Advertisement

Plant Ecology

, Volume 216, Issue 4, pp 599–613 | Cite as

Grazing and watering alter plant phenological processes in a desert steppe community

  • Juanjuan Han
  • Jiquan Chen
  • Jianyang Xia
  • Linghao LiEmail author
Article

Abstract

Phenology is well recognized as one of the most sensitive indicators of environmental change. Previous studies have focused on flowering phenology with few efforts given to the phenological successes and vegetative processes. Additionally, grazing is often characterized as a driver for community evolutionary processes, while precipitation is known as the most important abiotic cue in arid regions. Given this knowledge, we installed a nested experiment in a desert steppe to explore the coupled effects of grazing and watering on plant species’ reproductive successes and phenological timing in 2012–2013. We found that grazing increased the proportion of non-flowering individuals, with a greater proportion in 2013 than that in 2012. It decreased species richness and changed the habitat preferences in both years, and watering also reduced the richness in both years. Grazing also delayed the phenological timing for some dominant species and significantly delayed the green-up timing (5.67 days) and shortened the growing season length (GSL) in both 2012 (7.74 days) and 2013 (4.71 days). The application of watering, however, delayed some dominant species’ timing—including the browning timing of five dominate species ranging from 9.57 days in 2013 to 1.93 days in 2012—but it did not delay the species’ green-up timing. This resulted in a significantly prolonged growing season in 2013 (8.58 days). The high soil water and optimal soil temperature in the spring of 2013 contributed to an earlier green-up time (6.1 days) than in 2012.

Keywords

Reproductive phenology Foliar damage Phenotypic plasticity Arid environment 

Notes

Acknowledgments

We thank Dr. Guodong Han for maintaining the herbivory platform for many years. We also thank the faculty of the field station for their generous help in experiment establishment and measurements, Dr. Wenping Yuan and Guofang Liu for the experimental design and statistical analyses, and Dr. Shiping Chen for her climatic data from the EC tower. We thank Lisa Delp Taylor and Gabriela Shirkey for proofreading and polishing the language of the manuscript. This study was partially supported by the Natural Science Foundation of China (31229001, 31130008), the IceMe of the NUIST, and the “Dynamics of Coupled Natural and Human Systems (CNH)” Program of the NSF (#1313761).

Supplementary material

11258_2015_462_MOESM1_ESM.eps (59 kb)
Supplementary material 1 (EPS 59 kb). Figure S1. Changes in the reproductive phases under the treatments of grazing (G) and watering (W) across the two studied years. Negative values (−) indicate the contracted reproductive phases and positive values (+) indicate extended reproductive phases
11258_2015_462_MOESM2_ESM.eps (4 mb)
Supplementary material 2 (EPS 4082 kb). Figure S2. The phenological shifts on green-up, reproductive, and browning phases of Stipa breviflora
11258_2015_462_MOESM3_ESM.doc (29 kb)
Supplementary material 3 (DOC 29 kb)

