Plant Soil (2013) 373:829–842
DOI 10.1007/s11104-013-1822-x
REGULAR ARTICLE
Can savannas become forests? A coupled analysis of nutrient
stocks and fire thresholds in central Brazil
Lucas 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 the
seasonal tropics are maintained as savannas. The advance of forests into these areas depends on shifts in
species composition and the presence of sufficient
nutrients. Predicting such transitions, however, is difficult due to a poor understanding of the nutrient
Responsible Editor: Michael Denis Cramer.
Electronic supplementary material The online version of this
article (doi:10.1007/s11104-013-1822-x) contains
supplementary material, which is available to authorized users.
L. C. R. Silva (*) : W. R. Horwath
Department of Land, Air and Water Resources,
University of California,
Davis, CA 95616, USA
e-mail: [email protected]
W. A. Hoffmann
Department of Plant Biology,
North Carolina State University,
Raleigh, NC 27695, USA
D. R. Rossatto
Departamento de Biologia Aplicada, FCAV, Universidade
Estadual Paulista “Júlio de Mesquita Filho”-UNESP,
14884-900 Jaboticabal, SP, Brazil
M. Haridasan
Departamento de Ecologia, Universidade de Brasília,
70910-900 Brasília, DF, Brazil
A. C. Franco
Departamento de Botânica, Universidade de Brasília,
70910-900 Brasília, DF, Brazil
stocks required for different combinations of species
to resist and suppress fires.
Methods We compare the amounts of nutrients required by congeneric savanna and forest trees to reach
two thresholds of establishment and maintenance: that
of fire resistance, after which individual trees are large
enough to survive fires, and that of fire suppression,
after which the collective tree canopy is dense enough
to minimize understory growth, thereby arresting the
spread of fire. We further calculate the arboreal and
soil nutrient stocks of savannas, to determine if these
are sufficient to support the expansion of forests following initial establishment.
Results Forest species require a larger nutrient supply
to resist fires than savanna species, which are better
able to reach a fire-resistant size under nutrient limitation. However, forest species require a lower nutrient
supply to attain closed canopies and suppress fires;
therefore, the ingression of forest trees into savannas
facilitates the transition to forest. Savannas have sufficient N, K, and Mg, but require additional P and Ca
to build high-biomass forests and allow full forest
expansion following establishment.
Conclusions Tradeoffs between nutrient requirements
and adaptations to fire reinforce savanna and forest as
alternate stable states, explaining the long-term persistence of vegetation mosaics in the seasonal tropics.
Low-fertility limits the advance of forests into savannas, but the ingression of forest species favors the
formation of non-flammable states, increasing fertility
and promoting forest expansion.
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Keywords Cerrado . Ecosystem dynamics .
Fire . Forest expansion . Nutrient cycling . Soil-plant
interactions . Succession . Tradeoffs . Tropics
Introduction
Over the past few thousand years, expansion of forests
into savannas and grasslands has occurred in many
parts of South America, a phenomenon that has been
generally attributed to climate fluctuations (Behling et
al. 2005; Silva et al. 2008, 2011; Dumig et al. 2008;
Silva and Anand 2011). Savannas, however, continue
to persist over large areas where climatic conditions
are adequate to support forests (Lehmann et al. 2011).
In some of these areas, transitions to forest depend
upon shifts in tree species composition (Geiger et al.
2011; Ratnam et al. 2011; Silva and Anand 2011), but
predicting these is complicated by interacting effects
of fire and soil nutrients on forest and savanna species.
In dry tropical regions, climate alone prevents the
development of forests (Sankaran et al. 2005), but
throughout mesic savannas (i.e., regions where annual
precipitation >800 mm), gradual forest expansion may
occur upon fire suppression (Hopkins 1965; Durigan
and Ratter 2006; Pinheiro et al. 2010), and vegetation
mosaics commonly coincide with edaphic gradients
(Furley et al. 1992; Silva et al. 2008, 2010a, b). In
central Brazil, for example, savanna vegetation is typically found over nutrient-poor oxisols, dominating
the landscape, while disjunct forests are found in areas
of high soil fertility, such as riverbeds and limestone
outcrops (Guidão et al. 2002; Gottsberger and
Silberbauer-Gottsberger 2006; Furley 2007). Despite
these associations, the extent to which soil nutrients
and fire limit forest development is not well resolved.
Nutrient-poor soils may support savanna because
available pools of essential nutrients are simply insufficient to construct high tree biomass or, alternatively,
nutrient pools may be sufficient to construct forest
biomass (Bond 2010), but savannas persists because
growth rates are too low to overcome rates of biomass
loss caused by fire (Lehmann et al. 2011; Hoffmann et
al. 2012a, b).
