H. Jochen Schenk

Wood anatomy and wood density in shrubs: responses to varying aridity along transcontinental transects.

Wood density plays a key role in ecological strategies and life history variation in woody plants, but little is known about its anatomical basis in shrubs. We quantified the relationships between wood density, anatomy, and climate in 61 shrub species from eight field sites along latitudinal belts between 31° and 35° in North and South America. Measurements included cell dimensions, transverse areas of each xylem cell type and percentage contact between different cell types and vessels. Wood density was more significantly correlated with precipitation and aridity than with temperature. High wood density was achieved through reductions in cell size and increases in the proportion of wall relative to lumen. Wood density was independent of vessel traits, suggesting that this trait does not impose conduction limitations in shrubs. The proportion of fibers in direct contact with vessels decreased with and was independent of wood density, indicating that the number of fiber-vessel contacts does not explain the previously observed correlation between wood density and implosion resistance. Axial and radial parenchyma each had a significant but opposite association with wood density. Fiber size and wall thickness link wood density, life history, and ecological strategies by controlling the proportion of carbon invested per unit stem volume.

Hydraulic integration and shrub growth form linked across continental aridity gradients.

Both engineered hydraulic systems and plant hydraulic systems are protected against failure by resistance, reparability, and redundancy. A basic rule of reliability engineering is that the level of independent redundancy should increase with increasing risk of fatal system failure. Here we show that hydraulic systems of plants function as predicted by this engineering rule. Hydraulic systems of shrubs sampled along two transcontinental aridity gradients changed with increasing aridity from highly integrated to independently redundant modular designs. Shrubs in humid environments tend to be hydraulically integrated, with single, round basal stems, whereas dryland shrubs typically have modular hydraulic systems and multiple, segmented basal stems. Modularity is achieved anatomically at the vessel-network scale or developmentally at the whole-plant scale through asymmetric secondary growth, which results in a semiclonal or clonal shrub growth form that appears to be ubiquitous in global deserts.

Vertical Vegetation Structure Below Ground: Scaling from Root to Globe

The structure of vegetation that is below ground truly is the hidden half (Waisel et al. 2002), hidden from view and too often hidden from biological research. Over the last 30 years, the Biological Abstracts database has recorded almost twice as many publications in plant ecology that address the ecology of leaves than studies of root ecology. Biologists do not even have a term to refer to the subterranean parts of vegetation. In the English language, biologists use the term canopy to refer to the collective arrangement of all leaves in a plant community, but lack such a term for roots. (The old-fashioned word rootage suggests itself.) Despite this unequal attention to the visible and the hidden halves of vegetation, the two parts are equally important for the function of terrestrial plants and ecosystems and have general functions in common: Both halves are structured to enable resource capture. They are made up of organs that are specialized for resource acquisition, leaves above ground and the distal parts of roots below ground, and of the axes that support and connect these sites of resource acquisition within individual plants. Both also contain structures that are devoted to mechanical support, to storage of resources, and to reproduction; these are, however, beyond the scope of this chapter. Both exhibit a vertical structure that responds to resources that have a strong vertical dimension, light above ground, water, nutrients, and physical soil structure below ground.

Nanobubbles: a new paradigm for air-seeding in xylem

Long-distance water transport in plants relies on a system that typically operates under negative pressure and is prone to hydraulic failure due to gas bubble formation. One primary mechanism of bubble formation takes place at nanoporous pit membranes between neighboring conduits. We argue that this process is likely to snap off nanobubbles because the local increase in liquid pressure caused by entry of air-water menisci into the complex pit membrane pores would energetically favor nanobubble formation over instant cavitation. Nanobubbles would be stabilized by surfactants and by gas supersaturation of the sap, may dissolve, fragment into smaller bubbles, or create embolisms. The hypothesis that safe and stable nanobubbles occur in plants adds a new component supporting the cohesion-tension theory.

