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Effects of natural and experimental drought on soil fungi and biogeochemistry in an Amazon rain forest

  • 1.

    Lovejoy, T. E. & Nobre, C. Amazon tipping point. Sci. Adv. 4, eaat2340 (2018).

    Article  Google Scholar 

  • 2.

    Chadwick, R., Good, P., Martin, G. & Rowell, D. P. Large rainfall changes consistently projected over substantial areas of tropical land. Nat. Clim. Change 6, 177 (2015).

    Article  Google Scholar 

  • 3.

    Neelin, J. D., Münnich, M., Su, H., Meyerson, J. E. & Holloway, C. E. Tropical drying trends in global warming models and observations. Proc. Natl Acad. Sci. USA 103, 6110–6115 (2006).

    CAS  Article  Google Scholar 

  • 4.

    Barkhordarian, A., Saatchi, S. S., Behrangi, A., Loikith, P. C. & Mechoso, C. R. A recent systematic increase in vapor pressure deficit over tropical South America. Sci. Rep. 9, 15331 (2019).

    Article  CAS  Google Scholar 

  • 5.

    Cox, P. M. et al. Amazonian forest dieback under climate-carbon cycle projections for the 21st century. Theor. Appl. Climatol. 78, 137–156 (2004).

    Article  Google Scholar 

  • 6.

    Salazar, L. F., Nobre, C. A. & Oyama, M. D. Climate change consequences on the biome distribution in tropical South America. Geophys. Res. Lett. 34, L09708 (2007).

    Article  Google Scholar 

  • 7.

    Boisier, J. P., Ciais, P., Ducharne, A. & Guimberteau, M. Projected strengthening of Amazonian dry season by constrained climate model simulations. Nat. Clim. Change 5, 656 (2015).

    Article  Google Scholar 

  • 8.

    Amundson, R. & Jenny, H. On a state factor model of ecosystems. BioScience 47, 536–543 (1997).

    Article  Google Scholar 

  • 9.

    Schlesinger, W. H. et al. Forest biogeochemistry in response to drought. Glob. Change Biol. 22, 2318–2328 (2016).

    Article  Google Scholar 

  • 10.

    Bennett, E. M., Peterson, G. D. & Levitt, E. A. Looking to the future of ecosystem services. Ecosystems 8, 125–132 (2005).

    Article  Google Scholar 

  • 11.

    Phillips, O. L. et al. Drought sensitivity of the Amazon rain forest. Science 323, 1344–1347 (2009).

    CAS  Article  Google Scholar 

  • 12.

    Esquivel-Muelbert, A. et al. Compositional response of Amazon forests to climate change. Glob. Change Biol. 25, 39–56 (2019).

    Article  Google Scholar 

  • 13.

    Cox, P. M. et al. Sensitivity of tropical carbon to climate change constrained by carbon dioxide variability. Nature 494, 341 (2013).

    CAS  Article  Google Scholar 

  • 14.

    Eller, C. B. et al. Modelling tropical forest responses to drought and El Niño with a stomatal optimization model based on xylem hydraulics. Philos. Trans. R. Soc. B Biol. Sci. 373, 20170315 (2018).

    Article  CAS  Google Scholar 

  • 15.

    Meir, P. et al. Threshold responses to soil moisture deficit by trees and soil in tropical rain forests: insights from field experiments. Bioscience 65, 882–892 (2015).

    Article  Google Scholar 

  • 16.

    Davidson, E. A., Nepstad, D. C., Ishida, F. Y. & Brando, P. M. Effects of an experimental drought and recovery on soil emissions of carbon dioxide, methane, nitrous oxide, and nitric oxide in a moist tropical forest. Glob. Change Biol. 14, 2582–2590 (2008).

    Article  Google Scholar 

  • 17.

    da Costa, A. C. L. et al. Ecosystem respiration and net primary productivity after 8–10 years of experimental through-fall reduction in an eastern Amazon forest. Plant Ecol. Diversity 7, 7–24 (2014).

    Article  Google Scholar 

  • 18.

    Doughty, C. E. et al. Drought impact on forest carbon dynamics and fluxes in Amazonia. Nature 519, 78 (2015).

