A meta-analysis of plant physiological and growth responses to temperature and elevated CO 2

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1 Oecologi (212) 169:1 13 DOI 1.17/s CONCEPTS, REVIEWS AND SYNTHESES A met-nlysis of plnt physiologicl nd growth responses to temperture nd elevted CO 2 Dn Wng Scott A. Heckthorn Xinzhong Wng Stcy M. Philpott Received: 21 June 21 / Accepted: 1 Octoer 211 / Pulished online: 29 Octoer 211 Ó Springer-Verlg 211 Astrct Atmospheric cron dioxide (CO 2 ) nd glol men temperture re expected to e significntly higher y the end of the 21st century. Elevted CO 2 (eco 2 ) nd higher temperture ech ffect plnt physiology nd growth, ut their interctive effects hve not een reviewed sttisticlly with respect to higher chronic men tempertures nd rupt het stress. In this met-nlysis, we exmined the effect of CO 2 on the physiology nd growth of plnts sujected to different temperture tretments. The CO 2 tretments were ctegorized into mient (\4 ppm) or elevted ([56 ppm) levels, while temperture tretments were ctegorized into mient temperture (AT), elevted temperture (; AT? C), or het stress (; AT? [8 C). Plnt species were grouped ccording to photosynthetic pthwys (C 3, C 4 ), functionl types (legumes, non-legumes), growth forms (herceous, woody), nd economic purposes (crop, non-crop). eco 2 Communicted y Rm Oren. Electronic supplementry mteril The online version of this rticle (doi:1.17/s ) contins supplementry mteril, which is ville to uthorized users. D. Wng S. A. Heckthorn S. M. Philpott Deprtment of Environmentl Sciences, University of Toledo, Toledo, OH, USA Present Address: D. Wng (&) Institute for Genomic Biology, University of Illinois t Urn-Chmpign, 126 W. Gregory, Urn, IL 6181, USA e-mil: dwng@illinois.edu X. Wng Deprtment of Biology, Indin University Purdue University Indinpolis, Indinpolis, IN, USA enhnced net photosynthesis t AT,, nd in C 3 species (especilly t the level), ut in C 4 species, it hd no effect t AT, positive effect t, nd negtive effect t. The positive effect of eco 2 on net photosynthesis ws greter for legumes thn for non-legumes t, for non-crops thn crops t, nd for woody thn herceous species t nd. Totl (W T ) nd ove- (W AG ) nd elow-ground (W BG ) iomss were incresed y eco 2 for most species groups t ll tempertures, except for C 4 species nd W BG of legumes t. Hence, eco 2 9 het effects on growth were often not explined y effects on net photosynthesis. Overll, the results show tht eco 2 effects on plnt physiology nd growth vry under different temperture regimes, mong functionl groups nd photosynthetic pthwys, nd mong response vriles. These findings hve importnt implictions for iomss ccumultion nd ecosystem functioning in the future when the CO 2 level is higher nd climte extremes, such s het wves, ecome more frequent. Keywords Glol chnge Elevted CO 2 Het stress Met-nlysis Biomss Photosynthesis Arevitions A Net CO 2 ssimiltion rte (lmol m -2 s -1 ) AT Amient temperture Elevted temperture CO 2 Amient CO 2 eco 2 Elevted CO 2 F v /F m Photosystem II (PSII) efficiency g s Stomtl conductnce Het stress N L Lef nitrogen concentrtion N R Root nitrogen concentrtion RA Ruisco ctivity (lmol m -2 s -1 )

2 2 Oecologi (212) 169:1 13 SLA W T W AG W BG Introduction Specific lef re Totl plnt weight (dry mss) Aove-ground weight (dry mss) Below-ground weight (dry mss) As consequence of humn ctivities, glol tmospheric cron dioxide (CO 2 ) nd temperture, oth key vriles ffecting plnt growth, development, nd function, hve chnged in the recent pst nd re predicted to increse in the future. Increses in CO 2 nd other greenhouse gses re lrgely responsile for recent increses in glol men surfce tempertures, which rose y.6 C from 199 to 2 nd re projected to increse y nother C y the yer 21 (Houghton et l. 21; IPCC 21, 27). In ddition to rising men nnul tempertures, there will lso e increses in the frequency, durtion, nd severity of periods with exceptionlly high tempertures (Wgner 1996; Hldimnn nd Feller 24). Thus, plnts in the future will not only e exposed to elevted levels of CO 2 (eco 2 ), ut will lso likely experience more cute het stress (), which cn gretly impct ecosystem productivity (Ciis et l. 25) nd iodiversity (Dvis 1986; Thoms et l. 24). The interctive effects of eco 2 nd temperture on the physiology nd growth of lrge numer of plnt species hve een investigted, lthough mostly for increses in men tempertures (i.e., chronic wrming) (Morison nd Lwlor 1999), rther thn for rupt temperture increses (Wng et l. 28, nd references therein). Since net CO 2 ssimiltion rte per unit re (A) is ffected y the rtio of CO 2 nd tmospheric oxygen (O 2 ) s they compete for cron fixtion nd photorespirtion t the ctive site of the enzyme riulose-1,5-isphosphte croxylse-oxygense (Ruisco), incresed CO 2 reduces cron loss through photorespirtion. However, elevted temperture increses photorespirtion due to the reduced soluility of CO 2 compred with O 2 nd reduced specificity of Ruisco for CO 2 t higher tempertures (Sge nd Monson 1999). It hs therefore een predicted tht photosynthetic response to eco 2 in plnts with C 3 metolism will e lrger t higher tempertures (Long 1991; Gifford 1995; Bowes et l. 1996). In contrst, it hs een generlly considered tht C 4 species will show little CO 2 stimultion irrespective of temperture ecuse of the CO 2 concentrtion mechnism in C 4 species. Recent studies, however, hve shown sustntil stimultion of oth net photosynthesis nd iomss in C 4 species under non- conditions (Ghnnoum et l. 2). Therefore, the response of C 4 species to the interctive effect of temperture nd CO 2 requires further exmintion. Although lrge numer of empiricl studies hve exmined effects of eco 2 nd elevted growth temperture (typiclly 3 5 C) on photosynthesis (reviewed y Morison nd Lwlor 1999), the interctions etween eco 2 nd (typiclly [8 C ove the norml growth temperture) hve een investigted in only limited numer of studies (Wng et l. 28). The results hve een vrile nd hve not een reviewed sttisticlly. One of the negtive effects of on plnts is the dmge to photosynthesis, often y impiring photosystem