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Marine Biology

, Volume 155, Issue 3, pp 249–262 | Cite as

Contrasts between spawning times of Anguilla species estimated from larval sampling at sea and from otolith analysis of recruiting glass eels

  • James D. McCleave
Review

Abstract

This study reviewed literature on spawning times for three north temperate species of anguillid eels estimated by sampling for small leptocephali (larvae) at sea and for several temperate and tropical species by back-calculating from putative daily ages derived from otolith increment analysis of glass eels that recruited to coastal waters. Estimates from otoliths of European eels, Anguilla anguilla, American eels, Anguilla rostrata, and Japanese eels, Anguilla japonica, imply much more protracted spawning seasons than are indicated by sampling at sea during various times of year. European eels are inferred to spawn year-round from otolith analysis, but the smallest, recently hatched leptocephali are found only in late winter and spring. From otoliths, the spawning times of these three species are all estimated to occur much later in the year than when small leptocephali are found at sea, indicating that ages appear to be underestimated. For these and other temperate and tropical eels, there are inconsistencies in assigned ages among various studies, which are most extreme for the European eel. This species has the longest larval migration and often has an opaque zone in the glass eels’ otoliths where it is difficult to discern growth increments. These inconsistencies suggest that interpretation of otolith growth increments is incorrect at least in some studies, and the apparently consistent mismatch between otolith and sea-sampling studies suggests that increments may not always be formed at some period during the unusual early life history of anguillids. Because daily increments may be formed in eels during most of their early life history, future research is needed to determine the cause of the mismatch of glass eel aging studies and the apparent spawning times of eels offshore.

Keywords

Hatching Date Daily Increment Otolith Increment Protracted Spawning Small Leptocephali 
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

Acknowledgments

M. J. Miller provided many thoughtful ideas and suggestions during preparation of this article. The manuscript was improved by the suggestions of S. E. Campana and anonymous reviewers.

Supplementary material

227_2008_1026_MOESM1_ESM.doc (444 kb)
ESM (DOC 444 kb)

