Concentrations and resorption patterns of 13 nutrients in different plant functional types in the karst region of south-western China

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1 Annls of Botny 113: , 214 doi:1.193/o/mu5, ville online t Conentrtions nd resorption ptterns of 13 nutrients in different plnt funtionl types in the krst region of south-western Chin Chngheng Liu 1, Yuguo Liu 2,KeGuo 1,, Shijie Wng 3,4 nd Yo Yng 1,5 1 Stte Key Lortory of Vegettion nd Environmentl Chnge, Institute of Botny, Chinese Ademy of Sienes, Beijing 193, Chin, 2 Institute of Desertifition Studies, Chinese Ademy of Forestry, Beijing 191, Chin, 3 Stte Key Lortory of Environmentl Geohemistry, Institute of Geohemistry, Chinese Ademy of Sienes, Guiyng 552, Chin, 4 Puding Krst Eosystem Reserh Sttion, Chinese Ademy of Sienes, Puding 56211, Chin nd 5 University of Chinese Ademy of Sienes, Beijing 149, Chin For orrespondene. E-mil guoke@is..n Reeived: 26 June 213 Returned for revision: 9 Otoer 213 Aepted: 7 Jnury 214 Pulished eletronilly: 25 Ferury 214 Bkground nd Aims Eluidting the stoihiometry nd resorption ptterns of multiple nutrients is n essentil requirement for holisti understnding of plnt nutrition nd iogeohemil yling. However, most studies hve foused on nitrogen (N) nd phosphorus (P), nd lrgely ignored other nutrients. The urrent study imed to determine reltionships etween resorption ptterns nd lef nutrient sttus for 13 nutrient elements in krst vegettion region. Methods Plnt nd soil smples were olleted from four vegettion types in the krst region of south-western Chin nd divided into eight plnt funtionl types. Smples of newly expnded nd reently senesed leves were nlysed to determine onentrtions of oron (B), lium (C), opper (Cu), iron (Fe), potssium (K), mgnesium (Mg), mngnese (Mn), molydenum (Mo), N, sodium (N), P, sulphur (S) nd zin (Zn). Key Results Nutrient onentrtions of the krst plnts were lower thn those normlly found in other regions of Chin nd the rest of the world, nd plnt growth ws minly limited y P. Overll, four nutrients reveled resorption [N (resorption effiieny 34.6 %), P (48.4 %), K (63.2 %) nd Mg (13.2 %)], seven nutrients [B ( 16.1 %), C ( 44. %), Cu ( 14.5 %), Fe ( 25.5 %), Mn ( 72.5 %), Mo ( 35.6 %) nd Zn ( %)] showed umultion in senesed leves nd two nutrients (N nd S) showed no resorption or umultion. Resorption effiienies of K nd Mg nd umultion of B, C, Fe nd Mn differed mong plnt funtionl types, nd this strongly ffeted litter qulity. Resorption effiienies of N, P nd K nd umultion of C nd Zn inresed with deresing onentrtions of these nutrients in green leves. The N:P, N:K nd N:Mg rtios in green leves predited resorption profiieny for N, K nd Mg, respetively. Conlusions The results emphsize the ft tht nutrient resorption ptterns strongly depend on element nd plnt funtionl type, whih provides new insights into plnt nutrient use strtegies nd nutrient yling in krst eosystems. Key words: krst eosystem, multiple nutrients, nutrient onentrtion, nutrient limittion, plnt funtionl type, plnt nutrient use strtegy, resorption effiieny, resorption profiieny, stoihiometry. INTRODUCTION Plnts require multiple nutrients nd generlly quire them from the soil solution. Some nutrients re required in lrge quntities nd others in only smll mounts (Mrshner, 1995; Ågren, 28; White nd Brown, 21). Aording to eologil stoihiometry, it is essentil to mintin suffiient ontents nd stle proportions of multiple nutrients in plnt tissues for helthy growth (Elser et l., 2; Sterner nd Elser, 22). Nitrogen (N) nd phosphorus (P) re ritil omponents of plnt nutrition nd glolly re onsidered to e the most importnt nutrients limiting plnt growth nd ron storges in terrestril eosystems (Elser et l., 27). Aordingly, most studies on nutrient stoihiometry nd resorption ptterns hve foused on N nd P, while other nutrients hve een poorly investigted (Lynh nd St Clir, 24; Wtne et l., 27; Ågren, 28; Hn et l., 211). However, iogeohemil proess my e o-limited y multiple nutrients nd/or my experiene shifting degrees of limittion y different elements t multiple timesles (Vitousek, 24; Townsend et l., 211). Mny nutrients other thn N nd P lso ply importnt roles in plnt metoli proesses nd eosystem funtioning. Mny inorgni ions tke prt in photosynthesis, osmoti djustment nd ntioxidnt protetion (Mrshner, 1995). Minerl nutrients n influene plnt growth through oth limittion nd toxiity. Toxiities of mngnese (Mn) nd luminium ommonly our on id soils (White nd Brown, 21), while lkline soils re hrterized y poor vililities of P, iron (Fe), opper (Cu), Mn nd zin (Zn) (Lynh nd St Clir, 24). Reent studies suggested tht multiple nutrients my o-regulte the ron yle, y ffeting the funtions nd proesses of eosystems (Townsend et l., 211). For exmple, mny mironutrients shpe litter prodution nd deomposition rte (Kspri et l., 28). Mngnese enhnes lignin degrdtion in the litter of mny trees, suh s oks (Dvey et l., 27) nd pines (Berg et l., 21), while lium (C) n ffet tree growth nd litter prodution (Poli nd Currn, 27) nd forest floor turnover rte (Reih et l., 25). Molydenum (Mo) n promote N fixtion in tropil forests (Brron et l., 29). These results highlight tht studies of stoihiometri reltions nd the # The Author 214. Pulished y Oxford University Press on ehlf of the Annls of Botny Compny. All rights reserved. 