REVIEW

Cerrado vegetation and global change: the role of functionaltypes, resource availability and disturbance in regulatingplant community responses to rising CO2 levels and climatewarming

Augusto Cesar Franco Davi Rodrigo Rossatto

Lucas de Carvalho Ramos Silva

Cristiane da Silva Ferreira

Received: 8 December 2013 / Accepted: 18 December 2013 / Published online: 11 February 2014

The Author(s) 2014

Abstract The cerrado is the most extensive savanna

ecosystem of South America and a biodiversity

hotspot, harboring a diverse flora ([7,000 species)with high levels of endemism. More than 50 % of the

cerrados approximately 2 million km2 has been

converted into pasture and agricultural lands and it is

uncertain how the remaining areas will respond to

increasing pressures from land use and climate

change. Interactions between disturbance regime and

resource (water and nutrient) availability are known to

determine the distribution of the various plant com-

munities, of contrasting structure and composition,

which coexist in the region. We discuss how fire,

nutrients and species traits regulate plant community

responses to rising CO2 and global warming, exploring

constraints to forest expansion into savanna environ-

ments. We describe how climate change will likely

reverse a natural process of forest expansion, observed

in the region over the past few millennia, accelerating

tree cover loss through feedbacks involving fire and

resource limitation, and counteracting expected CO2stimulation effects. These involve changes in funda-

mental processes occurring above and below ground,

which will probably also impact species performance,

distribution and biodiversity patterns. We propose a

conceptual framework for predicting changes on

vegetation structure, highlighting the need for mech-

anistic models to accurately simulate vegetation

dynamics under climate change scenarios. We con-

clude by explaining why an effective research agenda

must necessarily include mitigation efforts, aimed at

minimizing impacts of land clearing through enforced

conservation and restoration policies in natural and

managed ecosystems.

Keywords Forestsavanna transitions Grasstree competition Savanna Vegetationfire dynamics

1 Introduction

Savannas are one of the largest terrestrial biomes,

comprising a dynamic mixture of trees and highly

flammable grasses. At the global scale, they cover

about 19 million km2 (Ramankutty and Foley 1999),

and are subjected to intense conversion to agricultural

and grazing land (Hoffmann et al. 2002). Here we

A. C. Franco (&) D. R. Rossatto C. da Silva FerreiraDepartamento de Botanica, Universidade de Braslia,

Braslia, DF, Brazil

e-mail: acfranco@unb.br

D. R. Rossatto

Departamento de Biologia Aplicada, FCAV, Universidade

Estadual Paulista Julio de Mesquita Filho, Jaboticabal,

SP, Brazil

L. de Carvalho Ramos Silva

Biogeochemistry and Nutrient Cycling Laboratory,

Department of Land Air and Water Resources, University

of California, Davis, CA, USA

123

Theor. Exp. Plant Physiol (2014) 26:1938

DOI 10.1007/s40626-014-0002-6

assess the impacts of human-induced climate change

on the mesic (annual precipitation [1,000 mm),floristically diverse savannas of Central Brazil, known

as cerrado, and considered a biodiversity hotspot,

where exceptional concentrations of endemic species

are being subjected to extensive loss of habitat (Myers

et al. 2000).

Given the expected global scenario of rising CO2levels, warming, increasing incidence of fire events

and of extreme droughts and floods (IPCC 2013), we

focus on plant traits related to carbon balance, and

constraints imposed by fire, water and nutrient limita-

tion. We also consider the three most representative

life forms of the cerrado vegetation (i.e., grasses,

eudicot herbs, and trees), the most prominent vegeta-

tion types (i.e., grasslands, savannas and forests) and

whenever possible, we address the effects of antici-

pated climate scenarios on species physiology, com-

munity dynamics and ecosystem services. We start

with a brief overview of the cerrado vegetation

including the major determinants of vegetation struc-

ture and function, followed by a synthesis of the

probable effects of rising CO2 levels, which will persist

throughout this century. In particular, we address how

fire disturbance, nutrient limitation and species traits

regulate plant community responses to rising CO2levels and climate variability. Next we address the

interactions between elevated CO2 and increasing

temperatures, followed by a discussion on how they

interact with drought events on their impacts on plant

community dynamics in cerrado ecosystems. Further-

more, we propose a conceptual model including

feedback loops and climate forcings to examine the

expected interactions between cerrado plant commu-

nities, soil resources and the atmosphere. Three

regional controls of alternate stable states are repre-

sented: fire, nutrients and atmospheric CO2, in con-

junction with expected effects on vegetation structure.

We conclude with a brief discussion on the impacts of

large-scale anthropogenic fires that are intimately

connected to the accelerated process of land clearing

as a result of the expansion of commercial agriculture,

cattle ranching, reclaiming of abandoned land and land

reform settlements. These are critical issues for cerrado

conservation, given that the current national forest

code of Brazil requires developers in the Amazon to

leave 80 % of the forest intact as legal reserves,

while the requirement to preserve the native vegetation

in most of the cerrado region is only of 20 %.

2 The cerrado of central Brazil: an overview

The cerrado is the second most extensive ecosystem in

South America and within Brazil, it originally covered

about 2 million km2 which accounts for 21 % of the

countrys land area, extending marginally into Para-

guay and Bolivia (Eiten 1972; Oliveira-Filho and

Ratter 2002). It is subject to a regular and predictable

drought period from May to September, which is a

major determinant of ecosystem structure and func-

tion. Average annual temperature is between 20 and

26 C with diurnal temperature ranges of 20 C beingcommon during the dry (winter) season (Eiten 1972).

Frost events are uncommon and occur only at the

southern limit of the cerrado region (Brando and

Durigan 2004). Average rainfall in most of the cerrado

biome ranges from 1,000 to 2,000 mm (Silva et al.

2008a), which characterizes it as a mesic savanna.

However, small enclaves of cerrado vegetation can be

found in drier (600800 mm) or wetter areas

(2,0002,400 mm).

High irradiances, elevated air temperatures and low

relative humidities impose a consistently high evap-

orative demand during the prolonged dry season, when

evapotranspiration greatly exceeds rainfall severely

depleting the upper soil layers of water (Franco 1998,

2002; Quesada et al. 2008). Under such conditions,

however, deeper soil layers remain moist and provide

water to deep-rooted trees even after several months

without rain (Jackson et al. 1999; Goldstein et al.

2008). Most of the cerrado occur on deep well-drained

soils, where leaching and extended periods of weath-

ering have depleted available nutrients. These nutri-

ent-poor, acid soils are characterized by high levels of

aluminum (Al) and iron (Fe). Phosphorus (P) and

calcium (Ca) are particularly limiting elements in

these ecosystems (Lopes and Cox 1977; Haridasan

2000, 2001, 2008).

