Dominant role of plant physiology in trend and variability of gross primary productivity in North America

Transcription

1 OPEN receved: 15 July 2016 accepted: 20 December 2016 Publshed: 01 February 2017 Domnant role of plant physology n trend and varablty of gross prmary productvty n North Amerca Sha Zhou 1,2, Yao Zhang 3, Phlppe Cas 4, Xangmng Xao 3,5, Yq Luo 6,7, Kelly K. Caylor 2, Yuefe Huang 1,8 & Guangqan Wang 1 Annual gross prmary productvty (GPP) vares consderably due to clmate-nduced changes n plant phenology and physology. However, the relatve mportance of plant phenology and physology on annual GPP varaton s not clear. In ths study, a Statstcal Model of Integrated Phenology and Physology (SMIPP) was used to evaluate the relatve contrbutons of maxmum daly GPP (GPP max ) and the start and end of growng season (GS start and GS end ) to annual GPP varablty, usng a regonal GPP product n North Amerca durng and GPP data from 24 AmerFlux stes. Clmatc senstvty of the three ndcators was assessed to nvestgate the clmate mpacts on plant phenology and physology. The SMIPP can explan 98% of nter-annual varablty of GPP over md- and hgh lattudes n North Amerca. The long-term trend and nter-annual varablty of GPP are domnated by GPP max both at the ecosystem and regonal scales. Durng warmer sprng and autumn, GS start s advanced and GS end delayed, respectvely. GPP max responds postvely to summer temperature over hgh lattudes (40 80 N), but negatvely n md-lattudes (25 40 N). Ths study demonstrates that plant physology, rather than phenology, plays a domnant role n annual GPP varablty, ndcatng more attenton should be pad to physologcal change under futher clmate change. The mportance of plant phenology shfts and physology change on annual GPP varablty s evdent 1 4. Warmng-nduced earler leaf emergence enhances terrestral carbon uptake n sprng, whereas later leaf senescence n autumn also leads to a smaller ncrease n carbon uptake n North Amercan temperate forests 5. However, drought events assocated wth hgh temperature and low water avalablty can decrease plant photosynthetc uptake 6 8. In regons exposed to summer drought, an ncrease of leaf area n earler sprng can accelerate sol dryng, and lead to ncreased vulnerablty of GPP n summer 9,10. In terms of net carbon balance, carbon loss durng summer drought can negate ncreased uptake n warmer sprngs and autumns 11 13, related to the negatve covarance between ncreased sprng productvty and decreased yearly productvty. The dfferent responses of plant phenology and physology to clmate anomales, and the contrbutons of phenologcal and physologcal changes to annual GPP varablty must thus be dsentangled. The jont control of plant phenology and physology on annual GPP can be expressed by constructng a statstcal model 4,14, whch uses ndcators to represent plant phenologcal and physologcal changes. Phenology s about the tme and duraton of a process or event. The length of carbon uptake perod (CUP), and the start (GS start ) and the end (GS end ) of the growng season, can be used as ndcators of plant phenology. Plant photosynthess s an mportant process of plant physology, and can reflect the responses of plant physology to 1 State Key Laboratory of Hydroscence and Engneerng, Department of Hydraulc Engneerng, Tsnghua Unversty, Bejng , Chna. 2 Department of Cvl and Envronmental Engneerng, Prnceton Unversty, Prnceton, NJ 08544, USA. 3 Department of Mcrobology and Plant Bology, Center for Spatal Analyss, Unversty of Oklahoma, Norman, OK 73019, USA. 4 Laboratore des Scences du Clmat et de l Envronnement, CEA CNRS UVSQ, Gf-sur- Yvette 91190, France. 5 Instttue of Bodversty Scence, Fudan Unversty, Shangha , Chna. 6 Department of Mcrobology and Plant Bology, Unversty of Oklahoma, Norman, Oklahoma 73019, USA. 7 Center for Earth System Scence, Tsnghua Unversty, Bejng , Chna. 8 College of Ecologcal and Envronmental Engneerng, Qngha Unversty, Xnng Qngha, Chna. Correspondence and requests for materals should be addressed to S.Z. (emal: zhous13@mals.tsnghua.edu.cn) or Y.H. (emal: yuefehuang@tsnghua.edu.cn) Scentfc Reports 7:41366 DOI: /srep

