, Volume 661, Issue 1, pp 65–79 | Cite as

Fish health changes in Lake Okaro, New Zealand: effects of nutrient remediation, season or eutrophication?

  • Michael J. Landman
  • Nicholas LingEmail author


The purpose of this investigation was to measure the in situ health of selected biota with respect to a large-scale application of an aluminium-amended zeolite (Z2G1) in Lake Okaro, New Zealand. We hypothesized that, based on previous laboratory toxicity testing, the Z2G1 application would have minimal or no significant health effects on lake fauna. To test this hypothesis, two sampling events were timed around the Z2G1 application to examine the health of two finfish species (Oncorhynchus mykiss and Gobiomorphus cotidianus) and crayfish (Paranephrops planifrons). Additionally, the same species were sampled from the neighbouring Lake Rerewhakaaitu in order to delineate seasonal and lake-specific effects. A general lack of aluminium accumulation in animal tissues following the application indicated that Z2G1-derived aluminium was not readily bioavailable. An unexplained osmoregulatory disturbance, indicated by increased blood plasma ion concentrations in Lake Okaro trout, was observed following the application, but could not be directly attributed to Z2G1 exposure. Changes in fish haematology over time and between lake populations were interpreted as physiological responses to seasonal changes in lake conditions. Using a broad range of specific and non-specific endpoints it was concluded that there were no obvious negative impacts on fish health resulting from Z2G1 exposure.


Eutrophication Lake restoration Zeolite Aluminium Fish health 



This research was funded by the Bay of Plenty Regional Council (EBOP) with additional support through the Foundation of Research, Science and Technology (Contract UOWX0505). The authors thank the following organisations and people for their help during this project: EBOP—John McIntosh, Andy Bruere, Paul Scholes and Rob Donald; Scion—Sean Taylor and Natalie Bleackley; Waikato University—Jeroen Brijs, Deniz Özkundakci, Dudley Bell, Warrick Powrie, Jenny Stockdill and Steve Cameron; Eastern Region Fish and Game—Rob Pitkethley; NIWA—Stephanie Parkyn and Aslan Wright-Stow. Special thanks are also due to Deniz Özkundakci for assistance with time/depth data plots.


