The 13C, 15N and 34S signatures of a rocky reef planktivorous fish indicate different coastal discharges of sewage
Troy F. Gaston A B C , Antionette Kostoglidis A and Iain M. Suthers AA School of Biological, Earth and Environmental Sciences, Faculty of Science, University of New South Wales, Sydney, NSW 2052, Australia.
B Present address: Faculty of Science, University of the Sunshine Coast, Maroochydore DC, Qld 4558, Australia.
C Corresponding author. Email: tgaston@usc.edu.au
Marine and Freshwater Research 55(7) 689-699 https://doi.org/10.1071/MF03142
Submitted: 23 September 2003 Accepted: 19 August 2004 Published: 1 October 2004
Abstract
We assessed the effects of primary, secondary and tertiary treated sewage on the stable isotope composition of the viscera and muscle of the zooplanktivorous eastern hula fish (Plesiopidae: Trachinops taeniatus). Fish were collected from three regions during three consecutive summer months for 2 years. In comparison to fish from control sites, the muscle δ15N of fish at outfall sites was significantly enriched by secondary and tertiary treated effluent. We estimate that 30–50% of nitrogen in hula fish near outfalls may be sewage-derived. The δ34S content of muscle was similar at all regions and sites (20–21‰), although it was significantly depleted by 1–2‰ at the tertiary treated outfall site. Detection of a comparatively minor volume of effluent (<6 ML day–1) in fish muscle may be due to its slower tissue turnover rate and the continuous discharge of effluent at outfall sites, compared to major yet sporadic rainfall or oceanographic events. The isotopic composition of hula fish from near a large primary treated sewage outfall off the coast of Sydney was not significantly different from one of the control sites, indicating a regional effect of four outfalls discharging >1000 ML day–1. With increasing upgrades to sewage treatment, stable isotopes may become useful tracers of anthropogenic nutrients in an oligotrophic environment.
Extra keywords: food chain dynamics, planktivorous fish, sewage, stable isotope analysis.
Acknowledgments
We acknowledge the financial support of the Australian Research Council and the Sea World Research and Rescue Foundation Inc. Thanks to Richard Piola who assisted with many of the analyses, and to Sharon Longford, Steven Rutten and Jocelyn Dela-Cruz for assistance with fieldwork.
Burnett, W. C. , and Schaeffer, O. A. (1980). Effect of ocean dumping on 13C/12C ratios in marine sediments from the New York Bight. Estuarine, Coastal and Shelf Science 11, 605–611.
Cloern, J. E. , Canuel, E. A. , and Harris, D. (2002). Stable carbon and nitrogen isotope composition of aquatic and terrestrial plants of the San Francisco Bay estuarine system. Limnology and Oceanography 47, 713–729.
Compton, T. (2000). ‘Tracing Marine Nutrients Using Novel 15N Stable Isotope Techniques.’ Honours Thesis. (University of New South Wales: Sydney, Australia.)
Darnaude, A. M. , Salen-Picard, C. , Polunin, N. V. C. , and Harmelin-Vivien, M. L. (2004). Trophodynamic linkage between river runoff and coastal fishery yield elucidated by stable isotope data in the Gulf of Lions (NW Mediterranean). Oecologia 138, 325–332.
| Crossref | GoogleScholarGoogle Scholar |
De Niro, M. J. , and Epstein, S. (1977). Mechanism of carbon isotope fractionation associated with lipid synthesis. Science 197, 261–263.
De Niro, M. J. , and Epstein, S. (1978). Influence of diet on the distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta 42, 495–506.
| Crossref | GoogleScholarGoogle Scholar |
De Niro, M. J. , and Epstein, S. (1981). Influence of diet on the distribution of nitrogen isotopes in animals. Geochimica et Cosmochimica Acta 45, 341–351.
| Crossref | GoogleScholarGoogle Scholar |
Faganeli, J. , Malej, A. , Pezdic, J. , and Malacic, V. (1988). C:N:P ratios and stable C isotopic ratios as indicators of sources of organic matter in the Gulf of Trieste (Northern Adriatic). Oceanologica Acta 11, 377–382.
Frazer, T. K. , Ross, R. M. , Quetin, L. B. , and Montoya, P. (1997). Turnover of carbon and nitrogen during growth of larval krill, Euphuasia superba Dana: a stable isotope approach. Journal of Experimental Marine Biology and Ecology 212, 259–275.
| Crossref | GoogleScholarGoogle Scholar |
Fry, B. (1988). Food web structure on Georges Bank from stable C, N and S isotopic compositions. Limnology and Oceanography 35, 1182–1190.
Fry, B. , and Sherr, E. B. (1984). δ13C measurements as indicators of carbon flow in marine and freshwater ecosystems. Contributions in Marine Science 27, 13–47.
Gannes, L. Z. , O'Brien, D. M. , and Martínez del Rio, C. (1997). Stable isotopes in animal ecology: assumptions, caveats, and a call for more laboratory experiments. Ecology 78, 1271–1276.
