Skip to main content
SpringerLink
Log in

Behavioral evidence suggests facultative scavenging by a marine apex predator during a food pulse

Behavioral Ecology and Sociobiology volume 70, pages 1777–1788 (2016)Cite this article

Abstract

The ability of predators to switch between hunting and scavenging (facultative scavenging) carries both short-term survival and long-term fitness advantages. However, the mechanistic basis for facultative scavenging remains poorly understood. The co-occurrence of tiger sharks (Galeocerdo cuvier) and green turtles (Chelonia mydas) at Raine Island (Australia), provides an opportunity to examine a top marine predator’s feeding mode in response to seasonal pulses in nesting turtles that offer both hunting and scavenging opportunities. Using satellite telemetry, we evaluated home range overlap between sharks and turtles and quantified their surfacing behavior around Raine Island during the turtle nesting season. We found core home range overlap to be highest during the nesting season. Both sharks and turtles spent significantly more time at the surface in areas of greatest range overlap closest to shore, where turtle density was highest. Both sharks and turtles showed decreased surfacing with increasing distance from Raine Island. Combined with published data on turtle demography at Raine Island, we propose the following: (1) sharks patrol the surface to increase scavenging opportunities on turtle carcasses and intercept weakened individuals after nesting; (2) healthy turtles may not perceive sharks as a major threat and/or other biological factors override anti-predatory responses; and (3) sharks during the nesting season may primarily scavenge on dead turtles individuals rather than actively hunt. Our study results and approach may be applicable to other situations in which direct observations of predator-prey interactions are limited.

Significance Statement

Every animal encounters dead or dying resources, yet the role of facultative scavenging has been difficult to study, and thus largely overlooked in marine behavioral ecological research. Movement analyses of tiger shark and green turtle movement and surfacing behavior at Raine Island (Australia) suggest that facultative scavenging may be a prevalent, yet underappreciated, feeding strategy in tiger sharks. Our integration of behavioral ecology theory with multi-species electronic tagging provided a valuable approach for investigating predator-prey interactions in situations where direct observations are limited or not possible.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Afonso AS, Hazin FHV (2015) Vertical movement patterns and ontogenetic niche expansion in tiger shark, Galeocerdo cuvier. PLoS One 10:e0116720. doi:10.1371/journal.pone.0116720

  • Beasley J, Olson CHZ, DeVault TL (2012) Carrion cycling in food webs: comparisons among terrestrial and marine ecosystems. Oikos 121:1021–1026

    Article  Google Scholar 

  • Bell IP, Seymour J, Fitzpatrick R, Hogarth J (2009) Inter-nesting dive and surface behavior of green turtles, Chelonia mydas at Raine Island, Northern Great Barrier Reef. Mar Turt Newsl 125:5–7

    Google Scholar 

  • Bernard Y, Belbeoch M (2010) Improving Argos Doppler location with Kalman filtering – Advantages for Argos Floats. CLS ARGOS User’s Manual. Argos System, http://www.argos-system.org/files/pmedia/public/r283_9_new_argos_location_for_argo.pdf

  • Bonazzo A, Collin SP (2000) Retinal ganglion cell topography in Elasmobranchs. Brain Behav Evol 55:191–208

    Article  Google Scholar 

  • Burkholder DA, Heithaus MR, Fourqurean JW, Wirsing A, Dill LM (2013) Patterns of top down control in a seagrass ecosystem: could a roving apex predator (Galeocerdo cuvier) induce a behavior-mediated trophic cascade? J Anim Ecol 82:1192–1202

    Article  PubMed  Google Scholar 

  • Carbonne C, Teacher A, Rowcliffe JM (2007) The costs of carnivory. PLoS Biol 5:e22

    Article  Google Scholar 

  • Clua E, Chauvet C, Read T, Werry JM, Lee SY (2013) Behavioral patterns of a tiger shark (Galeocerdo cuvier) feeding aggregation at a blue whale carcass in Prony Bay, New Caledonia. Mar Freshw Behav Physiol 46:1–20

    Article  Google Scholar 

  • DeVault TL, Rhodes OE, Shivik JA (2003) Scavenging by vertebrates: behavioral, ecological, and evolutionary perspectives on an important energy transfer pathway in terrestrial ecoystems. Oikos 102:225–234

    Article  Google Scholar 

  • Doyle TK, Bennison A, Jessopp M, Haberlin D, Harman LA (2015) A dawn peak in the occurrence of ‘knifing behavior’ in blue sharks. Anim Biotelem 3:46

