{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,22]],"date-time":"2026-02-22T07:41:45Z","timestamp":1771746105991,"version":"3.50.1"},"reference-count":62,"publisher":"MDPI AG","issue":"7","license":[{"start":{"date-parts":[[2020,4,10]],"date-time":"2020-04-10T00:00:00Z","timestamp":1586476800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"the strategic priority research program of the Chinese Academy of Sciences","award":["XDA19070303"],"award-info":[{"award-number":["XDA19070303"]}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["41901131, 41725003 and 41771047"],"award-info":[{"award-number":["41901131, 41725003 and 41771047"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Remote Sensing"],"abstract":"<jats:p>As a key biotic factor, phenology exerts fundamental influences on ecosystem carbon sequestration. However, whether spring phenology affects the subsequent seasonal ecosystem productivity and the underlying resource limitation mechanism remains unclear for the alpine grasslands of the Tibetan Plateau (TP). In this study, we investigated the direct and lagged seasonal responses of net primary productivity (NPP) to the beginning of growing season (BGS) along a precipitation gradient by integrating field observations, remote sensing monitoring and ecosystem model simulations. The results revealed distinct response patterns of seasonal NPP to BGS. Specifically, the BGS showed a significant and negative correlation with spring NPP (R = \u22120.73, p &lt; 0.01), as evidenced by the direct boosting effects of earlier BGS on spring NPP. Moreover, spring NPP was more responsive to BGS in areas with more annual precipitation. The boosting effects of earlier BGS on NPP tended to weaken in summer compared with that in spring. Sequentially, BGS exhibited stronger positive correlation with autumn NPP in areas with less annual precipitation, which suggested the enhanced lagged suppressing effects of earlier spring phenology on ecosystem carbon assimilation during the later growing season under aggravated water stress. Overall, the strengthened NPP in spring was offset by its decrement in autumn, resulting in no obvious relationship between BGS and annual NPP (R = \u22120.34, p &gt; 0.05) for the entire grasslands on the TP. The findings of this study imply that the lagged effects of phenology on the ecosystem productivity during the subsequent seasons should not be neglected in the future studies.<\/jats:p>","DOI":"10.3390\/rs12071223","type":"journal-article","created":{"date-parts":[[2020,4,13]],"date-time":"2020-04-13T10:41:52Z","timestamp":1586774512000},"page":"1223","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":28,"title":["Direct and Lagged Effects of Spring Phenology on Net Primary Productivity in the Alpine Grasslands on the Tibetan Plateau"],"prefix":"10.3390","volume":"12","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-8156-0602","authenticated-orcid":false,"given":"Zhoutao","family":"Zheng","sequence":"first","affiliation":[{"name":"Key Laboratory of Ecosystem Network Observation and Modeling, Institute of Geographic Sciences and Natural Resources Research, Chinese Academy of Sciences, Beijing 100101, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Wenquan","family":"Zhu","sequence":"additional","affiliation":[{"name":"Faculty of Geographical Science, Beijing Normal University, Beijing 100875, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yangjian","family":"Zhang","sequence":"additional","affiliation":[{"name":"Key Laboratory of Ecosystem Network Observation and Modeling, Institute of Geographic Sciences and Natural Resources Research, Chinese Academy of Sciences, Beijing 100101, China"},{"name":"CAS Center for Excellence in Tibetan Plateau Earth Sciences, Chinese Academy of Sciences, Beijing 100101, China"},{"name":"College of Resources and Environment, University of Chinese Academy of Sciences, Beijing 100190, China"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2020,4,10]]},"reference":[{"key":"ref_1","first-page":"1225","article-title":"Interannual variability of ecosystem carbon exchange: From observation to prediction","volume":"26","author":"Niu","year":"2017","journal-title":"Glob. Chang. Biol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1016\/j.agrformet.2015.02.007","article-title":"Biotic and climatic controls on interannual variability in carbon fluxes across terrestrial ecosystems","volume":"205","author":"Shao","year":"2015","journal-title":"Agric. For. Meteorol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1620","DOI":"10.1111\/j.1365-2486.2008.01599.x","article-title":"Interannual variability in carbon dioxide fluxes and flux-climate relationships on grazed and ungrazed northern mixed-grass prairie","volume":"14","author":"Polley","year":"2008","journal-title":"Glob. Chang. Biol."},{"key":"ref_4","first-page":"994","article-title":"Interannual variability of net ecosystem productivity in forests is explained by carbon flux phenology in autumn","volume":"22","author":"Wu","year":"2013","journal-title":"Glob. Chang. Biol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"3227","DOI":"10.1098\/rstb.2010.0102","article-title":"Influence of spring and autumn phenological transitions on forest ecosystem productivity","volume":"365","author":"Richardson","year":"2010","journal-title":"Philos. Trans. R. Soc. B-Biol. Sci."