Solving the conundrum of plant species coexistence: water in space and time matters most

Ecologists still wonder how so many competing plant species can coexist at the same site, defying the competitive-exclusion principle. All plants use and compete for the same basic resources (light, CO2, water, nutrients and space for growth); species with competitive advantage reduce resource availability for other species that will experience difficulties becoming established or remaining. However, if species sufficiently partition the abiotic and biotic environments, or if there are trade-offs in resource allocation (e.g. some species may allocate more resources to increase reproduction, whereas others might allocate more resources to survival or to growth), then different species can coexist by using different ranges and proportions of resources (Pacala & Tilman, 1994). The classical answer of this species coexistence conundrum states that stable coexistence between competing species requires them to occupy different niches. But the niche concept, which was initially conceived by zoologists and emphasized the role of habitat and food in defining an animal's niche (Chase & Leibold, 2002), does not offer an obvious explanation for coexistence among plants, because all plants use, and compete for, the same aforementioned resources and acquire them in similar ways. The question thus remains as to how competing plant species coexist apparently without the niche differences that classical theory predicts to be necessary. Apart from quantitative refinements (for instance, considering the differential resource consumption rate of species) and successional dynamics, two answers are possible: either the classical theory is wrong or incomplete and stabilizing mechanisms are unimportant (neutral models; Hubbell, 2001; de Aguiar et al., 2009), or there are niche differences between plants that have been overlooked (Silvertown, 2004). Plant ecologists keep trying to solve this question, most of them looking for the separation of niches and the quantification of the extent of the differences between two niches in order for corresponding species to coexist (Begon et al., 2006). In this issue of New Phytologist, Araya et al. (pp. 253–258) have elegantly shown separation of hydrological niches in two very different plant communities (in British wet meadows and in South African fynbos), quantified them and interestingly suggested the ecohydrological axis as potentially one of the most general drivers of niche differentiation for plants. '... the underlying mechanisms are ecophysiologically fundamental to plants and have the potential to govern niche segregation in many other communities.' The 'habitat' niche of a plant species may be defined as a spatial and temporal function of the ranges of water, light, nutrient, temperature and competition with neighbours that the plant is able to live with. This definition is made within large gradients of availability for each resource – arid–humid (water), oligotrophic–eutrophic (nutrients), shade–sun (light) and cold–hot (temperature) – and also as a function of microsite heterogeneity, climatic variability and disturbance that further contribute to generate local diversity. However, altogether the mechanisms that stabilize communities through such niche segregation merit further explanation (Chesson, 2000; Adler et al., 2007). Many such mechanisms have been proposed, and more than one may function simultaneously in particular plant communities. A few years ago, Silvertown et al. (1999) showed that segregation on hydrological gradients occurs in European wet meadows and that specialization of species into distinct niches is a result of a trade-off between tolerance of aeration stress and tolerance of drying stress. Araya et al. have now expanded this seminal work, testing this mechanism by quantifying the hydrological niches of floristically, functionally and phylogenetically distinct plants in fynbos communities in the Cape of South Africa. They have found this coinciding trade-off, supporting the existence of the same physiological constraints, and strengthening the generality of hydrological niche segregation. As pointed out by Araya et al., hydrological niche segregation occurs in a great variety of vegetation types across the entire spectrum of environments, from wet or mesic to arid. Araya et al.'s work connects such a single trade-off between aeration and water stress from a community (wet meadows), where aeration stress would be the limiting factor, to an ecologically and geographically distant one (South-African fynbos) where water stress is the rule. This result strongly suggests that the underlying mechanisms are ecophysiologically fundamental to plants and have the potential to govern niche segregation in many other communities. One probable mechanism is the competing demand of water conservation vs carbon acquisition along soil moisture gradients. Another mechanism is the need of nutrient acquisition along nutrient gradients that are correlated with soil moisture gradients. The first mechanism is a consequence of the fact that plants must regulate water loss through stomata while they acquire the CO2 required for photosynthesis and growth. Water use efficiency (WUE), the ratio of CO2 assimilated : stomatal conductance, should thus vary between species in a systematic manner along soil moisture gradients. Nutrient availability changes along soil moisture gradients, with a maximum in mesic soils and minima in waterlogged and very dry conditions (Araya, 2005). Plants must allocate resources to roots to compete successfully for nutrients, but to shoots to compete for light, and thus a nutrient gradient engenders a trade-off that forces plants to specialize. These