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Rhythmic activity of inshore migration of tropical freshwater glass eels of the genus Anguilla

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Abstract

Compared with temperate Anguilla, little is known about the early marine migration and recruitment mechanisms of these tropical eels. To understand the ecological and behavioural mechanisms of their inshore migration in tropical Anguilla, systematic research on their periodicity of inshore migration was conducted for 24 h over 9 to 13 consecutive days before and after the new moon dates four times in one year. Glass eel (juvenile) collections (151 to 4371 specimens during each survey period) in the Poigar River, north Sulawesi Island, Indonesia indicated a lunar periodicity, in which peak recruitment continued for 2 to 4 days during the new moon period; then, the recruitment sharply decreased before and after the new moon. Daily glass eel migration occurred in two peaks during the ebb (20:00) and flood (02:00) tides, while there was no significant different glass eel recruitment between the flood tide and ebb tides. Although the “selective tidal stream transport” that glass eels utilize during the flood tide for recruitment is widely accepted to be the main mechanism of inshore migration behaviour through estuaries to freshwater habitats for temperate glass eels, we did not find this mechanism during this study. These results suggest that the main recruitment mechanism for tropical glass eels may be associated with both endogenous rhythms (biological clock) and exogenous factors (tidal orientation) in the study site. The rhythmic activity of migrating tropical glass eels found in this study also contributes not only to understanding the biological and ecological implications but also provides clues for stock management and conservation of Anguilla, which have been critically declining in recruitment worldwide in recent decades.

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References

  • Aoyama J, Yoshinaga T, Shinoda A, Shirotori F, Yambot AV, Han YS (2015) Seasonal changes in species composition of glass eels of the genus Anguilla (teleostei: anguillidae) recruiting to the Cagayan River, Luzon Island, the Philippines. Pac Sci 69:263–270

    Google Scholar 

  • Arai T (2014) Do we protect freshwater eels or do we drive them to extinction? SpringerPlus 3:534

    PubMed  PubMed Central  Google Scholar 

  • Arai T (2016) Taxonomy and distribution. In: Arai T (ed) Biology and ecology of anguillid eels. CRC Press, pp 1–20 340 pp

  • Arai T, Aoyama J, Limbong D, Tsukamoto K (1999) Species composition and inshore migration of the tropical eels Anguilla spp. recruiting to the estuary of the Poigar River, Sulawesi Island. Mar Ecol Prog Ser 188:299–303

    Google Scholar 

  • Arribas C, Ferna’ndez-Delgado C, Olivia-Paterna FJ, Drake P (2012) Oceanic and local environmental conditions as forcing mechanisms of the glass eel recruitment to the southernmost European estuary. Estuar Coast Shelf Sci 107:45–57

    Google Scholar 

  • August SM, Hicks BJ (2008) Water temperature and upstream migration of glass eels in New Zealand: implications of climate change. Environ Biol Fish 81:195–205

    Google Scholar 

  • Bardonnet A, Dasse S, Parade M, Heland M (2003) Influence De L’alternance Jour/nuit Sur Les De’placements De Civelles En Fluvarium. Bull Fr Peche Piscic 368:9–20

    Google Scholar 

  • Barry J, McHarg K, Dodd JA, Adams CE (2015) Local scale, coastal currents influence recruitment to freshwater populations in the European eel Anguilla anguilla: a case study from the Isle of Man. J Fish Biol 86:1873–1880

    CAS  PubMed  Google Scholar 

  • Bonhommeau S, Chassot E, Planque B, Knap A, Le Pape O (2008) Impact of climate on eel populations of northern hemisphere. Mar Ecol Prog Ser 373:71–80

    Google Scholar 

  • Briand C, Fatin D, Legault A (2002) Role of eel odour on the efficiency of an eel, Anguilla anguilla, ladder and trap. Environ Biol Fish 65:473–477

    Google Scholar 

  • Budimawan, Lecomte-Finiger R (2005) Inshore migration of the tropical glass eels Anguilla marmorata recruiting to Poso estuary, Sulawesi Island, Indonesia. Vie et Milieu 55:7–14

    Google Scholar 

  • Bureau Du Colombier S, Bolliet V, Lambert P, Bardonnet A (2007) Energy and migratory behaviour in glass eels (Anguilla Anguilla). Physiol Behav 92:684–690

    CAS  PubMed  Google Scholar 

  • Castle PHJ, Williamson GR (1974) On the validity of the freshwater eel species Anguilla ancestralis Ege from Celebes. Copeia 2:569–570