2 Fgure year ( ) trends of annual GPP and the three ndcators n North Amerca. (a) Annual GPP. (b) Start of growng season (GS start ). (c) Maxmum daly GPP (GPP max ). (d) End of growng season (GS end ). A negatve sgn (red color) n (b) and (d) denotes an earler trend of GS start and GS end, and vce versa. Maps were generated usng MATLAB 2015b ( envronmental changes. As the maxmum photosynthetc carbon uptake (GPP max ) represents the mportant characterstcs of plant photosynthess, t can be used as an ndcator of plant physology. The varaton n the product of CUP by GPP max was found to explan more than 90% of the temporal varablty of annual GPP n most areas of North Amerca durng , and more than 95% of the spatal GPP gradents among 213 flux tower stes 4. Ths shows that even a smple statstcal model has an nterestng explanaton power of observed varablty of annual GPP. The Statstcal Model of Integrated Phenology and Physology (SMIPP) extends the approach of Xa et al. 4 by treatng separately GS start, GS end and GPP max, as predctors of annual GPP. Ths model descrbed n Zhou et al. 14 was shown to explan 90 ± 11% of the nter-annual varablty of GPP among 27 flux tower stes across North Amerca and Europe. The SMIPP decomposes annual GPP anomaly nto three components, whch are nduced by the anomales n GS start, GPP max and GS end, respectvely. These three predctors were shown to be statstcally ndependent of each other 14, even though there may be processes lnkng them through lagged effects of prevous season clmate mpactng the value of a predctor durng the followng seasons. Thus, the contrbutons of the changes n GS start, GPP max and GS end to annual GPP varablty can be lnked to the correspondng components of annual GPP anomaly. Because the annual GPP varablty s related to plant phenologcal and physologcal changes, the responses of the above three ndcators to clmate varablty s crucal to dagnose the drvers of annual GPP varablty through the SMIPP. The senstvty of plant phenology to clmate change has been assessed n many studes 5, Whle sprng phenology s unambguously advanced durng warmer sprngs, autumn phenology s affected not only by temperature, but also by precptaton, photoperod, and coolng degree-days In addton, the clmatc responses of plant phenology vary among dfferent speces and clmate regons Although the mpacts of clmate change on GPP max are more dffcult to assess, summer photosynthess s usually reduced by hot temperatures assocated wth dryer sols 9,13,27. Because plant phenology (here GS start and GS end ) and physology (here GPP max ) are nfluenced by clmatc factors n dfferent ways, t s mportant to nvestgate how plant phenology and physology medate mpacts of clmate varablty on annual GPP varablty through ther responses to clmate varablty. In ths study, we evaluate the relatve contrbutons of the changes n GS start, GPP max and GS end to the long-term trend and nter-annual varablty of GPP usng the SMIPP. Our study s based on a regonal GPP product from the vegetaton photosynthess model (VPM) n North Amerca over the perod The relatve contrbutons of the three ndcators are also nvestgated at ecosystem scale based on GPP measurements from 24 AmerFlux stes. In addton, we derve the clmatc senstvty of the three ndcators, and nvestgate the mechansm of annual GPP responses to temperature, precptaton and downward solar radaton through plant phenologcal and physologcal changes over dfferent regons. Results Long-term trend of annual GPP and the three ndcators. Fgure 1a shows the spatal pattern of the long-term trend of annual GPP from VPM over md- and hgh lattudes n North Amerca durng the perod Annual GPP trend ranges from 10 to 10 g C m 2 per year for 96.7% of the area, and the average rate s 1.40 g C m 2 per year over the whole area. The majorty (66.5% of the area) experenced a postve trend n annual GPP wth an ncreasng rate of 3.47 ± 3.36 g C m 2 per year. However, other regons experenced a negatve trend ( 2.72 ± 2.91 g C m 2 per year) n annual GPP. Regons wth decreasng GPP are manly located n the western US and south Alaska. Scentfc Reports 7:41366 DOI: /srep

