Marine Biology

, Volume 160, Issue 11, pp 2863–2875 | Cite as

The effects of cage-diving activities on the fine-scale swimming behaviour and space use of white sharks

  • Charlie Huveneers
  • Paul J. Rogers
  • Crystal Beckmann
  • Jayson M. Semmens
  • Barry D. Bruce
  • Laurent Seuront
Original Paper

Abstract

Wildlife tourism has become increasingly popular and is one of the fastest growing sectors of the tourism industry. A radio-acoustic positioning system was deployed to monitor the fine-scale movements of 21 white sharks (Carcharodon carcharias) and investigate the effects of shark cage-diving activities on their swimming behaviour and space use. This study contributes towards improving our understanding of the complex relationship between wildlife tourism and its effects on sharks, and assesses how tourism targeting sharks affects behaviour at a finer spatial scale than previously investigated. Our study demonstrated that shark cage-diving operators (SCDO) influenced the fine-scale three-dimensional spatial distribution and the rate of movement of white sharks at the Neptune Islands. White sharks stayed more than 30 m away from the SCDO on 21 % of the days detected, but spent a significant amount of time in close proximity to the SCDO on the remaining days. Individual variation was detected, with some sharks behaviourally responding to SCDO more than others. The degree of variation between individual sharks and the different levels of interaction (e.g. presence, proximity to SCDO, and consumption of tethered bait) highlights the complexity of the relationships between SCDO and the effects on sharks. To improve our understanding of these relationships, future monitoring of shark cage-diving operations requires proximity to SCDO to be recorded in addition to the presence within the area. Further work is needed to assess whether the observed behavioural changes would affect individual fitness and ultimately population viability, which are critical information to unambiguously assess the potential impacts of wildlife tourism targeting sharks.

Supplementary material

227_2013_2277_MOESM1_ESM.docx (285 kb)
Supplementary material 1 (DOCX 284 kb)

