Skip to main content

Advertisement

Log in

Early onset of a microcystin-producing cyanobacterial bloom in an agriculturally-influenced Great Lakes tributary

  • ICTC-10 Special Issue: Cyanobacteria and cyanotoxins: responses and detection
  • Published:
Journal of Oceanology and Limnology Aims and scope Submit manuscript

Abstract

In late May 2016, a cyanobacterial harmful algal bloom (cHAB) was detected in the Maumee River, the largest tributary to Lake Erie, the southernmost lake of the Laurentian Great Lakes system. Testing on 31 May identified Planktothrix agardhii as the dominant cyanobacterium with cell abundance exceeding 1.7×109 cells/L and total microcystins (MC) reaching 19 μg/L MC-LR equivalents, a level over 10-fold higher than the 2015 revised U.S. Environmental Protection Agency (EPA) national health advisory levels for drinking water exposure to adults. Low river discharge coincident with negligible precipitation through the latter half of May coincided with an 80% decline in river turbidity that likely favored bloom formation by a low-light adapted P. agardhii population. Also contributing to the cHAB were high initial nutrient loads and an increase of the river temperature from 13°C to 26°C over this same period. The bloom persisted through 5 June with microcystins exceeding 22 μg/L MC-LR equivalents at the bloom peak. By 6 June, the river had returned to its muddy character following a rain event and sampling on 7 June detected only low levels of toxin (<0.6 μg/L) at public water systems located near the bloom origin. The elevated toxin production associated with this early onset bloom was without precedent for the Maumee River and an unique attribute of the cHAB was the high proportion of potentially-toxic genotypes. Whereas Planktothrix spp. is common in lotic environments, and has been previously detected in the Maumee, blooms are not commonly reported. This early onset, microcystin-producing cHAB provided a rare opportunity to glean insights into environmental factors that promote bloom development and dominance by Planktothrix in lotic environments.

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.

Similar content being viewed by others

References

  • Acinas S G, Haverkamp T H, Huisman J, Stal L J. 2009. Phenotypic and genetic diversification of Pseudanabaena spp. (cyanobacteria). The ISME Journal, 3 (1): 31–46.

    Article  Google Scholar 

  • Allinger L E, Reavie E D. 2013. The ecological history of Lake Erie as recorded by the phytoplankton community. Journal of Great Lakes Research, 39 (3): 365–382.

    Article  Google Scholar 

  • Anagnostidis K, Komárek J. 1985. Modern approach to the classification system of cyanophytes. 1-Introduction. Algological Studies, 38–39: 291–302.

    Google Scholar 

  • Anagnostidis K, Komárek J. 1988. Modern approach to the classification system of cyanophytes. 3-Oscillatoriales. Algological Studies, 50–53: 327–472.

    Google Scholar 

  • Atkins R, Rose T, Brown R S, Robb M. 2001. The microcystis cyanobacteria bloom in the Swan River-February 2000. Water Science and Technology: A Journal of the International Association on Water Pollution Research, 43 (9): 107–114.

    Article  Google Scholar 

  • Berardo R, Formica F, Reutter J, Singh A. 2017. Impact of land use activities in the Maumee River watershed on harmful algal blooms in Lake Erie. Case Studies in the Environment, 1(1): 1–8. https://doi.org/10/1525/cse.2017.sc.450561.

    Article  Google Scholar 

  • Bertani I, Steger C E, Obenour D R, Fahnenstiel G L, Bridgeman T B, Johengen T H, Sayers M J, Shuchman R A., Scavia D. 2017. Tracking cyanobacteria blooms: do different monitoring approaches tell the same story? Science of the Total Environment, 575: 294–308.

    Article  Google Scholar 

  • Briand E, Gugger M, François J C, Bernard C, Humbert J F, Quiblier C. 2008a. Temporal variations in the dynamics of potentially microcystin-producing strains in a bloomforming Planktothrix agardhii (Cyanobacterium) population. Applied and Environmental Microbiology, 74 (12): 3 839–3 848.

    Article  Google Scholar 

  • Briand E, Yéprémian C, Humbert J F, Quiblier C. 2008b. Competition between microcystin-and non-microcystinproducing Planktothrix agardhii (Cyanobacteria) strains under different environmental conditions. Environmental Microbiology, 10 (12): 3 337–3 348.

