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

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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.

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References

  • 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 102:5443–5447

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 8:263–286

    Article  Google Scholar 

  • 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 17:151–162

    Article  Google Scholar 

  • 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 24:169–197

    Article  Google Scholar 

  • 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 23:468–474

    Article  Google Scholar 

  • Connell SD (1998) Patterns of piscivory by resident predatory reef fish at One Tree Reef, Great Barrier Reef. Mar Freshw Res 49:25–30

    Article  Google Scholar 

  • 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 54:726–738

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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:e00590

  • Elith J, Leathwick JR, Hastie T (2008) A working guide to boosted regression trees. J Anim Ecol 77:802–813

    Article  CAS  PubMed  Google Scholar 

  • 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:e106885

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 333:301–306

    Article  CAS  PubMed  Google Scholar 

  • 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 102:16–25

    Article  Google Scholar 

  • Farmer BM, Wilson SK (2011) Diet of finfish targeted by fishers in north west Australia and the implications for trophic cascades. Environ Biol Fish 91:71–85

    Article  Google Scholar 

  • 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 230:253–264

    Article  Google Scholar 

  • 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 161:61–73

    Article  Google Scholar 

  • 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:e51938

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heithaus MR, Frid A, Wirsing AJ, Worm B (2008) Predicting ecological consequences of marine top predator declines. Trends Ecol Evol 23:202–210

    Article  PubMed  Google Scholar 

  • 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 611–636

    Chapter  Google Scholar 

  • Heupel MR, Simpfendorfer CA, Fitzpatrick R (2010) Large-scale movement and reef fidelity of grey reef sharks. PLoS One 5:e9650

    Article  PubMed  PubMed Central  Google Scholar 

  • Heupel MR, Knip DM, Simpfendorfer CA, Dulvy NK (2014) Sizing up the ecological role of sharks as predators. Mar Ecol Prog Ser 495:291–298

    Article  Google Scholar 

  • Heyward MW, Kerley GIH (2008) Prey preferences and dietary overlap amongst Africa’s large predators. S Afr J Wildl Res 38:93–108

    Article  Google Scholar 

  • Hilting AK, Currin CA, Kosaki RK (2013) Evidence for benthic primary production support of an apex predator-dominated coral reef food web. Mar Biol 160:1681–1695

    Article  CAS  Google Scholar 

  • 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 318:1737–1742

    Article  CAS  PubMed  Google Scholar 

  • Hoey AS, Bellwood DR (2009) Limited functional redundancy in a high diversity system: single species dominates key ecological process on coral reefs. Ecosystems 12:1316–1328

    Article  Google Scholar 

  • 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:445–453

    Article  CAS  Google Scholar 

  • 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 17:239–250

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 17:768

    Article  PubMed Central  Google Scholar 

  • Hussey NE, MacNeil MA, Siple MC, Popp BN, Dudley SFJ, Fisk AT (2015) Expanded trophic complexity among large sharks. Food Webs 4:1–7

    Article  Google Scholar 

  • 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 80:595–602

    Article  PubMed  Google Scholar 

  • Kingsford MJ (1992) Spatial and temporal variation in predation on reef fishes by coral trout (Plectropomus leopardus, Serranidae). Coral Reefs 11:193–198

    Article  Google Scholar 

  • 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 18:231–250

    Article  Google Scholar 

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

    Google Scholar 

  • 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 47:203–211

    Article  Google Scholar 

  • 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 22:1711–1717

    Article  PubMed  Google Scholar 

  • Mourier J, Planes S, Buray N (2013) Trophic interactions at the top of the coral reef food chain. Coral Reefs 32:285

    Article  Google Scholar 

  • 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 311:98–101

    Article  CAS  PubMed  Google Scholar 

  • 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 315:1846–1850

    Article  CAS  PubMed  Google Scholar 

  • 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 48:119–128

    Article  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 

  • R Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Randall JE (1977) Contribution to the biology of the whitetip reef shark. Pac Sci 31:143–164

    Google Scholar 

  • 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 343:1241484

    Article  PubMed  Google Scholar 

  • Ritchie EG, Johnson CN (2009) Predator interactions, mesopredator release and biodiversity conservation. Ecol Lett 12:982–998

    Article  PubMed  Google Scholar 

  • Rizzari JR, Frisch AJ, Connolly SR (2014a) How robust are estimates of coral reef shark depletion? Biol Conserv 176:39–47

    Article  Google Scholar 

  • 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 161:2847–2855

    Article  Google Scholar 

  • Rizzari JR, Bergseth BJ, Frisch AJ (2015) Impact of conservation areas on trophic interactions between apex predators and herbivores on coral reefs. Conserv Biol 29:418–429

    Article  PubMed  Google Scholar 

  • Rizzari JR, Frisch AJ, Hoey AS, McCormick MI (2014c) Not worth the risk: apex predators suppress herbivory on coral reefs. Oikos 123:829–836

    Article  Google Scholar 

  • Roemer GW, Gompper ME, Valkenburgh BV (2009) The ecological role of the mammalian mesocarnivore. BioScience 59:165–173

    Article  Google Scholar 

  • 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:e74648

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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:e1548

    Article  PubMed  PubMed Central  Google Scholar 

  • Schoener T (1968) The Anolis lizards of Bimini: resource partitioning in a complex fauna. Ecology 49:704–726

    Article  Google Scholar 

  • 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 31:357–367

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Trebilco R, Baum JK, Salomon AK, Dulvy NK (2013) Ecosystem ecology: size-based constraints on the pyramids of life. Trends Ecol Evol 28:423–431

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • 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 93:121–136

    Article  Google Scholar 

  • 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 10:239–250

    Article  Google Scholar 

  • Woodward G, Hildrew AG (2002) Body-size determinants of niche overlap and intraguild predation within a complex food web. J Anim Ecol 71:1063–1074

    Article  Google Scholar 

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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).

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Correspondence to Ashley J. Frisch.

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Communicated by Ecology Editor Dr. Alastair Harborne

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Fig. S1

Relationship 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)

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Frisch, A.J., Ireland, M., Rizzari, J.R. et al. Reassessing the trophic role of reef sharks as apex predators on coral reefs. Coral Reefs 35, 459–472 (2016). https://doi.org/10.1007/s00338-016-1415-2

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