Phytoplankton nutrient deficiencies vary with season in sub-tropical lakes of Nepal

  • Freya E. Rowland
  • Rebecca L. NorthEmail author
  • Preston McEachern
  • Daniel V. Obrecht
  • Tek Bahadur Gurung
  • Susan B. Jones
  • John R. Jones
Primary Research Paper


This is one of few studies to comprehensively examine seasonality and phytoplankton nutrient deficiency in sub-tropical lakes over multiple years, to our knowledge. We tested whether phytoplankton communities in two sub-tropical impoundments in the mid-hills of Nepal were nitrogen (N)-, phosphorus (P)-, or co-deficient in N and P across pre-monsoon, monsoon, and post-monsoon seasons spanning a decade. Nutrient limitation to phytoplankton growth was assessed via in situ stoichiometry of N and P (N:P ratios) and nutrient stimulation experiments (NSEs). The experiments indicated co-deficiency of N and P in 97–100% of NSEs in all seasons. N-deficiency was common (> 60% of N:P ratios and ~ 90% of NSEs) during the rainy monsoon, but P-deficiency occurred twice as often as N-deficiency during drier seasons (pre- and post-monsoon). These findings provide perspective for the ongoing debate over N and P as limiting nutrients in freshwater ecosystems by incorporating seasonality and corresponding hydrology. We also re-visit long-standing assumptions regarding the nutrient status of sub-tropical lakes. The warm, stratified season does not fully illustrate lake processes, and more research during dry periods will inform how seasonality affects phytoplankton nutrient deficiencies across aquatic systems.


Limiting nutrient Monsoon Phytoplankton Nutrient stimulation experiments Nitrogen Phosphorus 



We thank Erin Petty for making Figure. 1. We also thank Jennifer Parris, Jennifer Graham, John MacEachern, Robert Bacon, Bruce Perkins, Glenn Wylie, Lance Dorsey, Prem Nepali, and IUCN Nepal for their assistance during the study. We thank Gertrud Nürnberg for advice on internal nutrient loading. This work was supported by the National Science Foundation (INT-9602105).

Supplementary material

10750_2019_3897_MOESM1_ESM.docx (67 kb)
Supplementary material 1 (DOCX 67 kb)


  1. Abell, J. M., D. Özkundakci & D. P. Hamilton, 2010. Nitrogen and phosphorus limitation of phytoplankton growth in New Zealand lakes: implications for eutrophication control. Ecosystems 13: 966–977.CrossRefGoogle Scholar
  2. Abell, J. M., D. Özkundakci, D. P. Hamilton & J. R. Jones, 2012. Latitudinal variation in nutrient stoichiometry and chlorophyll-nutrient relationships in lakes: A global study. Fundamental & Applied Limnology 181: 1–14.CrossRefGoogle Scholar
  3. An, K. G. & J. R. Jones, 2002. Reservoir response to the Asian monsoon with emphasis on longitudinal gradients. Journal of Freshwater Ecology 17: 151–160.CrossRefGoogle Scholar
  4. Arrigo, K. R., 2005. Marine microorganisms and global nutrient cycles. Nature 437: 349–355.CrossRefGoogle Scholar
  5. Arrigo, K. R., M. M. Mills, L. R. Kropuenske, G. L. van Dijken, A.-C. Alderkamp & D. H. Robinson, 2010. Photophysiology in two major Southern Ocean phytoplankton taxa: photosynthesis and growth of Phaeocystis antarctica and Fragilariopsis cylindrus under different irradiance levels. Integr Comp Biol 50: 950–966.CrossRefGoogle Scholar
  6. Bayer, T. K., M. Schallenberg & C. E. Martin, 2008. Investigation of nutrient limitation status and nutrient pathways in Lake Hayes, Otago, New Zealand: a case study for integrated lake assessment. New Zealand Journal of Marine and Freshwater Research 42: 285–295.CrossRefGoogle Scholar
  7. Blackman, F. F., 1905. Optima and limiting factors. Ann Bot 19: 281–295.CrossRefGoogle Scholar
