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Ecosystems

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Co-limitation by N and P Characterizes Phytoplankton Communities Across Nutrient Availability and Land Use

  • A. R. BrattEmail author
  • J. C. Finlay
  • J. R. Welter
  • B. A. Vculek
  • R. E. Van Allen
Article

Abstract

Historically, freshwater lakes have been widely assumed to be singly limited by phosphorus (P) because the dominant paradigm assumes that nitrogen fixation (N2 fixation) will compensate for any nitrogen (N) deficits. However, a growing body of evidence demonstrates that primary producer response to nutrient manipulation most frequently indicates co-limitation by N and P. Differences in N and P supply ratio have been shown to influence the identity and severity of nutrient limitation, but whether N and P concentration and the ratio of N to P concentrations can explain the frequency of co-limitation in aquatic primary producer assemblages remains unclear, especially in ecosystems subject to human perturbation that strongly increase nutrient availability. We determined how resource availability influences nutrient limitation by N and P of phytoplankton primary production across 12 lakes in Minnesota that vary in watershed land use and lake nutrient levels. We measured epilimnetic lake metabolism and indicators of N2 fixation to evaluate their influence on nutrient limitation status of planktonic algal assemblages. Despite large differences in land use (agricultural, urban, and suburban) and water column N and P availability, planktonic algal response to nutrient manipulation was consistently characterized by co-limitation by N and P across years and months. Neither P availability (as concentrations of total and inorganic forms) nor N2-flux rate predicted responses to nutrient additions. N availability significantly influenced responses of phytoplankton to nutrient additions across years, but this effect was small. The ratio of total N to total P significantly influenced the response to single additions of N and P (these effects were negative and positive, respectively) in summer 2013. Importantly, higher lake primary production and heterocyte count (number of nitrogen fixing cells) were also associated with a stronger, positive response to N + P addition. Overall, these data suggest that planktonic algal assemblages are predominantly characterized by co-limitation by N and P despite large and diverse human impacts on nutrient inputs. Additionally, higher rates of primary production increase the likelihood of co-limitation. Together, these results further support the paradigm shift toward dual management of N and P in aquatic ecosystems.

Keywords

nutrient limitation phytoplankton land use biogeochemical cycles phosphorus paradigm co-limitation 

Notes

Acknowledgments

We are grateful to Sandy Brovold, Michelle Rorer, and Katie Kemmit for laboratory analysis of samples at UMN and thank Kerrick Sarbacker, Adam Worm, Katie Kemmit, and Erika Senyk for field and laboratory assistance. We also thank two anonymous reviews for comments that much improved this manuscript. This research was supported by grants from the Institute on the Environment, Moos Graduate Research Fellowships in Aquatic Biology from the University of Minnesota and St. Catherine University undergraduate research support. ARB was supported by an Environmental Protection Agency’s STAR Ph.D. fellowship.

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10021_2019_459_MOESM1_ESM.pdf (2.7 mb)
Supplementary material 1 (PDF 2720 kb)

