Abstract
The timing of downstream migrations of anguillid silver eels in relation to environmental factors in rivers has been examined using various types of data. Less is known about the factors that affect when silver eels leave estuaries and enter the sea or about the onset of the spawning migrations of eels living in brackish-water coastal areas. The timing of collections of Japanese eels, Anguilla japonica, in shoreline set nets in Mikawa Bay, Japan, were analyzed in relation to environmental variables such as water temperature, lunar phase, rainfall and wind speed over a 10 year period from 1997 to 2006. Higher catches of silver eels occurred during new moon periods in November and December as water temperatures decreased in the bay, and when the gonadosomatic index values of the eels were highest. Hurdle model analyses for clarifying the relationship between the catch of eels and environmental factors (lunar cycle, rainfall and wind) indicated the catches of eels were correlated with the two different environmental factors of wind strength 2 days earlier and lunar cycle, while rainfall was not selected by the model. This suggests that different factors are important for determining when eels migrate in coastal waters compared to during their downstream migrations in freshwater.
Similar content being viewed by others
References
Aarastrup K, Økland F, Hansen MM, Righton D, Gargan P, Castonguay M, Bernatchez L, Howey P, Sparholt H, Pedersen MI, Mckinley RS (2009) Oceanic spawning migration of the European Eel (Anguilla anguilla). Science 325:1660
Aarestrup K, Thorstad EB, Koed A, Jepsen N, Svendsen JC, Pedersen MI, Skov C, Økland F (2008) Survival and behaviour of European silver eel in late freshwater and early marine phase during spring migration. Fish Manag Ecol 15:435–440
Acou A, Laffaille P, Legault A, Feunteun E (2008) Migration pattern of silver eel (Anguilla anguilla, L) in an obstructed river system. Ecol Freshw Fish 17:432–442
Allen JRM, Wootton RJ (1984) Temporal patterns of diet and rate of food consumption of the three-spined stickleback (Gasterosteus aculeatus) in Llyn Frongoch, upland Welsh lake. Freshw Biol 14:335–346
Aoyama J, Miller MJ (2003) The silver eel. In: Aida K, Tsukamoto K, Yamauchi K (eds) Eel biology. Springer, Tokyo, pp 107–117
Aoyama J, Sasai S, Miller MJ, Shinoda A, Nakamura A, KawazuK TK (2002) A preliminary study of the movements of yellow and silver eels, Anguilla japonica, in the estuary of the Fukui River, Japan, as revealed by acoustic tracking. Hydrobiology 470:31–36
Aroua S, Schmitz M, Baloche S, Vidal B, Rousseau K, Dufour S (2005) Endocrine evidence that silvering, a secondary metamorphosis in the eel, is a pubertal rather than a metamorphic event. Neuroendocrinol 82:221–232
Béguer-Pon M, Castonguay M, Benchetrit J, Dl H, Verreault G, Mailhot Y, Tremblay V, Lefaivre D, Legault M, Stanley D, Dodson JJ (2014) Large-scale migration patterns of silver American eels from the St. Lawrence river to the gulf of St. Lawrence using acoustic telemetry. Can J Fish Aquat Sci 71:1579–1592
Boëtius J (1967) Experimental indication of lunar activity in European silver eels Anguilla anguilla. Medellelser fra Danmarls Fiskeri og Havundersøgelser 6:1–6
Boubee JA, Mitchell CP, Chisnall BL, West DW, Bowman EJ, Haro A (2001) Factors regulating the downstream migration of mature eels (Anguilla spp.) at Aniwhenua Dam, Bay of Plenty, New Zealand. N Z J Mar Freshw Res 35:121–134
Bradford RG, Carr JW, Page FH, Whoriskey F (2009) Migation of silver American eels through a macrotidal estuary and bay. Am Fish Soc Symp 69:275–292
