Anna L. Jacobsen

Global convergence in the vulnerability of forests to drought.

Shifts in rainfall patterns and increasing temperatures associated with climate change are likely to cause widespread forest decline in regions where droughts are predicted to increase in duration and severity. One primary cause of productivity loss and plant mortality during drought is hydraulic failure. Drought stress creates trapped gas emboli in the water transport system, which reduces the ability of plants to supply water to leaves for photosynthetic gas exchange and can ultimately result in desiccation and mortality. At present we lack a clear picture of how thresholds to hydraulic failure vary across a broad range of species and environments, despite many individual experiments. Here we draw together published and unpublished data on the vulnerability of the transport system to drought-induced embolism for a large number of woody species, with a view to examining the likely consequences of climate change for forest biomes. We show that 70% of 226 forest species from 81 sites worldwide operate with narrow (<1 megapascal) hydraulic safety margins against injurious levels of drought stress and therefore potentially face long-term reductions in productivity and survival if temperature and aridity increase as predicted for many regions across the globe. Safety margins are largely independent of mean annual precipitation, showing that there is global convergence in the vulnerability of forests to drought, with all forest biomes equally vulnerable to hydraulic failure regardless of their current rainfall environment. These findings provide insight into why drought-induced forest decline is occurring not only in arid regions but also in wet forests not normally considered at drought risk.

Do Xylem Fibers Affect Vessel Cavitation Resistance

Possible mechanical and hydraulic costs to increased cavitation resistance were examined among six co-occurring species of chaparral shrubs in southern California. We measured cavitation resistance (xylem pressure at 50% loss of hydraulic conductivity), seasonal low pressure potential (Pmin), xylem conductive efficiency (specific conductivity), mechanical strength of stems (modulus of elasticity and modulus of rupture), and xylem density. At the cellular level, we measured vessel and fiber wall thickness and lumen diameter, transverse fiber wall and total lumen area, and estimated vessel implosion resistance using (t/b)h2, where t is the thickness of adjoining vessel walls and b is the vessel lumen diameter. Increased cavitation resistance was correlated with increased mechanical strength (r2 = 0.74 and 0.76 for modulus of elasticity and modulus of rupture, respectively), xylem density (r2 = 0.88), and Pmin (r2 = 0.96). In contrast, cavitation resistance and Pmin were not correlated with decreased specific conductivity, suggesting no tradeoff between these traits. At the cellular level, increased cavitation resistance was correlated with increased (t/b)h2 (r2 = 0.95), increased transverse fiber wall area (r2 = 0.89), and decreased fiber lumen area (r2 = 0.76). To our knowledge, the correlation between cavitation resistance and fiber wall area has not been shown previously and suggests a mechanical role for fibers in cavitation resistance. Fiber efficacy in prevention of vessel implosion, defined as inward bending or collapse of vessels, is discussed.

CAVITATION RESISTANCE AMONG 26 CHAPARRAL SPECIES OF SOUTHERN CALIFORNIA

Resistance to xylem cavitation depends on the size of xylem pit membrane pores and the strength of vessels to resist collapse or, in the case of freezing-induced cavitation, conduit diameter. Altering these traits may impact plant biomechanics or water transport efficiency. The evergreen sclerophyllous shrub species, collectively referred to as chaparral, which dominate much of the mediterranean-type climate region of southern California, have been shown to display high cavitation resistance (pressure potential at 50% loss of hydraulic conductivity; P50). We examined xylem functional and structural traits associated with more negative P50 in stems of 26 chaparral species. We correlated raw-trait values, without phylogenetic consideration, to examine current relationships between P50 and these xylem traits. Additionally, correlations were examined using phylogenetic independent contrasts (PICs) to determine whether evolutionary changes in these xylem traits correlate with changes in P50. Co-occurring chaparral species widely differ in their P50 (� 0.9 to � 11.0 MPa). Species experiencing the most negative seasonal pressure potential (Pmin) had the highest resistance to xylem cavitation (lowest P50). Decreased P50 was associated with increased xylem density, stem mechanical strength (modulus of rupture), and transverse fiber wall area when both raw values and PICs were analyzed. These results support a functional and evolutionary relationship among these xylem traits and cavitation resistance. Chaparral species that do not sprout following fire but instead recruit post-fire from seed had the greatest resistance to cavitation, presumably because they rely on post-fire survival of seedlings during the summer dry period to persist in the landscape. Raw values of hydraulic vessel diameter (dh), maximum vessel length, and xylem-specific hydraulic conductivity (Ks) were correlated to P50; however, dh, maximum vessel length, and Ks were not correlated to P50 when analyzed using PICs, suggesting that these traits have not undergone correlated evolutionary change. We found no difference in xylem traits between species occurring at freezing vs. nonfreezing sites, although freezing has been shown to affect the survival and distributions of some chaparral species. Stem mechanical strength, fiber properties, and post-fire regeneration type appear to be key factors in the evolution of cavitation resistance among chaparral shrubs.