    Google Scholar 

  • Castonguay M, Hodson PV, Moriarty C, Drinkwater KF, Jessop B (1994) Is there a role of ocean environment in American and European eel decline? Fish Oceanogr 3:197–203

    Google Scholar 

  • Chisnall BL, Martin ML, Hicks BJ (2003) Effect of harvest on size, abundance and production of freshwater eels (Anguilla australis and A. dieffenbachii) in a New Zealand stream. In: Dixon DA (ed) Biology, management and protection of catadromous eels. American Fisheries Society, Bethesda, pp 177–189

    Google Scholar 

  • Ciccotti E, Ricci T, Scardi M, Fresi E, Cataudella S (1995) Intraseasonal characterization of glass eel migration in the river Tiber: space and time dynamics. J Fish Biol 47:248–255

    Google Scholar 

  • Clevestam PD, Ogonowski M, Sjoberg NB, Wickstrom H (2011) Too short to spawn? Implications of small body size and swimming distance on successful migration and maturation of the European eel Anguilla anguilla. J Fish Biol 78:1073–1089

    CAS  PubMed  Google Scholar 

  • Creutzberg F (1958) Use of tidal streams by migrating elvers (Anguilla vulgaris, Turt.). Nature 181:357–358

  • Creutzberg F (1959) Discrimination between ebb and flood tide in migrating elvers (Anguilla vulgaris, Turt.) by means of olfactory perception. Nature. 184:1961–1962

    Google Scholar 

  • Creutzberg F (1961) On the orientation of migrating elvers (Anguilla vulgaris, Turt.) in a tidal area. Neth J Sea Res 1:257–338

    Google Scholar 

  • Crivelli AJ, Auphan N, Chauvelon P, Sandoz A, Menella JY, Poizat G (2008) Glass eel recruitment, Anguilla Anguilla (L.), in a Mediterranean lagoon assessed by a glass eel trap: factors explaining the catches. Hydrobiologia 602:79–86

    Google Scholar 

  • Crnjar R, Scalera G, Bigiani A, Tomassini Barbarossa I, Magherini PC, Pietra P (1992) Olfactory sensitivity to amino acids in the juvenile stages of the European eel Anguilla anguilla (L.). J Fish Biol 40:567–576

    CAS  Google Scholar 

  • De Casamajor MN, Bru N, Prouzet P (1999) Influence of night brightness and turbidity on the vertical migratory behavior of glass-eels (Anguilla anguilla L.) in the Adour estuary. Bull Fr Pêche Piscic 72:327–347

    Google Scholar 

  • De’saunay Y, Gue’rault D (1997) Seasonal and long-term changes in biometrics of eel larvae: a possible relationship between recruitment variation and North Atlantic ecosystem productivity. J Fish Biol 51(Suppl A):317–339

    Google Scholar 

  • Deelder CL (1952) On the migration of the elver (Anguilla vulgaris Turt.) at sea. J Cons perm int Explor Mer 20:187–218

    Google Scholar 

  • Deelder CL (1958) On the behaviour of elvers (Anguilla vulgaris Turt.) migrating from the sea into fresh water. J Cons Cons Int Explor Mer 24:135–146

  • Dekker W (2003) Did lack of spawners cause the collapse of the European eel, Anguilla anguilla? Fish Manag Ecol 10:365–376

    Google Scholar 

  • Dekker W (2008) Coming to grips with the eel stock slip-sliding away. In: Schechter MG, Leonard NJ (eds) International governance of fisheries ecosystems: learning from the past, finding solutions for the future. American Fisheries Society, Bethesda, pp 335–355

    Google Scholar 

  • Dou S, Tsukamoto K (2003) Observations on the nocturnal activity and feeding behabior of Anguilla japonica glass eels under laboratory conditions. Environ Biol Fish 67:389–395

    Google Scholar 

  • Dou S, Miller MJ, Tsukamoto K (2003) Growth, pigmentation and activity of juvenile Japanese eels in relation to temperature and fish size. J Fish Biol 63:152–165

    Google Scholar 

  • Edeline E, Dufour S, Elie P (2009) Proximate and ultimate control of eel continental dispersal. In: Van Den Thillart G, Dufour S, Rankin JC (eds) spawning migration of the european eel: reproduction index, a useful tool for conservation management. Fish and Fisheries Series 30:433–461

