Fire frequency drives decadal changes in soil carbon and nitrogen and ecosystem productivity
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- Frederica Reed
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1 doi:.38/nture24668 Fire frequency drives decdl chnges in soil cron nd nitrogen nd ecosystem productivity Adm F. A. Pellegrini, Anders Ahlström,2, Srh E. Hoie 3, Peter B. Reich 4,5, Lrs P. Nierdzik 6, A. Crl Stver 7, Brynt C. Schrenroch 8, Ari Jumpponen 9, Willim R. L. Anderegg, Jmes T. Rnderson & Roert B. Jckson,2 Fire frequency is chnging glolly nd is projected to ffect the glol cron cycle nd climte 3. However, uncertinty out how ecosystems respond to decdl chnges in fire frequency mkes it difficult to predict the effects of ltered fire regimes on the cron cycle; for instnce, we do not fully understnd the long-term effects of fire on soil cron nd nutrient storge, or whether fire-driven nutrient losses limit plnt productivity 4,5. Here we nlyse dt from 48 sites in svnn grsslnds, rodlef s nd needlelef s spnning up to 65 yers, during which time the frequency of fires ws ltered t ech site. We find tht frequently urned plots experienced decline in surfce soil cron nd nitrogen tht ws non-sturting through time, hving 36 per cent (±3 per cent) less cron nd 38 per cent (±6 per cent) less nitrogen fter 64 yers thn plots tht were protected from fire. Fire-driven cron nd nitrogen losses were sustntil in svnn grsslnds nd rodlef s, ut not in temperte nd orel needlelef s. We lso oserve comprle soil cron nd nitrogen losses in n independent field dtset nd in dynmic model simultions of glol vegettion. The model study predicts tht the long-term losses of soil nitrogen tht result from more frequent urning my in turn decrese the cron tht is sequestered y net primry productivity y out 2 per cent of the totl cron tht is emitted from urning iomss over the sme period. Furthermore, we estimte tht the effects of chnges in fire frequency on ecosystem cron storge my e 3 per cent too low if they do not include multidecdl chnges in soil cron, especilly in drier svnn grsslnds. Future chnges in fire frequency my shift ecosystem cron storge y chnging soil cron pools nd nitrogen limittions on plnt growth, ltering the cron sink cpcity of frequently urning svnn grsslnds nd rodlef s. Fire regimes hve een ltered y chnges in climte nd lnd use, nd re predicted to chnge further s tempertures rise nd popultions grow 3. In consequence, the response of ecosystems to long-term ltertions in fire frequency tht is, either more frequent urning or fire suppression will e essentil to the future of the terrestril cron sink 3,6. Although cron fluxes to the tmosphere from comusting plnt iomss hve een well chrcterized 7, uncertinties remin concerning the responses of soil cron nd nutrient pools 4,5, which lso regulte plnt primry productivity 8. On the one hnd, incresed urning my decrese soil orgnic mtter, s repeted urning reduces orgnic inputs to soils nd leds to declines in soil cron (C) nd nutrients 9. On the other hnd, incresed urning my enrich C nd nutrient concentrtions in soils y promoting the estlishment of more-productive plnt species 2 nd the leching of sh downwrds into soils 3. Oservtions generlly illustrte tht single fires deplete pools of C nd nutrients in the surfce litter lyer nd, in some cses, in shllow orgnic horizons 4,5. Criticlly, however, studies tht document chnges in soils over short timescles or in response to single fire (see, for exmple, refs 3, 4) offer limited insight into long-term chnges in the lrger minerl soil pools s result of shifting fire regimes, prticulrly in soils elow the