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Tansley review
Fire effects on tree physiology
Author for correspondence:
Andreas B€
ar
Tel.: +43 650 8709399
Email: andreas.baer@uibk.ac.at
Received: 21 January 2019
Accepted: 7 April 2019
Andreas B€ar
1
, Sean T. Michaletz
2
and Stefan Mayr
1
1
Department of Botany, University of Innsbruck, Sternwartestraße 15, Innsbruck 6020, Austria;
2
Department of Botany and
Biodiversity Research Centre, University of British Columbia, Vancouver, BC V6T 1Z4, Canada
Contents
Summary 1728
I. Introduction 1728
II. First- and second-order fire effects 1729
III. Cambium necrosis 1732
IV. Hydraulic dysfunction 1733
V. Biotic attacks 1736
VI. Conclusion 1737
Acknowledgements 1737
References 1737
New Phytologist (2019) 223: 1728–1741
doi: 10.1111/nph.15871
Key words: biotic attacks, cambium necrosis,
forest fires, hydraulic dysfunction, postfire
effects, tree physiology.
Summary
Heat injuries sustained in a fire can initiate a cascade of complex mechanisms that affect the
physiology of trees after fires. Uncovering the exact physiological mechanisms and relating
specific injuries to whole-plant and ecosystem functioning is the focus of intense current
research. Recent studies have made critical steps forward in our understanding of tree
physiological processes after fires, and have suggested mechanisms by which fire injuries may
interact with disturbances such as drought, insects and pathogens. We outline a conceptual
framework that unifies the involved processes, their interconnections, and possible feedbacks,
and contextualizes these responses with existing hypotheses for disturbance effects on plants
and ecosystems. By focusing on carbon and water as currencies of plant functioning, we
demonstrate fire-induced cambium/phloem necrosis and xylem damage to be main disturbance
effects. The resulting carbon starvation and hydraulic dysfunction are linked with drought and
insect impacts. Evaluating the precise process relationships will be crucial for fully understanding
how fires can affect tree functionality, and will help improve fire risk assessment and mortality
model predictions. Especially considering future climate-driven increases in fire frequency and
intensity, knowledge of the physiological tree responses is important to better estimate postfire
ecosystem dynamics and interactions with climate disturbances.
I. Introduction
Wildfires are one of the most important natural disturbances
acting on plant ecosystems world-wide. The degree to which
vegetation is impacted by fire depends on the heat fluxes incident
on various plant parts, which is an outcome of various fire
behavior variables such as fireline intensity and residence time
(Michaletz & Johnson, 2007; O’Brien et al., 2018). The water
content, arrangement and loading of fuels strongly influence fire
behavior and effects (Bond & Keeley, 2005; Keeley, 2009). High-
intensity crown fires consume live and dead canopy fuels, and the
combustion of all foliage and meristems in a tree crown can cause
immediate mortality, unless the tree is able to resprout from heat-
resistant organs (Clarke et al., 2013; Pausas & Keeley, 2017). By
contrast, low- to moderate-intensity fires often do not constitute a
direct lethal threat to mature trees, but rather, may cause a variety
of injuries that can subsequently interact to impact whole-tree
functioning.
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Review
Fire effects on trees can be classified as two types: first- and
second-order effects. First-order effects comprise the immediate
impacts of heat transfer on plant tissues (for a review, see Michaletz
& Johnson, 2007). Nonlethal first-order heat injuries can trigger
second-order effects, such as physiological limitations in carbon
(C) and water relations or increased susceptibility to insect attacks
and pathogenic infections (Michaletz & Johnson, 2008). Altered
physiology and a weakened defense against biotic agents can lead to
long-term restrictions of whole-plant function and may ultimately
cause latent postfire tree mortality (Figs 1, 2).
This review briefly summarizes first- and second-order effects in
roots, stems and crowns (section II), before outlining a framework
to advance a better understanding of physiological responses to fire
in context of tree mortality hypotheses (sections III –V). The main
emphasis is necessarily on stems as these have been studied the mos t.
Focusing on cambium necrosis, hydraulic dysfunction and biotic
attacks, we outline the physiological processes involved, their
consequences, their mechanistic connections and possible feedback
loops. The detailed process steps are described individually, and
illustrated in a conceptual framework (Fig. 3).
II. First- and second-order fire effects
1. First-order fire effects
First order fire effects result from heat transfer from combusting
fuels into tissues within the roots, stem or crown (Fig. 2; Michaletz
& Johnson, 2007; Bergman & Incropera, 2011). While convection
and radiation processes transfer heat to tissue and soil surfaces, heat
is further transferred within solid materials (soil particles and/or
plant parts) via conduction. Heat-induced injuries in roots occur as
a result of heat transfer through soil and successive heat conduction
into the root interior (Michaletz & Johnson, 2007). They can
manifest directly in root death, especially in fine roots, or cause
cambium and phloem necrosis. Tissue mortality, which is caused
by protein denaturation (Rosenberg et al., 1971), is generally
considered to be completed at 60°C. However, cell necrosis rates
increase exponentially with temperature and lower temperatures
also can result in cell death if exposed for longer periods (Hare,
1961; Dickinson & Johnson, 2004). Cambium and phloem
necrosis in roots of upper soil layers and close to the root crown are
most likely to occur during ground fires, where smoldering
combustion of organic soil (duff) over hours or days can lead to
substantial heating of soils and roots (Ryan & Frandsen, 1991;
Swezy & Agee, 1991; Smirnova et al., 2008).
Rates of heat transfer from the fire into tree tissues are mediated
by plant functional traits (Keeley et al., 2011). In tree stems heat
first has to be conducted through the bark to affect other tissues.
