The Khingan Mountain region, the most important and typical natural foci of tick-borne encephalitis (TBE) in China, is the largest and northernmost forest area and the one more sensitive to climate change. Taking this region as the study area, we investigated the spatio-temporal dynamics of deciduous broadleaf forest (DBF) and its phenology changes in relation to climate change and elevation. Based on MODIS Enhanced Vegetation Index (EVI) time series over the period of 2001 to 2009, the start-of-season (SOS), length-of-season (LOS) and another two vegetation variables (seasonal amplitude (SA) and integrated EVI (SI)) were derived. Over the past decade, the DBF in Khingan Mountains has generally degraded and over 65% of DBF has experienced negative SA and SI trends. Earlier trends in SOS and longer trends in LOS for DBF were observed, and these trends were mainly caused by climate warming. In addition, results from our analysis also indicated that the effects of temperature on DBF phenology were elevation dependent. The magnitude of advancement in SOS and extension in LOS with temperature increase significantly increased along a raising elevation gradient.
References
[1]
Hidalgo, P.J.; Galan, C.; Dominguez, E. Male phenology of three species of Cupressus: Correlation with airborne pollen. Trees-struct. Funct. 2003, 17, 336–344.
[2]
Estrella, N.; Menzel, A.; Kramer, U.; Behrendt, H. Integration of flowering dates in phenology and pollen counts in aerobiology: Analysis of their spatial and temporal coherence in Germany (1992-1999). Int. J. Biometeorol. 2006, 51, 49–59, doi:10.1007/s00484-006-0038-7.
[3]
Gao, J.; Liu, Y.S. De(re)forestation and climate warming in subarctic China. Appl. Geogr. 2012, 32, 281–290, doi:10.1016/j.apgeog.2011.04.002.
[4]
Grasso, M.; Manera, M.; Chiabai, A.; Markandya, A. The health effects of climate change: A survey of recent quantitative research. Int. J. Envrion. Res. Public Health 2012, 9, 1523–1547, doi:10.3390/ijerph9051523.
[5]
Huynen, M.M.T.E.; Martens, P.; Schram, D.; Weijenberg, M.P.; Kunst, A.E. The impact of heat waves and cold spells on mortality rates in the Dutch population. Environ. Health Persp. 2001, 109, 463–470, doi:10.1289/ehp.01109463.
[6]
Frei, T.; Gassner, E. Climate change and its impact on birch pollen quantities and the start of the pollen season an example from Switzerland for the period 1969-2006. Int. J. Biometeorol. 2008, 52, 667–674, doi:10.1007/s00484-008-0159-2.
[7]
Barrios, J.M.; Verstraeten, W.W.; Maes, P.; Clement, J.; Aerts, J.M.; Haredasht, S.A.; Wambacq, J.; Lagrou, K.; Ducoffre, G.; Van Ranst, M.; et al. Satellite derived forest phenology and its relation with Nephropathia Epidemica in Belgium. Int. J. Environ. Res. Public Health 2010, 7, 2486–2500, doi:10.3390/ijerph7062486.
[8]
Wang, X.; Piao, S.; Ciais, P.; Li, J.; Friedlingstein, P.; Koven, C.; Chen, A. Spring temperature change and its implication in the change of vegetation growth in North America from 1982 to 2006. PNAS 2011, 108, 1240–1245.
[9]
Piao, S.L.; Cui, M.D.; Chen, A.P.; Wang, X.H.; Ciais, P.; Liu, J.; Tang, Y.H. Altitude and temperature dependence of change in the spring vegetation green-up date from 1982 to 2006 in the Qinghai-Xizang Plateau. Agr. Forest. Meteorol. 2011, 151, 1599–1608, doi:10.1016/j.agrformet.2011.06.016.
[10]
Chen, X.Q.; Pan, W.F. Relationships among phenological growing season, time-integrated normalized difference vegetation index and climate forcing in the temperate region of eastern China. Int. J. Climatol. 2002, 22, 1781–1792, doi:10.1002/joc.823.
[11]
Avolio, E.; Orlandi, F.; Bellecci, C.; Fornaciari, M.; Federico, S. Assessment of the impact of climate change on the olive flowering in Calabria (southern Italy). Theor. Appl. Climatol. 2012, 107, 531–540, doi:10.1007/s00704-011-0500-2.
[12]
Zhou, L.M.; Tucker, C.J.; Kaufmann, R.K.; Slayback, D.; Shabanov, N.V.; Myneni, R.B. Variations in northern vegetation activity inferred from satellite data of vegetation index during 1981 to 1999. J. Geophys. Res. 2001, 106, 20069–20083.
[13]
Badeck, F.W.; Bondeau, A.; Bottcher, K.; Doktor, D.; Lucht, W.; Schaber, J.; Sitch, S. Responses of spring phenology to climate change. New Phytol. 2004, 162, 295–309, doi:10.1111/j.1469-8137.2004.01059.x.
[14]
Vitasse, Y.; Delzon, S.; Dufrene, E.; Pontailler, J.Y.; Louvet, J.M.; Kremer, A.; Michalet, R. Leaf phenology sensitivity to temperature in European trees: Do within-species populations exhibit similar responses? Agr. Forest. Meteorol. 2009, 149, 735–744, doi:10.1016/j.agrformet.2008.10.019.
