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Environmental Influences on Long-term Movement Patterns of a Euryhaline Elasmobranch (Carcharhinus leucas) Within a Subtropical Estuary

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Abstract

It is well established that juvenile bull sharks (Carcharhinus leucas) use rivers and estuaries as nursery areas; however, there is a large degree of variation in habitat preference (with respect to salinity and distance upstream) between studies at national and international scales. To investigate habitat preference and the influence of water quality on movement of bull sharks, we monitored 36 juveniles using an array of acoustic receivers in the Logan and Albert Rivers, Australia, for 30 months. Acoustic data were used to estimate mean daily distance upstream, and generalized additive models were used to determine the influence of flow, salinity, temperature, dissolved oxygen, turbidity, and chlorophyll a on movement. A model that included flow, salinity, dissolved oxygen, and chlorophyll a explained 89% of the variance. Movement was tightly correlated to both flow and salinity with sharks moving downstream in response to increasing flow/declining salinity and upstream during low flow/increasing salinity. During periods of negligible flow and stable salinity, animals moved upstream and downstream in response to decreasing and increasing dissolved oxygen, respectively. Dissolved oxygen and temperature were strongly negatively correlated and interchangeable within the model. Despite fluctuations in environmental salinity (0–32 psu) and a strong declining gradient in salinity with increasing distance upstream, bull sharks remained within a narrow band of salinity (6–10 psu) throughout the tracking period. The results of this study indicate that habitat choice by juvenile bull sharks is a complex tradeoff between physiology, food availability, and predator avoidance, resulting in large differences between adjacent systems and more broadly across their range.

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References

  • Bass, A. J. D., J. D. D’Aubrey, and N. Kistnasamy. 1973. Sharks of the east coast of southern Africa. 1. The genus Carcharhinus (Carcharhinidae). Oceanographic Research Institute Investigational Report No. 33. Durban, South Africa, 168 pp.

  • Boeuf, G., and P. Payan. 2001. How should salinity influence fish growth? Comparative Biochemistry and Physiology C 130 (4): 411–423. https://doi.org/10.1016/S1532-0456(01)00268-X.

    Article  CAS  Google Scholar 

  • BOM, 2013. Australian Government - Bureau of Meteorology. Special Climate Statement 44: Extreme rainfall and flooding in coastal Queensland and New South Wales. http://www.bom.gov.au/climate/current/statements/scs44.pdf. Accessed Sep 2019

  • Carlson, J.K., M.M. Ribera, C.L. Conrath, M.R. Heupel, and G.H. Burgess. 2010. Habitat use and movement patterns of bull sharks Carcharhinus leucas determined using pop-up satellite archival tags. Journal of Fish Biology 77: 661–675. https://doi.org/10.1111/j.1095-8649.2010.02707.x.

    Article  CAS  Google Scholar 

  • Christensen, F., B. Illing, N.S. Iversen, J.L. Johansen, P. Domenici, and J.F. Steffensen. 2018. Effects of salinity on swimming performance and oxygen consumption rate of shiner perch Cymatogaster aggregata. Journal of Experimental Marine Biology and Ecology 504: 32–37. https://doi.org/10.1016/j.jembe.2018.04.002.

    Article  CAS  Google Scholar 

  • Compagno, L.J.V., and S.F. Cook. 1995. The exploitation and conservation of freshwater elasmobranchs: Status of taxa and prospects for the future. In: The biology of freshwater elasmobranchs. A symposium to honour Thomas B. Thorson, ed. M. Oetinger, G. D. Zorzi. Journal of Aquariculture and Aquatic Science 7: 62–90.

    Google Scholar 

  • Compagno, L. J. V., and V. H. Niem. 1998. Carcharhinidae. In: Species identification guide for fishery purposes. The living marine resources of the Western Central Pacific. Volume 2. Cephalopods, crustaceans, holothurians and sharks, ed. K. E. Carpenter, V. H. Niem, 1312-1360. Rome: Food and Agriculture Organization of the United Nations.