In either case, to determine how fire interacts with
nutrient availability to govern the distribution of forest
and savanna, it is important to consider two thresholds. The first threshold marks the point at which an
individual tree becomes large enough to reliably avoid
Plant Soil (2013) 373:829–842
fire damage and topkill (i.e., stem death), which we
refer to as the fire-resistance threshold. The second
threshold marks the point beyond which the vegetation achieves sufficient foliage to exclude shadeintolerant understory vegetation (Hoffmann et al.
2012a). The absence of savanna understory vegetation
(mostly grasses) greatly reduces ecosystem flammability (Hoffmann et al. 2012b), so we refer to this as
the fire-suppression threshold. The ability of trees to
reach these thresholds is regulated by their growth
rate, which is at least in part dependent on resource
availability. Moreover, the accumulation of biomass
necessary to surpass these thresholds requires substantial uptake of nutrients from soils and if the required
stocks are large relative to availabilities in the environment, transitions to forest would be unlikely.
It has long been hypothesized that vegetation of
dystrophic soils are inherently more fire-prone than
vegetation of fertile soils, because of the slow rates
on which trees establish under limiting conditions
(Kellman 1984). To determine whether this hypothesis
holds, we must consider savanna and forest tree species as separate functional types, evaluating whether
nutrient stocks needed to resist or suppress fires depend on intrinsic species traits. Savanna species produce thick bark, which allows stems to become fire
resistant 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 at
generating a closed fire-suppressing canopy. If these
contrasting traits translate into differences in nutrients
requirements for reaching the fire-resistance and firesuppression thresholds, interacting effects of species
composition 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 trees
growing under similar (nutrient-poor) conditions at
fire-resistance and -suppression thresholds; and (ii)
estimate total arboreal (stem and crown) and soil nutrient stocks of savannas and four different types of
interspersed forests that co-exist in central Brazil, to
determine whether nutrient stocks in savanna ecosystems are sufficient to support a transition to forest. We
address these objectives describing how nutrient
requirements and adaptations to fire disturbance interact, elaborating on whether nutrient availability imposes a definite constraint on forest distribution in mesic
savanna regions.
Plant Soil (2013) 373:829–842
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Material and methods
Study sites
The present study combines some of our previously
published and unpublished data from forests and savannas of central Brazil. Our sites are located within 20
km from the urban limits of Brasilia, in the Brazilian
Federal District at altitudes of ca. 1,100 m above the sea
level. At all sites, the average annual temperature and
rainfall are about 22.5 °C and 1,400 mm, with most of
the precipitation occurring during the (southern) summer. Despite similar climatic conditions, our study sites
encompass vegetation gradients from open grasslands to
dense forests. We focused on typical savannas and adjacent 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 selected
savannas represent the regionally dominant (cerrado
sensu stricto) vegetation, with 20–30 % tree cover and
a continuous grass layer, established over deep dystrophic oxisols (Furley 1999). These savannas have persisted for several thousands of years in close proximity
to forests (Silva et al. 2008, 2010a) with no apparent
limitation imposed by soil physical properties (e.g. texture, density, depth of water table, etc.). The selected
forest sites represent two riparian, one xeromorphic and
one deciduous forest. Riparian forests, adjacent to two
of the savanna sites, are located at the Ecological
Reserve of the Institute of Geography and Statistics
RECOR-IBGE (15°56′S and 47°56′W). These forests
will be referred to as “dry” and “wet” riparian forests, as
they occur along a well-drained and a seasonally
flooded riverbed respectively. The xeromorphic forest
(locally known as cerradão), adjacent to our third savanna site, is located at the EMBRAPA Research
Reserve (15°36′S and 47°42 W). The deciduous forest
is located at the preservation area of CIPLAN Mining
Company (15°33′S and 47°51′W). Savannas are present
at this last site but are associated with unusually shallow
soils and abundant calcareous concretions and, for this
reason, were not included in our analysis.
Sampling design
To compare the nutritional requirements of savanna and
forest trees under the same environmental conditions,
Fig. 1 Leaf area index (Silva et al. 2008, 2010a), tree density,
number of tree species and total basal area (Fonseca and Silva
Junior 2004; Silva Júnior 2004, 2005; Ribeiro and Haridasan
1984; Haidar 2008) at each studied site. These parameters
represent ecosystem-wide estimates and therefore have no associated errors
we sampled 18 pairs of tree species, each consisting of
one forest and one savanna species of the same genus.
To classify each species into forest or savanna types, we
followed the same criteria used by Hoffmann et al.
832
(2005) and Rossatto et al. (2013), based on morphological attributes, herbarium comparisons and previously
published floristic surveys (Mendonça et al. 2008).
