Coral Reefs

, 30:1135 | Cite as

Carbon isotopes in otolith amino acids identify residency of juvenile snapper (Family: Lutjanidae) in coastal nurseries

  • K. W. McMahon
  • M. L. Berumen
  • I. Mateo
  • T. S. Elsdon
  • S. R. Thorrold


This study explored the potential for otolith geochemistry in snapper (Family: Lutjanidae) to identify residency in juvenile nursery habitats with distinctive carbon isotope values. Conventional bulk otolith and muscle stable isotope analyses (SIA) and essential amino acid (AA) SIA were conducted on snapper collected from seagrass beds, mangroves, and coral reefs in the Red Sea, Caribbean Sea, and Pacific coast of Panama. While bulk stable isotope values in otoliths showed regional differences, they failed to distinguish nursery residence on local scales. Essential AA δ13C values in otoliths, on the other hand, varied as a function of habitat type and provided a better tracer of residence in different juvenile nursery habitats than conventional bulk otolith SIA alone. A strong linear relationship was found between paired otolith and muscle essential AA δ13C values regardless of species, geographic region, or habitat type, indicating that otolith AAs recorded the same dietary information as muscle AAs. Juvenile snapper in the Red Sea sheltered in mangroves but fed in seagrass beds, while snapper from the Caribbean Sea and Pacific coast of Panama showed greater reliance on mangrove-derived carbon. Furthermore, compound-specific SIA revealed that microbially recycled detrital carbon, not water-column-based new phytoplankton carbon, was the primary carbon source supporting snapper production on coastal reefs of the Red Sea. This study presented robust tracers of juvenile nursery residence that will be crucial for reconstructing ontogenetic migration patterns of fishes among coastal wetlands and coral reefs. This information is key to determining the importance of nursery habitats to coral reef fish populations and will provide valuable scientific support for the design of networked marine-protected areas.


Mangroves Seagrass Migration Diet Coral reefs 



The authors would like to thank H. Walsh, L. Houghton, M. Noble, N. DesRosiers, and G. Nanninga for field assistance, C. Braun for creating Fig. 1 and Dream Divers, Jeddah, Saudi Arabia for logistic assistance with boating and diving operations. Work in the Red Sea was supported by King Abdullah University of Science and Technology (KAUST) Award Nos. USA 00002 and KSA 00011 to S. Thorrold. Collections of snapper in the Caribbean Sea were funded by a Puerto Rico Sea Grant Program (Grant No. AN05-05-030) to I. Mateo, PADI Aware Foundation, Sigma Xi, and the Caribbean Coral Reef Institute. Additional funding was provided by the Woods Hole Oceanographic Institution and an International Society for Reef Studies-Ocean Conservancy Coral Reef Fellowship to K. McMahon. K. McMahon received support from the National Science Foundation Graduate Research Fellowship Program.