INTERVESSEL PIT MEMBRANE THICKNESS AS A KEY DETERMINANT OF EMBOLISM RESISTANCE IN ANGIOSPERM XYLEM

Pit membranes in bordered pits between neighbouring vessels play a major role in the entry of air-water menisci from an embolised vessel into a water-filled vessel (i.e., air-seeding). Here, we investigate intervessel pit membrane thickness (TPM) and embolism resistance (P50, i.e., the water potential corresponding to 50% loss of hydraulic conductivity) across a broad range of woody angiosperm species. Data on TPM and double intervessel wall thickness (TVW) were compiled based on electron and light microscopy. Fresh material that was directly fixated for transmission electron microscopy (TEM) was investigated for 71 species, while non-fresh samples were frozen, stored in alcohol, or air dried prior to TEM preparation for an additional 60 species. TPM and P50 were based on novel observations and literature. A strong correlation between TPM and P50 was found for measurements based on freshly fixated material (r = 0.78, P >0.01, n = 37), and between TPM and TVW (r = 0.79, P >0.01, n = 59), while a slightly weaker relationship occurred between TVW and P50 (r = 0.40, P >0.01, n = 34). However, non-fresh samples showed no correlation between TPM and P50, and between TPM and TVW. Intervessel pit membranes in non-fresh samples were c.28% thinner and more electron dense than fresh samples. Our findings demonstrate that TPM measured on freshly fixated material provides one of the strongest wood anatomical correlates of droughtinduced embolism resistance in angiosperms. Assuming that cellulose microfibrils show an equal spatial density, TPM is suggested to affect the length and the shape of intervessel pit membrane pores, but not the actual pore size. Moreover, the shrinking effect observed for TPM after dehydration and frost is associated with an increase in microfibril density and porosity, which may provide a functional explanation for embolism fatigue.

Integration of vessel traits, wood density, and height in angiosperm shrubs and trees.

PREMISE OF THE STUDY Trees and shrubs tend to occupy different niches within and across ecosystems; therefore, traits related to their resource use and life history are expected to differ. Here we analyzed how growth form is related to variation in integration among vessel traits, wood density, and height. We also considered the ecological and evolutionary consequences of such differences. METHOD In a sample of 200 woody plant species (65 shrubs and 135 trees) from Argentina, Mexico, and the United States, standardized major axis (SMA) regression, correlation analyses, and ANOVA were used to determine whether relationships among traits differed between growth forms. The influence of phylogenetic relationships was examined with a phylogenetic ANOVA and phylogenetically independent contrasts (PICs). A principal component analysis was conducted to determine whether trees and shrubs occupy different portions of multivariate trait space. KEY RESULTS Wood density did not differ between shrubs and trees, but there were significant differences in vessel diameter, vessel density, theoretical conductivity, and as expected, height. In addition, relationships between vessel traits and wood density differed between growth forms. Trees showed coordination among vessel traits, wood density, and height, but in shrubs, wood density and vessel traits were independent. These results hold when phylogenetic relationships were considered. In the multivariate analyses, these differences translated as significantly different positions in multivariate trait space occupied by shrubs and trees. CONCLUSIONS Differences in trait integration between growth forms suggest that evolution of growth form in some lineages might be associated with the degree of trait interrelation.

Hydraulically integrated or modular? Comparing whole-plant-level hydraulic systems between two desert shrub species with different growth forms

* Hydraulic systems of shrubs vary between hydraulically integrated and modular architectures; the latter divide the shrub into independent hydraulic units. Hydraulic systems of two common North American desert shrub species, the multi-branched Ambrosia dumosa and the single-stemmed Encelia farinosa (both Asteraceae), were compared to test for division into independent hydraulic units and the implications of such a division for water loss through leaves and roots. * Hydraulic systems of mature shrubs in the field were characterized using dye tracers and by documenting the degree of stem segmentation. Young pot-grown shrubs were subjected to heterogeneous and homogeneous watering. Spatial within-canopy variation of leaf water potentials and stomatal conductances, as well as soil water contents, were measured in response to manipulated soil water heterogeneity. * Results show that young Ambrosia shrubs are divided into independent hydraulic units long before they physically split into separate ramets as mature shrubs, and that young and mature Encelia shrubs possess integrated hydraulic systems. No hydraulic redistribution was detected for eitherspecies. * Our study shows that functional segmentation into independent hydraulic units precedes physical axis splitting, rather than being the consequence of split axes, and suggests that mature shrubs with round basal stems are likely to be hydraulically integrated.