Distinctive aspects of the savannas of Central

Brazil are the high diversity of grasses, herbs and

woody plants and the large variation in vegetation

structure in the landscape, particularly along topo-

graphic gradients in watersheds. The determinants of

these vegetation forms are mainly edaphic factors and

variations in soil water regime. The most important

edaphic factors are soil fertility (availability of plant

nutrients) and effective soil depth as determined by the

presence of concretions in the soil profile and depth of

the water table to the soil surface (Oliveira-Filho and

20 Theor. Exp. Plant Physiol (2014) 26:1938

123

Ratter 2002; Amorim and Batalha 2006; Franco and

Haridasan 2008; Rossatto et al. 2012). The different

savanna vegetation types differ not only in structure

but also in composition and functioning, as reflected

by species distribution, soil nutrient and water use,

CO2 exchange, productivity and carbon storage above

and below ground (Miranda et al. 1996, 1997; Silva

et al. 2008b, 2010, 2013a; Giambelluca et al. 2009).

In addition to open vegetation types, dense wood-

lands (locally known as cerradao), seasonally decid-

uous or semi-deciduous forests and evergreen gallery

forests are scattered throughout the cerrado region.

Deciduous and semi-deciduous forests commonly

occur on base-rich soils (Oliveira-Filho and Ratter

2002; Silva et al. 2010) while gallery forests typically

occur in narrow bands along streams and rivers in

valley bottoms characterized by nutrient-rich alluvial

deposits (e.g., Oliveira-Filho and Ratter 2002; Ribeiro

and Walter 2008; Silva et al. 2008b). These forests are

usually in contact with savannas forming sharp

transitions zones (Cole 1992; Silva et al. 2009). As

in other parts of the world (see Ratnam et al. 2011 for a

review), sharp forest-savanna boundaries have been, at

least in part, maintained by widespread occurrence of

fires (Hoffmann et al. 2012a), but interactions between

fire frequency and limiting soil resources promote the

long-term stability of vegetation gradients. Tradeoffs

between nutrient requirements and adaptations to fire

observed in forest and savanna trees, for example,

explain the persistence of vegetation mosaics, as low-

fertility limits the advance of forests, but the ingres-

sion of trees into savannas favors the formation of non-

flammable states, increasing fertility and facilitating

forest expansion (Silva et al. 2013a).

At the community level, studies of savanna eco-

systems have focused more on competition for water

and nutrients than on facilitation mechanisms, gener-

ally comparing the ecophysiological performance of

grasses and trees, which are considered the major

components of diversity and dominance in these

systems (Medina and Silva 1990; Haridasan 2008;

Ward et al. 2013). In addition to trees and grasses, the

savannas of central Brazil are characterized by a

diverse herbaceous eudicot flora (Ribeiro and Walter

2008), that plays an important and often overlooked

role in regulating ecosystem structure and function

(Rossatto et al. 2013a). Though not readily distin-

guishable, there are three to five times as many plant

species in the ground layer vegetation than in the

arboreal community (Filgueiras 2002; Gottsberger and

Silberbauer-Gottsberger 2006). Although perennial

grasses are dominants in terms of space occupation

and biomass production in the ground layer, the

taxonomic diversity of legumes and asters is larger

than that of grasses. Most herbs have underground

structures which enable them to resprout after dry

periods or following fire events, also serving as a

means for vegetative propagation (Eiten 1972; Gotts-

berger and Silberbauer-Gottsberger 2006). Neverthe-

less, many herbs remain active rather than dormant

during the dry season, which is the typical behaviour

of perennial grasses in savanna ecosystems (Hoffmann

et al. 2005; Rossatto et al. 2013a).

Overall, any model aimed at evaluating the sensi-

tivity and vulnerability of the cerrado to climate

changes at the regional level has to take into consid-

eration the strong influence of fire, the patchiness of

resource distribution and the diversity of both life

forms and vegetation types. A watershed approach that

takes into consideration the dynamic nature of the

cerrado landscape would be perhaps an effective

framework to understand past and predict future

scenarios for the biome resulting from pressures

imposed by changes in land use, fire regime and

climate.

3 Fire disturbance, nutrient limitation and species

traits regulate community responses to rising

CO2 levels

Changes in CO2 assimilation rates and in stomatal

conductance triggered by increasing CO2 concentra-

tions result in cellular and physiological responses,

which typically enhance growth and reproductive

output (Springer and Ward 2007; Leakey and Lau

2012). Understanding how species and functional

groups diverge with respect to these key characteris-

tics is critical to predict the response of communities

and ecosystems to climate change. Even though it has

been recently suggested that the response to rising

CO2 in natural ecosystems has been globally overes-

timated (Silva and Horwath 2013), elevated CO2 has

been shown to stimulate growth in many C3 and C4plants (Wand et al. 1999; Ainsworth and Rogers

2007), with trees showing higher increases in produc-

tivity and greater reductions in transpiration than any

other functional type (Ainsworth and Long 2005;

Theor. Exp. Plant Physiol (2014) 26:1938 21

123

Huang et al. 2007). The prediction of CO2 effects is

complicated by the fact that responses vary among

species, environmental conditions (such as water and

nutrient availability) photosynthetic pathway and life

form (Owensby et al. 1999; Joel et al. 2001; Poorter

and Navas 2003; Ainsworth et al. 2008; Ghannoum

2009; McMurtrie et al. 2008; Hovenden and Williams

2010; Kgope et al. 2010; Granda et al. 2013; Oliveira

et al. 2013). As it is the case of growth, the largest

increases in reproductive output and in changes in

flowering time have been measured in cultivated C3plants (Jablonski et al. 2002; Springer and Ward

2007). Most (but not all) that exhibited differences in

flowering timing at elevated CO2 display accelerated

flowering. To a less extent, reproductive output of

undomesticated (wild) C3 plants also tend to increase

in response to CO2 enrichment, while flowering-time

responses are more variable (Springer and Ward

2007). The effects are less clear for C4 plants, due to

more limited available information. This is an area in

critical need of additional research, particularly for

wild perennial C4 grasses in which south-central South

America appears to be a major geographic centre of

origin of C4 lineages (Sage et al. 2011). Future studies

stand to gain valuable information from the analysis of

the multiple evolutionary pathways generating C4photosynthesis, the ensuing diversity of metabolic

pathways of CO2 acquisition and of physiological

responses to environmental gradients, which in turn

will play a major role on defining species distribution

patterns under climate change scenarios.

Although it is unfeasible to consider all the

potential genotypic variation in CO2 responses of

cerrado plants, we can group cerrado species into

major functional groups according to their life form,

here defined as trees, herbs and grasses. For simplicity,

we will also group the different cerrado vegetation

types into three major classes: grasslands, where the

ground layer is dominated by a continuous matrix of

shade intolerant C4 grasses and a diverse assemblage

of C3 herbs (here defined as small eudicot plants of

approximately 1040 cm in height, with or without a

small non-ramified stem partially lignified); savanna

physiognomies where the continuous ground layer

vegetation is partially covered by C3 trees and shrubs

of variable density and size; and forest type vegeta-

tion, in which the C3 arboreal component is dominant

and the ground layer vegetation is nearly absent.

