Advertisement

Marine Biology

, 164:118 | Cite as

Hatching time and larval growth of Atlantic eels in the Sargasso Sea

  • Mari Kuroki
  • Lasse Marohn
  • Klaus Wysujack
  • Michael J. Miller
  • Katsumi Tsukamoto
  • Reinhold Hanel
SHORT NOTES

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.

Keywords

Larval Growth Rate Somatic Growth Rate Otolith Microstructure Length Frequency Data Anguillid Species 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

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.

Compliance with ethical standards

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.

References

  1. 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 15:1903–1916CrossRefGoogle Scholar
  2. Avise JC, Nelson WS, Arnold J, Koehn RK, Williams GC, Thorsteinsson V (1990) The evolutionary genetic status of Icelandic eels. Evolution 44:1254–1262CrossRefGoogle Scholar
  3. Boëtius J, Harding EF (1985) A re-examination of Johannes Schmidt’s Atlantic eel investigations. Dana 4:129–163Google Scholar
  4. 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 373:71–80CrossRefGoogle Scholar
  5. Castonguay M (1987) Growth of American and European eel leptocephali as revealed by otolith microstructure. Can J Zool 65:875–878CrossRefGoogle Scholar
  6. 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 9:195–214CrossRefGoogle Scholar
  7. 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 3:197–203CrossRefGoogle Scholar
  8. 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 10:173–176CrossRefGoogle Scholar
  9. 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 74:1915–1933CrossRefGoogle Scholar
  10. 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 101:1041–1052CrossRefGoogle Scholar
  11. Kleckner RC, McCleave JD (1985) Spatial and temporal distribution of American eel larvae in relation to North Atlantic Ocean current systems. Dana 4:67–92Google Scholar
  12. 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 46:647–667CrossRefGoogle Scholar
  13. 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 52:1030–1036CrossRefGoogle Scholar
  14. 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 309:233–246CrossRefGoogle Scholar
  15. 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 59:1035–1047CrossRefGoogle Scholar
  16. 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 83:309–325CrossRefGoogle Scholar
  17. 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 34:31–38Google Scholar
  18. 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 92:749–770CrossRefGoogle Scholar
  19. Lecomte-Finiger R (1992) Growth history and age at recruitment of European glass eels (Anguilla anguilla) as revealed by otolith microstructure. Mar Biol 114:205–210CrossRefGoogle Scholar
  20. 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 155:249–262CrossRefGoogle Scholar
  21. 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 41:789–806Google Scholar
  22. McCleave JD, Kleckner RC, Castonguay M (1987) Reproductive sympatry of American and European eels and implications for migration and taxonomy. Am Fish Soc Symp 1:286–297Google Scholar
  23. 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 43:493–501CrossRefGoogle Scholar
  24. 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 90:1035–1064CrossRefGoogle Scholar
  25. 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 73:43–56CrossRefGoogle Scholar
  26. 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 277:3593–3599CrossRefGoogle Scholar
  27. 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 73:1241–1248Google Scholar
  28. Oliveira K, Hable WE (2010) Artificial maturation, fertilization and early development of the American eel, Anguilla rostrata. Can J Zool 88:1121–1128CrossRefGoogle Scholar
  29. 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 70:309–318CrossRefGoogle Scholar
  30. 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:e1501694CrossRefGoogle Scholar
  31. 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 41–60CrossRefGoogle Scholar
  32. 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 154:453–463CrossRefGoogle Scholar
  33. Schmidt J (1922) The breeding places of the eel. Philos Trans R Soc Lond B Biol Sci 211:179–208CrossRefGoogle Scholar
  34. Schmidt J (1925) The breeding places of the eel. Annu Rep Smithson Inst 1924:279–316Google Scholar
  35. Schoth M, Tesch F-W (1982) Spatial distribution of 0-group eel larvae (Anguilla sp.) in the Sargasso Sea. Helgol Meeresun 35:309–320CrossRefGoogle Scholar
  36. 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 219:241–250CrossRefGoogle Scholar
  37. 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 70:340–342CrossRefGoogle Scholar
  38. 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 21:591–611CrossRefGoogle Scholar
  39. 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 69:1081–1101CrossRefGoogle Scholar
  40. Tanaka H, Kagawa H, Ohta H (2001) Production of leptocephali of Japanese eel (Anguilla japonica) in captivity. Aquaculture 201:51–60CrossRefGoogle Scholar
  41. 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 DenmarkGoogle Scholar
  42. 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 29:912–915CrossRefGoogle Scholar
  43. 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 2:179CrossRefGoogle Scholar
  44. Umezawa A, Tsukamoto K (1991) Factors influencing otolith increment formation in Japanese eel, Anguilla japonica T. & S., elvers. J Fish Biol 39:211–223CrossRefGoogle Scholar
  45. 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 35:440–444Google Scholar
  46. 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 46:191–205CrossRefGoogle Scholar
  47. Yamamoto K, Yamauchi K (1974) Sexual maturation of Japanese eel and production of eel larvae in the aquarium. Nature 251:220–222CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Mari Kuroki
    • 1
  • Lasse Marohn
    • 2
  • Klaus Wysujack
    • 2
  • Michael J. Miller
    • 3
  • Katsumi Tsukamoto
    • 3
  • Reinhold Hanel
    • 2
  1. 1.Graduate School of Agricultural and Life SciencesThe University of TokyoBunkyoJapan
  2. 2.Thünen Institute of Fisheries EcologyHamburgGermany
  3. 3.Department of Marine Science and ResourcesNihon UniversityFujisawaJapan

Personalised recommendations