Aquatic Sciences

, 82:11 | Cite as

The life aquatic in high relief: shifts in the physical and biological characteristics of alpine lakes along an elevation gradient in the Rocky Mountains, USA

  • Kelly A. LoriaEmail author
  • Diane McKnight
  • Dillon M. Ragar
  • Pieter T. J. Johnson
Research Article


Rapidly occurring environmental changes in alpine lakes highlight the importance of better understanding the ecological structure and function associated with these systems. Previous research has identified how the physical characteristics of lakes change as a function of landscape position, but comparatively little is known about shifts in the biotic community across mountain regions. In 2016, we sampled 19 lakes across an elevation gradient (2480–3550 m a.s.l.) within the Rocky Mountains, USA, to evaluate how both the abiotic characteristics of lakes and their planktonic biological communities covaried with elevation. Based on generalized linear mixed models (GLMMs), increases in elevation were associated with decreases in most nutrient concentrations (with the exception of nitrate), dissolved organic carbon, water temperature and lake stratification. Conversely, elevation increases were positively related to nitrate concentrations and water clarity. Extending this analysis to the biological community, we found that higher-elevation lakes exhibited lower phytoplankton and zooplankton densities, whereas elevation associated positively with average zooplankton size. Our data are consistent with the hypothesis that the alpine environment acts as a strong niche filter, limiting the quantity and diversity of taxa to groups capable of tolerating the short growing season, high flushing rate, strong variation in interannual precipitation, intense ultraviolet radiation exposure, and lower resource availability associated with such habitats.


Landscape limnology Mountain lake Elevation gradient Freshwater ecology Zooplankton Phytoplankton 



We thank the Niwot Ridge Long-Term Ecological Research program for supporting this research; the various field team members Kathi Hell-Jaros, Josh Darling, Samuel Fonteneli, Dylan Rose, Henry Brandes and Holly Miller who helped collect and process the survey data; Johnson Laboratory, notably Dana Calhoun, for their comments on the manuscript; Travis McDevitt-Galles and Wynne Moss for their insights on data analysis; William Bowman, Jen Morse, and Katherine Suding for their logistical support of this project; and The City of Boulder, Rocky Mountain National Park, Arapahoe and Roosevelt National Forest and Boulder County Open Space for allowing us to collect data in their treasured aquatic environments. For comments helpful in revising the manuscript, we thank Sudeep Chandra, Steve Sadro, Stuart Findlay, and one anonymous reviewer. This work was supported through the National Science Foundation (DEB-1637686 and DEB-1754171) as well as a fellowship from the David and Lucile Packard Foundation.

Supplementary material

27_2019_684_MOESM1_ESM.docx (126 kb)
Supplementary material 1 (DOCX 125 kb)


  1. Alexander RB, Boyer EW, Smith RA, Schwarz GE, Moore RB (2007) The role of headwater streams in downstream water quality. JAWRA 43(1):41–59. CrossRefPubMedGoogle Scholar
  2. Álvarez E, Moyano M, López-Urrutia Á, Nogueira E, Scharek R (2014) Routine determination of plankton community composition and size structure: a comparison between FlowCAM and light microscopy. J Plankton Res 36(1):170–184. CrossRefGoogle Scholar
  3. Angilletta MJ, Steury TD, Sears MW (2004) Temperature, growth rate, and body size in ectotherms: fitting pieces of a life-history puzzle. Integr Comp Biol 44(6):498–509PubMedGoogle Scholar
  4. Baker AL et al (2012) Phycokey—an image based key to Algae (PS Protista), Cyanobacteria, and other aquatic objects. University of New Hampshire Center for Freshwater Biology.