II (PSII) in the light rections (electron trnsport) (Berry nd Bjorkmn 198; Heckthorn et l. 1998, 22) nd Ruisco ctivse in the Clvin-cycle (drk) rections (Eckrdt nd Portis 1997; Crfts-Brndner nd Lw 2; Crfts-Brndner nd Slvucci 2). While with mild temperture increses, eco 2 hs consistently positive effects on plnts, t, eco 2 cn hve positive (Fri et l. 1996, 1999; Huxmn et l. 1998; Ferris et l. 1998; Hmerlynck et l. 2; Tu et l. 2), negtive (Bssow et l. 1994; Roden nd Bll 1996; Huxmn et l. 1998; Tu et l. 2), or no effects (Colemn et l. 1991), or positive effects for C 3 species nd negtive effects for C 4 species (Wng et l. 28) on plnt photosynthesis nd growth. Due to the contrsting effect of CO 2 t elevted tempertures () nd, it is criticl to exmine the role of CO 2 under different temperture tretments nd for different functionl groups to etter understnd plnt responses to multiple environmentl chnges in the future. In ddition to temperture tretments nd species groups, tretment durtion nd growth fcility (pot or inground, growth chmer or greenhouse, etc.) might lso ffect CO 2 responses. In the short term, CO 2 fixtion my e stimulted y eco 2 ; however, in the long term, this effect my e prtly lost s result of down-regultion of photosynthesis (Gunderson nd Wullschleger 1994). This down-regultion of photosynthesis might e ssocited with n over-production of ssimiltes reltive to sink demnd nd my, therefore, e ssocited with n ccumultion of non-structurl crohydrtes in the leves (vn Oosten nd Besford 1996) or decresed Ruisco ctivity nd production cused y decresed nitrogen (N) concentrtion (Luo et l. 24). Therefore, in this met-nlysis, we ctegorized reports into groups sed on tretment durtion nd growth fcility. Key physiologicl vriles, such s Ruisco ctivity nd N concentrtion, were nlyzed sed on different temperture tretments nd species groups. In order to ssess the effects of eco 2 nd temperture on plnt iomss nd physiologicl performnce, we conducted comprehensive met-nlysis of CO 2 studies pulished efore the end of 21 in which plnt

3 Oecologi (212) 169: photosynthesis or growth ws reported t different temperture nd CO 2 tretments. In this met-nlysis, we summrized nd interpreted 466 oservtions of CO 2 effects on plnt physiology nd growth under different temperture tretments extrcted from 84 seprte pulictions [Electronic supplementry mteril (ESM)]. The mjor ojectives of this met-nlysis were twofold: (1) to provide estimtes of the mgnitude nd significnce of eco 2 effects on plnt iomss ccumultion nd prtitioning, net photosynthesis, PSII function, stomtl conductnce, Ruisco ctivity, specific lef re (SLA), nd lef nd root N concentrtion under different glol-wrming scenrios; (2) to test for differences mong plnt functionl groups nd growth forms in ffecting these responses. We hypothesized: (1) the enhncement of iomss nd net photosynthesis y eco 2 would e less pronounced t thn t AT or, which might e ssocited with het-dmge effects on PSII function, g s,or Ruisco ctivity; (2) C 4 species would hve smller enhncement thn C 3 species in iomss nd net photosynthesis in response to eco 2 t ll temperture tretments due to the CO 2 -concentrting mechnism in C 4 plnts; (3) legume species would show greter enhncement thn non-legumes, especilly t, s consequence of higher tissue N concentrtions, which cn limit N-dilution effects on plnt function under conditions of eco 2. Methods Dt collection The peer-reviewed journl rticles used to construct the dtse for this met-nlysis were otined y serching the Science Cittion Index (SCI) of the Institute of Scientific Informtion. The list of rticles otined were susequently cross-checked with references cited in lrge numer of CO 2 review rticles nd ooks to ensure the inclusion of ll rticles contining dt relevnt for this met-nlysis. Any rticle pulished in English efore the end of 21 tht met ll of the following criteri ws included: (1) CO 2 tretment [25 nd \4 lmol mol -1 nd eco 2 tretment etween 5 nd 1, lmol mol -1 ; (2) plnts were treted t mient temperture (AT) nd with either or het stress () under conditions of oth CO 2 nd eco 2 ; (3) photosynthetic mesurements were conducted t the growth CO 2 nd tempertures. In those studies from which we collected dt, the CO 2 tretment typiclly included mient (32 4 lmol mol -1 ) nd elevted (56 1, lmol mol -1 ) CO 2 concentrtions. Only one study hs CO 2 t 25 lmol mol -1 nd one study hs eco 2 t 1,3 lmol mol -1 (ESM). On verge, for the CO 2 nd eco 2 tretments included in the met-nlysis, the CO 2 levels were 366 nd 72 lmol mol -1 t AT, 362 nd 691 lmol mol -1 t, nd 364 nd 711 lmol mol -1 t, respectively. Response vriles extrcted from these rticles include net photosynthesis (net CO 2 ssimiltion) (A), PSII efficiency (F v /F m mesured in the drk), stomtl conductnce to wter vpor (g s ), Ruisco ctivity (RA), SLA, ove-ground (W AG ), elow-ground (W BG ), nd totl (W T ) weight of plnt dry mss, nd lef (N L ) nd root (N R ) N concentrtion. For multi-yer studies on nnul species, results from different sesons were considered independent, nd ll oservtions were included in this nlysis. For multi-yer studies on perennil species, only those studies with the longest CO 2 exposure were included. If study included more thn one species, ll of the oservtions were considered to e independent nd included in the dtse. If study exmined the interctive effects of CO 2 nd non-temperture stress fctors, only those mesurements from the non-stressed experiments, e.g., low ozone or well-wtered plnts, were included. Ctegoriztion of studies For this nlysis, temperture tretments were ctegorized into three levels: AT, (1.4 6 C ove mient), nd ([8 C ove mient). Originlly, the temperture ctegories used in this met-nlysis were intended to e ctegorized into AT nd (AT? C), s predicted y IPCC (21, 27), ut this ws modified to (AT? C) nd (AT? [8 C), since \6 nd [8 C? AT were used most frequently in the reference ppers. Thus, the temperture ctegories were essentilly ritrry nd should not e considered s defining fixed oundries for the specific temperture tretment. Plnt species were ctegorized sed on photosynthetic pthwy C 3 or C 4 ), N-fixing ility (legumes or non-legumes), growth form (herceous or woody), nd economic purpose (crop or non-crop). Reserch fcilities used to rise CO 2 concentrtion were divided into two rod clsses: (1) semi-open systems, which include open-top chmers (OTC) nd screen-ided CO 2 control (Ledley et l. 1997) nd (2) closed systems, which include greenhouses nd growth chmers. Pot size ws grouped into\1 L,[1 L, or in-ground. These size clsses hve een previously used in similr met-nlytic review looking t tree responses to CO 2 (Curtis 1996; Wnd et l. 1999). Met-nlyticl methods This met-nlysis followed the techniques descried in the work of Wng (27). We used the nturl logrithmtrnsformed rtio (ln r) of plnt responses t elevted to mient levels of CO 2 to estimte the effect size of the CO 2 tretment (Hedges et l. 1999). In order to include the lrge

