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.