R. B. Pratt

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.

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.

Mechanisms for tolerating freeze-thaw stress of two evergreen chaparral species: Rhus ovata and Malosma laurina (Anacardiaceae).

The response to freeze-thaw stress was examined for two co-occurring evergreen species, Malosma laurina and Rhus ovata. Laboratory and field experiments on adults and seedlings were made in the spring and winter in 1996 and again on adults in 2003 and 2004. Laboratory and field results indicated that the stem xylem for adults of M. laurina and R. ovata were similarly susceptible to freezing-induced cavitation (percentage loss of conductivity = 92 ± 2.6% for R. ovata and 90 ± 4.2% for M. laurina at ≤ -6°C). In contrast, leaves of M. laurina were more susceptible to freezing injury than leaves of R. ovata. Among seedlings in the field, leaves of M. laurina exhibited freezing injury at -4°C and total shoot mortality at -7.2°C, whereas co-occurring seedlings of R. ovata were uninjured. Surprisingly, R. ovata tolerates high levels of freezing-induced xylem embolism in the field, an apparently rare condition among evergreen plants. Rhus ovata avoids desiccation when xylem embolism is high by exhibiting low minimum leaf conductance compared to M. laurina. These results suggest a link between minimum leaf conductance and stem hydraulics as a mechanism permitting the persistence of an evergreen leaf habit in freezing environments.

Xylem Transport Safety and Efficiency Differ among Fynbos Shrub Life History Types and between Two Sites Differing in Mean Rainfall

Xylem safety and efficiency were analyzed for stems of evergreen shrubs that inhabit fynbos communities in the Mediterranean-type climate region of South Africa. We hypothesized that species with different life history types would differ in xylem function on account of their different regeneration niches. Comparisons were made among postfire nonsprouters, facultative sprouters, obligate sprouters, and opportunists. Measurements included xylem resistance to water stress–induced cavitation (xylem safety) and xylem-specific hydraulic conductivity (xylem efficiency) at a dry site and at a wetter site. Life history types differed in hydraulic traits: xylem safety was greater in life history types with disturbance-dependent recruitment. By contrast, water stress resistance was lowest in postfire obligate resprouters that recruit seedlings during fire-free intervals in the litter layer of shady microsites. Among life history types, greater xylem safety came at the cost of reduced hydraulic efficiency. This pattern was also observed between field sites, with most taxa from the drier site having greater levels of cavitation resistance and lower levels of xylem-specific hydraulic conductivity than taxa from the wetter site. We conclude that xylem traits are linked to differences in life history types in fynbos species.

Exotic deer diminish post-fire resilience of native shrub communities on Santa Catalina Island, southern California

Browsing by exotic mule deer on Santa Catalina Island (SCI) off the coast of southern California may diminish the post-fire resilience of native shrublands. To assess this, deer exclosures were established following a wildfire to monitor post-fire recovery of three dominant, native shrub species (Heteromeles arbutifolia, Rhus integrifolia, and Rhamnus pirifolia). Post-fire resprout growth, mortality, and tissue water status as well as pre- and post-fire shrub density and cover were measured inside and outside of deer exclosures. We found that deer browsing significantly limited post-fire resprout growth and led to increased mortality of resprouting H. arbutifolia shrubs (88 % mortality outside compared to 11 % inside exclosures). Post-fire resprouts maintained favorable water status during the study despite drought conditions, indicating that water stress was not a proximate cause of resprout mortality. Deer browsing resulted in a >93 % reduction in canopy coverage of dominant shrub species. The dramatic reduction of native shrubs at this site may create opportunities for displacement by exotic species, resulting in eventual vegetation-type conversion. The observed link between intense browsing and post-fire shrub mortality provides much needed information concerning the environmental impact of exotic deer on SCI and illustrates the interaction between exotic herbivores and fire on an island system.

Root resistance to cavitation is accurately measured using a centrifuge technique.

Plants transport water under negative pressure and this makes their xylem vulnerable to cavitation. Among plant organs, root xylem is often highly vulnerable to cavitation due to water stress. The use of centrifuge methods to study organs, such as roots, that have long vessels are hypothesized to produce erroneous estimates of cavitation resistance due to the presence of open vessels through measured samples. The assumption that roots have long vessels may be premature since data for root vessel length are sparse; moreover, recent studies have not supported the existence of a long-vessel artifact for stems when a standard centrifuge technique was used. We examined resistance to cavitation estimated using a standard centrifuge technique and compared these values with native embolism measurements for roots of seven woody species grown in a common garden. For one species we also measured vulnerability using single-vessel air injection. We found excellent agreement between root native embolism and the levels of embolism measured using a centrifuge technique, and with air-seeding estimates from single-vessel injection. Estimates of cavitation resistance measured from centrifuge curves were biologically meaningful and were correlated with field minimum water potentials, vessel diameter (VD), maximum xylem-specific conductivity (Ksmax) and vessel length. Roots did not have unusually long vessels compared with stems; moreover, root vessel length was not correlated to VD or to the vessel length of stems. These results suggest that root cavitation resistance can be accurately and efficiently measured using a standard centrifuge method and that roots are highly vulnerable to cavitation. The role of root cavitation resistance in determining drought tolerance of woody species deserves further study, particularly in the context of climate change.