Xylem Surfactants Introduce a New Element to the Cohesion-Tension Theory

Lipid-based xylem surfactants affect water transport under negative pressure by coating hydrophobic surfaces and nanobubbles and are hypothesized to reduce embolism under normal pressure conditions. Vascular plants transport water under negative pressure without constantly creating gas bubbles that would disable their hydraulic systems. Attempts to replicate this feat in artificial systems almost invariably result in bubble formation, except under highly controlled conditions with pure water and only hydrophilic surfaces present. In theory, conditions in the xylem should favor bubble nucleation even more: there are millions of conduits with at least some hydrophobic surfaces, and xylem sap is saturated or sometimes supersaturated with atmospheric gas and may contain surface-active molecules that can lower surface tension. So how do plants transport water under negative pressure? Here, we show that angiosperm xylem contains abundant hydrophobic surfaces as well as insoluble lipid surfactants, including phospholipids, and proteins, a composition similar to pulmonary surfactants. Lipid surfactants were found in xylem sap and as nanoparticles under transmission electron microscopy in pores of intervessel pit membranes and deposited on vessel wall surfaces. Nanoparticles observed in xylem sap via nanoparticle-tracking analysis included surfactant-coated nanobubbles when examined by freeze-fracture electron microscopy. Based on their fracture behavior, this technique is able to distinguish between dense-core particles, liquid-filled, bilayer-coated vesicles/liposomes, and gas-filled bubbles. Xylem surfactants showed strong surface activity that reduces surface tension to low values when concentrated as they are in pit membrane pores. We hypothesize that xylem surfactants support water transport under negative pressure as explained by the cohesion-tension theory by coating hydrophobic surfaces and nanobubbles, thereby keeping the latter below the critical size at which bubbles would expand to form embolisms.

Plant hydraulics: new discoveries in the pipeline

Increasing numbers of plant scientists are recognizing the importance of hydraulic design in determining plant function. Hydraulic design – which can be broadly defined as the functional properties of the plant vascular system – is a determinant not only of plant water balance but also of photosynthetic rates and ecological niche differentiation. Classic approaches (Tyree & Zimmermann, 2002) and newer concepts (Holbrook & Zwieniecki, 2005) are being applied to questions central to the evolution and ecology of plant species, ranging from organ to organism to ecosystem. A recent workshop held in southern California reflected diverse research programs but also highlighted a convergence of interest on key questions and promising approaches. Several breakout sessions focused on defining pressing questions of plant hydraulics and on addressing the critical need for standardization of practices for research on these topics.

Evolutionary Ecology of Plant Signals and Toxins: A Conceptual Framework

Plants are capable of acquiring information from other plants, but are they able to send signals and communicate with them? Evolutionary biologists define biological communication as information transmission that is fashioned or maintained by natural selection and signals as traits whose value to the signaler is that they convey information to receivers. Plants, then, can be said to communicate if the signaling plant derives a fitness benefit from conveying information to other plants. Examples for interplant communication that fit these definitions potentially include territorial root communications, self/non-self recognition between roots and associated with self-incompatibility, volatile signals that induce defenses against herbivores, signals from ovules to mother plants, signals associated with root graft formation, and male to female signals during pollen competition. Natural selection would favor signals that are costly to the signaler and therefore are likely to convey reliable information because they cannot be easily faked. Toxins in low concentrations may commonly act as signals between plants rather than as inhibitory allelochemicals. This explains why toxic concentrations of plant allelochemicals are rarely found in natural coevolved systems.