Soil Biology & Biochemistry

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1 Soil Biology & Biochemistry 41 (2009) Contents lists ville t ScienceDirect Soil Biology & Biochemistry journl homepge: Does ccelerted soil orgnic mtter decomposition in the presence of plnts increse plnt N vilility? Feike A. Dijkstr, *, Nichols E. Bder, Dle W. Johnson, Weixin Cheng Deprtment of Environmentl Studies, University of Cliforni, 1156 High Street, Snt Cruz, CA 95064, USA Deprtment of Nturl Resources nd Environmentl Science, University of Nevd, 1000 Vlley Rod, Reno, NV 89512, USA rticle info strct Article history: Received 23 My 2008 Received in revised form 23 Jnury 2009 Accepted 17 Ferury 2009 Aville online 9 Mrch 2009 Keywords: Net N minerliztion Plnt N cquisition Priming effect Rhizodeposits Soil type Tree species Plnt roots cn increse microil ctivity nd soil orgnic mtter (SOM) decomposition vi rhizosphere priming effects. It is virtully unknown how differences in the priming effect mong plnt species nd soil type ffect N minerliztion nd plnt uptke. In greenhouse experiment, we tested whether priming effects cused y Fremont cottonwood (Populus fremontii) nd Ponderos pine (Pinus ponderos) grown in three different soil types incresed plnt ville N. We mesured primed C s the difference in soil-derived CO 2 -C fluxes etween plnted nd non-plnted tretments. We clculted excess plnt ville N s the difference in plnt ville N (estimted from chnges in soil inorgnic N nd plnt N pools t the strt nd end of the experiment) etween plnted nd non-plnted tretments. Gross N minerliztion t dy 105 ws significntly greter in the presence of plnts cross ll tretments, while microil N mesured t the sme time ws not ffected y plnt presence. Gross N minerliztion ws significntly positively correlted to the rte of priming. Species effects on plnt ville N were not consistent mong soil types. Plnt ville N in one soil type incresed in the P. fremontii tretment ut not in the P. ponderos tretment, wheres in the other two soils, the effects of the two plnt species were reversed. There ws no reltionship etween the cumultive mount of primed C nd excess plnt ville N during the first 107 dys of the experiment when inorgnic N ws still undnt in ll plnted soils. However, during the second hlf of the experiment (dys ) when soil inorgnic N in the plnted tretments ws depleted y plnt N uptke, the cumultive mount of primed C ws significntly positively correlted to excess plnt ville N. Primed C explined 78% of the vriility in plnt ville N for five of the six plnt soil comintions. Excess plnt ville N could not e predicted from cumultive mount of primed C in one species soil type comintion. Possily, greter microil N immoiliztion due to lrge inputs of rhizodeposits with low N concentrtion my hve reduced plnt ville N or we my hve underestimted plnt ville N in this tretment ecuse of N loss through root exudtion nd deth. We conclude tht soil N vilility cnnot e determined y soil properties lone, ut tht is strongly influenced y root soil interctions. Pulished y Elsevier Ltd. 1. Introduction There is incresed recognition tht inputs of lile C sustrtes to the soil cn significntly stimulte soil orgnic mtter decomposition (Dijkstr nd Cheng, 2007; Fontine et l., 2007). Plnt roots re n importnt source of lile C (root exudtes nd other rhizodeposits, Hütsch et l., 2002), nd severl studies hve shown tht when plnts re present, soil orgnic mtter decomposition * Corresponding uthor. USDA-ARS, Rngelnd Resources Reserch Unit, 1701 Centre Ave, Fort Collins, CO 80526, USA. Tel.: ; fx: E-mil ddress: feike.dijkstr@rs.usd.gov (F.A. Dijkstr). cn increse up to 380% compred to soil incutions lcking plnts (Cheng et l., 2003). This stimultion of SOM decomposition cused y inputs of lile C sustrtes hs een referred to s the priming effect (Jenkinson et l., 1985; Kuzykov et l., 2000). Although it hs een rgued tht the priming effect is short-lived nd the respired cron is mostly derived from microil C pools (Dlenerg nd Jger, 1981, 1989; Weintru et l., 2007), recent studies hve shown tht priming effect cn e long-lsting (Dijkstr nd Cheng, 2007) nd cn ffect old C pools deep in the soil (Fontine et l., 2007). Incresed tmospheric CO 2 concentrtions cn led to n incresed priming effect ecuse of enhnced vilility of lile sustrtes (Cheng, 1999; Hooseek et l., 2004; Truemn nd Gonzlez-Meler, 2005). There is n incresed wreness tht the /$ see front mtter Pulished y Elsevier Ltd. doi: /j.soilio

2 F.A. Dijkstr et l. / Soil Biology & Biochemistry 41 (2009) rhizosphere priming effect should e considered s n importnt mechnism ffecting the glol C cycle (Heimnn nd Reichstein, 2008). The rhizosphere priming effect should lso lter N cycling ecuse of the linked nture of C nd N decomposition. It hs een suggested tht the microil decomposer community in the soil utilizes rhizodeposits s C source nd decompose SOM to cquire N(Kuzykov et l., 2000; Pterson, 2003). With priming, more N is then trnsferred from the inctive SOM pool into the ctive microil pool, which eventully could ecome ville for plnt uptke (Hungte, 1999; Jones et l., 2004). Rhizodeposition cn increse the rekdown of N-rich proteins (Weintru et l., 2007), while n increse in microil growth in response to rhizodeposition could further result in incresed N vilility for plnts when these microorgnisms re eing grzed (Clrholm, 1985). Prticulrly in soils where inorgnic N is scrce, N vilility for plnts could increse due to n incresed priming effect (Crdon, 1996). Hermn et l. (2006) reported