Comparative community physiology: nonconvergence in water relations among three semi‐arid shrub communities

Plant adaptations to the environment are limited, and therefore plants in similar environments may display similar functional and physiological traits, a pattern termed functional convergence. Evidence was examined for functional convergence among 28 evergreen woody shrubs from three plant communities of the semi-arid winter rainfall region of southern California. Both leaf and water relations traits were examined, including seasonal stomatal conductance (gs), specific leaf area (SLA), leaf specific conductivity (Kl), seasonal water potential (Psi w), stem cavitation resistance (Psi 50), and xylem density. Species display community-specific suites of xylem and leaf traits consistent with different patterns of water use among communities, with coastal sage scrub species utilizing shallow pulses of water, Mojave Desert scrub species relying on deeper water reserves, and chaparral species utilizing both shallow and deep moisture reserves. Communities displayed similar degrees of water stress, with a community-level minimum Psi w (Psi wmin) of c. -4.6 Mpa, similar to other arid communities. Pooled across sites, there was a strong correlation between Psi wmin and xylem density, suggesting that these traits are broadly related and predictive of one another. This comparative community physiology approach may be useful in testing hypotheses of functional convergence across structurally similar semi-arid communities.

LIFE HISTORY TYPE AND WATER STRESS TOLERANCE IN NINE CALIFORNIA CHAPARRAL SPECIES (RHAMNACEAE)

Chaparral species of California, USA, exhibit three life history types in response to fire: non-sprouters (NS), facultative sprouters (FS), and obligate sprouters (OS). Adult non-sprouters are killed by fire; thus populations reestablish only through fire- stimulated seed germination and seedling recruitment. Facultative sprouters reestablish by both vegetative sprouting and seed germination. Obligate sprouters reestablish only by vegetative sprouting and do not recruit seedlings post-fire. Previous data suggest that post-fire NS and FS seedlings reestablish as open-canopy gap specialists, whereas OS seedlings primarily reestablish in deep shade during fire-free intervals. Their non-refractory seeds are killed by fire. We hypothesized that these differences in life history, compared within the same taxonomic group, would result in a range of relative resistance to water stress such that NS . FS . OS. To test our hypothesis, we estimated resistance to water stress using resistance to xylem cavitation (the water potential at 50% loss in hydraulic conductivity; W50) for stems and roots in nine species of the family Rhamnaceae: Ceanothus megacarpus, C. crassifolius, and C. cuneatus (NS); C. spinosus, C. oliganthus, and C. leucodermis (FS); and Rhamnus ilicifolia, R. crocea, and R. californica (OS). Stems of NS species displayed greater resistance to cavitation (W50 ¼� 8.38 6 0.47 MPa) compared to both the FS (W50 ¼� 5.07 6 0.55 MPa) and OS species (W50 ¼� 5.99 6 0.38 MPa), whereas FS and OS species were not different. For roots, the general pattern was the same, but roots were generally less cavitation resistant than stems. A hydraulic model predicted that water uptake in OS species was limited by extensive cavitation in vulnerable root xylem, consistent with a reliance on deep soil water. Water uptake in cavitation-resistant NS species was most limited by soil hydraulic resistance, consistent with maximizing extraction of shallow soil water. These results suggest a link between life history and water stress tolerance in chaparral.

No evidence for an open vessel effect in centrifuge‐based vulnerability curves of a long‐vesselled liana (Vitis vinifera)

Vulnerability to cavitation curves are used to estimate xylem cavitation resistance and can be constructed using multiple techniques. It was recently suggested that a technique that relies on centrifugal force to generate negative xylem pressures may be susceptible to an open vessel artifact in long-vesselled species. Here, we used custom centrifuge rotors to measure different sample lengths of 1-yr-old stems of grapevine to examine the influence of open vessels on vulnerability curves, thus testing the hypothesized open vessel artifact. These curves were compared with a dehydration-based vulnerability curve. Although samples differed significantly in the number of open vessels, there was no difference in the vulnerability to cavitation measured on 0.14- and 0.271-m-long samples of Vitis vinifera. Dehydration and centrifuge-based curves showed a similar pattern of declining xylem-specific hydraulic conductivity (K(s)) with declining water potential. The percentage loss in hydraulic conductivity (PLC) differed between dehydration and centrifuge curves and it was determined that grapevine is susceptible to errors in estimating maximum K(s) during dehydration because of the development of vessel blockages. Our results from a long-vesselled liana do not support the open vessel artifact hypothesis.

