Skip to main content

Advertisement

Log in

Trophic ecology of reef sharks determined using stable isotopes and telemetry

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

Abstract

Establishing the ecological role of predators within an ecosystem is central to understanding community dynamics and is useful in designing effective management and conservation strategies. We analysed differences in the trophic ecology of four species of reef sharks (Carcharhinus melanopterus, Carcharhinus amblyrhynchos, Triaenodon obesus and Negaprion acutidens) at Ningaloo Reef, Western Australia, by analysing tissue stable isotopes (δ15N and δ13C). We also monitored animals using acoustic telemetry to determine long-term residency patterns in a bay at the southern end of the reef, Coral Bay. Overall, mean δ13C was similar among species, ranging between −10.9 and −11.8‰, suggesting a food-web dependency on coastal producers. Classification and regression tree analysis identified an effect of species on δ15N that separated C. amblyrhynchos and C. melanopterus from N. acutidens and T. obesus. For C. amblyrhynchos and C. melanopterus, animals were also divided by size classes, with smaller sharks having lower average δ15N than larger animals; this suggests that δ15N increases with size for these two species. Juvenile C. melanopterus, juvenile N. acutidens and adult T. obesus had trophic levels of 3.7, for juvenile C. amblyrhynchos and adult C. melanopterus it was 4, and adult C. amblyrhynchos had a value of 4.3. Trophic-level estimates for C. melanopterus and C. amblyrhynchos corroborate previous conclusions based on diet studies. We found no evidence for a difference in isotopic composition between resident and non-resident sharks. The lack of variation in isotopic composition was consistent with high mean residency of these species recorded using acoustic telemetry, which was 79% (±0.09 SE) of days monitored for T. obesus, followed by N. acutidens (57 ± 19.55%), C. amblyrhynchos (54 ± 13%) and C. melanopterus (33 ± 8.28%). High δ13C composition in reef sharks and long-term residency behaviour suggest that coastal marine reserves might provide effective conservation refuges for some species.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Bascompte J, Melian CJ, Sala E (2005) Interaction strength combinations and the overfishing of a marine food web. Proc Natl Acad Sci USA 102:5443–5447

    Article  PubMed  CAS  Google Scholar 

  • Bethea DM, Carlson JK, Buckel JA, Satterwhite M (2006) Ontogenetic and site-related trends in the diet of the Atlantic sharpnose shark Rhizoprionodon terraenovae from the Northeast Gulf of Mexico. Bull Mar Sci 78:287–307

    Google Scholar 

  • Stevens JD, Bonfil R, Dulvy NK, Walker PA (2000) The effects of fishing on sharks, rays and chimaeras (chondrichthyans), and the implications for marine ecosystems. ICES J Mar Sci 57:476–494

    Article  Google Scholar 

  • Bonfil R, Meyer MM, Scholl MC, Johnson R, O’Brien S, Oosthuizen H, Swanson S, Kotze D, Paterson M (2005) Transoceanic migration, spatial dynamics, and population linkages of white sharks. Science 310:100–103

    Article  PubMed  CAS  Google Scholar 

  • Borrell A, Cardona L, Kumarran RP, Aguilar A (2011) Trophic ecology of elasmobranchs caught off Gujarat, India, as inferred from stable isotopes. ICES J Mar Sci. doi:10.1093/icesjms/fsq1170

  • Cabana G, Rasmussen JB (1996) Comparison of aquatic food chains using nitrogen isotopes. Proc Natl Acad Sci USA 93:10844–10847

    Article  PubMed  CAS  Google Scholar 

  • Chapman DD, Pikitch EK, Babcock E, Shivji MS (2005) Marine reserve design and evaluation using automated acoustic telemetry: a case study involving coral reef-associated sharks in the Mesoamerican Caribbean. Mar Technol Soc J 39:42–55

    Article  Google Scholar 

  • Clementz MT, Koch PL (2001) Differentiating aquatic mammal habitat and foraging ecology with stable isotopes in tooth enamal. Oecologia 129:461–472