tht N minerliztion ws up to ten times higher in soil djcent to Aven rt roots thn in ulk soil. Fisher nd Stone (1969) long go noticed incresed vilility of oth N nd P in the root zone of conifers nd hypothesized tht the conifer rhizosphere minerlizes or otherwise extrcts some frction of the soil nitrogen tht hd een resistnt to microil ction under previous vegettion. It hs lso een suggested tht greter plnt N uptke with defolition nd under elevted CO 2 could e result of greter priming effect (Hmilton nd Frnk, 2001; Mrtín-Olmedo et l., 2002; Finzi et l., 2007; Phillips, 2007). The mgnitude of the rhizosphere priming effect on SOM decomposition differs mong plnt species, soil types, nd conditions of nutrient vilility (Cheng et l., 2003; Fontine et l., 2004; Dijkstr et l., 2006; Rsmussen et l., 2007). Priming of SOM ppers to e greter in dicotyledons thn in monocotyledons (Cheng nd Kuzykov, 2005), smller in ndesitic thn in grnitic or sltic soils (Rsmussen et l., 2007), nd cn ecome smller with nutrient ddition (Liljeroth et l., 1990; Crdon, 1996; Fontine et l., 2004), ut not lwys (Cheng et l., 2003). It is virtully unknown how differences in the priming effect mong plnt species nd soil type ffect N minerliztion nd plnt uptke. Erlier we reported priming effect in ll comintions of three different soil types nd two tree species (Fremont cottonwood, Populus fremontii, nd Ponderos pine, Pinus ponderos) in greenhouse study (Dijkstr nd Cheng, 2007). We determined the priming effect y periodiclly mesuring soil respirtion in plnted nd non-plnted control pots nd seprting soil respirtion into plnt- nd soil-derived CO 2 -C using 13 C continuous lelling technique. Soil-derived CO 2 -C incresed up to 225% compred to soil incutions without plnts nd lsted until the end of the experiment (395 dys). The cumultive mount of primed C (i.e., the difference in soil-derived CO 2 -C etween plnted nd nonplnted control tretments) ws lrger under P. ponderos thn under P. fremontii in ll three soil types. There were lso significnt differences mong the three soil types tht could not e relted to totl soil C, ut my hve een result of differences in soil fertility nd minerlogy. Here we report how the three different soil types nd two plnt species ffected plnt N cquisition, microil N pools, gross N minerliztion, nd plnt ville N in this greenhouse experiment. We mesured gross N minerliztion using the 15 N pooldilution method (Kirkhm nd Brtholomew, 1954) nd clculted plnt ville N sed on the difference etween finl nd initil inorgnic N pools in the soil nd the totl plnt iomss N pool. We hypothesized tht gross N minerliztion nd plnt ville N would e greter in the plnted thn in the non-plnted control tretments, nd tht microil N pools would not e ffected y plnt presence. We further hypothesized tht gross nd plnt ville N in excess of the control tretments would increse with greter mount of primed C. 2. Mterils nd methods 2.1. Experiment setup We grew Fremont cottonwood (P. fremontii S. Wts.) nd Ponderos pine (P. ponderos Dougls ex C. Lwson) in greenhouse t the University of Cliforni, Snt Cruz. During plnt growth, the mximum ir temperture inside the greenhouse ws kept elow 27 C with two cooling units (Mitsuishi Electronics, Lwrenceville, GA). Artificil lighting (1100 W lights, P.L. Light Systems, Bemsville, ON) went on whenever the nturl light intensity fell elow 200 W m 2 etween 7 AM nd 6 PM (Argus Control Systems Ltd., White Rock, BC). The CO 2 concentrtion ws kept t 760 ppm y injecting 13 C depleted CO 2 in order to lel the plnts with 13 C (Dijkstr nd Cheng, 2007). We filled 20 PVC pots (dim. 15 cm, height 40 cm) with 5.0 kg soil otined from mixed-conifer forest dominted y P. ponderos t UC Berkeley s Blodgett Forest Reserch Sttion in the Sierr Nevd foothills, CA ( Blodgett soil). We filled 20 pots with 6.8 kg soil otined from n open ok svnn, dominted y invsive nnul grsses t the UC Snt Cruz cmpus grounds ( UCSC grsslnd soil). Both P. fremontii nd P. ponderos grew nery in the djcent UCSC Aroretum. We filled nother 20 pots with 5.8 kg soil otined from P. ponderos grove on costl terrce in West Mrshll field, Snt Cruz, prt of the UCSC cmpus reserve ( Mrshll field soil). Soil properties of the three soil types re listed in Tle 1. Soils were ir-dried nd sieved (4 mm) efore pots were filled. We plnted eight pots of ech soil type with P. fremontii stem cuttings nd eight pots with P. ponderos seedlings tht, ecuse of their slow growth from seed, were previously grown for 10 months in smll continers (dim. 2.5 cm, height 10 cm). The dry weight of the P. fremontii stem cuttings ws on verge less thn 1 g contining less thn 7 mg N. The verge dry root nd shoot weight of 5 seprte P. ponderos seedlings mesured t the time of plnting were nd g respectively, with N contents of 25 1 nd 40 1 mg respectively (nlyzed in the sme wy s other plnt smples, see elow). The remining four pots of ech soil type were used s controls. Pots were wtered dily to 70% field cpcity (no leching occurred during wtering) nd were erted every 6 h for 15 min with n qurium pump (Apollo AM-3, Apollo Enterprises, Ventur, CA) ttched t the ottom of ech pot. In this wy N loss through leching/denitrifiction ws insignificnt (Cheng, 2008), lthough some N loss my hve occurred when we dded 15 N to the pots fter 105 dys of plnting (see elow). We hrvested four pots of ech species of ech soil type fter 107 dys of plnting nd the other hlf fter 398 dys of plnting Smpling nd nlyses We mesured soil respirtion on dys 24, 60, 100, 156, 206, 296, nd 395 fter plnting. Becuse plnts were lelled with 13 C, we Tle 1 Soil properties of the three soil types. Blodgett UCSC grsslnd Mrshll field Soil clss Ultic Hploxerlf Pchic Argixeroll Xeric Argiloll Texture Lom Sndy lom Lom ph Totl C (g kg 1 ) Totl N (g kg 1 ) C:N

