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In situ river experiments to explore variability in Microcoleus autumnalis mat expansion

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Abstract

Proliferations of benthic mats dominated by anatoxin-producing Microcoleus autumnalis (basionym Phormidium autumnale) pose an increasing health risk to human and animals worldwide. This study assessed M. autumnalis mats in two in situ experiments undertaken at three spatial scales: (1) reach-scale along a river; (2) reach-scale, focusing on two sites upstream and downstream of a tributary with substantial differences in naturally occurring M. autumnalis; and (3) patch-scale differences in light intensity. Most studies exploring drivers of proliferation have surveyed natural populations with correlative analyses; these in situ experiments aimed to validate previously hypothesised drivers. In experiment one, M. autumnalis mat area and expansion tended to increase downstream. This longitudinal variation was partially associated with increases in dissolved inorganic nitrogen, fine sediment and associated biologically available phosphorus. M. autumnalis mat area differed markedly at sites above and below the most downstream tributary. A second experiment with additional parameters (metals, grazing and light) was undertaken in this reach. None of the parameters conclusively explained differences in mat area, although numerous metals were identified for further investigation with a controlled experimental approach. These results posit that there are multiple non-linear drivers of M. autumnalis proliferation and their hierarchy of importance varies amongst sites.

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Data availability statement

Authors can confirm that most of the raw data are included in the article and/or its supplementary information files, and the remainder is available upon request from the corresponding author.

References

  • Agnieszka, P.-S., F. Edyta & F. Janusz, 2001. Phormidium autumnale (Cyanobacteria) defense against three ciliate grazer species. Aquatic Microbial Ecology 23: 237–244.

    Google Scholar 

  • Biggs, B. J., 1995. The contribution of flood disturbance, catchment geology and land use to the habitat template of periphyton in stream ecosystems. Freshwater Biology 33: 419–438.

    Google Scholar 

  • Bouma-Gregson, K., R. M. Kudela & M. E. Power, 2018. Widespread anatoxin-a detection in benthic cyanobacterial mats throughout a river network. PLoS ONE 13: e0197669.

    PubMed  PubMed Central  Google Scholar 

  • Carmichael, W. W., 1994. The toxins of cyanobacteria. Scientific American 270: 78–86.

    CAS  PubMed  Google Scholar 

  • Chadderton, W., 1988. Faunal and chemical characteristics of some Stewart Island streams. New Zealand Natural Sciences 15: 43–50.

    Google Scholar 

  • Chapman, M. A., M. H. Lewis & M. J. Winterbourn, 2011. Guide to the Freshwater Crustacea of New Zealand. New Zealand Freshwater Sciences Society, Christchurch.

    Google Scholar 

  • Christensen, V. G. & E. Khan, 2020. Freshwater neurotoxins and concerns for human, animal, and ecosystem health: a review of anatoxin-a and saxitoxin. Science of The Total Environment 736: 139515.

    CAS  Google Scholar 

  • Codd, G. A., 1995. Cyanobacterial toxins: occurrence, properties and biological significance. Water Science and Technology 32: 149–156.

    CAS  Google Scholar 

  • Codd, G. A., 2000. Cyanobacterial toxins, the perception of water quality, and the prioritisation of eutrophication control. Ecological Engineering 16: 51–60.

    Google Scholar 

  • Codd, G. A., S. G. Bell, K. Kaya, C. J. Ward, K. A. Beattie & J. S. Metcalf, 1999. Cyanobacterial toxins, exposure routes and human health. European Journal of Phycology 34: 405–415.

    Google Scholar 

  • Codd, G. A., L. F. Morrison & J. S. Metcalf, 2005. Cyanobacterial toxins: risk management for health protection. Toxicology and Applied Pharmacology 203: 264–272.

    CAS  PubMed  Google Scholar 

  • Cowie, B., 1980. Community dynamics of the bethnic fauna in a West Coast stream ecosystem. PhD thesis, University of Canterbury, Christchurch.

  • Drury, B., J. Scott, E. J. Rosi-Marshall & J. J. Kelly, 2013. Triclosan exposure increases triclosan resistance and influences taxonomic composition of benthic bacterial communities. Environmental Science & Technology 47: 8923–8930.

    CAS  Google Scholar 

  • Echenique-Subiabre, I., M. Tenon, J. F. Humbert & C. Quiblier, 2018. Spatial and temporal variability in the development and potential toxicity of Phormidium biofilms in the Tarn River, France. Toxins 10: 418.

    CAS  PubMed Central  Google Scholar 

  • Faassen, E. J., L. Harkema, L. Begeman & M. Lurling, 2012. First report of (homo)anatoxin-a and dog neurotoxicosis after ingestion of benthic cyanobacteria in The Netherlands. Toxicon 60: 378–384.