References

  1. Abell JM, Özkundakci D, Hamilton DP. 2010. Nitrogen and phosphorus limitation of phytoplankton growth in new zealand lakes: implications for eutrophication control. Ecosystems 13:966–77.CrossRefGoogle Scholar
  2. Bates D, Maechler M, Bolker B, Walker S. 2015. Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48.CrossRefGoogle Scholar
  3. Benfield MC, Grosjean P, Culverhouse PF, Irigoien X, Sierackie ME, Lopez-Urrutia A, Dam HG, Hu Q, Davis CS, Hansten A, Pilskaln CH, Riseman EM, Schultz H, Utgoff PE, Gorsky G. 2007. Research on automated plankton identification. Oceanography 20:172–87.CrossRefGoogle Scholar
  4. Bergström AK, Jansson M. 2006. Atmospheric nitrogen deposition has caused nitrogen enrichment and eutrophication of lakes in the northern hemisphere. Glob Chang Biol 12:635–43.CrossRefGoogle Scholar
  5. Bloom A. 1985. Resource limitation in plants—an economic analogy. Annu Rev Ecol Syst 16:363–92.CrossRefGoogle Scholar
  6. Bratt AR, Finlay JC, Hobbie SE, Janke BD, Worm AC, Kemmitt KL. 2017. Contribution of leaf litter to nutrient export during winter months in an urban residential watershed. Environ Sci Technol 51:3138–47.PubMedCrossRefGoogle Scholar
  7. Capitol Region Watershed District. 2010. Capitol Region Watershed District 2009 Monitoring Report. St. Paul, MN.Google Scholar
  8. Capitol Region Watershed District. 2013. Capitol Region Watershed District 2012 Stormwater Monitoring Report. St. Paul, MN.Google Scholar
  9. Carnelian-Marine St. Croix Watershed District. 2012. Square Lake Implementation Plan Refinement Project. Stillwater, MN.Google Scholar
  10. Chapin F. 1980. The mineral nutrition of wild plants. Annu Rev Ecol Syst 11:233–60.CrossRefGoogle Scholar
  11. Collins SM, Oliver SK, Lapierre JF, Stanley EH, Jones JR, Wagner T, Soranno PA. 2017. Lake nutrient stoichiometry is less predictable than nutrient concentrations at regional and sub-continental scales. Ecol Appl 27:1529–40.PubMedCrossRefGoogle Scholar
  12. Conley DJ, Paerl HW, Howarth RW, Boesch DF, Seitzinger SP, Havens KE, Lancelot C, Likens GE. 2009. Ecology. Controlling eutrophication: nitrogen and phosphorus. Science 323:1014–15.PubMedCrossRefGoogle Scholar
  13. Cordell D, Drangert J-O, White S. 2009. The story of phosphorus: Global food security and food for thought. Glob Environ Change 19:292–305.CrossRefGoogle Scholar
  14. Cotner JB. 2016. Nitrogen is not a ‘House of Cards’. Environ Sci Technol 51:3.PubMedCrossRefGoogle Scholar
  15. 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.PubMedCrossRefGoogle Scholar
  16. Donnell DRO, Wilburn P, Silow EA, Yampolsky LY, Litchman E. 2017. Nitrogen and phosphorus colimitation of phytoplankton in Lake Baikal: insights from a spatial survey and nutrient enrichment experiments.Google Scholar
  17. Easton ZM, Petrovic AM. 2008. Determining phosphorus loading rates based on land use in an urban watershed. Fate Nutr Pestic Urban Environ 997:19–42.CrossRefGoogle Scholar
  18. Elser J, Bracken M, Cleland E, Gruner DS, Harpole WS, Hillebrand H, Ngai JT, Seabloom EW, Shurin JB, Smith JE. 2007. Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10:1135–42.  https://doi.org/10.1111/j.1461-0248.2007.01113.x/full.CrossRefPubMedGoogle Scholar
  19. Francoeur SN, Biggs BJF, Smith R a, Lowe RL. 1999. Nutrient Limitation of algal biomass accrual in streams: seasonal patterns and a comparison of methods. J North Am Benthol Soc 18:242–60. http://www.jstor.org/stable/10.2307/1468463.CrossRefGoogle Scholar
