Microcystin concentrations can be predicted with phytoplankton biomass and watershed morphology

References

• Beaulieu M, Pick F, Gregory-Eaves I. 2013. Nutrients and water temperature are significant predictors of cyanobacterial biomass in a 1147 lakes dataset. Limnol Oceanogr. 58:1736–1746. doi: 10.4319/lo.2013.58.5.1736
   Web of Science ®Google Scholar
• Beaulieu M, Pick F, Palmer M, Watson S, Winter J, Zurawell R, Gregory-Eaves I, Prairie, Y. 2014. Comparing predictive cyanobacterial models from temperate regions. Can J Fish Aquat Sci. 71:1830–1839. doi: 10.1139/cjfas-2014-0168
   Web of Science ®Google Scholar
• Beaver JR, Manis EE, Loftin KA, Graham JL, Pollard AI, Mitchell RM. 2014. Land use patterns, ecoregion, and microcystin relationships in U.S. lakes and reservoirs: a preliminary evaluation. Harmful Algae. 36:57–62. doi: 10.1016/j.hal.2014.03.005
   Web of Science ®Google Scholar
• Beaver JR, Scotese KC, Minerovic AD, Buccier KM, Tausz CE, Clapham WB. 2012. Ecoregion, land use and phytoplankton relationships in productive Ohio reservoirs. Inland Waters. 2:101–108. doi: 10.5268/IW-2.2.481
   Web of Science ®Google Scholar
• Brett MT, Muller-Navarra DC, Park SK. 2000. Empirical analysis of the effect of phosphorus limitation on algal food quality for freshwater zooplankton. Limnol Oceanogr. 45:1564–1575. doi: 10.4319/lo.2000.45.7.1564
   Google Scholar
• Burnham KP, Anderson DR, Huyvaert KP. 2010. AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behav Ecol Sociobiol. 65:23–35. doi: 10.1007/s00265-010-1029-6
   Google Scholar
• Carey CC, Ibelings BW, Hoffmann EP, Hamilton DP, Brookes JD. 2012. Eco-physiological adaptations that favour freshwater cyanobacteria in a changing climate. Water Res. 46:1394–407. doi: 10.1016/j.watres.2011.12.016
   PubMed Web of Science ®Google Scholar
• Carmichael WW, Boyer GL. 2016. Health impacts from cyanobacteria harmful algae blooms: implications for the North American Great Lakes. Harmful Algae. 54:194–212. doi: 10.1016/j.hal.2016.02.002
   PubMed Web of Science ®Google Scholar
• Chorus I, Bartram J. 1999. Toxic cyanobacteria in water: a guide to their public health consequences, monitoring and management. 1st ed. In: Chorus I, Bartram J, editors. London (UK): E&FN Spon.
   Google Scholar
• Crumpton WG, Isenhart TM, Mitchell PD. 1992. Nitrate and organic N analyses with second-derivative spectroscopy. Limnol Oceanogr. 37:907–913. doi: 10.4319/lo.1992.37.4.0907
   Web of Science ®Google Scholar
• Davis TW, Berry DL, Boyer GL, Gobler CJ. 2009. The effects of temperature and nutrients on the growth and dynamics of toxic and non-toxic strains of Microcystis during cyanobacteria blooms. Harmful Algae. 8:715–725. doi: 10.1016/j.hal.2009.02.004
   Web of Science ®Google Scholar
• De Senerpont Domis LN, Elser JJ, Gsell AS, Huszar VLM, Ibelings BW, Jeppesen E, Kosten S, Mooij WM, Roland F, Sommer U, et al. 2013. Plankton dynamics under different climatic conditions in space and time. Freshwater Biol. 58:463–482. doi: 10.1111/fwb.12053
   Web of Science ®Google Scholar
• Dolman AM, Rücker J, Pick FR, Fastner J, Rohrlack T, Mischke U, Wiedner C. 2012. Cyanobacteria and cyanotoxins: the influence of nitrogen versus phosphorus. PLoS ONE 7:e38757. doi: 10.1371/journal.pone.0038757
   PubMed Web of Science ®Google Scholar
• Downing JA, Watson SB, McCauley E. 2001. Predicting cyanobacteria dominance in lakes. Can J Fish Aquat Sci. 58:1905–1908. doi: 10.1139/f01-143
   Web of Science ®Google Scholar
• Falconer IR. 2005. Cyanobacterial toxins of drinking water supplies: cylindrospermopsins and microcystins. New York (NY): CRC Press.
