REGULAR ARTICLE

Not all forests are expanding over central Brazilian savannas

Lucas C. R. Silva & Mundayatan Haridasan &

Leonel S. L. Sternberg & Augusto C. Franco &

William A. Hoffmann

Received: 1 December 2009 /Accepted: 16 March 2010 /Published online: 31 March 2010# Springer Science+Business Media B.V. 2010

Abstract Recently we reported on the expansion ofriparian forests into savannas in central Brazil. Toenlarge the scope of the earlier study we investigatedwhether upland deciduous and xeromorphic forestsbehaved similarly. We investigated past vegetationchanges that occurred in forest/savanna transitions usingcarbon isotope ratios (δ13C) measured in the soil organicmatter as a tracer. We analyzed the 14C activity whereδ13C showed major shifts in vegetation. The role of soilchemical and physical attributes in defining vegetationdistribution is discussed. Structural changes in vegeta-tion were found to be associated with shifts in theisotope composition (δ13C) of soil organic matter. Thiswas attributed to intrinsic differences in the biomass oftrees and grasses and allowed for the determination ofpast shifts in vegetation by evaluating δ13C at different

depths. The deciduous forest decreased in area approx-imately 980 years ago. Tree cover increased in thexeromorphic forest, but the border stayed stable throughtime. The deciduous forest and adjacent savanna haveeutrophic soils while the xeromorphic forest andadjacent savanna have dystrophic soils. However,greater organic carbon, nitrogen and phosphorus con-centrations are observed in the forests. We provideconcrete evidence of deciduous forest retreat unlike thestability observed in the xeromorphic forest/savannaboundary. These results contrast with the expansion ofriparian forests recently reported in the same region.

Keywords Carbon isotopes . Cerrado . Forestexpansion . Leaf area index . Tropical forests .

Tropical soils

Plant Soil (2010) 333:431–442DOI 10.1007/s11104-010-0358-6

Responsible Editor: Tibor Kalapos.

L. C. R. Silva (*)Department of Forest Engineering,University of Brasilia, Brazil and Embrapa CerradosAgricultural Research Center,Planaltina, DF, Brazile-mail: lsilva@uoguelph.ca

M. HaridasanDepartment of Ecology,University of Brasilia,Brasilia, DF 70904-970, Brazil

L. S. L. SternbergDepartmentof Biology, University of Miami,Coral Gables, FL 33124, USA

A. C. FrancoDepartment of Botany, University of Brasilia,Brasilia, DF 70904-970, Brazil

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

Present Address:L. C. R. SilvaGlobal Ecological Change (GEC) Laboratory,Department of Environmental Biology,University of Guelph,N1G 2W1 Guelph, ON, Canada

Introduction

Several recent studies have shown evidence ofexpansion of tropical forests in different parts of theworld (Dümig et al. 2008; Martinelli et al. 1996;Palmer and van Rooyen 1998; Puyravaud et al. 1994;Silva et al. 2008). This phenomenon is thought to be aresponse to climatic shifts that occurred during theHolocene. The change from a colder and drier to awarmer and wetter climate after the last glacial periodseems to have promoted the expansion of water-limited forests (Dümig et al. 2008; Silva et al. 2008).Little is known, however, about the responses of driertropical ecosystems. Humid tropical forests depend onabundant and regular water supply and reductions inprecipitation can lead to forest retraction (Behling2002; Pennington et al. 2004, 2006; Silva et al. 2009).Deciduous and xeromorphic forests on the other handare adapted to strong seasonality in terms of wateravailability (Furley 2007; Furley et al. 2006). Theseforests therefore would be expected to show oppositeresponses to climate changes as compared to humidforests.

There are, however, other factors that may play adefining role in long-term vegetation changes. Forestsof all kinds generally benefit from warmer interglacialperiods, which are associated with higher atmosphericCO2 concentrations. Within the tropics this favors thegrowth of woody C3 woody plants at the expense ofthe C4 grasses (Ehleringer et al. 1997). Reductions ingrass biomass, in turn, may lead to steep declines infire frequency, which likely contributes to the expan-sion of forests (Behling et al. 2005; Bond et al. 2003).Additionally, vegetation distribution obeys gradientsin soil fertility, texture and depth (Eiten 1972; Furley1992), which can further complicate the understand-ing of tropical ecosystems’ dynamics.

The Cerrado region of central Brazil offers aunique opportunity to study contrasting ecosystemswithin relatively small areas. The complex mosaic ofvegetation in this region includes savannas of variousstructures, riparian forests and upland deciduous andxeromorphic forests, often occurring side by side(Eiten 1972). Most previous studies of vegetationdistribution in this region focused on riparian forest-savanna boundaries (Furley 1992) and despite theacknowledged ecological importance of deciduousand xeromorphic forests, little is known about howtheir distribution has changed in the past. These

forests occur in fragments surrounded by opensavanna, which is the predominant vegetation typein this region. Palynological studies suggested that, atleast for deciduous forests, these fragments representrelicts of a previously well-distributed forest ecosys-tem (Ledru 1992; Pennington et al. 2004, 2006).However, the limitations of pollen studies, in whichthe information extracted from a single pollen profileis used to infer regional scale shifts in vegetation, hindera more detailed understanding on how such shiftsoccurred. For example, the xeromorphic forests (locallyknown as cerradão) commonly contain tree species thatare typical of savanna (Eiten 1972; Furley 2007;Mendonça et al. 1998), resulting in species assemb-lages similar to fire-suppressed savanna (Durigan andRatter 2006). This suggests that these xeromorphicforests may be relatively young, but palynology hasnot been able to shed light on past dynamics of thisforest type.