top few centimetres; such soils re generlly not suject to direct consumption 6 nd re influenced more y fire-induced chnges in plnt inputs nd microil ctivity,7. Thus generlized long-term effects of chnges in fire frequencies on soil C nd nitrogen, nd on their controlling mechnisms, remin uncler, with contrsting results oserved in studies of different regions or ecosystems,,7. A lck of consensus on the long-term response of soils to fire limits our ility to predict how vegettion productivity my chnge s fire lters soil nutrient vilility. Over the short-term, single fires cn stimulte plnt productivity 8 ; however, over the longer-term, potentil declines in soil nutrients with incresed fire frequency 9 hve een hypothesized to suppress productivity, lthough long-term evidence for this effect is limited. These interctions my determine whether fire reduces ecosystem C storge y depleting soil C nd nutrients, which my reduce plnt growth nd turnover, further constrining C storge in the ecosystem (Supplementry Fig. ). Here, we evlute these interctions y exmining how long-term differences in fire frequency lter soil C nd nutrients nd ccompnying shifts in plnt productivity, using three pproches. First, we use met-nlysis of dt from 48 sites worldwide (Fig. ) to test how frequent urning lters soil C nd nutrients over time spns s long s 65 yers. We then evlute our results using n independent dtset from 6 dditionl field sites, which were not replicted t the site scle (nd thus were not included in the met-nlysis), ut collectively re vlule given the high numer of sites nd stndrdized dt collection. Finlly, we use our results to vlidte n individul-sed dynmic glol vegettion model (the DGVM LPJ-GUESS-BLAZE) for quntifying the effect of fire-driven nutrient losses on vegettion productivity nd the degree to which soils contriute to ecosystem-level chnges in C. The sites included in the met-nlysis compred the effects of chnges in long-term fire frequencies on C nd nutrients in the upper soil lyer ( 2 cm depth); the verge tretment length ws 3 yers nd rnged from 9 65 yers. Sites generlly contined plots tht either experienced elevted fire frequency (4.3 ±.6 times more thn the estimted historicl men for tht ecosystem, clculted over the length of the study) or were protected from fire (complete fire exclusion in ll ut one cse), which we refer to herefter s elevted nd protected tretments, respectively (see Supplementry Informtion). Sites covered Deprtment of Erth System Science, Stnford University, Stnford, Cliforni 9435, USA. 2 Deprtment of Physicl Geogrphy nd Ecosystem Science, Lund University, Lund, Sweden. 3 Deprtment of Ecology, Evolution, nd Behvior, University of Minnesot, St Pul, Minnesot 558, USA. 4 Deprtment of Forest Resources, University of Minnesot, St Pul, Minnesot 558, USA. 5 Hwkesury Institute for the Environment, Western Sydney University, Sydney, New South Wles, Austrli. 6 Centre for Environmentl nd Climte Reserch, CEC, Lund University, Lund, Sweden. 7 Deprtment of Ecology nd Evolutionry Biology, Yle University, New Hven, Connecticut 652, USA. 8 College of Nturl Resources, University of Wisconsin Stevens Point, Stevens Point, Wisconsin 5448, USA. 9 Division of Biology, Knss Stte University, Mnhttn, Knss 6656, USA. Deprtment of Biology, University of Uth, Slt Lke City, Uth 842, USA. Deprtment of Erth System Science, University of Cliforni Irvine, Irvine, Cliforni 92697, USA. 2 Woods Institute for the Environment nd Precourt Institute for Energy, Stnford University, Stnford, Cliforni 9435, USA. 94 NATURE VOL 553 jnury Mcmilln Pulishers Limited, prt of Springer Nture. All rights reserved.