Gaston, T. F. (2003). ‘Nutrient Sources of Urban Coastal Food Chains.’ PhD Thesis. (University of New South Wales: Sydney, Australia.)
Gaston, T. F. , and Suthers, I. M. (2004). Spatial variation in δ13C and δ15N of liver, muscle and bone in a rocky reef planktivorous fish: the relative contribution of sewage. Journal of Experimental Marine Biology and Ecology 304, 17–33.
| Crossref | GoogleScholarGoogle Scholar |
Gearing, J. N. , Gearing, P. J. , Rudnick, D. T. , Requejo, A. G. , and Hutchings, M. J. (1984). Isotopic variability of organic carbon in a phytoplankton-based temperature estuary. Geochimica et Cosmochimica Acta 48, 1089–1098.
| Crossref | GoogleScholarGoogle Scholar |
Grigg, R. W. (1994). Effect of sewage discharge, fishing pressure and habitat complexity on coral ecosystems and reef fishes in Hawaii. Marine Ecology Progress Series 103, 25–34.
Hansson, S. , Hobbie, J. E. , Elmgren, R. , Larsson, U. , Fry, B. , and Johansson, S. (1997). The stable nitrogen isotope ratio as a marker of food-web interactions and fish migration. Ecology 78, 2249–2257.
Heaton, T. H. E. (1986). Isotopic studies of nitrogen pollution in the hydrosphere and atmosphere: a review. Chemical Geology 59, 87–102.
| Crossref | GoogleScholarGoogle Scholar |
Hesslein, R. H. , Hallard, K. A. , and Ramlal, P. (1993). Replacement of sulphur, carbon, and nitrogen tissue of growing broad whitefish (Coregonus nasus) in response to a change in diet traced by δ34S, δ13C, and δ15N. Canadian Journal of Fisheries and Aquatic Sciences 50, 2071–2076.
Holloway, P. E. (1996). A field investigation of water exchange between a small coastal embayment and an adjacent shelf. In (Ed C. Pattiaratchi) pp. 145–158. (American Geophysical Union: Washington DC, USA.)
Hutchins, B., and Swainston, R. (1986). (Swainston Publishing: Perth, Australia.)
Jones, A. B. , O’Donohue, M. J. , Udy, J. , and Dennison, W. C. (2001). Assessing ecological impacts of shrimp and sewage effluent, biological indicators with standard water quality analyses. Estuarine, Coastal and Shelf Science 52, 91–109.
| Crossref | GoogleScholarGoogle Scholar |
Kaplan, I. R. , Emery, K. O. , and Rittenberg, S. C. (1963). The distribution and isotopic abundance of sulfur in recent marine sediments off southern California. Geochimica et Cosmochimica Acta 27, 297–331.
| Crossref | GoogleScholarGoogle Scholar |
Lancaster, J. , and Waldron, S. (2001). Stable isotope values of lotic invertebrates: Sources of variation, experimental design and statistical interpretation. Limnology and Oceanography 46, 723–730.
Macko, S. S. , Lee, W. Y. , and Parker, P. L. (1982). Nitrogen and carbon isotope fractionation by two species of marine amphipods: laboratory and field studies. Journal of Experimental Marine Biology and Ecology 63, 145–149.
| Crossref | GoogleScholarGoogle Scholar |
MHL (1997). (Manly Hydraulics Laboratory, Department of Public Works and Services: Sydney, Australia.)
Minagawa, M. , and Wada, E. (1984). Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochimica et Cosmochimica Acta 48, 1135–1140.
| Crossref | GoogleScholarGoogle Scholar |
Moore, M. J. , Shea, D. , Hillman, R. E. , and Stegeman, J. J. (1996). Trends in hepatic tumours and hydropic vacuolation, fin erosion, organic chemicals and stable isotope ratios in winter flounder from Massachusetts, USA. Marine Pollution Bulletin 32, 458–470.
| Crossref | GoogleScholarGoogle Scholar |
Peterson, B. J. , and Fry, B. (1987). Stable isotopes in ecosystem studies. Annual Review of Ecology and Systematics 18, 293–320.
| Crossref | GoogleScholarGoogle Scholar |
Peterson, B. J. , Howarth, R. W. , and Garritt, R. H. (1985). Multiple stable isotopes used to trace the flow of organic matter in estuarine food webs. Science 227, 1361–1363.
Phillips, D. L. , and Gregg, J. W. (2001). Uncertainty in source partitioning using stable isotopes. Oecologia 127, 171–179.
| Crossref | GoogleScholarGoogle Scholar |
Pinnegar, J. K. , and Polunin, N. V. C. (1999). Differential fractionation of δ13C and δ15N among fish tissues: implications for the study of trophic interactions. Functional Ecology 13, 225–231.
| Crossref | GoogleScholarGoogle Scholar |
Radtke, R. L. , Showers, W. , Moksness, E. , and Lenz, P. (1996). Environmental information stored in otoliths: insights from stable isotopes. Marine Biology 127, 161–171.