    Google Scholar 

  • Ege V (1939) A revision of the genus Anguilla Shaw. Dana Rep 16:8–256

    Google Scholar 

  • Elie P, Rochard E (1994) Migration des civelles d’anguilles (Anguilla anguilla L.) dans l’estuaires, modalite’s du phe´-nome’ne et caracte’ristiques des individus. Bull Fr Pêche Piscic 335:81–98

    Google Scholar 

  • Fontaine M (1950) Facteurs externes et internes re’gissant les migrations chez les poissons. Ann Biol 27:337–348

    Google Scholar 

  • Friedland KD, Miller MJ, Knights B (2007) Oceanic changes in the Sargasso Sea and declines in the recruitment of European eel. ICES J Mar Sci 64:519–530

    Google Scholar 

  • Fukuda N, Aoyama J, Yokouchi K, Tsukamoto K (2016) Periodicities of inshore migration and selective tidal stream transport of glass eels, Anguilla japonica, in Hamana Lake, Japan. Environ Biol Fish 99:309–323

    Google Scholar 

  • Gandolfi G, Pesaro M, Tongiorgo P (1984) Environmental factors affecting the ascent of elvers, Anguilla anguilla (L.), into the Arno river. Oebalia 10:17–35

    Google Scholar 

  • Gascuel D (1986) Flow-carried and active swimming migration of the glass eel (Anguilla anguilla) in the tidal area of a small estuary on the French Atlantic coast. Helgoländ Meeresun 40:321–326

    Google Scholar 

  • Gibson R (1992) Tidally-synchronised behaviour in marine fishes. In: rhythms in fishes. NATO ASI series a: life sciences vol. 236. Springer, New York, pp 63–81

  • Graynoth E, Jellyman D, Bonnett M (2008) Spawning escapement of female longfin eels. Ministry of Fisheries, new Zealand fisheries assessment report 2008/7, Wellington

  • Haenen O, van Ginneken V, Engelsma M, van den Thillart G (2002) Impact of eel viruses on recruitment of European eel. In: van den Thillart G, Dufour S, Cliff Rankin J (eds) Spawning migration of the European eel. Springer, London, pp 387–400

    Google Scholar 

  • Han YS (2011) Temperature-dependent recruitment delay of the Japanese glass eel Anguilla japonica in East Asia. Mar Biol 158:2349–2358

    Google Scholar 

  • Haro AJ, Krueger WH (1988) Pigmentation, size, and migration of elvers Anguilla rostrata (Lesueur) in a coastal Rhode Island stream. Can J Zool 66:2528–2533

    Google Scholar 

  • Haro A, Richkus W, Whalen K, Hoar A, Busch WD, Lary S, Brush T, Dixon D (2000) Populations decline of the American eel: implications for future research and management. Fisheries 25:7–16

    Google Scholar 

  • Harrison AJ, Walker AM, Pinder AC, Briand C, Aprahamian MW (2014) A review of glass eel migratory behaviour, sampling techniques and abundance estimates in estuaries: implications for assessing recruitment, local production and exploitation. Rev Fish Biol Fish 24:967–983

    Google Scholar 

  • Hewavitharane CA, Pickering TD, Ciro R, Mochioka N (2018) Species composition, abundance and seasonal recruitment patterns of freshwater eels (Anguilla spp.) to Viti Levu, Fiji Islands, in the western South Pacific. Mar Freshw Res 69:1704–1711

  • Hoyle SD, Jellyman DJ (2002) Longfin eels need reserves: modeling the effects of commercial harvest on stocks of New Zealand eels. Mar Freshw Res 53:887–895

    Google Scholar 

  • 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

    Google Scholar 

  • Jellyman DJ (1977) Invation of a New Zealand freshwater stream by glass-eels of two Anguilla spp. NZ Mar Freshw Res 11:193–209

    Google Scholar 

  • Jellyman DJ (1979) Upstream migration of glass eels (Anguilla spp.) in the Waikato River. New Zealand J Mar Freshw Res 13:13–22

  • Jellyman DJ, Lambert PW (2003) Factors affecting recruitment of glass eels into the Grey River, New Zealand. J Fish Biol 63:1067–1079

    Google Scholar 

  • Jellyman DJ, Chisnall BL, Bonnett ML, Sykes JRE (1999) Seasonal arrival patterns of juvenile freshwater eels (Anguilla spp.) in New Zealand. NZ Mar Freshw Res 33:249–261

    Google Scholar 

  • Jellyman DJ, Graynoth E, Francis RICC, Chisnall BL, Beentjes MP (2000) A review of the evidence for a decline in the abundance of longfinned eels (Anguilla dieffenbachii) in New Zealand. Ministry of Fisheries Research Project EEL9802, final research report, Auckland