3 Fgure 2. Multple regresson results of the statstcal model of ntegrated phenology and physology (SMIPP). (a) R 2 of the SMIPP. Senstvty coeffcents of annual GPP to (b) GS start, (c) GPP max, and (d) GS end. Lattudnal dstrbutons of the senstvty coeffcents of annual GPP to (e) GPP max (purple), and (f) GS start (green) and GS end (red). Maps were generated usng MATLAB 2015b ( matlab/). Earler GS start s evdent across the boreal zone, whle most of the temperate zone show delayed GS start (Fg. 1b, see Fg. S1 for the clmate zones over North Amerca). The average advance of GS start s 0.29 day per year for 57% of the area, and the average delay s 0.32 day per year for the other area. GS end delays by 0.26 day per year for 58% of the area, most of whch are located at the western and central North Amerca (Fg. 1d). Spatal correlatons were performed usng the values of the long-term trends of annual GPP and the three ndcators from all the grd cells. The spatal correlaton between the long-term trends of ether GS start or GS end and annual GPP s weak (R 2 < 0.10). However, both the mean value (R 2 = 0.83, p < 0.001), and the trend of GPP max (R 2 = 0.90, p < 0.001) exhbt a nearly dentcal spatal pattern wth annual GPP (Fg. S2a,c and Fg. 1a,c). The hgh spatal correlatons of the mean values and trends between GPP max and annual GPP ndcate the mportance of GPP max n annual GPP and the major contrbuton of GPP max trend to annual GPP trend. Annual GPP varablty explaned by the SMIPP. Frst of all, the nterrelatonshps of the three ndcators were tested. R 2 s 0.26 ± 0.23 between GS start and GPP max (p > 0.05 over 56.8% of the area), 0.11 ± 0.13 between GPP max and GS end (p > 0.05 over 86.9% of the area), and 0.23 ± 0.20 between GS start and GS end (p > 0.05 over 62.7% of the area), respectvely, across all the grd cells (Fg. S4). Our correlaton analyss ndcates the ndependence of the three ndcators over most study area. The SMIPP was then appled to each grd cell and the regresson results are provded n Fg. 2. The SMIPP can explan 98.3 ± 4.7% of nter-annual varablty of the GPP from VPM across md- and hgh lattudes n North Amerca (p < over 99.1% of the area (Fg. S5a)). The model s robust over temperate, boreal and tundra clmate zones, and a lttle weak (R 2 < 0.90) n subtropcal and Medterranean clmate zones over southeast and west coast of the US. The data dsplayed n Fg. 2c and e show that annual GPP changes are less senstve to change n GPP max over hgher lattudes. An ncrease of 1 g C m 2 day 1 n GPP max contrbutes an ncrease of 95.9 ± 17.3 g C m 2 per year n annual GPP across the study area, but the value of the senstvty of annual GPP to GPP max decreases from South to North, from 125 around 35 N to 80 around 70 N. The senstvtes of annual GPP to GS start and GS end follow a smlar pattern over North of 45 N. However, ther senstvty coeffcents gradually dverge from 45 to 35 N because annual GPP s more senstve to GS start than to GS end over eastern subtropcal coasts of the US. Overall, the senstvty of annual GPP relatve to GS start (2.9 ± 2.2 g C m 2 day 1 ) s a lttle hgher than that relatve to GS end (2.4 ± 1.8 g C m 2 day 1 ). The senstvty coeffcent of annual GPP to GPP max s sgnfcant at level over 99.3% of the area and that to GS start and GS end s sgnfcant at 0.01 level over 89.2% and 85.2% of the area, respectvely (Fg. S5). Thus, the three senstvty coeffcents can capture the senstvty of annual GPP to GS start, GPP max, and GS end, respectvely, over md- and hgh lattudes n North Amerca. Contrbutons of the three ndcators to annual GPP varablty. The contrbutons of the three ndcators to the long-term trend n annual GPP were separated based on the results of the SMIPP (Fg. 3a c). The contrbuton s postve only when the ndcator and annual GPP have a trend of the same sgn, and vce versa. The GPP max related component of GPP, contrbutes postvely to annual GPP ncrease over 67.4% of the area, and negatvely over other areas, such as the western US and south Alaska area, where annual GPP shows decreasng trends. The postve and negatve contrbutons are 65.4 ± 20.3% and 61.2 ± 24.7%, respectvely. In addton, GPP max contrbutes more than half of annual GPP change for 77.1% of the area (54.3% postve and 22.8% negatve), ndcatng that the long-term trend n annual GPP s domnated by GPP max trend. By comparson, the postve and negatve contrbutons are 20.0 ± 14.0% and 21.9 ± 17.3% for GS start, and only 15.8 ± 14.0% Scentfc Reports 7:41366 DOI: /srep

