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.