Coral Reefs

, Volume 35, Issue 2, pp 459–472 | Cite as

Reassessing the trophic role of reef sharks as apex predators on coral reefs

  • Ashley J. Frisch
  • Matthew Ireland
  • Justin R. Rizzari
  • Oona M. Lönnstedt
  • Katalin A. Magnenat
  • Christopher E. Mirbach
  • Jean-Paul A. Hobbs
Report

Abstract

Apex predators often have strong top-down effects on ecosystem components and are therefore a priority for conservation and management. Due to their large size and conspicuous predatory behaviour, reef sharks are typically assumed to be apex predators, but their functional role is yet to be confirmed. In this study, we used stomach contents and stable isotopes to estimate diet, trophic position and carbon sources for three common species of reef shark (Triaenodon obesus, Carcharhinus melanopterus and C. amblyrhynchos) from the Great Barrier Reef (Australia) and evaluated their assumed functional role as apex predators by qualitative and quantitative comparisons with other sharks and large predatory fishes. We found that reef sharks do not occupy the apex of coral reef food chains, but instead have functional roles similar to those of large predatory fishes such as snappers, emperors and groupers, which are typically regarded as high-level mesopredators. We hypothesise that a degree of functional redundancy exists within this guild of predators, potentially explaining why shark-induced trophic cascades are rare or subtle in coral reef ecosystems. We also found that reef sharks participate in multiple food webs (pelagic and benthic) and are sustained by multiple sources of primary production. We conclude that large conspicuous predators, be they elasmobranchs or any other taxon, should not axiomatically be regarded as apex predators without thorough analysis of their diet. In the case of reef sharks, our dietary analyses suggest they should be reassigned to an alternative trophic group such as high-level mesopredators. This change will facilitate improved understanding of how reef communities function and how removal of predators (e.g., via fishing) might affect ecosystem properties.

Keywords

Elasmobranch Food web Stable isotope analysis Top-down control Trophic ecology 

Notes

Acknowledgments

We thank R. Baker, B. Bergseth, J. Frisch, S. Frisch and B. Bauerle for technical assistance and N. Hussey for reviewing an earlier draft of the manuscript. Funding was provided by a Lizard Island Research Station John and Laurine Proud Fellowship (AJF) and a grant from the Save Our Seas Foundation (JRR). This research was undertaken with permission from the GBR Marine Park Authority (permit number G12/34941.1), Fisheries Queensland (permit number 152940) and the James Cook University Animal Experimentation Ethics Committee (approval number A1742).

Supplementary material

338_2016_1415_MOESM1_ESM.tif (11.9 mb)
Fig. S1Relationship between δ13C (a–c), δ15N (d–f) and total length in (a, d) Triaenodon obesus, (b, e) Carcharhinus melanopterus and (c, f) C. amblyrhynchos. Other species are not included due to small sample sizes. Statistically significant relationships are depicted by regression lines (TIFF 12221 kb)

