Coral Reefs

, Volume 29, Issue 4, pp 883–891 | Cite as

Otolith geochemistry does not reflect dispersal history of clownfish larvae

  • M. L. Berumen
  • H. J. Walsh
  • N. Raventos
  • S. Planes
  • G. P. Jones
  • V. Starczak
  • S. R. Thorrold
Report

Abstract

Natural geochemical signatures in calcified structures are commonly employed to retrospectively estimate dispersal pathways of larval fish and invertebrates. However, the accuracy of the approach is generally untested due to the absence of individuals with known dispersal histories. We used genetic parentage analysis (genotyping) to divide 110 new recruits of the orange clownfish, Amphiprion percula, from Kimbe Island, Papua New Guinea, into two groups: “self-recruiters” spawned by parents on Kimbe Island and “immigrants” that had dispersed from distant reefs (>10 km away). Analysis of daily increments in sagittal otoliths found no significant difference in PLDs or otolith growth rates between self-recruiting and immigrant larvae. We also quantified otolith Sr/Ca and Ba/Ca ratios during the larval phase using laser ablation inductively coupled plasma mass spectrometry. Again, we found no significant differences in larval profiles of either element between self-recruits and immigrants. Our results highlight the need for caution when interpreting otolith dispersal histories based on natural geochemical tags in the absence of water chemistry data or known-origin larvae with which to test the discriminatory ability of natural tags.

Keywords

Amphiprion percula Connectivity Natural markers Otolith chemistry Papua New Guinea Pelagic larval duration 