Here we aimed to investigate how past vegetationchanges occurred in deciduous and xeromorphicforests using carbon isotope ratios measured in thesoil organic matter as a tracer. Our goal was to testwhether the boundary between each of these forestsand the neighboring savanna has been stable over time.We used the same methodology and design used bySilva et al. (2008), who recently described riparianforest expansion over savannas in the same region.This method is based on two assumptions: (i) thedifference in the mean carbon isotopic ratios (δ13C) inthe biomass of forest and savanna leads to differentsignatures in their soil organic matter (SOM). Thisdifference is due to the presence of C4 grasses insavannas, which discriminate less against CO2 mole-cules which contain the carbon isotope C13 than doforest C3 plants (Smith and Epstein 1971); (ii) theSOM in the soil profiles represents a chronologicalsequence of vegetation signature, with past vegetationrecorded at deeper levels (Boutton et al. 1998; Silva etal. 2008). Based on those assumptions we character-ized past shifts in vegetation structure by, firstly,determining the current leaf area index (LAI) of trees/shrubs and grasses along transects spanning theboundary of the forests and savannas and, secondly,determining the carbon isotopic signatures (δ13C) inthe superficial SOM of each of those ecosystems.Finally, by examining the δ13C of SOM at differentdepths in the soil profile, we investigated how thevegetation changed in the past. Since the distribution

432 Plant Soil (2010) 333:431–442

of forests within the savanna matrix of central Brazil isoften associated with variations in soil chemical and/orphysical features (Eiten 1972; Furley 1992, 2007;Ruggiero et al. 2002; Silva et al. 2008), we alsoquantified gradients of soil fertility, texture and bulkdensity across the forest/savanna boundaries. The roleof those edaphic traits in enhancing growth or limitingthe spread of trees from forests to savanna is discussedin the light of the measured shifts in vegetation.

Methods

Sites description

We studied a deciduous forest/savanna boundarywithin the preservation area of CIPLAN MiningEnterprise (15°33′S and 47°51′W) and a xeromorphicforest/savanna boundary within the reserve of theEMBRAPA—Cerrados Research Center (15°36′S and47°42 W), both in the Federal District of Brazil. Thesetwo sites share very similar climates with averageannual rainfall of 1,426 mm (1993–2002) with a well-defined dry season extending from May to Septemberand an average annual temperature of 22.5oC.

The deciduous forest transition is over an eutrophicentisol (US taxonomy), a very shallow soil withcalcareous parent material less than 0.5 m from thesurface, while the xeromorphic forest is establishedover a well-drained deep dystrophic oxisol(EMBRAPA 1978; Reatto et al. 2004). At both sites,the transition from forest to savanna vegetation is verysharp (< 10 m, Fig. 1a,b) and is not associated with avisible transition in soil type or topography. Thesavanna vegetation in both sites has very similarstructure, with a continuous grass layer that contributesmore than trees and shrubs to the overall vegetationcover (Fig. 1b). This allows the forests to be readilydistinguished from savanna based on their greatercanopy height, canopy cover, and basal area, togetherwith the scarcity of grasses, which permit an unam-biguous determination of the position of the boundary.

The xeromorphic forest type studied here is locallyknown as cerradão, a vegetation physiognomy typi-cally dominated by woody species, with canopy heightand crown cover up to 20 m and 90% respectively(Eiten 1972; Ribeiro and Walter 1998). Contrastingwith typical savanna areas, tree stems within thisvegetation type are straight with higher bifurcations

and thin fire sensitive barks (Waibel 1948). Treespecies are mostly evergreen and similarities with theAmazon and coastal Atlantic rain forests flora mayoccur, but in the regional scale more common speciesare found between xeromorphic forests and savannasthan between xeromorphic, riparian and/or deciduousforests (Eiten 1972; Furley 2007; Mendonça et al.1998). Some authors have classified the xeromorphicforests of central Brazil simply as a savanna woodlandsor dense wooded savannas (Furley 1999, 2007), butmany others have described this ecosystem as tropicalforest (Goodland 1971; Haridasan 1992; Oliveira-Filhoet al. 1989; Oliveira-Filho and Ratter 2002; Vourlitis etal. 2001). These inconsistencies are derived from site-specific structural variations of what is popularlyknown as cerradão. In the site studied here howeverthere is no doubt that the term forest is the mostappropriate. Ribeiro et al. (1985) published a detailedfloristic description of the site showing, among otherthings, that tree density is about 2.5 times higher thanin the adjacent savanna. Moreover, the leaf area index(LAI) values of trees and grasses (Fig. 1b) arecomparable with those typical of riparian forests inthe region (Silva et al. 2008).