    CAS  Article  Google Scholar 

  • 19.

    Fisher, R. A., Williams, M., Do Vale, R. L., Da Costa, A. L. & Meir, P. Evidence from Amazonian forests is consistent with isohydric control of leaf water potential. Plant Cell Environ. 29, 151–165 (2006).

    Article  Google Scholar 

  • 20.

    Rowland, L. et al. Death from drought in tropical forests is triggered by hydraulics not carbon starvation. Nature 528, 119–122 (2015).

    CAS  Article  Google Scholar 

  • 21.

    Nepstad, D. C., Tohver, I. M., Ray, D., Moutinho, P. & Cardinot, G. Mortality of large trees and lianas following experimental drought in a Amazon forest. Ecology 88, 2259–2269 (2007).

    Article  Google Scholar 

  • 22.

    da Costa, A. C. L. et al. Effect of 7 yr of experimental drought on vegetation dynamics and biomass storage of an eastern Amazonian rain forest. N. Phytol. 187, 579–591 (2010).

    Article  Google Scholar 

  • 23.

    Rowland, L. et al. Shock and stabilisation following long-term drought in tropical forest from 15 years of litterfall dynamics. J. Ecol. 106, 1673–1682 (2018).

    Article  Google Scholar 

  • 24.

    Sotta, E. D. et al. Effects of an induced drought on soil carbon dioxide (CO2) efflux and soil CO2 production in an Eastern Amazonian rain forest, Brazil. Glob. Change Biol. 13, 2218–2229 (2007).

    Article  Google Scholar 

  • 25.

    Bardgett, R. D. & van der Putten, W. H. Belowground biodiversity and ecosystem functioning. Nature 515, 505–511 (2014).

    CAS  Article  Google Scholar 

  • 26.

    Koyama, A., Steinweg, J. M., Haddix, M. L., Dukes, J. S. & Wallenstein, M. D. Soil bacterial community responses to altered precipitation and temperature regimes in an old field grassland are mediated by plants. FEMS Microbiol. Ecol. https://doi.org/10.1093/femsec/fix156 (2017).

  • 27.

    Kivlin, S. N. & Hawkes, C. V. Tree species, spatial heterogeneity, and seasonality drive soil fungal abundance, richness, and composition in Neotropical rain forests. Environ. Microbiol. 18, 4662–4673 (2016).

    Article  Google Scholar 

  • 28.

    Sinsabaugh, R. L. & Moorhead, D. L. Resource allocation to extracellular enzyme production: a model for nitrogen and phosphorus control of litter decomposition. Soil Biol. Biochem. 26, 1305–1311 (1994).

    Article  Google Scholar 

  • 29.

    Turner, B. L. & Romero, T. E. Stability of hydrolytic enzyme activity and microbial phosphorus during storage of tropical rain forest soils. Soil Biol. Biochem. 42, 459–465 (2010).

    CAS  Article  Google Scholar 

  • 30.

    Sinsabaugh, R. L. et al. Stoichiometry of soil enzyme activity at global scale. Ecol. Lett. 11, 1252–1264 (2008).

    Article  Google Scholar 

  • 31.

    Waring, B. G., Weintraub, S. R. & Sinsabaugh, R. L. Ecoenzymatic stoichiometry of microbial nutrient acquisition in tropical soils. Biogeochemistry 117, 101–113 (2014).

    CAS  Article  Google Scholar 

  • 32.

    Turner, B. L. & Joseph Wright, S. The response of microbial biomass and hydrolytic enzymes to a decade of nitrogen, phosphorus, and potassium addition in a lowland tropical rain forest. Biogeochemistry 117, 115–130 (2014).

    CAS  Article  Google Scholar 

  • 33.

    Weintraub, S. R., Wieder, W. R., Cleveland, C. C. & Townsend, A. R. Organic matter inputs shift soil enzyme activity and allocation patterns in a wet tropical forest. Biogeochemistry 114, 313–326 (2013).

    CAS  Article  Google Scholar 

  • 34.

    Firestone, M. K. & Davidson, E. A. in Exchange of Trace Gases between Terrestrial Ecosystems and The Atmosphere (eds. M. O. Andreae & D. S. Schimel) 7–21 (John Wiley and Sons, 1989).