3 1082 F.A. Dijkstr et l. / Soil Biology & Biochemistry 41 (2009) were le to seprte plnt-derived (root respirtion nd microil respirtion of rhizodeposits) from soil-derived CO 2 -C y mesuring the 13 C signture in soil respirtion. A detiled description is given y Dijkstr nd Cheng (2007). We clculted primed C s the difference in soil-derived CO 2 -C etween plnted nd non-plnted control tretments. We clculted the cumultive primed C nd the cumultive plnt-derived CO 2 -C y multiplying the verge dily rte of primed C nd plnt-derived CO 2 -C respectively etween two mesuring dtes y the time intervl etween two mesuring dtes, nd y dding the preceding primed C/plntderived CO 2 -C. We mesured gross N minerliztion nd nitrifiction on dy 105 using the pool-dilution method (Kirkhm nd Brtholomew, 1954). To study gross N minerliztion we dded 10.6 mg of 99.4 tom% 15 N s (NH 4 ) 2 SO 4 nd 10.4 mg of unlelled N s KNO 3 to hlf of the pots. In the other hlf of the pots we studied gross nitrifiction y dding 10.4 mg of 98.0 tom% 15 N s KNO 3 nd 10.6 mg of unlelled N s (NH 4 ) 2 SO 4. Even distriution of the N inside the pots ws estlished y dding the N s solution to 110% field cpcity. Excess solution ws pumped from the ottom of the pot into flsk. When the flsk ws full, the flsk ws emptied into the top of the pot. This procedure ws repeted twice for ech pot to ensure dequte dispersion of the 15 N lel. Excess solution ws drwn into the flsk third time to ensure tht the soil ws not ove field cpcity, nd the contents of the flsk were removed. Soil smples to 20 cm soil depth were tken from ech pot directly fter lelling nd gin fter 48 h (one 2.5 cm dimeter soil core per pot ech time to minimize root dmge in the pot). After removing roots nd recognizle plnt mteril the soil smples were homogenized. A 50 ml solution of 2 M KCl ws dded to 10 g susmple, shken for 1 h, nd filtered through pre-leched filter disks (Whtmn #1). The KCl extrcts were nlyzed for NH 4 nd NO 3 on flow injection nlyzer (Lcht QuikChem 8000, Milwukee, WI). For the pots lelled with 15 N s (NH 4 ) 2 SO 4, the NH 4 in the KCl extrcts ws collected using cidified filter-pper disks inside PTFE diffusion trps (Strk nd Hrt, 1996). For the pots lelled with 15 N s KNO 3,NH 4 ws first removed y dding MgO nd letting the smples sit for 5 dys. Then, Devrd s Alloy ws dded to convert the NO 3 into NH 4, which ws collected s ove. The filter disks were nlyzed for totl N nd d 15 N on Hydr continuous flow isotope mss spectrometer (PDZ Europ, Cheshire, UK). Gross N minerliztion nd nitrifiction were clculted using the equtions in Kirkhm nd Brtholomew (1954). For the plnted tretments we clculted excess gross N minerliztion y sutrcting the verge gross N minerliztion in the control tretment of ech soil type from the gross N minerliztion in the plnted tretment with tht soil type. We mesured microil N in the soils collected directly fter the 15 N lelling (105 dys fter plnting) using the chloroform fumigtion extrction method (Brookes et l., 1985). A 20 g susmple ws immeditely dded to 50 ml of 0.5 M K 2 SO 4, while nother 20 g susmple ws fumigted with chloroform for 48 h nd then dded to 50 ml of 0.5 M K 2 SO 4. Smples were shken for 1 h nd filtered through pre-leched filter disks (Whtmn #1). The orgnic N in the solution ws then oxidized to NO 3 in n utoclve using persulfte digestion (Crer nd Bere, 1993), nd the inorgnic N ws mesured on flow injection nlyzer. Microil iomss N ws clculted s the difference etween NO 3 concentrtions in the fumigted nd non-fumigted extrcts, divided y the conversion fctor 0.54 (Brookes et l., 1985). After hrvesting we seprted plnt iomss into shoot nd root iomss nd took soil smple from ech pot. We dried (65 C), weighed nd ground plnt iomss from oth hrvests nd dried nd ground susmple of the soil fter the finl hrvest. Ground soil nd plnt smples were nlyzed for totl C nd N, nd d 13 Con Hydr continuous flow isotope mss spectrometer (PDZ Europ, Cheshire, UK). After oth hrvests, we extrcted fresh soil susmple with 2 M KCl s ove nd nlyzed the extrcts for NH 4 nd NO 3 on flow injection nlyzer (Lcht QuikChem 8000, Milwukee, WI). We lso extrcted five pre-tretment soil smples of ech soil type with 2 M KCl nd nlyzed the extrcts for NH 4 nd NO 3. We clculted the mount of new root-derived soil orgnic cron (root-derived SOC, C new ) tht ws formed during the experiment with: C new ¼ C end ðd 13 C strt d 13 C end Þ=ðd 13 C strt d 13 C root Þ (1) where C end is the totl mount of SOC t the end of the experiment, nd d 13 C strt, d 13 C end, nd d 13 C root re the d 13 C vlues of SOC t the strt nd end of the experiment nd of root iomss, respectively. We clculted net plnt N cquisition (N cq, mg N pot 1 )y sutrcting totl N content of the cuttings nd seedlings t the time of plnting from the totl N content of the plnt t hrvest. We clculted plnt ville N (N pl,mgnkg 1 soil d 1 ) seprtely for the first period (dys 0 107) nd second period (dys ) s follows: h i N pl ¼ N cq =Soil wt InorgNsoil finl InorgNsoil initil =Dtime where Soil wt is the soil dry weight of the pot (kg pot 1 ), InorgNsoil finl is the sum of extrctle NH 4 nd NO 3 t the time of hrvesting (t dys 107 nd 398 for the first nd second period respectively, mg N kg 1 soil), InorgNsoil