Irrespective of the life form, it is reasonable to assume

that high-light and fire-prone grassland and savanna

environments have selected for drought tolerant

species that accumulate more biomass in underground

storage or in clonally spreading organs (Eiten 1972;

Gottsberger and Silberbauer-Gottsberger 2006), while

forest environments favor trees that invest preferen-

tially in leaf area and stem biomass (Hoffmann and

Franco 2003), and are resilient to occasional incursion

of fire, despite being unable to colonize frequently

burned savanna (Hoffmann et al. 2009).

As in other mesic savannas, the cerrado is charac-

terized by intense and rapid surface fires (Miranda

et al. 2002) and typical ranges of stem charring height

(as an estimate of flame height) are from 0.8 to 3 m

(Frost and Robertson 1987; Williams et al. 1998;

Hoffmann et al. 2009). Most leaves and tree branches

are not burnt but damaged by the hot air flow during

the fire. Leaf scorch height can be 36 times higher

than stem char heights (Williams et al. 1998; Gambiza

et al. 2005). These scorched leaves are dropped and a

new crop of leaves has to be produced. Stems of many

cerrado trees are not killed during fire events but

resprout epicormically in response to fires. Indeed,

bark thickness has been found to be a better and more

universal predictor of stem death than tree height

(Hoffmann et al. 2009; Lawes et al. 2011a, b; Brando

et al. 2012). We can therefore assume that cerrado tree

saplings will be kept in a suppressed state by repeated

episodes of topkill and resprouting, unless they have

accumulated sufficient bark during fire-free intervals

to avoid stem death or enough canopy (typically a

community process) to arrest the spread of subsequent

fires by preventing the development of the flammable

grass layer (Hoffmann et al. 2012a; Silva et al. 2013a).

The ability of plants to resprout under frequent

burning is dependent upon carbohydrate and nutrient

reserves, which have to be replenished between burns.

As a consequence of the short residence time of the fire

front, changes in soil temperature are small (Miranda

et al. 2002). Cerrado trees can increase the chance of

surviving and of reaching fire resistant sizes by

building below-ground reserves of carbon and nutri-

ents that promote rapid growth and that are not lost

during fire events. Growth rates of cerrado trees to fire-

resistant sizes may be particularly sensitive to CO2 as

the replacement of stem tissue and investment in

storage organs should be enhanced under elevated

CO2 by increasing pre-burn carbohydrate reserves and

increasing the rate at which carbohydrate reserves are

22 Theor. Exp. Plant Physiol (2014) 26:1938

123

replenished following fire (Drake et al. 1997; Hoff-

mann et al. 2000; Kgope et al. 2010; Bond and

Midgley 2012).

Stem loss by fire results in large losses of carbon,

whereas stem persistence and epicormic sprouting

sustain rapid full canopy recovery (Crisp et al. 2011),

which would promote the expansion of the cerrado

tree layer under rising CO2 conditions. However, the

nature and intensity of tree responses vary among

species and depend on the availability of limiting

resources (Joel et al. 2001). Nutrient availability of

cerrado soils is considered critically low, particularly

with regard to P and Ca (Lopes and Cox 1977). Low-

nutrient conditions usually cause a reduction in plant

responses to CO2 enrichment (Lovelock et al. 1998;

Joel et al. 2001; Poorter and Perez-Soba 2001).

Positive responses of C3 species in terms of growth

and biomass increment under elevated CO2 are better

characterized when nutrients are non-limiting (Curtis

and Wang 1998; Poorter 1993; Dijkstra et al. 2002). If

nutrients rather than carbohydrate reserves limit

growth and resprouting potential of cerrado trees,

elevated CO2 would have a limited effect. In addition

to experimental studies to characterize the response of

cerrado plants to elevated CO2 and nutrients, future

studies would benefit from examining the contribution

of the large pulse of nutrients into superficial soil

layers following fire (Batmanian and Haridasan 1985).

This could potentially compensate for the inherently

low nutrient status of the soils, permitting enhanced

resprouting under elevated CO2, but remains to be

verified. This effect would also depend on the timing

of resprouting (Bustamante et al. 2012), which might

change among species and life forms. In periodically

burned open cerrado vegetation, alkalinization and

fertilization effects on surface soil layers promoted by

ash deposition can persist for a few years (Pivello et al.

2010), but it remains unclear whether these can

significantly enhance resprouting and affect patterns

of vegetation recovery. However, increases in fire

frequency reduce the amount of nutrients in the

aboveground biomass at least for open savanna

vegetation in the cerrado (Oliveras et al. 2012)

It is perhaps more important to know if, given a

sufficiently large fire-free interval, savanna trees

would be able to develop a canopy dense enough to

suppress the flammable, shade intolerant grass layer.

In fact, stands comprised solely of savanna trees may

be incapable of forming a canopy that is sufficiently

dense to exclude savanna grasses entirely (Hoffmann

et al. 2005; Ratnam et al. 2011) due to shade

intolerance, open crown shape and the greater amount

of nutrients that they require in order to develop a

closed canopy in comparison to forest trees (Silva

et al. 2013a). However, elevated CO2 concentration is

expected to reduce the light compensation point of

photosynthesis, enhance photosynthetic capacity and

increase the photosynthetic nitrogen use efficiency

(Hattenschwiler 2001; Sefcik et al. 2006), thereby

allowing plants to support a larger leaf area in any

given community (Valladares et al. 2008). Although

this would benefit savanna and forest trees, the

enhancement should be greater in forest trees, which

show a higher biomass allocation to leaves and stems

(Hoffmann and Franco 2003). Forest trees tend to have

higher leaf area than savanna trees of similar size,

which is manifested as both broader and denser

crowns (Hoffmann et al. 2005; Rossatto et al. 2009;

Gotsch et al. 2010). Savanna trees have slow growth

and low specific leaf area (SLA) in contrast to high

growth rates and high SLA of shade-intolerant species

from moist forests.

Dry, fire-prone savanna environments impose fun-

damentally different tradeoffs and constraints than do

moister gallery forests (Poorter 2009). Specifically,

shade-intolerant species of moist forests are generally

pioneers, which depend on high growth rates to exploit

an ephemeral high-light environment, while savanna

trees grow in a lasting high-light environment that

requires a strategy of persistence under frequent

damage by fire (Bond and Midgley 2000). The

allocation to storage presumably has a cost of reduced

growth (Bond and Midgley 2000; Barros et al. 2012),

making savanna trees unsuited for colonizing short-

lived gaps in forest. The factors that select for

maximization of height growth are probably not the

same in these two environments; among forest

pioneers, growth in height should be particularly

important for overtopping competing vegetation

(Poorter et al. 2006), while for savanna trees, height

would reduce fire damage to the canopy (Archibald

and Bond 2003). Therefore, where forest species are

present, canopy closure and the suppression of the

flammable grass layer should be more rapid and

nutritionally less expensive than where only savanna

species are present. This reasoning is supported by

published descriptions of changes in vegetation in fire-

protected savannas, which indicate that the transition

Theor. Exp. Plant Physiol (2014) 26:1938 23

123

to forest is universally associated with the ingression

of forest tree species (Bowman and Fensham 1991;

San Jose et al. 1991; Swaine et al. 1992; Russell-Smith

2004; Hennenberg et al. 2005; Pinheiro and Monteiro

2006; Geiger et al. 2011), although it is difficult to

ascertain whether succession to forest is absolutely

dependent upon the presence of these species. How-

ever, it is evident that the thinner layer of protective

bark and higher rates of topkill than savanna species

would restrain the establishment of forest species in

savanna ecosystems subject to frequent fire (Hoff-

mann et al. 2009), particularly at the seedling or

juvenile stage (Gignoux et al. 2009) or when burned

repeatedly (Fensham et al. 2003). Thus, CO2 enrich-

ment could increase the rate of forest expansion into

the neighboring savanna physiognomies, mainly fol-

lowing fire suppression or a strong reduction in fire

frequency.