    Article  Google Scholar 

  • Dudley SF, Anderson-Reade MD, Thompson GS, McMullen PB (2000) Concurrent scavenging off a whale carcass by great white sharks, Carcharodon carcharias, and tiger sharks, Galeocerdo cuvier. Fish Bull 98:646–649

    Google Scholar 

  • Fallows C, Martin RA, Hammerschlag N (2012) Comparisons between white shark-pinniped interactions at Seal Island (South Africa) with other sites in California (United States). In: Domeier ML (ed) Global perspectives on the biology and life history of the great white shark. CRC Press, Boca Raton, FL, pp. 105–117

    Chapter  Google Scholar 

  • Fallows C, Gallagher AJ, Hammerschlag N (2013) White sharks (Carcharodon carcharias) scavenging on whales and its potential role in further shaping the ecology of an apex predator. PLoS One 8:e60797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ferriera LC, Thums M, Meeuwig JJ, Vianna GMS, Stevens J, McAuley R, Meekan MG (2015) Crossing latitudes-long distance tracking of an apex predator. PLoS One 10:e0116916

    Article  Google Scholar 

  • Fitzpatrick R, Thums M, Bell I, Meekan MM, Stevens JD, Barnett A (2012) A comparison of seasonal movements of tiger sharks and green turtles provides insight into their predator-prey relationship. PLoS One 7:e51927

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fu AL, Hammerschlag N, Lauder GV, Wilga CD, Kuo CY, Irschick DJ (2016) Ontogeny of head and caudal fin shape of an apex marine predator: The tiger shark (Galeocerdo cuvier). J Morphol DOI:10.1002/jmor.20515

  • Gallagher AJ, Jackson T, Hammerschlag N (2011) Occurrence of tiger shark (Galeocerdo cuvier) scavenging on avian prey and its possible connection to large-scale bird die-offs in the Florida Keys. Fla Sci 74:264–269

    Google Scholar 

  • Gallagher AJ, Wagner DN, Irschick DJ, Hammerschlag N (2014) Body condition predicts energy stores in apex predatory sharks. Conserv Physiol 2:cou022

    Article  PubMed  PubMed Central  Google Scholar 

  • Gallagher AJ, Hammerschlag N, Cooke SJ, Costa DP, Irschick DJ (2015) Evolutionary theory as a tool for predicting extinction risk. Trends Ecol Evol 30:61–65

    Article  PubMed  Google Scholar 

  • Hammerschlag N, Martin RA, Fallows C (2006) Effects of environmental conditions on predator-prey interactions between white sharks (Carcharodon carcharias) and Cape fur seals (Arctocephalus pusillus pusillus) at Seal Island, South Africa. Environ Biol Fish 76:341–350

    Article  Google Scholar 

  • Hammerschlag N, Gallagher AJ, Lazarre DM (2011) A review of shark satellite tagging studies. J Exp Mar Biol Ecol 398:1–8

    Article  Google Scholar 

  • Hammerschlag N, Gallagher AJ, Wester J, Luo J, Ault JS (2012) Don’t bite the hand that feeds: assessing ecological impacts of provisioning ecotourism on an apex marine predator. Funct Ecol 26:567–576

    Article  Google Scholar 

  • Hammerschlag N, Broderick AC, Coker JW, et al. (2015) Evaluating the landscape of fear between apex predatory sharks and mobile sea turtles across a large dynamic seascape. Ecology 96:2117–2126

    Article  PubMed  Google Scholar 

  • Hart N, Lisney T, Collin S (2006) Visual communication in elasmobranchs. In: Ladich F, Collin S, Moller P, Kapoor B (eds) Communication in fishes, 1st edn. Science Publishers, New Jersey, pp. 337–392

    Google Scholar 

  • Hays GC, Akesson S, Broderick AC, Glen F, Godley BJ, Lushi P, Martin C, Metcalfe JD, Papi F (2001) The diving behavior of green turtles undertaking oceanic migrations to and from Ascension Island: dive durations, dive profiles, and depth distribution. J Exp Biol 204:4093–4098

    CAS  PubMed  Google Scholar 

  • Heithaus MR (2001) The biology of tiger sharks, Galeocerdo cuvier, in Shark Bay, Western Australia: sex ratio, size distribution, diet, and seasonal changes in catch rates. Environ Biol Fish 61:25–36

