Log in

A Seasonally Dynamic Estuarine Ecosystem Provides a Diverse Prey Base for Elasmobranchs

  • Published:
Estuaries and Coasts Aims and scope Submit manuscript

Abstract

Tropical river and estuarine food webs sustain diverse biodiversity values and are important sources of nutrients and energy for connected aquatic and terrestrial ecosystems. High-order predators, such as euryhaline elasmobranchs, play critical roles in these food webs, but a lack of detailed information on food web structure limits our ability to manage these species within their ecosystems. We analysed stable carbon (δ13C) and nitrogen (δ15N) isotopes (SI) and fatty acid (FA) biochemical tracers from putative prey species in the estuary of the South Alligator River, northern Australia. These were compared with existing data on four species of elasmobranch from the system to examine food web structure and infer dietary linkages over wet and dry seasons along an environmental gradient of sites. Layman’s SI community metrics indicated that upstream food webs had the greatest trophic diversity, and analyses of FAs revealed distinct prey habitat associations that changed seasonally. Mixing models of SI indicated that most Glyphis glyphis and Glyphis garricki had similar freshwater and mid-river diets whilst Carcharhinus leucas and Rhizoprionodon taylori had largely marine signatures. Multivariate analyses of FA revealed some intraspecific differences, although specialisation indices suggested that the four shark species are trophic generalists. Our results show that riverine food webs can display complex spatiotemporal variations in trophic structure and that coastal and euryhaline mobile elasmobranchs forage in a range of coastal and freshwater habitats, demonstrating their influence on these food webs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

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

Similar content being viewed by others

References

  • Abrantes, Kátya, and Marcus Sheaves. 2009. Food web structure in a near-pristine mangrove area of the Australian wet tropics. Estuarine, Coastal and Shelf Science 82. Elsevier Ltd: 597–607. https://doi.org/10.1016/j.ecss.2009.02.021, 4.

  • Araújo, Márcio S., Daniel I. Bolnick, and Craig A. Layman. 2011. The ecological causes of individual specialisation. Ecology Letters 14 (9): 948–958. https://doi.org/10.1111/j.1461-0248.2011.01662.x.

    Article  Google Scholar 

  • Atwood, Trisha B., Tracy N. Wiegner, and Richard A. MacKenzie. 2012. Effects of hydrological forcing on the structure of a tropical estuarine food web. Oikos 121 (2): 277–289. https://doi.org/10.1111/j.1600-0706.2011.19132.x.

    Article  Google Scholar 

  • Belicka, Laura L., Philip Matich, Rudolf Jaffé, and Michael R. Heithaus. 2012. Fatty acids and stable isotopes as indicators of early-life feeding and potential maternal resource dependency in the bull shark Carcharhinus leucas. Marine Ecology Progress Series 455: 245–256. https://doi.org/10.3354/meps09674.

    Article  CAS  Google Scholar 

  • Blaber, Stephen J.M., David T. Brewer, and John P. Salini. 1994. Diet and dentition in tropical ariid catfishes from Australia. Environmental Biology of Fishes 40 (2): 159–174. https://doi.org/10.1007/BF00002543.

    Article  Google Scholar 

  • Blanchette, Melanie L, Aaron M Davis, Timothy D Jardine, and Richard G Pearson. 2014. Omnivory and opportunism characterize food webs in a large dry-tropics river system. Freshwater Science 33. University of Chicago PressChicago, IL: 142–158. https://doi.org/10.1086/674632, 1.

  • Bligh, E G, and W J Dyer. 1959. A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology 37. NRC Research Press Ottawa, Canada: 911–917. https://doi.org/10.1139/o59-099, 8.

  • Bolnick, Daniel I., Louie H. Yang, James A. Fordyce, Jeremy M. Davis, and Richard Svanbäck. 2002. Measuring individual-level resource specialization. Ecology 83 (10): 2936–2941. https://doi.org/10.1890/0012-9658(2002)083[2936:MILRS]2.0.CO;2.