initil is the sum of extrctle NH 4 nd NO 3 t the strt of ech period (from pretretment soil smples nd t dy 107 for the first nd second period respectively, mg kg 1 soil), nd Dtime is the time intervl of ech period (107 nd 291 dys for the first nd second period respectively). Some of the N in N cq my hve een tken up in orgnic form (P. ponderos in prticulr ecuse of its ssocition with ectomycorrhize). Thus, plnt ville N is the sum of net N minerliztion nd orgnic N uptke. As mentioned ove, N loss through leching/denitrifiction ws insignificnt. Becuse we dded totl of 21 mg N to ech of the pots on dy 105 (just efore the first hrvest) we included 21 mg N to InorgNsoil initil for clculting N min during the first period. When we discrded excess solution pumped from the ottom of the pots fter the N ws dded we my lso hve removed some of the N tht ws in the pots. Therefore, the plnt ville N clculted for the first period my hve een slightly underestimted (we did not mesure the inorgnic N concentrtion in the excess solution). For the plnted tretments we clculted excess plnt ville N y sutrcting the verge totl mount of plnt ville N (mg N kg 1 soil) in the control tretment of ech soil type from the totl mount of plnt ville N in the plnted tretment with tht soil type. We used nlysis of vrince (ANOVA) to test for min effects of soil type (Blodgett, UCSC grsslnd, Mrshll field) nd plnt tretment (control, P. fremontii, nd P. ponderos) nd for soil type plnt tretment interctions on plnt iomss, new rootderived SOC, net plnt N cquisition, inorgnic N pools in the soil, gross N minerliztion, nitrifiction, microil N, nd plnt ville N. We used post-hoc tests (Tukey s test) for ech soil type to test for differences in gross N minerliztion, microil N, nd plnt ville N mong the two tree species nd the control pots. We used liner nd non-liner regressions to relte excess gross N minerliztion to primed C t dy 100 nd excess plnt ville N to cumultive primed C nd cumultive plnt-derived CO 2 -C. We used the softwre pckge JMP for ll our sttisticl nlyses. (2)

4 F.A. Dijkstr et l. / Soil Biology & Biochemistry 41 (2009) Results Across soil types, P. ponderos hd significntly lrger root iomss thn P. fremontii t oth hrvests, ut significntly lrger shoot iomss only t the first hrvest (Tle 2). Becuse we strted with 10-month-old P. ponderos seedlings tht were igger in size thn the P. fremontii cuttings, this hed strt my hve contriuted to greter root iomss for P. ponderos t oth hrvests nd greter shoot iomss t the first hrvest. However, we expected P. fremontii in generl to e fster growing species thn P. ponderos, which ws corroorted y similr or slightly higher shoot iomss for P. fremontii thn for P. ponderos y the end of the second hrvest. There were significnt soil type effects on shoot nd root iomss nd sometimes significnt soil type plnt species interctions. These effects were not consistent for the two hrvests, e.g., shoot iomss ws highest in the UCSC grsslnd soil during the first hrvest, ut highest in the Blodgett soil during the second hrvest. Root iomss showed lrge increses etween the first nd second hrvest, except for P. fremontii in the Blodgett nd Mrshll field soils. New root-derived SOC t the second hrvest ws on verge significntly higher in soils with P. ponderos thn in soils with P. fremontii. As with plnt iomss, new root-derived SOC my hve een higher in soils with P. ponderos thn with P. fremontii ecuse we strted the experiment with 10-month-old seedlings. However, the root iomss of the 10-month-old P. ponderos seedlings we strted with ws on verge only 2.1 g or less thn 8% of the root iomss y the end of the experiment. The Blodgett soil with P. ponderos plnts hd the highest new root-derived SOC of ll soil type nd plnt species comintions. Across soil types, net plnt N cquisition in roots ws significntly lrger for P. ponderos thn for P. fremontii fter oth hrvests (Tle 3). On the other hnd, net N cquisition in shoots ws significntly higher for P. fremontii thn for P. ponderos cross soil types fter the first hrvest nd lmost 100% higher in the Blodgett soil fter the second hrvest. Totl net plnt N cquisition ws on verge not significntly different etween P. fremontii nd P. ponderos during the first hrvest, nd ws on verge significntly higher for P. ponderos thn for P. fremontii during the second hrvest. Net plnt N cquisition showed significnt soil type plnt species interctions. Notly, during the second hrvest P. ponderos hd higher totl net plnt N cquisition in the UCSC grsslnd nd Mrshll field soil, ut lower totl net plnt N cquisition in the Blodgett soil thn P. fremontii, despite the fct tht the priming effect ws lrgest in the Blodgett soil with P. ponderos mong ll soil type nd plnt species comintions (Dijkstr nd Cheng, 2007). The UCSC grsslnd soil hd the highest initil (pre-tretment) NO 3 nd the lowest NH 4 content (Tle 4). The NO 3 nd totl inorgnic N content in the control pots incresed over time ecuse of net N minerliztion nd nitrifiction. In the plnted pots NH 4 nd NO 3 decresed over time, indicting tht the plnts took up the inorgnic N tht ws minerlized s well s the inorgnic N tht ws lredy ville t the strt of the experiment. After the second hrvest reltively little NH 4 nd NO 3 were left in the plnted pots, except for P. fremontii in the Mrshll field soil, which hd the highest NO 3 concentrtion. This soil plnt comintion lso hd the lowest new root-derived SOC (Tle 2). Gross N minerliztion mesured on dy 105 ws not significntly ffected y soil type, ut ws