    Google Scholar 

  • Cortés E (1999) Standardized diet compositions and trophic levels of sharks. ICES J Mar Sci 56:707–717

    Article  Google Scholar 

  • Cortés E, Gruber SH (1990) Diet, feeding habits, and estimates of daily ration of young lemon sharks Negaprion brevirostris. Copeia 1:204–218

    Article  Google Scholar 

  • Cunjak RA, Roussel JM, Gray MA, Dietrich JP, Cartwright DF, Munkittrick KR, Jardine TD (2005) Using stable isotope analysis with telemetry or mark-recapture data to identify fish movement and foraging. Oecologia 144:636–646

    Article  PubMed  CAS  Google Scholar 

  • De’ath G, Fabricius KE (2000) Classification and regression trees: a powerful yet simple technique for ecological data analysis. Ecology 81:3178–3192

    Article  Google Scholar 

  • DEC (2005) Management plan for the Ningaloo Marine Park and Murion Islands Marine Management Area 2005–2011. DEC, Perth, Western Australia

  • Domi N, Bouquegneau JM, Das K (2005) Feeding ecology of five commercial shark species of the Celtic Sea through stable isotope and trace metal analysis. Mar Environ Res 60:551–569

    Article  PubMed  CAS  Google Scholar 

  • Eckert SA, Dolar LL, Kooyman GL, Perrin W, Rahman RA (2002) Movements of whale sharks (Rhincodon typus) in South-east Asian waters as determined by satellite telemetry. J Zool 257:111–115

    Article  Google Scholar 

  • Estrada JA, Rice AN, Lutcavage ME, Skomal GB (2003) Predicting trophic position in sharks of the north-west Atlantic Ocean using stable isotope analysis. J Mar Biol Assoc UK 83:1347–1350

    Article  CAS  Google Scholar 

  • Estrada JA, Rice AN, Natanson LJ, Skomal GB (2006) Use of isotopic analysis of vertebrae in reconstructing ontogenetic feeding ecology in white sharks. Ecology 87:829–834

    Article  PubMed  Google Scholar 

  • Ferretti F, Worm B, Britten GL, Heithaus MR, Lotze HK (2010) Patterns and ecosystem consequences of shark declines in the ocean. Ecol Lett 13:1055–1071

    PubMed  Google Scholar 

  • Field IC, Meekan M, Buckworth RC, Bradshaw CJA (2009) Susceptibility of sharks, rays and chimaeras to global extinction. Adv Mar Biol 56:275–363

    Article  PubMed  Google Scholar 

  • Field IC, Meekan MG, Speed CW, White W, Bradshaw CJA (2011) Quantifying movement patterns for shark conservation at remote coral atolls in the Indian Ocean. Coral Reefs 30:61–71

    Article  Google Scholar 

  • Fisk AT, Tittlemeier SA, Pranschke JL, Norstrom RJ (2002) Using anthropogenic contaminants and stable isotopes to assess the feeding ecology of the Greenland sharks. Ecology 83:2162–2172

    Article  Google Scholar 

  • France RL (1995) C-13 enrichment in benthic compared to planktonic algae—foodweb implications. Mar Ecol Prog Ser 124:307–312

    Article  Google Scholar 

  • Fry B, Scanlan RS, Parker PL (1983) 13C/12C ratios in marine food webs in the Torres Strait, Queensland. Aust J Mar Freshw Res 34:707–715

    Article  CAS  Google Scholar 

  • Hemminga MA, Mateo MA (1996) Stable carbon isotopes in seagrasses: variability in ratios and use in ecological studies. Mar Ecol Prog Ser 140:285–298

    Article  Google Scholar 

  • Heupel MR, Simpfendorfer CA (2005) Using acoustic monitoring to evaluate MPAs for shark nursery areas: the importance of long-term data. Mar Tech Soc J 39:10–18

    Article  Google Scholar 

  • Heupel MR, Williams AJ, Welch DJ, Ballagh A, Mapstone BD, Carlos G, Davies C, Simpfendorfer CA (2009) Effects of fishing on tropical reef associated shark populations on the Great Barrier Reef. Fish Res 95:350–361