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2 874 Liu et l. Nutrient stoihiometry nd resorption in plnts reltive needs nd limittions of multiple nutrients re urgently needed for holisti understnding of the eology of plnt nutrition (Ågren, 28; Hn et l., 211). Nutrient resorption is one of the most importnt strtegies employed y plntsto onserve nutrients, espeilly in low-nutrient environments (Aerts, 1996; Killingek, 1996), nd ffets mny eosystem proesses, suh s nutrient uptke, litter deomposition, plnt ompetition nd ron yling (Killingek, 1996; Yun nd Chen, 29; Vergutz et l., 212). Thus, nutrient resorption prmeters re essentil for the ury of eosystem nd iogeohemil models (Thornton et l., 27; Reed et l., 212; Vergutz et l., 212). Nutrient resorption n e quntified s resorption effiieny (RE) nd resorption profiieny (RP) (Aerts, 1996; Killingek, 1996). Resorption effiieny (defined s perentge redution of nutrient onentrtion etween green nd senesed leves) is est suited to quntifying the reltive degree to whih plnt n onserve nutrients invested in folige. Resorption profiieny (defined s the terminl nutrient onentrtion in senesed leves) ppers to e more definitive nd ojetive mesure of the degree to whih seletion hs ted to minimize nutrient loss (Killingek, 1996). Nutrient resorption usully vries mong plnt funtionl types. For exmple, the RE of N is higher in deiduous speies nd grminoids thn in evergreen speies nd fors (Aerts, 1996), nd higher in shrus thn in trees (Yun nd Chen, 29). Grminoids hve higher REs of P, K, C nd Mg thn evergreen nd deiduous ngiosperms (Vergutz et l., 212). These vritions n e ttriuted to differenes in hitt, lef lifespn nd the size of the non-lef nutrient pool (Kull nd Kruijt, 1999; Wright nd Westoy, 23; Koe et l., 25; Vergutz et l., 212). As nutrient resorption is onsidered to e prtiulrly importnt in low-fertility soils, previous studies hve extensively investigted the reltionships etween nutrient resorption nd nutrient vililities. Some studies found no ler reltionships (Aerts, 1996; Wright nd Westoy, 23; Kzkou et l., 27), while others suggested tht nutrient RE depended on plnt or soil nutrient sttus (Koe et l., 25; Rejmánková, 25; Rtnm et l., 28; Vergutz et l., 212). When nutrient vilility ws expressed s reltive nutrient limittion (e.g. N:P rtio in green leves), nutrient RP seemed to e more sensitive thn RE (Rejmánková, 25; Rtnm et l., 28). To dte, whether nd how nutrient resorption is regulted y plnt nutrient sttus ross plnt funtionl types nd eosystems remin unresolved (Aerts et l., 27; Rtnm et l., 28; Vergutz et l., 212). Moreover, most reserh hs only ddressed ptterns of N nd P resorption, while resorption ptterns of other essentil nutrients hve seldom een reported ut see Hgen-Thorn et l. (26) nd Vergutz et l.(212). It ws reported tht mro-nd miro-nutrient onentrtions in plnts n e hnged y experimentl drought nd wrming, nd tht the hnges depended on the nutrient nd speies (Srdns et l., 28), whih ould ffet plnt nutrient use strtegies, plnt growth nd eosystem proesses. This emphsizes the importne of eluidting the resorption ptterns of multiple nutrients in urtely modelling iogeohemil yling nd eosystem produtivity, espeilly under glol hnge (Aerts et l.,27; Reed et l., 212; Vergutz et l.,212). Krst topogrphy is widespred throughout the world nd overs out 12 % of the world s lnd re (Liu, 29). The krst lndspe of south-western Chin is one of the most typil lndspes developed on ronte edrok in the world, nd is hrterized y extremely slow soil formtion from the underlying limestone nd very shllow nd pthy soil with low wter retention pity (Zhu, 1997; Liu, 29). The typil vegettion in the sutropil krst region is mixed evergreen nd deiduous rod-leved forest. Due to humn disturnes, mny krst forests hve experiened vrying degrees of degrdtion. Mny vegettion types, suh s forest, shru forest, shrulnd nd grsslnd, our in this region, nd the grsslnds re the result of serious degrdtion of other vegettion types. For long time, wter vilility ws onsidered to e the most importnt ftor limiting plnt growth nd vegettion restortion in this krst region (Zhu, 1997; Liu, 29). However, reent studies hve suggested tht shortge of minerl nutrients resulting from the limited totl soil mss ould e ruil ftor limiting plnt growth nd eosystem produtivity in this region (Zhng nd Wng, 29; Du et l., 211; Guo et l., 211). It ws reported tht the men depth of topsoil on the krst hills ws only out 2 9 m (Zhng nd Wng, 29; Liu et l., 213). However, nutrient limittions nd nutrient onservtion strtegies of the ntive plnts in this region re still eing questioned, nd lrifition is urgently needed to improve our understnding of plnt nutrient use strtegies, speies ompositions, ompetitive reltionships nd dynmis of the ntive vegettion. The present study investigted the stoihiometry nd resorption ptterns of 13 minerl nutrients [oron (B), C, Cu, Fe, potssium (K), mgnesium (Mg), Mn, Mo, N, sodium (N), P, sulfur (S) nd Zn] in different plnt funtionl types from four different vegettion types (forests, shru forests, shrulnds nd grsslnds) in the krst region of south-western Chin. We ddressed the following questions. (1) Wht re the reltive limiting nutrients in this krst region? We expeted tht the multiple nutrients tht re required in lrge quntities would o-limit plnt growth in the krst region, due to the shllow soil lyer. Phosphorus would proly e the most importnt limiting ftor euse of the lowered moility of P in lreous soils. (2) How does plnt nutrient sttus influene nutrient resorption ross plnt funtionl types? It ws expeted tht nutrient resorption vlues would inrese s nutrient onentrtions in green leves deresed or nutrient reltive limittions inresed. This response would lso vry mong funtionl types. (3) How do resorption ptterns differ mong minerl nutrients? We hypothesized tht nutrients required in lrge quntities would e resored more effetively thn nutrients required in smll mounts. Mgnesium nd C would e less resored thn other nutrients, suh s N, P nd K, euse lreous soils re usully rih in Mg nd C. (4) How does vegettion degrdtion ffet nutrient stoihiometry nd resorption ptterns? We expeted tht soils would eome more sterile during the proess of deforesttion nd therefore plnt nutrient onentrtions would e lower nd nutrient resorption would e more effetive in grsslnds thn in forests. Study region MATERIALS AND METHODS The reserh ws rried out t the Puding Krst Eosystem Reserh Sttion of the Chinese Ademy of Sienes in Guizhou Provine, Chin ( N, E). The men nnul preipittion nd temperture of this region re 139 mm nd C, respetively. The topsoil Downloded from y guest on 31 August 218