References

  1. Adams HD, Guardiola-Claramonte M, Barron-Gafford GA, Villegas JC, Breshears DD, Zou CB, Troch PA, Huxman TE (2009) Temperature sensitivity of drought-induced tree mortality portends increased regional die-off under global-change-type drought. Proc Natl Acad Sci USA 106:7063–7066CrossRefPubMedCentralPubMedGoogle Scholar
  2. Aldridge G, Inouye DW, Forrest JRK, Barr WA, Miller-Rushing AJ (2011) Emergence of a mid-season period of low floral resources in a montane meadow ecosystem associated with climate change. J Ecol 99:905–913CrossRefGoogle Scholar
  3. Baptist F, Choler P (2008) A simulation of the importance of length of growing season and canopy functional properties on the seasonal gross primary production of temperate alpine meadows. Ann Bot 101:549–559CrossRefPubMedCentralPubMedGoogle Scholar
  4. Botta A, Viovy N, Ciais P, Friedlingstein P, Monfray P (2000) A global prognostic scheme of leaf onset using satellite data. Glob Chang Biol 6:709–725CrossRefGoogle Scholar
  5. CaraDonna PJ, Iler AM, Inouye DW (2014) Shifts in flowering phenology reshape a subalpine plant community. Proc Natl Acad Sci USA 111:4916–4921CrossRefPubMedCentralPubMedGoogle Scholar
  6. Churkina G, Schimel D, Braswell BH, Xiao XM (2005) Spatial analysis of growing season length control over net ecosystem exchange. Glob Chang Biol 11:1777–1787CrossRefGoogle Scholar
  7. Cleland EE, Chiariello NR, Loarie SR, Mooney HA, Field CB (2006) Diverse responses of phenology to global changes in a grassland ecosystem. Proc Natl Acad Sci USA 103:13740–13744CrossRefPubMedCentralPubMedGoogle Scholar
  8. Crimmins TM, Crimmins MA, Bertelsen CD (2010) Complex responses to climate drivers in onset of spring flowering across a semi-arid elevation gradient. J Ecol 98:1042–1051CrossRefGoogle Scholar
  9. Delph LF, Johannsson MH, Stephenson AG (1997) How environmental factors affect pollen performance: ecological and evolutionary perspectives. Ecology 78:1632–1639CrossRefGoogle Scholar
  10. Donohue K (2005) Niche construction through phenological plasticity: life history dynamics and ecological consequences. New Phytol 166:83–92CrossRefPubMedGoogle Scholar
  11. Dorji T, Totland O, Moe SR, Hopping KA, Pan J, Klein JA (2013) Plant functional traits mediate reproductive phenology and success in response to experimental warming and snow addition in Tibet. Glob Chang Biol 19:459–472CrossRefPubMedGoogle Scholar
  12. Dunne JA, Harte J, Taylor KJ (2003) Subalpine meadow flowering phenology responses to climate change: integrating experimental and gradient methods. Ecol Monogr 73:69–86CrossRefGoogle Scholar
  13. Edenhofer O, Seyboth K (2013) Intergovernmental panel on climate change (IPCC). In: Shogren JF (ed) Encyclopedia of energy, natural resource, and environmental economics. Elsevier, Waltham, pp 48–56CrossRefGoogle Scholar
  14. Engelbrecht BMJ, Kursar TA, Tyree MT (2005) Drought effects on seedling survival in a tropical moist forest. Trees-Struct Func 19:312–321CrossRefGoogle Scholar
  15. Euskirchen ES, McGuire AD, Kicklighter DW, Zhuang Q, Clein JS, Dargaville RJ, Dye DG, Kimball JS, McDonald KC, Melillo JM, Romanovsky VE, Smith NV (2006) Importance of recent shifts in soil thermal dynamics on growing season length, productivity, and carbon sequestration in terrestrial high-latitude ecosystems. Glob Chang Biol 12:731–750CrossRefGoogle Scholar
  16. Fitter AH, Fitter RSR (2002) Rapid changes in flowering time in British plants. Science 296:1689–1691CrossRefPubMedGoogle Scholar
  17. Foley JA, DeFries R, Asner GP, Barford C, Bonan G, Carpenter SR, Chapin FS, Coe MT, Daily GC, Gibbs HK (2005) Global consequences of land use. Science 309:570–574CrossRefPubMedGoogle Scholar
  18. Forrest J, Miller-Rushing AJ (2010) Toward a synthetic understanding of the role of phenology in ecology and evolution. Philos Trans R Soc B-Biol Sci 365:3101–3112CrossRefGoogle Scholar
