Artigo Savana Floresta Plant Soil

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Can savannas become forests? A coupled analysis of nutrient

stocks and fire thresholds in central BrazilLucas C. R. Silva &William A. Hoffmann &Davi R. Rossatto &

Mundayatan Haridasan &Augusto C. Franco &William R. Horwath

Received: 18 March 2013 / Accepted: 17 June 2013 / Published online: 27 July 2013# Springer Science+Business Media Dordrecht 2013

Abstract

Aims The effects of fire ensure that large areas of theseasonal tropics are maintained as savannas. The ad-vance of forests into these areas depends on shifts inspecies composition and the presence of sufficientnutrients. Predicting such transitions, however, is dif-ficult due to a poor understanding of the nutrient

stocks required for different combinations of speciesto resist and suppress fires.

Methods We compare the amounts of nutrients re-quired by congeneric savanna and forest trees to reachtwo thresholds of establishment and maintenance: thatof fire resistance, after which individual trees are largeenough to survive fires, and that of fire suppression,after which the collective tree canopy is dense enoughto minimize understory growth, thereby arresting thespread of fire. We further calculate the arboreal and

soil nutrient stocks of savannas, to determine if theseare sufficient to support the expansion of forests fol-lowing initial establishment.

Results Forest species require a larger nutrient supplyto resist fires than savanna species, which are betterable to reach a fire-resistant size under nutrient limi-tation. However, forest species require a lower nutrientsupply to attain closed canopies and suppress fires;therefore, the ingression of forest trees into savannasfacilitates the transition to forest. Savannas have suf-ficient N, K, and Mg, but require additional P and Ca

to build high-biomass forests and allow full forestexpansion following establishment.Conclusions Tradeoffs between nutrient requirementsand adaptations to fire reinforce savanna and forest asalternate stable states, explaining the long-term persis-tence of vegetation mosaics in the seasonal tropics.Low-fertility limits the advance of forests into savan-nas, but the ingression of forest species favors theformation of non-flammable states, increasing fertilityand promoting forest expansion.

Plant Soil (2013) 373:829842DOI 10.1007/s11104-013-1822-x

Responsible Editor: Michael Denis Cramer.

Electronic supplementary material The online version of this

article (doi:10.1007/s11104-013-1822-x) containssupplementary material, which is available to authorized users.

L. C. R. Silva (*) :W. R. HorwathDepartment of Land, Air and Water Resources,University of California,Davis, CA 95616, USAe-mail: [email protected]

W. A. HoffmannDepartment of Plant Biology,North Carolina State University,Raleigh, NC 27695, USA

D. R. RossattoDepartamento de Biologia Aplicada, FCAV, UniversidadeEstadual Paulista Jlio de Mesquita Filho-UNESP,14884-900 Jaboticabal, SP, Brazil

M. HaridasanDepartamento de Ecologia, Universidade de Braslia,70910-900 Braslia, DF, Brazil

A. C. FrancoDepartamento de Botnica, Universidade de Braslia,70910-900 Braslia, DF, Brazil
http://dx.doi.org/10.1007/s11104-013-1822-xhttp://dx.doi.org/10.1007/s11104-013-1822-x


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Keywords Cerrado . Ecosystem dynamics .

Fire . Forest expansion .Nutrient cycling . Soil-plantinteractions . Succession . Tradeoffs . Tropics

Introduction

Over the past few thousand years, expansion of forestsinto savannas and grasslands has occurred in many

parts of South America, a phenomenon that has beengenerally attributed to climate fluctuations (Behling etal.2005; Silva et al. 2008,2011; Dumig et al. 2008;Silva and Anand2011). Savannas, however, continueto persist over large areas where climatic conditionsare adequate to support forests (Lehmann et al.2011).In some of these areas, transitions to forest dependupon shifts in tree species composition (Geiger et al.

2011; Ratnam et al.2011; Silva and Anand2011), butpredicting these is complicated by interacting effectsof fire and soil nutrients on forest and savanna species.