  • Kirk RS (2003) The impact of Anguillicola crassus on European eels. Fish Manag Ecol 10:385–394

    Google Scholar 

  • Knights B (2003) A review of the possible impacts of long-term oceanic and climate changes and fishing mortality on recruitment of anguillid eels of the northern hemisphere. Sci Total Environ 310:237–244

    CAS  PubMed  Google Scholar 

  • Lafaille P, Caraguel JM, Legault A (2007) Temporal patterns in the upstream migration of European glass eels (Anguilla anguilla) at the Couesnon estuarine dam. Estuar Coast Shelf Sci 73:81–90

    Google Scholar 

  • Lambert P, Durozoi B, Beaulaton L (2007) Validation des hypothe’ses comportementales utilise’es dans la quantification du flux d’anguille (Anguilla anguilla) dans l’Isle. Contrat Indicang Rapport Cemagref No 115

  • Leatherland JF, Farbridge KJ, Boujard T (1992) Lunar and semilunar rhythms in fishes. In: rhythms in fishes. Springer: New York, vol 236:83–107

    Google Scholar 

  • Lin YJ, Chang YJ, Sun CL, Tzeng WN (2010) Evaluation of the Japanese eel fishery in the lower reaches of the Kao-Ping River, southwestern Taiwan using a per-recruit analysis. Fish Res 106:329–336

    Google Scholar 

  • McCleave JD, Jellyman DJ (2004) Male dominance in the New Zealand longfin eel population of a New Zealand river: probable causes and implications for management. North Am J Fish Manage 24:490–505

    Google Scholar 

  • McCleave JD, Kleckner RC (1982) Selective tidal stream transport in the estuarine migration of glass eels of the American eel (Anguilla rostrata). J Cons Cons Int Explor Me 40:262–271

    Google Scholar 

  • Moriarty C, Dekker W (1997) Management of the European eel Anguilla anguilla. Fish Bull 15:1–110

  • Palstra AP, Heppener DFM, van Ginneken VJT, Szekely C, van den Thillart G (2006) Are dioxin-like contaminants responsible for the eel (Anguilla anguilla) drama? Naturwissenschaften 93:145–148

    CAS  PubMed  Google Scholar 

  • Parker D, Weyl OLF, Tarachewski H (2011) Invasion of a south African Anguilla mossambica (Anguillidae) population by the alien gill worm Pseudodactylogyrus anguillae (Monogenea). Afric Zool 46:371–377

    Google Scholar 

  • 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 100:299–306

    Google Scholar 

  • Prouzet P, Odunlami M, Duquesne E, Boussouar A (2009) Analysis and visualization of the glass eel behavior (Anguilla anguilla) in the Adour estuary and estimate of its upstream migration speed. Aquat Living Resour 22:525–534

    Google Scholar 

  • Richkus WA, Whalen K (2000) Evidence for a decline in the abundance of the American eel, Anguilla rostrata (LeSueur), in North America since the early 1980s. Dana. 12:83–97

    Google Scholar 

  • Sheldon MR, McCleave JD (1985) Abundance of glass eels of the American eel Anguilla rostrata in mid-channel and near shore during estuarine migration. Le Nat Can 112:425–430

    Google Scholar 

  • Sola C (1995) Chemoattraction of upstream migrating glass eels Anguilla anguilla to earthy and green odorants. Environ Biol Fish 43:179–185

    Google Scholar 

  • Sorensen PW, Bianchini ML (1986) Environmental correlates of the freshwater migration of elvers of the American eel in a Rhode Island brook. Trans Am Fish Soc 115:258–268

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Sures B, Knopf K (2004) Parasites as a threat to freshwater eels? Sci 304:209–211 van Ginneken V, Bruijs M, murk T, Palstra a, van den Thillart G (2009) the effects of PCBs on the spawning migration of the European silver eel. In: van den Thillart G, Dufour S, Cliff Rankin J (eds) Spawning migration of the European eel. Springer, London, pp 365–386

    Google Scholar 

  • Tabeta O, Tanimoto T, Takai T, Matsui I, Imamura T (1976) Seasonal occurrence of anguillid elvers in Cagayan River, Luzon Island, the Philippines. Bull Jpn Soc Sci Fish 42:421–426

    Google Scholar 

  • Tesch FW (2003) The eel, 3rd edn. London, Blackwell Publishing

    Google Scholar 

  • Tongiorgi P, Tosi L, Balsamo M (1986) Thermal preferences inupstream migrating glass eels of Anguilla anguilla (L). J Fish Biol 28:501–510