  20. Fraterrigo JM, Downing JA. 2008. The influence of land use on lake nutrients varies with watershed transport capacity. Ecosystems 11:1021–34.CrossRefGoogle Scholar
  21. Gleeson S, Tilman D. 1992. Plant allocation and the multiple limitation hypothesis. Am Nat 139:1322–43.CrossRefGoogle Scholar
  22. Gruner DS, Smith JE, Seabloom EW, Sandin SA, Ngai JT, Hillebrand H, Harpole WS, Elser JJ, Cleland EE, Bracken MES, Borer ET, Bolker BM. 2008. A cross-system synthesis of consumer and nutrient resource control on producer biomass. Ecol Lett 11:740–55.PubMedCrossRefGoogle Scholar
  23. Halbach A. 2017. Trends in total phosphorus concentrations in urban and non-urban environments. Dissertation, University of MN (master’s thesis).Google Scholar
  24. Hall SJ, Weintraub SR, Eiriksson D, Brooks PD, Baker MA, Bowen GJ, Bowling DR. 2016. Stream nitrogen inputs reflect groundwater across a snowmelt-dominated montane to urban watershed. Environ Sci Technol 50:1137–46.PubMedCrossRefGoogle Scholar
  25. Harpole WS, Ngai JT, Cleland EE, Seabloom EW, Borer ET, Bracken MES, Elser JJ, Gruner DS, Hillebrand H, Shurin JB, Smith JE. 2011. Nutrient co-limitation of primary producer communities. Ecol Lett 14:852–62.PubMedCrossRefPubMedCentralGoogle Scholar
  26. Hayes NM, Vanni MJ, Horgan MJ, Renwick WHWH. 2015. Climate and land use interactively affect lake phytoplankton nutrient limitation status. Ecology 96:392–402.PubMedCrossRefPubMedCentralGoogle Scholar
  27. Hobbie SE, Finlay JC, Benjamin D, Nidzgorski DA, Millet DB, Lawrence A. 2017. Contrasting nitrogen and phosphorus budgets in urban watersheds and implications for managing urban water pollution. Proc Natl Acad Sci 114:4177–82.PubMedCrossRefPubMedCentralGoogle Scholar
  28. Howarth RW, Marino R. 2006. Nitrogen as the limiting nutrient for eutrophication in coastal marine ecosystems: evolving views over three decades. Limnol Oceanogr 51:364–76.CrossRefGoogle Scholar
  29. Interlandi S, Kilham S. 2001. Limiting resources and the regulation of diversity in phytoplankton communities. Ecology 82:1270–82.CrossRefGoogle Scholar
  30. Janke BD, Finlay JC, Hobbie SE. 2017. Trees and streets as drivers of urban stormwater nutrient pollution. Environ Sci Technol 51:9569–79.PubMedCrossRefGoogle Scholar
  31. Janke BD, Finlay JC, Hobbie SE, Baker LA, Sterner RW, Nidzgorski D, Wilson BN. 2014. Contrasting influences of stormflow and baseflow pathways on nitrogen and phosphorus export from an urban watershed. Biogeochemistry 121:209–28.CrossRefGoogle Scholar
  32. Kaspari M, Powers JS. 2016. Biogeochemistry and geographical ecology: embracing all twenty-five elements required to build organisms. Am Nat 188:S62–73.PubMedCrossRefPubMedCentralGoogle Scholar
  33. Keck F, Lepori F. 2012. Can we predict nutrient limitation in streams and rivers? Freshw Biol 57:1410–21.CrossRefGoogle Scholar
  34. Lewis WM, Wurtsbaugh WA. 2008. Control of lacustrine phytoplankton by nutrients: erosion of the phosphorus paradigm. Int Rev Hydrobiol 93:446–65.CrossRefGoogle Scholar
  35. Lin T, Gibson V, Cui S, Yu CP, Chen S, Ye Z, Zhu YG. 2014. Managing urban nutrient biogeochemistry for sustainable urbanization. Environ Pollut 192:244–50.PubMedCrossRefGoogle Scholar
  36. Marcarelli AM, Wurtsbaugh WA. 2007. Effects of upstream lakes and nutrient limitation on periphytic biomass and nitrogen fixation in oligotrophic, subalpine streams. Freshw Biol 52:2211–25.CrossRefGoogle Scholar
  37. Metropolitan Airport Commission. 1996. MSP long term comprehensive plan update.Google Scholar
  38. Minneapolis Park & Recreation Board. 2012. 2011 Water resources report. Minneapolis, MN.Google Scholar