significntly ffected y plnt tretment (Fig. 1A). All plnted pots showed on verge higher gross N minerliztion rtes thn the control pots, lthough only P. ponderos in the Blodgett nd UCSC grsslnd soil hd significntly higher gross N minerliztion rtes thn their controls. Notly, the Blodgett soil with P. ponderos tht showed the lrgest priming effect lso hd the gretest gross N minerliztion rte t dy 105. We oserved no significnt tretment effects on gross nitrifiction (dt not shown). The microil N pool mesured on dy 105 ws significntly greter in the Mrshll field soil thn in the other two soil types (Fig. 1B). In contrst to the gross N minerliztion rte, microil N ws not significntly ffected y the plnt tretment. Plnt ville N clculted ccording to eqution (2) ws similr in the plnted nd the control pots during the first 107 dys (Fig. 2), except for P. ponderos in the Mrshll field soil, which showed lower plnt ville N thn the control. During the lst 291 dys plnt ville N ws significntly higher for P. fremontii in the Blodgett soil nd significntly higher for P. ponderos in the UCSC grsslnd nd Mrshll field soils thn in the control pots. In generl, plnt ville N ws lower during the lst 291 dys thn during the first 107 dys. When we relted the excess gross N minerliztion (gross N minerliztion in plnted pots minus verge gross N minerliztion in control pots) mesured on dy 105 to the rte of primed C mesured on dy 100 we oserved wek ut significnt positive liner reltionship (Fig. 3A). A similr reltionship ws found etween gross N minerliztion on dy 105 nd soil-derived CO 2 -C mesured on dy 100 (P ¼ 0.05, R 2 ¼ 0.21). As cn e inferred from Fig. 2, excess plnt ville N ws not lwys positive. During the first period we oserved no significnt reltionship etween excess plnt ville N nd the cumultive primed C (P ¼ 0.92, R 2 ¼ , dt not shown). During the second period the reltionship ws mrginlly significnt (P ¼ 0.08, R 2 ¼ 0.17 for Tle 2 Averge plnt iomss (1 SE) t the first nd second hrvest nd new root-derived SOC t the second hrvest. Soil type Plnt species First hrvest Second hrvest New root-derived SOC (g C pot 1 ) Biomss (g pot 1 ) Biomss (g pot 1 ) Roots Shoots Totl Roots Shoots Totl Blodgett P. fremontii P. ponderos UCSC grsslnd P. fremontii P. ponderos Mrshll field P. fremontii P. ponderos ANOVA P-vlues Soil type Plnt species < < < Soil type plnt species

5 1084 F.A. Dijkstr et l. / Soil Biology & Biochemistry 41 (2009) Tle 3 Averge net plnt N cquisition in plnt iomss (1 SE) t the first nd second hrvest (plnt N content t hrvest minus initil plnt N content when plnted). Soil type Plnt species First hrvest Second hrvest Root N Shoot N Totl N Root N Shoot N Totl N Blodgett P. fremontii P. ponderos UCSC grsslnd P. fremontii P. ponderos Mrshll field P. fremontii P. ponderos ANOVA P-vlues Soil type Plnt species < < Soil type Plnt species cumultive primed C). However, when we excluded the Blodgett soil with P. ponderos tht showed mong the highest cumultive mounts of primed C ut tht hd negtive excess plnt ville N, then the reltionship ecme highly significnt, nd the reltionship incresed exponentilly (Fig. 3B). 4. Discussion During the first 107 dys of the experiment the presence of plnts resulted in incresed SOC decomposition nd gross N minerliztion, ut did not ffect plnt ville N nd microil N pools. These results suggest tht the priming effect during the first 107 dys incresed microil N turnover, ut not N vilility for plnts. Becuse roots did not fully occupy the pots efore the first hrvest, the plnts my hve competed less for N with microes during this period. Inorgnic N ws still reltively high during this period, so tht plnt N demnd my not hve een limited y microil N minerliztion during this period. The reltively high soil inorgnic N during the first period of the experiment my lso hve reduced the priming effect (Liljeroth et l., 1990; Crdon, 1996). The mount of primed C during the first period ws on verge 0.3 g C kg 1 soil or 13% of the mount of primed C during the whole experiment (Dijkstr nd Cheng, 2007). During the second prt of the experiment (dys ) the presence of plnts incresed plnt ville N in only three of the six soil type nd plnt species comintions. However, these differences in plnt ville N cn in lrge prt e explined y the differences in the cumultive mount of primed C mong the six plnt soil comintions. With the exception of the Blodgett soil with P. ponderos plnts, there ws significnt positive reltionship etween excess plnt ville N nd the cumultive mount of primed C during the second period. The plnt soil comintions of P. ponderos in the UCSC grsslnd nd Mrshll field soils lrgely drove the reltionship etween excess plnt ville N nd the cumultive mount of primed C, which hd lso mong the lrgest priming effects. However, the cumultive mount of primed C explined 78% of the vriility in plnt ville N when five of the six plnt soil comintions were included in the regression. Incresed net N minerliztion hs een inferred from priming effect in other studies (Hmilton nd Frnk, 2001; Mrtín-Olmedo et l., 2002). Here we show tht the increse in plnt ville N (including gross nd net N minerliztion) in the presence of plnt cn e directly linked to the mgnitude of the priming effect in terms of C minerliztion. The excess plnt ville N in the Blodgett soil with P. ponderos plnts ws much lower thn predicted from the reltionship with cumultive primed C. The Blodgett soil hd over three times more lile C nd C:N rtio more thn doule tht of the UCSC grsslnd nd Mrshll field soils (Tle 1, Dijkstr nd Cheng, 2007), which could hve kept microil N immoiliztion high nd net N minerliztion low. However, despite much lower mount of cumultive primed C (Dijkstr nd Cheng, 2007, Fig. 3B) nd potentil lg in growth ecuse we strted with cuttings rther thn 10-month-old seedlings, plnt ville N in the Blodgett soil plnted with P. fremontii ws significntly higher thn in the nonplnted control tretment. This suggests tht the low plnt ville N in the Blodgett soil with P. ponderos ws not solely due to soil chrcteristics. Tle 4 Averge soil inorgnic N efore plnting (pre-tretment) nd t the first nd second hrvest (1 SE). Soil type Plnt tretment Pre-tretment First hrvest Second hrvest NH 4 NO 3 Totl NH 4 NO 3 Totl NH 4 NO 3 Totl Blodgett Control P. fremontii P. ponderos UCSC grsslnd Control P. fremontii P. ponderos Mrshll field Control P. fremontii P. ponderos ANOVA P-vlues Soil type < Plnt tretment 0.04 < < < < Soil type plnt tretment

6 F.A. Dijkstr et l. / Soil Biology & Biochemistry 41 (2009) Gross N minerliztion (mg kg -1 d -1 ) A ANOVA: Soil type: 0.33 Plnt tr.: 0.02 Soil * Plnt tr.: 0.15 Microil N (mg pot -1 ) B ANOVA: Soil type: < Plnt tr.: 0.44 Soil * Plnt tr.: 0.32 Control P. fremontii P. ponderos 0.0 Blodgett UCSC grsslnd Mrshll field 0 Blodgett UCSC grsslnd Mrshll field Fig. 1. Gross N minerliztion (A) nd microil N (B) verged y soil type nd tree species mesured 105 dys fter trnsplnting. Different letters for ech soil type within ech period denote differences mong tree species nd control tretments (post-hoc Tukey s test, P < 0.05). One potentil explntion for the reltively low plnt ville N in the Blodgett soil with P. ponderos is tht decomposition of rhizodeposits my hve stimulted microil N immoiliztion. Rhizodeposits tend to hve lower N content thn older ntive SOM (Hungte, 1999). The Blodgett soil with P. ponderos hd the highest new root-derived SOC t the end of the experiment (two to three times higher thn in the other tretments). The presence of new root-derived SOC t the end of the experiment indictes tht these rhizodeposits resisted decomposition until the termintion of the experiment, lthough they lso my hve een incorported into microil iomss. Decomposition of N-poor rhizodeposits my hve incresed microil N immoiliztion. Thus, in the Blodgett soil with P. ponderos, incresed microil N immoiliztion ecuse of incresed decomposition of new root-derived SOM my hve offset the positive effects of priming on net N minerliztion. Another potentil explntion for the low plnt ville N in the Blodgett soil with P. ponderos my e tht we underestimted plnt ville N in the plnted tretments. Nitrogen tht ws minerlized, tken up y the plnt nd susequently lost y the plnt through root exudtion, ectomycorrhizl turnover, nd root deth during the experiment ws not included in the clcultion. The sustntil mounts of root-derived SOC in ll plnted tretments y the end of the experiment (Tle 2) indicte tht root exudtion nd deth were sustntil during the experiment, which most likely lso resulted in plnt N loss. Others hve suggested tht plnts cn lose sustntil mount of N through rhizodeposition (De Grff et l., 2007; Wichern et l., 2008). As mentioned ove, the root-derived SOC ws lrgest for the Blodgett soil with P. ponderos plnts, suggesting tht rpid root nd mycorrhizl turnover my hve led us to underestimte plnt ville N for this tretment. The exponentil increse in excess plnt ville N with incresed cumultive primed C during the second period indictes tht more excess N ws moilized per unit of primed C t greter rtes of priming. Also, the priming effect on SOM decomposition incresed t the end of the experiment (Dijkstr nd Cheng, 2007) t time when inorgnic N content in the soil ws low (Tle 4). Roots fully occupied the pots y this time nd my hve competed for N with microes more effectively during the second period. Thus, the priming effect on SOM decomposition my relese more N from soil pools for plnt N uptke t time when the inorgnic N content in the soil is low, nd when plnt N demnd is high. This is in ccordnce with the conceptul model proposed y Crdon (1996) nd Hungte (1999) who suggested tht when soil nutrients re scrce, microes use rhizodeposits to rekdown soil orgnic mtter therey moving nutrients to the ctive microil pool, where eventully these nutrients should ecome ville for plnts. Others hve suggested tht the nutrient sttus of the soil is n importnt fctor controlling the priming effect (Liljeroth et l., 1990; Fontine et l., 2004) nd rtes of N minerliztion nd immoiliztion (Chpin et l., 2002; Phillips nd Fhey, 2008). Our results suggest tht the increse in SOM decomposition cused y rhizosphere priming effects cn sometimes increse N minerliztion nd plnt N uptke. However, the reltionship etween priming nd plnt ville N ws not strightforwrd, nd my lso depend on the lnce etween rhizodeposits used for SOM decomposition nd rhizodeposits used for microil growth. On the one hnd, rhizodeposits could stimulte N-rich SOM decomposition nd enhnce net N minerliztion while on the Plnt ville N (mg kg -1 d -1 ) A ANOVA: Soil type: < Plnt tr.: 0.20 Soil * Plnt tr.: 0.37 B Control P. fremontii P. ponderos ANOVA: Soil type: 0.36 Plnt tr.: Soil * Plnt tr.: Blodgett UCSC grsslnd Mrshll field Blodgett UCSC grsslnd Mrshll field Fig. 2. Plnt ville N verged y soil type nd tree species during the first (A) nd second period (B). Different letters for ech soil type within ech period denote differences mong tree species nd control tretments (post-hoc Tukey s test, P < 0.05).

