Advertisement

Oecologia

, Volume 191, Issue 3, pp 685–696 | Cite as

Drought sensitivity of aboveground productivity in Leymus chinensis meadow steppe depends on drought timing

  • Bo Meng
  • Baoku Shi
  • Shangzhi Zhong
  • Hua Chai
  • Shuixiu Li
  • Yunbo Wang
  • Hugh A. L. Henry
  • Jian-Ying MaEmail author
  • Wei SunEmail author
Global change ecology – original research
  • 147 Downloads

Abstract

There is limited understanding of the combined effects of discrete climate extremes and chronic environmental changes on ecosystem processes and functioning. We assessed the interactions of extreme drought timing (45 days, in spring or summer) and nitrogen (N) addition in a full factorial field experiment in a Leymus chinensis-dominated meadow steppe in northeast China. We evaluated the resistance and recovery of the grassland (calculated in terms of aboveground biomass) to these two drought events. The spring drought reduced aboveground biomass by 28% in the unfertilized plots and by 33% in the fertilized plots, and the effects persisted during the subsequent post-drought period within the same growing season; however, the summer drought had no significant influence on aboveground biomass. Although there were no significant interactive effects between drought timing and N addition, we observed a potential trend of N addition increasing the proportion of aboveground biomass suppressed by spring drought but not summer drought. Moreover, the drought resistance of the aboveground biomass was positively correlated with the response of the belowground biomass to drought. One year after the extreme drought events, the spring drought effects on aboveground and belowground biomass were negligible. Our results indicate that the drought sensitivity of productivity likely depends on the phenological and morphological traits of the single highly dominant species (Leymus chinensis) in this meadow steppe.

Keywords

Climate extremes Drought timing Nitrogen addition Aboveground biomass productivity Root–shoot ratio 

Notes

Acknowledgements

This study was supported by the National Key Basic Research Program of China (2015CB150800), National Natural Science Foundation of China (31570470, 41671207, 31700449), the Fundamental Research Funds for the Central Universities (2412018ZD010).

Author contribution statement

WS and BM designed the experiment. BM, HC and SL performed the field and laboratory work. BM analyzed the data. WS, BM and BS wrote the manuscript. HH, SZ, YW and JM provided valuable comments and suggestions on draft. HH improved English writing quality.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

442_2019_4506_MOESM1_ESM.docx (535 kb)
Supplementary material 1 (DOCX 535 kb)