4 4 Oecologi (212) 169:1 13 percentge of studies tht did not dequtely report smple sizes nd vrinces, we performed unweighted nlysis using the sttisticl softwre progrm MetWin 2. (Rosenerg et l. 2). A mixed-effects model ws used in this nlysis with the ssumption tht there were rndom vritions in effect sizes mong the diverse studies included in this synthesis. Consequently, the confidence intervls generted re lrger thn those of fixed-effect model nd cn represent more conservtive interprettions. Confidence intervls (CI) for effect-size estimtes were generted y ootstrpping the unweighted dt using MetWin 2. with resmpling of 9,999 itertions. eco 2 ws considered to hve significnt effect on vrile if the ootstrp CIs of its percentge chnge did not overlp zero. The response to eco 2 ws considered to e significntly different etween temperture tretments if their CIs did not overlp. Significnce ws estlished t p \.5 unless otherwise noted. For the significnt effect of ln r, we looked for the potentil of puliction is in the met-nlysis. First, we clculted Spermn s rnk-order correltion, r s, sttistic tht descries the reltionship etween the effect size (ln r) nd the smple size of the nlysis (Begg nd Mzumdr 1994). A significnt correltion of r s (i.e., p \.5) demonstrted significnt is, wherey, for exmple, lrger effect sizes re more likely to e pulished thn smller effect sizes. We lso clculted Rosenthl s fil-sfe numer with Met-Win 2.. This vlue yields the numer of dditionl studies with men effect size of zero needed to eliminte the significnce of significnt effect (Rosenthl 1979). If the fil-sfe numer is lrger thn criticl vlue of 5n? 1, where n is the numer of studies, then puliction is my e sfely ignored (Rosenerg 25). Puliction is will e reported if it existed for certin effect size nd could not e ignored. Results Across ll plnts nd environmentl conditions synthesized in this nlysis, eco 2 impcted F v /F m nd SLA y different mgnitudes t different temperture tretments, ut the eco 2 effect ws not significntly different mong temperture tretments for A, g s, RA, nd N L (Fig. 1). Elevted CO 2 incresed A t AT (13.9%), (19.5%), nd (14.3%) (Fig. 1). In contrst, F v /F m ws unffected y eco 2 t AT nd, ut ws decresed y eco 2 t (.46 t CO 2 nd.43 t eco 2 ) (Fig. 1). There ws puliction is for the effect of eco 2 on F v /F m t (r s =.58, p =.24). Since the clculted Rosenthl s fil-sve numer (84.4) ws not ove the criticl vlue (85), the puliction is could not e ignored. Elevted CO 2 decresed g s nd RA t ll temperture tretments, ut there were no significnt differences mong different temperture tretments (Fig. 1c, d). SLA ws decresed y eco 2 t AT (-1.7%), unchnged t, nd incresed t (17.2%) (Fig. 1e). N L ws decresed y eco 2 t ll temperture tretments (Fig. 1f). Responses of A, F v /F m, nd g s to temperture 9 eco 2 vried in C 3,C 4, legume, nd non-legume species (Fig. 2). For C 3 species, eco 2 incresed A y 15.3, 19.9, nd 28.7% t AT,, nd, respectively (Fig. 2), nd the difference in response t AT versus ws significnt. However, for C 4 species, eco 2 hd no effect t AT, incresed A t y 17.7%, ut hd negtive effect on A t (-21.%). eco 2 incresed A y 12.3 (not significnt), 2.9, nd 36.6% t AT,, nd for legumes, nd y 15.4, 19.1, nd 6.4% (not significnt for ) for nonlegumes; the response of legumes differed from tht of non-legumes only t, wherein the effect of eco 2 ws greter in legumes thn in non-legumes. For the F v /F m of C 3 species, eco 2 hd slight positive effect t AT, no significnt effect t, nd negtive effect t. For C 4 nd non-legume species, eco 2 hd negtive effect on F v /F m t AT nd, ut no effect t. For legume species, eco 2 hd positive effect on F v /F m t AT, ut no effect t nd (Fig. 2). The decrese of F v /F m y eco 2 t ws greter in C 4 thn in C 3 species. For C 3, C 4, legume, nd non-legume species, g s ws decresed y eco 2 t ll temperture tretments, with the difference etween C 3 nd C 4 species t AT nd eing significnt; there ws less of decrese in g s y eco 2 in C 3 plnts thn in C 4 plnts t AT, ut more of n increse in C 3 thn C 4 plnts t (Fig. 2c). eco 2 incresed A t AT,, nd for ll herceous, woody, crop, nd non-crop species, nd there were significntly different responses etween nd for noncrop species (Fig. 3). Elevted CO 2 hd no significnt effect on F v /F m t AT, ut it did hve negtive effect t for ll herceous, woody, crop, nd non-crop species (Fig. 3). The decrese of F v /F m y eco 2 t ws more in herceous thn in woody species nd more in non-crop thn in crop species. At, eco 2 hd positive effect on F v /F m in herceous nd crop species, ut no effect on woody nd non-crop species. For ll species groups, g s ws decresed y eco 2 t ll temperture tretments (except for woody t ), with the difference eing significnt etween AT or nd for herceous species, etween AT or nd for crops, nd etween nd AT or for non-crop species (Fig. 3c). At AT nd, the decrese in g s y eco 2 ws greter in herceous thn in woody species, nd greter in crop thn in non-crop species. eco 2 decresed the N L of C 3 species y 5.2, 5.7, nd 16.5% t the AT,, nd levels, respectively, nd the difference ws not significnt mong different temperture tretments. The N L of C 4 species ws not significntly