The thermal insulation ability of bark, which is determined mainly
by bark thickness, density and moisture content (van Mantgem &
Schwartz, 2003; Lawes et al., 2011; Brando et al., 2012; Pausas,
2015), is therefore crucial for controlling heat fluxes through bark
and potential injuries of underlying tissues. Without sufficient bark
insulation, phloem and vascular cambium can exceed critical
temperatures for necrosis. If the insulation capability is too low,
lethal temperatures can be attained not only in phloem and vascular
cambium tissues, but also in the underlying xylem (Chatziefstratiou
et al., 2013). We are unaware of any empirical data for sapwood
temperatures during forest fires, but simulations based on
measured cambium data suggest that xylem often can achieve
critical necrosis temperatures (Michaletz et al., 2012).
Heat transfer into the crown can cause immediate bud and/or
foliage necrosis, as well as cambium and phloem damage in
branches. The degree of injuries on crown components is related to
their functional traits (thermophysical properties), fireline intensi ty
and residence time, as well as to crown base height (Van Wagner,
1973; Michaletz & Johnson, 2006, 2007). Crown component
traits such as width, surface area, shape, orientation and degree of
shielding by foliage control heat fluxes, whereas other traits such as
mass, water content, and specific heat capacity determine how
much energy is required to cause a temperature increase. For
example, species with relatively large buds such as ponderosa pine
(a) (b)
Fig. 1 Example of delayed postfire mortality in
a Norway spruce (Picea abies) specimen. The
tree survived a forest fire in March 2014
(Absam, Austria) with a scorched stem and leaf
and bud necroses in the lower crown portion,
but eventually died in the following year.
Although mortality occurred from interactions
of potential injuries to cambial, vascular, and
resource acquisition tissues, it is not known
whether carbon starvation or hydraulic
dysfunction was the ultimate cause. Pictures of
the same tree were taken shortly before (a,
June 2015) and after (b, September 2015) its
death.
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and longleaf pine are far less susceptible to bud necrosis than are
species with relatively small buds such as sugar maple and American
beech (Michaletz & Johnson, 2006). For larger crown components
like branches, fruits and cones, internal temperature gradients exist
and conduction within the component becomes important. In
these cases, diameter plays an important role in insulating tissues
against heat necrosis, because conduction rates decrease with radial
depth. Thus, as for stems, bark can help insulate vascular tissues and
cambium. Likewise, many cones and fruits can insulate seed
embryo tissues against heat necrosis. This has been widely
recognized in serotinous species that store seeds in aerial seed
banks, but it also can be important for nonserotinous species
provided that the fire occurs during a temporal window when seeds
are germinable but not yet abscised (Michaletz et al., 2013;
Pounden et al., 2014).
2. Second-order fire effects
Second-order fire effects are more complex and their mechanisms
are not as well-understood as those of first-order effects. The
response of plant function to fire injuries can vary widely. Fire-
surviving trees, on the one hand, can be compromised in their
physiological functionality, show reduced growth and be more
likely to succumb to delayed death (Fig. 1; e.g. Lambert &
Stohlgren, 1988; van Mantgem et al., 2003, 2011; Granzow-de la
Cerda et al., 2012; Nesmith et al., 2015; Maringer et al., 2016;
Thompson et al., 2017). On the other hand, it is known that
injured trees may also benefit in the short- and mid-term from
reduced competition (Pearson et al., 1972; Keyser et al., 2010;
Battipaglia et al., 2014b; Valor et al., 2015, 2018).
Crown injuries are relatively easy to assess and correlations
between fire-induced foliage loss and tree growth or mortality have
been established by many previous studies (Michaletz & Johnson,
2008; Woolley et al., 2012). In theory, necrotic foliage after a fire
reduces the leaf area of affected trees, which leads to improve d water
availability for the remaining foliage. Consequently, available water
can be used by undamaged leaves to increase stomatal conductance
and photosynthesis rates (Reich et al., 1990; Ryan, 2000; Wallin
et al., 2003). In combination with decreased competition from
herb and shrub layers for soil resources, trees with crown injuries
can show unaffected or even enhanced postfire production and
growth (Pearson et al., 1972; Keyser et al., 2010; Battipaglia et al.,
2014b; Valor et al., 2015, 2018). However, these beneficial effects
can be limited when levels of leaf necrosis are high. With extensive
Heat transfer Recovery
First-order effects
• Foliage and
bud necrosis
• Cambium and
phloem necrosis
• Xylem hydraulic
impairments
• Fine root necrosis
Carbon and
water relations
Functional and
growth limitations
Tree mortality
Second-order effects
• Photosynthesis and
C-supply limitations
• Water uptake and
transport restrictions
• Biotic attacks
Fig. 2 Overview of fire effects in trees. Heat
transfer into crown, stem and root tissues is
mediated by functional traits and can
immediately lead to first-order injuries, which
potentially can induce second-order effects.
Both first- and second-order effects can lead to
physiological impairments in tree carbon (C)
and water relations, consequently limiting
functioning and growth. Depending on
postfire environmental conditions and species-
specific traits (e.g. abilities to balance C and/or
water restrictions), affected trees may either
recover from postfire limitations or succumb to
fire legacy effects. All first-order fire effects
(red box) can also be found in Fig. 3, where
links with second-order effects and
physiological feedbacks are detailed. Carbon
starvation and reduction of the hydraulic
efficiency represent the key mechanisms in C
and water relations and are indicated with a
key symbol here and in Fig. 3.
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leaf necrosis (b11 in Fig. 3), remaining foliage might not be able to
sustain whole-tree carbohydrate requirements, which consequently
can lead to decreased growth (Pearson et al., 1972; Ryan, 1993;
Valor et al., 2018), altered root C dynamics (Sword & Haywood,
1999; Aubrey et al., 2012), or reduced C-based defense and
resistance to insect colonization (McHugh et al., 2003; Wallin
et al., 2003). Even if the remaining crown can fully support the
metabolic C demand, less obvious injuries to stem cambial and
vascular tissues can compromise the tree’s functionality, affecting
stomatal behavior and tree growth (Battipaglia et al., 2014a;
a1
Cambium and
phloem necrosis
a2
Blockage
of carbon
translocation
a5
Reduction of
root growth
a3
Root C
depletion
c2
Phloeophagous
attack
c3
Xylophagous
attack
c1
Biotic agents
b3
Reduction
of hydraulic
efficiency
b9
Reduction
of hydraulic
safety
b10
Reduction
of safety
margin
b5
Structural effects
on xylem hydraulics
b2
Xylem
embolism
b1
Nonstructural
effects on xylem
hydraulics
b6
Decrease in
water potential
b4
Fatal
runaway
embolism
Cambium
Xylem
Phloem
Bark
a4
C starvation
a6
Root
death
a7
Fine root
necrosis
Fig. 3 Conceptual diagram illustrating the
cascade of potential physiological responses to
postfire injuries in plant roots, stems, and
crowns. Gray boxes indicate first-order fire
effects induced via heat transfer and white
boxes indicate second-order mechanisms.