7 1086 F.A. Dijkstr et l. / Soil Biology & Biochemistry 41 (2009) Gross N minerliztion in excess of control (mg N kg -1 d -1 ) A R 2 = 0.31 P = Primed CO 2 -C (mg C kg -1 d -1 ) Plnt ville N in excess of control (mg kg -1 ) B Blodgett, P. fremontii Blodgett, P. ponderos UCSC grsslnd, P. fremontii UCSC grsslnd, P. ponderos Mrshll field, P fremontii Mrshll field, P. ponderos R 2 = 0.78 P < Cumultive primed CO 2 -C (mg kg -1 ) Fig. 3. Excess gross N minerliztion s function of primed C 105 dys fter trnsplnting (A) nd excess plnt ville N s function of cumultive primed C during the second period (B) for ech soil type nd tree species. Best-fit line in (B) excludes the P. ponderos Blodgett soil pots (see Discussion). other hnd decomposition of N-poor rhizodeposits could enhnce microil N immoiliztion (similr to the concept tht priming effects on SOM decomposition depend on the stimultion of slow growing K-strtegist microorgnisms vs. fst growing r-strtegist microorgnisms, Fontine et l., 2003). Becuse we did our experiment under elevted CO 2 conditions (roughly twice mient CO 2 concentrtion), rhizosphere priming effects my hve een lrger thn under mient CO 2 concentrtion (Cheng, 1999), nd the effects of priming on N cycling my lso hve een different. Nevertheless, our results suggest tht soil N vilility nd soil fertility re reltive terms, nd tht N vilility cnnot e determined y soil properties lone, ut is strongly influenced y root soil interctions. Acknowledgements This reserch ws supported y the Ntionl Reserch Inititive of USDA Coopertive Stte Reserch, Eduction nd Extension Service (Grnt no ) nd y reserch grnt from the Kerney Foundtion of Soil Science. We thnk Reginldo Gomez nd Pul Trn for their ssistnce with wtering plnts nd lortory work, Dvid Hrris for isotope nlyses, nd two nonymous reviewers for criticl reviews of previous version of the mnuscript. References Brookes, P.C., Lndmn, A., Pruden, G., Jenkinson, D.S., Chloroform fumigtion nd the relese of soil nitrogen: rpid direct extrction method to mesure microil iomss nitrogen in soil. Soil Biology & Biochemistry 17, Crer, M.L., Bere, M.H., Alkline persulfte oxidtion for determining totl nitrogen in microil iomss extrcts. Soil Science Society of Americ Journl 57, Crdon, Z.G., Influence of rhizodeposition under elevted CO 2 on plnt nutrition nd soil orgnic mtter. Plnt nd Soil 187, Chpin III, F.S., Mtson, P.A., Mooney, H.A., Principles of Terrestril Ecosystem Ecology. Springer, New York, 436 pp. Cheng, W., Rhizosphere feedcks in elevted CO 2. Tree Physiology 19, Cheng, W., Kuzykov, Y., Root effects on soil orgnic mtter decomposition. In: Zoel, R.W., Wright, S.F. (Eds.), Roots nd Soil Mngement: Interctions etween Roots nd the Soil. ASA-SSSA, Mdison, Wisconsin, pp Cheng, W.X., Johnson, D.W., Fu, S.L., Rhizosphere effects on decomposition: controls of plnt species, phenology, nd fertiliztion. Soil Science Society of Americ Journl 67, Cheng, W., Rhizosphere priming effects: its functionl reltionships with microil turnover, evpotrnspirtion, nd C N udgets. Soil Biology & Biochemistry, in press, doi: /j.soilio Clrholm, M., Interctions of cteri, protozo nd plnts leding to minerliztion of soil nitrogen. Soil Biology & Biochemistry 17, Dlenerg, J.W., Jger, G., Priming effect of smll glucose dditions to 14 C- lelled soil. Soil Biology & Biochemistry 13, Dlenerg, J.W., Jger, G., Priming effect of some orgnic dditions to 14 C- lelled soil. Soil Biology & Biochemistry 21, De Grff, M.A., Six, J., Vn Kessel, C., Elevted CO 2 increses nitrogen rhizodeposition nd microil immoiliztion of root-derived nitrogen. New Phytologist 173, Dijkstr, F.A., Cheng, W., Interctions etween soil nd tree roots ccelerte long-term soil cron decomposition. Ecology Letters 10, Dijkstr, F.A., Cheng, W., Johnson, D.W., Plnt iomss influences rhizosphere priming effects on soil orgnic mtter decomposition in two differently mnged soils. Soil Biology & Biochemistry 38, Finzi, A.C., Nory, R.J., Clfpietr, C., Gllet-Budynek, A., Gielen, B., Holmes, W.E., Hooseek, M.R., Iversen, C.M., Jckson, R.B., Kuiske, M.E., Ledford, J., Lierloo, M., Oren, R., Polle, A., Pritchrd, S., Zk, D.R., Schlesinger, W.H., Ceulemns, R., Increses