Abstract
The increased frequency of climate extremes in recent years has profoundly affected terrestrial ecosystem functions and the welfare of human society. The carbon cycle is a key process of terrestrial ecosystem changes. Therefore, a better understanding and assessment of the impacts of climate extremes on the terrestrial carbon cycle could provide an important scientific basis to facilitate the mitigation and adaption of our society to climate change. In this paper, we systematically review the impacts of climate extremes (e.g. drought, extreme precipitation, extreme hot and extreme cold) on terrestrial ecosystems and their mechanisms. Existing studies have suggested that drought is one of the most important stressors on the terrestrial carbon sink, and that it can inhibit both ecosystem productivity and respiration. Because ecosystem productivity is usually more sensitive to drought than respiration, drought can significantly reduce the strength of terrestrial ecosystem carbon sinks and even turn them into carbon sources. Large inter-model variations have been found in the simulations of drought-induced changes in the carbon cycle, suggesting the existence of a large gap in current understanding of the mechanisms behind the responses of ecosystem carbon balance to drought, especially for tropical vegetation. The effects of extreme precipitation on the carbon cycle vary across different regions. In general, extreme precipitation enhances carbon accumulation in arid ecosystems, but restrains carbon sequestration in moist ecosystems. However, current knowledge on the indirect effects of extreme precipitation on the carbon cycle through regulating processes such as soil carbon lateral transportation and nutrient loss is still limited. This knowledge gap has caused large uncertainties in assessing the total carbon cycle impact of extreme precipitation. Extreme hot and extreme cold can affect the terrestrial carbon cycle through various ecosystem processes. Note that the severity of such climate extremes depends greatly on their timing, which needs to be investigated thoroughly in future studies. In light of current knowledge and gaps in the understanding of how extreme climates affect the terrestrial carbon cycle, we strongly recommend that future studies should place more attention on the long-term impacts and on the driving mechanisms at different time scales. Studies based on multi-source data, methods and across multiple spatial-temporal scales, are also necessary to better characterize the response of terrestrial ecosystems to climate extremes.
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Adams H D, Zeppel M J B, Anderegg W R L, Hartmann H, Landhäusser S M, Tissue D T, Huxman T E, Hudson P J, Franz T E, Allen C D, Anderegg LDL, Barron-Gafford G A, Beerling D J, Breshears D D, Brodribb T J, Bugmann H, Cobb R C, Collins A D, Dickman LT, Duan H, Ewers B E, Galiano L, Galvez D A, Garcia-Forner N, Gaylord M L, Germino M J, Gessler A, Hacke U G, Hakamada R, Hector A, Jenkins M W, Kane J M, Kolb T E, Law D J, Lewis J D, Limousin J M, Love D M, Macalady A K, Martinez-Vilalta J, Mencuccini M, Mitchell P J, Muss J D, O’Brien M J, O’Grady A P, Pangle R E, Pinkard E A, Piper F I, Plaut J A, Pockman W T, Quirk J, Reinhardt K, Ripullone F, Ryan M G, Sala A, Sevanto S, Sperry J S, Vargas R, Vennetier M, Way D A, Xu C, Yepez E A, McDowell N G. 2017. A multi-species synthesis of physiological mechanisms in drought-induced tree mortality. Nat Ecol Evol, 1: 1285–1291
Allen C D, Breshears D D, McDowell N G. 2015. On underestimation of global vulnerability to tree mortality and forest die-off from hotter drought in the Anthropocene. Ecosphere, 6: 1–55
Amiro B D, Barr A G, Barr J G, Black T A, Bracho R, Brown M, Chen J, Clark K L, Davis K J, Desai A R, Dore S, Engel V, Fuentes J D, Goldstein A H, Goulden M L, Kolb T E, Lavigne M B, Law B E, Margolis H A, Martin T, McCaughey J H, Misson L, Montes-Helu M, Noormets A, Randerson J T, Starr G, Xiao J. 2010. Ecosystem carbon dioxide fluxes after disturbance in forests of North America. J Geophys Res, 115: G00k02
