Skip to main content

Advertisement

Log in

Anthropogenic land use is associated with N-fixing cyanobacterial dominance in lakes across the continental United States

  • Research Article
  • Published:
Aquatic Sciences Aims and scope Submit manuscript

Abstract

Cyanobacteria cause many water quality problems in lakes worldwide. Although many studies have examined factors that influence the structure of cyanobacterial communities, few have explicitly compared the effects of within-lake conditions (e.g., nutrient concentrations) and watershed parameters (e.g., land use) on a diverse array of cyanobacterial taxa. Here, we analyzed data from the 2007 U.S. Environmental Protection Agency’s National Lakes Assessment to quantify how lakeshore anthropogenic land use, nutrient concentrations and ratios, and surface water temperatures predict cyanobacterial biovolume and dominance in 236 naturally-formed lakes spanning the continental U.S. We observed that anthropogenic lakeshore land use was the best predictor for cyanobacterial dominance, whereas in-lake nitrogen (N) and phosphorus (P) concentrations were the best predictors for cyanobacterial biovolume. Our analyses suggest that anthropogenic land use may influence cyanobacterial dominance via means other than increased nutrient concentrations. The sum of agricultural and human-developed lakeshore land use was the best predictor of N-fixing cyanobacterial dominance, but there was no significant relationship between anthropogenic land use and non-N-fixing cyanobacterial dominance. In addition, we observed a total N:P ratio threshold for cyanobacterial dominance in the phytoplankton community (150:1) that was much higher than previously reported ratios. Consequently, management strategies to control cyanobacteria need to account for eco-physiological variation among different cyanobacterial taxa, and should consider nutrients and the other effects of land use to control overall lake cyanobacterial biovolume and cyanobacterial dominance, as the two cyanobacterial metrics may be sensitive to different drivers.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+
from $39.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • Bartram J, Chorus I (1999) Toxic cyanobacteria in water: a guide to their public health consequences, monitoring and management. Taylor and Francis, London

    Google Scholar 

  • Beaulieu M, Pick F, Gregory-Eaves I (2013) Nutrients and water temperature are significant predictors of cyanobacterial biomass in a 1147 lakes data set. Limnol Oceanogr 58:1736–1746

    Article  CAS  Google Scholar 

  • Beaver JR, Scotese KC, Minerovic AD, Buccier KM, Tausz CE, Clapham WB (2012) Land use patterns, ecoregion and phytoplankton relationships in productive Ohio reservoirs. Inland Waters 2:101–108

    Article  Google Scholar 

  • Bergman B, Gallon JR, Rai AN, Stal LJ (1997) N2 fixation by non-heterocystous cyanobacteria. FEMS Microbiol Rev 19:139–185

    Article  CAS  Google Scholar 

  • Bormans M, Sherman BS, Webster IT (1999) Is buoyancy regulation in cyanobacteria an adaptation to exploit separation of light and nutrients? Mar Freshw Res 50:897–906

    Article  Google Scholar 

  • Brookes JD, Carey CC (2011) Resilience to blooms. Science 334:46–47

    Article  CAS  PubMed  Google Scholar 

  • Brookes JD, Ganf GG, Green D, Whittington J (1999) The influence of light and nutrients on buoyancy, filament aggregation and flotation of Anabaena circinalis. J Plankton Res 21:327–341

    Article  Google Scholar 

  • Brookes JD, Regel R, Ganf GG (2002) Changes in the photochemistry of Microcystis aeruginosa in response to light and mixing. New Phytol 158:151–164

    Article  Google Scholar 

  • Carey CC, Weathers KC, Cottingham KL (2008) Gloeotrichia echinulata blooms in an oligotrophic lake: helpful insights from eutrophic lakes. J Plankton Res 30:893–904

    Article  CAS  Google Scholar 

  • Carey CC, Ewing HA, Cottingham KL, Weathers KC, Thomas RQ, Haney JF (2012a) Occurrence and toxicity of the cyanobacterium Gloeotrichia echinulata in low-nutrient lakes in the northeastern United States. Aquat Ecol 46:395–409

    Article  CAS  Google Scholar 

  • Carey CC, Ibelings BW, Hoffmann EP, Hamilton DP, Brookes JD (2012b) Eco-physiological adaptations that favour freshwater cyanobacteria in a changing climate. Water Res 46:1394–1407