  5. Baron JS, Schmidt TM, Hartman MD (2009) Climate-induced changes in high elevation stream nitrate dynamics. Glob Chang Biol 15(7):1777–1789. CrossRefGoogle Scholar
  6. Barton K, Barton MK (2015) Package ‘MuMIn’. Version 1:18Google Scholar
  7. Baselga A (2013) Separating the two components of abundance-based dissimilarity: balanced changes in abundance vs. abundance gradients. Methods Ecol Evol 4(6):552–557. CrossRefGoogle Scholar
  8. Baselga A, Orme CDL (2012) betapart: an R package for the study of beta diversity: betapart package. Methods Ecol Evol 3(5):808–812. CrossRefGoogle Scholar
  9. Bates D, Mächler M, Bolker B, Walker S (2014) Fitting linear mixed-effects models using lme4. arXiv:1406.5823
  10. Beniston M (2003) Climatic change in mountain regions: a review of possible impacts. In: Climate variability and change in high elevation regions: past, present and future. Advances in Global Change Research. Springer, Dordrecht, pp 5–31. Google Scholar
  11. Blumthaler M, Ambach W, Ellinger R (1997) Increase in solar UV radiation with altitude. J Photochem Photobiol 39(2):130–134. CrossRefGoogle Scholar
  12. Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White JSS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24(3):127–135. CrossRefPubMedPubMedCentralGoogle Scholar
  13. Bowman WD, Nemergut DR, McKnight DM, Miller MP, Williams MW (2015) A slide down a slippery slope—alpine ecosystem responses to nitrogen deposition. Plant Ecol Divers 8(5–6):727–738. CrossRefGoogle Scholar
  14. Brown PD, Wurtsbaugh WA, Nydick KR (2008) Lakes and forests as determinants of downstream nutrient concentrations in small mountain watersheds. Arct Antarct Alp Res 40(3):462–469.;2 Google Scholar
  15. Bueno de Mesquita CP, Tillmann LS, Bernard CD, Rosemond KC, Molotch NP, Suding KN (2018) Topographic heterogeneity explains patterns of vegetation response to climate change (1972–2008) across a mountain landscape, Niwot Ridge, Colorado. Arct Antarct Alp Res 50(1):1–16. CrossRefGoogle Scholar
  16. Buiteveld H (1995) A model for calculation of diffuse light attenuation (PAR) and Secchi depth. Aquat Ecol 29(1):55–65. CrossRefGoogle Scholar
  17. Caine NT (2002) Declining ice thickness on an alpine lake is generated by increased winter precipitation. Clim Chang 54(4):463–470. CrossRefGoogle Scholar
  18. Camarero L, Rogora M, Mosello R, Anderson NJ, Barbieri A, Botev I, Wright RF et al (2009) Regionalisation of chemical variability in European mountain lakes: regionalisation of mountain lakes chemistry. Freshwater Biol 54(12):2452–2469. CrossRefGoogle Scholar
  19. Camoying MG, Yñiguez AT (2016) FlowCAM optimization: attaining good quality images for higher taxonomic classification resolution of natural phytoplankton samples: FlowCAM optimization. Limnol Oceanogr Methods 14(5):305–314. CrossRefGoogle Scholar
  20. Catalan J, Barbieri MG, Bartumeus F, BitušíK P, Botev I, Brancelj A, Ventura M et al (2009) Ecological thresholds in European alpine lakes. Freshwater Biol 54(12):2494–2517. CrossRefGoogle Scholar
  21. Clow DW (2010) Changes in the timing of snowmelt and streamflow in Colorado: a response to recent warming. J Clim 23(9):2293–2306. CrossRefGoogle Scholar
  22. Cole JJ, Carpenter SR, Kitchell J, Pace ML, Solomon CT, Weidel B (2011) Strong evidence for terrestrial support of zooplankton in small lakes based on stable isotopes of carbon, nitrogen, and hydrogen. PNAS 108(5):1975–1980PubMedGoogle Scholar