References

  1. Ainsworth EA, Davey PA, Hymus GJ, Osborne CP, Rogers A, Blum H, NÖSberger J, Long SP (2003) Is stimulation of leaf photosynthesis by elevated carbon dioxide concentration maintained in the long term? A test with Lolium perenne grown for 10 years at two nitrogen fertilization levels under Free Air CO2 Enrichment (FACE). Plant Cell Environ 26:705–714.  https://doi.org/10.1046/j.1365-3040.2003.01007.x CrossRefGoogle Scholar
  2. Angert AL, Huxman TE, Chesson P, Venable DL (2009) Functional tradeoffs determine species coexistence via the storage effect. Proc Natl Acad Sci 106:11641–11645.  https://doi.org/10.1073/pnas.0904512106 CrossRefPubMedGoogle Scholar
  3. Bai Y (1997) A model of above-ground biomass of Aneurolepidium chinense community in response to seasonal precipitation. Acta Prataculturalence Sin 2:2–7 (in Chinese with English abstract) Google Scholar
  4. Bai Y, Wu J, Clark CM, Naeem S, Pan Q, Huang J, Zhang L, Guohan X (2010) Tradeoffs and thresholds in the effects of nitrogen addition on biodiversity and ecosystem functioning: evidence from inner Mongolia Grasslands. Glob Change Biol 16:358–372.  https://doi.org/10.1111/j.1365-2486.2009.01950.x CrossRefGoogle Scholar
  5. Beier C, Beierkuhnlein C, Wohlgemuth T, Penuelas J, Emmett BA, Korner C, De Boeck HJ, Christensen JH, Leuzinger S, Janssens IA (2012) Precipitation manipulation experiments: challenges and recommendations for the future. Ecol Lett 15:899–911.  https://doi.org/10.1111/j.1461-0248.2012.01793.x CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bobbink R, Hicks K, Galloway J, Spranger T, Alkemade R, Ashmore M, Bustamante M, Cinderby S, Davidson E, Dentener F, Emmett B, Erisman JW, Fenn M, Gilliam F, Nordin A, Pardo L, De Vries W (2010) Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis. Ecol Appl 20:30–59.  https://doi.org/10.1890/08-1140.1 CrossRefGoogle Scholar
  7. Borken W, Matzner E (2009) Reappraisal of drying and wetting effects on C and N mineralization and fluxes in soils. Glob Change Biol 15:808–824.  https://doi.org/10.1111/j.1365-2486.2008.01681.x CrossRefGoogle Scholar
  8. Burri S, Sturm P, Prechsl UE, Knohl A, Buchmann N (2013) The impact of extreme summer drought on the short-term carbon coupling of photosynthesis to soil CO2 efflux in a temperate grassland. Biogeosciences Discuss 10:961–975.  https://doi.org/10.5194/bg-11-961-2014 CrossRefGoogle Scholar
  9. Chaves MM, Maroco JP, Pereira JS (2003) Understanding plant responses to drought—from genes to the whole plant. Funct Plant Biol 30:239–264.  https://doi.org/10.1071/FP02076 CrossRefGoogle Scholar
  10. Chimner RA, Welker JM (2005) Ecosystem respiration responses to experimental manipulations of winter and summer precipitation in a Mixedgrass Prairie, WY, USA. Biogeochemistry 73:257–270.  https://doi.org/10.1007/s10533-004-1989-6 CrossRefGoogle Scholar
  11. Cohen D (1971) Maximizing final yield when growth is limited by time or by limiting resources. J Theor Biol 33:299–307.  https://doi.org/10.1016/0022-5193(71)90068-3 CrossRefPubMedGoogle Scholar
  12. Creese C, Oberbauer S, Rundel P, Sack L (2014) Are fern stomatal responses to different stimuli coordinated? Testing responses to light, vapor pressure deficit, and CO2 for diverse species grown under contrasting irradiances. New Phytol 204:92–104.  https://doi.org/10.1111/nph.12922 CrossRefPubMedGoogle Scholar
  13. Cui H, Wang Y, Jiang Q, Chen S, Ma J, Sun W (2015) Carbon isotope composition of nighttime leaf-respired CO2 in the agricultural-pastoral zone of the Songnen Plain, northeast China. PLoS One 10:e0137575.  https://doi.org/10.1371/journal.pone.0137575 CrossRefPubMedPubMedCentralGoogle Scholar
