Marine Biology

, Volume 161, Issue 11, pp 2645–2658 | Cite as

Tiger shark (Galeocerdo cuvier) movement patterns and habitat use determined by satellite tagging in eastern Australian waters

  • Bonnie J. Holmes
  • Julian G. Pepperell
  • Shane P. Griffiths
  • Fabrice R. A. Jaine
  • Ian R. Tibbetts
  • Mike B. Bennett
Original Paper

Abstract

Partial migration is considered ubiquitous among vertebrates, but little is known about the movements of oceanodromous apex predators such as sharks, particularly at their range extents. PAT-Mk10 and SPOT5 electronic tags were used to investigate tiger shark (Galeocerdo cuvier) spatial dynamics, site fidelity and habitat use off eastern Australia between April 2007 and May 2013. Of the 18 tags deployed, 15 recorded information on depth and/or temperature, and horizontal movements. Tracking times ranged between four and 408 days, with two recovered pop-up archival tags allowing 63 days of high-resolution archived data to be analysed. Overall mean proportions of time-at-depth revealed that G. cuvier spent the majority of time-at-depths of <20 m, but undertook dives as deep as 920 m. Tagged sharks occupied ambient water temperatures from 29.5 °C at the surface to 5.9 °C at depth. Deep dives (>500 m) occurred mostly around dawn and dusk, but no definitive daily dive patterns were observed. Horizontal movements were characterised by combinations of resident and transient behaviour that coincided with seasonal changes in water temperature. While the majority of movement activity was focused around continental slope waters, large-scale migration was evident with one individual moving from offshore Sydney, Australia, to New Caledonia (c. 1,800 km) in 48 days. Periods of tiger shark residency outside of Australia’s fisheries management zones highlight the potential vulnerability of the species to unregulated fisheries and the importance of cross-jurisdictional arrangements for species’ management and conservation.

References

  1. Aebischer NJ, Robertson PA, Kenward RE (1993) Compositional analysis of habitat use from animal radio-tracking data. Ecology 74:1313–1325CrossRefGoogle Scholar
  2. Baker JD, Antonelis GA, Fowler CW, York AE (1995) Natal site fidelity in northern fur seals, Callorhinus ursinus. Anim Behav 50:237–247CrossRefGoogle Scholar
  3. Baum JK, Myers RA, Kehler DG, Worm B, Harley SJ, Doherty PA (2003) Collapse and conservation of shark populations in the northwest Atlantic. Science 299:389–392CrossRefGoogle Scholar
  4. Bond ME, Babcock EA, Pikitch EK, Abercrombie DL, Lamb NF, Chapman DD (2012) Reef sharks exhibit site fidelity and higher relative abundance in marine reserves on the Mesoamerican barrier reef. PLoS One 7(3). doi:10.1371/journal.pone.0032983
  5. Brill RW, Holts DB, Chang RKC, Sullivan S, Dewar H, Carey FG (1993) Vertical and horizontal movements of striped marlin (Tetrapturus audax) near the Hawaiian Islands, determined by ultrasonic telemetry, with simultaneous measurement of oceanic currents. Mar Biol 117:567–574CrossRefGoogle Scholar
  6. Broderson J, Nicolle A, Nilsson PA, Skov C, Brönmark C, Hansson L (2011) Interplay between temperature, fish partial migration and trophic dynamics. Oikos 120:1838–1846. doi:10.111/j.1600-0706.2011.19433.x CrossRefGoogle Scholar
  7. Cagnacci F, Focardi S, Heurich M, Stache A, Hewison AJM, Morellet N, Kjellander P, Linnell JDC, Mysterud A, Neteler M, Delucchi L, Ossi F, Urbano F (2011) Partial migration in roe deer,: migratory and resident tactics are end points of a behavioural gradient determined by ecological factors. Oikos 120:1790–1802. doi:10.1111/j.1600-0706.2011.19441.x CrossRefGoogle Scholar
  8. Carey FG, Scharold JV (1990) Movements of blue shark (Prionace glauca) in depth and course. Mar Biol 106:329–342CrossRefGoogle Scholar
  9. Chan RWK (2001) Biological studies on sharks caught off the east coast of New South Wales. PhD thesis. University of New South Wales, AustraliaGoogle Scholar