  23. Cory RM, McKnight DM (2005) Fluorescence spectroscopy reveals ubiquitous presence of oxidized and reduced quinones in dissolved organic matter. Environ Sci Technol 39(21):8142–8149PubMedGoogle Scholar
  24. De Mendoza G, Catalan J (2010) Lake macroinvertebrates and the altitudinal environmental gradient in the Pyrenees. Hydrobiologia 648(1):51–72. CrossRefGoogle Scholar
  25. Dodds GS (1917) Altitudinal distribution of Entomostraca in Colorado. Proc U.S. Natl Museum 54(226):59–87Google Scholar
  26. Dodson SI (1974) Zooplankton competition and predation: an experimental test of the size-efficiency hypothesis. Ecology 55(3):605–613Google Scholar
  27. Dodson SI (1989) The ecological role of chemical stimuli for the zooplankton: predator-induced morphology in Daphnia. Oecologia 78(3):361–367PubMedGoogle Scholar
  28. Ebert D (2005) Ecology, epidemiology, and evolution of parasitism in Daphnia. National Library of Medicine, BaselGoogle Scholar
  29. Epstein DM, Neilson BT, Goodman KJ, Stevens DK, Wurtsbaugh WA (2013) A modeling approach for assessing the effect of multiple alpine lakes in sequence on nutrient transport. Aquat Sci 75(2):199–212. CrossRefGoogle Scholar
  30. Filker S, Sommaruga R, Vila I, Stoeck T (2016) Microbial eukaryote plankton communities of high-mountain lakes from three continents exhibit strong biogeographic patterns. Mol Ecol 25(10):2286–2301. CrossRefPubMedPubMedCentralGoogle Scholar
  31. Finlay BJ (2002) Global dispersal of free-living microbial eukaryote species. Science 296(5570):1061–1063. https://10.1126/science.1070710PubMedGoogle Scholar
  32. Fjellheim A, Raddum GG, Vandvik V, Lniceanu C, Boggero A, Brancelj A, Stuchlik E et al (2009) Diversity and distribution patterns of benthic invertebrates along alpine gradients. A study of remote European freshwater lakes. Adv Limnol 62:167–190Google Scholar
  33. Fleck JA, Gill G, Bergamaschi BA, Kraus TEC, Downing BD, Alpers CN (2014) Concurrent photolytic degradation of aqueous methylmercury and dissolved organic matter. Sci Total Environ 484:263–275. CrossRefPubMedGoogle Scholar
  34. Fox J, Weisberg S (2011) Multivariate linear models in R. An R companion to applied regression. Thousand Oaks, Los AngelesGoogle Scholar
  35. Füreder L, Ettinger R, Boggero A, Thaler B, Thies H (2006) Macroinvertebrate Diversity in Alpine Lakes: effects of altitude and catchment properties. Hydrobiologia 562(1):123–144. CrossRefGoogle Scholar
  36. Greenland D (1989) The climate of Niwot Ridge, Front Range, Colorado, U.S.A. Arct Antarct Alp Res 21(4):380. Google Scholar
  37. Hampton SE, Galloway AWE, Powers SM, Ozersky T, Woo KH, Batt RD, Xenopoulos MA et al (2017) Ecology under lake ice. Ecol Lett 20(1):98–111. CrossRefPubMedGoogle Scholar
  38. Haney JF et al (2013) An-image-based key to the zooplankton of North America. Version 5.0 released 2013. University of New Hampshire Center for Freshwater Biology <>Google Scholar
  39. Hansen AM, Kraus TEC, Pellerin BA, Fleck JA, Downing BD, Bergamaschi BA (2016) Optical properties of dissolved organic matter (DOM): effects of biological and photolytic degradation: DOM optical properties following degradation. Limnol Oceanogr 61(3):1015–1032. CrossRefGoogle Scholar
  40. Hansson LA, Hylander S, Sommaruga R (2007) Escape from UV threats in zooplankton: a cocktail of behavior and protective pigmentation. Ecology 88(8):1932–1939PubMedGoogle Scholar
  41. Havens KE, Pinto-Coelho RM, Beklioğlu M, Christoffersen KS, Jeppesen E, Lauridsen TL, Erdoğan Ş et al (2015) Temperature effects on body size of freshwater crustacean zooplankton from Greenland to the tropics. Hydrobiologia 743(1):27–35Google Scholar