In dry tropical regions, climate alone prevents thedevelopment of forests (Sankaran et al. 2005), butthroughout mesic savannas (i.e., regions where annual

precipitation >800 mm), gradual forest expansion mayoccur upon fire suppression (Hopkins 1965; Duriganand Ratter2006; Pinheiro et al.2010), and vegetationmosaics commonly coincide with edaphic gradients(Furley et al. 1992; Silva et al. 2008, 2010a, b). In

central Brazil, for example, savanna vegetation is typ-ically found over nutrient-poor oxisols, dominatingthe landscape, while disjunct forests are found in areasof high soil fertility, such as riverbeds and limestoneoutcrops (Guido et al. 2002; Gottsberger andSilberbauer-Gottsberger2006; Furley2007). Despitethese associations, the extent to which soil nutrientsand fire limit forest development is not well resolved.

Nutrient-poor soils may support savanna becauseavailable pools of essential nutrients are simply insuf-ficient to construct high tree biomass or, alternatively,

nutrient pools may be sufficient to construct forestbiomass (Bond2010), but savannas persists becausegrowth rates are too low to overcome rates of biomassloss caused by fire (Lehmann et al.2011; Hoffmann etal.2012a,b).

In either case, to determine how fire interacts withnutrient availability to govern the distribution of forestand savanna, it is important to consider two thresh-olds. The first threshold marks the point at which anindividual tree becomes large enough to reliably avoid

fire damage and topkill (i.e., stem death), which werefer to as the fire-resistance threshold. The secondthreshold marks the point beyond which the vegeta-tion achieves sufficient foliage to exclude shade-intolerant understory vegetation (Hoffmann et al.2012a). The absence of savanna understory vegetation

(mostly grasses) greatly reduces ecosystem flamma-bility (Hoffmann et al.2012b), so we refer to this asthe fire-suppression threshold. The ability of trees toreach these thresholds is regulated by their growthrate, which is at least in part dependent on resourceavailability. Moreover, the accumulation of biomassnecessary to surpass these thresholds requires substan-tial uptake of nutrients from soils and if the requiredstocks are large relative to availabilities in the envi-ronment, transitions to forest would be unlikely.

It has long been hypothesized that vegetation of

dystrophic soils are inherently more fire-prone thanvegetation of fertile soils, because of the slow rateson which trees establish under limiting conditions(Kellman1984). To determine whether this hypothesisholds, we must consider savanna and forest tree spe-cies as separate functional types, evaluating whethernutrient stocks needed to resist or suppress fires de-

pend on intrinsic species traits. Savanna species pro-duce thick bark, which allows stems to become fireresistant at a smaller size (Hoffmann et al. 2012a).Forest species, on the other hand, produce greater leaf

area (Rossatto et al. 2009), and are more effective atgenerating a closed fire-suppressing canopy. If thesecontrasting traits translate into differences in nutrientsrequirements for reaching the fire-resistance and fire-suppression thresholds, interacting effects of speciescomposition and soil fertility would be the key to

predict forest expansion/contraction.To test for such differences, here we: (i) compare

the nutritional requirement of forest and savanna treesgrowing under similar (nutrient-poor) conditions atfire-resistance and -suppression thresholds; and (ii)

estimate total arboreal (stem and crown) and soil nu-trient stocks of savannas and four different types ofinterspersed forests that co-exist in central Brazil, todetermine whether nutrient stocks in savanna ecosys-tems are sufficient to support a transition to forest. Weaddress these objectives describing how nutrientrequirements and adaptations to fire disturbance inter-act, elaborating on whether nutrient availability impo-ses a definite constraint on forest distribution in mesicsavanna regions.

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Material and methods

Study sites

The present study combines some of our previouslypublished and unpublished data from forests and sav-

annas of central Brazil. Our sites are located within 20km from the urban limits of Brasilia, in the BrazilianFederal District at altitudes of ca. 1,100 m above the sealevel. At all sites, the average annual temperature andrainfall are about 22.5 C and 1,400 mm, with most ofthe precipitation occurring during the (southern) sum-mer. Despite similar climatic conditions, our study sitesencompass vegetation gradients from open grasslands todense forests. We focused on typical savannas and ad-

jacent forests, delimited by sharp (few meters wide)boundaries, where structural parameters (Fig. 1) and

species composition have been well described.Our datasets were obtained at fire-protected areas that