On research priorities to advance understanding of the safety-efficiency tradeoff in xylem: A response to Bittencourt et al.'s (2016) comment 'On xylem hydraulic efficiencies, wood space-use and the safety-efficiency tradeoff': in this issue of New Phytologist, pp. 1152-1155

We appreciate Bittencourt et al.’s (2016) constructive contributions following our paper, Gleason et al. (2016), on the proposed tradeoff between hydraulic safety and efficiency. To continue this dialog we would like to comment on which of the research directions proposed by Bittencourt et al. seem most promising to us. We agree that various xylem tissue fractions could potentially modify the safety–efficiency relationship. In principle, any tissue fraction could trade off with any other tissue fraction. However, as a matter of observation, parenchyma fraction is negatively correlated with fiber fraction, whereas parenchyma and fiber fractions are not strongly correlated with vessel lumen fraction (Ziemi! nska et al., 2015; Morris et al., 2016). As such, vessel lumen fraction, vessel diameter, and vessel frequency are largely uncoupled from nonvessel tissue fractions across self-supporting angiosperm species (Zanne et al., 2010), and are therefore unlikely to trade off with mechanical safety and hydraulic efficiency (or safety). Furthermore, vessel lumen fraction itself does not vary markedly across angiosperms, ranging from c. 5% to 20% (mean! 15%) (Zanne et al., 2010; Morris et al., 2016), although larger fractions are not uncommon in ring-porous and climbing species. Contrasts between climbing (e.g. lianas) and freestanding growth forms are more likely to show differences in allocation to vessel vs nonvessel space, and the climbing habit therefore may offer a more appropriate system for evaluating this idea (Gartner, 1991). Gymnosperm xylem differs from angiosperm xylem in that it generally lacks axial parenchyma, and conduits are both conductive and load-bearing. Greater mechanical safety may be negatively correlated with both hydraulic safety and efficiency across gymnosperm species (Mayr & Cochard, 2003; Mayr et al., 2003). Considering angiosperms, it is likely that nonvessel tissue fractions influence the safety–efficiency tradeoff indirectly (e.g. via their contribution to xylem capacitance, or whole-plant growth), rather than being forced by limited xylem space. Bittencourt et al. suggest that expressing conductivity as a ratio with mass, rather than cross-sectional area, might better characterize the energetic costs associated with xylem. We agree with this suggestion and did consider the influence of specific gravity on the safety–efficiency tradeoff in our paper (Table 2 and Figs 3d, 4d in Gleason et al., 2016). Here, we formulate these results by expressing the y axis explicitly as xylem-specific conductivity/ specific gravity (Fig. 1), as suggested by Bittencourt et al. Specific gravity, safety and efficiency values were generally obtained from the same published reports. Similar to the results we report in Gleason et al. (2016), including specific gravity in the analyses increases the tradeoff r 2 in both angiosperms (0.11–0.14) and gymnosperms (0.10–0.15) when safety is defined as P50. A similar increase in r 2 is achieved when defining safety as P88 and there is no change when defining safety as P12. Although including xylem density does increase the amount of variation explained by the models, they still fall far short of explaining why many species exhibit both low safety and low efficiency. Despite the analysis provided in Fig. 1, we feel that the clearest approach to analyzing these inter-correlated variables will be to consider all known sources of variation (e.g. structural equation models) rather than expressing them as a ratio with conductivity (e.g. conductivity/parenchyma fraction). Such ratios build an assumption of proportionality between the two elements of the ratio, which are not necessarily what we should expect. It remains a possibility that xylem safety, expressed as the xylem water potential at which a fraction of maximal conductance is lost, may not be an accurate approximation for all species in all situations. Although we agree in principle that safety (e.g. P50) may not correlate with mortality similarly across species, there is good evidence to suggest that it does for many angiosperm and gymnosperm species (Pratt et al., 2008; Brodribb & Cochard, 2009; Brodribb et al., 2010). This suggests that there may be an intrinsic property of xylem to resist desiccation (angiosperm Ψleaf > P88; gymnosperm Ψleaf > P50), beyond which the probability of mortality increases precipitously. Measurements of hydraulic safety, as well as conductivity during drought, should serve as more appropriate predictors of mortality than other measurements of water status (e.g. turgor loss point in leaves or stomatal response) because percentage loss of conductance is a meaningful representation of xylem desiccation. However, it is also clear that there are mechanisms that delay the time to reach a desiccation–mortality threshold. As suggested by Bittencourt et al. and Brodersen (2016), these would include deciduousness, deep rooting, reduced stomatal ‘leakiness’, reduced cuticular conductance, CAM and C4 metabolism, and capacitance. However, considering tradeoffs with either safety or efficiency, in isolation of one another (e.g. safety–capacitance), does not inform our efforts to understand the proposed link between safety and efficiency. For example, if greater capacitance reduces the requirement for safety, natural selection should still be free to improve efficiency, which would provide benefit via greater