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Resilience of pond communities to extreme thermal regime shifts: an alpine–montane reciprocal transplant experiment

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Abstract

Elevational gradients are ideal ecological venues for testing how communities respond to environmental changes associated with global warming. Recent warming rates have been shown to increase with elevation, hypothetically translating into heat waves that more adversely affect cold-adapted alpine communities than lower montane communities exposed to cold waves. We tested this hypothesis by conducting a replicated two-factor (source × elevation) experiment involving a reciprocal transplant of regional alpine and montane pond communities across two elevational sites (2345 m versus 1390 m asl). At each elevation, half of the mesocosms were inoculated with zooplankton and sedimentary egg-banks collected from alpine ponds while the other mesocosms were similarly seeded with zooplankton and sediment collected from montane ponds in 2016. After overwintering, the mesocosms were sampled for temperature and plankton during the ice-free periods of 2017 and 2018. The mesocosms at the low elevation were 8.0 ± 1.2 °C °C warmer than those at the high elevation. Elevation significantly affected total zooplankton biomass, whereas source effects were not significant. Elevation effects revealed that the temperature difference between sites affected the phenology of species within the assembled communities, but not their total biomass. Functional trait analysis revealed that the warmer environment selected for smaller body size and asexual reproduction as a warmer thermal regime stimulated several small parthenogenetic herbivores while suppressing larger, obligate sexual omnivores. Nevertheless, thermal regime shifts did not substantially affect the abundance-weighted mean functional identities of either transferred pond community, highlighting ponds as potential sources of functional insurance against increasingly extreme climate events.

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Data availability

The data that support the findings of this study are available from the corresponding author on request.

References

  • Adobe Systems Incorporated (2015) Adobe Illustrator CC. Version 19.2.0. Adobe, San Jose, California, USA. https://www.adobe.com/ca/

  • Altermatt F, Ebert D (2008) Genetic diversity of Daphnia magna populations enhances resistance to parasites. Ecol Lett 11:918–928

    PubMed  Google Scholar 

  • Batty M (2006) Rank clocks. Nature 444:592–596

    CAS  PubMed  Google Scholar 

  • Bohonak AJ, Jenkins DG (2003) Ecological and evolutionary significance of dispersal by freshwater invertebrates. Ecol Lett 6:783–796

    Google Scholar 

  • Brandl SJ, Emslie MJ, Ceccarelli DM (2016) Habitat degradation increases functional originality in highly diverse coral reef fish assemblages. Ecosphere 7:e01557

    Google Scholar 

  • Brendonck L, De Meester L (2003) Egg banks in freshwater zooplankton: evolutionary and ecological archives in the sediment. Hydrobiologia 491:65–84

    Google Scholar 

  • Brooks JL, Dodson SI (1965) Predation, body size, and composition of plankton. Science 150:28–35

    CAS  PubMed  Google Scholar 

  • Cardinale BJ, Duffy JE, Gonzalez A, Hooper DU, Perrings C, Venail P, Narwani A, Mace GM, Tilman D, Wardle DA, Kinzig AP, Daily GC, Loreau M, Grace JB, Larigauderie A, Srivastava DS, Naeem S (2012) Biodiversity loss and its impact on. Nature 489(326):326

    CAS  Google Scholar 

  • Carpenter SR, Cole JJ, Hodgson JR et al (2001) Trophic cascades, nutrients, and lake productivity: whole-lake experiments. Ecol Monogr 71:163–186. https://doi.org/10.2307/2657215

    Article  Google Scholar 

  • Cavalheri HB, Symons CC, Schulhof M, Jones NT, Shurin JB (2018) Rapid evolution of thermal plasticity in mountain lake Daphnia populations. Oikos 128:692–700

    Google Scholar 

  • Collins SL, Suding KN, Cleland EE, Batty M, Pennings SC, Gross KL, Grace JB, Gough L, Fargione JE, Clark CM (2008) Rank clocks and plant community dynamics. Ecology 89:3534–3541

    PubMed  Google Scholar 

  • Diffenbaugh NS, Singh D, Mankin JS, Horton DE, Swain DL, Touma D, Charland A, Liu Y, Haugen M, Tsiang M, Rajaratnam B (2017) Quantifying the influence of global warming on unprecedented extreme climate events. Proc Natl Acad Sci USA 114:4881–4886

    CAS  PubMed  Google Scholar 

  • Downing JA (2010) Emerging global role of small lakes and ponds: little things mean a lot. Limnetica 29:9–24

    Google Scholar 

  • Downing JA, Prairie YT, Cole JJ, Duarte CM, Tranvik LJ, Striegl RG, McDowell WH, Kortelainen P, Caraco NF, Melack JM, Middelburg JJ (2006) The global abundance and size distribution of lakes, ponds, and impoundments. Limnol Oceanogr 51:2388–2397