2 RESEARCH n = 2 Study length (yers) n = 6 n = n = 4 n = 8 Numer of pixels with fire ctivity, 5, Men nnul temperture ( C) Men nnul precipittion (cm yr ) 6 Borel Svnn grsslnd Numer of pixels with fire ctivity 4, 8, Figure Distriution of study sites., Geogrphicl distriution of sites (n = 48), with dot size representing study durtion., Climtic distriution of sites. Bottom left, vegettion types re indicted y different colours plotted over modified digrm of Whittker s iomes 3 (, tundr; 2, orel ; 3, woodlnd/shrulnd; 4, temperte grsslnd/ desert; 5, temperte ; 6, temperte rin; 7, sutropicl desert; 8, tropicl nd svnn; 9, tropicl rin). Dots re slightly trnsprent to llow overlp to e visulized. The histogrms ove nd to the right illustrte the frequency distriution of glol fire ctivity for given climtic condition. Fire ctivity ws determined using gridded mps of men fire occurrence tken from the glol fire emissions dtse 4 with smll fires (GFED4s) 7. rod rnge of men nnul temperture ( 5 27 C) nd precipittion (4 2,4 mm yr ) (Fig. nd Supplementry Fig. 2). To evlute whether fire effects depended on plnt communities, we ctegorized sites on the sis of the dominnt plnt functionl type into svnn grsslnds, rodlef s nd needlelef s. Sttisticl significnce ws evluted using mixed-effects models of the logrithmic response rtio (nturl logrithm of the quotient etween elementl concentrtion in elevted nd protected plots), weighted y site repliction nd vrince 9 (Supplementry Fig. 3). We found tht elevted fire frequencies sustntilly decresed totl soil C nd nitrogen (N) concentrtions glolly, with the lrgest effects oserved in rodlef s nd svnn grsslnds. Averged cross ll sites, vegettion types, nd tretment lengths, higher fire frequencies reduced the concentrtions of totl soil C nd N concentrtions y 2.% (confidence intervl ±.2%; P =.2) nd.4% (±.%; P =.4), respectively, compred with plots protected from fire (Fig. 2, nd Supplementry Tle ; 3-yer men tretment length). Within vegettion types, fires hd strong depletion effects on soils in oth rodlef s (27% less C nd 25% less N in elevted versus protected plots; P <. nd P =.2, respectively) nd svnn grsslnds (2% less C nd N in elevted versus protected plots; P <. for ech; Fig. 2, nd Supplementry Tle ). By contrst, soil C nd N in needlelef s incresed y 26% nd 2%, respectively, in elevted compred with protected plots (P <. for ech; Fig. 2, nd Supplementry Tle ). The different responses tht we oserved in needlelef s were unlikely to e cused y climtic vriles or study design, given tht, in our dtset, there were no differences etween sites in temperte needlelef s nd those in svnn.5 Cron Nitrogen Totl Svnn grsslnd c Cron Nitrogen Figure 2 Effects of fire on soil cron nd nitrogen cross ecosystems nd over time.,, Logrithmic response rtios of the concentrtions of C (, n = 4) nd N (, n = 38) for the totl dtset compiled nd prtitioned into different vegettion types (see Supplementry Tles nd 2 for sttistics). The response rtio is defined s the concentrtion of C or N in elevted plots divided y the concentrtion in protected plots. c, d, Regressions etween the response rtios of C (c, n = 3) or N (d, n = 27) nd the length of time during which plots experienced contrsting fire frequencies, fitted for svnn grsslnds (SG) plus d Length of tretment (yers) NL SG + BL NL SG + BL e Soil C flux (Mg C h yr ) f Soil N flux (kg N h yr ) Svnn grsslnd.. rodlef s (BL) using met-regression. Pink dots represent dt from needlelef s (NL), which were not used in the regression. e, f, Totl fluxes of C (e) nd N (f), determined s the solute rte of chnge in soil C or N etween the fire frequency tretments (negtive vlues indicte losses under frequent urning). Dshed lines represent 95% confidence intervls (for c, d) nd error rs represent either 95% confidence intervls (for,, e, f) or the vrince round the logrithmic response rtio (for c, d; see ref. 9), with sterisks indicting significnce t P <.5 nd dots t P <. (Supplementry Tles 4 nd 5). jnury 28 VOL 553 NATURE Mcmilln Pulishers Limited, prt of Springer Nture. All rights reserved.
