RESOURCE PARTITIONING OF SOIL ORGANIC PHOSPHORUS: INVESTIGATIONS FROM A TROPICAL MOUNTAIN FOREST BRIAN S. STEIDINGER THESIS

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1 RESOURCE PARTITIONING OF SOIL ORGANIC PHOSPHORUS: INVESTIGATIONS FROM A TROPICAL MOUNTAIN FOREST BY BRIAN S. STEIDINGER THESIS Sumitted in prtil fulfillment of the requirements for the degree of Mster of Siene in Biology in the Grdute College of the University of Illinois t Urn-Chmpign, 211 Urn, Illinois Advisor: Professor Jmes W. Dlling

2 Astrt One of the mjor limittions of resoure-nihe theory to explin plnt speies diversity nd distriution is the puity of reognized resoures. Reent investigtions in grsslnd nd tundr eosystems indite tht plnt speies n speilize to exploit different forms of soil nitrogen. I hypothesized tht similr phenomen ours in the tropis with soil phosphorus (P). I grew seedlings of rusulr myorrhizl (AM) Mollinedi drensi nd Podorpus olieofolius, etomyorrhizl (EM) Oreomunni mexin, nd nonmyorrhizl (NM) Roupl montn tree speies in hydroponi growth medium ontining exlusively either inorgni, monoester, diester, inositol-p, or no-p ontrol. In ddition, I ssyed the prodution of P-mono nd diesterse enzymes tivity of eh speies to determine their pity to reminerlize P from orgni soures. My results support the potentil for resoure prtitioning to promote oexistene etween myorrhizl nd nonmyorrhizl speies. The myorrhizl tree speies exhiited similr growth, nutritionl, nd llotionl responses ross tretments, with growth nd totl P ontent high in inorgni-p nd monoester-p nd low in the inositol nd diester-p tretments. When limited to inositol P, R. montn (NM) exhiited high growth, signifintly greter totl nd speifi lef re, nd signifintly greter P use effiieny when ompred to the other experimentl tretments. R. montn (NM) lso hd 3 fold greter totl P in the inositol P tretment thn in the no-p ontrol (p=.64), nd hd signifintly greter P-mono nd diesterse tivity thn oth AM nd EM speies. Together these results indite tht the potentil exists for prtitioning of soil P etween myorrhizl nd NM plnts, ut not etween AM nd EM plnts. ii

3 Aknowledgements I would like to thnk Jim Dlling nd Ben Turner for the intelletul, institutionl nd finnil ssistne without whih this projet would not hve een possile. Crlos Espinoz, Alerto Gonzles, nd Arturro Morris provided invlule ssistne in olleting nd identifying plnts, onstruting the grow house, nd mintining the experiment t the Fortun Field Sttion. Clire Bldek provided vlule editing for oth this thesis work, presenttions sed off of it, nd grnt nd fellowship pplitions to support its ompletion. Mike O Mr ssisted in the hrvest, trnsporttion, nd weighing of plnt mteril. MKenn Kelly helped ollet seedlings from the field nd trnsfer them to hydroponi growth medium, edited every srp of text nd presenttion, nd kept me sne throughout this msters degree. Finnilly, I m indeted to the Smithsonin Tropil Reserh Institute, Clrk, Tinker nd Msters Reserh Support Grnts, nd the Govindjee nd Rjni Awrd for Exellene in Biologil Siene. iii

4 Tle of Contents Introdution..1 Methods 6 Results 11 Disussion..14 Tles nd Figures. 18 Referenes..32 iv

5 Introdution The prtitioning of limiting resoures promotes speies oexistene y reduing inter-speies ompetition (Huthinson 1959, Tilmn 1982). In lssi exmple, different speies of Glpgos ground finh (Geospiz spp.) oupying the sme islnd hve evolved ek morphologies to feed on seeds of different sizes, reduing interspeies ompetition for food (Grnt 1986). While numerous other se studies orroorte the suess of resoure prtitioning in niml ommunities (Shoener 1974, Pyke 1982, Grnt nd Grnt 26), there is less evidene to suggest its importne in plnt ommunities (Connell 1978, Huston 1979). This is reflets oth the diffiulty of resolving the mehnisms of elow ground ompetition (Csper nd Jkson 1997, Silvertown et l. 1999), nd the puity of defined resoures limiting plnt produtivity ross the gloe (sometimes referred to s the prdox of diversity ). While the ompetitive exlusion priniple predits tht the numer of speies nnot exeed the numer of limiting resoures (Stewrt nd Levin 1973, Armstrong nd MGhee 1983), there re pproximtely 3, terrestril plnt speies, nd only 2 reognized resoures (inluding light, wter, nd minerl nutrients) (Hrrison 1987). Further, glol nlyses revel tht most terrestril plnt produtivity is limited y either soil nitrogen (N), phosphorus (P), or o-limited y oth (Aerts nd Chpin 2, Elser et l. 27). Resolving the prdox of plnt speies diversity involves redefining soil N nd P s omposite resoures, present in host of different hemil ompounds. If plnt speies differ in their ility to exploit different hemil forms of limiting soil resoure, then the potentil exists for resoure prtitioning to promote plnt speies oexistene. In ft, severl studies suggest tht oexisting plnts speies re dpted to quire N from different hemil soures. In lndmrk study, MKne et l. (22) exposed plnt speies from N-limited rti tundr to 15 N-lelled mmonium, nitrte, or glyine ( simple mino id). They oserved mrked differenes in whih form of N different speies exploit. Further, they found tht dominnt plnt speies exploit the most undnt form of soil N ville. This suggests tht plnt speies turnover n e determined y the distriution of different hemil forms of soil N. Resoure prtitioning of soil N hs lso een demonstrted in temperte grsslnds (Weigelt et l. 25, Khmen et l. 26). However, the ility of plnts to prtition soil P remins less ler, despite the diversity of hemil forms of soil P, the unique physiologil hllenges they pose for plnts, nd their heterogeneous distriution (Turner 1