5 Oecologi (212) 169: Fig. 1 Responses to elevted CO 2 (eco 2 ) in net photosynthetic rte (A; ), photosystem II (PSII) efficiency (F v /F m ; ), stomtl conductnce (g s ; c), ruisco ctivity (RA; d), specific lef re (SLA; e), nd nitrogen (N) content in lef (N L ; f) for plnts grown under different tempertures (AT mient temperture, elevted temperture, het stress). Ech dt point represents the men ± 95% confidence intervl (CI; whiskers). The numer of oservtions for ech ctegory used in the nlysis is given t the ottom of ech grph, under the corresponding CI. p \.5 nd p \.1 for comprison etween temperture tretment ctegories whose CIs do not overlp Chnge t elevted CO 2 (%) c d A e F v /F SLA m g s f RA N L AT AT -3 Fig. 2 Photosynthetic responses to eco 2 in C 3,C 4, legume, nd non-legume species t different temperture tretments for net photosynthetic rte (A; ), PSII efficiency (F v /F m ; ), nd stomtl conductnce (g s ; c). Ech dt point represents the men ± 95% CI (whiskers). The numer of oservtions for ech ctegory used in the nlysis is given t the ottom of ech grph, under the corresponding CI. p \.5 nd p \.1 for comprison etween temperture tretment ctegories whose CIs do not overlp Chnge t elevted CO 2 (%) c AT A F v /F M g s C 3 species C 4 species Legumes Non-legumes -6

6 6 Oecologi (212) 169:1 13 Fig. 3 Photosynthetic responses to eco 2 in herceous, woody, crop, nd non-crop species t different temperture tretments for net photosynthetic rte (A; ), PSII efficiency (F v /F m ; ), nd stomtl conductnce (g s ; c). Ech dt point represents the men ± 95% CI (whiskers). The numer of oservtions for ech ctegory used in the nlysis is given t the ottom of ech grph, under the corresponding CI. p \.5 nd p \.1 for comprison etween temperture tretment ctegories whose CIs do not overlp Chnge t elevted CO 2 (%) 4 AT A F v /F M c g s Herceous Woody Crop Non-crop ffected y eco 2 t ll temperture tretments (Fig. 4), nd the N R of C 3 nd C 4 species ws not ffected y eco 2 t ll tempertures (Fig. 4). For N R, there ws puliction is for C 3 (r s =.83, p =.42) nd C 4 (r s =.83, p =.42) species t, nd in oth cses, the puliction is could not e ignored sed on Rosenthl s vlue. The W T, W AG, nd W BG were ll incresed y eco 2 in C 3, legume, nd non-legume species t ll temperture tretments (except for legumes t ) (Fig. 5). For C 4 species, CO 2 hd no effect on W T, W AG, nd W BG t AT, ut it tended to hve positive effect t nd, lthough the puliction is could not e ignored. Elevted CO 2 incresed W T, W AG, nd W BG in herceous, woody, crop, nd non-crop species t ll temperture tretments (Fig. 6). At, the enhncement of W T nd W AG y eco 2 ws greter in crops thn in non-crops; the increse in W AG nd W BG y eco 2 in crops ws greter thn tht in non-crops t AT (Fig. 6). At AT, the effect of eco 2 on A ws greter in plnts grown in\1-l pots thn in those in[1-l pots; t nd, this effect did not differ etween plnts grown in smller pots nd those grown in lrger ones. However, the effect of eco 2 on A ws smller for plnts grown in the ground t AT nd thn in those grown in pots (Fig. 7). At nd, the effect of eco 2 on W T ws greter in plnts grown in [1-L-pots thn on those grown in \1-L pots or in the ground (Fig. 7). Photosynthetic enhncement y eco 2 ws lowest in plnts exposed to eco 2 t AT for [1 yer nd gretest in plnts exposed to eco 2 for 1 3 dys. The effect of eco 2 on A ws not different mong exposure durtions t. At, the effect of eco 2 on A ws higher in plnts exposed to eco 2 for dys tht in those with \1-dy tretment (Fig. 8). In ddition, stimultion of A y eco 2 tended to decrese in versus AT in plnts exposed to eco 2 for \1 or 1 3 dys, ut increse in heted versus AT plnts in plnts exposed to eco 2 for dys. W T lwys incresed with eco 2, regrdless of the tretment durtion. At, the enhncement of W T ws greter in plnts exposed to eco 2 for [1 yer thn in those exposed to eco 2 for dys (Fig. 8). Discussion In this met-nlysis, consistent with the prediction tht high temperture stress is expected to e llevited y eco 2 due to improved photosynthesis in most species under hot conditions (Long 1991; Morison nd Lwlor 1999), when verged cross ll species, net photosynthesis ws

7 Oecologi (212) 169: Chnge of Nirogen concentrtion t elevted CO 2 (%) 4 AT C 3 species C 4 species Fig. 4 Response of plnt tissue nitrogen concentrtion to eco 2 in C 3 nd C 4 species t different temperture tretments for lef N concentrtion (N L ; ) nd root N concentrtion (N R ; ). Ech dt point represents the men ± 95% CI (whiskers). The numer of oservtions for ech ctegory used in the nlysis is given t the ottom of ech grph, under the corresponding CI. p \.5 nd p \.1 for comprison etween temperture tretment ctegories whose CIs do not overlp enhnced y eco 2 t nd (Fig. 1). However, plnts with different photosynthetic pthwys responded differently to eco 2 nd temperture. In C 3 species, which comprise pproximtely 9% of ll plnt species, net photosynthesis ws enhnced y eco 2 t ll tempertures, with the enefit eing the gretest t nd the lest t AT. For C 4 species, eco 2 hd no effect t AT, positive effect t (s in Wnd et l. 1999), nd negtive effect t (s in Wng et l. 28) (Fig. 2). In C 3 species, the enefits of eco 2 t high tempertures re likely due to decreses in photorespirtion tht offset decreses in F v /F m, RA, g s,or N L. In C 4 species, however, which hve low levels of photorespirtion nd re CO 2 sturted t the current CO 2 level, the negtive effect of eco 2 on net photosynthesis t my e relted to decresed N L or higher lef tempertures cused y lower stomtl conductnce (Wng et l. 28). Growth temperture is known to strongly influence the response nd tolernce of orgnisms nd photosynthesis to (Bru nd Heckthorn 24). It hs een reported tht growing cool-seson C 3 species t lower temperture (25 C) increses the enefits of eco 2 on the photosynthetic tolernce to of these plnts compred with growing them t higher temperture (3 C) (Wng et l. 28). However, the verge growth temperture for C 3 (29.5 ± 1.8 C, n = 32) nd C 4 (3.1 ± 2.5 C, n = 15) N L N R species ws not significntly different in the tretment of this study. The enhncement of