Review of drought impacts on carbon cycling in grassland ecosystems

Abstract

Grasslands play a key role in both carbon and water cycles. In semi-arid and arid grassland areas, the frequency and intensity of droughts are increasing. However, the influence of a drought on grassland carbon cycling is still unclear. In this paper, the relationship between drought and grassland carbon cycling is described from the perspective of drought intensity, frequency, duration, and timing. Based on a large amount of literature, we determined that drought is one of the most prominent threats to grassland carbon cycling, although the impacts of different drought conditions are uncertain. The effects of a drought on grassland carbon cycling are more or less altered by drought-induced disturbances, whether individually or in combination. Additionally, a new conceptual model is proposed to better explain the mechanism of droughts on grassland carbon cycling. At present, evaluations of the effects of droughts on grassland carbon cycling are mainly qualitative. A data fusion model is indispensable for evaluating the fate of carbon cycling in a sustainable grassland system facing global change. In the future, multi-source data and models, based on the development of single and multiple disturbance experiments at the ecosystem level, can be utilized to systematically evaluate drought impacts on grassland carbon cycling at different timescales. Furthermore, more advanced models should be developed to address extreme drought events and their consequences on energy, water, and carbon cycling.

Key words： drought; carbon cycling; grasslands; conceptual model; interactive mechanisms; data fusion

Acknowledgments

This research was supported by National Natural Science Foundation of China (Grant Nos. 41601569 and 51779269), National Key R&D Program of China (Nos. 2017YFC1502404 and 2017YFB0503005), and IWHR Research & Development Support Program (No. JZ0145B-612016). Thanks to Barbara Ryan for the language polishing and modification of this manuscript.

References

1 Acharya B S, Rasmussen J, Eriksen J (2012). Grassland carbon sequestration and emissions following cultivation in a mixed crop rotation. Agric Ecosyst Environ, 153(24): 33–39

2 Ali Z, Hussain I, Faisal M, Nazir M, Moemen M A, Hussain T, Shamsuddin S (2017). A novel multi-Scalar drought index for monitoring drought: the standardized precipitation temperature index. Water Resour Manage, 31(15): 4957–4969

3 Allaby M (2009). Grasslands. New York: Infobase Publishing

4 Amézquita M C, Murgueitio E, Ibrahim M, Ramírez B(2010). Carbon sequestration in pasture and silvopastoral systems compared with native forests in ecosystems of tropical America. Grassland carbon sequestration: management, policy and economics, 11: 153–161

5 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(6247): 528–532

PMID

6 Andresen L C, Domínguez M T, Reinsch S, Smith A R, Schmidt I K, Ambus P, Beier C, Boeckx P, Bol R, de Dato G, Emmett B A, Estiarte M, Garnett M H, Kröel-Dulay G, Mason S L, Nielsen C S, Peñuelas J, Tietema A (2018). Isotopic methods for non-destructive assessment of carbon dynamics in shrublands under longterm climate change manipulation. Methods Ecol Evol, 9(4): 866–880

7 Aseeva T A, Karacheva G S, Lomakina I V, Ruban Z S (2018). Forming the productivity of spring and winter wheat in the conditions of the middle priamurye region. Russ Agric Sci, 44(2): 113–117

8 Astiani D, Curran L M Burhanuddin, Taherzadeh M, Mujiman, Hatta M, Pamungkas W, Gusmayanti E (2018). Fire-driven biomass and peat carbon losses and post-fire soil CO₂ emission in a west kalimantan peatland forest. J Trop For Sci, 30(4): 570–575

9 Baldocchi D (2011). The grass response. Nature, 476(7359): 160–161

PMID

10 Balogh J, Fóti S, Pintér K, Burri S, Eugster W, Papp M, Nagy Z (2015). Soil CO₂ efflux and production rates as influenced by evapotranspiration in a dry grassland. Plant Soil, 388(1–2): 157–173

11 Battisti R, Sentelhas P C (2017). Improvement of soybean resilience to drought through deep root system in Brazil. Agron J, 109(4): 1612–1622

12 Bloor J M, Bardgett R D (2012). Stability of above-ground and below-ground processes to extreme drought in model grassland ecosystems: interactions with plant species diversity and soil nitrogen availability. Perspect Plant Ecol Evol Syst, 14(3): 193–204

13 Brookshire E N J, Weaver T (2015). Long-term decline in grassland productivity driven by increasing dryness. Nat Commun, 6(1): 1–7

PMID

14 Canarini A, Kiær L P, Dijkstra F A (2017). Soil carbon loss regulated by drought intensity and available substrate: a meta-analysis. Soil Biol Biochem, 112: 90–99

15 Caracciolo D, Istanbulluoglu E, Noto L V, Collins S L (2016). Mechanisms of shrub encroachment into northern chihuahuan desert grasslands and impacts of climate change investigated using a cellular automata model. Adv Water Resour, 91: 46–62

16 Carlsson M, Merten M, Kayser M, Isselstein J, Wrage-Mönnig N (2017). Drought stress resistance and resilience of permanent grasslands are shaped by functional group composition and N fertilization. Agric Ecosyst Environ, 236: 52–60

17 Chen D, Deng X, Jin G, Samie A, Li Z (2017). Land-use-change induced dynamics of carbon stocks of the terrestrial ecosystem in Pakistan. Phys Chem Earth Parts ABC, 101: 13–20

18 Chen G, Tian H, Zhang C, Liu M, Ren W, Zhu W, Chappelka A H, Prior S A, Lockaby G B (2012). Drought in the Southern United States over the 20th century: variability and its impacts on terrestrial ecosystem productivity and carbon storage. Clim Change, 114(2): 379–397

