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Article << Previous     |     Next >>   Contents Vol 62(12)

A multi-faceted approach for quantifying the estuarine–nearshore transition in the life cycle of the bull shark, Carcharhinus leucas

J. M. Werry A B F, S. Y. Lee A, N. M. Otway C, Y. Hu D and W. Sumpton E

A Australian Rivers Institute and School of Environment, Griffith University Gold Coast campus, Qld 4222, Australia.
B Ocean and Coast Research, PO Box 299, Main Beach, Qld 4217, Australia.
C Department of Primary Industries, Port Stephens Fisheries Institute, Taylors Beach, NSW 2316, Australia.
D Advanced Analytical Centre, James Cook University, Townsville, Qld 4810, Australia.
E Queensland Department of Employment, Economic Development and Innovation, Southern Fisheries Centre, PO Box 76, Deception Bay Queensland, Australia.
F Corresponding author. Email: jwerry@oc-research.com

Marine and Freshwater Research 62(12) 1421-1431 http://dx.doi.org/10.1071/MF11136
Submitted: 15 June 2011  Accepted: 3 September 2011   Published: 2 November 2011

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Understanding the ontogenetic habitat linkages of sharks is important for conservation and managing human interactions. We used acoustic telemetry, catch data, elemental and stable isotope signatures and dietary analyses to investigate ontogenetic habitat use in south-east Queensland, Australia, by the bull shark Carcharhinus leucas, a IUCN ‘near-threatened’ species that is implicated in many shark attacks on humans in urban estuaries. Sequential analyses for δ15N and δ13C of vertebrae from five adult C. leucas and laser ablation inductively coupled plasma mass spectrometry (LA-ICPMS) for elemental composition from 23 C. leucas, including a pregnant female, were also used to trace ontogenetic habitat dependence. Acoustic telemetry indicated large juvenile and subadult C. leucas remained in estuarine habitats. δ15N values across shark vertebrae showed an ontogenetic shift in diet with total length (TL), confirmed by stomach contents. LA-ICPMS data reflected the ontogenetic movements of C. leucas from natal habitats. Differences among adults were gender related. Shifts in habitat use by subadults were correlated with a sigmoidal δ13C relationship with TL. C. leucas have a multipartite, stage-specific dependency in their transition between habitats along the freshwater–estuarine–marine continuum, making them particularly susceptible to the habitat alteration that is occurring globally.

Additional keywords: acoustic telemetry, LA-ICPMS elemental analysis, ontogenetic habitat shift, stable isotope analysis.


Bass, A. J., D’Aubrey, J. D., and Kitnasamy, N. (1973). Sharks of the east coast of Southern Africa. I. Genus Carcharhinus (Carcharhinidae). Oceanographic Research Institute Investigational Report 33, 1–168.

Bruce, B. D., Stevens, J. D., and Malcolm, H. (2006). Movements and swimming behaviour of white sharks (Carcharodon carcharias) in Australian waters. Marine Biology 150, 161–172.
CrossRef |

Brunnschweiler, J. M., Queiroz, N., and Sims, D. W. (2010). Oceans apart? Short-term movements and behaviour of adult bull sharks Carcharhinus leucas in Atlantic and Pacific Oceans determined from pop-off satellite archival tagging. Journal of Fish Biology 77, 1343–1358.
CrossRef | CAS |

Cavanagh, R., Kyne, P., Fowler, S. L., Musick, J. A., and Bennett, M. B. (2003). The conservation status of Australasian chondrichthyans. Report of the IUCN Shark Specialist Group Australia and Oceania Regional Red List workshop, 7–9 March 2003, University of Queensland, Brisbane, Australia. Available at http://www.uf.edu/fish/organizations/ssg/region8/Austfinal.pdf [accessed 1 February 2011].

Cliff, G., and Dudley, S. F. J. (1991). Sharks caught in the protective nets off Natal, South Africa. 4. The bull shark Carcharhinus leucas Valenciennes. South African Journal of Marine Science 10, 253–270.
CrossRef |

Coffin, R. B., Cifuentes, L. A., and Elderidge, P. M. (1994). The use of stable carbon isotopes to study microbial processes in estuaries. In ‘Stable Isotopes in Ecology and Environmental Science’. (Eds K. Lajtha and R. H. Michener.) pp. 222–240. (Blackwell Scientific: Oxford.)