References

  1. Antunes C, Tesch FW (1997) A critical consideration of the metamorphosis zone when identifying daily rings in otoliths of European eel, Anguilla anguilla (L.). Ecol Freshw Fish 6:102–107. doi: https://doi.org/10.1111/j.1600-0633.1997.tb00150.x CrossRefGoogle Scholar
  2. Aoyama J, Mochioka N, Otake T, Ishikawa S, Kawakami Y, Castle P, Nishida M, Tsukamoto K (1999) Distribution and dispersal of anguillid leptocephali in the western Pacific Ocean revealed by molecular analysis. Mar Ecol Prog Ser 188:193–200. doi: https://doi.org/10.3354/meps188193 CrossRefGoogle Scholar
  3. Aoyama J, Wouthuyzen S, Miller MJ, Inagaki T, Tsukamoto K (2003) Short-distance spawning migration of tropical freshwater eels. Biol Bull 204:104–108. doi: https://doi.org/10.2307/1543500 CrossRefGoogle Scholar
  4. Arai T, Otake T, Tsukamoto K (1997) Drastic changes in otolith microstructure and microchemistry accompanying the onset of metamorphosis in the Japanese eel Anguilla anguilla. Mar Ecol Prog Ser 161:17–22. doi: https://doi.org/10.3354/meps161017 CrossRefGoogle Scholar
  5. Arai T, Otake T, Jellyman D, Tsukamoto K (1999a) Differences in the early life history of the Australian shortfinned eel Anguilla australis from Australia and New Zealand, as revealed by otolith microstructure and microchemistry. Mar Biol (Berl) 135:381–389. doi: https://doi.org/10.1007/s002270050637 CrossRefGoogle Scholar
  6. Arai T, Limbong D, Otake T, Tsukamoto K (1999b) Metamorphosis and inshore migration of tropical eels Anguilla spp. in the Indo-Pacific. Mar Ecol Prog Ser 182:283–293. doi: https://doi.org/10.3354/meps182283 CrossRefGoogle Scholar
  7. Arai T, Otake T, Limbong D, Tsukamoto K (1999c) Early life history and recruitment of the tropical eel Anguilla bicolor pacifica, as revealed by otolith microstructure and microchemistry. Mar Biol (Berl) 133:319–326. doi: https://doi.org/10.1007/s002270050470 CrossRefGoogle Scholar
  8. Arai T, Otake T, Tsukamoto K (2000a) Timing of metamorphosis and larval segregation of the Atlantic eels Anguilla rostrata and A. anguilla, as revealed by otolith microstructure and microchemistry. Mar Biol (Berl) 137:39–45. doi: https://doi.org/10.1007/s002270000326 Google Scholar
  9. Arai T, Limbong D, Tsukamoto K (2000b) Validation of otolith daily increments in the tropical eel Anguilla celebesensis. Can J Zool 78:1078–1084. doi: https://doi.org/10.1139/cjz-78-6-1078 CrossRefGoogle Scholar
  10. Arai T, Limbong D, Otake T, Tsukamoto K (2001a) 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. doi: https://doi.org/10.3354/meps216253 CrossRefGoogle Scholar
  11. Arai T, Aoyama J, Ishikawa S, Miller MJ, Otake T, Inagaki T, Tsukamoto K (2001b) Early life history of tropical Anguilla leptocephali in the western Pacific Ocean. Mar Biol (Berl) 138:887–895. doi: https://doi.org/10.1007/s002270000532 CrossRefGoogle Scholar
  12. Arai T, Marui M, Miller MJ, Tsukamoto K (2002) Growth history and inshore migration of the tropical eel, Anguilla marmorata, in the Pacific. Mar Biol (Berl) 140:309–316. doi: https://doi.org/10.1007/s002270100699 CrossRefGoogle Scholar
  13. Arai T, Limbong D, Tsukamoto K (2003) Migration and recruitment of tropical glass eels to the mouth of the Poigar River, Saluwesi Island, Indonesia. Am Fish Soc Symp 33:37–46Google Scholar
  14. Boëtius J, Harding EF (1985) A re-examination of Johannes Schmidt’s Atlantic eel investigations. Dana 4:129–162Google Scholar
  15. Budimawan (1997) The early life history of the tropical eel Anguilla marmorata (Quoy & Gaimard, 1824) from four Pacific estuaries, as revealed from otolith microstructural analysis. J Appl Ichthyol 13: 57–62CrossRefGoogle Scholar
  16. Budimawan, Lecomte-Finiger R (2005) Inshore migration of the tropical glass eels Anguilla marmorata recruiting to Poso Estuary, Sulawesi Island, Indonesia. Vie Milieu 55:7–14Google Scholar