19 Cleland E E, Goodale U M (2019). Co-limitation by nitrogen and water constrains allocation response to drought in deciduous and evergreen shrubs in a semi-arid ecosystem. Plant Ecol, 220(2): 213–225

20 Conant R T (2010). Challenges and opportunities for carbon sequestration in grassland systems. In Integrated Crop Management; FAO: Rome, Italy, 1–67

21 Coupe M D, Stacey J, Cahill J F Jr (2009). Limited effects of above-and belowground insects on community structure and function in a species-rich grassland. J Veg Sci, 20(1): 121–129

22 Craine J M, Towne E, Tolleson D, Nippert J B (2013). Precipitation timing and grazer performance in a tallgrass prairie. Oikos, 122(2): 191–198

23 Cuny M A C, Gendry J, Hernández-Cumplido J, Benrey B (2018). Changes in plant growth and seed production in wild lima bean in response to herbivory are attenuated by parasitoids. Oecologia, 187(2): 447–457

PMID

24 Daly E, Oishi A C, Porporato A, Katul G G (2008). A stochastic model for daily subsurface CO₂ concentration and related soil respiration. Adv Water Resour, 31(7): 987–994

25 Dias M, Brüggemann W (2010). Limitations of photosynthesis in Phaseolus vulgaris under drought stress: gas exchange, chlorophyll fluorescence and Calvin cycle enzymes. Photosynthetica, 48(1): 96–102

26 Diez J M, D’Antonio C M, Dukes J S, Grosholz E D, Olden J D, Sorte C J, Blumenthal D M, Bradley B A, Early R, Ibáñez I, Jones S J, Lawler J J, Miller L P (2012). Will extreme climatic events facilitate biological invasions? Front Ecol Environ, 10(5): 249–257

27 Han D, Wang G, Liu T, Xue B L, Kuczera G, Xu X (2018). Hydroclimatic response of evapotranspiration partitioning to prolonged droughts in semiarid grassland. J Hydrol (Amst), 563: 766–777

28 Dubois M, Claeys H, Van den Broeck L, Inzé D (2017). Time of day determines Arabidopsis transcriptome and growth dynamics under mild drought. Plant Cell Environ, 40(2): 180–189

PMID

29 Dulamsuren C, Klinge M, Bat-Enerel B, Ariunbaatar T, Tuya D (2019). Effects of forest fragmentation on organic carbon pool densities in the Mongolian forest-steppe. For Ecol Manage, 433: 780–788

30 Eagle R A, Risi C, Mitchell J L, Eiler J M, Seibt U, Neelin J D, Li G, Tripati A K (2013). High regional climate sensitivity over continental China constrained by glacial-recent changes in temperature and the hydrological cycle. Proc Natl Acad Sci USA, 110(22): 8813–8818

PMID

31 Ebrahimi M, Sarikhani M R, Sinegani A A S, Ahmadi A, Keesstra S (2019). Estimating the soil respiration under different land uses using artificial neural network and linear regression models. Catena, 174: 371–382

32 Evans S E, Wallenstein M D (2012). Soil microbial community response to drying and rewetting stress: does historical precipitation regime matter? Biogeochemistry, 109(1–3): 101–116

33 Eze S, Palmer S M, Chapman P J (2018). Negative effects of climate change on upland grassland productivity and carbon fluxes are not attenuated by nitrogen status. Sci Total Environ, 637-638: 398–407

PMID

34 Falloon P, Jones C D, Ades M, Paul K (2011). Direct soil moisture controls of future global soil carbon changes: an important source of uncertainty. Global Biogeochem Cycles, 25(3): GB3010

35 Fauset S, Baker T R, Lewis S L, Feldpausch T R, Affum-Baffoe K, Foli E G, Hamer K C, Swaine M D (2012). Drought-induced shifts in the floristic and functional composition of tropical forests in Ghana. Ecol Lett, 15(10): 1120–1129

PMID

36 Ford C R, McGee J, Scandellari F, Hobbie E A, Mitchell R J (2012). Long-and short-term precipitation effects on soil CO₂ efflux and total belowground carbon allocation. Agric Meteorol, 156: 54–64

37 Franks P J, Drake P L, Froend R H (2007). Anisohydric but isohydrodynamic: seasonally constant plant water potential gradient explained by a stomatal control mechanism incorporating variable plant hydraulic conductance. Plant Cell Environ, 30(1): 19–30

PMID

38 Ganjurjav H, Hu G, Wan Y, Li Y, Danjiu L, Gao Q (2018). Different responses of ecosystem carbon exchange to warming in three types of alpine grassland on the central Qinghai-Tibetan Plateau. Ecol Evol, 8(3): 1507–1520

PMID

39 Gao Y, Xia J, Chen Y, Zhao Y, Kong Q, Lang Y (2017). Effects of extreme soil water stress on photosynthetic efficiency and water consumption characteristics of Tamarix chinensis in China’s Yellow River Delta. J For Res, 28(3): 491–501

40 Gidey E, Dikinya O, Sebego R, Segosebe E, Zenebe A (2018). Predictions of future meteorological drought hazard (~ 2070) under the representative concentration path (RCP) 4.5 climate change scenarios in raya, northern ethiopia. Model Earth Syst Environ, 4(2): 475–488

41 Green J K, Seneviratne S I, Berg A M, Findell K L, Hagemann S, Lawrence D M, Gentine P (2019). Large influence of soil moisture on long-term terrestrial carbon uptake. Nature, 565(7740): 476–479