Red-framed boxes (a) describe processes
affected by injuries to cambium and phloem
tissues. Blue-frames boxes (b) indicate
processes related to fire effects on xylem
hydraulics. Green-framed boxes (c) indicate
postfire biotic agents that may have an
amplifying effect on processes influenced by
both cambium/phloem necrosis and hydraulic
dysfunction. The progressive numbers inside
the boxes refer to the physiological processes,
which are illustrated in the diagram and
discussed in the text. Carbon (C) starvation
and reduction of the hydraulic efficiency (key
symbol) constitute crucial physiological
junctures within the carbon and the water
cycle, respectively. The severity and duration
of these two key processes depend upon
postfire environmental conditions, and can
manifest as growth limitations and ultimately
determine whether a tree will live or die (see
also Fig. 2).
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Thompson et al., 2017). Although it has been shown that fires can
considerably reduce fine root biomass (a7 in Fig. 3; Swezy & Agee,
1991; Smirnova et al., 2008), the knowledge on how root injuries
can compromise postfire tree viability and productivity is scarce. As
fine root degradation reduces water uptake, root injuries can
potentially mediate tree decline and mortality via hydraulic
limitation. Denaturation of aquaporins, which play a crucial role
in the water uptake process (Groszmann et al., 2017), may disable
radial water transport in roots, even when heat damage of root cells
was not lethal.
There are two main hypotheses for how fire injuries can impact
second-order functionality and mortality (Michaletz, 2018). The
cambium necrosis hypothesis assumes that fire-induced cambium
and phloem necrosis limits carbohydrate translocation and initiates
C starvation (see section III Cambium necrosis), whereas the
hydraulic dysfunction hypothesis assumes that the heat of forest
fires can impair the xylem of trees and cause hydraulic failure (see
section IV Hydraulic dysfunction). Both hypothesized mecha-
nisms are considered to be able to trigger physiological cascades,
which impact whole-plant function and/or eventually cause tree
mortality, independently or in combination.
In general, even without the effects of fire, the complex
physiological processes that often interact with biotic disturbance
agents and lead to vigor loss or tree mortality have not yet been fully
disentangled (McDowell et al., 2008, 2011, 2018; Sala et al., 2010;
Sevanto et al., 2014; Anderegg et al., 2015; Hartmann, 2015;
Mencuccini et al., 2015; Gessler et al., 2017). For example,
McDowell et al. (2008) postulated generalized hypotheses of
physiological mortality mechanisms under drought: C starvation
and hydraulic failure. Carbon starvation is hypothesized to occur
when prolonged stomatal closure during drought limits photosyn-
thetic C assimilation and the metabolic demand for carbohydrates
needs to be covered by the plant’s C reserves. With persistent
drought, C reserves will become exhausted or unable to be
metabolized or translocated (Sala et al., 2010; McDowell, 2011)
and cellular metabolism can no longer be maintained. Hydraulic
failure is expected to occur when drought intensity induces water
column tensions, which exceed the plant’s hydraulic safety margin
and cause substantial embolism formation. Resulting lethal
conductivity losses can then lead to irreversible desiccation before
C starvation occurs. In addition, biotic mortality agents (see section
V Biotic attacks) can act as amplifiers for both mechanisms, and vice
versa, C starvation and hydraulic failure can facilitate insect attacks
or pathogenic infections by weakening the plant defense system
(McDowell et al., 2011; Anderegg et al., 2015).
III. Cambium necrosis
During forest fires, the bark insulation capability may not be
sufficient to prevent critical increases of cambium temperatures.
The extent of cambium necrosis around the circumference of a stem
depends on the interaction of the fire with the air-flow patterns
around the tree stem. Interactions of leeward vortices with moving
firelines increase flame temperatures and residence times in the lee
of a tree as compared with the windward side (Gill, 1974; Tunstall
et al., 1976; Gutsell & Johnson, 1996). Therefore, partial cambial
necrosis and fire scars will be found preferentially on the tree’s
leeward side. If flame temperatures, residence times and mixing/
convection rates are sufficiently high, or the bark is sufficiently thin
(e.g. in small plants), cambium necrosis often occurs around the
entire bole. Necrotic vascular cambium initiates compartmental-
ization and wound closure as part of the scar formation process to
avoid insect and pathogen infestation, and to restore functionality
(Shigo, 1984; Smith & Sutherland, 2001). Depending on tree
species and fire scar size, it can take years or decades until wound
closure is completed and even longer until the circuit continuity of
the cambium and full physiological functionality is regained
(Smith & Sutherland, 1999; Smith et al., 2016; Stambaugh et al.,
2017).
During the heat transfer process (for further details, see
Michaletz & Johnson, 2007) from the bark surface to the vascular
cambium, heat is conducted through the intermediate phloem
tissue. Heat fluxes and maximum temperatures of phloem will be
generally equal to (if not slightly greater than) those of the vascular
cambium. Therefore, it can be assumed that cambium necrosis is
preceded by phloem necrosis (a1 in Fig. 3; Michaletz & Johnson,
2007). As phloem regeneration relies on cambial cell activity,
cambium necrosis causes a permanent interruption of the phloem
pathway and blockage of the downward translocation of photo-
synthates (a2 in Fig. 3). This is equivalent to a heat-induced girdle if
the entire bole circumference is affected (Noel, 1970). It is well
known from nonheat-related experiments that girdling triggers the
depletion of nonstructural carbohydrates (NSCs; soluble sugars
and starch) below the girdling zone (Daudet et al., 2005; De
Schepper et al., 2010; Oberhuber et al., 2017). Depletion of NSCs
also was observed after stem heating during controlled fires (Varner
et al., 2009). Depending on the root’s C pool size, it may take
several years to decades until the root’s carbohydrate demand can
no longer be sustained and C reserves have been completely
depleted (a3 in Fig. 3; Noel, 1970). Once C reserves are fully
exhausted, roots are considered to suffer from C starvation (a4 in
Fig. 3), which then will lead to a cessation of fine root production
(a5 in Fig. 3; Marshall & Waring, 1985).
