Introduction
Unveiling the mechanisms of species co-existence in plant communities
has been one of the greatest challenges in ecological research
(Valladares, Bastias, Godoy, Granda, &
Escudero, 2015). Over the past seven decades, many studies have
concluded that species coexist by sharing limited resources and
occupying different niches (de la Riva,
Marañón, Violle, Villar, & Pérez-Ramos, 2017;
Peñuelas et al., 2019). An ecological
niche is an abstraction of a time-space continuum, where individual
species have exclusive access to limited resources thereby sharing them
with coexisting species in spatially and / or temporally segregated
pools (Gause, 1934;
MacArthur, 1968;
Noble & Fagan, 2015;
Whittaker, 1969). In terms of sharing
water soil resources by two or more plant species,
Araya et al. (2011) introduced the concept
of hydrological niche segregation (HNS), where species specialize in the
use of distinct niches as a result of trade-offs between tolerance to
aeration stress and tolerance to drying stress
(Jonathan Silvertown, Dodd, Gowing, &
Mountford, 1999). Hydrological niche segregation has been defined as
partitioning of i) space along fine-scale moisture gradients, ii) water
as a resource or iii) recruitment opportunities between years when
species respond differentially to distinct patterns of temporal variance
in water supply (storage effect) (Araya et
al., 2011; Jonathan Silvertown, Araya, &
Gowing, 2015).
Since all plants require the same principal resources (light, carbon
dioxide, water, mineral nutrients)
(Jonathan Silvertown, 2004) and acquire
them in a highly limited number of ways, as mentioned by
Jonathan Silvertown et al. (1999), this
might result in frequent niche overlaps. Even though niche segregation
among species has being identified as a mechanism to reduce niche
overlap in several studies (Araya et al.,
2011; Bartelheimer, Gowing, & Silvertown,
2010; Jonathan Silvertown, 2004;
Jonathan Silvertown et al., 2015;
Jonathan Silvertown et al., 1999;
J. Silvertown & Law, 1987), it is still
unresolved how physiological, phenological, and anatomical traits of
coexisting species may potentially act together, i.e. are coupled, to
sense and garner spatially and/or temporally available resources and
thereby avoid or reduce competition.
Thus far, species coexistence studies have assumed a certain substrate
homogeneity, even though individual niches may actually exhibit complex
geological, geomorphological and edaphic properties
(Gray, 2004;
Kukowski, Schwinning, & Schwartz, 2013).
It is this geodiversity that eventually contributes to the spatial and
temporal segregation and use of resources and thereby facilitate species
coexistence. Critical non-resource factors (soil depth, precipitation
patterns, rockiness, etc.) (Maestre,
Callaway, Valladares, & Lortie, 2009) may also control resource
availability and species adaptations and thereby contribute to an
ecological niche. Consequently, it is the spatial, temporal (both
referring to resource availability) and biological (trait based)
dimensions of a niche that permit differential resource use and
therefore species coexistence. Plant functional traits are measurable
morphological, anatomical, physiological and phenological features that
species employ to effectively capture resources and to adapt and
acclimate to and tolerate a wide spectrum of environmental conditions
(Adler et al., 2014;
Muscarella & Uriarte, 2016). In highly
resource limited environments, the coexistence of long-lived species
reflects species-specific, selective, complementary plant-resource
response spectra spanning all developmental stages. Therefore, adult
individuals of co-existing species exhibit distinct plant responses to
resource availability, which are controlled by a set of traits (e.g.,
differential spatial placement of coarse and fine roots with distinct
root anatomy access different water sources, etc.) together forming a
dynamic biological niche axis along an environmental gradient, such that
each interacting species occupies a certain niche along the space and
time continuum (axes). Some species traits are fine-tuned sensors (for
example, when reaching a physiological threshold) that detect
environmental signals of niche quality and thus may induce a switch in
niche occupation; for instance, when resources become depleted.
To examine hydrological niche segregation, it is necessary to understand
the complexity of the “nichescape” in a real-world setting. With
nichescape we refer to the set of traits employed by plants to garner
resources, that are spatially and temporally distributed in the
soil-rock continuum. The ideal model system to study this should include
a minimum set of well-differentiated, measurable spatial niches, which
are occupied differentially and/or temporally in a complementary manner
by naturally coexisting species. This setting is present in the
semi-arid pine-oak forest of the Sierra San Miguelito Volcanic Complex
(SSMVC) in Central Mexico. Recent explorations
(Rodriguez-Robles, Arredondo,
Huber-Sannwald, & Vargas, 2015) identified potential
geoecohydrological niches derived indirectly from plant and soil water
potential values, where deep roots of oak (Quercus potosina )
trees apparently explored, acquired and remobilized water stored in
belowground rock cracks, while pine (Pinus cembroides ) trees
apparently fulfilled their water demand by root uptake from shallow
soil. Given the extreme water scarcity, and the suite of inherently
different functional traits of pine and oak (i.e., root distribution,
phenology, plant water relations)
(Rodriguez-Robles et al., 2015), their
coexistence must have evolved in a complex dynamic “nichescape”
allowing spatially and temporally complementary water use by the two
species.
In this study, we examined whether differential water uptake capacities
of coexisting species in response to recurring fine-scale spatial
moisture gradients (i.e. occurring within a few cm, generated by water
movements in substrates with different water holding capacities) are the
main mechanisms of hydrologic niche segregation, or whether tree
functional traits as well as the water dynamics in the substrate
together control such niche segregation. Based on the HNS concept, we
hypothesized that even an apparently simple geological microenvironment
(i.e. shallow soil over fractured rock) partitions into a
multidimensional niche consisting of spatial soil humidity gradients,
temporal variability of water access, and different plant functional
traits that effectively exploit each potential water source. We further
hypothesized that the humidity gradients and water partitioning between
species are coupled to the wetting/drying cycles in this forest
ecosystem. Using hydrogeological and geophysical prospection methods
(Rodríguez-Robles, Arredondo,
Huber-Sannwald, Ramos-Leal, & Yépez, 2017) coupled with intensive
monitoring of natural abundance of stable isotope ratios of water, heavy
water labelling studies, eco-physiological and anatomical measurements,
we describe for the first time the identity, spatial extent and
temporality of several niches used by two coexisting forest species, as
well as the plant functional traits employed of their occupation and
use, jointly forming the multidimensional nature of niches (nichescape)
in a semiarid forest ecosystem.