PMID

42 Grimstead D N, Reynolds A C, Hudson A M, Akins N J, Betancourt J L (2016). Reduced population variance in strontium isotope ratios informs domesticated turkey use at Chaco Canyon, New Mmexico, USA. J Archaeol Method Theory, 23(1): 127–149

43 Guo L, Cheng J, Luedeling E, Koerner S E, He J S, Xu J, Gang C, Li W, Luo R, Peng C (2017). Critical climate periods for grassland productivity on China’s Loess Plateau. Agric Meteorol, 233: 101–109

44 Han D, Wang G, Liu T, Xue B L, Kuczera G, Xu X (2018). Hydroclimatic response of evapotranspiration partitioning to prolonged droughts in semiarid grassland. J Hydrol (Amst), 563: 766–777

45 Harde H (2017). Scrutinizing the carbon cycle and CO₂ residence time in the atmosphere. Global Planet Change, 152: 19–26

46 Harper C W, Blair J M, Fay P A, Knapp A K, Carlisle J D (2005). Increased rainfall variability and reduced rainfall amount decreases soil CO₂ flux in a grassland ecosystem. Glob Change Biol, 11(2): 322–334

47 He B, Liu J, Guo L, Wu X, Xie X, Zhang Y, Chen Z, Zhong Z, Chen Z (2018). Recovery of ecosystem carbon and energy fluxes from the 2003 drought in Europe and the 2012 drought in the United States. Geophys Res Lett, 45(10): 4879–4888

48 Heitschmidt R, Haferkamp M(2003). Ecological consequences of drought and grazing on grasslands of the Northern Great Plains. Book Chapter, 207–226

49 Heitschmidt R, Vermeire L (2006). Can abundant summer precipitation counter losses in herbage production caused by spring drought? Rangeland Ecol Manag, 59(4): 392–399

50 Heschel M S, Riginos C (2005). Mechanisms of selection for drought stress tolerance and avoidance in Impatiens capensis (Balsaminaceae). Am J Bot, 92(1): 37–44

PMID

51 Hofer D, Suter M, Haughey E, Finn J A, Hoekstra N J, Buchmann N, Lüscher A (2016). Yield of temperate forage grassland species is either largely resistant or resilient to experimental summer drought. J Appl Ecol, 53(4): 1023–1034

52 Hoover D L, Rogers B M (2016). Not all droughts are created equal: the impacts of interannual drought pattern and magnitude on grassland carbon cycling. Glob Change Biol, 22(5): 1809–1820

PMID

53 Hoover D L, Knapp A K, Smith M D (2017). Photosynthetic responses of a dominant C₄ grass to an experimental heat wave are mediated by soil moisture. Oecologia, 183(1): 303–313

PMID

54 Huang J, Zhai J, Jiang T, Wang Y, Li X, Wang R, Xiong M, Su B, Fischer T (2018). Analysis of future drought characteristics in china using the regional climate model cclm. Clim Dyn, 50(1–2): 507–525

55 Huang L, He B, Han L, Liu J, Wang H, Chen Z (2017). A global examination of the response of ecosystem water-use efficiency to drought based on MODIS data. Sci Total Environ, 601–602: 1097–1107

PMID

56 Hussain M, Grünwald T, Tenhunen J, Li Y, Mirzae H, Bernhofer C, Otieno D, Dinh N, Schmidt M, Wartinger M, Owen K (2011). Summer drought influence on CO₂ and water fluxes of extensively managed grassland in Germany. Agric Ecosyst Environ, 141(1–2): 67–76

57 Ingrisch J, Karlowsky S, Anadon-Rosell A, Hasibeder R, König A, Augusti A, Gleixner G, Bahn M (2018). Land use alters the drought responses of productivity and CO₂ fluxes in mountain grassland. Ecosystems (NY), 21(4): 689–703

PMID

58 Jaksic V, Kiely G, Albertson J, Oren R, Katul G, Leahy P, Byrne K A (2006). Net ecosystem exchange of grassland in contrasting wet and dry years. Agric Meteorol, 139(3–4): 323–334

59 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(3): 689–702

60 Jeong Y W, Choi S K, Choi Y S, Kim S J (2015). Production of biocrude-oil from swine manure by fast pyrolysis and analysis of its characteristics. Renew Energy, 79: 14–19

61 Jia B, Wang Y, Xie Z (2018). Responses of the terrestrial carbon cycle to drought over china: modeling sensitivities of the interactive nitrogen and dynamic vegetation. Ecol Modell, 368: 52–68

62 Jia H, Zhang Y, Tian S, Emon R M, Yang X, Yan H, Wu T, Lu W, Siddique K H M, Han T (2017). Reserving winter snow for the relief of spring drought by film mulching in northeast China. Field Crops Res, 209: 58–64

63 Jiang Y, Xu Z, Zhou G, Liu T (2016). Elevated CO₂ can modify the response to a water status gradient in a steppe grass: from cell organelles to photosynthetic capacity to plant growth. BMC Plant Biol, 16(1): 157–173

PMID

64 Jongen M, Pereira J S, Aires L M I, Pio C A (2011). The effects of drought and timing of precipitation on the inter-annual variation in ecosystem-atmosphere exchange in a Mediterranean grassland. Agric Meteorol, 151(5): 595–606

65 Joos O, Hagedorn F, Heim A, Gilgen A, Schmidt M, Siegwolf R, Buchmann N (2010). Summer drought reduces total and litter-derived soil CO₂ effluxes intemperate grassland-clues from a ¹³C litter addition experiment. Biogeosciences, 7(3): 1031–1041

66 Kallenbach C M, Conant R T, Calderón F, Wallenstein M D (2019). A novel soil amendment for enhancing soil moisture retention and soil carbon in drought-prone soils. Geoderma, 337: 256–265