  10. Chapman BB, Brönmark C, Nilsson J, Hansson L (2011) The ecology and evolution of partial migration. Oikos 120:1764–1775. doi:10.1111/j.1600-0706.2011.20131.x CrossRefGoogle Scholar
  11. Chapman BB, Hulthén K, Broderson J, Nilsson PA, Skov C, Hansson LA, Brönmark C (2012) Partial migration in fishes: causes and consequences. Fish Biol 81:456–478. doi:10.1111/j.1095-8649.2012.03342.x CrossRefGoogle Scholar
  12. CLS (2011) Argos Users Manual. http://www.argos-system.org. Accessed 17 Aug 2011
  13. da Silva C, Kerwath SE, Attwood CG, Thorstad EB, Cowley PD, Okland PD, Wilke CG, Naesje TF (2013) Quantifying the degree of protection afforded by no-take marine reserve on an exploited shark. Africa J Mar Sci 35:57–66. doi:10.2989/1814232X.2013.769911 CrossRefGoogle Scholar
  14. Dingle H (1996) Migration: the biology of life on the move. Oxford University Press, New YorkGoogle Scholar
  15. Dingle H, Drake VA (2007) What is Migration? BioOne 57(2):113–121Google Scholar
  16. Dulvy NK, Jennings S, Rogers SI, Maxwell DL (2006) Threat and decline in fishes: an indicator of marine biodiversity. Can J Fish Aquat Sci 63:1267–1275CrossRefGoogle Scholar
  17. Dulvy NK, Baum JK, Clarke S, Compagno LJV, Cortés E, Domingo A, Fordham S, Fowler S, Francis MP, Gibson C, Martínez J, Musick JA, Soldo A, Stevens JD, Valenti S (2008) You can swim but you can’t hide: the global status and conservation of oceanic pelagic sharks and rays. Aquat Conserv 18:459–482CrossRefGoogle Scholar
  18. 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 LJV, Ebert DA, Gibson C, Heupel MR, Livingstone SR, Sanciangco JC, Stevens JD, Valenti S, White WT (2013) Extinction risk and conservation of the world’s sharks and rays. eLIFE 3. doi:10.7554/eLife.00590
  19. Everett JD, Baird ME, Oke PR, Suthers IM (2012) An avenue of eddies: quantifying the biophysical properties of mesoscale eddies in the Tasman Sea. Geophys Res Lett 39:LI6608. doi:10.1029/2012GL053091
  20. Field IC, Meekan MG, Buckworth RC, Bradshaw CJA (2009) Protein mining the world’s oceans: Australasia as an example of illegal expansion-and-displacement fishing. Fish Fish 10(3):323–328CrossRefGoogle Scholar
  21. Fitzpatrick R, Thums M, Bell I, Meekan MG, Stevens JD, Barnett A (2012) A comparison of the seasonal movements of tiger sharks and green turtles provides insight into their predator-prey relationship. PLoS One 7(12). doi:10.1371/journal.pone.0051927
  22. Forchhammer MC, Post E, Stenseth NC (2002) North Atlantic Oscillation timing of long- and short-distance migration. J Anim Ecol 71:1002–1014CrossRefGoogle Scholar
  23. Gillanders BM, Ferrell DJ, Andrew NL (2001) Estimates of movements and life-history parameters of yellow-tail kingfish (Seriola lalandi): how useful are data from a cooperative tagging programme? Mar Fres Res 52:179–192CrossRefGoogle Scholar
  24. Green M, Ganassin C, Reid D (2009) Report into the NSW shark meshing (bather protection) program. New South Wales, AustraliaGoogle Scholar
  25. 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 26:567–576CrossRefGoogle Scholar
  26. Harris PT, Nichol SL, Anderson TJ, Heap AD (2012) Habitats and Benthos of a Deep-Sea Marginal Plateau, Lord Howe Rise, Australia. In: Harris PT, Baker EK (eds) Seafloor geomorphology as benthic habitat. Elsevier, USA. ISBN: 978-0-12-385140-6Google Scholar
  27. Hazin FHV, Afonso AS, De Castilho PC, Ferreira LC, Rocha BCLM (2013) Regional movements of the tiger shark, Galeocerdo cuvier, off northeastern Brazil: inferences regarding shark attack hazard. Ann Braz Acad Sci 85(3):1053–1062CrossRefGoogle Scholar
  28. 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(1):25–36CrossRefGoogle Scholar
  29. Heithaus MR, Dill LM (2002) Food availability and tiger shark predation risk influence bottlenose dolphin habitat use. Ecology 83(2):480–491CrossRefGoogle Scholar