3 RESEARCH Letter grsslnds nd rodlef s in climtic conditions, smpling depths, or fire frequency in elevted plots (Supplementry Tles 2 nd 3). The effect of fire in orel needlelef s, which differ sustntilly in climte compred with the other vegettion types (Fig. ), ws similr to its effect in temperte needlelef s (see Supplementry Informtion). N stocks in minerl soils tended to increse with more frequent urning (r 2 =.24, P =.58), wheres C stocks displyed no trend (Supplementry Fig. 4). In svnn grsslnds nd rodlef s, the severity of firedriven losses of soil C nd N incresed significntly with the length of time for which plots experienced ltered fire frequencies. Soils in elevted plots were estimted to hve 36% nd 38% less C (P =.26) nd N (P =.22), respectively, thn those in protected plots fter 64 yers (the mximum durtion in svnn grsslnd nd rodlef sites; Fig. 2c, d nd Supplementry Tle 4). Furthermore, for oth C nd N, the difference etween elevted nd protected plots differed significntly (P <.5) only fter 8 yers of contrsting fire frequencies, highlighting tht effects emerge over decdl timescles. By contrst, the responses in needlelef s were unchnged with incresing durtion of fire tretment (P >.5 for C nd N; Fig. 2c, d). To further evlute the generlity of our glol met-nlysis, we nlysed n independent dtset from network of 6 dditionl field experiments cross the southestern United Sttes (see Supplementry Informtion). Of those sites tht experienced different fire frequencies for durtion sufficient to detect potentil effect, 83% showed declines in C nd 67% showed declines in N with frequent urning; elevted sites hd on verge 3% nd % lower C nd N, respectively, thn did protected plots (Supplementry Fig. 5). Considering the shorter verge length of time tht these plots experienced different fire frequencies (22 yers), the men responses re consistent with results from the glol met-nlysis regression etween C nd N losses nd study length (7% ± % for C nd N; Supplementry Fig. 5). To determine chnges in totl stocks of C nd N in response to fire ltertions, we comined elementl concentrtions with soil ulk densities to stndrdized depth of cm, nd normlized stock chnges to n nnul rte from the met-nlysis. The suset of studies tht did not provide ulk density dt required vlues to e extrpolted on the sis of soil texture or y using the men vlue (see Supplementry Informtion). Plots exposed to elevted fire frequencies experienced lrge verge losses of soil C nd N stocks reltive to protected plots in svnn grsslnds (.2 Mg C h yr nd 4.5 kg N h yr ; P <. for oth) nd rodlef s (.57 Mg C h yr nd 24.3 kg N h yr ; P <.5 nd P <., respectively) (Fig. 2e, f nd Supplementry Tle 5). By contrst, there ws no chnge in soil C stocks, nd mrginlly significnt enrichment of soil N, in needlelef s in elevted plots (+8.4 kg N h yr ; P <.) (Fig. 2e, f nd Supplementry Tle 5). We found little evidence tht incresed fire frequencies depleted other elements esides C nd N. Averged cross ll sites, surfce minerl soils in elevted plots showed no chnge in concentrtions of phosphorus (P) reltive to protected plots (Fig. 3 nd Supplementry Tle 6), ut they were enriched in clcium (+52%; P <.) nd potssium (+3%; P =.2) (Supplementry Tle 6). The durtion of fire frequency ltertions influenced the direction nd significnce of results only for soil P. Concentrtions of P were initilly enriched in the elevted plots fter decde of urning (+5%; P =.), ut this effect disppered fter out 3 yers of frequency ltertions (Fig. 3 nd Supplementry Tle 7). Longer-term studies re needed to determine whether exposure to fire will deplete soil P ecuse of enhnced erosion; however, of the five sites in our nlysis tht experienced more thn 5 yers of ltered fire frequencies, only one ws depleted in P. The lck of P, potssium nd