Abstract
Several surveys and studies have examined the Atlantic anguillid eels’ larval distributions, but little is known about their larval growth rates. Otoliths of 17 European eel Anguilla anguilla (8.8–46.0 mm) and 19 American eel Anguilla rostrata (9.8–59.9 mm) leptocephali collected in the Sargasso Sea (25–31°N, 58–70°W) in March and April 2011 were analyzed and their spawning times and larval growth rates were estimated. Ages calculated from the number of otolith increments of European and American eel larvae showed ranges of 10–127 days and 14–233 days, respectively. Linear relationships between age and total length indicated early larval growth rates of 0.31 mm/day for the European eel and 0.35 mm/day for the American eel. This suggested slower growth rates in low temperatures in the Sargasso Sea compared to other anguillid species in the Indo-Pacific, where water temperatures are higher. The back-calculated hatching dates of small leptocephali (8.8–26.7 mm) were in February and March 2011. More American eels hatched in February and more European eels hatched in March. The hatching times of two larger European eel leptocephali (38.7 and 46.0 mm) and a larger American eel leptocephalus (59.9 mm) were back-calculated to November and December 2010 and July 2010, respectively, suggesting hatching times outside of the primary spawning seasons. These novel observations provide important information on the timing of spawning and larval growth characteristics of Atlantic eels, which would benefit from validation by additional otolith studies of leptocephali.
References
Albert V, Jónsson B, Bernatchez L (2006) Natural hybrids in Atlantic eels (Anguilla anguilla, A. rostrata): evidence for successful reproduction and fluctuating abundance in space and time. Mol Ecol 15:1903–1916
Avise JC, Nelson WS, Arnold J, Koehn RK, Williams GC, Thorsteinsson V (1990) The evolutionary genetic status of Icelandic eels. Evolution 44:1254–1262
Boëtius J, Harding EF (1985) A re-examination of Johannes Schmidt’s Atlantic eel investigations. Dana 4:129–163
Bonhommeau S, Chassot E, Planque B, Rivot E, Knap AH, Le Pape O (2008) Impact of climate on eel populations of the northern hemisphere. Mar Ecol Prog Ser 373:71–80
Castonguay M (1987) Growth of American and European eel leptocephali as revealed by otolith microstructure. Can J Zool 65:875–878
Castonguay M, McCleave JD (1987) Vertical distributions, diel and ontogenetic vertical migrations and net avoidance of leptocephali of Anguilla and other common species in the Sargasso Sea. J Plankt Res 9:195–214
Castonguay M, Hudson PV, Moriarty C, Drinkwater KF, Jessop BM (1994) Is there a role of ocean environment in American and European eel decline? Fish Oceanogr 3:197–203
Frankowski J, Bastrop R (2010) Identification of Anguilla anguilla (L.) and Anguilla rostrata (Le Sueur) and their hybrids based on a diagnostic single nucleotide polymorphism in nuclear 18S rDNA. Mol Ecol 10:173–176
Fukuda N, Kuroki M, Shinoda A, Yamada Y, Okamura A, Aoyama J, Tsukamoto K (2009) Influence of water temperature and feeding regime on otolith growth in Anguilla japonica glass eels and elvers: does otolith growth cease at low temperatures? J Fish Biol 74:1915–1933
Hanel R, Stepputtis D, Bonhommeau S, Castonguay M, Schaber M, Wysujack K, Vobach M, Miller MJ (2014) Low larval abundance in the Sargasso Sea: new evidence about reduced recruitment of the Atlantic eels. Naturwissenschaften 101:1041–1052
Kleckner RC, McCleave JD (1985) Spatial and temporal distribution of American eel larvae in relation to North Atlantic Ocean current systems. Dana 4:67–92
Kleckner RC, McCleave JD (1988) The northern limit of spawning by Atlantic eels (Anguilla spp.) in the Sargasso Sea in relation to thermal fronts and surface water masses. J Mar Res 46:647–667