  39. Minnesota Conservation Department. 1968. An inventory of Minnesota lakes. St. Paul, MN.Google Scholar
  40. Minnesota Pollution Control Agency. 2007. Twin and Ryan Lakes Nutrient TMDL. St. Paul, MN.Google Scholar
  41. Minnesota Pollution Control Agency. 2009. Peltier Lake. St. Paul, MN.Google Scholar
  42. North RL, Guildford SJ, Smith REH, Havens SM, Twiss MR. 2007. Evidence for phosphorus, nitrogen, and iron colimitation of phytoplankton communities in Lake Erie. Limnol Oceanogr 52:315–28.CrossRefGoogle Scholar
  43. Paerl HW, Hall NS, Peierls BL, Rossignol KL. 2014. Evolving paradigms and challenges in estuarine and coastal eutrophication dynamics in a culturally and climatically stressed world. Estuaries Coasts 37:243–58.CrossRefGoogle Scholar
  44. Paerl HW, Otten TG, Kudela R. 2018. Mitigating the expansion of harmful algal blooms across the freshwater-to-marine continuum. Environ Sci Technol 52:5519–29.PubMedCrossRefGoogle Scholar
  45. Paerl HW, Xu H, Hall NS, Rossignol KL, Joyner AR, Zhu G, Qin B. 2015. Nutrient limitation dynamics examined on a multi-annual scale in Lake Taihu, China: implications for controlling eutrophication and harmful algal blooms. J Freshw Ecol 30:5–24.CrossRefGoogle Scholar
  46. Pallardy J, Keseley S, Erdmann J. 2013. Upper cannon lakes excess nutrient TMDL: Jefferson-German Lake Chain.Google Scholar
  47. Ptacnik R, Andersen T, Tamminen T. 2010. Performance of the redfield ratio and a family of nutrient limitation indicators as thresholds for phytoplankton N vs P limitation. Ecosystems 13:1201–14.CrossRefGoogle Scholar
  48. R Core Team. 2018. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.
  49. Rabalais NN, Wiseman WJ. 2002. Gulf of Mexico Hypoxia, A.K.A. “The Dead Zone”. Annu Rev Ecol Syst 33:235–63.CrossRefGoogle Scholar
  50. Rastetter E, Shaver G. 1992. A model of multiple-element limitation for acclimating vegetation. Ecology 73:1157–74.CrossRefGoogle Scholar
  51. Read EK, Patil VP, Oliver SK, Hetherington AL, Brentrup JA, Zwart JA, Winters KM, Corman JR, Emily R, Woolway RI, Dugan HA, Jaimes A, Santoso AB, Grace S, Winslow LA, Hanson PC, Weathers KC. 2018. The importance of lake-specific characteristics for water quality across the continental United States. Ecol Appl 25:943–55.CrossRefGoogle Scholar
  52. Saito MA, Goepfert TJ, Ritt JT. 2008. Some thoughts three definitions on the concept of colimitation: and the importance of bioavailability. Limnol Oceanogr 53:276–90.CrossRefGoogle Scholar
  53. Schallenberg M, Burns CW. 2001. Tests of autotrophic picoplankton as early indicators of nutrient enrichment in an ultra-oligotrophic lake. Freshw Biol 46:27–37.CrossRefGoogle Scholar
  54. Schindler DW. 1977. Evolution of phosphorus limitation in lakes. Science 195:260–2.PubMedCrossRefGoogle Scholar
  55. Schindler DW. 2006. Recent advances in the understanding and management of eutrophication. Limnol Oceanogr 51:356–63.CrossRefGoogle Scholar
  56. Schindler DW. 2012. The dilemma of controlling cultural eutrophication of lakes. Proc Biol Sci 279:4322–33.PubMedPubMedCentralCrossRefGoogle Scholar
  57. Schindler DW, Carpenter SR, Chapra SC, Hecky RE, Orihel DM. 2016. Reducing phosphorus to curb lake eutrophication is a success. Environ Sci Technol 50:8923–9.PubMedCrossRefGoogle Scholar
  58. Schindler DW, Carpenter SR, Chapra SC, Hecky RE, Orihel DM. 2017. Response to the letter, nitrogen is not a ‘house of Cards’. Environ Sci Technol 51:1943.PubMedCrossRefGoogle Scholar
  59. 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 U S A 105:11254–8.PubMedPubMedCentralCrossRefGoogle Scholar
