Skip to main content

Advertisement

SpringerLink
Log in

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

  • Report
  • Published:
Coral Reefs Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  • Abed-Navandi D, Dworschak PC (2005) Food sources of tropical thalassidean shrimps: a stable-isotope study. Mar Ecol Ser Prog 291:159–168

    Article  CAS  Google Scholar 

  • 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 318:287–301

    Article  Google Scholar 

  • 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 51:633–641

    Article  Google Scholar 

  • 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 54:901–903

    Article  CAS  Google Scholar 

  • Campana SE (1999) Chemistry and composition of fish otoliths: pathways, mechanisms and applications. Mar Ecol Prog Ser 188:263–297

    Article  CAS  Google Scholar 

  • 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 308:169–183

    Article  Google Scholar 

  • 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 144:139–145

    Article  Google Scholar 

  • Dansgaard W (1964) Stable isotopes in precipitation. Tellus 16:436–468

    Article  Google Scholar 

  • Degens ET, Deuser WG, Haedrich RL (1969) Molecular structure and composition of fish otoliths. Mar Biol 2:105–113

    Article  CAS  Google Scholar 

  • 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 70:203–209

    Article  Google Scholar 

  • 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 17:23–28

    Article  Google Scholar 

  • 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 46:297–330

    Article  Google Scholar 

  • Faunce CH, Serafy JE (2006) Mangroves as fish habitats: 50 years of field studies. Mar Ecol Prog Ser 318:1–18

    Article  Google Scholar 

  • Fogel ML, Tuross N (1999) Transformation of plant biochemicals to geological macromolecules during early diagenesis. Oecologia 120:336–346

    Article  Google Scholar 

  • Fry B (1981) Natural stable isotope tag traces in Texas shrimp migrations. Fish Bull 79:337–345

    Google Scholar 

  • Gottschalk G (1988) Bacterial metabolism. Springer, New York

    Google Scholar 

  • 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 26:201–216

    Article  Google Scholar 

  • 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 18:277–292

    Article  Google Scholar 

  • 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 106:291–301

    Article  Google Scholar 

  • Herzka SZ (2005) Assessing connectivity of estuarine fishes based on stable isotope ratio analysis. Estuar Coast Shelf Sci 64:58–69

    Article  Google Scholar 

  • 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 13:54–65

    Article  Google Scholar 

  • 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 70:1554–1567

    Article  Google Scholar 

  • 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 39:269–303

    Google Scholar 

  • 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 95:1055–1062

    Article  CAS  Google Scholar 

  • 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 62:2451–2461

    Article  CAS  Google Scholar 

  • 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 392:551–50

    Google Scholar 

  • 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 74:271–285

    Google Scholar 

  • 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 46:14–23

    Article  CAS  Google Scholar 

  • Laegdsgaard P, Johnson C (2001) Why do juvenile fish utilise mangrove habitats? J Exp Mar Biol Ecol 257:229–253

    Article  PubMed  Google Scholar 

  • Layman CA (2007) What can stable isotope ratios reveal about mangroves as fish habitat? Bull Mar Sci 80:513–527

    Google Scholar 

  • 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 80:497–512

    Google Scholar 

  • 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 380:255–269

    Article  Google Scholar 

  • 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 43:483–513

    Google Scholar 

  • 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 151:115–121

    Article  CAS  Google Scholar 

  • 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 402:197–212

    Article  CAS  Google Scholar 

  • 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 92:123–134

    Article  CAS  Google Scholar 

  • 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 28:353–366

    Article  Google Scholar 

  • 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 79:1132–1141

    Article  PubMed  Google Scholar 

  • 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 68:1330–1340

    Google Scholar 

  • Morales-Nin B (1986) Structure and composition of otoliths of Cape hake Merluccius capensis. S Afr J Mar Sci 4:3–10

    Article  Google Scholar 

  • Nagelkerken I (2007) Are non-estuarine mangroves connected to coral reefs through fish migration? Bull Mar Sci 80:595–607

