Xylem dysfunction in fires: towards a hydraulic theory of plant responses to multiple disturbance stressors

Abstract

It is often thought that a wildfire will consume and kill all of the vegetation within its perimeter, but this is more an exception than a rule. Indeed, heterogeneity of fuels and microclimate leads to heterogeneity of fire behavior and effects, so that injured but surviving plants often remain after a wildfire. This has important emergent outcomes spanning levels of biological organization, from cellular photosynthesis and respiration to ecosystem production and evapotranspiration. However, despite more than half a century of research, the mechanisms by which fire injuries occur and interact are not well understood.

Full text

Commentary
Xylem dysfunction in fires:
towards a hydraulic theory of
plant responses to multiple
disturbance stressors
It is often thought that a wildfire will consume and kill all of the
vegetation within its perimeter, but this is more an exception than a
rule. Indeed, heterogeneity of fuels and microclimate leads to
heterogeneity of fire behavior and effects, so that injured but
surviving plants often remain after a wildfire (Bond & Van Wilgen,
1996). This has important emergent outcomes spanning levels of
biological organization, from cellular photosynthesis and respira-
tion to ecosystem production and evapotranspiration. However,
despite more than half a century of research, the mechanisms by
which fire injuries occur and interact are not well understood
(Michaletz & Johnson, 2007).
‘They also show for the first time that wildfires
can permanently alter xylem vulnerability to
cavitation, rendering plants more susceptible to future
disturbances ...’
In this issue of New Phytologist,B€ar et al. (pp. 1484-1493)
provide a critical step forward in our understanding of fire effects on
plants by presenting the first quantitative evidence that wildfires
cause xylem dysfunction. Using branches collected from trees that
survived a recent wildfire, they show that fires can permanently
reduce xylem conductivity via conduit wall deformation. This had
previously only been shown in laboratory experiments (Michaletz
et al., 2012; West et al., 2016). They also show for the first time that
wildfires can permanently alter xylem vulnerability to cavitation,
rendering plants more susceptible to future disturbances such as fire
(Brando et al., 2014) and drought (Anderegg et al., 2013). This had
not been observed in previous studies that tested for it (Michaletz
et al., 2012; Battipaglia et al., 2016). The findings of B€ar et al. shed
new light on the complex set of mechanisms governing fire effects
on plants, and contribute to a growing framework for understand-
ing and predicting plant responses to multiple interacting distur-
bance stressors.
How do fires injure plants?
Heat transfer from a fire into a plant can injure the roots, stem, or
crown (Fig. 1; Mi chaletz & Johnson, 2007). Root injuries occur via
conduction heat transfer through soil and into the roots, while
stems and crowns are heated by radiation and convection to the
plant and conduction within the plant. Heating by fire can cause
necrosis of living cells if they exceed a threshold temperature of
c.60°C. Necrosis of meristematic tissues can limit or prevent
growth of other critical tissues and organs such as phloem, xylem,
roots and leaves. Heating may also cause dysfunction of xylem
tissue, which limits xylem water flow. This can reduce stomatal
conductance and rates of carbon assimilation.
Heat injuries may then interact to influence whole-plant function
and mortality. There are two main hypotheses for post-fire plant
mortality: the cambium necrosis hypothesis and the xylem
dysfunction hypothesis (Balfour & Midgley, 2006; Kavanagh
et al., 2010; Midgley et al., 2011; Michaletz et al., 2012). According
to the cambium necrosis hypothesis, phloem and cambium necrosis
limits carbon translocation to roots, so that root growth must rely
upon stored carbon reserves. When these reserves ar e depleted, fine-
root production ceases and plant mortality occurs as a result of
hydraulic failure (McDowell et al., 2008). According to the xylem
dysfunction hypothesis, heating reduces the hydraulic conductivity
of the xylem, which increases xylem water tensions, increases
periods of stomatal closure, and limits carbon assimilation and
growth. Plant mortality may then result from hydraulic failure or
carbon starvation (McDowell et al., 2008; Sevanto et al., 2014).