Compagno, L. J. (2002). ‘FAO Species Catalogue. Sharks of the World. An Annotated and Illustrated Catalogue of Shark Species Known to Date. Vol. 2. Bullhead, Mackerel and Carpet Sharks (Heterodontiformes, Lamniformes and Orectolobiformes).’ (FAO: Rome.)

Campana, S. E., Natanson, L. J., and Myklevoll, S. (2002). Bomb dating and age determination of large pelagic sharks. Canadian Journal of Fisheries and Aquatic Sciences 59, 450–455.
CrossRef |

Cortés, E. (1997). A critical review of methods of studying fish feeding based on analysis of stomach contents: application to elasmobranch fishes. Canadian Journal of Fisheries and Aquatic Sciences 54, 450–455.
CrossRef |

Cortés, E. (1999). Standardized diet compositions and trophic levels of sharks. ICES Journal of Marine Science 56, 707–717.
CrossRef |

Davenport, S. R., and Bax, N. J. (2002). A trophic study of a marine ecosystem off southeastern Australia using stable isotopes of carbon and nitrogen. Canadian Journal of Fisheries and Aquatic Sciences 59, 514–530.
CrossRef |

Ebert, D. A. (2002). Ontogenetic changes in the diet of the sevengill shark (Notorynchus cepediantus). Marine and Freshwater Research 53, 517–523.
CrossRef |

Estrada, J. A., Rice, A. N., Natanson, L. J., and Skomal, G. B. (2006). Use of isotopic analysis of vertebrae in reconstructing ontogenetic feeding ecology in white sharks. Ecology 87, 829–834.
CrossRef |

Fry, B. (2006). ‘Stable Isotope Ecology.’ (Springer: New York.)

Gillanders, B. M. (2005). Using elemental chemistry of fish otoliths to determine connectivity between estuarine and coastal habitats. Estuarine, Coastal and Shelf Science 64, 47–57.
CrossRef |

Gillanders, B. M., and Kingsford, M. J. (2000). Elemental fingerprints of otoliths may distinguish estuarine ‘nursery’ habitats. Marine Ecology Progress Series 201, 273–286.
CrossRef | CAS |

Gillanders, B. M., Able, K. W., Brown, J. A., Eggleston, D. B., and Sheridan, P. F. (2003). Evidence of connectivity between juvenile and adult habitats for mobile marine fauna: an important component of nurseries. Marine Ecology Progress Series 247, 281–295.
CrossRef |

Hale, L., Dudgeon, J., Mason, A., and Lowe, C. (2006). Elemental signatures in the vertebral cartilage of the round stingray, Urobatis halleri, from Seal Beach, California. Environmental Biology of Fishes 77, 317–325.
CrossRef |

Hart, P. J. B. (1997). Foraging tactics. In ‘Behavioural Ecology of Teleost Fishes’. (Ed. J. G. J. Godin.) pp. 104–133. (Oxford University Press: Oxford.)

Heithaus, M. R. (2004). Predator–prey interactions. In ‘Biology of Sharks and Their Relatives’. (Eds J.C. Carrier, J.A. Musick and M.R. Heithaus.) pp. 487–522 (CRC Press: Florida.)

Heithaus, M. R., Dill, L. M., Marshall, G. J., and Buhleier, B. (2002). Habitat use and foraging behaviour of tiger sharks (Galeocerdo cuvier) in a seagrass ecosystem. Marine Biology 140, 237–248.
CrossRef |

Heithaus, M. R., Frid, A., Wirsing, A. J., Bejder, L., and Dill, L. (2005). Biology of sea turtles under risk from tiger sharks at a foraging ground. Marine Ecology Progress Series 288, 285–294.
CrossRef |

Heithaus, M. R., Delius, B. K., Wirsing, A. J., and Dunphy-Daly, M. M. (2009). Physical factors influencing the distribution of a top predator in a subtropical oligotrophic estuary. Limnology and Oceanography 54, 472–482.
CrossRef | CAS |

Heupel, M. R., and Hueter, R. E. (2002). Importance of prey density in relation to the movement patterns of juvenile blacktip sharks (Carcharhinus limbatus) within a coastal nursery area. Marine and Freshwater Research 53, 543–550.
CrossRef |

Heupel, M. R., and Simpfendorfer, C. A. (2008). Movement and distribution of young bull sharks Carcharhinus leucas in a variable estuarine environment. Aquatic Biology 1, 277–289.
CrossRef |

Heupel, M. R., Simpfendorfer, C. A., and Hueter, R. E. (2004). Estimation of shark home ranges using passive monitoring techniques. Environmental Biology of Fishes 71, 135–142.
CrossRef |