    Article  Google Scholar 

  • Heupel MR, Simpfendorfer CA, Fitzpatrick R (2010) Large-scale movement and reef fidelity of Grey Reef Sharks. PLoS ONE 5(3):e9650. doi:10.1371/journal.pone.0009650

  • Hill J, McQuaid C, Kaehler S (2006) Biogeographic and nearshore–offshore trends in isotope ratios of intertidal mussels and their food sources around the coast of southern Africa. Mar Ecol Prog Ser 318:63–73

    Article  CAS  Google Scholar 

  • Hobson KA, Piatt JF, Pitocchelli J (1994) Using stable isotopes to determine seabird trophic relationships. J Anim Ecol 63:786–798

    Article  Google Scholar 

  • Hussey NE, MacNeil MA, Fisk AT (2010a) The requirement for accurate diet-tissue discrimination factors for interpreting stable isotopes in sharks. Hydrobiologia 654:1–5

    Article  CAS  Google Scholar 

  • Hussey NE, Brush J, McCarthy ID, Fisk AT (2010b) [delta] 15N and [delta] 13C diet-tissue discrimination factors for large sharks under semi-controlled conditions. Comp Biochem Physiol 155:445–453

    Article  Google Scholar 

  • Jackson JBC, Kirby MX, Berger WH, Bjorndal KA, Botsford LW, Bourque BJ, Bradbury RH, Cooke R, Erlandson J, Estes JA, Hughes TP, Kidwell S, Lange CB, Lenihan HS, Pandolfi JM, Peterson CH, Steneck RS, Tegner MJ, Warner RR (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629–638

    Article  PubMed  CAS  Google Scholar 

  • Last PR, Stevens JD (2009) Sharks and rays of Australia. CSIRO Publishing, Collingwood

    Google Scholar 

  • Logan JM, Lutcavage ME (2010) Stable isotope dynamics in elasmobranch fishes. Hydrobiologia 644:231–244

    Article  CAS  Google Scholar 

  • Lowe CG, Wetherbee BM, Crow GL, Tester AL (1996) Ontogenetic dietary shifts and feeding behavior of the tiger shark, Galeocerdo cuvier, in Hawaiian waters. Environ Biol Fish 47:203–211

    Article  Google Scholar 

  • MacNeil MA, Skomal GB, Fisk AT (2005) Stable isotopes from multiple tissues reveal diet switching in sharks. Mar Ecol Prog Ser 302:199–206

    Article  Google Scholar 

  • Maljković A, Côté IM (2011) Effects of tourism-related provisioning on the trophic signatures and movement patterns of an apex predator, the Caribbean reef shark. Biol Conserv 144:859–865

    Article  Google Scholar 

  • Matich P, Heithaus MR, Layman CA (2010) Size-based variation in intertissue comparisons of stable carbon and nitrogen isotopic signatures of bull sharks (Carcharhinus leucas) and tiger sharks (Galeocerdo cuvier). Can J Fish Aquat Sci 67:877–885

    Article  CAS  Google Scholar 

  • Matich P, Heithaus MR, Layman CA (2011) Contrasting patterns of individual specialization and trophic coupling in two marine apex predators. J Anim Ecol 80:294–305

    Article  PubMed  Google Scholar 

  • McElroy WD, Wetherbee BM, Mostello CS, Lowe CG, Crow GL, Wass RC (2006) Food habits and ontogenetic changes in the diet of the sandbar shark, Carcharhinus plumbeus, in Hawaii. Environ Biol Fish 76:81–92

    Article  Google Scholar 

  • McKibben JN, Nelson DR (1986) Patterns of movement and grouping of gray reef sharks, Carcharhinus amblyrhynchos, at Enewetak, Marshall Island. Bull Mar Sci 38:89–110