Kurokawa T, Kagawa H, Ohta H, Tanaka H, Okuzawa K, Hirose K (1995) Development of digestive organs and feeding ability in larvae of Japanese eel (Anguilla japonica). Can J Fish Aquat Sci 52:1030–1036
Kuroki M, Aoyama J, Miller MJ, Wouthuyzen S, Arai T, Tsukamoto K (2006) Contrasting patterns of growth and migration of tropical anguillid leptocephali in the western Pacific and Indonesian Seas. Mar Ecol Prog Ser 309:233–246
Kuroki M, Aoyama J, Miller MJ, Watanabe S, Shinoda A, Jellyman DJ, Feunteun E, Tsukamoto K (2008a) Distribution and early life-history characteristics of anguillid leptocephali in the western South Pacific. Mar Freshwater Res 59:1035–1047
Kuroki M, Kawai M, Jónsson B, Aoyama J, Miller MJ, Noakes DLG, Tsukamoto K (2008b) Inshore migration and otolith microstructure/microchemistry of anguillid glass eels recruited to Iceland. Environ Biol Fish 83:309–325
Kuroki M, Fukuda N, Yamada Y, Okamura A, Tsukamoto K (2010) Morphological changes and otolith growth during metamorphosis of Japanese eel leptocephali in captivity. Coast Mar Sci 34:31–38
Kuroki M, Miller MJ, Tsukamoto K (2014) Diversity of early life history traits in freshwater eels and the evolution of their oceanic migrations. Can J Zool 92:749–770
Lecomte-Finiger R (1992) Growth history and age at recruitment of European glass eels (Anguilla anguilla) as revealed by otolith microstructure. Mar Biol 114:205–210
McCleave JD (2008) Contrasts between spawning times of Anguilla species estimated from larval sampling at sea and from otolith analysis of recruiting glass eels. Mar Biol 155:249–262
McCleave JD, Kleckner RC (1987) Distribution of leptocephali of the catadromous Anguilla species in the western Sargasso Sea in relation to water circulation and migration. Bull Mar Sci 41:789–806
McCleave JD, Kleckner RC, Castonguay M (1987) Reproductive sympatry of American and European eels and implications for migration and taxonomy. Am Fish Soc Symp 1:286–297
Miller MJ, Stepputtis D, Bonhommeau S, Castonguay M, Schaber M, Vobach M, Wysujack K, Hanel R (2013) Comparisons of catches of large leptocephali using an IKMT and a large pelagic trawl in the Sargasso Sea. Mar Biodivers 43:493–501
Miller MJ, Bonhommeau S, Munk P, Castonguay M, Hanel R, McCleave JD (2015) A century of research on the larval distributions of the Atlantic eels: a reexamination of the data. Biol Rev 90:1035–1064
Miller MJ, Feunteun E, Tsukamoto K (2016) Did a “perfect storm” of oceanic changes and continental anthropogenic impacts cause northern hemisphere anguillid recruitment reductions? ICES J Mar Sci 73:43–56
Munk P, Hansen MM, Maes GE, Nielsen TG, Castonguay M, Riemann L, Sparholt H, Als TD, Aarestrup K, Andersen NG, Bachler M (2010) Oceanic fronts in the Sargasso Sea control the early life and drift of Atlantic eels. Proc Biol Sci 277:3593–3599
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
Oliveira K, Hable WE (2010) Artificial maturation, fertilization and early development of the American eel, Anguilla rostrata. Can J Zool 88:1121–1128
Prigge E, Marohn L, Oeberst R, Hanel R (2013) Model prediction vs. reality—testing the predictions of a European eel (Anguilla anguilla) stock dynamics model against the in situ observation of silver eel escapement in compliance with the European eel regulation. ICES J Mar Sci 70:309–318
Righton D, Westerberg H, Feunteun E, Økland F, Gargan P, Amilhat E, Metcalfe J, Lobon-Cervia J, Sjöberg N, Simon J, Acou A, Vedor M, Walker A, Trancart T, Brämick U, Aarestrup K (2016) Empirical observations of the spawning migration of European eels: the long and dangerous road to the Sargasso Sea. Sci Adv 2:e1501694