include three savanna and four forest sites. The selectedsavannas represent the regionally dominant (cerrado

sensu stricto) vegetation, with 2030 % tree cover anda continuous grass layer, established over deep dystro-

phic oxisols (Furley1999). These savannas have per-sisted for several thousands of years in close proximityto forests (Silva et al. 2008,2010a) with no apparentlimitation imposed by soil physical properties (e.g. tex-ture, density, depth of water table, etc.). The selected

forest sites represent two riparian, one xeromorphic andone deciduous forest. Riparian forests, adjacent to twoof the savanna sites, are located at the EcologicalReserve of the Institute of Geography and StatisticsRECOR-IBGE (1556S and 4756W). These forestswill be referred to asdryand wetriparian forests, asthey occur along a well-drained and a seasonallyflooded riverbed respectively. The xeromorphic forest(locally known as cerrado), adjacent to our third sa-vanna site, is located at the EMBRAPA ResearchReserve (1536S and 4742 W). The deciduous forest

is located at the preservation area of CIPLAN MiningCompany (1533S and 4751W). Savannas are presentat this last site but are associated with unusually shallowsoils and abundant calcareous concretions and, for thisreason, were not included in our analysis.

Sampling design

To compare the nutritional requirements of savanna andforest trees under the same environmental conditions,

we sampled 18 pairs of tree species, each consisting ofone forest and one savanna species of the same genus.To classify each species into forest or savanna types, wefollowed the same criteria used by Hoffmann et al.

Fig. 1 Leaf area index (Silva et al. 2008,2010a), tree density,number of tree species and total basal area (Fonseca and SilvaJunior2004; Silva Jnior2004, 2005; Ribeiro and Haridasan1984; Haidar 2008) at each studied site. These parametersrepresent ecosystem-wide estimates and therefore have no asso-ciated errors

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(2005) and Rossatto et al. (2013), based on morpholog-ical attributes, herbarium comparisons and previously

published floristic surveys (Mendona et al. 2008).Generally, the evolutionary history of each species in-fluence trait variability (Hendry et al. 2011) and phylo-genetic differences often appear correlated with resource

use strategies and biomass allocation (e.g. Burns andStrauss2012) in plant communities. Here, all 18 conge-neric pairs (Supplementary information) were sampledunder nutrient-poor (savanna) conditions. Each of these

pairs belongs to a different botanical family, ensuringphylogenetic independence when comparing speciesattributes and nutrient stocks in relation to their ecosys-tem of origin (forest or savanna).

Additionally, we sampled species that occur in bothforest and savanna environments, to compare nutrientrequirements of these species across ecosystems. Most

of these species were the same forest species sampledin savannas for the congeneric comparison describedabove, but we also sampled five additional species thatcould be found in both ecosystem types, namely:

Agonandra brasiliensis, Copaifera langsdorfii, Qualeagrandiflora,Kielmeyera coriacea, and Myrcia tomen-tosa; sampling a total of 17 species common to forestsand savannas (Supplementary information) for thiscomparison.

These two sets of data permitted the analysis ofdifferences between savanna and forest trees growing

in a common environment (savanna), as well as bet-ween different forests and savanna environmentsusing tree species common to both ecosystems.

Plant collection and analysis

During May and June of 2007, we collected leafand wood samples from three to five individualtrees per species at each site where a species was

present. All sampled trees had stem diameters great-er than 10 cm. From every individual we collected

fully expanded mature leaves from the outer (sunlit)portion of the crown and wood cores at approxi-mately 1.3 m above the ground level. We deter-mined the specific leaf area (SLA), wood density,leaf and wood N, P, K, Ca, Mg concentrations, ofall sampled trees. Prior to analyses, plant sampleswere washed with distilled water, dried at 80 C,and milled to a particle size of


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(Hoffmann et al. 2012a, b). We estimated the vege-tation nutrient pools at this threshold using the arbi-trary condition in which all trees have a stem diam-eter of 10 cm. According to intrinsic differences instem vs. crown biomass allocations between forestand savanna trees (Fig. 2a), the corresponding leaf

areas (5.57 m2

for savanna and 16.61 m2

for forest)determine the estimated tree density (5,400 and1,800 ha1) necessary to attain the fire-suppressionthreshold (LAI of 3 or 30,000 m2 ha1).