clcium losses following long-term chnges in fire frequency is consistent with the hypothesis tht their higher oxidtion tempertures nd/or soil sorption cpcities decrese losses during frequent urning compred with C nd N 2. Chnges in fire frequency cn lso lter plnt-ville nutrients. Across the glol dtset, elevted-frequency plots hd 25% lower concentrtions of inorgnic N (the min form of N ville to plnts) reltive to protected plots (P <.), with positive correltion found etween totl N nd inorgnic N response rtios (Supplementry Fig. 6). By contrst, there ws no significnt effect of fire frequency on concentrtions of inorgnic P (the min form of P ville to plnts). The responses of inorgnic P nd totl P were positively correlted (Supplementry Fig. 7). Our dt clerly show tht the oserved significnt increses in inorgnic N immeditely following fires (see, for exmple, ref. 4) re trnsient, nd often reverse with repeted urning. Given the importnce of soil N for sustined productivity, we next evluted the degree to which N losses might constrin plnt net primry productivity (NPP), potentilly restricting C uptke. To do so, we simulted the effect of fire on ecosystem C nd N y using the DGVM LPJ-GUESS 2 with the process-sed fire module BLAZE (see Supplementry Informtion). For ech study site, we simulted ecosystem dynmics for the period 95 23, using fire frequencies, climte, nd N deposition specific to ech site, s well s chnges in glol CO 2 concentrtions (see Supplementry Informtion). Like our empiricl dt, the model showed losses (leit smller ones) of totl soil C nd N in response to frequent urning in oth rodlef s nd svnn grsslnds (Supplementry Figs 8 nd 9). However, the model lso simulted net losses of soil C nd N from needlelef sites, unlike the empiricl dt (Supplementry Fig. ), illustrting the need for further model development nd dditionl dt. In rodlef s nd svnn grsslnds, simulted declines in totl soil C were equivlent to 2% of the cumultive nnul C fluxes y comustion of plnt iomss nd 3% of the decrese in the totl plnt iomss C in plot. Compring pired simultions t ech site, either including or excluding N losses, illustrted tht fire-driven N losses reduced cumultive NPP y out 5% over the entire 63-yer period of the simultion on verge cross sites (Supplementry Fig. 8). The chnges in NPP were of sustntil mgnitude reltive to other C fluxes, with the totl reduction in C drwdown from NPP eing equivlent to 2% of the totl nnul C emissions from comustion of plnt iomss summed over the simultion period, verged cross sites. We next ssessed the potentil generlity of fire-induced soil C nd N losses chnging ecosystem C storge nd productivity y performing simultions cross svnn grsslnds glolly; these ecosystems represent out 7% of ctul glol urned re 7 (see Supplementry Informtion). When ll loctions were urned t iennil frequency, declines in soil C stocks were equivlent to 4% of the chnges in P C K Totl Svnn grsslnds s s Soil P Length of tretment (yers) Figure 3 Responses of P, C nd K to chnges in fire frequency., Logrithmic response rtios of the concentrtions of P (n = 6), C (n = 6) nd K (n = 8) for the totl dtset compiled nd prtitioned into different ecosystem ctegories. The response rtio is defined s the concentrtion of P, C or K in elevted plots divided y the concentrtion in protected plots., Chnge in the logrithmic response rtio of soil P s function of the length of time during which plots experienced contrsting fire frequencies. Error rs in indicte the 95% confidence intervls nd those in indicte the vrince round the response rtio nd dshed lines in re 95% confidence intervls, with n sterisk indicting significnt effects (P <.5). See Supplementry Tles 6 nd 7 for sttistics. 96 NATURE VOL 553 jnury Mcmilln Pulishers Limited, prt of Springer Nture. All rights reserved.