  • Compagno, L.J.V., W.T. White, and P.R. Last. 2008. Glyphis garricki sp. nov., a new species of river shark (Carcharhiniformes: Carcharhinidae) from northern Australia and Papua New Guinea, with a redescription of Glyphis glyphis (Müller and Henle, 1839). In Descriptions of new Australian chondrichthyans, CSIRO Marine and Atmospheric Research Paper 022, ed. P.R. Last, W.T. White, and J.J. Pogonoski, 203–225. Hobart.

  • Cortés, E. 2000. Life history patterns and correlations in sharks. Reviews in Fisheries Science 8 (4): 299–344. https://doi.org/10.1080/10408340308951115.

    Article  Google Scholar 

  • Daly, R., M.J. Smale, P.D. Cowley, and P.W. Froneman. 2014. Residency patterns and migration dynamics of adult bull sharks (Carcharhinus leucas) on the east coast of southern Africa. PLoS One 9 (10): e109357. https://doi.org/10.1371/journal.pone.0109357.

    Article  CAS  Google Scholar 

  • Dennison, W. C., and E. G. Abal. 1999. Moreton Bay study. A scientific basis for healthy waterways campaign. Brisbane: South East Queensland Regional Water Quality Management Strategy, Healthy Waterways.

  • Dulvy, N.K., and R.E. Forrest. 2010. Life histories, population dynamics, and extinction risks in chondrichthyans. In Sharks and their Relatives II: Biodiversity, Adaptive Physiology, and Conservation, ed. J.C. Carrier, J.A. Musick, and M.R. Heithaus, 635–676. Boca Raton: CRC Press.

    Google Scholar 

  • Dulvy, N.K., S.L. Fowler, J.A. Musick, R.D. Cavanagh, P.M. Kyne, L.R. Harrison, J.K. Carlson, L.N. Davidson, S.V. Fordham, M.P. Francis, C.M. Pollock, C.A. Simpfendorfer, G.H. Burgess, K.E. Carpenter, L.J.V. Compagno, D.A. Ebert, C. Gibson, M.R. Heupel, S.R. Livingstone, J.C. Sanciango, J.D. Stevens, S. Valenti, and W.T. White. 2014. Extinction risk and conservation of the world’s sharks and rays. Elife 3: e00590. https://doi.org/10.7554/eLife.00590.

    Article  Google Scholar 

  • Ern, R., D.T.T. Huong, N.V. Cong, M. Bayley, and T. Wang. 2014. Effect of salinity on oxygen consumption in fishes: A review. Journal of Fish Biology. 84 (4): 1210–1220. https://doi.org/10.1111/jfb.12330.

    Article  CAS  Google Scholar 

  • Evans, D.H., and J.B. Claiborne. 2008. Osmotic and Ionic Regulation in Fishes. In Osmotic and Ionic Regulation: Cells and Animals, ed. D.H. Evans, 295–346. Boca Raton: CRC Press.

    Google Scholar 

  • Gibbes, B., A. Grinham, D. Neil, A. Olds, P. Maxwell, R. Connolly, T. Weber, N. Udy, and J. Udy. 2014. Moreton Bay and its estuaries: A sub-tropical system under pressure from rapid population growth. In Estuaries of Australia in 2050 and Beyond. Estuaries of the World, ed. E. Wolanski, 203–222. Dordrecht: Springer.

    Google Scholar 

  • Harding, D.J., R.G. Dwyer, T.M. Mullins, M.J. Kennard, R.D. Pillans, and D.T. Roberts. 2017. Migration patterns and estuarine aggregations of a catadromous fish, Australian bass (Percalates novemaculeata) in a regulated river system. Marine and Freshwater Research 68 (8): 1544–1553. https://doi.org/10.1071/MF16125.

    Article  Google Scholar 

  • Hazon, N., A. Wells, R.D. Pillans, J.P. Good, W.G. Anderson, and C.E. Franklin. 2003. Urea based osmoregulation and endocrine control in elasmobranch fish with special reference to euryhalinity. Comparative Biochemistry and Physiology Part B 136 (4): 685–700. https://doi.org/10.1016/S1096-4959(03)00280-X.

    Article  CAS  Google Scholar 

  • Heithaus, M.R., B.K. Delius, A.J. Wirsing, and M.M. Dunphy-Daly. 2009. Physical factors influencing the distribution of a top predator in a subtropical oligotrophic estuary. Limnology and Oceanography 54 (2): 472–482. https://doi.org/10.4319/lo.2009.54.2.0472.