photosynthesis y eco 2 ws found to e greter for woody species thn for herceous species t nd, which might e due to the inclusion of the more-responsive juvenile nd exponentilly growing trees in mny CO 2 studies (Wng 27), nd the enefit of eco 2 ws found to e greter in non-crop thn crop species t (Fig. 2). It is importnt to note tht low smple sizes for some functionl groups used in this nlysis (e.g., C 4, legumes, nd trees) require tht some results in this nlysis e interpreted with cution; nevertheless, results from these under-represented groups demonstrte tht further study of these groups is criticl, nd these results provide hypotheses for future studies to test. The response of g s to eco 2 is criticl for modeling ecosystem nd lndscpe-scle wter flux. We found decresed stomtl conductnce (g s ) t eco 2 for ll species groups (excluding woody species t ), regrdless of different temperture tretments, which is consistent with the findings from other reviews (Long et l. 24; Ainsworth nd Long 25; Ainsworth nd Rogers 27). g s ws decresed less y eco 2 for C 4 thn for C 3 t, which suggested tht the negtive effect of eco 2 on A for C 4 species ws not directly cused y the decrese in g s. The decrese of g s y eco 2 ws less for woody thn for herceous nd for non-crop thn for crop species t AT nd. Hence, these results from this current study re similr to the trend reported for trees, shrus, nd fors, showing lower percentge decrese in g s compred to C 3 nd C 4 grsses nd herceous crops (Sxe et l. 1998; Ainsworth nd Rogers 27). As suggested in Wrren et l. (211), the decrese in g s my increse lef temperture resulting from decline in ltent het loss through evportion, which my further ffect net cron lnce. It hs een hypothesized tht t supr-optiml tempertures, oth electron trnsport cpcity nd Ruisco ctivse cpcity cn limit net photosynthesis t eco 2 (Sge nd Kuien 27). In this nlysis, PSII efficiency (F v /F m ) ws negtively ffected y eco 2 t (except for legumes), regrdless of the photosynthetic pthwy, indicting tht eco 2 enhnced photoinhiition t higher tempertures (s in Roden nd Bll 1996). More reserch is needed on the effect of CO 2 on PSII efficiency t, since the puliction is on this effect could not e ignored in this met-nlysis. At AT, elevted CO 2 increses F v /F m in legumes ut decreses it in non-legumes, which indirectly supports the hypothesis tht eco 2 decreses photoinhiition under conditions of high N ut increses photoinhiition under conditions of low N (Hymus et l. 21). RA ws negtively ffected y eco 2 t AT,, nd (Fig. 1d). High-CO 2 effects on RA often closely mtch reductions in N content nd increses in solule crohydrte levels (Korner 26; Reich et l. 26; Rustd 26).

8 8 Oecologi (212) 169:1 13 Fig. 5 Biomss response to eco 2 in C 3,C 4, legume, nd non-legume species t different temperture tretments for whole-plnt dry weight (W T ; ), ove-ground dry weight (W AG ; ), nd elow-ground dry weight (W BG ; c). Ech dt point represents the men ± 95% CI (whiskers). The numer of oservtions for ech ctegory used in the nlysis is given t the ottom of ech grph, under the corresponding CI. p \.5 nd p \.1 for comprison etween temperture tretment ctegories whose CIs do not overlp Biomss chnge t elevted CO 2 (%) c AT W T W AG W BG Legume Non-legume C 3 species C 4 species Decresed RA could e cused y reduced Ruisco content or y decresed specificity of Ruisco (Arnjuelo et l. 25; Korner 26; Gutschick 27). It hs een well documented tht the vilility of minerl nutrients, prticulrly N, cn gretly modify plnt growth responses to eco 2 (Diz et l. 1993; Heeisen et l. 1997; Luo et l. 24; Reich et l. 26). The negtive effect of eco 2 on net photosynthesis in C 4 species t, including F v /F m, might lso e relted to decresed N concentrtion, which could result in the impired synthesis of photosynthetic enzymes nd protecting systems; such dmge would not e compensted for y decresed photorespirtion t eco 2,sinC 3 species (Bunce 2; Arnjuelo et l. 25). Perhps due to the smller dtset, we were unle to detect significnt decrese of N L for C 4 species t eco 2. However, we did find tht cross ll species, N L tended to decrese t ll tempertures with eco 2 nd tht the mgnitude of the decrese ws gretest t, lthough it ws not significntly different from tht t AT nd (Fig. 1f). We further tested this hypothesis y seprting plnts into legumes nd non-legumes, on which eco 2 imposed similr effects on A t AT nd. However, t, eco 2 hd significntly greter positive effect on legumes thn on non-legumes (Fig. 2), which indirectly suggests tht N L might ply role in plnt tolernce to t eco 2.In this met-nlysis, due to the smller smple sizes t, specific mechnisms of eco 2 on N L nd N R t nd should e generlized with cution, nd more studies re needed to further understnd these CO 2 9 temperture effects nd their underlying cuses, such s chnges in lef temperture nd increses in het-shock proteins (Wng et l., unpulished dt), protective comptile solutes (Willims et l. 1992), nd isoprene production (Velikov nd Loreto 25). It is importnt to note tht A per unit lef re is not the most importnt fctor for predicting overll plnt growth (Korner 1991). The comintion of crohydrte production, which is determined y photosynthetic rte nd lef re, nd the consumption of crohydrtes for growth, respirtion, storge, nd root exudtion, ccount for most of the overll growth enhncement under conditions of eco 2 (Morison nd Lwlor 1999). The negtive effect of eco 2 on A in C 4 species t might e offset y the positive effects of eco 2 on lef re, respirtion, nd wter use efficiency (Owensy et l. 1993, 1999; Hmerlynck et l. 1997), or the imlnce etween source (photosynthesis) nd sink (growth). Consistent with the finding tht LMA (lef mss per unit re, the inverse of SLA) increses t higher CO 2 levels (Poorter et l. 29), in our