  19. Forrest JRK, Thomson JD (2011) An examination of synchrony between insect emergence and flowering in Rocky Mountain meadows. Ecol Monogr 81:469–491CrossRefGoogle Scholar
  20. Forrest J, Inouye DW, Thomson JD (2010) Flowering phenology in subalpine meadows: does climate variation influence community co-flowering patterns? Ecology 91:431–440CrossRefPubMedGoogle Scholar
  21. Ghazanfar SA (1997) The phenology of desert plants: a 3-year study in a gravel desert wadi in northern Oman. J Arid Environ 35:407–417CrossRefGoogle Scholar
  22. Gordo O, Jose Sanz J (2009) Long-term temporal changes of plant phenology in the Western Mediterranean. Glob Chang Biol 15:1930–1948CrossRefGoogle Scholar
  23. Gunarathne R, Perera GAD (2014) Climatic factors responsible for triggering phenological events in Manilkara hexandra (Roxb.) Dubard., a canopy tree in tropical semi-deciduous forest of Sri Lanka. Trop Ecol 55:63–73Google Scholar
  24. Hao L, Sun G, Liu Y, Gao Z, He J, Shi T, Wu B (2014) Effects of precipitation on grassland ecosystem restoration under grazing exclusion in Inner Mongolia, China. Landsc Ecol 1–17Google Scholar
  25. Hegland SJ, Nielsen A, Lazaro A, Bjerknes A-L, Totland O (2009) How does climate warming affect plant-pollinator interactions? Ecol Lett 12:184–195CrossRefPubMedGoogle Scholar
  26. Hendrix SD (1988) Herbivory and its impact on plant reproduction. Plant Reprod Ecol 246–263Google Scholar
  27. Hirsch AI, Little WS, Houghton RA, Scott NA, White JD (2004) The net carbon flux due to deforestation and forest re-growth in the Brazilian Amazon: analysis using a process-based model. Glob Chang Biol 10:908–924CrossRefGoogle Scholar
  28. Inouye DW (2008) Effects of climate change on phenology, frost damage, and floral abundance of montane wildflowers. Ecology 89:353–362CrossRefPubMedGoogle Scholar
  29. John R, Chen J, Lu N, Wilske B (2009) Land cover/land use change in semi-arid Inner Mongolia: 1992–2004. Environ Res Lett 4:045010CrossRefGoogle Scholar
  30. Johnson MTJ, Stinchcombe JR (2007) An emerging synthesis between community ecology and evolutionary biology. Trends Ecol Evol 22:250–257CrossRefPubMedGoogle Scholar
  31. Lehtilä K, Strauss SY (1999) Effects of foliar herbivory on male and female reproductive traits of wild radish, Raphanus raphanistrum. Ecology 80:116–124CrossRefGoogle Scholar
  32. Llorens L, Penuelas J (2005) Experimental evidence of future drier and warmer conditions affecting flowering of two co-occurring Mediterranean shrubs. Int J Plant Sci 166:235–245CrossRefGoogle Scholar
  33. Medina-Roldan E, Paz-Ferreiro J, Bardgett RD (2012) Grazing-induced effects on soil properties modify plant competitive interactions in semi-natural mountain grasslands. Oecologia 170:159–169CrossRefPubMedGoogle Scholar
  34. Menzel A (2002) Phenology: its importance to the global change community—an editorial comment. Clim Chang 54:379–385CrossRefGoogle Scholar
  35. Miller-Rushing AJ, Inouye DW (2009) Variation in the impact of climate change on flowering phenology and abundance: an examination of two pairs of closely related wildflower species. Am J Bot 96:1821–1829CrossRefPubMedGoogle Scholar
  36. Miller-Rushing AJ, Primack RB (2008) Global warming and flowering times in Thoreau’s Concord: a community perspective. Ecology 89:332–341CrossRefPubMedGoogle Scholar
  37. Miller-Rushing AJ, Inouye DW, Primack RB (2008) How well do first flowering dates measure plant responses to climate change? The effects of population size and sampling frequency. J Ecol 96:1289–1296CrossRefGoogle Scholar
  38. Miller-Rushing AJ, Hoye TT, Inouye DW, Post E (2010) The effects of phenological mismatches on demography. Philos Trans R Soc B-Biol Sci 365:3177–3186CrossRefGoogle Scholar
  39. Moulin S, Kergoat L, Viovy N, Dedieu G (1997) Global-scale assessment of vegetation phenology using NOAA/AVHRR satellite measurements. J Clim 10:1154–1170CrossRefGoogle Scholar