A global analysis of xylem vessel length in woody plants

UNLABELLED PREMISE OF THE STUDY Vessels are the chief conduit for long-distance water transport in the majority of flowering plants. Vessel length is a key trait that determines plant hydraulic efficiency and safety, yet relatively little is known about this xylem feature. • METHODS We used previously published studies to generate a new global data set of vessel length in woody plants. These data were used to examine how evolutionary history, plant habit, environment, and growth ring porosity influenced vessel length. We also examined the relationship between mean vessel length and mean vessel diameter and maximum vessel length. • KEY RESULTS Data on mean vessel length were available for stems of 130 species and on maximum vessel length for stems of 91 species. A phylogenetic analysis indicated that vessel length did not exhibit significant phylogenetic signal. Liana species had longer vessel lengths than in tree or shrub species. Vessel diameter was not predictive of mean vessel length, but maximum vessel length strongly predicted mean vessel length. Vessel length did not vary between species that differed in growth ring porosity. • CONCLUSIONS Many traits often assumed to be linked to vessel length, including growth ring porosity and vessel diameter, are not associated with vessel length when compared interspecifically. Sampling for vessel length has been nonrandom, e.g., there are virtually no data available for roots, and sampling for environment has been confounded with sampling for habit. Increased knowledge of vessel length is key to understanding the structure and function of the plant hydraulic pathway.

Xylem function of arid‐land shrubs from California, USA: an ecological and evolutionary analysis

Xylem traits were examined among 22 arid-land shrub species, including measures of vessel dimensions and pit area. These structural measures were compared with the xylem functional traits of transport efficiency and safety from cavitation. The influence of evolution on trait relationships was examined using phylogenetic independent contrasts (PICs). A trade-off between xylem safety and efficiency was supported by a negative correlation between vessel dimensions and cavitation resistance. Pit area was correlated with cavitation resistance when cross species data were examined, but PICs suggest that these traits have evolved independently of one another. Differences in cavitation resistance that are not explained by pit area may be related to differences in pit membrane properties or the prevalence of tracheids, the latter of which may alter pit area through the addition of vessel-to-tracheid pits or through changes in xylem conduit connectivity. Some trait relationships were robust regardless of species ecology or evolutionary history. These trait relationships are likely to be the most valuable in predictive models that seek to examine anatomical and functional trait relationships among extant and fossil woods and include the relationship among hydraulic conductivity and vessel diameter, between vessel diameter and vessel length, and between hydraulic conductivity and wood density.

Mortality of resprouting chaparral shrubs after a fire and during a record drought: physiological mechanisms and demographic consequences.

We examined postfire regeneration of chaparral shrubs during an intense drought. This study focused on the demography and physiology of shrub species that resprout from a basal lignotuber following fire. We found significant levels of resprout mortality when intense drought occurred in the year following fire during the period of shrub recovery. Three of the seven sampled resprouting species had the greatest or near greatest levels of mortality ever recorded when compared to previous studies. Most shrub mortality occurred during the drought after individuals had resprouted (i.e. individuals survived fire, resprouted and then subsequently died). Physiological measurements of species with high mortality suggested that resprout stems were highly embolized and xylem hydraulic conductivities were close to zero during the peak of the drought. In addition, lignotubers of two of the three species experiencing high mortality were depleted of starch. Population densities of most shrub species declined after the drought compared with their prefire levels, with the exception of one drought tolerant obligate seeding species. Resprouting shrub species may deplete their carbohydrate reserves during the resprouting process, making them particularly vulnerable to drought because of the need to transpire water to acquire the CO2 that is used to supply energy to a large respiring root system. Drought appears to interact with fire by altering postfire shrub recovery and altering species abundances and composition of chaparral communities.

Towards understanding resprouting at the global scale.

Understanding and predicting plant response to disturbance is of paramount importance in our changing world. Resprouting ability is often considered a simple qualitative trait and used in many ecological studies. Our aim is to show some of the complexities of resprouting while highlighting cautions that need be taken in using resprouting ability to predict vegetation responses across disturbance types and biomes. There are marked differences in resprouting depending on the disturbance type, and fire is often the most severe disturbance because it includes both defoliation and lethal temperatures. In the Mediterranean biome, there are differences in functional strategies to cope with water deficit between resprouters (dehydration avoiders) and nonresprouters (dehydration tolerators); however, there is little research to unambiguously extrapolate these results to other biomes. Furthermore, predictions of vegetation responses to changes in disturbance regimes require consideration not only of resprouting, but also other relevant traits (e.g. seeding, bark thickness) and the different correlations among traits observed in different biomes; models lacking these details would behave poorly at the global scale. Overall, the lessons learned from a given disturbance regime and biome (e.g. crown-fire Mediterranean ecosystems) can guide research in other ecosystems but should not be extrapolated at the global scale.