It is important to note that different forest types

occur throughout the Cerrado region and they may be

subjected to different environmental pressures that

might constrain or enhance forest expansion into

neighboring savanna physiognomies. Whether

edaphic characteristics would prevent substantial

forest expansion into savanna in the absence of fire

across the entire cerrado region is still unresolved. The

retreat of deciduous forest and the stability of the

xeromorphic forest (Silva et al. 2010) contrast with

research that documented the expansion of riparian

forests over savannas in Central Brazil (Silva et al.

2008b), and in the Amazon and Atlantic forests in

northern and southern Brazil respectively (Martinelli

et al. 1996; Pinheiro and Durigan 2009; Dumig et al.

2008). In the case of cerrado ecosystems, the expan-

sion of gallery (riparian) forests into the neighboring

savannas deserves special attention and scientific

interest. The large perimeter to area ratios of gallery

forests implies that any small incremental expansion

of forests into savanna would result in a relatively

large increase in forest area (Silva et al. 2008b) and,

consequently, in above and below ground carbon and

nutrient stocks (Silva and Anand 2013a; Silva et al.

2013a).

As mentioned earlier, the advance of forests into

savanna-type environments depends not only on

shifts in species composition (here represented by

the two different functional types) but the presence

of sufficient nutrients to allow forest expansion. The

scant available information suggests that forest

species require a larger nutrient supply to reach a

fire-resistant size than savanna species, whereas

forest species require a lower nutrient supply to

attain closed canopies and suppress the spread of

fires (Silva et al. 2013a). It seems there are enough

nutrients in these soils to support savanna woodland,

but it would require additional P and Ca to build

high-biomass forests with a sufficiently dense tree

canopy to suppress the grass layer, and allow full

forest expansion into the savanna (Silva et al.

2013a).

However, fires result in significant losses of nutrients

by volatilization or particle transport, even though part

returns as dry and wet deposition (Kauffman et al.

1994). A large fraction of biomass N is often lost during

fires, depleting the pool of actively cycling ecosystem N

and resulting in N limitation. Pellegrini et al. (2014)

provide evidence for high carbon sequestration poten-

tial with forest encroachment on savanna but that

nitrogen limitation may play a large and persistent role

in governing carbon sequestration on savanna or other

equally disturbed tropical landscapes. Patterns may be

even more complex and difficult to predict on land-

scapes that have been managed for pasture or agricul-

ture for several years, eventually abandoned for

economic reasons and are being recolonized by a low-

diverse assemblage of native savanna and exotic

species that resembles a savanna in terms of vegetation

structure. In addressing tropical vegetation transitions it

is clearly important to distinguish between native

species-diverse ecosystems and low-diverse vegetation

of similar structure (Veldman and Putz 2011). The

disruption of the biogeochemical processes, nutrient

imbalances because of fertilization or nutrient removal

and changes in soil physical properties that are brought

about by farming activity are just a few of the

uncertainties that have to be faced to project the

impacts of future climate scenarios on the recovery of

degraded savanna landscapes. This is particularly

relevant given the strong possibility that these highly

modified landscapes would be colonized by a low

diverse assemblage of native and exotic species, where

more fertile soils are more likely to be colonized by few

highly productive exotic grasses rather than native

cerrado species (Veldman and Putz 2011; Silva et al.

2013b).

The effects of rising CO2 levels are more challeng-

ing to predict in cerrado grasslands, which generally

contains a diverse flora of shade intolerant C4 grasses

24 Theor. Exp. Plant Physiol (2014) 26:1938

123

and C3 herbs. Even though C3 herbs would not be able

to exclude grasses by overtopping or achieving a fire-

resistant size, elevated CO2 may enhance resprouting

following fire events or after drought, as discussed in

the previous paragraphs. In particular, the diverse

assemblage of legumes that are part of the cerrado

groundlayer vegetation have the potential to maximize

the benefit of elevated CO2 by matching stimulated

photosynthesis with increased N2 fixation (Rogers

et al. 2009). Based on d15N measurements, Sprentet al. (1996) presented some evidence that N fixation

by nodules is a significant N source for small

nodulated legume shrubs and herbs of the cerrado.

Tripartite symbiosis (Rhizobiummycorrhizal fungi

legume) were reported in hemicryptophyte legumes of

Trachypogon savannas in Venezuela (Medina and

Bilbao 1991). However, it is not known how effective

this symbiosis is in reducing P deficiency in these

small legumes under natural conditions. This greatly

limits characterization of the environmental condi-

tions under which N2 fixation can or cannot be

stimulated at elevated CO2. Given the nutrient-poor

status of the soils, feedback effects of nutrient

limitation on N2 fixation and photosynthesis have to

be considered in future studies. The effectiveness of

mycorrhiza-Rhizobium associations to enhance

legume growth at elevated CO2 in cerrado grasslands

has yet to be quantitatively assessed. Shifts in the

composition and in species dominance of the grass

community may occur, because individual C4 native

grass species may react differently to CO2 enhance-

ment and C3 grasses are present in open cerrado

physiognomies (Klink and Joly 1989). In fact, some C3grasses like Echinolaena inflexa (Poir.) Chase can be

locally abundant. On the other hand, cerrado grass-

lands are amenable to long-term free air CO2 enrich-

ment (FACES) experiments which are much more

difficult and expensive to be installed in savanna or

forest formations.

Finally, any projections of the effects of elevated

CO2 on cerrado ecosystems has to consider the effects

of invasive species. Fire-tolerant exotic grasses have

invaded fire-prone systems in many parts of the world,

resulting in modified fire regimes and substantial

negative effects on native vegetation (DAntonio et al.

2000; Rossiter et al. 2003; Douglas and OConnor

2004; Foxcroft et al. 2010). Many of these exotic

grasses are fast growing and fire-tolerant, producing

large amounts of highly flammable fuels, increasing

fire intensity, frequency and spread (Ziska et al. 2005).

Although species-specific responses do occur, in

general the biomass of invasive exotic grasses is

greater than that of native species when they were

subjected to elevated CO2 (Smith et al. 2000; Nagel

et al. 2004) or CO2 and burning (Tooth and Leishman

2013). Elevated CO2 promotes germination, seedling

size and biomass accumulation in adult plants of

Melinis minutiflora (Baruch and Jackson 2005), an

introduced African grass which is abundant in richer

soils near gallery forests in Central Brazil. There is

some evidence that the presence of this grass nega-

tively affects woody plant regeneration and increases

fuel accumulation probably slowing the rate of gallery

forest expansion into the savanna (Hoffmann et al.