  30. Heithaus MR, Marshall GJ, Buhleier BM, Dill LM (2001) Employing Crittercam to study habitat use and behavior of large sharks. Mar Ecol Prog Ser 209:307–310CrossRefGoogle Scholar
  31. Heithaus MR, Dill LM, Marshall GJ, Buhleier B (2002) Habitat use and foraging behavior of tiger sharks (Galeocerdo cuvier) in a seagrass ecosystem. Mar Biol 140(2):237–248CrossRefGoogle Scholar
  32. Heithaus MR, Wirsing AJ, Dill LM, Heithaus LI (2007) Long-term movements of tiger sharks satellite-tagged in Shark Bay, Western Australia. Mar Biol 151:1455–1461CrossRefGoogle Scholar
  33. Heithaus MR, Frid A, Wirsing AJ, Worm B (2008) Predicting ecological consequences of marine top predator declines. Trends Ecol Evol 23(4):202–210CrossRefGoogle Scholar
  34. Holdsworth JC, Sippel TJ, Block BA (2009) Near real time satellite tracking of striped marlin (Kajikia audax) movements in the Pacific Ocean. Mar Biol 156:505–514CrossRefGoogle Scholar
  35. Holland KN, Wetherbee BM, Lowe CG, Meyer CG (1999) Movements of tiger sharks (Galeocerdo cuvier) in coastal Hawaiian waters. Mar Biol 134(4):665–673CrossRefGoogle Scholar
  36. 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 129–130:38–45CrossRefGoogle Scholar
  37. Jaine FRA (2013) The movement ecology of the reef manta ray Manta alfredi in eastern Australia. PhD Thesis, The University of Queensland, AustraliaGoogle Scholar
  38. Jorgensen SJ, Reeb CA, Chapple TK, Anderson S, Perle C, Van Sommeran SR, Fritz-Cope C, Brown AC, Klimley AP, Block BA (2010) Philopatry and migration of Pacific white sharks. Proc R Soc B-Biol Sci 277:679–688. doi:10.1098/rspb.2009.1155 CrossRefGoogle Scholar
  39. Kailola PJ, Williams MJ, Stewart PC, Reichelt RE, McNee A, Grieve C (1993) Australian fisheries resource. FRDC, CanberraGoogle Scholar
  40. Klimley AP (1993) Highly directional swimming by scalloped hammerhead sharks, Sphyrna lewini, and subsurface irradiance, temperature, bathymetry, and geomagnetic field. Mar Biol 117:1–22CrossRefGoogle Scholar
  41. Klimley AP, Beavers SC, Curtis TH, Jorgensen SJ (2002) Movements and swimming behaviour of three species of sharks in La Jolla Canyon, California. Environ Biol Fish 63:117–135CrossRefGoogle Scholar
  42. Knip DM, Heupel MR, Simpfendorfer CA (2012) To roam or to home: site fidelity in a tropical coastal shark. Mar Biol 159:1647–1657CrossRefGoogle Scholar
  43. Kohler NE, Turner PA (2001) Shark tagging: a review of conventional methods and studies. Environ Biol Fish 60:191–223CrossRefGoogle Scholar
  44. Lam VYY, Sadovy de Mitcheson Y (2011) The sharks of South East Asia—unknown, unmonitored and unmanaged. Fish Fish 12:51–74. doi:10.1111/j.1467-2979.2010.00383.x CrossRefGoogle Scholar
  45. Lam CH, Nielsen A, Sibert JR (2008) Improving light and temperature based geolocation by unscented Kalman filtering. Fish Res 91:15–25CrossRefGoogle Scholar
  46. Last PR, Stevens JD (2009) Sharks and rays of Australia, 2nd edn. CSIRO Publishing, AustraliaGoogle Scholar
  47. Litvinov F (2007) Fish visitors to seamounts: aggregations of large pelagic sharks above seamounts. Fish Aqua Res Ser 12:202–206Google Scholar
  48. 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(2):203–211CrossRefGoogle Scholar
  49. Lowe CG, Wetherbee BM, Meyer CG (2006) Using acoustic telemetry monitoring techniques to quantify movement patterns and site fidelity of sharks and giant trevally around French Frigate Shoals and Midway Atoll. Atoll Res Bull 543:281–303Google Scholar
  50. Lowry M, Murphy J (2003) Monitoring the recreational gamefish fishery off southeastern Australia. Mar Fresh Res 54:425–434CrossRefGoogle Scholar
  51. Lynch PD, Shertzer KW, Latour RJ (2012) Performance of methods used to estimate indices of abundance for highly migratory species. Fish Res 125–126:27–39. doi:10.1016/j.fishres.2012.02.005 CrossRefGoogle Scholar
  52. Macbeth WG, Geraghty PT, Peddemors VM, Gray CA (2009) Observer-based study of targeted commercial fishing for large shark species in waters off northern New South Wales. Industry and Investment New South Wales, CronullaGoogle Scholar