  8. Beutel, M. W., 2006. Inhibition of ammonia release from anoxic profundal sediments in lakes using hypolimnetic oxygenation. Ecological Engineering 28: 271–279.CrossRefGoogle Scholar
  9. Burford, M. A., S. A. Green, A. J. Cook, S. A. Johnson, J. G. Kerr & K. R. O’Brien, 2012. Sources and fate of nutrients in a subtropical reservoir. Aquatic Sciences 74: 179–190.CrossRefGoogle Scholar
  10. Carpenter, S. R., 1996. Microcosm experiments have limited relevance for community and ecosystem ecology. Ecology 77: 677–680.CrossRefGoogle Scholar
  11. Collins, R. & A. Jenkins, 1996. The impact of agricultural land use on stream chemistry in the Middle Hills of the Himalayas. Nepal. Journal of Hydrology 185: 71–86.CrossRefGoogle Scholar
  12. Corman, J. R., E. Carlson, M. Dix, N. Girón, A. Roegner, J. Veselá, S. Chandra, J. J. Elser & E. Rejmánková, 2015. Nutrient dynamics and phytoplankton resource limitation in a deep tropical mountain lake. Inland Waters 5: 371–386.CrossRefGoogle Scholar
  13. Crumpton, W. G., T. M. Isenhart & P. D. Mitchell, 1992. Nitrate and organic N analyses with second-derivative spectroscopy. Limnology & Oceanography 37: 907.CrossRefGoogle Scholar
  14. Dahal, B. M., I. Nyborg, B. K. Sitaula & R. M. Bajracharya, 2009. Agricultural intensification: food insecurity to income security in a mid-hill watershed of Nepal. International Journal of Agricultural Sustainability 7: 249–260.CrossRefGoogle Scholar
  15. Dahal, B. M., B. K. Sitaula, S. Sharma & R. M. Bajracharya, 2007. Effects of agricultural intensification on the quality of rivers in rural watersheds of Nepal. J Food Agric Environ 5: 341.Google Scholar
  16. Davis, M. F., T. B. Gurung, B. Shrestha, S. B. Jones, G. D. Wylie, B. D. Perkins & J. R. Jones, 1998. Use of a subsurface plankton layer to benefit a cage-culture fishery in Lake Phewa. Nepal. Internationale Vereinigung fur Theoretische und Angewandte Limnologie Verhandlungen 26: 2220–2227.Google Scholar
  17. Döll, P. & J. Zhang, 2010. Impact of climate change on freshwater ecosystems: a global-scale analysis of ecologically relevant river flow alterations. Hydrology and Earth System Sciences 14: 783–799.CrossRefGoogle Scholar
  18. Dore, M. H., 2005. Climate change and changes in global precipitation patterns: what do we know? Environ Int 31: 1167–1181.CrossRefGoogle Scholar
  19. Downing, J., M. McClain, R. Twilley, J. Melack, J. Elser, N. Rabalais, W. Lewis, R. Turner, J. Corredor & D. Soto, 1999. The impact of accelerating land-use change on the N-cycle of tropical aquatic ecosystems: current conditions and projected changes. Biogeochemistry 46: 109–148.Google Scholar
  20. Downs, T., M. Schallenberg & C. Burns, 2008. Responses of lake phytoplankton to micronutrient enrichment: a study of two New Zealand lakes and an analysis of published data. Aquatic Sciences 70: 347–360.CrossRefGoogle Scholar
  21. Dubourg, P., R. L. North, K. Hunter, D. M. Vandergucht, O. Abirhire, G. M. Silsbe, S. J. Guildford & J. J. Hudson, 2015. Light and nutrient co-limitation of phytoplankton communities in a large reservoir: Lake Diefenbaker, Saskatchewan, Canada. Journal of Great Lakes Research 41: 129–143.CrossRefGoogle Scholar
  22. Dussart, B., 1974. Biology of inland waters in humid tropical Asia. UNESCO Natural Resources of Humid Tropical Asia Nat Resour Res 12: 331–353.Google Scholar
  23. Elser, J. J., M. E. Bracken, E. E. Cleland, D. S. Gruner, W. S. Harpole, H. Hillebrand, J. T. Ngai, E. W. Seabloom, J. B. Shurin & J. E. Smith, 2007. Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecology Letters 10: 1135–1142.CrossRefGoogle Scholar
  24. Falkowski, P. G. & J. A. Raven, 2007. Aquatic Photosynthesis. Princeton University Press, Princeton, New Jersey.Google Scholar
