Environmental Biology of Fishes

, Volume 98, Issue 1, pp 457–468 | Cite as

Migratory history of African longfinned eel Anguilla mossambica from Maningory River, Madagascar: discovery of a unique pattern in otolith Sr:Ca ratios

  • Yu-Jia LinEmail author
  • Brian M. Jessop
  • Olaf L. F. Weyl
  • Yoshiyuki Iizuka
  • Shih-Huan Lin
  • Wann-Nian Tzeng


The migratory life histories were investigated for 30 African longfinned eels (Anguilla mossambica) of the yellow eel stage from the Maningory River, East Madagascar using otolith Sr:Ca ratios and parasite composition. The Sr:Ca ratio patterns of nine eels resembled those of A. mossambica in South Africa and of other anguillids and were classified as “typical” Sr:Ca ratio pattern eels. Typical pattern eels were further classified into freshwater residents (five eels) and habitat shifters (four eels) depending on whether they spent their first several years in saltwater. An unique Sr:Ca ratio pattern was found in 21 eels whereby the Sr:Ca ratios in the yellow eel stage increased drastically to extremely high values of 10 to 30 × 10−3 which have not been observed for any Elopomorpha species. These individuals were categorized as “elevated” Sr:Ca ratio pattern eels. The elevated pattern eels were characterized by significantly older ages, lower somatic growth rates, a much higher intensity and abundance of the gastrointestinal parasite Heliconema africanum and a lower abundance of the swim bladder parasite Anguillicoloides papernai. The extremely elevated Sr:Ca ratios of the yellow eel stage result most likely from inhabiting freshwater areas characterized by a high strontium concentration because the ratios far exceeded the known values for Elopomorpha species. Cyclical lows in the otolith Sr:Ca ratios of the elevated type eels corresponded to annuli, revealing either an overwintering movement pattern between habitats with different Sr:Ca ratios, or a seasonal change in the ambient environment.


Anguilla mossambica Otolith Sr:Ca ratio Parasite Age and growth Madagascar 



This work was facilitated by a grant from the National Research Foundation of South Africa (NRF) SA/Germany research cooperation programme (UID 72088). The South African Department of Economic Development and Environmental Affairs, Marine and Coastal Management and the Department of Agriculture are thanked for providing the relevant import and research permits. The research presented within this paper complies with the ethical clearance requirements of the South African Institute for Aquatic Biodiversity.