  14. De Boeck HJ, Dreesen FE, Janssens IA, Nijs I (2011) Whole-system responses of experimental plant communities to climate extremes imposed in different seasons. New Phytol 189:806–817.  https://doi.org/10.1111/j.1469-8137.2010.03515.x CrossRefPubMedGoogle Scholar
  15. DeAngelis DL, Bartell SM, Brenkert AL (1989) Effects of nutrient recycling and food-chain length on resilience. Am Nat 134:778–805.  https://doi.org/10.1086/285011 CrossRefGoogle Scholar
  16. Denton EM, Dietrich JD, Smith MD, Knapp AK (2016) Drought timing differentially affects above- and belowground productivity in a mesic grassland. Plant Ecol 218:1–12.  https://doi.org/10.1007/s11258-016-0690-x CrossRefGoogle Scholar
  17. Dietrich JD, Smith MD (2016) The effect of timing of growing season drought on flowering of a dominant C4 grass. Oecologia 181:391–399.  https://doi.org/10.1007/s00442-016-3579-4 CrossRefPubMedGoogle Scholar
  18. Dong G, Guo J, Chen J, Sun G, Gao S, Hu L, Wang Y (2011) Effects of spring drought on carbon sequestration, evapotranspiration and water use efficiency in the Songnen Meadow Steppe in northeast China. Ecohydrology 4:211–224.  https://doi.org/10.1002/eco.200 CrossRefGoogle Scholar
  19. Dreesen FE, De Boeck HJ, Janssens IA, Nijs I (2012) Summer heat and drought extremes trigger unexpected changes in productivity of a temperate annual/biannual plant community. Environ Exp Bot 79:21–30.  https://doi.org/10.1016/j.envexpbot.2012.01.005 CrossRefGoogle Scholar
  20. Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78:9–19CrossRefGoogle Scholar
  21. Gao Y, He N, Zhang X (2014) Effects of reactive nitrogen deposition on terrestrial and aquatic ecosystems. Ecol Eng 70:312–318.  https://doi.org/10.1016/j.ecoleng.2014.06.027 CrossRefGoogle Scholar
  22. Gaul D, Hertel D, Leuschner C (2008) Effects of experimental soil frost on the fine-root system of mature Norway spruce. J Plant Nutr Soil Sci 171:690–698.  https://doi.org/10.1002/jpln.200700284 CrossRefGoogle Scholar
  23. Gilgen AK, Buchmann N (2009) Response of temperate grasslands at different altitudes to simulated summer drought differed but scaled with annual precipitation. Biogeosciences 6:2525–2539.  https://doi.org/10.5194/bg-6-2525-2009 CrossRefGoogle Scholar
  24. Gleeson SK, Tilman D (1992) Plant allocation and the multiple limitation hypothesis. Am Nat 139:1322–1343.  https://doi.org/10.1086/285389 CrossRefGoogle Scholar
  25. Griffinnolan RJ, Carroll CJW, Denton EM, Johnston MK, Collins SL, Smith MD, Knapp AK (2018) Legacy effects of a regional drought on aboveground net primary production in six central US grasslands. Plant Ecol 219:505–515.  https://doi.org/10.1007/s11258-018-0813-7 CrossRefGoogle Scholar
  26. Harrison S, LaForgia M (2019) Seedling traits predict drought-induced mortality linked to diversity loss. Proc Natl Acad Sci 116:5576–5581.  https://doi.org/10.1073/pnas.1818543116 CrossRefPubMedGoogle Scholar
  27. Hasibeder R, Fuchslueger L, Richter A, Bahn M (2015) Summer drought alters carbon allocation to roots and root respiration in mountain grassland. New Phytol 205:1117–1127.  https://doi.org/10.1111/nph.13146 CrossRefPubMedGoogle Scholar
  28. He C, Liu X, Fangmeier A, Zhang F (2007) Quantifying the total airborne nitrogen input into agroecosystems in the North China Plain. Agr Ecosyst Environ 121:395–400.  https://doi.org/10.1016/j.agee.2006.12.016 CrossRefGoogle Scholar
  29. Heitschmidt RK, Vermeire LT (2006) Can abundant summer precipitation counter losses in herbage production caused by spring drought? Rangel Ecol Manag 59:392–399.  https://doi.org/10.2111/05-164R2.1 CrossRefGoogle Scholar
  30. Heitschmidt RK, Klement KD, Haferkamp MR (2005) Interactive effects of drought and grazing on northern great plains rangelands. Rangel Ecol Manag 58:11–19.  https://doi.org/10.2111/1551-5028(2005)58%3c11:IEODAG%3e2.0.CO;2 CrossRefGoogle Scholar
