Received: 7 January 2019 | Accepted: 10 April 2019

DOI: 10.1111/1365-2745.13195

E S S AY R E V I E W

Droughts and the ecological future of tropical savanna

vegetation

Mahesh Sankaran1,2

1
National Centre for Biological Sciences,
Tata Institute of Fundamental Research, Abstract
Bangalore , India 1. Climate change is expected to lead to more frequent, intense and longer droughts
2
School of Biology, University of Leeds,
in the future, with major implications for ecosystem processes and human liveli-
Leeds , UK
hoods. The impacts of such droughts are already evident, with vegetation dieback
Correspondence
reported from a range of ecosystems, including savannas, in recent years.
Mahesh Sankaran
Email: [email protected] 2. Most of our insights into the mechanisms governing vegetation drought responses
have come from forests and temperate grasslands, while responses of savannas
Handling Editor: Carla Staver
have received less attention. Because the two life forms that dominate savannas—
C3 trees and C4 grasses—respond differently to the same environmental controls,
savanna responses to droughts can differ from those of forests and grasslands.
3. Drought‐driven mortality of savanna vegetation is not readily predicted by just
plant drought‐tolerance traits alone, but is the net outcome of multiple factors,
including drought‐avoidance strategies, landscape and neighborhood context, and
impacts of past and current stressors including fire, herbivory and inter‐life form
competition.
4. Many savannas currently appear to have the capacity to recover from moderate to
severe short‐term droughts, although recovery times can be substantial. Factors
facilitating recovery include the resprouting ability of vegetation, enhanced flow-
ering and seeding and post‐drought amelioration of herbivory and fire. Future
increases in drought severity, length and frequency can interrupt recovery trajec-
tories and lead to compositional shifts, and thus pose substantial threats, particu-
larly to arid and semi‐arid savannas.
5. Synthesis. Our understanding of, and ability to predict, savanna drought re-
sponses is currently limited by availability of relevant data, and there is an urgent
need for campaigns quantifying drought‐survival traits across diverse savannas.
Importantly, these campaigns must move beyond reliance on a limited set of plant
functional traits to identifying suites of physiological, morphological, anatomical
and structural traits or “syndromes” that encapsulate both avoidance and toler-
ance strategies. There is also a critical need for a global network of long‐term
savanna monitoring sites as these can provide key insights into factors influenc-
ing both resistance and resilience of different savannas to droughts. Such efforts,
coupled with site‐specific rainfall manipulation experiments that characterize
plant trait–drought response relationships, and modelling efforts, will enable a
more comprehensive understanding of savanna drought responses.

Journal of Ecology. 2019;107:1531–1549. wileyonlinelibrary.com/journal/jec

© 2019 The Author. Journal of Ecology | 1531
© 2019 British Ecological Society
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1532 | Journal of Ecology SANKARAN

KEYWORDS
avoidance, hydraulic safety margins, resilience, resistance, tolerance

1 | I NTRO D U C TI O N altered rainfall regimes, specifically droughts, on savanna dynamics.

My focus on drought is prompted by the recognition that: (a) water
In environments in which there is a recurrence of availability is a key determinant of savanna structure and func-
natural hazards, populations may spend most of their tion (Bond, Midgley, & Woodward., 2003; Bucini & Hanan, 2007;
time recovering from the hazards…. Harper (1967) D'Onofrio, Hardenberg, & Baudena, 2018; Good & Caylor, 2011;
Lehmann et al., 2014; Sankaran et al., 2005; Sankaran, Ratnam, &
This statement is particularly true of the Earth's tropical savannas. Hanan, 2008; Scholes & Archer, 1997), (b) changes in precipitation
Tropical savannas are indeed a curious biome, neither grassland nor regimes, coupled with warmer temperatures that increase evapo-
forest, but one in which two contrasting life forms—C3 trees and C4 rative demand, are projected to lead to more intense and frequent
grasses—compete for dominance in the face of limited resource avail- regional‐scale droughts across large parts of the globe, including sa-
ability and frequent disturbances such as fire and herbivory. In fact, vanna regions (Dai, 2013; IPCC, 2014; Mitchell, O'Grady, Hayes, &
savannas were long perceived as degraded ecosystems, derived from Pinkard, 2014; Trenberth et al., 2014), (c) savannas are expected to
forests as a result of disturbances, anthropogenic or otherwise (Bond be particularly responsive to precipitation changes given the tight
& Parr, 2010; Parr, Lehmann, Bond, Hoffmann, & Andersen, 2014; coupling between rainfall and production in these systems (Knapp
Ratnam, Tomlinson, Rasquinha, & Sankaran, 2016; Scholes & Walker, & Smith, 2001; Sala, Gherardi, Reichmann, Jobbagy, & Peters, 2012;
1993; Veldman et al., 2015). However, tropical savannas are ancient bi- Sala et al., 2000; Xu et al., 2018), and (d) in contrast to forests, the
omes, their origins dating back to the late Miocene and early Pliocene, role of droughts in regulating tropical savanna dynamics has received
~4–8 Mya, and the near‐synchronous expansion of C4 grasses around relatively less attention. Importantly, inferring savanna responses
the world (Beerling & Osborne, 2006; Edwards et al., 2010; Osborne, based on studies carried out in other ecosystems is not straight-
2008; Simon & Pennington, 2012). This global rise to dominance of forward. Because the two dominant life forms that characterize
C4 grasses occurred fairly rapidly in geological terms, within about a savanna ecosystems—C4 grasses and C3 trees and shrubs—respond
million years, and represents one of the most dramatic examples of differently to the same environmental controls, and because many
biome assembly in the geological record (Beerling & Osborne, 2006; vegetation traits of tropical savanna trees and grasses differ consis-
Edwards et al., 2010). tently from those of forests and temperate grasslands (Craine, Lee,
Savannas and grasslands are among the most extensive vegeta- Bond, Williams, & Johnson, 2005; Hoffmann, Franco, Moreira, &
tion types in tropical and sub‐tropical regions (Scholes & Archer, 1997; Haridasan, 2005; Ratnam et al., 2011; Charles‐Dominique, Beckett,
Solbrig, Medina, & Silva, ). However, over the last couple of centu- Midgley, & Bond 2015), savannas are likely to respond to climate
ries, they have been drastically altered by human activities (Lambin, change in ways that forests and grasslands may not (Lehmann et al.,
Geist, & Lepers, 2003; Miles et al., 2006; Murphy, Andersen, & Parr, 2014; Osborne et al., 2018).
2016; Ramankutty & Foley, 1999; Ratnam et al., 2016; Strassburg et Tropical savannas are characterized by highly seasonal rain-
al., 2017). As human populations grow and expand, the remaining fall, with pronounced dry seasons ranging anywhere from 3
savanna habitats are increasingly threatened by a range of anthropo- to 8 months (Scholes & Walker, 1993). The high irradiance and
genic activities, including land‐use transformation, tree plantations heat that characterize these habitats creates a high evaporative
for carbon–sequestration initiatives and alterations of fire and her- demand, with the result that most savannas are in water deficit
bivory regimes (Abreu et al., 2017; Bond, 2016; Bond & Parr, 2010; for large parts of the year, including the wet season (Scholes &
Murphy et al., 2016; Osborne et al., 2018; Parr et al., 2014; Ratnam Walker, 1993). In addition, inter‐annual rainfall variability is also
et al., 2016; Strassburg et al., 2017; Veldman et al., 2015). Further, a defining feature of the savanna biome, typically increasing with
global changes in the form of altered precipitation and temperature decreasing mean annual rainfall (Fensham, Fairfax, & Ward, 2009;
regimes, elevated atmospheric [CO2] and atmospheric N and P depo- Knapp & Smith, 2001; Sala et al., 2012). Thus, multiple consecu-
sition have emerged as major threats to the ecological integrity of tive years with below average rainfall are not uncommon in most
these biomes (Bond & Midgley, 2012; Midgley & Bond, 2015; Parr savannas (Fensham et al., 2009). Although savanna vegetation has
et al., 2014), prompting Bond and Midgley (2012) to ask if the rise to evolved a diverse range of strategies to cope with such variability
dominance of this biome in the Late Miocene is likely to be matched (O'Brien et al., 2017), extreme and/or protracted periods of rain-
by an equally dramatic decline in the Anthropocene. fall deficit, especially when coupled with warmer temperatures,
Changes in savanna structure, composition and function as a can nevertheless result in the widespread mortality of both sa-
result of ongoing and future climate change can have major impli- vanna grasses (Staver, Wigley‐Coetsee, & Botha, 2018; Swemmer
cations for human wellbeing and ecosystem processes (Midgley & et al., 2018; Walker, Emslie, Owen‐Smith, & Scholes, 1987) and
Bond, 2015; Osborne et al., 2018). Here, I focus on the effects of trees (Fensham et al., 2009; Fensham, Laffineur, & Allen, 2019).
 13652745, 2019, 4, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1111/1365-2745.13195 by Cochrane Colombia, Wiley Online Library on [20/03/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
SANKARAN Journal of Ecology | 1533