    Article  Google Scholar 

  • Heithaus MR, Frid A (2003) Optimal diving under the risk of predation. J Theor Biol 223:79–92

    Article  PubMed  Google Scholar 

  • Heithaus MR, Frid A, Dill L (2002) Shark-inflicted injury frequencies, escape ability, and habitat use of green and loggerhead turtles. Mar Biol 140:229–236

    Article  Google Scholar 

  • Heithaus MR, Frid A, Wirsing AJ, Dill LM, Fourqurean JW, Burkholder D, Thomson J, Bejder L (2007) State-dependent risk taking by green sea turtles mediates top-down effects of tiger shark intimidation in a marine ecosystem. J Anim Ecol 76:837–844

    Article  PubMed  Google Scholar 

  • Heithaus MR, Wirsing AJ, Thomson JA, Burkholder DA (2008) A review of lethal and non-lethal effects of predators on adult marine turtles. J Exp Mar Biol Ecol 356:43–51

    Article  Google Scholar 

  • Holmes BJ, Sumpton WD, Mayer DG, Tibbetts IR, Neil DT, Bennett MB (2012) Declining trends in annual catch rates of the tiger shark (Galeocerdo cuvier) in Queensland, Australia. Fish Res 129-130:38–45

    Article  Google Scholar 

  • Jackson JBC, Kirby MX, Berger WH, et al. (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629–637

    Article  CAS  PubMed  Google Scholar 

  • Jessop TJ (2001) Modulation of adrenocortical stress response in marine turtles (Cheloniidae): evidence for a hormonal tactic maximizing maternal reproductive investment. J Zool 254:57–65

    Article  Google Scholar 

  • Limpus CJ, Miller JD, Parmenter CJ, Limpus DJ (2003) The green turtle Chelonia mydas, populations of Raine Island the northern Great Barrier Reef: 1843–2001. Mem Queensl Mus 49:349–440

    Google Scholar 

  • Lotze HK, Worm B (2009) Historical baselines for large marine animals. Trends Ecol Evol 24:254–262

    Article  PubMed  Google Scholar 

  • Madsen T, Shine R (1996) Seasonal migration of predators and prey: a study of pythons and rats in tropical Australia. Ecology 71:149–156

    Article  Google Scholar 

  • Martin RA, Hammerschlag N, Collier R, Fallows C (2005) Predatory behavior of white sharks (Carcharodon carcharias) at Seal Island, South Africa. J Mar Biol Assoc UK 85:1121–1135

    Article  Google Scholar 

  • McShea WM (2000) The influence of acorn crops on annual variation in rodent and bird populations within oak dominated forests. Ecology 8:228–238

    Article  Google Scholar 

  • Meyer CG, Papastamatiou YP, Holland KN (2010) A multiple instrument approach to quantifying the movement patterns and habitat use of tiger (Galeocerdo cuvier) and Galapagos sharks (Carcharhinus galapagensis) at French Frigate Shoals, Hawaii. Mar Biol 157:1857–1868

    Article  Google Scholar 

  • Nakamura I, Watanabe YY, Papastamatiou YP, Sato K, Meyer CG (2011) Yo-yo vertical movements suggest a foraging strategy for tiger sharks Galeocerdo cuvier. Mar Ecol Prog Ser 424:237–246

    Article  Google Scholar 

  • Nakamura I, Goto Y, Sato K (2015) Ocean sunfish rewarm at the surface after deep excursions to forage for siphonophores. J Anim Ecol 84:590–603

    Article  PubMed  Google Scholar 

  • Newton I (2008) The migration ecology of birds. Academic Press, London

    Google Scholar 

  • Ostfeld RS, Keesing F (2000) Pulsed resources and community dynamics of consumers in terrestrial ecoystems. Trends Ecol Evol 15:232–237

    Article  PubMed  Google Scholar 

  • Papastamatiou YP, Meyer CG, Carvalho F, Dale JJ, Hutchinson MR, Holland KM (2013) Telemetry and random-walk models reveal complex patterns of partial migration in a large marine predator. Ecology 94:2595–2606

    Article  PubMed  Google Scholar 

  • Paquet PC (1992) Prey use strategies of sympatric wolves and coyotes in Riding Mountain National Park, Manitoba. J Mammal 73:337–343

    Article  Google Scholar 

  • Pereira LM, Owen-Smith N, Moleon M (2014) Facultative predation and scavenging by mammalian carnivores: seasonal, regional, and intra-guild comparisons. Mammal Rev 44:44–55