4 Fgure 3. Relatve contrbutons (%) of the three ndcators to annual GPP varablty n North Amerca. Contrbutons of (a,e) GS start, (b,f) GPP max, and (c,g) GS end to the long-term trend and nter-annual varablty n annual GPP, respectvely. Contrbutons of the three ndcators to the (d) long-term trend and (h) nter-annual varablty n annual GPP for the 24 AmerFlux stes. Maps were generated usng MATLAB 2015b ( mathworks.com/products/matlab/). and 14.4 ± 13.7% for GS end. The prmary contrbuton of GPP max and the secondary contrbutons of GS start and GS end are n agreement wth the spatal correlaton results between the long-term trends of annual GPP and the three ndcators. The nter-annual varablty of GPP s also domnated by the varablty of the GPP max related component, whose contrbuton accounts for 84.6 ± 14.7%, and for more than 50% over 98.8% of the area (Fg. 3e g). The contrbuton of GS start s 13.8 ± 13.70%, wth postve values n 87.9% of the area. In most of the northern plans area, GS start vares oppostely wth annual GPP and contrbutes negatvely to annual GPP varablty. GS end explans the least of the nter-annual varablty of GPP, and ts contrbuton s as low as 1.6 ± 8.7%, rangng only from 15% to 15% for more than 90% of the area. Thus, GS start plays a more mportant role than GS end n terms of ts contrbuton to the long-term trend and nter-annual varablty of GPP. The domnant contrbuton of the GPP max related component of GPP to the long-term trend and nter-annual varablty of GPP s also supported by the AmerFlux data. The SMIPP was calbrated at 24 flux stes wth the R 2 of 0.94 ± 0.05 (Table S2). The postve contrbuton of GPP max to the long-term trend of annual GPP s observed at 14 of the 24 stes wth mean contrbuton of 65.4%, and the mean negatve contrbuton s 58.7% (Fg. 3d). In addton, GPP max contrbutes 74.2 ± 19.7% to the nter-annual varablty of GPP over the 24 stes (Fg. 3h). The attrbuton analyses consstently demonstrate the domnant role of GPP max n the long-term trend and nter-annual varablty of GPP across md- and hgh lattudes n North Amerca. Clmatc senstvty of the three ndcators and of annual GPP. The responses of the three ndcators to the changes n temperature, precptaton and solar radaton were nvestgated. Both GS start and GS end are strongly related to preseason (30 days before the mean dates of GS start and GS end, respectvely) temperature (r = 0.48 ± 0.24 for GS start and r = 0.32 ± 0.26 for GS end ) n most study area (Fg. 4a and e). GS start occurs 1.9 ± 1.4 days earler, and GS end occurs 1.7 ± 1.8 days later, wth an ncrease of 1 C n preseason temperature (Fg. 4b and f). Earler GS start and later GS end n response to warmer temperature lead to more carbon assmlaton n sprng and autumn, especally over md-lattudes, where annual GPP shows hgher senstvty to GS start and GS end than n hgh lattudes (Fg. 2). It appears that hgher preseason precptaton delays GS start and advances GS end, respectvely, over most areas (Fg. S6). However, the correlaton of GS start or GS end wth precptaton s weaker than that wth temperature (Fgs 4 and S6). In addton to temperature, GS end s also delayed by hgher preseason solar radaton over 81.7% of the study area, although ts correlaton wth solar radaton s a lttle weaker (r = 0.27 ± 0.28) (Fg. S7). GS start s weakly correlated wth preseason solar radaton over most study area, suggestng that GS start s manly affected by temperature, whch s also supported by the partal correlaton analyss (Fg. S8). GPP max presents opposte responses to summer temperature over dfferent regons. GPP max s greatly enhanced n hgh lattudes (40 80 N) whle reduced n md-lattudes (25 40 N) wth warmer summer temperature (Fg. 4c Scentfc Reports 7:41366 DOI: /srep