Generally, the evolutionary history of each species influence trait variability (Hendry et al. 2011) and phylogenetic differences often appear correlated with resource
use strategies and biomass allocation (e.g. Burns and
Strauss 2012) in plant communities. Here, all 18 congeneric pairs (Supplementary information) were sampled
under nutrient-poor (savanna) conditions. Each of these
pairs belongs to a different botanical family, ensuring
phylogenetic independence when comparing species
attributes and nutrient stocks in relation to their ecosystem of origin (forest or savanna).
Additionally, we sampled species that occur in both
forest and savanna environments, to compare nutrient
requirements of these species across ecosystems. Most
of these species were the same forest species sampled
in savannas for the congeneric comparison described
above, but we also sampled five additional species that
could be found in both ecosystem types, namely:
Agonandra brasiliensis, Copaifera langsdorfii, Qualea
grandiflora, Kielmeyera coriacea, and Myrcia tomentosa; sampling a total of 17 species common to forests
and savannas (Supplementary information) for this
comparison.
These two sets of data permitted the analysis of
differences between savanna and forest trees growing
in a common environment (savanna), as well as between different forests and savanna environments
using tree species common to both ecosystems.
Plant collection and analysis
During May and June of 2007, we collected leaf
and wood samples from three to five individual
trees per species at each site where a species was
present. All sampled trees had stem diameters greater than 10 cm. From every individual we collected
fully expanded mature leaves from the outer (sunlit)
portion of the crown and wood cores at approximately 1.3 m above the ground level. We determined the specific leaf area (SLA), wood density,
leaf and wood N, P, K, Ca, Mg concentrations, of
all sampled trees. Prior to analyses, plant samples
were washed with distilled water, dried at 80 °C,
and milled to a particle size of <1.5 mm. N concentration was determined by the micro-Kjeldahl
method (Allen et al. 1974). We used a mixture of
Plant Soil (2013) 373:829–842
sulphuric, nitric, and perchloric acids (1:10:2) to
digest plant samples, and determined P content
colorimetrically, whereas K, Ca, and Mg were determined by atomic absorption spectrophotometry
(Allen et al. 1974). To calculate SLA, leaf disks
from at least five leaves per individual tree were
measured and dried to constant mass at 60 °C. To
determine wood density, the ratio of dry mass to
fresh volume of radial sections was calculated for
each wood core sampled.
Comparisons between savanna and forest trees
We combined information on SLA, allometry, and
nutrient concentration in the leaf and wood tissue
to estimate total above-ground nutrient stocks of
savanna and forest tree species at their firesuppression (Fig. 2a) and fire-resistance (Fig. 2b)
thresholds.
Following a compilation of field data we determined that the fire-resistance threshold is achieved at
bark thickness of 5.9 mm (Hoffmann et al. 2012a).
This bark thickness ensures a 50 % chance of trees
avoiding topkill in a low-intensity fire characteristic of
Brazilian savannas. For a typical savanna tree species,
this corresponds to a stem diameter of 4.7 cm, while
for forest species this corresponds to a stem diameter
of 10.1 cm (Fig. 2b). Stem biomass at these diameters
was estimated using an allometric equation for forest
trees (Chambers 2001). Although allometric relationships have been published for savanna trees, we use
the same relationship to yield conservative comparisons between functional types. Leaf areas at these
threshold sizes were estimated from the relationships
in Fig. 2a. Crown biomass, here represented by foliage
mass, was estimated by dividing leaf area by the SLA
of each tree. Total nutrient content of the aboveground biomass (stem and crown) for savanna and
forest species was calculated at the individual level,
as the product of estimated biomass and measured
nutrient concentrations.
We used an analogous approach to compare the
above-ground nutrient stocks needed by savanna or
forest tree species to attain a closed-canopy state
corresponding to the fire-suppression threshold. We
previously showed that grasses are eliminated when
overstory leaf area index (LAI) exceeds 3.0, so we
used this value as a reference point for an ecosystem
that has reached a relatively non-flammable state
Plant Soil (2013) 373:829–842
(Hoffmann et al. 2012a, b). We estimated the vegetation nutrient pools at this threshold using the arbitrary condition in which all trees have a stem diameter of 10 cm. According to intrinsic differences in
stem vs. crown biomass allocations between forest
and 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 and
1,800 ha−1) necessary to attain the fire-suppression
threshold (LAI of 3 or 30,000 m2 ha−1).