References

  1. Almany GR, Berumen ML, Thorrold SR, Planes S, Jones GP (2007) Local replenishment of coral reef fish populations in a marine reserve. Science 316:742–744CrossRefPubMedGoogle Scholar
  2. Bath GE, Thorrold SR, Jones CM, Campana SE, McLaren JW, Lam JWH (2000) Strontium and barium uptake in aragonitic otoliths of marine fish. Geochim Cosmochim Acta 64:1705–1714CrossRefGoogle Scholar
  3. Becker BJ, Fodrie FJ, McMillan PA, Levin LA (2005) Spatial and temporal variation in trace elemental fingerprints of mytilid mussel shells: a precursor to invertebrate larval tracking. Limnol Oceanogr 50:48–61CrossRefGoogle Scholar
  4. Ben-Tzvi O, Kiflawi M, Gaines SD, Al-Zibdah M, Sheehy MS, Paradis GL, Abelson A (2008) Tracking recruitment pathways of Chromis viridis in the Gulf of Aqaba using otolith chemistry. Mar Ecol Prog Ser 359:229–238CrossRefGoogle Scholar
  5. Campana SE (2005) Otolith science entering the 21st century. Mar Freshw Res 56:485–495CrossRefGoogle Scholar
  6. Campana SE, Thorrold SR (2001) Otoliths, increments, and elements: keys to a comprehensive understanding of fish populations? Can J Fish Aquat Sci 58:30–38CrossRefGoogle Scholar
  7. Campana SE, Fowler AJ, Jones CM (1994) Otolith elemental fingerprinting for stock identification of Atlantic cod (Gadus morhua) using laser ablation ICPMS. Can J Fish Aquat Sci 51:1942–1950CrossRefGoogle Scholar
  8. Cowen RK, Gawarkiewicz G, Pineda J, Thorrold SR, Werner FE (2007) Population connectivity in marine systems: an overview. Oceanography 20:14–21Google Scholar
  9. Dixson DL, Jones GP, Munday PL, Planes S, Pratchett MS, Srinivasan M, Syms C, Thorrold SR (2008) Coral reef fish smell leaves to find island homes. Proc R Soc B 275:2831–2839CrossRefPubMedGoogle Scholar
  10. Elsdon TS, Gillanders BM (2005) Consistency of patterns between laboratory experiments and field collected fish in otolith chemistry: an example and applications for salinity reconstructions. Mar Freshw Res 56:609–617CrossRefGoogle Scholar
  11. Elsdon TS, Wells BK, Campana SE, Gillanders BM, Jones CM, Limburg KE, Secor DE, Thorrold SR, Walther BD (2008) Otolith chemistry to describe movements and life-history measurements of fishes: hypotheses, assumptions, limitations, and inferences using five methods. Oceanogr Mar Biol Annu Rev 46:297–330CrossRefGoogle Scholar
  12. Farrell J, Campana SE (1996) Regulation of calcium and strontium deposition on the otoliths of juvenile tilapia, Oreochromis niloticus. Comp Biochem Physiol A 115:103–109CrossRefGoogle Scholar
  13. FitzGerald JL, Thorrold SR, Bailey KM, Brown AL, Severin KP (2004) Elemental signatures in otoliths of larval walleye pollock (Theragra chalcogramma) from the northeast Pacific Ocean. Fish Bull 102:604–616Google Scholar
  14. Fogarty MJ, Botsford LW (2007) Population connectivity and spatial management of marine fisheries Oceanography 20:112–123Google Scholar
  15. Fowler AJ (1995) Annulus formation in the otoliths of coral reef fish: a review. In: Secor DH, Dean JM, Campana SE (eds) Recent developments in fish otolith research. University of South Carolina Press, Columbia, pp 45–63Google Scholar
  16. Fricke HW (1979) Mating system, resource defence and sex change in the anemonefish Amphiprion akallopisos. Z Tierpsychol 50:313–326CrossRefGoogle Scholar
  17. Gaines SD, Gaylord B, Gerber LR, Hastings A, Kinlan BP (2007) Connecting places: the ecological consequences of dispersal in the sea. Oceanography 20:90–99Google Scholar
  18. Gerber S, Chabrier P, Kremer A (2003) FAMOZ: a software for parentage analysis using dominant, codominant and uniparentally inherited markers. Mol Ecol Notes 3:479–481CrossRefGoogle Scholar
  19. Gillanders BM, Kingsford MJ (2000) Elemental fingerprints of otoliths of fish may distinguish estuarine ‘nursery’ habitats. Mar Ecol Prog Ser 201:273–286CrossRefGoogle Scholar
  20. Hamilton SL, Regetz J, Warner RR (2008) Postsettlement survival linked to larval life in a marine fish. Proc Nat Acad Sci USA 105:1561–1566CrossRefPubMedGoogle Scholar
  21. Hofmann GE, Gaines SD (2008) New tools to meet new challenges: emerging technologies for managing marine ecosystems for resilience. Bioscience 58:43–52CrossRefGoogle Scholar
  22. Johnson RA, Wichern DW (2007) Applied multivariate statistical analysis, 6th edn. Prentice Hall, Englewood CliffsGoogle Scholar
  23. Jones GP, Milicich MJ, Emslie MJ, Lunow C (1999) Self-recruitment in a coral reef fish population. Nature 402:802–804CrossRefGoogle Scholar
  24. Jones GP, Planes S, Thorrold SR (2005) Coral reef fish larvae settle close to home. Curr Biol 15:1314–1318CrossRefPubMedGoogle Scholar
  25. Jones GP, Srinivasan M, Almany GR (2007) Population connectivity and conservation of marine biodiversity. Oceanography 20:42–53Google Scholar
  26. Leis JM, McCormick MI (2002) The biology, behavior, and ecology of the pelagic, larval stage of coral reef fishes. In: Sale PF (ed) Coral reef fishes. Academic Press, San Diego, pp 171–199CrossRefGoogle Scholar
  27. Levin LA (2006) Recent progress in understanding larval dispersal: new directions and digressions. Integr Comp Biol 46:282–297CrossRefGoogle Scholar
  28. Martin GB, Thorrold SR, Jones CM (2004) Temperature and salinity effects on strontium incorporation in otoliths of larval spot (Leiostomus xanthurus). Can J Fish Aquat Sci 61:34–42CrossRefGoogle Scholar
  29. McCook LJ, Almany GR, Berumen ML, Day JC, Green AL, Jones GP, Leis JM, Planes S, Russ GR, Sale PF, Thorrold SR (2009) Management under uncertainty: guide-lines for incorporating connectivity into the protection of coral reefs. Coral Reefs 28:353–366CrossRefGoogle Scholar