    Article  Google Scholar 

  • Simpfendorfer CA, Goodreid AB, McAuley RB (2001) Size, sex, and geographic variation in the diet of the tiger shark, Galeocerdo cuvier, from Western Australian waters. Environ Biol Fish 61:37–46

    Article  Google Scholar 

  • Sims DW, Witt MJ, Richardson AJ, Southall EJ, Metcalfe JD (2006) Encounter success of free-ranging marine predator movements across a dynamic prey landscape. Proc R Soc Lond B 273:1195–1201

    Article  Google Scholar 

  • Werry JM, Planes S, Berumen ML, Lee KA, Braun CD, Clua E (2014) Reef-fidelity and migration of tiger sharks, Galeocerdo cuvier, across the Coral Sea. PLoS One 9:e83249

    Article  PubMed  PubMed Central  Google Scholar 

  • Wilson EE, Wolkovich EM (2011) Scavenging: how carnivores and carrion structure communities. Trends Ecol Evol 26:129–135

    Article  PubMed  Google Scholar 

  • Witt MJ, Akesoon S, Broderick AC, Coyne MS, Ellick J, Formia A, Hays GC, Luschi P, Stroud S, Godley BJ (2010) Assessing accuracy and utility of satellite-tracking data using Argos-linked Fastloc-GPS. Anim Behav 80:571–581

    Article  Google Scholar 

  • Witzell WN (1987) Selective predation on large cheloniid sea turtles by tiger sharks (Galeocerdo cuvier). Jpn J Herpetol 12:22–29

    Google Scholar 

Download references

Acknowledgments

We thank J. Rumney from Eye to Eye Marine Encounters and the crew of Undersea Explorer for help with data acquisition. Thanks also to Emily Nelson, Julia Whidden, and Rachel Skubel for helping with formatting and proof editing the manuscript. Thanks to the editor and reviewers, whose comments helped significantly strengthen this paper.

Author information

Authors and Affiliations

  1. Rosenstiel School of Marine and Atmospheric Science, University of Miami, 4600 Rickenbacker Causeway, Miami, FL, 33149, USA

    Neil Hammerschlag & Austin J. Gallagher

  2. Leonard and Jayne Abess Center for Ecosystem Science and Policy, University of Miami, Coral Gables, FL, USA

    Neil Hammerschlag & Austin J. Gallagher

  3. Queensland Department of Environment and Heritage Protection, Townsville, QLD, Australia

    Ian Bell

  4. College of Marine and Environmental Sciences, James Cook University, Townsville, Qld, Australia

    Richard Fitzpatrick & Adam Barnett

  5. Beneath the Waves, Incorporated, Syracuse, NY, USA

    Austin J. Gallagher

  6. Centre for Ecology & Conservation, University of Exeter, Cornwall, UK

    Lucy A. Hawkes

  7. Australian Institute of Marine Science, c/o UWA Oceans Institute, Crawley, WA, Australia

    Mark G. Meekan & Michele Thums

  8. CSIRO Marine and Atmospheric Research, Hobart, TAS, Australia

    John D. Stevens

  9. Environment and Sustainability Institute, University of Exeter, Cornwall, UK

    Matthew J. Witt

  10. TropWATER (Centre for Tropical Water and Aquatic Ecosystem Research), James Cook University, Townsville, QLD, Australia

    Adam Barnett

Authors
  1. Neil Hammerschlag
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ian Bell
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Richard Fitzpatrick
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Austin J. Gallagher
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lucy A. Hawkes
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mark G. Meekan
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. John D. Stevens
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Michele Thums
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Matthew J. Witt
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Adam Barnett
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Neil Hammerschlag.

Ethics declarations

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. Research was approved and conducted under Australian Fisheries Management Authority Scientific Permit #901193 and Great Barrier Reef Marine Park Authority G11/33231.1. Funding was supplied by Digital Dimensions, Australia, through the production of documentaries related to shark research. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. All authors confirm no conflict of interest or competing interests with respect to this study.

Additional information

Communicated by C. M. Garcia

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hammerschlag, N., Bell, I., Fitzpatrick, R. et al. Behavioral evidence suggests facultative scavenging by a marine apex predator during a food pulse. Behav Ecol Sociobiol 70, 1777–1788 (2016). https://doi.org/10.1007/s00265-016-2183-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-016-2183-2

Keywords

search

Navigation