3 Liu et l. Nutrient stoihiometry nd resorption in plnts 875 in this region is extremely shllow nd pthy, in the rnge of 3 m deep. The typil vegettion is mixed evergreen nd deiduous rod-leved forest. Due to humn disturne, four min vegettion types our in this region: mixed evergreen nd deiduous rod-leved forests, shru forests, shrulnds nd grsslnds. Pltyry longipes, Crpinus puesens, Lithorpus onfines nd Ite yunnnensis dominte the forest vegettion. The men height of nopy trees is out 15 m nd the men nopy overge is out 9 %. The shru forest vegettion is dominted y P. longipes nd I. yunnnensis, ompnied y mny thorny shrus suh s Ros ymos nd Rhmnus heterophyll. The men height of the nopy trees in shru forest vegettion is out 6 m. The shrulnd vegettion is dominted y mny thornyshru speies (2 m height), suh s Ro. ymos, Rh. heterophyll, Znthoxylum plnispinum nd Pyrnth fortunen. The grsslnd vegettion is dominted y Themed jponi nd Heteropogon ontortus nd ontins some dwrf shrus. More detils out the four vegettion types were desried y Liu et l. (211). Nutrient ontents of topsoil of the four vegettion types re desried in Supplementry Dt Tle S1. The min differenes mong the vegettion types re the onsequenes of humn-indued vegettion degrdtion. The forest vegettion is onsidered referene for the nturl vegettion in this region nd shows little disturne, while shrulnd nd grsslnd vegettion re the results of intensive disturnes. Smpling nd hemil nlysis Plnt nd soil smples were olleted from the four vegettion types, with eh type hving three studied sites (Supplementry Dt Tle S2). Aording to previous vegettion inventories of smpling plots in these sites (Liu et l., 211), we olleted mture green nd senesed leves of dominnt nd ommon speies in eh smpling plot. New fully expnded nd intt green leves were smpled during July nd August 211, nd reently senesed tree nd shru leves nd stnding ded her leves were smpled during Novemer nd Deemer. Mture green leves situted t the sme height were tken t 4 5 m for trees, 1 2 m for shrus nd.1.3 m for hers. For eh speies t eh site, three to five smples were rndomly olleted from different helthy individuls. Beuse mny speies o-our in different sites, we lelled eh speies t eh site s site speies. In totl we olleted 172 site speies, whih elonged to 64 plnt speies, with mthed pirs of green nd senesed leves. Smpled speies were lssified into eight plnt funtionl types: six ferns, 18 fors, 12 grsses (Cyperee nd Grminee), 34 evergreen shrus, 22 evergreen trees, 28 deiduous shrus, 37 deiduous trees nd 15 lins (Supplementry Dt Tle S3). Five topsoil smples ( 2 m) per site were lso olleted simultneously with smpling the green leves. All smples were ir-dried in the field efore eing shipped to the lortory for nlysis. Totl N onentrtion ws nlysed using the Kjeldhl method nd onentrtions of other nutrients (B, C, Cu, Fe, K, Mg, Mn, Mo, N, P, S nd Zn) were determined with n indutive oupled plsm emission spetrometer fter digestion of the smples in onentrted HNO 3. Dt nlysis To determine the reltive limittions of multiple nutrients, we used the physiologil onentrtion requirements (Mrshner, 1995; Hn et l., 211) nd the optiml rtios of multiple nutrients (Linder, 1995; Kneht nd Görnsson, 24). Aording to Mrshner (1995) nd Hn et l. (211), the physiologil onentrtion requirements of N, K, C, Mg, P, S, Fe, Mn, Zn, B, Cu nd Mo for dequte plnt growth re 15, 1, 5, 2, 2, 1,.1,.5,.2,.2,.6 nd.1 g kg 21, respetively. Aording to Linder (1995), the optiml rtios of multiple nutrients re: N:P:K:C:S:Mg:Fe:Mn:Zn:Cu:B:Mo ¼ 1:1:35:2.5:5:4:.2:.5:.5:.3:.5:.7. Conentrtions of the other 11 nutrients in green leves were plotted ginst N onentrtions nd line representing the optiml rtio ws dded. As N is required in lrge mounts nd ommonly limits plnt growth in terrestril eosystems, we judged reltive N limittion or limittions of other nutrients in the krst plnts in reltion to the optiml rtios. Men nutrient onentrtions in green ([nutrient] green ) nd senesed ([nutrient] sen ) leves for eh speies t eh site were lulted from individul smples. Nutrient resorption ws expressed s RE nd RP. Beuse we ould not mth [nutrient] green nd [nutrient] sen t the individul level, we lulted nutrient RE for different plnt funtionl types sed on the men nutrient onentrtions t speies level t eh site. We used the method of Koe et l. (25) to lulte RE for different funtionl types nd the whole dt set, nd to determine the effet of plnt nutrient sttus on RE: [ nutrient] sen = ( [ nutrient] green ) (1) The prmeter is n index of nutrient RE, while exponent determines how [nutrient] green ontrols RE. When ¼ 1, the nutrient sttus of green leves hs no effet on RE. In this se, RE is equl to (1 )%.When. 1, RE dereses with inresing nutrient onentrtion, while, 1 implies inresing RE with inresing nutrient onentrtion (Koe et l.,25). When = 1, RE = 1 ( [ nutrient] ) green 1 % (2) [ nutrient] green Log 1 trnsformtion of eqution 1 yields the liner form: log 1 ([ nutrient] sen )= + log 1 ([ nutrient] green ) (3) where is log 1 nd nd re estimted from the dt. To determine the effet of [nutrient] green on RE, we fitted eqn (3) using mjor xis regression, whih is pproprite in stoihiometri studies (Koe et l., 25; Nikls, 26). Regression prmeters were estimted using the SMATR lirry (version 2.; Wrton et l., 26). The nutrient vriles ([nutrient] green, [nutrient] sen nd nutrient RE) of plnt ommunity were weighted verges lulted from the lef men vlues of the dominnt speies nd the importne vlues (IV) of the dominnt speies in the ommunity: [ nutrient vriles] ommunity = n i ([ nutrient vriles] i IV i )/ n i IV i (4) where [nutrient vriles] ommunity re the [nutrient] green, [nutrient] sen nd nutrient RE of plnt ommunity, [nutrient Downloded from y guest on 31 August 218