    Google Scholar 

  • Menard F, Lorrain A, Potier M, Marsac F (2007) Isotopic evidence of distinct feeding ecologies and movement patterns in two migratory predators (yellowfin tuna and swordfish) of the western Indian Ocean. Mar Biol 153:141–152

    Article  Google Scholar 

  • Myers RA, Worm B (2003) Rapid worldwide depletion of predatory fish communities. Nature 423:280–283

    Article  PubMed  CAS  Google Scholar 

  • Myers RA, Baum JK, Shepard TD, Powers SP, Peterson CH (2007) Cascading effects of the loss of apex predatory sharks from a coastal ocean. Science 315:1846–1850

    Article  PubMed  CAS  Google Scholar 

  • Olin JA, Hussey NE, Fritts M, Heupel MR, Simpfendorfer CA, Poulakis GR, Fisk AT (2011) Maternal meddling in neonatal sharks: implications for interpreting stable isotopes in young animals. Rapid Commun Mass Spectrom 25:1008–1016

    Article  PubMed  CAS  Google Scholar 

  • Papastamatiou YP, Wetherbee BM, Lowe CG, Crow GL (2006) Distribution and diet of four species of carcharhinid shark in the Hawaiian Islands: evidence for resource partitioning and competitive exclusion. Mar Ecol Prog Ser 320:239–251

    Article  Google Scholar 

  • Papastamatiou YP, Lowe CG, Caselle JE, Friedlander AM (2009) Scale-dependent effects of habitat on movement and path structure of reef sharks at a predator-dominated atoll. Ecology 90:996–1008

    Article  PubMed  Google Scholar 

  • Papastamatiou YP, Friedlander AM, Caselle JE, Lowe CG (2010a) Long-term movement patterns and trophic ecology of blacktip reef sharks (Carcharhinus melanopterus) at Palmyra Atoll. J Exp Mar Biol Ecol 386:94–102

    Article  Google Scholar 

  • Papastamatiou YP, Itano DG, Dale JJ, Meyer CG, Holland KN (2010b) Site fidelity and movements of sharks associated with ocean-farming cages in Hawaii. Mar Freshw Res 61:1366–1375

    Article  CAS  Google Scholar 

  • Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18:293–320

    Article  Google Scholar 

  • Post DM (2002) Using stable isotopes to estimate trophic positions: models, methods and assumptions. Ecology 83:703–718

    Article  Google Scholar 

  • Randall JE (1977) Contribution to the biology of the Whitetip Reef Shark. Pac Sci 31:143–164

    Google Scholar 

  • Revill AT, Young JW, Lansdell M (2009) Stable isotopic evidence for trophic groupings and bio-regionalization of predators and their prey in oceanic waters off eastern Australia. Mar Biol 156:1241–1253

    Article  Google Scholar 

  • Robbins WD, Hisano M, Connolly SR, Choat HJ (2006) Ongoing collapse of coral-reef shark populations. Curr Biol 16:2314–2319

    Article  PubMed  CAS  Google Scholar 

  • Salini JP, Blaber SJM, Brewer DT (1992) Diets of sharks from estuaries and adjacent waters of the north-eastern Gulf of Carpentaria, Australia. Aust J Mar Freshw Res 43:87–96

    Article  Google Scholar 

  • Scharf FS, Juanes F, Rountree RA (2000) Predator size—prey size relationships of marine fish predators: interspecific variation and effects of ontogeny and body size on trophic-niche breadth. Mar Ecol Prog Ser 208:229–248

    Article  Google Scholar 

  • Shepard TD, Myers RA (2005) Direct and indirect fishery effects on small coastal elasmobranchs in the northern Gulf of Mexico. Ecol Lett 8:1095–1104

    Article  Google Scholar 

  • Sherwood GD, Rose GA (2005) Stable isotope analysis of some representative fish and invertebrates of the Newfoundland and Labrador continental shelf food web. Estuar Coast Shelf Sci 63:537–549

    Article  CAS  Google Scholar 

  • Speed CW, Field IC, Meekan MG, Bradshaw CJA (2010) Complexities of coastal shark movements and their implications for management. Mar Ecol Prog Ser 408:275–305