Heupel, M. R., Yeiser, B. G., Collins, A. B., Ortega, L., and Simpfendorfer, C. A. (2010). Long-term presence and movement patterns of juvenile bull sharks, Carcharhinus leucas, in an estuarine river system. Marine and Freshwater Research 61, 1–10.
CrossRef | CAS |

Hight, B. V., and Lowe, C. G. (2007). Elevated body temperatures of adult female leopard sharks, Triakis semifasciata, while aggregating in shallow nearshore embayments: evidence for behavioural thermoregualtion? Journal of Experimental Marine Biology and Ecology 352, 114–128.
CrossRef |

Hopkins, T. E., and Cech, J. J. (2003). The influence of environmental variables on the distribution and abundance of three elasmobranchs in Tomales Bay, California. Environmental Biology of Fishes 66, 279–291.
CrossRef |

IUCN (2008). Carcharhinus leucas IUCN (International Union for Conservation of Nature) Red list of threatened species. Available at www.iucnredlist.org [accessed 15 March 2010].

Jensen, N. H. (1976). Reproduction of the bull shark, Carcharhinus leucas, in the Lake Nicaragua Rio San Juan system. In ‘Investigation of the Icthyofauna of Nicaraguan Lakes’. (Ed. T. B. Thorson.) pp. 539–559. (University of Nebraska Press: Lincoln, NE.)

Kennedy, H., Beggins, J., Duarte, C. M., Fourqurean, J. W., Holmer, M., Marbà, N., and Middelburg, J. J. (2010). Seagrass sediments as a global carbon sink: isotopic constraints. Global Biogeochemical Cycles 24, GB4026.
CrossRef |

Kerr, L., Andrews, A., Cailliet, G., Brown, T., and Coale, K. (2006). Investigations of Δ14C, δ13C, and δ15N in vertebrae of white shark (Carcharodon carcharias) from the eastern North Pacific Ocean. Environmental Biology of Fishes 77, 337–353.
CrossRef |

Knip, D. M., Heupel, M. R., Simpfendorfer, C. A., Tobin, A. J., and Moloney, J. (2011). Ontogenetic shifts in movement and habitat use of juvenile pigeye sharks Carcharhinus amboinensis in a tropical nearshore region. Marine Ecology Progress Series 425, 233–246.
CrossRef |

Last, P. R., and Stevens, J. D. (2009). ‘Sharks and Rays of Australia.’ (CSIRO Publishing: Melbourne.)

Lin, H. S., Kao, W. Y., and Wang, Y. T. (2007). Analyses of stomach contents and stable isotopes reveal food sources of estuarine detritvorous fish in tropical/subtropical Taiwan. Estuarine, Coastal and Shelf Science 73, 527–537.
CrossRef |

Loneragan, N. R., and Bunn, S. E. (1999). River flows and estuarine ecosystems: implications for coastal fisheries from a review and a case study of the Logan River, southeast Queensland. Australian Journal of Ecology 24, 431–440.
CrossRef |

Macpherson, E. (1998). Ontogenetic shifts in habitat-use and aggregation in juvenile sparid fishes. Journal of Experimental Marine Biology and Ecology 220, 127–150.
CrossRef |

McCord, M. E., and Lamberth, S. J. (2009). Catching and tracking the world’s largest Zambezi (bull) shark Carcarhinus leucas in the Breede Estuary, South Africa: the first 43 hours. African Journal of Marine Science 31, 107–111.
CrossRef |

McCutchan, J. H., Lewis, W. M., Kendall, C., and McGrath, C. C. (2003). Variation in trophic shift for stable isotope ratios of carbon, nitrogen and sulphur. Oikos 102, 378–390.
CrossRef | CAS |

Merson, R. R., and Pratt, H. L. (2001). Distribution, movements and growth of young sandbar, Carcharhinus plumbeus, in the nursery grounds of Delaware Bay. Environmental Biology of Fishes 61, 13–24.
CrossRef |

Myers, R. A., Baum, J. K., Shepherd, T. D., Powers, S., and Peterson, C. H. (2007). Cascading effects of the loss of apex predatory sharks from a coastal ocean. Science 315, 1846–1850.
CrossRef | CAS |

