Tree Physiology 33, 669–671
doi:10.1093/treephys/tpt046
Commentary
Predicting thresholds of drought-induced mortality in woody
plant species
Brendan Choat1
University of Western Sydney, Hawkesbury Institute for the Environment, Richmond, New South Wales 2753, Australia; 1Corresponding author ([email protected])
Received May 2, 2013; accepted June 2, 2013; published online July 21, 2013; handling Editor Danielle Way
Climate change is expected to result in an increased frequency
of extreme events; while in some areas, heavier precipitation is
predicted, other areas will suffer from more intense heat waves
and droughts (Allison et al. 2009). Disturbingly, there is already
evidence that increasing temperatures and reduced rainfall
associated with climate change are responsible for an acceleration of large-scale forest dieback over the last century
(Breshears et al. 2005; Allen et al. 2010). In the absence of
mass mortality events, severe droughts can cause forest ecosystems to flip from net sinks to huge sources of CO2, with the
response of the Amazon rainforest to recent droughts being
the clearest example of this (Phillips et al. 2009). Increasingly,
severe droughts are therefore expected to have profound
effects on biodiversity, primary productivity and ecosystem
function in many forested regions.
Recent analyses have demonstrated that the majority of
woody plant species across all forest biomes operate close to
their safety margins for hydraulic failure, rendering them vulnerable to future shifts in precipitation and temperature (Choat
et al. 2012). The safety margin referred to is the difference
between the level of water stress experienced by a species in
the field and the level of water stress that is likely to induce
hydraulic failure in that species. In order to make accurate predictions of how different forest ecosystems and keystone species will be affected by drought, we require a detailed
understanding of the physiology of plant death. The development of quantitative indices for mortality thresholds in woody
plants is therefore essential for predictive models of vegetation
response to drought. Despite this seemingly straight forward
question (when is a plant dead?), reliable mortality indices are
conspicuously lacking in the plant physiologist’s tool kit
(Anderegg et al. 2012).
Hydraulic failure is now widely recognized as one of the key
mechanisms of drought-induced mortality in woody plants
(Tyree and Sperry 1989; McDowell et al. 2008). As the soil
dries, greater tension develops in the xylem water column
leading to an increased probability of embolism formation. Gas
emboli block xylem vessels, reducing the capacity of the plant
to move water to the canopy. In intense or prolonged droughts,
xylem embolism becomes extensive, causing the death of the
whole plant.
In this issue of Tree Physiology, Urli et al. (2013) examine
thresholds for hydraulic failure in a range of angiosperm species with a view to linking drought tolerance, survival and
embolism resistance in five angiosperm tree species. Their
results show that a physiological ‘point of no return’ can be
predicted for these species based on the half time of their
recovery after rewatering. This approach defines a critical
water potential beyond which plants were unable to recover,
even after 1 year of rewatering (Brodribb and Cochard 2009).
The authors then compared the minimum recoverable water
potential with vulnerability to embolism curves for each species. This represents an important step because we already
possess vulnerability curve data from hundreds of species
across the full range of forest biomes (Maherali et al. 2004;
Choat et al. 2012). Vulnerability curves describe the relationship between xylem water potential and loss of hydraulic conductivity due to embolism for a given species. Species are
most commonly compared by the water potential at which
50% of hydraulic conductivity is lost (P50). In a previous work,
Brodribb and Cochard (2009) demonstrated that the minimum
recoverable water potential for four gymnosperm species was
very close to species P50 values. In contrast, Urli et al. (2013)
show that the minimum recoverable water potential of five
© The Author 2013. Published by Oxford University Press. All rights reserved. For Permissions, please email: [email protected]
670 Choat
Figure 1. ​(a) Transverse sections of xylem from a gymnosperm (top) and an angiosperm (bottom). The xylem of gymnosperms consists of 95%
tracheids with a small proportion of ray parenchyma. Angiosperm vessels can attain greater diameters than gymnosperms and are surrounded by
thick-walled fibres that provide biomechanical support. (b) Relationship between embolism resistance (P50) and the minimum water potenial
observed in the field (Ψmin) for angiosperm and gymnosperm species. The dashed line is the 1 : 1 relationship between P50 and Ψmin. The safety
margin is the difference bewteen the Ψmin and P50 for each group. Modified from Choat et al. (2012).
angiosperm species was closer to the point at which 88% loss
of conductivity occurred (P88).
This finding provides insight into how basic differences in
xylem structure between gymnosperms and angiosperms
translate to the physiological behaviour of these groups
(Figure 1a). Gymnosperm xylem consists almost entirely of unicellular tracheids, which perform both transport and support
functions for the plant. In angiosperm xylem, support and
transport functions are performed by more specialized cell
types than the tracheid: thick-walled fibres provide support,
while multicellular vessels can attain much greater lengths and
diameters (Choat et al. 2008).
