7.2 The perplexing case of Q. alba
Our finding that Q. alba had the most vulnerable xylem was
unexpected. Quercus species are often considered more drought
tolerant than many co-dominants, attributed to their morphological and
physiological adaptations that allow them to withstand soil moisture
deficits (Abrams, 2003). Our results complicate this perspective. We
found that Q. alba had particularly high P50 (consistent with
previous work: Maherali et al ., 2006; Kannenberg et al.,2019) but were also more anisohydric.
We
used the variation in ΨL to quantify the degree of
isohydricity in order to incorporate stomatal responses to both
declining soil water and increasing D , noting that the latter is
the predominant factor limiting conductance for these sites and species
(Novick et al., 2016; Yi et al., 2019; Denham et
al., 2021). However, prior work using other approaches for quantifying
isohydricity in these study sites and elsewhere also concludes thatQuercus species are more anisohydric than many of their
co-dominant counterparts (Abrams, 1990; Cavender-Barres & Bazzaz, 2000;
Ewers et al. , 2007; Meinzer et al., 2013; Roman et
al., 2015; Kannenberg et al ., 2019). Here, our results further
revealed that Q. alba trees had a high degree of estimated native
embolism and negative Ψsafety suggesting they are
remarkably vulnerable to drought.
While rooting depth is an important component of a plant’s water use
strategy, species-specific differences in rooting depth cannot explain
our results. Quercus species tend to be more deeply rooted than
cohabiting tree species in eastern US forests (Abrams, 1990), an
expectation recently confirmed by our study team in IN 85yo (Lanninget al ., 2020). However, periodic observations of pre-dawn
ΨL, a commonly used proxy for integrated
ΨS across the rooting zone (Richter, 1997), were less
conclusive about the extent to which functional rooting depth varied
across species (Table S3). In any event, if Q. alba have deeper
roots, then access to more stable moisture pools should keep midday
ΨL elevated relative to other species; instead, we findQ. alba typically had more negative midday ΨL(Fig. 6) despite the fact they may have access to deeper pools of water.
While the hydraulic metrics
quantified here are widely used to characterize drought-susceptibility,
drought impacts on whole-plant physiological function are more complex
than stomatal regulation of xylem water tension. For example,
drought-susceptibility is determined not only by the risk of xylem
dysfunction, but also the plant’s ability to cope with and recover from
hydraulic damage (Meinzer & McCulloh, 2013). We therefore consider howQ. alba can exhibit a seemingly risky hydraulic strategy while
adhering to drought-tolerance. First, we note that our methodology
permits an evaluation of the vulnerability of the entire sapwood depth.
However, it is not clear that Q. alba rely on the entire depth of
sapwood to actively conduct water (Cochard & Tyree, 1990). In a related
study from IN 85yo, Yi et al . (2017) found that the inner sapwood
of Q. alba conducted a more significant fraction of water during
drought, with water transport largely restricted to outer rings during
well-watered periods. Additionally, internal water storage can also play
an important role in determining the relationship between leaf gas
exchange and stem xylem traits. Ring-porous species are known to use
smaller amounts of stored water than diffuse-porous species because of
their low number of active rings (Köcher et al ., 2013). Q.
alba has much higher wood density than either L. tulipifera orA. saccharum, and species with greater wood density tend to have
low capacitance (e.g., Meinzer et al., 2008). Unlike L.
tulipifera and A. saccharum that bear large sapwood volume and
have low wood density, the small water storage capacity of Q.
alba cannot provide enough water to limit the rapid drop in water
potential due to stomatal water loss, which could also explain its
anisohydric behavior (Matheny et al ., 2015).
