Contrasting survival strategies for seedlings of two northern conifer species to extreme droughts and floods.

Lowland northern white-cedar (Thuja occidentalis) forests are increasingly exposed to extreme droughts and floods that cause tree mortality. However, it is not clear the extent to which these events may differentially affect regeneration of cedar and its increasingly common associate, balsam fir (Abies balsamea). To test this, we measured how seedlings of cedar and fir were able to avoid, resist, and recover from experimental drought and flood treatments of different lengths (8-66 days). Overall, we found that cedar exhibited a strategy of stress resistance and growth recovery (resilience) from moderate drought and flood stress. Fir, on the other hand, appears to be adapted to avoid drought and flood stress and exhibited overall lower growth resilience. In drought treatments, we found evidence of different stomatal behaviors. Cedar used available water quickly and therefore experienced more drought stress than fir but cedar was able to survive at water potentials > 3 MPa below key hydraulic thresholds. On the other hand, fir employed a more conservative water use strategy and therefore avoided extremely low water potential. In response to flood treatments, cedar survival was higher and only reached 50% if exposed to 23.1 days of flooding in contrast to only 7.4 days to reach 50% mortality for fir. In both droughts and floods, many stressed cedar were able to maintain partially brown canopies and often survived the stress, albeit with reduced growth, suggesting a strategy of resistance and resilience. In contrast, fir that experienced drought or flood stress had a threshold-type responses and they either had full live canopies with little effect on growth or they died suggesting reliance on a strategy of drought avoidance. Combined with increasingly variable precipitation regimes, seasonal flooding, and complex microtopography that can provide safe sites in these forests, these results inform conservation and management of lowland cedar stands.

Linking physiological drought resistance traits to growth and mortality of three northeastern tree species.

Climate change is raising concerns about how forests will respond to extreme droughts, heat waves and their co-occurrence. In this greenhouse study, we tested how carbon and water relations relate to seedling growth and mortality of northeastern US trees during and after extreme drought, warming, and combined drought and warming. We compared the response of our focal species red spruce (Picea rubens Sarg.) with a common associate (paper birch, Betula papyrifera Marsh.) and a species expected to increase abundance in this region with climate change (northern red oak, Quercus rubra L.). We tracked growth and mortality, photosynthesis and water use of 216 seedlings of these species through a treatment and a recovery year. Each red spruce seedling was planted in containers either alone or with another seedling to simulate potential competition, and the seedlings were exposed to combinations of drought (irrigated, 15-d 'short' or 30-d 'long') and temperature (ambient or 16 days at +3.5 °C daily maximum) treatments. We found dominant effects of the drought reducing photosynthesis, midday water potential, and growth of spruce and birch, but that oak showed considerable resistance to drought stress. The effects of planting seedlings together were moderate and likely due to competition for limited water. Despite high temperatures reducing photosynthesis for all species, the warming imposed in this study minorly impacted growth only for oak in the recovery year. Overall, we found that the diverse water-use strategies employed by the species in our study related to their growth and recovery following drought stress. This study provides physiological evidence to support the prediction that native species to this region like red spruce and paper birch are susceptible to future climate extremes that may favor other species like northern red oak, leading to potential impacts on tree community dynamics under climate change.

Hydraulic failure as a primary driver of xylem network evolution in early vascular plants.

The earliest vascular plants had stems with a central cylindrical strand of water-conducting xylem, which rapidly diversified into more complex shapes. This diversification is understood to coincide with increases in plant body size and branching; however, no selection pressure favoring xylem strand-shape complexity is known. We show that incremental changes in xylem network organization that diverge from the cylindrical ancestral form lead to progressively greater drought resistance by reducing the risk of hydraulic failure. As xylem strand complexity increases, independent pathways for embolism spread become fewer and increasingly concentrated in more centrally located conduits, thus limiting the systemic spread of embolism during drought. Selection by drought may thus explain observed trajectories of xylem strand evolution in the fossil record and the diversity of extant forms.

The functional implications of tracheary connections across growth rings in four northern hardwood trees.

BACKGROUND AND AIMS: Deciduous angiosperm trees transport xylem sap through trunks and branches in vessels within annual growth rings. Utilizing previous growth rings for sap transport could increase vessel network size and redundancy but may expose new xylem to residual air embolisms in the network. Despite the important role of vessel networks in sap transport and drought resistance, our understanding of cross-ring connections within and between species is limited. METHODS: We studied cross-ring connections in four temperate deciduous trees using dye staining and X-ray microcomputed tomography (microCT) to detect xylem connectivity across growth rings and quantify their impact on hydraulic conductivity. KEY RESULTS: Acer rubrum and Fraxinus americana had cross-ring connections visible in microCT but only A. rubrum used previous growth rings for axial sap flow. Fagus grandifolia and Quercus rubra, however, did not have cross-ring connections. Accounting for the number of growth rings that function for axial transport improved hydraulic conductivity estimates. CONCLUSIONS: These data suggest that the presence of cross-ring connections may help explain aspects of whole-tree xylem sap transport and should be considered for plant hydraulics measurements in these species and others with similar anatomy.