  53. Maunder MN, Punt AE (2004) Standardizing catch and effort: a review of recent approaches. Fish Res 70:141–159. doi:10.1016/j.fishres.2004.08.002 CrossRefGoogle Scholar
  54. Meyer CG, Clark TB, Papastamatiou YP, Whitney NM, Holland KN (2009) Long-term movement patterns of tiger sharks Galeocerdo cuvier in Hawaii. Mar Ecol Prog Ser 381:223–235CrossRefGoogle Scholar
  55. 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 157:1857–1868CrossRefGoogle Scholar
  56. Meyer CG, O’Malley JM, Papastamatiou YP, Dale JJ, Hutchinson MR, Anderson JM, Royer MA, Holland KN (2014) Growth and maximum size of tiger sharks (Galeocerdo cuvier) in Hawaii. PLoS One 9(1):e84799. doi:10.1371/journalpone.0084799 CrossRefGoogle Scholar
  57. Myers RA, Baum JK, Shepherd TD, Powers SP, Peterson CH (2007) Cascading effects of the loss of apex predatory sharks from a coastal ocean. Science 315:1846–1850CrossRefGoogle Scholar
  58. Mysterud A, Loe LE, Zimmermann B, Bischof R, Veiberg V, Meisingset E (2011) Partial migration in expanding red deer populations in northern latitudes—a role for density dependence? Oikos 120:1817–1825. doi:10.1111/j.1600-0706.2010.19439.x CrossRefGoogle Scholar
  59. Nakamura I, Wantanabe YY, Papastamatiou YP, Katsufumi S, Meyer CG (2011) Yo-yo vertical movements suggest a foraging strategy for tiger sharks Galeocerdo cuvier. Mar Ecol Prog Ser 424:237–246CrossRefGoogle Scholar
  60. Nathan R, Getz WM, Revilla E, Holyoak M, Kadmon R, Saltz D, Smouse PE (2008) A movement ecology paradigm for unifying organismal movement research. Proc Nat Acad 105:19052–19059. doi:10.1073/pnas.0800375105 CrossRefGoogle Scholar
  61. Nielsen A, Bigelow KA, Musyl MK, Sibert JR (2006) Improving light-based geolocation by including sea surface temperature. Fish Ocean 15(4):314–325. doi:10.1111/j.1365-2419.2005.00401.x CrossRefGoogle Scholar
  62. 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
  63. Papastamatiou YP, Cartamil DP, Lowe CG, Meyer CG, Wetherbee BM, Holland KN (2011) Scales of orientation, directed walks and movement path structure in sharks. J Anim Ecol 80:864–874. doi:10.1111/j.1365-2656.2011.01815.x CrossRefGoogle Scholar
  64. Papastamatiou YP, Meyer CG, Carvalho F, Dale JJ, Hutchinson MR, Holland KN (2013) Telemetry and random walk models reveal complex patterns of partial migration in a large marine predator. Ecol Soc Am 94:2595–2606. doi:10.1890/12-2014.1 Google Scholar
  65. Park T (2007) NSW gamefish tournament monitoring. Angling research tournament monitoring program. NSW Department of Primary Industries, CronullaGoogle Scholar
  66. Paterson RA (1990) Effects of long-term anti-shark measures on target and non-target species in Queensland, Australia. Biol Conserv 52:147–159CrossRefGoogle Scholar
  67. Pepperell JG (2008) Monitoring and research on landed fish at game fishing tournaments in NSW. Pepperell Research and Consulting Pty Ltd, AustraliaGoogle Scholar
  68. Pratt HL, Carrier JC (2001) A review of elasmobranch reproductive behaviour with a case study on the nurse shark, Ginglymostoma cirratum. Environ Biol Fish 60(1–3):157–188CrossRefGoogle Scholar
  69. R Core Team (2012) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN: 3-900051-07-0, URL http://www.R-project.org/
  70. Reid DD, Krough M (1992) Assessment of catches from protective shark meshing off New South Wales beaches between 1950 and 1990. Aust J Mar Fres Res 43:283–296. doi:10.1071/MF9920283 CrossRefGoogle Scholar
  71. Reid DD, Robbins WD, Peddemors VM (2011) Decadal trends in shark catches and effort from the New South Wales Shark Meshing Program 1950 to 2010. Mar Fresh Res 62:676–693CrossRefGoogle Scholar
  72. Ridgway KR, Godfrey JS (1997) Seasonal cycle of the East Australian Current. J Geophys Res 102(10):921–936Google Scholar
  73. Rowling K, Hegarty A, Ives M (2010) Status of fisheries resources in NSW 2008/09. NSW Industry and Investment, CronullaGoogle Scholar