6 28). Totl soil P is present in vriety of different hemil forms, inluding lile inorgni nd orgni frtions. Inorgni P (P i ) n e tken up diretly, without the id of speilized ell trnsporters or enzymes (Silverush nd Brer 1983). Orgni P (P o ), whih n onstitute nywhere from 3-9% of the totl soil P (Hrrison 1987), is present in ompounds tht differ mrkedly in their iologil vilility (Condron et l. 25). These inlude P monoesters (gluose phosphte, mononuleotides), diesters (RNA, DNA), nd monoester inositols (phyti id) (Turner 28). In order for plnts to exploit P o, they must first re-minerlize it into P i (Trfdr nd Clssen 1988, Adms nd Pte 1992). This proess n e hieved through the exudtion of speilized phosphtse enzymes, whih leve ester onds nd lierte phosphte from P o (Antius et l. 1992). The different forms of soil P n e pled long grdient of inresing investment required for exploittion, depending on the metoli ost of produing enzymes ple of lierting P i from orgni sustrtes (Turner 28). Thus, monoester P requires hydolysis y the enzyme monoesterse, diester P y oth mono nd diesterse, nd inositol P y monoesterse nd phytse (Fig. 1). Chnges in reltive undne of inorgni, monoester, diester, nd inositol P long grdients of deresing soil P roughly mirror their iovilility to plnts (Turner et l. 27). Soils high in totl P re mde up primrily of P i. As soils ge nd totl soil P delines, there is n inrese in reltive proportion of P o (Syers nd Wlker 1969, Prfitt et l. 25). Initilly, this P o is omposed primrily of P monoesters nd inositols. As totl P dereses still further, monoester nd inositol P deline rpidly, nd diester P inreses in undne (Turner et l. 27) (Fig. 2). Finlly, the most P poor soils on erth ontin low mounts of P o, with most P i sored to soil tions (Al nd Fe in id soils, C in lkline soils) (Lmers et l. 28). Conomitntly, there is turnover of plnt speies tht employ different P-quisition strtegies long grdients of totl P vilility. These inlude ssoition with different funtionl groups of myorrhiz (rusulr nd etomyorrhiz) nd/or formtion of proteiod luster roots (Lmers et l. 28, Turner 28). Soils high in inorgni P tend to host rusulr myorrhizl (AM) plnt speies, while more wethered soils host etomyorrhizl (EM) plnts, nd the most P-defiient soils tend to host nonmyorrhizl (NM) plnts tht form root lusters (Rihrdson et l. 24, Lmers et l. 26, Crews et l. 1995) (Fig. 3). 2

7 Of prtiulr interest is whether plnts with different P-quisition strtegies speilize to tke up different hemil forms of P. Myorrhizs provide plnts with myeli tht expnd the volume of soil where P n e otined, providing s muh s 8% of plnts totl P uptke (Douds et l. 2). In ddition, severl studies hve demonstrted tht AM nd EM differ in their prodution of phosphtse enzymes. AM speies re generlly onsidered P svengers, whih use myeli to extensively serh the soil for inorgni P (Smith nd Red 1993). To ontrst, EM speies re well known to re-minerlize P from orgni esters through the prodution of mono nd diesterse, nd phytse enzymes (Antius et l. 1992). However, this prdigm my e shifting, s more reent studies heve demonstrted the ility of some AM speies to omplete their life yle when limited to orgni P (Joner et l. 2, Koide nd Kir 2). Plnt speies tht form proteiod luster roots, prtiulrly in the fmily Proteee, exist on some of the most P-defiient soils on erth nd re often desried s P miners. While these speies re lmost exlusively non-myorrhizl (Lmers et l. 28), their roots exude oth phosphtse enzymes nd undnt orgni ids ple of re-minerlizing orgni P nd relesing P i sored to soil tions, respetively (Adms nd Pte 1992, Wtts nd Evns 1999). P-limited soils re distriuted primrily t tropil nd sutropil ltitudes, where the lk of reent glitions hs llowed oth physil wethering nd iologil sequestrtion of soil P to proeed uninterrupted over long periods of time ( yers) (Vitousek 24). These ltitudes lso ontin the most speies rih plnt ssemlges on the plnet, with tropil forests lone ontining more thn hlf of ll plnt speies on less thn 5% of the erth s surfe (Prne 1982). Moreover, nthropogeni inreses in other limiting resoures, vi tmospheri N deposition nd inresed CO2 emissions, threten to drive tropil plnts towrds more mrked P-limittion (Norisd et l. 26, Pheonix et l. 26). If these environmentl inputs ffet similr inrese in interspeies ompetition, they my led to the extintion of plnt speies tht re poor ompetitors for soil P. Alterntively, resoure prtitioning of soil P ould uffer interspeies ompetition ginst inresed P-limittion, filitting oexistene in the fe of glol limte hnge. Mehnistilly, plnt speies tht re dpted to quire P from different soures should lso differ in their prodution of phosphtse enzymes. Assys of P-monoesterse re used s proxies of oth the pity to reminerlize simple P-monoesters (e.g. gluose-phosphte) s well s 3

8 monoester inositol P (phyti id) (Antius et l. 1992). Additionlly, if plnts speilize to exploit different forms of P, they should eliit severl growth, llotionl, funtionl, nd nutritionl retions when limited preferred P forms, reltive to less preferred forms. These inlude: (1) inresed growth (2) inresed llotion in photosyntheti strutures (leves) reltive to nutrient quisition strutures (roots) (Shipley nd Mezine 22). (3) inresed speifi lef re (SLA), funtionl lef trit desriing the rtio of lef re to lef mss tht orreltes positively with plnt nutrition nd light limittion (Hirose et l. 1988, Witkowski et l. 1992, vn Arendonk et l. 1997, Mezine nd Shipley 1999). (4) inresed P-onentrtion ([P]), whih should orrespond inversely to P limittion, ut is lso sujet to inreses due to luxury onsumption of exess P nd trnslotion from sised lef nd root tissues. (5) inresed totl P, whih indites the uptke of P. (6) inresed P use effiieny (PUE), whih mesures the effiieny with whih plnt iomss is umulted per unit of P uptke. While previous studies hve estlished differenes in root enzyme tivities in plnt speies (Adms nd Pte 1992, Antius et l. 1992, Wtts nd Evns 1999), these studies hve not ontrsted the enzyme prodution, growth, llotion, nutrition, nd funtionl hrteristis of oexisting plnt speies representtive of multiple P-quisition strtegies. This depth is required in order to ridge the gp etween pot studies nd eology due to the myrid influenes ffeting ompetitive suess, suh s growth/p uptke trde-offs. These hrteristis re importnt s plnts with omprle ility to re-minerlize the sme P soure my lso differ in their P- requirements nd uptke effiieny oth ftors tht would ffet fitness nd, therefore, pity to oexist on shred soil sustrte. Moreover, previous studies hve foused exlusively on temperte plnt speies, while mjority of terrestril plnts growing on P- defiient soils re found t tropil ltitudes. Here I provide the first growth experiment 4