    Article  CAS  PubMed  Google Scholar 

  • Carpenter SR, Caraco NF, Correll DL, Howarth RW, Sharpley AN, Smith VH (1998) Nonpoint pollution of surface waters with phosphorus and nitrogen. Ecol Appl 8:559–568

    Article  Google Scholar 

  • Carpenter SR, Ludwig D, Brock WA (1999) Management of eutrophication for lakes subject to potentially irreversible change. Ecol Appl 9:751–771

    Article  Google Scholar 

  • Carpenter SR, Stanley EH, Vander Zanden MJ (2011) State of the world’s freshwater ecosystems: physical, chemical, and biological changes. Annu Rev Environ Res 36:75–99

    Article  Google Scholar 

  • Codd GA, Morrison LF, Metcalf JS (2005) Cyanobacterial toxins: risk management for health protection. Toxicol Appl Pharmacol 203:264–272

    Article  CAS  PubMed  Google Scholar 

  • Conley DJ, Paerl HW, Howarth RW, Boesch DF, Seitzinger SP, Havens KE, Lancelot C, Likens GE (2009) Controlling eutrophication: nitrogen and phosphorus. Science 323:1014–1015

    Article  CAS  PubMed  Google Scholar 

  • Cooke GD, Welch EB, Peterson SA, Nichols SA (2005) Restoration and management of lakes and reservoirs. Taylor and Francis, Boca Raton

    Book  Google Scholar 

  • Dodds WK, Bouska WW, Eitzmann JL, Pilger TJ, Pitts KL, Riley AJ, Schloesser JT, Thornbrugh DJ (2009) Eutrophication of U.S. freshwaters: analysis of potential economic damages. Environ Sci Technol 43:12–19

    Article  CAS  PubMed  Google Scholar 

  • Dokulil MT, Teubner K (2000) Cyanobacterial dominance in lakes. Hydrobiologia 438:1–12

    Article  CAS  Google Scholar 

  • Downing JA, Watson SB, McCauley E (2001) Predicting cyanobacteria dominance in lakes. Can J Fish Aquat Sci 58:1905–1908

    Article  Google Scholar 

  • Fergus CE, Soranno PA, Cheruvelil KS, Bremigan MT (2011) Multiscale landscape and wetland drivers of lake total phosphorus and water color. Limnol Oceanogr 56:2127–2146

    Article  CAS  Google Scholar 

  • Fraterrigo JM, Downing JA (2008) The influence of land use on lake nutrients varies with watershed transport capacity. Ecosystems 11:1021–1034

    Article  CAS  Google Scholar 

  • Gemesi Z, Downing JA, Cruse RM, Anderson PF (2011) Effects of watershed configuration and composition on downstream lake water quality. J Environ Qual 40:517–527

    Article  CAS  PubMed  Google Scholar 

  • Gorham E (1964) Morphometric control of annual heat budgets in temperate lakes. Limnol Oceanogr 9:525–529

    Article  Google Scholar 

  • Gorham E, Boyce FM (1989) Influence of lake surface area and depth upon thermal stratification and the depth of the summer thermocline. J Great Lakes Res 15:233–245

    Article  Google Scholar 

  • Hall RI, Leavitt PR, Quinlan R, Dixit AS, Smol JP (1999) Effects of agriculture, urbanization, and climate on water quality in the northern Great Plains. Limnol Oceanogr 44:739–756

    Article  CAS  Google Scholar 

  • Hallegraeff GM (1993) A review of harmful algal blooms and their apparent global increase. Phycologia 32:79–99

    Article  Google Scholar 

  • Hu W, Zhou W, He H (2015) The effect of land-use intensity on surface temperature in the Dongting Lake Area, China. Adv Meteor 2015:1–11. doi:10.1155/2015/632151

    Google Scholar 

  • Huisman J, Matthijs HCP, Visser PM (2005) Harmful cyanobacteria. Springer, Dordrecht

    Book  Google Scholar 

  • Ibelings BW, Mur LR, Walsby AE (1991) Diurnal changes in buoyancy and vertical distribution in populations of Microcystis in two shallow lakes. J Plankton Res 13:419–436