9 Oecologi (212) 169: Fig. 6 Biomss response to eco 2 in herceous, woody, crop, nd non-crop species t different temperture tretments for whole-plnt dry weight (W T ; ), ove-ground dry weight (W AG ; ), nd elow-ground dry weight (W BG ; c). Ech dt point represents the men ± 95% CI (whiskers). The numer of oservtions for ech ctegory used in the nlysis is given t the ottom of ech grph, under the corresponding CI. p \.5 nd p \.1 for comprison etween temperture tretment ctegories whose CIs do not overlp Biomss chnge t elevted CO 2 (%) c AT W T W AG W BG Herceous Woody Crop Non-crop study, t AT, SLA decresed t eco 2 (Fig. 1e). SLA declines when the increse in lef size is less thn the increse in lef mss t eco 2 (Yin 22). We found tht the decrese in SLA with eco 2 ws less pronounced t thn t AT (Fig. 1e). It hs lso een reported tht C 3 nd C 4 species differ in their response, with C 4 species showing decrese in LMA (=n increse in SLA) t the higher CO 2 concentrtions (Ackerly et l. 1992; Wolfe et l. 1998; Ghnnoum et l. 2; Poorter et l. 29). Higher SLA is eneficil for otining more extensive folir disply tht cptures more light for constnt iomss investment (Niinemets 1999), which could contriute to the positive effect of CO 2 on iomss gin t for C 4 species, despite the negtive effect on A. It hs lso een found tht eco 2 cn reduce trnspirtion (Bruhn et l. 22; Gonzelez- Meller et l. 24; Bunce 25). Reduced stomtl conductnce t eco 2 will slow the rte of trnspirtion nd therefore decrese the onset, severity, nd impct of wter stress, which is often ccompnied y high temperture stress (Morison 1993). More experiments re needed to ssess the lnce of these processes nd the extent nd direction of cclimtion of these processes to temperture nd CO 2 interction. It is essentil tht potentil confounding fctors e considered in met-nlysis which synthesizes results from lrge numer of studies tht were conducted under vriety of growing conditions on different plnt species. In our nlysis, studies in which plnts were grown under environmentl stresses (e.g., drought, low nutrients, light deficiency, or elevted ozone) were excluded. A lrge vrition in CO 2 effects on unstressed plnts, however, ws still found, due to differences in experimentl protocols nd temperture regimes in the empiricl studies. Growth temperture might interct with CO 2 to influence the response of photosynthesis to temperture tretments. Trees from tropicl nd sutropicl regions hve een reported to e more susceptile to growth declines in wrmer climte thn trees from higher ltitudes (Wy nd Oren 21). We found tht the durtion of the tretment ws nother importnt fctor ffecting plnt responses to high-temperture tretments. Photosynthetic enhncement in plnts exposed to eco 2 for more thn 1 yer ws not significnt t AT (Fig. 8). This temporl pttern suggests down-regultion of photosynthesis reltive to its initil cpcity t eco 2 nd is consistent with results from erlier studies with spruce (vn Oosten et l. 1992) nd ornge trees (Adm et l. 24). Down-regultion of photosynthesis y eco 2 hs een suggested to e correlted with reduced protein content nd enzyme ctivtion, sed on results relting to ltertions in the expression of genes

10 1 Oecologi (212) 169:1 13 Chnge t elevted CO AT Ground < 1 L > 1 L Fig. 7 Responses to eco 2 in net photosynthetic rte (A; ) nd whole-plnt dry weight (W T ; ) y plnts grown in the ground, in \1-L pots, or in [1-L pots nd under different temperture tretments. Ech dt point represents the men ± 95% CI (whiskers). The numer of oservtions for ech ctegory used in the nlysis is given t the ottom of ech grph, under the corresponding CI. p \.5 nd p \.1 for comprison etween temperture tretment ctegories whose CIs do not overlp encoding Ruisco t the trnscriptionl nd/or post-trnscriptionl level (Vn Oosten nd Besford 1994; Moore et l. 1999). Species differences in the photosynthetic responses to eco 2 could e ecologiclly importnt if they influence species productivity nd distriution nd, susequently, species dynmics. Another issue of concern out the effects of eco 2 hs een centered on how much the effects re influenced y the prticulr culturl or exposure systems used. The exposure systems used in the studies included in this met-nlysis were mostly closed systems, including greenhouses nd growth chmers. This metnlysis reveled no significnt effect of exposure systems on photosynthetic responses to CO 2 or temperture. Pot size is lso thought to e nother importnt fctor ffecting the mgnitude of photosynthetic responses to eco 2, y implicting root sink strength (Arp 1991). Contrry to the expecttion tht the effect of eco 2 on A would e smller for plnts grown in smll pots, we found tht the effect of eco 2 on A ws smllest for plnts grown in the ground, which perhps ws minly cused y the fct tht mny experiments in which plnts were grown in the ground lsted for more thn 1 yer. These results on pot size should e interpreted with cution, since we do not hve informtion on root temperture nd the pot size-to-plnt size rtios in studies used in this nlysis, or the extent to which nutrients were flushed through the pots during growth (Korner 23). A third potentil confounding fctor we considered is the ised choice of species in the empiricl studies, nd hence unlnced composition of species in different ctegories in this met-nlysis. For exmple, C 4 species, which re ll non-legumes, might ccount for the lower photosynthetic nd growth responses to eco 2 in nonlegumes, since the C 3 species used in this met-nlysis included numer of legumes. We excluded ll C 4 species from the non-legumes nd performed nother nlysis on plnt species tht were ll C 3 species. The results showed tht t AT nd, photosynthetic responses to eco 2 were similr for legumes nd non-legumes; ut t, eco 2 hd more pronounced effect (36%, n = 19) for legumes thn Fig. 8 Responses to elevted CO 2 in net photosynthetic rte (A; ) nd whole-plnt dry weight (W T ; ) under different temperture tretments for different tretment (CO 2 9 temperture) durtions. Ech dt point represents the men ± 95% CI (whiskers). The numer of oservtions for ech ctegory used in the nlysis is given t the ottom of ech grph, under the corresponding CI. p \.5 nd p \.1 for comprison etween temperture tretment ctegories whose CIs do not overlp Chnge of A t elevted CO 2 (%) AT < 1 dy 1-3 dys dys > 1 yer

