Abstract
The spatial and temporal variability of potentially harmful phytoplankton was examined in the oyster-growing estuaries of New South Wales. Forty-five taxa from 31 estuaries were identified from 2005 to 2009. Harmful species richness was latitudinally graded for rivers, with increasing number of taxa southward. There were significant differences (within an estuary) in harmful species abundance and richness for 11 of 21 estuaries tested. Where differences were observed, these were predominately due to species belonging to the Pseudo-nitzschia delicatissima group, Dinophysis acuminata, Dictyocha octonaria and Prorocentrum cordatum with a consistent upstream versus downstream pattern emerging. Temporal (seasonal or interannual) patterns in harmful phytoplankton within and among estuaries were highly variable. Examination of harmful phytoplankton in relation to recognised estuary disturbance measures revealed species abundance correlated to estuary modification levels and flushing time, with modified, slow flushing estuaries having higher abundance. Harmful species richness correlated with bioregion, estuary modification levels and estuary class, with southern, unmodified lakes demonstrating greater species density. Predicting how these risk taxa and risk zones may change with further estuary disturbance and projected climate warming will require more focused, smaller scale studies aimed at a deeper understanding of species-specific ecology and bloom mechanisms. Coupled with this consideration, there is an imperative for further taxonomic, ecological and toxicological investigations into poorly understood taxa (e.g. Pseudo-nitzschia).
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Anderson, D. M., Burkholder, J. M., Cochlan, W. P., Glibert, P. M., Gobler, C. J., Heil, C. A., et al. (2008). Harmful algal blooms and eutrophication: examining linkages from selected coastal regions of the United States. Harmful Algae, 8(1), 39–53.
Clarke, K.R., & Gorley, R.N. (2006). PRIMER v5 (& v6): User manual/tutorial, PRIMER-E. (pp. 1–192). Plymouth UK.
Clarke, K.R., & Warwick, R.M. (2001). Change in marine communities: an approach to statistical analysis and interpretation. 2nd edition: PRIMER-E. (pp. 1–172). Plymouth, UK.
Cloern, J. E. (2001). Our evolving conceptual model of the coastal eutrophication problem. Marine Ecology-Progress Series, 210, 223–253.
Cloern, J. E., & Jassby, A. D. (2010). Patterns and scales of phytoplankton variability in estuarine-coastal ecosystems. Estuaries and Coasts, 33(2), 230–241.
Davis, J. R., & Koop, K. (2006). Eutrophication in Australian rivers, reservoirs and estuaries—a southern hemisphere perspective on the science and its implications. Hydrobiologia, 559, 23–76.
Falkowski, P. G., Barber, R. T., & Smetacek, V. (1998). Biogeochemical controls and feedbacks on ocean primary production. Science, 281, 200–206.
Fan, C., & Glibert, P. M. (2005). Effects of light on nitrogen and carbon uptake during a Prorocentrum minimum bloom. Harmful Algae, 4(3), 629–641.
Fan, C., Glibert, P. M., & Burkholder, J. M. (2003). Characterization of the affinity for nitrogen, uptake kinetics, and environmental relationships for Prorocentrum minimum in natural blooms and laboratory cultures. Harmful Algae, 2(4), 283–299.
Fehling, J., Davidson, K., Bolch, C., & Tett, P. (2006). Seasonality of Pseudo-nitzschia spp. (Bacillariophyceae) in western Scottish waters. Marine Ecology-Progress Series, 323, 91–105.
Figueiras, F.G., Pitcher, G.C., Estrada, M. (2006). Harmful algal bloom dynamics in relation to physical processes. In Granéli, E. and Turner, J.T. (Eds) Ecology of harmful algae. Springer, pp. 127-138.
Fritz, L., & Triemer, R. E. (1985). A rapid simple technique utilizing calcofluor white M2R for the visualization of dinoflagellate thecal plates. Journal of Phycology, 21(4), 662–664.
Glibert, P. M., Burkholder, J. M., Graneli, E., & Anderson, D. M. (2008). Advances and insights in the complex relationships between eutrophication and HABs: preface to the special issue. Harmful Algae, 8(1), 1–2.
Glibert, P. M., Mayorga, E., & Seitzinger, S. (2008). Prorocentrum minimum tracks anthropogenic nitrogen and phosphorus inputs on a global basis: application of spatially explicit nutrient export models. Harmful Algae, 8(1), 33–38.