Comparisons of savanna and forest environments

For each of our study sites, we estimated totalabove-ground nutrient stocks, scaling from individ-ual trees to the ecosystem level, by combining

estimates of wood and canopy biomass. Due toinherent variations in the structure of predominanttrees, different allometric equations are typicallyused to quantify wood biomass of forest and savan-na ecosystems. Forest-calibrated equations generallyunderestimate savanna biomass, while savanna-calibrated equations tend to overestimate forest bio-mass. To address this issue and yield comparablevalues, we used two different allometric equations,one calibrated to savanna and another to forest trees(Brown et al. 1989; Delitti et al. 2006), reporting

the average values of these calculations:

WBexp 3:114 0:972ln D2H

WB 28:77D2H=1000

where WB (kg ha1) represents wood biomass, giv-en the average stand height H (m) and diameter D(cm), calculated from total basal area and tree den-sity at each ecosystem (Fig. 1).

Ecosystem level canopy biomass and nutrientstocks were estimated using measurements of total leaf

area index (LAI) at each site (Fig.1). Because LAI is adimensionless ratio of leaf area covering a unit ofground area (m2/m2), we used SLA measurements toestimate total leaf biomass. Since SLA represents totalarea per mass of leaf (cm2 g1), the ratio between LAIand SLA provides an integrated estimate of total leafmass per unit of ground area. Based on biomass esti-mates and measurements of leaf nutrient concentrationwe calculated whole canopy nutrient stocks, presen-ting results as average values obtained using data fromall studied species.

Wood and canopy biomass are expressed as totalmass of carbon per hectare, accounting for variationsin wood density and SLA, and assuming carbon con-tent to be 50 % of the total dry mass. We did not useherbaceous strata in these calculations.

Soil collection and analysis

We used 15 composite soil samples (five subsampleseach), collected at the top 020 cm depth, to charac-terize the surface soil fertility at each site (three savan-

nas and four forest sites). We also characterized deepsoils by pressing 100 cm3 tubes into 10 cm layers ofsequentially dug soil pits, up to 100 cm depth, in soil

profiles evenly distributed across forest-savanna

Fig. 2 Allometric relationships between tree diameter leaf areaand bark thickness, measured in forest and savanna speciesnaturally occurring in savannas. a Fire-suppression threshold,defined by total leaf area, determined using data compiled fromseedlings saplings, and adults (Gotsch et al.2010) of forest andsavanna species. b Fire-resistance threshold, defined by

diameters at which bark thickness prevents tree mortality (Hoff-mann et al.2009,2012a) at high and low fire intensity scenarios.In both panels each point represents a single individual tree andregression lines represent significant relationships (Pearsonscorrelation;p


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transitions. Tubes were inserted so that pressure wasonly exerted on the tube walls, thereby preventing soilcompaction and overestimation of soil bulk density.Ten such profiles were sampled at each transition,totaling 15 profiles in savannas and five at each forestecosystem.

We analyzed soil samples for density using the drymass of soil samples, and estimated total stocks ofcarbon and nutrient in mass per hectare. We deter-mined total N concentration in soils using theKjeldahl method (Bremner and Mulvaney 1982).Levels of P, K, Ca and Mg were determined by atomicabsorption spectrophotometry using extraction meth-ods (Mehlich and KCl) that allow the measurement ofconcentration of nutrients available to plants. Totalorganic carbon content was analyzed by wet oxidation(Walkley and Black1934). Carbon levels and nutrient

stocks are expressed on a mass basis, after accountingfor variation in soil density, in the surface soil layer(020 cm depth) and integrated to 100 cm depth in soil

profiles.The amount of a given nutrient existing (or miss-

ing) for building a forest was determined by the dif-ference between savanna biomass and soil stocks up to100 cm depth, and in the above-ground biomass ofeach forest ecosystems. Nutrients contained in theunderstory vegetation or root biomass were not inclu-ded in our calculations, but their potential relevance is

discussed.