Experimental support for the xylem dysfunction
hypothesis
Plant mortality in fires has traditionally been thought to result from
cambium necrosis (Michaletz & Johnson, 2007), but there is
growing support for a more hydraulics-based view of fire effects on
plants. Stem heating experiments have shown that heat impairs
plant hydraulic function. For example, stem heating caused
reductions in sap flux density, stomatal conductance, and net
photosynthesis (Ducrey et al., 1996). While these results are
consistent with the xylem dysfunction hypothesis, they are not
conclusive since the experiments also caused phloem and cambium
necrosis. Thus, it is unclear whether the results reflect limitation of
fine-root growth by phloem necrosis, limitation of xylem growth by
cambium necrosis, or heat-induced xylem dysfunction. In another
study, stem heating reduced the cross-sectional area of functional
xylem, which by definition reduces the hydraulic conductivity of the
stem (Balfour & Midgley, 2006). These reductions were semi-
permanent following reflushing to remove air embolisms, suggest-
ing that heating reduced the xylem conductivity by one or more
mechanisms that were not fully consistent with air seed cavitation.
This article is a Commentary on B€ar et al., 217: 1484–1493.
Ó2018 The Author
New Phytologist Ó2018 New Phytologist Trust
New Phytologist (2018) 217: 1391–1393 1391
www.newphytologist.com
Forum

Building on this work, Michaletz et al. (2012) used laboratory air
injection experiments to demonstrate that heating reduces the
hydraulic conductivity of xylem via at least two mechanisms: (1) air
seed cavitation resulting from temperature-dependent changes in
sap surface tension; and (2) conduit wall deformation resulting
from thermal softening of viscoelastic cell wall polymers (lignin,
hemicelluloses, and cellulose). Both of these mechanisms were
subsequently observed to reduce xylem conductivity in laboratory
heat plume experiments (West et al., 2016). While air seed
cavitation can be repaired, conduit wall deformation is permanent
once the xylem cools and viscoelastic polymers return to a glassy
state. Thus, conduit wall deformation is especially injurious.
Thermal softening effects on pit membrane structure would also
permanently alter cavitation vulnerability, but only marginal and
nonsignificant changes were observed in these experiments
(Michaletz et al., 2012).
Can wildfires cause xylem dysfunction?
Although air seed cavitation and conduit wall deformation have
been observed in laboratory experiments, it has been less clear how
common they are in real wildfires. Several studies provide indirect
evidence for xylem dysfunction in wildfires. For example, heat
transfer simulations forced with wildfire temperature data pre-
dicted that tree stems can experience substantial reductions in the
cross-sectional area of functional xylem (Michaletz et al., 2012).
Consistent with these predictions, analyses of xylem anatomy in
fire-injured tree stems have revealed large areas of discolored and
presumably nonfunctional wood (Fig. 2; Smith et al., 2016).
Wildfires have also been shown to reduce stomatal cond uctance and
predawn water potential (Thompson et al., 2017), and also cause
higher mortality rates compared with stems that had their phloem
and cambium removed (Midgley et al., 2011). Post-fire mortality
rates also vary inversely with wood density (Brando et al., 2012),
which likely reflects the role of wood density in prevention of heat-
induced cavitation and conduit wall deformation (Hacke et al.,
2001; Michaletz et al., 2012). While all of these results are
consistent with xylem dysfunction in fires, they also likely reflect the
influence of other fire injuries and thus cannot confirm the xylem
dysfunction hypothesis (Fig. 1).
Towards a hydraulic theory of plant responses to
disturbance
The results of B€ar et al. provide the first direct quantitative evidence
for xylem dysfunction in wildfires. This is an important contribution
to our understanding of plant responses to disturbance and helps set
an agenda for future research. For example, B€ar et al. observed
reduced xylem conductivity in angiosperms but not gymnosperms,
and these results were associated with differences in the severity of
conduit wall deformation between angiosperms and gymnosperms.
This suggests that angiosperms and gymnosperms may differ in the
kinetics of conduit wall polymer softening, or that softened vessels
and tracheids may differ in their responses to stresses imposed by
tensile sap water. Further work is needed to identify how variation in
xylem traits operates via these mechanisms to drive variation in fire
effects. B€ar et al. also provide the first documentation of changes in
vulnerability to cavitation following wildfire. While all tested species
experienced increases in vulnerability, the magnitude of these
changes varied among species in a manner more complex than
Convecon
Conducon
Radiaon
Crown injury
•Leaf necrosis
•Bud meristem necrosis
•Phloem & cambium necroses
•Xylem dysfuncon
Stem injury
•Phloem & cambium necroses
•Xylem dysfuncon
Root in jury
•Fine root necrosis
•Phloem & cambium necroses
•Xylem dysfuncon
Fig. 1 Heat transfer from a wildfire to a plant, and key injuries that may result
from heat conduction within the plant.