The deciduous forests of central Brazil tend to occurin disjunct patches surrounded by savannas (Furley etal. 2006; Pennington et al. 2000). The familiesBromeliaceae, Compositae, Malvaceae and Maranta-ceae predominate in the understorey of these forestswith the soil only sparsely covered with a few grassspecies in contrast to savanna vegetation where grassespredominate (Felfili et al. 2007). These forests form atree cover of 50% to 70% during the rainy season, butthe majority of species become leafless in the dryseason, when the canopy cover is less than 50%(Pennington et al. 2000). The trunks are straight withcanopy emergents reaching up to 20 to 30 meters.Epiphytes are not very common while Bromeliaceaeand Cactaceae are frequent (Felfili et al. 2007). It hasbeen suggested based on floristic evidence thatdeciduous forests fragments in central Brazil act as“stepping-stones” connecting the larger seasonal for-mations of northeast Brazil (caatinga) with theArgentinean Chaco (Felfili et al. 2007; Pennington etal. 2000). However the flora of deciduous forests isvery distinct than that of the savannas. For example,tree species such as Myracrodruon urundeuva, Cam-pomanesia velutina, Dilodendron bipinnatum andLuehea grandiflora dominate (have the highest com-

Plant Soil (2010) 333:431–442 433

bined abundance, frequency and basal area) thedeciduous forest studied here (Haidar 2007), but arenot typically found in savannas (Mendonça et al.1998). A detailed floristic and phytosociologicaldescription of the study site is provided by Netto etal. (2005) and Haidar (2007).

Leaf area index

Using the same design as used by Silva et al. (2008),who recently described riparian forest expansion intosavannas in this region, we sampled two transects one

at each forest savanna boundary. The transects wereplaced perpendicularly to the vegetation boundary ateach site and consisted of 11 sampling points. Thecentral point of each transect was chosen to coincidewith the savanna/forest border and designated as point0. From this central point the transects extended 50 m(5 sampling points 10 m apart) in opposite directionsinto each vegetation type for a total of 100 m.

The LAI, or the ratio of total upper leaf surface perunit of the surface area of the land on which thevegetation grows, was measured every 10 m along thetransects with a CI110 plant canopy imager (CID,

Fig. 1 Representation of a forest/savanna boundary (a), leaf area index for trees/shrubs and grasses (b) and δ13C values of superficialsoil organic matter along deciduous and xeromorphic forest transition with savanna in central Brazil

434 Plant Soil (2010) 333:431–442

Inc., Camas, WA, USA) in March 2007, near the endof the wet season. This instrument estimates canopyLAI indirectly based on a digital hemispherical imageof the vegetation overhead. To partition total LAI intograsses in the ground layer and tree/shrub compo-nents, separate images were taken at a height of 1 mand at the soil surface (after removal of herbaceousdicots) (Hoffmann et al. 2005; Silva et al. 2008). LAIvalues obtained at a height of 1 m were considered torepresent the tree/shrub LAI. Grass LAI, in turn, wascalculated by subtracting the tree/shrub LAI fromtotal LAI as measured at the soil surface. The valuesobtained in this manner are a measure of totalvegetation area index, and as such are meant toquantify vegetation density. For trees, our values ofLAI include stem area as well as leaf area. Forgrasses, LAI comprises both living and dead leaf area.

Soil sampling and analyses

Soil profiles were examined every 10 m along thesame transect above described for LAI measurements.A total of eleven profiles, five within the forest, fivewithin the savanna and one at the border, wereexamined at each transect. Soil samples were collect-ed to a depth of 1 m in 10 cm increments. Surfacesoils were considered the ones collected between 0and 10 cm depth at each soil profile. Soil sampleswere acquired by pressing 100 cm3 tubes into eachlayer of sequentially dug soil pits. Tubes wereinserted so that pressure was only exerted on the tubewalls. This prevents soil compaction and the overes-timation of soil density, which was calculated bydetermining the ratio between the dry mass of the soiland the volume of the tubes.

Standard methods, considered the most adequate toanalyze soils from Cerrado region, were used todetermine soil fertility and texture. Samples weredried at room temperature and fine roots wereremoved by passing through a 2 mm mesh sieve.Total nitrogen was determined by the Kjeldahlmethod (Bremner and Mulvaney 1982). Availablephosphorus and potassium were determined by themethod of Mehlich (1953). Exchangeable calciumwas extracted by a 1 M KCl solution and determinedby atomic absorption. Organic carbon content wasdetermined by wet oxidation (Walkley and Black1934). Soil texture was determined by the interna-tional pipette method (Day 1965).

Carbon isotope ratios of soil samples were deter-mined at the Laboratory of Stable Isotope Ecology inTropical Ecosystems (LSIETE) at the University ofMiami. Soil samples (10 mg) were loaded in tin cups(3 mm diameter and 8 mm height, Elementar, Hanau,Germany), which were placed in an automatedelemental analyzer (Euro EA Elemental Analyzer,Eurovector, Milan, Italy) connected to a continuousflow isotope ratio mass spectrometer (Isoprime,Elementar Hanau, Germany). Carbon-13 abundanceswere expressed as δ13C (‰)=(Rsample/RPDB−1)×1000 where Rsample and RPDB represent the 13C/12Cratios and PeeDee standard respectively. The preci-sion of analysis was ± 0.1‰ (±SD).

We analyzed the 14C activity of carbon in SOM atthe deciduous forest border at 70–80 cm depth, wherethe soil profiles showed major shifts from forest tosavanna. Carbon-14 activity of SOM was analyzed byaccelerator mass spectrometry (AMS) and convertedto mean age of SOM at the Beta Analytic Radiocar-bon Dating Laboratory (Miami, USA).