5 Fgure 4. Correlaton coeffcent (r) and slope between the three ndcators and respectve seasonal temperature n North Amerca. (a,b) GS start and preseason (30 days before the mean date of GS start ) temperature. (c, d) GPP max and summer temperature (mean temperature n June-July-August). (e,f) GS end and preseason (30 days before the mean date of GS end ) temperature. Maps were generated usng MATLAB 2016a ( and d). The senstvty n GPP max to hgher summer temperature ncreases from less than 0.1 g C m 2 day 1 / C around 80 N to 0.33 g C m 2 day 1 / C around 60 N and decreases to 0.2 g C m 2 day 1 / C around 35 N (Fg. 5d). Although earler GS start and later GS end enhance carbon uptake, the declnng GPP max wth hgher temperature would probably decrease summer GPP and even cancel out the enhanced sprng and autumn GPP, resultng n annual GPP declne over most of the great plan areas (Fg. S9a and b). On the contrary, warmer temperature has a postve mpact on annual GPP anomaly n the boreal forests where advanced GS start, ncreased GPP max and delayed GS end durng warmer sprng, summer, autumn consstently contrbute to ncreasng annual GPP (Fg. S9a and b). Smlarly, GPP max responds postvely to hgher summer solar radaton n hgh lattudes, whle negatvely n most md-lattudes, especally the great plan areas (Fg. S7c and d). It s worth notng that the spatal pattern of the senstvty n GPP max to summer precptaton s dfferent from that to summer temperature and solar radaton, postvely n md-lattudes (central US) and negatvely n most hgh-lattudes (Fg. S6c and d). The sgnfcant trends of rsng temperature and hgher solar radaton n summer strongly enhance carbon assmlaton n hgh lattudes for the perod (Fgs 1a and S10a and c), and mply more carbon to be assmlated under future clmate warmng. The recent ncreasng trend of summer precptaton, wll partally releve the stress of hgh temperature and solar radaton, and accelerate summer GPP n md-lattudes (Fg. S10a c). Dscusson In ths study, we found that plant physology plays a more mportant role than phenology n determnng the long-term trend and nter-annual varablty of VPM GPP and ste scale AmerFlux GPP. The mportance of plant phenology on seasonal and annual GPP varablty has been shown n many studes 1,2,5,28,29. However, phenologcal changes cannot explan GPP reducton caused by the clmate extreme events, whch account for the majorty of global nter-annual varablty n GPP 30,31. Because of the drect lnk between photosynthetc physology and carbon assmlaton, GPP max used n ths study s strongly correlated to annual GPP and contrbutes to most of the nter-annual varablty of GPP. The results of Xa et al. 4 also ndcated that the contrbuton of GPP max s larger than CUP to the spatal varablty of GPP over most bome types, based on partal correlaton analyss 4. Gven the domnant role of GPP max n the long-term trend and nter-annual varablty of GPP, more focus should be pad to plant physologcal change to better explan GPP varablty and mprove GPP montor n terrestral ecosystems 32. The plant phenologcal and physologcal changes were related to temperature, precptaton, and solar radaton. The temperature control of GS start s stronger than the effects of precptaton and solar radaton over most study area. Snce bud burst depends on accumulated temperature, and plant photosynthess s also temperature dependent, preseason temperature s responsble for trggerng phenologcal events. Many studes also ndcated that the phenology of the boreal and temperate forests s manly drven by temperature 5,15,33. Apart from Scentfc Reports 7:41366 DOI: /srep