Anderegg W R L, Klein T, Bartlett M, Sack L, Pellegrini A F A, Choat B, Jansen S. 2016. Meta-analysis reveals that hydraulic traits explain cross-species patterns of drought-induced tree mortality across the globe. Proc Natl Acad Sci USA, 113: 5024–5029
Anderegg W R L, Plavcová L, Anderegg LDL, Hacke U G, Berry J A, Field C B. 2013. Drought’s legacy: Multiyear hydraulic deterioration underlies widespread aspen forest die-off and portends increased future risk. Glob Change Biol, 19: 1188–1196
Anderegg W R L, Schwalm C, Biondi F, Camarero J J, Koch G, Litvak M, Ogle K, Shaw J D, Shevliakova E, Williams A P, Wolf A, Ziaco E, Pacala S. 2015. Pervasive drought legacies in forest ecosystems and their implications for carbon cycle models. Science, 349: 528–532
Aragão L E O C, Malhi Y, Barbier N, Lima A, Shimabukuro Y, Anderson L, Saatchi S. 2008. Interactions between rainfall, deforestation and fires during recent years in the Brazilian Amazonia. Philos Trans R Soc B-Biol Sci, 363: 1779–1785
Aragão L E O C, Malhi Y, Roman-Cuesta R M, Saatchi S, Anderson L O, Shimabukuro Y E. 2007. Spatial patterns and fire response of recent Amazonian droughts. Geophys Res Lett, 34: L07701
Asner G P, Alencar A. 2010. Drought impacts on the Amazon forest: The remote sensing perspective. New Phytol, 187: 569–578
Barriopedro D, Fischer E M, Luterbacher J, Trigo R M, Garcia-Herrera R. 2011. The hot summer of 2010: Redrawing the temperature record map of europe. Science, 332: 220–224
Bastos A, Gouveia C M, Trigo R M, Running S W. 2014. Analysing the spatio-temporal impacts of the 2003 and 2010 extreme heatwaves on plant productivity in Europe. Biogeosciences, 11: 3421–3435
Bonal D, Bosc A, Ponton S, Goret J Y, Burban B, Gross P, Bonnefond J M, Elbers J, Longdoz B, Epron D, Guehl J M, Granier A. 2008. Impact of severe dry season on net ecosystem exchange in the Neotropical rainforest of French Guiana. Glob Change Biol, 14: 1917–1933
Brando P M, Balch J K, Nepstad D C, Morton D C, Putz F E, Coe M T, Silvério D, Macedo M N, Davidson E A, Nóbrega C C, Alencar A, Soares-Filho B S. 2014. Abrupt increases in Amazonian tree mortality due to drought-fire interactions. Proc Natl Acad Sci USA, 111: 6347–6352
Bréda N, Huc R, Granier A, Dreyer E. 2006. Temperate forest trees and stands under severe drought: A review of ecophysiological responses, adaptation processes and long-term consequences. Ann For Sci, 63: 625–644
Brodribb T J, Cochard H. 2009. Hydraulic failure defines the recovery and point of death in water-stressed conifers. Plant Physiol, 149: 575–584
Brodribb T J, Skelton R P, McAdam S A M, Bienaimé D, Lucani C J, Marmottant P. 2016. Visual quantification of embolism reveals leaf vulnerability to hydraulic failure. New Phytol, 209: 1403–1409
Buermann W, Bikash P R, Jung M, Burn D H, Reichstein M. 2013. Earlier springs decrease peak summer productivity in North American boreal forests. Environ Res Lett, 8: 024027
Choat B, Badel E, Burlett R, Delzon S, Cochard H, Jansen S. 2016. Noninvasive measurement of vulnerability to drought-induced embolism by X-ray microtomography. Plant Physiol, 170: 273–282
Choat B, Brodribb T J, Brodersen C R, Duursma R A, López R, Medlyn B E. 2018. Triggers of tree mortality under drought. Nature, 558: 531–539
Ciais P, Reichstein M, Viovy N, Granier A, Ogée J, Allard V, Aubinet M, Buchmann N, Bernhofer C, Carrara A, Chevallier F, De Noblet N, Friend A D, Friedlingstein P, Grünwald T, Heinesch B, Keronen P, Knohl A, Krinner G, Loustau D, Manca G, Matteucci G, Miglietta F, Ourcival J M, Papale D, Pilegaard K, Rambal S, Seufert G, Soussana J F, Sanz M J, Schulze E D, Vesala T, Valentini R. 2005. Europe-wide reduction in primary productivity caused by the heat and drought in 2003. Nature, 437: 529–533