  • Brett, Michael T. 2014. Resource polygon geometry predicts Bayesian stable isotope mixing model bias. Marine Ecology Progress Series 514: 1–12. https://doi.org/10.3354/meps11017.

    Article  Google Scholar 

  • Brewer, D.T., S.J.M. Blaber, J.P. Salini, and M.J. Farmer. 1995. Feeding ecology of predatory fishes from Groote Eylandt in the Gulf of Carpentaria, Australia, with special reference to predation on penaeid prawns. Estuarine, Coastal and Shelf Science 40 (5): 577–600. https://doi.org/10.1006/ecss.1995.0039.

    Article  Google Scholar 

  • Brind’Amour, Anik, and Stanislas F Dubois. 2013. Isotopic diversity indices: How sensitive to food web structure? Edited by David William Pond. PLoS ONE 8. Public Library of Science: e84198, https://doi.org/10.1371/journal.pone.0084198.

  • Budge, Suzanne M., Sara J. Iverson, W. Don Bowen, and Robert G. Ackman. 2002. Among- and within-species variability in fatty acid signatures of marine fish and invertebrates on the Scotian Shelf, Georges Bank, and southern Gulf of St. Lawrence. Canadian Journal of Fisheries and Aquatic Sciences 59 (5): 886–898. https://doi.org/10.1139/f02-062.

    Article  CAS  Google Scholar 

  • Bunn, Stuart E., Catherine Leigh, and Timothy D. Jardine. 2013. Diet-tissue fractionation of δ15N by consumers from streams and rivers. Limnology and Oceanography 58 (3): 765–773. https://doi.org/10.4319/lo.2013.58.3.0765.

    Article  CAS  Google Scholar 

  • Caut, Stéphane, Elena Angulo, and Franck Courchamp. 2009. Variation in discrimination factors (Δ15N and Δ13C): The effect of diet isotopic values and applications for diet reconstruction. Journal of Applied Ecology 46 (2): 443–453. https://doi.org/10.1111/j.1365-2664.2009.01620.x.

    Article  CAS  Google Scholar 

  • Clarke, K.R., and R.N. Gorley. 2006. PRIMER v6 PRIMER-E Ltd. UK: Plymouth. https://doi.org/10.1109/IEMBS.2006.260840.

    Book  Google Scholar 

  • Couturier, Lydie I.E., Christoph A. Rohner, Anthony J. Richardson, Andrea D. Marshall, Fabrice R.A. Jaine, Michael B. Bennett, Kathy A. Townsend, Scarla J. Weeks, and Peter D. Nichols. 2013. Stable isotope and signature fatty acid analyses suggest reef manta rays feed on demersal zooplankton. PLoS One 8 (10): e77152. https://doi.org/10.1371/journal.pone.0077152.

    Article  CAS  Google Scholar 

  • Cyrus, Digby P., and Stephen J.M. Blaber. 1992. Turbidity and salinity in a tropical northern Australian estuary and their influence on fish distribution. Estuarine, Coastal and Shelf Science 35 (6): 545–563. https://doi.org/10.1016/S0272-7714(05)80038-1.

    Article  CAS  Google Scholar 

  • Daly, Ryan, Pierre W. Froneman, and Malcolm J. Smale. 2013. Comparative feeding ecology of bull sharks (Carcharhinus leucas) in the coastal waters of the southwest Indian Ocean inferred from stable isotope analysis. PLoS One 8 (10): 1–11. https://doi.org/10.1371/journal.pone.0078229.

    Article  CAS  Google Scholar 

  • Dantas, David Valença, Mario Barletta, Jonas de Assis Almeida Ramos, André Ricardo Araújo Lima, and Monica Ferreira da Costa. 2012. Seasonal diet shifts and overlap between two sympatric catfishes in an estuarine nursery. Estuaries and Coasts 36 (2): 237–256. https://doi.org/10.1007/s12237-012-9563-2.