Functional Status of Xylem Through Time.

Water transport in vascular plants represents a critical component of terrestrial water cycles and supplies the water needed for the exchange of CO2 in the atmosphere for photosynthesis. Yet, many fundamental principles of water transport are difficult to assess given the scale and location of plant xylem. Here we review the mechanistic principles that underpin long-distance water transport in vascular plants, with a focus on woody species. We also discuss the recent development of noninvasive tools to study the functional status of xylem networks in planta. Limitations of current methods to detect drought-induced xylem blockages (e.g., embolisms) and quantify corresponding declines in sap flow, and the coordination of hydraulic dysfunction with other physiological processes are assessed. Future avenues of research focused on cross-validation of plant hydraulics methods are discussed, as well as a proposed fundamental shift in the theory and methodology used to characterize and measure plant water use.

Hydraulic safety margins and air-seeding thresholds in roots, trunks, branches and petioles of four northern hardwood trees.

During drought, xylem sap pressures can approach or exceed critical thresholds where gas embolisms form and propagate through the xylem network, leading to systemic hydraulic dysfunction. The vulnerability segmentation hypothesis (VSH) predicts that low-investment organs (e.g. leaf petioles) should be more vulnerable to embolism spread compared to high-investment, perennial organs (e.g. trunks, stems), as a means of mitigating embolism spread and excessive negative pressures in the perennial organs. We tested this hypothesis by measuring air-seeding thresholds using the single-vessel air-injection method and calculating hydraulic safety margins in four northern hardwood tree species of the northeastern United States, in both saplings and canopy height trees, and at five points along the soil-plant-atmosphere continuum. Acer rubrum was the most resistant to air-seeding and generally supported the VSH. However, Fagus grandifolia, Fraxinus americana and Quercus rubra showed little to no variation in air-seeding thresholds across organ types within each species. Leaf-petiole xylem operated at water potentials close to or exceeding their hydraulic safety margins in all species, whereas roots, trunks and stems of A. rubrum, F. grandifolia and Q. rubra operated within their safety margins, even during the third-driest summer in the last 100 yr.

MicroCT imaging as a tool to study vessel endings in situ.

PREMISE OF THE STUDY: Despite the strong influence of the frequency and distribution of vessel endings on both hydraulic safety and efficiency, detailed anatomical descriptions or measurements of these structures are generally lacking. METHODS: Here we used high-resolution x-ray microcomputed tomography (microCT) to identify and describe xylem vessel endings within Acer rubrum root segments (1.0-2.1 mm diameter, ∼2 mm long). We then compared vessel-lumen diameter, pit density, vessel element length, and perforation plate angle between non-ending vessels (those that traverse an entire segment) and those that end within a segment using three-dimensional image analysis. KEY RESULTS: We found 214 vessel endings, 37 complete vessels, and 385 non-ending vessels within four A. rubrum root segments. Vessels that ended within the segments tended to have more acute perforation plate angles and had a smaller diameter than those that did not end within the segments. Most vessel diameters tapered within the last few vessel elements, but the perforation plate angle apparently changed over longer distances. Intervessel pit density and vessel element length did not differ between ending and non-ending vessels. CONCLUSIONS: Vessel endings were surprisingly frequent in A. rubrum roots despite the common perception that root vessels are longer than vessels in other tissues. MicroCT proved to be a useful tool for studying the three-dimensional arrangement of vessel endings within xylem networks, and these data will be helpful in developing a better understanding of vessel ending microstructure and function.

Tree demography suggests multiple directions and drivers for species range shifts in mountains of Northeastern United States.

Climate change is expected to lead to upslope shifts in tree species distributions, but the evidence is mixed partly due to land-use effects and individualistic species responses to climate. We examined how individual tree species demography varies along elevational climatic gradients across four states in the northeastern United States to determine whether species elevational distributions and their potential upslope (or downslope) shifts were controlled by climate, land-use legacies (past logging), or soils. We characterized tree demography, microclimate, land-use legacies, and soils at 83 sites stratified by elevation (~500 to ~1200 m above sea level) across 12 mountains containing the transition from northern hardwood to spruce-fir forests. We modeled elevational distributions of tree species saplings and adults using logistic regression to test whether sapling distributions suggest ongoing species range expansion upslope (or contraction downslope) relative to adults, and we used linear mixed models to determine the extent to which climate, land use, and soil variables explain these distributions. Tree demography varied with elevation by species, suggesting a potential upslope shift only for American beech, downslope shifts for red spruce (more so in cool regions) and sugar maple, and no change with elevation for balsam fir. While soils had relatively minor effects, climate was the dominant predictor for most species and more so for saplings than adults of red spruce, sugar maple, yellow birch, cordate birch, and striped maple. On the other hand, logging legacies were positively associated with American beech, sugar maple, and yellow birch, and negatively with red spruce and balsam fir - generally more so for adults than saplings. All species exhibited individualistic rather than synchronous demographic responses to climate and land use, and the return of red spruce to lower elevations where past logging originally benefited northern hardwood species indicates that land use may mask species range shifts caused by changing climate.