  40. Obrist D, Verburg PSJ, Young MH, Coleman JS, Schorran DE, Arnone JA (2003) Quantifying the effects of phenology on ecosystem evapotranspiration in planted grassland mesocosms using EcoCELL technology. Agric For Meteorol 118:173–183CrossRefGoogle Scholar
  41. Olff H, Ritchie ME (1998) Effects of herbivores on grassland plant diversity. Trends Ecol Evol 13:261–265CrossRefPubMedGoogle Scholar
  42. Penuelas J, Filella I (2001) Phenology—responses to a warming world. Science 294:793–795CrossRefPubMedGoogle Scholar
  43. Penuelas J, Filella I, Zhang XY, Llorens L, Ogaya R, Lloret F, Comas P, Estiarte M, Terradas J (2004) Complex spatiotemporal phenological shifts as a response to rainfall changes. New Phytol 161:837–846CrossRefGoogle Scholar
  44. Petraglia A, Tomaselli M, Mondoni A, Brancaleoni L, Carbognani M (2014) Effects of nitrogen and phosphorus supply on growth and flowering phenology of the snowbed forb Gnaphalium supinum L. Flora—Morphol Distrib Func Ecol Plants 209:271–278CrossRefGoogle Scholar
  45. Piao S, 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 Cycles 21: GB3018Google Scholar
  46. Poveda K, Steffan-Dewenter I, Scheu S, Tscharntke T (2003) Effects of below- and above-ground herbivores on plant growth, flower visitation and seed set. Oecologia 135:601–605CrossRefPubMedGoogle Scholar
  47. Price MV, Waser NM (1998) Effects of experimental warming on plant reproductive phenology in a subalpine meadow. Ecology 79:1261–1271CrossRefGoogle Scholar
  48. Prieto P, Peñuelas J, Ogaya R, Estiarte M (2008) Precipitation-dependent flowering of Globularia alypum and Erica multiflora in Mediterranean shrubland under experimental drought and warming, and its inter-annual variability. Ann Bot 102:275–285CrossRefPubMedCentralPubMedGoogle Scholar
  49. Primack RB, Miller-Rushing AJ (2011) Broadening the study of phenology and climate change. New Phytol 191:307–309CrossRefPubMedGoogle Scholar
  50. Quesada M, Bollman K, Stephenson AG (1995) Leaf damage decreases pollen production and hinders pollen performance in Cucurbita texana. Ecology 76:437–443CrossRefGoogle Scholar
  51. Randerson JT, Field CB, Fung IY, Tans PP (1999) Increases in early season ecosystem uptake explain recent changes in the seasonal cycle of atmospheric CO2 at high northern latitudes. Geophys Res Lett 26:2765–2768CrossRefGoogle Scholar
  52. Richardson AD, Hollinger DY, Dail DB, Lee JT, Munger JW, O’Keefe J (2009) Influence of spring phenology on seasonal and annual carbon balance in two contrasting New England forests. Tree Physiol 29:321–331CrossRefPubMedGoogle Scholar
  53. Root TL, MacMynowski DP, Mastrandrea MD, Schneider SH (2005) Human-modified temperatures induce species changes: joint attribution. Proc Natl Acad Sci USA 102:7465–7469CrossRefPubMedCentralPubMedGoogle Scholar
  54. Rosenzweig C (2007) Assessment of observed changes and responses in natural and managed systems. Cambridge University Press, CambridgeGoogle Scholar
  55. Schwinning S, Sala OE (2004) Hierarchy of responses to resource pulses in arid and semi-arid ecosystems. Oecologia 141:211–220CrossRefPubMedGoogle Scholar
  56. Shao C, Chen J, Li L (2013) Grazing alters the biophysical regulation of carbon fluxes in a desert steppe. Environ Res Lett 8:025012CrossRefGoogle Scholar
  57. Shen M, Tang Y, Chen J, Zhu X, Zheng Y (2011) Influences of temperature and precipitation before the growing season on spring phenology in grasslands of the central and eastern Qinghai-Tibetan Plateau. Agric For Meteorol 151:1711–1722CrossRefGoogle Scholar
  58. Sherry RA, Zhou X, Gu S, Arnone JA, Schimel DS, Verburg PS, Wallace LL, Luo Y (2007) Divergence of reproductive phenology under climate warming. Proc Natl Acad Sci USA 104:198CrossRefPubMedCentralPubMedGoogle Scholar
  59. Shi T, Liu Y, Zhang L, Hao L, Gao Z (2014) Burning in agricultural landscapes: an emerging natural and human issue in China. Landsc Ecol 29:1785–1798CrossRefGoogle Scholar