References

  1. Ballantyne R, Packer J, Hughes K, Dierking L (2007) Conservation learning in wildlife tourism settings: lessons from research in zoos and aquariums. Environ Educ Res 13:367–383CrossRefGoogle Scholar
  2. Barker SM, Peddemors V, Williamson JE (2011a) Recreational SCUBA diver interactions with the critically endangered Grey Nurse Shark. Pac Conserv Biol 16:261–269Google Scholar
  3. Barker SM, Peddemors V, Williamson JE (2011b) A video and photographic study of aggregation, swimming and respiratory behaviour changes in the Grey Nurse Shark (Carcharias taurus) in response to the presence of SCUBA divers. Mar Freshw Behav Physiol 44:75–92CrossRefGoogle Scholar
  4. Barnett A, Abrantes K, Stevens J, Bruce B, Semmens JM (2010) Fine-Scale movements of the broadnose sevengill shark and its main prey, the gummy shark. PLoS ONE 5:e15464CrossRefGoogle Scholar
  5. Bejder L, Samuels A, Whitehead H, Gales N, Mann J, Connor R, Heithaus M, Watson-Capps J, Flaherty C, Krutzen M (2006) Decline in relative abundance of bottlenose dolphins exposed to long-term disturbance. Conserv Biol 20:1791–1798CrossRefGoogle Scholar
  6. Bonfil R, Meyer M, 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(5745):100–103CrossRefGoogle Scholar
  7. Boustany AM, Davis SF, Pyle P, Anderson SD, Le Boeuf BJ, Block BA (2002) Expanded niche for White Sharks. Nature 415:35–36CrossRefGoogle Scholar
  8. Bruce BD, Bradford RW (2012) Spatial dynamics and habitat preferences of juvenile white sharks in eastern Australia. In: Domeier ML (ed) Global Perspectives on the biology and life history of the great white shark. CRC Press, Boca Raton, pp 225–254CrossRefGoogle Scholar
  9. Bruce BD, Bradford RW (2013) The effects of shark cage-diving operations on the behaviour and movements of white sharks, Carcharodon carcharias, at the Neptune Islands, South Australia. Mar Biol 160:889–907CrossRefGoogle Scholar
  10. Bruce BD, Stevens JD, Bradford RW (2005) Site fidelity, residence times and home range patterns of white sharks around pinniped colonies. Australian Government Department of Environment and Heritage, HobartGoogle Scholar
  11. Bruce BD, Stevens JD, Malcolm H (2006) Movements and swimming behaviour of white sharks (Carcharodon carcharias) in Australian waters. Mar Biol 150:161–172CrossRefGoogle Scholar
  12. Brunnschweiler JM, Barnett A (2013) Opportunistic visitors: long-term behavioural response of bull sharks to food provisioning in Fiji. PLoS ONE 8:e58522CrossRefGoogle Scholar
  13. Buckley R (2004) Impacts of ecotourism on birds. In: Buckley R (ed) Environmental impacts of ecotourism. CAB International, Cambridge, pp 187–209CrossRefGoogle Scholar
  14. Calow P (1979) Adaptive aspects of energy allocation. In: Tyler P, Calow P (eds) Fish energetics: new perspectives. Croom Helm, Kent, pp 13–32Google Scholar
  15. Carey FG, Kanwisher JW, Brazier O, Gabrielson G, Casey JG, Pratt HLJ (1982) Temperature and activities of white shark, Carcharodon carcharias. Copeia 1982:254–260CrossRefGoogle Scholar
  16. Christiansen F, Lusseau D, Stensland E, Berggren P (2010) Effects of tourist boats on the behaviour of Indo-Pacific bottlenose dolphins off the south coast of Zanzibar. Endanger Species Res 11:91–99CrossRefGoogle Scholar
  17. Clua E, Buray N, Legendre P, Mourier J, Planes S (2010) Behavioural response of sicklefin lemon sharks Negaprion acutidens to underwater feeding for ecotourism purposes. Mar Ecol Prog Ser 414:257–266CrossRefGoogle Scholar
  18. Culik BM (1994) Energy requirements of Pygoscelid penguins: a synopsis. Rep Polar Res 150:1–76Google Scholar
  19. DEWHA (2010) Draft recovery plan for the conservation and management of White Sharks (Carcharodon carcharias). Department of the Environment, Water, Heritage and the Arts, ACTGoogle Scholar
  20. Domeier ML, Nasby-Lucas N (2008) Migration patterns of white sharks Carcharodon carcharias tagged at Guadalupe Island, Mexico, and identification of an eastern Pacific shared offshore foraging area. Mar Ecol Prog Ser 370:221–237CrossRefGoogle Scholar
  21. Domeier ML, Nasby-Lucas N, Lam CH (2012) Fine-scale habitat use by white sharks at Guadalupe Island, Mexico. In: Domeier ML (ed) Global perspectives on the biology and life history of the white shark. CRC Press, Boca Raton, pp 121–132CrossRefGoogle Scholar
  22. Driscoll JW (1995) Attitude toward animals: species ratings. Soc Anim 3:139–150CrossRefGoogle Scholar
  23. Duchesne M, Cote SD, Barette C (2000) Responses of woodland caribou to winter ecotourism in the Charlevoix Biosphere Reserve, Canada. Biol Conserv 96:311–317CrossRefGoogle Scholar
  24. Duffus DA, Dearden P (1990) Non-consumptive wildlife oriented recreation: a conceptual framework. Biol Conserv 53:213–231CrossRefGoogle Scholar
  25. Duffy C, Francis MP, Manning MJ, Bonfil R (2012) Regional population connectivity, oceanic habitat, and return migration revealed by satellite tagging of white sharks, Carcharodon carcharias, at New Zealand aggregation sites. In: Domeier ML (ed) Global perspectives on the biology and life history of the white shark. CRC Press, Boca Raton, pp 301–318CrossRefGoogle Scholar