11 Oecologi (212) 169: for non-legumes (18%, n = 41). These results demonstrte tht the inclusion of C 4 species did not oscure the comprison etween non-legumes nd legumes. In summry, we found significnt interctive effects of eco 2 nd temperture on numer of plnt physiologicl nd growth vriles. The most surprising result ws tht t, eco 2 hd negtive effect on photosynthesis in C 4 species, compred with positive effect in C 3 species. Compred with legumes, non-legumes showed less enhncement of photosynthesis in response to eco 2 t, suggesting tht the interctive effects of het nd eco 2 re prtly dependent on N sttus. W T responded positively to eco 2 in ll species group t ll tempertures, except in C 4 species. The negtive effects of eco 2 in C 4 species on photosynthesis under my e llevited y higher wter-use efficiency nd lef re of C 4 species, especilly in times of wter stress, nd the enefits of eco 2 to C 3 species my e offset y likely chnges in other environmentl fctors which influence thermotolernce differentilly (e.g., chnges in precipittion which might increse or decrese tolernce, nd incresing ozone which might decrese tolernce). This met-nlysis highlights the importnce of improving our mechnistic understnding of plnt responses to the interctive effects of eco 2 nd other iotic fctors, prticulrly higher temperture, incresed N deposition, nd ltered ptterns of precipittion, ll of which re expected in the future. References Ackerly DD, Colemn JS, Morse SR, Bzzz FA (1992) CO 2 nd temperture effects on lef-re production in two nnul plntspecies. Ecology 73(4): Adm NR, Wll GW, Kimll BA et l (24) Photosynthetic downregultion over long-term CO 2 enrichment in leves of sour ornge (Citrus urntium) trees. New Phytol 163: Ainsworth EA, Long SP (25) Wht hve we lerned from 15 yers of free-ir CO 2 enrichment (FACE)? A met-nlytic review of the responses of photosynthesis, cnopy properties nd plnt production to rising CO 2. New Phytol 165(2): Ainsworth EA, Rogers A (27) The response of photosynthesis nd stomtl conductnce to rising [CO 2 ]: mechnisms nd environmentl interctions. Plnt Cell Environ 3(3): Arnjuelo I, Perez P, Hernndez L, Irigoyen JJ, Zit G, Mrtinez- Crrsco R, Snchez-Diz M (25) The response of nodulted lflf to wter supply, temperture nd elevted CO 2 : photosynthetic downregultion. Physiol Plnt (3): Arp WJ (1991) Effects of source-sink reltions on photosynthetic cclimtion to elevted CO 2. Plnt Cell Environ 14(8): Bru D, Heckthorn SA (24) Acclimtion of the temperture setpoints of the het-shock response. J Therm Biol 29: Bssow SL, McConnughy KDM, Bzzz FA (1994) The response of temperte tree seedlings grown in elevted CO 2 to extreme temperture events. Ecol Appl 4(3): Begg CB, Mzumdr M (1994) Operting chrcteristic of rnd correltion test for puliction is. Biometrics 5: Berry J, Bjorkmn O (198) Photosynthetic response nd dpttion to temperture in higher-plnts. Annu Rev Plnt Physiol Plnt Mol Biol 31: Bowes G, Vu JCV, Hussin MW, Pennnen AH, Allen LH (1996) An overview of how Ruisco nd crohydrte metolism my e regulted t elevted tmospheric CO 2 nd temperture. Agric Food Sci Finlnd 5(3): Bruhn D, Mikkelsen TN, Atkin OK (22) Does the direct effect of tmospheric CO 2 concentrtion on lef respirtion vry with temperture? Responses in two species of plntgo tht differ in reltive growth rte. Physiol Plnt 114(1):57 64 Bunce JA (2) Acclimtion to temperture of the response of photosynthesis to incresed cron dioxide concentrtion in Trxcum officinle. Photosynth Res 64(1):89 94 Bunce JA (25) Response of respirtion of soyen leves grown t nd elevted cron dioxide concentrtions to dy-to-dy vrition in light nd temperture under field conditions. Ann Bot 95(6): Ciis P, Reichstein M, Viovy N, Grnier A, Ogee J, Allrd V et l (25) Europe-wide reduction in primry productivity cused y the het, drought in 23. Nture 437(758): Colemn JS, Rochefort L, Bzzz FA, Woodwrd FI (1991) Atmospheric CO 2, plnt nitrogen sttus nd the susceptiility of plnts to n cute increse in temperture. Plnt Cell Environ 14(7): Crfts-Brndner SJ, Lw RD (2) Effect of het stress on the inhiition nd recovery of the riulose-1, 5-isphosphte croxylse/oxygense ctivtion stte. Plnt 212(1):67 74 Crfts-Brndner SJ nd Slvucci ME (2) Ruisco ctivse constrins the photosynthetic potentil of leves t high temperture nd CO 2. Proc Ntl Acd Sci USA 97(24): Curtis PS (1996) A met-nlysis of lef gs exchnge nd nitrogen in trees grown under elevted cron dioxide. Plnt Cell Environ 19(2): Dvis MB (1986) Climtic instility, time lgs, nd community disequilirium. In: Dimond J, Cse TJ (eds) Community ecology. Hrper & Row, New York, pp Diz S, Grime JP, Hrris J, McPherson E (1993) Evidence of feedck mechnism limiting plnt-response to elevted crondioxide. Nture 364(6438): Eckrdt NA, Portis AR (1997) Het denturtion profiles of riulose- 1, 5-isphosphte croxylse/oxygense (ruisco) nd ruisco ctivse nd the inility of ruisco ctivse to restore ctivity of het-dentured ruisco. Plnt Physiol 113(1): Fri T, Wilkins D, Besford RT, Vz M, Pereir JS, Chves MM (1996) Growth t elevted CO 2 leds to down-regultion of photosynthesis nd ltered response to high temperture in Quercus suer L. seedlings. J Exp Bot 47(34): Fri T, Vz M, Schwnz P, Polle A, Pereir JS, Chves MM (1999) Responses of photosynthetic nd defense systems to high temperture stress in Quercus suer L. seedlings crown under elevted CO 2. Plnt Biol 1(3): Ferris R, Wheeler TR, Hdley P, Ellis RH (1998) Recovery of photosynthesis fter environmentl stress in soyen grown under elevted CO 2. Crop Sci 38(4): Ghnnoum O, Von Cemmerer S, Zisk LH, Conroy JP (2) The growth response of C-4 plnts to rising tmospheric CO 2 prtil pressure: ressessment. Plnt Cell Environ 23(9): Gifford RM (1995) Whole plnt respirtion nd photosynthesis of whet under incresed CO 2 concentrtion nd temperture: longterm versus short-term distinctions for modelling. Glo Chnge Biol 1(6): Gonzelez-Meller MA, Tnev L, Truemn RJ (24) Plnt respirtion nd elevted tmospheric CO 2 concentrtion: cellulr responses nd glol significnce. Ann Bot 94(5):