  31. Hodge A, Berta G, Doussan C, Merchan F, Crespi M (2009) Plant root growth, architecture and function. Plant Soil 321:153–187.  https://doi.org/10.1007/s11104-009-9929-9 CrossRefGoogle Scholar
  32. Hofer D, Suter M, Haughey E, Finn JA, Hoekstra NJ, Buchmann N, Lüscher A, Bennett J (2016) Yield of temperate forage grassland species is either largely resistant or resilient to experimental summer drought. J Appl Ecol 53:1023–1034.  https://doi.org/10.1111/1365-2664.12694 CrossRefGoogle Scholar
  33. Hoover DL, Duniway MC, Belnap J (2015) Pulse-drought atop press-drought: unexpected plant responses and implications for dryland ecosystems. Oecologia 179:1211–1221.  https://doi.org/10.1007/s00442-015-3414-3 CrossRefPubMedGoogle Scholar
  34. Hovenden MJ, Newton PCD, Wills KE (2014) Seasonal not annual rainfall determines grassland biomass response to carbon dioxide. Nature 511:583–586.  https://doi.org/10.1038/nature13281 CrossRefPubMedGoogle Scholar
  35. Jiao J, Grodzinski B (1996) The effect of leaf temperature and photorespiratory conditions on export of sugars during steady-state photosynthesis in Salvia splendens. Plant Physiol 111:169–178.  https://doi.org/10.1104/pp.111.1.169 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Kinugasa T, Tsunekawa A, Shinoda M (2012) Increasing nitrogen deposition enhances post-drought recovery of grassland productivity in the Mongolian steppe. Oecologia 170:857–865.  https://doi.org/10.1007/s00442-012-2354-4 CrossRefPubMedGoogle Scholar
  37. Knapp AK, Ciais P, Smith MD (2017) Reconciling inconsistencies in precipitation-productivity relationships: implications for climate change. New Phytol 214:41–47.  https://doi.org/10.1111/nph.14381 CrossRefPubMedGoogle Scholar
  38. Koevoets IT, Venema JH, Elzenga JTM, Testerink C (2016) Roots withstanding their environment: exploiting root system architecture responses to abiotic stress to improve crop tolerance. Front Plant Sci 7:1335.  https://doi.org/10.3389/fpls.2016.01335 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Kong Q, Ge Q, Zheng J, Xi J (2015) Prolonged dry episodes over northeast China during the period 1961–2012. Theoret Appl Climatol 122:711–719.  https://doi.org/10.1007/s00704-014-1320-y CrossRefGoogle Scholar
  40. LeBauer DS, Treseder KK (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89:371–379.  https://doi.org/10.1890/06-2057.1 CrossRefPubMedGoogle Scholar
  41. Lei Y, Duan A (2011) Prolonged dry episodes and drought over China. Int J Climatol 31:1831–1840.  https://doi.org/10.1002/joc.2197 CrossRefGoogle Scholar
  42. Li Q, Zhou D, Denton MD, Cong S (2019) Alfalfa monocultures promote soil organic carbon accumulation to a greater extent than perennial grass monocultures or grass-alfalfa mixtures. Ecol Eng 131:53–62.  https://doi.org/10.1016/j.ecoleng.2019.03.002 CrossRefGoogle Scholar
  43. Mironchenko A, Kozłowski J (2014) Optimal allocation patterns and optimal seed mass of a perennial plant. J Theor Biol 354:12–24.  https://doi.org/10.1016/j.jtbi.2014.03.023 CrossRefPubMedGoogle Scholar
  44. Monson RK, Jaeger CH (1991) Photosynthetic characteristics of C3-C4 intermediate Flaveria floridana (Asteraceae) in natural habitats: evidence of advantages to C3-C4 photosynthesis at high leaf temperatures. Am J Bot 78:795–800.  https://doi.org/10.1104/pp.71.4.944 CrossRefGoogle Scholar
  45. Monson RK, Littlejohn RO, Williams GJ (1983) Photosynthetic adaptation to temperature in four species from the Colorado shortgrass steppe: a physiological model for coexistence. Oecologia 58:43–51.  https://doi.org/10.1007/BF00384540 CrossRefPubMedGoogle Scholar