  74. Simpfendorfer C (1992) Biology of tiger sharks (Galeocerdo cuvier) caught in the Queensland shark meshing program off Townsville, Australia. Aust J Mar Fres Res 43:33–43. doi:10.1071/MF9920033 CrossRefGoogle Scholar
  75. Simpfendorfer C (2009) Galeocerdo cuvier. The IUCN Red List of Threatened Species. Version 2014.2. www.iucnredlist.org
  76. Sippel T, Holdsworth J, Dennis T, Montgomery J (2011) Investigating behaviour and population dynamics of striped marlin (Kajikia audax) from the southwest Pacific Ocean with satellite tags. PLoS One 6(6). doi:10.1371/journal.pone.0021087
  77. Skov C, Aarestrup K, Baktoft H, Brodersen J, Brönmark C, Hansson L, Nielsen EE, Nielsen T, Nilsson PA (2010) Influences of environmental cues, migration history, and habitat familiarity on partial migration. Behav Ecol 21:1140–1146. doi:10.1093/beheco/arq121 CrossRefGoogle Scholar
  78. Steinberg C (2007) Impacts of climate change on the physical oceanography of the Great Barrier Reef. In: Johnson JE, Marshall PA (eds) Climate change and the great barrier reef. Great Barrier Reef Marine Park Authority and Australian Greenhouse Office, AustraliaGoogle Scholar
  79. Stevens JD (1984) Biological observations on sharks caught by sport fishermen off New South Wales. Aust J Mar Fres Res 35:573–590CrossRefGoogle Scholar
  80. Stevens JD, West GJ, McLoughlin KJ (2000) Movements, recapture patterns, and factors affecting the return rate of carcharhinid and other sharks tagged off northern Australia. Mar Fresh Res 51:127–141CrossRefGoogle Scholar
  81. Tavares R, Ortiz M, Arocha F (2012) Population structure, distribution and relative abundance of the blue shark (Prionace glauca) in the Caribbean Sea and adjacent waters of the North Atlantic. Fish Res 129–130:137–152. doi:10.1016/j.fishres.2012.06.018 CrossRefGoogle Scholar
  82. Vaudo JJ, Wetherbee BM, Harbey G, Nemeth RS, Aming C, Burnie N, Howey-Jordan LA, Shivji MS (2014) Intraspecific variation in vertical habitat use by tiger sharks (Galeocerdo cuvier) in the western North Atlantic. Ecol Evol 4(10):1768–1786CrossRefGoogle Scholar
  83. Weng KC, Boustany AM, Pyle P, Anderson SD, Brown A, Block BA (2007) Migration and habitat of white sharks (Carcharhodon carcharias) in the eastern Pacific Ocean. Mar Biol 152(4):877–894. doi:10.1007/s00227-007-0739-4 CrossRefGoogle Scholar
  84. 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(1):e83249. doi:10.1371/journal.pone.0083249 CrossRefGoogle Scholar
  85. Williams LE (2002) Queensland’s fisheries resources: current conditions and recent trends 1988–2000. Department of Primary Industries, QueenslandGoogle Scholar
  86. Wirsing AJ, Heithaus MR, Dill LM (2006) Tiger shark (Galeocerdo cuvier) abundance and growth in a subtropical embayment: evidence from 7 years of standardized fishing effort. Mar Biol 149:961–968CrossRefGoogle Scholar
  87. Zischke MT, Griffiths SP, Tibbetts IR (2012) Catch and effort from a specialised recreational pelagic sport fishery off eastern Australia. Fish Res 127–128:61–72CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Bonnie J. Holmes
    • 1
  • Julian G. Pepperell
    • 2
  • Shane P. Griffiths
    • 3
  • Fabrice R. A. Jaine
    • 4
    • 5
  • Ian R. Tibbetts
    • 6
  • Mike B. Bennett
    • 7
  1. 1.School of Biological SciencesThe University of QueenslandSt LuciaAustralia
  2. 2.Pepperell Research and Consulting Pty LtdNoosaville BCAustralia
  3. 3.CSIRO Oceans and Atmosphere FlagshipBrisbaneAustralia
  4. 4.Biophysical Oceanography Group, School of Geography, Planning and Environmental ManagementThe University of QueenslandSt LuciaAustralia
  5. 5.Manta Ray and Whale Shark Research CentreMarine Megafauna FoundationTofo BeachMozambique
  6. 6.School of Biological SciencesThe University of QueenslandSt LuciaAustralia
  7. 7.School of Biomedical SciencesThe University of QueenslandSt LuciaAustralia

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