  1. Begg GA, Waldman JR (1999) An holistic approach to fish stock identification. Fish Res 43:35–44CrossRefGoogle Scholar
  2. Benstea JP, De Rham PH, Gattolliat JL, Gibon FM, Loiselle PV, Sartori M, Sparks JS, Stiassny MLJ (2003) Conserving Madagascar’s freshwater biodiversity. Bioscience 53:1101–1111CrossRefGoogle Scholar
  3. Bertrand M, Cabana G, Macrogliese DJ, Magnan P (2011) Estimating the feeding range of a mobile consumer in a river-flood plain system using δ13C gradients and parasites. J Anim Ecol 80:1313–1323PubMedCrossRefGoogle Scholar
  4. Brown RJ, Severin KP (2009) Otolith chemistry analyses indicate that water Sr:Ca is the primary factor influencing otolith Sr:Ca for freshwater and diadromous fish but not for marine fish. Can J Fish Aquat Sci 66:1790–1808CrossRefGoogle Scholar
  5. Bruton NM, Bok AH, Davies MT (1987) Life history styles of diadromous fishes in inland waters of southern Africa. In: Dadswell MJ, Klauda RJ, Moffitt CM, Saunders RL, Rulifson RA, Cooper JE (eds) Common Strategies of Anadromous and Catadromous Fishes. Am Fish Soc Sym 1: 104 – 121.Google Scholar
  6. Bush AO, Lafferty KD, Lotz JM, Shostak AW, Margolis (1997) Parasitology meets ecology on its own terms. J Parasitol 83:575–583PubMedCrossRefGoogle Scholar
  7. Campana SE (1999) Chemistry and composition of fish otoliths: pathways, mechanisms and applications. Mar Ecol Prog Ser 188:263–297CrossRefGoogle Scholar
  8. Campana SE (2005) Otolith science entering the 21st century. Mar Freshw Res 56:485–495CrossRefGoogle Scholar
  9. Campana SE, Neilson JD (1985) Microstructure of fish otoliths. Can J Fish Aquat Sci 42:1014–1032CrossRefGoogle Scholar
  10. Cone RS (1989) The need to reconsider the use of condition indices in fishery science. Trans Am Fish Soc 118:510–514CrossRefGoogle Scholar
  11. Crass RA (1969) The effects of land use on freshwater fish in South Africa, with particular reference to Natal. Hydrobiologia 34:38–56CrossRefGoogle Scholar
  12. Daverat F, Tomas J, Lahaye M, Palmer M, Elie P (2005) Tracking continental habitat shifts of eels using otolith Sr/Ca ratios: validation and application to the coastal, estuarine and riverine eels of the Gironde-Garonne-Dordogne watershed. Mar Freshw Res 56:619–627CrossRefGoogle Scholar
  13. de Villiers S (1999) Seawater strontium and Sr/Ca variability in the Atlantic and Pacific Oceans. Earth Planet Sci Lett 171:623–634CrossRefGoogle Scholar
  14. Elsdon TS, Wells BK, Campana SE, Gillanders BM, Jones CM, Limburg KE, Secor DH, Thorrold SR, Walther BD (2008) Otolith chemistry to describe movements and life-history parameters of fishes: hypotheses, assumptions, limitations and inferences. Oceanogr Mar Biol 46:297–330CrossRefGoogle Scholar
  15. Jackson PBN (1976) The distribution and growth of eels of the genus Anguilla Shaw, 1830, in the Western Indian Ocean. Travaux Docums ORSTOM 47:189–192Google Scholar
  16. Jessop BM, Shiao JC, Iizuki Y, Tzeng WN (2002) Migratory behaviour and habitat use by American eels Anguilla rostrata as revealed by otolith microchemistry. Mar Ecol Prog Ser 233:217–229CrossRefGoogle Scholar
  17. Jessop BM, Cairns DK, Thibault I, Tzeng WN (2008) Life history of American eel Anguilla rostrata: new insights from otolith microchemistry. Aquat Biol 1:205–216CrossRefGoogle Scholar
  18. Jubb RA (1964) The eels of South African rivers and observations on their ecology. In: David DHS (ed) Ecological Studies in Southern Africa, Junk, Den Haag, Holland. pp. 186–206.Google Scholar
  19. Katahira H, Mizuno K, Nagasawa K (2011) Host size-and habitat-dependent intensity of Heliconema longissimum (Nematoda: Physalopteridae) in the Japanese eel (Anguilla japonica). J Parasitol 97:994–998PubMedCrossRefGoogle Scholar
  20. Kirk RS, Kennedy CR, Lewis JW (2000) Effect of salinity on hatching, survival and infectivity of Anguillicola crassus (Nematoda: Dracunculoidea) larvae. Dis Aquat Org 40:211–218PubMedCrossRefGoogle Scholar
  21. Kraus RT, Secor DH (2004) Incorporation of strontium into otoliths of an estuarine fish. J Exp Mar Biol Ecol 302:85–106CrossRefGoogle Scholar