Breukelaar AW, Ingendahl D, Vriese T, De Laak G, Staas S, Klein Breteler JGP (2009) Route choices, migration speeds and daily migration activity European silver eels Anguilla anguilla in the River Rhine, north-west Europe. J Fish Biol 74:2139–2157
Bruijs MCM, Durif CMF (2009) Silver eel migration and behaviour. In: Thillart G, Dufour S, Rankin JC (eds) Spawning migration of the European Eel. Springer, Netherlands, pp 65–95
Bultel E, Lasne E, Acou A, Guillaudeau J, Bertier C, Feunteun E (2014) Migration behaviour of silver eels (Anguilla anguilla) in a large estuary of Western European inferred from acoustic telemetry. Estuar Coast Shelf Sci 137:23–31
Burnet AMR (1969) Migrating eels in a Canterbury river, New Zealand. N Z J Mar Freshw Res 3:230–244
Cairns D (1941) Life-history of the two species of New Zealand fresh-water eel. Part I. Taxonomy, age and growth, migration and distribution. N Z J Sci Technol B23:53b–72b
Carassou L, Dzwonkowski B, Hernandez FJ, Powers SP, Park K, Graham WM, Mareska J (2011) Environmental influences on juvenile fish abundances in a river-dominated coastal system. Mar Coast Fish 3:411–427
Crook DA, Macdonald JI, Morrongiello JR, Belcher CA, Lovett D, Walker A, Nicol S (2014) Environmental cues and extended estuarine residence in seaward migrating eels (Anguilla australis). Freshw Biol 59:1710–1720
Daverat F, Limburg KE, Thibault I, Shiao JC, Dodson JJ, Caron FO, Tzeng WN, Iizuka Y, Wickstrom H (2006) Phenotypic plasticity of habitat use by three temperate eel species, Anguilla anguilla A. japonica and A. rostrata. Mar Ecol Prog Ser 308:231–241
Davidsen JG, Finstad B, Okland F, Thorstad EB, Mo TA, Rikardsen AH (2011) Early marine migration of European silver eel Anguilla anguilla in northern Norway. J Fish Biol 78:1390–1404
Deelder CL (1954) Factors affecting the migration of the silver eel in Dutch inland waters. Journal du Conseil, Conseil International Pour l’Exploration de la Mer 20:177–185
Durif CMF, Elie P (2008) Predicting downstream migration of silver eels in a large river catchment based on commercial fishery data. Fish Manag Ecol 15:127–13
Durif C, Elie P, Gosset C, Rives J, Travade F, Dixon DA (2003) Behavioral study of downstream migrating eels by radio-telemetry at a small hydroelectric power plant. In: Bethesda DD (ed) Biology, management, and protection of Catadromous eels. American Fisheries Society, Maryland, pp 343–356
Durif C, Dufour S, Elie P (2005) The silvering process of Anguilla anguilla: a new classification from the yellow resident to the silver migrating stage. J Fish Biol 66:1025–1043
Fraser NHC, Metcalfe NB (1997) The cost of being nocturnal: feeding efficiency in relation to light intensity in juvenile Atlantic salmon. Funct Ecol 11:385–391
Han YS, Liao IC, Huang YS, He JT, Chang CW, Tzeng WN (2003) Synchronous changes of morphology and gonadal development of silvering Japanese eel Anguilla japonica. Aquaculture 219:783–796
Haraldstad O, Vøllestad LA, Jonsson B (1985) Descent of European silver eels, Anguilla anguilla L., in a Norwegian watercourse. J Fish Biol 26:37–41
Haro A (2003) Downstream migration of silver-phase anguillid eels. In: Aida K, Tsukamoto K, Yamauchi K (eds) Eel biology. Springer, Tokyo, pp 215–222
Higham TE, Stewart WJ, Wainwright PC (2015) Turbulence, temperature, and turbidity: the ecomechanics of predator–prey interactions in fishes. Integr Comp Biol 55:6–20
Hvidsten NA (1985) Yield of silver eel and factors effecting downstream migration in the stream Imsa Norway. Institute of Freshwater Research Drottningholm Report.pp75-85
