Effects of Herbivory, Fire and N 2 -fixation on Nutrient Limitation in a Humid African Savanna

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1 Ecosystems (28) 11: DOI: 1.17/s Effects of Herivory, Fire nd N 2 -fixtion on Nutrient Limittion in Humid Africn Svnn Ptrick G. Cech, 1,2 * Thoms Kuster, 1 Peter J. Edwrds, 1 nd Hrry Olde Venterink 1 1 Institute of Integrtive Biology, ETH Zurich, Universitätsstrsse 16, 892 Zurich, Switzerlnd; 2 Swiss Tropicl Institute, Socinstrsse 57, P.O. Box 42, Bsel, Switzerlnd ABSTRACT The quntities nd sptil distriution of nutrients in svnn ecosystems re ffected y mny fctors, of which fire, herivory nd symiotic N 2 - fixtion re prticulrly importnt. We mesured soil nitrogen (N) pools nd the reltive undnce of N nd phosphorus (P) in herceous vegettion in five vegettion types in humid svnn in Tnzni. We lso performed fctoril fertiliztion experiment to investigte which nutrients most limit herceous production. N pools in the top 1 cm of soil were low t sites where fires were frequent, nd higher in res with woody legume encrochment, or high herivore excretion. Biomss production ws co-limited y N nd P t sites tht were frequently urnt or hevily grzed y ntive herivores. In contrst, oveground production ws limited y N in res receiving lrge mounts of excret from livestock. N 2 -fixtion y woody legumes did not led to P-limittion, ut did increse the vilility of N reltive to P. We conclude tht the effects of fire, herivory nd N 2 - fixtion upon soil N pools nd N:P-stoichiometry in svnn ecosystems re, to lrge extent, predictle. Key words: Acci woodlnd; cttle; grsslnd; grzing; N:P rtios; nitrogen fixtion; phosphorus; stoichiometry; tllgrss. INTRODUCTION In svnn ecosystems, grsses nd trees co-exist, forming mosic tht is neither grsslnd nor forest. The vst mjority of svnns owe their existence to fire, nd without it would eventully e replced y forests (Bond nd others 25). However, in drier climtes the lnce etween woody Received 4 June 28; ccepted 1 July 28; pulished online 21 August 28 Electronic supplementry mteril: The online version of this rticle (doi:1.17/s ) contins supplementry mteril, which is ville to uthorized users. Author Contriutions: P.C., H.O.V. nd P.E. designed the study nd wrote the pper. P.C. nd T.K. performed the reserch nd nlyzed the dt. *Corresponding uthor; e-mil: ptrick.cech@unis.ch nd grss cover nd productivity ppers to e minly determined y wter vilility (Arnir nd others 24; Snkrn nd others 25). Compred to humid svnns, these dry svnns re nutrient-rich (Bell 1982; Huntley 1982), though t some sites the productivity of herceous vegettion is limited y the vilility of nitrogen (N) (Ludwig nd others 21; Snymn 22; Augustine nd others 23). In contrst, humid svnns re often on hevily leched soils nd re chrcterized y low phosphorus (P) vilility (Snchez 1976); plnt growth in these ecosystems my e limited y shortges of N, P or oth (Högerg 1986; Medin 1987), lthough which nutrient is limiting in ny prticulr cse hs rrely een investigted. 991

2 992 P. G. Cech nd others Mny fctors ffect the quntities nd sptil distriution of nutrients in svnn soils, with fire, herivory nd tmospheric N 2 -fixtion eing prticulrly importnt. In Figure 1, we present conceptul frmework to show how these fctors re likely to ffect soil N pools nd N:P-stoichiometry. (1) Fire cn cuse considerle losses of ll nutrients to the tmosphere, with losses of N eing much greter thn those of other nutrients (Cook 1994; Kuffmn nd others 1995); s result, repeted fires re likely to promote shortge of N, nd mny svnns re thought to e primrily N-limited. (2) Herivores cn ffect nutrient conditions in vrious wys. The first reltes to the sptil pttern of hitt use for feeding nd excretion. Some herivores re-distriute nutrients y feeding in certin res while depositing their excret in others (Edwrds nd Hollis 1982; Jewell nd others 27), thus cusing locl depletion or enrichment of nutrients. In A B defolition y herivores tllgrss svnn fire grzed ptches 2 Acci woodlnd pddock mrgin N 2 -fixtion excretion from herivores forest gps forest N:P N-limittion P-limittion N-limittion P-limittion N:P soil N pool soil N pool Figure 1. Conceptul frmework of the effects of fire, herivory nd N 2 -fixtion on soil N pool, N:P-stoichiometry nd the type of nutrient limittion (A), nd hypothesized sttus of N pools nd N:P rtios of five vegettion types differentilly ffected y fire, herivory nd N 2 -fixtion in reltion to the presumed climx forest vegettion (B). contrst, others feed nd return their excret in the sme, intensively used res, therey potentilly mintining nutrient rich ptches in otherwise nutrient-poor vegettion (Lmoot nd others 24). Second, significnt proportion of the N in dung nd urine my e lost through mmoni voltiliztion nd leching (Ruess nd McNughton 1988; Frnk nd Zhng 1997; Augustine 23), leding to locl excess of P reltive to N (providing tht the dung nd urine re excreted in the sme res, which is commonly the cse; Edwrds nd Hollis 1982). Third, herivores my hve positive net effect on the soil N pool y reducing the mount of iomss exposed to fire, nd therey reducing the ssocited losses to the tmosphere (Hos nd others 1991; Holdo nd others 27). Hence, depending on the ptterns of grzing nd excretion, herivory hs neutrl effect on the rtio of N:P vililities (defolition) or potentilly shifts the nutrient