Skip to main content
Log in

Carbon and nitrogen stable isotope analysis indicates freshwater shrimp Paratya australiensis Kemp, 1917 (Atyidae) assimilate cyanobacterial accumulations

  • MYALL LAKES
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Large areas of uncompacted cyanobacterial accumulations (or “gyttja”) have been observed in Myall Lake, New South Wales, Australia. To determine whether the cyanobacterial accumulations were assimilated into the local food web, carbon and nitrogen stable isotopes were used to identify the primary food sources of a primary consumer in Myall Lake, the freshwater atyid shrimp Paratya australiensis. Suspended particulate organic matter (POM) and the macrophyte Myriophyllum salsugineum were identified as major dietary sources of P. australiensis. Enriched stable isotope signatures (δ13C and δ15N) of shrimp from gyttja-affected sites, relative to shrimp from unaffected locations, also indicated that P. australiensis were deriving a considerable portion of their dietary carbon and nitrogen requirements from gyttja. Stable isotope mixing models estimated that cyanobacterial accumulations might constitute up to 69% of P. australiensis biomass carbon and nitrogen requirements at gyttja-affected locations. To our knowledge, this is the first study to use stable isotope analysis to trace the assimilation of potentially toxic cyanobacterial accumulations into the trophic pathways of an affected system.

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

Access this article

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
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Ahlgran, G., I.-B. Gustafsson & M. Boberg, 1992. Fatty acid content and chemical composition of freshwater microalgae. Journal of Phycology 28: 37–50.

    Article  Google Scholar 

  • Bauld, J., 1986. Benthic microbial communities of Australian saline lakes. In De Deckker, P., & W. D. Williams (eds), Limnology in Australia. Dr. W. Junk Publishers, Dordrecht, 95–111.

    Google Scholar 

  • Boon, P. I., S. E. Bunn, J. D. Green & R. J. Shiel, 1994. Consumption of Cyanobacteria by freshwater zooplankton: implications for the success of ‘top-down’ control of cyanobacterial blooms in Australia. Australian Journal of Marine and Freshwater Research 45: 875–887.

    Article  Google Scholar 

  • Bowling, L. C. & P. D. Baker, 1996. Major Cyanobacterial Bloom in the Barwon-Darling River, Australia, in 1991, and Underlying Limnological Conditions. Marine and Freshwater Research 47: 643–657.

    Article  CAS  Google Scholar 

  • Bunn, S. E. & P. I. Boon, 1993. What sources of carbon drive food webs in billabongs? A study based on stable isotope analysis. Oecologia 96: 85–94.

    Article  Google Scholar 

  • Burns, C. W. & B. Hegarty, 1994. Diet selection by copepods in the presence of cyanobacteria. Journal of Plankton Research 16: 1671–1690.

    Article  Google Scholar 

  • Burns, A. & K. F. Walker, 2000. Biofilms as food for decapods (Atyidae, Palaemonidae) in the River Murray, South Australia. Hydrobiologia 437: 83–93.

    Article  Google Scholar 

  • Burns, C. W. & Z. Xu, 1990. Calanoid copepods feeding on algae and filamentous cyanobacteria: rates of ingestion, defaecation and effects on trichome length. Journal of Plankton Research 12: 201–213.

    Article  Google Scholar 

  • Chen, J. & P. Xie, 2005. Tissue distributions and seasonal dynamics of the hepatotoxic microcystins-LR and -RR in two freshwater shrimps, Palaemon modestus and Macrobrachium nipponensis, from a large shallow, eutrophic lake of the subtropical China. Toxicon 45: 615–625.

    Article  PubMed  CAS  Google Scholar 

  • Dasey, M., N. Ryan, J. Wilson, G. McGregor, L. Fabbro, B. A. Neilan, B. P. Burns, H. Kankaanpää, L. F. Morrison, G. A. Codd, D. Rissik & L. Bowling, 2004. Investigations into the taxonomy, toxicity and ecology of benthic cyanobacterial accumulations in Myall Lake, Australia. Marine and Freshwater Research 56: 45–55.

    Article  Google Scholar 

  • Davie, P. J. F., 2002. Crustacea: Malacostraca: Phyllocarida, Hoplocarida, Eucarida (Part 1). In Wells, A., & W. W. K. Houston (eds), Zoological Catalogue of Australia, Vol. 19.3A. CSIRO Publishing, Melbourne, Australia.

  • DeMott, W. R., 1998. Utilization of a cyanobacterium and a phosphorus-deficient green alga as complementary resources by daphnids. Ecology 79: 2463–2481.

    Article  Google Scholar 

  • DeMott, W. R. & F. Moxter, 1991. Foraging on cyanobacteria by copepods: responses to chemical defenses and resource abundance. Ecology 72: 1820–1834.