  60. Silveira AP, Martins FR, Araujo FS (2013) Do vegetative and reproductive phenophases of deciduous tropical species respond similarly to rainfall pulses? J For Res 24:643–651CrossRefGoogle Scholar
  61. Suzuki R, Nomaki T, Yasunari T (2003) West-east contrast of phenology and climate in northern Asia revealed using a remotely sensed vegetation index. Int J Biometeorol 47:126–138PubMedGoogle Scholar
  62. Tucker CJ, Slayback DA, Pinzon JE, Los SO, Myneni RB, Taylor MG (2001) Higher northern latitude normalized difference vegetation index and growing season trends from 1982 to 1999. Int J Biometeorol 45:184–190CrossRefPubMedGoogle Scholar
  63. Wang D, Heckathorn SA, Barua D, Joshi P, Hamilton EW, LaCroix JJ (2008) Effects of elevated CO2 on the tolerance of photosynthesis to acute heat stress in C3, C4, and CAM species. Am J Bot 95:165–176CrossRefPubMedGoogle Scholar
  64. Wang J, Brown DG, Chen J (2013) Drivers of the dynamics in net primary productivity across ecological zones on the Mongolian Plateau. Landsc Ecol 28:725–739CrossRefGoogle Scholar
  65. Wang S, Wang C, Duan J, Zhu X, Xu G, Luo C, Zhang Z, Meng F, Li Y, Du M (2014) Timing and duration of phenological sequences of alpine plants along an elevation gradient on the Tibetan plateau. Agric For Meteorol 189:220–228CrossRefGoogle Scholar
  66. Woodcock BA, Pywell RF (2010) Effects of vegetation structure and floristic diversity on detritivore, herbivore and predatory invertebrates within calcareous grasslands. Biodivers Conserv 19:81–95CrossRefGoogle Scholar
  67. Wu C, Gonsamo A, Chen JM, Kurz WA, Price DT, Lafleur PM, Jassal RS, Dragoni D, Bohrer G, Gough CM, Verma SB, Suyker AE, Munger JW (2012) Interannual and spatial impacts of phenological transitions, growing season length, and spring and autumn temperatures on carbon sequestration: a North America flux data synthesis. Glob Planet Chang 92–93:179–190CrossRefGoogle Scholar
  68. Xia J, Wan S (2012) The effects of warming-shifted plant phenology on ecosystem carbon exchange are regulated by precipitation in a semi-arid grassland. PLoS One 7:e32088CrossRefPubMedCentralPubMedGoogle Scholar
  69. Xia J, Wan S (2013) Independent effects of warming and nitrogen addition on plant phenology in the Inner Mongolian steppe. Ann Bot 111:1207–1217CrossRefPubMedCentralPubMedGoogle Scholar
  70. Xia J, Luo Y, Niu S, Ciais P, Janssens I, Chen J, Ammann C, Blanken P, Cescatti A, Bonal D, Buchmann N, Curtis P, Chen S, Dong J, Flanagan L, Frankenberg C, Georgiadis T, Gough C (2015) Joint control of terrestrial ecosystem productivity by plant phenology and physiology. Proc Natl Acad Sci USA (In press)Google Scholar
  71. Yin XY, Goudriaan J, Lantinga EA, Vos J, Spiertz HJ (2003) A flexible sigmoid function of determinate growth. Ann Bot 91:361–371CrossRefPubMedCentralPubMedGoogle Scholar
  72. Yu H, Luedeling E, Xu J (2010) Winter and spring warming result in delayed spring phenology on the Tibetan Plateau. Proc Natl Acad Sci USA 107:22151–22156CrossRefPubMedCentralPubMedGoogle Scholar
  73. Yuan W, Zhou G, Wang Y, Han X (2007) Simulating phenological characteristics of two dominant grass species in a semi-arid steppe ecosystem. Ecol Res 22:784–791CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Juanjuan Han
    • 1
    • 2
  • Jiquan Chen
    • 1
    • 3
  • Jianyang Xia
    • 4
  • Linghao Li
    • 2
    Email author
  1. 1.International Center for Ecology, Meteorology, and Environment (IceMe)Nanjing University of Information Science and Technology (NUIST)NanjingChina
  2. 2.Key Laboratory of Vegetation and Environmental Change, Institute of BotanyChinese Academy of SciencesBeijingChina
  3. 3.CGCEO/GeographyMichigan State UniversityEast LansingUSA
  4. 4.Department of Microbiology and Plant BiologyUniversity of OklahomaNormanUSA

Personalised recommendations