Results

Savanna: Leaf and wood nutrients as determinedby species origin

When growing in the same environment (savanna),leaves of forest tree species have significantly higherconcentrations of N (23 %), P (25 %), and K (47 %),

but lower levels of Ca (18 %), than savanna species(Table1). Leaf levels of Mg do not differ significantlyaccording to species origin. Forest trees have signifi-cantly greater SLA (27 %), but wood density does notdiffer in relation to species origin. Similarly, mostwood nutrients (P, K, Ca and Mg) show no significantdifferences between forest and savanna trees.Significant differences only occur in wood N concen-trations, which are higher in savanna than in foresttrees (Table1).

Savanna: Nutrient stocks at fire-resistanceand -suppression thresholds

Our calculations show that, forest species require amuch greater nutrient supply than savanna species toreach a size at which they can resist fires. Stem stocks

of N, P, K, Ca, and Mg are approximately 5-foldgreater, while crown (foliar) stocks are about one orderof magnitude higher in forest than in savanna speciesat the fire-resistance threshold (Fig. 3). To reach thecanopy cover necessary to suppress fires, however,stands composed entirely of savanna species requiregreater nutrient stocks than those composed of forestspecies. Due to intrinsically higher allocation to stem

biomass relative to leaves (Gotsch et al.2010), woodstocks of N, P, K, Ca, and Mg would be much higherin savanna than in forest trees at the fire-suppression

threshold. At this threshold, crown stocks would besimilar between forests and savannas, with the excep-tions of Ca levels, which are higher in savanna trees(Fig.3). In short, compared to forest species, savannatrees require significantly lower nutrient stocks to

become fire resistant, but need significantly highernutrient stock to create a closed canopy that can sup-

press fires. These effects are quite large despite sub-stantial interspecific variation.

Forests vs. Savanna: Leaf and wood nutrients

of individual trees

When the same species are analyzed across differentecosystems, leaf N, P, K, Ca and Mg concentrationsvary significantly, with the lowest and highest leaf nu-trient levels (and SLA) observed in savannas and ripar-ian forests, respectively (Table2). Nutrient concentra-tions are less variable in wood than in leaves. Wood Caand Mg content, as well as wood density, do not varysignificantly among ecosystems. Wood N and P con-centrations, on the other hand, are higher in savanna

than in riparian forest trees, while K concentration ishighest in the dry riparian forest and no differences areobserved among the other ecosystems (Table2).

Forests vs. Savanna: Total biomass and nutrient stocksat the ecosystem level

Above-ground biomass varies widely across eco-systems. Total carbon stocks in the biomass of xero-morphic and deciduous forests (>24 Mg ha1) is more

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than 4 times greater than in savannas (


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develop high-biomass riparian forests additional Pand Ca inputs (>40 and 600 kg ha1 respectively),would have to be several fold higher than what iscurrently found in savannas.

Discussion

Savanna: Nutrient requirements at fire-resistanceand -suppression thresholds

Our results show that differences in nutritionalrequirements affect the ability of forest and savannatrees to resist and suppress fires. Confirming previousstudies (Hoffmann et al. 2005; Rossatto et al. 2013),we found that forest species have higher nutrientcontent per mass of leaf than their congeneric sa-vanna counterparts, even when growing under

nutrient-limiting conditions (Table 1). Stem nutrientconcentrations are similar between forest and savan-na trees, but savanna species allocate more biomassto stem relative to leaves, requiring a lower nutrientsupply to reach a fire resistant size (Fig. 3).However, stands composed entirely of savanna spe-cies would require over three times more nutrientcapital than those composed of forest species to

produce sufficient leaf area to exclude grasses andsuppress fires. Forest species are able to generate a

closed canopy with lower nutrient capital than sa-vanna species, because of a greater leaf area perunit of stem biomass (Gotsch et al. 2010).Consequently, the establishment of forest speciesinto savannas would favor canopy closure, facilita-ting a transition to a non-flammable state. Thisresult corroborates observations that succession of

mesic savanna to forest is associated with the pre-sence of forest species (Geiger et al. 2011; Ratnamet al. 2011; Silva and Anand 2011), a pattern thathas been previously explained by the higher shadetolerance of forest trees (Rossatto et al. 2009), buthere receives an alternative explanation.