Olsen, Y. S., Fox, S. E., Teichberg, M., Otter, M., and Valiela, I. (2011). δ15N and δ13C reveal differences in carbon flow through estuarine benthic food webs in response to the relative availability of macroalgae and eelgrass. Marine Ecology Progress Series 421, 83–96.
CrossRef |

Pillans, R. D., and Franklin, C. E. (2004). Plasma osmolyte concentrations and rectal gland mass of bull sharks Carcharhinus leucas, captured along a salinity gradient. Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology 138, 363–371.
CrossRef |

Pillans, R. D., Andersond, G., Goode, J. P., Hyodof, S., Takeif, Y., Hazone, N., and Franklin, C. E. (2006). Plasma and erythrocyte solute properties of juvenile bull sharks, Carcharhinus leucas, acutely exposed to increasing environmental salinity. Journal of Experimental Marine Biology and Ecology 331, 145–157.
CrossRef | CAS |

Pittman, S. J., and McAlpine, C. A. (2001). Movements of marine fish and decapod crustaceans: process, theory and application. Advances in Marine Biology 44, 205–294.
CrossRef |

Rasalato, E., Maginnity, V., and Brunnschweiler, J. M. (2010). Using local ecological knowledge to identify shark river habitats in Fiji (South Pacific). Environmental Conservation 37, 90–97.
CrossRef |

Sheaves, M. (1995). Large lutjanid and serranid fishes in tropical estuaries: are they adults or juveniles? Marine Ecology Progress Series 129, 31–41.
CrossRef |

Simpfendorfer, C., Freitas, G., Wiley, T., and Heupel, M. (2005). Distribution and habitat partitioning of immature bull sharks (Carcharhinus leucas) in a Southwest Florida estuary. Estuaries and Coasts 28, 78–85.
CrossRef |

Sims, D. W. (2003). Tractable models for testing theories about natural strategies: foraging behaviour and habitat selection of free ranging sharks. Journal of Fish Biology 63, 53–73.
CrossRef |

Thorrold, S. R., Latkoczy, C., Swart, P. K., and Jones, G. P. (2001). Natal homing in a marine fish metapopoulation. Science 291, 297–299.
CrossRef | CAS |

Thorson, T. B. (1971). Movement of bull sharks, Carcharhinus leucas, between Caribbean Sea and Lake Nicaragua demonstrated by tagging. Copeia 1971, 336–338.
CrossRef |

Thorson, T. B., Cowan, C. M., and Watson, D. E. (1973). Body fluid solutes of juveniles and adults of the euryhaline bull shark Carcharhinus leucas from freshwater and saline environments. Physiological Zoology 46, 29–42.
| CAS |

Tillett, B. J., Meekan, M. G., Parry, D., Munksgaard, N., Field, I. C., Thorburn, D., and Bradshaw, C. J. A. (2011). Decoding fingerprints: elemental composition of vertebrae correlates to age-related habitat use in two morphologically similar sharks. Marine Ecology Progress Series 434, 133–142.
CrossRef | CAS |

Vanderklift, M. A., and Ponsard, S. (2003). Sources of variation in consumer-diet δ15N enrichment: a meta analysis. Oecologia 136, 169–182.
CrossRef |

Vorenberg, M. M. (1962). Cannibalistic tendencies of lemon and bull sharks. Copeia 1962, 455–456.
CrossRef |

Watsky, M. A., and Gruber, S. H. (1990). Induction and duration of tonic immobility in the lemon shark, Negaprion brevirostris. Fish Physiology and Biochemistry 8, 207–210.
CrossRef |

Werry, J. M. (2010). Habitat ecology of the bull shark, Carcharhinus leucas, on urban coasts in eastern Queensland, Australia. PhD Thesis, Griffith University, Australia.

Wetherbee, B. M., and Cortes, E. (2004). Food consumption and feeding habitats. In ‘ Biology of Sharks and Their Relatives’. (Eds J. C. Carrier, J. A. Musick and M. R. Heithaus.) pp. 225–246. (CRC Press: Boca Raton, FL.)

Yeiser, B. G., Heupel, M. R., and Simpfendorfer, C. A. (2008). Occurrence, home range and movement patterns of juvenile bull (Carcharhinus leucas) and lemon (Negaprion brevirostris) sharks within a Florida estuary. Marine and Freshwater Research 59, 489–501.
CrossRef |

Zeller, B. M. (1999). ‘Bull Shark Carcharhinus leucas Valenciennes in Estuarine and Nearshore Waters of the Gold Coast, Queensland.’ (Department of Primary Industries and Fisheries: Brisbane.)

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