12 12 Oecologi (212) 169:1 13 Gunderson CA, Wullschleger SD (1994) Photosynthetic cclimtion in trees to rising tmospheric CO 2 roder perspective. Photosynth Res 39(3): Gutschick VP (27) Plnt cclimtion to elevted CO 2 from simple regulrities to iogeogrphic chos. Ecol Model 2(3 4): Hldimnn P, Feller U (24) Inhiition of photosynthesis y high temperture in ok (Quercus puescens L.) leves grown under nturl conditions closely correltes with reversile hetdependent reduction of the ctivtion stte of riulose-1, 5-isphosphte croxylse/oxygense. Plnt Cell Environ 27(9): Hmerlynck EP, McAllister CA, Knpp AK, Hm JM, Owensy CE (1997) Photosynthetic gs exchnge nd wter reltion responses of three tllgrss pririe species to elevted cron dioxide nd moderte drought. Int J Plnt Sci 158(5): Hmerlynck EP, Huxmn TE, Loik ME, Smith SD (2) Effects of extreme high temperture, drought nd elevted CO 2 on photosynthesis of the Mojve Desert evergreen shru, Lrre tridentt. Plnt Ecol 148(2): Heeisen T, Luscher A, Noserger J (1997) Effects of elevted tmospheric CO 2 nd nitrogen fertilistion on yield of Trifolium repens nd Lolium perenne. Act Oecol-Int J Ecol 18(3): Heckthorn SA, Downs CA, Shrkey TD, Colemn JS (1998) The smll, methionine-rich chloroplst het-shock protein protects photosystem ii electron trnsport during het stress. Plnt Physiol 116(1): Heckthorn SA, Ryn SL, Bylis JA, Wng DF, Hmilton EW, Cundiff L et l (22) In vivo evidence from n Agrostis stolonifer selection genotype tht chloroplst smll het-shock proteins cn protect photosystem II during het stress. Funct Plnt Biol 29(8): Hedges LV, Gurevitch J, Curtis PS (1999) The met-nlysis of response rtios in experimentl ecology. Ecology 8(4): Houghton J, Ding Y, Griggs D (21) Climte chnge of 21. The scientific sis. Cmridge University Press, Cmridge Huxmn TE, Hmerlynck EP, Loik ME, Smith SD (1998) Gs exchnge nd chlorophyll fluorescence responses of three southwestern yucc species to elevted CO 2 nd high temperture. Plnt Cell Environ 21(12): Hymus GJ, Bker NR, Long SP (21) Growth in elevted CO 2 cn oth increse nd decrese photochemistry nd photoinhiition of photosynthesis in predictle mnner. Dctylis glomert grown in two levels of nitrogen nutrition. Plnt Physiol 127: IPCC (21) Climte chnge 21: the scientific sis. Contriution of Working Group I to the Third Assessment Report of the Intergovernmentl Pnel on Climte Chnge. Cmridge University Press, Cmridge IPCC (27) Climte chnge 27: the physicl science sis. Contriution of Working Group I to the Fourth Assessment Report of the Intergovernmentl Pnel on Climte Chnge. Cmridge University Press, Cmridge Korner C (1991) Some often overlooked plnt chrcteristics s determinnts of plnt-growth reconsidertion. Funct Ecol 5(2): Korner C (23) Nutrients nd sink ctivity drive plnt CO 2 responses cution with literture-sed nlysis. New Phytol 159(3): Korner C (26) Plnt CO 2 responses: n issue of definition, time nd resource supply. New Phytol 172(3): Ledley PW, Niklus P, KÖrner Ch (1997) Screen-ided CO 2 control (SACC): middle ground etween FACE nd open-top chmers. Act Ecol 18: Long SP (1991) Modifiction of the response of photosynthetic productivity to rising temperture y tmospheric CO 2 concentrtions hs its importnce een underestimted. Plnt Cell Environ 14(8): Long SP, Ainsworth EA, Rogers A, Ort DR (24) Rising tmospheric cron dioxide: plnts fce the future. Annu Rev Plnt Biol 55: Luo Y, Su B, Currie WS, Dukes JS, Finzi A, Hrtwig U et l (24) Progressive nitrogen limittion of ecosystem responses to rising tmospheric cron dioxide. Bioscience 54(8): Moore BD, Cheng SH, Sims D, Seemnn JR (1999) The iochemicl nd moleculr sis for photosynthetic cclimtion to elevted tmospheric CO 2. Plnt Cell Environ 22(6): Morison JIL (1993) Response of plnts to CO 2 under wter limited conditions. Vegettion 14: Morison JIL, Lwlor DW (1999) Interctions etween incresing CO 2 concentrtion nd temperture on plnt growth. Plnt Cell Environ 22(6): Niinemets U (1999) Components of lef dry mss per re - thickness nd density lter lef photosynthetic cpcity in reverse directions in woody plnts. New Phytol 144:35 47 Owensy CE, Coyne PI, Hm JM, Auen LM, Knpp AK (1993) Biomss production in tllgrss pririe ecosystem exposed to nd elevted CO 2. Ecol Appl 3(4): Owensy CE, Hm JM, Knpp AK, Auen LM (1999) Biomss production nd species composition chnge in tllgrss pririe ecosystem fter long-term exposure to elevted tmospheric CO 2. Glo Chnge Biol 5(5): Poorter H, Niinemets Ü, Poorter L et l (29) Cuses nd consequences of vrition in lef mss per re (LMA): met-nlysis. New Phytol 182: Reich PB, Hungte BA, Luo YQ (26) Cron-nitrogen interctions in terrestril ecosystems in response to rising tmospheric cron dioxide. Annu Rev Ecol Evol Syst 37: Roden JS, Bll MC (1996) Growth nd photosynthesis of two euclypt species during high temperture stress under mient nd elevted [CO 2 ]. Glo Chnge Biol 2(2): Roden JS, Bll MC (1996) Growth nd photosynthesis of two euclypt species during high temperture stress under mient nd elevted CO 2. Glo Chnge Biol 2(2): Rosenerg NJ, Adms DC, Gurevitch J (2) MetWin: sttisticl softwre for met-nlysis. Sinuer Assocites, Sunderlnd Rosenerg MS (25) The file-drwer prolem revisited: generl weighted method for clculting fil-sfe numers in metnlysis. Evolution 59: Rosenthl R (1979) The file drwer prolem nd tolernce for null results. Psychol Bull 86: Rustd LE (26) From trnsient to stedy-stte response of ecosystems to tmospheric CO 2 -enrichment nd glol climte chnge: conceptul chllenges nd need for n integrted pproch. Plnt Ecol 182(1 2):43 62 Sge RF, Kuien DS (27) The temperture response of C 3 nd C 4 photosynthesis. Plnt Cell Environ 3(9): Sge RF, Monson RK (1999) C 4 plnt iology. Acdemic Press, Sn Diego Sxe H, Ellsworth DS, Heth J (1998) Tree nd forest functioning in n enriched CO 2 tmosphere. New Phytol 139(3): Tu DR, Seemnn JR, Colemn JS (2) Growth in elevted CO 2 protects photosynthesis ginst high-temperture dmge. Plnt Cell Environ 23(6): Thoms CD, Cmeron A, Green RE (24) Extinction risk from climte chnge. Nture 427(697): vn Oosten JJ, Besford RT (1994) Sugr feeding mimics effect of cclimtion of high CO2. Rpid down regultion of RuBisCO smll suunit trnscripts ut not of the lrge suunit trnscripts. J Plnt Physiol 143:36 312