Recovery from hydraulic impairment may also explain how Q. albatolerates drought while possessing vulnerable xylem. Refilling of
embolized conduits is a possible strategy for ring-porous species to
maintain hydraulic function (Brodersen et al ., 2010; Ogasaet al ., 2013; Trifilò et al ., 2019; Zeppel et al .,
2019), although whether xylem refilling routinely occurs in long vessel
species is debated (Lamarque et al., 2018). Moreover, Q.
alba bears only a few hydraulically active sapwood rings
(<10), with the newest rings being the most efficient at
moving water (Phillips et al ., 1996). Therefore, Q. albacould potentially repair a 50% loss of conductivity in fewer than five
years just by the production of new annual rings. While metabolically
costly, growth and assimilation for Quercus species is often less
sensitive to water stress than their more isohydric co-dominants
(Elliott et al. , 2015; Roman et al., 2015; Au et
al., 2020). Thus, the hydraulic strategy of Q. alba may be to
maximize carbon assimilation at the risk of hydraulic impairment such
that hydraulic function can be readily recovered through new growth.Quercus species also have an abundance of embolism-resistant
vasicentric tracheids that can account for as much as 15% of hydraulic
conductivity in stems (Percolla et al., 2021). These tracheid
networks likely play an important role in sustaining water transport and
growth when vulnerable vessels have embolized (Fontes & Cavender-Bares,
2020).
Xylem vulnerability assessments must be conducted with care and a clear
recognition of potential sources of methodological bias (Cochardet al., 2013, Johnson et al., 2018; Lobo et al.,2018). The air-injection technique used in this study remains the most
popular tool for generating vulnerability curves, though it is sensitive
to open vessel artifacts which may produce excessive variability in the
derived estimates of P50 (Martin-StPaul et al., 2014). As
discussed extensively in our methods, we deployed a thorough set of
quality control measures to minimize this source of error in our data.
These measures included: [1] limiting samples to young, distal
branches which have shorter vessels, [2] direct testing for the
presence of open vessels on every sample using the air-infiltration
technique, and [3] careful post-facto screening of curves to remove
those that were conspicuously ‘r-shaped’. If Q. alba samples were
characterized by a greater number of open vessels, then we would have
expected a high percentage of Q. alba curves to be ‘r-shaped.’
Instead, variability in P50 was similar across species (coefficient of
variation = 0.26, 0.19, & 0.19 for Q. alba , A. saccharumand L. tulipifera , respectively) suggesting that focusing on
young branches and directly testing for open vessels were effective at
limiting open vessel bias.
We recognize that this study focused only on three tree species and that
others have found stomatal regulation and embolism vulnerability to be
generally coordinated across species in other temperate regions (e.g.,
Vogt, 2001). Nonetheless, our results are consistent with other studies
employing different strategies to generate ‘s-shaped’ vulnerability
curves for Quercus species. Using the cavitron technique, Loboet al., (2018) found that species-specific curves of six EuropeanQuercus species were highly consistent and sigmoidal when
branches were screened for open vessels.
Johnson et al., (2018)
found good agreement between the air-injection and centrifuge methods
for Q. fusiform branches when checked for open vessels, as they
were in our study. Moreover, Kannenberg et al., (2019) used the
air-injection technique to generate xylem vulnerability curves for the
entire stem of tree saplings, which should be especially insensitive to
open vessel artifacts; that study also concluded that the P50 ofQ. alba was higher than L. tulipifera and A.
saccharum . Finally, Skelton et al. (2021) used cutting edge
techniques to visually monitor embolism formation. While they concluded
that western North American Quercus species that dominate
desert/chaparral environments have substantially negative P50s, they
also reported that Quercus species growing in more temperate
western forests have less negative P50 which were similar to those
observed for the Q. alba trees growing in our temperate and mesic
study sites (e.g., P50 ≥ −3 MPa).
Altogether, it appears that Q. alba sustain high rates of gas
exchange at the cost of operating with damaging water potential
gradients and low Ψsafety. Moreover, much of the
variability in stomatal conductance and water potential for eastern US
trees, and especially Quercus species, are determined by the
dynamics of D (Yi et al., 2019, Novick et al.,2019; Denham et al., 2021). Thus, these species may be
particularly vulnerable to hydraulic dysfunction linked to future
droughts that will be characterized by increasingly high D(Ficklin & Novick, 2017). In that regard, strategies to sustainQuercus dominated forest may need to recognize that they may in
fact be quite sensitive to drought stress.