67 Kardol P, Cregger M A, Campany C E, Classen A T (2010). Soil ecosystem functioning under climate change: plant species and community effects. Ecology, 91(3): 767–781

PMID

68 Karlowsky S, Augusti A, Ingrisch J, Hasibeder R, Lange M, Lavorel S, Bahn M, Gleixner G (2018). Land use in mountain grasslands alters drought response and recovery of carbon allocation and plant-microbial interactions. J Ecol, 106(3): 1230–1243

PMID

69 Khalifa M, Elagib N A, Ribbe L, Schneider K (2018). Spatio-temporal variations in climate, primary productivity and efficiency of water and carbon use of the land cover types in Sudan and Ethiopia. Sci Total Environ, 624: 790–806

PMID

70 Kim D, Lee M I, Seo E (2019). Improvement of soil respiration parameterization in a dynamic global vegetation model and its impact on the simulation of terrestrial carbon fluxes. J Clim, 32(1): 127–143

71 Kipling R P, Virkajärvi P, Breitsameter L, Curnel Y, De Swaef T, Gustavsson A M, Hennart S, Höglind M, Järvenranta K, Minet J, Nendel C, Persson T, Picon-Cochard C, Rolinski S, Sandars D L, Scollan N D, Sebek L, Seddaiu G, Topp C F E, Twardy S, Van Middelkoop J, Wu L, Bellocchi G (2016). Key challenges and priorities for modelling European grasslands under climate change. Sci Total Environ, 566–567: 851–864

PMID

72 Knapp A K, Beier C, Briske D D, Classen A T, 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(9): 811–821

73 Kukumägi M, Ostonen I, Uri V, Helmisaari H S, Kanal A, Kull O, Lõhmus K (2017). Variation of soil respiration and its components in hemiboreal Norway spruce stands of different ages. Plant Soil, 414(1–2): 265–280

74 Kwon H, Pendall E, Ewers B E, Cleary M, Naithani K (2008). Spring drought regulates summer net ecosystem CO₂ exchange in a sagebrush-steppe ecosystem. Agric Meteorol, 148(3): 381–391

75 Larionov G A, Bushueva O G, Dobrovol’Skaya N G, Kiryukhina Z P, Litvin L F, Krasnov S F (2016). Assessing the contribution of nonhydraulic forces to the destruction of bonds between soil particles during water erosion. Eurasian Soil Sci, 49(5): 546–550

76 Lei T, Pang Z, Wang X, Li L, Fu J, Kan G, Zhang X, Ding L, Li J, Huang S, Shao C (2016). Drought and carbon cycling of grassland ecosystems under global change: a review. Water, 8(10): 460

77 Lei T, Wu J, Li X, Geng G, Shao C, Zhou H, Wang Q, Liu L (2015). A new framework for evaluating the impacts of drought on net primary productivity of grassland. Sci Total Environ, 536: 161–172

PMID

78 Li M, Dong Y, Qi Y C, Geng Y B (2004). Impact of extreme drought on the fluxes of CO₂, CH₄, N₂O from temperate steppe ecosystems. Resour Sci, 26(3): 89–95

79 Li Y, Liu Y, Harris P, Sint H, Murray P J, Lee M R F, Wu L (2017). Assessment of soil water, carbon and nitrogen cycling in reseeded grassland on the North Wyke Farm Platform using a process-based model. Sci Total Environ, 603-604: 27–37

PMID

80 Li L, Fan W, Kang X, Wang Y, Cui X, Xu C, Griffin K, Hao Y (2016). Responses of greenhouse gas fluxes to climate extremes in a semiarid grassland. Atmos Environ, 142: 32–42

81 Li P, Zhang L, Yu G, Liu C, Ren X, He H, Liu M, Wang H, Zhu J, Ge R, Zeng N (2018). Interactive effects of seasonal drought and nitrogen deposition on carbon fluxes in a subtropical evergreen coniferous forest in the East Asian monsoon region. Agric Meteorol, 263: 90–99

82 Li Y, Chen L, Wen H, Zhou T, Zhang T, Gao X (2014). 454 pyrosequencing analysis of bacterial diversity revealed by a comparative study of soils from mining subsidence and reclamation areas. J Microbiol Biotechnol, 24(3): 313–323

PMID

83 Liu Y, Li J, Jin Y, Zhang Y, Sha L, Grace J, Song Q, Zhou W, Chen A, Li P, Zhang S (2018). The influence of drought strength on soil respiration in a woody savanna ecosystem, southwest China. Plant Soil, 428(1–2): 321–333

84 Liu Y, Yang Y, Wang Q, Du X, Li J, Gang C, Zhou W, Wang Z (2019). Evaluating the responses of net primary productivity and carbon use efficiency of global grassland to climate variability along an aridity gradient. Sci Total Environ, 652: 671–682

PMID

85 Longo M, Knox R G, Levine N M, Alves L F, Bonal D, Camargo P B, Fitzjarrald D R, Hayek M N, Restrepo-Coupe N, Saleska S R, da Silva R, Stark S C, Tapajós R P, Wiedemann K T, Zhang K, Wofsy S C, Moorcroft P R (2018). Ecosystem heterogeneity and diversity mitigate Amazon forest resilience to frequent extreme droughts. New Phytol, 219(3): 914–931

PMID

86 Louhaichi M, Tastad A (2010). The Syrian steppe: past trends, current status, and future priorities. Rangelands, 32(2): 2–7