  1. Abed-Navandi D, Dworschak PC (2005) Food sources of tropical thalassidean shrimps: a stable-isotope study. Mar Ecol Ser Prog 291:159–168CrossRefGoogle Scholar
  2. Adams AJ, Dahlgren CP, Kellison GT, Kendall MS, Layman CA, Ley JA, Nagelkerken I, Serafy JE (2006) Nursery function of tropical back-reef systems. Mar Ecol Prog Ser 318:287–301CrossRefGoogle Scholar
  3. Beck MW, Heck KL, Able KW, Childers DL, Eggleston DB, Gillanders BM, Halpern B, Hays CG, Hoshino K, Minello TJ, Orth RJ, Sheridan PF, Weinstein MR (2001) The identification, conservation, and management of estuarine and marine nurseries for fish and invertebrates. Bioscience 51:633–641CrossRefGoogle Scholar
  4. Bouillon S, Raman AV, Dauby P, Dehairs F (2002) Carbon and nitrogen stable isotope ratios of subtidal benthic invertebrates in an estuarine mangrove ecosystem (Andhra Pradesh, India). Estuar Coast Shelf Sci 54:901–903CrossRefGoogle Scholar
  5. Campana SE (1999) Chemistry and composition of fish otoliths: pathways, mechanisms and applications. Mar Ecol Prog Ser 188:263–297CrossRefGoogle Scholar
  6. Chittaro PM, Fryer BJ, Sale PF (2004) Discrimination of French grunts (Haemulon flavolineatum, Desmarest, 1823) from mangrove and coral reef habitats using otolith microchemistry. J Exp Mar Biol Ecol 308:169–183CrossRefGoogle Scholar
  7. Cocheret de la Moriniere E, Nagelkerken I, van der Meij H, van der Velde G (2004) What attracts juvenile coral reef fish to mangroves: habitat complexity or shade? Mar Biol 144:139–145CrossRefGoogle Scholar
  8. Dansgaard W (1964) Stable isotopes in precipitation. Tellus 16:436–468CrossRefGoogle Scholar
  9. Degens ET, Deuser WG, Haedrich RL (1969) Molecular structure and composition of fish otoliths. Mar Biol 2:105–113CrossRefGoogle Scholar
  10. Dorenbosch M, Verweij MC, Nagelkerken I, Jiddawi N, van der Velde G (2004) Homing and daytime tidal movements of juvenile snappers (Lutjanidae) between shallow-water nursery habitats in Zanzibar, Western Indian Ocean. Environ Biol Fish 70:203–209CrossRefGoogle Scholar
  11. Dufour V, Pierre C, Rancher J (1998) Stable isotopes in fish otoliths discriminate between lagoonal and oceanic residents of Taiaro Atoll (Tuamotu Archipelago, French Polynesia). Coral Reefs 17:23–28CrossRefGoogle Scholar
  12. Elsdon TS, Wells KB, 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 Annu Rev 46:297–330CrossRefGoogle Scholar
  13. Faunce CH, Serafy JE (2006) Mangroves as fish habitats: 50 years of field studies. Mar Ecol Prog Ser 318:1–18CrossRefGoogle Scholar
  14. Fogel ML, Tuross N (1999) Transformation of plant biochemicals to geological macromolecules during early diagenesis. Oecologia 120:336–346CrossRefGoogle Scholar
  15. Fry B (1981) Natural stable isotope tag traces in Texas shrimp migrations. Fish Bull 79:337–345Google Scholar
  16. Gottschalk G (1988) Bacterial metabolism. Springer, New YorkGoogle Scholar
  17. Grober-Dunsmore R, Frazer TK, Lindberg WJ, Beets J (2007) Reef fish habitat relationships in a Caribbean seascape: the importance of reef context. Coral Reefs 26:201–216CrossRefGoogle Scholar
  18. Hare PE, Fogel ML, Stafford TW, Mitchell AD, Hoering TC (1991) The isotopic composition of carbon and nitrogen in individual amino-acids isolated from modern and fossil proteins. J Archaeol Sci 18:277–292CrossRefGoogle Scholar
  19. Hemminga MA, Slim FJ, Kazungu J, Ganssen GM, Nieuwenhuize J, Kruyt NM (1994) Carbon outwelling from a mangrove forest with adjacent seagrass beds and coral reefs (Gazi Bay, Kenya). Mar Ecol Prog Ser 106:291–301CrossRefGoogle Scholar
  20. Herzka SZ (2005) Assessing connectivity of estuarine fishes based on stable isotope ratio analysis. Estuar Coast Shelf Sci 64:58–69CrossRefGoogle Scholar
  21. Howland MR, Corr LT, Young SMM, Jones V, Jim S, Van der Merwe NJ, Mitchell AD, Evershed RP (2003) Expression of the dietary isotope signal in the compound-specific delta(13) values of pig bone lipids and amino acids. Int J Osteoarchaeol 13:54–65CrossRefGoogle Scholar
  22. Huxham M, Kimani E, Newton J, Augley J (2007) Stable isotope records from otoliths as tracers of fish migration in a mangrove system. J Fish Biol 70:1554–1567CrossRefGoogle Scholar
  23. Jackson EL, Rowden AA, Attrill MJ, Bossey SJ, Jones MB (2001) The importance of seagrass beds as a nursery for fisheries species. Oceanogr Mar Biol Annu Rev 39:269–303Google Scholar