Results

The LAI of trees and shrubs changed from highvalues of 2 to 3 inside the forests to values lower than1 within 10 m from the border into the savanna(Fig. 1a,b). The xeromorphic forest had a higher treeLAI than the deciduous forest (Fig. 1b) while grassLAI in both savannas was similar, with values (∼2) atleast twice as high as the LAI measured for trees andshrubs in the savanna. Grass LAI quickly declined to0 inside the forests (Fig. 1b).

These shifts in vegetation structure produceddistinct δ13C signatures in the surface soil organicmatter (Fig. 1c). The SOM δ13C in the savannas wasalways higher than −20‰ (near the border) reachingvalues as high as -16‰ farther from the forest. Theδ13C in the forest soils on the other hand variedbetween −23 and −25.5‰ (Fig. 1c). The less negativeδ13C values of the savanna soils reflect the dominanceof C4 plants, while the SOM δ13C of the forests wastypical of C3 plant dominance (Sanaiotti et al. 2002;Silva et al. 2008).

The δ13C of the SOM also changed with depth, butpatterns differed between the two sites (Fig. 2). TheSOM δ13C values were relatively constant with depthin all the profiles inside the deciduous forest, while

Plant Soil (2010) 333:431–442 435

the profiles taken at the border and in the adjacentsavanna are stable until 50 cm depth and then dropgradually, eventually reaching typical values forforests or borders in deeper layers (Fig. 2a). Theseshifts in vegetation occurred around 980 (±40) YBPand since then the transition zone has remained stable(Fig. 2a). In contrast, there were no shifts among thexeromorphic forest and the surrounding savanna.However, the SOM δ13C increased rapidly at lowerdepths (Fig. 2b) inside the forest. The profiles locatedat 50 and 10 m inside the forest increased byapproximately 2‰, while soils at 40, 30 and 20 mexhibited more than 4‰ change, indicating a greatercontribution of grasses and/or a lower contribution oftrees for the SOM in the past. The δ13C values of theadjacent savanna vegetation and border are consistentwith open vegetation (mixture of trees and grasses)through the entire profiles.

In spite of some spatial heterogeneity, soil organiccarbon, total N, available P, K and exchangeable Caconcentrations at the soil surface (0–10 cm) and up

to 1 m depth tended to be higher in the deciduousforest than in the adjacent savanna (Fig. 3). Theseshifts, however, were not as sharp as changes invegetation structure (Fig. 1a,b). While at the decid-uous forest/savanna transition organic carbon valuesand overall fertility levels inside the forest werehigher, the xeromorphic forest showed slightlygreater organic carbon, N and P, but similar levelsof Ca and lower concentrations of K than theadjacent savanna (Figs. 2 and 3).

However, the savanna adjacent to the deciduousforest had higher concentrations of K, Ca and pH(Fig. 3) than xeromorphic forest and adjacent savanna.All soils contain more than 50% clay, with onlymodest differences between savannas and forests. Thexeromorphic forest had significantly greater claycontent in the surface soils than the adjacent savanna(60% vs 50%, p<0.001), but these differences dis-appeared below 50 cm and no difference in claycontent existed at the deciduous forest-savanna transi-tion (data not shown). Soil bulk density generally

Fig. 2 Variation in δ13Cvalues of soil organic mat-ter for the profiles across theforest (−10, −20, −30, −40and −50 m from the border)savanna boundaries (10, 20,30, 40 and 50 m from theborder): (a) deciduous for-est; (b) xeromorphic forest.Vertical dashed line repre-sents the limit of δ13C val-ues of superficial soilorganic matter from savannavegetation (right)

436 Plant Soil (2010) 333:431–442

Fig. 3 Average soil concen-trations of total N, availableP, K, exchangeable Ca, pHand organic carbon, in thesurface and in the top 1 msoil from forests (left) tosavanna (right) along thedeciduous (left column) andxeromorphic (right column)forest/savanna transitions incentral Brazil. Error barsrepresent 1 SD for the aver-age nutrient concentrationsmeasured at each 10 cmdepth up to 1 m

Plant Soil (2010) 333:431–442 437

increased with depth in the deciduous forest/savannatransition, ranging from 0.7 to 1.1 g dm−3 at thesurface and reaching values over 1.5 g dm−3 in deeperlayers. In the xeromorphic forest/savanna transitionsoil density was stable across the profiles in thesavanna and border (∼1 g dm−3), but increased from0.6 to 0.9 g dm−3 at the first 30 cm depth in the forest,remaining then constant (data not shown).

Discussion

The partitioning of tree and grass abundance betweenthe forest and the savanna physiognomies produceddistinct differences in the δ13C of the surface soilorganic matter (SOM) (Fig. 1b,c). Most tropicalgrasses have the C4 photosynthetic pathway (Klinkand Joly 1989; Sanaiotti et al. 2002) and discriminateless against 13C in comparison to C3 trees and shrubs.Typical δ13C ranges from −15‰ to −10‰ in C4

grasses and from −30‰ to −24‰ in C3 plants (Smithand Epstein 1971). The isotopic differences in themodern bulk biomass between forests and savannasare recorded in the surface SOM (Fig. 1c, Boutton etal. 1998), but changes in the δ13C values of SOMacross the soil profiles reflect past changes in thevegetation structure (Dümig et al. 2008; Martinelli etal. 1996; Sanaiotti et al. 2002; Silva et al. 2008).

