4. Introduction
When plants are water-limited, adaptive stomatal closure can alleviate
stress on the plant hydraulic system by reducing water loss to the
atmosphere and preventing the development of excessively low water
potentials within the plant (Buckley, 2005). However, because stomatal
closure down-regulates both water and carbon fluxes at the leaf surface,
there can be deleterious consequences for plant health from reduced
photosynthesis. Tree species differ widely in their ability to regulate
plant water status. Often, this behavior is described along an isohydric
spectrum by characterizing plant regulation of leaf water potential
(ΨL) as soil water potential (Ψs)
declines (e.g., \(\partial\Psi_{L}/\ \partial\Psi_{S}\)) (Tardieu &
Simonneau, 1998; McDowell et al ., 2008; Klein, 2014; Mathenyet al., 2016; Meinzer et al ., 2016). More anisohydric
species loosely regulate stomatal conductance with rising evaporative
demand, allowing ΨL to decline as soils dry
(Martínez-Vilalta et al ., 2014). In contrast, more isohydric
species strictly regulate plant water loss by closing their stomata to
minimize ΨL decline. A less negative ΨLmaintains the turgor pressure necessary for leaf cell growth and
expansion and is an important factor determining the risk of damage to
the hydraulic system from xylem embolism (Tyree & Zimmermann, 2013).
Embolism occurs when hydrologic stress causes excessively large tension
forces (e.g., very low water potential) in the plant hydraulic system.
As a result, xylem conduits become cavitated and embolized, and no
longer function to transport water (Tyree & Sperry, 1989; Daviset al ., 1999). The coordination of ΨL regulation
and vulnerability of xylem tissues is therefore fundamental for
understanding the tradeoffs between carbon uptake and risk of hydraulic
damage across vegetative species. The prevailing paradigm is that trees
with more vulnerable xylem tend to be more isohydric (Bond & Kavanagh,
1999; Shultz, 2003; McDowell et al ., 2008; Taneda & Sperry,
2008; Choat et al ., 2012; Plaut et al ., 2012; Meinzeret al ., 2014; Skelton et al., 2015; Sperry & Love, 2015;
Garcia-Forner et al ., 2016), as they operate with smaller safety
margins to xylem embolism and therefore require careful regulation of
ΨL to avoid hydraulic damage.
This view on the coordination of stomatal regulation of
ΨL and xylem vulnerability is implicit in the recent
incorporation of new plant hydraulic schemes into terrestrial ecosystem
models (TEM) (Naudts et al. , 2015; Kennedy et al., 2019;
Mirfenderesgi et al ., 2019). The TEM frameworks differ in the way
that hydraulics and leaf-level gas exchange processes are mathematically
linked; however, all fundamentally relate the stomatal sensitivity to
declining plant or soil water potential to the shape of the xylem
vulnerability curve. The ability of a model to link xylem vulnerability
to isohydric behavior is even viewed as an important check on a model’s
functionality (Sperry & Love, 2015).
Much of what we know about coordination between ΨL and
xylem vulnerability to embolism has relied on a legacy of observations
from dryland ecosystems (McDowell et al ., 2008; Taneda & Sperry,
2008; Plaut et al ., 2012; Skelton et al ., 2015), where
plants are generally adapted to arid environments, but excessive drought
conditions have promoted widespread mortality (Macalady & Bugmann,
2014; Meddens et al ., 2015). Less is known about the coordination
of these hydraulic traits in more temperate forests, where drought
stress is often less severe than dryland ecosystems but is predicted to
increase in frequency and severity into the future (Dai, 2011; Novicket al ., 2016). Eastern US temperate forests are characterized by
tall canopies and dense foliage cover in which plants must compete for
space (Olivier et al ., 2016). While drought-induced mortality
periodically occurs in these ecosystems (Elliott & Swank, 1994; Dietze
& Moorecraft, 2011; Wood et al ., 2018), trees must balance
conserving hydraulic function with maintaining sufficient productivity
and growth to compete for light. Given these constraints, it is not
clear that water-use strategies which adhere to strict coordination
between stomatal regulation and xylem vulnerability should necessarily
confer a universal advantage across diverse ecosystems.
Our understanding of tradeoffs between xylem vulnerability and
ΨL regulation is further challenged by a tenuous
understanding of intraspecific patterns of vulnerability (Anderegg,
2015). Species which encompass broad climate envelopes sometimes
acclimate their xylem tissues to thrive across diverse environmental
conditions (Maherali & Delucia, 2000; Herbette et al ., 2010;
Wortemann et al ., 2011). Coordination of hydraulic traits may
also change over time, reflecting long-term, plastic responses to
drought such as changes in xylem anatomy (e.g., vessel diameter) that
produce more resistant xylem (Maherali et al ., 2006).
Understanding intraspecific embolism vulnerability in both space and
time is particularly important for eastern US deciduous forests, which
are species-rich, environmentally diverse, and characterized by
uneven-aged stands from a legacy of management and disturbance (Panet al ., 2011). Nevertheless, spatio-temporal patterns of
hydraulic vulnerability across this region are poorly understood.
In this paper, we focus on identifying inter- and intraspecific patterns
of hydraulic traits in eastern US deciduous forests that determine plant
responses to both vapor pressure deficit (D ) and declining soil
moisture, both of which affect the evolution of ΨL and
stomatal regulation thereof (Tardieu & Simonneau 1998; Domec &
Johnson, 2012; Novick et al ., 2019). Our analysis also explicitly
tests assumptions that guide the parameterization of plant hydraulics in
TEMs. Our work is guided by the overarching question: Do the drought
response paradigms developed from observations of dryland vegetation
apply in temperate deciduous forests of the eastern US? To answer this
question, we tested the following three hypotheses:
1) Trees invest in more resistant xylem when growing in regions that
more regularly experience moisture stress.
2) Stem tissues are more vulnerable to embolism in shorter, younger
stands than in taller, more mature stands, because taller trees will
have developed more resistant xylem to overcome additional constraints
on water movement from increased canopy height (McDowell et al .,
2002; Novick et al ., 2009).
3) Stem tissues from trees that display anisohydric behavior will be
more resistant to hydraulic dysfunction than trees that more rapidly
close their stomata to limit ΨL decline (e.g., isohydric
behavior). This hypothesis reflects the prevailing paradigm, based
largely on dryland studies, that the vulnerability of xylem tissues to
embolism is linked to more isohydric behavior.
To test these hypotheses, we analyzed stem xylem anatomy, stem embolism
vulnerability, and ΨL observations of three
common deciduous forest species with contrasting xylem anatomy and
stomatal regulation, Acer saccharum Marsh., Quercus albaL., and Liriodendron tulipifera L. We conducted this study across
ten forest stands of differing age and climates that broadly represented
moisture availability for deciduous vegetation across the eastern US. We
characterized the plasticity of critical hydraulic traits that determine
drought-tolerance and productivity. Additionally, we sought to
understand if the functional coordination of ΨLregulation and risk of xylem dysfunction commonly observed in dryland
vegetation is indicative of drought-response behavior of temperate
forests.