A reduced role for water transport during the Cenozoic evolution of epiphytic Eupolypod ferns.

The Cretaceous-Cenozoic expansion of tropical forests created canopy space that was subsequently occupied by diverse epiphytic communities including Eupolypod ferns. Eupolypods proliferated in this more stressful niche, where lower competition enabled the adaptive radiation of thousands of species. Here, we examine whether xylem traits helped shape the Cenozoic radiation of Eupolypod ferns. We characterized the petiole xylem anatomy of 39 species belonging to the Eupolypod I and Eupolypod II clades occupying the epiphytic, hemiepiphytic, and terrestrial niche, and we assessed vulnerability to embolism in a subset of species. The transition to the canopy was associated with reduced xylem content and smaller tracheid diameters, but no differences were found in species vulnerability to embolism and pit membrane thickness. Phylogenetic analyses support selection for traits associated with reduced water transport in Eupolypod 1 species. We posit that in Eupolypod epiphytes, selection favored water retention via thicker leaves and lower stomatal density over higher rates of water transport. Consequently, lower leaf water loss was coupled with smaller quantities of xylem and narrower tracheid diameters. Traits associated with water conservation were evident in terrestrial Eupolypod 1 ferns and may have predisposed this clade toward radiation in the canopy.

Xylem biomechanics, water storage, and density within roots and shoots of an angiosperm tree species.

Xylem is a complex tissue that forms the bulk of tree bodies and has several functions, including to conduct water, store water and nutrients, and biomechanically support the plant body. We examined how xylem functional traits varied at different positions within 9-year-old Populus balsamifera subsp. trichocarpa. Whole trees were excavated, and xylem samples were collected at 1-m increments along the main root-to-shoot axis of six trees, from root tip to shoot tip. We examined biomechanical and water-storage traits of the xylem, including using a non-invasive imaging technique to examine water content within long, intact branches (high-resolution computed tomography; microCT). Xylem density, strength, and stiffness were greater in shoots than roots. Along the main root-to-shoot axis, xylem strength and stiffness were greatest at shoot tips, and the tissue became linearly weaker and less stiff down the plant and through the root. Roots had greater water storage with lower biomechanical support, and shoots had biomechanically stronger and stiffer xylem with lower water storage. These findings support trade-offs among xylem functions between roots and shoots. Understanding how xylem functions differ throughout tree bodies is important in understanding whole-tree functioning and how terrestrial plants endure numerous environmental challenges over decades of growth.

Primary tissues may affect estimates of cavitation resistance in ferns.

Different methods of measuring cavitation resistance in fern petioles lead to variable results, particularly with respect to the P50 metric. We hypothesised that the fern dictyostele structure affects air entry into the xylem, and therefore impacts the shape of the vulnerability curve. Our study examined this variation by comparing vulnerability curves constructed on petioles collected from evergreen and deciduous ferns in the field, with curves generated using the standard centrifuge, air-injection and bench-top dehydration methods. Additional experiments complemented the vulnerability curves to better understand how anatomy shapes estimates of cavitation resistance. Centrifugation and radial air injection generated acceptable vulnerability curves for the deciduous species, but overestimated drought resistance in the two evergreen ferns. In these hardy plants, axial air injection and bench-top dehydration produced results that most closely aligned with observations in nature. Additional experiments revealed that the dictyostele anatomy impedes air entry into the xylem during spinning and radial air injection. Each method produced acceptable vulnerability curves, depending on the species being tested. Therefore, we stress the importance of validating the curves with in situ measures of water potential and, if possible, hydraulic data to generate realistic results with any of the methods currently available.

Leaf water relations in epiphytic ferns are driven by drought avoidance rather than tolerance mechanisms.