87 Luo Y, Zhou X (2010). Soil Respiration and the Environment. Norman:Academic Press, 3–133

88 Ma Q, Zhang J, Wang R, Ha S, Zhu M, Li D (2016). System design of loss fast evaluation for grassland drought disaster based on RS, GIS and GPS. In: 7th Annual Meeting of Risk Analysis Council of China Association for Disaster Prevention (RAC-2016). Changsha: Springer, 759–763

89 Malone S L, Tulbure M G, Pérez-Luque A J, Assal T J, Bremer L L, Drucker D P, Hillis V, Varela S, Goulden M L (2016). Drought resistance across California ecosystems: evaluating changes in carbon dynamics using satellite imagery. Ecosphere, 7(11): e01561

90 Manzoni S, Schaeffer S M, Katul G, Porporato A, Schimel J P (2014). A theoretical analysis of microbial eco-physiological and diffusion limitations to carbon cycling in drying soils. Soil Biol Biochem, 73: 69–83

91 Manzoni S, Taylor P, Richter A, Porporato A, Ågren G I (2012). Environmental and stoichiometric controls on microbial carbon-use efficiency in soils. New Phytol, 196(1): 79–91

PMID

92 Martí-Roura M, Casals P, Romanyà J (2011). Temporal changes in soil organic C under Mediterranean shrublands and grasslands: impact of fire and drought. Plant Soil, 338(1–2): 289–300

93 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(4): 719–739

PMID

94 Miranda A, Miranda H, Lloyd J, Grace J, Francey R, McIntyre J, Meir P, Riggan P, Lockwood R, Brass J (1997). Fluxes of carbon, water and energy over Brazilian cerrado: an analysis using eddy covariance and stable isotopes. Plant Cell Environ, 20(3): 315–328

95 Mirzaei H, Kreyling J, Zaman Hussain M, Li Y, Tenhunen J, Beierkuhnlein C, Jentsch A (2008). A single drought event of 100-year recurrence enhances subsequent carbon uptake and changes carbon allocation in experimental grassland communities. J Plant Nutr Soil Sci, 171(5): 681–689

96 Mishra A K, Singh V P (2011). Drought modeling—a review. J Hydrol (Amst), 403(1–2): 157–175

97 Mueller B, Seneviratne S I (2012). Hot days induced by precipitation deficits at the global scale. Proc Natl Acad Sci USA, 109(31): 12398–12403

PMID

98 Neely C, Bunning S, Wilkes A (2009). Review of evidence on drylands pastoral systems and climate change: implications and opportunities for mitigation and adaptation. In: Land Tenure and Management Unit (NRLA), FAO. Rome: 1–50

99 Niboyet A, Bardoux G, Barot S, Bloor J M (2017). Elevated CO₂ mediates the short-term drought recovery of ecosystem function in low-diversity grassland systems. Plant Soil, 420(1–2): 289–302

100 Nogueira C, Bugalho M N, Pereira J S, Caldeira M C (2017). Extended autumn drought, but not nitrogen deposition, affects the diversity and productivity of a mediterranean grassland. Environ Exp Bot, 138: 99–108

101 Nogueira C, Nunes A, Bugalho M N, Branquinho C, McCulley R L, Caldeira M C (2018). Nutrient addition and drought interact to change the structure and decrease the functional diversity of a Mediterranean grassland. Front Ecol Evol, 6: 155

102 Nogueira C, Werner C, Rodrigues A, Caldeira M C (2019). A prolonged dry season and nitrogen deposition interactively affect CO₂ fluxes in an annual Mediterranean grassland. Sci Total Environ, 654: 978–986

PMID

103 Nowak R S (2017). Average is best. Nat Clim Chang, 7(2): 101–102

104 Obermeier W A, Lehnert L W, Kammann C I, Müller C, Grünhage L, Luterbacher J, Erbs M, Moser G, Seibert R, Yuan N, Bendix J (2017). Reduced CO₂ fertilization effect in temperate C3 grasslands under more extreme weather conditions. Nat Clim Chang, 7(2): 137–141

105 Ochoa-Hueso R, Collins S L, Delgado-Baquerizo M, Hamonts K, Pockman W T, Sinsabaugh R L, Smith M D, Knapp A K, Power S A (2018). Drought consistently alters the composition of soil fungal and bacterial communities in grasslands from two continents. Glob Change Biol, 24(7): 2818–2827

PMID

106 Padgham J, Jabbour J, Dietrich K (2015). Managing change and building resilience: a multi-stressor analysis of urban and peri-urban agriculture in africa and asia. Urban Climate, 12: 183–204

107 Peck M R, Kaina G S, Hazell R J, Isua B, Alok C, Paul L, Stewart A J (2017). Estimating carbon stock in lowland Papua New Guinean forest: low density of large trees results in lower than global average carbon stock. Austral Ecol, 42(8): 964–975

108 Peng D, Zhang B, Wu C, Huete A R, Gonsamo A, Lei L, Ponce-Campos G E, Liu X, Wu Y (2017). Country-level net primary production distribution and response to drought and land cover change. Sci Total Environ, 574: 65–77

PMID

109 Perveen N, Barot S, Alvarez G, Klumpp K, Martin R, Rapaport A, Herfurth D, Louault F, Fontaine S (2014). Priming effect and microbial diversity in ecosystem functioning and response to global change: a modeling approach using the SYMPHONY model. Glob Change Biol, 20(4): 1174–1190

PMID

110 Valluru R, Davies W J, Reynolds M P, Dodd I C (2016). Foliar abscisic acid-to-ethylene accumulation and response regulate shoot growth sensitivity to mild drought in wheat. Front Plant Sci, 7: 461