4 RESEARCH NPP with N losses/ without N losses > NPP (kg C m 2 yr ) Bseline High fire, no N losses High fire, N losses c NPP N losses/ NPP no N losses Glol svnn grsslnds Yer Figure 4 Effect of N losses on net primry productivity (NPP) cross svnn grsslnds glolly. Simultions were run y inititing high fire frequency in 95 (with grid cells urned every two yers) nd trcking NPP until 23 with nd without N losses., Reltive rtio of cumultive NPP etween the two scenrios, with the colour r scled y quntiles (vlues re minimum (.63), first, second nd third quntiles (.89,.92 nd.96), nd mximum ()). Green cells illustrte res where N losses stimulted NPP (where the rtio is greter thn )., Men NPP simulted cross svnn grsslnds, weighted y the re of grid cell. The shrp reduction in NPP in 95 (grey verticl line) is cused y the initition of plnt iomss C stocks, on verge, with the reltive contriution of declines in soil C eing gretest in driest loctions (Supplementry Fig. ; r 2 =.45). Furthermore, N losses resulted in widespred declines in NPP (Fig. 4), with the lrgest effect on NPP seen in wet tropicl regions, proly ecuse of higher potentil productivity nd N demnd. The effect of N losses on NPP incresed through time (Fig. 4, c), mounting to 9% reduction of NPP in svnn grsslnds glolly when summed over the entire simultion period nd re. Consequently, omitting the multidecdl chnges in soil pools tht result from shifting fire frequencies my sustntilly underestimte ecosystem C losses. Our results revel severl fctors tht regulte how fire ffects C nd N in soils, nd shed light on potentil responses under future fire regimes. First, the effect of fire on oth C nd N strengthened through time nd emerged only over multiple decdes. The lck of sturting response ws surprising, nd suggests tht shifts in fire frequency during the twenty-first century 3 my lter soil C nd N over n extensive lnd re. Considering chnges in soil C over longer time periods especilly through the formtion of pyrogenic C, which cn influence long-term C storge nd nutrient dynmics 22,23 will provide dditionl insight into the stility of C in the soils nd when effects my sturte. Second, whether fire chnged soil C nd N nd y how much depended on vegettion type cross our nlysis. The enrichment of N in needlelef soils could e ttriutle to numer of processes, such s coloniztion y N-fixing plnt species 24 or redistriution of moilized N during the smouldering of the thick floor tht is chrcteristic of needlelef s 25. Whether our results from needlelef s tht primrily received frequent, low-intensity prescried fires re representtive of colder needlelef s tht experience less frequent, ut more intense, wildfires requires further evlution, especilly for orel s. Although we found qulittively similr responses Yer the prescried higher fire frequency scenrios, where N is lost y fire (lue line) or not lost y fire (red line). The grey line shows the evolution of NPP s predicted internlly in the dynmic glol vegettion model LPJ-GUESS with fires determined vi BLAZE operting dynmiclly (for exmple, s for the period efore 95). c, Model simultions of the rtio etween NPP with N losses versus without N losses through time, verged cross svnn grsslnds glolly (ech circle is glol verge within yer); the solid line represents five-yer rolling verge nd the dshed lines represent the stndrd errors cross grid cells. of orel nd temperte needlelef s, more orel studies in prticulr re needed to test the generlity in the response nd ppliction over longer fire-return intervls nd for severe crown fires tht cn consume the soil orgnic lyer 26. Studies of grdients in longterm fire frequencies re lcking t present nd do not lwys exmine chnges in minerl soils (see, for exmple, ref. 26). Further considertion is lso needed for reltively wet ecosystems, such s some tropicl rins, tht re now experiencing more frequent urning ecuse of humn ctivities nd drying climtes 27. More frequent slsh-nd-urn cycles, for exmple, hve een shown to deplete soil C, N nd P 28 in tropicl rins. Our oservtion tht the initil P enrichment fdes through time my e criticl component in determining the response of P-limited tropicl rins 29 to chnges in fire frequency. Projecting the effect of chnges in fire frequency on ecosystem C storge lso needs etter understnding of historicl fire regimes. We compred historicl fire frequencies to our elevted nd protected fire tretments y using dt from suset of the loctions included in the met-nlysis (n = 25) tht hd intermedite fire frequencies to pproxi mte historicl nturl urning (see Supplementry Informtion). Compred with these intermedite fire frequencies, more frequent urning significntly decresed C nd N concentrtions ( 3% C nd N, P =.7 nd P <., respectively), wheres less frequent urning significntly incresed C nd N concentrtions (+9% C nd +8% N, P =.5 nd P <., respectively) in svnn grsslnds (Supplementry Tle 8 nd Supplementry Fig. 2). Anlyses of rodlef sites hd less sttisticl power, ut suggested tht differences occurred primrily ecuse of greter losses in elevted-frequency reltive to historicl-frequency plots. In needlelef s, fire tended to enrich N in historicl-frequency versus protected plots, ut elevted versus historicl-frequency plots were comprle. Consequently, the significnt chnges we oserved when jnury 28 VOL 553 NATURE Mcmilln Pulishers Limited, prt of Springer Nture. All rights reserved.