6 Fgure 5. Lattudnal dstrbutons of r and slope for the relatonshps between GPP max and clmatc factors. (a,d) GPP max v.s. summer temperature (mean temperature n June-July-August). (b,e) GPP max v.s. summer precptaton (mean monthly precptaton n June-July-August). (c,f) GPP max v.s. summer solar radaton (mean solar radaton n June-July-August). temperature, GS end s also regulated by preseason solar radaton. The solar radaton s typcally not lmtng when ar temperature trggers the onset of plant photosynthess n sprng 34. However, hgher solar radaton can delay leaf senescence n autumn. For one thng, the accumulaton of abscsc acd whch s responsble for leaf senescence can be nhbted by hgher solar radaton; for the other, the plant photosynthetc capacty s enhanced by hgher solar radaton, resultng n hgher photosynthetc rate and later leaf senescence 19. In comparson wth the consstent temperature responses of GS start and GS end over most of the area, GPP max responds postvely to summer temperature n hgh lattudes, whle negatvely n md-lattudes, where GPP max s manly enhanced by summer precptaton. The opposte responses of GPP max to summer temperature between md- and hgh lattudes can support the smulaton results that global warmng would ncrease the productvty at northern hgh-lattudes but tend to reduce t n the md-lattudes and tropcs 35. The nter-annual varablty of tree rng wdth n Europe s also manly controlled by temperature n hgh lattudes whle by precptaton (or water avalablty) n md-lattudes based on the radal tree growth analyss 36, but tree rng data cannot be easly related to clmate varable durng a specfc season, gven speces-specfc onthogenc controls of cambal wood growth durng perods of the growng season. The lattudnal patterns of the temperature senstvty of GS start and GS end and the opposte temperate senstvty of GPP max over md- and hgh lattudes are very mportant n predctng the phenologcal and physologcal responses to clmate change. Recent clmate warmng seems to have a generally postve mpact on forest productvty when water s not lmtng 37. Because the boreal forests are manly lmted by sunlght and temperature, and the temperate forests are manly lmted by water 38, GPP max tends to ncrease n hgh lattudes and decrease n md-lattudes wth ncreasng temperature. The negatve response of GPP max to the summer temperature over most md-lattudes of North Amerca ndcates a decreasng strength of temperate and sub-tropcal ecosystems n carbon assmlaton under recent warmng. Although the advanced GS start and delayed GS end can compensate part of GPP max nduced GPP declne, annual GPP s stll negatvely correlated wth annual temperature over the Central Great Plans n the US (Fg. S9a and b), where annual productvty s hghly lmted by water. The warmng trend seems to slow down n recent years, however, the projected North Amerca temperature wll contnue ncreasng over the next several decades 39,40. Thus, warmng nduced GPP declne s expected n part of the low and md-lattudes n the future. The results ndcate that advanced GS start, ncreased GPP max and delayed GS end under warmng clmate consstently contrbute to ncrease annual mean GPP n hgh lattudes, but ncreasng GPP wll not necessarly result Scentfc Reports 7:41366 DOI: /srep

7 n an ncrease n net ecosystem productvty (NEP). It was reported that the growth of western North Amercan boreal forests s constraned by both the ncreasng costs of autotrophc respraton 41,42 and frequent summer drought 9,12,43,44, because hgher temperature and longer growng season wll accelerate greater ecosystem respraton and may exacerbate water stress n summer. However, much larger seasonal CO 2 ampltude change was found over north of 45 N, whch s manly due to summer carbon uptake, than that for 10 to 45 N from 1960 s to 2010 s n the North Hemsphere 45, ndcatng that summer NEP was more greatly enhanced at boreal than temperate zones over the 50-year perod. Although the hgh potental of carbon assmlaton n North Amercan hgh lattude ecosystems may be offset by the warmng nduced hgh respraton and drought stress n some regons, the boreal forest ecosystems wll contnue to play an mportant role n sequesterng atmospherc CO 2 durng the growng season under warmng clmate. Ths study shows that the long-term trend and nter-annual varablty of GPP s domnated by GPP max based on both VPM GPP and data from 24 AmerFlux stes. Although GS start and GS end also exert strong control over annaul GPP, ther contrbutons to annual GPP change are much weaker than GPP max, ndcatng great mportance of physologcal change on annual GPP varablty under changng