Here, I primarily focus on the effects of such extreme droughts on The most well documented and dramatic examples of tree die‐
savanna vegetation. offs come from forested ecosystems, where as many as 300 million
For the purposes of this review, I use the term drought to broadly trees are estimated to have died in some drought events (Allen,
refer to periods where lowered rainfall during the growing season re- 2009; Allen et al., 2010; Anderegg, Berry, & Field, 2012; Choat et al.,
duces plant water availability to levels significantly below average an- 2018). However, there are also reports of significant drought‐related
nual conditions (Greenwood et al., 2017; O'Brien et al., 2017). I do not tree die‐back in savannas (Fensham, 1998; Fensham & Fairfax, 2007;
specifically consider how vegetation responses change with drought Fensham et al., 2009, 2019; Fensham, Fraser, Macdermott, & Firn,
intensity per se, but acknowledge that the magnitude of observed re- 2015; Fensham & Holman, 1999; MacGregor & O'Connor, 2002;
sponses will undoubtedly be more pronounced as droughts become Rice, Matzner, Byer, & Brown, 2004; Scholes, 1985; Swemmer et al.,
more extreme and protracted (Greenwood et al., 2017; Ruppert et al., 2018; Twidwell et al., 2014; Viljoen, 1995; Wonkka, Twidwell, Franz,
2015; Young et al., 2017). I draw on both observational studies that Taylor, & Rogers, 2016). These cases come from a diverse array of
have recorded responses of savanna trees and grasses to droughts, as savanna types across multiple continents, but a common theme
well asexperimental studies that have manipulated plant wateravail- emerging from these studies, consistent with work from other sys-
ability under controlled conditions. Although experimentsallow for tems, is that the extent to which meteorological droughts translate
clearer attribution of causes (Greenwood et al., 2017; Smith, 2011), to physiological droughts, that is, water stress experienced by an
manipulating water availability for adult savanna trees is challenging individual leading to mortality, varies spatially within landscapes,
given their size and longevity (O'Brien et al., 2017). Consequently, among different species within sites, and across different life history
experiments are typically limited to grasses and tree seedlings, and stages within species.
do not capture adult tree responses, which observational studies do. Drought‐induced tree mortality in savannas, and indeed other
I begin by considering the independent direct effects of droughts ecosystems, is typically spatially variable across the landscape in ways
on the survival of savanna trees and grasses, and the traits that gov- that are not just related to patchiness in rainfall, but also to topogra-
ern their ability to tolerate or alternately avoid droughts (tolerance vs. phy, local edaphic features, patterns of tree density and composition,
avoidance). I then look at how increasing water stress can influence local disturbances and management history (Fan, Miguez‐Macho,
tree‐grass interactions,bothdirectly by altering their competitivedy- Jobbagy, Jackson, & Otero‐Casal, 2017; Fensham, 1998; Fensham
namics, as well as indirectly by mediating changes in the strength & Fairfax, 2007; Fensham & Holman, 1999; MacGregor & O'Connor,
and intensity of top–down drivers such as fire and herbivory, with 2002; O'Brien et al., 2017; O'Connor, 1998; Rice et al., 2004; Scholes,
implications for the ability of the vegetation to withstand change 1985; Swemmer et al., 2018; Twidwell et al., 2014; Viljoen, 1995).
(resistance) as well as recover following droughts (resilience; Hoover, Topographic and edaphic features drive drainage and infiltration in-
Knapp, & Smith, 2014; Lloret, Escudero, Iriondo, Martínez‐Vilalta, & fluencing both surface soil water availability and water table depth
Valladares, 2012; Smith, 2011; Vicente‐Serrano et al., 2013). Finally, and in turn, rooting depths (Fan et al., 2017). Such variability across
I synthesize findings to provide a framework to assess drought ef- the landscape (e.g. between upslope and foot slope locations in sa-
fects in savannas, highlight data gaps and identify research priorities vanna landscapes; Scholes & Walker, 1993) can lead to differences
to enable us to better understand and predict savanna responses to in the extent of water‐stress, and in turn mortality, experienced by
future droughts. different individuals during droughts (Fan et al., 2017; Hartmann et
al., 2018; McDowell et al., 2008). Patchiness in mortality can also
result from underlying differences in tree densities across the land-
2 | D I R EC T E FFEC T S O F D RO U G HT S O N scape, with higher density sites typically suffering greater mortality,
SAVA N N A TR E E M O RTA LIT Y potentially a result of more intense competition for limited water
in these sites during drought (Dwyer, Fensham, Fairfax, & Buckley,
Increasing drought stress, particularly when coupled with warmer 2010; Fensham & Fairfax, 2007; Fensham et al., 2017; MacGregor &
temperatures, can render trees more susceptible to mortality, with O'Connor, 2002; Young et al., 2017).
major implications for the land carbon sink (Phillips et al., 2009; Tree species also differ inherently in their ability to withstand
Schwalm et al., 2017). Warmer temperatures increase evaporative and recover from droughts (Breshears et al., 2009; Fensham &
demand and thereby exacerbate drought stresses, leading to earlier Fairfax, 2007; Fensham et al., 2015; Greenwood et al., 2017; O'Brien
and more widespread mortality in trees (Zeppel, Adams, & Anderegg, et al., 2017; O'Connor, 1998; Rice et al., 2004; Viljoen, 1995). Tree
2011). There is already evidence for episodes of enhanced tree mor- mortality during droughts can arise from one or more non‐exclusive
tality in response to drought across many parts of the globe, with a mechanisms including hydraulic failure and loss of vascular trans-
marked increase in the number of documented regional scale tree port capacity as a result of xylem cavitation, carbon starvation as
die‐off events since the 2000s (Adams, Macalady, & Breshears, a result of depletion of carbohydrate reserves, and increased sus-
2010; Allen, 2009; Allen et al., 2010; Anderegg, Kane, & Anderegg, ceptibility to herbivore and pathogen attacks (Anderegg, Berry, et
2012; Anderegg et al., 2015, 2016; Breshears et al., 2009; Fensham al., 2012; Anderegg et al., 2015, 2016; Breshears et al., 2009; Choat
et al., 2009; Greenwood et al., 2017; McDowell et al., 2008, 2011; et al., 2018; McDowell et al., 2008). Hydraulic failure occurs when
Phillips et al., 2009, 2010; amongst others). droughts are particularly severe, causing the xylem and rhizosphere
 13652745, 2019, 4, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1111/1365-2745.13195 by Cochrane Colombia, Wiley Online Library on [20/03/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
1534 | Journal of Ecology SANKARAN