The δ13C found here in deeper layers of the soilprofiles show that the deciduous forest once extendedbeyond its present limits (Fig. 2). While the profilesinside the forest show that trees were always thedominant growth form, soil profiles at the currentborder (that represents a mixture between grasses andtrees) and up to 50 m inside the savanna show clearsignatures of forest or transitional vegetation (valuesfound for the actual border) at depths greater than60 cm. This represents a forest retreat of at least 50 m,which occurred approximately 980 (±40) years ago.

According to Furley (2007) shifts in the distribu-tion of deciduous forest in central Brazil could haveresulted from indigenous activity at a local scale. On abroader scale on the other hand, palynological studieshave shown that the scattered distribution of thisforest physiognomy in the region probably representremnants of a previously more extensive formationthat expanded during the colder, drier Late GlacialMaximum and retreated during the Quaternary (Ledru1992; Miles et al. 2006; Pennington et al. 2006).

Although these assumptions were recently questioned(Mayle 2006), the carbon isotope results presentedhere indicates that deciduous forests covered greaterareas in the past. To confirm this trend on a widerscale, however, similar studies should be conducted inother deciduous forests fragments that occur through-out the Cerrado region.

The carbon isotope ratios measured along thexeromorphic forest/savanna transition did not showevidence of past changes in the position of theecotone (Fig. 2). However, there was a clear shift inthe profiles inside the forest, from more positive δ13Cat lower depths, to more negative values near thesurface. This represents an increase in the contribu-tion of trees to the ecosystem bulk biomass. Incontrast to other tropical forests, these xeromorphicforests often support low densities of grasses (Hoff-mann et al. 2005) and usually do not have a 100%tree coverage, even under undisturbed conditions(Eiten 1972). At this site, the forest appears to haveonce supported some grasses in its understory, but notof sufficient density to leave an isotopic signaturerepresentative of savanna. So, despite an increase intree cover and a decline in grasses, the extent ofxeromorphic forest has remained stable.

It is important to mention that shifts in δ13C can insome cases be caused by factors other than changes invegetation. Differential degradation of chemical com-pounds (Benner et al. 1987), microbial activity andheterotrophic fixation of CO2 (Ehleringer et al. 2000)are some post-depositional factors that can altercarbon isotope ratios in the soil organic matter.Changes in the atmospheric isotopic composition(Farquhar et al. 1982) and differences betweensavanna and forest vegetation (Silva et al. 2008) areexamples of pre-depositional factors that determinedifferent isotopic signature through soil profiles.

Post-depositional changes are correlated with changesin soil organic matter concentration (Balesdent et al.1993; Krull et al. 2002), which in tropical regionsusually occur within the top 20 cm (Krull et al.2002). Here, the changes in the δ13C values occur upto a 100 cm and 50 cm depth in the deciduous andxeromorphic forest/savanna transitions respectively(Fig. 2). Moreover, we did not observe a correlationbetween the δ13C and SOM below 20 cm (data notshown) and, therefore, there is no reason to believethat post-depositional effects are causing the ob-served isotopic changes. The differences in atmospheric

438 Plant Soil (2010) 333:431–442

δ13C within the last 10,000 years have also been small(lower than 1.0‰, Marino et al. 1992) and they wouldequally affect all soil profiles. Since it is unlikely thatchanges in the range observed here (from 2 to 6‰)would not be accompanied by changes in vegeta-tion, we conclude that shifts in the δ13C alongprofiles were caused by structural changes in the pastvegetation.

The retreat of deciduous forest and the stability ofthe xeromorphic forest contrast with research thatrecently documented the expansion of riparian forestsover savannas in the same region (Silva et al. 2008),and in the Amazon and Atlantic forests in northernand southern Brazil respectively (Dümig et al. 2008;Martinelli et al. 1996). In these studies the expansionof forest is attributed to changes in mid-Holoceneclimate towards a recently warmer and wetter condi-tion. Such changes in climate led to the expansion offorests not just in the tropics but also in temperate andboreal regions (Williams et al. 2004). In general, treeswould benefit more than grasses from the warmerinterglacial periods that are associated with a higheratmospheric CO2 (Ehleringer et al. 1997). Addition-ally, a reduction in fire frequency as consequence of arelative reduction in grass biomass, along with greaterpostglacial water availability, would also favor theexpansion of forests (Bond et al. 2003).

However, our results show that deciduous andxeromorphic forests, whose flora is adapted to strongseasonality in water regime or overall drier conditions(Furley et al. 2006), did not respond to past shifts inclimate the same way as tropical humid forests. In thecase of the deciduous forest, the seasonal loss ofleaves would favor the establishment of grasses insidethe forest in a recent scenario of wetter conditions.The biomass of grasses would increase closer to theforest boundary during the less intense dry seasonwhile the canopy is still open and tree productivity islow (Franco et al. 2005). This would eventually allowgrasses to outcompete trees during their establish-ment, pushing the former border further inside theforest until a new equilibrium is reached.