clmate. The consstently postve responses of the three ndcators to warmng temperature reveal that annual carbon assmlaton wll beneft from the warmng clmate n hgh lattudes, although the ecosystem respraton and drought stress may reduce the net ecosystem productvty n some regons; on the contrary, the dvergent responses of plant phenology and physology to the warmng temperature reduce annual carbon uptake over part of low and md-lattudes n North Amerca. Methods Data sets. A regonal GPP product n North Amerca from 2000 to 2014 was produced usng the vegetaton photosynthess model (VPM) 46,47. VPM s a producton effcency model whch uses the product of the photosynthetcally actve radaton absorbed by chlorophyll and a lght use effcency factor to estmate GPP 48. The regonal VPM GPP product has been valdated usng both flux tower data and the solar-nduced chlorophyll fluorescence (SIF) data from the Global Ozone Montorng Experment-2 (GOME-2) across North Amerca 46. The VPM GPP agrees well wth flux tower derved GPP at 39 AmerFlux stes (R 2 = 0.82 for all stes) and shows good consstency wth the GOME-2 SIF data n terms of spatal dstrbuton and seasonal dynamcs 46. The three ndcators were derved from the 8-day 0.05 degree VPM GPP product for each grd cell n ths study over the perod across North Amerca. The three ndcators were also derved at ecosystem scale usng the eddy covarance data from 24 AmerFlux stes (Table S1). There are sx vegetaton types among the 24 stes, ncludng Decduous Broadleaf Forest (DBF), Evergreen Needle-leaf Forest (ENF), Mxed Forest (MF), Cropland (CRO), Grassland (GRA), Closed Shrub Land (CSH). Most of the stes are located at temperate clmate zones, and only two ENF stes located at boreal clmate zones (Fg. S1). The data records at ndvdual stes range from 6 to 21 years, and there are 253 ste-years n total. Half-hourly GPP estmates were derved from net ecosystem exchange measurements, whch were gap-flled and parttoned usng the R package REddyProc ( followng the method of Rechsten et al. 49. The half-hourly GPP was aggregated to daly GPP tme seres to derve the three ndcators for each ste year. The temperature, precptaton and downward solar radaton data used for senstvty analyss are from the Natonal Center for Envronmental Predcton-North Amercan Regonal Reanalyss (NARR) products 50. Daly NARR temperature, precptaton and solar radaton data at 32 km spatal resoluton were spatally nterpolated nto 0.05 degree and then temporally aggregated to obtan the seasonal and annual data. The clmatc data durng the preseason perod,.e., 30 days precedng the mean dates of GS start and GS end durng , were calculated for clmatc senstvty analyses. Snce GPP max occurred n June-August for more than 99.9% of the study area (Fg. S3), we used the clmatc data n summer (June-July-August) to evaluate the clmatc senstvty of GPP max. Annual GPP was correlated to annual temperature, precptaton and solar radaton to nvestgate the clmatc senstvty of annual GPP. In vew of the strong relatonshps between GS start and sprng GPP, GPP max and summer GPP, and GS end and autumn GPP 14, the clmatc senstvty of annual GPP can be better understood by combnng the responses of the three ndcators to ther respectve seasonal clmatc factors. Indcator dentfcaton. The three ndcators, GS start, GPP max and GS end, were determned from the smoothed tme seres of GPP for each year. In case of some abnormal values, the sngular spectrum analyss was performed to derve smoothed daly GPP curves for the 253 ste-years. The Rssa package ( org/web/packages/rssa/ndex.html) n R was used to obtan smoothed daly GPP curve. Frst, the daly GPP seres were decomposed nto new tme seres whch consst of dfferent frequency components and noses accordng to the sngular value decomposton. Second, the seasonal sgnal,.e., the smoothed daly GPP, was reconstructed from the decomposed components. In ths study, we used the frst four components correspondng to the lowest frequency sub-sgnals to derve the smoothed daly GPP curve from the orgnal tme seres. In terms of the VPM GPP product, a least-square regresson analyss was performed between the 8-day GPP and the correspondng day of year (DOY) for the whole year. We used a sxth-degree polynomal functon to ft the seasonal GPP curve as a functon of DOY 15 GPP = a + a DOY + a DOY + a DOY + a DOY + a DOY + a DOY + ε (1) where a ( = 0~6) are the ftted parameters and ε s the error term. Based on the equaton (1), a smoothed GPP curve can be constructed for the determnaton of the three ndcators. GPP max was determned as the peak value of the smoothed GPP curve. GS start and GS end were dentfed as the frst and last days when the smoothed GPP Scentfc Reports 7:41366 DOI: /srep