Rindom S, Tomkiewicz J, Munk P, Aarestrup K, Damm Als TD, Pedersen MI, Graver C, Anderberg C (2014) Eels in culture, fisheries and science in Denmark. In: Tsukamoto K, Kuroki M (eds) Eels and humans, humanity and the sea. Springer, Tokyo, pp 41–60
Robinet T, Réveillac E, Kuroki K, Aoyama J, Tsukamoto K, Rabenevanana MW, Valade P, Gagnaire PA, Berrebi P, Feunteun E (2008) New clues for freshwater eels (Anguilla spp.) migration routes to eastern Madagascar and surrounding islands. Mar Biol 154:453–463
Schmidt J (1922) The breeding places of the eel. Philos Trans R Soc Lond B Biol Sci 211:179–208
Schmidt J (1925) The breeding places of the eel. Annu Rep Smithson Inst 1924:279–316
Schoth M, Tesch F-W (1982) Spatial distribution of 0-group eel larvae (Anguilla sp.) in the Sargasso Sea. Helgol Meeresun 35:309–320
Shiao JC, Tzeng WN, Collins A, Jellyman DJ (2001) Dispersal pattern of glass eel stage of Anguilla australis revealed by otolith growth increments. Mar Ecol Prog Ser 219:241–250
Shinoda A, Tanaka H, Kagawa H, Ohta H, Tsukamoto K (2004) Otolith microstructural analysis of reared larvae of the Japanese eel Anguilla japonica. Fish Sci 70:340–342
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 of the Japanese eel in the western North Pacific. Rev Fish Biol Fish 21:591–611
Sullivan MC, Able KW, Hare JA, Walsh HJ (2006) Anguilla rostrata glass eel ingress into two, US east coast estuaries: patterns, processes and implications for adult abundance. J Fish Biol 69:1081–1101
Tanaka H, Kagawa H, Ohta H (2001) Production of leptocephali of Japanese eel (Anguilla japonica) in captivity. Aquaculture 201:51–60
Tomkiewicz J (ed) (2012) Reproduction of European eel in aquaculture (REEL). Consolidation and new production methods. DTU Aqua Report 249-2012, National Institute of Aquatic Resources, Technical University of Denmark
Trautner JH (2013) Stocking the right eel species: a fast PCR-based identification assay to discriminate European (Anguilla anguilla (Linnaeus, 1758)), American (A. rostrata (Lesueur, 1817)) and Japanese eel (A. japonica (Temminck & Schlegel, 1846)). J Appl Ichthyol 29:912–915
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 2:179
Umezawa A, Tsukamoto K (1991) Factors influencing otolith increment formation in Japanese eel, Anguilla japonica T. & S., elvers. J Fish Biol 39:211–223
Umezawa A, Tsukamoto K, Tabeta O, Yamakawa H (1989) Daily growth increments in the larval otolith of the Japanese eel, Anguilla japonica. Jpn J Ichthyol 35:440–444
Wang CH, Tzeng WN (2000) The timing of metamorphosis and growth rates of American and European eel leptocephali: a mechanism of larval segregative migration. Fish Res 46:191–205
Yamamoto K, Yamauchi K (1974) Sexual maturation of Japanese eel and production of eel larvae in the aquarium. Nature 251:220–222
Acknowledgements
We thank the captain and crew of the R/V Walther Herwig III for their technical support, and the editor and reviewers for their constructive comments on the manuscript. This study was funded by grants from the German Federal Ministry of Food and Agriculture, the University of Tokyo, and Nihon University.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declared that they have no conflict of interest.
Ethical approval
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
Additional information
Responsible Edtior: E. Hunter.
Reviewed by F. Daverat, M. Castonguay, A. Walker.
Rights and permissions
About this article
Cite this article
Kuroki, M., Marohn, L., Wysujack, K. et al. Hatching time and larval growth of Atlantic eels in the Sargasso Sea. Mar Biol 164, 118 (2017). https://doi.org/10.1007/s00227-017-3150-9
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00227-017-3150-9