    Article  CAS  Google Scholar 

  • Davis, T.L.O. 1985. The food of barramundi, Lates calcarifer (Bloch), in coastal and inland waters of Van Diemen Gulf and the Gulf of Carpentaria, Australia. Journal of Fish Biology 26 (6): 669–682. https://doi.org/10.1111/j.1095-8649.1985.tb04307.x.

    Article  Google Scholar 

  • Douglas, Michael M, Stuart E Bunn, and Peter M Davies. 2005. River and wetland food webs in Australia’s wet–dry tropics: General principles and implications for management. Marine and Freshwater Research 56. CSIRO PUBLISHING: 329–342. https://doi.org/10.1071/MF04084, 3.

  • Dufrêne, M., and P. Legendre. 1997. Species assemblages and indicator species: The need for a flexible asymmetrical approach. Ecological Monographs 67: 345–366.

    Google Scholar 

  • Dulvy, Nicholas K., Sarah L. Fowler, John A. Musick, Rachel D. Cavanagh, Peter M. Kyne, Lucy R. Harrison, John K. Carlson, et al. 2014. Extinction risk and conservation of the world’s sharks and rays. eLife 3: 1–34. https://doi.org/10.7554/eLife.00590.

    Article  Google Scholar 

  • Every, Sharon L., Heidi R. Pethybridge, David A. Crook, Peter M. Kyne, and Christopher J. Fulton. 2016. Comparison of fin and muscle tissues for analysis of signature fatty acids in tropical euryhaline sharks. Journal of Experimental Marine Biology and Ecology 479: 46–53. https://doi.org/10.1016/j.jembe.2016.02.011.

    Article  CAS  Google Scholar 

  • Every, Sharon L., Heidi R. Pethybridge, Christopher J. Fulton, Peter M. Kyne, and David A. Crook. 2017. Niche metrics suggest euryhaline and coastal elasmobranchs provide trophic connections among marine and freshwater biomes in northern Australia. Marine Ecology Progress Series 565: 181–196. https://doi.org/10.3354/meps11995.

    Article  CAS  Google Scholar 

  • Froese, R, and Daniel Pauly. 2015. FishBase World Wide Web electronic publication. www.fishbase.org (10/2015), https://doi.org/10.1017/S0140525X14000892.

  • Gallagher, Austin J., Peter M. Kyne, and Neil Hammerschlag. 2012. Ecological risk assessment and its application to elasmobranch conservation and management. Journal of Fish Biology 80 (5): 1727–1748. https://doi.org/10.1111/j.1095-8649.2012.03235.x.

    Article  CAS  Google Scholar 

  • Grubbs, R Dean, John K Carlson, Jason G Romine, Tobey H Curtis, W David McElroy, Camilla T McCandless, Charles F Cotton, and John A Musick. 2016. Critical assessment and ramifications of a purported marine trophic cascade. Scientific Reports 6. Nature Publishing Group: 20970. https://doi.org/10.1038/srep20970, 1.

  • Heithaus, Michael R., Jeremy J. Vaudo, S. Kreicker, Craig A. Layman, M. Krützen, Derek A. Burkholder, K. Gastrich, C. Bessey, R. Sarabia, K. Cameron, A. Wirsing, J.A. Thomson, and M.M. Dunphy-Daly. 2013. Apparent resource partitioning and trophic structure of large-bodied marine predators in a relatively pristine seagrass ecosystem. Marine Ecology Progress Series 481: 225–237. https://doi.org/10.3354/meps10235.

    Article  Google Scholar 

  • Heupel, Michelle R., John K. Carlson, and Colin A. Simpfendorfer. 2007. Shark nursery areas: Concepts, definition, characterization and assumptions. Marine Ecology Progress Series. 337: 287–297. https://doi.org/10.3354/meps337287.

    Article  Google Scholar 

  • Hussey, Nigel E., Demian D. Chapman, Erin Donnelly, Debra L. Abercrombie, and Aaron T. Fisk. 2011. Fin-icky samples: An assessment of shark fin as a source material for stable isotope analysis. Limnology and Oceanography: Methods 9 (11): 524–532. https://doi.org/10.4319/lom.2011.9.524.