8 crossed a gven threshold. In ths study, the threshold was set to be 10% of the long-term average GPP max over all the avalable years for each ste and over for each grd cell 14. The SMIPP model. The three ndcators, GS start, GPP max, and GS end, are nvolved n the SMIPP to represent the phenologcal and physologcal mpacts on annual GPP, and ther contrbutons to annual GPP change are seperated based on a total dfferental functon. Frstly, annual GPP s expressed as a functon of the three ndcators, that s GPP = f ( GS, GPP, GS ) (2) start max end Assumng the three ndcators are ndependent of one another, the total dfferental of GPP wth respect to all the three ndcators s = GPP dgpp dgs GS start start + GPP GPP max dgpp max + GPP dgs GS Snce the three partal dervatves denote the senstvty of annual GPP wth respect to the changes n the three ndcators, we use three senstvty coeffcents η start, η max, η end to represent the three partal dervatves. In practce, the dfferentals of annual GPP and of the three ndcators are approxmated by the anomales (Δ) of the varables, namely, the dfferences between the varables wth respect to ther long-term mean values. Thus, the equaton (3) transforms nto GPP = η GS + η GPP + η GS (4) end start start max max end end To make the anomales of GS start easer to compare wth those of GS end, anomales are by conventon, counted postve when GS start advances and when GS end delays relatve to ther long-term mean values. Wth the observed anomales of annual GPP and the three ndcators, the three senstvty coeffcents can be estmated based on a multple regresson for each grd cell of the VPM GPP product or of GPP observed at each flux tower ste. Thus, the annual GPP anomaly s separated nto three ndependent components,.e., η start ΔGS start, η max ΔGpp max, η end ΔGS end, representng the annual GPP change nduced by the three ndcators, respectvely. Attrbuton analyss. The relatve contrbutons of the changes n the three ndcators to the long-term trend and nter-annual varablty were calculated. As shown n equaton (4), annual GPP anomaly conssts of three ndependent components, thus, the long-term trend of annual GPP can also be separated nto three ndependent trends, expressed by Slope start, Slope max and Slope end. Because the three ndcators may contrbute postvely or negatvely to the long-term trend of annual GPP, the relatve contrbutons of them were calculated as the ratos of Slope start, Slope gpp, Slope end over the total absolutes of these three slopes. ξ = s, start Slopestart Slope + Slope + Slope (5) start max end end (3) ξ = smax, Slopemax Slope + Slope + Slope (6) start max end ξ = send, Slopeend Slope + Slope + Slope (7) start max end where ξ s, start, ξ smax,, and ξ send, represent the relatve contrbutons of the trends of the three ndcators related components of GPP to the long-term lnear trend of annual GPP. In equatons (5) (7), a postve sgn denotes an ncreasng trend of annual GPP contrbuted by the correspondng ndcator, and vce versa, and the magntude denotes the amount of the relatve contrbuton. The relatve contrbutons of the changes n the three ndcators to the nter-annual varablty of GPP were calculated accordng to the consstency of η GS start start, η max GPP max, η end GS end wth annual GPP anomaly over the perod ξ ξ vstart, vmax, ξ vend, η = η = GPP GS start start, GPP GPP (8) GPP max max GPP, GPP GPP (9) GPP η GS end end, GPP = GPP (10) Scentfc Reports 7:41366 DOI: /srep

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