lnce towrds N-limittion (excretion) (Figure 1). (3) Woody legumes, especilly of the genus Acci, re conspicuous elements of mny svnns, nd the mjority re thought to fix N 2 symioticlly. The undnce nd distriution of these trees is significntly ffected y the ctivities of herivores. For exmple, grzing y domestic livestock is often responsile for extensive encrochment of svnn grsslnds y woody species (Brown nd Archer 1989; Hudk 1999; Toler nd others 23), of which legumes re dominnt component (Archer 1995; Crmer nd others 27). It hs een shown tht much greter mounts of N ccumulte in the ushlnd thn in the open grsslnd it replces; this ccumultion could in turn led to P-limittion under Acci cnopies (Figure 1). There hve een mny griculturl studies of nutrient limittion in tropicl svnn ecosystems (for exmple, Weinmnn 1938; Brockington 1961; Normn 1966), including severl tht investigted the effects of either fire or domestic herivory (Brger nd others 22; Augustine 23). However, we re unwre of ny study of svnn ecosystem designed to investigte the interctive effects of fire nd ntive nd domestic herivores. Also, most studies hve focussed on N nd sometimes P, nd the extent to which ctions such s potssium my lso limit plnt production is not known. However, the concentrtions of ctions in svnn vegettion re typiclly low, nd re

3 Nutrient Limittion in Svnn 993 known to e fctor influencing food selection y lrge herivores (McNughton 1988, 199). The im of this study ws to investigte the type of nutrient limittion in different types of humid svnn vegettion in Sdni Ntionl Prk, Tnzni. We selected five contrsting types of vegettion which from our conceptul frmework (compre Figure 1B) we predicted would differ with respect to soil N pool nd N:P-stoichiometry. These vegettion types were: forest gps, tllgrss svnn, Acci woodlnd, surroundings of former cttle pddocks nd lwns grzed y wild ungultes. In ech of these vegettion types, we mesured the soil N pools nd performed fctoril fertiliztion experiment to determine ptterns of nutrient limittion. METHODS Study Are The study re is locted in Sdni Ntionl Prk on the Tnznin cost (5 43 S, E). The northern prt of the ntionl prk ws operted s cttle rnch from 1954 to 2 with up to 13, hed of cttle on pproximtely 46 km 2. The southern prt ws gme reserve from 1969 until it ecme ntionl prk in 22. The re is grzed y wild herivores including wrthog, wteruck, reeduck, ufflo, wildeeest, girffe nd elephnt. Densities nd diversity of wild herivores re much higher in the southern prt of the prk compred to the former rnch re (Treydte nd others 25). Men nnul temperture recorded t the former rnch complex is 25 C ( ). Annul precipittion from 1957 to 1998 hs rnged from 61 to 1,7 mm, with men of 1,4 mm. The wet seson lsts from Mrch until June, nd there is short riny seson from mid-octoer to mid- Novemer. The driest months re Jnury nd Ferury nd August nd Septemer, nd during these periods fires re common, mny of them eing strted deliertely y the locl people. The reltively nutrient-poor soils consist of greyish, fine or lomy snd in the flts, nd reddish, lomy snd over cly on slopes nd hilltops (Klötzli 198). For more detiled description of the study re see Toler nd others (23). The vegettion of the re is dominted minly y ushlnd nd grsslnd, ut there re extensive res of evergreen forest. The nnul precipittion is sufficient to llow for 1% woody cover (Snkrn nd others 25), nd the fct tht the vegettion is now minly svnn is proly due to recurrent fires of nthropogenic origin (Bond nd others 25). We selected representtive site in ech of the following five vegettion types: (1) Gps in remnnt forest. These grss-dominted ptches re surrounded y remnnt forest nd connected to the open svnn y nrrow grss corridors. Becuse fires rrely rech these res ( conclusion sed on eril photogrphs nd personl oservtions), they served s reference for the more frequently urnt vegettion types. The site selected ws dominted y the grsses Sporoolus pyrmidlis nd Schoenefeldi trnsiens, nd the sedge Aildgrdi triflor. The vegettion ws 5-cm tll with flowering tillers reching to 1.5 m; the verge sl cover ws 85%. (2) Tllgrss vegettion. This type of vegettion is known to e the most frequently urnt due to its high iomss (Frost nd Roertson 1987), nd we predicted tht it would hve the gretest cumultive nutrient losses, especilly of N. The site chosen ws dominted y the grsses Hypertheli dissolut, Diheteropogon mplectens nd Andropogon schirensis. Vegettion ws 2-m tll, nd sl cover ws 7%. (3) Acci woodlnds. This open woodlnd hs developed from tll grss communities s result of cttle grzing (Toler nd others 23); compred to the tll grss svnn, we expected it to e reltively N-rich ecuse of symiotic N 2 -fixtion. At the chosen site, there were scttered trees of Acci znziric 6-m high nd with sl re of 1.3 m 2 /h. A. znziric trees were nodulted (P.G. Cech, personl oservtion), nd d 15 N dt indicted tht they derived pproximtely 58% of their N from fixtion (Cech 28). The understory ws dominted y the grsses Heteropogon contortus, Pnicum infestum nd Digitri milnjin nd the sedge A. triflor. This lyer ws 6-cm tll, nd sl cover reched 9%. (4) Pddock mrgins. The former pddocks ( oms ), which were used until 2 to hold the cttle overnight, nd their surroundings, were very nutrient enriched. We predicted these res would e reltively P-rich due to lrge N- losses from mmoni voltiliztion. The site selected ws dominted y the grsses Ergrostis super nd D. milnjin nd the sedge Cyperus ulipes. Vegettion height ws 6 cm nd sl cover 1%. (5) Grzed lwns. Grzed ptches (sensu Archild nd others 25) re loclized res of intensive grzing tht re not continuously mintined y wild herivores. We explicitly ssumed tht