in nitrogen uptke rther thn nitrogen-use efficiency support higher rtes of temperte forest productivity under elevted CO 2. Proceedings of the Ntionl Acdemy of Sciences of the United Sttes of Americ 104, Fisher, R.F., Stone, E.L., Incresed vilility of nitrogen nd phosphorus in the root zone of conifers. Soil Science Society of Americ Journl 33, Fontine, S., Mriotti, A., Adie, L., The priming effect of orgnic mtter: question of microil competition? Soil Biology & Biochemistry 35, Fontine, S., Brdoux, G., Adie, L., Mriotti, A., Cron input to soil my decrese soil cron content. Ecology Letters 7, Fontine, S., Brot, S., Brré, P., Bdioui, N., Mry, B., Rumpel, C., Stility of orgnic cron in deep soil lyers controlled y fresh cron supply. Nture 450, Hmilton, E.W., Frnk, D.A., Cn plnts stimulte soil microes nd their own nutrient supply? Evidence from grzing tolernt grss. Ecology 82, Heimnn, M., Reichstein, M., Terrestril ecosystem cron dynmics nd climte feedcks. Nture 451, Hermn, D.J., Johnson, K.K., Jeger III, C.H., Schwrtz, E., Firestone, M.K., Root influence on nitrogen minerliztion nd nitrifiction in Aven rt rhizosphere soil. Soil Science Society of Americ Journl 70, Hooseek, M.R., Lukc, M., vn Dm, D., Godold, D.L., Velthorst, E.J., Biondi, F.A., Peressotti, A., Cotrufo, M.F., de Angelis, P., Scrsci-Mugnozz, G., More new cron in the minerl soil of poplr plnttion under Free Air Cron Enrichment (POPFACE): cuse of incresed priming effect? Glol Biogeochemicl Cycles 18, in press, /2003GB Hungte, B.A., Ecosystem responses to rising tmospheric CO 2 : feedcks through the nitrogen cycle. In: Luo, Y., Mooney, H.A. (Eds.), Cron Dioxide nd Environmentl Stress. Acdemic Press, Sn Diego, pp Hütsch, B.W., Augustin, J., Merch, W., Plnt rhizodeposition n importnt source for cron turnover in soils. Journl of Plnt Nutrition nd Soil Science 165, Jenkinson, D.S., Fox, R.H., Ryner, J.H., Interctions etween fertilizer nitrogen nd soil nitrogen the so-clled priming effect. Journl of Soil Science 36, Jones, D.L., Hodge, A., Kuzykov, Y., Plnt nd mycorrhizl regultion of rhizodeposition. New Phytologist 163, Kirkhm, D., Brtholomew, W.V., Equtions for following nutrient trnsformtions in soil, utilizing trcer dt. Soil Science Society of Americ Proceedings 18, Kuzykov, Y., Friedel, J.K., Sthr, K., Review of mechnisms nd quntifiction of priming effects. Soil Biology & Biochemistry 32, Liljeroth, E., vn Veen, J.A., Miller, H.J., Assimilte trnsloction to the rhizosphere of two whet lines nd susequent utiliztion y rhizosphere microorgnisms t two soil nitrogen concentrtions. Soil Biology & Biochemistry 22, Mrtín-Olmedo, P., Rees, R.M., Grce, J., The influence of plnts grown under elevted CO 2 nd N fertiliztion on soil nitrogen dynmics. Glol Chnge Biology 8, Pterson, E., Importnce of rhizodeposition in the coupling of plnt nd microil productivity. Europen Journl of Soil Science 54,

8 F.A. Dijkstr et l. / Soil Biology & Biochemistry 41 (2009) Phillips, R.P., Towrds rhizo-centric view of plnt microil feedcks under elevted tmospheric CO 2. New Phytologist 173, Phillips, R.P., Fhey, T.J., The influence of soil fertility on rhizosphere effects in northern hrdwood forest soils. Soil Science Society of Americ Journl 72, Rsmussen, C., Southrd, R.J., Horwth, W.R., Soil minerlogy ffects conifer forest soil cron source utiliztion nd microil priming. Soil Science Society of Americ Journl 71, Strk, J.M., Hrt, S.C., Diffusion technique for prepring slt solutions, Kjeldhl digests, nd persulfte digests for nitrogen-15 nlysis. Soil Science Society of Americ Journl 60, Truemn, R.J., Gonzlez-Meler, M.A., Accelerted elowground C cycling in mnged griforest ecosystem exposed to elevted cron dioxide concentrtions. Glol Chnge Biology 11, Weintru, M., Scott-Denton, L., Schmidt, S., Monson, R., The effects of tree rhizodeposition on soil exoenzyme ctivity, dissolved orgnic cron, nd nutrient vilility in sulpine forest ecosystem. Oecologi 154, 327. Wichern, F., Eerhrdt, E., Myer, J., Joergensen, R.G., Müller, T., Nitrogen rhizodeposition in griculturl crops: methods, estimtes nd future prospects. Soil Biology & Biochemistry 40,

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