  60. Scott JT, McCarthy MJ. 2010. Nitrogen fixation may not balance the nitrogen pool in lakes over timescales relevant to eutrophication management. Limnol Oceanogr 55:1265–70.CrossRefGoogle Scholar
  61. South Washington Watershed District. 2011. Colby lake water quality monitoring report.Google Scholar
  62. Staehr P, Bade D, Van de Bogert MC, Koch GR, Williamson C, Hanson P, Cole JJ, Kratz TK. 2010. Lake metabolism and the diel oxygen technique: state of the science. Limnol Ocean Methods 8:628–44.CrossRefGoogle Scholar
  63. Sterner RW, Andersen T, Elser JJ, Hessen DO, Hood JM, McCauley E, Urabe J. 2008. Scale-dependent carbon:nitrogen:phosphorus seston stoichiometry in marine and freshwaters. Limnol Oceanogr 53:1169–80. http://www.aslo.org/lo/toc/vol_53/issue_3/1169.html.CrossRefGoogle Scholar
  64. Sterner RW. 2008. On the phosphorus limitation paradigm for lakes. Int Rev Hydrobiol 93:433–45.CrossRefGoogle Scholar
  65. Tank JL, Dodds WK. 2003. Nutrient limitation of epilithic and epixylic biofilms in ten North American streams. Freshw Biol 48:1031–49.CrossRefGoogle Scholar
  66. Taranu ZE, Köster D, Hall RI, Charette T, Forrest F, Cwynar LC, Gregory-Eaves I. 2009. Contrasting responses of dimictic and polymictic lakes to environmental change: a spatial and temporal study. Aquat Sci 72:97–115.CrossRefGoogle Scholar
  67. Turner RE, Rabalais NN. 2013. Nitrogen and phosphorus phytoplankton growth limitation in the northern Gulf of Mexico. Aquat Microb Ecol 68:159–69.CrossRefGoogle Scholar
  68. United States Environmental Protection Agency. 2015. Preventing eutrophication: scientific support for dual nutrient criteria.Google Scholar
  69. Van Drecht G, Bouwman AF, Harrison J, Knoop JM. 2009. Global nitrogen and phosphate in urban wastewater for the period 1970 to 2050. Glob Biogeochem Cycles 23:1–19.Google Scholar
  70. 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.CrossRefGoogle Scholar
  71. Vitousek PM, Aber JD, Howarth RW, Likens GE, Matson PA, Schindler DW, Schlesinger WH, Tilman DG. 1997. Human alteration of the global nitrogen cycle: sources and consequences. Ecol Appl 7:737–50.Google Scholar
  72. Walsh CJ, Roy AH, Feminella J, Cottingham P, Groffman PM, Morgan RP. 2005. The urban stream syndrome: current knowledge and the search for a cure. J North Am Benthol Soc 24:706–23.CrossRefGoogle Scholar
  73. Welschmeyer NA. 1994. Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and pheopigments. Limnol Oceanogr 39:1985–92.CrossRefGoogle Scholar
  74. Wyatt KH, Stevenson RJ, Turetsky MR. 2010. The importance of nutrient co-limitation in regulating algal community composition, productivity and algal-derived DOC in an oligotrophic marsh in interior Alaska. Freshw Biol 55:1845–60.CrossRefGoogle Scholar
  75. Zhang X, Wu Y, Gu B. 2015. Urban rivers as hotspots of regional nitrogen pollution. Environ Pollut 205:139–44.PubMedCrossRefPubMedCentralGoogle Scholar
  76. Zuur A, Ieno EN, Walker N, Saveliev AA, Smith GM. 2009. Mixed effects models and extensions in ecology with R. New York: Springer.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • A. R. Bratt
    • 1
    • 3
    Email author
  • J. C. Finlay
    • 1
  • J. R. Welter
    • 2
  • B. A. Vculek
    • 2
  • R. E. Van Allen
    • 1
  1. 1.Department of Ecology, Evolution and BehaviorUniversity of MinnesotaSt. PaulUSA
  2. 2.Department of BiologySt. Catherine UniversitySt. PaulUSA
  3. 3.Department of Environmental StudiesDavidson CollegeDavidsonUSA

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