9 ompring tropil AM, EM, nd NM (with luster roots) plnt speies ility to grow nd quire P from inorgni, monoester, diester, nd inositol P. 5

10 Methods Plnt speies exhiiting AM, EM, nd NM root systems were olleted from the Fortun Forester Reserve nd either grown in soilless medi with P provided exlusively in different hemil forms or ssyed for the prodution of P-mono nd diesterse enzymes. Study Site Fieldwork ws onduted within the Fortun Forest Reserve (19,5 h), Chiriqui Provine, long the Centrl Cordiller of Pnm (Fig. 4). Fortun onsists of lower montne forests etween 1 nd 15 m.s.l., with men nnul rinfll from mm nd men nnul temperture rnging from 19 to 22 C (Cvelier et l. 1996). Seedlings were olleted from outside 1-hetre plots t Querd Chorro, Hond B, nd Hornito. Both Querd Chorro nd Querd Hond "B" hve soil formed on rhyolite tuff with very low onentrtions of N nd P (Tle. 1). The Chorro plot is dominted primrily y plm speies, ut lso ontins the AM fol speies Podorpus oleifolius. Hond "B" is dominted y the EM emergent nopy tree Oreomunne mexinum, Junglndee (29% of the trees > 1 m DBH; 42% of the sl re). Hornito is hrterized y reltively nutrient rih diti soils (Anderson et l. 21, Dlling unpulished dt). Study Speies Mollinedi drienensis (AM). Order: Lurles, Fmily: Monimiee. M. driensis is shde-tolernt nopy tree with wide distriution ross sites t the Fortun Forest Reserve. It ours from Cost Ri to southern Colomi (GBIF 211). It is lssified s AM on the sis of the doumented ssoition of other gener within Monimiee (Duousso et l. 28, Ruiz nd Dvey 25). It ws olleted outside Hond B. Podorpus oleifolius (AM with root nodules). Order: Pinles, Fmily : Podorpee. P. oleifolius is shde-tolernt onifer found on rhyolti tuff soils t the Hond nd Chorro sites within the Fortun Forest Reserve, with lustering of emergent nopy trees t the Chorro site. It ours from southern Mexio, throughout Centrl Ameri, nd long western South Ameri into Boliv (GBIF 211). Plnts in the Podorpee form spheril root nodules, whih n eome infeted with AM myorrhiz. Podorps re known to ssoite on wethered soils high 6

11 in inositol nd diester P (Turner et l. 27). P. oleoifolius is lssified s AM due to the onsistent doumenttion of AM infetion oth within Podorpee nd the genus Podorpus (Wng nd Qui 26). It ws olleted outside Chorro. Oreomunne mexin (EM) Order: Fgles, Fmily: Juglndee. O. mexin is shde tolernt nopy tree found with wide distriution ross sites t the Fortun Forest Reserve, ut with mrked lustering round the rhyolyti soils of Hond A nd B. It hieves monodominne only within the Hond B site, where it forms thik swths of seedlings. It ours from southern Mexio to entrl Pnm (GBIF 211). O. mexin ws previously hrterized s EM y Quist et l. (2). Surfe oservtions of infeted root tips of O. mexin t Fortun support this hrteriztion. It ws olleted outside Hond B. Roupl montn (NM). Order: Proteles, Fmily: Proteee. R. montn is shdetolernt nopy tree with wide distriution ross the sites t the Fortun Forest Reserve. It ours from southern Mexio, throughout Centrl Ameri, nd into Southern Brzil (GBIF 211). It forms lusters of fine roots, whih is ommon trit mongst the Proteee. It is hrterized s NM on the sis of the ommon lk of myorrhizl infetion doumented within the Proteee (Brundrett 28, Lmers et l. 28). However, some evidene suggests tht even luster root forming speies n host AM fungi, though they re onsidered redundnt in terms of ugmenting host-plnt nutrition (Boulette & Lmers 26). It ws olleted outside of Hornito. Nutrient Stok Solutions Experimentl nd ontrol plnts were fertilized every other dy with 3 ml of solution ontining ll essentil nutrients. Nutrient stok solutions were prepred y first prepring mster no-p ontrol solution with Sott s (mss rtio of N:P:K) Drk Wether Feed fertilizer, supplemented with MgSO 4. For the P tretment solutions, the nutrient solution lso inluded the ddition of sodium phosphte monosi (PO4, Sigm S761), D-gluose 6- phosphte disodium slt hydride (G6P, Sigm G725), phyti id sodium slt hydride (INS, Sigm P19), or RNA from torul yest (Sigm R6625) (Tle. 2). Plnt Colletions 7