  1. Agius, C. & R. J. Roberts, 2003. Melano-macrophage centres and their role in fish pathology. Journal of Fish Diseases 26: 499–509.CrossRefPubMedGoogle Scholar
  2. APHA, 1995. Standard Methods, 19th ed. American Public Health Association, Washington, DC.Google Scholar
  3. Bariero, R., R. E. Carlson, G. D. Cooke & A. W. Beals, 1988. The effects of a continuous application of aluminum sulfate on lotic benthic invertebrates. Lake and Reservoir Management 4: 63–72.CrossRefGoogle Scholar
  4. Buergel, P. M. & R. A. Soltero, 1983. The distribution and accumulation of aluminum in rainbow trout following a whole-lake alum treatment. Journal of Freshwater Ecology 2: 37–44.Google Scholar
  5. Chapman, M. A., V. H. Jolly & E. A. Flint, 1981. Limnology of Lake Rerewhakaaitu. New Zealand Journal of Marine and Freshwater Research 15: 207–224.CrossRefGoogle Scholar
  6. Cooke, G. D., E. B. Welch, A. B. Martin, D. G. Fulmer, J. B. Hyde & G. D. Schrieve, 1993. Effectiveness of Al, Ca and Fe salts for control of internal phosphorous loading in shallow and deep lakes. Hydrobiologia 253: 323–335.CrossRefGoogle Scholar
  7. Dacie, J. V. & S. M. Lewis, 1991. Basic Haematological Techniques. Practical Haematology. Churchill Livingstone, London, England: 37–85.Google Scholar
  8. De Vico, G., M. Cataldi, F. Carella, F. Marino & A. Passantino, 2008. Histological, histochemical and morphometric changes of splenic melanomacrophage centers (Smmcs) in sparicotyle-infected cultured sea breams (Sparus aurata). Immunopharmacology and Immunotoxicology 30: 27–35.CrossRefPubMedGoogle Scholar
  9. Doke, J. L., W. H. Funk, S. T. J. Juul & B. C. Moore, 1995. Habitat availability and benthic invertebrate population changes following alum treatment and hypolimnetic oxygenation in Newman Lake, Washington. Journal of Freshwater Ecology 10: 87–102.Google Scholar
  10. Effler, S. W., C. M. Brooks, M. T. Auer & S. M. Doerr, 1990. Free ammonia and toxicity criteria in a polluted urban lake. Research Journal of the Water Pollution Control Federation 62: 771–779.Google Scholar
  11. Fishelson, L., 2006. Cytomorphological alterations of the thymus, spleen, head-kidney, and liver in cardinal fish (Apogonidae, Teleostei) as bioindicators of stress. Journal of Morphology 267: 57–69.CrossRefPubMedGoogle Scholar
  12. Forsyth, D. J., S. J. Dryden, W. F. James & W. F. Vincent, 1988. The Lake Okaro ecosystem. 1. Background limnology. New Zealand Journal of Marine and Freshwater Research 22: 17–28.CrossRefGoogle Scholar
  13. Fourine, J. W., J. K. Summers, L. A. Courtney & V. D. Engle, 2001. Utility of splenic macrophage aggregates as an indicator of fish exposure to degraded environments. Journal of Aquatic Animal Health 13: 105–116.CrossRefGoogle Scholar
  14. Gensemer, R. W. & R. C. Playle, 1999. The bioavailability and toxicity of aluminium in aquatic environments. Critical Reviews in Environmental Sciences and Technology 29: 315–450.CrossRefGoogle Scholar
  15. Gibbs, M. & D. Ozkundakci, 2010. Effects of a modified zeolite on P and N processes and fluxes across the lake sediment–water interface using core incubations. Hydrobiologia. doi: 10.1007/s10750-009-0071-8.
  16. Gulati, R. D. & E. van Donk, 2002. Lakes in the Netherlands, their origin, eutrophication and restoration: state-of-the-art review. Hydrobiologia 478: 73–106.CrossRefGoogle Scholar
  17. Holk, K. & G. Lykkeboe, 1998. The impact of endurance training on arterial plasma K+ levels and swimming performance of rainbow trout. Journal of Experimental Biology 201: 1373–1380.PubMedGoogle Scholar
  18. Houston, A. H., N. Dobric & R. Kahurananga, 1996. The nature of hematological response in fish. Studies on rainbow trout Oncorhynchus mykiss exposed to simulated winter, spring and summer conditions. Fish Physiology and Biochemistry 15: 339–347.CrossRefGoogle Scholar
  19. Jeppesen, E., M. Sondergaard, J. P. Jensen & T. L. Lauridsen, 2003. Restoration of eutrophic lakes: a global perspective. In Kumagai, M. & W. F. Vincent (eds), Freshwater Management: Global Versus Local Perspectives. Springer-Verlag, Tokyo.Google Scholar