   Google Scholar
• Finlay K, Patoine A, Donald DB, Bogard MJ, Leavitt PR. 2010. Experimental evidence that pollution with urea can degrade water quality in phosphorus-rich lakes of the Northern Great Plains. Limnol Oceanogr. 55:1213–1230. doi: 10.4319/lo.2010.55.3.1213
   Web of Science ®Google Scholar
• Fox GA. 2015. What you don’t know can hurt you: censored and truncated data in ecological research. In: Fox GS, Negrete-Yankelevich S, Sosa VJ, editors. Ecological statistics contemporary theory application. Oxford (UK): Oxford University Press; p. 416.
   Google Scholar
• Fraterrigo JM, Downing JA. 2008. The influence of land use on lake nutrients varies with watershed transport capacity. Ecosystems. 11:1021–1034. doi: 10.1007/s10021-008-9176-6
   Web of Science ®Google Scholar
• Giani A, Bird DF, Prairie YT, Lawrence JF. 2005. Empirical study of cyanobacterial toxicity along a trophic gradient of lakes. Can J Fish Aquat Sci. 62:2100–2109. doi: 10.1139/f05-124
   Web of Science ®Google Scholar
• Glibert PM, Allen JI, Bouwman AF, Brown CW, Flynn KJ, Lewitus AJ, Madden CJ. 2010. Modeling of HABs and eutrophication: status, advances, challenges. J Mar Syst. 83:262–275. doi: 10.1016/j.jmarsys.2010.05.004
   Web of Science ®Google Scholar
• Graham JL, Jones JR, Jones SB, Downing JA, Clevenger TE. 2004. Environmental factors influencing microcystin distribution and concentration in the Midwestern United States. Water Res. 38:4395–404. doi: 10.1016/j.watres.2004.08.004
   PubMed Web of Science ®Google Scholar
• Guildford SJ, Hecky RE. 2000. Total nitrogen, total phosphorus, and nutrient limitation in lakes and oceans: is there a common relationship? Limnol Oceanogr. 45:1213–1223. doi: 10.4319/lo.2000.45.6.1213
   Web of Science ®Google Scholar
• Hayes NM, Vanni MJ, Horgan MJ, Renwick WH. 2015. Drought and land use interactively affect lake phytoplankton nutrient limitation status. Ecology. 96:392–402. doi: 10.1890/13-1840.1
   Google Scholar
• Heisler J, Glibert PM, Burkholder JM, Anderson DM, Cochlan W, Dennison WC, Dortch Q, Gobler CJ, Heil CA, Humphries E, et al. 2008. Eutrophication and harmful algal blooms: a scientific consensus. Harmful Algae. 8:3–13. doi: 10.1016/j.hal.2008.08.006
   PubMed Web of Science ®Google Scholar
• Helsel DR. 2006. Fabricating data: how substituting values for nondetects can ruin results, and what can be done about it. Chemosphere. 65:2434–2439. doi: 10.1016/j.chemosphere.2006.04.051
   PubMed Web of Science ®Google Scholar
• Hillebrand H, Durselen CD, Kirschtel D, Pollingher U, Zohary T. 1999. Biovolume calculation for pelagic and benthic algae. J Phycol. 35:403–424. doi: 10.1046/j.1529-8817.1999.3520403.x
   Web of Science ®Google Scholar
• Hotto A, Satchwell M, Boyer G. 2005. Seasonal production and molecular characterization of microcystins in Oneida Lake, New York, USA. Environ Toxicol. 20:243–248. doi: 10.1002/tox.20104
   PubMed Web of Science ®Google Scholar
• Knoll LB, Hagenbuch EJ, Stevens MH, Vanni MJ, Renwick WH, Denlinger JC, Hale RS, González MJ. 2015. Predicting eutrophication status in reservoirs at large spatial scales using landscape and morphometric variables. Inland Waters. 5:203–214. doi: 10.5268/IW-5.3.812
   Web of Science ®Google Scholar
• Knoll LB, Sarnelle O, Hamilton SK, Kissman CEH, Wilson AE, Rose JB, Morgan MR. 2008. Invasive zebra mussels (Dreissena polymorpha) increase cyanobacterial toxin concentrations in low-nutrient lakes. Can J Fish Aquat Sci. 65:448–455. doi: 10.1139/f07-181
   Web of Science ®Google Scholar
• Knoll LB, Vanni MJ, Renwick WH. 2003. Phytoplankton primary production and photosynthetic parameters in reservoirs along a gradient of watershed land use. Limnol Oceanogr. 48:608–617. doi: 10.4319/lo.2003.48.2.0608