12 Forty-six re-root seedlings of eh fol speies were olleted from field soil t the Fortun Forest Reserve etween Ferury 22-Mrh 23, 21. Six seedlings from eh speies were hrvested efore the experiment egn to estimte speies initil vlues for ll dependent vriles. The roots of the remining 4 seedlings were gently wshed with wter nd the plnts were trnsplnted into 3 5 m (length dimeter) ontiners filled with id wshed mrine snd (4.3 μg/m 3 resin P, 1.9μg/m 3 miroil P, Dlling unpulished dt). Seedlings were divided into 5 tretment groups with 8 replites eh. Replites were orgnized to minimize the differene etween verge stem height nd lef numer etween tretments. These tretments orrespond to plnts provided with ll essentil nutrients with P s either (1) inorgni phosphte (PO4), (2) orgni monoester phosphte (G6P), (3) inositol phosphte (INS), (4) diester phosphte (RNA), nd (5) P-free ontrol. Initil stem height nd lef numer were reorded for eh replite for use s potentil ovrites. Conetiners were pled in growing house with trnsprent plsti roof nd 75% shde-loth. Speies were grouped together on the sme enh with the plement of tretments rndomized. Approximtely every 2 weeks the position of eh plnt ws hnged on the enh to orret for ny heterogeneity in light nd temperture. After the first four weeks, the shde loth ws redued to 5%. After 4-months plnts were removed from the snd medi. Leves were snned on flted snner to determine lef re, nd plnts were dried for three dys t 7 C nd weighed to determine totl dry mss, nd lef, stem, nd root dry mss independently. All of the lef, stem, nd root tissue were ground into fine powder. The P onentrtion of rndom smple tken of the omposite powder ws digested in id, mesured using indutively oupled plsm spetrosopy, nd expressed on mg P g -1 sis. Anlysis Plnt dry mss ws used to lulte reltive growth rte (RGR), RGR=[ln(M f ) ln(m i )]/(Δt) where M f is finl mss, M i is initil mss estimted s the verge dry mss of the preexperimentl hrvest, nd Δt is the durtion of the experiment in dys. Speifi lef re, mesure of lef thinness, ws lulted s the sum of lef re over lef dry mss. Mss rtios were lulted s the rtio of lef, stem, nd root dry mss over totl plnt dry mss. Totl P 8

13 mesurements were lulted s the produt of P-onentrtion nd totl dry mss. P use effiieny (PUE) ws lulted s PUE= (M f -M i )/(P f M f ) where P f is the finl P onentrtion. To ssess the signifine of speies nd speies*tretment intertion on the dependent vriles, omposite ANOVAs with the four speies were run with speies, tretment, speies*tretment intertion, nd initil lef numer (when signifint) s model sttements. For eh speies seprtely, differenes in tretment mens for eh dependent vrile were nlyzed using ANOVA, with initil lef numer used s ovrite when it explined signifint mount of vrition (p<.5). When within-speies ANOVA returned p-vlues.5, differenes in tretment mens were nlyzed using lest signifint differene (LSD). Enzyme Assys 1-14 individuls from eh of the fol speies used in the growth experiment were potted in field soil for pproximtely 1 months nd then hrvested to ssy their prodution of P-mono nd diesterse using protool modified from Antius et l. (1992). Assy uffer ws prepred y tking 2mM solution of sodium ette (Sigm), djusted to ph 5. y ddition of eti id. Stok solutions of 25mM p-nitrophenyl phosphte (Fisher Sientifi, NPP), nd is(p-nitrophenyl)phosphte (Sigm, BNPP) were prepred in ssy uffer nd kept frozen until the dy ssys were run. Plnt roots were rinsed gently in deionized wter. Foreps were used to remove soil prtiles tht remined dhered to fine roots. For eh plnt, 3 to 5 root tips per vil were removed nd pled in one of five 7.5 ml glss vils filled with either 4.9 ml (experimentl tretments) or 5. ml (ontrol) of ssy uffer. Glss vils were kept in n inutor (Boekel Sientifi) for pproximtely 3 minutes to rise the temperture to 26 C. The ssys egn with the ddition of 1 ul of enzyme sustrte, for finl sustrte onentrtion of.5mm in 5.mL. The glss vils were then trnsferred to shker (Eerh 61) operting t 3 Hz, where they remined for 45 minutes. To terminte the retions, 5 ul of the retion mixture of NPP, BNPP, nd no-sustrte ontrol were dded to 4.5 ml of.125 M NOH (ph 1). The relese of produt ws mesured 9

14 y reding the sorne of smples t 45 nm in spetrophotomoter (Hh DR5). Asorne vlues were onverted to mm using stndrd urves prepred with p-nitrophenyl (Sigm). Roots were removed from glss vils, pled in leled luminum foil envelopes, nd dried t 15 C for 24 hrs. Enzyme tivity ws expressed s μm produt mg -1 dry root mss hour -1, with ontrol vlues for eh plnt replite sutrted from the experimentl vlues. For eh ssy, speies were nlyzed using ANOVA, with signifint differenes determined t (p<.5). Differenes in speies mens were nlyzed using lest signifint differene (LSD). 1

15 Results Nerly ll dependent vriles vried signifintly with tretment, with the exeptions of root mss frtion (RMF) nd phosphorus use effiieny (PUE). The most signifint tretment effets were oserved in P onentrtion, totl P, RGR, nd totl lef re (TLA). Most dependent vriles vried more signifintly etween speies, with the exeptions of SLA nd P onentrtion. The most signifint of these inlude the growth nd iomss llotion vriles TLA, root mss frtion (RMF), nd lef mss frtion (LMF). Further, signifint speies x tretment intertions were found in ll vriles with the exeption of LMF nd totl P, with the most signifint ourring in TLA, P onentrtion, SLA nd RGR. When R. montn (NM) ws removed from the model, the speies x tretment intertion disppered for ll vriles. This did not our for ny of the other speies. The lef ovrite hd signifint effet on RGR nd P-onentrtion only. There ws no signifint intertion etween initil lef numer nd speies or tretment for ll dependent vriles (Tle 3). Within eh speies, tretment hd signifint effet on most dependent vriles. Exeptions inlude M. driensis TLA nd SLA, P. oleifolius SLA, nd O. mexin RMF nd SLA (Tle 4). The lef ovrite hd signifint effet on M. driensis TLA nd LMF, O. mexin totl P, nd R. montn RGR nd TLA. There ws no signifint intertion etween initil lef numer nd tretment for ll omintions of speies nd dependent vriles. Reltive Growth Rte AM P. oleifolius nd M. driensis hd similr ptterns of growth etween tretments, with reltively high growth in PO4 nd G6P, nd lower growth in INS nd RNA. However, in oth speies, only growth in the PO4 tretment vried onsiderly from the NO/P ontrol. O. Mexin (EM) hd mximum growth rte of nerly one-third the other speies, nd experiened negtive growth in the RNA tretment (onsistent with lef nd/or root sission). R. montn (NM) ws the fstest growing of the four speies, with unique pttern of growth etween tretments. Its mximum RGR ws the in INS tretment. Further, R. montn ws the only speies with signifintly different RGR etween the monoesters G6P nd INS. However, growth in oth the PO4 nd INS tretments did not differ signifintly from the NO/P ontrol (Fig. 5). 11