Opportunistic diversification has allowed ferns to radiate into epiphytic niches in angiosperm dominated landscapes. However, our understanding of how ecophysiological function allowed establishment in the canopy and the potential transitionary role of the hemi-epiphytic life form remain unclear. Here, we surveyed 39 fern species in Costa Rican tropical forests to explore epiphytic trait divergence in a phylogenetic context. We examined leaf responses to water deficits in terrestrial, hemi-epiphytic and epiphytic ferns and related these findings to functional traits that regulate leaf water status. Epiphytic ferns had reduced xylem area (-63%), shorter stipe lengths (-56%), thicker laminae (+41%) and reduced stomatal density (-46%) compared to terrestrial ferns. Epiphytic ferns exhibited similar turgor loss points, higher osmotic potential at saturation and lower tissue capacitance after turgor loss than terrestrial ferns. Overall, hemi-epiphytic ferns exhibited traits that share characteristics of both terrestrial and epiphytic species. Our findings clearly demonstrate the prevalence of water conservatism in both epiphytic and hemi-epiphytic ferns, via selection for anatomical and structural traits that avoid leaf water stress. Even with likely evolutionarily constrained physiological function, adaptations for drought avoidance have allowed epiphytic ferns to successfully endure the stresses of the canopy habitat.

Limited hydraulic adjustments drive the acclimation response of Pteridium aquilinum to variable light.

BACKGROUND AND AIMS: The success of invasive plants can be attributed to many traits including the ability to adapt to variable environmental conditions. Whether by adaptation, acclimation or phenotypic plasticity, these plants often increase their resource-use efficiency and, consequently, their fitness. The goal of this study was to examine the hydraulic and eco-physiological attributes of sun and shade populations of Pteridium aquilinum, a weedy fern, to determine whether the presence of vessels and other hydraulic attributes affects its success under a variety of light conditions. METHODS: Hydraulic traits such as cavitation resistance, hydraulic conductivity, photosynthesis and water potential at turgor loss point were measured on fronds from sun and shade populations. Anatomical and structural traits such as conduit diameter and length, stomatal density and vein density were also recorded. Diurnal measures of leaf water potential and stomatal conductance complement these data. KEY RESULTS: Gas exchange was nearly double in the sun plants, as was water-use efficiency, leaf-specific conductivity, and stomatal and vein density. This was largely achieved by a decrease in leaf area, coupled with higher xylem content. There was no significant difference in petiole cavitation resistance between the sun and shade leaves, nor in xylem-specific conductivity. Hydraulic conduit diameters were nearly equivalent in the two leaf types. CONCLUSIONS: Shifts in leaf area and xylem content allow P. aquilinum to occupy habitats with full sun, and to adjust its physiology accordingly. High rates of photosynthesis explain in part the success of this fern in disturbed habitats, although no change was observed in intrinsic xylem qualities such as cavitation resistance or conduit length. This suggests that P. aquilinum is constrained by its fundamental body plan, in contrast to seed plants, which show greater capacity for hydraulic adjustment.

Geometry, Allometry and Biomechanics of Fern Leaf Petioles: Their Significance for the Evolution of Functional and Ecological Diversity Within the Pteridaceae.

Herbaceous plants rely on a combination of turgor, ground tissues and geometry for mechanical support of leaves and stems. Unlike most angiosperms however, ferns employ a sub-dermal layer of fibers, known as a hypodermal sterome, for support of their leaves. The sterome is nearly ubiquitous in ferns, but nothing is known about its role in leaf biomechanics. The goal of this research was to characterize sterome attributes in ferns that experience a broad range of mechanical stresses, as imposed by their aquatic, xeric, epiphytic, and terrestrial niches. Members of the Pteridaceae meet this criteria well. The anatomical and functional morphometrics along with published values of tissue moduli were used to model petiole flexural rigidity and susceptibility to buckling in 20 species of the Pteridaceae. Strong allometric relationships were observed between sterome thickness and leaf size, with the sterome contributing over 97% to petiole flexural rigidity. Surprisingly, the small-statured cheilanthoid ferns allocated the highest fraction of their petiole to the sterome, while large leaves exploited aspects of geometry (second moment of area) to achieve bending resistance. This pattern also revealed an economy of function in which increasing sterome thickness was associated with decreasing fiber cell reinforcement, and fiber wall fraction. Lastly, strong petioles were associated with durable leaves, as approximated by specific leaf area. This study reveals meaningful patterns in fern leaf biomechanics that align with species leaf size, sterome attributes and life-history strategy.