While the ingression of forest trees may permitsavannas to attain a non-flammable state with lowernutrient capital than would be required by savannatrees, reaching this state would also require long inter-vals without fire. Since fire is common in savannas,

transition to forest is typically interrupted while still inearly stages of succession, when tree cover is suscep-tible to fire because of high mortality of small stems.To avoid severe fire damage, trees must reach a fire-resistant size, which is more easily attained by savannaspecies not only because of their relatively lower nutri-ent requirements, but also because they have thicker

bark than forest species and become fire-resistant at asmaller stem size (Hoffmann et al. 2009, 2012a).Differences in species nutrient requirements and

Table 2 Average values of specific leaf area (SLA), wooddensity, and macronutrient levels in leaves and wood of treespecies (3 to 5 individuals of 17 species; Supplementary

information) sampled in savannas and at least one forest eco-system. Letters represent significant differences (Tukeys HSD,

p


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Fig. 4 Carbon and nutrientstocks at each studied eco-system. Above-ground esti-mates were based on vege-tation structure (Fig.1) andallometric equations and ac-count for interspecific varia-tion in nutrient concentra-

tion, wood density, and spe-cific leaf area (Table2). Soilstocks account for variationin density, carbon and nutri-ent content, of superficial(020 cm) and deep (20100cm) soil layers. Bars repre-sent average values and er-ror bars show standard de-viation of the average

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soil fertility and leaf or wood nutrient concentrations.These results emphasize the role of intrinsic speciestraits and vegetation structure in generating and rein-forcing gradients of resource accumulation, as a result ofa slow redistribution from deep to surface soils throughorganic matter deposition.

Our calculations show that savanna soils haveenough nutrients to allow tree communities to attainfire-resistant and -suppression thresholds (Figs.3 and4). However, savannas require additional nutrients toallow a full forest expansion following initial estab-lishment. Comparing soils and vegetation stocks, wefind that total N in savanna soils is orders of magni-tude larger than the amount needed to develop a forest,supporting the notion that nutrients other than N limitthe distribution of tropical forests (Reich and Oleksyn2004; Cleveland et al.2011). Even though this assess-

ment is based on total soil N rather than availableforms, given the high potential for organic N mineral-ization and symbiotic fixation of tropical soils(Cleveland et al.2011), we conclude that soil N wouldnot impose an absolute constraint on forest develop-ment at our study sites. Savannas also have sufficientK and Mg to develop low-biomass xeromorphic for-ests. However, additional P and Ca inputs would berequired to support a transition to any forested state.

The amount of additional P required to build axeromorphic forest is relatively small and could

perhaps be attained if understory vegetation stockswere also considered. Previous studies (Castro andKauffman 1998) have shown that the above-ground

biomass in open grasslands near our study sites isabout 5.5 Mg ha1 (ca. 2.8 Mg C ha1), which repre-sents roughly half of the arboreal biomass of savannas.The concentration of P in native and exotic grassesthat occur in the region, range from 0.04 to 0.07 %(Silva and Haridasan 2007), which falls within therange found in savanna trees (Table1). At these con-centrations, grasses could provide up to 3.9 kg P ha1,

which would only be sufficient to build a xeromorphicforest (Table3). The average concentration of Ca ingrasses (0.2 %; Silva and Haridasan2007) is, howev-er, much lower than that found in the wood of savannatrees (>0.6 %; Table1) and is not sufficient to coverthe deficit of Ca to build a low-biomass forest. FurtherCa inputs, of over one third of the existing stock in thearboreal biomass of savannas, would be necessaryfrom atmospheric and erosional deposition, or soildepths greater than 100 cm, to build a xeromorphic

forest. These inputs would, have to be, however, overone order of magnitude larger to attain high-biomassstates, such as riparian forests.