4 994 P. G. Cech nd others wild herivores not only et the vegettion, ut lso deposit dung nd urine in these ptches. In support of this ssumption, we found much more dung in grzed lwns thn in the other vegettion types where dung counts were mde (tllgrss svnn, Acci woodlnd, medium height svnn) (Cech 28). Therefore we expected grzed ptches to e generlly nutrient-rich (though less so thn the pddock mrgins) nd with reltively high levels of P compred to N. We selected n re where vegettion dominted y the grsses D. milnjin, D. mplectens nd P. infestum hd een mintined t less thn 1-cm height y wild herivores for t lest 12 months (P.G. Cech, personl oservtion). During the riny seson prior to the strt of our experiment, however, grzing pressure decresed, nd t the strt of the experiment the vegettion ws 4-cm tll nd hd sl cover of 95%. The first four sites were locted on sndy soil in the re of the former cttle rnch. The grzed lwn ws on similr sndy soil in the southern prt of the ntionl prk where wild herivores were much more undnt. Experimentl Design nd Tretments The experiment ws strted t the end of the wet seson in June 26. At ech site we set up n experimentl plot in ptch of homogeneous vegettion. Plots comprised 3 locks of 1 m 2 seprted from ech other y 1 m uffer zones, nd were surrounded y 1.5-m tll fence to exclude smll nd lrge mmml herivores. Blocks were rndomly ssigned to one of six nutrient tretments: control, N, P, N nd P (N + P), ctions (+ctions) nd ll nutrients (N + P + ctions). Ctions ws comintion of the mcronutrients K, C nd Mg, nd the micronutrients Fe, Mn, Zn, B, Cu nd Mo. The rtionle for this tretment ws to determine whether production ws limited y nutrient other thn N or P. N ws supplied s NH 4 NO 3 t 2 g/m 2, P s N 2 HPO 4 t 5 g/m 2, potssium s KCl t 5 g/m 2, clcium s CCl 2 t 5 g/m 2 nd mgnesium s MgSO 4 t 1.4 g/m 2. These supply levels were sufficiently high to offset growth limittion without eing toxic (Augustine nd others 23), nd re similr to those used in other fertiliztion experiments in comprle ecosystems (reported in Tle 3). The micronutrients, in the form of oxides or minerl slts of chloride or sulphte, were supplied in the sme proportions reltive to N s re used in Hoglnd s solution. Nutrient ddition ws split into two pplictions of 1.5 l of queous solution; one hlf ws dded t the strt of the experiment nd the second 2 weeks lter. Becuse the topsoil hd ecome visily drier y the second ppliction of nutrients, infiltrtion ws improved y wetting the soil with 1.5 l of wter efore dding the nutrient solution. Control locks received n equivlent mount of wter only. Hrvest nd Chemicl Anlyses Before the first ppliction of nutrients, locks were clipped to 3-cm height nd the hrvested iomss ws weighed. Regrowth ws hrvested fter 46 dys nd gin fter 172 dys, nd dried to constnt weight. Biomss smples from control locks nd those receiving the complete nutrient dressing were ground, nd nlyzed for N nd P concentrtions fter Kjeldhl digestion. Totl N nd P concentrtions in the digests were mesured y mens of continuous flow injection nlyzer (FIAStr, Foss Tector, Högnäs, Sweden). A second susmple ws extrcted with.5 M HCl nd nlyzed for K, C nd Mg concentrtions, using tomic sorption spectrometry (Hunt 1982) (SPECTRAA 24 FS, Vrin AG, Zug, Switzerlnd). Soil smples (2.8-cm dimeter cores, top 1-cm soil) were tken t the strt of the experiments (one mixed smple of five cores per site), nd t the second hrvest (one core per unfertilized control lock; five replictes per site). The mixed smples were used for K, C nd Mg nlyses; totl C nd N s well s extrctle N nd P were determined on soil cores tken t the second hrvest. Totl C nd N were mesured on dry comustion nlyzer (CN-2, LECO Corp., St. 2- Joseph, Minnesot, USA). Soil extrctle PO 4 ws determined y extrction of 5 g of fresh soil with 5 ml Bry-2 solution (Bry nd Kurtz 1945). Exchngele NH + 4 nd NO - 3 were determined y the extrction of 1 g fresh soil in 5 ml.2 M KCl solution. Extrction ws done within 12 h of collection of the soil cores. KCl-extrcts were cidified with 5% H 2 SO 4 for conservtion until nlysis. Concentrtions of PO 2-4,NO - 3 nd NH + 4 in the extrcts were mesured colorimetriclly using continuous flow injection nlyzer (FIAStr, Foss Tector, Högnäs, Sweden). K, C nd Mg were mesured y tomic sorption spectrometry from 1 M mmonium cette extrcts (Crter 1993) (SPECTRAA 24 FS, Vrin AG, Zug, Switzerlnd). Rinfll, temperture nd reltive humidity were recorded with tipping ucket rin guges nd dt