  • 35.

    Meir, P. et al. Short-term effects of drought on tropical forest do not fully predict impacts of repeated or long-term drought: gas exchange versus growth. Philos. Trans. R. Soc. B Biol. Sci. 373, 20170311 (2018).

    Article  Google Scholar 

  • 36.

    Robertson, G. P. in Mineral Nutrients in Troical Forest and Savanna Ecosystems (ed. J. Proctor) 55–69 (Blackwell Scientific, 1989).

  • 37.

    Silver, W. L., Lugo, A. E. & Keller, M. Soil oxygen availability and biogeochemistry along rainfall and topographic gradients in upland wet tropical forest soils. Biogeochemistry 44, 301–328 (1999).

    Google Scholar 

  • 38.

    Pett-Ridge, J. & Firestone, M. K. Redox fluctuation structures microbial communities in a wet tropical soil. Appl. Environ. Microbiol. 71, 6998–7007 (2005).

    CAS  Article  Google Scholar 

  • 39.

    Cleveland, C. C., Reed, S. C. & Townsend, A. R. Nutrient regulation of organic matter decomposition in a tropical rain forest. Ecology 87, 492–503 (2006).

    Article  Google Scholar 

  • 40.

    Cleveland, C. C., Wieder, W. R., Reed, S. C. & Townsend, A. R. Experimental drought in a tropical rain forest increases soil carbon dioxide losses to the atmosphere. Ecology 91, 2313–2323 (2010).

    Article  Google Scholar 

  • 41.

    Wallenstein, M. D. & Hall, E. K. A trait-based framework for predicting when and where microbial adaptation to climate change will affect ecosystem functioning. Biogeochemistry 109, 35–47 (2012).

    Article  Google Scholar 

  • 42.

    Knapp, A. K. et al. Consequences of more extreme precipitation regimes for terrestrial ecosystems. BioScience 58, 811–821 (2008).

    Article  Google Scholar 

  • 43.

    Greenland, D., Goodin, D. G. & Smith, R. C. Climate Variability and Ecosystem Response at Long-Term Ecological Research Sites. (Oxford University Press, 2003).

  • 44.

    Kayler, Z. E. et al. Experiments to confront the environmental extremes of climate change. Science 13, 219–225 (2015).

    Google Scholar 

  • 45.

    McGuire, K. L., Fierer, N., Bateman, C., Treseder, K. K. & Turner, B. L. Fungal community composition in neotropical rain forests: the influence of tree diversity and precipitation. Microb. Ecol. 63, 804–812 (2012).

    Article  Google Scholar 

  • 46.

    Buscardo, E. et al. Spatio-temporal dynamics of soil bacterial communities as a function of Amazon forest phenology. Sci. Rep. 8, 4382 (2018).

    Article  CAS  Google Scholar 

  • 47.

    Quesada, C. A. et al. Variations in chemical and physical properties of Amazon forest soils in relation to their genesis. Biogeosciences 7, 1515–1541 (2010).

    CAS  Article  Google Scholar 

  • 48.

    Bonfim, J. A., Vasconcellos, R. L. F., Baldesin, L. F., Sieber, T. N. & Cardoso, E. Dark septate endophytic fungi of native plants along an altitudinal gradient in the Brazilian Atlantic forest. Fung. Ecol. 20, 202–210 (2016).

    Article  Google Scholar 

  • 49.

    Carson, J. K. et al. Low pore connectivity increases bacterial diversity in soil. Appl. Environ. Microbiol. 76, 3936–3942 (2010).

    CAS  Article  Google Scholar 

  • 50.

    Schimel, J. & Schaeffer, S. Microbial control over carbon cycling in soil. Front. Microbiol. 3, 1–11 (2012).

    Article  CAS  Google Scholar 

  • 51.

    Daws, S. C. et al. Do shared traits create the same fates? Examining the link between morphological type and the biogeography of fungal and bacterial communities. Fung. Ecol. 46, 100948 (2020).

    Article  Google Scholar 

  • 52.