  22. Laetsch DR, Heitlinger EG, Taraschewski H, Nadler SA, Blaxter ML (2012) The phylogenetics of Anguillicolidae (Nematoda: Anguillicolidea), swim bladder parasites of eels. BMC Evol Biol 12:60PubMedCentralPubMedCrossRefGoogle Scholar
  23. Lévêque C, Oberdoff T, Paugy D, Staiassny MLJ, Tedesco PA (2008) Global diversity of fish (Pisces) in freshwater. Hydrobiologia 595:545–567CrossRefGoogle Scholar
  24. Lin SH, Chang CW, Iizuka Y, Tzeng WN (2007) Salinities, not diets, affect strontium/calcium ratios in otoliths of Anguilla japonica. J Exp Mar Biol Ecol 341:254–263CrossRefGoogle Scholar
  25. Lin YJ, Shiao JC, Lozys L, Plikshs M, Minde A, Iizuka Y, Rashal I, Tzeng WN (2009) Do otolith annular structures correspond to the first freshwater entry for yellow European eels Anguilla anguilla in the Baltic countries? J Fish Biol 75:2709–2722PubMedCrossRefGoogle Scholar
  26. Lin YJ, Yalçìn-Özdilek Ş, Iizuka Y, Gümüş A, Tzeng WN (2011) Migratory life history of European eel Anguilla anguilla from freshwater regions of the River Asi, southern Turkey and their high otolith Sr:Ca ratios. J Fish Biol 78:860–868PubMedCrossRefGoogle Scholar
  27. Lin YJ, Jessop BM, Weyl OLF, Iizuka Y, Lin SH, Tzeng WN, Sun CL (2012) Regional variation in otolith Sr:Ca ratios of African longfinned eel Anguilla mossambica and mottled eel Anguilla marmorata: a challenge to the classic tool for reconstructing migratory histories of fishes. J Fish Biol 81:421–447CrossRefGoogle Scholar
  28. Ling YJ, Iizuka Y, Tzeng WN (2005) Decreased Sr/Ca ratios in the otoliths of two marine eels, Gymnothorax reticularis and Muraenesox cinereus, during metamorphosis. Mar Ecol Prog Ser 304:201–206CrossRefGoogle Scholar
  29. MacKenzie K, Abaunza P (1998) Parasites as biological tags for stock discrimination of marine fish: a guide to procedures and methods. Fish Res 38:45–56CrossRefGoogle Scholar
  30. MacKenzie K, Abaunza, P (2005) Parasites as biological tags. In: Cadrin SX, Friedland KD, Waldman JR (eds). Stock identification methods. Elsevier Inc. p 211–226.Google Scholar
  31. McEwan A, Hecht T (1984) Age and growth of the longfin eel, Anguilla mossambica Peters, 1852 (Pisces: Anguillidae) in Transkei rivers. S Afr J Zool 19:280–285Google Scholar
  32. Moore BR, Welch DJ, Newman SJ, Lester RJG (2012) Parasites as indicators of movement and population connectivity of a non-diadromous, tropical estuarine teleost: king threadfin Polydactylus macrochir. J Fish Biol 81:230–252PubMedCrossRefGoogle Scholar
  33. Moravec F, Taraschewski H, Weyl OLF (2013) Re description of Heliconema africanum (Linstow, 1899) n. comb. (Nematoda: Physalopteridae), a nematode parasite of freshwater eels (Anguilla spp.) in South Africa. Syst Parasitol 85:263–269PubMedCrossRefGoogle Scholar
  34. Munro AR, McMahon TE, Ruzycki JR (2005) Natural chemical markers identify source and date of introduction of an exotic species: lake trout (Salvelinus namaycush) in Yellowstone Lake. Can J Fish Aquat Sci 62:79–87CrossRefGoogle Scholar
  35. Reinthal PN, Stiassny MLJ (1991) The freshwater fishes of Madagascar: a study of an endangered fauna with recommendations for a conservation strategy. Conserv Biol 5:231–242CrossRefGoogle Scholar
  36. Réveillac É, Robinet T, Rabenevanana MW, Valade P, Feunteun É (2009) Clues to the location of the spawning area and larval migration characteristics of Anguilla mossambica as inferred from otolith microstructural analyses. J Fish Biol 74:1866–1877PubMedCrossRefGoogle Scholar
  37. Robinet T, Réveillac E, Kuroki M, Aoyama J, Tsukamoto K, Rabenevanana MW, Valade P, Gagnaire PA, Berrebi P, Feunteun É (2008) New clues for freshwater eels (Anguilla spp.) migration routes to eastern Madagascar and surrounding islands. Mar Biol 154:453–463CrossRefGoogle Scholar
  38. Shen KN, Chang CW, Iizuka Y, Tzeng WN (2009) Facultative habitat selection in Pacific tarpon Megalops cyprinoides as revealed by otolith Sr:Ca ratios. Mar Ecol Prog Ser 387:255–263CrossRefGoogle Scholar