5 Nutrient Limittion in Svnn 995 loggers (HOBO RG3-M, HOBO H8 Pro, Onset Computer Corp., Bourne, Msschusetts, USA) t two loctions: one in the northern nd one in the southern prt of the ntionl prk t proximity of the experimentl plots. During the wet seson prior to the experiment, the northern prt hd received pproximtely 63 mm of precipittion nd the southern prt 43 mm. From the strt of the experiment until the first hrvest on dy 46, cumultive rinfll ws 3 mm in oth prts of the ntionl prk. Between the first nd the second hrvest on dy 172, precipittion mounted to 48 mm in the north nd 28 mm in the south. During the experiment, men dily temperture nd men dily reltive humidity were 24.9 C nd 88% in the north, nd 25.7 C nd 79% in the south. Sttisticl Anlysis Sttisticl nlysis ws crried out with JMP 6..3 (SAS Institute, Cry, USA). Soil nd vegettion chrcteristics (including concentrtions nd rtios of N, P, K, C nd Mg) of the five study sites were compred using one-wy ANOVAs, with site s the fixed effect. Differences in oveground iomss production etween nutrient tretments were tested with one-wy ANOVAs, with nutrient tretment s fixed effect with six levels. Between-site differences in concentrtions nd rtios of N, P, K, C nd Mg in oveground iomss of control plots were tested with one-wy ANOVAs, with site s fixed effect. If ssumptions of normlity nd homoscedscity were not fulfilled, dt were log or squre-root trnsformed. Multiple comprisons were mde with the Tukey-Krmer HSD test (P <.5). Additionlly, the effect of fertilizer tretment on nutrient concentrtions in oveground iomss ws tested for ech site y compring concentrtions nd rtios of N, P, K, C nd Mg etween control plots nd plots receiving N + P + ctions, using t-test ssuming unequl vrinces. RESULTS Soil Nutrients Men vlues of totl N in the top 1 cm soil vried mong sites y fctor of more thn 4, from.24 in the tllgrss svnn plot to 1.7 mg g -1 in the forest gp (Tle 1). The second highest N pool ws in the secondry Acci woodlnd, ut this ws only 6% of tht in the forest gp. Vrition mong sites in the N pool prlleled vrition in the topsoil C pools (Tle 1), nd C:N rtios were similr t ll sites (men vlues rnged from 14. to 14.7, no significnt differences) except the pddock mrgin where they were significntly lower (men 11.4). Men extrctle inorgnic N vried y fctor of round 2, with high vlues in the forest gp nd the pddock mrgin (.34 nd.36 mg g -1, respectively) nd lowest vlues in the grzed ptch (.17 mg g -1 ; Tle 1). The men concentrtions of extrctle P vried fivefold mongst sites, eing highest in the pddock mrgin (.88 mg g -1 ), nd 4% lower in the grzed ptch; this in turn hd significntly higher P concentrtions thn the other three types of site ( mg g -1 ). Nutrient Limittion of Biomss Production Biomss production in the control tretments rnged from 23 in the grzed ptches to 1 g m -2 in the pddock mrgin t the first hrvest (46 dys), wheres the corresponding yields t the second hrvest (172 dys) were 94 nd 286 g m -2, respectively (Figure 2). At the second hrvest, when there ws mrked growth response t ll sites, the lowest men N concentrtions in regrowth were in the tllgrss svnn, wheres the highest vlues were in the forest gp nd Acci woodlnd (Tle 2). Men P concentrtions rnged more thn threefold, eing lowest in the Acci woodlnd nd highest in the pddock mrgin. As result, N:P rtios in the regrowth on control plots rnged widely, from 4.8 in the pddock mrgin to 16.7 in Acci woodlnd (second hrvest, Tle 2). In the forest gp plot, none of the nutrient tretments hd significnt effect upon regrowth t the first hrvest, ut production t the second hrvest ws incresed y the comined ddition of N, P nd ctions (Figure 2). The increse in iomss production cused y the ddition of N + P ws on verge equl to the increse oserved y the N + P + ctions tretment, ut it ws sttisticlly not significntly different from the control due to the lrge vrition (Figure 2). Strictly speking, these results therefore led to the conclusion tht growth ws co-limited y N, P nd ctions; however, in view of the high verge response to N + P we interpret them s indicting N nd P co-limittion. Tissue N nd P concentrtions oth significntly incresed t the first hrvest in response to the full nutrient tretment, ut not t the second hrvest (Tle 2). In the tllgrss svnn site, production t the first hrvest ws incresed in the N + P tretment (Figure 2), wheres N + P + ctions incresed growth even more. In contrst, t the second hrvest N ddition lone ws sufficient to increse

6 996 P. G. Cech nd others Tle 1. Soil nd Vegettion Chrcteristics of the Five Study Sites in Sdni Ntionl Prk n Forest gp Tllgrss svnn Acci woodlnd Grzed ptch Pddock mrgin Totl N (mg/g) ±.1 A.24 ±.1 D.56 ±.3 B.35 ±.3 C.47 ±.3 BC Topsoil N pool (g/m 2 ) ± 13 A 33 ± 1 D 78 ± 5 B 54 ± 6 C 67 ± 4 BC Topsoil C pool (kg/m 2 ) ±.19 A.46 ±.2 D 1.11 ±.5 B.75 ±.5 C.76 ±.5 C Extrctle N (g/m 2 ) 5.34 ±.4 AB.21 ±.1 BC.24 ±.4 ABC.17 ±.4 C.36 ±.4 A Extrctle P (g/m 2 ) 5.18 ±.3 C.17 ±.2 C.15 ±.2 C.57 ±.2 B.88 ±.1 A Extrctle N:P ±.66 A 1.26 ±.7 A 1.57 ±.18 A.29 ±.7 B.43 ±.3 B Extrctle K (g/m 2 ) Extrctle C (g/m 2 ) Extrctle Mg (g/m 2 ) Bulk density (g/cm 3 ) ±.9 B 1.38 ±.12 AB 1.38 ±.15 AB 1.53 ±.15 A 1.42 ±.11 A Soil wter content t dy (g/g) 5.14 ±.2 A.17 ±.1 A.17 ±.4 A.7 ±.1 C.11 ±.1 B Soil wter content t dy 172 (g/g) 5.9 ±.1 A.11 ±.1 A.9 ±.2 A.2 ±.4 C.6 ±.1 B Totl oveground iomss t dy (g/m 2 ) ± 39 AB 543 ± 22 BC 499 ± 19 C 484 ± 18 C 671 ± 23 A Proportion of ded iomss t dy 5.76 ±.8 A.34 ±.1 BC.37 ±.8 BC.28 ±.15 C.52 ±.5 B Vlues re mens ± stndrd errors. Extrctle N: extrctle nitrte nd mmonium (.2 M KCl). Extrctle P: extrctle phosphorus (Bry-2). Extrctle K, C, nd Mg: extrctle potssium, clcium nd mgnesium determined from mixed smple of 5 pooled soil cores (1 M mmonium cette). Vlues not shring the sme letter indicte significnt differences etween sites (Tukey-HSD, P <.5).