    Google Scholar 

  • 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 194:55–64

    Article  Google Scholar 

  • 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 368:155–164

    Article  Google Scholar 

  • 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 89:155–185

    Article  Google Scholar 

  • 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 355:257–266

    Article  Google Scholar 

  • 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 15:353–360

    Article  Google Scholar 

  • Rawn DJ (1989) Biochemistry. Harper and Row, New York

    Google Scholar 

  • Rodelli MR, Gearing JN, Gearing PJ, Marshall N, Sasekumar A (1984) Stable isotope ratio as a tracer of mangrove carbon in Malaysian ecosystems. Oecologia 61:326–333

    Article  Google Scholar 

  • Rooker JR, Dennis GD (1991) Diel, lunar and seasonal changes in a mangrove fish assemblage off southwestern Puerto Rico. Bull Mar Sci 49:684–698

    Google Scholar 

  • Sheaves M, Molony B (2000) Short-circuit in the mangrove food chain. Mar Ecol Prog Ser 199:97–109

    Article  Google Scholar 

  • Sheridan P, Hays C (2003) Are mangroves nursery habitat for transient fishes and decapods? Wetlands 23:449–458

    Article  Google Scholar 

  • Siegenthaler U, Oeschger H (1980) Correlation of 18O in precipitation with temperature and altitude. Nature 285:314–317

    Article  CAS  Google Scholar 

  • 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 63:370–374

    Article  CAS  Google Scholar 

  • Smallwood BJ, Woller MJ, Myrna EJ, Fogel ML (2003) Isotopic and molecular distributions of biochemicals from fresh and buried Rhizophora mangle leaves. Geochem Trans 4:38–46

    Article  Google Scholar 

  • 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 24:295–311

    Google Scholar 

  • 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 70:291–308

    Google Scholar 

  • 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 5:85–95

    Article  Google Scholar 

  • 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 306:257–268

    Article  Google Scholar 

  • Verweij MC, Nagelkerken I, Hans I, Ruseler SM, Mason PDR (2008) Seagrass nurseries contribute to coral reef fish populations. Limnol Oceanogr 53:1540–1547

    Article  Google Scholar 

  • West J, Bowen GJ, Dawson TE, Tu KP (2010) Isoscapes: understanding movement, pattern and process on earth through isotope mapping. Springer, New York

    Google Scholar 

  • Ziegler S, Fogel ML (2003) Seasonal and diel relationships between the isotopic compositions of dissolved and particulate organic matter in freshwater ecosystems. Biogeochemistry 64:25–52

    Article  CAS  Google Scholar 

  • 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 35:380–392

    Google Scholar 

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

  1. Biology Department, Woods Hole Oceanographic Institution, Woods Hole, MA, 02543, USA

    K. W. McMahon, M. L. Berumen & S. R. Thorrold

  2. Red Sea Research Center, King Abdullah University of Science and Technology, Thuwal, Kingdom of Saudi Arabia

    K. W. McMahon & M. L. Berumen

  3. Department of Fisheries, Animal and Veterinary Sciences, University of Rhode Island, Kingston, RI, 02881, USA

    I. Mateo

  4. Southern Seas Ecology Laboratories, School of Earth and Environmental Sciences, University of Adelaide, Adelaide, SA, 5005, Australia

    T. S. Elsdon

Authors
  1. K. W. McMahon
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. L. Berumen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. I. Mateo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. T. S. Elsdon
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. S. R. Thorrold
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to K. W. McMahon.

Additional information

Communicated by Biology Editor Dr. Stephen Swearer

Rights and permissions

Reprints and permissions

About this article

Cite this article

McMahon, K.W., Berumen, M.L., Mateo, I. et al. Carbon isotopes in otolith amino acids identify residency of juvenile snapper (Family: Lutjanidae) in coastal nurseries. Coral Reefs 30, 1135–1145 (2011). https://doi.org/10.1007/s00338-011-0816-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-011-0816-5

Keywords

Search

Navigation