16 Totl Lef Are AM M. driensis nd P. oleifolius hd nerly identil ptterns of TLA etween tretments, whih mirror the ptterns of RGR etween tretments. O. mexin (EM) hd the highest TLA mongst speies, ut with the PO4 tretment not differing signifintly from the NO/P ontrol. Further, O. mexin TLA ws signifintly lower in the RNA tretment thn in the NO/P ontrol. R. montn (NM) TLA ws signifintly greter in INS thn in ll other tretments. This tretment effet is lso strong in mgnitude the TLA of the INS tretment is etween 2 to 3 fold higher thn in the PO4 nd NO/P tretments (Fig. 6). Speifi Lef Are Myorrhizl M. driensis, P. oleifolius, nd O. mexin hd no signifint differenes in SLA etween tretments. R. montn (NM) hd signifintly greter SLA in INS thn in ll other tretments (Fig. 7). Lef Mss Frtion M. driensis (AM) nd O. mexin (EM) hd no differenes in LMF etween tretments. AM P. oleifolius LMF in PO4 nd G6P ws signifintly greter thn in NO/P ontrol. R. montn (NM) LMF ws signifintly greter in INS thn in the G6P nd RNA tretments. However, LMF of INS nd PO4 did not differ signifintly from the NO/P ontrol. Both O. mexin nd R. montn exhiit signifintly higher LMF thn the other speies (Fig. 8). Stem Mss Frtion In generl, there ws n inverse reltionship etween SMF nd RGR. Both M. driensis (AM) nd O. mexin (EM) hd signifintly greter SMF in RNA thn ll the other tretments. P. oleifolius (AM) hd similrly high SMF in RNA, though it did not differ signifintly from the INS tretment. R. montn (NM) hd the gretest nd lest SMF in the two monoester tretments G6P nd INS, respetively. In ddition, R. montn SMF ws signifintly greter in the NO/P thn it is in the INS tretment (Fig. 8). Root Mss Frtion Neither M. driensis (AM) nor O. mexin (EM) exhiit signifint differenes in RMF etween tretments. P. oleifolius (AM) hd signifintly greter RMF in NO/P thn in ll other tretments. R. montn (NM) RMF ws signifintly higher in NO/P nd RNA tretments thn in the INS tretment, whih exhiits the lowest RMF (Fig. 8). R. montn roots in the NO/P tretment lso differed qulittively from the other tretments. Wheres t the eginning of the experiment none of the R. montn replites ontined luster roots, t hrvest 12

17 6 of 8 R. montn hd developed simple root lusters. Cluster root formtion ws not oserved in ny other tretment. Phosphorus Conentrtion ([P]) AM M. driensis, P. oleifolius, nd NM R. montn hd similr ptterns of [P] etween tretments, with PO4, G6P, nd RNA signifintly greter thn NO/P [P]. O. mexin (EM) [P] ws gretest in the RNA tretment, with nerly 2.5 fold differene etween [P] in the RNA nd NO/P tretments. R. montn hd wide rnge of [P] vlues etween tretments with similr RGR, inluding nerly 8-fold differene in [P] etween PO4 nd NO/P tretments. There ws no signifint differene in R. montn [P] etween the INS nd NO/P tretments (Fig. 9). Totl Phosphorus Of the myorrhizl speies, only M. driensis (AM) nd O. mexin (EM) hd signifintly higher totl P in G6P thn in the other tretments. R. montn (NM) totl P ws signifintly greter in PO4 nd RNA thn in the other tretments, wheres G6P did not differ from the NO/P ontrol (Fig. 1). The totl P in the INS tretment ws nerly 3-fold greter thn in the NO/P ontrol, with ner-signifint p-vlue of.64. Phosphorus Use Effiieny (PUE) The myorrhizl speies ll hd signifintly less PUE in the RNA ompred to the other tretments. R. montn (NM) PUE ws mrkedly greter in the NO/P ontrol, with roughly 6-fold greter PUE thn the PO4 tretment. In ddition, R. montn PUE ws signifintly greter in the INS tretment thn in ny of the other experimentl tretments, with roughly 3-fold the mgnitude of the PO4 vlue (Fig. 11). P mono nd diesterse R. montn (NM) produed signifintly more P-monoesterse thn the other fol speies. R. montn lso produed signifintly more P-monoesterse in root lusters thn in fine roots. R. montn lso produed signifintly more P-diesterse thn the other speies, though root lusters nd fine roots did not differ signifintly (Fig. 12). 13