Glibert, P. M., Fullerton, D., Burkholder, J. M., Cornwell, J. C., & Kana, T. M. (2011). Ecological stoichiometry, biogeochemical cycling, invasive species, and aquatic food webs: San Francisco estuary and comparative systems. Reviews in Fisheries Science, 19(4), 358–417.
Glibert, P. M., Burkholder, J. M., & Kana, T. M. (2012). Recent insights about relationships between nutrient availability, forms, and stoichiometry, and the distribution, ecophysiology, and food web effects of pelagic and benthic Prorocentrum species. Harmful Algae, 14, 231–259.
Hallegraeff, G. M. (1993). A review of harmful algal blooms and their apparent global increase. Phycologia, 32(2), 79–99.
Hallegraeff, G. M. (1994). Species of the diatom genus Pseudo-nitzschia in Australian Waters. Botanica Marina, 37(5), 397–412.
Hallegraeff, G. M. (2010). Ocean climate change, phytoplankton community responses, and harmful algal blooms: a formidable predictive challenge. Journal of Phycology, 46(2), 220–235.
Hallegraeff, G. M., Anderson, D. M., & Cembella, A. D. (Eds.). (2003). Manual on harmful marine microgalgae (p. 793). Paris: UNESCO Publishing.
Hasle, G. R. (2002). Are most of the domoic acid-producing species of the diatom genus Pseudo-nitzschia cosmopolites? Harmful Algae, 1(2), 137–146.
Heil, C. A., Glibert, P. M., & Fan, C. (2005). Prorocentrum minimum (Pavillard) Schiller: a review of a harmful algal bloom species of growing worldwide importance. Harmful Algae, 4(3), 449–470.
Heisler, J., Glibert, P. M., Burkholder, J. M., Anderson, D. M., Cochlan, W., & Dennison, W. C. (2008). Eutrophication and harmful algal blooms: a scientific consensus. Harmful Algae, 8(1), 3–13.
Henriksen, P., Knipschildt, F., Moestrup, Ø., & Thomsen, H. A. (1993). Autecology, life history and toxicology of the silicoflagellate Dictyocha speculum (Silicoflagellata, Dictyochophyceae). Phycologia, 32(1), 29–39.
Hernandez-Becerril, D. U., Alonso-Rodriguez, R., Alvarez-Gongora, C., Baron-Campis, S. A., Ceballos-Corona, G., Herrera-Silveira, J., et al. (2007). Toxic and harmful marine phytoplankton and microalgae (HABs) in Mexican Coasts. Journal of Environmental Science and Health Part a-Toxic/Hazardous Substances & Environmental Engineering, 42(10), 1349–1363.
Hill, M. O. (1973). Diversity and evenness: a unifying notation and its consequences. Ecology, 54(2), 427–432.
Integrated Marine and Coastal Regionalisation of Australia (IMCRA), 2011. http://www.environment.gov.au/coasts/mbp/imcra/index.html
Jester, R., Lefebvre, K., Langlois, G., Vigilant, V., Baugh, K., & Silver, M. W. (2009). A shift in the dominant toxin-producing algal species in central California alters phycotoxins in food webs. Harmful Algae, 8(2), 291–298.
Kromkamp, J. C., & Van Engeland, T. (2010). Changes in phytoplankton biomass in the Western Scheldt estuary during the period 1978-2006. Estuaries and Coasts, 33(2), 270–285.
Lapworth, C., Hallegraeff, G.M., & Ajani, P.A. (2001). Identification of domoic-acid producing Pseudo-nitzschia species in Australian waters. In G. M. Hallegraeff, Blackburn, S.I., Bolch, C.J. and Lewis, R.J. (eds) (Ed.), Harmful algal blooms 2000 (pp. 39-42): Intergovernmental Oceanographic Commission of UNESCO 2001.
Leibold, M. A., Holyoak, M., Mouquet, N., Amarasekare, P., Chase, J. M., Hoopes, M. F., et al. (2004). The metacommunity concept: a framework for multi-scale community ecology. Ecology Letters, 7(7), 601–613.