Comparisons of savanna and forest environments
For each of our study sites, we estimated total
above-ground nutrient stocks, scaling from individual trees to the ecosystem level, by combining
estimates of wood and canopy biomass. Due to
inherent variations in the structure of predominant
trees, different allometric equations are typically
used to quantify wood biomass of forest and savanna ecosystems. Forest-calibrated equations generally
underestimate savanna biomass, while savannacalibrated equations tend to overestimate forest biomass. To address this issue and yield comparable
values, 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:
WB ¼ exp −3:114 þ 0:972ln D2 H
WB ¼ 28:77D2 H =1000
Fig. 2 Allometric relationships between tree diameter leaf area
and bark thickness, measured in forest and savanna species
naturally occurring in savannas. a Fire-suppression threshold,
defined by total leaf area, determined using data compiled from
seedlings saplings, and adults (Gotsch et al. 2010) of forest and
savanna species. b Fire-resistance threshold, defined by
833
where WB (kg ha−1) represents wood biomass, given the average stand height H (m) and diameter D
(cm), calculated from total basal area and tree density at each ecosystem (Fig. 1).
Ecosystem level canopy biomass and nutrient
stocks were estimated using measurements of total leaf
area index (LAI) at each site (Fig. 1). Because LAI is a
dimensionless ratio of leaf area covering a unit of
ground area (m2/m2), we used SLA measurements to
estimate total leaf biomass. Since SLA represents total
area per mass of leaf (cm2 g−1), the ratio between LAI
and SLA provides an integrated estimate of total leaf
mass per unit of ground area. Based on biomass estimates and measurements of leaf nutrient concentration
we calculated whole canopy nutrient stocks, presenting results as average values obtained using data from
all studied species.
Wood and canopy biomass are expressed as total
mass of carbon per hectare, accounting for variations
in wood density and SLA, and assuming carbon content to be 50 % of the total dry mass. We did not use
herbaceous strata in these calculations.
Soil collection and analysis
We used 15 composite soil samples (five subsamples
each), collected at the top 0–20 cm depth, to characterize the surface soil fertility at each site (three savannas and four forest sites). We also characterized deep
soils by pressing 100 cm3 tubes into 10 cm layers of
sequentially dug soil pits, up to 100 cm depth, in soil
profiles evenly distributed across forest-savanna
diameters at which bark thickness prevents tree mortality (Hoffmann et al. 2009, 2012a) at high and low fire intensity scenarios.
In both panels each point represents a single individual tree and
regression lines represent significant relationships (Pearson’s
correlation; p<0.01)
834
transitions. Tubes were inserted so that pressure was
only exerted on the tube walls, thereby preventing soil
compaction and overestimation of soil bulk density.
Ten such profiles were sampled at each transition,
totaling 15 profiles in savannas and five at each forest
ecosystem.
We analyzed soil samples for density using the dry
mass of soil samples, and estimated total stocks of
carbon and nutrient in mass per hectare. We determined total N concentration in soils using the
Kjeldahl method (Bremner and Mulvaney 1982).
Levels of P, K, Ca and Mg were determined by atomic
absorption spectrophotometry using extraction methods (Mehlich and KCl) that allow the measurement of
concentration of nutrients available to plants. Total
organic carbon content was analyzed by wet oxidation
(Walkley and Black 1934). Carbon levels and nutrient
stocks are expressed on a mass basis, after accounting
for variation in soil density, in the surface soil layer
(0–20 cm depth) and integrated to 100 cm depth in soil
profiles.
The amount of a given nutrient existing (or missing) for building a forest was determined by the difference between savanna biomass and soil stocks up to
100 cm depth, and in the above-ground biomass of
each forest ecosystems. Nutrients contained in the
understory vegetation or root biomass were not included in our calculations, but their potential relevance is
discussed.
Results
Savanna: Leaf and wood nutrients as determined
by species origin
When growing in the same environment (savanna),
leaves of forest tree species have significantly higher
concentrations of N (23 %), P (25 %), and K (47 %),
but lower levels of Ca (18 %), than savanna species
(Table 1). Leaf levels of Mg do not differ significantly
according to species origin. Forest trees have significantly greater SLA (27 %), but wood density does not
differ in relation to species origin. Similarly, most
wood nutrients (P, K, Ca and Mg) show no significant
differences between forest and savanna trees.
Significant differences only occur in wood N concentrations, which are higher in savanna than in forest
trees (Table 1).
Plant Soil (2013) 373:829–842
Savanna: Nutrient stocks at fire-resistance
and -suppression thresholds
Our calculations show that, forest species require a
much greater nutrient supply than savanna species to
reach a size at which they can resist fires. Stem stocks
of N, P, K, Ca, and Mg are approximately 5-fold
greater, while crown (foliar) stocks are about one order
of magnitude higher in forest than in savanna species
at the fire-resistance threshold (Fig. 3). To reach the
canopy cover necessary to suppress fires, however,
stands composed entirely of savanna species require
greater nutrient stocks than those composed of forest
species. Due to intrinsically higher allocation to stem
biomass relative to leaves (Gotsch et al. 2010), wood
stocks of N, P, K, Ca, and Mg would be much higher
in savanna than in forest trees at the fire-suppression
threshold. At this threshold, crown stocks would be
similar between forests and savannas, with the exceptions of Ca levels, which are higher in savanna trees
(Fig. 3). In short, compared to forest species, savanna
trees require significantly lower nutrient stocks to
become fire resistant, but need significantly higher
nutrient stock to create a closed canopy that can suppress fires. These effects are quite large despite substantial interspecific variation.