2004).

However, not all invasive species respond to

elevated CO2 by enhancing biomass accumulation.

The native fern, Pteridium aquilinum, has recently

become invasive at many wet gallery forest edges.

Individuals of this species remain upright following

senescence, generate high loads of fine fuels and are

favored by fires (Alonso-Amelot and Rodulfo-Baech-

ler 1996; Silva and Matos 2006). Elevated CO2 had

little impact on the growth or allocation of dry mass in

Pteridium aquilinum that were kept in containers in

controlled-environment glasshouses (Whitehead et al.

1997; Caporn et al. 1999). In contrast to the small

effects of high CO2, the high nutrient treatment caused

a three-fold stimulation of total plant dry mass and an

increase in the allocation of dry mass to aboveground

when compared with low nutrient grown plants

(Caporn et al. 1999).

In summary, the complex mosaic structure of the

cerrado vegetation, the high species diversity and the

inherently low nutrient stocks in the soil and in the

biomass create the potential for highly variable

ecological impacts of rising CO2 levels across the

landscape and over a wide range of timescales.

Furthermore, any evaluation of CO2 effects in cerrado

ecosystems cannot be studied in isolation from rainfall

seasonality and the frequent disturbances by fire. It

should also incorporate direct anthropogenic impacts,

and the ensuing spread of highly productive exotic

species, that can adversely affect and even disrupt

biophysical and biogeochemical cycles and self-rein-

forcing feedback loops and therefore drive the

conversion of the species-rich cerrado vegetation

types into low diversity systems.

Theor. Exp. Plant Physiol (2014) 26:1938 25

123

4 Interactions between global warming and rising

CO2 levels: the importance of experimental

ecophysiology

The current increase in atmospheric CO2 concentra-

tions and climate warming are predict to act in concert

to produce major impacts on ecosystems around the

world (Norby and Luo 2004; Warren et al. 2011;

Hickler et al. 2012). Elevated CO2 has been shown to

stimulate photosynthesis and reduces stomatal con-

ductance in most plant species, with woody plants

being the most responsive functional type (Ainsworth

and Long 2005). All other responses, including

accelerated growth and flowering, changes in biomass

allocation and declines in foliar N concentration,

result from increases in C supply and its interaction

with water loss through transpiration. However,

warmer temperature can affect all biological pro-

cesses, including those that respond primarily to CO2levels (Norby and Luo 2004). Projected increases in

CO2 are thought to be spatially uniform, but temper-

ature is projected to rise more or less depending on

location (e.g., altitude and latitude; IPCC 2013).

Importantly, the degree of uncertainty regarding

climate warming that will occur in future years is

much larger than that of future CO2 concentrations.

The consensus is that both variables will move in the

same direction, showing the same positive association

observed in over the past millennia in decades to come

(IPCC 2013). However, even slight increases in

temperature can have cumulative effects over time,

significantly affecting growth and ontogenetic devel-

opment (Morison and Lawlor 1999).

Irrespective of the broad biological effects of

temperature, it is reasonable to anticipate that at the

plant level, the interplay between photosynthesis,

photorespiration and respiration are key processes that

will be affected by global warming and rising CO2levels. Interactions between these fundamental pro-

cesses will likely define how much carbon is available

for plant growth and for resprouting in the event of

drought or fire, which are not only common events in

neotropical savannas but accelerated fire frequencies

and prolonged droughts are expected scenarios under

global warming (Hoffmann et al. 2002; Hirota et al.

2010; Silva and Anand 2013a). As any biological

phenomena, these physiological processes have a

temperature optimum, and can decline rapidly with

further increases in temperature. Hence, warmer

temperature might have either positive or negative

effects on growth and carbon storage depending on

whether the current temperature is above or below the

optimum and the acclimation potential of the studied

species, plant community or ecosystem.

We argue that the predicted increase in CO2 levels

will probably offset any increase in photorespiration

caused by higher temperatures. However, our under-

standing of the temperature responses of C3 and C4photosynthesis across thermal ranges that do not harm

the photosynthetic apparatus, are still not complete.

There is controversy over the limiting processes

controlling photosynthesis at elevated temperature.

In C3 plants, the reduction in photosynthesis at

supraoptimal temperatures is a function of either

declining capacity of electron transport to regenerate

RuBP, or reductions in the capacity of Rubisco

activase to maintain Rubisco in an active configura-

tion. In contrast, the mechanisms controlling photo-

synthesis in C4 plants at elevated temperature are still

unclear (Sage and Kubien 2007; Sage et al. 2008).

Biochemical and gas exchange assessments can

unravel these processes and are currently critical for

a better assessment of temperature effects on photo-

synthesis of cerrado species. It is evident that the same

set of species or functional groups should be chosen to

obtain the temperature dependence of respiration;

however leaf respiration is not the only factor to be

considered. Whole-plant respiration should be evalu-

ated and their temperature dependence, which is much

more complicated to obtain, particularly for trees.

Moreover, if nighttime temperatures increase more

than daytime temperatures (Karl et al. 1993; Horton

1995), maintenance respiration in plants could

increase (Ryan 1991; Griffin et al. 2002), thus

increasing the ratio of dark respiration to photosyn-

thesis and decreasing plant growth. Because of the

larger investment in non-photosynthetic tissues, trees

should be more affected than grasses or herbs.

Therefore, biochemical and gas exchange assessments

have to be combined with growth (biomass) measure-

ments to better evaluate the impacts of warming on

plant carbon balance, particularly on the build-up of

plant reserves to support resprouting and growth to

fire-proof sizes.

It is of course not possible to perform these types of

analysis for all cerrado species. We suggest that

studies should at least be performed with a represen-

tative group of species of cerrado trees, herbs and C3

26 Theor. Exp. Plant Physiol (2014) 26:1938

123

and C4 grasses, which are the dominant life forms of

the cerrado. These studies will be particularly valuable

if they take into consideration intraspecific trait

variability and phylogenetic relationships (Hoffmann

and Franco 2003; Batalha et al. 2011, Rossatto 2011;

Cianciaruso et al. 2012). Moreover, given the on-

going colonization of savanna habitats by forest trees

in the Cerrado, particularly on fire-protected sites

(Pinheiro and Monteiro 2006; Pinheiro and Durigan

2009; Geiger et al. 2011), it is also critical to compare

the temperature response and acclimation potential of

photosynthesis of savanna and forest trees under

current and elevated CO2 levels. Phylogenetic studies

suggest that savanna species have evolved from forest

species over the past 10 million years or so (Simon and

Pennington 2012). As a result, many tree genera from

different taxonomic families currently contain both

savanna and forest species, allowing for comparative

studies aimed at understanding the different selective

pressures to which these two contrasting types of

vegetation are subjected. Using congeneric species

pairs can ensure phylogenetic independence, an

important condition for inference in comparative

studies (Felsenstein 1985), and improves the statistical

power of comparisons between the two groups when

there is a large amount of variation among genera

(Garnier 1992; Ackerly 1999). These comparative

studies can be expanded by including a small number

of species that play a particularly important role in

early stages of forest expansion and are better

characterized as intermediate based on their distribu-

tion across the forestsavanna boundaries (Geiger

et al. 2011). They either occur frequently in both

savanna and forest, or are typical of mixed habitats,

such as forest edges or cerradao, a dense, tall

woodland physiognomy in which both savanna and

forest species are present (Pinheiro and Monteiro

2006; Walter 2006).