  42. Helms JR, Stubbins A, Ritchie JD, Minor EC, Kieber DJ, Mopper K (2008) Absorption spectral slopes and slope ratios as indicators of molecular weight, source, and photobleaching of chromophoric dissolved organic matter. Limnol Oceanogr 53(3):955–969. CrossRefGoogle Scholar
  43. Hessen DO (1996) Competitive trade-off strategies in ArcticDaphnia linked to melanism and UV-B stress. Polar Biol 16(8):573–579Google Scholar
  44. Hessen DO (2002) Responses in pigmentation and anti-oxidant expression in Arctic Daphnia along gradients of DOC and UV exposure. J Plankton Res 24(10):1009–1018. CrossRefGoogle Scholar
  45. Hessen DO, Borgeraas J, Kessler K, Refseth UH (1999) UV-B susceptibility and photoprotection of Arctic Daphnia morphotypes. Polar Res 18(2):345–352. CrossRefGoogle Scholar
  46. Hill RA, Weber MH, Debbout RM, Leibowitz SG, Olsen AR (2018) The Lake-Catchment (LakeCat) Dataset: characterizing landscape features for lake basins within the conterminous USA. Freshw Sci 37(2):208–221. CrossRefPubMedPubMedCentralGoogle Scholar
  47. Hood EW, Williams MW, Caine N (2003a) Landscape controls on organic and inorganic nitrogen leaching across an alpine/subalpine ecotone, Green Lakes Valley, Colorado Front Range. Ecosystems 6(1):31–45Google Scholar
  48. Hood EW, McKnight DM, Williams MW (2003b) Sources and chemical character of dissolved organic carbon across an alpine/subalpine ecotone, Green Lakes Valley, Colorado Front Range, United States. Water Resour Res 39(7):1–12. CrossRefGoogle Scholar
  49. Humphries HC, Bourgeron PS, Mujica-Crapanzano LR (2008) Tree spatial patterns and environmental relationships in the forest–alpine tundra ecotone at Niwot Ridge, Colorado, USA. Ecol Res 23(3):589–605. CrossRefGoogle Scholar
  50. Jacobsen D, Dangles O (2017) Ecology of high altitude waters. Oxford University Press, New York, pp 1–15Google Scholar
  51. Kamenik C, Schmidt R, Kum G, Psenner R (2001) The influence of catchment characteristics on the water chemistry of Mountain Lakes. Arct Antarct Alp Res 33(4):404–409. CrossRefGoogle Scholar
  52. Kissman CE, Williamson CE, Rose KC, Saros JE (2017) Nutrients associated with terrestrial dissolved organic matter drive changes in zooplankton: phytoplankton biomass ratios in an alpine lake. Freshw Biol 62(1):40–51Google Scholar
  53. Kolesar SE, McKnight DM, Waters SB (2002) Late fall phytoplankton dynamics in three lakes, Rocky Mountain National Park. Hydrobiologia 472(1–3):249–263Google Scholar
  54. Kraemer BM, Anneville O, Chandra S, Dix M, Kuusisto E, Livingstone DM, McIntyre PB et al (2015) Morphometry and average temperature affect lake stratification responses to climate change: lake stratification responses to climate. Geophys Res Lett 42(12):4981–4988. CrossRefGoogle Scholar
  55. Kraemer BM, Chandra S, Dell AI, Dix M, Kuusisto E, Livingstone DM, McIntyre PB et al (2017) Global patterns in lake ecosystem responses to warming based on the temperature dependence of metabolism. Glob Chang Biol 23(5):1881–1890. CrossRefPubMedGoogle Scholar
  56. Kratz T, Webster K, Bowser C, Maguson J, Benson B (1997) The influence of landscape position on lakes in northern Wisconsin. Freshw Biol 37(1):209–217Google Scholar
  57. Kuhn M (2001) The nutrient cycle through snow and ice: a review. Aquat Sci 63(2):150–167. CrossRefGoogle Scholar
  58. Kuznetsova A, Brockhoff PB, Christensen RHB (2017) lmerTest package: tests in linear mixed effects models. J Stat Softw 82(13).