    Article  CAS  Google Scholar 

  • Iverson, Sara J. 2009. Tracing aquatic food webs using fatty acids: From qualitative indicators to quantitative determination lipids in aquatic ecosystems. In Lipids in aquatic ecosystems, ed. Martin Kainz, Michael T. Brett, and Michael T. Arts, 281–307. New York, NY: Springer New York. https://doi.org/10.1007/978-0-387-89366-2.

    Chapter  Google Scholar 

  • Jackson, Andrew L., Richard Inger, Andrew C. Parnell, and Stuart Bearhop. 2011. Comparing isotopic niche widths among and within communities: SIBER – Stable Isotope Bayesian Ellipses in R. Journal of Animal Ecology 80 (3): 595–602. https://doi.org/10.1111/j.1365-2656.2011.01806.x.

    Article  Google Scholar 

  • Jardine, Timothy D., Nicholas R. Bond, Michele A. Burford, Mark J. Kennard, Douglas P. Ward, Peter Bayliss, Peter M. Davies, Michael M. Douglas, Stephen K. Hamilton, John M. Melack, Robert J. Naiman, Neil E. Pettit, Bradley J. Pusey, Danielle M. Warfe, and Stuart E. Bunn. 2015. Does flood rhythm drive ecosystem responses in tropical riverscapes? Ecology 96 (3): 684–692. https://doi.org/10.1890/14-0991.1.

    Article  Google Scholar 

  • Jardine, Timothy D, Thomas S Rayner, Neil E Pettit, Dominic Valdez, Douglas P Ward, Garry Lindner, Michael M Douglas, and Stuart E Bunn. 2017. Body size drives allochthony in food webs of tropical rivers. Oecologia 183. Springer Berlin Heidelberg: 505–517. doi:https://doi.org/10.1007/s00442-016-3786-z, 2.

  • Jepsen, David B., and Kirk O. Winemiller. 2002. Structure of tropical river food webs revealed by stable isotope ratios. Oikos 96 (1): 46–55. https://doi.org/10.1034/j.1600-0706.2002.960105.x.

    Article  Google Scholar 

  • Kelly, JR, and RE Scheibling. 2012. Fatty acids as dietary tracers in benthic food webs. Marine Ecology Progress Series 446. Inter-Research, Nordbunte 23, D-21385 Oldendorf Luhe, Germany: 1–22. https://doi.org/10.3354/meps09559.

  • Kim, Sora Lee, and Paul L. Koch. 2012. Methods to collect, preserve, and prepare elasmobranch tissues for stable isotope analysis. Environmental Biology of Fishes 95 (1): 53–63. https://doi.org/10.1007/s10641-011-9860-9.

    Article  Google Scholar 

  • Last, Peter R. 2002. Freshwater and estuarine elasmobranchs of Australia. In Elasmobranch biodiversity, conservation and management. Proceedings of the International Seminar and Workshop, ed. Sarah L. Fowler, T. M. Reed, and F. A. Dipper, 185–193, https://doi.org/10.1016/S0749-3797(02)00505-6.

  • Layman, Craig A., and J.E. Allgeier. 2012. Characterizing trophic ecology of generalist consumers: A case study of the invasive lionfish in the Bahamas. Marine Ecology Progress Series 448: 131–141. https://doi.org/10.3354/meps09511.

    Article  Google Scholar 

  • Layman, Craig A., and David M. Post. 2005. Can stable isotope ratios provide for community -wide measures of trophic structure? Reply. Ecological Society of America 89: 2358–2359. https://doi.org/10.1038/news050808-1.

    Article  Google Scholar 

  • Layman, Craig A., D. Albrey Arrington, Carman G. Montaña, and David M. Post. 2007. Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology 88 (1): 42–48. https://doi.org/10.1890/0012-9658(2007)88[42:CSIRPF]2.0.CO;2.