References

  1. Bascompte J, Melian CJ, Sala E (2005) Interaction strength combinations and the overfishing of a marine food web. Proc Natl Acad Sci U S A 102:5443–5447CrossRefPubMedPubMedCentralGoogle Scholar
  2. Blaber SJM, Milton DA, Rawlinson NJF, Tiroba G, Nichols PV (1990) Diets of lagoon fishes of the Solomon Islands: predators of tuna baitfish and trophic effects of bait fishing on the subsistence fishery. Fish Res 8:263–286CrossRefGoogle Scholar
  3. Bozec YM, Gascuel D, Kulbicki M (2004) Trophic model of lagoonal communities in a large open atoll (Uvea, Loyalty Islands, New Caledonia). Aquat Living Resour 17:151–162CrossRefGoogle Scholar
  4. Ceccarelli DM, Frisch AJ, Graham NAJ, Ayling AM, Beger M (2014) Habitat partitioning and vulnerability of sharks in the Great Barrier Reef Marine Park. Rev Fish Biol Fish 24:169–197CrossRefGoogle Scholar
  5. Chin A, Heupel MR, Simpfendorfer CA, Tobin AJ (2013) Ontogenetic movements of juvenile blacktip reef sharks: evidence of dispersal and connectivity between coastal habitats and coral reefs. Aquat Conserv 23:468–474CrossRefGoogle Scholar
  6. Connell SD (1998) Patterns of piscivory by resident predatory reef fish at One Tree Reef, Great Barrier Reef. Mar Freshw Res 49:25–30CrossRefGoogle Scholar
  7. Cortés E (1997) A critical review of methods of studying fish feeding based on analysis of stomach contents: application to elasmobranch fishes. Can J Fish Aquat Sci 54:726–738CrossRefGoogle Scholar
  8. Cortés E (1999) Standardized diet compositions and trophic levels of sharks. ICES J Mar Sci 56:707–717CrossRefGoogle Scholar
  9. Dulvy NK, Fowler SL, Musick JA, Cavanagh RD, Kyne PM, Harrison LR, Carlson JK, Davidson LNK, Fordham SV, Francis MP, Pollock CM, Simpfendorfer CA, Burgess GH, Carpenter KE, Compagno LVJ, Ebert DA, Gibson C, Heupel MR, Livingstone SR, Sanciangco JC, Stevens JD, Valenti D, White WT (2014) Extinction risk and conservation of the world’s sharks and rays. eLife 3:e00590Google Scholar
  10. Elith J, Leathwick JR, Hastie T (2008) A working guide to boosted regression trees. J Anim Ecol 77:802–813CrossRefPubMedGoogle Scholar
  11. Espinoza M, Cappo M, Heupel MR, Tobin AJ, Simpfendorfer CA (2014) Quantifying shark distribution patterns and species-habitat associations: implications of marine park zoning. PLoS One 9:e106885CrossRefPubMedPubMedCentralGoogle Scholar
  12. Estes JA, Terborgh J, Brashares JS, Power ME, Berger J, Bond W, Carpenter SR, Essington TE, Holt RD, Jackson JBC, Marquis RJ, Oksanen L, Oksanen T, Paine RT, Pikitch EK, Ripple WJ, Sandin SA, Scheffer M, Schoener TW, Shurin JB, Sinclair AR, Soulé ME, Virtanen R, Wardle DA (2011) Trophic downgrading of planet Earth. Science 333:301–306CrossRefPubMedGoogle Scholar
  13. Evans RD, van Herwerden L, Russ GR, Frisch AJ (2010) Strong genetic but not spatial subdivision of two reef fish species targeted by fishers on the Great Barrier Reef. Fish Res 102:16–25CrossRefGoogle Scholar
  14. Farmer BM, Wilson SK (2011) Diet of finfish targeted by fishers in north west Australia and the implications for trophic cascades. Environ Biol Fish 91:71–85CrossRefGoogle Scholar
  15. Friedlander AM, DeMartini EE (2002) Contrasts in density, size, and biomass of reef fishes between the northwestern and the main Hawaiian Islands: the effects of fishing down apex predators. Mar Ecol Prog Ser 230:253–264CrossRefGoogle Scholar
  16. Frisch AJ, Ireland M, Baker R (2014) Trophic ecology of large predatory reef fishes: energy pathways, trophic level, and implications for fisheries in a changing climate. Mar Biol 161:61–73CrossRefGoogle Scholar
  17. Frisch AJ, Cole AJ, Hobbs JA, Rizzari JR, Munkres KP (2012) Effects of spearfishing on reef fish populations in a multi-use conservation area. PLoS One 7:e51938CrossRefPubMedPubMedCentralGoogle Scholar
  18. Heithaus MR, Frid A, Wirsing AJ, Worm B (2008) Predicting ecological consequences of marine top predator declines. Trends Ecol Evol 23:202–210CrossRefPubMedGoogle Scholar
  19. Heithaus MR, Frid A, Vaudo JJ, Worm B, Wirsing AJ (2010) Unravelling the ecological importance of elasmobranchs. In: Carrier JC, Musick JA, Heithaus MR (eds) Sharks and their relatives II: biodiversity, adaptive physiology and conservation. CRC Press, Boca Raton, pp 611–636CrossRefGoogle Scholar