    Google Scholar 

  • Downing AL, Brown BL, Leibold MA (2014) Multiple diversity—stability mechanisms enhance population and community stability in aquatic food webs. Ecology 95:173–184

    PubMed  Google Scholar 

  • Dupuis AP, Hann BJ (2009) Climate change, diapause termination and zooplankton population dynamics: an experimental and modelling approach. Freshw Biol 54:221–235

    Google Scholar 

  • Edmondson WT (1959) Fresh-water biology, 2nd edn. Wiley, New York

    Google Scholar 

  • Frisch D, Green AJ, Figuerola J (2007) High dispersal capacity of a broad spectrum of aquatic invertebrates via waterbirds. Aquat Sci 69:568–574

    Google Scholar 

  • Graham MD, Vinebrooke RD (2009) Extreme weather events alter planktonic communities in boreal lakes. Limnol Oceanogr 54:2481–2492

    Google Scholar 

  • Gyllström M, Hansson L-A (2004) Dormancy in freshwater zooplankton: induction, termination and the importance of benthic-pelagic coupling. Aquat Sci 66:274–295

    Google Scholar 

  • Hallett LM, Jones SK, MacDonald AAM, Jones MB, Flynn DFB, Ripplinger J, Slaughter P, Gries C, Collins SL (2016) Codyn: an r package of community dynamics metrics. Methods Ecol Evol 7:1146–1151

    Google Scholar 

  • Hansson L-A, Nicolle A, Granéli W, Hallgren P, Kritzberg E, Persson A, Björk J, Nilsson A, Brönmark C (2013) Food-chain length alters community responses to global change in aquatic systems. Nat Clim Change 3:228–233

    Google Scholar 

  • Hébert MP, Beisner BE, Maranger R (2017) Linking zooplankton communities to ecosystem functioning: toward an effect-trait framework. J Plankton Res 39(3):12

    Google Scholar 

  • Hillebrand H, Blasius B, Borer ET, Chase JM, Downing JA, Eriksson BK, Filstrup CT, Harpole WS, Hodapp D, Larsen S, Lewandowska AM, Seabloom EW, Van de Waal DB, Ryabov AB (2018) Biodiversity change is uncoupled from species richness trends: consequences for conservation and monitoring. J Appl Ecol 55:169–184

    Google Scholar 

  • Holzapfel AM, Vinebrooke RD (2005) Environmental warming increases invasion potential of alpine lake communities by imported species. Glob Change Biol 11:2009–2015

    Google Scholar 

  • Hooper DU, Chapin FS III, Ewel JJ, Hector A, Inchausti P, Lavorel S, Hawton JH, Lodge DM, Loreau M, Naeem S, Schmid B, Setälä H, Symstad AJ, Vandermeer J, Wardle DA (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75:3–35

    Google Scholar 

  • IPCC (2014) Summary for policymakers. Page climate change 2014: synthesis report. Contribution of working groups I, II and III to the fifth assessment report of the intergovernmental panel on climate change.

  • Jaccard P (1912) The distribution of the flora in the alpine zone. New Phytol 11:37–50

    Google Scholar 

  • Kramer AM, Sarnelle O, Knapp RA (2008) Allee effect limits colonization success of sexually reproducing zooplankton. Ecology 89:2760–2769

    PubMed  Google Scholar 

  • Laliberté E, Legendre P, Shipley B (2015) Measuring functional diversity (FD) from multiple traits, and other tools for functional ecology, version, 1.0-12

  • Legendre P, Legendre L (1998) Numerical ecology, 2nd edn. Elsevier, Amsterdam

    Google Scholar 

  • Leibold MA, Holyoak M, Mouquet N, Amarasekare P, Chase JM, Hoopes MF, Holt RD, Shurin JB, Law R, Tilman D, Loreau M, Gonzalez A (2004) The metacommunity concept: a framework for multi-scale community ecology. Ecol Lett 7:601–613

    Google Scholar 

  • Loewen CJG, Strecker AL, Larson GL, Vogel A, Fischer JM, Vinebrooke RD (2018) Macroecological drivers of zooplankton communities across the mountains of western North America. Ecography 42:791–803

    Google Scholar 

  • Loewen CJG, Vinebrooke RD (2016) Regional diversity reverses the negative impacts of an alien predator on local species-poor communities. Ecology 97:2740–3274

    PubMed  Google Scholar 

  • Loreau M, Hector A (2001) Partitioning selection and complementarity in biodiversity experiments. Nature 412:72–76

    CAS  PubMed  Google Scholar 

  • Loreau M, de Mazancourt C (2013) Biodiversity and ecosystem stability: a synthesis of underlying mechanisms. Ecol Lett 16:106–115