to cavitate (become filled with air‐pockets), impeding water flow and in stems and branches during droughts, although explicit tests of this
eventually resulting in desiccation and death (Hartmann et al., 2018; are currently lacking.
McDowell et al., 2008). When droughts are less severe but more Low physiological drought tolerance capability, however, does
protracted, stomatal closure by trees to prevent hydraulic failure can not necessarily always mean higher mortality in the field during
limit carbon fixation, resulting in carbon‐starvation in the long‐term droughts. In addition to tolerance, trees also employ a range of
as trees are unable to meet their continued metabolic demand for different strategies to avoid or delay desiccation stress during
carbohydrates (Hartmann et al., 2018; McDowell et al., 2008). droughts (avoidance), including leaf shedding, internal water stor-
The xylem water potentials at which cavitation occurs (cavitation age, reduced leaf area and greater allocation to deeper roots that
resistance; characterized as the pressure that induces 50% (Ψ50) or provide access to the water table, among others (Table 1; Choat
88% (Ψ88) loss of xylem hydraulic conductivity) differs between spe- et al., 2012, 2018; Eamus, 1999). Such avoidance strategies can
cies and is largely determined by xylem anatomical features includ- be quite effective, and there is evidence from savannas to sug-
ing the diameter, length, connectivity and density of xylem conduits gest that “avoiders”, despite being more vulnerable to drought‐
and the porosity of pit membranes (Anderegg et al., 2016; Choat et induced cavitation, suffered lower mortality than “tolerators”
al., 2012, 2018). Tree species also differ in the extent to which they during droughts as a consequence of their deep‐rootedness which
regulate their internal water status through the opening and closing allowed them to access deep soil water during droughts (Rice et
of their stomata. Isohydric species, on the one hand, use stomatal al., 2004). Similarly, available data across a range of different eco-
regulation to maintain more or less constant midday plant water po- system types including some Southern African savannas suggest
tentials and avoid cavitation. However, with stomata closed, pho- no consistent differences in the levels of mortality experienced by
tosynthesis is curtailed, and these species run the risk of carbon deciduous species (avoiders) when compared to evergreen species
starvation during droughts (Konings & Gentine, 2017; McDowell (tolerators) during droughts (Anderegg et al., 2016; Greenwood et
et al., 2008; Zeppel et al., 2011). Anisohydric species, on the other al., 2017).
hand, allow plant water potentials to drop as soil water potentials Just as all species are not equally susceptible to drought, indi-
drop, both diurnally and seasonally, and so potentially run a greater viduals within species also vary in the extent to which they suffer
risk of hydraulic failure during droughts (Konings & Gentine, 2017; mortality during droughts. Across forested ecosystems, suscep-
Konings, Williams, & Gentine, 2017; McDowell et al., 2008; Zeppel tibility is often skewed towards the smallest and/or largest size
et al., 2011). The difference between the typical minimum xylem classes (Bennett, Mcdowell, Allen, & Anderson‐Teixeira, 2015;
water potential experienced by trees and that which causes xylem Choat et al., 2018; Giardina et al., 2018; Greenwood et al., 2017;
dysfunction provides a measure of the “hydraulic safety margin McDowell et al., 2008; O'Brien et al., 2017; Phillips et al., 2010).
(HSM)” within which trees operate, and serves as a useful index of Seedlings and young individuals have poorly developed root and
the physiological vulnerability of trees to drought‐induced mortality vascular systems and limited carbohydrate reserves, while larger
(Anderegg et al., 2016; Choat et al., 2012, 2018). individuals may be more vulnerable because of their greater over-
Recent studies attempting to link patterns of drought‐induced all water requirements, greater inherent vulnerability to hydraulic
mortality of forest trees to underlying plant traits suggest that spe- stress, or because of the greater cumulative effects of earlier ex-
cies with low cavitation resistance, low hydraulic safety margins, ogenous stressors such as fires, herbivory, pathogens and com-
low wood density and high specific leaf area typically suffer greater petition in larger, older individuals (Allen et al., 2010; Anderegg,
mortality during droughts (Anderegg et al., 2016; Greenwood et Berry, et al., 2012; Bennett et al., 2015; Rice et al., 2004; Zhang
al., 2017; O'Brien et al., 2017; Phillips et al., 2010). However, com- et al., 2009). However, tree size is often a poor proxy for age in
pared to forests, there are only a few studies at present linking savannas. In savannas, frequent fires “top‐kill” small individuals,
tree traits to drought‐related mortality in tropical savannas, largely but mortality as a result of fire is often low (Bond, 2008; Grady &
limited to inferring relationships between rooting characteristics, Hoffmann, 2012; Higgins, Bond, & Trollope, 2000). Most individ-
species growth rates and storage allocation patterns on mortality. uals typically resprout from below‐ground reserves and can per-
Results from these studies, although varied, are broadly consistent sist for decades in a “fire trap” of repeated top–kill and resprouting
with those observed in other ecosystems and suggest that species (Bond & Midgley, 2001; Grady & Hoffmann, 2012; Higgins et al.,
with higher root densities, slower growth rates and greater alloca- 2000). Chronic browsing can similarly restrict the height of indi-
tion to storage typically experience lower mortality during droughts vidual trees, maintaining them within a “browse trap” for extended
(Fensham & Fairfax, 2007; Fensham et al., 2015, 2017). In addition, periods (Bond, 2008; Sankaran, Augustine, & Ratnam, 2013;
resprouting ability, a common feature of many savanna trees, has Staver & Bond, 2014). It is therefore not surprising that size is not
also been linked to higher survival during droughts, presumably a a consistent predictor of drought‐induced mortality in savannas.
consequence of the greater allocation to roots and higher stores Mortality appears unrelated to size for some species (Fensham,
of non‐structural carbohydrates in resprouting compared to non‐ 1998; Fensham et al., 2015; Fensham & Holman, 1999; Rice et al.,
resprouting species (Zeppel et al., 2015, but also see Pausas et al., 2004), is higher in the large‐size classes for some (Fensham et al.,
2016). It is also plausible that the multi‐stemmed nature of resprout- 2015; Rice et al., 2004; Twidwell et al., 2014), while smaller stems
ing species allows them to better compartmentalize hydraulic failure suffer greater mortality in others (Dwyer et al., 2010; Fensham,
 13652745, 2019, 4, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1111/1365-2745.13195 by Cochrane Colombia, Wiley Online Library on [20/03/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
SANKARAN Journal of Ecology | 1535

TA B L E 1 Representative tolerance (a) and avoidance traits (b) that influence growth and survival of trees and grasses during droughts
(resistance)

Traits Description

(a) Tolerance traits

Cavitation or embolism resistance (Ψ50 and (T,G) Xylem pressure that induces 50% or 88% loss of xylem hydraulic conductivity. Species
Ψ88) with more negative values can tolerate drier conditions before cavitation occurs
Xylem conduit dimensions and connectivity (T,G) Xylem anatomical features that determine vulnerability to cavitation. Species with nar-
rower and shorter xylem elements and lower connectivity are less vulnerable to cavitation
Pit membrane thickness and porosity (T,G) Determines vulnerability to cavitation. Species with larger pores are more susceptible to
cavitation
Minimum leaf water potential (Ψmin) (T) Typical minimum xylem water potential experienced by trees under normal conditions.
Isohydric species regulate stomata to maintain more or less constant midday plant water po-
tentials to avoid cavitation, but run the risk of carbon starvation. Anisohydric species, on the
other hand, allow plant water potentials to drop as soil water potentials drop, both diurnally
and seasonally, and so potentially run a greater risk of hydraulic failure during droughts
Leaf water potential corresponding to stomatal (G) Leaf water potentials at which stomatal conductance falls below critical values. Lower
closure (Ψcrit) values indicate greater drought tolerance.
Hydraulic safety margins (HSM) (T, G) Difference between the typical minimum xylem water potential experienced by trees
and that which causes xylem dysfunction. For grasses, commonly estimated as the difference
between leaf water potentials at 95% stomatal closure and Ψ50. Species with greater HSMs
fare better during droughts.
Leaf turgor loss point (T,G) Leaf water potential at which wilting occurs. Species with lower values can maintain gas
exchange and growth at lower soil moisture levels, i.e. better tolerate droughts
Non‐structural carbohydrate reserves (stem, (T,G) Species with greater stores of carbohydrate reserves fare better under droughts
root & leaf)
Root:shoot ratios (T,G) Species that allocate relatively more to roots perform better under droughts
Leaf: sapwood area ratio (T) Species with low leaf:sapwood ratios have a greater capacity to supply water to leaves
Resprouting ability (T) Resprouting species have greater allocation to roots and higher stores of non‐structural
carbohydrates which can confer greater drought‐tolerance compared to non‐resprouters
Wood density (T) Soft wooded species (low wood density) typically suffer greater mortality during droughts
Specific leaf area (T, G) Species with high specific leaf area typically suffer greater mortality during droughts
Leaf width (G) Wide leaved grasses tend to be more drought tolerant, while narrow leaved species show a
range of tolerance levels
C4 Photosynthetic pathway (NADP‐ME, (G) NAD‐ME species have higher whole‐plant water use efficiency under water stress and are
NAD‐ME, PCK) potentially more drought tolerant
Associations with symbionts (AMF) (T, G) Drought‐tolerance of both trees and grasses can also be enhanced by associations with
AMF that facilitate water acquisition
(b) Avoidance traits
Deep roots (T, G) Provides access to deep soil water and/or water table
Leaf shedding (T, G) Reduces transpirational loss, water use and lowers vulnerability to cavitation
Internal water storage (T) Reduces reliance on soil water
Leaf rolling (G) Reduces water loss
Cuticular wax (G) Reduces water loss

The letters T and G in brackets at the start of the description indicate whether the traits are typically quantified for trees or grasses, respectively. For
a more detailed description of these traits and their quantification, also see Holloway‐Phillips and Brodribb (2011), Craine et al. (2013), O'Brien et al.
(2017) and Choat et al. (2018) and references therein.