7 Nutrient Limittion in Svnn 997 Regrowth (g m -2 ) st hrvest (dy 46) 2 nd hrvest (dy 172) Forest gp Tllgrss svnn cd c cd Acci woodlnd Grzed ptch d Pddock mrgin c c c c control N P N+P ctions N+P+ctions production significntly, nd there ws no dditionl effect of dding either P or P + ctions. Thus, production in the first period ws co-limited y N nd P, ut in the second period only y N (Figure 2). In the Acci woodlnd plot, only the ddition of oth N nd P (tht is, N + P nd N + P + ctions) incresed herceous iomss production significntly, indicting tht growth ws co-limited y cd c cd c d c c control N P N+P ctions N+P+ctions Figure 2. Aoveground iomss production in five different vegettion types s ffected y the ddition of N, P, ctions (= ll nutrients other thn N nd P) nd comintions thereof. Brs show men oveground iomss hrvested fter 46 nd gin fter 172 dys (± SE; n = 5). Brs not shring the sme letters re significntly different from ech other (Tukey-HSD, P <.5). these nutrients (Figure 2). Nutrient nlyses of oveground iomss show tht only P concentrtions incresed significntly under full nutrient supply compred to the controls (Tle 2). The Acci woodlnd hd the highest N:P rtio in iomss (Tle 2). In the grzed ptch, none of the nutrient tretments hd ny effect upon yield t the first hrvest; however, t the second hrvest there ws significnt increse in oveground iomss in the N + P tretment, nd n even greter increse in the N + P + ctions tretment (Figure 2). These results suggest tht regrowth ws co-limited y N nd P, ut only t the second hrvest. Concentrtions of N nd K in the iomss were higher in the N + P + ctions tretment t the first hrvest, wheres N nd P concentrtions were higher t the second hrvest (Tle 2). In the pddock mrgin plot, N ddition significntly incresed productivity, ut there ws no extr effect when P or P + ctions were lso dded; thus, growth ws clerly N-limited (Figure 2). The full nutrient ddition did increse tissue N concentrtions, though the effect ws only significnt t the first hrvest (Tle 2). DISCUSSION This study ws designed to test predictions out long-term effects of fire, herivory nd N 2 -fixtion on soil N, N:P-stoichiometry nd the type of nutrient limittion (Figure 1). This reserch ws conducted t five sites representtive for the studied vegettion types, with only within-site repliction. To get more generl impression of the type of nutrient limittion in these svnn vegettion types, we compred our results with dt from studies in other tropicl svnns nd forested res, which were similr to our sites with regrds to the influence of fire, herivory nd N 2 -fixtion (Tle 3). The min trends tht emerge from these comprisons re generlly consistent with our conceptul model (Figure 1B). They include: (1) tllgrss svnn or comprle vegettion types re N- limited or NP-co-limited; (2) res receiving lrge mounts of excret from wild nd domestic herivores (grzing lwns nd oms) re N-limited; (3) vegettion growing in res of clered nd urned tropicl forest is minly NP-co-limited; (4) mture tropicl forests pper to e primrily limited y P (Tle 3); (5) N 2 -fixtion tends to cuse P-limittion (Tle 3). This lst point ws supported y two pulished studies, ut we found co-limittion y N nd P in the Acci woodlnd plot. However, the

8 998 P. G. Cech nd others Tle 2. Nutrient Concentrtions nd Rtios in Aoveground Biomss t the Five Study Sites Forest gp Tllgrss svnn Acci woodlnd Grzed ptch Pddock mrgin Control N + P + ctions Control N + P + ctions Control N + P + ctions Control N + P + ctions Control N + P + ctions Dy 46 N (mg/g) 12.8 ±.5 AB 17.9 ±.1** 1.9 ±.6 B 16.7 ± 1.2** 14. ±.8 A 16.2 ± ± 1.3 A 22.8 ±.6*** 1.2 ±.6 B 14.8 ±.5** P (mg/g).86 ±.2 C 1.19 ±.3*** 1.21 ±.18 BC 2.4 ±.1**.83 ±.4 C 1.2 ±.7** 1.61 ±.12 AB 1.68 ± ±.16 A 1.88 ±.6 Potssium 6.5 ±.9 C 5.9 ± ±.5 AB 16. ±.5* 1.4 ±.9 BC 1.1 ± ± 1.4 AB 17.8 ±.3* 17.2 ± 1.4 A 18.1 ± 1.5 (mg/g) Clcium (mg/g) Mgnesium (mg/g) 3.6 ±.4 B 3.2 ± ±.2 B 3.6 ± ±.4 A 5.2 ± ±.2 B 4.2 ± ±.2 C 2.6 ± ±.2 B 1.4 ± ±. A 2.8 ± ±.1 A 2.7 ± ±.1 A 2.8 ± ±.1 B 2. ±.2 N:P 15. ±.8 A 15.1 ± ± 1.2 B 8.3 ± ±.6 A 13.6 ±.6** 9.1 ±.1 B 13.6 ±.4*** 5.5 ±.5 C 7.9 ±.2* N:K 2.1 ±.3 A 3.2 ±.3*.8 ±. CD 1. ±.** 1.4 ±.1 AB 1.5 ± ±.1 BC 1.3 ±..6 ±.1 D.8 ±.1 K:P 7.5 ± 1.1 B 5. ± ± 1.4 AB 7.9 ±.5* 12.8 ± 1.4 A 9.2 ± ± 1. AB 1.6 ± ± 1.2 AB 9.7 ± 1. Dy 172 N (mg/g) 1.6 ±.4 A 1.2 ± ±.3 C 7.4 ± ±.3 B 8.4 ± ±.3 AB 12.2 ±.3*** 8.8 ±.5 B 9.6 ±.4 P (mg/g).94 ±.13 B.97 ± ±.16 BC 1.26 ± ±.2 C.96 ±.5***.98 ±.7 B 1.72 ±.4*** 1.9 ±.11 A 2.1 ±.18 N:P 12.5 ± 2.3 AB 12.7 ± ± 1.7 BC 7.7 ± ±.5 A 8.8 ±.5*** 1. ±.4 BC 7.1 ±.1** 4.8 ±.5 C 4.8 ±.5 Vlues re mens (±SE) of five locks. Vlues of controls not shring the sme letter indicte significnt differences etween sites (Tukey-HSD, P <.5). *P<.5, ** P <.1, *** P <.1 indicte significnt differences etween control locks nd those receiving N + P + ctions.