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1016\/j.tree.2007.04.003","article-title":"Shifting plant phenology in response to global change","volume":"22","author":"Cleland","year":"2007","journal-title":"Trends Ecol. Evol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1038\/nature01286","article-title":"A globally coherent fingerprint of climate change impacts across natural systems","volume":"421","author":"Parmesan","year":"2003","journal-title":"Nature"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"343","DOI":"10.1111\/j.1365-2486.2005.01097.x","article-title":"Onset of spring starting earlier across the Northern Hemisphere","volume":"12","author":"Schwartz","year":"2006","journal-title":"Glob. Chang. Biol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1038\/nature01333","article-title":"Fingerprints of global warming on wild animals and plants","volume":"421","author":"Root","year":"2003","journal-title":"Nature"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"156","DOI":"10.1016\/j.agrformet.2012.09.012","article-title":"Climate change, phenology, and phenological control of vegetation feedbacks to the climate system","volume":"169","author":"Richardson","year":"2013","journal-title":"Agric. For. Meteorol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"2335","DOI":"10.1111\/j.1365-2486.2009.01910.x","article-title":"Intercomparison, interpretation, and assessment of spring phenology in North America estimated from remote sensing for 1982\u20132006","volume":"15","author":"White","year":"2009","journal-title":"Glob. Chang. Biol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"454","DOI":"10.1093\/nsr\/nwv058","article-title":"Plant phenological responses to climate change on the Tibetan Plateau: Research status and challenges","volume":"2","author":"Shen","year":"2015","journal-title":"Natl. Sci. Rev."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"428","DOI":"10.1016\/j.scib.2019.03.009","article-title":"Current status and future directions of the Tibetan Plateau ecosystem research","volume":"64","author":"Zhang","year":"2019","journal-title":"Sci. Bull."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1016\/j.gloplacha.2012.08.009","article-title":"Impacts of climate and CO2 changes on the vegetation growth and carbon balance of Qinghai-Tibetan grasslands over the past five decades","volume":"98\u201399","author":"Piao","year":"2012","journal-title":"Glob. Planet. Chang."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"13711","DOI":"10.1038\/srep13711","article-title":"Does the climate warming hiatus exist over the Tibetan Plateau?","volume":"5","author":"Duan","year":"2015","journal-title":"Sci. Rep."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"4309","DOI":"10.1073\/pnas.1210423110","article-title":"Green-up dates in the Tibetan Plateau have continuously advanced from 1982 to 2011","volume":"110","author":"Zhang","year":"2013","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"194","DOI":"10.1016\/j.agrformet.2016.04.012","article-title":"Continuous but diverse advancement of spring-summer phenology in response to climate warming across the Qinghai-Tibetan Plateau","volume":"223","author":"Zheng","year":"2016","journal-title":"Agric. For. Meteorol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1016\/j.scitotenv.2019.01.324","article-title":"Impact of physiological and phenological change on carbon uptake on the Tibetan Plateau revealed through GPP estimation based on spaceborne solar-induced fluorescence","volume":"663","author":"Chen","year":"2019","journal-title":"Sci. Total. Environ."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"641","DOI":"10.1016\/j.scitotenv.2019.02.293","article-title":"Grassland production in response to changes in biological metrics over the Tibetan Plateau","volume":"666","author":"Jin","year":"2019","journal-title":"Sci. Total. Environ."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1016\/j.agrformet.2016.08.020","article-title":"Responses of net primary productivity to phenological dynamics in the Tibetan Plateau, China","volume":"232","author":"Wang","year":"2017","journal-title":"Agric. For. Meteorol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"105880","DOI":"10.1016\/j.ecolind.2019.105880","article-title":"Elevation-dependent effects of growing season length on carbon sequestration in Xizang Plateau grassland","volume":"110","author":"Tao","year":"2020","journal-title":"Ecol. Indic."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"110","DOI":"10.1038\/s41586-018-0555-7","article-title":"Widespread seasonal compensation effects of spring warming on northern plant productivity","volume":"562","author":"Buermann","year":"2018","journal-title":"Nature"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"321","DOI":"10.1093\/treephys\/tpn040","article-title":"Influence of spring phenology on seasonal and annual carbon balance in two contrasting New England forests","volume":"29","author":"Richardson","year":"2009","journal-title":"Tree Physiol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"886","DOI":"10.1111\/j.1365-2486.2010.02281.x","article-title":"Evidence of increased net ecosystem productivity associated with a longer vegetated season in a deciduous forest in south-central Indiana, USA","volume":"17","author":"Dragoni","year":"2011","journal-title":"Glob. Chang. Biol."