    Article  CAS  Google Scholar 

  • Heupel, M.R., and R.E. Hueter. 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 (2): 543–550. https://doi.org/10.1071/MF01132.

    Article  Google Scholar 

  • Heupel, M.R., and C.A. Simpfendorfer. 2008. Movement and distribution of young bull sharks Carcharhinus leucas in a variable estuarine environment. Aquatic Biology 277: 277–289. https://doi.org/10.3354/ab00030.

    Article  Google Scholar 

  • Heupel, M.R., and C.A. Simpfendorfer. 2011. Estuarine nursery areas provide a low-mortality environment for young bull sharks Carcharhinus leucas. Marine Ecology Progress Series 433: 237–244. https://doi.org/10.3354/meps09191.

    Article  Google Scholar 

  • Heupel, M.R., C.A. Simpfendorfer, and R.E. Hueter. 2003. Running before the storm: Blacktip sharks respond to falling barometric pressure associated with Tropical Storm Gabrielle. Journal of Fish Biology 63 (5): 1357–1363. https://doi.org/10.1046/j.1095-8649.2003.00250.x.

    Article  Google Scholar 

  • IPCC. 2014. Climate Change 2014: Impacts, adaptation, and vulnerability. In: Part A: Global and sectoral aspects. In Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change, ed. C.B. Field, V.R. Barros, D.J. Dokken, M.J. Mach, M.D. Mastrandrea, T.D. Bilir, M. Chatterjee, K.L. Ebi, Y.O. Estrada, R.C. Genova, B. Girma, E.S. Kissel, A.N. Levy, S. MacCracken, P.R. Mastrandrea, and L.L. White, 1132. United Kingdom: Cambridge University Press.

    Google Scholar 

  • Last, P.R., and J.D. Stevens. 2009. Sharks and rays of Australia. Collingwood: CSIRO Publishing.

    Google Scholar 

  • Ley, J.A., T.A. Halliday, A.J. Tobin, R.N. Garrett, and N.A. Gribble. 2002. Ecosystem effects of fishing closures in mangrove estuaries of tropical Australia. Marine Ecology Progress Series 245: 223–238. https://doi.org/10.3354/meps245223.

    Article  Google Scholar 

  • Lyon, B.L., R.G. Dwyer, R.D. Pillans, H.D. Campbell, and E.F. Franklin. 2017. Distribution, seasonal movements and habitat utilisation of an endangered shark, Glyphis glyphis from northern Australia. Marine Ecology Progress Series 573: 203–213. https://doi.org/10.3354/meps12200.

    Article  Google Scholar 

  • Martin, R.A. 2005. Conservation of freshwater and euryhaline elasmobranchs: A review. Journal of the Marine Biological Association of the United Kingdon 85 (5): 1049–1073. https://doi.org/10.1017/S0025315405012105.

    Article  Google Scholar 

  • Matich, P., and M.R. Heithaus. 2012. Effects of an extreme temperature event on the behavior and age structure of an estuarine top predator, Carcharhinus leucas. Marine Ecology Progress Series 447: 165–178. https://doi.org/10.3354/meps09497.

    Article  Google Scholar 

  • Matveev, V.F., and A.D.L. Steven. 2014. The effects of salinity, turbidity and flow on fish biomass estimated acoustically in two tidal rivers. Marine and Freshwater Research 65 (3): 267–274. https://doi.org/10.1071/MF12266.

  • McAuley, R.B. Simpfendorfer, C.A. Hyndes, G.A. Lenanton, R.C.J. (2007) Distribution and reproductive biology of the sandbar shark, Carcharhinus plumbeus (Nardo), in Western Australian waters. Marine and Freshwater Research 58 (1):116

  • Musick, J.A. 1999. Criteria to define extinction risk in marine fishes: The American Fisheries Society Initiative. Fisheries 24 (12): 6–14. https://doi.org/10.1577/1548-8446(1999)024<0006:CTDERI>2.0.CO;2.