The wide vessels of angiosperm xylem allow them to attain
much higher hydraulic conductivity than gymnosperms. How­
ever, angiosperms also engage in a much riskier hydraulic
strategy than gymnosperms. While angiosperms converge on
their P50 safety margins, gymnosperms maintain much greater
safety margins to P50, especially species with greater resistance to embolism (Figure 1b; Choat et al. 2012). This more
conservative hydraulic strategy is logical if gymnosperm species tend to die closer to P50, while angiosperms die closer to
P88. The fact that the stomatal behaviour of angiosperms leads
them to more regularly experience higher levels of embolism
may also be indicative of higher capacity for rapid embolism
repair, although this remains to be confirmed (Johnson et al.
2012).
Readers may note that if gymnosperms die close to P50, then
hydraulic failure in the stem is clearly not directly responsible
for the death of the plant. Roots and leaves are usually less
resistant to embolism within a plant and it is therefore possible
Tree Physiology Volume 33, 2013
that hydraulic failure in the root system and needles of gymnosperms may be a more direct driver of mortality than failure in
the stem. Further research is required to establish whether this
is the case and whether rundown of carbohydrate reserves
plays a great role in some species (Mitchell et al. 2013).
. . . and of course, some caveats. First, while the relationships
between minimum recoverable water potential and P88 were
strong in Urli et al. (2013), this relationship is based on a small
number of species. Full confidence in this approach, and the
observed differences between angiosperms and gymnosperms,
will require data from a greater number of species. This
approach may prove less precise in drought deciduous species,
where leaf abscission occurs well before the minimum recoverable water potential has been reached. Plants capable of
resprouting may present complications for the approach of
defining a minimum survivable water potential. Finally, it is
important to recognize that there is no magic line across which
all species will consistently die. The data of Urli et al. (2013)
and earlier studies (Kursar et al. 2009) show, while angiosperm species die close to P88, that there can be substantial
between-species variation around this point.
However, these issues are certainly not insurmountable and
the work of Urli et al. (2013) brings us closer to an index that
will allow for prediction of drought mortality thresholds for
woody plant species across a wide range of environments.
References
Allen CD, Macalady AK, Chenchouni H et al. (2010) A global overview
of drought and heat-induced tree mortality reveals emerging climate
change risks for forests. For Ecol Manag 259:660–684.
Predicting thresholds of drought-induced mortality in woody plant species 671
Allison I, Bindoff NL, Bindschadler RA et al. (2009) The Copenhagen
Diagnosis: updating the world on the latest climate science. The
University of New South Wales Climate Research Centre, Sydney,
Australia.
Anderegg WRL, Berry JA, Field CB (2012) Linking definitions, mechanisms, and modeling of drought-induced tree death. Trends Plant Sci
17:693–700.
Breshears DD, Cobb NS, Rich PM et al. (2005) Regional vegetation
die-off in response to global-change-type drought. Proc Natl Acad
Sci USA 102:15144–15148.
Brodribb TJ, Cochard H (2009) Hydraulic failure defines the recovery
and point of death in water-stressed conifers. Plant Physiol
149:575–584.
Choat B, Cobb AR, Jansen S (2008) Structure and function of bordered pits: new discoveries and impacts on whole-plant hydraulic
function. New Phytol 177:608–625.
Choat B, Jansen S, Brodribb TJ et al. (2012) Global convergence in the
vulnerability of forests to drought. Nature 491:752–755.
Johnson DM, McCulloh KA, Woodruff DR, Meinzer FC (2012) Hydraulic
safety margins and embolism reversal in stems and leaves: why are
conifers and angiosperms so different? Plant Sci 195:48–53.
Kursar TA, Engelbrecht BMJ, Burke A, Tyree MT, El Omari B, Giraldo JP
(2009) Tolerance to low leaf water status of tropical tree seedlings
is related to drought performance and distribution. Funct Ecol
23:93–102.
Maherali H, Pockman WT, Jackson RB (2004) Adaptive variation in the
vulnerability of woody plants to xylem cavitation. Ecology
85:2184–2199.
McDowell N, Pockman WT, Allen CD et al. (2008) Mechanisms of plant
survival and mortality during drought: why do some plants survive
while others succumb to drought? New Phytol 178:719–739.
Mitchell PJ, O’Grady AP, Tissue DT, White DA, Ottenschlaeger ML,
Pinkard EA (2013) Drought response strategies define the relative
contributions of hydraulic dysfunction and carbohydrate depletion
during tree mortality. New Phytol 197:862–872.
Phillips OL, Aragão LEOC, Lewis SL et al. (2009) Drought sensitivity of
the amazon rainforest. Science 323:1344–1347.
Tyree MT, Sperry JS (1989) Vulnerability of xylem to cavitation and
embolism. Annu Rev Plant Physiol Plant Mol Biol 40:19–38.
Urli M, Porté AJ, Cochard H, Guengant Y, Burlett R, Delzon S (2013)
Xylem embolism threshold for catastrophic hydraulic failure in angiosperm trees. Tree Physiol 33:672–683.
Tree Physiology Online at http://www.treephys.oxfordjournals.org