Lelong, A., Hégaret, H., Soudant, P., & Bates, S. S. (2012). Pseudo-nitzschia (Bacillariophyceae) species, domoic acid and amnesic shellfish poisoning: revisiting previous paradigms. Phycologia, 51(2), 168–216.
Li, Y., Lü, S., Jiang, T., Xiao, Y., & You, S. (2011). Environmental factors and seasonal dynamics of Prorocentrum populations in Nanji Islands National Nature Reserve, East China Sea. Harmful Algae, 10(5), 426–432.
Lucas, L. V., & Cloern, J. E. (2002). Effects of tidal shallowing and deepening on phytoplankton production dynamics: a modeling study. Estuaries, 25(4A), 497–507.
Macintyre, H. L., Stutes, A. L., Smith, W. L., Dorsey, C. P., Abraham, A., & Dickey, R. W. (2011). Environmental correlates of community composition and toxicity during a bloom of Pseudo-nitzschia spp. in the northern Gulf of Mexico. Journal of Plankton Research, 33(2), 273–295.
Margalef, R. (1978). Life-forms of phytoplankton as survival alternatives in an unstable environment. Oceanology Acta, 1, 493–509.
Moore, S. K., Trainer, V. L., Mantua, N. J., Parker, M. S., Laws, E. A., & Backer, L. C. (2008). Impacts of climate variability and future climate change on harmful algal blooms and human health. Environmental Health, 7. doi:10.1186/1476-069x-7-s2-s4.
National Land and Water Resources Audit (NLWRA) 2001. Australian Water Resources Assessment 2000 http://www.anra.gov.au/topics/water/pubs/national/water_contents.html
New South Wales Food Authority, 2011. http://www.foodauthority.nsw.gov.au/industry/industry-sector-requirements/shellfish
New South Wales Industry and Investment (NSW I & I), 2010. Aquaculture Production Report 2009-2010, 17 pp.
NSW Marine Biotoxin Management Plan (2011). NSW Shellfish Program NSW/FA/FI115/1105, NSW Food Authority.
O’Connor W. A., Dove M. (2009). The changing face of oyster culture in New South Wales, Australia. Journal of Shellfish Research, 28, 803–812.
Ozcoasts (2011). http://www.ozcoasts.gov.au. Accessed 1 Apr 2011.
Phlips, E. J., Badylak, S., Christman, M. C., & Lasi, M. A. (2010). Climatic trends and temporal patterns of phytoplankton composition, abundance, and succession in the Indian River Lagoon, Florida, USA. Estuaries and Coasts, 33(2), 498–512.
Phlips, E. J., Badylak, S., Christman, M. Wolny, J., Brame, J. Garland, J. Hall, L., Hart, J., Landsberg, J., Lasi, M., Lockwood, J., Paperno, R., Scheidt, D., Staples, A., Steidinger, K. (2011). Scales of temporal and spatial variability in the distribution of harmful algae species in the Indian River Lagoon, Florida, USA. Harmful Algae, 10, 277–290.
Pitcher, G. C. (2012). Harmful algae-the requirement for species-specific information. Harmful Algae, 14, 1–4.
Puigserver, M., Monerris, N., Pablo, J., Alos, J., & Moya, G. (2010). Abundance patterns of the toxic phytoplankton in coastal waters of the Balearic Archipelago (NW Mediterranean Sea): a multivariate approach. Hydrobiologia, 644(1), 145–157.
Reguera, B., Velo-Suárez, L., Raine, R., & Park, M. G. (2012). Harmful Dinophysis species: a review. Harmful Algae, 14, 87–106.
Rhodes, R. H., Bertler, N. A. N., Baker, J. A., Sneed, S. B., Oerter, H., & Arrigo, K. R. (2009). Sea ice variability and primary productivity in the Ross Sea, Antarctica, from methylsulphonate snow record. Geophysical Research Letters, 36, L10704. doi:10.1029/2009GL037311.
Rigual-Hernandez, A. S., Barcena, M. A., Sierro, F. J., Flores, J. A., Hernandez-Almeida, I., Sanchez-Vidal, A., et al. (2010). Seasonal to interannual variability and geographic distribution of the silicoflagellate fluxes in the Western Mediterranean. Mar. Micropaleontol., 77, 46–57.