  59. Larson GL, Hoffman R, McIntire CD, Lienkaemper G, Samora B (2008) Zooplankton assemblages in montane lakes and ponds of Mount Rainier National Park, Washington State, USA. J Plankton Res 31(3):273–285. CrossRefGoogle Scholar
  60. Laurion I, Ventura M, Catalan J, Psenner R, Sommaruga R (2000) Attenuation of ultraviolet radiation in mountain lakes: factors controlling the among- and within-lake variability. Limnol Oceanogr 45(6):1274–1288. CrossRefGoogle Scholar
  61. Legendre P, Fortin MJ, Borcard D (2015) Should the mantel test be used in spatial analysis? Methods Ecol Evol 6(11):1239–1247. CrossRefGoogle Scholar
  62. Livingstone DM (1997) Break-up dates of Alpine Lakes as proxy data for local and regional mean surface air temperatures. Clim Change 37(2):407–439Google Scholar
  63. Loewen CJG, Vinebrooke RD (2016) Regional diversity reverses the negative impacts of an alien predator on local species-poor communities. Ecology 97(10):2740–2749. CrossRefPubMedGoogle Scholar
  64. Loewen CJG, Strecker AL, Larson GL, Vogel A, Fischer JM, Vinebrooke RD (2019) Macroecological drivers of zooplankton communities across the mountains of western North America. Ecography. CrossRefGoogle Scholar
  65. Lyons DA, Vinebrooke RD (2016) Linking zooplankton richness with energy input and insularity along altitudinal and latitudinal gradients: species richness in mountain lakes. Limnol Oceanogr 61(3):841–852. CrossRefGoogle Scholar
  66. Markager S, Vincent WF (2000) Spectral light attenuation and the absorption of UV and blue light in natural waters. Limnol Oceanogr 45(3):642–650. CrossRefGoogle Scholar
  67. Martin SL, Soranno PA (2006) Lake landscape position: relationships to hydrologic connectivity and landscape features. Limnol Oceanogr 51(2):801–814Google Scholar
  68. Martiny JBH, Bohannan BJM, Brown JH, Colwell RK, Fuhrman JA, Green JL, Staley JT et al (2006) Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol 4(2):102–112. CrossRefPubMedGoogle Scholar
  69. McCauley E (1984) The estimation of the abundance and biomass of zooplankton in samples. Manual Methods Assess Second Product Fresh Water 17:228–265Google Scholar
  70. McCutcheon SC, Martin JL, Barnwell TO (1993) Water quality. In: Maidment DR (ed) Handbood of hydrology. McGraw-Hill, New York, NY, p 113Google Scholar
  71. McGuire KJ, McDonnell JJ, Weiler M, Kendall C, McGlynn BL, Welker JM, Seibert J (2005) The role of topography on catchment-scale water residence time: catchment-scale water residence time. Water Resour Res 41(5):1–14. CrossRefGoogle Scholar
  72. McKnight DM, Andrews ED, Spaulding SA, Aiken GR (1994) Aquatic fulvic acids in algal-rich Antarctic ponds. Limnol Oceanogr 39(8):1972–1979Google Scholar
  73. McKnight DM, Harnish R, Wershaw RL, Baron JS, Schiff S (1997) Chemical characteristics of particulate, colloidal, and dissolved organic material in Loch Vale Watershed, Rocky Mountain National Park. Biogeochemistry 36(1):99–124. CrossRefGoogle Scholar
  74. McKnight DM, Boyer EW, Westerhoff PK, Doran PT, Kulbe T, Andersen DT (2001) Spectrofluorometric characterization of dissolved organic matter for indication of precursor organic material and aromaticity. Limnol Oceanogr 46(1):38–48Google Scholar
  75. McNaught AS, Schindler DW, Parker BR, Paul AJ, Anderson RS, Donald DB, Agbeti M (1999) Restoration of the food web of an alpine lake following fish stocking. Limnol Oceanogr 44(1):127–136. CrossRefGoogle Scholar