Rau, G. H. , Ainley, D. G. , Bengston, J. L. , Torres, J. J. , and Hopkins, T. L. (1992). 15N/14N and 13C/12C in Weddell Sea birds, seals and fish: implications for diet and trophic structure. Marine Ecology Progress Series 84, 1–8.
Rau, G. H. , Mearns, A. J. , Young, D. R. , Olson, R. J. , Schafer, H. A. , and Kaplan, I. R. (1983). Animal 13C/12C correlates with trophic level in pelagic food webs. Ecology 64, 1314–1318.
Rau, G. H. , Sullivan, C. W. , and Gordon, L. I. (1991). δ13C and δ15N variations in Weddell Sea particulate organic matter. Marine Chemistry 35, 355–369.
Richard, P. , Riera, P. , and Galois, R. (1997). Temporal variations in the chemical and carbon isotope compositions of marine and terrestrial organic inputs in the Bay of Marennes-Oléron, France. Journal of Coastal Research 13, 879–889.
Riera, P. (1998). δ15N of organic matter sources and benthic invertebrates along an estuarine gradient in Marennes-Oléron Bay (France): implications for the study of trophic structure. Marine Ecology Progress Series 166, 143–150.
Scanes, P. R., Scanes, K. and Otway, N. M. (1995). Environmental problems due to disposal of wastes. In (Eds. A. J. Underwood and M. G. Chapman) pp. 297–310. (UNSW Press: Sydney, Australia.)
Schoeninger, M. J. , and De Niro, M. J. (1984). Nitrogen and carbon isotopic composition of bone collagen from marine and terrestrial animals. Geochimica et Cosmochimica Acta 48, 625–639.
| Crossref | GoogleScholarGoogle Scholar |
Sholto-Douglas, A. D. , Field, J. G. , James, A. G. , and van der Merwe, N. J. (1991). 13C/12C and 15N/14N isotope ratios in the Southern Benguela Ecosystem: indicators of food web relationships among different size-classes of plankton and pelagic fish; differences between fish muscle and bone collagen tissues. Marine Ecology Progress Series 78, 23–31.
Smith, A. K. , and Suthers, I. M. (1999). Effects of sewage effluent discharge on the abundance, condition and mortality of hulafish, Trachinops taeniatus (Plesiopidae). Environmental Pollution (Barking, Essex: 1987) 106, 97–106.
| Crossref | GoogleScholarGoogle Scholar |
Smith, A. K. , Ajani, P. A. , and Roberts, D. E. (1999). Spatial and temporal variation in fish assemblages exposed to sewage and implications for management. Marine Environmental Research 47, 241–260.
| Crossref | GoogleScholarGoogle Scholar |
Smith, S. D. A. (1994). Impact of domestic sewage effluent versus natural background variability: an example from Jervis Bay, New South Wales. Australian Journal of Marine and Freshwater Research 45, 1045–1064.
Spies, R. B. , Kruger, H. , Ireland, R. , and Rice, D. W. (1989). Stable isotope ratios and contaminant concentrations in a sewage-distorted food web. Marine Ecology Progress Series 54, 157–170.
Sweeney, R. E. , and Kaplan, I. R. (1980). Natural abundances of 15N as a source indicator for near-shore marine sedimentary and dissolved nitrogen. Marine Chemistry 9, 81–94.
| Crossref | GoogleScholarGoogle Scholar |
Sweeney, R. E. , Kalil, E. K. , and Kaplan, I. R. (1980). Characterisation of domestic and industrial sewage in Southern California coastal sediments using nitrogen, carbon, sulphur and uranium tracers. Marine Environmental Research 3, 225–243.
| Crossref | GoogleScholarGoogle Scholar |
Thomas, C. J. , and Cahoon, L. B. (1993). Stable isotope analyses differentiate between different trophic pathways supporting rocky-reef fishes. Marine Ecology Progress Series 95, 19–24.
Thornton, S. F. , and McManus, J. (1994). Application of organic carbon and nitrogen stable isotope and C/N ratios as sources indicators of organic matter provenance in estuarine systems: evidence from the Tray Estuary, Scotland. Estuarine, Coastal and Shelf Science 38, 219–233.
| Crossref | GoogleScholarGoogle Scholar |
Tieszen, L. L. , Boutton, T. W. , Tesdahl, K. G. , and Slade, N. A. (1983). Fractionation and turnover of stable carbon isotopes in animal tissues: implications for δ13C analysis of diet. Oecologia 57, 32–37.
Tucker, J. , Sheats, N. , Giblin, A. E. , Hopkinson, C. S. , and Montoya, J. P. (1999). Using stable isotopes to trace sewage-derived material through Boston Harbor and Massachusetts Bay. Marine Environmental Research 48, 353–375.
| Crossref | GoogleScholarGoogle Scholar |
Underwood, A. J., Chapman, M. G., and Richards, S. A. (1998). (Institute of Marine Ecology, University of Sydney: Sydney, Australia.)
Wong, W. W. , and Sackett, W. M. (1978). Fractionation of stable carbon isotopes by marine phytoplankton. Geochimica et Cosmochimica Acta 42, 1809–1815.
| Crossref | GoogleScholarGoogle Scholar |