  25. Fox, J. & S. Weisberg. 2011. An R Companion to Applied Regression, Second Edition. Thousand Oaks CA: Sage.
  26. Gal, J.-K., G. Ock, H.-K. Park & K.-H Shin, 2016. The effect of summer monsoon on pelagic and littoral food webs in a large regulated reservoir (Lake Paldang, Korea): A stable isotope approach. Journal of Freshwater Ecology 31 (3): 327–340.CrossRefGoogle Scholar
  27. Guildford, S. J. & R. E. Hecky, 2000. Total nitrogen, total phosphorus, and nutrient limitation in lakes and oceans: Is there a common relationship? Limnology & Oceanography 45: 1213–1223.CrossRefGoogle Scholar
  28. Guildford, S. J., R. E. Hecky, W. D. Taylor, R. Mugidde & H. A. Bootsma, 2003. Nutrient enrichment experiments in tropical great lakes Malawi/Nyasa and Victoria. Journal of Great Lakes Research 29: 89–106.CrossRefGoogle Scholar
  29. Gurung, T. B., R. P. Dhakal & J. D. Bista, 2006. Phytoplankton primary production, chlorophyll-a and nutrient concentrations in the water column of mountainous Lake Phewa, Nepal. Lakes and Reservoirs: Research and Management 11 (3): 141–148.CrossRefGoogle Scholar
  30. Gurung, T. B., R. P. Dhakal, M. Husen & J. R. Jones, 2010. Abundance and nutrient limiting growth rate of heterotrophic bacterio-plankton in Himalayan foot hill Lake Phewa, Nepal. Lakes & Reservoirs: Research & Management 15: 53–61.CrossRefGoogle Scholar
  31. Harpole, W. S., J. T. Ngai, E. E. Cleland, E. W. Seabloom, E. T. Borer, M. E. Bracken, J. J. Elser, D. S. Gruner, H. Hillebrand & J. B. Shurin, 2011. Nutrient co-limitation of primary producer communities. Ecology Letters 14: 852–862.CrossRefGoogle Scholar
  32. Healey, F. P. & L. L. Hendzel, 1980. Physiological Indicators of Nutrient Deficiency in Lake Phytoplankton. Canadian Journal of Fisheries & Aquatic Sciences 37: 442–453.CrossRefGoogle Scholar
  33. Hecky, R. & P. Kilham, 1988. Nutrient limitation of phytoplankton in freshwater and marine environments: a review of recent evidence on the effects of enrichment. Limnology & Oceanography 33: 796–822.Google Scholar
  34. Higgins, S. N., M. J. Paterson, R. E. Hecky, D. W. Schindler, J. J. Venkiteswaran & D. L. Findlay, 2017. Biological Nitrogen fixation prevents the response of a eutrophic lake to reduced loading of nitrogen: evidence from a 46-year whole-lake experiment. Ecosystems 21: 1–13. Scholar
  35. Hothorn, T., F. Bretz & P. Westfall, 2008. Simultaneous inference in general parametric models. Biometrical Journal 50: 346–363.CrossRefGoogle Scholar
  36. Huszar, V. L., N. F. Caraco, F. Roland & J. Cole, 2006. Nutrient-chlorophyll relationships in tropical-subtropical lakes: do temperate models fit? Nitrogen Cycling in the Americas: Natural and Anthropogenic Influences and Controls. Springer, New York: 239–250.Google Scholar
  37. Jones, S. B. & J. R. Jones, 2002. Seasonal variation in cyanobacterial toxin production in two Nepalese lakes. Internationale Vereinigung fur Theoretische und Angewandte Limnologie Verhandlungen 8: 1017–1022.Google Scholar