  • Loneragan, N.R., Stuart E. Bunn, and D.M. Kellaway. 1997. Are mangrove and seagrasses sources of organic carbon for penaeid prawns in a tropical estuary? A multiple isotope study. Marine Biology 130 (2): 289–300. https://doi.org/10.1007/s002270050248.

    Article  Google Scholar 

  • Lucifora, Luis O., Marcelo R. de Carvalho, Peter M. Kyne, and William T. White. 2015. Freshwater sharks and rays. Current Biology 25 (20): R971–R973. https://doi.org/10.1016/j.cub.2015.06.051.

    Article  CAS  Google Scholar 

  • MacNeil, M. Aaron, Gregory B. Skomal, and Aaron T. Fisk. 2005. Stable isotopes from multiple tissues reveal diet switching in sharks. Marine Ecology Progress Series 302: 199–206. https://doi.org/10.3354/meps302199.

    Article  Google Scholar 

  • Magnone, Larisa, Martin Bessonart, Juan Gadea, and María Salhi. 2015. Trophic relationships in an estuarine environment: A quantitative fatty acid analysis signature approach. Estuarine, Coastal and Shelf Science 166: 24–33. https://doi.org/10.1016/j.ecss.2014.12.033.

    Article  CAS  Google Scholar 

  • March, James G., Catherine M. Pringle, Matt J. Townsend, and Amanda I. Wilson. 2002. Effects of freshwater shrimp assemblages on benthic communities along an altitudinal gradient of a tropical island stream. Freshwater Biology 47 (3): 377–390. https://doi.org/10.1046/j.1365-2427.2002.00808.x.

    Article  Google Scholar 

  • Matich, Philip, and Michael R. Heithaus. 2014. Multi-tissue stable isotope analysis and acoustic telemetry reveal seasonal variability in the trophic interactions of juvenile bull sharks in a coastal estuary. The Journal of Animal Ecology 83 (1): 199–213. https://doi.org/10.1111/1365-2656.12106.

    Article  Google Scholar 

  • Matich, Philip, Michael R. Heithaus, and Craig A. Layman. 2011. Contrasting patterns of individual specialization and trophic coupling in two marine apex predators. The Journal of Animal Ecology 80 (1): 294–305. https://doi.org/10.1111/j.1365-2656.2010.01753.x.

    Article  Google Scholar 

  • Matley, J.K., Aaron T. Fisk, Andrew J. Tobin, Michelle R. Heupel, and Colin A. Simpfendorfer. 2016. Diet-tissue discrimination factors and turnover of carbon and nitrogen stable isotopes in tissues of an adult predatory coral reef fish, Plectropomus leopardus. Rapid Communications in Mass Spectrometry 30 (1): 29–44. https://doi.org/10.1002/rcm.7406.

    Article  CAS  Google Scholar 

  • McMeans, Bailey C., Michael T. Arts, Christian Lydersen, Kit M. Kovacs, Haakon Hop, Stig Falk-Petersen, and Aaron T. Fisk. 2013. The role of Greenland sharks (Somniosus microcephalus) in an Arctic ecosystem: Assessed via stable isotopes and fatty acids. Marine Biology 160 (5): 1223–1238. https://doi.org/10.1007/s00227-013-2174-z.

    Article  Google Scholar 

  • Montoya, José M., Stuart L. Pimm, and Ricard V. Solé. 2006. Ecological networks and their fragility. Nature 442 (7100): 259–264. https://doi.org/10.1038/nature04927.

    Article  CAS  Google Scholar 

  • Moore, Jonathan W., and Brice X. Semmens. 2008. Incorporating uncertainty and prior information into stable isotope mixing models. Ecology Letters 11 (5): 470–480. https://doi.org/10.1111/j.1461-0248.2008.01163.x.