Jansen HM, Winter HV, Bruijs MCM, Polman HJG (2007) Just go with the flow? route selection and mortality during downstream migration of silver eels in relation to river discharge. ICES J Mar Sci 64:1437–1443
Jessop BM, Cairns DK, Thibault I, Tzeng WN (2008) Life history of American eel Anguilla rostrata: new insights from otolith microchemistry. Aquat Biol 1:205–216
Kotake A, Okamura A, Yamada Y, Utoh T, Arai T, Miller MJ, Oka HP, Tsukamoto K (2005) Seasonal variation in the migratory history of the Japanese eel Anguilla japonica in Mikawa Bay, Japan. Mar Ecol Prog Ser 293:213–221
Kotake A, Arai T, Okamura A, Yamada Y, Utoh T, Oka HP, Miller MJ, Tsukamoto K (2007) Ecological aspects of the Japanese eel, Anguilla japonica, collected from coastal areas of Japan. Zool Sci 24:1213–1221
Lowe RH (1952) The influence of light and other factors on the seaward migration of the silver eel (Anguilla anguilla L). J Anim Ecol 21:275–309
Mazur MJ, Beauchamp DA (2003) A comparison of visual prey detection among species of piscivorous salmonids: effects of light and low turbidities. Environ Biol Fish 67:397–405
McCleave JD, Arnold GP (1999) Movements of yellow- and silver-phase European eels (Anguilla anguilla L.) tracked in the western North Sea. ICES J Mar Sci 56:510–536
Miyai T, Aoyama J, Sasai S, Inoue JG, Miller MJ, Tsukamoto K (2004) Ecological aspects of the downstream migration of introduced European eels in the Uono River, Japan. Environ Biol Fish 71:105–114
Okamura A, Yamada Y, Tanaka S, Horie N, Utoh T, Mikawa N, Akazawa A, Oka HP (2002) Atmospheric depression as the final trigger for the seaward migration of the Japanese eel Anguilla japonica. Mar Ecol Prog Ser 234:281–288
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 80:77–89
Parker SJ, McCleave JD (1997) Selective tidal stream transport by American eels during homing movements and estuarine migration. J Mar Biol Assoc UK 77:871–889
Poole WR, Reynolds JD (1996) Growth rate and age at migration of Anguilla anguilla. J Fish Biol 48:633–642
Pursiainen M, Tulonen J (1986) Eel escapement from small forest lakes. Vie et Milieu 36:287–290
R Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria. URL http://www.Rproject.org/
Robertis AD, Ryer CH, Veloza A, Brodeur RD (2003) Differential effects of turbidity on prey consumption of piscivorous and planktivorous fish. Can J Fish Aquat Sci 60:1517–26
Rohr DH, Lokman PM, Davie PS, Young G (2001) 11-Ketotestosterone induces silvering-related changes in immature female short-finned eels, Anguilla australis. Comp Biochem Physiol A Mol Integr Physiol 130:701–714
Sasai S, Aoyama J, Watanabe S, Kaneko T, Miller MJ, Tsukamoto K (2001) The occurrence of migrating silver eels, Anguilla japonica, in the East China Sea. Mar Ecol Prog Ser 212:305–310
Schabetsberger R, Økland F, Aarestrup K, Kalfatak D, Sichrowsky U, Tambets M, Dall’Olmo G, Kaiser R, Miller PI (2013) Oceanic migration behaviour of tropical Pacific eels from Vanuatu. Mar Ecol Prog Ser 475:177–190
Setiawan AL, Wylie JW, Forbes EL, Lokman PM (2012) The effects of 11-ketotestosternoe on occupation of downstream location and seawater in the New Zealand shortfinned eel, Anguilla australis. Zool Sci 29:1–5
Smith MW, Saunders JW (1955) The American eel in certain fresh waters of the Maritime Provinces of Canada. J Fish Res Board Can 12:238–269
Stein F, Doering-Arjes P, Fladung E, Brämick U, Schröder B (2016) Downstream migration of the European eel (Anguilla Anguilla) in the Elbe river, Germany: Movement patterns and the potential impact of environment factors. River Res Appl 32:666–676
Sudo R, Tsukamoto K (2015) Migratory restlessness and the role of androgen for increasing behavioral drive in the spawning migration of the Japanese eel. Sci Rep 5:17430