(a) (b)
Fig. 2 Anatomical evidence is consistent with heat-induced xylem dysfunction following wildfire (Smithet al., 2016). (a) Cross-section of western larch (Larix
occidentalis Nutt.) containing healed fire scars and areas of xylem discoloration. (b) Detail from white box in (a) shows a substantial area of discolored wood
(DW), heartwood (HW), and sapwood (SW; functional xylem). The areas of discoloration are likely nonfunctional xylem, but this has not been confirmed by
hydraulic conductivity measurements. Photographs courtesy of Kevin Smith.
New Phytologist (2018) 217: 1391–1393 Ó2018 The Author
New Phytologist Ó2018 New Phytologist Trust
www.newphytologist.com
Commentary
Forum
New
Phytologist
1392

simple angiosperm/gymnosperm or vessel/tracheid dichotomies.
Along with previous experiments reporting nonsignificant increases
in vulnerability (Michaletz et al., 2012), this suggests future work is
needed to understand the mechanisms by which variation in thermal
softening and pit membrane morphology leads to variation in post-
fire cavitation vulnerability.
Despite our growing knowledge of how plant physiology responds
to disturbances such as fire and drought, we still have a limited
understanding of how the responses interact to control whole-plant
function and mortality, especially over longer periods of time
(Michaletz & Johnson, 2007; Allen et al., 2010; van Mantgem et al.,
2013). Conduit wall deformation and increased cavitation vulner-
ability are permanent fire injuries that may contribute to cumulative
xylemdysfunctionandmakeplantsmoresusceptibletofuture
disturbances (Anderegg et al., 2013). Indeed, post-fire mortality rates
are strongly influenced by the number of fires a tree experiences
(Brando et al., 2012), and are higher for water-stressed plants subject
to drought (van Mantgem et al., 2013; Brando et al., 2014). This
indicates an important role for fire-induced xylem dysfunction in the
long-term responses of plants to climate and disturbance, and
suggests that understanding and predicting these responses is more
complex than previously thought. Additional work is required to
understand the relative roles of cavitation and deformation in
reduction of xylem conductivity, and how xylem dysfunction in
roots, stems, and branches correlates and interacts with other injuries
to influence plant function and mortality (Fig. 1; Michaletz et al.,
2012). For example, necrosis and cavi tation (hydrauli c segmentation)
of leaves may act as a ‘hydraulic fuse’ that limits tension and cavitation
in proximal parts of the xylem network (Kavanagh et al., 2010; West
et al., 2016; Wolfe et al., 2016). Understanding how such processes
may correlate and interact with those demonstrated by B€ar et al. is a
next step towards incorporating cumulative disturbance impacts into
climate–vegetation models (Anderegg et al., 2013).
Acknowledgements
The author thanks Kevin Smith for kindly providing the
photographs used in Fig. 2, and acknowledges the support from
the Thomas R. Brown Family Foundation.
ORCID
Sean T. Michaletz Xhttp://orcid.org/0000-0003-2158-6525
Sean T. Michaletz
1,2
X
1
Biosphere 2, University of Arizona, Tucson, AZ 85721, USA; and
2
Department of Ecology and Evolutionary Biology, University of
Arizona, Tucson, AZ 85721, USA
(tel+1 520 626 3336; email michaletz@email.arizona.edu)
References
Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M,
Kitzberger T, Rigling A, Breshears DD, Hogg EH (T.) et al. 2010. A global
overview of drought and heat-induced tree mortality reveals emerging climate
change risks for forests. Forest Ecology and Management 259: 660–684.
Anderegg WRL, Plavcova L, Anderegg LDL, Hacke UG, Berry JA, Field CB.
2013. Drought’s legacy: multiyear hydraulic deterioration underlies widespread
aspen forest die-off and portends increased future risk. Global Change Biology 19:
1188–1196.
Balfour DA, Midgley JJ. 2006. Fire induced stem death in an African acacia is not
caused by canopy scorching. Austral Ecology 31: 892–896.