  17. Campana SE (2001) Accuracy, precision and quality control in age determination, including a review of the use and abuse of age validation methods. J Fish Biol 59:197–242. doi: https://doi.org/10.1111/j.1095-8649.2001.tb00127.x CrossRefGoogle Scholar
  18. Campana SE (2005) Otolith science entering the 21st century. Mar Freshw Res 56:485–495. doi: https://doi.org/10.1071/MF04147 CrossRefGoogle Scholar
  19. Campana SE, Neilson JD (1985) Microstructure of fish otoliths. Can J Fish Aquat Sci 42:1014–1032. doi: https://doi.org/10.1139/f85-127 CrossRefGoogle Scholar
  20. Castonguay M (1987) Growth of American and European eel leptocephali as revealed by otolith microstructure. Can J Zool 65:875–878CrossRefGoogle Scholar
  21. Chen HL, Tzeng WN (2006) Daily growth increment formation in otoliths of Pacific tarpon Megalops cyprinoides during metamorphosis. Mar Ecol Prog Ser 312:255–263. doi: https://doi.org/10.3354/meps312255 CrossRefGoogle Scholar
  22. Cheng PW, Tzeng WN (1996) Timing of metamorphosis and estuarine arrival across the dispersal range of the Japanese eel Anguilla japonica. Mar Ecol Prog Ser 131:97–96. doi: https://doi.org/10.3354/meps131087 CrossRefGoogle Scholar
  23. Chenghua L (1998) Interrelationships among daily age, body length, birth date and sampling location at recruitment of Anguilla japonica elvers in the Chinese coast. Acta Oceanol Sin 20:107–113 in ChineseGoogle Scholar
  24. Cieri MD, McCleave JD (2001) Validation of daily otolith increments in glass-phase American eels Anguilla rostrata (Lesueur) during estuarine residency. J Exp Mar Biol Ecol 257:219–227. doi: https://doi.org/10.1016/S0022-0981(00)00333-6 CrossRefGoogle Scholar
  25. Correia AT, Able KW, Antunes C, Coimbra J (2004) Early life history of the American conger eel (Conger oceanicus) as revealed by otolith microstructure and microchemistry of metamorphosing leptocephali. Mar Biol (Berl) 145:477–488. doi: https://doi.org/10.1007/s00227-004-1349-z CrossRefGoogle Scholar
  26. Correia AT, Antunes C, Wilson JM, Coimbra J (2006) An evaluation of the otolith characteristics of Conger conger during metamorphosis. J Fish Biol 68:99–119. doi: https://doi.org/10.1111/j.0022-1112.2006.00881.x CrossRefGoogle Scholar
  27. Dannewitz J, Maes GE, Johansson L, Wickström H, Volckaert FAM, Järvi T (2005) Panmixia in the European eel: a matter of time. Proc Roy Soc B Biol Sci 272:1129–1137CrossRefGoogle Scholar
  28. Désaunay Y, Guérault D (1997) Seasonal and long term changes in biometrics of Anguilla anguiilla (L.) eel larvae: a possible relationship between recruitment variation and North Atlantic ecosystem productivity. J Fish Biol 51A:317–339. doi: https://doi.org/10.1111/j.1095-8649.1997.tb06106.x CrossRefGoogle Scholar
  29. Désaunay Y, Guérault D, Lecomte-Finiger R (1996a) Variation of the oceanic larval migration of Anguilla anguilla (L.) glass eels from a two year study in the Vilaine Estuary (France). Arch Pol Fish 4:195–210Google Scholar
  30. Désaunay Y, Lecomte-Finger R, Guérault D (1996b) Mean age and migration patterns of Anguilla anguilla (L.) glass eels from three French estuaries (Somme, Vilaine and Adour rivers). Arch Pol Fish 4:187–194Google Scholar
  31. Fox CJ, Folkvord A, Geffen AJ (2003) Otolith micro-increment formation in herring Clupea harengus larvae in relation to growth rate. Mar Ecol Prog Ser 264:83–94. doi: https://doi.org/10.3354/meps264083 CrossRefGoogle Scholar
  32. Ishikawa S, Suzuki K, Inagaki T, S. W, Kimura Y, Okamura A, Otake T, Mochioka N, Suzuki Y, Hashumoto H, Oya M, Miller MJ, Lee TW, Fricke H, Tsukamoto K (2001) Spawning time and place of the Japanese eel Anguilla japonica in the North Equatorial Current of the western North Pacific Ocean. Fish Sci 67:1097–1103. doi: https://doi.org/10.1046/j.1444-2906.2001.00366.x
  33. 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 51:343–353. doi: https://doi.org/10.1007/s10228-004-0241-7 CrossRefGoogle Scholar