    Article  Google Scholar 

  • Piermarini, P.M., and D.H. Evans. 1998. Osmoregulation of the Atlantic stingray (Dasyatis sabina) from the freshwater Lake Jesup of the St. Johns River, Florida. Physiological Zoology 71 (5): 553–560. https://doi.org/10.1086/515973.

    Article  CAS  Google Scholar 

  • Piermarini, P.M., and D.H. Evans. 2001. Immunochemical analysis of the vacuolar proton-ATPase b-subunit in the gills of a euryhaline stringray (Dasyatis sabina): Effects of salinity and relation to Na+/K+-ATPase. Journal of Experimental Biology and Ecology 204: 3251–3259.

    CAS  Google Scholar 

  • Pillans, R. D. 2006. The physiological ecology of the bull shark Carcharhinus leucas in the Brisbane River. PhD dissertation, The University of Queensland, Brisbane, Australia.

  • Pillans, R.D., and C.E. Franklin. 2004. Plasma osmolyte concentrations and rectal gland mass of bull sharks Carcharhinus leucas, captured along a salinity gradient. Comparative Biochemisty and Physiology A 138 (3): 363–371. https://doi.org/10.1016/j.cbpb.2004.05.006.

    Article  CAS  Google Scholar 

  • Pillans, R.D., J.P. Good, W.G. Anderson, and C.E. Franklin. 2005. Freshwater to seawater acclimation of juvenile Carcharhinus leucas: A comparison of plasma osmolytes and Na+/K+-ATPase activity in gill, rectal gland, kidney and intestine. Journal of Comparative Physiology and Biochemistry 175 (1): 37–44. https://doi.org/10.1007/s00360-004-0460-2.

    Article  CAS  Google Scholar 

  • Pillans, R.D., W.G. Anderson, J.P. Good, S. Hyodo, Y. Takei, N. Hazon, and C.E. Franklin. 2006. Plasma and erythrocyte solute properties of juvenile bull sharks, Carcharhinus leucas, acutely exposed to increasing environmental salinity. Journal of Experimental Biology and Ecology 331 (2): 145–157. https://doi.org/10.1016/j.jembe.2005.10.013.

    Article  CAS  Google Scholar 

  • Pillans, R.D., W.G. Anderson, J.P. Good, N. Hazon, and C.E. Franklin. 2008. Rectal gland morphology of freshwater and seawater acclimated bull sharks Carcharhinus leucas. Journal of Fish Biology 72 (7): 1559–1571. https://doi.org/10.1111/j.1095-8649.2008.01765.x.

    Article  Google Scholar 

  • Pillans, R.D., J.D. Stevens, P.M. Kyne, and J. Salini. 2009. Observations on the distribution, biology, short-term movements and habitat requirements of river sharks Glyphis spp. in northern Australia. Endangered Species Research 10: 321–332. https://doi.org/10.3354/esr00206.

    Article  Google Scholar 

  • Reilly, B.D., R.L. Cramp, J.M. Wilson, H.A. Campbell, and C.E. Franklin. 2011. Branchial osmoregulation in the euryhaline bull shark, Carcharhinus leucas: A molecular analysis of ion transporters. Journal of Experimental Biology 214: 2883–2895. https://doi.org/10.3354/esr00206.

    Article  CAS  Google Scholar 

  • Robertson, J.D. 1975. Osmotic constituents of blood-plasma and parietal muscle of Squalus-acanthias. L. Biological Bulletin 148 (2): 303–319. https://doi.org/10.2307/1540549.

    Article  CAS  Google Scholar 

  • Seqwater. 2016. Queensland bulk water supply authority. http://www.seqwater.com.au/water-supply/dam-levels. Accessed 12 August 2019.

  • Shuttleworth, T.J. 1988. Salt and water balance - extrarenal mechanisms. In Physiology of Elasmobranch Fishes, ed. T.J. Shuttleworth, 171–199. Berlin, Heidelberg: Springer-Verlag.

    Google Scholar 

  • Simpfendorfer, C.A., G.A. Freitas, T.R. Wiley, and M.R. Heupel. 2005. Distribution and habitat partitioning of immature bull sharks (Carcharhinus leucas) in a Southwest Florida estuary. Estuaries 28 (1): 78–85. https://doi.org/10.1007/BF02732755.