    Article  Google Scholar 

  • Jeppesen E, Sondergaard M, Jensen JP, Havens KE, Anneville O, Carvalho L, Coveney MF, Deneke R, Dokulil MT, Foy B, Gerdeaux D, Hampton SE, Hilt S, Kangur K, Kohler J, Lammens EHHR, Lauridsen TL, Manca M, Miracle MR, Moss B, Noges P, Persson G, Phillips G, Portielje R, Schelske CL, Straile D, Tatrai I, Willen E, Winder M (2005) Lake responses to reduced nutrient loading—an analysis of contemporary long-term data from 35 case studies. Freshw Biol 50:1747–1771

    Article  CAS  Google Scholar 

  • Jöhnk KD, Huisman J, Sharples J, Sommeijer B, Visser PM, Stroom JM (2008) Summer heatwaves promote blooms of harmful cyanobacteria. Glob Change Biol 14:495–512

    Article  Google Scholar 

  • Katsiapi M, Mazaris AD, Charalampous E, Moustaka-Gouni M (2012) Watershed land use types as drivers of freshwater phytoplankton structure. Hydrobiologia 698:121–131

    Article  CAS  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

    Article  Google Scholar 

  • Kosten S, Huszar VLM, Bécares E, Costa LS, van Donk E, Hansson LA, Jeppesen E, Kruk C, Lacerot G, Mazzeo N, De Meester L, Moss B, Lürling M, Nõges T, Romo S, Scheffer M (2012) Warmer climates boost cyanobacterial dominance in shallow lakes. Glob Change Biol 18:118–126

    Article  Google Scholar 

  • LeBlanc RT, Brown RD, FitzGibbon JE (1997) Modeling the effects of land use change on the water temperature in unregulated urban streams. J Environ Manag 49:445–469

    Article  Google Scholar 

  • Lehman JT, Doubek JP, Jackson EW (2013) Effect of reducing allochthonous P load on biomass and alkaline phosphatase activity of phytoplankton in an urbanized watershed, Michigan. Lake Reserv Manag 29:116–125

    Article  CAS  Google Scholar 

  • Lürling M, Eshetu F, Faassen EJ, Kosten S, Huszar VLM (2013) Comparison of cyanobacterial and green algal growth rates at different temperatures. Freshw Biol 58:552–559

    Article  Google Scholar 

  • Naddafi R, Pettersson K, Eklov P (2007) The effect of seasonal variation in selective feeding by zebra mussels (Dreissena polymorpha) on phytoplankton community composition. Freshw Biol 52:823–842

    Article  Google Scholar 

  • Nielsen A, Trolle D, Sondergaard M, Lauridsen TL, Bjerring R, Olesen JE, Jeppesen E (2012) Watershed land use effects on lake water quality in Denmark. Ecol Appl 22:1187–1200

    Article  PubMed  Google Scholar 

  • Otieno VO, Anyah RO (2012) Effects of land use changes on climate in the Greater Horn of Africa. Clim Res 52:77–95

    Article  Google Scholar 

  • Paerl HW (2009) Controlling eutrophication along the freshwater-marine continuum: dual nutrient (N and P) reductions are essential. Estuar Coast 32:593–601

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Paerl HW, Otten TG (2013) Harmful cyanobacterial blooms: causes, consequences, and controls. Microb Ecol 65:995–1010

    Article  CAS  PubMed  Google Scholar 

  • Paul WJ, Hamilton DP, Ostrovsky I, Miller SD, Zhang A, Muraoka K (2012) Catchment land use and trophic state impacts on phytoplankton composition: a case study from the Rotorua lakes’ district, New Zealand. Hydrobiologia 698:133–146

    Article  CAS  Google Scholar 

  • Ptacnik R, Lepistö L, Willén E, Brettum P, Andersen T, Rekolainen S, Lyche Solheim A, Carvalho L (2008) Quantitative responses of lake phytoplankton to eutrophication in Northern Europe. Aquat Ecol 42:227–236

    Article  CAS  Google Scholar 

  • Reynolds CS (2006) The ecology of phytoplankton. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Rigosi A, Carey CC, Ibelings BW, Brookes JD (2014) The interaction between climate warming and eutrophication to promote cyanobacteria is dependent on trophic state and varies among taxa. Limnol Oceanogr 59:99–114

    Article  Google Scholar 

  • Schindler DW (2006) Recent advances in the understanding and management of eutrophication. Limnol Oceanogr 51:356–363

    Article  Google Scholar 

  • Schindler DW (2012) The dilemma of controlling cultural eutrophication of lakes. Proc R Soc B Biol Sci 279:4322–4333