    Article  Google Scholar 

  • Engström, J., M. Viherluoto & M. Viitasalo, 2001. Effects of toxic and non-toxic cyanobacteria on grazing, zooplanktivory and survival of the mysid shrimp Mysis mixta. Journal of Experimental Marine Biology and Ecology 257: 269–280.

    Article  PubMed  Google Scholar 

  • France, R. L. & R. H. Peters, 1997. Ecosystem differences in the trophic enrichment of 13C in aquatic food webs. Canadian Journal of Fisheries and Aquatic Sciences 54: 1255–1258.

    Article  Google Scholar 

  • Gemmell, P., 1978. Feeding habits and structure of the gut of the Australian freshwater prawn Paratya australiensis Kemp (Crustacea, Caridea, Atyidae). Proceedings of the Linnean Society of New South Wales 103: 209–216.

    Google Scholar 

  • Goedkoop, W., N. Akerblom & M. H. Demandt, 2006. Trophic fractionation of carbon and nitrogen stable isotopes in Chironomus riparius reared on food of aquatic and terrestrial origin. Freshwater Biology 51: 878–886.

    Article  CAS  Google Scholar 

  • Hamill, K. D., 2001. Toxicity in benthic freshwater cyanobacteria (blue-green algae): first observations in New Zealand. New Zealand Journal of Marine and Freshwater Research 35: 1057–1059.

    Google Scholar 

  • Hancock, M. A. & S. E. Bunn, 1997. Population dynamics and life history of Paratya australiensis Kemp, 1917 (Decapoda: Atyidae) in upland rainforest streams, south-eastern Queensland, Australia. Marine and Freshwater Research 48: 361–369.

    Article  Google Scholar 

  • Howell, T., L. J. Laurenson, J. H. Myers & P. L. Jones, 2004. Spatial, temporal and size-class variation in the diet of estuary perch (Macquaria colonorum) in the Hopkins River, Victoria, Australia. Hydrobiologia 515: 29–37.

    Article  Google Scholar 

  • Johannsson, O. E., M. F. Leggett, L. G. Rudstam, M. R. Servos, M. Ali Mohammadian, G. Gal, R. M. Dermott & R. H. Hesslein, 2001. Diet of Mysis relicta in Lake Ontario as revealed by stable isotope and gut content analysis. Canadian Journal of Fisheries and Aquatic Sciences 58: 1975.

    Article  Google Scholar 

  • Kankaanpää, H., J. Holliday, H. Schröder, T. J. Goddard, R. von Fister & W. W. Carmichael, 2005. Cyanobacteria and prawn farming in northern New South Wales, Australia–a case study on cyanobacteria diversity and hepatotoxin bioaccumulation. Toxicology and Applied Pharmacology 203: 243–256.

    Article  PubMed  CAS  Google Scholar 

  • Keough, J. R., M. E. Sierszen & C. A. Hagley, 1996. Analysis of a Lake Superior coastal food web with stable isotope analysis. Limnology and Oceanography 41: 136–146.

    CAS  Google Scholar 

  • Koski, M., J. Engström & M. Viitasalo, 1999. Reproduction and survival of calanoid copepod Euryemora affinis fed with toxic and non-toxic cyanobacteria. Marine Ecology and Progress Series 186: 187–197.

    Article  Google Scholar 

  • Leberer, T. & S. G. Nelson, 2001. Factor affecting the distribution of atyidae shrimps in two tropical insular rivers. Pacific Science 55: 389–398.

    Article  Google Scholar 

  • Macko, S. A. & M. L. F. Estep, 1984. Microbial alteration of stable nitrogen and carbon isotopic compositions of organic matter. Organic Geochemistry 6: 787–790.

    Article  CAS  Google Scholar 

  • Magalhães, V. F., M. M. Marinho, P. Domingos, A. C. Oliveira, S. M. Costa, L. O. Azevedo & S. M. F. O. Azevedo, 2003. Microcystins (cyanobacteria hepatotoxins) bioaccumulation in fish and crustaceans from Sepetiba Bay (Brazil, RJ). Toxicon 42: 289–295.

    Article  PubMed  CAS  Google Scholar 

  • Matveev, V., L. Matveeva & G. J. Jones, 1994. Study of the Ability of Daphnia carinata King to Control Phytoplankton and Resist Cyanobacterial Toxicity: Implications for Biomanipulation in Australia. Australian Journal of Marine and Freshwater Research 45: 889–904.

    Article  Google Scholar 

  • McCutchan , J. H. Jr, W. M. Lewis Jr, C. Kendall & C. C. McGrath, 2003. Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102: 378–390.

    Article  CAS  Google Scholar 

  • Mez, K., K. A. Beattie, G. A. Codd, K. Hanselmann, B. Hauser, H. Naegeli & H. R. Preisig, 1997. Identification of a microcystin in benthic cyanobacteria linked to cattle deaths on alpine pastures in Switzerland. European Journal of Phycology 32: 111–117.