    Article  Google Scholar 

  • Smith, H.W. 1931. The absorption and excretion of water and salts by the elasmobranch fishes. In: Fresh water Elasmobranchs, ed. H. W. Smith. American Journal of Physiology 98 (2): 279–295. https://doi.org/10.1152/ajplegacy.1931.98.2.279.

    Article  CAS  Google Scholar 

  • Steven, A., and G. Carlin. 2019. TERN supersites water quality data 2019. v2. CSIRO. ftp://ftp.csiro.au/LoganRiver/index2.htm. Accessed 2 August 2019.

  • Steven, A. D. L., J. Hodge, T. Cannard, G. Carlin, H. Franklin, D. McJannet, C. Moeseneder, and R. Searle. 2015. Continuous water quality monitoring on the Great Barrier Reef. In CSIRO Final Report to Great Barrier Reef Foundation. CSIRO.

  • Thorson, T.B. 1976. The status of the Lake Nicaragua shark: An updated appraisal. In Investigations of the Ichthyofauna of Nicaraguan Lakes, ed. T.B. Thorson, 561–574. University of Nebraska-Lincoln: School of Life Sciences.

  • Werry, J., S.Y. Lee, N. Otway, Y. Hu, and W. Sumpton. 2011. A multi-faceted approach for quantifying the estuarine–nearshore transition in the life cycle of the bull shark, Carcharhinus leucas. Marine and Freshwater Research 62 (12): 1421–1431. https://doi.org/10.1071/MF11136.

    Article  Google Scholar 

  • Werry, J.M., S.Y. Lee, C.J. Lemckert, and N.M. Otway. 2012. Natural or artificial? Habitat-use by the bull shark, Carcharhinus leucas. PLoS One 7 (11): e49796. https://doi.org/10.1371/journal.pone.0049796.

    Article  CAS  Google Scholar 

  • Wood, S.N. 2006. Generalized additive models: An introduction with R. Boca Raton: CRC Press.

    Google Scholar 

  • Yeiser, B.G., M.R. Heupel, and C.A. Simpfendorfer. 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 (6): 489–501. https://doi.org/10.1071/MF07181.

    Article  Google Scholar 

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Acknowledgments

Russ Babcock provided valuable input into the design of the study, and M. Haywood and D. Dennis provided assistance to retrieve acoustic receivers. Douglas Harding provided data from upstream detections, and G. Carlin provided data from the fixed water quality monitoring station. Steven Edgar and C. Moeseneder assisted with access to the water quality data.

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  1. CSIRO Oceans and Atmosphere, 306 Carmody Road, St Lucia, Queensland, 4072, Australia

    R. D. Pillans, G. C. Fry & A. D. L. Steven

  2. CSIRO Oceans and Atmosphere, Castray Esplanade, Hobart, Tasmania, 7000, Australia

    T. Patterson

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Communicated by Mark S. Peterson

Electronic Supplementary Material

Supplementary Fig. S1.

(a). QQ plot of deviance residuals against approximate theoretical quantiles of the deviance residual distribution. Points should largely fall along the line if the errors are Gaussian, (b) Histogram of fitted model residuals indicating normality, (c) observed versus fitted variables shows a strong linear relationship along the identity line indicating that the model predicts the observations well across the range of observations. Red line shows intercept of zero and slope of one. (PNG 130 kb)

Supplementary Fig. S2.

(a). Mean (± SD) of temperature, (b) mean (± SD) of dissolved oxygen, (c) mean (± SD) of turbidity and (d) mean (± SD) of chlorophyll a at increasing distance from the mouth of the Logan River to 29 and 33 upstream in the Albert and Logan River. Means were calculated from monthly data collected between March 2012 and January 2015 by the Queensland Governments EHMP program. (PNG 106 kb)

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Pillans, R.D., Fry, G.C., Steven, A.D.L. et al. Environmental Influences on Long-term Movement Patterns of a Euryhaline Elasmobranch (Carcharhinus leucas) Within a Subtropical Estuary. Estuaries and Coasts 43, 2152–2169 (2020). https://doi.org/10.1007/s12237-020-00755-8

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