  38. Jones, J. R., M. F. Knowlton & D. B. Swar, 1989. Limnological reconnaissance of waterbodies in central and southern Nepal. Hydrobiologia 184: 171–189.CrossRefGoogle Scholar
  39. Jones, J. R., B. D. Perkins, A. Witt Jr., M. S. Kaiser, S. Thamasara, M. Siriworakul & P. Benyasut, 2000. Limnological characteristics of some reservoirs in Thailand. Internationale Vereinigung fur Theoretische und Angewandte Limnologie Verhandlungen 27: 2158–2166.Google Scholar
  40. Jones, J. R., A. Thompson, C. N. Seong, J. S. Jung & H. Yang, 2006. Monsoon influences on the limnology of Juam Lake, South Korea. Internationale Vereinigung fur Theoretische und Angewandte Limnologie Verhandlungen 29: 1215–1222.Google Scholar
  41. Jones, J. R., D. V. Obrecht, B. D. Perkins, M. F. Knowlton, A. P. Thorpe, S. Watanabe & R. R. Bacon, 2008. Nutrients, seston, and transparency of Missouri reservoirs and oxbow lakes: An analysis of regional limnology. Lake and Reservoir Management 24: 155–180.CrossRefGoogle Scholar
  42. Jones, J., P. McEachern & D. Seo, 2009. Empirical evidence of monsoon influences on Asian Lakes. Aquatic Ecosystem Health & Management 12: 129–137.CrossRefGoogle Scholar
  43. Knowlton, M. F., 1984. Flow-through microcuvette for fluorometric determination of chlorophyll. Water Research Bulletin 20: 795–799.CrossRefGoogle Scholar
  44. Lacoul, P. & B. Freedman, 2005. Physical and chemical limnology of 34 lentic waterbodies along a tropical-to-alpine altitudinal gradient in Nepal. International Review of Hydrobiologia 90: 254–2460.CrossRefGoogle Scholar
  45. Lewis, W. M. & W. A. Wurtsbaugh, 2008. Control of lacustrine phytoplankton by nutrients: erosion of the phosphorus paradigm. International Review of Hydrobiology 93: 446–465.CrossRefGoogle Scholar
  46. Li, Y., C. Y. Tang, Z. B. Yu & K. Acharya, 2014. Correlations between algae and water quality: factors driving eutrophication in Lake Taihu, China. International Journal of Environmental Science and Technology 11: 169–182.CrossRefGoogle Scholar
  47. Lohman, K., J. R. Jones, M. F. Knowlton, D. B. Swar, M. A. Pamperl & B. J. Brazos, 1988. Pre- and postmonsoon limnological characteristics of lakes in the Pokhara and Kathmandu Valleys, Nepal. Internationale Vereinigung fur Theoretische und Angewandte Limnologie Verhandlungen 3: 558–565.Google Scholar
  48. McCullough, G. K., S. J. Page, R. H. Hesslein, M. P. Stainton, H. J. Kling, A. G. Salki & D. G. Barber, 2012. Hydrological forcing of a recent trophic surge in Lake Winnipeg. Journal of Great Lakes Research 38: 95–105.CrossRefGoogle Scholar
  49. Mitchell, S. F. & C. W. Burns, 1981. Phytoplankton photosynthesis and its relation to standing crop and nutrients in two warm-monomictic South Island lakes. New Zealand Journal of Marine and Freshwater Research 15: 51–67.CrossRefGoogle Scholar
  50. Morris, D. P. & W. M. Lewis, 1988. Phytoplankton nutrient limitation in Colorado mountain lakes. Freshwater Biology 20: 315–327.CrossRefGoogle Scholar
  51. Mortimer, C. H., 1941. The exchange of dissolved substances between mud and water in lakes. Journal of Ecology 29: 280–329.CrossRefGoogle Scholar