  20. Klapper, H., 2003. Technologies for lake restoration. Journal of Limnology 62: 73–90.Google Scholar
  21. Kortet, R., J. Taskinen, T. Sinisalo & I. Jokinen, 2003. Breeding-related seasonal changes in immunocompetence, health state and condition of the cyprinid fish, Rutilus rutilus, L. Biological Journal of the Linnean Society 78: 117–127.CrossRefGoogle Scholar
  22. Landman, M. J. & N. Ling, 2006. Lake Okareka and Tikitapu fish health monitoring 2006. Contract Report to Environment Bay of Plenty: 52.Google Scholar
  23. Landman, M. J., M. R. van den Heuvel & N. Ling, 2005. Relative sensitivities of common freshwater fish and invertebrates to acute hypoxia. New Zealand Journal of Marine and Freshwater Research 39: 1061–1067.CrossRefGoogle Scholar
  24. Lewandowski, J., I. Schauser & M. Hupfer, 2003. Long term effects of phosphorus precipitations with alum in hypereutrophic Lake Süßer See (Germany). Water Research 37: 3194–3204.CrossRefPubMedGoogle Scholar
  25. Lochmiller, R. L., J. D. Weichman & A. V. Zale, 1989. Hematological assessment of temperature and oxygen stress in a reservoir population of striped bass (Morone saxatilis). Comparative Biochemistry and Physiology Part A 93: 535–541.CrossRefGoogle Scholar
  26. Mallat, J., 1985. Fish gill structural changes induced by toxicants and other irritants, a statistical review. Canadian Journal of Fisheries and Aquatic Sciences 42: 630–648.CrossRefGoogle Scholar
  27. Marti-Cardona, B., T. E. Steissberg, S. G. Schladow & S. J. Hook, 2008. Relating fish kills to upwellings and wind patterns in the Salton Sea. Hydrobiologia 604: 85–95.CrossRefGoogle Scholar
  28. McCormick, S. D., 1990. Cortisol directly stimulates differentiation of chlorine cells in tilapia opercular membrane. The American Journal of Physiology 28: 857–863.Google Scholar
  29. Mehner, T., M. Diekmann, T. Gonsiorczyk, P. Kasprzak, R. Koschel, L. Krienitz, M. Rumpf, M. Schulz & G. Wauer, 2008. Rapid recovery from eutrophication of a stratified lake by disruption of internal nutrient load. Ecosystems 11: 1142–1156.CrossRefGoogle Scholar
  30. Özkundakci, D., I. C. Duggan & D. P. Hamilton, 2009. Does sediment capping have post-application effects on zooplankton and phytoplankton? Hydrobiologia. doi: 10.1007/s10750-009-9938-y.
  31. Özkundakci, D., D. P. Hamilton & P. Scholes, 2010. Effect of intensive catchment and in-lake restoration procedures on phosphorus concentrations in a eutrophic lake. Ecological Engineering 36: 396–405.CrossRefGoogle Scholar
  32. Parkyn, S. M., C. H. Hickey & S. J. Clearwater, 2010. Measuring sub-lethal effects on freshwater crayfish (Paranephrops planifrons) behaviour and physiology: laboratory and in situ exposure to modified zeolite. Hydrobiologia. doi: 10.10750-010-0241-8.
  33. Paul, W. J., D. P. Hamilton & M. M. Gibbs, 2008. Lose-dose alum application trialled as a management tool for internal nutrient loads in Lake Okaro, New Zealand. New Zealand Journal of Marine and Freshwater Research 42: 207–217.CrossRefGoogle Scholar
  34. Perry, S. F., 1997. The chloride cell: structure and function in the gills of freshwater fishes. Annual Review of Physiology 59: 325–347.CrossRefPubMedGoogle Scholar
  35. Perry, S. F., 1998. Relationship between branchial chloride cells and gas transfer in freshwater fish. Comparative Biochemistry and Physiology A Molecular and Integrative Physiology 119: 9–16.CrossRefGoogle Scholar
  36. Pickering, A. D., 1986. Changes in blood cell composition of the brown trout, Salmo trutta L., during the spawning season. Journal of Fish Biology 29: 335–347.CrossRefGoogle Scholar
  37. Pickering, A. D. & T. G. Pottinger, 1987. Lymphocytopenia and interrenal activity during sexual maturation in the brown trout, Salmo trutta L. Journal of Fish Biology 30: 41–50.CrossRefGoogle Scholar
  38. Pilgrim, K. M. & P. L. Brezonik, 2005. Evaluation of the potential adverse effects of lake inflow treatment with alum. Lake and Reservoir Management 21: 78–88.Google Scholar