    DeAngelis, K. M., Silver, W. L., Thompson, A. W. & Firestone, M. K. Microbial communities acclimate to recurring changes in soil redox potential status. Environ. Microbiol. 12, 3137–3149 (2010).

    CAS  Article  Google Scholar 

  • 53.

    Bradford, M. A. et al. Thermal adaptation of soil microbial respiration to elevated temperature. Ecol. Lett. 11, 1316–1327 (2008).

    Article  Google Scholar 

  • 54.

    Coleman, D. C., Callaham, M. A. Jr. & Crossley, D. A. Jr. Fundamentals of Soil Ecology 3rd edn. (Academic Press, 2018).

  • 55.

    de Meester, L. in Biogeography of Microscopic Organisms: Is Everything Small Everywhere? (ed. D. Fontaneto) 324–334 (Cambridge University Press, 2011).

  • 56.

    Leibold, M. A. et al. The metacommunity concept: a framework for multi-scale community ecology. Ecology Letters 7, 601–613 (2004).

    Article  Google Scholar 

  • 57.

    Barberán, A. et al. Continental-scale distributions of dust-associated bacteria and fungi. Proc. Natl Acad. Sci. USA 112, 5756–5761 (2015).

    Article  CAS  Google Scholar 

  • 58.

    Cáliz, J., Triadó-Margarit, X., Camarero, L. & Casamayor, E. O. A long-term survey unveils strong seasonal patterns in the airborne microbiome coupled to general and regional atmospheric circulations. Proc. Natl Acad. Sci. USA 115, 12229–12234 (2018).

    Article  CAS  Google Scholar 

  • 59.

    Prospero, J. M., Glaccum, R. A. & Nees, R. T. Atmospheric transport of soil dust from Africa to South America. Nature 289, 570–572 (1981).

    CAS  Article  Google Scholar 

  • 60.

    Rime, T., Hartmann, M. & Frey, B. Potential sources of microbial colonizers in an initial soil ecosystem after retreat of an alpine glacier. ISME J. 10, 1625 (2016).

    CAS  Article  Google Scholar 

  • 61.

    Elena, S. F. & Lenski, R. E. Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nat. Rev. Genet. 4, 457–469 (2003).

    CAS  Article  Google Scholar 

  • 62.

    terHorst, C. P., Lennon, J. T. & Lau, J. A. The relative importance of rapid evolution for plant-microbe interactions depends on ecological context. Proc. R. Soc. B Biol. Sci. 281, 20140028 (2014).

    Article  Google Scholar 

  • 63.

    Read, D. J. & Haselwandter, K. Observations on the mycorrhizal status of some alpine plant communities. N. Phytol. 88, 341–352 (1981).

    Article  Google Scholar 

  • 64.

    Bell, A. A. & Wheeler, M. H. Biosynthesis and functions of fungal melanins. Ann. Rev. Phytopathol. 24, 411–451 (1986).

    CAS  Article  Google Scholar 

  • 65.

    Mandyam, K. & Jumpponen, A. Seeking the elusive function of the root-colonising dark septate endophytic fungi. Studies Mycol. 53, 173–189 (2005).

    Article  Google Scholar 

  • 66.

    da Costa, A. C. L. et al. Stand dynamics modulate water cycling and mortality risk in droughted tropical forest. Glob. Change Biol. 24, 249–258 (2018).

    Article  Google Scholar 

  • 67.

    Jumpponen, A. & Trappe, J. M. Dark septate endophytes: a review of facultative biotrophic root-colonizing fungi. N. Phytol. 140, 295–310 (1998).

    Article  Google Scholar 

  • 68.

    Fisher, R. A. et al. The response of an Eastern Amazonian rain forest to drought stress: results and modelling analyses from a throughfall exclusion experiment. Glob. Change Biol. 13, 2361–2378 (2007).

    Article  Google Scholar 

  • 69.

    Newsham, K. K. A meta-analysis of plant responses to dark septate root endophytes. N. Phytol. 190, 783–793 (2011).

    CAS  Article  Google Scholar 

  • 70.

    Smith, S. E. & Read, D. J. Mycorrhizal symbiosis. 3rd edn. (Academic Press, 2008).

  • 71.

    IPCC. Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. (Cambridge University Press, 2013).