5 RESEARCH Letter compring elevted-frequency versus protected plots re ttriu tle oth to C nd N ccumultion during fire protection, nd to C nd N loss during incresed urning. In conclusion, our results revel the sensitivity of surfce soils to fire nd the sustntil effects tht chnges in soil pools hve on long-term ecosystem C exchnge. The lrge empiricl nd conservtive modelsed estimtes of soil C chnges suggest tht present estimtes of fire-driven C losses 7, which primrily consider losses from plnt iomss pools, my sustntilly underestimte the effects of long-term trends in fire frequencies in svnn grsslnds nd rodlef s in prticulr. Our findings suggest tht future ltertions in fire regimes in svnn grsslnds nd rodlef s my shift ecosystem C storge y chnging soil C levels nd chnging the N limittion of plnt growth, ltering the cron-sink cpcity of these fire-prone ecosystems. Dt Avilility The dtsets generted nd nlysed during this study re ville from the corresponding uthor on request nd in the corresponding ppers cited in Supplementry Informtion. received 8 April; ccepted 9 Octoer 27. Pulished online Decemer 27.. Westerling, A. L., Hidlgo, H. G., Cyn, D. R. & Swetnm, T. W. Wrming nd erlier spring increse western US wildfire ctivity. Science 33, (26). 2. Knorr, W., Arneth, A. & Jing, L. Demogrphic controls of future glol fire risk. Nt. Clim. Chng. 6, (26). 3. Andel, N. et l. A humn-driven decline in glol urned re. Science 356, (27). 4. Joágy, E. G. & Jckson, R. B. The verticl distriution of soil orgnic cron nd its reltion to climte nd vegettion. Ecol. Appl., (2). 5. Jckson, R. B., Bnner, J. L., Joágy, E. G., Pockmn, W. T. & Wll, D. H. Ecosystem cron loss with woody plnt invsion of grsslnds. Nture 48, (22). 6. Rnderson, J. T. et l. The impct of orel fire on climte wrming. Science 34, 3 32 (26). 7. vn der Werf, G. R. et l. Glol fire emissions estimtes during Erth Syst. Sci. Dt 9, (27). 8. LeBuer, D. S. & Treseder, K. K. Nitrogen limittion of net primry productivity in terrestril ecosystems is glolly distriuted. Ecology 89, (28). 9. Pellegrini, A. F. A., Hoffmnn, W. A. & Frnco, A. C. Cron ccumultion nd nitrogen pool recovery during trnsitions from svnn to in centrl Brzil. Ecology 95, (24).. DeLuc, T. H. & Sl, A. Frequent fire lters nitrogen trnsformtions in ponderos pine stnds of the inlnd northwest. Ecology 87, (26).. Reich, P. B., Peterson, D. W., Wedin, D. A. & Wrge, K. Fire nd vegettion effects on productivity nd nitrogen cycling cross -grsslnd continuum. Ecology 82, (2). 2. Newlnd, J. A. & DeLuc, T. H. Influence of fire on ntive nitrogen-fixing plnts nd soil nitrogen sttus in ponderos pine Dougls-fir s in western Montn. Cn. J. For. Res. 3, (2). 3. Boerner, R. E. J., Hung, J. & Hrt, S. C. Impcts of fire nd fire surrogte tretments on soil properties: met-nlyticl pproch. Ecol. Appl. 9, (29). 4. Wn, S., Hui, D. & Luo, Y. Fire effects on nitrogen pools nd dynmics in terrestril ecosystems: met-nlysis. Ecol. Appl., (2). 5. Nery, D. G., Kloptek, C. C., DeBno, L. F. & Ffolliott, P. F. Fire effects on elowground sustinility: review nd synthesis. For. Ecol. Mnge. 22, 5 7 (999). 6. Kuffmn, J. B., Cummings, D. L., Wrd, D. E. & Bitt, R. Fire in the Brzilin Amzon:. Biomss, nutrient pools, nd losses in slshed primry s. Oecologi 4, (995). 7. Pellegrini, A. F. A., Hedin, L. O., Stver, A. C. & Govender, N. Fire lters ecosystem cron nd nutrients ut not plnt nutrient stoichiometry or composition in tropicl svnn. Ecology 96, (25). 