Plant functional mechanisms of species contributing to niche partitioning
Mechanisms of water partitioning between species involved environmental clues and plant sensors, physiological responses and anatomical adaptations. During the dry periods, we identified two environmental cues that were directly linked to tree physiological thresholds and hence induced shifts in niche use by oak. The sharp drop in soil water potential indicating extremely dry environmental conditions after the winter season, was mirrored in equally low leaf water potentials in oak (lowest oak Ψleaf andΨsoil measured in the depletion period in January and February 2013, Fig. 5, S3.2a,b). This triggered oak trees to switch water uptake from surface soil to fractured rocks (well water, Fig. S3.2b), however under the same conditions pine remained using surface soil water as showed by the stable isotope signature (δO -11.2, δD -73.6 to δO -9.3, δD -55.4) of precipitation originating from the Atlantic (Figs. S3.2 b-d).
The second environmental cue occurred when oak experienced the highest vapor pressure deficit in the air in March and April 2013 as it started redistributing water from fractured rocks to the surface soil (Rodríguez-Robles et al., 2017) through hydraulic lift. After five months (Dec 2012 to April 2013) of seasonal drought, oak Ψleaf recovered by 1.5 MPa in both stands (Fig. 5) by having accessed water from both soil fractures and surface soil to where water had been remobilized by hydraulic lift. On the other hand, pine Ψleaf recovered by 1.0 MPa yet only in mixed stands, where water had been made available by oak via hydraulic lift. The isotopic δ18O and δD signatures of water extracted from twig xylem of both species was similar to that of groundwater in the dry season. The isotopic enrichment of local surface soil water near oak indicates that oak roots were extracting and vertically redistributing enriched water from deep soil layers and fractured rock and therefore were likely responsible for the observed hydraulic lift (Fig 4c). This response type was consistent with that observed in other studies conducted in the Mediterranean, where most of the roots of Q. ilex were in all soil horizons, to maximize the use of topsoil water during most of the year, and groundwater together with hydraulically lifted water (enhancing nutrient supply) during seasonal droughts (Aranda, Ramírez-Valiente, & Rodríguez-Calcerrada, 2014; David et al., 2007).
Oak and pine wood anatomical adaptations exhibit remarkable differences that explain species-specific functional adaptations to both highly variable water availability and rapid local soil and rock water depletion (Hacke, Sperry, & Pittermann, 2005; Sperry, Hacke, & Pittermann, 2006) and thus potentially efficient responses to shifts in niche use (Fig. S6). In pine roots a parenchyma surrounding the tracheids grants highly efficient soil water uptake and conduction to the canopy (von Arx, Arzac, Olano, & Fonti, 2015) (Figs. S6g, f, S4), particularly in response to small precipitation pulses. In contrast, in oak trunks a particular structural anatomy of specialized tissue formed by fiber tracheids connects vessel tissue (Cai et al., 2014) (conductive structures, Fig. S6b, d), which provides a high capacity of water storage (Fig. S6c). Besides, oak has a considerable number of vessels adapted to xeric conditions (i.e., mixture of different diameter vessels) to improve the hydraulic efficiency by water pumping (Thomas Tyree, Salleo, Nardini, Assunta Lo Gullo, & Mosca, 1999) (Fig. S6a, S5c). Unlike pine, oak wood anatomy allows plastic shrinkage and expansion of trunk diameter for water storage or trunk capacitance in response to changing ecohydrological conditions (63 ± 6.1% and 37 ± 4.8% wood moisture content of its weight for oak and pine, respectively, P < 0.001, Fig. S7). Oak disposes of adaptations in functional root anatomy; it located its finest roots inside rock fractures (Rodríguez-Robles et al., 2017) (Fig. 3f). These roots exhibit a triple layer of epidermal tissue and contain calcium oxalate crystals (druzes), which facilitate root penetration and biophysical breakup of incipient rocks fractures (Franceschi & Nakata, 2005) (Fig. S5b). Under extremely dry conditions, oak vessel diameter of roots decreases by the formation of tyloses (Gottwald, 1972), which is an outgrowth of parenchyma cells into vessels to reduce water conduction and to prevent cavitation (Spicer, 2014), (Fig. S5d). Deep oak roots exhibited 83% more vessels with tyloses and 60% more druzes than surface roots (Fig. S5). Pine roots did not exhibit these kinds of anatomical adaptations. With the injection of labelled water into the rock fractures (3/4 L, δD = 485‰), we confirmed that pine roots could not garner water directly from water reservoirs in rock fractures. After a 10-day sampling period, the isotopic tracer was not detected in pine xylem water. In contrast, in the same assay, the oak tree closest to the injection (3.22 ± 0.78 m) presented the tracer in its trunk’s xylem water after four days of water injection (Fig. S8).