    Article  Google Scholar 

  • Bridgeman T B, Chaffin J D, Kane D D, Conroy J D, Panek S E, Armenio P M. 2012. From River to Lake: phosphorus partitioning and algal community compositional changes in Western Lake Erie. Journal of Great Lakes Research, 38 (1): 90–97.

    Article  Google Scholar 

  • Bullerjahn G S, McKay R M, Davis T W, Baker D B, Boyer G L, D’Anglada L V, Doucette G J, Ho J C, Irwin E G, Kling C L, Kudela R M, Kurmayer R, Michalak A M, Ortiz J D, Otten T G, Paerl H W, Qin B Q, Sohngen B L, Stumpf R P, Visser P M, Wilhelm S W. 2016. Global solutions to regional problems: collecting global expertise to address the problem of harmful cyanobacterial blooms. A Lake Erie case study. Harmful Algae, 54: 223–238.

    Article  Google Scholar 

  • Chaffin J D, Bridgeman T B, Bade D L. 2013. Nitrogen constrains the growth of late summer cyanobacterial blooms in Lake Erie. Advances in Microbiology, 3 (6A): 37 926.

    Google Scholar 

  • Chaffin J D, Sigler V, Bridgeman T B. 2014. Connecting the blooms: tracking and establishing the origin of the recordbreaking Lake Erie Microcystis bloom of 2011 using DGGE. Aquatic Microbial Ecology, 73 (1): 29–39.

    Article  Google Scholar 

  • Christiansen G, Molitor C, Philmus B, Kurmayer R. 2008. Nontoxic strains of cyanobacteria are the result of major gene deletion events induced by a transposable element. Molecular Biology and Evolution, 25 (8): 1 695–1 704.

    Article  Google Scholar 

  • Conroy J D, Kane D D, Briland R D, Culver D A. 2014. Systemic, early-season Microcystis blooms in western Lake Erie and two of its major agricultural tributaries (Maumee and Sandusky rivers). Journal of Great Lakes Research, 40 (3): 518–523.

    Article  Google Scholar 

  • Davis T W, Bullerjahn G S, Tuttle T, McKay R M, Watson S B. 2015. Effects of increasing nitrogen and phosphorus concentrations on phytoplankton community growth and toxicity during Planktothrix blooms in Sandusky Bay, Lake Erie. Environmental Science & Technology, 49 (12): 7 197–7 207.

    Article  Google Scholar 

  • DeSantis T Z, Hugenholtz P, Larsen N, Rojas M, Brodie E L, Keller K, Huber T, Dalevi D, Hu P, Andersen G L. 2006. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Applied and Environmental Microbiology, 72 (7): 5 069–5 072.

    Article  Google Scholar 

  • Foy R H, Gibson C E, Smith R V. 1976. The influence of daylength, light intensity and temperature on the growth rates of planktonic blue-green algae. British Phycological Journal, 11 (2): 151–163.

    Article  Google Scholar 

  • Harke M J, Steffen M M, Gobler C J, Otten T G, Wilhelm S W, Wood S A, Paerl H W. 2016. A review of the global ecology, genomics, and biogeography of the toxic cyanobacterium, Microcystis spp. Harmful Algae, 54: 4–20.

    Article  Google Scholar 

  • Havens K E, James R T, East T L, Smith V H. 2003. N: P ratios, light limitation, and cyanobacterial dominance in a subtropical lake impacted by non-point source nutrient pollution. Environmental Pollution, 122 (3): 379–390.

    Article  Google Scholar 

  • Hufford T L. 1965. A comparison of photosynthetic yields in the Maumee River, Steidtmann's Pond, and Urschel's Quarry under natural conditions. Ohio Journal of Science,65 (4): 176–182.

    Google Scholar 

  • Illumina. 2014. Illumina 16S metagenomics sequencing workflow. 1270-2014-003-B, https://doi.org/support.illumina.com/content/dam/illumina-marketing/documents/products/other/16s-metagenomics-faq-1270-2014-003.pdf.