4 876 Liu et l. Nutrient stoihiometry nd resorption in plnts vriles] i re the [nutrient] green, [nutrient] sen nd nutrient RE of the ith plnt speies, nd IV i is the importne vlue of the ith plnt speies in plnt ommunity. One-wy ANOVA ws performed to determine differenes mong plnt funtionl types or vegettion types. Beuse of the limited mount of dt, dt on evergreen shrus, deiduous shrus nd deiduous trees were sujeted to two-wy ANOVA to determine the effets of funtionl type, vegettion type nd their intertion on nutrient vriles. The signifines of differenes etween mens were determined y Tukey s test t P,.5. The men nutrient RE of the whole dt set nd plnt funtionl types ws ssessed for differene from % RE y the t-test. To determine the effets of reltive nutrient limittions on nutrient resorption, the orreltions etween the rtios of green lef N to other nutrients nd nutrient RE nd RP were explored y Person s orreltion nlysis nd liner regression. To test the effets of soil nutrient ontents on lef nutrient onentrtions, the orreltions etween men soil nutrient ontents of eh vegettion type nd men lef nutrient onentrtions nd nutrient RE for evergreen shrus, deiduous shrus nd deiduous trees were lso explored y Person s orreltion nlysis. The rtios of N to other nutrients, [nutrient] green nd [nutrient] sen of eh speies t eh site were log 1 -trnsformed to meet ssumptions of normlity. Sttistil nlyses were performed with SPSS version 15. (SPSS, USA). RESULTS Conentrtions of multiple nutrients in different plnt funtionl types The men onentrtions of the 13 nutrients in green leves of the krst plnts vried gretly, rnging from.23 g kg 21 for Mo to g kg 21 for C (Tle 1), with C:N:K:Mg:S:P: N:Fe:Mn:B:Zn:Cu:Mo ¼ 111:1:59:18:14:8.6:.85:.82:.48:.18:.13:.75:.13. The reltive vriility of the 13 nutrient onentrtions in green leves [indited y their oeffiient of vrition (CV, %)] inresed in the order P (21.6%), N (25.7%), Mo (3.%), Cu (3.8%), Fe (38.3%), B (44.9%), Mg (51.4%), C (53.6%), S (57.1%), K (61.8%), N (64.4%), Zn (68.2%), Mn (11 %). The men [nutrient] sen followed similr orders of mgnitude to [nutrient] green, vrying from.28 g kg 21 for Mo to 26.9 g kg 21 for C (Tle 1), with C:N:K:Mg:S:P:N:Fe:Mn:B:Zn:Cu:Mo ¼ 231:1:33:24:21:6.8:1.1:3.8:1.2:.31:.5:.12:.25. The N onentrtion in senesed leves showed the smllest CV (29.2%) nd Mn the lrgest (158.1%). Conentrtions of multiple nutrients showed signifint differenes mong plnt funtionl types (Tle 1). Deiduous trees hd the highest N onentrtions in green nd senesed leves, nd evergreen trees nd shrus the lowest vlues. Ferns hd the highest P onentrtions in green nd senesed leves, while evergreen shrus hd the lowest vlues. Most of the lowest onentrtions of B, C, Fe, K, Mg, Mn, S nd Z in green nd senesed leves were in grsses or evergreen speies, nd the highest in fors nd/or lins. There were no signifint differenes mong funtionl types in Cu, Mo nd N onentrtions in green nd senesed leves. Reltive limittions of nutrients in krst plnts Among the 12 nutrients (B, C, Cu, Fe, K, Mg, Mn, Mo, N, P, S nd Zn), only men P onentrtions in green leves of krst plnts (1.5gkg 21 ;Tle1) were signifintly lower thn the physiologil onentrtion requirement of P (2.gkg 21 ; t-test, P,.5). When dtwere grouped y plnt funtionl type, the P onentrtion of eh funtionl type ws lso lower thn the physiologil onentrtion requirement (Tle 1; P,.5). Men K onentrtions in green leves of evergreen nd deiduous shrus nd trees ( g kg 21 ; Tle 1) were lower thn the physiologil onentrtion requirement of K (1 g kg 21 ; P,.5), while onentrtions of the other ten nutrients were generlly not lower thn the physiologil onentrtion requirements (Tle 1). For P, vlues mostly fell elow the optiml line (Fig. 1). For the other ten nutrients, most vlues were ove the optiml line, with only few vlues elow the line ut still very lose to it. Nutrient RE nd RP Considering ll dt s whole, four nutrients (N, P, K nd Mg) reveled resorption, while the other nine nutrients tended to umulte in senesed leves (Fig. 2). Averge nutrient RE inresed in the following order: Mg (13.2%), N(34.6%), P(48.4%), K(63.2 %). Men umultion ws gretest for Fe (RE 25.5 %) nd lowest for S (RE 1.4%).Theumultions of N nd S were not signifint (Fig. 2). Nutrient RE or umultion differed signifintly mong funtionl types (Fig. 2). For N, Pnd K, resorption ws oserved in ll funtionl types. RE for N ws highest in lins (41.7 %) nd lowest in grsses (26.2 %). RE for P ws highest in deiduous trees (54.7 %) nd lowest in deiduous shrus (4.4 %). RE for K ws higher in ferns, fors nd grsses ( %) thninother funtionl types. There ws signifint Mg resorption in grsses, evergreen trees, deiduous shrus nd trees, nd lins, with the highest RE in grsses (39.1 %). Only deiduous trees reveled signifint S resorption (12.5 %), nd fors nd evergreen shrus showed N resorption (31.1 nd 24.6 %, respetively). All funtionl types showed signifint umultions of B (exept for fors nd grsses), C (exept for grsses), Fe, Mn nd Zn (Fig. 2). Aumultions of B (41.8%;RE 41.8 %), C (123.1 %) nd Mn (255. %) were highest in ferns. Grsses showed the highest Fe umultion (487.6 %) nd deiduous shrus the highest Zn umultion (249.4 %). However, Cu umultion only ourred in fors nd deiduous trees (25.7 nd 19.5 %, respetively) nd Mo umultion ws oserved in shrus nd trees ( %). Beuse only N, P, K nd Mg reveled resorption ross ll dt, we minly foused on the RPs (onentrtions in senesed leves) of these four nutrients. Aross ll dt, men RPs of N, P, K nd Mg were 1.13,.77,.38 nd.27 %, respetively (Tle 1). The highest RPs for N nd P were in evergreen shrus nd the highest RPs for K nd Mg were in grsses (Tle 1), wheres the lowest RPs for N, P nd K were in deiduous trees, ferns nd lins, respetively. Effet of plnt nutrient sttus on nutrient resorption Aross ll dt, the vlues of [nutrient] sen were positively orrelted with [nutrient] green for the 13 nutrients exept for Cu, Mo nd N (Supplementry Dt Fig. S1). For N, P nd K the vlue ws.1(p,.5; Tle 2; Supplementry Dt Fig. S1), inditing tht REs of N, P nd K inresed with deresing Downloded from y guest on 31 August 218