  39. Postlethwaite, E. K. & D. G. McDonald, 1995. Machanisms of Na+ and Cl regulation in freshwater-adapted rainbow trout (Oncorhynchus mykiss) during exercise and stress. Journal of Experimental Biology 198: 295–304.PubMedGoogle Scholar
  40. Randall, S., D. Harper & B. Brierley, 1999. Ecological and ecophysiological impacts of ferric dosing in reservoirs. Hydrobiologia 195(196): 355–364.CrossRefGoogle Scholar
  41. Robb, M., B. Greenop, Z. Goss, G. Douglas & J. Adeney, 2003. Application of Phoslock™, an innovative phosphorus binding clay, to two Western Australian waterways: preliminary findings. Hydrobiologia 494: 237–243.CrossRefGoogle Scholar
  42. Scott, D. M., M. C. Lucas & R. W. Wilson, 2005. The effect of high pH on ion balance, nitrogen excretion and behaviour in freshwater fish from an eutrophic lake: a laboratory and field study. Aquatic Toxicology 73: 31–43.CrossRefPubMedGoogle Scholar
  43. Smeltzer, E., 1990. A successful alum/aluminate treatment of Lake Morey, Vermont. Lake and Reservoir Management 6: 9–19.CrossRefGoogle Scholar
  44. Smeltzer, E., R. A. Kirn & S. Fiske, 1999. Long-term water quality and biological effects of alum treatment of Lake Morey, Vermont. Lake and Reservoir Management 15: 173–184.CrossRefGoogle Scholar
  45. Smith, V., 2003. Eutrophication of freshwater and coastal marine ecosystems—a global problem. Environmental Science and Pollution Research 10: 126–139.CrossRefPubMedGoogle Scholar
  46. Smith, V. H., G. D. Tilman & J. C. Nekola, 1999. Eutrophication: impacts of excess nutrient inputs on freshwater, marine, and terrestrial ecosystems. Environmental Pollution 100: 179–196.CrossRefPubMedGoogle Scholar
  47. Sokal, R. R. & F. J. Rohlf, 1973. Introduction to Biostatistics. W. H. Freeman and Company, San Francisco, CA.Google Scholar
  48. Tierney, K. B., A. P. Farrell & C. J. Kennedy, 2004. The differential leucocyte landscape of four teleosts: juvenile Oncorhynchus kisutch, Clupea pallasi, Culaea inconstans and Pimephales promelas. Journal of Fish Biology 65: 906–919.CrossRefGoogle Scholar
  49. USEPA, 1987. Determination of metals in fish tissue by inductively coupled plasma-atomic emission spectrometry. EPA Method 200.11, Revision 1.3, April 1987.Google Scholar
  50. Van Hullebusch, E., V. Deluchat, P. M. Chazal & M. Baudu, 2002. Environmental impact of two successive chemical treatments in a shallow eutrophied lake: Part I. Case of aluminium sulphate. Environmental Pollution 120: 616–626.CrossRefGoogle Scholar
  51. Welch, E. B. & G. D. Cooke, 1999. Effectiveness and longevity of phosphorus inactivation with alum. Lake and Reservoir Management 15: 5–27.CrossRefGoogle Scholar
  52. Wilkie, M. P. & C. M. Wood, 1991. Nitrogenous waste excretion, acid-base regulation, and ionoregulation in rainbow trout (Oncorhynchus mykiss) exposed to extremely alkaline water. Physiological Zoology 64: 1069–1086.Google Scholar
  53. Wilkie, M. P. & C. M. Wood, 1996. The adaptations of fish to extremely alkaline environments. Comparative Biochemistry and Physiology B 113: 665–673.CrossRefGoogle Scholar
  54. Wolke, R. E., 1992. Piscine macrophage aggregates: a review. Annual Review of Fish Diseases 2: 91–108.CrossRefGoogle Scholar
  55. Wood, C. M., 1989. The physiological problems of fish in acid waters. In Morris, R., E. W. Taylor, D. J. A. Brown & J. A. Brown (eds), Acid Toxicity and Aquatic Animals. Cambridge University Press, Cambridge: 125–152.Google Scholar
  56. Wood, C. M., 2001. Toxic responses of the gill. In Schlenk, D. & W. H. Benson (eds), Target Organ Toxicity in Marine and Freshwater Teleosts: Volume 1—Organs. Taylor and Francis, London, UK: 1–89.Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  1. 1.Sustainable Design, ScionRotoruaNew Zealand
  2. 2.Centre for Biodiversity and Ecology ResearchUniversity of WaikatoHamiltonNew Zealand
  3. 3.Department of Biological SciencesThe University of WaikatoHamiltonNew Zealand

Personalised recommendations