  26. Fay MP (2010) Two-sided exact tests and matching confidence intervals for discrete data. R J 2:53–58Google Scholar
  27. Ferguson K (2006) Submerged realities: shark documentaries at depth. Atenea 26:115–129Google Scholar
  28. Fitzpatrick R, Abrantes KG, Seymour J, Barnett A (2011) Variation in depth of whitetip reef sharks: does provisioning ecotourism change their behaviour? Coral Reefs 30:569–577CrossRefGoogle Scholar
  29. Giese M, Handsworth R, Stephenson R (1999) Measuring resting heart rates in penguins using an artificial egg. J Field Ornithol 70:49–54Google Scholar
  30. Gosling S (2001) From mice to men: what can we learn about personality from animal research. Psychol Bull 127:45–86CrossRefGoogle Scholar
  31. Green R, Giese M (2004) Negative effects of wildlife tourism on wildlife. In: Higginbottom K (ed) Wildlife tourism: impacts, management and planning. Sustainable Tourism Cooperative Research Centre, Gold Coast, pp 81–97Google Scholar
  32. Green RJ, Higginbottom K (2001) Status assessment of wildlife tourism in Australia series: the negative effects of wildlife tourism on wildlife. Wildlife Tourism Research Report CRC for Sustainable Tourism, Gold Coast, QueenslandGoogle Scholar
  33. Higginbottom K, Tribe A (2004) Contributions of wildlife tourism to conservation. In: Higginbottom K (ed) Wildlife tourism: impacts, management and planning. Common Ground Publishing, CRC for Sustainable Tourism, Gold Coast, pp 99–123Google Scholar
  34. Iosilevskii G, Weihs D (2008) Speed limits on swimming of fishes and cetaceans. J R Soc 5:329–338CrossRefGoogle Scholar
  35. Jorgensen SJ, Reeb CA, Chapple TK, Anderson SP, Van Sommeran SRF-C, Brown AC, Klimley AP, Block BA (2009) Philopatry and migration of Pacific White Sharks. Proc R Soc B Biol Sci 277:679–688CrossRefGoogle Scholar
  36. Kerbiriou C, Le Viol I, Robert A, Porcher E, Gourmelon F, Julliard R (2009) Tourism in protected areas can threaten wild populations: from individual response to population viability of the chough Pyrrhocorax pyrrhocorax. J Appl Ecol 46:657–665CrossRefGoogle Scholar
  37. Klimley A, Le Boeuf B, Cantara K, Richert J, Davis S, Van Sommerman S (2001a) Radio acoustic positioning as a tool for studying site-specific behavior of the white shark and other large marine species. Mar Biol 138:429–446CrossRefGoogle Scholar
  38. Klimley AP, Le Boeuf BJ, Cantara K, Richert J, Davis SF, Van Sommerman S, Kelly JT (2001b) The hunting strategy of white sharks (Carcharodon carcharias) near a seal colony. Mar Biol 138:617–636CrossRefGoogle Scholar
  39. Klimley AP, Beavers SC, Curtis TH, Jorgensen SJ (2002) Movements and swimming behavior of three species of sharks in La Jolla Canyon, California. Environ Biol Fishes 63:117–135CrossRefGoogle Scholar
  40. Knight RL, Cole DN (1995) Factors that influence wildlife responses to recreationists. In: Knight RL, Gutzwiller KJ (eds) Wildlife and recreationists: coexistence through management and research. Island Press, Washington, pp 71–80Google Scholar
  41. Koolhaas J, Korte S, De Boer S, Van Der Vegt B, Van Reenen C, Hopster H, De Jong I, Ruis M, Blokhuis H (1999) Coping styles in animals: current status in behavior and stress-physiology. Neurosci Behav Rev 23:925–935CrossRefGoogle Scholar
  42. Laroche KR, Kock AA, Dill LM, Oosthuizen H (2007) Effects of provisioning ecotourism activity on the behaviour of white sharks Carcharodon carcharias. Mar Ecol Prog Ser 338:199–209CrossRefGoogle Scholar
  43. Laroche KR, Kock AA, Dill LM, Oosthouizen WH (2008) Running the gauntlet: a predator-prey game between sharks and two age classes of seals. Anim Behav 76:1901–1917CrossRefGoogle Scholar
  44. Le Boeuf BJ (2004) Hunting and migratory movements of white sharks in the eastern North Pacific. Memoirs Natl Inst Polar Res 58:89–100Google Scholar
  45. Lott D, McCoy M (1995) Asian Rhinos Rhinoceros unicornis on the run? Impact of tourist visits on one population. Biol Conserv 73:23–26CrossRefGoogle Scholar
  46. Lusseau D, Bain D, Williams R, Smith J (2009) Vessel traffic disrupts the foraging behavior of southern resident killer whales Orcinus orca. Endanger Species Res 6:211–221CrossRefGoogle Scholar
  47. Lynch A-MJ, Sutton SG, Simpfendorfer CA (2010) Implications of recreational fishing for elasmobranch conservation in the Great Barrier Reef Marine Park. Aquat Conserv 20:312–318CrossRefGoogle Scholar
  48. Maljković A, Côté I (2011) Effects of tourism-related provisioning on the trophic signatures and movement patterns of an apex predator, the Caribbean reef shark. Biol Conserv 144:859–865CrossRefGoogle Scholar
  49. Martin JGA, Réale D (2008) Animal temperament and human disturbance: implications for the response of wildlife to tourism. Behav Process 77:66–72CrossRefGoogle Scholar
  50. Martin RA, Rossmo DK, Hammerschlag N (2009) Hunting patterns and geographic profiling of white shark predation. J Zool 279:111–118CrossRefGoogle Scholar