  20. Heupel MR, Simpfendorfer CA, Fitzpatrick R (2010) Large-scale movement and reef fidelity of grey reef sharks. PLoS One 5:e9650CrossRefPubMedPubMedCentralGoogle Scholar
  21. Heupel MR, Knip DM, Simpfendorfer CA, Dulvy NK (2014) Sizing up the ecological role of sharks as predators. Mar Ecol Prog Ser 495:291–298CrossRefGoogle Scholar
  22. Heyward MW, Kerley GIH (2008) Prey preferences and dietary overlap amongst Africa’s large predators. S Afr J Wildl Res 38:93–108CrossRefGoogle Scholar
  23. Hilting AK, Currin CA, Kosaki RK (2013) Evidence for benthic primary production support of an apex predator-dominated coral reef food web. Mar Biol 160:1681–1695CrossRefGoogle Scholar
  24. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742CrossRefPubMedGoogle Scholar
  25. Hoey AS, Bellwood DR (2009) Limited functional redundancy in a high diversity system: single species dominates key ecological process on coral reefs. Ecosystems 12:1316–1328CrossRefGoogle Scholar
  26. Hussey NE, Brush J, McCarthy ID, Fisk AT (2010) δ15N and δ13C diet-tissue discrimination factors for large sharks under semi-controlled conditions. Comp Biochem Physiol 155A:445–453CrossRefGoogle Scholar
  27. Hussey NE, MacNeil MA, McMeans BC, Olin JA, Dudley SFJ, Cliff GC, Wintner SP, Fennessy ST, Fisk AT (2014a) Rescaling the trophic structure of marine food webs. Ecol Lett 17:239–250CrossRefPubMedPubMedCentralGoogle Scholar
  28. Hussey NE, MacNeil MA, McMeans BC, Olin JA, Dudley SFJ, Cliff GC, Wintner SP, Fennessy ST, Fisk AT (2014b) Corrigendum to Hussey, et al. (2014). Ecol Lett 17:768CrossRefPubMedCentralGoogle Scholar
  29. Hussey NE, MacNeil MA, Siple MC, Popp BN, Dudley SFJ, Fisk AT (2015) Expanded trophic complexity among large sharks. Food Webs 4:1–7CrossRefGoogle Scholar
  30. Jackson AL, Inger R, Parnell AC, Bearhop S (2011) Comparing isotopic niche widths among and within communities: SIBER – stable isotope Bayesian ellipses in R. J Anim Ecol 80:595–602CrossRefPubMedGoogle Scholar
  31. Kingsford MJ (1992) Spatial and temporal variation in predation on reef fishes by coral trout (Plectropomus leopardus, Serranidae). Coral Reefs 11:193–198CrossRefGoogle Scholar
  32. Kulbicki M, Bozec YM, Labrosse P, Letourneur Y, Mou-Tham G, Wantiez L (2005) Diet composition of carnivorous fishes from coral reef lagoons of New Caledonia. Aquat Living Resour 18:231–250CrossRefGoogle Scholar
  33. Last PR, Stevens JD (2009) Sharks and rays of Australia. CSIRO Publishing, CollingwoodGoogle Scholar
  34. Lowe CG, Wetherbee BM, Crow GL, Tester AL (1996) Ontogenetic dietary shifts and feeding behaviour of the tiger shark, Galeocerdo cuvier, in Hawaiian waters. Environ Biol Fish 47:203–211CrossRefGoogle Scholar
  35. McCauley DJ, Young HS, Dunbar RB, Estes JA, Semmens BX, Micheli F (2012) Assessing the effects of large mobile predators on ecosystem connectivity. Ecol Appl 22:1711–1717CrossRefPubMedGoogle Scholar
  36. Mourier J, Planes S, Buray N (2013) Trophic interactions at the top of the coral reef food chain. Coral Reefs 32:285CrossRefGoogle Scholar
  37. Mumby PJ, Dahlgren CP, Harborne AR, Kappel CV, Micheli F, Brumbaugh DR, Holmes KE, Mendes JM, Broad K, Sanchirico JN, Buch K, Box S, Stoffle RW, Gill AB (2006) Fishing, trophic cascades, and the process of grazing on coral reefs. Science 311:98–101CrossRefPubMedGoogle Scholar
  38. Myers RA, Baum JK, Shepherd TD, Powers SP, Peterson CH (2007) Cascading effects of the loss of apex predator sharks from a coastal ocean. Science 315:1846–1850CrossRefPubMedGoogle Scholar
  39. Newman SJ, Williams DM, Russ GR (1997) Patterns of zonation of assemblages of the Lutjanidae, Lethrinidae and Serranidae (Epinephelinae) within and among mid-shelf and outer-shelf reefs in the central Great Barrier Reef. Mar Freshw Res 48:119–128CrossRefGoogle Scholar
  40. 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 320:239–251CrossRefGoogle Scholar
  41. R Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  42. Randall JE (1977) Contribution to the biology of the whitetip reef shark. Pac Sci 31:143–164Google Scholar