   Web of Science ®Google Scholar
• Mazerolle MJ. 2016. AICcmodavg: model selection and multimodel inference based on (Q)AIC(c).R package verion 2.1-1. https://cran.r-project.org/package = AICcmodav
   Google Scholar
• Mette EM, Vanni MJ, Newell JM, González MJ. 2011. Phytoplankton communities and stoichiometry are interactively affected by light, nutrients, and fish. Limnol Oceanogr. 56:1959–1975. doi: 10.4319/lo.2011.56.6.1959
   Web of Science ®Google Scholar
• Monchamp ME, Pick FR, Beisner BE, Maranger R. 2014. Nitrogen forms influence microcystin concentration and composition via changes in cyanobacterial community structure. PLOS ONE. 9:e85573. doi: 10.1371/journal.pone.0085573
   Google Scholar
• Oh HM, Lee SJ, Jang MH, Yoon BD. 2000. Microcystin production by Microcystis aeruginosa in a phosphorus-limited chemostat. Appl Environ Microbiol. 66:176–179. doi: 10.1128/AEM.66.1.176-179.2000
   PubMed Web of Science ®Google Scholar
• O’Neil JM, Davis TW, Burford MA, Gobler CJ. 2012. The rise of harmful cyanobacteria blooms: the potential roles of eutrophication and climate change. Harmful Algae. 14:313–334. doi: 10.1016/j.hal.2011.10.027
   Web of Science ®Google Scholar
• Orihel DM, Bird DF, Brylinsky M, Huirong C, Donald DB, Huang DY, Giani A, Kinniburgh D, Kling H, Kotak BG, et al. 2012. High microcystin concentrations occur only at low nitrogen-to-phosphorus ratios in nutrient-rich Canadian lakes. Can J Fish Aquat Sci. 69:1457–1462. doi: 10.1139/f2012-088
   Web of Science ®Google Scholar
• Paerl HW, Fulton RS, Moisander PH, Dyble J. 2001. Harmful freshwater algal blooms, with an emphasis on cyanobacteria. Sci World J. 1:76–113. doi: 10.1100/tsw.2001.16
   Google Scholar
• Paerl HW, Huisman J. 2008. Blooms like it hot. Science. 320:57–58. doi: 10.1126/science.1155398
   PubMed Web of Science ®Google Scholar
• Paerl HW, Paul VJ. 2012. Climate change: links to global expansion of harmful cyanobacteria. Water Res. 46:1349–1363. doi: 10.1016/j.watres.2011.08.002
   PubMed Web of Science ®Google Scholar
• Pick FR. 2016. Blooming algae: a Canadian perspective on the rise of toxic cyanobacteria. Can J Fish Aquat Sci. 1158 :1–10.
   Google Scholar
• Poste AE, Hecky RE, Guildford SJ. 2011. Evalutaing microcystin exposure risk through fish consumption. Environ Sci Technol. 45:5806–5811. doi: 10.1021/es200285c
   PubMed Web of Science ®Google Scholar
• Romo S, Soria J, Fernández F, Ouahid Y, Barón-Solá Á. 2013. Water residence time and the dynamics of toxic cyanobacteria. Freshwater Biol. 58:513–522. doi: 10.1111/j.1365-2427.2012.02734.x
   Web of Science ®Google Scholar
• Sarnelle, O, Wilson AE. 2005. Local adaptation of Daphnia pulicaria to toxic cyanobacteria. Limnol Oceanogr. 50:1565–1570. doi: 10.4319/lo.2005.50.5.1565
   Web of Science ®Google Scholar
• Scott JT, McCarthy MJ, Otten TG, Steffen MM, Baker BC, Grantz EM, Wilhelm SW, Paerl HW. 2013. Comment: an alternative interpretation of the relationship between TN:TP and microcystins in Canadian lakes. Can J Fish Aquat Sci. 70:1265–1268. doi: 10.1139/cjfas-2012-0490
   Google Scholar
• Sivonen K. 1996. Cyanobacterial toxins and toxin production. Phycologia. 36:12–24.
   Google Scholar
• Smayda TJ. 2008. Complexity in the eutrophication–harmful algal bloom relationship, with comment on the importance of grazing. Harmful Algae. 8:140–151. doi: 10.1016/j.hal.2008.08.018
   Web of Science ®Google Scholar
• Smith VH. 1983. Low nitrogen to phosphorus ratios favor dominance by blue-green algae in lake phytoplankton. Science. 221:669–671.