  76. Miller MP, McKnight DM (2015) Limnology of the Green Lakes Valley: phytoplankton ecology and dissolved organic matter biogeochemistry at a long-term ecological research site. Plant Ecol Divers 8(5–6):689–702. CrossRefGoogle Scholar
  77. Miller MP, McKnight DM, Chapra SC, Williams MW (2009) A model of degradation and production of three pools of dissolved organic matter in an alpine lake. Limnol Oceanogr 54(6):2213–2227. CrossRefGoogle Scholar
  78. Moeller RE, Gilroy S, Williamson CE, Grad G, Sommaruga R (2005) Dietary acquisition of photoprotective compounds (mycosporine-like amino acids, carotenoids) and acclimation to ultraviolet radiation in a freshwater copepod. Limnol Oceanogr 50(2):427–439. CrossRefGoogle Scholar
  79. Moser KA, Baron JS, Brahney J, Oleksy IA, Saros JE, Hundey EJ, Strecker AL et al (2019) Mountain lakes: eyes on global environmental change. Glob Planet Chang 178:77–95. CrossRefGoogle Scholar
  80. Nevalainen L, Luoto TP, Rantala MV, Galkin A, Rautio M (2015) Role of terrestrial carbon in aquatic UV exposure and photoprotective pigmentation of meiofauna in subarctic lakes. Freshw Biol 60(11):2435–2444Google Scholar
  81. Obertegger U, Flaim G, Braioni MG, Sommaruga R, Corradini F, Borsato A (2007) Water residence time as a driving force of zooplankton structure and succession. Aquat Sci 69(4):575–583Google Scholar
  82. Oikonomou A, Filker S, Breiner HW, Stoeck T (2015) Protistan diversity in a permanently stratified meromictic lake (Lake Alatsee, SW Germany). Environ Microbiol 17(6):2144–2157. CrossRefPubMedGoogle Scholar
  83. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’hara RB, Oksanen MJ et al (2013) Package ‘vegan’. Community ecology package, version, 2(9)Google Scholar
  84. Pinel-Alloul B, André A, Legendre P, Cardille JA, Patalas K, Salki A (2013) Large-scale geographic patterns of diversity and community structure of pelagic crustacean zooplankton in Canadian lakes: biodiversity patterns of crustacean zooplankton in Canada. Glob Ecol Biogeogr 22(7):784–795. CrossRefGoogle Scholar
  85. Poulton NJ, Martin JL (2010) Imaging flow cytometry for quantitative phytoplankton analysis-FlowCAM. Microscopic and molecular methods for quantitative phytoplankton analysis. In: KarlsonB, Cusack C, Bresnan E (eds), IOC manuals and guides (55):47–54Google Scholar
  86. Prescott GW (1964) How to know the freshwater algae. Wm C. Brown Company Publishers, Dubuque IowaGoogle Scholar
  87. Preston DL, Caine N, McKnight DM, Williams MW, Hell K, Miller MP, Johnson PTJ et al (2016) Climate regulates alpine lake ice cover phenology and aquatic ecosystem structure. Geophys Res Lett 43(10):5353–5360Google Scholar
  88. Read EK, Patil VP, Oliver SK, Hetherington AL, Brentrup JA, Zwart JA, Weathers KC et al (2015) The importance of lake-specific characteristics for water quality across the continental United States. Ecol Appl 25(4):943–955. CrossRefPubMedGoogle Scholar
  89. Reche I, Pulido-Villena E, Morales-Baquero R, Casamayor EO (2005) Does ecosystem size determine aquatic bacterial richness? Ecology 86(7):1715–1722Google Scholar
  90. Rhodes C, Bingham A, Heard AM, Hewitt J, Lynch J, Waite R, Bell MD (2017) Diatoms to human uses: linking nitrogen deposition, aquatic eutrophication, and ecosystem services. Ecosphere. Google Scholar