    PubMed  Google Scholar 

  • Loreau M, Mouquet N, Gonzalez A (2003) Biodiversity as spatial insurance in heterogeneous landscapes. Proc Natl Acad Sci USA 100:12765–12770

    CAS  PubMed  Google Scholar 

  • Lyons DA, Vinebrooke RD (2016) Linking zooplankton richness with energy input and insularity along altitudinal and latitudinal gradients. Limnol Oceanogr 61:841–852

    Google Scholar 

  • MacLennan MM, Vinebrooke RD (2016) Effects of non-native trout, higher temperatures and regional biodiversity on zooplankton communities of alpine lakes. Hydrobiologia 770:193–208

    CAS  Google Scholar 

  • McGill BJ, Enquist BJ, Weiher E, Westoby M (2006) Rebuilding community ecology from functional traits. Trend Ecol Evol 21:178–185

    Google Scholar 

  • McMaster NL (2003) The effects of climate change and nitrogen deposition on the limnology of alpine ponds. Dissertation, University of Alberta

  • Mouillot D, Graham NAJ, Villéger S, Mason NWH, Bellwood DR (2013) A functional approach reveals community responses to disturbances. Trend Ecol Evol 28:167–177

    Google Scholar 

  • Nicolle A, Hallgren P, Von Einem J, Kritzberg ES, Graneli W, Persson A, Bronmark C, Hansson L-A (2012) Predicted warming and browning affect timing and magnitude of plankton phenological events in lakes: a mesocosm study. Freshw Biol 57:684–695

    Google Scholar 

  • Oliphant AJ, Spronken-Smith RA, Sturman AP, Owens IF (2003) Spatial variability of surface radiation fluxes in mountainous terrain. J Appl Meteorol Climatol 42:113–128

    Google Scholar 

  • Padisák J, Reynolds CS (2003) Shallow lakes: the absolute, the relative, the functional and the pragmatic. Hydrobiologia 506–509:1–11

    Google Scholar 

  • Parker BR, Wilhelm FM, Schindler DW (1996) Recovery of Hesperodiaptomus arcticus populations from diapausing eggs following elimination by stocked salmonids. Can J Zool 74:1292–1297

    Google Scholar 

  • Parker BR, Schindler DW, Donald DB, Anderson RS (2001) The effects of stocking and removal of a nonnative salmonid on the plankton of an alpine lake. Ecosystems 4:334–345

    Google Scholar 

  • Parker BR, Vinebrooke RD, Schindler DW (2008) Recent climate extremes alter alpine lake ecosystems. Proc Natl Acad Sci USA 105:12927–12931

    CAS  PubMed  Google Scholar 

  • Pepin N, Bradley RS, Diaz HF, Baraer M, Caceres ED, Forsythe N, Fowler H, Greenwood G, Hashmi MZ, Liu XD, Miller JR, Ning L, Ohmura A, Palazzi E, Rangwala I, Schöner W, Severskiy I, Shahgedanova M, Wang MB, Williamson SN, Yang D (2015) Elevation-dependent warming in mountain regions of the world. Nat Clim Change 5:424–430

    Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D, Heisterkamp S, Van Willigen B (2017) Package ‘nlme’. Linear and nonlinear mixed effects models, version, 3-1

  • Preston DL, Caine N, McKnight DM, Williams MW, Hell K, Miller MP, Hart SJ, Johnson PTJ (2016) Climate regulates alpine lake ice cover phenology and aquatic ecosystem structure. Geophys Res Lett 43:5353–5360

    Google Scholar 

  • R Core Development Team (2017) R: a language and environment for statistical computing. Version 3.4.3. R Foundation for Statistical Computing, Vienna, Austria. https://www.r-project.org

  • Redmond LE, Loewen CJG, Vinebrooke RD (2018) A functional approach to zooplankton communities in mountain lakes stocked with non-native sportfish under a changing climate. Water Resour Res 54:2362–2375

    Google Scholar 

  • Ripley B, Venables B, Bates DM, Hornik K, Gebhardt A, Firth D (2013) Package ‘mass’. Support functions and datasets for Venables and Ripley’s MASS, version, 7-3.

  • Rood SB, Foster SG, Hillman EJ, Luek A, Zanewich KP (2016) Flood moderation: declining peak flows along some Rocky Mountain rivers and the underlying mechanism. J Hydrol 536:174–182

    Google Scholar 

  • Roulin AC, Routtu J, Hall MD, Janicke T, Colson I, Haag CR, Ebert D (2013) Local adaptation of sex induction in a facultative sexual crustacean: insights from QTL mapping and natural populations of Daphnia magna. Mol Ecol 22:3567–3579

    CAS  PubMed  Google Scholar 

  • Roulin AC, Mariadassou M, Hall MD, Walser J-C, Haag C, Ebert D (2015) High genetic variation in resting-stage production in a metapopulation: is there evidence for local adaptation? Evolution 69:2747–2756