    Article  Google Scholar 

  • Munroe, Samatha E.M., Michelle R. Heupel, Aaron T. Fisk, and Colin A. Simpfendorfer. 2014. Geographic and temporal variation in the trophic ecology of a small-bodied shark: Evidence of resilience to environmental change. Canadian Journal of 72: 343–351.

    Google Scholar 

  • Munroe, Samatha E.M., Michelle R. Heupel, Aaron T. Fisk, John M. Logan, and Colin A. Simpfendorfer. 2015. Regional movement patterns of a small-bodied shark revealed by stable-isotope analysis. Journal of Fish Biology 86 (5): 1567–1586. https://doi.org/10.1111/jfb.12660.

    Article  CAS  Google Scholar 

  • Olin, Jill A., Nigel E. Hussey, Mark Fritts, Michelle R. Heupel, Colin A. Simpfendorfer, Gregg R. Poulakis, and Aaron T. Fisk. 2011. Maternal meddling in neonatal sharks: Implications for interpreting stable isotopes in young animals. Rapid Communications in Mass Spectrometry : RCM 25 (8): 1008–1016. https://doi.org/10.1002/rcm.4946.

    Article  CAS  Google Scholar 

  • Parnell, Andrew C., Richard Inger, Stuart Bearhop, and Andrew L. Jackson. 2010. Source partitioning using stable isotopes: Co** with too much variation. PLoS One 5 (3): 1–5. https://doi.org/10.1371/journal.pone.0009672.

    Article  CAS  Google Scholar 

  • Parnell, Andrew C., Donald L. Phillips, Stuart Bearhop, Brice X. Semmens, Eric J. Ward, Jonathan W. Moore, Andrew L. Jackson, Jonathan Grey, David J. Kelly, and Richard Inger. 2013. Bayesian stable isotope mixing models. Environmetrics 24: 387–399. https://doi.org/10.1002/env.2221.

    Article  Google Scholar 

  • Parrish, Christopher C., Peter D. Nichols, Heidi R. Pethybridge, and Jock W. Young. 2015. Direct determination of fatty acids in fish tissues: Quantifying top predator trophic connections. Oecologia 177 (1): 85–95. https://doi.org/10.1007/s00442-014-3131-3.

    Article  Google Scholar 

  • Peterson, B J, and Brian Fry. 1987. Stable isotopes in ecosystem studies. Annual Review of Ecology and Systematics 18. Annual Reviews 4139 El Camino Way, P.O. Box 10139, Palo Alto, CA 94303–0139, USA: 293–320. https://doi.org/10.1146/annurev.es.18.110187.001453, 1.

  • Pethybridge, Heidi R., Ross K. Daley, and Peter D. Nichols. 2011. Diet of demersal sharks and chimaeras inferred by fatty acid profiles and stomach content analysis. Journal of Experimental Marine Biology and Ecology 409 (1-2): 290–299. https://doi.org/10.1016/j.jembe.2011.09.009.

    Article  Google Scholar 

  • Peverell, Stirling Charles, G.R. Mcpherson, R.N. Garrett, and N.A. Gribble. 2006. New records of the river shark Glyphis (Carcharhinidae) reported from Cape York Peninsula, northern Australia. Zootaxa 68: 53–68.

    Article  Google Scholar 

  • Post, David M., Craig A. Layman, D. Albrey Arrington, Gaku Takimoto, John P. Quattrochi, and Carman G. Montaña. 2007. Getting to the fat of the matter: Models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152 (1): 179–189. https://doi.org/10.1007/s00442-006-0630-x.

    Article  Google Scholar 

  • Pusey, Bradley J., Mark J. Kennard, Helen K. Larson, Quentin Alsop, Duncan Buckle, and Hammer Michael. 2015. Estuarine fishes of the South Alligator River, Kakadu National Park, northern Australia. Marine and Freshwater Research 67: 1797–1812. https://doi.org/10.1071/mf15221 2016.