The water relations and xylem attributes of albino redwood shoots (Sequioa sempervirens (D. Don.) Endl.).

Plants that lack chlorophyll are rare and typically restricted to holoparasites that obtain their carbon, water and mineral resources from a host plant. Although not parasites in the traditional sense, albino foliage, such as the sprouts that sometimes develop from redwood tree trunks, are comparable in function. They occur sporadically, and can reach the size of shrubs and in rare cases, trees. Albino redwoods are interesting because in addition to their reduced carbon resources, the absence of chloroplasts may impede proper stomatal function, and both aspects may have upstream consequences on water transport and xylem quality. We examined the water relations, water transport and xylem anatomical attributes of albino redwoods and show that similar to achlorophyllous and parasitic plants, albino redwoods have notably higher stomatal conductance than green sprouts. Given that stem xylem tracheid size as well as water transport efficiency are nearly equivalent in both albino and green individuals, we attribute the increased leaf water loss in albino sprouts to lower leaf to xylem area ratios, which favour improved hydration relative to green sprouts. The stems of albino redwoods were more vulnerable to drought-induced embolism than green stems, and this was consistent with the albino's weaker tracheids, as characterized by wall thickness to lumen diameter measures. Our results are both complementary and consistent with previous research on achlorophyllous plants, and suggest that the loss of stomatal control and photosynthetic capacity results in substantial vascular and anatomical adjustments.

Not dead yet: the seasonal water relations of two perennial ferns during California's exceptional drought.

The understory of the redwood forests of California's coast harbors perennial ferns, including Polystichum munitum and Dryopteris arguta. Unusual for ferns, these species are adapted to the characteristic Mediterranean-type dry season, but the mechanisms of tolerance have not been studied. The water relations of P. munitum and D. arguta were surveyed for over a year, including measures of water potential (Ψ), stomatal conductance (gs) and frond stipe hydraulic conductivity (K). A dehydration and re-watering experiment on potted P. munitum plants corroborated the field data. The seasonal Ψ varied from 0 to below -3 MPa in both species, with gs and K generally tracking Ψ; the loss of K rarely exceeded 80%. Quantile regression analysis showed that, at the 0.1 quantile, 50% of K was lost at -2.58 and -3.84 MPa in P. munitum and D. arguta, respectively. The hydraulic recovery of re-watered plants was attributed to capillarity. The seasonal water relations of P. munitum and D. arguta are variable, but consistent with laboratory-based estimates of drought tolerance. Hydraulic and Ψ recovery following rain allows perennial ferns to survive severe drought, but prolonged water deficit, coupled with insect damage, may hamper frond survival. The legacy effects of drought on reproductive capacity and community dynamics are unknown.

Heavy browsing affects the hydraulic capacity of Ceanothus rigidus (Rhamnaceae).

Defoliation by herbivores can reduce carbon assimilation, change plant water relations, and even shift the biotic structure of plant communities. In this study, we took advantage of a long-term deer exclosure experiment to examine the consequences of persistent deer herbivory on plant water relations and the xylem structure-function relationships in Ceanothus rigidus, a maritime chaparral shrub in coastal California. Browsed plants had thicker stems with many intertwined short distal twigs, and significantly higher sapwood-to-leaf area ratios than their non-browsed counterparts. Leaf area-specific hydraulic conductivity was similar in both browsed and non-browsed plants, but xylem area-specific conductivity was significantly lower in the browsed plants. Vessel diameters were equivalent in both plant groups, but the number of vessels on a transverse area basis was nearly 40% lower in the browsed plants, accounting for their lower transport efficiency. Mid-day in situ water potentials and losses of hydraulic conductivity due to embolism were similar in both groups of plants but stomatal conductance was higher in the browsed shrubs in the early part of the growing season. We discuss our findings in the context of whole-plant ecophysiology, and explore the consequences of herbivory on hormonal signals, wood anatomy, and xylem function.