18 Disussion My results support the potentil for myorrhizl nd nonmyorrhizl speies to prtition soil orgni P. The dispperne of the signifint speies x tretment intertion for RGR, totl lef re, SLA, RMF, P onentrtion, nd PUE (Tle 3) when R. montn (NM), ut not the other speies, were removed from the model indites tht the AM nd EM speies did not differ signifintly in their response to different hemil forms of P. Reltive the myorrhizl plnt speies, R. montn (NM) exhiits numer of unique retions to inositol nd diester P. While R. montn growth did not differ signifintly etween the inositol-p tretment nd no-p ontrol (Fig. 5d), resoure llotion nd funtionl hrteristis indite tht the inositol-p tretment were primrily light limited, while plnts in the no-p ontrol were nutrient limited. Thus, R. montn in the inositol-p tretment invested signifintly more resoures in photosyntheti strutures (greter lef re nd thinner leves) thn in ny other tretment (Figs. 6d, 7d), nd lloted signifintly less iomss to roots thn in the no-p ontrol (Fig. 8d). Moreover, R. montn produed root lusters only in the no-p ontrol, inditing tht it ws not stressed for dditionl P in the experimentl tretments. The nutritionl dt further orroortes R. montn s signifint nd unique exploittion of inositol P. R. montn produed signifintly greter levels of P-monoesterse thn the other speies (Fig. 12), whih hs een demonstrted to t s n effetive proxy of P-uptke from inosoitol-p (Antius et l. 1992). Further, R. montn totl P ws more thn 3 fold greter in the inositol-p tretment thn in the no-p ontrol, nd PUE in the inositol-p tretment ws signifintly greter thn ny of the other experimentl groups unique result mongst speies (Fig. 11). The mrked differenes in PUE etween tretments reflet R. montn s ility to sustin high growth under wide rnge of different P onentrtions. While plnts in the inorgni-p nd no-p ontrol did not differ signifintly in RGR, they vried more thn 8-fold in P-onentrtion, nd 6-fold in totl P (Figs. 9d, `1d). Thus, the pprently uniform growth of R. montn in inorgni-p, inositol-p, nd the no-p ontrol elies host of llotionl, funtionl, nd nutritionl differenes inditing (1) luxury onsumption of P in inorgni-p, (2) effiient nd iologilly signifint exploittion of P in inositol-p, nd (3) effiient moiliztion of P reserves nd the onset of P-stress in the no-p ontrol. This result suggests NM Proteee 14

19 possess hereto unppreited verstility of dpttions to growth on soils with different forms of soil P. While the myorrhizl speies exhiit enhned growth nd nutrition when limited to gluose reltive to inositol-p, the NM R. montn hd n opposite retion. Thus, R. montn hd signifintly greter RGR nd PUE in the inositol thn in the gluose-p tretment (Fig. 5d,11d). Further, while oth M. driensis (AM) nd O. mexin (EM) hd signifintly greter totl P in the gluose-p tretment thn the no-p ontrol, R. montn did not (Fig. 1). Both inositol P nd gluose-phosphte re monoesters, nd thus suseptile to hydrolysis y the high levels of R. montn P-monoesterse (Fig. 12d). As myorrhiz n tke up nd metolize simple sugrs pplied externlly to infeted root tips (Büking nd Shhr-Hill 25), it is possile tht gluose ddition inresed the fitness of C-limited mutulisti AM nd EM, while the effet on R. montn (NM) ws only to inrese the fitness of free living miroes with whih it ompeted for ville N nd P. If so, future experimenttion should revel tht myorrhizl plnt speies, ut not uninnoulted ontrols, enefit more from unphosphorylted gluose ddition thn NM plnt speies. P. oleifolius (AM with nodules) ppers to hve no enhned ility to exploit orgni P reltive either M. driensis (AM) or O. mexin (EM), despite its doumented ffinity for low P soils with high proportions of diester nd inositol P (Turner et l. 27, Turner 28). It seems likely tht P. oleifolius re dpted to respond to grdients of inorgni P vilility, rther thn for the quisition of orgni P. Generlly, podorps respond to mixed-fertilizer ddition with deresed growth nd survivility (Crswell et l. 23, Preliussen et l. 26). It is lso possile for podorps to promote low P onditions y reting high C:P lef litter, whih resists deomposition (Wrdle et l. 28). The role of the root nodules s dpttions to low nutrient soils remins unknown; though they re urrently implited in (1) hosting fulttive N-fixing teri nd (2) inresing the effiieny of AM mutulists (MGee et l. 1999). Of these two possiilities, the first is proly spurious, nd sed on the onfounding of N-fixtion of freeliving teri in soil round podorp roots for symioti N-fixtion vi podorp nodules (Khn nd Vlder 1972, Silvester nd Bennett 1973). The seond possiility wrrnts further investigtion, perhps y ssessing the mgnitude tht AM inoulum enhnes podorp growth nd nutrition reltive to other symptri plnt speies. 15

20 Although EM speies re doumented to oth produe greter mounts of phosphtse enzymes nd to outompete AM speies on soils high in orgni P, the P-mono nd diesterse of O. mexin did not differ signifintly from the AM speies, while the RGR of AM speies ws greter thn O. mexin in ll tretments. In other tropil eto-monodominnt forests the estlishment of ommon hyphl networks is thought to ugment oth the shde tolerne nd nutrition of EM seedlings (Nr 26, MGuire 27). However, the RGR of O. mexin growing in field soils is not known, so it is not possile t this point to ssess the effet of lost iologil intertion under experimentl onditions. Further, in forest soils EM hyph expnd horizontlly to inrese the rhizosphere volume within thin surfe lyers of orgni mtter. This sptilly expnsive svenger strtegy my not e menle to growth in reltively nrrow dimeter onetiners. The low growth response mongst ll speies when limited to diester-p group (Fig. 1) does not pper to e used y P-defiieny. Eh speies produes signifint levels of P-diesterse, hd signifintly greter P-onentrtion in the diester-p tretment thn in the no-p ontrol. Most speies totl P did not differ signifintly etween the diester nd inorgni-p tretments (with the exeption of O. mexin, whih hd signifintly greter P-onentrtion in the diester-p tretment) (Fig. 5). It ppers tht either diester-p posed formidle metoli ost for plnts to quire or produed toxi effet retrding plnt growth. Some support exists for the inresed metoli ost of reminerlizing diester-p, whih ourred t round one hlf the rte of monoester-p mongst the fol speies in this experiment (Figure 12). However, differenes in RGR nd totl P etween tretments indite tht R. montn is the only speies to mke trdeoff etween growth nd P-uptke from diesters. R. montn, whih hd the greter P-diesterse tivity thn the myorrhizl plnt speies (Fig. 12), ws the only speies with signifintly higher totl P in the diester-p group reltive the no-p ontrol, despite growing signifintly less (Figs. 5d, 1d). To ontrst, the myorrhizl speies hd deresed growth nd similr totl P etween the diester-p nd no-p ontrol group (Fig5-, Fig 1-). An interesting possiility is tht the uptke of inomplete produts of RNA re-minerliztion, suh s short-hin RNA moleules nd mononuleotides, negtively ffets plnt growth. Pungfoo-Lonhienne (21) hs estlished plnts n tke up intt nulei ids, whih n t oth s P soure nd signling moleule. I suggest metolomi pproh imed t estlishing the reltionship of 16