5 TABLE 1. Nutrient onentrtions in green nd senesed leves of different plnt funtionl types (g kg 21 ) Nutrient Lef type All dt (n ¼ 172) Ferns (n ¼ 6) Fors (n ¼ 18) Grsses (n ¼ 12) Evergreen shrus (n ¼ 34) Evergreen trees (n ¼ 22) Deiduous shrus (n ¼ 28) Deiduous trees (n ¼ 37) Lins (n ¼ 15) C Green Senesed N Green Senesed K Green Senesed Mg Green Senesed d d d d S Green Senesed P Green Senesed N Green Senesed Fe Green Senesed Mn Green Senesed B Green Senesed Zn Green Senesed Cu Green Senesed Mo Green Senesed Dt re men + s.e. Different letters in the sme row denote signifint differenes mong plnt funtionl types t P,.5 n, numer of site speies. Liu et l. Nutrient stoihiometry nd resorption in plnts 877 Downloded from y guest on 31 August 218

6 878 Liu et l. Nutrient stoihiometry nd resorption in plnts B (g kg 1 ) B C (g kg 1 ) C Cu Fe Cu (g kg 1 ) Fe (g kg 1 ) N (g kg 1 ) N (g kg 1 ) N (g kg 1 ) N (g kg 1 ) K (g kg 1 ) 6 K N (g kg 1 ) Mg (g kg 1 ) Mg Mn Mo Mn (g kg 1 ) N (g kg 1 ) N (g kg 1 ) N (g kg 1 ) Mo (g kg 1 ) P (g kg 1 ) P S Zn S (g kg 1 ) Zn (g kg 1 ) Ferns Fors Grsses Evergreen shrus Evergreen trees Deiduous shrus Deiduous trees Lins N (g kg 1 ) N (g kg 1 ) N (g kg 1 ) F IG. 1. Conentrtions of 11 nutrients (B, C, Cu, Fe, K, Mg, Mn, Mo, P, S nd Zn) versus N onentrtions in green leves of krst plnts of south-western Chin (n ¼ 172). Dt re mens of site speies. The solid lines denote the optiml rtios suggested y Linder (1995). onentrtions of N, P nd K in green leves, respetively. The vlue for Mg did not differ from 1, inditing no effet of Mg onentrtion in green leves on RE of Mg. Moreover, the effet of [nutrient] green on nutrient RE depended on funtionl type (Tle 2). The vlue ws.1 for N in fors, evergreen shrus nd trees nd for P in fors, evergreen shrus nd trees, nd deiduous trees. For K, ll funtionl types hd. 1 exept for grsses nd lins, while vlues for Mg did not signifintly differ from 1 in ll funtionl types. The vlues were lso estimted forother nutrients (B, C, Fe, Mn, S nd Zn) tht umulted in senesed leves. Aross ll dt, for C nd Zn, 1 (Supplementry Dt Fig. S1), while vlues did not differ from 1 for B, Mn nd S. For Fe the vlue ws.1, ut the orreltion etween Fe onentrtions in green nd senesed leves ws very wek (R 2 ¼.13). The responses in estimted for B, C, Fe, Mn, S nd Zn lso depended on funtionl type (Tle 2). Aross ll dt, the orreltions etween nutrient RE nd the rtios of N to other nutrients in green leves were not signifint (dt not shown), while the vlues of [nutrient] sen were signifintly orrelted with the rtios of N to other nutrients for the 13 nutrients exept for P, Cu, Mo nd N (Tle 3; Supplementry Dt Fig. S2). The RP of N deresed with inresing N:P rtio in green leves, while the RPs of K nd Mg inresed with inresing N:K nd N:Mg rtios, respetively, whih indited tht the RPs of N, K nd Mg inresed sthe reltive limittions of these nutrients inresed. Signifint orreltions for K nd Mg were lso oserved in most funtionl types, while orreltions for N were found in fors, grsses nd deiduous shrus nd for P only in deiduous trees (Tle 3). For B, C, Fe, Mn, S nd Zn, the vlues of [nutrient] sen were negtively orrelted with the N:B, N:C, N:Fe, N:Mn, N:S nd N:Zn rtios in green leves, respetively (Supplementry Dt Fig. S2), suggesting tht onentrtions of these nutrients in senesed leves deresed with their inresing reltive limittions ompred with N. The orreltions for these nutrients lso depended on funtionl type (Tle 3). Nutrient onentrtions nd resorption ptterns mong vegettion types For evergreen shrus, deiduous shrus nd deiduous trees, differenes in nutrient onentrtions nd resorption mong vegettion types were usully not signifint, ut there were Downloded from y guest on 31 August 218

7 Liu et l. Nutrient stoihiometry nd resorption in plnts B 16 C Cu Fe K Mg Resorption effiieny (%) Mn N Resorption effiieny (%) Mo N Zn All dt Ferns Fors Grsses P Evergreen shrus Funtionl type Evergreen trees Deiduous shrus Deiduous trees Lins All dt Ferns Fors Grsses Evergreen shrus S Evergreen trees Funtionl type Deiduous shrus Deiduous trees Lins FIG. 2. Resorption effiienies of 13 nutrients in different plnt funtionl types (men + s.e.). Different letters denote signifint differenes mong different plnt funtionl types t P,.5. Signifintly different from % resorption effiieny t P,.5. Downloded from y guest on 31 August 218

8 88 Liu et l. Nutrient stoihiometry nd resorption in plnts TABLE 2. oeffiients for different plnt funtionl types All dt Fors Grsses Evergreen shrus Evergreen trees Deiduous shrus Deiduous trees Lins Nutrient R 2 R 2 R 2 R 2 R 2 R 2 R 2 R 2 B C Fe K Mg Mn N P S Zn The oeffiients were estimted y fitting eqn (3) using mjor xis regression. Dt on Cu, Mo nd N were not inluded euse signifint orreltions etween onentrtions in green nd senesed leves for these three nutrients were not oserved in ll plnt funtionl types. Empty ells denote tht there ws no signifint reltionship etween nutrient onentrtions in green nd senesed leves. is signifintly different from 1 (P,.5), inditing tht nutrient resorption effiieny depends on nutrient onentrtion in green leves. Ferns were not inluded due to limited dt. TABLE 3. Summry of Person s orreltion oeffiients (R) relting the rtios of N to other nutrients in green leves nd nutrient onentrtions in senesed leves for different funtionl types Nutrient All dt Fors Grsses Evergreen shrus Evergreen trees Deiduous shrus