    Google Scholar 

  • Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, Glöckner F O. 2013. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and nextgeneration sequencing-based diversity studies. Nucleic Acids Research, 41 (1): e1, https://doi.org/10.1093/nar/gks808.

    Article  Google Scholar 

  • Kurmayer R, Christiansen G, Fastner J, Börner T. 2004. Abundance of active and inactive microcystin genotypes in populations of the toxic cyanobacterium Planktothrix spp. Environmental Microbiology, 6 (8): 831–841.

    Article  Google Scholar 

  • Kutovaya O A, McKay R M L, Beall B F N, Wilhelm S W, Kane D D, Chaffin J D, Bridgeman T B, Bullerjahn G S. 2012. Evidence against fluvial seeding of recurrent toxic blooms of Microcystis spp. in Lake Erie’s western basin. Harmful Algae, 15: 71–77.

    Article  Google Scholar 

  • Maier H R, Burch M D, Bormans M. 2001. Flow management strategies to control blooms of the cyanobacterium, Anabaena circinalis, in the River Murray at Morgan, South Australia. River Research and Applications, 17 (6): 637–650.

    Google Scholar 

  • McCarty C L, Nelson L, Eitniear S, Zgodzinski E, Zabala A, Billing L, DiOrio M. 2016. Community needs assessment after microcystin toxin contamination of a municipal water supply—Lucas County, Ohio, September 2014. MMWR. Morbidity and Mortality Weekly Report, 65 (35): 925–929.

    Article  Google Scholar 

  • McKay R M L, Geider R J, LaRoche J. 1997. Physiological and biochemical response of the photosynthetic apparatus of two marine diatoms to Fe stress. Plant Physiology, 114 (2): 615–622.

    Article  Google Scholar 

  • Michalak A M, Anderson E J, Beletsky D, Boland S, Bosch N S, Bridgeman T B, Chaffin J D, Cho K, Confesor R, Daloğlu I, DePinto J V, Evans M A, Fahnenstiel G L, He L L, Ho J C, Jenkins L, Johengen T H, Kuo K C, LaPorte E, Liu X J, McWilliams M R, Moore M R, Posselt D J, Richards R P, Scavia D, Steiner A L, Verhamme E, Wright D M, Zagorski M A. 2013. Record-setting algal bloom in Lake Erie caused by agricultural and meteorological trends consistent with expected future conditions. Proceedings of the National Academy of Sciences of the United States of America, 110 (16): 6 448–6 452.

    Article  Google Scholar 

  • Muenich R L, Kalcic M, Scavia D. 2016. Evaluating the impact of legacy P and agricultural conservation practices on nutrient loads from the Maumee River Watershed. Environmental Science & Technology, 50 (15): 8 146–8 154.

    Article  Google Scholar 

  • Munawar M, Munawar I F. 1976. A lakewide study of phytoplankton biomass and its species composition in Lake Erie, April–December 1970. Journal of the Fisheries Research Board of Canada, 33 (3): 581–600.

    Article  Google Scholar 

  • Murphy J, Riley J P. 1962. A modified single solution method for the determination of phosphate in natural waters. Analytica Chimica Acta, 27: 31–36.

    Article  Google Scholar 

  • Ohio EPA Division of Drinking and Ground Waters. 1999. State of Ohio source water assessment and protection program. https://doi.org/epa.ohio.gov/portals/28/documents/swap/swapdoc.pdf.

    Google Scholar 

  • Ohio EPA Division of Environmental Services. 2015. Ohio EPA total (extracellular and intracellular) microcystins-ADDA by ELISA analytical methodology. Ohio EPA, Reynoldsburg, OH, November 2015, https://doi.org/epa.ohio.gov/Portals/28/documents/labcert/OhioEPADES701.0Version2.2.pdf.

    Google Scholar 

  • Ostermaier V, Schanz F, Köster O, Kurmayer R. 2012. Stability of toxin gene proportion in red-pigmented populations of the cyanobacterium Planktothrix during 29 years of reoligotrophication of Lake Zürich. BMC Biology, 10: 100, https://doi.org/www.biomedcentral.com/1741-7007/10/100.