Forests vs. Savanna: Leaf and wood nutrients
of individual trees
When the same species are analyzed across different
ecosystems, leaf N, P, K, Ca and Mg concentrations
vary significantly, with the lowest and highest leaf nutrient levels (and SLA) observed in savannas and riparian forests, respectively (Table 2). Nutrient concentrations are less variable in wood than in leaves. Wood Ca
and Mg content, as well as wood density, do not vary
significantly among ecosystems. Wood N and P concentrations, on the other hand, are higher in savanna
than in riparian forest trees, while K concentration is
highest in the dry riparian forest and no differences are
observed among the other ecosystems (Table 2).
Forests vs. Savanna: Total biomass and nutrient stocks
at the ecosystem level
Above-ground biomass varies widely across ecosystems. Total carbon stocks in the biomass of xeromorphic and deciduous forests (>24 Mg ha−1) is more
Plant Soil (2013) 373:829–842
835
than 4 times greater than in savannas (<6 Mg ha−1)
(Fig. 4). However, soils in these forests have approximately half of the carbon stored in savanna soils (170
and 210 vs. 380 Mg ha−1). Among all studied ecosystems, the largest carbon stocks are observed in riparian
forests, where the high and low ends of the spectrum
are represented by wet and dry forests, with between
78 and 92 Mg C ha−1 stored above-ground and 600 to
1,600 Mg C ha−1 in soils (100 cm depth). In all
ecosystems, the amount of carbon stored in soils is
much higher than in the vegetation.
In forests and savannas, above-ground N stocks
match changes in biomass and increase progressively
across the spectrum: savanna < xeromorphic < deciduous < riparian forests. Total N and available K and
Mg stocks are always higher in soils than in the aboveground biomass of savannas and forests (Fig. 4). Stocks
of P, on the other hand, are higher in the above-ground
biomass of all ecosystems, with the greatest difference
observed in the xeromorphic forest, where the amount
of P stored in the vegetation is about 7 times higher than
available levels measured in soils. Similarly, Ca stocks
are higher in the above-ground biomass than in soils of
savannas and most forest ecosystems. The only exception is the deciduous forest, where available soil pools
are over 10 times higher than total Ca measured in the
vegetation (Fig. 4).
Savanna soils have sufficient nutrients (Fig. 4)
to support a transition to a non-flammable state
(Fig. 3b), when comparing total stocks, we find
that savannas have sufficient N, K, and Mg, but
require additional P and Ca, to support a full
transition to forest (Table 3). The amount of additional P required to build a xeromorphic forest
over savannas is relatively small (3 kg ha−1).
However, Ca deficits to build this same relatively
low-biomass forest are substantial (46 kg ha−1),
representing two thirds of the existing soil stock
in savannas. To build a deciduous forest, this
deficit would increase about five times, while to
Fig. 3 Box plots of total crown (foliar) and stem nutrient stocks
measured averaged over 36 forest and savanna tree species
(Table 1) at the fire resistance and suppression thresholds (Fig.
