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Trophic dynamics of shrinking Subarctic lakes: naturally eutrophic waters impart resilience to rising nutrient and major ion concentrations

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Abstract

Shrinking lakes were recently observed for several Arctic and Subarctic regions due to increased evaporation and permafrost degradation. Along with lake drawdown, these processes often boost aquatic chemical concentrations, potentially impacting trophic dynamics. In particular, elevated chemical levels may impact primary productivity, which may in turn influence populations of primary and secondary consumers. We examined trophic dynamics of 18 shrinking lakes of the Yukon Flats, Alaska, that had experienced pronounced increases in nutrient (>200 % total nitrogen, >100 % total phosphorus) and ion concentrations (>100 % for four major ions combined) from 1985–1989 to 2010–2012, versus 37 stable lakes with relatively little chemical change over the same period. We found that phytoplankton stocks, as indexed by chlorophyll concentrations, remained unchanged in both shrinking and stable lakes from the 1980s to 2010s. Moving up the trophic ladder, we found significant changes in invertebrate abundance across decades, including decreased abundance of five of six groups examined. However, these decadal losses in invertebrate abundance were not limited to shrinking lakes, occurring in lakes with stable surface areas as well. At the top of the food web, we observed that probabilities of lake occupancy for ten waterbird species, including adults and chicks, remained unchanged from the period 1985–1989 to 2010–2012. Overall, our study lakes displayed a high degree of resilience to multi-trophic cascades caused by rising chemical concentrations. This resilience was likely due to their naturally high fertility, such that further nutrient inputs had little impact on waters already near peak production.

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References

  • Anderson L, Birks J, Rover J, Guldager N (2013) Controls on recent Alaskan lake changes identified from water isotopes and remote sensing. Geophys Res Lett 40:3413–3418

    Article  Google Scholar 

  • Bates D, M Maechler, B Bolker, S Walker (2014) lme4: linear mixed-effects models using Eigen and S4. R package version 1.1–7. http://CRAN.R-project.org/package=lme4. Accessed 5 May 2015

  • Burnham KP, Anderson DR (2002) Model selection and multi-model inference: a practical information-theoretic approach, 2nd edn. Springer, New York

    Google Scholar 

  • Carpenter SR (2003) Regime shifts in lake ecosystems: patterns and variation. International Ecological Institute, Lodendorf

    Google Scholar 

  • Carpenter S, Kitchell JF, Hodgson JR (1985) Cascading trophic interactions and lake productivity. BioScience 35:634–639

    Article  Google Scholar 

  • Carroll ML, Townshend JRG, DiMiceli CM, Loboda T, Sohlberg RA (2011) Shrinking lakes of the Arctic: spatial relationships and trajectory of change. Geophys Res Lett 38:L20406

    Google Scholar 

  • Corcoran RM, Lovvorn JR, Heglund PJ (2009) Long-term change in limnology and invertebrates in Alaskan boreal wetlands. Hydrobiologyogy 620:77–89

    Article  CAS  Google Scholar 

  • Dodson SI, Arnott SE, Cottingham KL (2000) The relationship in lake communities between primary productivity and species richness. Ecol 81:2662–2679

    Article  Google Scholar 

  • Ferrington LC Jr (2008) Global diversity of non-biting midges (Chironomidae; Insecta-Diptera) in freshwater. Hydrobiologyogy 595:447–455

    Article  Google Scholar 

  • Ford J, Bedford B (1987) The hydrology of Alaskan wetlands, USA: a review. Arct Alp Res 19:209–229

    Article  Google Scholar 

  • Fritz S (1996) Paleolimnological records of climate change in North America. Limnol Oceanogr 41:882–889

    Article  CAS  Google Scholar 

  • Gelman A, Hill J (2007) Data analysis using regression and multilevel/hierarchical models. Cambridge University Press, New York

    Google Scholar 

  • Greig HS, Kratina P, Thompson PL, Palen WJ, Richardson JS, Shurin JB (2012) Warming, eutrophication, and predator loss amplify subsidies between aquatic and terrestrial ecosystems. Glob Chang Biol 18:504–514

    Article  Google Scholar 

  • Gurney KE (2011) Reproductive ecology of temperate-nesting waterfowl: temporal and spatial patterns of investment and success in lesser scaup (Aythya affinis). PhD dissertation, Department of Biology, University of Saskatchewan, Saskatoon