1998; Fensham et al., 2015; Fensham & Holman, 1999; O'Connor, (b) the actual levels of water stress experienced during droughts
1998). These divergent responses across species likely arise from by small versus large individuals. Differences in mortality can arise
variation in (a) size‐related changes in rooting strategies, carbon even in the absence of any size‐related differences in drought tol-
allocation patterns, carbohydrate reserves, hydraulic architecture, erance per se if different sized individuals “experience” droughts to
gas exchange and vulnerability to cavitation (Bennett et al., 2015; different degrees. For example, larger individuals with access to the
Fensham et al., 2017; Rice et al., 2004; Zhang et al., 2009), and water table might not “experience” droughts to the same extent as
 13652745, 2019, 4, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1111/1365-2745.13195 by Cochrane Colombia, Wiley Online Library on [20/03/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
1536 | Journal of Ecology SANKARAN

smaller, shallow rooted individuals, and vice versa (Chitra‐Tarak et help identify alternate “syndromes” that plants employ to deal with
al., 2018; Giardina et al., 2018). droughts, and provide insights into how these change across broad
Several physiological, morphological and anatomical traits have environmental gradients.
been identified that provide measurable indices of the vulnerabil-
ity of tree species to drought‐induced mortality (Table 1; also see
table 1 in O'Brien et al. (2017) and Table S1 in Choat et al. (2018)). 3 | D I R EC T E FFEC T S O F D RO U G HT S O N
Unfortunately, information on many of these traits, particularly SAVA N N A G R A S S E S
hydraulic traits and safety margins, are currently lacking for most
savanna species (O'Brien et al., 2017), with available data largely Tropical savanna C4 grasses typically use water more efficiently,
restricted to a few easily measurable traits such as wood density and are more physiologically responsive to intermittent rain-
and specific leaf area. These traits, although reflective of hydrau- fall events, compared to C 3 trees and shrubs (Ghannoum, 2009;
lic architecture and plant‐water relations (Anderegg et al., 2016; Ghannoum et al., 2003; Ripley, Gilbert, Ibrahim, & Osborne, 2007;
Bucci et al., 2004, 2008; Franco et al., 2005; Markesteijn, Poorter, Swemmer, Knapp, & Smith, 2006; Volder, Tjoelker, & Briske, 2010;
Paz, Sack, & Bongers, 2011), are not directly mechanistically re- Williams, Wilsey, McNaughton, & Banyikwa, 1998). However, this
lated to drought tolerance per se, and thus only explain a limited greater water use efficiency does not necessarily translate into
amount of variability in observed drought mortality responses of a greater tolerance for protracted water stress compared to C 3
species (Adams et al., 2017; Anderegg et al., 2016; Greenwood et plants (Ghannoum, 2009; Ripley, Frole, & Gilbert, 2010; Ripley et
al., 2017; O'Brien et al., 2017). Given that the majority of tree spe- al., 2007; Taylor, Ripley, Woodward, & Osborne, 2011; Volder et
cies globally are estimated to be operating with narrow hydraulic al., 2010). Although they are capable of assimilating large amounts
safety margins and potentially vulnerable to drought induced mor- of carbon when soil water is available, this capacity diminishes
tality (Choat et al., 2012), there is an urgent need for campaigns rapidly as soil water content decreases (Connor & Hawkes, 2018;
that quantify, in the first instance, hydraulic traits and safety mar- Ghannoum, 2009; Ripley et al., 2007; Taylor et al., 2011; Volder
gins of savanna trees. et al., 2010). Thus, although C4 grasses may be better able to
Ultimately, the ability of trees to withstand and survive droughts deal with and recover from low to moderate drought, they may
is the net outcome of interactions between a number of physical, be equally or even more sensitive to periods of severe or pro-
morphological and life‐history traits that enable trees to tolerate tracted water stress when compared to C 3 plants (Ghannoum,
desiccation stress, or alternately avoid or delay it to the extent 2009; Ripley et al., 2007; Volder et al., 2010; Walker et al., 1987).
possible (Choat et al., 2018; O'Brien et al., 2017). It is becoming in- Drought impacts on grass mortality in savannas can thus be sub-
creasingly apparent that many easily measurable traits such as wood stantial (Danckwerts & Stuart‐Hill, 1988; Mott, Ludlow, Richards,
density and specific leaf area are rarely successful at fully predicting & Parson, 1992; O'Connor, 1994, 1995; Scholes, 1985; Swemmer
drought mortality patterns in the field by themselves, and extrap- et al., 2018; Walker et al., 1987), with grasses often dying before
olations based on single traits, including hydraulic safety margins woody plants (Walker et al., 1987).
can often be misleading (Adams et al., 2017; Pausas et al., 2016). Physiological drought tolerance of grasses, assessed based on
For example, high wood density species have been shown to survive leaf water potentials at which stomatal conductance falls below
better during droughts in some systems, but suffer greater mortal- critical thresholds for ecological functioning, has been shown to
ity in others (Hoffmann, Marchin, Abit, & Lau, 2011; O'Brien et al., vary nearly 10‐fold between grass species, both across and within
2017). Similarly, mortality has been reported to be higher in shal- sites (Craine et al., 2013). Using data from 426 tropical and temper-
low‐rooted species in some instances, but greater in deeper‐rooted ate grass species spanning a range of rainfall, biogeographic and
species in others (Chitra‐Tarak et al., 2018; Fensham et al., 2015; phylogenetic affinities, Craine et al. (2013) showed that physio-
Rice et al., 2004). It is unlikely that plants have evolved to rely on a logically drought tolerant grasses, that is, those with critical leaf
single strategy to deal with drought (Anderegg, Berry, et al., 2012) water thresholds below the median value for all species assessed
and there is thus a need for drought survival to be considered in (−4.1 MPa), typically have higher photosynthetic rates and stoma-
the context of suites of multiple physiological, morphological, ana- tal conductance, and narrower xylem elements consistent with
tomical and structural traits or “syndromes” that encapsulate both mechanisms of cavitation resistance. Leaf‐width also appears to be
avoidance and tolerance strategies. Such an expanded campaign correlated with drought tolerance with wide‐leaved grasses tend-
will yield rich dividends and is less unwieldy that it may seem. Many ing to be drought‐intolerant and narrow‐leaved species displaying
hydraulic and physiological traits appear to covary in a coordinated a wide range of abilities from tolerance to intolerance (Craine et
fashion, suggesting that the complexity of hydraulic traits can be al., 2013).
collapsed into one or a few axes of physiological drought tolerance As in the case of trees, the ability to physiologically tolerate
strategies (Bartlett, Klein, Jansen, Choat, & Sack, 2016; Choat et al., droughts is not always reflective of grass mortality patterns in the
2018; Mencuccini, Minunno, Salmon, Martínez‐Vilalta, & Hölttä, field, which is also contingent on other factors including allocation
2015). Combining these with axes that similarly capture anatomical, patterns, life‐history attributes and drought avoidance strategies
morphological (e.g. rooting characteristics) and avoidance traits can (Table 1). Species with deep roots and those that allocate more
 13652745, 2019, 4, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1111/1365-2745.13195 by Cochrane Colombia, Wiley Online Library on [20/03/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
SANKARAN Journal of Ecology | 1537