    Article  Google Scholar 

  • Roach, Katherine A, Kirk O Winemiller, Craig A Layman, and Steven C Zeug. 2009. Consistent trophic patterns among fishes in lagoon and channel habitats of a tropical floodplain river: Evidence from stable isotopes. Acta Oecologica 35. Elsevier Masson SAS: 513–522. doi:https://doi.org/10.1016/j.actao.2009.03.007, 4.

  • Roberts, D W. 2016. Package “labdsv.” Ordination and Multivariate.

  • Rohner, Christoph A., Lydie I.E. Couturier, Anthony J. Richardson, Simon J. Pierce, Clare E.M. Prebble, Mark J. Gibbons, and Peter D. Nichols. 2013. Diet of whale sharks Rhincodon typus inferred from stomach content and signature fatty acid analyses. Marine Ecology Progress Series 493: 219–235. https://doi.org/10.3354/meps10500.

    Article  CAS  Google Scholar 

  • Roughgarden, Jonathan. 1972. Evolution of niche width. The American Naturalist 106 (952): 683–718. https://doi.org/10.1086/282807.

    Article  Google Scholar 

  • Sasaki, K. 2001. Sciaenidae. Croakers (drums). In FAO species identification guide for fishery purposes. The living marine resources of the Western Central Pacific. Volume 5. Bony fishes part 3 (Menidae to Pomacentridae), ed. K.E. Carpenter and V.H. Niem, 3117–3174. Rome.

  • Simpfendorfer, Colin A. 1998. Diet of the Australian Sharpnose shark, Rhizoprionodon taylori, from northern Queensland. Marine and Freshwater Research 49 (7): 757–761. https://doi.org/10.1071/MF97044.

    Article  Google Scholar 

  • Snelson, Franklin F. Jr, Timothy J. Mulligan, and Sherry E. Williams. 1984. Food habits, occurrence, and population structure of the bull shark, Carcharhinus leucas, in Florida coastal lagoons. Bulletin of Marine Science 34: 71–80.

    Google Scholar 

  • Team, R Development Core. 2014. R: A language and environment for statistical computing. Austria: Vienna.

    Google Scholar 

  • Thorburn, Dean C., and David L. Morgan. 2004. The northern river shark Glyphis sp. C (Carcharhinidae) discovered in Western Australia. Zootaxa 685: 1–8.

    Article  Google Scholar 

  • Thorburn, Dean C., and Andrew J. Rowland. 2008. Juvenile bull sharks Carcharhinus leucas (Valenciennes, 1839) in northern Australian rivers. The Beagle: Records of The Museums And Art Galleries of The Northern Territory 24: 79–86.

    Google Scholar 

  • Thorburn, Dean C., Howard S. Gill, and David L. Morgan. 2014. Predator and prey interactions of fishes of a tropical Western Australia river revealed by dietary and stable isotope analyses. Journal of Royal Society of Western Australia 97: 363–387.

    Google Scholar 

  • Tillett, Bree J., Mark G. Meekan, and Ian C. Field. 2014. Dietary overlap and partitioning among three sympatric carcharhinid sharks. Endangered Species Research 25 (3): 283–293. https://doi.org/10.3354/esr00615.

    Article  Google Scholar 

  • Tilley, Alexander, Juliana López-Angarita, and John R. Turner. 2013. Diet reconstruction and resource partitioning of a Caribbean marine mesopredator using stable isotope Bayesian modelling. PLoS One 8 (11): e79560. https://doi.org/10.1371/journal.pone.0079560.

    Article  CAS  Google Scholar 

  • Turchini, G.M., D.S. Francis, S.P.S.D. Senadheera, T. Thanuthong, and S.S. De Silva. 2011. Fish oil replacement with different vegetable oils in Murray cod: Evidence of an “omega-3 sparing effect” by other dietary fatty acids. Aquaculture 315 (3-4): 250–259. https://doi.org/10.1016/j.aquaculture.2011.02.016.

    Article  CAS  Google Scholar 

  • Vaudo, Jeremy J., and Michael R. Heithaus. 2011. Dietary niche overlap in a nearshore elasmobranch mesopredator community. Marine Ecology Progress Series 425: 247–260. https://doi.org/10.3354/meps08988.