Deiduous trees Lins B C Fe K Mg Mn N P S Zn Ferns were not inluded due to limited dt. For N, the reltionship etween N:P rtio in green leves nd N onentrtion in senesed leves ws explored. For Cu, Mo nd N, there were no signifint orreltions in ny plnt funtionl type. P,.5; P,.1. some exeptions (Supplementry Dt Fig. S3). For exmple, deiduous shrus showed the lowest Mg onentrtions in green nd senesed leves nd the lowest RE for Mg in shrulnds nd the highest vlues in grsslnds. Deiduous trees showed the highest S onentrtions nd RE for S in grsslnds nd the lowest vlues in forests. Evergreen nd deiduous shrus lso showed the lowest K onentrtions nd highest RE for K in grsslnds. Usully, the effets of soil nutrient ontents on lef nutrient onentrtions were smll, exept tht B nd S onentrtions in green leves of evergreen shrus nd K onentrtions in deiduous shrus were positively orrelted with ontents of B, S nd K in soils (R 2 ¼.92,.95 nd.92 for B, S nd K, respetively). Evergreen shrus showed trend of inresing P (R 2 ¼.94, P ¼.33), K (R 2 ¼.61, P,.2) nd Mg (R 2 ¼.72, P ¼.15) REs with deresing soil P, K nd Mg ontents, respetively. Deiduous trees tended to inrese the RE of N s soil N ontent deresed (R 2 ¼.84, P ¼.84). Evergreen shrus lso reveled signifint inreses in K (R 2 ¼.99, P ¼.6) ndmg(r 2 ¼.93, P ¼.35) RPs with deresing soil Mg nd K ontents, respetively. Deiduous shrus trended to inrese the RPs of N (R 2 ¼.78, P ¼.12) nd K (R 2 ¼.73, P ¼.15) ssoilnndkontentsderesed. The 13 nutrients showed different hnge ptterns mong the vegettion types (Fig. 3). For Cu, Mo, N nd P, there ws no signifint differene in nutrient vriles mong the four vegettion types. The B, Fe, S nd Zn onentrtions in senesed leves differed mong the four vegettion types, with grsslnds hving the highest Fe, S nd Zn onentrtions nd shrulnds the highest B onentrtion. The C, K, Mg, Mn nd N onentrtions in oth green nd senesed leves were signifintly different mong the four vegettion types. Forests hd the highest N, C nd Mn onentrtions in green nd senesed leves, while grsslnds hd the lowest. Shrulnds showed the highest K nd the lowest Mg onentrtions. Grsslnds hd the highest REs for K nd Mg nd highest umultions of Fe, Zn nd Mn. Downloded from y guest on 31 August 218

9 Liu et l. Nutrient stoihiometry nd resorption in plnts B 4 C Conentrtions in green nd senesed leves (g kg 1 ) Cu K Mn N Resorption effiieny (%) Conentrtions in green nd senesed leves (g kg 1 ) Fe Mg Mo N Resorption effiieny (%) P 1 Zn FSFSG FSFSG FSFSG Vegettion type S FSFSG FSFSG FSFSG Vegettion type Conentrtion in green leves Conentrtion in senesed leves Resorption effiieny FIG. 3. Nutrient onentrtions nd resorption effiienies of the four vegettion types: forest (F), shru forest (SF), shrulnd (S) nd grsslnd (G). Dt re mens of three smpling sites for eh vegettion type. Different letters denote signifint differenes mong vegettion types t P,.5. Signifintly different from % resorption t P,.5. Downloded from y guest on 31 August 218

10 882 Liu et l. Nutrient stoihiometry nd resorption in plnts DISCUSSION Nutrient onentrtions in krst plnts The vlues of [nutrient] green of the krst plnts in the present study were in ordne with previous oservtions in this region (Hou, 1982; Zhou, 1997; Yng et l., 27) nd within the norml rnges for helthy plnt growth (Mrshner, 1995; White nd Brown, 21). The men onentrtions of Fe, K, Mn, N, N, P nd S in the green leves of krst plnts were signifintly lower thn verge vlues for Chinese plnts reported y Hn et l. (211). The men onentrtions of Cu, Mn, N, N nd P in green leves were lso lower thn glol verges (Elser et l., 2; Reih nd Oleksyn, 24; Wtne et l., 27). The reltively low nutrient onentrtions of krst plnts ould e explined y the shortge of soil nutrients resulting from the shllow soil nd the limited totl soil mss (Zhng nd Wng, 29; Guo et l., 211). For exmple, the verge depth of topsoil on krst hills ws 2 9 m, whih ws muh lower thn depths in other non-krst hitts (Zhng nd Wng, 29; Liu et l., 213). Totl N nd P stoks in the topsoil of forests in the krst region (totl N 4.29 t hm 22, totl P.24 t hm 22 ; Du et l., 21) were lso mrkedly lower thn those of sutropil evergreen rod-leved forests in non-krst region in the sme ltitudinl zone (totl N t hm 22, totl P 1.45 t hm 22 ; Yn et l., 27). Generlly, nutrient onentrtions re higher in deiduous thn in evergreen speies nd higher in fors thn in grsses (Aerts, 1996; Hn et l., 211). However, we found tht not ll the 13 nutrients in the studied krst plnts followed suh generl ptterns. For exmple, the onentrtions of N, Cu nd Mo in green nd senesed leves did not differ mong funtionl types (Tle 1). Nutrient onentrtions differed etween fors nd grsses only for C, K, Mg, B nd Fe. Signifint differenes in nutrient onentrtions etween deiduous nd evergreen speies were oserved only for B, C, Mn, Mg, N nd P. Our results indited tht the previously demonstrted onsistent differenes were not universl in krst plnts, espeilly for nutrients required in only smll mounts. Reltive nutrient limittions to krst plnts The onentrtions of C, K, Mg, S, Fe, Mn, B, Zn, Cu nd Mo in green leves were mostly higher thn the optiml rtios (Fig. 1), inditing tht N limittion ws dominnt ompred with these nutrients (Kneht nd Görnsson, 24). However, most P onentrtions were lower thn the optiml rtio, inditing tht for most plnts P limittion ws more importnt thn N limittion. This ws onfirmed y the men P onentrtion in green leves of either ll plnts or eh funtionl type eing lower thn the physiologil onentrtion requirement of P. The K onentrtions in shrus nd trees were lso lower thn the physiologil onentrtion requirement. However, most K:P rtios in krst plnts (dt not shown) were higher thn the optiml K:P (3.5) suggested y Linder (1995). Olde Venterink et l. (23) lso suggested tht K:P. 3.4 indited P limittion ompred with K. Aording to the