Ecosystem-scale warming and elevated CO2 exper-

iments are constrained by technological limitations,

high installation and maintenance costs. Limitations

on the number of experimental units, due to financial,

technological constraints, or space availability often

result in insufficient statistical power to detect inter-

active effects of CO2 enrichment and warming (Norby

and Luo 2004). Nonetheless such experiments are

important for testing concepts and provide new

insights demonstrating the reality of multiple-factor

influences. However, we should keep in mind that the

net effect of elevated CO2, warming, and their

interaction on ecosystem structure and function is

the result of many contributing processes. Responses

will vary in magnitude and direction depending on

many site-specific factors (Norby and Luo 2004).

5 The impact of climate warming and extreme

drought events on community dynamics

Although fire play a major role in determining the

distribution of savanna and forest formations in the

seasonal tropics, this effect is not necessarily present

every year and well-designed policies can be effective

in reducing fire frequencies and to promote its use as a

management tool (Durigan and Ratter 2006). In

contrast, seasonal drought occurs every year, subject-

ing the vegetation to a prolonged period of water

stress, and extreme events of drought are predicted to

become increasingly frequent, particularly at the

northeastern boundaries of the cerrado region, where

more arid conditions prevail and the effects of small

decreases in precipitation may be severe (Hirota et al.

2010). Examples are available at the global scale of

impacts on the vegetation of change in water avail-

ability driven by climate fluctuations in recent geo-

logical past. For instance, during the last glacial

period, the ice buildup in the northern hemisphere led

to displacement of the monsoon system in lower

latitudes, but systematic glacier retreat that followed

the mid Holocene warming led to increased water

input in lower latitudes (Vimeux et al. 2009; Strikis

et al. 2011). This phenomenon could explain the

delayed expansion of evergreen forests and the retreat

of tropical deciduous forests, which attained their

greatest distribution during the last glacial period, but

lost areas during the late Holocene (Ledru et al. 1998;

Silva et al. 2010). This conclusion is further supported

by descriptions of ecophysiological performance of

tree species adapted to either forest or savanna

ecosystems (Saha et al. 2008; Rossatto et al. 2009,

2013b).

At the regional scale, drought-induced tree death

seems to be a natural phenomenon in savannas and other

water-limited environments worldwide (Fensham et al.

2009; Hoffmann et al. 2012b). In the more xeric

savannas, rainfall deficit over several years results in the

exhaustion of soil moisture reserves (Bowman and Prior

2005; Fensham and Fairfax 2007), increasing the risk of

Theor. Exp. Plant Physiol (2014) 26:1938 27

123

drought-induced tree death, whose effects can be

exacerbated by global warming (Rice et al. 2004; Allen

et al. 2010). Hydraulic failure and carbon starvation are

the two most common, non-excluding mechanisms that

are raised to explain large-scale patterns of tree

mortality (Allen et al. 2010). The hydraulic failure

hypothesis postulates that extreme drought and heat

events results in reduced soil water supply coupled

with high evaporative demand, which causes xylem

conduits to cavitate (become air-filled), stopping the

flow of water, desiccating plant tissues and leading to

tree death (Rennenberg et al. 2006; Zweifel and

Zeugin 2008). The carbon starvation hypothesis

predicts that that plants respond to extended periods

of water stress with stomatal closure to prevent

hydraulic failure. The consequent reduction in pho-

tosynthetic uptake of carbon results in metabolic

limitations that lead to carbon starvation and reduced

ability to defend against attack by biotic agents such

as insects or fungi (McDowell et al. 2008, Breshears

et al. 2009; Adams et al. 2009). This process may be

exacerbated by photoinhibition or increased respira-

tory demands associated with elevated temperatures

during drought. Therefore, carbon starvation is

hydraulically driven but non-hydraulic mechanisms

also contribute (McDowell et al. 2008).

In mesic savannas on deep well-drained soils, the

exhaustion of deep soil moisture is less probable and

increased atmospheric CO2 may allow for more

sustained increases in the dominance of woody plants

(Fensham et al. 2009). However, tree seedlings or

shallow rooted herbs could be particularly susceptible

to extreme drought events because they did not have a

deep root system that would allow access to more

stable soil water reserves (Hoffmann et al. 2004;

Rossatto et al. 2013a). On the other hand, C4 grasses

are particularly well-suited to overcome extended

drought periods, as explained in the previous section.

However, the dry period in the cerrado region extends

from late spring to the end of the winter. Increasing

aridity and warming would decrease the amount of

water available to herbs and grasses in the form of

dew. There is some evidence that dew is an important

source of water for cerrado grasses and herbs (Oliveira

et al. 2005; Rossatto et al. 2013a) and increasing

aridity could reduce water condensation during the

cold period of the night, which occur in the majority of

days during the dry season in the cerrado (Hoffmann

et al. 2012b; Rossatto et al. 2013a).

The balance between forest expansion and forest

retreat into savanna might also be strongly affected by

extreme drought events and warming. The available

evidence suggests that forest tree species are more

sensitive to drought than savanna trees, particularly

when they invade savanna environments (Hoffmann

et al. 2004; Rossatto et al. 2009, 2013b). Although

seedlings of forest trees are able to colonize savanna

environments (see previous sections), their establish-

ment success is low, even in fire-protect sites. The low

survival of forest species in the savanna appears

related to drought stress, as seedlings of forest species

had lower predawn leaf water potential than savanna

species (Hoffmann et al. 2004). Seedlings of savanna

species have greater root: shoot ratios and root total

nonstructural carbohydrate (TNC) concentration, par-

ticularly among evergreen genera, which may largely

determine resprout capacity (Hoffmann et al. 2004).

Moreover, differences in biomass allocation affect

the ability of forest and savanna trees to maintain

water balance during the dry period. In general, adult

savanna trees had higher Huber values (sapwood area:

leaf area) relative to forest species, conferring them a

greater transport capacity on a leaf area basis, while

forest trees have a lower capacity to maintain homeo-

stasis in leaf water potential due to greater allocation

to leaf area relative to savanna species (Gotsch et al.

2010). These differences in water stress susceptibility

were confirmed by studies of hydraulic traits. Hydrau-

lic vulnerability curves of stems and leaves indicated

that leaves were more vulnerable to drought-induced

cavitation than terminal branches in both forest and

savanna trees (Hao et al. 2008). However, savanna

species took longer for their leaf water potentials to

drop from predawn values to values corresponding to

50 % loss of maximum leaf hydraulic conductance or

to the turgor loss points, suggesting that these species

have greater buffer capacity with respect to changes in

leaf water potential.