   Google Scholar
• Taranu ZE, Gregory-Eaves I, Leavitt PR, Bunting L, Buchaca T, Catalan J, Domaizon I, Gulizzoni P, Lami A, McGowan S, et al. 2015. Acceleration of cyanobacterial dominance in north temperate-subarctic lakes during the Anthropocene. Ecol Lett. 18:375–384. doi: 10.1111/ele.12420
   PubMed Web of Science ®Google Scholar
• Taranu ZE, Gregory-Eaves I, Steele RJ, Beaulieu M, Legendre P. 2017. Predicting microcystin concentrations in lakes and reservoirs at a continental scale: a new framework for modelling an important health risk factor. Glob Ecol Biogeogr. 26:625–637. doi: 10.1111/geb.12569
   Web of Science ®Google Scholar
• Therneau TM. 2015. A package for survival analysis in S. version 2.38. https://CRAN.R-project.org/package=survival
   Google Scholar
• Thornton KW. 1990. Persepctives on reservoir limnology. In: Thornton KW, Kimmel BL, Payne FE, editors. Reservoir limnology ecological perspectives. New York (NY): Wiley; p. 1–14.
   Google Scholar
• [USEPA] US Environmental Protection Agency. 2009. National lake assessment: a collaborative survey of the nation’s lakes. EPA 841-R-09-00 U.S. Environmental Protection Agency Office of Water and Office of Research and Development, Washington, D.C. 90 p.
   Google Scholar
• Vanni MJ, Renwick WH, Bowling AM, Horgan MJ, Christian AD. 2011. Nutrient stoichiometry of linked catchment-lake systems along a gradient of land use. Freshwater Biol. 56:791–811. doi: 10.1111/j.1365-2427.2010.02436.x
   Google Scholar
• Visser PM, Verspagen JMH, Sandrini G, Stal LJ, Matthijs HCP, Davis TW, Paerl HW, Huisman J. 2016. How rising CO2 and global warming may stimulate harmful cyanobacterial blooms. Harmful Algae. 54:145–159. doi: 10.1016/j.hal.2015.12.006
   PubMed Web of Science ®Google Scholar
• Vollenweider RA. 1976. Advances in defining critical loading levels of phosphorus in lake eutrophication. Mem Ist Ital Hdrobiol. 33:53–83.
   Google Scholar
• Van de Waal DB, Smith VH, Declerck SAJ, Stam ECM, Elser JJ. 2014. Stoichiometric regulation of phytoplankton toxins. Ecol Lett. 17:736–742. doi: 10.1111/ele.12280
   PubMed Web of Science ®Google Scholar
• Van de Waal DB, Verspagen JMH, Lürling M, Van Donk E, Visser PM, Huisman J. 2009. The ecological stoichiometry of toxins produced by harmful cyanobacteria: an experimental test of the carbon-nutrient balance hypothesis. Ecol Lett. 12:1326–1335. doi: 10.1111/j.1461-0248.2009.01383.x
   PubMed Web of Science ®Google Scholar
• Wagner C, Adrian R. 2009. Exploring lake ecosystems: hierarchy responses to long-term change? Glob Change Biol. 15:1104–1115. doi: 10.1111/j.1365-2486.2008.01833.x
   Google Scholar
• Wagner C, Adrian R. 2011. Consequences of changes in thermal regime for plankton diversity and trait composition in a polymictic lake: a matter of temporal scale. Freshwater Biol. 56:1949–1961. doi: 10.1111/j.1365-2427.2011.02623.x
   Web of Science ®Google Scholar
• Warton DI, Hui FKC. 2011. The arcsine is asinine: the analysis of proportions in ecology. Ecology. 92:3–10. doi: 10.1890/10-0340.1
   PubMed Web of Science ®Google Scholar
• Watson SB, McCauley E, Downing JA. 1997. Patterns in phytoplankton taxonomic composition across temperate lakes of differing nutrient status. Limnol Oceanogr. 42:487–495.
   Google Scholar
• Wetzel RG, Likens GE. 1991. Limnological analyses. 2nd ed. New York (NY): Springer-Verlag.
   Google Scholar
• Whittingham MJ, Stephens PA, Bradbury RB, Freckleton RP. 2006. Why do we still use stepwise modelling in ecology and behaviour? J Anim Ecol. 75:1182–1189. doi: 10.1111/j.1365-2656.2006.01141.x
   PubMed Web of Science ®Google Scholar
• Yuan LL, Pollard AI, Pather S, Oliver JL, D’Anglada L. 2014. Managing microcystin: identifying national-scale thresholds for total nitrogen and chlorophyll a. Freshwater Biol. 59:1970–1981. doi: 10.1111/fwb.12400
   Google Scholar