  24. Jim S, Jones V, Ambrose SH, Evershed RP (2006) Quantifying dietary macronutrient sources of carbon for bone collagen biosynthesis using natural abundance stable carbon isotope analysis. British J Nutr 95:1055–1062CrossRefGoogle Scholar
  25. Johnson BJ, Fogel ML, Miller GH (1998) Stable isotopes in modern ostrich eggshell: a calibration for paleoenvironmental applications in semi-arid regions of southern Africa. Geochim Cosmochim Acta 62:2451–2461CrossRefGoogle Scholar
  26. Jolivet A, Bardeau J-F, Fablet R, Paulet Y-M, De Pontual H (2008) Understanding otolith biomineralization processes: new insights into microscale spatial distributions of organic and mineral fractions from Raman microspectrometry. Anal Bioanal Chem 392:551–50Google Scholar
  27. Kieckbusch DK, Hock MS, Serafy JE, Anderson WT (2004) Trophic linkages among primary producers and consumers in fringing mangroves of subtropical lagoons. Bull Mar Sci 74:271–285Google Scholar
  28. Keil RG, Fogel ML (2001) Reworking of amino acids in marine sediments: stable carbon isotopic composition of amino acids in sediments along the Washington coast. Limnol Oceanogr 46:14–23CrossRefGoogle Scholar
  29. Laegdsgaard P, Johnson C (2001) Why do juvenile fish utilise mangrove habitats? J Exp Mar Biol Ecol 257:229–253PubMedCrossRefGoogle Scholar
  30. Layman CA (2007) What can stable isotope ratios reveal about mangroves as fish habitat? Bull Mar Sci 80:513–527Google Scholar
  31. Lugendo BR, Nagelkerken I, Kruitwagen G, van der Velde G, Mgaya YD (2007) Relative importance of mangroves as feeding habitats for fishes: a comparison between mangrove habitats with different settings. Bull Mar Sci 80:497–512Google Scholar
  32. Luo J, Serafy J, Sponaugle S, Teare PB, Kieckbusch D (2009) Movement of gray snapper Lutjaus griseus among subtropical seagrass, mangrove and coral reef habitats. Mar Ecol Prog Ser 380:255–269CrossRefGoogle Scholar
  33. Manson FJ, Loneragan NR, Skilleter GA, Phinn SR (2005) An evaluation of the evidence for linkages between mangroves and fisheries: a synthesis of the literature and identification of research directions. Oceanogr Mar Biol Annu Rev 43:483–513Google Scholar
  34. Marguillier S, van der Velde G, Dehairs F, Hemminga MA, Rajagopal S (1997) Trophic relationships in an interlinked mangrove-seagrass ecosystem as traced by δ13C and δ15N. Mar Ecol Prog Ser 151:115–121CrossRefGoogle Scholar
  35. Mateo I, Durbin EG, Appeldoorn RS, Adams AJ, Juanes F, Kingsley R, Swart P, Durant D (2010) Role of mangroves as nurseries for French grunt Haemulon flavolinatum and schoolmaster Lutjanus apodus assessed by otolith elemental fingerprints. Mar Ecol Prog Ser 402:197–212CrossRefGoogle Scholar
  36. McCarthy MD, Benner R, Lee C, Hedges JI, Fogel ML (2004) Amino acid carbon isotopic fractionation patterns in oceanic dissolved organic matter: an unaltered photoautotrophic source for dissolved organic nitrogen in the ocean? Mar Chem 92:123–134CrossRefGoogle Scholar
  37. 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
  38. McMahon KW, Fogel ML, Elsdon T, Thorrold SR (2010) Carbon isotope fractionation of amino acids in fish muscle reflects biosynthesis and isotopic routing from dietary protein. J Anim Ecol 79:1132–1141PubMedCrossRefGoogle Scholar
  39. McMahon KW, Fogel ML, Johnson BJ, Houghton LA, Thorrold SR (2011) A new method to reconstruct fish diet and movement patterns from δ13C values in otolith amino acids. Can J Fish Aquat Sci 68:1330–1340Google Scholar
  40. Morales-Nin B (1986) Structure and composition of otoliths of Cape hake Merluccius capensis. S Afr J Mar Sci 4:3–10CrossRefGoogle Scholar
  41. Nagelkerken I (2007) Are non-estuarine mangroves connected to coral reefs through fish migration? Bull Mar Sci 80:595–607Google Scholar
  42. Nagelkerken I, Dorenbosch M, Verberk WCEP, Cocheret de la Moriniere E, van der Velde G (2000) Day-night shifts of fishes between shallow-water biotopes of a Caribbean bay, with emphasis on the nocturnal feeding of Haemulidae and Lutjanidae. Mar Ecol Prog Ser 194:55–64CrossRefGoogle Scholar
  43. Nagelkerken I, Bothwell J, Nemeth RS, Pitt JM, van der Velde G (2008a) Interlinkage between Caribbean coral reefs and seagrass beds through feeding migrations by grunts (Haemilidae) depends on habitat accessibility. Mar Ecol Prog Ser 368:155–164CrossRefGoogle Scholar