Rissik, D., Doherty, M., & van Senden, D. (2006). A management focused investigation into phytoplankton blooms in a sub-tropical Australian estuary. Aquatic Ecosystem Health & Management, 9(3), 365–378.
Roper, T., Creese, B., Scanes, P., Stephens, K., Williams, R., Dela-Cruz, J., et al. (2011). Assessing the condition of estuaries and coastal lake ecosystems in NSW. NSW State of the Catchments 2010 (p. 239). NSW: Office of Environment and Heritage.
Roy, P. S., Williams, R. J., Jones, A. R., Yassini, I., Gibbs, P. J., Coates, B., et al. (2001). Structure and function of south-east Australian estuaries. Estuarine, Coastal and Shelf Science, 53(3), 351–384.
Scanes, P., Coade, G., Doherty, M., & Hill, R. (2007). Evaluation of the utility of water quality based indicators of estuarine lagoon condition in NSW, Australia. Estuarine, Coastal and Shelf Science, 74(1–2), 306–319.
Smayda, T. J., & Reynolds, C. S. (2001). Community assembly in marine phytoplankton: application of recent models to harmful dinoflagellate blooms. Journal of Plankton Research, 23(5), 447–461.
Smayda, T. J., & Reynolds, C. S. (2003). Strategies of marine dinoflagellate survival and some rules of assembly. Journal of Sea Research, 49(2), 95–106.
Sunda, W. G., & Shertzer, K. W. (2012). Modeling ecosystem disruptive algal blooms: positive feedback mechanisms. Marine Ecology Progress Series, 447, 31–47.
Takahashi, E., Yu, Q., Eaglesham, G., Connell, D. W., McBroom, J., & Costanzo, S. (2007). Occurrence and seasonal variations of algal toxins in water, phytoplankton and shellfish from North Stradbroke Island, Queensland, Australia. Marine Environmental Research, 64(4), 429–442.
Thomas, A. C., Weatherbee, R., Xue, H., & Liu, G. (2010). Interannual variability of shellfish toxicity in the Gulf of Maine: time and space patterns and links to environmental variability. Harmful Algae, 9(5), 458–480.
Thompson, P. A., Baird, M. E., Ingleton, T., & Doblin, M. A. (2009). Long-term changes in temperate Australian coastal waters: implications for phytoplankton. Marine Ecology-Progress Series, 394, 1–19.
Trainer, V. L., Bates, S. S., Lundholm, N., Thessen, A. E., Cochlan, W. P., Adams, N. G., et al. (2012). Pseudo-nitzschia physiological ecology, phylogeny, toxicity, monitoring and impacts on ecosystem health. Harmful Algae, 14, 271–300.
Underwood, A. J. (1997). Experiments in ecology: Their logical design and interpretation using analysis of variance (p. 524). Cambridge: Cambridge University Press.
UNESCO (1996 ). Design and implementation of some harmful algal monitoring systems. International Oceanographic Committee Technical Series No. 44.
van Dolah, F.M. (2000). Marine algal toxins: origins, health effects, and their increased occurrence. Environmental Health Perspectives, 108, 133–141.
Vershinin, A. O., & Orlova, T. Y. (2008). Toxic and harmful algae in the coastal waters of Russia. Oceanology, 48(4), 524–537.
Zingone, A., Phlips, E. J., & Harrison, P. J. (2010). Multiscale variability of twenty-two coastal phytoplankton time series: a global scale comparison. Estuaries and Coasts, 33(2), 224–229.
Acknowledgments
The authors would like to thank Anthony Zammit (NSW Food Authority), Mr. Jamie Potts (NSW Office of the Environment and Heritage), Dr. Shauna Murray (University of New South Wales), Dr. Ana Rubio (University of Wollongong) and Professor Gustaaf Hallegraeff (University of Tasmania) for the useful discussions throughout this study. This work was supported by an Australian Postgraduate Award, New South Wales Food Authority and the Australian Government’s Australian Biological Resource Study (CT210-19).
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Ajani, P., Brett, S., Krogh, M. et al. The risk of harmful algal blooms (HABs) in the oyster-growing estuaries of New South Wales, Australia. Environ Monit Assess 185, 5295–5316 (2013). https://doi.org/10.1007/s10661-012-2946-9
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DOI: https://doi.org/10.1007/s10661-012-2946-9