Tree growth, transpiration, and water-use efficiency between shoreline and upland red maple (Acer rubrum) trees in a coastal forest

Highlights

• Whole-tree transpiration, radial growth, and δ¹³C were measured in a coastal forest.

• Shoreline trees had higher transpiration rates than the nearby upland trees.

• Shoreline trees had similar growth and gas exchange compared to the upland trees.

• Trees adapted to shoreline conditions by maintaining homeostasis in water relations and growth.

Abstract

Coastal shoreline forests are vulnerable to seawater exposure, the impacts of which will increase due to sea-level rise, but the long-term adaptation strategies and vulnerability of coastal forests are not well understood. We used whole-tree transpiration, leaf water potential, tree-ring width, and tree-ring δ¹³C (a proxy for intrinsic water use efficiency, iWUE) to examine the long-term adaptation strategies of red maple (Acer rubrum) trees at the coastal interface (i.e., shoreline) and nearby upland in Maryland, USA. Red maple trees that grew along the shoreline and were exposed to slightly saline water (up to two PSU) had higher transpiration rates than those growing in the nearby upland forest during a wet year, but these differences disappeared during a normal precipitation year. Shoreline trees grew more slowly than upland trees over the last four decades, but these growth differences have disappeared in the last six years. Shoreline and upland red maple trees had similar variation in iWUE, indicating that higher transpiration rates of the seawater-exposed trees did not translate into differences in water use efficiency. There were no differences in predawn and midday water potential between upland and shoreline trees, suggesting no additional water stress occurs in shoreline trees. These findings indicate that mature red maple in our coastal study site maintains gas exchange and growth at a consistent or homeostatic level under slight soil salinity.

Introduction

Low-lying forests play a critical role in water, energy, and biogeochemical cycles and provide substantial ecosystem services through buffering the impacts of storms and erosion (IPCC, 2019; Wong et al., 2014). Accelerating sea-level rise (SLR) and increasing frequency and intensity of storms due directly or indirectly to global warming is driving freshwater forested wetlands towards salt marsh (Kirwan and Gedan, 2019; Thorne et al., 2018). However, our understanding of coastal forest growth and the role of seawater stress in affecting ecohydrological cycling is insufficient, which limits our ability to represent the function and sensitivity of coastal interfaces in global system models (Krauss et al., 2015a; Ward et al., 2020).

Seawater exposure can impact non-halophyte woody plant function through both belowground and aboveground mechanisms, with large impacts on ecosystem ecohydrological cycling and even widespread tree mortality (Kirwan and Gedan, 2019; Kozlowski, 1997; Krauss et al., 2015a). Existing eco-physiological knowledge of coastal (non-halophytic) trees’ response to seawater comes mostly from studies of water salinity impacts on seedlings of wetland tree species (Conner and Askew, 1993; McLeod et al., 1996; Negrão et al., 2017; Woods et al., 2020). Under soil salinity stress, the soil-to-root water potential gradient is reduced, thereby limiting water uptake and also causing osmotic imbalances (Boursiac et al., 2005). As the soil-to-root flow declines so do hydraulic flow and stomatal flow, the latter exacerbated by the need to maintain foliar osmotic pressure ultimately driving strong reductions in gas exchange and growth (Conner and Askew, 1993; Ewers et al., 2004; Stavridou et al., 2017; Sutka et al., 2011). Salinity damage can also involve the accumulation of foliar ions to toxic concentrations, causing premature senescence and ultimately reduced growth and even death (Munns and Tester, 2008; Negrão et al., 2017). Rare studies of non-halophyte mature trees growing in low-to-moderate levels of salinity suggest that only 2-3 PSU (practical salinity unit) salinity levels (<1 PSU is freshwater, and open seawater is near 35 PSU) can have dramatic impacts on plant hydraulics (Duberstein et al., 2020; Krauss et al., 2015b). Knowledge of the response of non-halophytic upland tree species (e.g. red maple) to salinity stress at coastal shorelines can greatly improve understanding of coastal water budgets and ecosystem dynamics (Krauss et al., 2015a).

Transpiration, growth, and intrinsic water-use efficiency (iWUE) are three essential and sensitive indices of plant performance that can be assessed at the whole-tree level in mature forests (Eamus et al., 2013). Transpiration plays a critical role in ecosystem evapotranspiration (Schlesinger and Jasechko, 2014). The ability to maintain whole-crown transpiration at control (freshwater) tree levels while under saline conditions (defined here as “homeostasis”) is an important indicator of salt adaptation strategies (Munns and Tester, 2008; Negrão et al., 2017). Empirical studies have revealed large transpiration reductions in response to seawater exposure (Duberstein et al., 2020; Krauss and Duberstein, 2010). Additionally, relationships between canopy transpiration and environmental variables such as VPD and PAR can give insight into how forest ecohydrological processes respond to seawater exposure (Krauss et al., 2015a; Krauss et al., 2015b). Like transpiration, growth integrates the physiological processes of gas exchange and carbon allocation, and is a sensitive indicator of salinity stress (Desantis et al., 2007; Wang et al., 2019). Finally, iWUE is a sensitive indicator of salinity stress, with both mangroves and non-halophytic tree species showing an increase in iWUE due to a decline in stomatal conductance with salinity exposure (Brienen et al., 2016; Brugnoli and Lauteri, 1991; Wang et al., 2019).

Tree-rings are a valuable tool to retrospectively understand long-term tree radial growth and iWUE responses to changing environmental conditions (Babst et al., 2017; Dannenberg et al., 2019). Tree growth integrates the physiological processes of gas exchange and carbon allocation, and is a fundamental indicator of salinity stress (Desantis et al., 2007; Fernandes et al., 2018). Annual tree-ring widths have exhibited substantial growth declines in response to seawater in Florida, South Carolina, Georgia, and Virginia coastal forests (Fernandes et al., 2018; Saha et al., 2011; Thomas et al., 2015). In addition, one can assess gas exchange constraints on photosynthesis through the use of tree-ring stable carbon isotope ratios (δ¹³C), which simultaneously reflect changes in assimilation rate (A) and adjustments in stomatal conductance (g_s), and allows quantification of whole-tree gas exchange and iWUE (Farquhar et al., 1989; Guerrieri et al., 2019; McCarroll and Loader, 2004). By combining whole-tree estimates of transpiration, tree-ring width, and δ¹³C, we can assess seawater stress on coastal mature forests over extended time periods.

To examine the long-term shifts in tree impacts that may be occurring due to precipitation and saline groundwater exposure near an estuarine shoreline, we compared mature red maple (Acer rubrum) trees located at the shoreline versus neighboring trees growing at higher elevations in an upland forest (~100 m distant and ~2 m above sea level). Though salinity levels are below 3 PSU at our site, such levels of salt have previously been shown to have large impacts on water use and growth of upland tree species (Duberstein et al., 2020). We investigated some of the potential adaptation mechanisms of shoreline trees through transpiration, tree growth, and iWUE. Red maple is a “super-generalist” species, as it is widely distributed across a large range of moisture and nutrient availabilities (Abrams, 1998; Iverson and Prasad, 1998), and is considered somewhat flood and salt-tolerant (Anella and Whitlow, 1999; Hallett et al., 2018). We specifically tested whether red maple radial growth rates differed between shoreline and upland locations, and whether these differences were related to transpiration and iWUE. We hypothesized that 1) red maples at the shoreline would have lower radial growth rates than those in upland locations; 2) transpiration would be lower in shoreline than upland trees; and 3) iWUE would be higher in shoreline trees than upland trees.