to roots and less in reproductive structures have been shown to Savannas are complex systems whose structure is ultimately de-
fare better under conditions of repeated water stress (Nippert & termined by a suite of factors, including inter‐ and intra‐life form com-
Holdo, 2015; Swemmer et al., 2006). Maximum rooting depth is petition between trees and grasses, climate, soils, fire, browsing and
generally considered a good indicator of the ability of species to grazing (Sankaran & Anderson, 2009). Thus, the effects of droughts on
withstand protracted dry periods, but factors such as root mor- savanna structure and function cannot be fully understood by study-
phology, root biomass allocation with depth, functional plasticity ing responses of the major functional groups, C3 trees and C4 grasses,
in water uptake in relation to availability, variation in water trans- in isolation as net effects can be altered depending on how droughts
port capabilities and symbiotic associations with arbuscular my- impact fire and herbivory regimes, as well as the nature and intensity
corrhizal fungi (AMF) are also important (Nippert & Holdo, 2015; of tree‐grass competition.
Petipas, González, Palmer, & Brody, 2017). Grass species also show Grazing, browsing and fire are integral components of savannas
a range of drought avoidance strategies including leaf folding and that play key roles in regulating the growth and survival of both trees
rolling, rapid leaf shedding and large amounts of cuticular wax that and grasses in savannas (Archibald, Bond, Stock, & Fairbanks, 2005;
can help delay the onset of physiological droughts (Bolger, Rivelli, Staver & Bond, 2014; Staver, Bond, Stock, Rensburg, & Waldram,
& Garden, 2005). 2009; Staver, Botha, & Hedin, 2017). Droughts can alter the extent
Drought tolerance also potentially differs between different and intensity with which these drivers act to influence mortality
C4 grass photosynthetic subtypes, the distributions of which are and growth of vegetation, with these effects varying both spatially
strongly influenced by rainfall (Ghannoum, 2009; Ripley et al., 2010, and temporally over the course of the drought. Intense grazing can
2007). C4 grasses are grouped into three photosynthetic subtypes suppress grass biomass and productivity during drought years, in-
based on the major C4 acid decarboxylation enzyme in their bundle creasing grass mortality and reducing grass basal area (Augustine
sheaths: NAD‐ME (NAD malic enzyme), NADP‐ME (NADP malic en- & McNaughton, 2006; Swemmer et al., 2018; Walker et al., 1987),
zyme) and PCK (phosphoenolpyruvate carboxykinase; Ghannoum, with such effects being particularly pronounced closer to permanent
2009). NAD‐ME grasses tend to increase in abundance, while sources of surface water which the herbivores rely on (Walker et al.,
NADP‐ME grasses decrease, across a gradient of decreasing rainfall 1987). When grazers move out of droughted areas, they can also
(from 900 to 50 mm mean annual precipitation) while the distribu- extend the ecological impacts of droughts into non‐droughted re-
tion of PCK species does not appear to be strongly correlated with gions which subsequently suffer higher levels of defoliation and re-
rainfall (Ghannoum, 2009 and references therein). Data, albeit from ductions in grass biomass (Staver et al., 2018). Browsers can similarly
a very limited number of species, suggest that NAD‐ME species pos- significantly suppress tree growth during droughts, particularly of
sess traits better suited to arid conditions and tend to have higher individuals in smaller‐size classes (Augustine & McNaughton, 2004).
whole‐plant water use efficiency under water stress than NADP‐ME Intense browsing during droughts, when coupled with lowered plant
species (Carmo‐Silva et al., 2009; Ghannoum, Von Caemmerer, & photosynthetic rates, can also reduce and prevent the replenish-
Conroy, 2002; Taylor et al., 2011). ment of starch reserves in woody plants (Pausas & Keeley, 2014;
At present, there are only a few studies that have quantified Schutz, Bond, & Cramer, 2011; Zeppel et al., 2015), with potential
drought tolerance traits of grasses, and data are currently avail- longer‐term consequences for survival of individuals. Other forms
able only for a restricted number of savanna species. There is a of damage such as bark stripping of trees by elephants have also
clear need for more rigorous efforts to characterize drought toler- been shown to increase during droughts, which can further com-
ance and avoidance traits for a greater number of savanna grasses pound tree mortality (Walker et al., 1987). Because widespread
across a broader range of climatic conditions. As in the case of herbivore mortality typically occurs only in the later stages of the
trees, such efforts should focus on identifying drought survival drought (Walker et al., 1987), browser and grazer effects on mortal-
syndromes that encapsulate both tolerance and avoidance traits ity of vegetation are likely to be particularly pronounced during the
of species. early stages, with effects weakening in the later stages of drought
following herbivore die‐off.
Like herbivory, the importance of fire as an agent of savanna
4 | D RO U G HT S , TR E E– G R A S S woody plant mortality can also change over the course of the
I NTE R AC TI O N S A N D TH E FE E D BAC K drought. Because fuel loads can carry over from year to year, the
E FFEC T S O F FI R E A N D H E R B I VO RY extent and intensity of fires in any given year are not just contingent
on current–year rainfall but also rainfall in the preceding wet‐season
It may be argued, therefore, that the essential qual- or two (Archibald, Roy, Wilgen, & Scholes, 2009; Balfour & Howison,
ities which determine the ecology of a species may 2002; Sala et al., 2012). Fires that occur early in the drought, par-
only be detected by studying the reaction of its indi- ticularly when droughts are preceded by periods of above‐average
viduals to their neighbours and that the behaviour of rainfall, are therefore likely to be more widespread and intense than
individuals of the species in isolation may be largely those that occur later in the drought. Such intense wildfires as a re-
irrelevant to understanding their behaviour in the sult of hotter and drier conditions during droughts can significantly
community. Harper, 1964 enhance tree mortality (Breshears et al., 2016; Twidwell, Rogers,
 13652745, 2019, 4, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1111/1365-2745.13195 by Cochrane Colombia, Wiley Online Library on [20/03/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
1538 | Journal of Ecology SANKARAN

Wonkka, Taylor, & Kreuter, 2016), particularly in wet sites with low grazed sites that retain herbaceous cover (MacGreggor & O'Connor,
grazing pressure where grass biomass is high. In contrast, during the 2002). Similarly, over‐browsing can predispose sites to higher mor-
later stages of drought where fuel loads are low, either because of tality during droughts by reducing starch reserves of trees (Schutz et
the cumulative negative effects of droughts on grass productivity, al., 2011; Zeppel et al., 2015). In contrast, drought‐related tree mor-
or in sites supporting significant grazer populations, fire effects can tality could potentially be lower in sites with a history of frequent
be minimal because of reductions in the frequency and intensity of burning. Frequent fires reduce tree densities which can result in
fires. There is evidence to indicate that both size of individual burns lowered competition for limiting water, and in turn lowered mortal-
and total area burnt tend to be lower, and fire return intervals lon- ity, during droughts when compared to unburned or less frequently
ger, during dry phases when compared to wet phases (Balfour & burned sites that support higher tree densities.
Howison, 2002).
The net effects of droughts and disturbances such as fire and
herbivory on savanna structure and function is ultimately contin- 5 | LO N G ‐TE R M E FFEC T S O F D RO U G HT S
gent on the extent to which grass biomass and productivity are O N SAVA N N A S : S TA B I LIZ I N G A N D
suppressed relative to woody plants, which determines both the D E S TA B I LIZ I N G PRO C E S S E S
intensity of tree–grass competition for limited soil moisture as
well as the nature of feedback effects arising through changes in There is growing concern that increases in the frequency and inten-
fire regimes. Grasses are indeed formidable competitors for soil sity of extreme events can potentially trigger abrupt shifts in vegeta-
moisture, and there is ample evidence to suggest that grasses can tion in the future (Allen & Breshears, 1998; Breshears et al., 2016;
suppress growth of adult and especially juvenile trees in savan- Lloret et al., 2012; Smith, 2011). At present, instances of abrupt veg-
nas (Scholes & Archer, 1997; Sankaran, Ratnam, & Hanan, 2004; etation shifts following extreme droughts are rare, and most studies
Bond, 2008; Riginos, 2009; February, Higgins, Bond, & Swemmer, thus far seem to suggest that savannas and many grassland commu-
2013; Ward, Weigand, & Getzin, 2013; Campbell & Holdo, 2017; nities have the capacity to recover from periodic droughts, although
Morisson, Holdo, Rugemalila, Nzunda, & Anderson, 2019). When recovery times can be substantial in some cases (Breshears et al.,
droughts do not significantly impact grass productivity and bio- 2016; Fensham et al., 2019; Fuhlendorf, Briske, & Smeins, 2001;
mass, mortality rates of tree seedlings, often vulnerable to grass Fuhlendorf & Smeins, 1997; Hoover et al., 2014; Lloret et al., 2012;
competition, may be exacerbated. In contrast, when grass pro- Swemmer et al., 2018; Walker et al., 1987). Several stabilizing pro-
ductivity and biomass are significantly depressed, droughts can cesses underlie this inertia to abrupt vegetation change, including
benefit the survival and growth of woody plants both directly by those that serve to attenuate mortality of trees and grasses during
reducing grass competition for limited soil moisture, as well as in- droughts (resistance), and factors that contribute to foster recovery
directly by reducing the frequency and intensity of grass‐fueled of productivity and species composition following droughts (resil-
fires (February et al., 2013; Higgins et al., 2000; Morrison et al., ience; Lloret et al., 2012; Table 2).
2019; Scholes & Archer, 1997). The extent to which tree seed- Factors that attenuate mortality of vegetation during droughts
lings are suppressed by grasses also appear to differ between spe- include site characteristics, lowered competition, facilitation, at-
cies, with tree species with higher photosynthetic rates suffering tenuation of stressors and functional trait diversity in communities
greater reductions in biomass in the presence of grasses (Campbell (Lloret et al., 2012). As discussed, spatial variability in topographic
& Holdo, 2017). Droughts can therefore differentially favour sur- and edaphic factors can generate a heterogeneous abiotic tem-
vival and establishment of fast‐growing savanna trees, potentially plate that can result in a mosaic of drought severity across the
leading to longer‐term compositional shifts in adult tree commu- landscape, enabling localized persistence of tree and grass pop-
nities. Thus, although savanna tree cover and basal area typically ulations during droughts and providing a source pool for subse-
increase with rainfall over broad gradients (Lehmann et al., 2014; quent recolonization (Lloret et al., 2012; O'Connor, 1995). In drier
Sankaran et al., 2005), reduced rainfall during droughts can para- sites, grasses can persist under tree canopies which provide ame-
doxically facilitate tree establishment, contingent on drought in- liorated conditions and protection from grazing during droughts,
tensity and its relative effects on grasses (February et al., 2013; even if populations are substantially reduced in tree interspaces
Scholes & Archer, 1997). (O'Connor, 1995). Similarly, heterogeneity in tree densities across
Site history also plays an important role in regulating the ex- the landscape can result in lowered mortality in low density sites
tent to which these different stressors impact growth and mortal- as a result of less intense competition for water. There is evidence
ity of savanna vegetation during droughts. A long history of heavy to suggest that reductions in tree densities following initial mor-
grazing can “precondition” sites for enhanced tree dieback during tality can increase available water for surviving individuals, low-
droughts (MacGreggor & O'Connor, 2002). Loss of perennial herba- ering competition and subsequent mortality of trees during later
ceous cover and increased cover of bare patches as a consequence stages of the drought (Lloret et al., 2012; Wonkka et al., 2016).
of overgrazing can accelerate erosion leading to increased run‐off Reductions in grazing and browsing intensity as a result of herbi-
and decreased infiltration in patches, enhancing soil water stresses vore die‐off or movement during droughts, as well as reductions
and tree mortality during droughts compared to light or moderately in fire frequencies and intensities as a result of lowered grass–fuel
 13652745, 2019, 4, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1111/1365-2745.13195 by Cochrane Colombia, Wiley Online Library on [20/03/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
SANKARAN Journal of Ecology | 1539