Radial growth of forest trees, an important aspect

related to forest expansion into savanna (Rossatto

et al. 2009; Hoffmann et al. 2012a), is particularly

susceptible to changes in rainfall. In a field study using

12 congeneric species pairs, each containing one

savanna species and one forest species, Rossatto et al.

(2009) reported that radial growth was tightly coupled

to monthly rainfall in forest species whereas the

growth of savanna trees generally ceased before the

end of the wet season. This implies that forest trees are

28 Theor. Exp. Plant Physiol (2014) 26:1938

123

more dependent on current rainfall for growth and

should be more sensitive to episodes of extended

drought. Savanna trees in turn cease above-ground

growth at a time of active photosynthesis which may

reflect a shift in allocation to root biomass and storage.

Although forest and savanna trees do not show

much difference in minimum and maximum values of

leaf water potential, this was achieved by a stronger

regulation of stomatal conductance and of CO2assimilation on an area basis in forest trees, particu-

larly toward the end of the dry season (Rossatto et al.

2013b). This suggests that forest trees invading

savanna would be more susceptible to develop carbon

deficits and metabolic limitations that lead to carbon

starvation and reduced ability to defend against attack

by biotic agents. Moreover, forest trees are more

susceptible to top kill by fire than savanna trees

(Hoffmann et al. 2009).

Thus, extreme drought events that are predicted by

climate change projections for tropical regions could

counteract the positive effect of increasing CO2 in

promoting forest tree colonization of savanna envi-

ronments, particularly under frequent fire disturbance

intervals and warmer temperatures that would further

prevent the build-up of enough plant reserves to

support resprouting.

6 Feedback loops and climate forcings: expected

interactions between plants, soils

and the atmosphere

The processes described in the recent literature can be

summarized in a conceptual model (Fig. 1), where we

describe positive (?) and negative (-) climate

forcings regulated by savannas and forests. The

relative magnitude of these effects is described

qualitatively as weak, moderate or strong (Bonan

2008, Silva and Anand 2013a). Three regional controls

of alternate stable states are presented; namely, fire

(Hoffmann et al. 2012a), nutrients (Silva et al. 2013a,

b) and atmospheric CO2 (Higgins and Scheiter 2012),

alongside expected effects on vegetation structure.

The direction of these relationships should hold

regardless of changes in climatic patterns. For exam-

ple, global warming and drought are expected to

exacerbate the effect of natural fires, but the effect of

fire on vegetation structure is unidirectional (Fig. 1),

by maintaining it in an open, highly flammable state.

Hence, temperature and precipitation are not included

in the model. The same holds for nutrients and

atmospheric CO2. Facilitation mechanisms, which

involve increases in soil fertility that allow the

establishment of woody species, are necessary to

allow transitions from savannas to forests (Silva and

Anand 2011; Silva et al. 2013a, b). Rising CO2 levels

are expected to increase water use efficiency of C3plants, shifting the balance between C3 and C4 species

in herbaceous and woody communities.

We argue that species coexistence within commu-

nities depend on the ability of plants to adjust their

ecophysiological performance (Valladares et al.

2007). Facilitation represents the main organizing

force within communities undergoing environmental

stress, while the importance of competition increases

under low stress conditions (Callaway 1997; Callaway

et al. 2002). Shifts in predominant interactions are

therefore intrinsically linked with species ecophysio-

logical performance. By overcoming stressful condi-

tions, a single or a group of species can assure the

perpetuation or promote migration of entire ecosys-

tems. For example, the conifer Araucaria angustifolia

is known for colonizing grasslands, creating suitable

habitats for the establishment of other woody taxa in

Southern Brazil (Oliveira and Pillar 2004; Duarte et al.

2006). This species is not a good competitor in dense

forests (Franco et al. 2005), but by establishing along

borders it allows the long-term persistence of forest

patches, promoting forest expansion under favorable

climatic conditions (Silva et al. 2009; Silva and Anand

2011). Analogous pathways are possible in the cerrado

where many forest tree species are able to establish in

savanna-type environments (Rossatto et al. 2009). The

development of new analytical tools to determine how

individual species interact at distribution limits (e.g.,

forest patches, forestsavanna transitions) is therefore

critical to understand the mechanisms driving

responses of cerrado plant communities to atmo-

spheric change and their interaction with the climate

system (Silva and Anand 2013b).

At the community level it is already possible to

predict some general effects of warming and elevated

CO2 based on a paleoecological perspective and

current physiological evidence. Expansion of C4grasses in the late Miocene (10-6 MYa) is proposed

to result from increased aridity, seasonality, fire

frequency and low CO2 concentrations (Sage et al.

2012; Stromberg 2011). In fact, Sage et al. (2012)

Theor. Exp. Plant Physiol (2014) 26:1938 29

123

suggest that high photorespiration was the main driver

of C4 evolution and that low humidity, drought, high

light, low CO2 and elevated temperatures are contrib-

uting factors, particularly in combination. When

contrasting life forms (e.g. trees versus grasses) also

represent contrasting metabolic pathways, indirect

effects are also relevant. For example, while frequent

and intense fires (direct effect) favor C4 grasses at the

expense of C3 woody plants at local to regional scales

(Hoffmann et al. 2003; Behling et al. 2004), elevated

atmospheric CO2 (indirect effect) can promote large-

scale shifts in distribution and transitions to stable

states characterized by an abundance of C3 herbs and

more woody biomass (Silva et al. 2011). It is more

likely, however, that higher temperatures and

expected increases in fire frequency and drought-

induced mortality, would lead to widespread treeless

stable states, by favoring C4 grasses and reducing

(through competitive exclusion) the positive impact of

CO2 enrichment on C3 plants (Fig. 1).

Although climatic models do predict a possible

expansion of grass-dominated savanna landscapes

towards the northern limits of the cerrado (Hirota

et al. 2010), the available evidence indicates that

species-poor, grass-dominated, rather than species-

diverse savannas, will replace degraded forests on the

southern edge of the Amazon Basin (Veldman and

Putz 2011). The same pattern might happen in the

southern limits of the cerrado, where warmer temper-

atures and higher fire frequencies may extend the

range of exotic and native C4 grasses and the risk of

impoverished savannas replacing the Atlantic forest or

C3 grasslands in disturbed and natural landscapes.

7 Final remarks

The central role of fire on shaping cerrado ecosystems

is unquestionable. Fire is of widespread occurrence

within the cerrado region and has imposed a strong

selective pressure on cerrado flora since the late

Miocene to Pliocene (Beerling and Osborne 2006;

Simon et al. 2009). Indeed, fire events naturally

triggered by lightning are still of common occurrence,

Fig. 1 Conceptual model of expected feedback loops linkingcontrols of vegetation structure and composition (arrows) and

positive or negative (? and -) biophysical and biogeochemical

climate forcings, expressed as weak, moderate or strong, in

relation to an open grassland. The relative importance of

competition and facilitation mechanisms determines commu-

nity organization and productivity. These effects are described

qualitatively based on the cited literature (see text for details)

30 Theor. Exp. Plant Physiol (2014) 26:1938

123

especially early in the wet season (Mistry 1998;

Ramos-Neto and Pivello 2000; Miranda et al. 2002).