Ciais P, Sabine C, Bala G, Bopp L, Brovkin V, Canadell J, Chhabra A, DeFries R, Galloway J, Heimann M, Jones C, Le Quere C, Myneni R B, Piao S, Thornton P, Sabine C, Bala G, Bopp L, Brovkin V, Canadell J, Chhabra A, DeFries R, Galloway J, Heimann M, Jones C, Le Quere C, Myneni R B, Piao S, Thornton P. 2013. Carbon and other biogeochemical cycles. In: Stocker T F, Qin D, Plattner G K, Tignor M, Allen S K, Boschung J, Nauels A, Xia Y, Bex V, Midgley P M, eds. 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: Cambridge University Press. 465–570
Cox P M, Betts R A, Collins M, Harris P P, Huntingford C, Jones C D. 2004. Amazonian forest dieback under climate-carbon cycle projections for the 21st century. Theor Appl Climatol, 78: 137–156
Cox P M, Betts R A, Jones C D, Spall S A, Totterdell I J. 2000. Acceleration of global warming due to carbon-cycle feedbacks in a coupled climate model. Nature, 408: 184–187
De Boeck H J, Dreesen F E, Janssens I A, Nijs I. 2010. Climatic characteristics of heat waves and their simulation in plant experiments. Glob Change Biol, 16: 1992–2000
De Boeck H J, Dreesen F E, Janssens I A, Nijs I. 2011. Whole-system responses of experimental plant communities to climate extremes imposed in different seasons. New Phytol, 189: 806–817
Della-Marta P M, Haylock M R, Luterbacher J, Wanner H. 2007. Doubled length of western European summer heat waves since 1880. J Geophys Res, 112: D15103
Delpierre N, Soudani K, François C, Köstner B, Pontailler J Y, Nikinmaa E, Misson L, Aubinet M, Bernhofer C, Granier A, Grünwald T, Heinesch B, Longdoz B, Ourcival J M, Rambal S, Vesala T, Dufrêne E. 2009. Exceptional carbon uptake in European forests during the warm spring of 2007: A data-model analysis. Glob Change Biol, 15: 1455–1474
Dittmar C, Fricke W, Elling W. 2006. Impact of late frost events on radial growth of common beech (Fagus sylvatica L.) in Southern Germany. Eur J For Res, 125: 249–259
Doughty C E, Metcalfe D B, Girardin C A J, Amézquita F F, Cabrera D G, Huasco W H, Silva-Espejo J E, Araujo-Murakami A, da Costa M C, Rocha W, Feldpausch T R, Mendoza A L M, da Costa A C L, Meir P, Phillips O L, Malhi Y. 2015. Drought impact on forest carbon dynamics and fluxes in Amazonia. Nature, 519: 78–82
Esquivel-Muelbert A, Baker T R, Dexter K G, Lewis S L, Brienen R J W, Feldpausch T R, Lloyd J, Monteagudo-Mendoza A, Arroyo L, Álvarez-Dávila E, Higuchi N, Marimon B S, Marimon-Junior B H, Silveira M, Vilanova E, Gloor E, Malhi Y, Chave J, Barlow J, Bonal D, Davila Cardozo N, Erwin T, Fauset S, Hérault B, Laurance S, Poorter L, Qie L, Stahl C, Sullivan M J P, Ter Steege H, Vos VA, Zuidema P A, Almeida E, Almeida de Oliveira E, Andrade A, Vieira S A, Aragão L, Araujo-Murakami A, Arets E, Aymard C G A, Baraloto C, Camargo P B, Barroso J G, Bongers F, Boot R, Camargo J L, Castro W, Chama Moscoso V, Comiskey J, Cornejo Valverde F, Lola da Costa A C, Del Aguila Pasquel J, Di Fiore A, Fernanda Duque L, Elias F, Engel J, Flores Llampazo G, Galbraith D, Herrera Fernández R, Honorio Coronado E, Hubau W, Jimenez-Rojas E, Lima A J N, Umetsu R K, Laurance W, Lopez-Gonzalez G, Lovejoy T, Aurelio Melo Cruz O, Morandi P S, Neill D, Núñez Vargas P, Pallqui Camacho N C, Parada Gutierrez A, Pardo G, Peacock J, Peña-Claros M, Peñuela-Mora M C, Petronelli P, Pickavance G C, Pitman N, Prieto A, Quesada C, Ramírez-Angulo H, Réjou-Méchain M, Restrepo Correa Z, Roopsind A, Rudas A, Salomão R, Silva N, Silva Espejo J, Singh J, Stropp J, Terborgh J, Thomas R, Toledo M, Torres-Lezama A, Valenzuela Gamarra L, van de Meer P J, van der Heijden G, van der Hout P, Vasquez Martinez R, Vela C, Vieira I C G, Phillips O L. 2019. Compositional response of Amazon forests to climate change. Glob Change Biol, 25: 39–56
Fay P A, Blair J M, Smith M D, Nippert J B, Carlisle J D, Knapp A K. 2011. Relative effects of precipitation variability and warming on tall-grass prairie ecosystem function. Biogeosciences, 8: 3053–3068
Field C, Barros V, Stocker T, Dahe Q. 2012. Managing the Risks of Extreme Events and disasters to Advance Climate Change Adaptation: Special Report of the Intergovernmental Panel on Climate Change. Cambridge: Cambridge University Press