TA B L E 2 Community and ecosystem level determinants of the resistance and resilience of savannas to droughts

Resistance Resilience

Woody stratum Neighbourhood tree densities High representation of species with the ability to resprout
Species and functional trait diversity within the Increased post‐drought flowering and seeding by surviving trees
community Large soil seedbanks
Extent to which browsing intensity is altered dur- Reduced competition from grasses following droughts
ing droughts as a result of browser mortality and Lowered fire frequencies immediately following droughts
movement Reduced browsing pressure post‐drought
Extent to which frequency and intensity of fires Colonization ability of dominant species
are altered during droughts
Past stressors including previous browsing and
fire management, extent of desertification, past
history of droughts, and time since last drought
Understory Species and functional trait diversity within the Large soil seed banks
community Increased post‐drought flowering and seeding by surviving
Relative abundance of unpalatable grasses grasses
Extent to which grazing intensity is altered during Low extent of desertification (increase in bare ground) as a result
droughts as a result of grazer mortality and move- of the drought
ment Reduced competition from trees following droughts
Extent to which frequency and intensity of fires Reduced grazing pressure post‐drought
are altered during droughts Colonization ability of dominant species
Distance to permanent sources of surface water
Past stressors including previous grazing and fire
management, extent of desertification, past his-
tory of droughts, and time since last drought

loads can similarly lower mortality rates in the later stages of species (Cianciaruso, Silva, Batalha, Gaston, & Petchey, 2012; Simon
droughts. In addition, standing dead grass canopies have also & Pennington, 2012). Although detailed information from savanna
been shown to enhance survival and establishment of juvenile ecosystems are lacking, available data from across different vege-
trees during droughts by reducing irradiation and increasing soil tation types suggest that for both trees and grasses, physiological
moisture, thereby ameliorating abiotic conditions for seedlings (de drought tolerance ability (cavitation resistance) as well as variation in
Dios, Weltzin, Sun, Huxman, & Williams, 2014). vulnerability to cavitation across species (i.e. a measure of hydraulic
Plant species richness and functional diversity are also likely to trait diversity) increases with decreasing rainfall, with the greatest
be important determinants of the resistance and resilience of sa- range of variability observed between ~250 and 1,000 mm MAP,
vanna ecosystem processes to droughts. It is well established that that is, the rainfall regime that characterize savannas (Choat et al.,
the productivity of grasslands with higher plant species richness and 2012; Craine et al., 2013). These results are indicative of the poten-
functional diversity declines less, and recovers sooner, following tial for high functional trait diversity in savannas, and suggest that
droughts (Bloor & Bardgett, 2012; Isbell et al., 2015; Tilman, Reich, most savannas are likely to contain some species that are adapted
& Knops, 2006). Similarly, the functional diversity of woody plant to, and can tolerate and recover from, droughts (Choat et al., 2012;
hydraulic traits (hydraulic safety margins and cavitation resistance) Craine et al., 2013).
has been shown to be an important determinant of the extent to Indeed, many savannas appear surprisingly resilient to moderate
which land‐atmosphere fluxes of water, carbon and energy in for- and even severe short‐term droughts, capable of regaining produc-
ests are altered during droughts, with more functionally diverse tivity of both the herbaceous and woody strata within a year or two
communities buffered to a greater extent during periods of water (Fensham et al., 2019; Ruppert et al., 2015; Swemmer et al., 2018;
stress (Anderegg et al., 2018). However, unlike forests, most savan- Walker et al., 1987; Zeppel et al., 2015). Although droughts dras-
nas tend to be species poor (with the exception of the mesic savan- tically reduce above‐ground production of the grass layer, below‐
nas of S. America and the Miombo woodlands of southern Africa), ground biomass and production tend to be less affected, allowing
and dominated by one of a few families of woody plants (Bond & for post‐drought recovery (Koerner & Collins, 2014; Ruppert et al.,
Parr, 2010; Lehmann et al., 2014; Murphy et al., 2016; Sankaran & 2015). Similarly, resprouting ability, a common feature of many sa-
Ratnam, 2013). Such low phylogenetic diversity can be a potential vanna trees, allows trees to re‐establish quickly following distur-
cause for concern, particularly if drought‐tolerance traits tend to be bances compared to non‐resprouters that need to establish from
phylogenetically conserved. At present, it is unclear how diversity seed (Zeppel et al., 2015). Many resprouters have been shown to
of drought‐tolerance traits is related to phylogenetic diversity in sa- recoup much of their lost leaf area within a year following droughts
vanna species, but it is possible that drought traits, like those related (Zeppel et al., 2015), although some delay resprouting until after the
to fire‐tolerance, are phylogenetically over‐dispersed in savanna first summer rains following drought (Viljoen, 1995). Many savanna
 13652745, 2019, 4, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1111/1365-2745.13195 by Cochrane Colombia, Wiley Online Library on [20/03/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
1540 | Journal of Ecology SANKARAN

