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 plant water
potentials (Buckley, 2005). However, because stomatal closure also
down-regulates leaf carbon fluxes, there can be deleterious consequences
for plant health from reduced photosynthesis.
Regulation
of plant water status differs widely across tree species and is often
characterized along a continuum of quantitative metrics describing leaf
water potential (ΨL) regulation in response to
hydrologic stress (Tardieu & Simonneau, 1998; McDowell et al .,
2008; Klein, 2014; Meinzer et al ., 2016; Matheny et al.,2017; Hochberg et al., 2018). Across this continuum, species may
exhibit relative loose regulation of stomatal conductance in response to
declining soil water and/or rising evaporative demand, allowing
ΨL to decline as hydrologic stress evolves (i.e., more
‘anisohydric’ behavior, Martínez-Vilalta et al ., 2014).
By comparison, other species may
exhibit stricter regulation of plant water loss by closing their stomata
to minimize ΨL decline (i.e., more ‘isohydric’
behavior). A less negative ΨL maintains 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 & Zimmerman, 2013).
Embolisms propagate throughout
xylem elements when hydrologic stress causes excessively large tension
forces (e.g., very low water potential) in the plant hydraulic system
(Tyree & Sperry, 1989; Davis et al ., 1999). As a result, water
transport to active sites of photosynthesis becomes restricted. 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 view is that trees with more vulnerable xylem tend to be
more isohydric (Bond & Kavanagh, 1999; Schultz, 2003; McDowell et
al ., 2008; Taneda & Sperry, 2008; Choat et al ., 2012; Plautet al ., 2012; Meinzer et 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 (ΨS) 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 temperate eastern US deciduous forests,
where drought stress is relatively less severe but may become more
frequent in the future (Dai, 2011; Novick et al ., 2016). Eastern
deciduous forests have tall canopies and dense foliage in which plants
must compete for space (Olivier et al ., 2016). While
drought-induced mortality periodically occurs in these ecosystems
(Elliott & Swank, 1994; Dietze & Moorcroft, 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 behavior and xylem vulnerability
should necessarily confer a universal advantage across diverse
ecosystems.
A tenuous understanding of intraspecific patterns of vulnerability
(Anderegg, 2015) further challenges our understanding of tradeoffs
between xylem vulnerability and ΨL regulation. 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 highly productive, species-rich,
environmentally diverse, and characterized by uneven-aged stands from a
legacy of management and disturbance (Pan et al ., 2011).
Our objective is to identify inter- and intraspecific patterns of
hydraulic traits in important eastern US deciduous forest species,
focusing on those traits which determine stomatal regulation of
ΨL in response to rising vapor pressure deficit
(D ) and declining soil moisture (Tardieu & Simonneau 1998; Domec
& Johnson, 2012; Novick et al ., 2019). Our study species areQuercus alba L., Acer saccharum Marsh., Liriodendron
tulipifera L.− which are among the region’s most dominant. Q.
alba , A. saccharum , and L. tulipifera are the
5th, 6th, and 17thmost abundant species (out of 134) in eastern US forests (Iversonet al., 2008). These species differ widely in terms of xylem
anatomy (Q. alba are ring-porous whereas A. saccharum andL. tulipifera and are diffuse-porous) and in terms of stomatal
regulation strategy (Q. alba are more anisohydric than the other
species, Meinzer et al ., 2013; Roman et al., 2015, Mathenyet al ., 2017, Denham et al. 2021). We seek to understand:
1) to what extent is regulation of ΨL coordinated with
embolism resistant tissues across these three species? and 2) how does
this relationship vary as a function of the diverse hydroclimatological
conditions and regenerative states that these species occupy? To that
end, we test 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 of more anisohydric trees 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 view 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 across ten
forest stands of differing age and climates that broadly represented the
climate envelopes of the study species’ native range. By testing these
hypotheses, we will better understand the extent to which coordination
of hydraulic traits in primarily energy-limited forests aligns with
paradigms emerging from more water-limited biomes. Our results may also
inform our understanding of an ongoing and persistent decline in eastern
US Quercus species across much of their native range (Feiet al ., 2011). Quercus species rank high in species
diversity, biomass, and carbon storage (Cavender-Bares, 2016), and
account for ~25% of all growing timber stock in the
eastern US (Fei et al ., 2011). While the causes of decline are a
matter of debate (McEwan et al., 2011), most of them are rooted
in assumptions about how Quercus versus non-Quercusspecies function during periods of hydrologic stress. WhetherQuercus species – which are putatively drought-tolerant species
(Abrams, 1990; Cavender-Bares, 2019) – will thrive or falter under
future conditions characterized by more frequent and severe drought
stress is an important unresolved question.