PMID

111 Reichstein M, Bahn M, Ciais P, Frank D, Mahecha M D, Seneviratne S I, Zscheischler J, Beer C, Buchmann N, Frank D C, Papale D, Rammig A, Smith P, Thonicke K, van der Velde M, Vicca S, Walz A, Wattenbach M (2013). Climate extremes and the carbon cycle. Nature, 500(7462): 287–295

PMID

112 Riis T, Levi P S, Baattrup-Pedersen A, Jeppesen K G, Rosenhøj Leth S (2017). Experimental drought changes ecosystem structure and function in a macrophyte-rich stream. Aquat Sci, 79(4): 841–853

113 Roby M C, Salas Fernandez M G, Heaton E A, Miguez F E, Vanloocke A (2017). Biomass sorghum and maize have similar water-use-efficiency under non-drought conditions in the rain-fed midwest US. Agric Meteorol, 247: 434–444

114 Roy J, Picon-Cochard C, Augusti A, Benot M L, Thiery L, Darsonville O, Landais D, Piel C, Defossez M, Devidal S, Escape C, Ravel O, Fromin N, Volaire F, Milcu A, Bahn M, Soussana J F (2016). Elevated CO₂ maintains grassland net carbon uptake under a future heat and drought extreme. Proc Natl Acad Sci USA, 113(22): 6224–6229

PMID

115 Saladyga T, Hessl A, Nachin B, Pederson N (2013). Privatization, drought, and fire exclusion in the Tuul River watershed, Mongolia. Ecosystems (NY), 16(6): 1139–1151

116 Salehnia N, Alizadeh A, Sanaeinejad H, Bannayan M, Zarrin A, Hoogenboom G (2017). Estimation of meteorological drought indices based on agmerra precipitation data and station-observed precipitation data. J Arid Land, 9(6): 797–809

117 Sanaullah M, Chabbi A, Girardin C, Durand J L, Poirier M, Rumpel C (2014). Effects of drought and elevated temperature on biochemical composition of forage plants and their impact on carbon storage in grassland soil. Plant Soil, 374(1–2): 767–778

118 Sanaullah M, Chabbi A, Rumpel C, Kuzyakov Y (2012). Carbon allocation in grassland communities under drought stress followed by ¹⁴C pulse labeling. Soil Biol Biochem, 55: 132–139

119 Sándor R, Barcza Z, Acutis M, Doro L, Hidy D, Köchy M, Minet J, Lellei-Kovács E, Ma S, Perego A, Rolinski S, Ruget F, Sanna M, Seddaiu G, Wu L, Bellocchi G (2017). Multi-model simulation of soil temperature, soil water content and biomass in Euro-Mediterranean grasslands: uncertainties and ensemble performance. Eur J Agron, 88: 22–40

120 Sayer E J, Oliver A E, Fridley J D, Askew A P, Mills R T E, Grime J P (2017). Links between soil microbial communities and plant traits in a species-rich grassland under long-term climate change. Ecol Evol, 7(3): 855–862

PMID

121 Scasta J D, Thacker E T, Hovick T J, Engle D M, Allred B W, Fuhlendorf S D, Weir J R (2016). Patch-burn grazing (pbg) as a livestock management alternative for fire-prone ecosystems of north America. Renew Agric Food Syst, 31(6): 550–567

122 Schrama M, Bardgett R D (2016). Grassland invasibility varies with drought effects on soil functioning. J Ecol, 104(5): 1250–1258

123 Scott R L, Hamerlynck E P, Jenerette G D, Moran M S, Barron-Gafford G A(2010). Carbon dioxide exchange in a semidesert grassland through drought-induced vegetation change. J Geophys Res-Biogeo, (2005–2012): 115

124 Scott R L, Jenerette G D, Potts D L, Huxman T.E(2009). Effects of seasonal drought on net carbon dioxide exchange from a woody-plant-encroached semiarid grassland. J Geophys Res-Biogeo, (2005–2012): 114

125 Scurlock J, Hall D (1998). The global carbon sink: a grassland perspective. Glob Change Biol, 4(2): 229–233

126 Prudhomme C, Giuntoli I, Robinson E L, Clark D B, Arnell N W, Dankers R, Fekete B M, Franssen W, Gerten D, Gosling S N, Hagemann S, Hannah D M, Kim H, Masaki Y, Satoh Y, Stacke T, Wada Y, Wisser D (2014). Hydrological droughts in the 21st century, hotspots and uncertainties from a global multimodel ensemble experiment. Proc Natl Acad Sci USA, 111(9): 3262–3267

PMID

127 Shinoda M, Nachinshonhor G, Nemoto M (2010). Impact of drought on vegetation dynamics of the Mongolian steppe: a field experiment. J Arid Environ, 74(1): 63–69

128 Shrestha B, Maskey S, Babel M S, van Griensven A, Uhlenbrook S (2018). Sediment related impacts of climate change and reservoir development in the Lower Mekong River Basin: a case study of the Nam Ou basin, Lao PDR. Clim Change, 149(1): 13–27

129 Signarbieux C, Feller U (2012). Effects of an extended drought period on physiological properties of grassland species in the field. J Plant Res, 125(2): 251–261

PMID

130 Smith M D (2011). An ecological perspective on extreme climatic events: a synthetic definition and framework to guide future research. J Ecol, 99(3): 656–663

131 Song X, Wang Y, Lv X (2016). Responses of plant biomass, photosynthesis and lipid peroxidation to warming and precipitation change in two dominant species (Stipa grandis and Leymus chinensis) from North China Grasslands. Ecol Evol, 6(6): 1871–1882

PMID

132 Soussana J F, Soussana J F, Loiseau P, Vuichard N, Ceschia E, Balesdent J, Chevallier T, Arrouays D (2004). Carbon cycling and sequestration opportunities in temperate grasslands. Soil Use Manage, 20(2): 219–230