  • Hanson MA, Butler MG (1994) Responses of plankton, turbidity, and macrophytes to biomanipulation in a shallow prairie lake. Can J Fish Aquat Sci 51:1180–1188

    Article  Google Scholar 

  • Haszard S, Clark RG (2007) Wetland use by white-winged Scoters (Melanitta fusca) in the Mackenzie Delta region. Wetl 27:855–863

    Article  Google Scholar 

  • Heglund PJ, Jones JR (2003) Limnology of shallow lakes in the Yukon Flats National Wildlife Refuge, interior Alaska. Lake Reserv Manage 19:133–140

    Article  CAS  Google Scholar 

  • Hershey AE (1992) Effects of experimental fertilization on the benthic macroinvertebrate community of an Arctic lake. J N Am Benthol Soc 11:204–217

    Article  Google Scholar 

  • Hobbie JE, Peterson BJ, Bettez N, Deegan L, O’Brien WJ, Kling GW, Kipphut GW, Bowden WB, Hershey AE (1999) Impact of global change on the biogeochemistry and ecology of an Arctic freshwater system. Polar Res 18:207–214

    Article  Google Scholar 

  • James KR, Cant B, Ryan T (2003) Responses of freshwater biota to rising salinity levels and implications for saline water management: a review. Aust J Bot 51:703–713

    Article  CAS  Google Scholar 

  • Jepsen SM, Voss CI, Walvoord MA, Minsley BJ, Rover J (2013a) Linkages between lake shrinkage/expansion and sublacustrine permafrost distribution determined from remote sensing of interior Alaska, USA. Geophys Res Lett 40:882–887

    Article  Google Scholar 

  • Jepsen SM, Voss CI, Walvoord MA, Rose JR, Minsley BJ, Smith BD (2013b) Sensitivity analysis of lake mass balance in discontinuous permafrost: the example of disappearing Twelvemile Lake, Yukon Flats, Alaska (USA). Hydrogeol J 21:185–200

    Article  Google Scholar 

  • Jorgenson MT, Racine CH, Walters JC, Osterkamp TE (2001) Permafrost degradation and ecological changes associated with a warming climate in central Alaska. Clim Change 48:551–579

    Article  CAS  Google Scholar 

  • Kéry M, Schaub M (2011) Bayesian population analysis using WinBUGS: a hierarchical perspective. Academic Press, Burlington

    Google Scholar 

  • Knowlton MF (1984) Flow-through microcuvette for flourometric determination of chlorophyll. Water Resour Bull 20:1198–1205

    Google Scholar 

  • Lewis TL, Lindberg MS, Schmutz JA, Heglund PJ, Rover J, Koch JC, Bertram MR (2015a) Pronounced chemical response of Subarctic lakes to climate-driven losses in surface area. Glob Chang Biol 21:1140–1152

    Article  PubMed  Google Scholar 

  • Lewis TL, Lindberg MS, Schmutz JA, Bertram MR, Dubour AJ (2015b) Species richness and distributions of boreal waterbird broods in relation to nesting and brood-rearing habitats. J Wildl Manage 79:296–310

    Article  Google Scholar 

  • Lougheed VL, Butler MG, McEwen DC, Hobbie JE (2011) Changes in tundra pond limnology: re-sampling Alaska ponds after 40 years. Ambio 40:589–599

    Article  PubMed  PubMed Central  Google Scholar 

  • Lunn DJ, Thomas A, Best N, Spiegelhalter D (2000) WinBUGS—a Bayesian modeling framework: concepts, structure, and extensibility. Stat Comput 10:325–337

    Article  Google Scholar 

  • MacKenzie DI, Nichols JD, Lachman GB, Droege S, Royle JA, Langtimm CA (2002) Estimating site occupancy rates when detection probabilities are less than one. Ecol 83:2248–2255

    Article  Google Scholar 

  • MacKenzie DJ, Nichols JD, Royle JA, Pollock KH, Baily LL, Hines JE (2006) Occupancy estimation and modeling. Academic Press, San Diego

    Google Scholar 

  • Magnuson JJ, Robertson DM, Benson BJ, Wynne RH, Livingstone DM, Arai T, Assel RA, Barry RG, Card V, Kuusisto E, Granin NG, Prowse TD, Stewart KM, Vuglinski VS (2000) Historical trends in lake and river ice cover in the Northern Hemisphere. Sci 289:1743–1746