  34. Jellyman DJ (2003) The distribution and biology of the South Pacific species of Anguilla. In: Aida K, Tsukamoto K, Yamauchi K (eds) Eel biology. Springer, Tokyo, pp 275–292CrossRefGoogle Scholar
  35. Kajihara T (1988) Distribution of Anguilla japonica leptocephali in western Pacific during September 1986. Bull Jap Soc Sci Fish 54:929–933CrossRefGoogle Scholar
  36. Kawakami Y, Mochioka N, Nakazono A (1998) Immigration period and age of Anguilla japonica glass-eels entering rivers in Northern Kyushu, Japan during 1994. Fish Sci 64:235–239CrossRefGoogle Scholar
  37. Kawakami Y, Mochioka N, Nakazono A (1999) Immigration patterns of glass-eels Anguilla japonica entering rivers in northern Kyushu, Japan. Bull Mar Sci 64:315–327Google Scholar
  38. Kettle AJ, Haines K (2006) How does the European eel (Anguilla anguilla) retain its population structure during its larval migration across the North Atlantic Ocean? Can J Fish Aquat Sci 63:90–106. doi: https://doi.org/10.1139/f05-198 CrossRefGoogle Scholar
  39. 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
  40. 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
  41. Kracht R (1982) On the geographic distribution and migration of I- and II-group eel larvae as studied during the 1979 Sargasso Sea Expedition. Helgoländer Meeresun 35:321–327. doi: https://doi.org/10.1007/BF02006140 CrossRefGoogle Scholar
  42. 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. doi: https://doi.org/10.3354/meps309233 CrossRefGoogle Scholar
  43. Lecomte-Finiger R (1992) Growth history and age at recruitment of European glass eels (Anguilla anguilla) as revealed by otolith microstructure. Mar Biol (Berl) 114:205–210. doi: https://doi.org/10.1007/BF00349520 CrossRefGoogle Scholar
  44. Liao C, Kuo C-L, Tzeng W-N, Hwang S-T, Wu C-L, Wang C-H, Wang Y-Z (1996) The first time of leptocephali of Japanese eel Anguilla japonica collected by Taiwanese researchers. J Taiwan Fish Res 4:107–116Google Scholar
  45. Martin MH (1995) Validation of daily growth increments in otoliths of Anguilla rostrata (Lesueur) elvers. Can J Zool 73:208–211CrossRefGoogle Scholar
  46. Marui M, Arai T, Miller MJ, Jellyman DJ, Tsukamoto K (2001) Comparison of early life history between New Zealand temperate eels and Pacific tropical eels revealed by otolith microstructure and microchemistry. Mar Ecol Prog Ser 213:273–284. doi: https://doi.org/10.3354/meps213273 CrossRefGoogle Scholar
  47. 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
  48. 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
  49. McCleave JD, Brickley PJ, O’Brien KM, Kistner DA, Wong MW, Gallagher M, Watson SM (1998) Do leptocephali of the European eel swim to reach continental waters? Status of the question. J Mar Biol Assoc UK 78:285–306CrossRefGoogle Scholar
  50. Miller MJ, Mochioka N, Otake T, Tsukamoto K (2002) Evidence of a spawning area of Anguilla marmorata in the western North Pacific. Mar Biol (Berl) 140:809–814. doi: https://doi.org/10.1007/s00227-001-0754-9 CrossRefGoogle Scholar
  51. Mochioka N, Otake T, Tsukamoto K (1994) Anguilla japonica leptocephali. In: Otake T, Tsukamoto K (eds) Preliminary Report of the Hakuho Maru Cruise KH-91–4. Ocean Research Institute, University of Tokyo, Tokyo, pp 28–36Google Scholar
  52. Mochioka N, Hasumoto H, Otake T, Inagaki T, Tsukamoto K (1995) Horizontal distribution of Anguilla japonica leptocephali. In: Inagaki T, Tsukamoto K (eds) Preliminary Report of the Hakuho Maru Cruise KH-94-2 (Leg 3). Ocean research Institute, University of Tokyo, Tokyo, pp 33–38Google Scholar
  53. Oyadomari JK, Auer NN (2007) Influence of rearing temperature and feeding regime on otolith increment deposition in larval ciscoes. Trans Am Fish Soc 136:766–777. doi: https://doi.org/10.1577/T06-011.1 CrossRefGoogle Scholar