  44. Nagelkerken I, Blaber SJM, Bouillon S, Green P, Haywood M, Kirton LG, Meyneck J-O, Pawlik J, Penrose HM, Sadekumar A, Somerfield PJ (2008b) The habitat function of mangroves for terrestrial and marine fauna: a review. Aquat Bot 89:155–185CrossRefGoogle Scholar
  45. Nakamura Y, Horinouchi M, Shibuno T, Tanaka Y, Miyajima T, Koike I, Kurokura H, Sano M (2008) Evidence of ontogenetic migration from mangroves to coral reefs by black-tail snapper Lutjanus fulvus: stable isotope approach. Mar Ecol Prog Ser 355:257–266CrossRefGoogle Scholar
  46. Ostermann DR, Curry WB (2000) Calibration of stable isotopic data: an enriched delta O-18 standard used for source gas mixing detection and correction. Paleoceanogr 15:353–360CrossRefGoogle Scholar
  47. Rawn DJ (1989) Biochemistry. Harper and Row, New YorkGoogle Scholar
  48. Rodelli MR, Gearing JN, Gearing PJ, Marshall N, Sasekumar A (1984) Stable isotope ratio as a tracer of mangrove carbon in Malaysian ecosystems. Oecologia 61:326–333CrossRefGoogle Scholar
  49. Rooker JR, Dennis GD (1991) Diel, lunar and seasonal changes in a mangrove fish assemblage off southwestern Puerto Rico. Bull Mar Sci 49:684–698Google Scholar
  50. Sheaves M, Molony B (2000) Short-circuit in the mangrove food chain. Mar Ecol Prog Ser 199:97–109CrossRefGoogle Scholar
  51. Sheridan P, Hays C (2003) Are mangroves nursery habitat for transient fishes and decapods? Wetlands 23:449–458CrossRefGoogle Scholar
  52. Siegenthaler U, Oeschger H (1980) Correlation of 18O in precipitation with temperature and altitude. Nature 285:314–317CrossRefGoogle Scholar
  53. Silfer JA, Engel MH, Macko SA, Jumeau EJ (1991) Stable carbon isotope analysis of amino-acid enantiomers by conventional isotope ratio mass spectrometry and combined gas-chromatography isotope ratio mass-spectrometry. Anal Chem 63:370–374CrossRefGoogle Scholar
  54. Smallwood BJ, Woller MJ, Myrna EJ, Fogel ML (2003) Isotopic and molecular distributions of biochemicals from fresh and buried Rhizophora mangle leaves. Geochem Trans 4:38–46CrossRefGoogle Scholar
  55. Stewart MK, Taylor CB (1981) Environmental isotopes in New Zealand hydrology 1. Introduction: the role of 18O, deuterium, and tritium in hydrology. N Z J Sci 24:295–311Google Scholar
  56. 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 70:291–308Google Scholar
  57. Unsworth RKF, Garrard SL, Salinas de Leon P, Cullen LC, Smith DJ, Sloman KA, Bell JJ (2009) Structuring of Indo-Pacific fish assemblages along the mangrove-seagrass continuum. Aquat Biol 5:85–95CrossRefGoogle Scholar
  58. Verweij MC, Nagelkerken I, de Graaff D, Peeters M, Bakker EJ, van der Velde G (2006) Structure, food and shade attract juvenile coral reef fish to mangrove and seagrass habitats: a field experiment. Mar Ecol Prog Ser 306:257–268CrossRefGoogle Scholar
  59. Verweij MC, Nagelkerken I, Hans I, Ruseler SM, Mason PDR (2008) Seagrass nurseries contribute to coral reef fish populations. Limnol Oceanogr 53:1540–1547CrossRefGoogle Scholar
  60. West J, Bowen GJ, Dawson TE, Tu KP (2010) Isoscapes: understanding movement, pattern and process on earth through isotope mapping. Springer, New YorkGoogle Scholar
  61. Ziegler S, Fogel ML (2003) Seasonal and diel relationships between the isotopic compositions of dissolved and particulate organic matter in freshwater ecosystems. Biogeochemistry 64:25–52CrossRefGoogle Scholar
  62. Zieman JC, Macko SA, Mills AL (1984) Role of seagrasses and mangroves in estuarine food webs: temporal and spatial changes in stable isotope composition and amino acid content during decomposition. Bull Mar Sci 35:380–392Google Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • K. W. McMahon
    • 1
    • 2
  • M. L. Berumen
    • 1
    • 2
  • I. Mateo
    • 3
  • T. S. Elsdon
    • 4
  • S. R. Thorrold
    • 1
  1. 1.Biology DepartmentWoods Hole Oceanographic InstitutionWoods HoleUSA
  2. 2.Red Sea Research CenterKing Abdullah University of Science and TechnologyThuwalKingdom of Saudi Arabia
  3. 3.Department of Fisheries, Animal and Veterinary SciencesUniversity of Rhode IslandKingstonUSA
  4. 4.Southern Seas Ecology Laboratories, School of Earth and Environmental SciencesUniversity of AdelaideAdelaideAustralia

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