Most of trees in xeromorphic forests are ever-greens, so a similar reasoning is not valid for thetransition to savanna. Other forces are expected tomaintain the stability of this boundary. Previousstudies have emphasized the importance of soils toexplain the origin and distribution of xeromorphicforests and hypothesized that the much greater woody

biomass, as compared to that of the savannas, wouldbe a result of past differences in soil fertility(Marimon and Haridasan 2005). The same authorssuggest that the structure of these forests has beenmaintained to present by an efficient nutrient cycling,since there is often no difference in soil fertilitybetween the xeromorphic forests and the savannasunder present conditions. Our results confirm thatsoils inside both ecosystems are dystrophic anddifferences in soil fertility (Fig. 3) would thereforenot be able to explain the abrupt change in vegetationstructure.

It is likely, that the continuous input of organicmatter is the keystone for the maintenance of thexeromorphic forest structure. It is greater inside thexeromorphic forest, which raises the levels oforganic related nutrients such as N and P in thesurface soil. Along with shaded conditions under thecanopy, this greater organic matter content alsoimproves microbial activity in the soils and enablesa more efficient nutrient cycling from the litter(Haridasan 2001). This would explain not just thestability of the border between xeromorphic forest andsavanna but also the increasing tree biomass insidethe forest as a possible result of continuous soil plantfeedbacks within the forest as ecosystem nutrientpools accumulate (Funk and Vitousek 2007; Vitousekand Matson 1984).

Similarly, deciduous forests rely on a rapid andefficient nutrient uptake at the beginning of the wetseason (Furley et al. 2006; Pennington et al. 2006)when the greatest part of the annual biomassproduction takes place (Lisi et al. 2008). This foresttype is often associated with eutrophic soils (Furley2007), as is the case here (Fig. 3). Therefore, thisforest is not as nutrient limited. In fact the concentra-tion of all analyzed nutrients in the surroundingsavanna was higher than in most forest types of theregion, despite being somewhat lower than theadjacent deciduous forest (Eiten 1972; Haridasan1992). Therefore, the differences among sites can bemuch greater than the differences between forest andsavanna at a given site. This brings up questionsabout the general assumption that forests withinCerrado region obey an edaphic climax (Eiten 1972;Haridasan 1992). The gradient in soil characteristicsfrom the savanna to the deciduous forest for instance,although not as sharp as the structural change invegetation, corresponds to the current rather than the

Plant Soil (2010) 333:431–442 439

past border position among those ecosystems. Thisshows that the forest may create or reinforce soilgradients rather than solely being defined by them.

Previous studies have shown that in similarsituations, where soil fertility does not explain limitsbetween forests and savannas, tree density is oftenassociated with soil texture and denser vegetation isrelated to higher clay content (Ruggiero et al. 2002).Here we found a 10% higher clay content inside thexeromorphic forest than in the adjacent savanna. Thismight represent a greater water retention capacity andalso enhance soil microbiota, which is a fundamentalaspect for the maintenance of xeromorphic foreststructure as previously discussed. On the other hand,no difference in soil texture was found between thesavanna and the deciduous forest. Soil density wasalso similar between both forest types and theadjacent savannas, ranging from 0.6 to 1.1 g dm−3.These values are below the critical values for treesestablishment (1.4 g dm−3) in the region (Goedert etal. 2002). Soil physical properties are thus not likelyto limit forest distribution across the studied bound-aries.

Acknowledgements We thank Jose´ Carlos Sousa Silva atEMBRAPA Cerrados and Ricardo Flores Haidar, GabrielDamasco do Vale and Regina Kruse for field assistance andvaluable comments. This research is based upon worksupported by the National Science Foundation Grant No.DEB-0542912 (W. H.), AW Mellon Foundation (W. H.) andNational Science Foundation Grant No. EAR-BE-332051.

References

Balesdent J, Girarden C, Mariotti A (1993) Site-related d13C oftree leaves and soil organic matter in a temperate forest.Ecology 74:1713–1721

Benner R, Fogel ML, Sprague K, Hodson RE (1987) Depletionof 13C in lignin and its implications for stable carbonisotope studies. Nature 329:708–710

Behling H (2002) South and Southeast Brazilian grasslandsduring late Quaternary times: a synthesis. PalaeogeogrPalaeoclimatol Palaeoecol 177:19–27

Behling H, Pillar VP, Bauermann SG (2005) Late Quaternarygrassland (Campos), gallery forest, fire and climatedynamics, studied by pollen, charcoal and multivariateanalysis of the Sao Francisco de Assis core in western RioGrande do Sul (southern Brazil). Rev Palaeobot Palynol-ogy 133:235–248

Bond WJ, Midgley GF, Woodward FI (2003) The importanceof low atmospheric CO2 and fire in promoting the spreadof grasslands and savannas. Global Change Biol 9:973–982

Boutton TW, Archer SR, Midwood AJ, Zitzer SF, Bol R (1998)δ13C values of soil organic carbon and their use indocumenting vegetation change in a subtropical savannaecosystem. Geoderma 82:5–41

Bremner JM, Mulvaney CS (1982) Nitrogen total. In: Page AL,Miller RH, Keeney DR (eds) Methods of soil analysis:chemical and microbiological properties vol. 2, 2nd edn.American Society of Agronomy, Madison, pp 595–624

Day PR (1965) Particle fractionation and particle-size analysis.In: Black CA (ed) Methods of soil analysis. AmericanSociety of Agronomy, Madison, pp 545–567

Dümig A, Schad P, Rumpel C, Dignac M, Kögel-Knabner I(2008) Araucaria forest expansion on grassland in thesouthern Brazilian highlands as revealed by 14C and δ13Cstudies. Geoderma 145:143–147