2). The boxes correspond to the 25th and 75th percentiles, the
line inside the box represents the median and error bars show the
minimum and maximum values. The asterisk (*) shows significant differences (ANOVA, p<0.05) between forest and savanna
species
Table 1 Average values (± standard deviation) of specific leaf
area (SLA), wood density, and macronutrient concentrations, in
leaves and wood of savanna and forest trees co-occurring in
savanna environments. Between 3 and 5 individual trees of 36
species (18 congeneric pairs; Supplementary information) were
analyzed and p-values represent differences (t-test) between
means according to species origin
Savanna species
Forest species
p‐value
N (mg g−1)
11.69±0.62
14.45±0.73
<0.01
P (mg g−1)
0.69±0.04
0.86±0.04
<0.01
K (mg g−1)
4.60±0.37
6.77±0.58
<0.001
Ca (mg g−1)
7.46±0.51
6.05±0.39
0.03
Leaf
−1
Mg (mg g )
SLA (cm2 g−1)
1.76±0.14
1.88±0.14
0.5
54.64±1.83
69.48±1.88
<0.001
Wood
N (mg g−1)
3.61±0.20
2.82±0.20
<0.01
P (mg g−1)
0.55±0.05
0.55±0.02
0.9
−1
K (mg g )
1.80±0.17
1.74±0.14
0.7
Ca (mg g−1)
6.24±0.69
5.75±0.49
0.5
Mg (mg g−1)
0.57±0.07
0.57±0.07
0.9
Density (g cm3)
0.74±0.02
0.76±0.02
0.5
836
Plant Soil (2013) 373:829–842
Table 2 Average values of specific leaf area (SLA), wood
density, and macronutrient levels in leaves and wood of tree
species (3 to 5 individuals of 17 species; Supplementary
Savanna
Xeromorphic
Forest
information) sampled in savannas and at least one forest ecosystem. Letters represent significant differences (Tukey’s HSD,
p<0.05) between ecosystems
Deciduous
Forest
Dry riparian
Forest
Wet riparian
Forest
Leaf
N (mg g−1)
13.41 B
16.14 A
15.72 AB
13.10 B
P (mg g−1)
0.81 B
1.15 A
0.97 AB
0.83 B
1.19 A
K (mg g−1)
6.61 C
11.87 A
10.13 AB
6.30 C
7.03 B
Ca (mg g−1)
6.81 C
7.60 BC
19.57 A
Mg (mg g−1)
1.91 B
2.70 AB
2.56 B
3.66 A
69.97 C
96.57 AB
101.60 AB
90.65 B
2
−1
SLA (cm g )
7.61 BC
14.35 AB
10.89 B
2.74 AB
111.13 A
Wood
N (mg g−1)
2.66 AB
2.89 A
3.36 A
2.69 AB
P (mg g−1)
0.53 A
0.45 B
0.51 A
0.43 B
0.45 B
K (mg g−1)
1.62 B
1.61 B
1.33 B
2.30 A
0.88 B
1.92 B
Ca (mg g−1)
6.38 A
5.15 A
6.01 A
5.21 A
4.48 A
Mg (mg g−1)
2.29 A
0.73 A
0.45 A
0.96 A
0.51 A
Density (g cm3)
0.79 A
0.83 A
0.84 A
0.76 A
0.76 A
develop high-biomass riparian forests additional P
and Ca inputs (>40 and 600 kg ha−1 respectively),
would have to be several fold higher than what is
currently found in savannas.
Discussion
Savanna: Nutrient requirements at fire-resistance
and -suppression thresholds
Our results show that differences in nutritional
requirements affect the ability of forest and savanna
trees to resist and suppress fires. Confirming previous
studies (Hoffmann et al. 2005; Rossatto et al. 2013),
we found that forest species have higher nutrient
content per mass of leaf than their congeneric savanna counterparts, even when growing under
nutrient-limiting conditions (Table 1). Stem nutrient
concentrations are similar between forest and savanna trees, but savanna species allocate more biomass
to stem relative to leaves, requiring a lower nutrient
supply to reach a fire resistant size (Fig. 3).
However, stands composed entirely of savanna species would require over three times more nutrient
capital than those composed of forest species to
produce sufficient leaf area to exclude grasses and
suppress fires. Forest species are able to generate a
closed canopy with lower nutrient capital than savanna species, because of a greater leaf area per
unit of stem biomass (Gotsch et al. 2010).
Consequently, the establishment of forest species
into savannas would favor canopy closure, facilitating a transition to a non-flammable state. This
result corroborates observations that succession of
mesic savanna to forest is associated with the presence of forest species (Geiger et al. 2011; Ratnam
et al. 2011; Silva and Anand 2011), a pattern that
has been previously explained by the higher shade
tolerance of forest trees (Rossatto et al. 2009), but
here receives an alternative explanation.
While the ingression of forest trees may permit
savannas to attain a non-flammable state with lower
nutrient capital than would be required by savanna
trees, reaching this state would also require long intervals without fire. Since fire is common in savannas,
transition to forest is typically interrupted while still in
early stages of succession, when tree cover is susceptible to fire because of high mortality of small stems.
To avoid severe fire damage, trees must reach a fireresistant size, which is more easily attained by savanna
species not only because of their relatively lower nutrient requirements, but also because they have thicker
bark than forest species and become fire-resistant at a
smaller stem size (Hoffmann et al. 2009, 2012a).
Differences in species nutrient requirements and
Plant Soil (2013) 373:829–842
Fig. 4 Carbon and nutrient
stocks at each studied ecosystem. Above-ground estimates were based on vegetation structure (Fig. 1) and
allometric equations and account for interspecific variation in nutrient concentration, wood density, and specific leaf area (Table 2). Soil
stocks account for variation
in density, carbon and nutrient content, of superficial
(0–20 cm) and deep (20–100
cm) soil layers. Bars represent average values and error bars show standard deviation of the average
837
838
Plant Soil (2013) 373:829–842
Table 3 Comparison of savanna nutrient stocks with the
amount needed to build each of the forest types. Top: Measured
stocks in soils (0–100 cm depth) and above-ground biomass of
savannas, and above-ground biomass of four forest ecosystems.
