Advertisement

Estuaries and Coasts

, Volume 42, Issue 2, pp 580–595 | Cite as

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

  • Sharon L. EveryEmail author
  • Christopher J. Fulton
  • Heidi R. Pethybridge
  • Peter M. Kyne
  • David A. Crook
Article

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.

Keywords

Fatty acids Stable isotopes Elasmobranchs Food webs Estuary 

Notes

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 information

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).

Compliance with Ethical Standards

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).

Supplementary material

12237_2018_458_MOESM1_ESM.docx (1.1 mb)
ESM 1 (DOCX 1161 kb)

References

  1. 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.
  2. 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.Google Scholar
  3. 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.Google Scholar
  4. 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.Google Scholar
  5. 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.Google Scholar
  6. 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.
  7. 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.
  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.Google Scholar
  9. 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.Google Scholar
  10. 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.Google Scholar
  11. 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.
  12. 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.Google Scholar
  13. 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.Google Scholar
  14. 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.Google Scholar
  15. Clarke, K.R., and R.N. Gorley. 2006. PRIMER v6 PRIMER-E Ltd. UK: Plymouth.  https://doi.org/10.1109/IEMBS.2006.260840.Google Scholar
  16. 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.Google Scholar
  17. 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.Google Scholar
  18. 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.Google Scholar
  19. 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.Google Scholar
  20. 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.Google Scholar
  21. 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.
  22. 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
  23. 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.Google Scholar
  24. 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.Google Scholar
  25. 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.Google Scholar
  26. Froese, R, and Daniel Pauly. 2015. FishBase World Wide Web electronic publication. www.fishbase.org (10/2015),  https://doi.org/10.1017/S0140525X14000892.
  27. 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.Google Scholar
  28. 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.
  29. 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.Google Scholar
  30. 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.Google Scholar
  31. 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.Google Scholar
  32. 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.Google Scholar
  33. 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.Google Scholar
  34. 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.Google Scholar
  35. 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.
  36. 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.Google Scholar
  37. 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.
  38. 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.Google Scholar
  39. 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.
  40. 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.Google Scholar
  41. 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.Google Scholar
  42. 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.Google Scholar
  43. 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.Google Scholar
  44. 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.Google Scholar
  45. 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.Google Scholar
  46. 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.Google Scholar
  47. 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.Google Scholar
  48. 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.Google Scholar
  49. 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.Google Scholar
  50. 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.Google Scholar
  51. 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.Google Scholar
  52. 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.Google Scholar
  53. 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.Google Scholar
  54. 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
  55. 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.Google Scholar
  56. 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.Google Scholar
  57. Parnell, Andrew C., Richard Inger, Stuart Bearhop, and Andrew L. Jackson. 2010. Source partitioning using stable isotopes: Coping with too much variation. PLoS One 5 (3): 1–5.  https://doi.org/10.1371/journal.pone.0009672.Google Scholar
  58. 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.Google Scholar
  59. 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.Google Scholar
  60. 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.
  61. 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.Google Scholar
  62. 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.Google Scholar
  63. 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.Google Scholar
  64. 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.Google Scholar
  65. 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.
  66. Roberts, D W. 2016. Package “labdsv.” Ordination and Multivariate.Google Scholar
  67. 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.Google Scholar
  68. Roughgarden, Jonathan. 1972. Evolution of niche width. The American Naturalist 106 (952): 683–718.  https://doi.org/10.1086/282807.Google Scholar
  69. 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.Google Scholar
  70. 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.Google Scholar
  71. 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
  72. Team, R Development Core. 2014. R: A language and environment for statistical computing. Austria: Vienna.Google Scholar
  73. Thorburn, Dean C., and David L. Morgan. 2004. The northern river shark Glyphis sp. C (Carcharhinidae) discovered in Western Australia. Zootaxa 685: 1–8.Google Scholar
  74. 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
  75. 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
  76. 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.Google Scholar
  77. 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.Google Scholar
  78. 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.Google Scholar
  79. 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.Google Scholar
  80. 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.Google Scholar
  81. 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.Google Scholar
  82. 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.Google Scholar
  83. 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.Google Scholar
  84. 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.Google Scholar

Copyright information

© Coastal and Estuarine Research Federation 2018

Authors and Affiliations

  1. 1.Research Institute for the Environment and LivelihoodsCharles Darwin UniversityDarwinAustralia
  2. 2.North Australia Marine Research Alliance, Arafura-Timor Sea Research FacilityBrinkinAustralia
  3. 3.Research School of BiologyThe Australian National UniversityCanberraAustralia
  4. 4.Ocean and AtmosphereCommonwealth Scientific and Industrial Research OrganisationHobartAustralia

Personalised recommendations