Frank D, Reichstein M, Bahn M, Thonicke K, Frank D, Mahecha M D, Smith P, van der Velde M, Vicca S, Babst F, Beer C, Buchmann N, Canadell J G, Ciais P, Cramer W, Ibrom A, Miglietta F, Poulter B, Rammig A, Seneviratne S I, Walz A, Wattenbach M, Zavala M A, Zscheischler J. 2015. Effects of climate extremes on the terrestrial carbon cycle: Concepts, processes and potential future impacts. Glob Change Biol, 21: 2861–2880
Fu Y S H, Zhao H F, Piao S L, Peaucelle M, Peng S S, Zhou G Y, Ciais P, Huang M T, Menzel A, Uelas J P, Song Y, Vitasse Y, Zeng Z Z, Janssens I A. 2015. Declining global warming effects on the phenology of spring leaf unfolding. Nature, 526: 104–107
Gatti L V, Gloor M, Miller J B, Doughty C E, Malhi Y, Domingues L G, Basso L S, Martinewski A, Correia C S C, Borges V F, Freitas S, Braz R, Anderson L O, Rocha H, Grace J, Phillips O L, Lloyd J. 2014. Drought sensitivity of Amazonian carbon balance revealed by atmospheric measurements. Nature, 506: 76–80
Haddad N M, Tilman D, Knops J M H. 2002. Long-term oscillations in grassland productivity induced by drought. Ecol Lett, 5: 110–120
Hartmann H, Moura C F, Anderegg W R L, Ruehr N K, Salmon Y, Allen C D, Arndt S K, Breshears D D, Davi H, Galbraith D, Ruthrof K X, Wunder J, Adams H D, Bloemen J, Cailleret M, Cobb R, Gessler A, Grams TEE, Jansen S, Kautz M, Lloret F, O’Brien M. 2018. Research frontiers for improving our understanding of drought-induced tree and forest mortality. New Phytol, 218: 15–28
He Q, Silliman B R, Liu Z Z, Cui B S. 2017. Natural enemies govern ecosystem resilience in the face of extreme droughts. Ecol Lett, 20: 194–201
Heisler-White J L, Blair J M, Kelly E F, Harmoney K, Knapp A K. 2009. Contingent productivity responses to more extreme rainfall regimes across a grassland biome. Glob Change Biol, 15: 2894–2904
Hoffmann T, Schlummer M, Notebaert B, Verstraeten G, Korup O. 2013. Carbon burial in soil sediments from Holocene agricultural erosion, Central Europe. Glob Biogeochem Cycle, 27: 828–835
Hoffmann W A, Marchin R M, Abit P, Lau O L. 2011. Hydraulic failure and tree dieback are associated with high wood density in a temperate forest under extreme drought. Glob Change Biol, 17: 2731–2742
Hoover D L, Knapp A K, Smith M D. 2014. Resistance and resilience ofa grassland ecosystem to climate extremes. Ecology, 95: 2646–2656
Huang K, Wang S Q, Zhou L, Wang H M, Liu Y F, Yang F T. 2013. Effects of drought and ice rain on potential productivity of a subtropical coniferous plantation from 2003 to 2010 based on eddy covariance flux observation. Environ Res Lett, 8: 035021
Huang M T, Wang X H, Keenan T F, Piao S L. 2018. Drought timing influences the legacy of tree growth recovery. Glob Change Biol, 24: 3546–3559
Hufkens K, Friedl M A, Keenan T F, Sonnentag O, Bailey A, O’Keefe J, Richardson A D. 2012. Ecological impacts of a widespread frost event following early spring leaf-out. Glob Change Biol, 18: 2365–2377
Inouye D W. 2000. The ecological and evolutionary significance of frost in the context of climate change. Ecol Lett, 3: 457–463
Inouye D W. 2008. Effects of climate change on phenology, frost damage, and floral abundance of montane wildflowers. Ecology, 89: 353–362
IPCC. 2013. 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: Cambridge University Press
Isbell F, Craven D, Connolly J, Loreau M, Schmid B, Beierkuhnlein C, Bezemer T M, Bonin C, Bruelheide H, de Luca E, Ebeling A, Griffin J N, Guo Q, Hautier Y, Hector A, Jentsch A, Kreyling J, Lanta V, Manning P, Meyer S T, Mori A S, Naeem S, Niklaus P A, Polley H W, Reich P B, Roscher C, Seabloom E W, Smith M D, Thakur M P, Tilman D, Tracy B F, van der Putten W H, van Ruijven J, Weigelt A, Weisser W W, Wilsey B, Eisenhauer N. 2015. Biodiversity increases the resistance of ecosystem productivity to climate extremes. Nature, 526: 574–577
Jentsch A, Kreyling J, Elmer M, Gellesch E, Glaser B, Grant K, Hein R, Lara M, Mirzae H, Nadler S E, Nagy L, Otieno D, Pritsch K, Rascher U, Schädler M, Schloter M, Singh B K, Stadler J, Walter J, Wellstein C, Wöllecke J, Beierkuhnlein C. 2011. Climate extremes initiate ecosystem-regulating functions while maintaining productivity. J Ecol, 99: 689–702