  52. Muhid, P. & M. A. Burford, 2012. Assessing nutrient limitation in a subtropical reservoir. Inland Waters 2: 185–192.CrossRefGoogle Scholar
  53. North, R., S. Guildford, R. Smith, S. Havens & M. Twiss, 2007. Evidence for phosphorus, nitrogen, and iron colimitation of phytoplankton communities in Lake Erie. Limnology & Oceanography 52: 315–328.CrossRefGoogle Scholar
  54. North, R., S. Guildford, R. Smith, M. Twiss & H. Kling, 2008. Nitrogen, phosphorus, and iron colimitation of phytoplankton communities in the nearshore and offshore regions of the African Great Lakes. Internationale Vereinigung fur Theoretische und Angewandte Limnologie Verhandlungen 30: 259–264.Google Scholar
  55. Orihel, D. M., H. M. Baulch, N. J. Casson, R. L. North, C. T. Parsons, D. C. M. Seckar & J. J. Venkiteswaran, 2017. Internal phosphorus loading in Canadian fresh waters: A critical review and data analysis. Canadian Journal of Fisheries and Aquatic Sciences 74 (12): 2005–2029.CrossRefGoogle Scholar
  56. Overpeck, J. T. & J. E. Cole, 2007. Climate change: Lessons from a distant monsoon. Nature 445: 270–271.CrossRefGoogle Scholar
  57. Paerl, H. W., J. T. Scott, M. J. McCarthy, S. E. Newell, W. S. Gardner, K. E. Havens, D. K. Hoffman, S. W. Wilhelm & W. A. Wurtsbaugh, 2016. It Takes Two to Tango: When and Where Dual Nutrient (N & P) Reductions Are Needed to Protect Lakes and Downstream Ecosystems. Environmental Science & Technology 50: 10805–10813.CrossRefGoogle Scholar
  58. Paerl, H. W., H. Xu, M. J. McCarthy, G. Zhu, B. Qin, Y. Li & W. S. Gardner, 2011. Controlling harmful cyanobacterial blooms in a hyper-eutrophic lake (Lake Taihu, China): the need for a dual nutrient (N & P) management strategy. Water Research 45: 1973–1983.CrossRefGoogle Scholar
  59. Park, C.-K. & S. D. Schubert, 1997. On the nature of the 1994 East Asian summer drought. Journal of Climate 10: 1056–1070.CrossRefGoogle Scholar
  60. Prepas, E. E. & F. H. Rigler, 1982. Improvements in quantifying the phosphorus concentration in lake water. Canadian Journal of Fisheries and Aquatic Sciences 39: 822–829.CrossRefGoogle Scholar
  61. Présing, M., S. Herodek, T. Preston & L. Vörös, 2001. Nitrogen uptake and the importance of internal nitrogen loading in Lake Balaton. Freshwater Biology 46: 125–139.CrossRefGoogle Scholar
  62. R Core Team (2018). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
  63. Rai, A. K., 2000. Limnological characteristics of subtropical Lakes Phewa, Begnas, and Rupa in Pokhara Valley, Nepal. Limnology 1: 33–46.CrossRefGoogle Scholar
  64. Rangel, L. M., L. H. S. Silva, P. Rosa, F. Roland & V. L. M. Huzar, 2012. Phytoplankton biomass is mainly controlled by hydrology and phosphorus concentrations in trophic hydroelectric reservoirs. Hydrobiologia 693: 13–28.CrossRefGoogle Scholar
  65. Ross, J. & R. Gilbert, 1999. Lacustrine sedimentation in a monsoon environment: the record from Phewa Tal, middle mountain region of Nepal. Geomorphology 27: 307–323.CrossRefGoogle Scholar
  66. Sartory, D. P. & J. U. Grobbelaar, 1986. Extraction of chlorophyll a from freshwater phytoplankton for spectrophotometric analysis. Hydrobiologia 114: 177–187.CrossRefGoogle Scholar