21 plnt tissue RNA onentrtions, growth, nd nutrition ould shed light on the potentilly toxi effet of nulei id P. Results from this study led to some working preditions on the reltive fitness of the fol speies growing in soils with vrying P vilility. Thus, R. montn (AM) should e suessful on oth young soils rih in inorgni P, nd on older wethered soils with high proportions of inositol nd diester P. M. driensis (AM) nd O. mexin (EM) my outompete R. montn on soils ontining P-monoesters ound to simple sugrs. P. oleifolius (AM with root nodules) should not ompete with plnts over orgni P, ut rely on host of other dpttions to persist on low P soils. Future studies should utilize oth desriptive methods imed t relting the distriution of plnt tx to the mgnitude nd proportions of soil P present in different hemil forms, s well s experimentl mnipultions of (1) ommon grdens of fol speies growing on different soil sustrtes nd (2) trking P 32 nd P 32 /C 14 trers tthed to orgni sustrtes s they re tken up y plnts. NM plnt speies, suh s those of Proteee, my hve the ility to form n eologil nihe sed upon the exploittion of inositol nd diester-p. However, given tht mjority of terrestril plnt speies re myorrhizl (Brundrett 29), resoure prtitioning of soil orgni P my not ply primry role in promoting their oexistene. Resoure prtitioning should e onsidered seprtely from dpttions tht llow plnts to grow on soil with low P-vilility, suh s low growth rte, long lived leves, nd high folir C:P. This is prtiulrly relevnt given inreses in N-deposition nd tmospheri CO 2, whih my fvor NM speies tht invest in exploiting relitrnt inositol nd diester-p pools to mintin high growth rtes on soils with low P vilility. Thus, omprehensive understnding of plnt speies oexistene should inlude resoure prtitioning of soil orgni P. 17

22 Tles nd Figures Tle 1. Adpted from Anderson et l. (21). Site lotion, tree speies olleted, nd environmentl hrteristis of three 1-h plots in lower montne forests in western Pnm. Temperture is estimted using diti lpse rtes in Cvelier et l. (1996). All soil hemistry vlues re mens of 15 smples (-1 m depth) ± stndrd errors. Vlues with different letters indite signifintly different mens fter Bonferroni orretion (P<.5). Environmentl Chorro Hond B Hornito Vriles Sustrte Rhyoliti tuff Rhyoliti tuff Dtiti Topsoil Orgni Orgni Orgni Tress speies olleted P. oliofolius (AM with root nodules) O. mexin (EM), M. drienensis (AM) R. montn (NM) Ltitude (N) Longitude (W) Elevtion (m) Temperture ( C) Annul rinfll (mm yer -1 ) Fisher s α Soil properties Bulk density (g m -3 ).8 ±.6.13 ±.3.39 ±.9 ph 3.91 ± ± ±.12 N:P.25 ±.3.36 ±.12.5 ±.1 Inorgni N (μg m -3 ).63 ±.6.8 ± ±.99 P (μg m -3 ) 2.74 ± ± ± 1.94 Al (μg m -3 ) 316 ± ± ± 12 C (μg m -3 ) 97 ± 22 4 ± ± 229 Fe (μg m -3 ) 55 ± ± ± 26 K (μg m -3 ) 18.8 ± ± ± 7.9 Mg (μg m -3 ) 18.9 ± ± ± 44.7 CEC (%) 53.3 ± ± ± 3.1 Bse sturtion (%) 19.4 ± ± ±

23 Tle 2. The mm onentrtion nd hemil form of ll mro nd mironutrients in the hydroponi feed solution. Note tht experimentl tretments reeived one of the four possile forms of P, while the different forms of N were provided simultneously (perentges indite the reltive mss of eh form). Nutrient Chemil Form mm in feed solution Phosphorus (P) Sodium phosphte.833 Gluose Phosphte Phyti id Rionulei id Nitrogen (N) 82.6 % nitrte % ure 3.5% mmoni Potssium (K) Potssium nitrte Mgnesium (Mg) Mgnesium sulfte Sulfur (S) Mgnesium sulfte Clium (C) Clium nitrte 6.44 Iron (Fe) Fe-EDTA.21 Mngnese (Mn) Mn-EDTA.11 Copper (Cu) Cu-EDTA.1 Boron (B) Bori id.15 Zin (Zn) Zn-EDTA.1 Molydenum (Mo) Ammonium molydte.218 Tle 3. F tle of omposite ANOVA for ll dependent vriles of the growth experiment, with lef rows shded when they do not explin signifint mount of vrition. Attriute speies tretment speies lef tretment Reltive growth rte 31.3*** 12.78*** 2.43** 4.32* Totl lef re 95.83*** 1.44*** 6.25*** Lef mss frtion 55.58*** 6.46*** 1.55 Stem mss frtion 1.41*** 1.21*** 2.39** Root mss frtion 61.16*** ** Speifi lef re * 2.55** P-Conentrtion 21.74*** 39.1*** 6.17*** 3.95* Totl P 34.22*** 14.92*** 1.58 PUE 6.25** ** * P<.5, **P<.1, ***P<.1 19