Massive reductions in fine root biomass following a forest fire
were detected by Smirnova et al. (2008), who attributed the loss
mainly to the effect of heat girdling at the stem base (see also Swezy
& Agee, 1991). As most water uptake occurs via the fine root surface
area, a decrease in fine root biomass theoretically leads to curtailed
water supply to the stem and crown (b3 in Fig. 3). In consequence,
lowered leaf water and xylem potentials (b6 in Fig. 3) can trigger
premature stomatal closure (b7 in Fig. 3) and/or potentially fatal
embolism (b2 in Fig. 3), respectively (Tyree & Zimmermann,
2002). Increased periods of stomatal closure limit C assimilation
(b8 in Fig. 3), which can reduce plant growth or lead to whole-plant
mortality via C starvation. Potential embolism –ultimately
induced by cambium and phloem necrosis –during the phase of
C starvation may cause mortality (McDowell, 2011; Sevanto et al.,
2014), before entering an irreversible state of desiccation caused by
definitive root death (a6 in Fig. 3).
The idea that heat can alter tree physiology by damaging
cambium and phloem, and thereby disrupting carbohydrate
transport to the root, was proposed in the early 1960s (Hare,
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1961, 1965; Wagener, 1961; Fahnestock & Hare, 1964) and soon
was quoted as the standard explanation for postfire tree mortality.
However, direct links between heat-injured cambial tissue and
delayed tree mortality were first examined by Ryan et al. (1988).
They assessed several potential predictors of mortality (e.g.
diameter at breast height (DBH), average scorch height and the
scorched crown volume), and found the circumferential extent of
cambial necrosis to be the best predictor of mortality for injured
Douglas-fir 8 yr following a fire. Mortality occurred in all of the
trees that had cambium necrosis around their entire circumference,
which is consistent with the cambium necrosis hypothesis of
postfire mortality (Noel, 1970; Michaletz et al., 2012; Michaletz,
2018). Cambium and phloem necrosis also can occur in roots as a
result of conduction heat transfer through soil (Michaletz &
Johnson, 2007). Necrosis close to the root crown is most likely to
occur during ground fires, where smoldering combustion of duff
over hours or days can lead to substantial heating of soils and roots
(Ryan & Frandsen, 1991; Swezy & Agee, 1991), causing a fatal
disruption of carbohydrate downward translocation.
In later studies, heat girdling experiments were performed to
study the physiological effects of heat-induced cambium injuries in
isolation of crown injuries (Ducrey et al., 1996) or xylem injuries
(Ryan, 2000). When excluding heat-caused disruptions of the
xylem, mortality occurred only in trees that were completely or
almost completely girdled around the bole circumference (Ryan,
2000), indicating that processes other than cambium and phloem
necrosis were responsible for postfire mortality in partially girdled
trees. In girdling experiments, where heat was potentially able to
penetrate the xylem (Ducrey et al., 1996), trees showed clear signs
of water stress. An immediate decrease of sap flux density, lowered
stomatal conductance and increased daily trunk diameter variations
led the authors to speculate about possible heat-related hydraulic
limitations in the xylem.
IV. Hydraulic dysfunction
More recently, a growing number of studies increasingly have been
documenting fire impacts on xylem hydraulic function. Strong
support for a hydraulic mechanism affecting postfire tree physiol-
ogy was found by Balfour & Midgley (2006). By combining
manual girdling (bark, phloem and cambium were removed
without wounding the xylem) with heat girdling experiments, they
were able to analyze the effects of heat on the xylem. All heat-treated
trees started to shed leaves immediately and experienced stem death
within 4 wk, whereas manually girdled trees did not show any sign
of rapid leaf loss. Leaf-shedding and subsequent stem death of
burnt plants were attributed to heat-induced reduction of sapwood
area, which was detected using staining techniques. Also consistent
with these effects of a wildfire, was a study demonstrating that
branch death in fire-injured Protea repens specimens occurred much
quicker than in manually girdled ones, and was linked to hydraulic
dysfunction and subsequent dehydration (Midgley et al., 2011).
Further indications for hydraulic dysfunction after wildfires were
provided by the visualization of nonfunctional sapwood via dye
techniques (B€ar et al., 2018), electrical resistivity tomography
(Fig. 4) and wood-anatomical observations (Shigo & Marx, 1977;
Smith & Sutherland, 1999, 2001; Schoonenberg et al., 2003; De
Micco et al., 2013; Smith et al., 2016). Fire-induced wounding can
initiate the formation of discolored areas within the sapwood
(Smith et al., 2016). Surrounded by barrier zones, these areas are
thought to be hydraulically isolated from healthy sapwood, which
would lead to a reduction of the functional sapwood area. Due to
the exclusion of these discolored areas from the hydraulic pathway,
they remain unstained when branch or stem segments are flushed
with dye solutions, and they also can cause resistivity shifts in
electrical resistivity tomograms (Fig. 4). Finally, forest fires have
been shown to trigger physiological responses associated with a
compromised hydraulic system. In theory, stomatal conductance
should increase in trees with crown scorch due to improved water
supply to the remaining leaf area. However, partially defoliated
trees surprisingly showed reduced stomatal conductance, no
change in water-use efficiency, and lowered predawn water
potential, which strongly points towards fire-induced impairment
of the water transport system (Thompson et al., 2017). Thus,
substantial evidence suggests a critical role for hydraulic dysfunc-
tion in postfire tree physiology. In the following, we summarize the
100 200 400 800 1500 3000
Electrical resistivity ( m)
Control Fire-exposed
Fig. 4 Electrical resistivity tomograms of control and fire-exposed Picea
abies stems. Electrical resistivity tomography can be used to estimate the
impaired sapwood area within living plants after forest fires. With this
nondestructive method, the electrical resistivities of cross-sections can be
measured and functional sapwood can be differentiated from heartwood
(Guyot et al., 2013) and impaired sapwood (Bieker et al., 2010). Water-
conducting sapwood appears as a distinct ring (blue, low electrical
resistivity), surrounding the central area of heartwood (red, high electrical
resistivity) in intact control trees. The resistivity shifts in tomography patterns
of stems, which were exposed to a natural forest fire, indicate profound
losses of functional sapwood areas. Note that the upper limit of the displayed
resistivity range was set to 3000 Om. Resistivity values within fire-impaired
areas can by far exceed this limit.