  67. Schindler, D., 1976. Biogeochemical evolution of phosphorus limitation in nutrient-enriched lakes of the Precambrian Shield. Ann Arbor Science Publishers, Ann Arbor.Google Scholar
  68. Schindler, D. W., S. R. Carpenter, S. C. Chapra, R. E. Hecky & D. M. Orihel, 2016. Reducing Phosphorus to Curb Lake Eutrophication is a Success. Environmental Science & Technology 50: 8923–8929.CrossRefGoogle Scholar
  69. Sterner, R. W., 2008. On the phosphorus limitation paradigm for lakes. International Review of Hydrobiology 93: 433–445.CrossRefGoogle Scholar
  70. Sterner, R. W. & J. J. Elser, 2002. Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, Princeton, N.J.Google Scholar
  71. Sthapit, K. M. & K. Leminen, 1992. Siltation Survey of Phewa Lake—Annual report of 1992. Integrated Watershed Management. Project Technical Paper No. 3r1992, pp: 24.Google Scholar
  72. Tilman, D., 1976. Ecological competition between algae: experimental confirmation of resource-based competition theory. Science 192: 463–465.CrossRefGoogle Scholar
  73. Vincent, W. F., W. Wurtsbaugh, C. L. Vincent & P. Richerson, 1984. Seasonal dynamics of nutrient limitation in a tropical high-altitude lake (Lake Titicaca, Peru-Bolivia): Application of physiological bioassays. Limnology & Oceanography 29: 540–552.CrossRefGoogle Scholar
  74. White, E., K. Law, G. Payne & S. Pickmere, 1985. Nutrient demand and availability among planktonic communities- an attempt to assess nutrient limitation to plant growth in 12 central volcanic plateau lakes. New Zealand Journal of Marine and Freshwater Research 19: 49–62.CrossRefGoogle Scholar
  75. White, E., G. Payne, S. Pickmere & P. Woods, 1991. Seasonal variation in nutrient limitation of the algal community in Lake Horowhenua, New Zealand. New Zealand Journal of Marine and Freshwater Research 25: 311–316.CrossRefGoogle Scholar
  76. Wu, Z., Y. Liu, Z. Liang, S. Wu & H. Guo, 2017. Internal cycling, not external loading, decides the nutrient limitation in eutrophic lake: A dynamic model with temporal Bayesian hierarchical inference. Water Research 116: 231–240.CrossRefGoogle Scholar
  77. Yan, Z., W. Han, J. Peñuelas, J. Sardans, J. J. Elser, E. Du, P. B. Reich & J. Fang, 2016. Phosphorus accumulates faster than nitrogen globally in freshwater ecosystems under anthropogenic impacts. Ecology Letters 19: 1237–1246.CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Freya E. Rowland
    • 1
    • 5
  • Rebecca L. North
    • 2
    Email author
  • Preston McEachern
    • 2
    • 3
  • Daniel V. Obrecht
    • 2
  • Tek Bahadur Gurung
    • 4
  • Susan B. Jones
    • 2
  • John R. Jones
    • 2
  1. 1.Division of Biological SciencesUniversity of MissouriColumbiaUSA
  2. 2.School of Natural ResourcesUniversity of MissouriColumbiaUSA
  3. 3.Civil and Environmental EngineeringUniversity of AlbertaEdmontonCanada
  4. 4.Nepal Agricultural Research CouncilKathmanduNepal
  5. 5.Cooperative Institute for Great Lakes Research (CIGLR)University of MichiganAnn ArborUSA

Personalised recommendations