24 Tle 4. F tle for within speies ANOVA for ll dependent vriles of the growth experiment, with lef rows omitted when they do not explin signifint mount of vrition. Attriute Sttement (degrees of freedom) Mollinedi (AM) Podorpus (AM w/ nodules) Oreomunni (EM) Roupl (NM) Reltive tretment (4) 5.5** 5.31** 4.78** 3.9* growth rte lef (1) 5.54* Totl lef tretment (4) 4.48** 8.36** 7.18** 9.74*** re lef (1) 4.32* 4.71* Lef mss tretment (4) ** 5.33** 3.97* frtion lef (1) 5.23* Stem mss tretment (4) 4.32** 4.9** 4.48** 3.18* frtion lef (1) Root mss tretment (4) ** * frtion lef (1) Speifi lef tretment (4) ** re lef (1) P- tretment (4) 5.95** 7.2** 9.51*** 18.31*** Conentrtion lef (1) Totl P tretment (4) 4.66** 1.1*** 2.94* 7.7** lef (1) 4.36* PUE tretment (4) 4.27** 3.17* *** lef (1) * P<.5, **P<.1, ***P<.1 2

25 Figure 1. Adpted from Turner (28). A oneptul digrm of different plnt speies (A- D) either ompletely (solid line) or prtilly (dotted line) exploiting monoesters (), diester (), nd inositol () P long grdient of inresing investment. Figure 2. Adpted from Turner et l. 27. The % of totl orgni P (y xis, note differene in sle) found in monoester P, inositol P, nd diester P long 1, yer grdient of soil ge (x-xis) in the Frnz Joseph hronosequene, NZ. 21

26 Figure 3. Adpted from Lmers et l. 28. A oneptul digrm showing hnges in totl soil P (purple) nd N (lue) long grdients of soil ge. The reltive undne of plnts with different P quisition strtegies is indited y the width of the orresponding tringles. 22

27 Figure 4. Adpted from Anderson et l. (21). A mp showing the lotion, elevtion, nd soil type of ten 1-h plots in the Fortun (Chiriqui) nd Plo Seo (Bos del Toro) Forest Reserves. Plnt olletions were mde t (from top to ottom) Hond B, Chorro, nd Hornito. 23

28 RGR (mg g 1 dy 1 ) Mollinedi (AM) RGR (mg g 1 dy 1 ) Podorpus (AM w/nodules) RGR (mg g 1 dy 1 ) Oreomunni (EM) d RGR (mg g 1 dy 1 ) Roupl (NM) 4 Figure 5. Men reltive growth rte +/- stndrd error for eh tretment of () Mollinedi drienensis, () Podorpus olieofolius, (d) Oreomunni mexin, nd (d) Roupl montn. Within eh speies, rs with different letters re signifintly different. Note the differene in sle for O. mexin. 24

29 Totl Le Are (m 2 ) Mollinedi (AM) Totl Le Are (m 2 ) Podorpus (AM w/nodules) Totl Le Are (m 2 ) Oreomunni (EM) d Totl Le Are (m 2 ) Roupl (NM) Figure 6. Men totl lef re +/- stndrd error for eh tretment of () M. drienensis, () P. olieofolius, () O. mexin, nd (d) R. montn. Within eh speies, rs with different letters re signifintly different. Note the differenes in sle. 25

30 Speifi Lef Are (m 2 g 1 ) Mollinedi (AM) Speifi Lef Are (m 2 g 1 ) Podorpus (AM w/ nodules) Speifi Lef Are (m 2 g 1 ) Oreomunni (EM) d Speifi Lef Are (m 2 g 1 ) Roupl (NM) Figure 7. Men speifi lef re +/- stndrd error for eh tretment of () M. drienensis, () P. olieofolius, () O. mexin, nd (d) R. montn. Within eh speies, rs with different letters re signifintly different. Note the differenes in sle. 26

31 mss frtion (mg/mg) Mollinedi (AM) mss frtion (mg/mg) Podorpus (AM w/ nodules) mss frtion (mg/mg) KEY Oreomunni (EM) d mss frtion (mg/mg) Roupl (NM).1 Figure 8. Men frtion of totl mss +/- stndrd error for the leves, stem, nd roots for eh tretment of () M. drienensis, () P. olieofolius, () O. mexin, nd (d) R. montn. Within eh speies nd plnt prt, rs with different letters re signifintly different. 27

32 [P] (mg P g 1 ) Mollinedi (AM) [P] (mg P g 1 ) Podorpus (AM w/nodules) Oreomunni (EM) d 6 5 Roumon (NM) [P] (mg P g 1 ) [P] (mg P g 1 ) Figure 9. Men [P] of omposite smples ontining leves, stem, nd roots +/- stndrd error for eh tretment of () M. drienensis, () P. olieofolius, () O. mexin, nd (d) R. montn. Within eh speies, rs with different letters re signifintly different. Note the differene in sle in R. montn. 28

33 Totl P (mg) Mollinedi (AM) Totl P (mg) Podorpus (AM w/ nodules) NOP PO4 G6P INS RNA NOP PO4 G6P INS RNA Totl P (mg) Oreomunni (EM) d Totl P (mg) Roupl (NM) NOP PO4 G6P INS RNA Figure 1. Men totl P +/- stndrd error for eh tretment of () M. drienensis, () P. olieofolius, () O. mexin, nd (d) R. montn. Within eh speies, rs with different letters re signifintly different. Note the differenes in sle. 29

34 PUE (g mg 1 P) Mollinedi (AM) PUE (g mg 1 P) Podorpus (AM w/ nodules) PUE (g mg 1 P) Oreomunni (EM) d PUE (g mg 1 P) Roupl (NM) Figure 11. Men totl PUE +/- stndrd error for eh tretment of () M. drienensis, () P. olieofolius, () O. mexin, nd (d) R. montn. Within eh speies, rs with different letters re signifintly different. Note the differenes in sle. 3

35 enzyme tivity (μm NP g 1 hr 1 ) monoesterse Mollinedi Podorpus Oreomunni Roupl (NC) Roupl (C) enzyme tivity (μm NP g 1 hr 1 ) P diesterse Mollinedi Podorpus Oreomunni Roupl Figure 12. Men () P monoesterse nd () P diesterse tivity +/ stndrd error for M. drienensis, P. oliefolius, O. mexin, nd R. montn fine roots (NC) nd root lusters (C). 31

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