    Article  Google Scholar 

  • Paerl H W, Huisman J. 2008. Blooms like it hot. Science, 320(5872): 57–58.

    Article  Google Scholar 

  • Patton C J, Kryskalla J R. 2011. Colorimetric determination of nitrate plus nitrite in water by enzymatic reduction, automated discrete analyzer methods: U.S. Geological Survey Techniques and Methods, U.S. Geological Survey, Reston, VA. p.34.

    Google Scholar 

  • Platt T, Gallegos C L, Harrison W G. 1980. Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. Journal of Marine Research, 38: 687–701.

    Google Scholar 

  • Post A F, Loogman J G, Mur L R. 1985. Regulation of growth and photosynthesis by Oscillatoria agardhii grown with a light/dark cycle. FEMS Microbiology Letters, 31 (2): 97–102.

    Article  Google Scholar 

  • Reynolds C S. 2003. Pelagic community assembly and the habitat template. Bocconea, 16 (1): 323–339.

    Google Scholar 

  • Richards R P, Baker D B, Crumrine J P, Stearns A M. 2010. Unusually large loads in 2007 from the Maumee and Sandusky Rivers, tributaries to Lake Erie. Journal of Soil and Water Conservation, 65 (6): 450–462.

    Article  Google Scholar 

  • Rücker J, Wiedner C, Zippel P. 1997. Factors controlling the dominance of Planktothrix agardhii and Limnothrix redekei in eutrophic shallow lakes. Hydrobiologia, 342–343: 107–115.

    Article  Google Scholar 

  • Scavia D, Allan J D, Arend K K, Bartell S, Beletsky D, Bosch N S, Brandt S B, Briland R D, Daloğlu I, DePinto J V, Dolan D M, Evans M A, Farmer T M, Goto D, Han H, Höök T O, Knight R, Ludsin S A, Mason D, Michalak A M, Peter R R, Roberts J J, Rucinski D K, Rutherford E, Schwab D J, Sesterhenn T M, Zhang H Y, Zhou Y T. 2014. Assessing and addressing the re-eutrophication of Lake Erie: central basin hypoxia. Journal of Great Lakes Research, 40 (2): 226–246.

    Article  Google Scholar 

  • Scheffer M, Rinaldi S, Gragnani A, Mur L R, van Nes E H. 1997. On the dominance of filamentous cyanobacteria in shallow, turbid lakes. Ecology, 78 (1): 272–282.

    Article  Google Scholar 

  • Steffen M M, Belisle B S, Watson S B, Boyer G L, Wilhelm S W. 2014. Status, causes and controls of cyanobacterial blooms in Lake Erie. Journal of Great Lakes Research, 40 (2): 215–225.

    Article  Google Scholar 

  • Steffen M M, Davis T W, McKay R M L, Bullerjahn G S, Krausfeldt L E, Stough J M A, Neitzey M L, Gilbert N E, Boyer G L, Johengen T H, Gossiaux D C, Burtner A M, Palladino D, Rowe M D, Dick G J, Meyer K A, Levy S, Boone B E, Stumpf R P, Wynne T T, Zimba P V, Gutierrez D, Wilhelm S W. 2017. Ecophysiological examination of the Lake Erie Microcystis bloom in 2014: linkages between biology and the water supply shutdown of Toledo, OH. Environmental Science & Technology, 51 (12): 6 745–6 755.

    Article  Google Scholar 

  • Stow C A, Cha Y, Johnson L T, Confesor R, Richards R P. 2015. Long-term and seasonal trend decomposition of Maumee River nutrient inputs to western Lake Erie. Environmental Science & Technology, 49 (6): 3 392–3 400.

    Article  Google Scholar 

  • U. S. Geological Survey. 2015. National field manual for the collection of water-quality data: U.S. Geological Survey Techniques of Water-Resources Investigations, book 9. Chapters A1–A10, https://doi.org/pubs.water.usgs.gov/twri9A.

    Google Scholar 

  • Van den Wyngaert S, Salcher M M, Pernthaler J, Zeder M, Posch T. 2011. Quantitative dominance of seasonally persistent filamentous cyanobacteria (Planktothrix rubescens) in the microbial assemblages of a temperate lake. Limnology and Oceanography, 56 (1): 97–109.

