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.