Savanna
Bottom: The difference between total savanna pools and forest
aboveground pools, which represents the excess (or deficit) of
nutrients after building each forest type on savanna sites
Forest biomass
Soils
Biomass
Xeromorphic
Deciduous
Dry riparian
Wet riparian
C
383320
5420
24506
33049
78387
94196
N
15696
62
172
248
463
400
P
9.3
10
23
35
68
86
K
165.4
36
103
106
269
186
Ca
77.8
121
245
426
826
863
72.7
43
39
34
161
102
Total stock (kg.ha−1)
Mg
Stock difference (kg.ha−1)
Savanna (soil + biomass)
Excess after building forests (savanna-forest)
N
15758
15586
15510
15295
15358
P
20
−3
−15
−48
−67
K
201
98
95
−68
15
Ca
199
−46
−227
−627
−664
Mg
116
76
81
−46
13
biomass allocation probably reflect evolutionary adaptations to resource availability and disturbance regimes
characteristic of their original environments (Haridasan
2008; Hendry et al. 2011). Here, these differences define
savanna and forest trees as separate functional types,
supporting the notion that trait divergence decreases
phylogenetic signals (interspecific differences) when
competition for resources regulates community assembly (Burns and Strauss 2012).
After becoming able to resist or suppress fires, the
ability of trees to modify soil properties may be the key
to explain the very slow, but ongoing, process of forest
expansion identified in some ecotonal regions of South
America (Silva et al 2008, 2011; Silva and Anand 2011).
In dystrophic savannas and grasslands, colonizing trees
alter patterns of nutrient cycling and accumulation, triggering biogeochemical feedback loops that increase fertility and lead to further changes in ecosystem structure
and composition (Dahlgren et al. 2003; Rice et al. 1996;
Saha et al. 2009; Silva et al. 2013). Under fire suppression, this effect should be maximized, as forest species
grow faster than their savanna counterparts (Hoffmann
et al. 2005; Rossatto et al. 2009, 2013). Furthermore,
forest species enhancing soil fertility by means of increasing litter quality and quantity (Silva and Anand 2011).
Thus, despite large demand for nutrients, soil fertility
would likely increase following the establishment of forest
communities. In addition, the exclusion of the grass layer
would simultaneously reduce competition for limiting
nutrients and loss from burning. Savanna fires result in
significant losses of nutrients by volatilization or particle
transport, even though part of it returns as dry and wet
deposition (Kauffman et al. 1994).
Forests vs. Savanna: Nutrient stocks and limitations
to forest expansion
Based on what we have seen, differences in soil fertility
commonly found across forest-savanna transitions
(Furley et al. 1992; Silva et al. 2008, 2010a, b), could
be a result of biotic processes that create fertility gradients and facilitate establishment of forest trees, rather
than determined solely by pre-existing edaphic conditions. When the same species are compared across vegetation types, wood density and nutrient concentrations
are fairly consistent, but leaf nutrient concentration and
SLA are always higher in forest sites (Table 2). While
differences in leaf nutrient concentration contribute to
the higher nutrient stocks in forest habitats, this effect is
not large because stem biomass accounts for most (>70
%) of the above-ground stocks of all nutrients (Fig. 4).
At the ecosystem level, the larger stock of nutrients in
forests compared to savannas is, therefore, mostly due to
wood biomass and we found no relationships between
Plant Soil (2013) 373:829–842
soil fertility and leaf or wood nutrient concentrations.
These results emphasize the role of intrinsic species
traits and vegetation structure in generating and reinforcing gradients of resource accumulation, as a result of
a slow redistribution from deep to surface soils through
organic matter deposition.
Our calculations show that savanna soils have
enough nutrients to allow tree communities to attain
fire-resistant and -suppression thresholds (Figs. 3 and
4). However, savannas require additional nutrients to
allow a full forest expansion following initial establishment. Comparing soils and vegetation stocks, we
find that total N in savanna soils is orders of magnitude larger than the amount needed to develop a forest,
supporting the notion that nutrients other than N limit
the distribution of tropical forests (Reich and Oleksyn
2004; Cleveland et al. 2011). Even though this assessment is based on total soil N rather than available
forms, given the high potential for organic N mineralization and symbiotic fixation of tropical soils
(Cleveland et al. 2011), we conclude that soil N would
not impose an absolute constraint on forest development at our study sites. Savannas also have sufficient
K and Mg to develop low-biomass xeromorphic forests. However, additional P and Ca inputs would be
required to support a transition to any forested state.