species also flower profusely following droughts (Viljoen, 1995). initial period of death (2 years), but continued drought led to the loss
Resultant increases in seed availability, when coupled with reduced of herbaceous vegetation and increases in the extent of bare ground
competition following adult tree die‐off and reduction in herba- (Wonkka et al., 2016). There is substantial evidence, both empiri-
ceous cover, can compensate for adult tree mortality by enhanc- cal and theoretical, to suggest that increased cover of bare ground
ing post‐drought recruitment (Lloret et al., 2012). Such enhanced can cause arid and semi‐arid systems to switch to an alternate stable
post‐drought recruitment can even occur several years following the state characterized by low water infiltration and high run‐off, where
drought, as has been reported for Sahelian woodlands (Hiernaux et original plant communities cannot re‐establish without human inter-
al., 2009; Lloret et al., 2012). vention (Rietkerk & van de Koppel, 1997; Rietkerk, Dekker, Ruiter, &
Changes in herbivory and fire regimes can also serve to facili- Koppel, 2004; van de Koppel, Rietkerk, & Weissing, 1997).
tate post‐drought vegetation recovery in savannas. Lowered herbi- Projected increases in the frequency of droughts potentially
vore populations as a result of movement, widespread mortality and pose the biggest threat for savannas, with the ability to impact
reduced and delayed calving success during droughts (Augustine, both the resistance and resilience of these ecosystems to future
2010; Ellis & Swift, 1988; Ogutu, Piepho, Dublin, Bhola, & Reid, droughts. Cumulative physiological damage and cavitation fatigue,
2010; Walker et al., 1987) can reduce post‐drought pressure on veg- i.e. increased vulnerability to cavitation as a result of previous dam-
etation, allowing vegetation to recover before herbivore populations age, can render individuals more susceptible to mortality during fu-
build up again. Similarly, drought‐induced reductions in grass bio- ture droughts (Anderegg, Berry, et al., 2012; Hartmann et al., 2018).
mass, and thus fuel loads, can result in fewer, smaller and less intense Recovery can also be slowed if frequent droughts diminish the ca-
fires immediately following droughts (Archibald et al., 2009; Balfour pacity of individuals to replenish stored reserves, which can impact
& Howison, 2002), benefitting woody communities in both the short vegetation recovery through resprouting, or when it reduces seed
and longer term by providing a window of opportunity for savanna production, impacting recovery through recolonization (Hartmann
tree saplings to grow and establish by escaping the “fire trap”. et al., 2018; Ruppert et al., 2015). Recurrent droughts can also in-
However, despite the existence of such stabilizing mecha- crease the likelihood of directional shifts in understory and woody
nisms, frequent, longer and more intense droughts can never- species composition when droughts recur before vegetation has re-
theless serve to destabilize savannas and lead to structural and covered, particularly where dominant species are disproportionately
compositional shifts in the future. Severe and protracted droughts affected by droughts. During successive droughts in the 1990s and
can significantly depress productivity and elicit widespread mor- 2000s, dominant Eucalypts in semi‐arid Australian savannas suf-
tality of vegetation in savannas (Fensham et al., 2009; Ruppert et fered greater mortality than sub‐dominant species (Fensham et al.,
al., 2015; Swemmer et al., 2018; Walker et al., 1987), and can also 2015; Fensham & Holman, 1999). Importantly, tree mortality pat-
drive compositional shifts in communities (Cipriotti, Flombaum, terns did not change between successive droughts and seedling to
Sala, & Aguiar, 2008; Evans, Byrne, Lauenroth, & Burke, 2011). adult ratios of the dominants following droughts was low, suggest-
Even if ecosystem productivity is regained quickly following re- ing that the cumulative effects of recurrent droughts could drive an
turn to normal conditions (Walker et al., 1987; Hoover et al., eventual shift in adult tree community composition in this system
2014), compositional shifts in tree and grass communities can (Fensham et al., 2015).
have longer term impacts on savanna function. Severe droughts
coupled with intense grazing can cause transitions from commu-
nities dominated by palatable, perennial grasses to systems com- 6 | A H I E R A RC H Y O F D R I V E R S
posed of unpalatable, annual grasses and forbs (Fuhlendorf et al.,
2001; Fuhlendorf & Smeins, 1997; Jin et al., 2018; Scholes, 1985; The extent to which meteorological droughts translate into physi-
O'Connor, 1994; ). Such changes in understory composition can ological droughts to influence the growth and survival of individual
be particularly hard to reverse, with recovery times ranging from trees and grasses in savannas is thus determined by a range of fac-
a few years to over a decade or more, and potentially requiring tors that operate at different spatial and temporal scales, and levels
the provisioning of seeds (Fuhlendorf & Smeins, 1997; O'Connor, of organization (Figure 1). At the broadest level, drought effects on
1998; Walker et al., 1987). Because annual‐dominated communi- the survival and growth of vegetation are a function of the severity
ties are less resistant to droughts than perennial‐dominated ones, and length of drought relative to what has been historically experi-
i.e. suffer greater reductions in productivity for the same drought enced by the community, that is, historical baseline (Smith, 2011). It
intensity, such compositional shifts can also impair the ability of is well recognized that all extreme events, including droughts do not
savannas to deal with future droughts (Ruppert et al., 2015). necessarily elicit extreme ecological responses (Smith, 2011). The
Of greater concern possibly is that protracted droughts have magnitude of the ecological responses elicited in any site depends
been shown to lead to desertification, i.e. increases in the cover of on both the severity and duration of drought relative to the historical
bare ground relative to vegetated patches (Vicente‐Serrano, Zouber, baseline, as well as vegetation and edaphic properties. Where me-
Lasanta, & Pueyo, 2012; Walker et al., 1987; Wonkka et al., 2016). teorological droughts translate into physiological droughts, the ex-
For example, during a severe 4‐year drought in a semi‐arid savanna tent to which any individual “experiences” the drought then depends
in west Central Texas, USA, tree mortality did not change after the on the landscape context within which it exists (e.g. topographic
 13652745, 2019, 4, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1111/1365-2745.13195 by Cochrane Colombia, Wiley Online Library on [20/03/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
SANKARAN Journal of Ecology | 1541

F I G U R E 1 A conceptual representation of the factors influencing the resistance and resilience of savanna ecosystems to droughts. (a)
A range of factors operating at different spatial scales and levels of organization collectively determine the extent to which meteorological
droughts influence productivity and mortality of individuals. Note that these are not nested factors that operate at increasingly finer
spatial scales, for example, stressors such as fire and herbivory can operate at scales larger than the landscape, and even extend beyond
drought impacted areas. (b) The extent to which such effects then translate to impact savanna vegetation state and ecosystem productivity
(depicted in (c)) is contingent on both individual responses as well as the species and functional trait diversity within the community. (c)
As droughts become more severe and extended (moving from top to bottom, i.e. from green to brown), vegetation responses become
increasingly pronounced from an initial loss of productivity to widespread tree and grass dieback and potentially desertification in arid and
semi‐arid savannas, that is, return to the initial state (green curved and dashed arrows) becomes progressively harder with these transitions
(as depicted by the decreasing width of the arrows), and is contingent on a range of different factors (d) that collectively determine savanna
resilience. When these are met (positive; green block arrow), vegetation is resilient. However, when conditions in (d) are not met (negative;
red block arrow), and when droughts are particularly severe, it can lead to compositional shifts (e) in vegetation. Such compositional shifts
in turn can feedback (f) to influence the ability of savannas to deal with future droughts by altering both the presence and diversity (i.e.
functional diversity) of drought‐tolerance and avoidance traits in the community (dashed arrows)

position) as well as its neighbourhood context (e.g. tree densities) differentially impacted by the drought. Community‐wide reductions
and size. For individuals who do experience significant physiological in biomass and productivity are likely to be more pronounced when
droughts, the ability to cope with drought is then determined by their the dominant species and large size classes of individuals are more
drought tolerance and avoidance strategies. However, additional risk negatively impacted. Greater species and functional trait richness
factors can further predispose individuals to suffer greater reduc- can buffer these impacts to some extent by increasing the proba-
tions in growth and increased mortality during droughts, including bility of species being present in the community that can cope with
past stressors (e.g. previous history of drought exposure, past dam- droughts. As droughts become more severe and/or protracted, loss
age by herbivores and fire) as well as those that operate during the of productivity becomes more pronounced as large‐scale grass and
drought (increased inter‐life form competition, herbivory and fire). tree dieback occurs, potentially leading to desertification in arid and
The extent to which such individual‐level effects then scale up semi‐arid regions.
to influence biomass, productivity and other processes at the eco- Post‐drought recovery of biomass, productivity and species
system level depends on how different species and size‐classes are composition is similarly a function of multiple factors that govern
 13652745, 2019, 4, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1111/1365-2745.13195 by Cochrane Colombia, Wiley Online Library on [20/03/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
1542 | Journal of Ecology SANKARAN