Knapp A K, Beier C, Briske D D, Classen AT, Luo Y, Reichstein M, Smith M D, Smith S D, Bell J E, Fay P A, Heisler J L, Leavitt S W, Sherry R, Smith B, Weng E. 2008. Consequences of more extreme precipitation regimes for terrestrial ecosystems. Bioscience, 58: 811–821
Knapp A K, Fay P A, Blair J M, Collins S L, Smith M D, Carlisle J D, Harper C W, Danner B T, Lett M S, McCarron J K. 2002. Rainfall variability, carbon cycling, and plant species diversity in a mesic grassland. Science, 298: 2202–2205
Knapp A K, Smith M D. 2001. Variation among biomes in temporal dynamics of aboveground primary production. Science, 291: 481–484
Kramer K, Vreugdenhil S J, van der Werf D C. 2008. Effects of flooding on the recruitment, damage and mortality of riparian tree species: A field and simulation study on the Rhine floodplain. For Ecol Manage, 255: 3893–3903
Kreyling J, Wenigmann M, Beierkuhnlein C, Jentsch A. 2008. Effects of extreme weather events on plant productivity and tissue die-back are modified by community composition. Ecosystems, 11: 752–763
Kurz WA, Stinson G, Rampley G J, Dymond C C, Neilson E T. 2008. Risk of natural disturbances makes future contribution of Canada’s forests to the global carbon cycle highly uncertain. Proc Natl Acad Sci USA, 105: 1551–1555
Lal R. 2003. Global potential of soil carbon sequestration to mitigate the greenhouse effect. Critical Rev Plant Sci, 22: 151–184
Le Quéré C, Andrew R M, Friedlingstein P, Sitch S, Pongratz J, Manning A C, Korsbakken J I, Peters G P, Canadell J G, Jackson R B, Boden T A, Tans P P, Andrews O D, Arora V K, Bakker D C E, Barbero L, Becker M, Betts R A, Bopp L, Chevallier F, Chini L P, Ciais P, Cosca C E, Cross J, Currie K, Gasser T, Harris I, Hauck J, Haverd V, Houghton R A, Hunt C W, Hurtt G, Ilyina T, Jain A K, Kato E, Kautz M, Keeling R F, Klein Goldewijk K, Körtzinger A, Landschützer P, Lefèvre N, Lenton A, Lienert S, Lima I, Lombardozzi D, Metzl N, Millero F, Monteiro P M S, Munro D R, Nabel J E M S, Nakaoka S, Nojiri Y, Padín X A, Peregon A, Pfeil B, Pierrot D, Poulter B, Rehder G, Reimer J, Rödenbeck C, Schwinger J, Séférian R, Skjelvan I, Stocker B D, Tian H, Tilbrook B, van der Laan-Luijkx I T, van der Werf G R, van Heuven S, Viovy N, Vuichard N, Walker A P, Watson A J, Wiltshire A J, Zaehle S, Zhu D. 2018. Global carbon budget 2017. Earth Syst Sci Data Discuss, 10: 405–448
Le Quéré C, Raupach M R, Canadell J G, Marland G, Le Quéré C, Raupach M R, Canadell J G, Marland G, Bopp L, Ciais P, Conway T J, Doney S C, Feely R A, Foster P, Friedlingstein P, Gurney K, Houghton R A, House J I, Huntingford C, Levy P E, Lomas M R, Majkut J, Metzl N, Ometto J P, Peters G P, Prentice I C, Randerson J T, Running S W, Sarmiento J L, Schuster U, Sitch S, Takahashi T, Viovy N, van der Werf G R, Woodward F I. 2009. Trends in the sources and sinks of carbon dioxide. Nat Geosci, 2: 831–836
Lewis S L, Brando P M, Phillips O L, van der Heijden G M F, Nepstad D. 2011. The 2010 amazon drought. Science, 331: 554
Li X, Li Y, Chen A, Gao M, Slette I J, Piao S. 2019. The impact of the 2009/2010 drought on vegetation growth and terrestrial carbon balance in Southwest China. Agric For Meteor, 269–270: 239–248
Liu Q, Fu Y S H, Zhu Z C, Liu Y W, Liu Z, Huang M T, Janssens I A, Piao S L. 2016. Delayed autumn phenology in the Northern Hemisphere is related to change in both climate and spring phenology. Glob Change Biol, 22: 3702–3711
Liu Q, Piao S L, Janssens I A, Fu Y S, Peng S S, Lian X, Ciais P, Myneni R B, Penuelas J, Wang T. 2018. Extension of the growing season increases vegetation exposure to frost. Nat Commun, 9: 426
Liu W X, Zhang Z, Wan S Q. 2009. Predominant role ofwater in regulating soil and microbial respiration and their responses to climate change in a semiarid grassland. Glob Change Biol, 15: 184–195
Liu Y, Zhou Y, Ju W, Wang S, Wu X, He M, Zhu G. 2014. Impacts of droughts on carbon sequestration by China’s terrestrial ecosystems from 2000 to 2011. Biogeosciences, 11: 2583–2599
