016/j.aquaculture.2013.03.003
Melia P, Bevacqua D, Crivelli AJ, Leo GAD, Panfili J, Gatto M (2006) Age and growth of Anguilla anguilla in the Camargue lagoons. J Fish Biol 68(3):876–890. https://doi.org/10.1111/j.0022-1112.2006.00975.x
Miller MJ, Mochioka N, Otake T, Tsukamoto K (2002) Evidence of a spawning area of Anguilla marmorata in the western North Pacific. Mar Biol 140(4):809–814. https://doi.org/10.1007/s00227-001-0754-9
Minegishi Y, Aoyama J, Tsukamoto K (2008) Multiple population structure of the giant mottled eel, Anguilla marmorata. Mol Ecol 17(13):3109–3122. https://doi.org/10.1111/j.1365-294X.2008.03822.x
Nakasone K (2003) Anthropogenic disturbances and organisms of the terrestrial environment of the Ryukyu archipelago. In: Nishida M, Shikatani N, Shokita S (eds) The Flora and Fauna of island waters in the Ryukyu Islands. Tokai University Press, Tokyo, pp 43–72 (in Japanese)
Nishi G, Imai S (1969) On the juvenile of Anguilla marmorata Quoy et Gaimard in Yakushima (Yaku Island). Memoirs Faculty Fisheries Kagoshima University 18:65–76 (in Japanese with English abstract)
Okamura A, Yamada Y, Yokouchi K, Horie N, Mikawa N, Utoh T, Tanaka S, Tsukamoto K (2007) A silvering index for the Japanese eel Anguilla japonica. Environ Biol Fish 80(1):77–89. https://doi.org/10.1007/s10641-006-9121-5
Okinawa Prefectural Government Department of Environmental Affairs, Environmental Policy Division (2014) Annual report on the environment 2014. Okinawa prefectural government Department of Environmental Affairs. Environmental Policy Division Okinawa, Japan https://www.pref.okinawa.jp/site/kankyo/seisaku/kikaku/hakusho/documents/h24_hompen.pdf
Paul MJ, Meyer JL (2001) Streams in the urban landscape. Annu Rev Ecol Syst 32(1):333–365. https://doi.org/10.1146/annurev.ecolsys.32.081501.114040
Poole WR, Reynolds JD (1996) Growth rate and age at migration of Anguilla anguilla. J Fish Biol 48(4):633–642. https://doi.org/10.1111/j.1095-8649.1996.tb01458.x
Resh VH, Moser M, Poole M (1999) Feeding habits of some freshwater fishes in streams of Moorea, French Polynesia. Annales de Limnologie-International Journal of Limnology 35(3):205–210. https://doi.org/10.1051/limn/1999029
Satoh H, Nakamura N, Hibiya T (1962) Studies on the sexual maturation of the eel-I. on the sex differentiation and the maturing process of the gonad. Bull Jpn Soc Sci Fish 28(6):579–584 (in Japanese)
Siegel JE, McPhee MV, Adkison MD (2017) Evidence that marine temperatures influence growth and maturation of Western Alaskan Chinook Salmon. Marine and Coastal Fisheries 9(1):441–456. https://doi.org/10.1080/19425120.2017.1353563
Shimazu N (2014) Individual density and total length distribution of the giant mottled eels (Anguilla marmorata) found after a mass mortality of fishes in the Noha River, a substream of Kokuba River system, Okinawa Island in august 2013. The Biological Magazine Okinawa 52:69–72 (in japanese)
Sugeha HY, Arai T, Miller MJ, Limbong D, Tsukamoto K (2001) Inshore migration of the tropical eels Anguilla spp. recruiting to the Poigar River estuary on North Sulawesi Island. Mar Ecol Prog Ser 221:233–243. https://doi.org/10.3354/meps221233
Tesch FW (2003) The eel. Blackwell Publishing, London
Toyama E. (1985) Water and environment on Okinawa. Okinawa Institute of Physical and Chemical Research (ed), Okinawa, pp 134–135. (in Japanese)
Tsukamoto K, Aoyama J, Miller MJ (2002) Migration, speciation, and the evolution of diadromy in anguillid eels. Can J Fish Aquat Sci 59(12):1989–1998. https://doi.org/10.1139/f02-165
Tsukamoto K, Chow S, Otake T, Kurogi H, Mochioka N, Miller MJ, Shinoda A (2011) Oceanic spawning ecology of freshwater eels in the western North Pacific. Nat Commun 2:179. https://doi.org/10.1038/ncomms1174
Tzeng WN, Lin HR, Wang CH, Xu SN (2000) Differences in size and growth rates of male and female migrating Japanese eels in Pearl River, China. J Fish Biol 57(5):1245–1253. https://doi.org/10.1111/j.1095-8649.2000.tb00484.x
Wakiya R, Itakura H, Kaifu K (2019) Age, growth, and sex ratios of the Giant mottled eel, Anguilla marmorata, in freshwater habitats near their northern geographic limit: a comparison to tropical regions. Zool Stud 58:34. https://doi.org/10.6620/ZS.2019.58-34
Watanabe S, Aoyama J, Miller MJ, Ishikawa S, Feunteun E, Tsukamoto K (2008) Evidence of population structure in the giant mottled eel, Anguilla marmorata, using total number of vertebrae. Copeia 2008(3):680–688
Watanabe S, Aoyama J, Tsukamoto K (2009a) A new species of freshwater eel Anguilla luzonensis (Teleostei: Anguillidae) from Luzon Island of the Philippines. Fish Sci 75(2):387–392. https://doi.org/10.1007/s12562-009-0087-z
Watanabe S, Miller MJ, Aoyama J, Tsukamoto K (2009b) Morphological and meristic evaluation of the population structure of Anguilla marmorata across its range. J Fish Biol 74(9):2069–2093. https://doi.org/10.1111/j.1095-8649.2009.02297.x
Williamson GR (1993) The eels Anguilla marmorata and A. japonica in the Pearl River, China, and Hong Kong. Asian Fisheries Science 6:129–138
Yokouchi K, Daverat F, Miller MJ, Fukuda N, Sudo R, Tsukamoto K, Elie P, Poole WR (2018) Growth potential can affect timing of maturity in a long-lived semelparous fish. Biol Lett 14:20180269. https://doi.org/10.1098/rsbl.2018.0269
Acknowledgements
We are grateful to all members of the Laboratory of Fisheries Biology and Coral Reef Studies in the Faculty of Science at the University of the Ryukyus for support of our study. We are also grateful to Assoc. Prof. N. Mochioka (University of Kyusyu), Assoc. Prof. S. Ijiri (University of Hokkaido), Dr. T. Kunishima (Wakayama Prefectural Museum of Natural History), and anonymous reviewers for their useful advice. We would like to thank Editage (www.editage.com) for English language editing.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Kita, T., Tachihara, K. Age, growth, and gonadal condition of the Giant mottled eel, Anguilla marmorata, in Okinawa-Jima Island, Japan. Environ Biol Fish 103, 927–938 (2020). https://doi.org/10.1007/s10641-020-00994-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10641-020-00994-5