    Article  Google Scholar 

  • Speed CW, Meekan MG, Field IC, McMahon CR, Stevens JD, McGregor F, Huveneers C, Berger Y, Bradshaw CJA (2011) Spatial and temporal movement patterns of a multi-species coastal reef shark aggregation. Mar Ecol Prog Ser 429:261–275

    Article  Google Scholar 

  • Stephenson PC, Edmonds JS, Moran MJ, Caputi N (2001) Analysis of stable isotope ratios to investigate stock structure of red emperor and Rankin cod in northern Western Australia. J Fish Biol 58:126–144

    Article  Google Scholar 

  • Stevens JD (1984) Life-history and ecology of sharks at Aldabra Atoll, Indian Ocean. Proc R Soc London Ser B 222:79–106

    Article  Google Scholar 

  • Stevens JD, McLoughlin KJ (1991) Distribution, size and sex composition, reproductive biology and diet of sharks from Northern Australia. Aust J Mar Freshw Res 32:151–199

    Article  Google Scholar 

  • Suryan RM, Fischer KN (2010) Stable isotope analysis and satellite tracking reveal interspecific resource partitioning of nonbreeding albatrosses off Alaska. Can J Zool 88:299–305

    Article  CAS  Google Scholar 

  • Vander Zanden MJ, Rasmussen JB (1999) Primary consumer delta C-13 and delta N-15 and the trophic position of aquatic consumers. Ecology 80:1395–1404

    Article  Google Scholar 

  • Vaudo JJ, Heithaus MR (2011) Dietary niche overlap in a nearshore elasmobranch mesopredator community. Mar Ecol Prog Ser 425:247–260

    Article  Google Scholar 

  • Ward-Paige CA, Mora C, Lotze HK, Pattengill-Semmens C, McClenachan L, Arias-Castro E, Myers RA (2010) Large-scale absence of sharks on reefs in the Greater-Caribbean: a footprint of human pressures. PLoS ONE 5:e11968. doi:10.1371/journal.pone.0011968

  • Wetherbee BM, Cortés E (2004) Food consumption and feeding habits. In: Carrier JC, Musick JA, Heithaus MR (eds) Biology of sharks and their relatives. CRC Press, Florida

    Google Scholar 

  • Wetherbee BM, Crow GL, Lowe CG (1997) Distribution, reproduction and diet of the gray reef shark Carcharhinus amblyrhinchos in Hawaii. Mar Ecol Prog Ser 151:181–189

    Article  Google Scholar 

  • Wyatt ASJ, Waite AM, Humphries S (2010) Variability in isotope discrimination factors in coral reef fishes: Implications for diet and food web reconstruction. PLoS ONE 5(10):e13682. doi:10.1371/journal.pone.0013682

Download references

Acknowledgments

We thank O. O’Shea, F. McGregor, G. Vianna, J. Ruppert, F. Wylie, S. Baccarella, P. Haskell, D. Simpson, I. Ford, C. Lochu and F. Cerutti for assistance with field work. We thank K. and W. McCarthy for provision of cryogenic facilities for sample storage. We are grateful to G. Hyndes for providing baseline isotopic information from Ningaloo Reef. Isotope processing and analysis were done by J. Tranter at Natural Isotopes, Edith Cowan University. All research was done with approval from the Charles Darwin University Animal Ethics Committee (#A07035). Access to Ningaloo Reef Marine Park and fauna sampling was done in compliance with the Department of Environment and Conservation (#CE002881 and #1719-2010-39) and the Western Australian Department of Fisheries (#SF7536).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to C. W. Speed.

Additional information

Communicated by Biology Editor Prof. Philip Munday

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 45 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Speed, C.W., Meekan, M.G., Field, I.C. et al. Trophic ecology of reef sharks determined using stable isotopes and telemetry. Coral Reefs 31, 357–367 (2012). https://doi.org/10.1007/s00338-011-0850-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-011-0850-3

Keywords

Navigation