Durigan G, Ratter JA (2006) Successional changes in cerradoand cerrado/forest ecotonal vegetation in western SaoPaulo State, Brazil, 1962–2000. Edinburgh J Bot 63:119–130

Ehleringer JR, Cerling TE, Helliker BR (1997) C4 photosyn-thesis, atmospheric CO2 and climate. Oecologia 112:285–299

Ehleringer JR, Buchmann N, Flanagan LB (2000) Carbonisotope ratios in belowground carbon cycle processes.Ecol Appl 10:412–422

Eiten G (1972) The cerrado vegetation of central Brazil. BotRev 38:201–341

EMBRAPA (1978) Levantamento de reconhecimento dos solosdo Distrito Federal. Boletim Técnico, no. 53, ServiçoNacional de Levantamento e Conservação de Solos. Riode Janeiro

Farquhar GD, O’Leary MH, Berry JA (1982) On therelationship between carbon isotope discrimination andthe inter-cellular carbon-dioxide concentration in leaves.Aust J Plant Physiol 9:121–137

Felfili JM, Nascimento ART, Fagg CW, Meirelles EM (2007)Floristic composition and community structure of aseasonally deciduous forest on limestone outcrops inCentral Brazil. Rev Bras Bot 30:611–621

Franco AC, Bustamante M, Caldas LS, Goldstein G, MeinzerFC, Kozovits AR, Rundel P, Coradin VTR (2005) Leaffunctional traits of neotropical savanna trees in relation toseasonal water deficit. Trees 129:326–335

Funk J, Vitousek PM (2007) Resource use efficiency and plantinvasion in low-resource systems. Nature 446:1078–1081

Furley PA (1992) Nature and dynamics of forest-savannaboundaries. Chapman and Hall, London

Furley PA (1999) The nature and diversity of neotropicalsavanna vegetation with particular reference to the Brazil-ian cerradões. Global Ecol Biogeogr 8:223–241

Furley PA (2007) Tropical savannas and associated forests:vegetation and plant ecology. Prog Phys Geogr 31:203–211

Furley PA, Grace J, Meir P (2006) Tropical savannas andseasonally dry forests: vegetation and environment. Spe-cial issue. J Biogeogr 33:164

Goedert WJ, Schermack MJ, Freitas FC (2002) Estado decompactação do solo em áreas cultivadas no sistema deplantio direto. Pesq Agropec Bras 37:233–227

Goodland R (1971) A physiognomic analysis of the “cerrado”vegetation of Central Brasil. J Ecol 59:411–419

440 Plant Soil (2010) 333:431–442

Haidar RF (2007) Fitossociologia, diversidade e sua relaçãocom variáveis ambientais em florestas estacionais dobioma Cerrado no planalto central e nordeste do Brasil.Universidade de Brasília, Dissertation

Haridasan M (1992) Observations on soils, foliar nutrientconcentrations and floristic composition of cerradão sensustricto and cerradão communities in central Brazil. In:Furley PA, Proctor J, Ratter JA (eds) Nature and dynamicsof forest-savanna boundaries. Chapman and Hall, London,pp 171–184

Haridasan M (2001) Nutrient cycling as a function of landscapeand biotic characteristics in the cerrado of central Brazil.In: McClain ME, Victoria RL, Richey JE (eds) Biogeo-chemistry of the amazon basin and its role in a changingworld. Oxford University Press, New York, pp 68–83

Hoffmann WA, Silva ER, da Machado GC, Bucci SJ, ScholzFG, Goldstein G, Meinzer FC (2005) Seasonal leafdynamics across a tree density gradient in a Braziliansavanna. Oecologia 145:307–316

Klink CA, Joly CA (1989) Identification and distribution of C3

and C4 grasses in open and shaded habitats in Sao Paulostate, Brazil. Biotropica 21:30–34

Krull ES, Bestland EA, Gates WP (2002) Soil organic matterdecomposition and turnover in a tropical ultisol: evidencefrom δ13C, δ15N and geochemistry. Radiocarbon 44:93–112

Ledru MP (1992) Late Quaternary environmental and climaticchanges in central Brazil. Quatern Res 39:90–98

Lisi CS, Tomazello M, Botoss PC, Roig FA, Maria VRB,Ferreira-Fedele L, Voigt ARA (2008) Tree-ring formation,radial increment periodicity, and phenology of tree speciesfrom a seasonal semi-deciduous forest in southeast Brazil.Iawa J 29:189–207

Marimon BH, Haridasan M (2005) Comparação da vegetaçãoarbórea e características edáficas de um cerradão e umcerrado sensu stricto em áreas adjacentes sobre solodistrófico no leste de Mato Grosso. Acta Bot Bras19:913–926

Marino BD, McElroy MB, Salawitch RJ, Spaulding WG (1992)Glacial-to-interglacial variations in the carbon isotopiccomposition of atmospheric CO2. Nature 357:461–466

Martinelli LA, Pessenda LCR, Espinoza E (1996) Carbon-13depth variation in soil of Brazil and relations with climatechanges during the Quaternary. Oecologia 106:376–381

Mayle F (2006) The Late Quaternary biogeographical history ofSouth American seasonally dry tropical forests: insightsfrom palaeo-ecological data. In: Pennington T, Lewis GP,Ratter JA (eds) Neotropical savannas and seasonally dryforests. Systematics Association, CRC-Taylor and Francis,pp 395–416