    Article  CAS  Google Scholar 

  • Mordecai RS, Mattsson BJ, Tzilkowski CJ, Cooper RJ (2011) Addressing challenges when studying mobile or episodic species: hierarchical Bayes estimation of occupancy and use. J Appl Ecol 48:56–66

    Article  Google Scholar 

  • New M, Liverman D, Schroder H, Anderson K (2011) Four degrees and beyond: the potential for a global temperature increase of four degrees and its implications. Philos Trans R Soc A 369:6–19

    Article  Google Scholar 

  • O’Brien WJ, Barfield M, Bettez N, Hershey AE, Hobbie JE, Kipphut G, Kling G, Miller MC (2005) Long-term response and recovery to nutrient addition of a partitioned arctic lake. Freshwater Biol 50:731–741

    Article  Google Scholar 

  • Ogbebo FE, Evans MS, Waiser MJ, Tumber VP, Keating JJ (2009) Nutrient limitation of phytoplankton growth in Arctic lakes of the lower Mackenzie River Basin, northern Canada. Can J Fish Aquat Sci 66:247–260

    Article  CAS  Google Scholar 

  • Pastick NJ, Jorgenson MT, Wylie BK, Minsley BJ, Ji L, Walvoord MA, Smith BD, Abraham JD, Rose JR (2013) Extending airborne electromagnetic surveys for regional active layer and permafrost mapping with remote sensing and ancillary data, Yukon Flats ecoregion, central Alaska. Permafr Periglac Process 24:184–199

    Article  Google Scholar 

  • Peterson BJ, Deegan L, Helfrich J, Hobbie JE, Hullar M, Moller B, Ford TE, Hershey A, Hiltner A, Kipphut G, Lock MA, Fiebig DM, McKinley V, Miller MC, Robie Vestal J, Ventullo R, Volk G (1993) Biological responses of a tundra river to fertilization. Ecol 74:653–672

    Article  CAS  Google Scholar 

  • Petrone KC, Jones JB, Hinzman LD, Boone RD (2006) Seasonal export of carbon, nitrogen, and major solutes from Alaskan catchments with discontinuous permafrost. J Geophys Res 111:G02020

    Google Scholar 

  • Pinder AM, Halse SA, McRae JM, Shiel RJ (2005) Occurrence of aquatic invertebrates of the wheatbelt region of Western Australia in relation to salinity. Hydrobiology 543:1–24

    Article  Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D (2013) nlme: linear and nonlinear mixed effects models. R package version 3.1-108. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Quinlan R, Douglas MSV, Smol JP (2005) Food web changes in arctic ecosystems related to climate warming. Glob Chang Biol 11:1381–1386

    Article  Google Scholar 

  • Rautio M, Dufresne F, Laurion I, Bonilla S, Vincent WF, Christoffersen KS (2011) Shallow freshwater ecosystems of the circumpolar Arctic. Ecoscience 18:204–222

    Article  Google Scholar 

  • Riordan B, Verbyla D, McGuire AD (2006) Shrinking ponds in subarctic Alaska based on 1950–2002 remotely sensed images. J Geophys Res 111:G04002

    Article  Google Scholar 

  • Roach J, Griffith B, Verbyla D, Jones J (2011) Mechanisms influencing changes in lake area in Alaskan boreal forest. Glob Chang Biol 17:2567–2583

    Article  Google Scholar 

  • Rover J, Ji L, Wylie BK, Tieszen LL (2012) Establishing water body areal extent trends in interior Alaska from multi-temporal Landsat data. Remote Sens Lett 3:595–604

    Article  Google Scholar 

  • Saether OA (1979) Chironomid communities as water quality indicators. Holarct Ecol 2:65–74

    Google Scholar 

  • Schindler DW (1978) Factors regulating phytoplankton production and standing crop in the world’s freshwaters. Limnol Oceanogr 23:478–486

    Article  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 105:11254–11258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Slavik K, Peterson BJ, Deegan LA, Bowden WB, Hershey AE, Hobbie JE (2004) Long-term responses of the Kuparuk River ecosystem to phosphorus fertilization. Ecology 85:939–954

    Article  Google Scholar 

  • Smith LC, Sheng Y, MacDonald GM, Hinzman LD (2005) Disappearing arctic lakes. Science 308:1429