  51. Meyer CG, Dale JJ, Papastamatiou YP, Whitney NM, Holland KN (2009) Seasonal cycles and long-term trends in abundance and species composition of sharks associated with cage diving ecotourism activities in Hawaii. Environ Conserv 36:104–111CrossRefGoogle Scholar
  52. Newsome D, Dowling R, Moore S (2005) Wildlife tourism. Channel View, ClevendonGoogle Scholar
  53. O’Dor RK, Andrade Y, Webber D, Sauer W, Roberts M, Smale M, Voegeli F (1998) Applications and performance of Radio-Acoustic Positioning and Telemetry (RAPT) systems. Hydrobiologia 371:3721–3728Google Scholar
  54. Orams M (2002) Feeding wildlife as a tourism attraction: a review of issues and impacts. Tour Manage 23:281–293CrossRefGoogle Scholar
  55. Robbins RL (2007) Environmental variables affecting the sexual segregation of great white sharks Carcharodon carcharias at the Neptune Islands, South Australia. J Fish Biol 70:1350–1364CrossRefGoogle Scholar
  56. Roes D, Leader-Williams N, Dalal-Clayton B (1997) Take only photographs, leave only footprints: the environmental impacts of wildlife tourism. International Institute for Environment and Development Wildlife and Development Series, vol 10. International Institute for Environment and Development, LondonGoogle Scholar
  57. Scheyvens R (1999) Ecotourism and the empowerment of local communities. Tour Manage 20:245–249CrossRefGoogle Scholar
  58. Semeniuk CAD, Speers-Roesch B, Rothley KD (2007) Using fatty-acid profile analysis as an ecologic indicator in the management of tourist impacts on marine wildlife: a case of stingray-feeding in the Caribbean. Environ Manag 40:665–677CrossRefGoogle Scholar
  59. Semmens JM, Payne N, Huveneers C, Sims DW, Bruce BD (2013) Feeding requirements of white sharks may be higher than originally thought. Sci Rep 3:1471CrossRefGoogle Scholar
  60. Shackley M (1996) Wildlife tourism. International Thomson Business Press, LondonGoogle Scholar
  61. Shaughnessy PD, McKeown A (2002) Trends in abundance of New Zealand fur seals, Arctocephalus fosteri, at the Neptune Islands, South Australia. Wildl Res 29:363–370CrossRefGoogle Scholar
  62. Sih A, Bell A, Johnson JC (2004) Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19:372–378CrossRefGoogle Scholar
  63. Smith K, Scarr M, Scapaci C (2010) Grey nurse shark (Carcharias taurus) diving tourism: tourist compliance and shark behaviour at Fish Rock, Australia. Environ Manag 46:699–710CrossRefGoogle Scholar
  64. Steven R, Pickering C, Castley JG (2011) A review of the impacts of nature based recreation on birds. J Environ Manag 92:2287–2294CrossRefGoogle Scholar
  65. Strong WR, Murphy RC, Bruce BD, Nelson DR (1992) Movements and associated observations of bait-attracted white sharks, Carcharodon carcharias: a preliminary report. Aust J Mar Freshw Res 43:13–20CrossRefGoogle Scholar
  66. Strong WR, Bruce BD, Nelson DR, Murphy RD (1996) Population dynamics of white sharks in Spencer Gulf, South Australia. In: Klimley AP, Ainley DG (eds) Great white sharks: the biology of Carcharadon carcharias. Academic, San Diego, pp 401–414CrossRefGoogle Scholar
  67. Techera EJ, Klein N (2011) Fragmented governance: reconciling legal strategies for shark conservation and management. Mar Policy 35:73–78CrossRefGoogle Scholar
  68. Wearing S, Neil J (2009) Ecotourism: impacts, potentials, and possibilities, 2nd edn. Butterworth-Heinemann, OxfordGoogle Scholar
  69. Weng KC, Boustany AM, Pyle P, Anderson SD, Brown A, Block BA (2007) Migration and habitat of white sharks (Carcharodon carcharias) in the eastern Pacific Ocean. Mar Biol 152:877–894CrossRefGoogle Scholar
  70. Williams R, Lusseau D, Hammond P (2006) Estimating relative energetic costs of human disturbance to killer whales (Orcinus orca). Biol Conserv 133:301–311CrossRefGoogle Scholar
  71. Worlf ID, Croft DB (2010) Minimizing disturbance to wildlife by tourists approaching on foot or in a car: a study of kangaroos in the Australian rangelands. Appl Anim Behav Sci 126:75–84CrossRefGoogle Scholar
  72. Zamora L, Moreno-Amich R (2002) Quantifying the activity and movement of perch in a temperate lake by integrating acoustic telemetry and a geographic information system. Hydrobiologia 483:209–218CrossRefGoogle Scholar

Copyright information

© Her Majesty the Queen in Right of Australia 2013

Authors and Affiliations

  • Charlie Huveneers
    • 1
    • 2
  • Paul J. Rogers
    • 1
  • Crystal Beckmann
    • 2
  • Jayson M. Semmens
    • 3
  • Barry D. Bruce
    • 4
  • Laurent Seuront
    • 2
  1. 1.Threatened, Endangered and Protected Species Sub ProgramSARDI—Aquatic SciencesWest BeachAustralia
  2. 2.School of Biological SciencesFlinders UniversityBedford ParkAustralia
  3. 3.Fisheries, Aquaculture and Coasts CentreInstitute for Marine and Antarctic StudiesHobartAustralia
  4. 4.Wealth from Oceans FlagshipCommonwealth Scientific Institute Research OrganisationHobartAustralia

Personalised recommendations