},{"key":"ref_25","first-page":"1","article-title":"Earlier leaf-flushing suppressed ecosystem productivity by draining soil water in the Mongolian Plateau","volume":"250","author":"Yu","year":"2018","journal-title":"Agric. For. Meteorol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"107845","DOI":"10.1016\/j.agrformet.2019.107845","article-title":"Legacy effect of spring phenology on vegetation growth in temperate China","volume":"281","author":"Zhou","year":"2020","journal-title":"Agric. For. Meteorol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1960","DOI":"10.1029\/2018JG004438","article-title":"Warming-induced earlier greenup leads to reduced stream discharge in a temperate mixed forest catchment","volume":"123","author":"Kim","year":"2018","journal-title":"J. Geophys. Res.-Biogeosci."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"eaax0255","DOI":"10.1126\/sciadv.aax0255","article-title":"Summer soil drying exacerbated by earlier spring greening of northern vegetation","volume":"6","author":"Lian","year":"2020","journal-title":"Sci. Adv."},{"key":"ref_29","first-page":"e00814","article-title":"Seasonally and spatially varied controls of climatic factors on net primary productivity in alpine grasslands on the Tibetan Plateau","volume":"21","author":"Zheng","year":"2020","journal-title":"Glob. Ecol. Conserv."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"L1940519","DOI":"10.1029\/2007GL031447","article-title":"Diverse responses of vegetation phenology to a warming climate","volume":"34","author":"Zhang","year":"2007","journal-title":"Geophys. Res. Lett."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"332","DOI":"10.1016\/j.rse.2004.03.014","article-title":"A simple method for reconstructing a high-quality NDVI time-series data set based on the Savitzky-Golay filter","volume":"91","author":"Chen","year":"2004","journal-title":"Remote. Sens. Environ."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1417","DOI":"10.1080\/01431168608948945","article-title":"Characteristics of maximum-value composite images from temporal AVHRR data","volume":"7","author":"Holben","year":"1986","journal-title":"Int. J. Remote. Sens."},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Zheng, Z., and Zhu, W. (2017). Uncertainty of remote sensing data in monitoring vegetation phenology: A comparison of MODIS C5 and C6 vegetation index products on the Tibetan Plateau. Remote. Sens., 9.","DOI":"10.3390\/rs9121288"},{"key":"ref_34","unstructured":"China Meteorological Administration (1993). Observation Criterion of Agricultural Meteorology."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"2323","DOI":"10.1029\/2018JG004616","article-title":"Climatic controls of the spatial patterns of vegetation phenology in midlatitude grasslands of the Northern Hemisphere","volume":"123","author":"Ren","year":"2018","journal-title":"J. Geophys. Res.-Biogeosci."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"390","DOI":"10.1016\/j.tree.2015.04.006","article-title":"Towards a standardized rapid ecosystem function assessment (REFA)","volume":"30","author":"Meyer","year":"2015","journal-title":"Trends Ecol. Evol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1341","DOI":"10.1007\/s11430-007-0049-1","article-title":"Terrestrial vegetation carbon sinks in China, 1981\u20152000","volume":"50","author":"Fang","year":"2007","journal-title":"Sci. China Ser. D Earth Sci."},{"key":"ref_38","first-page":"114","article-title":"Evaporation from a water surface in relation to solar radiation","volume":"64","author":"Prescott","year":"1940","journal-title":"Trans. R. Soc. S. Aust."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1002\/qj.49705021008","article-title":"Solar and terrestrial radiation","volume":"50","author":"Angstrom","year":"1924","journal-title":"Q. J. R. Meteorol. Soc."},{"key":"ref_40","unstructured":"Hutchinson, M.F. (2004). Anusplin Version 4.3, Center for Resource and Environmental Studies, The Australian National University."},{"key":"ref_41","unstructured":"Editorial Board of Vegetation Map of China, Chinese Academy of Sciences (2007). Vegetation Map of the People\u2019s Republic of China (1:1000000) (Digital Version), Geology Press."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"471","DOI":"10.1016\/S0034-4257(02)00135-9","article-title":"Monitoring vegetation phenology using MODIS","volume":"84","author":"Zhang","year":"2003","journal-title":"Remote. Sens. Environ."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1016\/0034-4257(94)00066-V","article-title":"Global net primary production: Combining ecology and remote sensing","volume":"51","author":"Field","year":"1995","journal-title":"Remote. Sens. Environ."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"811","DOI":"10.1029\/93GB02725","article-title":"Terrestrial ecosystem production-a process model-based on global satellite and surface data","volume":"7","author":"Potter","year":"1993","journal-title":"Glob. Biogeochem. Cycles"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"457","DOI":"10.1007\/s11434-006-0457-1","article-title":"Simulation of maximum light use efficiency for some typical vegetation types in China","volume":"51","author":"Zhu","year":"2006","journal-title":"Chin. Sci. Bull."