  30. McCulloch M, Cappo M, Aumend J, Müller W (2005) Tracing the life history of individual barramundi using laser ablation MC-ICP-MS Sr-isotopic and Sr/Ba ratios in otoliths. Mar Freshw Res 56:637–644CrossRefGoogle Scholar
  31. Montgomery JC, Jeffs A, Simpson SD, Meekan MG, Tindle C (2006) Sound as an orientation clue for the pelagic larvae of reef fish and crustaceans. Adv Mar Biol 51:143–196CrossRefPubMedGoogle Scholar
  32. Mugiya Y, Hakomori T, Hatsutori K (1991) Trace metal incorporation into otoliths and scales in the goldfish, Carassius auratus. Comp Biochem Phys C 99C:327–331CrossRefGoogle Scholar
  33. Patterson HM, Kingsford MJ, McCulloch MT (2004) Elemental signatures of Pomacentrus coelestis otoliths at multiple spatial scales on the Great Barrier Reef, Australia. Mar Ecol Prog Ser 270:229–239CrossRefGoogle Scholar
  34. Patterson HM, Kingsford MJ, McCulloch MT (2005) Resolution of the early life history of a reef fish using otolith chemistry. Coral Reefs 24:222–229CrossRefGoogle Scholar
  35. Planes S, Jones GP, Thorrold SR (2009) Larval dispersal connects fish populations in a network of marine protected areas. Proc Nat Acad Sci USA 106:5693–5697CrossRefPubMedGoogle Scholar
  36. Ralston S (1976) Age determination of a tropical reef butterflyfish utilizing daily growth rings of otiliths. US Fish Bull 74:990–994Google Scholar
  37. Raventos N, Macpherson E (2001) Planktonic larval duration and settlement marks on the otoliths of Mediterranean littoral fishes. Mar Biol 138:1115–1120CrossRefGoogle Scholar
  38. Ruttenberg BI, Haupt AJ, Chiriboga AI, Warner RR (2005) Patterns, causes and consequences of regional variation in the ecology and life history of a reef fish. Oecologia 145:394–403CrossRefPubMedGoogle Scholar
  39. Ruttenberg BI, Hamilton SL, Warner RR (2008) Spatial and temporal variation in the natal otolith chemistry of a Hawaiian reef fish: prospects for measuring population connectivity. Can J Fish Aquat Sci 65:1181–1192CrossRefGoogle Scholar
  40. Sandin SA, Regetz J, Hamilton SL (2005) Testing larval fish dispersal hypotheses using maximum likelihood analysis of otolith chemistry data. Mar Freshw Res 56:725–734CrossRefGoogle Scholar
  41. Sponaugle S, Cowen RK, Shanks A, Morgan SG, Leis JM, Pineda J, Boehlert GW, Kingsford MJ, Lindeman K, Grimes C, Munro JL (2002) Predicting self-recruitment in marine populations: Biophysical correlates and mechanisms. Bull Mar Sci 70S:341–375Google Scholar
  42. Standish JD, Sheehy M, Warner RR (2008) Use of otolith natal elemental signatures as natural tags to evaluate connectivity among open-coast fish populations. Mar Ecol Prog Ser 356:259–268CrossRefGoogle Scholar
  43. Sturgeon RE, Willie SN, Yang L, Greenberg R, Spatz RO, Chen Z, Scriver C, Clancy V, Lam JW, Thorrold SR (2005) Certification of a fish otolith reference material in support of quality assurance for trace element analysis. J Anal At Spectrom 20:1067–1071CrossRefGoogle Scholar
  44. Swearer SE, Caselle JE, Lea DW, Warner RR (1999) Larval retention and recruitment in an island population of a coral-reef fish. Nature 402:799–802CrossRefGoogle Scholar
  45. Thorrold SR, Latkoczy C, Swart PK, Jones CM (2001) Natal homing in a marine fish metapopulation. Science 291:297–299CrossRefPubMedGoogle Scholar
  46. Thorrold SR, Jones GP, Hellberg ME, Burton RS, Swearer SE, Neigel JE, Morgan SG, Warner RR (2002) Quantifying larval retention and connectivity in marine populations with artificial and natural markers. Bull Mar Sci 70:S291–S308Google Scholar
  47. Thorrold SR, Jones GP, Planes S, Hare JA (2006) Transgenerational marking of embryonic otoliths in marine fishes using barium stable isotopes. Can J Fish Aquat Sci 63:1193CrossRefGoogle Scholar
  48. Thorrold SR, Zacherl DC, Levin LA (2007) Population connectivity and larval dispersal using geochemical signatures in calcified structures. Oceanography 20:80–89Google Scholar
  49. Walther BD, Thorrold SR (2006) Water, not food, contributes the majority of strontium and barium deposited in the otoliths of a marine fish. Mar Ecol Prog Ser 311:125–130CrossRefGoogle Scholar
  50. Warner RR, Swearer SE, Caselle JE, Sheehy M, Paradis G (2005) Natal trace-elemental signatures in the otoliths of an open-coast fish. Limnol Oceanogr 50:1529–1542CrossRefGoogle Scholar
  51. Wellington GM, Victor BC (1992) Regional differences in duration of the planktonic larval stage of reef fishes in the eastern Pacific Ocean. Mar Biol 113:491–498CrossRefGoogle Scholar
  52. Zacherl DC, Manríquez PH, Paradis G, Day RW, Castilla JC, Warner RR, Lea DW, Gaines SD (2003) Trace elemental fingerprinting of gastropod statoliths to study larval dispersal trajectories. Mar Ecol Prog Ser 248:297–303CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • M. L. Berumen
    • 1
    • 2
    • 3
  • H. J. Walsh
    • 2
  • N. Raventos
    • 4
  • S. Planes
    • 5
  • G. P. Jones
    • 3
    • 6
  • V. Starczak
    • 2
  • S. R. Thorrold
    • 2
  1. 1.Red Sea Research CenterKing Abdullah University of Science and TechnologyThuwalKingdom of Saudi Arabia
  2. 2.Biology DepartmentWoods Hole Oceanographic InstitutionWoods HoleUSA
  3. 3.ARC Centre of Excellence for Coral Reef StudiesJames Cook UniversityTownsvilleAustralia
  4. 4.Centro de Estudios Avanzados de Blanes, Consejo Superior de Investigaciones CientificasCamino Acceso a la Cala San FrancescGironaSpain
  5. 5.USR 3278 CNRS EPHECenter de Recherches Insulaires et Observatoire de l’Environnement (CRIOBE)MooreaFrench Polynesia
  6. 6.School of Marine and Tropical BiologyJames Cook UniversityTownsvilleAustralia

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