  54. Ozawa T, Kakizoe F, Tabeta O, Maeda T, Yuwaki Y (1991) Japanese eel leptocephali from three cruises in the western North Pacific. Bull Jap Soc Sci Fish 57:1877–1881CrossRefGoogle Scholar
  55. Pannella G (1971) Fish otoliths: daily growth layers and periodical patterns. Science 173:1124–1127. doi: https://doi.org/10.1126/science.173.4002.1124 CrossRefGoogle Scholar
  56. Payan P, De Pontual H, Edeyer A, Borelli G, Boeuf G, Mayer-Gostan N (2004) Effects of stress on plasma homeostasis, endolymph chemistry, and check formation during otolith growth in rainbow trout (Oncorhynchus mykiss). Can J Fish Aquat Sci 61:1247–1255. doi: https://doi.org/10.1139/f04-059 CrossRefGoogle Scholar
  57. Powles PM, Warlen SM (2002) Recruitment season, size, and age of young American eels (Anguilla rostrata) entering an estuary near Beaufort, North Carolina. Fish Bull (Wash DC) 100:299–306Google Scholar
  58. Powles PM, Hare JA, Laban EH, Warlen SM (2006) Does eel metamorphosis cause a breakdown in the tenets of otolith applications? A case study using the speckled worm eel (Myrophis punctatus, Ophichthidae). Can J Fish Aquat Sci 63:1460–1468. doi: https://doi.org/10.1139/F06-052 CrossRefGoogle Scholar
  59. Robinet T, Lecomte-Finiger R, Escoubeyrou K, Feunten E (2003) Tropical eels Anguilla spp. recruiting to Réunion Island in the Indian Ocean: taxonomy, patterns of recruitment and early life histories. Mar Ecol Prog Ser 259:263–272. doi: https://doi.org/10.3354/meps259263 CrossRefGoogle Scholar
  60. Schmidt J (1922) The breeding places of the eel. Philos T R Soc B 211:179–208. doi: https://doi.org/10.1098/rstb.1923.0004 CrossRefGoogle Scholar
  61. Schmidt J (1935) Danish eel investigations during 25 years (1905–1930). The Carlsberg Foundation’s Oceanographical Expedition Round the World 1928–1930 and Previous Danish Oceanographical Expeditions under the Leadership of the Late Professor Johannes Schmidt. The Carlsberg Foundation, CopenhagenGoogle Scholar
  62. Schoth M, Tesch F-W (1982) Spatial distribution of 0-group eel larvae (Anguilla sp.) in the Sargasso Sea. Helgoländer Meeresun 35:309–320. doi: https://doi.org/10.1007/BF02006139 CrossRefGoogle Scholar
  63. Shiao J-C, Tzeng W-N, Collins A, Jellyman DJ (2001) Dispersal pattern of glass eel stage of Anguilla australis revealed by otoloth growth stages. Mar Ecol Prog Ser 219:241–250. doi: https://doi.org/10.3354/meps219241 CrossRefGoogle Scholar
  64. Shiao J-C, Tzeng W-N, Collins A, Iizuka Y (2002) Role of marine larval duration and growth rate of glass eels in determining the distribution of Anguilla reinhardtii and A. australis on Australian eastern coasts. Mar Freshw Res 53:687–695. doi: https://doi.org/10.1071/MF01037 CrossRefGoogle Scholar
  65. 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 70:339–341. doi: https://doi.org/10.1111/j.1444-2906.2003.00810.x CrossRefGoogle Scholar
  66. Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn. Freeman, New YorkGoogle Scholar
  67. Sugeha HY, Shinoda A, Marui M, Arai T, Tsukamoto K (2001) Validation of otolith daily increments in the tropical eel Anguilla marmorata. Mar Ecol Prog Ser 220:291–294. doi: https://doi.org/10.3354/meps220291 CrossRefGoogle Scholar
  68. Tabeta O, Takai T (1975) Leptocephali of Anguilla japonica found in the waters south of the Okinawa Islands. Bull Jap Soc Sci Fish 41:137–145CrossRefGoogle Scholar
  69. Tabeta O, Mochioka N (1988) Anguillid leptocephali from the waters south of Okinawa and east of Taiwan and Luzon, western North Pacific, in 1986. Bull Jap Soc Sci Fish 54:935–940CrossRefGoogle Scholar
  70. Tabeta O, Mochioka N (2003) The glass eel. In: Aida K, Tsukamoto K, Yamauchi K (eds) Eel Biology. Springer, Tokyo, pp 75–87CrossRefGoogle Scholar
  71. Tabeta O, Tanaka K, Yamada J, Tzeng WN (1987) Aspects of the early life history of the Japanese eel Anguilla japonica determined from otolith microstructure. Bull Jap Soc Sci Fish 53:1727–1734CrossRefGoogle Scholar