133 Sponseller R A (2007). Precipitation pulses and soil CO₂ flux in a Sonoran Desert ecosystem. Glob Change Biol, 13(2): 426–436

134 Stampfli A, Bloor J M G, Fischer M, Zeiter M (2018). High land-use intensity exacerbates shifts in grassland vegetation composition after severe experimental drought. Glob Change Biol, 24(5): 2021–2034

PMID

135 Su P, Lou J, Brookes P C, Luo Y, He Y, Xu J (2017). Taxon-specific responses of soil microbial communities to different soil priming effects induced by addition of plant residues and their biochars. J Soils Sediments, 17(3): 674–684

136 Suseela V, Conant R T, 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(1): 336–348

137 Tang L L, Cai X B, Gong W S, Lu J Z, Chen X L, Lei Q, Yu G L (2018). Increased vegetation greenness aggravates water conflicts during lasting and intensifying drought in the Poyang Lake Watershed, China. Forests, 9(1): 24

138 Tardieu F, Granier C, Muller B (2011). Water deficit and growth. Co-ordinating processes without an orchestrator? Curr Opin Plant Biol, 14(3): 283–289

PMID

139 Tessema Z K, de Boer W F, Prins H H T (2016). Changes in grass plant populations and temporal soil seed bank dynamics in a semi-arid African savanna: implications for restoration. J Environ Manage, 182: 166–175

PMID

140 Thiessen S, Gleixner G, Wutzler T, Reichstein M (2013). Both priming and temperature sensitivity of soil organic matter decomposition depend on microbial biomass–an incubation study. Soil Biol Biochem, 57: 739–748

141 Thomey M L, Ford P L, Reeves M C, Finch D M, Litvak M E, Collins S L (2014). Climate change impacts on future carbon stores and management of warm deserts of the United States. Rangelands, 36(1): 16–24

142 Thomson L J, Macfadyen S, Hoffmann A A (2010). Predicting the effects of climate change on natural enemies of agricultural pests. Biol Control, 52(3): 296–306

143 Thorpe J (2011). Vulnerability of Prairie Grasslands to Climate Change; No. 12855–2E11; Saskatchewan Research Council: Saskatoon

144 Tollerud H, Brown J, Loveland T, Mahmood R, Bliss N (2018). Drought and land-cover conditions in the great plains. Earth Interact, 22(17): 1–25

145 Trifilò P, Casolo V, Raimondo F, Petrussa E, Boscutti F, Lo Gullo M A, Nardini A (2017). Effects of prolonged drought on stem non-structural carbohydrates content and post-drought hydraulic recovery in Laurus Nobilis L.: the possible link between carbon starvation and hydraulic failure. Plant Physiol Biochem, 120: 232–241

PMID

146 Trzcinski M K, Srivastava D S, Corbara B, Dézerald O, Leroy C, Carrias J F, Dejean A, Céréghino R (2016). The effects of food web structure on ecosystem function exceeds those of precipitation. J Anim Ecol, 85(5): 1147–1160

PMID

147 Tubi A, Feitelson E (2019). Changing drought vulnerabilities of marginalized resource-dependent groups: a long-term perspective of Israel’s Negev Bedouin. Reg Environ Change, 19(2): 477–487

148 Urbanek E, Doerr S H (2017). CO₂ efflux from soils with seasonal water repellency. Biogeosciences, 14(20): 4781–4794

149 Valliere J M, Irvine I C, Santiago L, Allen E B (2017). High N, dry: experimental nitrogen deposition exacerbates native shrub loss and nonnative plant invasion during extreme drought. Glob Change Biol, 23(10): 4333–4345

PMID

150 van der Molen M K, Dolman A J, Ciais P, Eglin T, Gobron N, Law B E, Meir P, Peters W, Phillips O L, Reichstein M, Chen T, Dekker S C, Doubková M, Friedl M A, Jung M, van den Hurk B J J M, de Jeu R A M, Kruijt B, Ohta T, Rebel K T, Plummer S, Seneviratne S I, Sitch S, Teuling A J, van der Werf G R, Wang G (2011). Drought and ecosystem carbon cycling. Agric Meteorol, 151(7): 765–773

151 van Eekeren N, Bommelé L, Bloem J, Schouten T, Rutgers M, de Goede R, Reheul D, Brussaard L (2008). Soil biological quality after 36 years of ley-arable cropping, permanent grassland and permanent arable cropping. Appl Soil Ecol, 40(3): 432–446

152 Varga B, Vida G, Varga-László E, Hoffmann B, Veisz O (2017). Combined effect of drought stress and elevated atmospheric CO₂ concentration on the yield parameters and water use properties of winter wheat (triticum aestivum l.) genotypes. J Agron Crop Sci, 203(3): 192–205

153 Vargas J, Paneque P (2019). Challenges for the integration of water resource and drought-risk management in Spain. Sustainability, 11(2): 308

154 Wagena M B, Sommerlot A, Abiy A Z, Collick A S, Langan S, Fuka D R, Easton Z M (2016). Climate change in the Blue Nile Basin Ethiopia: implications for water resources and sediment transport. Clim Change, 139(2): 229–243

155 Waldrop M P, Holloway J M, Smith D B, Goldhaber M B, Drenovsky R E, Scow K M, Dick R, Howard D, Wylie B, Grace J B (2017). The interacting roles of climate, soils, and plant production on soil microbial communities at a continental scale. Ecology, 98(7): 1957–1967