hypothesis of stility of limiting elements (Hn et l., 211), nutrients tht re frequently limiting ftors would e more stle nd less sensitive to environmentl grdients. Among the 13 nutrients, the reltive vriility in green leves (indited y CV) ws lest for P (21.6 %) followed y N, inditing tht P limittion ws most importnt for krst plnts. As high N deposition (3.1 g m 22 yer 21 ) hs ourred in this region (Liu et l., 28), defiieny of plnt-ville P tends to limit plnt produtivity in krst hitts due to lowered moility of P ound to lium phosphtes in lreous soils (Niinemets nd Kull, 25; Pio et l., 25; Du et l., 211). Nutrient resorption nd plnt funtionl types Most previous studies hve foused on N nd P resorption, ignoring other nutrients tht re importnt for modelling nutrient yling nd eosystem produtivity (Hn et l., 211; Vergutz et l., 212). We reported the resorption ptterns of 13 nutrients in krst plnts. The verge RE of N (34.6 %) ws lower thn the glol verges ( %; t-test, P,.5), while the verge RE of P (48.4 %) ws lose to the glol vlues ( %) reported y Aerts (1996) nd Yun nd Chen (29). The men REs of K (63.2 %) nd Mg (13.2 %) were lower thn the glol verges (7.1 nd 28.6 %, respetively) lulted y Vergutz et l. (212), who introdued mss loss orretion ftor into resorption estimtes to overome the error resulting from lef mss loss during senesene. In ontrst to the glol verge RE of C (1.9%)(Vergutz et l., 212), C umulted in senesed leves of krst plnts. Previous studies suggested tht, s struturl element in plnts, C is usully onserved in leves (Lmers et l., 1998; vn Heerwrden et l., 23). Moreover, the plot of C versus N (Fig. 1) suggested tht exessive uptke of C generlly ourred in krst plnts on lreous soils. A previous study reported signifint REs of S, Fe, Cu nd Mn in deiduous trees (Hgen-Thorn et l., 26). In our study, only very low RE of S (12.5 %) ws oserved in deiduous trees, nd Fe, Cu nd Mn showed umultions in senesed leves (Fig. 2). It seemed tht most nutrients tht were required in only smll mounts were exessively tken up y plnts (Fig. 1) nd retined in leves. Differenes in RE mong plnt funtionl types hve well een doumented (Aerts, 1996; Yun nd Chen, 29; Vergutz et l., 212). In the present study, the differenes in the REs of N nd P mong funtionl types were smll, onsistent withthe results ofaerts (1996), while lrgedifferenes inthe REsof K nd Mg were oserved (Fig. 2). Lrge differenes in umultions of B, C, Fe nd Mn mong funtionl types were lso oserved (Fig. 2). Similr ptterns of REs for K nd Mg mong funtionl types were reported y Vergutz et l. (212). Beuse nutrient RE depends on the trnsfer of nutrients etween lef nd other plnt pools, the size of the non-lef nutrient pools ould gretly ffet nutrient resorption (Kull nd Kruijt, 1999; Vergutz et l., 212). The smller non-lef pools in grsses ould led to greter need for nutrient resorption ompred with other funtionl types, suh s shrus nd trees (Vergutz et l., 212). Nutrient resorption ould ply n importnt role in regulting eosystem nutrient yling, minly ffeting litter qulities tht ontrol deomposition rtes (Aerts, 1997; Reed et l., 212). In the krst region, different nutrient resorption ptterns mong plnt funtionl types gretly ffeted litter nutrient onentrtions. For exmple, grsses with higher REs for K nd Mg produed litter with lower K nd Mg onentrtions thn deiduous shrus nd trees (Fig. 2; Tle 1). Residues with poor levels of nutrients relese these nutrients more slowly thn those with Downloded from y guest on 31 August 218

11 Liu et l. Nutrient stoihiometry nd resorption in plnts 883 high levels (Prton et l., 27). Thus, the hnges in reltive ompositions of different plnt funtionl types during vegettion degrdtion would signifintly influene nutrient yling in krst eosystems. The return of nutrients from vegettion pools to soil pools ws slower in shrulnds nd grsslnds, whose dominnt speies (e.g. evergreen shrus nd grsses) usully hd low litter nutrient onentrtions (Tle 1). The men RPs of N (1.13 %) nd P (.77 %) of the krst plnts were lower thn the glol verges of N ( %) (Killingek, 1996; Yun nd Chen, 29; Vergutz et l., 212) nd P (.6 %) (Killingek, 1996); while men vlues of K (.38 %) nd Mg (.27 %) were higher thn the respetive glol verges of.47 nd.35 % reported y Vergutz et l. (212) (t-test, P,.5). Killingek (1996) suggested tht N onentrtions in senesed leves of,.7 % nd P onentrtions,.4.5 % ould e onsidered s omplete resorption. Aording to this riterion, most of the plnt funtionl types did not resor N nd P ompletely (Tle 1). Differenes in RP tended to e lrger thn those in RE mong funtionl types. For instne, the RPs of N nd P were higher in evergreen thn in deiduous shrus (Tle 1), wheres the REs of N nd P did not differ etween the two funtionl types (Fig. 2). The RP of K ws higher in grsses thn in fors, wheres the RE of K did not differ. These results onfirmed tht nutrient RP ppered to e more definitive nd ojetive mesure of the degree to whih seletion hs ted to minimize nutrient loss (Killingek, 1996; Wright nd Westoy, 23). Nutrient resorption nd nutrient sttus The reltionships etween nutrient resorption nd plnt nutrient sttus re still eing deted. In the present study, ross ll dt,the REs ofn,pndkinresedwiththeirderesingonentrtions in green leves (. 1). The RE of Mg ws not ontrolled y Mg onentrtion in green leves ( ¼ 1; Supplementry Dt Fig. S1), whih ws in ontrst to. 1estimtedforMgfrom glol dt set (Vergutz et l., 212). Nutrient resorption reflets the trde-off of the energy ost for plnts etween tking up nutrients from soil nd resoring nutrients from senesent leves (Wright nd Westoy, 23; Jing et l., 212). The vlue of RE is expeted to inrese with lowered [nutrient] green (. 