Luterbacher J, Dietrich D, Xoplaki E, Grosjean M, Wanner H. 2004. European seasonal and annual temperature variability, trends, and extremes since 1500. Science, 303: 1499–1503
McDowell N, Pockman W T, Allen C D, Breshears D D, Cobb N, Kolb T, Plaut J, Sperry J, West A, Williams D G, Yepez E A. 2008. Mechanisms of plant survival and mortality during drought: Why do some plants survive while others succumb to drought? New Phytol, 178: 719–739
Meir P, Metcalfe D B, Costa A C L, Fisher R A. 2008. The fate of assimilated carbon during drought: Impacts on respiration in Amazon rainforests. Philos Trans R Soc B-Biol Sci, 363: 1849–1855
Mou C, Sun G, Luo P, Wang Z, Luo G. 2013. Flowering responses of alpine meadow plant in the Qinghai-Tibetan Plateau to extreme drought imposed in different periods. Chin J Appl Environ Biol, 19: 272–279
Nemani R R, Keeling C D, Hashimoto H, Jolly W M, Piper S C, Tucker C J, Myneni R B, Running S W. 2003. Climate-driven increases in global terrestrial net primary production from 1982 to 1999. Science, 300: 1560–1563
Perkins S E, Alexander L V, Nairn J R. 2012. Increasing frequency, intensity and duration of observed global heatwaves and warm spells. Geophys Res Lett, 39: 2012GL053361
Perkins-Kirkpatrick S E, Gibson P B. 2017. Changes in regional heatwave characteristics as a function of increasing global temperature. Sci Rep, 7: 12256
Phillips O L, Aragão L E O C, Lewis S L, Fisher J B, Lloyd J, López-González G, Malhi Y, Monteagudo A, Peacock J, Quesada C A, van der Heijden G, Almeida S, Amaral I, Arroyo L, Aymard G, Baker T R, Bánki O, Blanc L, Bonal D, Brando P, Chave J, de Oliveira A C A, Cardozo N D, Czimczik C I, Feldpausch T R, Freitas M A, Gloor E, Higuchi N, Jiménez E, Lloyd G, Meir P, Mendoza C, Morel A, Neill D A, Nepstad D, Patino S, Peñuela M C, Prieto A, Ramirez F, Schwarz M, Silva J, Silveira M, Thomas A S, Steege H T, Stropp J, Vásquez R, Zelazowski P, Alvarez Dávila E, Andelman S, Andrade A, Chao K J, Erwin T, Di Fiore A, Honorio C E, Keeling H, Killeen T J, Laurance W F, Peña Cruz A, Pitman N C A, Núñez Vargas P, Ramírez-Angulo H, Rudas A, Salamão R, Silva N, Terborgh J, Torres-Lezama A. 2009. Drought sensitivity of the Amazon rainforest. Science, 323: 1344–1347
Piao S L, Friedlingstein P, Ciais P, Viovy N, Demarty J. 2007. Growing season extension and its impact on terrestrial carbon cycle in the Northern Hemisphere over the past 2 decades. Glob Biogeochem Cycle, 21: GB3018
Piao S L, Sitch S, Ciais P, Friedlingstein P, Peylin P, Wang X H, Ahlstrom A, Anav A, Canadell J G, Cong N, Huntingford C, Jung M, Levis S, Levy P E, Li J S, Lin X, Lomas M R, Lu M, Luo Y Q, Ma Y C, Myneni R B, Poulter B, Sun Z Z, Wang T, Viovy N, Zaehle S, Zeng N. 2013. Evaluation of terrestrial carbon cycle models for their response to climate variability and to CO2 trends. Glob Change Biol, 19: 2117–2132
Polle A, Kroniger W, Rennenberg H. 1996. Seasonal fluctuations of ascorbate-related enzymes: Acute and delayed effects of late frost in spring on antioxidative systems in needles of Norway spruce (Picea abies L.). Plant Cell Physiol, 37: 717–725
Reichstein M, Ciais P, Papale D, Valentini R, Running S, Viovy N, Cramer W, Granier A, Ogée J, Allard V, Aubinet M, Bernhofer C, Buchmann N, Carrara A, Grünwald T, Heimann M, Heinesch B, Knohl A, Kutsch W, Loustau D, Manca G, Matteucci G, Miglietta F, Ourcival J M, Pilegaard K, Pumpanen J, Rambal S, Schaphoff S, Seufert G, Soussana J F, Sanz M J, Vesala T, Zhao M. 2007. Reduction of ecosystem productivity and respiration during the European summer 2003 climate anomaly: A joint flux tower, remote sensing and modelling analysis. Glob Change Biol, 13: 634–651
Rodriguez-Dominguez C M, Carins Murphy M R, Lucani C, Brodribb T J. 2018. Mapping xylem failure in disparate organs ofwhole plants reveals extreme resistance in olive roots. New Phytol, 218: 1025–1035
Saleska S R, Didan K, Huete A R, da Rocha H R. 2007. Amazon forests green-up during 2005 drought. Science, 318: 612
Salvucci M E, Crafts-Brandner S J. 2004. Inhibition of photosynthesis by heat stress: The activation state of Rubisco as a limiting factor in photosynthesis. Physiol Plant, 120: 179–186