PMID

156 Walter J, Nagy L, Hein R, Rascher U, Beierkuhnlein C, Willner E, Jentsch A (2011). Do plants remember drought? Hints towards a drought-memory in grasses. Environ Exp Bot, 71(1): 34–40

157 Wang J S, Kawa S R, Collatz G J, Sasakawa M, Gatti L V, Machida T, Liu Y, Manyin M (2018a). A global synthesis inversion analysis of recent variability in CO₂ fluxes using gosat and in situ observations. Atmos Chem Phys, 18(15): 11097–11124

158 Wang K, Shen C, Sun B, Wang X. N, Wei D, Liu L Y (2018a). Effects of drought stress on C, N and P stoichiometry of Ulmus pumila seedlings in Horqin sandy land, China. J of Appl Ecol, 29(7): 2286–2294

159 Wang Y, Hu C, Dong W, Li X, Zhang Y, Qin S, Oenema O (2015). Carbon budget of a winter-wheat and summer-maize rotation cropland in the North China Plain. Agric Ecosyst Environ, 206: 33–45

160 Wang Y, Hao Y, Cui X Y, Zhao H, Xu C, Zhou X, Xu Z (2014). Responses of soil respiration and its components to drought stress. J Soils Sediments, 14(1): 99–109

161 Wang Z, Ma Q, Wang J, Chen S, Fan Y, Deng L (2018b). Empirical study on agricultural drought adaptation of typical rainfed areas in Shidian County, China. Int J Disaster Risk Reduct, 28: 394–403

162 Weißhuhn K, Auge H, Prati D (2011). Geographic variation in the response to drought in nine grassland species. Basic Appl Ecol, 12(1): 21–28

163 Whitford W, Steinberger Y (2012). Effects of seasonal grazing, drought, fire, and carbon enrichment on soil microarthropods in a desert grassland. J Arid Environ, 83: 10–14

164 Williams N, Holland K (2007). The ecology and invasion history of hawkweeds (Hieracium species) in Australia. Plant Prot Q, 22(2): 76–80

165 Xiao L, Zhang Y, Li P, Xu G, Shi P, Zhang Y (2019). Effects of freeze-thaw cycles on aggregate-associated organic carbon and glomalin-related soil protein in natural-succession grassland and chinese pine forest on the loess plateau. Geoderma, 334: 1–8

166 Xu Z, Li Z, Liu H, Zhang X, Hao Q, Cui Y, Yang S, Liu M, Wang H, Gielen G, Song Z (2018). Soil organic carbon in particle-size fractions under three grassland types in Inner Mongolia, China. J Soils Sediments, 18(5): 1896–1905

167 Hao Y, Zhang H, Biederman J A, Li L, Cui X, Xue K, Du J, Wang Y (2018). Seasonal timing regulates extreme drought impacts on CO₂ and H₂O exchanges over semiarid steppes in Inner Mongolia, China. Agric Ecosyst Environ, 266: 153–166

168 Yang J, Tian H, Pan S, Chen G, Zhang B, Dangal S (2018). Amazon drought and forest response: largely reduced forest photosynthesis but slightly increased canopy greenness during the extreme drought of 2015/2016. Glob Change Biol, 24(5): 1919–1934

PMID

169 Yuhui W, Jiquan C, Guangsheng Z, Changliang S, Jun C, Yu W, Jianmin S (2018). Predominance of precipitation event controls ecosystem CO₂ exchange in an Inner Mongolian desert grassland, China. J Clean Prod, 197(1): 781–793

170 Yuste J C, Penuelas J, Estiarte M, Garcia-Mas J, Mattana S, Ogaya R, Pujol M, Sardans J (2011). Drought-resistant fungi control soil organic matter decomposition and its response to temperature. Glob Change Biol, 17(3): 1475–1486

171 Zaka S, Ahmed L Q, Escobar-Gutiérrez A J, Gastal F, Julier B, Louarn G (2017). How variable are non-linear developmental responses to temperature in two perennial forage species? Agric Meteorol, 232: 433–442

172 Zaka S, Frak E, Julier B, Gastal F, Louarn G (2016). Intraspecific variation in thermal acclimation of photosynthesis across a range of temperatures in a perennial crop. AoB Plants, 8

PMID

173 Zhang C, Zhang J, Zhang H, Zhao J, Wu Q, Zhao Z, Cai T (2015). Mechanisms for the relationships between water-use efficiency and carbon isotope composition and specific leaf area of maize (zea maysl.) under water stress. Plant Growth Regul, 77(2): 233–243

174 Zhao M, Running S W (2010). Drought-induced reduction in global terrestrial net primary production from 2000 through 2009. Science, 329(5994): 940–943

PMID

175 Zhong Y, Yan W, Zong Y, Shangguan Z (2016). Biotic and abiotic controls on the diel and seasonal variation in soil respiration and its components in a wheat field under long-term nitrogen fertilization. Field Crops Res, 199: 1–9

176 Zhou L, Wang S, Chi Y, Ju W, Huang K, Mickler R, Wang M, Yu Q (2018). Changes in the carbon and water fluxes of subtropical forest ecosystems in south-western China related to drought. Water, 10(7): 821–838

177 Zhou X, Sherry R A, An Y, Wallace L L, Luo Y (2006). Main and interactive effects of warming, clipping, and doubled precipitation on soil CO₂ efflux in a grassland ecosystem. Global Biogeochem Cycles, 20(1)

178 Zwicke M, Alessio G A, Thiery L, Falcimagne R, Baumont R, Rossignol N, Soussana J F, Picon-Cochard C (2013). Lasting effects of climate disturbance on perennial grassland above-ground biomass production under two cutting frequencies. Glob Change Biol, 19(11): 3435–3448

PMID