    Article  CAS  Google Scholar 

  • Schindler DW, Hecky RE, Findlay DL, Stainton MP, Parker BR, Paterson MJ, Beaty KG, Lyng M, Kasian SEM (2008) Eutrophication of lakes cannot be controlled by reducing nitrogen input: results of a 37-year whole-ecosystem experiment. Proc Natl Acad Sci USA 105:11254–11258

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Schindler DW, Hecky RE, McCullough GK (2012) The rapid eutrophication of Lake Winnipeg: greening under global change. J Great Lakes Res 38:6–13

    Article  CAS  Google Scholar 

  • Sharpley AN, Chapra SC, Wedepohl R, Sims JT, Daniel TC, Reddy KR (1994) Managing agricultural phosphorus for protection of surface waters: issues and options. J Environ Qual 23:437–451

    Article  CAS  Google Scholar 

  • Sharpley AN, McDowell RW, Kleinman PJA (2001) Phosphorus loss from land to water: integrating agricultural and environmental management. Plant Soil 237:287–307

    Article  CAS  Google Scholar 

  • Smith VH (1983) Low nitrogen to phosphorus ratios favor dominance by blue-green algae in lake phytoplankton. Science 221:669–671

    Article  CAS  PubMed  Google Scholar 

  • Soranno PA, Hubler SL, Carpenter SR, Lathrop RC (1996) Phosphorus loads to surface waters: a simple model to account for spatial pattern of land use. Ecol Appl 6:865–878

    Article  Google Scholar 

  • Thompson AM, Kim K, Vandermuss AJ (2008a) Thermal characteristics of stormwater runoff from asphalt and sod surfaces. J Am Water Resour Assoc 44:1325–1336

    Article  Google Scholar 

  • Thompson AM, Wilson T, Norman J, Gemechu AL, Roa-Espinosa A (2008b) Modeling the effect of summertime heating on urban runoff temperature. J Am Water Resour Assoc 44:1548–1563

    Article  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. Freshw Biol 56:791–811

    Article  CAS  Google Scholar 

  • Wagner C, Adrian R (2009) Cyanobacteria dominance: quantifying the effects of climate change. Limnol Oceanogr 54:2460–2468

    Article  Google Scholar 

  • Wagner T, Soranno PA, Webster KE, Cheruvelil KS (2011) Landscape drivers of regional variation in the relationship between total phosphorus and chlorophyll in lakes. Freshw Biol 56:1811–1824

    Article  Google Scholar 

  • Warton DI, Hui FKC (2011) The arcsine is asinine: the analysis of proportions in ecology. Ecology 92:3–10

    Article  PubMed  Google Scholar 

  • Wetzel RG (1990) Reservoir ecosystems: Conclusions and speculations. In: Thornton KW, Kimmel BL, Payne FE (eds) Reservoir limnology: ecological perspectives. Wiley, New York, pp 227–238

    Google Scholar 

  • Wetzel RG (2001) Limnology: lake and river ecosystems. Academic Press, San Diego

    Google Scholar 

  • White JD, Kaul RB, Knoll LB, Wilson AE, Sarnelle O (2011) Large variation in vulnerability to grazing within a population of the colonial phytoplankter, Microcystis aeruginosa. Limnol Oceanogr 56:1714–1724

    Google Scholar 

  • Wilson MA, Carpenter SR (1999) Economic valuation of freshwater ecosystem services in the United States: 1971-1997. Ecol Appl 9:772–783

    Google Scholar 

  • Xu H, Paerl HW, Qin BQ, Zhu GW, Gao G (2010) Nitrogen and phosphorus inputs control phytoplankton growth in eutrophic Lake Taihu, China. Limnol Oceanogr 55:420–432

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank the EPA for making their NLA dataset publicly available. This manuscript benefitted from helpful comments by A.B. Gerling. This study was supported by the Virginia Tech Department of Biological Sciences and U.S. National Science Foundation grants DEB-1157992 and DEB-1046121.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jonathan P. Doubek.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 179 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Doubek, J.P., Carey, C.C. & Cardinale, B.J. Anthropogenic land use is associated with N-fixing cyanobacterial dominance in lakes across the continental United States. Aquat Sci 77, 681–694 (2015). https://doi.org/10.1007/s00027-015-0411-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00027-015-0411-x

Keywords