  43. Ripple WJ, Estes JA, Beschta RL, Wilmers CC, Ritchie EG, Hebblewhite M, Berger J, Elmhagen B, Letnic M, Nelson MP, Schmitz OJ, Smith DW, Wallach AD, Wirsing AJ (2014) Status and ecological effects of the world’s largest carnivores. Science 343:1241484CrossRefPubMedGoogle Scholar
  44. Ritchie EG, Johnson CN (2009) Predator interactions, mesopredator release and biodiversity conservation. Ecol Lett 12:982–998CrossRefPubMedGoogle Scholar
  45. Rizzari JR, Frisch AJ, Connolly SR (2014a) How robust are estimates of coral reef shark depletion? Biol Conserv 176:39–47CrossRefGoogle Scholar
  46. Rizzari JR, Frisch AJ, Magnenat KA (2014b) Diversity, abundance, and distribution of reef sharks on outer-shelf reefs of the Great Barrier Reef, Australia. Mar Biol 161:2847–2855CrossRefGoogle Scholar
  47. Rizzari JR, Bergseth BJ, Frisch AJ (2015) Impact of conservation areas on trophic interactions between apex predators and herbivores on coral reefs. Conserv Biol 29:418–429CrossRefPubMedGoogle Scholar
  48. Rizzari JR, Frisch AJ, Hoey AS, McCormick MI (2014c) Not worth the risk: apex predators suppress herbivory on coral reefs. Oikos 123:829–836CrossRefGoogle Scholar
  49. Roemer GW, Gompper ME, Valkenburgh BV (2009) The ecological role of the mammalian mesocarnivore. BioScience 59:165–173CrossRefGoogle Scholar
  50. Ruppert JLW, Travers MJ, Smith LL, Fortin MJ, Meekan MG (2013) Caught in the middle: combined impacts of shark removal and coral loss on the fish communities of coral reefs. PLoS One 8:e74648CrossRefPubMedPubMedCentralGoogle Scholar
  51. Sandin SA, Smith JE, DeMartini EE, Dinsdale EA, Donner SD, Friedlander AM, Konotchick T, Malay M, Maragos JE, Obura D, Pantos O, Paulay G, Richie M, Rohwer F, Schroeder RE, Walsh S, Jackson JBC, Knowlton N, Sala E (2008) Baselines and degradation of coral reefs in the Northern Line Islands. PLoS One 3:e1548CrossRefPubMedPubMedCentralGoogle Scholar
  52. Schoener T (1968) The Anolis lizards of Bimini: resource partitioning in a complex fauna. Ecology 49:704–726CrossRefGoogle Scholar
  53. Speed CW, Meekan MG, Field IC, McMahon CR, Abrantes K, Bradshaw CJA (2012) Trophic ecology of reef sharks determined using stable isotopes and telemetry. Coral Reefs 31:357–367CrossRefGoogle Scholar
  54. Stevens JD (1984) Life-history and ecology of sharks at Aldabra Atoll, Indian Ocean. Proc R Soc Lond B Biol Sci 222:79–106CrossRefGoogle Scholar
  55. Trebilco R, Baum JK, Salomon AK, Dulvy NK (2013) Ecosystem ecology: size-based constraints on the pyramids of life. Trends Ecol Evol 28:423–431CrossRefPubMedGoogle Scholar
  56. Wetherbee BM, Crow GL, Lowe CG (1997) Distribution, reproduction and diet of the gray reef shark Carcharhinus amblyrhynchos in Hawaii. Mar Ecol Prog Ser 151:181–189CrossRefGoogle Scholar
  57. Whitney NM, Pyle RL, Holland KN, Barcz JT (2012) Movements, reproductive seasonality, and fisheries interactions in the whitetip reef shark (Triaenodon obesus) from community-contributed photographs. Environ Biol Fish 93:121–136CrossRefGoogle Scholar
  58. Williams DM, Hatcher AI (1983) Structure of fish communities on outer slopes of inshore, mid-shelf and outer-shelf reefs of the Great Barrier Reef. Mar Ecol Prog Ser 10:239–250CrossRefGoogle Scholar
  59. Woodward G, Hildrew AG (2002) Body-size determinants of niche overlap and intraguild predation within a complex food web. J Anim Ecol 71:1063–1074CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Ashley J. Frisch
    • 1
  • Matthew Ireland
    • 2
  • Justin R. Rizzari
    • 1
    • 2
  • Oona M. Lönnstedt
    • 2
    • 3
  • Katalin A. Magnenat
    • 2
  • Christopher E. Mirbach
    • 2
  • Jean-Paul A. Hobbs
    • 4
  1. 1.Australian Research Council Centre of Excellence for Coral Reef StudiesJames Cook UniversityTownsvilleAustralia
  2. 2.College of Marine and Environmental SciencesJames Cook UniversityTownsvilleAustralia
  3. 3.Department of Ecology and Genetics, LimnologyUppsala UniversityUppsalaSweden
  4. 4.Department of Environment and AgricultureCurtin UniversityPerthAustralia

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