The amount of additional P required to build a
xeromorphic forest is relatively small and could
perhaps be attained if understory vegetation stocks
were also considered. Previous studies (Castro and
Kauffman 1998) have shown that the above-ground
biomass in open grasslands near our study sites is
about 5.5 Mg ha−1 (ca. 2.8 Mg C ha−1), which represents roughly half of the arboreal biomass of savannas.
The concentration of P in native and exotic grasses
that occur in the region, range from 0.04 to 0.07 %
(Silva and Haridasan 2007), which falls within the
range found in savanna trees (Table 1). At these concentrations, grasses could provide up to 3.9 kg P ha−1,
which would only be sufficient to build a xeromorphic
forest (Table 3). The average concentration of Ca in
grasses (0.2 %; Silva and Haridasan 2007) is, however, much lower than that found in the wood of savanna
trees (>0.6 %; Table 1) and is not sufficient to cover
the deficit of Ca to build a low-biomass forest. Further
Ca inputs, of over one third of the existing stock in the
arboreal biomass of savannas, would be necessary
from atmospheric and erosional deposition, or soil
depths greater than 100 cm, to build a xeromorphic
839
forest. These inputs would, have to be, however, over
one order of magnitude larger to attain high-biomass
states, such as riparian forests.
Stocks of Ca should pose a strong constraint particularly 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 redistribution
could explain the ongoing expansion of riparian forests over savannas (Silva et al. 2008). Among other
essential nutrients, Ca occupies a unique position in
regulating growth from individual trees to entire ecosystems, controlling cell wall synthesis, biomass production and structure of woody tissues (Lautner and
Fromm 2010). Savannas and most forest ecosystems
studied here have larger Ca stocks in the above-ground
biomass than in soil pools, indicating that any interruption on Ca recycling would favor the formation of
less productive (i.e., open) stable states. Stocks of P
show similar distribution and, in contrast with less
limiting nutrients, Ca and P are both found in higher
concentrations at the surface (0–20 cm) than in deeper
soil layers (Fig. 4), suggesting a continuous and rapid
recycling process following litter deposition. The deciduous forest is the only ecosystem where we observed
greater nutrient stocks in soils than in the above-ground
biomass. Its unusual soil fertility originates from the
weathering of shallow parent materials (entisols) and
calcareous concretions often found within less than 0.5
m from the soil surface. Such soils are rare in central
Brazil, where its occurrence is typically characterized by
the presence of deciduous trees (Moura et al. 2010;
Haidar 2008), which under high fertility conditions are
able to outcompete evergreen species that dominate
other forest ecosystems.
Final considerations
We show that interactions between species composition, disturbance, and resource availability favor the
long-term persistence of forest-savanna mosaics. At
our study sites, and probably elsewhere, savanna and
forest trees represent different functional types.
Tradeoffs between nutrient requirements and adaptations to resist fires reinforce savanna and forest as
alternate stable states, with low fertility hindering forest
expansion. Forest species require a larger amount of
nutrients to become fire-resistant, so the combined
840
effect of fire and nutrient limitation should favor the
persistence of savanna communities.When only savanna species are present, the transition to a forested state
requires a larger nutrient supply than is available in the
soil. Canopy closure in this case depends upon the
ingression of forest species, which can facilitate forest
expansion by increasing soil fertility.
The above-ground biomass of savannas and forests at
our sites is lower than measured in other tropical ecosystems. Above-ground carbon stocks of forests in the
Amazon region, for example, range from 155 to 217
Mg C ha−1(Kauffman et al. 1995), whereas the largest
value we observed in any of our forest sites was 95 Mg C
ha−1 (ca. 20 times more carbon than stored in savannas).
Across all ecosystems, soil carbon stocks are larger than
in 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 dependent upon adequate nutrient availability and even though
savannas may occur under high fertility conditions (e.g.
Moura et al. 2010; Haidar 2008; Silva et al. 2010b;), our
results show that the indigenous fertility typical of
Brazilian savannas will not allow widespread forest expansion 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 ha−1) from open grasslands to treedominated savannas near our study sites (Castro and
Kauffman 1998). The exclusion of root nutrient pools
in our study, thus, probably underestimates nutritional
limitations to develop forests. The next phase of understanding will come from manipulations of limiting
resources in fertilization experiments using traceable
nutrients, coupled with quantitative assessments of
changes 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 (Rossatto
et 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 been
indicated as important factors controlling vegetation
distribution in mesic savannas, but their interactions
with 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
Plant Soil (2013) 373:829–842
and logistic support. We also thank Ricardo Haidar, Gabriel
Damasco, Daniel Marra, Gabriel Ribeiro, and Artur Paiva, for
help with field work and species identification, and Timothy
Doane and three anonimous reviewers for valuable comments
on the manuscript. This research is based upon work supported
by the National Science Foundation Grant No. DEB-0542912
(W. H.), AW Mellon Foundation (W. H.), National Science
Foundation 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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