9 Nutrient Limittion in Svnn 999 vlues for N:P rtios suggest tht N 2 -fixtion y Acci did cuse shift of N:P-stoichiometry in the direction of P-limittion (Tle 2). In ll our sites, oveground production ws limited y N or co-limited y N nd P, ut there ws no evidence of primry limittion y ny other nutrients (Figure 2). Indeed, the mjority of studies on nutrient limittion in svnn ecosystems hve ssumed tht no nutrient other thn N nd P limits productivity, lthough without testing this ssumption explicitly. It is worth noting tht nutrients were not lwys the fctor limiting growth in our experiment; thus, in the first period the nutrient tretments hd no effect upon oveground production in the forest gp or in the grzed ptch, presumly ecuse of low wter vilility. The herceous vegettion in the forest gp is likely to hve experienced drought ecuse of wter uptke y surrounding trees (Bourliere nd Hdley 1983), wheres the grzed ptch in the southern prt of the study re received significntly less rin thn the other sites (reflected in lower soil wter content t the strt of the experiment; Tle 1). Thus, lthough nutrients hve een shown to limit plnt production t nnul levels of precipittion s low s 2 mm y -1 (Penning de Vries nd others 198), the lrge sesonl fluctutions in wter vilility chrcteristic of svnns my temporlly result in wter limittion. Vrious lines of evidence suggest tht our tllgrss site, s well s mny other tllgrss svnns, is t the oundry etween N-limittion nd NPco-limittion. First, consistent with some other studies (Tle 3), production t our tllgrss site ws limited y N during the second period, ut y oth N nd P during the first period. Second, in comprle types of vegettion where N lone stimulted production, the joint ddition of N nd P lwys cused further increse in growth (Tle 3). These findings demonstrte tht esides N vilility P vilility is lso low in tllgrss svnn nd comprle vegettion. There re vrious possile explntions for low levels of P in this hitt: for exmple, losses of P through fire (lthough eing clerly less thn for N nd minly occurring in prticulte form; Cook 1994; Lclu nd others 22), or the leching of P from ncient highly wethered tropicl soils (Lmers nd others 28). At the tllgrss site, the iomss t the first hrvest ws greter in the N + P + ctions tretment thn in the N + P tretment. The fct tht the N + P + ctions tretment incresed concentrtions of potssium in regrowth ut not of clcium nd mgnesium (Tle 2) suggests tht K ecme limiting when N nd P were supplied. Indeed, the losses of K during comustion re usully found to e higher thn those of C nd Mg (Cook 1994; Vn de Vijver nd others 1999; Lclu nd others 22). The use of the tllgrss site s cttle psture etween 1954 nd 2 could hve contrsting effects upon N nd P conditions: on the one hnd it could hve incresed losses of N nd P ecuse more nutrients were ingested in this re thn were returned in excret; on the other hnd, y reducing the intensity nd frequency of fires, grzing could lso hve reduced N losses reltive to those efore the re ws grzed (Hos nd others 1991). However, ecuse concentrtions of totl N nd extrctle P in the soil of tllgrss sites in the former rnch re were similr to those in n re to the south of our study sites tht hd never een grzed y cttle (P.G. Cech nd others, unpulished dt), we conclude tht ny such effects must hve een rther smll. In contrst to the tllgrss pstures, cttle hd lrge effect upon soils in the vicinity of pddocks, which received high mounts of dung nd urine for severl decdes. Soil N pool, extrctle N nd extrctle P were higher in the pddock mrgin smples thn in the tllgrss svnn smples, the difference eing prticulrly pronounced for extrctle P (Tle 1). As predicted, iomss production in the pddock mrgin plot ws limited y N (Figure 1), with dditionl P producing no extr effect. A similr concentrtion of nutrients y livestock hs een reported for semi-rid svnn in Keny, with the effects persisting for decdes (Augustine 23). The grzed ptches in our study re were not used continuously y wild herivores, ut were ndoned if the grss grew ove criticl height; such n re would then not e grzed gin until the ccumulted iomss ws removed y fire (P.G. Cech, personl oservtion). This pttern of hitt use y wild herivores, which hs lso een oserved elsewhere (Archild nd others 25), might explin why the grzed ptch ws only modertely enriched compred to tllgrss svnn of the kind from which our grzed ptch proly developed (sed on similrity in plnt species). In the experiment, iomss production in the grzed ptch ws co-limited y N nd P t the second hrvest. There is rther little informtion on nutrient vililities in grzing lwns (s defined y McNugthon 1984) nd in temporrily grzed ptches, nd we know of no other studies investigting nutrient limittion in such res. However, McIvor nd others (25) report tht the soil in

10 1 P. G. Cech nd others Tle 3. Types of Nutrient Limittion in Tropicl Svnn nd Forest Ecosystems Vegettion type Loction Nutrient limittion Study type N:P rtio Compres est to Source Tropicl forests 62 sites worldwide P Litter NUE Forest (1) Secondry tropicl forest Amzon, Brzil P N:P rtios 28.8 Forest (2) Cerrdo sensu stricto Brzil P Litter NUE 18 Forest (3) Old secondry dry tropicl forest Yuctn, Mexico P F Forest (4) + (5) Gp in remnnt forest (FG) Tnzni NPctions F TS Young secondry dry tropicl forest Yuctn, Mexico NP F FG (4) + (5) Succession fter removl of mture tropicl forest Amzon, Brzil N or NP Modelling FG (6) Herceous cover in secondry dry forest Amzon, Brzil NP F 1.2 FG (7) Humid tllgrss svnn (TG) Tnzni N nd NP (NPctions) F TS Mesic svnn, nturl pstures Tnzni N (NP) F TG (8) Semi-rid svnn Tnzni N (NP) F 6 4 TG (9) Hyprrheni dominnt grsslnd Zmi N (NP) F TG (1) Hyprrheni dominnt grsslnd Keny N (NP) F 8.2 TG (11) Shelin C4 grsslnds Mli N? (NP) 1 F TG (12) Humid svnn, ntive