8. Knpp, A. K. & Sestedt, T. R. Detritus ccumultion limits productivity of tllgrss pririe. Bioscience 36, (986). 9. Hedges, L. V., Gurevitch, J. & Curtis, P. S. The met-nlysis of response rtios in experimentl ecology. Ecology 8, 5 56 (999). 2. DeBno, L. F., Nery, D. G. & Ffolliott, P. F. Fire Effects on Ecosystems (John Wiley, 998). 2. Smith, B. et l. Implictions of incorporting N cycling nd N limittions on primry production in n individul-sed dynmic vegettion model. Biogeosciences, (24). 22. Sntín, C. et l. Towrds glol ssessment of pyrogenic cron from vegettion fires. Glo. Chnge Biol. 22, 76 9 (26). 23. DeLuc, T. H. & Aplet, G. H. Chrcol nd cron storge in soils of the Rocky Mountin West. Front. Ecol. Environ. 6, 8 24 (28). 24. DeLuc, T. H., Zckrisson, O., Nilsson, M.-C. & Sellstedt, A. Quntifying nitrogen-fixtion in fether moss crpets of orel s. Nture 49, (22). 25. McKee, W. H. Chnges In Soil Fertility Following Prescried Burning On Costl Plin Pine Sites (Southestern Forest Experiment Sttion, 982). 26. Wrdle, D. A., Hörnerg, G., Zckrisson, O., Klel-Brundin, M. & Coomes, D. A. Long-term effects of wildfire on ecosystem properties cross n islnd re grdient. Science 3, (23). 27. Dvidson, E. A. et l. The Amzon sin in trnsition. Nture 48, (22). 28. Rmkrishnn, P. S. & Toky, O. P. Soil nutrient sttus of hill gro-ecosystems nd recovery pttern fter slsh nd urn griculture (Jhum) in north-estern Indi. Plnt Soil 6, 4 64 (98). 29. Vitousek, P. M., Porder, S., Houlton, B. Z. & Chdwick, O. A. Terrestril phosphorus limittion: mechnism, implictions, nd nitrogen-phosphorus interctions. Ecol. Appl. 2, 5 5 (2). 3. Ricklefs, R. E. The Economy of Nture (WH Freemn, 28). Supplementry Informtion is ville in the online version of the pper. Acknowledgements We thnk ll uthors of the studies used in the metnlysis; the Cedr Creek Long Term Ecologicl Reserch progrmme; The Morton Aroretum Center for Tree Science progrmme; nd J. Hrden, L. Hedin, S. Pcl nd M. Turner for providing feedck. Funding ws provided y Ntionl Ocenic nd Atmospheric Administrtion (NOAA) Climte nd Glol Chnge Postdoctorl Fellowship (to A.F.A.P.); the Gordon nd Betty Moore Foundtion (R.B.J.); the ModElling the Regionl nd Glol Erth system (MERGE) (L.P.N.); nd the Deprtment of Energy Office of Science Biologicl nd Environmentl Reserch (J.T.R.). Author Contriutions A.F.A.P. nd R.B.J. conceived of nd designed the study, with input from A.A.; A.F.A.P., S.E.H., P.B.R., B.C.S. nd A.J. collected nd contriuted dt; A.F.A.P. performed sttisticl nlyses; L.P.N. developed the fire model; nd L.P.N. nd A.A. performed model simultions. A.F.A.P. wrote the first drft nd ll uthors contriuted feedck. Author Informtion Reprints nd permissions informtion is ville t The uthors declre no competing finncil interests. Reders re welcome to comment on the online version of the pper. Pulisher s note: Springer Nture remins neutrl with regrd to jurisdictionl clims in pulished mps nd institutionl ffilitions. Correspondence nd requests for mterils should e ddressed to A.F.A.P. (fpelle@stnford.edu). Reviewer Informtion Nture thnks T. DeLuc, A. D. McGuire nd the other nonymous reviewer(s) for their contriution to the peer review of this work. 98 NATURE VOL 553 jnury Mcmilln Pulishers Limited, prt of Springer Nture. All rights reserved.
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