    Google Scholar 

  • Tosi L, Sola C (1993) Role of geosmin, a typical inland water odour, in guiding glass eel Anguilla anguilla (L.) migration. Ethology 95:177–185

    Google Scholar 

  • Tosi L, Sala L, Sola C, Spampanato A, Tongiorgi P (1988) Experimental analysis of the thermal and salinity preferences of glass-eels, Anguilla anguilla (L.), before and during the upstream migration. J Fish Biol 33:721–733

    Google Scholar 

  • Trancart T, Lambert P, Rochard E, Daverat F, Coustillas J, Roqueplo C (2012) Alternative flood tide transport tactics in catadromous species: Anguilla anguilla, Liza ramada and Platichthys flesus. Estuar Coast Shelf Sci 99:191–198

    Google Scholar 

  • Tzeng WN (1985) Immigration timing and activity rhythms of the eel, Anguilla japonica, elvers in the estuary of northern Taiwan, with emphasis on environmental influences. Bull Jpn Soc Fish Oceanogr 47:11–27

    Google Scholar 

  • van Ginneken, V, Bruijs M, Murk AJ, Palstra AP, van den Thillart G (2009) The effect of PCBs on the spawning migration of European silver eel (Anguilla anguilla L.). In: Thillart GVD (ed) Spawning migration of the European eel. Springer, Germany, p 365–386

  • Verreault G, Dumont P, Mailhot Y (2004) Habitat losses and anthropogenic barriers as a cause of population decline for American eel (Anguilla rostrata) in St. Lawrence watershed, Canada. In: 2004 ICES annual science conference, Vigo, 22–25 September 2004. ICES, Copenhagen

  • Watanabe S, Aoyama J, Tsukamoto K (2009) A new species of freshwater eel, Anguilla luzonensis (Teleostei: Anguillidae) from Luzon Island of the Philippines. Fish Sci 75:387–392

    CAS  Google Scholar 

  • Weihs D (1978) Tidal stream transport as an efficient method for migration. J Cons Cons Int Explor Mer 38:92–99

    Google Scholar 

  • White EM, Knights B (1997) Environmental factors affecting migration of the European eel in the Rivers Severn and Avon, England. J Fish Biol 50:1104–1116

    Google Scholar 

  • Winter HV, Jansen HM, Breukelaar AW (2007) Silver eel mortality during downstream migration in the river Meuse, from a population perspective. ICES J Mar Sci 64:1444–1449

    Google Scholar 

  • Wippelhauser GS, McCleave JD (1987) Precision of behavior of migrating juvenile American eels (Anguilla rostrata) utilizing selective tidal stream transport. J Cons Cons Int Explor Mer 44:80–89

    Google Scholar 

  • Zompola S, Katselis G, Koutsikopoulos C, Cladas Y (2008) Temporal patterns of glass eel migration (Anguilla anguilla L. 1758) in relation to environmental factors in the Western Greek inland waters. Estuar Coast Shelf Sci 80:330–338

    Google Scholar 

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Acknowledgements

We are grateful to the students of Aquatic Resources Management Laboratory, Sam Ratulangi University, Indonesia, for their assistance during the field study. All specimens used in this study were cared in accordance with the guide for animal experimentation at Universiti Brunei Darussalam and fish-handling approval was granted by the animal experiment committee of the university. Furthermore, the Universiti Brunei Darussalam Ethics Committee also approved all experimental protocols in this study.

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  1. Environmental and Life Sciences Programme, Faculty of Science, Universiti Brunei Darussalam, Jalan Tungku Link, Gadong, BE, 1410, Brunei Darussalam

    Takaomi Arai

  2. Research Centre for Oceanography, Indonesian Institute of Sciences, Ancol Timur, Jakarta, 14430, Indonesia

    Hagi Yulia Sugeha

  3. Sintuwu Maroso University, Poso, 94619, Indonesia

    Daniel Limbong

  4. Graduate School of Agricultural and Life Sciences, The University of Tokyo, 1-1-1, Yayoi, Bukyo, Tokyo, 113-8657, Japan

    Katsumi Tsukamoto

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  1. Takaomi Arai
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Arai, T., Sugeha, H.Y., Limbong, D. et al. Rhythmic activity of inshore migration of tropical freshwater glass eels of the genus Anguilla. Environ Biol Fish 103, 1295–1308 (2020). https://doi.org/10.1007/s10641-020-01023-1

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