    CAS  PubMed  Google Scholar 

  • Facey, J. A., S. C. Apte & S. M. Mitrovic, 2019. A review of the effect of trace metals on freshwater cyanobacterial growth and toxin production. Toxins 11: 643.

    CAS  PubMed Central  Google Scholar 

  • Fox, J., M. Friendly & G. Monette, 2018. heplots: Visualizing tests in multivariate linear models. R package version 1.3-5.

  • Francis, G., 1878. Poisonous Australian lake. Nature 18: 11–12.

    Google Scholar 

  • Gibbs, M. & B. Woodward, 2017. CSSI-based sediment source tracking study for the Maitai River, Nelson. Prepared for Nelson City Council. National Institute of Water & Atmospheric Research Report No. 2017256HN, 33.

  • Gugger, M., S. Lenoir, C. Berger, A. Ledreux, J.-C. Druart, J.-F. Humbert, C. Guette & C. Bernard, 2005. First report in a river in France of the benthic cyanobacterium Phormidium favosum producing anatoxin-a associated with dog neurotoxicosis. Toxicon 45: 919–928.

    CAS  PubMed  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 

  • Harland, F. M. J., S. A. Wood, E. Moltchanova, W. M. Williamson & S. Gaw, 2013. Phormidium autumnale growth and anatoxin – a production under iron and copper stress. Toxins 5: 2504–2521.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Harland, F. M. J., S. A. Wood, P. A. Broady, S. Gaw & W. M. Williamson, 2014. Polyphasic studies of cyanobacterial strains isolated from benthic freshwater mats in Canterbury, New Zealand. New Zealand Journal of Botany 52: 116–135.

    Google Scholar 

  • Hart, D. D., B. J. F. Biggs, V. I. Nikora & C. A. Flinders, 2013. Flow effects on periphyton patches and their ecological consequences in a New Zealand river. Freshwater Biology 58: 1588–1602.

    Google Scholar 

  • Heath, M. W., S. A. Wood & K. G. Ryan, 2010. Polyphasic assessment of fresh-water benthic mat-forming cyanobacteria isolated from New Zealand. FEMS Microbiology Ecology 73: 95–109.

    CAS  PubMed  Google Scholar 

  • Heath, M. W., S. A. Wood & K. G. Ryan, 2011. Spatial and temporal variability in Phormidium mats and associated anatoxin-a and homoanatoxin-a in two New Zealand rivers. Aquatic Microbial Ecology 64: 69–79.

    Google Scholar 

  • Heath, M. W., S. A. Wood, K. Brasell, R. Young & K. Ryan, 2013. Development of habitat suitability criteria and in-stream habitat assessment for the benthic cyanobacteria Phormidium. River Research and Applications 31: 98–108.

    Google Scholar 

  • Hill, W. R. & S. E. Fanta, 2008. Phosphorus and light colimit periphyton growth at subsaturating irradiances. Freshwater Biology 53: 215–225.

    CAS  Google Scholar 

  • Holomuzki, J. R. & B. J. F. Biggs, 2006. Food limitation affects algivory and grazer performance for New Zealand stream macroinvertebrates. Hydrobiologia 561: 83–94.

    Google Scholar 

  • Hsieh-Lo, M., G. Castillo, M. A. Ochoa-Becerra & L. Mojica, 2019. Phycocyanin and phycoerythrin: strategies to improve production yield and chemical stability. Algal Research 42: 101600.

    Google Scholar 

  • Huisman, J., G. A. Codd, H. W. Paerl, B. W. Ibelings, J. M. H. Verspagen & P. M. Visser, 2018. Cyanobacterial blooms. Nature Reviews Microbiology 16: 471–483.

    CAS  PubMed  Google Scholar 

  • Jaarsma, N., S. De Boer, C. Townsend, R. Thompson & E. Edwards, 1998. Characterising food-webs in two New Zealand streams. New Zealand Journal of Marine and Freshwater Research 32: 271–286.

    Google Scholar 

  • Kelly, L. T., K. G. Ryan & S. A. Wood, 2019. Differential strain response in alkaline phosphatase activity to available phosphorus in Microcoleus autumnalis. Harmful Algae 89: 101664.

    CAS  PubMed  Google Scholar 

  • Kuznetsova, A., P. B. Brockhoff & R. H. B. Christensen, 2017. lmerTest Package: tests in linear mixed effects models. Journal of Statistical Software 82: 1–26.