  91. Rofner C, Peter H, Catalán N, Drewes F, Sommaruga R, Pérez MT (2017) Climate-related changes of soil characteristics affect bacterial community composition and function of high altitude and latitude lakes. Glob Chang Biol 23(6):2331–2344. CrossRefPubMedGoogle Scholar
  92. Rose KC, Williamson CE, Saros JE, Sommaruga R, Fischer JM (2009) Differences in UV transparency and thermal structure between alpine and subalpine lakes: implications for organisms. Photochem Photobiol 8(9):1244–1256. CrossRefGoogle Scholar
  93. Rose KC, Williamson CE, Kissman CEH, Saros JE (2015) Does allochthony in lakes change across an elevation gradient? Ecology 96(12):3281–3291PubMedGoogle Scholar
  94. Sadro S, Melack JM (2012) The effect of an extreme rain event on the biogeochemistry and ecosystem metabolism of an oligotrophic high-elevation lake. Arct Antarct Alp Res 44(2):222–231. CrossRefGoogle Scholar
  95. Sadro S, Melack JM, MacIntyre S (2011) Depth-integrated estimates of ecosystem metabolism in a high-elevation lake (Emerald Lake, Sierra Nevada, California). Limnol Oceanogr 56(5):1764–1780. CrossRefGoogle Scholar
  96. Sadro S, Nelson CE, Melack JM (2012) The influence of landscape position and catchment characteristics on aquatic biogeochemistry in high-elevation lake-chains. Ecosystems 15(3):363–386. CrossRefGoogle Scholar
  97. Sadro S, Sickman JO, Melack JM, Skeen K (2018) Effects of climate variability on snowmelt and implications for organic matter in a high-elevation lake. Water Resour Res 54(7):4563–4578. CrossRefGoogle Scholar
  98. Sadro S, Melack JM, Sickman JO, Skeen K (2019) Climate warming response of mountain lakes affected by variations in snow. Limnol Oceanogr Lett 4(1):9–17. CrossRefGoogle Scholar
  99. Saros JE, Rose KC, Clow DW, Stephens VC, Nurse AB, Arnett HA, Wolfe AP et al (2010) Melting alpine glaciers enrich high-elevation lakes with reactive nitrogen. Environ Sci Technol 44(13):4891–4896. CrossRefPubMedGoogle Scholar
  100. Seastedt TR, Bowman WD, Caine TN, McKnight DM, Townsend A, Williams MW (2004) The landscape continuum: a model for high-elevation ecosystems. Bioscience 54(2):111–121Google Scholar
  101. Skála I (2015) Zooplankton community composition of high mountain lakes in the Tatra Mts., the Alps in North Tyrol, and Scotland: relationship to pH, depth, organic carbon, and chlorophyll-a concentration. Acta Mus Siles Sci Nat 64(2):175–189. Google Scholar
  102. Smith GM (1933) Fresh-water algae of the United States. McGraw-Hill, New YorkGoogle Scholar
  103. Sommaruga R (2001) The role of solar UV radiation in the ecology of alpine lakes. J Photochem Photobiol 62(1–2):35–42. CrossRefGoogle Scholar
  104. Soranno PA, Cheruvelil KS, Webster KE, Bremigan MT, Wagner T, Stow CA (2010) Using landscape limnology to classify freshwater ecosystems for multi-ecosystem management and conservation. Bioscience 60(6):440–454. CrossRefGoogle Scholar
  105. Soranno PA, Bacon LC, Beauchene M, Bednar KE, Bissell EG, Boudreau CK, Yuan S et al (2017) LAGOS-NE: a multi-scaled geospatial and temporal database of lake ecological context and water quality for thousands of US lakes. GigaScience. CrossRefPubMedPubMedCentralGoogle Scholar