  72. Tesch F-W, Wegner G (1990) The distribution of small larvae of Anguilla sp. related to hydrographic conditions 1981 between Bermuda and Puerto Rico. Int Rev Gesamten Hydrobiol 75:845–858. doi: https://doi.org/10.1002/iroh.19900750629 CrossRefGoogle Scholar
  73. Tseng M-C, Tzeng W-N, Lee S-C (2006) Population genetic structure of the Japanese eel Anguilla japonica in the northwest Pacific Ocean: evidence of non-panmictic populations. Mar Ecol Prog Ser 308:221–230. doi: https://doi.org/10.3354/meps308221 CrossRefGoogle Scholar
  74. Tsukamoto K (1989) Otolith daily increments in the Japanese eel. Bull Jap Soc Sci Fish 55:1017–1021CrossRefGoogle Scholar
  75. Tsukamoto K (1990) Recruitment mechanism of the eel, Anguilla japonica, to the Japanese coast. J Fish Biol 36:659–671. doi: https://doi.org/10.1111/j.1095-8649.1990.tb04320.x CrossRefGoogle Scholar
  76. Tsukamoto K (1992) Discovery of the spawning area for Japanese eel. Nature 356:789–791. doi: https://doi.org/10.1038/356789a0 CrossRefGoogle Scholar
  77. Tsukamoto K (1995) Leptocephalus biology: Anguilla japonica leptocephali collected during KH–94–2. In: Inagaki T, Tsukamoto K (eds) Preliminary Report of the Hakuho Maru Cruise KH-94-2 (Leg 3). Ocean research Institute, University of Tokyo, Tokyo, p 15Google Scholar
  78. Tsukamoto K (2006) Spawning of eels near a seamount. Nature 439:929. doi: https://doi.org/10.1038/439929a CrossRefGoogle Scholar
  79. Tsukamoto K, Lee T-W, Fricke H (2003) Spawning area of the Japanese eel. In: Aida K, Tsukamoto K, Yamauchi K (eds) Eel Biology. Springer, Tokyo, pp 121–140CrossRefGoogle Scholar
  80. Tzeng WN (1990) Relationship between growth rate and age at recruitment of Anguilla japonica elvers in a Taiwan estuary as inferred from otolith growth increments. Mar Biol (Berl) 107:75–81. doi: https://doi.org/10.1007/BF01313244 CrossRefGoogle Scholar
  81. Tzeng WN, Tsai YC (1992) Otolith microstructure and daily age of Anguilla japonica, Temminck & Schlegel elvers from the estuaries of Taiwan with reference to unit stock and larval migration. J Fish Biol 40:845–857. doi: https://doi.org/10.1111/j.1095-8649.1992.tb02631.x CrossRefGoogle Scholar
  82. Umezawa A, Tsukamoto K (1990) Age and birth date of the glass eel, Anguilla japonica, collected in Taiwan. Bull Jap Soc Sci Fish 56:1199–1202CrossRefGoogle Scholar
  83. Umezawa A, Tsukamoto K (1991) Factors influencing otoloth increment formation in Japanese eel, Anguilla japonica T. & S., elvers. J Fish Biol 39:211–223. doi: https://doi.org/10.1111/j.1095-8649.1991.tb04357.x CrossRefGoogle Scholar
  84. 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
  85. Wang C-H, Tzeng W-N (1998) Interpretation of geographic variation in size of American eel Anguilla rostrata elvers on the Atlantic coast of North America using their life history and otolith ageing. Mar Ecol Prog Ser 168:35–43. doi: https://doi.org/10.3354/meps168035 CrossRefGoogle Scholar
  86. Wang CH, Tzeng WN (2000) The timing of metamorphosis and growth rates of American and European eel leptcephali: a mechanism of larval segregative migration. Fish Res 46:191–205. doi: https://doi.org/10.1016/S0165-7836(00)00146-6 CrossRefGoogle Scholar
  87. Wippelhauser GS, McCleave KD, Kleckner RC (1985) Anguilla rostrata leptocephali in the Sargasso Sea during February and March 1981. Dana 4:93–98Google Scholar
  88. Wirth T, Bernatchez L (2001) Genetic evidence against panmixia in the European eel. Nature 409:1037–1040. doi: https://doi.org/10.1038/35059079 CrossRefGoogle Scholar
  89. Wirth T, Bernatchez L (2003) Decline of North Atlantic eels: a fatal synergy? Proc Roy Soc B Biol Sci 270:681–688CrossRefGoogle Scholar

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© Springer-Verlag 2008

Authors and Affiliations

  1. 1.School of Marine SciencesUniversity of MaineOronoUSA

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