    Google Scholar 

  • Lester, P. J., S. F. Mitchell & D. Scott, 1994. Effects of riparian willow trees (Salix fragilis) on macroinvertebrate densities in two small Central Otago, New Zealand, streams. New Zealand Journal of Marine and Freshwater Research 28: 267–276.

    Google Scholar 

  • Maule, A. & S. J. L. Wright, 1984. Herbicide effects on the population growth of some green algae and cyanobacteria. Journal of Applied Bacteriology 57: 369–379.

    CAS  Google Scholar 

  • McAllister, T. G., 2014. Environmental factors that promote Phormidium blooms in Canterbury rivers. In Waterways Centre for Freshwater Management Report, WCFM, p. 44.

  • McAllister, T. G., S. A. Wood & I. Hawes, 2016. The rise of toxic benthic Phormidium proliferations: a review of their taxonomy, distribution, toxin content and factors regulating prevalence and increased severity. Harmful Algae 55: 282–294.

    CAS  PubMed  Google Scholar 

  • McAllister, T. G., S. A. Wood, J. Atalah & I. Hawes, 2018a. Spatiotemporal dynamics of Phormidium cover and anatoxin concentrations in eight New Zealand rivers with contrasting nutrient and flow regimes. Science of the Total Environment 612: 71–80.

    CAS  Google Scholar 

  • McAllister, T. G., S. A. Wood, M. J. Greenwood, F. Broghammer & I. Hawes, 2018b. The effects of velocity and nitrate on Phormidium accrual cycles: a stream mesocosm experiment. Freshwater Science 37: 496–509.

    Google Scholar 

  • McAllister, T. G., S. Wood, E. Mackenzie & I. Hawes, 2020. Reach and mat scale dynamics of the benthic cyanobacterium Microcoleus along velocity and nitrate gradients in three New Zealand rivers. Canadian Journal of Fisheries and Aquatic Sciences 77: 401–412.

    CAS  Google Scholar 

  • Méjean, A., G. Paci, V. Gautier & O. Ploux, 2014. Biosynthesis of anatoxin-a and analogues (anatoxins) in cyanobacteria. Toxicon 91: 15–22.

    PubMed  Google Scholar 

  • MfE and MoH, 2009. New Zealand guidelines for cyanobacteria in recreational fresh waters – Interim Guidelines. Prepared for the Ministry for the Environment and the Ministry of Health by SA Wood, DP Hamilton, WJ Paul, KA Safi and WM Williamson. Wellington: Ministry for the Environment.

  • Moorhead, D. L., C. F. Wolf & R. A. Wharton Jr., 1997. Impact of light regimes on productivity patterns of benthic microbial mats in an antarctic lake: a modeling study. Limnology and Oceanography 42: 1561–1569.

    CAS  PubMed  Google Scholar 

  • O’Neil, J. M., T. W. Davis, M. A. Burford & C. J. Gobler, 2012. The rise of harmful cyanobacteria blooms: the potential roles of eutrophication and climate change. Harmful Algae 14: 313–334.

    Google Scholar 

  • Paerl, H. W. & V. J. Paul, 2012. Climate change: links to global expansion of harmful cyanobacteria. Water Research 46: 1349–1363.

    CAS  PubMed  Google Scholar 

  • Paerl, H. W., R. S. Fulton 3rd, P. H. Moisander & J. Dyble, 2001. Harmful freshwater algal blooms, with an emphasis on cyanobacteria. Scientific World Journal 1: 76–113.

    CAS  PubMed  Google Scholar 

  • Powell, H. A., N. W. Kerbby & P. Rowell, 1991. Natural tolerance of cyanobacteria to the herbicide glyphosate. New Phytologist 119: 421–426.

    CAS  Google Scholar 

  • Psenner, R., 1988. Fractionation of phosphorus in suspended matter and sediment. Arch Hydrobiol Beih 30: 98–110.

    Google Scholar 

  • Quiblier, C., S. Wood, I. Echenique-Subiabre, M. Heath, A. Villeneuve & J.-F. Humbert, 2013. A review of current knowledge on toxic benthic freshwater cyanobacteria – ecology, toxin production and risk management. Water Research 47: 5464–5479.

    Google Scholar 

  • Quinn, J. M. & C. W. Hickey, 1990. Magnitude of effects of substrate particle size, recent flooding, and catchment development on benthic invertebrates in 88 New Zealand rivers. New Zealand Journal of Marine and Freshwater Research 24: 411–427.

    Google Scholar 

  • R Core Team, 2016. A language and environment for statistical computing. R Foundation for statistical computing, 2015; Vienna, Austria.

  • R Studio Team, 2015. RStudio: Integrated Development for R. RStudio Inc, Boston, MA.