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possible underlying mechanisms, which can be categorized as
nonstructural (b1 in Fig. 3) and structural effects (b5 in Fig. 3).
1. Nonstructural effects on xylem hydraulics
Perhaps the most important nonstructural impact of heat is reduced
hydraulic efficiency (hydraulic conductivity of the xylem) due to an
enhanced risk of embolism formation (Michaletz et al., 2012;
Lodge et al., 2018). Leaf transpiration causes water to evaporate
from mesophyll cell walls into the surrounding atmosphere
(Venturas et al., 2017). As described by the cohesion-tension
theory (Dixon & Joly, 1895), tensile forces at the evaporative
surface in cell walls pull water molecules through the hydraulic
network of the xylem from the soil to leaves. This water transport
requires a continuous column of metastable water, which can be
disrupted by cavitation on high tensions (i.e. low water potential) in
the xylem sap (Oertli, 1971; Pickard, 1981). Xylem cavitation
occurs through the entry of air (air seeding) from adjacent air-filled
compartments and ultimately leads to embolization of conduits (b2
in Fig. 3; Cochard et al., 1992; Tyree et al., 1994a; Tyree &
Zimmermann, 2002). It is initiated when the pressure difference
across an air–water interface in pit membranes exceeds the
cavitation pressure required to displace the meniscus from the
pore (Oertli, 1971; Pickard, 1981; Tyree & Zimmermann, 2002).
In the case of conifers the valve like torus-margo architecture can
fail and allow air entry, whereby surface tension forces also may play
a role (Tyree & Zimmermann, 2002; Hacke & Jansen, 2009;
Delzon et al., 2010; Losso et al., 2017). Embolized conduits are not
able to transport water and, as a consequence, cause a reduction of
the conductive xylem area and the hydraulic efficiency of the
sapwood (b3 in Fig. 3).
Increased temperatures during forest fires enhance cavitation
events as the surface tension decreases with heating (Vargaftik et al.,
1983). Lowered sap surface tensions have been shown to crucially
impact the vulnerability to cavitation (Cochard et al., 2009;
Michaletz et al., 2012; West et al., 2016; Losso et al., 2017; Lodge
et al., 2018). If the hydraulic integrity of embolized conduits
cannot be restored by refilling (Zwieniecki & Holbrook, 2009;
Nardini et al., 2011; Brodersen & McElrone, 2013; Mayr et al.,
2014), hydraulic limitations may persist and increase the risk of
postfire mortality, for example, by induction of run-away
embolism (b4 in Fig. 3) under drought conditions. However,
additional work is required to understand the interplay of
instantaneous effects on water potential and embolism formation
during fire as well as long-term effects on xylem function.
It also has been hypothesized that wildfires cause abrupt shifts of
atmospheric conditions as the hot and dry air of a heat plume
suddenly creates a high leaf-to-air vapor pressure deficit (VPD;
Kavanagh et al., 2010). Plants respond to VPD elevations with
stomatal closure to prevent water loss and high tensions within the
xylem (Merilo et al., 2017). However, Kavanagh et al. (2010)
assumed that the stomatal response is not fast enough to prevent
extensive water loss, decreases of water potential (b6 in Fig. 3) and
xylem embolism. By modeling the xylem water potential for trees
exposed to high VPD during fires, they predicted that the
atmospheric conditions during a fire can cause embolism
formation. Experimental confirmation of heat plume-induced
xylem embolism (b2 in Fig. 3) was later provided by West et al.
(2016), although the VPDs achieved experimentally are likely to be
substantially higher than those experienced in wildfires, where fuel
drying and combustion lead to relatively humid fire plumes
(O’Brien et al., 2018). Heat-plume simulations at 100°C caused
hydraulic conductivity losses of up to 80% in Eucalyptus cladocalyx
and K. africana shoots (West et al., 2016). High VDP deficits may
account for rapid tree mortality after fires as such high conductivity
losses are suggested to be lethal (Adams et al., 2017). However,
more tests are required to understand the relevance of this effect.
2. Structural effects on xylem hydraulics
By contrast to nonstructural impacts, heating by fire also can cause
structural effects (b5 Fig. 3, Fig. 5) related to direct, physical
alterations of the xylem conduits. Xylem conduit walls are
composed of viscoelastic polymers (lignin, cellulose and hemicel-
luloses) that start to soften and behave like viscous liquids above
temperature thresholds (‘glass transition point’). Although th e glass
transition of lignin occurs between 60 and 90°C, it is thought that
the glass transition of hemicellulose can occur at c. 50°C (Irvine,
1984; Hillis & Rozsa, 1985; Olsson & Salmen, 1997, 2004).
However, additional research is needed to better quantify glass
transitions of cell wall polymers and to understand possible
interactions with tensile sap water. When lignin and hemicellulose
temperatures exceed their glass transition points, the overall xylem
rigidity decreases and alterations of the conduit cell walls can occur
in response to stresses imposed by tensile sap water (Hacke et al.,
2001). On cooling, cell wall polymers return to their glassy state
and heat-induced structural changes can become manifest in two
important hydraulic aspects.