    Article  CAS  PubMed  Google Scholar 

  • Smol JP, Douglas MSV (2007a) Crossing the final ecological threshold in high Arctic ponds. Proc Natl Acad Sci 104:12395–12397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smol JP, Douglas MSV (2007b) From controversy to consensus: making the case for recent climate change in the Arctic using lake sediments. Front Ecol Environ 5:466–474

    Article  Google Scholar 

  • Sprague JB (1963) Resistance of four freshwater crustaceans to lethal high temperature and low oxygen. J Fish Res Board Can 20:387–415

    Article  Google Scholar 

  • Sturtz S, Ligges U, Gelman A (2005) R2WinBUGS: a package for running WinBUGS from R. J Stat Softw 12:1–16

    Article  Google Scholar 

  • Surdu CM, Duguay CR, Brown LC, Fernandez Prieto D (2014) Response of ice cover on shallow lakes of the North Slope of Alaska to contemporary climate conditions (1950–2011): radar remote-sensing and numerical modeling data analysis. Cryosphere 8:167–180

    Article  Google Scholar 

  • Verpoorter C, Kuster T, Seekell SA, Tranvik LJ (2014) A global inventory of lakes based on high-resolution satellite imagery. Geophys Res Lett 41:6396–6402

    Article  Google Scholar 

  • Walker J, Rotella JJ, Schmidt JH, Loesch CR, Reynolds RE, Lindberg MS, Ringelman JK, Stephens SE (2013) Distribution of duck broods relative to habitat characteristics in the Prairie Pothole region. J Wildl Manage 77:392–404

    Article  Google Scholar 

  • Wrona FJ, Prowse TD, Reist JD, Hobbie JE, Levesque LMJ, Vincent WF (2006) Climate change effects on aquatic biota, ecosystem structure and function. Ambio 33:359–369

    Article  Google Scholar 

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Acknowledgments

Funding was provided by the US Geological Survey (Alaska Science Center), US Fish and Wildlife Service (Yukon Flats National Wildlife Refuge), and US National Park Service. I. Isler, A. Simnor, C. Michaud, J. Rose, L. Payne, C. Parrish, M. Pfander, L. Marks, and C. Mandeville provided field assistance. J. R. Jones and D. Obrecht analyzed water samples at the University of Missouri—Columbia. Use of trade, product, or firm names in this publication is for descriptive purposes only and does not imply endorsement by the US Government.

Author contribution statement

T. L. L., P. J. H., and A. J. D. collected the data. T. L. L. analyzed the data and wrote the manuscript. P. J. H., M. S. L., J. A. S., and M. R. B. conceived and designed the research. J. H. S. developed mathematical models. A. J. D. processed the invertebrate samples. J. R. developed remote-sensing models.

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Authors and Affiliations

  1. Department of Biology and Wildlife and Institute of Arctic Biology, University of Alaska Fairbanks, Fairbanks, AK, 99775, USA

    Tyler L. Lewis, Mark S. Lindberg & Adam J. Dubour

  2. US Fish and Wildlife Service, 2630 Fanta Reed Road, La Crosse, WI, 54603, USA

    Patricia J. Heglund

  3. US Geological Survey, Alaska Science Center, 4210 University Drive, Anchorage, AK, 99508, USA

    Tyler L. Lewis & Joel A. Schmutz

  4. US National Park Service, Central Alaska Network, 4175 Geist Road, Fairbanks, AK, 99709, USA

    Joshua H. Schmidt

  5. US Geological Survey, Earth Resources Observation and Science (EROS) Center, 47914 252nd Street, Sioux Falls, SD, 57198, USA

    Jennifer Rover

  6. US Fish and Wildlife Service, Yukon Flats National Wildlife Refuge, 101 12th Avenue, Room 264, Fairbanks, AK, 99701, USA

    Mark R. Bertram

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  1. Tyler L. Lewis
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  2. Patricia J. Heglund
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Correspondence to Tyler L. Lewis.

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Communicated by Ulrich Sommer.

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Lewis, T.L., Heglund, P.J., Lindberg, M.S. et al. Trophic dynamics of shrinking Subarctic lakes: naturally eutrophic waters impart resilience to rising nutrient and major ion concentrations. Oecologia 181, 583–596 (2016). https://doi.org/10.1007/s00442-016-3572-y

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