Stocks of Ca should pose a strong constraint par-ticularly because mineral sources of this element are

present in negligible amounts in the acidic soils that

predominate in the region. Based on our calculations,only a landscape-level process of Ca redistributioncould explain the ongoing expansion of riparian for-ests over savannas (Silva et al. 2008). Among otheressential nutrients, Ca occupies a unique position inregulating growth from individual trees to entire eco-systems, controlling cell wall synthesis, biomass pro-duction and structure of woody tissues (Lautner andFromm2010). Savannas and most forest ecosystemsstudied here have larger Ca stocks in the above-ground

biomass than in soil pools, indicating that any inter-

ruption on Ca recycling would favor the formation ofless productive (i.e., open) stable states. Stocks of Pshow similar distribution and, in contrast with lesslimiting nutrients, Ca and P are both found in higherconcentrations at the surface (020 cm) than in deepersoil layers (Fig.4), suggesting a continuous and rapidrecycling process following litter deposition. The decid-uous forest is the only ecosystem where we observedgreater nutrient stocks in soils than in the above-ground

biomass. Its unusual soil fertility originates from theweathering of shallow parent materials (entisols) and

calcareous concretions often found within less than 0.5m from the soil surface. Such soils are rare in centralBrazil, where its occurrence is typically characterized bythe presence of deciduous trees (Moura et al. 2010;Haidar2008), which under high fertility conditions areable to outcompete evergreen species that dominateother forest ecosystems.

Final considerations

We show that interactions between species composi-tion, disturbance, and resource availability favor thelong-term persistence of forest-savanna mosaics. Atour study sites, and probably elsewhere, savanna andforest trees represent different functional types.Tradeoffs between nutrient requirements and adapta-tions to resist fires reinforce savanna and forest asalternate stable states, with low fertility hindering forestexpansion. Forest species require a larger amount ofnutrients to become fire-resistant, so the combined

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effect of fire and nutrient limitation should favor thepersistence of savanna communities.When only savan-na species are present, the transition to a forested staterequires a larger nutrient supply than is available in thesoil. Canopy closure in this case depends upon theingression of forest species, which can facilitate forest

expansion by increasing soil fertility.The above-ground biomass of savannas and forests atour sites is lower than measured in other tropical ecosys-tems. Above-ground carbon stocks of forests in theAmazon region, for example, range from 155 to 217Mg C ha1(Kauffman et al. 1995), whereas the largestvalue we observed in any of our forest sites was 95 Mg Cha1 (ca. 20 times more carbon than stored in savannas).Across all ecosystems, soil carbon stocks are larger thanin the above-ground biomass (Fig. 4), illustrating the

potential for long-term carbon storage in the absence of

fire. Developing non-flammable forested states is depen-dent upon adequate nutrient availability and even thoughsavannas may occur under high fertility conditions (e.g.Moura et al.2010; Haidar2008; Silva et al.2010b;), ourresults show that the indigenous fertility typical ofBrazilian savannas will not allow widespread forest ex-

pansion unless external inputs of P and Ca occur.Roots were not included in our calculations, but we

know that root biomass increases over three-fold (ca.8 to 26 Mg C ha1) from open grasslands to tree-dominated savannas near our study sites (Castro and

Kauffman1998). The exclusion of root nutrient poolsin our study, thus, probably underestimates nutritionallimitations to develop forests. The next phase of un-derstanding will come from manipulations of limitingresources in fertilization experiments using traceablenutrients, coupled with quantitative assessments ofchanges in vegetation structure and composition.Differences in plant-soil water relations should also

be assessed under multiple nutritional constraints.Variations in tree structure and phenology (Rossattoet al. 2009, 2012), physiological adjustments to

changes in water availability, evaporative demand(Bucci et al. 2008), and alternative water sources(e.g., shoot uptake; Oliveira et al. 2005), have beenindicated as important factors controlling vegetationdistribution in mesic savannas, but their interactionswith fire disturbance and nutrient limitation remain to

be investigated.

Acknowledgments We thank the staff of RECOR-IBGE,CIPLAN, and Embrapa Cerrados, for the research infrastructure

and logistic support. We also thank Ricardo Haidar, GabrielDamasco, Daniel Marra, Gabriel Ribeiro, and Artur Paiva, forhelp with field work and species identification, and TimothyDoane and three anonimous reviewers for valuable commentson the manuscript. This research is based upon work supportedby the National Science Foundation Grant No. DEB-0542912(W. H.), AW Mellon Foundation (W. H.), National ScienceFoundation Grant No. EAR-BE-332051 (L. S.,M. H., F. M.-

W., A. F.), and the J. G. Boswell Endowed Chair in Soil Science.

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