  46. Muller B, Pantin F, Genard M, Turc O, Freixes S, Piques M, Gibon Y (2011) Water deficits uncouple growth from photosynthesis, increase C content, and modify the relationships between C and growth in sink organs. J Exp Bot 62:1715–1729.  https://doi.org/10.1093/jxb/erq438 CrossRefPubMedGoogle Scholar
  47. Nilsen P (1990) Effect of nitrogen on drought resistance of Norway spruce and scots pine. Sci Total Environ 96:189–198.  https://doi.org/10.1016/0048-9697(90)90017-O CrossRefGoogle Scholar
  48. Oliver TH, Heard MS, Isaac NJB, Roy DB, Procter D, Eigenbrod F, Freckleton R, Hector A, Orme CDL, Petchey OL, Proença V, Raffaelli D, Suttle KB, Mace GM, Martín-López B, Woodcock BA, Bullock JM (2015) Biodiversity and resilience of ecosystem functions. Trends Ecol Evol 30:673–684.  https://doi.org/10.1016/j.tree.2015.08.009 CrossRefPubMedGoogle Scholar
  49. Pimm SL (1984) The complexity and stability of ecosystems. Nature 307:321–326.  https://doi.org/10.1038/307321a0 CrossRefGoogle Scholar
  50. Reynolds HL, D’Antonio C (1996) The ecological significance of plasticity in root weight ratio in response to nitrogen: opinion. Plant Soil 185:75–97.  https://doi.org/10.1007/BF02257566 CrossRefGoogle Scholar
  51. Schaffer WM, Inouye RS, Whittam TS (1982) Energy allocation by an annual plant when the effects of seasonality on growth and reproduction are decoupled. Am Nat 120:787–815.  https://doi.org/10.1086/284030 CrossRefGoogle Scholar
  52. Shi B, Wang Y, Meng B, Zhong S, Sun W (2018) Effects of nitrogen addition on the drought susceptibility of the Leymus chinensis meadow ecosystem vary with drought duration. Front Plant Sci 9:254.  https://doi.org/10.3389/fpls.2018.00254 CrossRefPubMedPubMedCentralGoogle Scholar
  53. Song MH, Yu FH (2015) Reduced compensatory effects explain the nitrogen-mediated reduction in stability of an alpine meadow on the Tibetan Plateau. New Phytol 207:70–77.  https://doi.org/10.1111/nph.13329 CrossRefPubMedGoogle Scholar
  54. Sun G, Wang Z, Xia Z-B, Zhang N, Wu N, Liu L, Lei Y (2016) Biotic and abiotic controls in determining exceedingly variable responses of ecosystem functions to extreme seasonal precipitation in a mesophytic alpine grassland. Agric For Meteorol 228–229:180–190.  https://doi.org/10.1016/j.agrformet.2016.07.010 CrossRefGoogle Scholar
  55. Swemmer AM, Knapp AK (2006) Growth responses of two dominant C4 grass species to altered water availability. Int J Plant Sci 167:1001–1010.  https://doi.org/10.1111/gcb.12888 CrossRefGoogle Scholar
  56. Tilman D (1996) Biodiversity: population versus ecosystem stability. Ecology 77:350–363.  https://doi.org/10.2307/2265614 CrossRefGoogle Scholar
  57. Tilman D, Reich PB, Knops JMH (2006) Biodiversity and ecosystem stability in a decade-long grassland experiment. Nature 441:629–632.  https://doi.org/10.1038/nature04742 CrossRefPubMedPubMedCentralGoogle Scholar
  58. Vogel A, Fester T, Eisenhauer N, Scherer-Lorenzen M, Schmid B, Weisser WW, Weigelt A (2013) Separating drought effects from roof artifacts on ecosystem processes in a grassland drought experiment. PLoS One 8:e70997.  https://doi.org/10.1371/journal.pone.0070997 CrossRefPubMedPubMedCentralGoogle Scholar
  59. Wagg C, Obrien MJ, Vogel A, Schererlorenzen M, Eisenhauer N, Schmid B, Weigelt A (2017) Plant diversity maintains long-term ecosystem productivity under frequent drought by increasing short-term variation. Ecology 98:2952–2961.  https://doi.org/10.1002/ecy.2003 CrossRefPubMedGoogle Scholar
  60. Wang Y, Yu S, Wang J (2007) Biomass-dependent susceptibility to drought in experimental grassland communities. Ecol Lett 10:401–410.  https://doi.org/10.1111/j.1461-0248.2007.01031.x CrossRefPubMedGoogle Scholar