Samanta A, Ganguly S, Hashimoto H, Devadiga S, Vermote E, Knyazikhin Y, Nemani R R, Myneni R B. 2010. Amazon forests did not green-up during the 2005 drought. Geophys Res Lett, 37: L05401
Schwalm C R, Williams C A, Schaefer K, Arneth A, Bonal D, Buchmann N, Chen J, Law B E, Lindroth A, Luyssaert S, Reichstein M, Richardson A D. 2010. Assimilation exceeds respiration sensitivity to drought: A FLUXNET synthesis. Glob Change Biol, 16: 657–670
Seidl R, Klonner G, Rammer W, Essl F, Moreno A, Neumann M, Dullinger S. 2018. Invasive alien pests threaten the carbon stored in Europe’s forests. Nat Commun, 9: 1626
Shi Z, Thomey M L, Mowll W, Litvak M, Brunsell N A, Collins S L, Pockman W T, Smith M D, Knapp A K, Luo Y. 2014. Differential effects of extreme drought on production and respiration: Synthesis and modeling analysis. Biogeosciences, 11: 621–633
Sippel S, Reichstein M, Ma X, Mahecha M D, Lange H, Flach M, Frank D. 2018. Drought, heat, and the carbon cycle: A review. Curr Clim Change Rep, 4: 266–286
Sippel S, Zscheischler J, Reichstein M. 2016. Ecosystem impacts ofclimate extremes crucially depend on the timing. Proc Natl Acad Sci USA, 113: 5768–5770
Snyder R, Melo-Abreu J. 2005. Frost protection: Fundamentals, practice and economics. Frost Prot Fund Pract Econ. 1–240
Stallard R F. 1998. Terrestrial sedimentation and the carbon cycle: Coupling weathering and erosion to carbon burial. Glob Biogeochem Cycle, 12: 231–257
Suseela V, Conant RT, Wallenstein M D, Dukes J S. 2012. Effects of soil moisture on the temperature sensitivity of heterotrophic respiration vary seasonally in an old-field climate change experiment. Glob Change Biol, 18: 336–348
Thakur M P, Reich P B, Hobbie S E, Stefanski A, Rich R, Rice K E, Eddy W C, Eisenhauer N. 2018. Reduced feeding activity of soil detritivores under warmer and drier conditions. Nat Clim Change, 8: 75–78
Urli M, Porté A J, Cochard H, Guengant Y, Burlett R, Delzon S. 2013. Xylem embolism threshold for catastrophic hydraulic failure in angiosperm trees. Tree Physiol, 33: 672–683
Van Oost K, Quine T A, Govers G, De Gryze S, Six J, Harden J W, Ritchie J C, McCarty G W, Heckrath G, Kosmas C, Giraldez J V, Marques da Silva J R, Merckx R. 2007. The impact of agricultural soil erosion on the global carbon cycle. Science, 318: 626–629
Van Oost K, Verstraeten G, Doetterl S, Notebaert B, Wiaux F, Broothaerts N, Six J. 2012. Legacy of human-induced C erosion and burial on soil-atmosphere C exchange. Proc Natl Acad Sci USA, 109: 19492–19497
Van Ruijven J, Berendse F. 2010. Diversity enhances community recovery, but not resistance, after drought. J Ecol, 98: 81–86
Vanoni M, Bugmann H, Nötzli M, Bigler C. 2016. Drought and frost contribute to abrupt growth decreases before tree mortality in nine temperate tree species. For Ecol Manage, 382: 51–63
Vicca S, Bahn M, Estiarte M, van Loon E E, Vargas R, Alberti G, Ambus P, Arain M A, Beier C, Bentley L P, Borken W, Buchmann N, Collins S L, de Dato G, Dukes J S, Escolar C, Fay P, Guidolotti G, Hanson P J, Kahmen A, Kröel-Dulay G, Ladreiter-Knauss T, Larsen K S, Lellei-Kovacs E, Lebrija-Trejos E, Maestre F T, Marhan S, Marshall M, Meir P, Miao Y, Muhr J, Niklaus P A, Ogaya R, Peñuelas J, Poll C, Rustad L E, Savage K, Schindlbacher A, Schmidt I K, Smith A R, Sotta E D, Suseela V, Tietema A, van Gestel N, van Straaten O, Wan S, Weber U, Janssens I A. 2014. Can current moisture responses predict soil CO2 efflux under altered precipitation regimes? A synthesis of manipulation experiments. Biogeosciences, 11: 2991–3013
von Buttlar J, Zscheischler J, Rammig A, Sippel S, Reichstein M, Knohl A, Jung M, Menzer O, Altaf Arain M, Buchmann N, Cescatti A, Gianelle D, Kiely G, Law B E, Magliulo V, Margolis H, McCaughey H, Merbold L, Migliavacca M, Montagnani L, Oechel W, Pavelka M, Peichl M, Rambal S, Raschi A, Scott R L, Vaccari F P, van Gorsel E, Varlagin A, Wohlfahrt G, Mahecha M D. 2018. Impacts of droughts and extremetemperature events on gross primary production and ecosystem respiration: A systematic assessment across ecosystems and climate zones. Biogeosciences, 15: 1293–1318