Sudo R, Tosaka R, Ijiri S, Adachi S, Suetake H, Suzuki Y, Horie N, Tanaka S, Aoyama J, Tsukamoto K (2011) The effect of temperature decrease on oocyte development, sex steroids and gonadotropin β-subunit mRNA expression levels in female Japanese eels Anguilla japonica. Fish Sci 77:575–582
Sudo R, Tosaka R, Ijiri S, Adachi S, Aoyama J, Tsukamoto K (2012) 11-ketotestosterone synchronously induces oocyte development and silvering related changes in the Japanese eel, Anguilla japonica. Zool Sci 29:254–259
Sudo R, Yamada Y, Mnabe R, Tsukamoto K (2014) Effect of lunar periodicity on the locomotor activity of silver-stage Japanese eel. Anguilla japonica J Ethol 32:111–115
Svendäng H, Neuman E, Wickström H (1996) Maturation patterns in female European eel: age and size at the silver eel stage. J Fish Biol 48:342–351
Tesch FW (2003) The eel. Blackwell Publishing, London
Tesch FW, Rohlf N (2003) Migration from continental waters to the spawning grounds. In: Aida K, Tsukamoto K, Yamauchi K (eds) Eel biology. Springer, Tokyo, pp 223–234
Todd PR (1981) Timing of periodicity of migrating New Zealand freshwater eels (Anguilla spp.). New Zeal J Mar Fresh 15:225–235
Trancat T, Acou A, Oliveira ED, Feunteun E (2013) Forecasting animal migration using SARIMAX: an efficient means of reducing silver eel mortality caused by turbines. Endanger Species Res 21:181–190
Tsukamoto K, Arai T (2001) Facultative catadromy of the eel Anguilla japonica between freshwater and seawater habitats. Mar Ecol Prog Ser 220:265–276
Tsukamoto K, Nakai I, Tesch FW (1998) Do all freshwater eels migrate? Nature 396:635–636
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
Tzeng WN, Shiao JC, Yamada Y, Oka HP (2003) Life history patterns of Japanese eel Anguilla japonica in Mikawa Bay, Japan. Am Fish Soc Symp 33:285–293
Utoh T, Mikawa N, Okamura A, Yamada Y, Tanaka S, Horie N, Akazawa A, Oka HP (2004) Ovarian morphology of the Japanese eel in Mikawa Bay. J Fish Biol 64:502–513
Vøllestad LA (1986) Temperature dependent activity of brackish water yellow eels Anguilla anguilla. Aquac Fish Manag 17:201–206
Westin L, Nyman L (1979) Activity, orientation and migration of Baltic eel (Anguilla anguilla L.). Rapp P-V Réun Cons Int Explor Mer 174:115–123
Winn HE, Richkus WA, Winn LK (1975) Sexual dimorphism and natural movements of the American eel, Anguilla rostrata, in Rhode Island streams and estuaries. Helgoländer Meeresun 27:156–166
Zamor RM, Grossman GD (2007) Turbidity affects foraging success of drift-feeding rosyside dace. T Am Fish Soc 136:167–176
Zeileis A, Kleiber C, Jackman S (2008) Regression models for count data in R. J. Stat. Software 27 (8), URL http://www.jstatsoft.org/v27/i08/.
Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York, p 574
Acknowledgements
We thank the ten fishermen and members of the IRAGO Institute for their kind collaboration in collecting eels and dissecting samples. This work was supported in part by a KAKEN S grant (No. 21–228005) from the Ministry of Education, Culture, Sports, Science and Technology of Japan. The first author was supported by a Research Fellowship of the Japan Society for the Promotion of Science for Young Scientists (No. 25–5842).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Sudo, R., Okamura, A., Fukuda, N. et al. Environmental factors affecting the onset of spawning migrations of Japanese eels (Anguilla japonica) in Mikawa Bay Japan. Environ Biol Fish 100, 237–249 (2017). https://doi.org/10.1007/s10641-017-0575-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10641-017-0575-4