    Article  Google Scholar 

  • Miller, B., 1979. Ecology of the Little Black Cormorant, Phalacrocorax sulcirostris, and Little Pied Cormorant, P. melanoleucos, in Inland New South Wales I. Food and Feeding Habits. Australian Wildlife Research 6: 79–95.

    Article  Google Scholar 

  • Müller-Navarra, D., 1995. Evidence that a highly unsaturated fatty acid limits Daphnia growth in nature. Arch. Hydrobiol. 132: 297–307.

    Google Scholar 

  • NPWS, 2002. Myall Lakes National Park, Little Broughton Island and Stormpetrel Nature Reserves: Plan of Management. NSW National Parks and Wildlife Service, Hunter Region, NSW.

    Google Scholar 

  • Phillips, D. L. & J. W. Gregg, 2003. Source partitioning using stable isotopes: coping with too many sources. Oecologia 136: 261–269.

    Article  PubMed  Google Scholar 

  • Pinho, G. L. L., C. Moura da Rosa, J. S. Yunes, C. M. Luquet, A. Bianchini & J. M. Monserrat, 2003. Toxic effects of microcystins in the hepatopancreas of the estuarine crab Chasmagnathus granulatus (Decapoda, Grapsidae). Comparative Biochemistry and Physiology Part C 135: 459–468.

    PubMed  CAS  Google Scholar 

  • Piola, R. F., S. K. Moore & I. M. Suthers, 2006. Carbon and nitrogen stable isotope analysis of three types of oyster tissue in an impacted estuary. Estuarine, Coastal and Shelf Science 66: 255–266.

    Article  Google Scholar 

  • Porter, K. G. & G. D. Orcutt, 1980. Nutritional adequacy, manageability, and toxicity as factors that determine food quality of green and blue-green algae for Daphnia. American Society of Limnology and Oceanography. Special Symposium 3: 268–281.

    Google Scholar 

  • Pringle, C. M., 1996. Atyid shrimps (Decapoda: Atyidae) influence the spatial heterogeneity of algal communities over different scales in tropical montane streams, Puerto Rico. Freshwater Biology 35: 125–140.

    Article  Google Scholar 

  • Richardson, A. J., J. E. Growns & R. A. Cook, 2004. Distribution and life history of caridean shrimps in regulated lowland rivers in southern Australia. Marine and Freshwater Research 55: 295–308.

    Article  Google Scholar 

  • Russell-Hunter, W., 1970, Aquatic Productivity: An Introduction to Some Basic Aspects of Biological Oceanography and Limnology. Macmillan, New York.

    Google Scholar 

  • Sheldon, F. & K. F. Walker, 1997. Changes in biofilms induced by flow regulation could explain extinctions of aquatic snails in the lower River Murray, Australia. Hydrobiologia 347: 97–108.

    Article  CAS  Google Scholar 

  • Sheldon, F. & K. F. Walker, 1998. Spatial distribution of littoral invertebrates in the lower Murray–Darling River system, Australia. Marine and Freshwater Research 49: 171–182.

    Article  Google Scholar 

  • Vander Zanden, J. M. & J. B. Rasmussen, 2001. Variation in δ15N and δ13C trophic fractionation: Implications for aquatic food web studies. Limnology and Oceanography 46: 2061–2066.

    Article  CAS  Google Scholar 

  • Vasconcelos, V., S. Oliveira & F. O. Teles, 2001. Impact of a toxic and a non-toxic strain of Microcystis aeruginosa on the crayfish Procambarus clarkii. Toxicon 39: 1461–1470.

    Article  PubMed  CAS  Google Scholar 

  • Williams, W. D., 1977. Some aspects of the ecology of Paratya australiensis (Crustacea, Decapoda: Atyidae). Australian Journal of Marine and Freshwater Research 28: 403–415.

    Article  Google Scholar 

Download references

Acknowledgements

We thank S. Moore, K. Wright and J. Everett for field assistance and advice, and J. Wilson and our three referees for their helpful comments and many suggested improvements to the final manuscript. We also thank R. Diocares at Griffith University for all stable isotope sample analysis. This study was partly supported by funding from the New South Wales Department of Infrastructure, Planning and Natural Resources.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Richard F. Piola.

Additional information

Guest editors: J. Wilson, L. Bowling & J. Tibby

The Myall Lakes: patterns and processes in an unusual coastal lake system in eastern Australia

Rights and permissions

Reprints and permissions

About this article

Cite this article

Piola, R.F., Suthers, I.M. & Rissik, D. Carbon and nitrogen stable isotope analysis indicates freshwater shrimp Paratya australiensis Kemp, 1917 (Atyidae) assimilate cyanobacterial accumulations. Hydrobiologia 608, 121–132 (2008). https://doi.org/10.1007/s10750-008-9374-4

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-008-9374-4

Keywords

Navigation