Cerrado species displays a large range of morpholog-

ical and physiological adaptations to endure fires

(Miranda et al. 2002; Gottsberger and Silberbauer-

Gottsberger 2006; Hoffmann et al. 2009, 2012a, b;

Simon et al. 2009). However, current land use and

agricultural practices have considerably changed the

natural fire regime, with major impacts on vegetation

structure and composition. In contrast to natural fires,

anthropogenic fires are more frequent, occur in the dry

season and burn much larger areas (Coutinho 1990;

Barbosa and Fearnside 2005; Pivello 2011). Annually,

73 % of all burned areas in Brazil fall within the

cerrado region (Araujo et al. 2012). As a matter of fact,

in the cerrado, an average area of about 60,000 km2

(range from 11,000 to 147,000 km2) was burned every

year during the period of 20022010 (Araujo et al.

2012). Most of these burns occurred in landscapes

dominated by savanna vegetation, and even protected

forest areas are not free of fires, since accidental and

arson fires are not uncommon (Pivello 2011). Invasive

exotic grasses aggravate the effects of fire. They

produce higher fuel loads than native grasses (Hoff-

mann et al. 2004; Setterfield et al. 2010) and much

more intense fires (Setterfield et al. 2010).

Global warming will accelerate an inevitable on-

going process driven by fire feedbacks that are

resulting in tree cover loss, large changes in

ecosystem processes (Hoffmann et al. 2002; Busta-

mante et al. 2012) and that will probably impact

species distribution and biodiversity in the cerrado

region. Siqueira and Peterson (2003) applied eco-

logical niche modeling techniques to develop an

assessment of effects of climate change on the

distribution of 162 cerrado tree species. A drastic

([50 %) reduction in potential distributional areawas projected for most species.

It is also clear that climate warming and increased

frequencies of anthropogenic fires are not the only

major threats that cerrado ecosystems are subjected to.

The rapid change in land use in Central Brazil in the

last 5060 years has been overwhelming. Land clear-

ing for cash crops and for pasture and intense use of

fire have transformed the cerrado into a fragmented

landscape of degraded savannas, agriculture and

pasture land, interspaced with remnants of native

savanna vegetation of variable extent. These impacts

in the native vegetation are not expected to decrease

throughout this century, but they will probably

increase given the rapid expansion of agroenergy

business in the Brazilian Amazon and Cerrado (Saw-

yer 2008) and the continuous need for food supply

(mainly grains) within and outside the country. In fact,

given a conservative annual rate of land clearing in the

cerrado of about 7,500 km2 and that about 50 % of the

whole region has already been cleared of native

savanna vegetation (http://siscom.ibama.gov.br/

monitorabiomas/cerrado; accessed on 21 November

2013), we should expect that not more than about

30 % of the cerrado region will still be covered with

native but frequently burned (Araujo et al. 2012)

savanna vegetation by the year 2055. It is therefore

essential that we develop our predictive capabilities

for the spatial extent of cerrado biome under changing

climate and fire regimes and that takes into consider-

ation the effect of changes in land use on vegetation-

mediated climate forcings. In particular, we need to

refine and parameterize fire-vegetation models for

simulating savanna-forest dynamics, that could be

coupled to general climate circulation models in order

to achieve a better understanding of environmental

controls on the distribution of savanna and forest

ecosystems (Hirota et al. 2011; Higgins and Scheiter

2012; Hoffmann et al. 2012a). Tests could be provided

by the information available from paleoecological

studies, but new experimental and observational

studies are also required.

Fortunately, the native savanna vegetation is very

resilient and fragmentsunder different degrees of

degradation- can be found thriving even within urban

areas of Central Brazil (Fig. 2). This raises the

question of what is the minimum level or intensity of

disturbance that would transform a resilient cerrado

landscape into irrevocable degraded land that would

require major human intervention and not only

disturbance suppression to achieve ecosystem recov-

ery. For instance, in severely degraded sites (e.g.,

opencast mines), resource inputs have been shown to

promote plant colonization, leading to unprecedented

levels of carbon sequestration (Silva et al. 2013b).

This comes at the cost of excluding native species, but

resource manipulation and management of invasive

species could be used to optimize restoration strate-

gies, counteracting degradation, increasing carbon

sequestration, while maintaining the high species

diversity that is characteristic of cerrado ecosystems

(Silva et al. 2013b).

Theor. Exp. Plant Physiol (2014) 26:1938 31

123

In conclusion, the continued increase in the levels

of atmospheric CO2 is an undisputable component of

anthropogenic environmental change will, in all

likelihood, have a major impact on cerrado plant

communities and hence in ecosystem structure and

function. It is now understood that the positive

radiative forcing that takes place due to anthropogenic

releases of CO2 could be irreversible even if emissions

are interrupted (Solomon et al. 2009). However, as

observed in the geological history (Silva and Anand

2013b), the expansion of forests could mitigate global

warming through evaporative cooling and carbon

sequestration (Bonan 2008), but the net outcome of

biogeochemical and biophysical (e.g., evaporative

cooling and changes in albedo; Fig. 1) feedbacks from

tropical forests and savannas remain uncertain (Silva

and Anand 2013b). Recent studies suggest that

globally, rising CO2 levels were not accompanied by

large increases in productivity of forest ecosystems

particularly at lower latitudes (Silva and Anand

2013a). It has been shown that responses to CO2 were

overestimated in forest biomes (Silva and Horwath

2013), raising doubts about their role in counteracting

climate warming. On the other hand, rising CO2 levels

have apparently increased biomass production and

woody-plant dominance in savanna ecosystems under

unchanged fire disturbance regimes (Bond and Midg-

ley 2012; Buitenwerf et al. 2012). The global

relevance of these contrasting responses remains

uncertain. Experimental studies on CO2 responses of

savanna plants are critically needed, given the limited

number of experiments developed so far (Hovenden

and Williams 2010; Bond and Midgley 2012; Oliveira

et al. 2013). Moreover, the role of fire management

needs to be better assessed by carefully designed

experiments. There is also an urgent need of develop-

ing and parameterizing models that can more accu-

rately simulate vegetationfire dynamics of cerrado

Fig. 2 Fragments of cerrado vegetation undergoing differentdegrees of degradation in the city of Brasilia (AC) and in theoutskirts of the city (D). A Green space with native cerrado treesnear the National Congress, B road verge along the L4 highway

near the University of Brasilia, C remnants of frequently burnedcerrado vegetation on the campus of the University of Brasilia,

D Cerrado landscape in the ecological reserve of the Universityof Brasilia, located approximately 18 km Southeast of the city

32 Theor. Exp. Plant Physiol (2014) 26:1938

123

ecosystems under climate change and nutrient limita-

tion scenarios. A research agenda to minimize the

impacts of changes in land use and climate warming

on cerrado ecosystems will not be effective, unless it is

coupled with strong conservation policies, effectively

enforced at the regional and national level.

Acknowledgments We thank the Brazilian National Counselof Technological and Scientific Development (CNPq), the J.

G. Boswell Endowed Chair in Soil Science and the UC-Mexus

Research Program for financial support.

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