    Google Scholar 

  • Rydin, E., 2000. Potentially mobile phosphorus in Lake Erken sediment. Water Research 34: 2037–2042.

    CAS  Google Scholar 

  • Sand-Jensen, K., 1983. Physical and chemical parameters regulating growth of periphytic communities. Periphyton of Freshwater Ecosystems. Springer, Dordrecht: 63–71.

    Google Scholar 

  • Tee, H. S., D. Waite, L. Payne, M. Middleditch, S. Wood & K. M. Handley, 2020. Tools for successful proliferation: diverse strategies of nutrient acquisition by a benthic cyanobacterium. The ISME Journal 14: 2164–2178.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, C., Y. Zhang, H. Li & R. J. Morrison, 2013. Sequential extraction procedures for the determination of phosphorus forms in sediment. Limnology 14: 147–157.

    CAS  Google Scholar 

  • Wickham, H., 2016. ggplot2: Elegant Graphics for Data Analysis. Springer, New York.

    Google Scholar 

  • Winterbourn, M. J., K. L. D. Gregson & C. L. Dolphin, 2006. Guide to the Aquatic Insects of New Zealand, Bulletin 14. Entomological Society of New Zealand, Christchurch.

    Google Scholar 

  • Wood, S. A. & B. Bridge, 2014. Preliminary analysis of Phormidium abundance in the Maitai River and recommendation for on-going monitoring. Prepared for Nelson City Council. Cawthron Report No. 2537, 16.

  • Wood, S. A., A. Wagenhoff & D. Kelly, 2015b. Phormidium blooms – relationships with flow, nutrients and fine sediment in the Maitai River. Prepared for Nelson City Council. Cawthron Report No. 2723, 44 plus appendices.

  • Wood, S. A., A. I. Selwood, A. Rueckert, P. T. Holland, J. R. Milne, K. F. Smith, B. Smits, L. F. Watts & C. S. Cary, 2007. First report of homoanatoxin-a and associated dog neurotoxicosis in New Zealand. Toxicon 50: 292–301.

    CAS  PubMed  Google Scholar 

  • Wood, S. A., J. M. Kuhajek, M. de Winton & N. R. Phillips, 2012. Species composition and cyanotoxin production in periphyton mats from three lakes of varying trophic status. FEMS Microbiology Ecology 79: 312–326.

    CAS  PubMed  Google Scholar 

  • Wood, S. A., C. Depree, L. Brown, T. McAllister & I. Hawes, 2015a. Entrapped sediments as a source of phosphorus in epilithic cyanobacterial proliferations in low nutrient rivers. PLoS ONE 10: e0141063.

    PubMed  PubMed Central  Google Scholar 

  • Wood, S. A., J. Atalah, A. Wagenhoff, L. Brown, K. Doehring, R. G. Young & I. Hawes, 2017. Effect of river flow, temperature, and water chemistry on proliferations of the benthic anatoxin-producing cyanobacterium Phormidium. Freshwater Science 36: 63–76.

    Google Scholar 

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Acknowledgements

The authors acknowledge Annabel Tidy (University of Birmingham) and Bethany Bucknall (University of Birmingham) for sample collection and field assistance, Sean Waters (Cawthron Institute) for advice on phosphorus extractions, Laura Kelly (Cawthron) for reviewing earlier versions of the draft, Jonathan Puddick (Cawthron Institute) for input on pigment analysis and Karen Shearer (Cawthron Institute) for assistance with macroinvertebrates identification. This work received funding from the Nelson City Council and the authors thank Joanna Wilson (Nelson City Council) and Paul Fisher (Nelson City Council) for their support throughout the project. SAW received support for this study from the National Institute of Water and Atmospheric Research Ltd. under the causes and effects of water quality degradation: eutrophication risk assessment programme.

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  1. Cawthron Institute, Private Bag 2, Nelson, 7010, New Zealand

    Georgia Thomson-Laing, Niamh Dyer, Ruby Whyte-Wilding & Susanna A. Wood

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  1. Georgia Thomson-Laing
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  2. Niamh Dyer
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Contributions

SW and GTL contributed to the conception and design of the study. RW-W and ND acquired the samples and data. GT-L and SW contributed to the analysis and interpretation of the data. GT-L and SW wrote the first draft of the manuscript. All authors contributed to the manuscript revision, read, and approved the submitted version.

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Correspondence to Georgia Thomson-Laing.

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Thomson-Laing, G., Dyer, N., Whyte-Wilding, R. et al. In situ river experiments to explore variability in Microcoleus autumnalis mat expansion. Hydrobiologia 848, 445–467 (2021). https://doi.org/10.1007/s10750-020-04453-1

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