B€ar A, Nardini A, Mayr S. 2018. Post-fire effects in xylem hydraulics of Picea abies,
Pinus sylvestris and Fagus sylvatica.New Phytologist 217: 1484–1493.
Battipaglia G, Savi T, Ascoli D, Castagneri D, Esposito A, Mayr S, Nardini A.
2016. Effects of prescribed burning on ecophysiological, anatomical and stem
hydraulic properties in Pinus pinea L. Tree Physiology 36: 1019–1031.
Bond WJ, Van Wilgen BW. 1996. Fire and plants (population and community biology
series 14). Population and community biology. London, UK: Chapman & Hall.
Brando PM, Balch JK, Nepstad DC, Morton DC, Putz FE, Coe MT, Silverio D,
Macedo MN, Davidson EA, Nobrega CC et al. 2014. Abrupt increases in
Amazonian tree mortality due to drought–fire interactions. Proceedings of the
National Academy of Sciences, USA 111: 6347–6352.
Brando PM, Nepstad DC, Balch JK, Bolker B, Christman MC, Coe M, Putz FE.
2012. Fire-induced tree mortality in a neotropical forest: the roles of bark traits,
tree size, wood density and fire behavior. Global Change Biology 18: 630–641.
Ducrey M, Duhoux F, Huc R, Rigolot E. 1996. The ecophysiological and growth
responses of Aleppo pine (Pinus halepensis) to controlled heating applied to the
base of the trunk. Canadian Journal of Forest Research 26: 1366–1374.
Hacke UG, Sperry JS, Pockman WT, Davis SD, McCulloh KA. 2001. Trends in
wood density and structure are linked to prevention of xylem implosion by
negative pressure. Oecologia 126: 457–461.
Kavanagh KL, Dickinson MB, Bova AS. 2010. A way forward for fire-caused tree
mortality prediction: modeling a physiological consequence of fire. Fire Ecology 6:
80–94.
van Mantgem PJ, Nesmith JC, Keifer M, Knapp EE, Flint A, Flint L. 2013.
Climatic stress increases forest fire severity across the western United States.
Ecology Letters 16: 1151–1156.
McDowell N, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, Plaut J,
Sperry J, West A, Williams DG et al. 2008. Mechanisms of plant survival and
mortality during drought: why do some plants survive while others succumb to
drought? New Phytologist 178: 719–739.
Michaletz ST, Johnson EA. 2007. How forest fires kill trees: a review of the
fundamental biophysical processes. Scandinavian Journal of Forest Research 22:
500–515.
Michaletz ST, Johnson EA, Tyree MT. 2012. Moving beyond the cambium
necrosis hypothesis of post-fire tree mortality: cavitation and deformation of
xylem in forest fires. New Phytologist 194: 254–263.
Midgley JJ, Kruger LM, Skelton R. 2011. How do fires kill plants? The hydraulic
death hypothesis and Cape Proteaceae ‘fire-resisters’. South African Journal of
Botany 77: 381–386.
Sevanto S, McDowell NG, Dickman LT, Pangle R, Pockman WT. 2014. How do
trees die? A test of the hydraulic failure and carbon starvation hypotheses. Plant,
Cell & Environment 37: 153–161.
Smith KT, Arbellay E, Falk DA, Sutherland EK. 2016. Macroanatomy and
compartmentalization of recent fire scars in three North American conifers.
Canadian Journal of Forest Research 46: 535–542.
ThompsonMTC, Koyama A, Kavanagh KL.2017. Wildfire effects on physiological
properties in conifers of central Idaho forests, USA. Trees 31: 545–555.
West AG, Nel JA, Bond WJ, Midgley JJ. 2016. Experimental evidence for heat
plume-induced cavitation and xylem deformation as a mechanism of rapid post-
fire tree mortality. New Phytologist 211: 828–838.
Wolfe BT, Sperry JS, Kursar TA. 2016. Does leaf shedding protect stems from
cavitation during seasonal droughts? A test of the hydraulic fuse hypothesis. New
Phytologist 212: 1007–1018.
Key words: cavitation, disturbance, drought, embolism, fire, global change,
hydraulic conductivity, mortality.
Ó2018 The Author
New Phytologist Ó2018 New Phytologist Trust
New Phytologist (2018) 217: 1391–1393
www.newphytologist.com
New
Phytologist Commentary Forum 1393