Wang X H, Piao S L, Ciais P, Friedlingstein P, Myneni R B, Cox P, Heimann M, Miller J, Peng S S, Wang T, Yang H, Chen A P. 2014. A two-fold increase of carbon cycle sensitivity to tropical temperature variations. Nature, 506: 212–215
White M A, Running S W, Thornton P E. 1999. The impact of growingseason length variability on carbon assimilation and evapotranspiration over 88 years in the eastern US deciduous forest. Int J Biometeorol, 42: 139–145
Wolf S, Keenan T F, Fisher J B, Baldocchi D D, Desai A R, Richardson A D, Scott R L, Law B E, Litvak M E, Brunsell N A, Peters W, van der Laan-Luijkx I T. 2016. Warm spring reduced carbon cycle impact of the 2012 US summer drought. Proc Natl Acad Sci USA, 113: 5880–5885
Xiao J F, Zhuang Q L, Liang E Y, McGuire A D, Moody A, Kicklighter D W, Shao X M, Melillo J M. 2009. Twentieth-century droughts and their impacts on terrestrial carbon cycling in China. Earth Interact, 13: 1–31
Xu L A, Samanta A, Costa M H, Ganguly S, Nemani R R, Myneni R B. 2011. Widespread decline in greenness of Amazonian vegetation due to the 2010 drought. Geophys Res Lett, 38: L07402
Xu X, Piao S, Wang X, Chen A, Ciais P, Myneni R B. 2012. Spatiotemporal patterns of the area experiencing negative vegetation growth anomalies in China over the last three decades. Environ Res Lett, 7: 035701
Yi C X, Rustic G, Xu X Y, Wang J X, Dookie A, Wei S H, Hendrey G, Ricciuto D, Meyers T, Nagy Z, Pinter K. 2012. Climate extremes and grassland potential productivity. Environ Res Lett, 7: 035703
Yue Y, Ni J R, Ciais P, Piao S L, Wang T, Huang M T, Borthwick A G L, Li T H, Wang Y C, Chappell A, Van O K. 2016. Lateral transport ofsoil carbon and land-atmosphere CO2 flux induced by water erosion in China. Proc Natl Acad Sci USA, 113: 6617–6622
Zeglin L H, Bottomley P J, Jumpponen A, Rice C W, Arango M, Lindsley A, McGowan A, Mfombep P, Myrold D D. 2013. Altered precipitation regime affects the function and composition of soil microbial communities on multiple time scales. Ecology, 94: 2334–2345
Zeng N, Yoon J H, Marengo J A, Subramaniam A, Nobre C A, Mariotti A, Neelin J D. 2008. Causes and impacts of the 2005 Amazon drought. Environ Res Lett, 3: 014002
Zeppel M J B, Wilks J V, Lewis J D. 2014. Impacts of extreme precipitation and seasonal changes in precipitation on plants. Biogeosciences, 11: 3083–3093
Zhang L, Xiao J F, Li J, Wang K, Lei L P, Guo H D. 2012. The 2010 spring drought reduced primary productivity in southwestern China. Environ Res Lett, 7: 045706
Zhao M S, Running S W. 2010. Drought-induced reduction in global terrestrial net primary production from 2000 through 2009. Science, 329: 940–943
Zscheischler J, Mahecha M D, von Buttlar J, Harmeling S, Jung M, Rammig A, Randerson J T, Schölkopf B, Seneviratne S I, Tomelleri E, Zaehle S, Reichstein M. 2014a. A few extreme events dominate global interannual variability in gross primary production. Environ Res Lett, 9: 035001
Zscheischler J, Michalak A M, Schwalm C, Mahecha M D, Huntzinger D N, Reichstein M, Berthier G, Ciais P, Cook R B, El-Masri B, Huang M, Ito A, Jain A, King A, Lei H, Lu C, Mao J, Peng S, Poulter B, Ricciuto D, Shi X, Tao B, Tian H, Viovy N, Wang W, Wei Y, Yang J, Zeng N. 2014b. Impact of large-scale climate extremes on biospheric carbon fluxes: An intercomparison based on MsTMIP data. Glob Biogeochem Cycle, 28: 585–600
Acknowledgements
The authors wish to thank Prof. Zehao Shen, Prof. Tao Wang, Dr. Yongwen Liu, Xiangyi Li and Kai Wang for their contribution to the text. This work was supported by the National Natural Science Foundation of China (Grant No. 41530528).
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Piao, S., Zhang, X., Chen, A. et al. The impacts of climate extremes on the terrestrial carbon cycle: A review. Sci. China Earth Sci. 62, 1551–1563 (2019). https://doi.org/10.1007/s11430-018-9363-5
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DOI: https://doi.org/10.1007/s11430-018-9363-5