    Article  Google Scholar 

  • Ward, Douglas P., Neil E. Pettit, M.F. Adame, Michael M. Douglas, S.A. Setterfield, and Stuart E. Bunn. 2016. Seasonal spatial dynamics of floodplain macrophyte and periphyton abundance in the Alligator Rivers region (Kakadu) of northern Australia. Ecohydrology 9 (8): 1675–1686. https://doi.org/10.1002/eco.1757.

    Article  Google Scholar 

  • Warfe, Danielle M., Neil E. Pettit, Peter M. Davies, Bradley J. Pusey, S.K. Hamilton, Mark J. Kennard, Simon A. Townsend, et al. 2011. The “wet-dry” in the wet-dry tropics drives river ecosystem structure and processes in northern Australia. Freshwater Biology 56 (11): 2169–2195. https://doi.org/10.1111/j.1365-2427.2011.02660.x.

    Article  Google Scholar 

  • Winemiller, Kirk O., and David B. Jepsen. 1998. Effects of seasonality and fish movement on tropical river food webs. Journal of Fish Biology 53 (sa): 267–296. https://doi.org/10.1111/j.1095-8649.1998.tb01032.x.

    Article  Google Scholar 

  • Young, Jock W., Brian P.V. Hunt, Timothée R. Cook, Joel K. Llopiz, Elliott L. Hazen, Heidi R. Pethybridge, Daniela Ceccarelli, Anne Lorrain, Robert J. Olson, Valerie Allain, Christophe Menkes, Toby Patterson, Simon Nicol, Patrick Lehodey, Rudy J. Kloser, Haritz Arrizabalaga, and C. Anela Choy. 2015. The trophodynamics of marine top predators: Current knowledge, recent advances and challenges. Deep Sea Research Part II: Topical Studies in Oceanography 113: 170–187. https://doi.org/10.1016/j.dsr2.2014.05.015.

    Article  Google Scholar 

  • Zaccarelli, Nicola, Daniel I. Bolnick, and Giorgio Mancinelli. 2013. RInSp: An R package for the analysis of individual specialization in resource use. Methods in Ecology and Evolution 4 (11): 1018–1023. https://doi.org/10.1111/2041-210X.12079.

    Article  Google Scholar 

Download references

Acknowledgements

This research was conducted on the traditional country of the Bininj and Mungguy people. We gratefully acknowledge the traditional custodians for allowing access to this country. We thank Peter Nichols, Peter Mansour, Grant Johnson, Mark Grubert, Duncan Buckle, Roy Tipiloura, Dominic Valdez, Francisco Zillamarin, Edward Butler, Claire Streten, Kirsty McAllister, Mirjam Kaestli and the crew of R.V. Solander for fieldwork and laboratory assistance and to Martin Lysy (nicheROVER) and Andrew Jackson (SIAR) for their advice and assistance.

Funding

This study is financially supported by the Charles Darwin University, CSIRO and the North Australia Marine Research Alliance (NAMRA), alongside collaborative partnerships in the Marine Biodiversity and Northern Australia Hubs of the Australian Government’s National Environmental Research Program (NERP).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sharon L. Every.

Ethics declarations

Ethical Approval

All procedures performed in this study were conducted with the approval of the Charles Darwin University Animal Ethics Committee (A12016), in conjunction with permits from NT Fisheries S17/3268 and Kakadu National Park (RK805).

Additional information

Communicated by Nadine A. Strydom

Electronic supplementary material

ESM 1

(DOCX 1161 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Every, S.L., Fulton, C.J., Pethybridge, H.R. et al. A Seasonally Dynamic Estuarine Ecosystem Provides a Diverse Prey Base for Elasmobranchs. Estuaries and Coasts 42, 580–595 (2019). https://doi.org/10.1007/s12237-018-0458-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12237-018-0458-8

Keywords

Navigation