First, the hydraulic efficiency may be permanently reduced by
heat-induced structural alterations (b3 in Figs 3, 5; Michaletz et al.,
2012; West et al., 2016; B€ar et al., 2018). During thermal
softening, destabilized conduit cell walls are prone to deformation
and rupture. The simultaneous occurrence of low water potentials
in the xylem generates additional stress on cell walls (Hacke et al.,
2001; Cochard et al., 2004; Bouche et al., 2016) and may increase
the likelihood of destabilization. Deformations can affect overall
wall geometry as well as pit pore geometry, whereas ruptured parts
of the cell wall can potentially occlude pit membrane pores. In
theory, both aspects can lead to reductions in hydraulic conduc-
tivity (Tyree & Zimmermann, 2002; Sperry et al., 2006; Choat
et al., 2007).
Michaletz et al. (2012) were the first to discover heat-related
reductions of xylem conductivity in laboratory experiments on
Populus balsamifera. Heating xylem to 65°C caused permanent and
significant conductivity losses. Experimentally induced, long-
lasting conductivity limitations were further demonstrated for
K. africana (West et al., 2016) and Fagus sylvatica (B€ar et al., 2018).
The first evidence that hydraulic conductivity also can be reduced
by natural forest fires was provided by B€ar et al. (2018), who found
the xylem of F. sylvatica to be 39% less conductive in fire-damaged
branches than in undamaged control branches, a result not related
to embolism. In that study, two coniferous species (Picea abies and
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Pinus sylvestris) also were tested for their susceptibility to heat-
induced conductivity losses. No heat-related effects were found in
either species, and it was hypothesized that the high wall
reinforcement (conduit thickness-to-span ratio; Hacke et al.,
2001; Sperry et al., 2006) of conifer tracheids might provide
mechanical protection against heat-induced destabilization.
Although heat-induced reductions of xylem conductivity were
demonstrated in heat experiments and after a wildfire, available
data are still limited, and species-specific responses and thermal
thresholds for structural alterations still have to be evaluated. Also,
no attention has yet been paid to the potential role of living cells of
the xylem, where, for example, heat-induced impairments of
aquaporins may impair radial conductance or capacitance (Sevanto
et al., 2011).
Reductions in hydraulic efficiency can have important impacts
on postfire plant physiology. For example, they can cause steep
water potential gradients within the xylem (Sperry et al., 1993), low
leaf water potentials and eventually turgor loss (b6 in Fig. 3). As
stomatal regulation is closely connected to leaf water status
(Brodribb et al., 2003; Tombesi et al., 2015), low leaf water
potentials can trigger stomatal closure (b7 in Fig. 3), for instance at
midday or already under nonsevere drought. Therefore, heat-
induced reductions in hydraulic conductivity can, on the one hand,
result in long-term decreases in stomatal conductance and
respective reductions in assimilation and productivity (b8 in Fig. 3;
Tyree et al., 1994b; Thompson et al., 2017). If the residual
photosynthetic activity is not able to support the plant’s metabolic
C demand, a heat-induced loss of hydraulic conductivity can
initiate the cascading effect of C starvation (a3, a4 in Fig. 3). On the
other hand, with increased xylem tensions, cavitation and
embolism (b2 in Fig. 3) become more likely (Sperry et al., 1993).
The formation of embolism can further increase hydraulic
resistances and, unless stomata close, even lead to ‘run-away’
embolism (b4 in Fig. 3; Tyree & Sperry, 1988), which ends in fatal
hydraulic failure, and consequently, to irreversible whole-plant
desiccation. In addition, the effect of deformed conduits on
hydraulic conductivity might be enhanced by the occurrence of
traumatic resinosis as response to fire-induced wounding (Lom-
bardero et al., 2006; Arbellay et al., 2014; Smith et al., 2016). Resin
gets mobilized to seal the fire wound and to build a chemical and
physical barrier against postfire insect attack and pathogen
infection (Franceschi et al., 2005). This also can affect the water
Pit membrane
microfibril
reorientation
Gymnosperms Angiosperms
Intact
Heat-damaged
(a) (b)
(c) (d)
Air
Functional
torus sealing
Meniscus-stabilizing
sap surface tension
Reduced sap
surface tension
Torus/porus
modifications
Cell wall
deformations
and ruptures
Water
Pw
Water
Pw
Pa
Air
Pa
ΔPΔP
Fig. 5 Mechanisms of xylem dysfunction by heat for gymnosperm and angiosperm conduits. For comparison, intact (a, b) and heat-damaged (c, d) conduits are
illustrated, respectively. Aspiration of gaseous bubbles via the pits from adjacent, already embolized conduits (air seeding) is initiated when the pressure
difference (DP=P
w
P
a;
where P
w
is the negative pressure in the water-filled and P
a
is the atmospheric pressure in the air-filled conduit) between the
compartments exceeds the cavitation pressure required to cause a rupture of an air-water meniscus in the pit membrane pore or a failure of the torus sealing
mechanism. During a fire, air seed cavitation and subsequent embolism become more likely as xylem heating reduces the surface tension of sap water, affecting
the critical cavitation pressure threshold. Thermal softening of cell wall polymers can result in modifications of the pit porus and/ortorus, and in reorientation of
pit membrane microfibrils, both of which affect the hydraulic safety of conduits by increasing the likelihood of air seeding. Limitations in hydraulic conductivity
can be caused by heat-induced cell wall deformations affecting overall wall geometry, by ruptured cell wall particles occluding pit membrane pores, or by
changes of the pit pore geometry. Low P
w
in water-filled conduits and high pressure differences between water-filled and air-filled conduits potentially create
additional stresses on cell walls (hoop and bending stresses; Hacke et al., 2001), that favor deformations and ruptures during the thermal softening phase.
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Phytologist Tansley review Review 1735
flow through the sapwood as conduit pits can occlude with resin
release. However, the extent to which resin-caused blockages can
reduce xylem conductivity is currently unknown.