    Article  Google Scholar 

  • Verduin J. 1959. Photosynthesis by aquatic communities in northwestern Ohio. Ecology, 40 (3): 377–383.

    Article  Google Scholar 

  • Wagner R J, Boulger Jr R W, Oblinger C J, Smith B A. 2006. Guidelines and standard procedures for continuous waterquality monitors: Station operation, record computation, and data reporting. Techniques and Methods 1–D3, p.51, https://doi.org/pubs.water.usgs.gov/tm1d3.

    Google Scholar 

  • Wang Q, Garrity G M, Tiedje J M, Cole J R. 2007. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology, 73 (16): 5 261–5 267.

    Article  Google Scholar 

  • Watson S B, Miller C, Arhonditsis G, Boyer G L, Carmichael W, Charlton M N, Confesor R, Depew D C, Höök T O, Ludsin S A, Matisoff G, McElmurry S P, Murray M W, Richards R P, Rao Y R, Steffen M M, Wilhelm S W. 2016. The re-eutrophication of Lake Erie: harmful algal blooms and hypoxia. Harmful Algae, 56: 44–66.

    Article  Google Scholar 

  • Webster I T, Sherman B S, Bormans M, Jones G. 2000. Management strategies for cyanobacterial blooms in an impounded lowland river. Regulated Rivers: Research & Management, 16 (5): 513–525.

    Article  Google Scholar 

  • Welschmeyer N A. 1994. Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and pheopigments. Limnology and Oceanography, 39(8): 1 985–1 992.

    Article  Google Scholar 

  • Xia J, Cheng S B, Hao X P, Xia R, Liu X J. 2010. Potential impacts and challenges of climate change on water quality and ecosystem: case studies in representative rivers in China. Journal of Resources and Ecology, 1 (1): 31–35.

    Google Scholar 

  • Xia R, Chen Z, Zhou Y. 2012. Impact assessment of climate change on algal blooms by a parametric modeling study in Han River. Journal of Resources and Ecology, 3 (3): 209–219.

    Article  Google Scholar 

  • Znachor P, Nedoma J. 2010. Importance of dissolved organic carbon for phytoplankton nutrition in a eutrophic reservoir. Journal of Plankton Research, 32 (3): 367–376.

    Article  Google Scholar 

  • Zotina T, Köster O, Jüttner F. 2003. Photoheterotrophy and light-dependent uptake of organic and organic nitrogenous compounds by Planktothrix rubescens under low irradiance. Freshwater Biology, 48 (10): 1 859–1 872.

    Article  Google Scholar 

  • Zwart G, Kamst-van Agterveld M P, Van Der Werff-Staverman I, Hagen F, Hoogveld H L, Gons H J. 2005. Molecular characterization of cyanobacterial diversity in a shallow eutrophic lake. Environmental Microbiology, 7 (3): 365–377.

    Article  Google Scholar 

Download references

Acknowledgement

The authors thank Heather Raymond, State HAB Coordinator for Ohio EPA for alerting us to the Maumee River cHAB described in this contribution. Thanks are also extended to Scott Hoover and Jeff Weis of the City of Napoleon and Donna Francy of the USGS Michigan-Ohio Water Science Center for their assistance providing data from the Maumee River. Chaoxuan Guo (Nanjing Institute of Geography and Limnology) shared helpful information regarding recent cHABs in Chinese rivers. Ben Beall contributed the map showing sampling sites. The manuscript also benefitted from helpful comments of two anonymous reviewers.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Robert Michael L. Mckay.

Additional information

Supported by a Harmful Algal Bloom Research Initiative Grant (No. R/HAB-2-ODHE) from the Ohio Department of Higher Education (GSB, RMLM) and Ohio Sea Grant College Program grant R/ER-114 (GSB, RMLM)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mckay, R.M.L., Tuttle, T., Reitz, L.A. et al. Early onset of a microcystin-producing cyanobacterial bloom in an agriculturally-influenced Great Lakes tributary. J. Ocean. Limnol. 36, 1112–1125 (2018). https://doi.org/10.1007/s00343-018-7164-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00343-018-7164-z

Keyword

Navigation