  39. Shiao JC, Ložys L, Iizuka Y, Tzeng WN (2006) Migratory patterns and contribution of stocking to the population of European eel in Lithuanian waters as indicated by otolith Sr : Ca ratios. J Fish Biol 69:749–769CrossRefGoogle Scholar
  40. Sparks JS, Stiassny MLJ (2005) Madagascar’s freshwater fishes: an imperiled treasure. In: Thieme ML, Abell R, Stiassny MLJ, Skelton P, Lehner B, Tugels GG, Dinerstein E, Toham AK, Burgess N, Olson D (eds) Freshwater ecoregions of Africa: a conservation assessment. Island Press, Washington, pp 62–70Google Scholar
  41. Tabouret H, Bareille G, Claverie F, Pécheyran C, Prouzet P, Donard OFX (2010) Simultaneous use of strontium: calcium and barium: calcium ratios in otoliths as markers of habitat: application to the European eel (Anguilla anguilla) in the Adour basin, South West France. Mar Environ Res 70:35–45PubMedCrossRefGoogle Scholar
  42. Taraschewski H, Boomker J, Knopf K, Moravec F (2005) Anguillicola papernai (Nematoda: Anguillicolidae) and other helminths parasitizing the African longfin eel Anguilla mossambica. Dis Aquat Org 63:185–195PubMedCrossRefGoogle Scholar
  43. Tesch FW (2003) The eel. 5th edit. Wiley-Blackwell, Oxford, UK. 436 ppGoogle Scholar
  44. Thibault I, Dodson JJ, Caron F, Tzeng WN, Iizuka Y, Shiao JC (2007) Facultative catadromy in American eels: testing the conditional strategy hypothesis. Mar Ecol Prog Ser 344:219–229CrossRefGoogle Scholar
  45. Thieme ML, Abell R, Stiassny MLJ, Skelton P, Burgess N, Lehner B, Dinerstein E, Olson D (2005) Freshwater ecoregions of Africa and Madagascar: a conservation assessment. World Wildlife Fund, United States, WashingtonGoogle Scholar
  46. Tsukamoto K, Arai T (2001) Facultative catadromy of the eel Anguilla japonica between freshwater and seawater habitats. Mar Ecol Prog Ser 220:265–276CrossRefGoogle Scholar
  47. Tsukamoto K, Nakai I, Tesch WV (1998) Do all freshwater eels migrate? Nature 396:635–636CrossRefGoogle Scholar
  48. Tzeng WN, Severin KP, Wickström H (1997) Use of otolith microchemistry to investigate the environmental history of European eel Anguilla anguilla. Mar Ecol Prog Ser 149:73–81CrossRefGoogle Scholar
  49. Tzeng WN, Shiao JC, Iizuka Y (2002) Use of otolith Sr:Ca ratios to study the riverine migratory behaviours of Japanese eel Anguilla japonica. Mar Ecol Prog Ser 245:213–221CrossRefGoogle Scholar
  50. USGS (2010). 2010 Minerals Yearbook. Madagascar. U.S. Geological Survey, U.S. Department of the Interior. Available at
  51. Voarintsoa NRG, Cox R, Razanatseheno MOM, Rakotondrazafy AFM (2012) Relation between bedrock geology, topography and lavaka distribution in Madagascar. S Afr J Geol 115:225–250CrossRefGoogle Scholar
  52. Walther BD, Limburg KE (2012) The use of otolith chemistry to characterize diadromous migrations. J Fish Biol 81:796–825PubMedCrossRefGoogle Scholar
  53. Williams HH, MacKenzie K, McCarthy M (1992) Parasites as biological, indicators of the population biology, migrations, diet, and phylogenetics of fish. Rev Fish Biol Fish 2:144–176CrossRefGoogle Scholar
  54. Wilson WE (2010) Famous mineral localities: the Sakoany celestine deposit, Mahajanga Province, Madagascar. Mineral Rec 41:405–416Google Scholar
  55. Yokouchi K, Fukuda N, Shirai K, Aoyama J, Daverat F, Tsukamoto K (2011) Time lag of the response on the otolith strontium/calcium ratios of the Japanese eel, Anguilla japonica to changes in strontium/calcium ratios of ambient water. Environ Biol Fish 92:469–478CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Yu-Jia Lin
    • 1
    • 5
    Email author
  • Brian M. Jessop
    • 2
  • Olaf L. F. Weyl
    • 3
  • Yoshiyuki Iizuka
    • 4
  • Shih-Huan Lin
    • 1
  • Wann-Nian Tzeng
    • 1
  1. 1.Institute of Fisheries SciencesNational Taiwan UniversityTaipeiTaiwan
  2. 2.Department of Fisheries and Oceans, Bedford Institute of OceanographyDartmouthCanada
  3. 3.South African Institute for Aquatic Biodiversity (SAIAB)GrahamstownSouth Africa
  4. 4.Institute of Earth Sciences, Academia SinicaTaipeiTaiwan
  5. 5.Marine Studies Section, Center for Environment and Water, Research InstituteKing Fahd University of Petroleum and MineralsDhahranSaudi Arabia

Personalised recommendations