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).