subsequent colonization, establishment (or re‐establishment) and open grasslands to closed woodlands, and differing in the character-
growth of vegetation (Figure 1, Table 2), with longer recovery times istics of the dominant trees (deciduous vs. evergreen, broad‐leaved
following droughts that are more protracted and severe. The herba- vs. fine‐leaved trees) and herbaceous vegetation (tall vs. short
ceous layer can generally be expected to recover biomass quicker grasses, annual vs. perennial). This variability arises from underly-
than the woody layer given their higher growth rates. The rate of ing differences in resource availability (rainfall and soil nutrients),
recovery of species composition on the other hand depends on the strength of top‐down forces (fire and herbivory) and evolutionary
extent to which species are differentially affected by droughts, with history (Lehmann et al., 2014; Lehmann, Archibald, Hoffmann, &
recovery times longer in systems where the dominant species are Bond, 2011; Sankaran et al., 2004; Scholes & Archer, 1997; Scholes
disproportionately impacted and are poor colonizers. However, as & Walker, 1993), and can pose challenges when generalizing drought
droughts become more frequent, or where desertification occurs, it effects across savannas. Understanding how these diverse savan-
can lead to compositional shifts in savanna understory and woody nas differ in their resistance and resilience to droughts represents a
communities. Such shifts can then feedback to influence the ability major task ahead for savanna ecologists; one that requires an inte-
of savannas to resist future droughts by altering both the distribu- grative approach that combines trait data quantification with obser-
tion of drought tolerance and avoidance traits as well as species and vation, experiments and modelling.
functional trait diversity in the community.
The relative roles of these different factors, and in turn the re-
7.1 | Expanded trait campaigns
sistance and resilience of savanna communities, can change across
rainfall gradients. Mesic savannas experience less inter‐annual There is an urgent need to move beyond reliance on one or a few eas-
variability and have historically been exposed to fewer extreme ily measurable traits to considering drought‐survival as the collec-
droughts, and so may be expected to be less resistant to longer and tive outcome of different combinations of tolerance and avoidance
more intense future droughts (Greenwood et al., 2017). However, traits, that is, syndromes. Initial efforts should aim to characterize
post‐drought recovery of productivity in these systems may be these syndromes, and identify representative tolerance and avoid-
faster (i.e. resilience higher) given the higher growth rates of vege- ance traits that encapsulate these strategies, which can then serve
tation. In contrast, arid and semi‐arid savannas display greater inter‐ as the basis for extended trait data collection campaigns in savan-
annual rainfall variability and experience more extreme droughts nas. In particular, traits regulating responses of understory species
compared to mesic systems, but also characterized by flora that have to droughts have received relatively less attention thus far compared
evolved to deal with protracted periods of water stress and may to the woody component, but are a prerequisite to predicting sa-
thus be expected to be more resistant to droughts (Fensham et al., vanna responses to droughts.
2009; Knapp & Smith, 2001; McDowell et al., 2008; O'Brien et al.,
2017; Vicente‐Serrano et al., 2013). When damage occurs though,
7.2 | Long‐term savanna monitoring plots
recovery of productivity typically tends to be slower in arid savannas
(Schwalm et al., 2017; Vicente‐Serrano et al., 2013). The likelihood Measures of population turnover can only be ob-
of drought‐induced desertification is also greater in arid and semi‐ tained by the detailed observation of individuals‐they
arid sites (Scholes et al., 2018), particularly those with high abun- are totally obscured by vegetational study and re-
dance of livestock, which can further undermine recovery following vealed by population studies only if plants are marked
severe droughts. In many arid and semi‐arid savannas, native her- for repeated observations. Harper, 1967
bivore assemblages have been replaced by domestic livestock that
are maintained at artificially high densities, and also buffered against As we go forward, a network of long‐term savanna monitoring
mortality during droughts, as a result of supplemental provisioning plots where individuals are tagged and monitored over time will be
of water and forage by humans, and predator and disease control invaluable. Such efforts can provide us with insights into vegeta-
(Hempson, Archibald, & Bond, 2015, 2017). The “sedantarization” tion dynamics and demography that other kinds of studies cannot
of livestock has also resulted in grazing and browsing regimes being (Harper, 1967). In fact, many of our insights into drought responses
more “chronic” in these systems, with significant negative conse- of vegetation have come fortuitously from opportunistic studies
quences for the ability of vegetation to both withstand droughts, as in forested ecosystems where droughts have occurred during the
well as recover from them. These arid and semi‐arid rangelands are course of ongoing long‐term observational and experimental stud-
potentially at the greatest risk of drought‐driven shifts in vegetation ies (Breshears et al., 2009; Fensham et al., 2017; Phillips et al., 2009;
structure and composition in the future. Smith, 2011). However, in contrast to forests, a network of long‐
term monitoring plots that spans the climatic, edaphic and biotic
gradients that characterize savanna ecosystems is currently lack-
7 | TH E WAY A H E A D ing (Staver, 2018). Such long‐term efforts are particularly insightful
because: (a) detailed pre‐drought data on vegetation are available,
Tropical savannas are highly variable in structure and composition which is useful for understanding the role of previous stressors and
across their distributional range, spanning the gradient from nearly past individual performance on drought survival, (b) concurrent
 13652745, 2019, 4, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1111/1365-2745.13195 by Cochrane Colombia, Wiley Online Library on [20/03/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
SANKARAN Journal of Ecology | 1543

data on physiological parameters and water stress metrics are often eutrophic sites while non‐fixers dominate in mesic, dystrophic sites
available, or can be gathered, which can provide us with a more (Pellegrini, Staver, Hedin, Charles‐Dominique, & Tourgee, 2016;
nuanced understanding of drought responses of vegetation, (c) Scholes & Walker, 1993). Few studies have evaluated differences
sustained monitoring can provide us with key information on post‐ in drought tolerance abilities of N‐fixing and non N‐fixing savanna
drought recovery and factors affecting resilience of vegetation, for species, but evidence from other systems suggests that the high
which data are currently limited, as well as help understand how tissue N and water‐use efficiencies of N‐fixing species might help
repeated droughts impact the resistance and resilience of savanna them survive and compete better during prolonged droughts (Liao,
vegetation, and (d) data are available even when the ecological Menge, Lichstein, & Ángeles‐Pérez, 2017; Wurzburger & Ford
responses to climatic droughts are not extreme. This last point is Miniat, 2014).
critical because in order to effectively predict savanna responses,
we need to understand plant traits and site characteristics that con-
7.4 | Process‐based models
fer resistance as well as render vegetation susceptible to droughts
(Breshears et al., 2009; Fensham et al., 2009; Mitchell et al., 2014; Finally, data from experiments, observational studies and trait
Smith, 2011). campaigns need to feed into process‐based vegetation models
to better predict future savanna responses to droughts. Process
based models offer some of the most promising approaches for
7.3 | Targeted field experiments
predicting future vegetation responses to drought, and can also
There is a large body of experimental work that has provided us with capture spatial variability in mortality patterns (Anderegg et al.,
a wealth of understanding on the responses of temperate grasslands 2015). However, mechanisms of drought‐induced mortality are
to changes in precipitation patterns, including extreme drought currently poorly represented in most dynamic vegetation models,
(Cherwin & Knapp, 2012; Fay, Carlisle, Knapp, Blair, & Collins, 2003; and they do not always successfully predict observed patterns of
Heisler‐White, Blair, Kelly, Harmoney, & Knapp, 2009; Heisler‐White, drought‐induced mortality (Anderegg et al., 2015, Choat et al.,
Knapp, & Kelly, 2008; Knapp et al., 2008; Thomey et al., 2011 and 2018, and references therein). A more comprehensive understand-
others). However, rainfall manipulation studies in savannas are cur- ing of how trait variability across species and plant functional types
rently very limited (but see February et al., 2013, Manea & Leishman, in savannas influences mortality and demographic outcomes dur-
2015). Experimental manipulations in the field can be logistically ing droughts can help refine model parameterization and greatly
challenging, particularly in the presence of fire and mega‐herbivores improve their forecasting ability (Anderegg et al., 2015; Choat et
such as elephants, but are needed to better understand how changes al., 2018).
in the intensity, duration and timing of droughts influence vegetation Moving forward, there are several key questions that need
responses across diverse savanna types. Experimental manipula- addressing: What are the drought characteristics (severity, length
tions that impose droughts on large trees will also be needed (Choat and frequency) that elicit ecological responses in savannas, and
et al., 2018) for a more comprehensive understanding of drought ef- how do these vary across the rainfall gradient from arid to mesic
fects in savannas. savannas? How do drought‐survival syndromes change across
Importantly, all these efforts, from trait data collection to mon- rainfall gradients, and do they differ between dominant plant
itoring and experiments, must span the rainfall, soil fertility, fire functional types in savannas? What is the role of evolutionary his-
and herbivory gradients, as well as the diversity of tree and grass tory in determining drought tolerance trait distribution patterns
functional types that characterize the diverse savannas on different across different savannas of the world, that is, are some traits
continents. Savannas on different continents differ in the extent to phylogenetically conserved while others over‐dispersed within
which they are dominated by different functional groups (evergreen local flora, and are these patterns consistent across savannas on
vs. deciduous, fine‐leaved N‐fixers vs. broadleaved non‐fixers). different continents? How are resistance traits correlated with
African and Asian savannas are dominated by deciduous trees, S. resilience traits? Is there a trade‐off between traits that confer
American savannas are largely evergreen while Australian savannas drought resistance with those that allow savanna vegetation to
are characterized by a mix of evergreen, deciduous, semi‐deciduous persist in the face of other disturbances such as fire and herbivory,
and brevi‐deciduous species (Bowman & Prior, 2005; Eamus, 1999). or deal with future global changes?
Few studies have explicitly considered how drought tolerance and Our understanding of the mechanisms, physiological thresholds
the mechanisms driving mortality differ between deciduous and and traits that govern vegetation responses to drought, especially
evergreen savanna trees, but it could be argued that evergreen trees, has improved substantially in the last decade, thanks largely
species are under greater risk of mortality through cavitation to a substantial body of recent work emanating from forest ecosys-
during severe droughts, while deciduous species that shed leaves tems. However, in order to predict savanna responses to drought
are under greater risk of carbon starvation as droughts get longer. this body of knowledge needs to be integrated with a detailed under-
Similarly, dominance by N‐fixing species also differs between con- standing of not just grass responses to droughts, but also feedback
tinents; N‐fixers are more abundant in African and Asian savannas effects arising through alterations in herbivory and fire regimes. It
compared to S. America and Australia, and tend to dominate in arid, is now fairly well‐established that savannas on different continents,
 13652745, 2019, 4, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1111/1365-2745.13195 by Cochrane Colombia, Wiley Online Library on [20/03/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
1544 | Journal of Ecology SANKARAN

while structurally similar, differ functionally in their sensitivities and Anderegg, W. R., Berry, J. A., & Field, C. B. (2012). Linking definitions,
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Anderegg, W. R. L., Kane, J. M., & Anderegg, L. D. L. (2012). Consequences
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Anderegg, W. R., Konings, A. G., Trugman, A. T., Yu, K., Bowling, D. R.,
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