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"870","DOI":"10.1007\/s00376-014-4106-3","article-title":"Dryland expansion in northern China from 1948 to 2008","volume":"32","author":"Li","year":"2015","journal-title":"Adv. Atmos. Sci."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"111675","DOI":"10.1016\/j.rse.2020.111675","article-title":"Land surface phenology in the highland pastures of montane Central Asia: Interactions with snow cover seasonality and terrain characteristics","volume":"240","author":"Tomaszewska","year":"2020","journal-title":"Remote. Sens. Environ."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"598","DOI":"10.1038\/nclimate2253","article-title":"Net carbon uptake has increased through warming-induced changes in temperate forest phenology","volume":"4","author":"Keenan","year":"2014","journal-title":"Nat. Clim. Chang."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"1069","DOI":"10.1093\/treephys\/24.9.1069","article-title":"Enhancement of understory productivity by asynchronous phenology with overstory competitors in a temperate deciduous forest","volume":"24","author":"Jolly","year":"2004","journal-title":"Tree Physiol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"2110","DOI":"10.1111\/j.1365-2486.2007.01432.x","article-title":"Photosynthesis drives anomalies in net carbon-exchange of pine forests at different latitudes","volume":"13","author":"Luyssaert","year":"2007","journal-title":"Glob. Chang. Biol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"254","DOI":"10.1007\/s00442-004-1682-4","article-title":"Precipitation pulses and carbon fluxes in semiarid and arid ecosystems","volume":"141","author":"Huxman","year":"2004","journal-title":"Oecologia"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"1626","DOI":"10.1890\/11-2247.1","article-title":"Precipitation-driven carbon balance controls survivorship of desert biocrust mosses","volume":"93","author":"Coe","year":"2012","journal-title":"Ecology"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"701","DOI":"10.1111\/ele.13474","article-title":"Alpine grassland plants grow earlier and faster but biomass remains unchanged over 35 years of climate change","volume":"23","author":"Wang","year":"2020","journal-title":"Ecol. Lett."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"771","DOI":"10.1111\/j.1365-2486.2009.01967.x","article-title":"Longer growing seasons lead to less carbon sequestration by a subalpine forest","volume":"16","author":"Hu","year":"2010","journal-title":"Glob. Chang. Biol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"45501","DOI":"10.1088\/1748-9326\/6\/4\/045501","article-title":"Satellite observations of high northern latitude vegetation productivity changes between 1982 and 2008: Ecological variability and regional differences","volume":"6","author":"Beck","year":"2011","journal-title":"Environ. Res. Lett."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"24027","DOI":"10.1088\/1748-9326\/8\/2\/024027","article-title":"Earlier springs decrease peak summer productivity in North American boreal forests","volume":"8","author":"Buermann","year":"2013","journal-title":"Environ. Res. Lett."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1007\/s11104-011-0995-4","article-title":"How does drought stress influence the decomposition of plant litter with contrasting quality in a grassland ecosystem?","volume":"352","author":"Sanaullah","year":"2012","journal-title":"Plant Soil"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"924","DOI":"10.1111\/nph.12952","article-title":"Drought effect on plant nitrogen and phosphorus: A meta-analysis","volume":"204","author":"He","year":"2014","journal-title":"New Phytol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1007\/s00442-009-1364-3","article-title":"The importance of nutritional regulation of plant water flux","volume":"161","author":"Cramer","year":"2009","journal-title":"Oecologia"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1016\/j.gloplacha.2012.05.021","article-title":"Interannual and spatial impacts of phenological transitions, growing season length, and spring and autumn temperatures on carbon sequestration: A North America flux data synthesis","volume":"92\u201393","author":"Wu","year":"2012","journal-title":"Glob. Planet. Chang."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1016\/j.tree.2015.01.004","article-title":"Autumn, the neglected season in climate change research","volume":"30","author":"Gallinat","year":"2015","journal-title":"Trends Ecol. Evol."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1016\/j.agrformet.2016.11.193","article-title":"Land surface phenology derived from normalized difference vegetation index (NDVI) at global FLUXNET sites","volume":"233","author":"Wu","year":"2017","journal-title":"Agric. For. Meteorol."}],"container-title":["Remote Sensing"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2072-4292\/12\/7\/1223\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T09:17:19Z","timestamp":1760174239000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2072-4292\/12\/7\/1223"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,4,10]]},"references-count":62,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2020,4]]}},"alternative-id":["rs12071223"],"URL":"https:\/\/doi.org\/10.3390\/rs12071223","relation":{},"ISSN":["2072-4292"],"issn-type":[{"value":"2072-4292","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,4,10]]}}}