  • 72.

    Janzen, D. H. Herbivores and the number of tree species in tropical forests. Am. Natural. 104, 501–528 (1970).

    Article  Google Scholar 

  • 73.

    Connell, J. H. in Dynamics of Populations (eds. P. J. den Boer & G. R. Gradwell) 298–312 (Centre for Agricultural Publishing and Documentation, 1971).

  • 74.

    Comita, L. S. et al. Testing predictions of the Janzen–Connell hypothesis: a meta-analysis of experimental evidence for distance- and density-dependent seed and seedling survival. J. Ecol. 102, 845–856 (2014).

    Article  Google Scholar 

  • 75.

    Buscardo, E. et al. in Interactions between Biosphere, Atmosphere and Human Land Use in The Amazon Basin (eds. Laszlo Nagy, Bruce R. Forsberg, & Paulo Artaxo) 225–266 (Springer Berlin Heidelberg, 2016).

  • 76.

    Singh, J. S., Raghubanshi, A. S., Singh, R. S. & Srivastava, S. C. Microbial biomass acts as a source of plant nutrients in dry tropical forest and savanna. Nature 338, 499 (1989).

    Article  Google Scholar 

  • 77.

    Luizão, F., Luizão, R. & Chauvel, A. Premiers résultats sur la dynamique des biomasses racinaires et microbiennes dans un latosol d’Amazonie centrale (Brésil) sous forêt et sous pâturage. Cahiers ORSTOM. Série Pédologie 27, 69–79 (1992).

    Google Scholar 

  • 78.

    Vasconcelos, H. L. & Luizão, F. J. Litter production and litter nutrient concentrations in a fragmented Amazonian landscape. Ecol. Appl. 14, 884–892 (2004).

    Article  Google Scholar 

  • 79.

    Cornejo, F. H., Varela, A. & Wright, S. J. Tropical forest litter decomposition under seasonal drought: nutrient release, fungi and bacteria. Oikos 70, 183–190 (1994).

    Article  Google Scholar 

  • 80.

    Garcia-Montiel, D. C. et al. Controls on soil nitrogen oxide emissions from forest and pastures in the Brazilian Amazon. Glob. Biogeochem. Cycles 15, 1021–1030 (2001).

    CAS  Article  Google Scholar 

  • 81.

    Malhi, Y. et al. The productivity, metabolism and carbon cycle of two lowland tropical forest plots in south-western Amazonia, Peru. Plant Ecol. Diversity 7, 85–105 (2014).

    Article  Google Scholar 

  • 82.

    Cleveland, C. C. & Townsend, A. R. Nutrient additions to a tropical rain forest drive substantial soil carbon dioxide losses to the atmosphere. Proc. Natl Acad. Sci. USA 103, 10316–10321 (2006).

    CAS  Article  Google Scholar 

  • 83.

    Allison, S. D., Weintraub, M. N., Gartner, T. B. & Waldrop, M. P. in Soil enzymology (eds. Girish Shukla & Ajit Varma) 229–243 (Springer Berlin Heidelberg, 2011).

  • 84.

    Classen, A. T. et al. Direct and indirect effects of climate change on soil microbial and soil microbial-plant interactions: What lies ahead? Ecosphere 6, 1–21 (2015).

    Article  Google Scholar 

  • 85.

    Hoeksema, J. D. et al. Ectomycorrhizal plant-fungal co-invasions as natural experiments for connecting plant and fungal traits to their ecosystem consequences. Front. Forests Glob. Change https://doi.org/10.3389/ffgc.2020.00084 (2020).

  • 86.

    Allison, S. D. Cheaters, diffusion and nutrients constrain decomposition by microbial enzymes in spatially structured environments. Ecol. Lett. 8, 626–635 (2005).

    Article  Google Scholar 

  • 87.

    Nottingham, A. T. et al. Microbes follow Humboldt: temperature drives plant and soil microbial diversity patterns from the Amazon to the Andes. Ecology 99, 2455–2466 (2018).

    Article  Google Scholar 

  • 88.

    Štursova, M., Crenshaw, C. L. & Sinsabaugh, R. L. Microbial responses to long-term N deposition in a semiarid grassland. Microb. Ecol. 51, 90–98 (2006).