Second, the hydraulic safety of the xylem may be impacted by
heat-induced structural alterations (b9 in Figs 3, 5). There are
species-specific thresholds in water potential, at which air can enter
water-filled conduits (see section ‘IV 1. Nonstructural effects on
xylem hydraulics’) and block water transport. Vulnerability to
drought-induced embolism is thus closely linked to pit architecture
and especially to the distribution of pit membrane pore sizes and pit
membrane thickness (Wheeler et al., 2005; Hacke et al., 2006; Li
et al., 2016). Any physical irregularities in pit structures are thought
to reduce the embolism-resistance (Plavcovaet al., 2013). It is
assumed that softened lignin and hemicellulose polymers allow
movements of the (more heat-resistant) cellulose microfibrils in
conduit walls (Hillis & Rozsa, 1985). Microfibril movement can
widen pit membrane pore diameters, which increases the likelihood
of air aspiration from adjacent air-filled conduits in angiosperms (air
seeding; Oertli, 1971; Tyree et al., 1994a), and it can destabilize the
connection between fibrils, hemicellulose and lignin within conduit
walls, which favors pit membrane ruptures and torus sealing failures
in gymnosperms (Sperry & Tyree, 1990; Cochard et al., 2009;
Delzon et al., 2010). In theory, the liquefaction of wall components
may further lead to alterations of the porus opening, deformations
of the pit torus, as well as to detachments of the torus from the margo
membrane (Fengel, 1966; Kollmann & Sachs, 1967). These
changes may weaken the reliability of pit-sealing mechanisms
during drought stress, which increases the risk of postfire hydraulic
failure. Heat transfer into the xylem also may affect living
parenchyma cells that are connected to angiosperm vessels. They
are thought to regulate the sap composition by releasing surfactants
into the vessel (Morris et al., 2018). According to Schenk et al.
(2015, 2017), surfactants coat and stabilize nanobubbles and,
therefore, reduce their likelihood to expand under negative pressure
and form embolism. If vessel-associated parenchyma cells are killed
by heat, this regulating mechanisms could potentially break down,
increasing the vulnerability to xylem embolism.
The ability of heat to shift vulnerability thresholds was tested in
controlled heating experiments (P. balsamifera: Michaletz et al.,
2012; P. abies, P. sylvestris, F. sylvatica:B€ar et al., 2018) and after
prescribed (Pinus pinea: Battipaglia et al., 2016) and natural
wildfires (B€ar et al., 2018). Heat experiments and wildfires caused
pronounced effects on the hydraulic safety of P. sylvestris and
F. sylvatica, whereas small or negligible effects were observed in the
other species. However, it has to be mentioned that the stem surface
temperatures and residence times reported for P. pinea were
insufficient to cause neither cambium necrosis (Battipaglia et al.,
2016), nor cavitation or deformation, which require even higher
heat fluxes (Michaletz et al., 2012); thus, results of Battipaglia et al.
(2016) cannot be interpreted as evidence against the xylem
dysfunction hypothesis. Further research is needed to understand
how heat can structurally alter the hydraulic safety in different
species and to clearly demonstrate the underlying biophysical
processes. Fire-caused reductions of the hydraulic safety imply that
injured trees have to cope with reduced hydraulic ‘safety margins’ in
the field (b10 in Fig. 3), being less tolerant to water stress during
future drought events and more prone to cavitation (b2 in Fig. 3).
This particularly affects species that already operate near their point
of catastrophic hydraulic failure (Tyree & Sperry, 1988; Choat
et al., 2012).
Structural alterations of xylem conduits will affect the hydraulic
integrity of trees until respective sapwood areas are completely
replaced. Sapwood lifespans vary strongly with species and range
from few years up to >100 yr (Zweifel & Sterck, 2018). Species
with few active tree rings, such as oaks, are able to replace large
proportions of impaired xylem within the first year postfire (e.g.
trees with sapwood lifespan of 5 yr renew c. 20% conductive xylem
area each year). Different replacement times of impaired xylem may
thus help to explain species-specific susceptibility to postfire tree
decline and mortality.
V. Biotic attacks
Postfire mortality of surviving trees often is associated with insect
attacks and microbial infections (c1 in Fig. 3; e.g. McHugh et al.,
2003; Lombardero et al., 2006; Parker et al., 2006; Hood & Bentz,
2007; Breece et al., 2008; Conedera et al., 2010; Maringer et al.,
2016; Catry et al., 2017; Westlind & Kelsey, 2019). Trees respond
to fire injuries with compartmentalization and wound closure
processes to avoid infestation and wood decay. It can take several
years until wound closure processes are completed, and barrier
zones can adequately protect against insect, pathogen and air entry
(Smith & Sutherland, 2001; Smith et al., 2016). During this time,
wounded trees are particularly vulnerable as their defense system
can be additionally weakened by fire-induced changes in carbohy-
drate dynamics (McDowell, 2011; Wiley et al., 2016). Although
postfire insect attacks are often short-lived and recede within a few
years after fire (Hood & Bentz, 2007; Davis et al., 2012), the
defense system of trees can benefit in return from fires over the
longer term. For example, low-severity fires stimulate resin duct-
related defenses in ponderosa pine, increasing their resistance to
insect attacks. It has been shown that these defenses decline without
fire disturbances (Hood et al., 2015).
Fire-injured trees release high amounts of ethanol and volatile
terpenes, which attract bark beetles and other wood-boring insects
(Wood, 1982; Kelsey & Westlind, 2017a,b; Valor et al., 2017).