[15]
Zheng, J. Relationships of the distribution of schistosomiasis and elevation in highland moutains in Yunnan. Strait J. Prev. Med. 2000, 6, 17–18. (in Chinese).
[16]
Lu, Z.; Broker, M.; Liang, G.D. Tick-borne encephalitis in mainland China. Vector-Borne Zoonotic Dis. 2008, 8, 713–720, doi:10.1089/vbz.2008.0028.
[17]
Bi, W.M.; Deng, H.P.; Bu, X.Y. Studies on regionalization of natural foci of tick-borne encephalitis. J. Capital Norm. Univ. 1997, 18, 100–107. (in Chinese).
[18]
Zhang, J.; Chen, S.; Zhao, X. Spatial divergency of temperature change during 1951-2000 in China and its correlation with global climate change. J. Arid Land Resour. Environ. 2006, 20, 1–6, doi:10.1080/15324980500369392.
[19]
Cai, H.Y.; Zhang, S.W.; Bu, K.; Yang, J.C.; Chang, L.P. Integrating geographical data and phenological characteristics derived from MODIS data for improving land cover mapping. J. Geogr. Sci. 2011, 21, 705–718, doi:10.1007/s11442-011-0874-1.
[20]
Huete, A.; Didan, K.; Miura, T.; Rodriguez, E.P.; Gao, X.; Ferreira, L.G. Overview of the radiometric and biophysical performance of the MODIS vegetation indices. Remote Sens. Environ. 2002, 83, 195–213, doi:10.1016/S0034-4257(02)00096-2.
[21]
Sirikul, N. Comparison of MODIS Vegetation Indices with Biophysical and Flux Measurement. Ph.D Dissertation, The University of Arizona, Tucson, AZ, USA, 2006.
Paruelo, J.M.; Epstein, H.E.; Lauenroth, W.K.; Burke, I.C. ANPP estimates from NDVI for the Central Grassland Region of the United States. Ecology 1997, 78, 953–958, doi:10.1890/0012-9658(1997)078[0953:AEFNFT]2.0.CO;2.
[24]
Yu, X.; Zhang, D. Monitoring forest phenophases of Northeast China based on MODIS NDVI data. Resour. Sci. 2006, 28, 111–117.
[25]
J？nsson, P.; Eklundh, L. Seasonality extraction by function fitting to time-series of satellite sensor data. IEEE Trans. Geosci. Remot. Sen. 2002, 40, 1824–1832, doi:10.1109/TGRS.2002.802519.
Heumann, B.W.; Seaquist, J.W.; Eklundh, L.; J？nsson, P. AVHRR derived phenological change in the Sahel and Soudan, Africa, 1982-2005. Remote Sens. Environ. 2007, 108, 385–392, doi:10.1016/j.rse.2006.11.025.
[28]
Olsson, L.; Eklundh, L.; Ardo, J. A recent greening of the Sahel—Trends, patterns and potential causes. J. Arid Environ. 2005, 63, 556–566, doi:10.1016/j.jaridenv.2005.03.008.
[29]
Dong, J.H.; Zhu, J.H.; Yin, F.R. Epidemiologic investigations of tick-borne encephalitis and lyme disease in Great Khingan Mountains in Inner Mongolia. Chin. Prev. Med. 2007, 8, 718–719.
[30]
Guo, Z.X. Research on Vegetation Changing and Reaction to Climate in Northeast China from 1982 to 2003; Northeast Institute of Geography and Agroecology: Changchun, China, 2008.
[31]
Sun, F.H.; Yang, S.Y.; Chen, P.S. Climatic warming-drying trend in Northeastern China during the last 44 years and its effects. Chin. J. Ecol. 2005, 24, 751–755.
[32]
Westerling, A.L.; Hidalgo, H.G.; Cayan, D.R.; Swetnam, T.W. Warming and earlier spring increase western U.S. forest wildfire activity. Science 2006, 313, 940–943.
[33]
Wang, J.; Ji, L.Z.; Khomutova, M. Relationships between forest insect pest occurrence area and meteorological factors in Great Xing’an Mountains of Heilongjiang Province, Northeast China. Chin. J. Ecol. 2007, 26, 673–677.
[34]
Menzel, A.; Fabian, P. Growing season extended in Europe. Nature 1999, 397, 659–659, doi:10.1038/17709.
[35]
Tucker, C.J.; Slayback, D.A.; Pinzon, J.E.; Los, S.O.; Myneni, R.B.; Taylor, M.G. Higher northern latitude normalized difference vegetation index and growing season trends from 1982 to 1999. Int. J. Biometeorol. 2001, 45, 184–190, doi:10.1007/s00484-001-0109-8.
[36]
White, M.A.; Thornton, P.E.; Running, S.W. A continental phenology model for monitoring vegetation responses to interannual climatic variability. Global. Biogeochem. Cy. 1997, 11, 217–234, doi:10.1029/97GB00330.
[37]
Chen, X.Q.; Hu, B.; Yu, R. Spatial and temporal variation of phenological growing season and climate change impacts in temperate eastern China. Global. Change. Biol. 2005, 11, 1118–1130, doi:10.1111/j.1365-2486.2005.00974.x.
[38]
Klemola, T.; Pettersen, T.; Stenseth, N.C. Trophic interactions in population cycles of voles and lemmings: A model-based synthesis. Adv. Ecol. Res. 2003, 33, 75–160, doi:10.1016/S0065-2504(03)33010-7.