1), if tking up nutrients from soil with poor nutrient onditions is more expensive for plnts thn resoring them from senesent leves (Wright nd Westoy, 23; Koe et l., 25; Kzkou et l., 27). In the krst region, soil developed on dolomite or limestone rok is usully rih in Mg (Zhng nd Wng, 29). Plnts n esily quire Mg from soil, whih ould explin why the vlue for Mg did not differ from 1 (Tle 2). For C nd Zn, whih umulted in senesed leves,, 1, suggesting tht umultions of C nd Zn deresed with their inresing onentrtions in green leves. When dt were grouped y funtionl type, the effet of [nutrient] green on nutrient RE seemed to dispper for mny funtionl types (Tle 2); similr results were oserved in glol dt set (Vergutz et l., 212). It ws likely tht smll rnge of [nutrients] green nd smll smple size in single funtionl type filed to revel this effet (Koe et l., 25), s nutrient onentrtions differed mong funtionl types in the present study (Tle 1). Unexpetedly, we found no reltionship etween nutrient REs nd the rtios of N to other nutrients in green leves, suggesting tht the reltive nutrient limittions indited y the rtios of N to other nutrients were poor preditors of nutrient RE. In svnn eosystem, folir N:P rtios lso did not predit the REs of N nd P(Rtnm et l., 28), wheres the N:P rtio ws good inditor for the RE of P in P-limited wetlnd (Rejmánková, 25). In ontrst, the RPs of N, K nd Mg were indited y the N:P, N:K nd N:Mg rtios, respetively (Tle 3; Supplementry Dt Fig. S2), suggesting tht reltive nutrient limittions ould predit RPs of N, K nd Mg in the krst hitts, in ordne with previous oservtions in other eosystems (Rejmánková, 25; Rtnm et l., 28). In ddition, for nutrients (B, C, Fe, Mn, S nd Zn) tht umulted in senesed leves, their onentrtions in senesed leves inresed with their lowered reltive limittions ompred with N. In ontrst to our expettion, vegettion degrdtion did not derese most soil nutrient ontents exept for K, nd differenes in soil nutrients mong vegettion types were usully smll (Supplementry Dt Tle S1). However, effets of soil nutrients on plnt nutrient resorption were deteted, espeilly for evergreen shrus, whih tended to inrese the REs of P, K nd Mg nd RPs of K nd Mg s soil P, K nd Mg ontents deresed. Evergreen shrus (e.g. I. yunnnensis, P. fortunen nd Rh. heterophyll) usully dominte in the krst soils tht hve low nutrient vililities, whih ould e explined y their enhned nutrient reuse from senesed leves nd lowered nutrient requirements from soil. Nutrient onentrtions nd resorption ptterns mong vegettion types Nutrient onentrtions of the sme funtionl types usully showed no signifint differenes mong the four vegettion types (Supplementry DtFig.S3), whih my edue tothe smllvriility in most soil nutrients (Supplementry Dt Tle S1). The remrkly low K ontent in the soil of grsslnds proly used the lowest K onentrtions of evergreen nd deiduous shrus in this vegettion type. Consequently, we ttriuted the signifint differenes in nutrient onentrtions of different vegettion types to the different speies ompositions rther thn soil onditions. For exmple, grsslnds showed the highest K onentrtion in green leves nd RE for K (Fig. 3), euse the dominnt funtionl types (grsses nd fors) hd higher K onentrtions (Tle 1)ndREsforK(Fig.2). Conlusions Aording to the stoihiometry of 13 nutrients in green leves, plnt growth ws minly limited y P in the krst region of Chin. However, further fertiliztion experiments should e onduted to test this. Overll, four nutrients (N, P, K nd Mg) reveled resorption, seven (B, C, Cu, Fe, Mn, Mo nd Zn) umulted in senesed leves nd two (N nd S) did not show resorption or umultion. The RE of N, P nd K nd the umultion of C nd Zn inresed with their deresing onentrtions in green leves. The N:P, N:K nd N:Mg rtios in green leves predited the RPs of N, K nd Mg, respetively. As different nutrient resorption ptterns mong plnt funtionl types signifintly ffeted litter qulities, further studies re needed to revel how litter nutrient onentrtions regulte the proess of Downloded from y guest on 31 August 218

12 884 Liu et l. Nutrient stoihiometry nd resorption in plnts deomposition nd to improve our understnding of nutrient yling in krst eosystems. SUPPLEMENTARY INFORMATION Supplementry dt re ville online t oxfordjournls.org nd onsist of the following. Tle S1: nutrient ontents of topsoil of the four vegettion types. Tle S2: detiled informtion of the smpling sites of the four vegettion types. Tle S3: list of the studied plnt speies in the four vegettion types. Figure S1: reltionships etween nutrient onentrtions in green nd senesed leves. Figure S2: reltionships etween the rtios of N to other nutrients in green leves nd nutrient onentrtions in senesed leves. Figure: S3: nutrient onentrtions nd resorption effiienies of evergreen shrus, deiduous shrus nd deiduous trees in the four vegettion types. ACKNOWLEDGEMENTS We thnk Professor Sho Jin Zheng nd the nonymous referees for their vlule omments on the mnusript. This study ws supported y the Ntionl Key Bsi Reserh Progrm of Chin (213CB95671), the Ntionl Nturl Siene Foundtion of Chin ( ), the Strtegi Priority Reserh Progrm of the Chinese Ademy of Sienes (XDA574) nd the Ministry of Environmentl Protetion of Chin (212928). LITERATURE CITED Aerts R Nutrient resorption from senesing leves of perennils: re there generl ptterns? Journl of Eology 84: Aerts R Climte, lef litter hemistry nd lef litter deomposition in terrestril eosystems: tringulr reltionship. Oikos 79: Aerts R, Cornelissen JHC, vn Logtestijn RSP, Cllghn TV. 27. Climte hnge hs only minor impt on nutrient resorption prmeters in highltitude petlnd. Oeologi 151: Ågren GI. 28. Stoihiometry nd nutrition of plnt growth in nturl ommunities. Annul Review of Eology Evolution nd Systemtis 39: Brron AR, Wurzurger N, Bellenger JP, Wright SJ, Krepiel AML, Hedin LO. 29. Molydenum limittion of symioti nitrogen fixtion in tropil forest soils. Nture Geosiene 2: Berg B, Dvey MP, De Mro A, et l. 21. 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