    Article  Google Scholar 

  • 89.

    Henry, H. A. L., Juarez, J. D., Field, C. B. & Vitousek, P. M. Interactive effects of elevated CO2, N deposition and climate change on extracellular enzyme activity and soil density fractionation in a California annual grassland. Glob. Change Biol. 11, 1808–1815 (2005).

    Article  Google Scholar 

  • 90.

    Lashermes, G., Gainvors-Claisse, A., Recous, S. & Bertrand, I. Enzymatic strategies and carbon use efficiency of a litter-decomposing fungus grown on maize leaves, stems, and roots. Front. Microbiol. 7, 1315 (2016).

  • 91.

    Chet, I. in Innovative Approaches to Plant Disease Control (ed. I. Chet) (Wiley, 1987).

  • 92.

    Boller, T. in Cellular and Molecular Biology of Plant Stress (eds. J. L. Key & T. Kosuge) (Liss, A.R., 1985).

  • 93.

    Bond-Lamberty, B., Bailey, V. L., Chen, M., Gough, C. M. & Vargas, R. Globally rising soil heterotrophic respiration over recent decades. Nature 560, 80–83 (2018).

    CAS  Article  Google Scholar 

  • 94.

    Ruivo, M. & Cunha, E. in Ecosystems and Sustainable Development (eds. E. Tiezzi, C. A. Brebbia, & J. L. Uso) 1113–1121 (WIT Press, 2003).

  • 95.

    Eastman, J. R. TerrSet Manual (Clark University, 2015).

  • 96.

    Ihrmark, K. et al. New primers to amplify the fungal ITS2 region—evaluation by 454-sequencing of artificial and natural communities. FEMS Microbiol. Ecol. 82, 666–677 (2012).

    CAS  Article  Google Scholar 

  • 97.

    White, T. J., Bruns, T. D., Lee, S. B. & Taylor, J. W. in PCR—Protocols and applications—A laboratory manual (eds. N. Innis, D. Gelfand, J. Sninsky, & T. White) 315–322 (Academic Press, 1990).

  • 98.

    Lindahl, B. D. et al. Fungal community analysis by high-throughput sequencing of amplified markers—a user’s guide. N. Phytol. 199, 288–299 (2013).

    CAS  Article  Google Scholar 

  • 99.

    Kõljalg, U. et al. Towards a unified paradigm for sequence-based identification of fungi. Mol. Ecol. 22, 5271–5277 (2013).

    Article  CAS  Google Scholar 

  • 100.

    Nguyen, N. H. et al. FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fung. Ecol. 20, 241–248 (2016).

    Article  Google Scholar 

  • 101.

    Oksanen, J. et al. vegan: community ecology package. R package version 2.3-5. http://CRAN.R-project.org/package=vegan. (2016).

  • 102.

    Pritsch, K. et al. Optimized assay and storage conditions for enzyme activity profiling of ectomycorrhizae. Mycorrhiza 21, 589–600 (2011).

    CAS  Article  Google Scholar 

  • 103.

    Souza, R. C. et al. Responses of soil extracellular enzyme activities to experimental warming and CO2 enrichment at the alpine treeline. Plant Soil 416, 527–537 (2017).

    CAS  Article  Google Scholar 

  • 104.

    Baselga, A. & Orme, C. D. L. betapart: an R package for the study of beta diversity. Methods Ecol. Evol. 3, 808–812 (2012).

    Article  Google Scholar 

  • 105.

    Vohník, M. & Albrechtová, J. The co-occurrence and morphological continuum between ericoid mycorrhiza and dark septate endophytes in roots of six european Rhododendron species. Folia Geobotanica 46, 373–386 (2011).

    Article  Google Scholar 

  • 106.

    Grelet, G., Martino, E., Dickie, I. A., Tajuddin, R. & Artz, R. in Molecular mycorrhizal Symbiosis (ed. F. Martin) (John Wiley & Sons, Inc, 2017).

  • 107.

    Benjamini, Y. & Hochberg, Y. Controlling the false diiscovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B 57, 289–300 (1995).

    Google Scholar 


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