Mehlich A (1953) Determination of P, Ca, Mg, K, Na and NH4.North Carolina Soil Test Division, North Carolina Depart-ment of Agriculture, Raleigh

Mendonça RC, Felfili JM, Walter BMT, Silva-Júnior MC,Rezende AV, Filgueira T, Nogueira PE (1998) A floravascular do cerrado. In: Sano SM, Almeida SP (eds)Cerrado ambiente e flora. EMBRAPA, Planaltina, pp 279–556

Miles L, Newton AC, DeFries RS, Ravilious C, May I, KaposV, Gordon JL (2006) A global overview of the conserva-tion status of tropical dry forests. J Biogeogr 33:491–505

Netto PB, Mecenas VV, Cardoso ES (2005) APA de Cafuringa:a última fronteira natural do DF. Secretaria do MeioAmbiente e Recursos Hídricos

Oliveira-Filho AT, Shepherd GJ, Martins FR, Stubblebine WH(1989) Environmental factors affecting physiognomicaland floristic variation in a Cerrado of Central Brazil. JTrop Ecol 5:413–431

Oliveira-Filho AT, Ratter JA (2002) Vegetation physiognomiesand woody flora of the Cerrado Biome. In: Oliveira PS,Marquis RJ (eds) The Cerrados of Brazil: ecology andnatural history of a Neotropical savanna. ColumbiaUniversity Press, New York, pp 91–120

Palmer AR, Van Rooyen AF (1998) Detecting vegetationchange in the southern Kalahari using Landsat TM data.J Arid Environ 3:143–153

Pennington RT, Prado DE, Pendry CA (2000) Neotropicalseasonally dry forests and quaternary vegetation changes.J Biogeogr 27:261–273

Pennington RT, Lavin M, Prado DE, Pendry CA, Pell S,Butterworth CA (2004) Historical climate change andspeciation: neotropical seasonally dry forest plants showpatterns of both Tertiary and Quaternary diversification.Philos Trans R Soc 359:515–538

Pennington T, Lewis G, Ratter JA (2006) Neotropical savannasand seasonally dry forests: plant diversity, biogeography,and conservation. Systematics association, special volumeseries 69. CRC-Taylor and Francis, Boca Raton

Puyravaud JP, Pascal JP, Dufour C (1994) Ecotone structure asan indicator of changing forest-savanna boundaries (Linga-namakki Region, southern India). J Biogeogr 21:581–593

Reatto A, Martins ES, Farias MFR, Silva AV, Carvalho JuniorOA (2004) Mapa pedológico digital—SIG atualizado doDistrito Federal Escala 1: 100.000 e uma síntese do textoexplicativo. EMBRAPA Cerrados, Planaltina

Ribeiro JF, Silva JCS, Batmanian GJ (1985) Fitossociologia detipos fisionômicos de cerrado em Planaltina, DF. Rev BrasBot 8:131–142

Ribeiro JF, Walter BMT (1998) Fitofisionomias do BiomaCerrado. In: Sano S, Almeida S (eds) Cerrado: ambiente eflora. EMBRAPA Cerrados, Brasília, pp 89–166

Ruggiero PGC, Batalha MA, Pivello VR, Meiralles ST (2002)Soil-vegetation relationships in cerrado (Brazilian savan-na) and semideciduous forest, Southeastern Brazil. PlantEcol 160:1–16

Sanaiotti TM, Martinelli LA, Victoria RL, Trumbore SE,Camargo PB (2002) Past vegetation changes in Amazonsavannas determined using carbon isotopes of soil organicmatter. Biotropica 34:2–16

Silva LCR, Sternberg L, Haridasan M, Hoffmann WA,Miralles-Wilhelm F, Franco AC (2008) Expansion ofgallery forests into central Brazilian savannas. GlobalChange Biol 14:1–11

Silva LCR, Anand M, Oliveira JM, Pillar VD (2009) Pastcentury changes in Araucaria angustifolia (Bertol.) Kun-tze water use efficiency and growth in forest and grasslandecosystems of southern Brazil: implications for forestexpansion. Glob Chang Biol 5:2387–2396

Smith BN, Epstein S (1971) Two categories of 13C/12C ratiosfor higher plants. Plant Physiol 47:380–394

Vitousek P, Matson P (1984) Mechanisms of nitrogen retentionin forest ecosystems: a field experiment. Science 225:51–52

Plant Soil (2010) 333:431–442 441

Vourlitis GL, Priante Filho N, Hayashi MMS, Nogueira JS,Caseiro FT, Holanda-Campelo J (2001) Seasonal varia-tions in the net ecosystem CO2 exchange of a matureAmazonian transitional tropical forest (cerradão). FunctEcol 15:388–395

Waibel L (1948) Vegetation and land use in the planalto centralof Brazil. Geogr Rev 38:529–554

Walkley A, Black IA (1934) An examination of the Degtjareffmethod for determining soil organic matter and a proposedmodification of the chromic acid titration method. Soil Sci37:29–38

Williams JW, Shuman BN, WebbIII T, Bartlein PJ, Leduc PL(2004) Late-quaternary vegetation dynamics in north Amer-ica: scaling from taxa to biome. Ecol Monogr 74:309–334

442 Plant Soil (2010) 333:431–442