Bark and ambrosia beetles constitute one of the major biotic agents
affecting postfire tree health (Parker et al., 2006). Within these
subfamilies of weevils (Curculionidae), two different feeding
strategies can be found. Most of the true bark beetles (Scolytinae)
construct their breeding galleries in the inner bark of trees, where
larvae feed on phloem and cambium (phloeophagous). By contrast,
ambrosia beetles (Platypodinae) are predominantly xylophagous –
they colonize the xylem for reproduction. They actively introduce
fungal symbionts via their excavated tunnels to the sapwood, where
the fungi predigest xylem for the larvae. This symbiosis habit can
cause severe damage to the xylem and also is known from
phloeophagous bark beetles. Therefore, phloeophagous attacks (c2
in Fig. 3) are often accompanied by xylophagous attacks (c3 in
Fig. 3; Hulcr et al., 2007; Six, 2012). Wood borers (insects
belonging to the families of Buprestidae, Cerambycidae and
Siricidae) also have been shown to affect the xylem of fire-weakened
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1736
trees by creating holes and extended tunnels in sap- and heartwood,
which often provide gateways for fungal infections (Parker et al.,
2006; Costello et al., 2011; Negron et al., 2016). The feeding habit
and the possible introduction of fungi decide upon the type of
infestation mechanism and thus how a tree is weakened or even the
tree’s death caused. The creation of galleries, larval activity, spread
of the fungal symbiont and the tree’s defense response (exuded resin
also can affect phloem integrity) during a phloeophagous attack can
cause serious damage to the carbohydrate translocation pathway.
For plants that are not injured by fire, it is assumed that the mere
phloem feeding activity is not a primary cause of mortality
(Craighead, 1928; Paine et al., 1997; Hubbard et al., 2013; Wiley
et al., 2016). Rather, the accompanied introduction of fungi to the
xylem can induce fatal impairments of the hydraulic system, as
fungal growth can substantially reduce xylem conductivity. Rapid
declines in sap flux and transpiration along with lowered pre-dawn
water potential were demonstrated after xylophagous attacks
(Edburg et al., 2012; Hubbard et al., 2013; Frank et al., 2014),
all of which reflect fungal-caused hydraulic conductivity losses.
However, beetle-related phloem consumption in partially girdled
trees, which have been shown to exhibit an increased probability of
infestation followed by mortality (Amman & Ryan, 1991;
Rasmussen et al., 1996), further reduces the already limited
downward translocation of C (a2 in Fig. 3). Even though the exact
contribution of insect activity to tree death cannot not yet be
assessed, phloem feeding can theoretically lead to a complete
disruption of the C transport pathway within partially girdled
stems and initiate the cascading processes of C starvation (a4 in
Fig. 3).
Maringer et al. (2016) and Conedera et al. (2010) highlighted
the protective function of bark and the decay resistance of wood
against secondary fungal infections after fires. Both studies
attributed the high postfire mortality risk of F. sylvatica to fungal
activity, which was favored by cracks and open lesions in the thin
bark and the slow wounding response after heating. Further, root-
inhabiting fungi (e.g. Poria spp., Leptographium spp. and
Heterobasidium annosum) were observed to be involved in postfire
tree decline and mortality (Littke & Gara, 1986; Otrosina et al.,
1999, 2002). Xylem decay and tissue occlusion by hyphal growth
and resinosis during infestation may lead to considerable hydraulic
conductivity losses in roots (Joseph et al., 1998). Any additional
loss in xylem conductivity (b3 in Fig. 3) caused by biotic agents may
amplify hydraulic limitations in fire-injured trees and thus be
critical for tree survival.
Vigorous trees may successfully defend themselves from biotic
attacks by killing or compartmentalizing the invading organism.
The highly evolved defense mechanisms of conifers (Franceschi
et al., 2005) are based on resin stored in axial and radial ducts.
When attacked, coniferous trees can alter the nature of the resin by
producing toxic chemicals and initiate resin flow to the wound site,
thereby compartmentalizing the intruding organism. Angiosperms
respond with accumulation of tannins, formation of tyloses, as well
as anatomical and chemical modifications to isolate the infected
area (Shigo, 1984; Salleet al., 2014). Subsequently, callus forma-
tion in the cambial zone constitutes an important wound-closure
and healing process that initiates the development of a wound
periderm and the restoration of phloem and cambium continuity
(Franceschi et al., 2005). Although these mechanisms can poten-
tially stop insects and fungi from causing fatal damage to the
hydraulic system, especially bark and ambrosia beetles are known to
attack and kill trees with a weakened defense system (e.g. Negron
et al., 2016; Catry et al., 2017). Therefore, the state of the defense
system, which is connected to the tree’s pre-fire condition, extents
of fire injuries and postfire physiology, is crucial for the vulnera-
bility to biotic attacks and for postfire recovery.
VI. Conclusion
Postfire functional limitations and mortality of injured trees are
governed by complex physiological mechanisms that can act
independently or in combination. Accordingly, processes of the C
starvation and/or hydraulic failure pathway may be initiated either
separately by cambial necrosis, hydraulic dysfunction and biotic
agents, or by a combination of these triggers. Even though the
knowledge of postfire physiological responses is growing, our
understanding of how these processes are linked or coupled and
how they can be mutually activated is incomplete. Evaluating the
precise relationships between these physiological mechanisms is
crucial for better understanding how fires affect the functional
integrity of trees and for improving models of postfire tree mortality
(Hood et al., 2018). Continued research is needed to enhance our
knowledge on the underlying biophysical processes (e.g. cell wall
kinetics during thermal softening) and to better understand how
different species respond to fire injuries under varying postfire
environmental and ecological conditions. Holistic process-based
approaches, considering heat transfer processes, first-order effects
and second-order physiological responses, will improve predictions
of postfire tree growth and mortality. Therefore, data on functional
traits that control heat transfer (e.g. bark insulation capability), heat
resistance of tissues, wound closure behavior and hydraulics need to
be linked with postfire physiological parameters to develop
improved management and risk assessment tools.
Acknowledgements
This work was supported by grants of the ‘Doktoratsstipendium
neu aus der Nachwuchsf€orderung der Leopold-Franzens-
Universit€at Innsbruck’. The study was conducted in the frame of
the research area ‘Mountain Regions’ of the University of
Innsbruck. STM was supported by SERDP project RC18-1346.
ORCID
Andreas B€ar https://orcid.org/0000-0002-0059-3964
Stefan Mayr https://orcid.org/0000-0002-3319-4396
Sean T. Michaletz https://orcid.org/0000-0003-2158-6525
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