  61. Wang Y, Jiang Q, Yang Z, Sun W, Wang D (2015) Effects of water and nitrogen addition on ecosystem carbon exchange in a meadow steppe. PLoS One 10:e0127695.  https://doi.org/10.1371/journal.pone.0127695 CrossRefPubMedPubMedCentralGoogle Scholar
  62. Wang Y, Meng B, Zhong S, Wang D, Ma J, Sun W (2018) Aboveground biomass and root/shoot ratio regulated drought susceptibility of ecosystem carbon exchange in a meadow steppe. Plant Soil 432:259–272.  https://doi.org/10.1007/s11104-018-3790-7 CrossRefGoogle Scholar
  63. Wiles LJ, Dunn G, Printz J, Patton B, Nyren A (2011) Spring precipitation as a predictor for peak standing crop of mixed-grass prairie. Rangel Ecol Manag 64:215–222.  https://doi.org/10.2111/REM-D-09-00024.1 CrossRefGoogle Scholar
  64. Winslow JC, Hunt ER, Piper SC (2003) The influence of seasonal water availability on global C3 versus C4 grassland biomass and its implications for climate change research. Ecol Model 163:153–173.  https://doi.org/10.1016/S0304-3800(02)00415-5 CrossRefGoogle Scholar
  65. Wopereis MCS, Kropff MJ, Maligaya AR, Tuong TP (1996) Drought-stress responses of two lowland rice cultivars to soil water status. Field Crop Res 46:21–39.  https://doi.org/10.1016/0378-4290(95)00084-4 CrossRefGoogle Scholar
  66. Wu X, Liu H, Li X, Ciais P, Babst F, Guo W, Zhang C, Magliulo V, Pavelka M, Liu S, Huang Y, Wang P, Shi C, Ma Y (2018) Differentiating drought legacy effects on vegetation growth over the temperate Northern Hemisphere. Glob Change Biol 24:504–516.  https://doi.org/10.1111/gcb.13920 CrossRefGoogle Scholar
  67. Xu Z, Ren H, Cai J, Wang R, Li MH, Wan S, Han X, Lewis BJ, Jiang Y (2014) Effects of experimentally-enhanced precipitation and nitrogen on resistance, recovery and resilience of a semi-arid grassland after drought. Oecologia 176:1187–1197.  https://doi.org/10.1007/s00442-014-3081-9 CrossRefPubMedGoogle Scholar
  68. Zeiter M, Schärrer S, Zweifel R, Newbery DM, Stampfli A (2016) Timing of extreme drought modifies reproductive output in semi-natural grassland. J Veg Sci 27:238–248.  https://doi.org/10.1111/jvs.12362 CrossRefGoogle Scholar
  69. Zelitch I (1992) Control of plant productivity by regulation of photorespiration. Bioscience 42:510–516.  https://doi.org/10.2307/1311881 CrossRefGoogle Scholar
  70. Zhong S, Chai H, Xu Y, Li Y, Ma JY, Sun W (2017) Drought sensitivity of the carbon isotope composition of leaf dark-respired CO2 in C3 (Leymus chinensis) and C4 (Chloris virgata and Hemarthria altissima) grasses in northeast China. Front Plant Sci 8:1996.  https://doi.org/10.3389/fpls.2017.01996 CrossRefPubMedPubMedCentralGoogle Scholar
  71. Zhou DW, Qiang LI, Song YT, Wang XZ (2011) Salinization-alkalization of Leymus chinensis grassland in Songnen Plain of northeast China. Chin J Appl Ecol 22:1423–1430.  https://doi.org/10.3724/SP.J.1011.2011.00353 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Bo Meng
    • 1
  • Baoku Shi
    • 1
  • Shangzhi Zhong
    • 1
  • Hua Chai
    • 1
  • Shuixiu Li
    • 1
  • Yunbo Wang
    • 1
    • 2
  • Hugh A. L. Henry
    • 3
  • Jian-Ying Ma
    • 4
    Email author
  • Wei Sun
    • 1
    Email author
  1. 1.Key Laboratory for Vegetation Ecology, Institute of Grassland ScienceNortheast Normal University, Ministry of EducationChangchunPeople’s Republic of China
  2. 2.Key Laboratory of Grassland Resources, College of Grassland, Resources and EnvironmentInner Mongolia Agricultural University, Ministry of EducationHohhotPeople’s Republic of China
  3. 3.Department of BiologyUniversity of Western OntarioLondonCanada
  4. 4.CAS Key Laboratory of Biogeography and Bioresource in Arid Land, Xinjiang Institute of Ecology and GeographyUrumqiPeople’s Republic of China

Personalised recommendations