pstures Austrli NP F 14.8 TG (13) Flooded svnn Venezuel NP (NPKS) F TG (14) Secondry svnn Venezuel N (NPK) F TG (15) Trchypogon svnn Venezuel N nd P (NP, NPK) F 9.8 TG (16) Trchypogon svnn Venezuel NP? 2 F 11. TG (17) Rngelnd South Afric N (NP) F TG (18) Humid svnn, secondry Acci woodlnd (AW) Tnzni NP F TS Semi-rid svnn under Acci tortilis cnopy Tnzni P F 12 4 AW (9) Overgrzed Shelin psture dominted y legume Zorni sp. Mli P 3 F 2 3 AW (12) Humid svnn, grzed ptches (GP) Tnzni NP (NPctions) F TS Grzing lwns, humid Guine svnn Cmeroon N N:P rtios 5.8 GP/PM (19) Humid svnn, soils derived from oms (PM) Tnzni N F TS Semi-rid svnn, soils derived from oms Keny N (NP) F 5.2 PM (2) Nutrient limittion: the min limiting nutrient(s) is/re reported, in rckets re nutrient comintions which further incresed iomss production compred to the min limiting nutrient(s). Study type: F, fctoril fertiliztion experiment; Litter NUE, nutrient use efficiencies s clculted from litterfll; N:P rtios, limittion ssessed ccording to reltive undnce of N nd P in plnt tissue; Modelling, model of chnges in nutrient pools upon forest clering sed on the dtset from study site. N:P rtios: clculted from N nd P concentrtions in folige of severl tree species in the cse of forests, from concentrtions in totl oveground herceous iomss, or s weighed verge from concentrtions in oveground iomss of one or severl herceous species if they represent t lest 75% of totl iomss nd their reltive undnce is known in order to prevent is due to the lrge vrition of N:P rtios mong plnt species (compre Güsewell nd Koerselmn 22). Compres est to: indictes the vegettion types from the conceptul model in Figure 1B to which the respective study site is most similr (sed on the influence of herivory, fire nd N2-fixtion). FG: forest gps, TG: tllgrss svnn, AW: Acci woodlnd, GP: grzed ptches, PM: pddock mrgin. 1 Effect of N ddition lone ws not tested, ecuse ll plots receiving vrying levels of N fertilizer were given sic P dressing first. 2 Neither N nor P ddition incresed oveground iomss in cut plots, joint ddition of oth nutrients ws not tested. 3 Ntive vegettion ws removed nd pure stnds of two grss nd four legume species were sown, N:P rtios of legume species on control plots verged 19.9 nd the N:P rtio of one grss species ws 2.7 (no dt ville for the second grss species). 4 N:P rtios were determined from young fully expnded leves of the dominnt grss species. Source: (TS) this study; see Appendix A for references.

11 Nutrient Limittion in Svnn 11 ptches of lwn formed y cttle ws enriched in P ut less so in N. This is consistent with our finding tht soil extrctle P ws enriched more in the grzed ptch reltive to the tllgrss site thn were totl nd extrctle N (Tle 1). Dt from recent study of grzing lwns in Cmeroon indicte N:P rtios in oveground iomss round 6 (Verweij nd others 26), which is lower thn wht we oserved in the grzed ptch (9 1, Tles 2 nd 3). However, those grzing lwns re continuously mintined y herivores nd my thus e expected to e more hevily impcted thn our grzed ptches. In the Acci woodlnd plot, iomss production ws co-limited y N nd P during oth growth periods. Although we did not oserve P limittion, s reported for two other svnns with N 2 -fixing legumes (Tle 3), the N:P rtio in the vegettion of the control plots suggests tht growth limittion in our Acci woodlnd ws closer to P-limittion thn in our other NP-co-limited sites (Tle 2). N 2 -fixing plnts often hve higher P requirement thn other plnts (Pte 1986), nd severl studies hve shown N 2 -fixtion in legumes to e limited y P- vilility (Isrel 1987; Crews 1993; Perreijn 22; Binkley nd others 23). N 2 -fixing plnts increse the overll vilility of N, which proly increses the demnd nd uptke of P y other plnts s well. The high P demnd of A. znziric trees nd the incresed P demnd y other plnts my thus hve reduced soil P vilility, s hs lredy een reported for nother woody legume (Binkley 1997). Thus, the high N:P rtio in herceous vegettion in the Acci woodlnd (Tle 2) ws proly due to the comined effect of incresed N nd reduced P. N 2 -fixtion my thus hve stronger effect on N:P-stoichiometry reltive to its effect on N-ccumultion thn ws hypothesized in Figure 1. Additionlly, the herceous cover of the Acci woodlnd is urnt occsionlly (P.G. Cech, personl oservtion), which my slow down the ccumultion of N in the soil. In the forest gp, which ws selected s the reference for the other vegettion types, iomss production tended to e co-limited y N nd P during the second growth period (Figure 2). Undistured tropicl forests re thought to e most commonly limited y P ecuse of the dvnced wethering of soils (Vitousek 1984), nd there is some experimentl evidence supporting this view (Tle 3; Elser nd others 27), lthough t the level of individul trees the picture might e more complex with some trees limited y N nd others y P (Perreijn 22). We expected tht, strting from P-limited undistured forest conditions, urning would led in the direction of N-limittion (compre Kuffmn nd others 1995; Bustmnte nd others 26) nd hence frequently urned sites (like tll grss svnn) would e N-limited, nd less frequently urned sites (like forest gps) would hve n intermedite position etween P- nd N- limited conditions. The responses of re-growth to nutrient ddition in the forest gp were thus in line with our hypothesis tht where fire is infrequent the nutrient lnce lies in the rnge of NP-colimittion. A reltively high totl-n:totl-p rtio of 19 in the soil of remnnt forest ner our forest gps indicted tht the originl forest might indeed hve een P-limited (P.G. Cech, unpulished dt). The shift from P-limittion towrds N-limittion following the removl of tropicl forest is lso supported y other studies (see Tle 3). Our conceptul frmework of the effects of fire, herivory nd N 2 -fixtion on soil N