    PubMed  Google Scholar 

  • Scherrer D, Körner C (2010) Infra-red thermometry of alpine landscapes challenges climatic warming projections. Glob Change Biol 16:2602–2613

    Google Scholar 

  • Schindler DW (1998) Whole-ecosystem experiments: replication versus realism: the need for ecosystem-scale experiments. Ecosystems 1:323–334

    Google Scholar 

  • Shanafelt DW, Dieckmann U, Jonas M, Franklin O, Loreau M, Perrings C (2015) Biodiversity, productivity, and the spatial insurance hypothesis revisited. J Theor Biol 380:426–435

    PubMed  PubMed Central  Google Scholar 

  • Strecker AL, Cobb TP, Vinebrooke RD (2004) Effects of experimental greenhouse warming on phytoplankton and zooplankton communities in fishless alpine ponds. Limnol Oceanogr 49:1182–1190

    CAS  Google Scholar 

  • Symons C, Arnott S (2013) Regional zooplankton dispersal provides spatial insurance for ecosystem function. Glob Change Biol 19:1610–1619

    Google Scholar 

  • Thibaut LM, Connolly SR (2013) Understanding diversity–stability relationships: towards a unified model of portfolio effects. Ecol Lett 16:140–150

    PubMed  Google Scholar 

  • Thompson PL, Shurin JB (2012) Regional zooplankton biodiversity provides limited buffering of pond ecosystems against climate change. J Anim Ecol 81:251–259

    PubMed  Google Scholar 

  • Thompson PL, Beisner BE, Gonzalez A (2015) Warming induces synchrony and destabilizes experimental pond zooplankton metacommunities. Oikos 124:1171–1180

    Google Scholar 

  • Vanschoenwinkel B, Gielen S, Seaman M, Brendonck L (2008) Any way the wind blows—frequent wind dispersal drives species sorting in ephemeral aquatic communities. Oikos 117:125–134

    Google Scholar 

  • Viana DS, Santamaría L, Figuerola J (2016) Migratory birds as global dispersal vectors. Trend Ecol Evol 31:763–775

    Google Scholar 

  • Villéger S, Mason NW, Mouillot D (2008) New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology 89:2290–2301

    PubMed  Google Scholar 

  • Vinebrooke RD, Maclennan MM, Bartrons M, Zettel JP (2014) Missing effects of anthropogenic nutrient deposition on sentinel alpine ecosystems. Glob Change Biol 20:2173–2182

    Google Scholar 

  • Watkins J, Rudstam L, Holeck K (2011) Length–weight regressions for zooplankton biomass calculations—a review and a suggestion for standard equations. eCommons Cornell

  • Weidman PR, Schindler DW, Thompson PL, Vinebrooke RD (2014) Interactive effects of higher temperature and dissolved organic carbon on planktonic communities in fishless mountain lakes. Freshw Biol 59:889–904

    CAS  Google Scholar 

  • Wetzel RG, Likens GE (2013) Limnological analyses. Springer Science and Business Media, New York

    Google Scholar 

  • Wickham H, Chang W, Henry L, Pedersen TL, Takahashi K, Wilke C, Woo K (2018) Package ‘ggplot2’. Create elegant data visualizations using the grammar of graphics, version, 3.1.0

  • Williamson CE, Saros JE, Schindler DW (2009) Sentinels of change. Science 323:887–888

    CAS  PubMed  Google Scholar 

  • Winder M, Schindler DE (2004) Climate change uncouples trophic interactions in an aquatic ecosystem. Ecology 85:2100–2106

    Google Scholar 

  • Yachi S, Loreau M (1999) Biodiversity and ecosystem productivity in a fluctuating environment: the insurance hypothesis. Proc Natl Acad Sci 96:1463–1468

    CAS  PubMed  Google Scholar 

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Acknowledgements

Our study was supported by an Alberta Conservation Association (ACA) Grant in Biodiversity award to M.A. Johnsen, and a Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grant award to R.D. Vinebrooke. We thank the University of Calgary Biogeoscience Institute for the use of their facilities at the Barrier Lake Field Station. We would also like to thank Mark Taylor and his staff at Parks Canada for aiding in execution of the experiment. As well, we wish to thank Alex McClymont, Laura Redmond, Katie Keenan, Sarah Heemskerk, Lindsay Boucher, Charlotte Dawe, Thomas Brown, Caleb Sinn, and Mark Graham for their technical field and/or lab assistance.

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Correspondence to Mitchell A. Johnsen.

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Johnsen, M.A., Stuparyk, B.R., Cook, J. et al. Resilience of pond communities to extreme thermal regime shifts: an alpine–montane reciprocal transplant experiment. Aquat Sci 82, 38 (2020). https://doi.org/10.1007/s00027-020-0709-1

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