  106. Spaulding SA, Jewson DH, Bixby RJ, Nelson H, McKnight DM (2012) Automated measurement of diatom size: automated measurement of diatom size. Limnol Oceanogr Methods 10(11):882–890. CrossRefGoogle Scholar
  107. Stoddard JL (1987) Microcrustacean communities of high-elevation lakes in the Sierra Nevada, California. J Plankton Res 9(4):631–650. CrossRefGoogle Scholar
  108. Stomp M, Huisman J, Mittelbach GG, Litchman E, Klausmeier CA (2011) Large-scale biodiversity patterns in freshwater phytoplankton. Ecology 92(11):2096–2107. CrossRefPubMedGoogle Scholar
  109. Vadeboncoeur Y, Vander Zanden MJ, Lodge DM (2002) Putting the Lake Back Together: Reintegrating Benthic Pathways into Lake Food Web Models: Lake ecologists tend to focus their research on pelagic energy pathways, but, from algae to fish, benthic organisms form an integral part of lake food webs. Bioscience 52(1):44-54.;2 Google Scholar
  110. Vannote RL, Minshall GW, Cummins KW, Sedell JR, Cushing CE (1980) The river continuum concept. Can J Fish Aquat Sci 37(1):130–137Google Scholar
  111. Ventura M, Camarero L, Buchaca T, Bartumeus F, Livingstone DM, Catalan J (2000) The main features of seasonal variability in the external forcing and dynamics of a deep mountain lake (Redó, Pyrenees). J Limnol 59(1):97–108. CrossRefGoogle Scholar
  112. Verpoorter C, Kutser T, Seekell DA, Tranvik LJ (2014) A global inventory of lakes based on high-resolution satellite imagery. Geophys Res Lett 41(18):6396–6402. CrossRefGoogle Scholar
  113. Vincent WF, Roy S (1993) Solar ultraviolet-B radiation and aquatic primary production: damage, protection, and recovery. Environ Rev 1(1):1–12. CrossRefGoogle Scholar
  114. Viviroli D, Dürr HH, Messerli B, Meybeck M, Weingartner R (2007) Mountains of the world, water towers for humanity: typology, mapping, and global significance. Water Resour Res 43(7):1–26. CrossRefGoogle Scholar
  115. Ward H, Marsh C, Birge E (1904) A biological reconnoissance of some elevated lakes in the sierras and the rockies, with reports on the copepoda and on the cladocera. Trans Am Microsc Soc 25:127–154. CrossRefGoogle Scholar
  116. Weglenska T (1976) A review of some problems in zooplankton production studies. Norwegian J, ZoolGoogle Scholar
  117. Weyhenmeyer GA, Meili M, Livingstone DM (2004) Nonlinear temperature response of lake ice breakup. Geophys Res Lett 31(7):1–4. CrossRefGoogle Scholar
  118. Williams MW, Davinroy T, Brooks PD (1997) Organic and inorganic nitrogen pools in talus fields and subtalus water, Green Lakes Valley, Colorado Front Range. Hydrol Process 11(13):1747–1760.;2-B CrossRefGoogle Scholar
  119. Williamson CE, Salm C, Cooke SL, Saros JE (2010) How do UV radiation, temperature, and zooplankton influence the dynamics of alpine phytoplankton communities? Hydrobiologia 648(1):73–81. CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Niwot Ridge Long Term Ecological Research Program, Institute of Arctic and Alpine ResearchUniversity of ColoradoBoulderUSA
  2. 2.Department of Civil, Environmental and Architectural Engineering, Environmental Studies, Hydrological Sciences, Institute of Arctic and Alpine ResearchUniversity of ColoradoBoulderUSA
  3. 3.Boulder Creek Critical Zone Observatory, Institute of Arctic and Alpine ResearchUniversity of ColoradoBoulderUSA
  4. 4.Department of Ecology and Evolutionary BiologyUniversity of ColoradoBoulderUSA

Personalised recommendations