pool nd N:Pstoichiometry (Figure 1) ws supported y good mtch etween the hypothesized rrngement of the investigted vegettion types nd mesured soil N pools nd N:P-stoichiometry (represented y the N:P rtio in the oveground vegettion) (compre Figures 1B nd 3). In the cse of the Acci woodlnd nd the grzed ptch mesured N:P rtios devited from our predictions, we hve discussed possile cuses for these devitions ove. The dt on soil N pools lso support the conceptul frmework in vrious wys. First, the site tht hs proly urnt most frequently the tllgrss svnn (Frost nd Roertson 1987; P.G. Cech, personl oservtion) hd the lowest soil N pool (Figure 3, Tle 1). This result is in line with lower soil N reported for long-term urning experiments (Ojim nd others 1994; Fynn nd others 23). Secondly, the loclized return of dung nd urine y domestic nd wild herivores incresed soil N in oth the grzed ptch nd the pddock mrgin. Enrichment of soil N y domestic herivores hs lso een demonstrted in semi-rid svnn (Augustine 23). Thirdly, the secondry Acci woodlnd hd significntly higher mounts of soil N thn the tllgrss svnn, the grzed ptch or the pddock mrgin (Tle 1, Figure 3). Severl studies report tht woody legumes invding grsslnds increse totl soil N nd N vilility, these effects eing ttriuted t lest prtly to their ility to fix tmospheric N 2 (Stock nd others 1995; Geesing nd others 2; Archer 21; Hgos nd Smit 25; Scherer-Lorenzen nd others 27). Finlly, the forest gp hd the lrgest soil N pool (Tle 1), which my e explined y low fire frequency nd possily y the N input from tree litter (Hudk nd others 23). The correltion

12 12 P. G. Cech nd others N:P rtio in vegettion A B TG TG GP GP PM PM AW AW Soil N pool (g m -2 ) Figure 3. Totl soil N in topsoil nd N:P rtios in oveground iomss of five sites in Sdni Ntionl Prk: forest gp (FG), tllgrss svnn (TG), secondry Acci woodlnd (AW), grzed ptch (GP), pddock mrgin (PM), t the first hrvest (A) nd the second hrvest (B). Open symols indicte tht N:P rtio in vegettion my not e good indictor of nutrient limittion, ecuse wter ws likely the limiting resource. Dt re shown s men per site nd error rs represent stndrd errors (n = 5). etween soil N nd C pools (Tle 1) suggests tht the loss nd ccumultion of N is closely ound to the loss nd ccumultion of orgnic mtter. The rtio of N:P in the oveground herceous vegettion hs een used to ssess nutrient limittion in temperte ecosystems (Koerselmn nd Meulemn 1996; Olde Venterink nd others 23; Güsewell 24). Koerselmn nd Meulemn (1996) proposed tht t N:P rtios elow 14, productivity ws limited y N, etween 14 nd 16 production ws co-limited y N nd P, nd ove 16 limited y P. Whether NP-co-limittion cn e seprted from P- limittion sed on N:P rtios is not fully cler (see Olde Venterink nd others 23), ut the level of less thn out 14 for N-limittion is consistent nd supported y other studies in temperte regions (Olde Venterink nd others 23; Güsewell 24). For dry svnn, Ludwig nd others (21) reported vrition in N:P rtios mong growing sesons, nd the results of fertiliztion experiment did not support the predicted type of limittion sed on criticl vlues of N:P from temperte regions. They FG FG suggested tht the criticl N:P vlues for the oundries etween N-limittion nd NP-co-limittion should e t 6 for svnn vegettions, nd tht etween NP-co-limittion nd P-limittion t 12. As possile explntion, they suggested the higher N use efficiency of C 4 grsses compred to C 3 plnts. However, it should e noted tht N:P rtios reported in the study of Ludwig nd others (21) were mesured from young, fully expnded leves of the dominnt grss species nd not from oveground iomss. From our dt, we suggest tht the criticl N:P rtio reflecting the trnsition from N- limittion to NP-co-limittion lies etween 8.6 nd 1. (compre type of nutrient limittion s determined y fertiliztion, nd N:P rtios of the control plots for the plots not limited y wter; Figure 2 nd Tle 2). If P-limittion nd NP-co-limittion cn e seprted y N:P rtios, the criticl oundry vlue should e higher thn These rnges come close to the oundries vlues of 6.7 nd 2.4 given y Penning de Vries nd others (198) for Shelin grsslnds. Considering the dt ville from literture, we conclude tht the criticl N:P vlue indicting N-limittion in tropicl svnns is proly less thn out 9; this vlue is less thn the elow 14 determined for temperte regions, ut N:P rtio in vegettion N N&P P Limiting nutrient Figure 4. N:P rtios versus type of limittion in oveground herceous vegettion of tropicl svnns. N:P rtios re from unfertilized control plots nd type of limittion ws determined y fertiliztion experiments (dt from Tle 3). Open circles show dt for which N:P rtios represents t lest 75% of oveground herceous iomss, solid circles show dt from Ludwig nd others (21) who mesured N:P rtios in young fully expnded leves of the dominnt grss species.

13 Nutrient Limittion in Svnn 13 more thn the less thn 6 mentioned y Ludwig nd others (21) (Figure 4). We gree with Ludwig nd others (21) tht the difference compred with temperte ecosystems is proly due to the very high N use efficiency of tropicl C 4 grsses (Sge nd Percy 1987; Le Roux nd Mordelet 1995). ACKNOWLEDGEMENTS This study ws finnced y the Swiss Ntionl Science Foundtion grnt No We thnk Prof. S.L.S. Mgng, Mrkus Schneider- Mmry nd the uthorities of Sdni Ntionl Prk for their logisticl support in Tnzni, nd Benjmin Donld, John Willims nd Hmis Willims for their ssistnce in the field. We lso cknowledge comments provided y Michel Scherer-Lorenzen, D.A. Frnk nd two nonymous reviewers tht helped to improve this mnuscript. REFERENCES Arnir JN, Otter L, Mcko SA, Ferl CJW, Epstein HE, Dowty PR, Eckrdt F, Shugrt HH, Swp RJ. 24. Nitrogen cycling in the soil-plnt system long precipittion grdient in the Klhri snds. 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