fine-scale hydrological gradients are thus strongly linked to the 'biogeochemical' niche, defined as the species position in the multivariate space generated by their content, not only of macronutrients such as nitrogen (N), phosphorus (P) or potassium (K), but also of micronutrients such as molybdenum (Mo), magnesium (Mg) and calcium (Ca), and trace elements such as lead (Pb) and arsenic (As) (Peñuelas et al., 2008). Usually, there is a strong differentiation in the total and relative (stoichiometry) content of the different elements in coexisting plant species, and, there is, moreover, a differential species-specific plasticity in the response of this elemental composition to changes in environmental conditions (Peñuelas et al., 2008). Araya et al. define the hydrological niche segregation as partitioning of space on fine-scale soil-moisture gradients, and as partitioning of water as a resource through different acquisition strategies, such as different phenologies or rooting depths. By using the variable 'sum of exceedance value' relative to the threshold depths of each site for both aeration and water stress, they quantify the niche segregation and capture all three components of soil moisture variation in space, depth and time. Nevertheless, in order to capture more comprehensively this latter temporal component of niche partitioning, we propose that the variance in the intensity and seasonal distribution of both these aeration and water stress 'exceedances' should also be considered because such variances may play a significant additional or synergic niche segregation role. The ecological rationale for enhanced coexistence with increasing variances or fluctuations ('fluctuation' niche; Terradas et al., 2009) is based on the different growth response of species to water availability. If water availability fluctuates, the temporal advantage of one species becomes balanced by the advantage of the other species at another time, but if water availability remains constant, competitive exclusion is more likely to occur. A good example of the importance of the 'fluctuation niche' and of the presence of different syndromes is found in the Mediterranean environment (Fig. 1), which shows characteristic large seasonal and interannual rain fluctuations (Terradas et al., 2009). As a result, the depth of roots profoundly affects the variance of water availability, which in turn affects the variance of nutrient availability and the variances in the leaf water and nutrient status (Filella & Peñuelas, 2003). In fact, the main division in Mediterranean communities is established between species with deep roots, with more constant water and nutrient resources, and species with shallow roots, which use episodic rainwater and associated nutrient uptake. Plants develop several responses between the two extremes of this constant–episodic gradient. At one extreme there is a great, but slow, development of permanent vertical structure, both aboveground and belowground, to ensure minimum between-year and between-season fluctuation in availability of resources. At the other extreme there is a high turnover of structural components, mostly leaves and roots, as a result of high growth rates in favourable periods, which is associated with the existence of short life cycles and small plants when water resources are persistently scarce or when disturbances preclude the development of continuous canopies by larger plants. Thus, there is a gradient from a conservative strategy, when fluctuations are scarce, to an opportunistic strategy, which withstands larger fluctuations with a more discontinuous activity. Thermodynamically, conservative species use the resources more efficiently with less energy dissipation, obtaining greater benefit at the end of succession (Margalef, 1997). However, disturbances allow different strategies to occur simultaneously and to configure complementarily the communities. Mediterranean shrubland in the Prades mountains (Catalonia, north-east Spain) with many competing plant species coexisting in the same site, thus defying the competitive-exclusion principle. There are other drivers of niche segregation linked to the temporal axis. Species could coexist even in temporally and spatially homogeneous environments, because the mechanisms of coexistence differ throughout the developing stages of the species' life history (Nakashizuka, 2001). The so-called 'life history' basis for niche segregation considers the different developing stages of a species as well as the different species' life span and size. Obviously, the interactions of the 'habitat' with the 'fluctuation' and the 'life history' components geometrically increase the number of possible niches enhancing segregation. Variation at the individual scale further explains why large numbers of intensely competing species coexist (Clark, 2010). In any case, as the authors comment, their results emphasize the well-known importance of soil moisture and hydrology for structuring plant communities through space and time, which therefore has implications for the conservation of plant communities that now face changing hydrological conditions caused by water extraction and climate change (IPCC, 2007). These results should thus be considered not only in niche ecological studies trying to disentangle the conundrum of plant species coexistence, but also in the risk assessment of climate and environmental change impacts on species richness. Of course, the main message of this interesting and elegant study of Araya et al. is to remind us once more of the fundamental role of water availability in space and time to shape life in Earth. The research conducted by the authors is supported by the Spanish Government projects CGL2006-04025/BOS, CGC2010-17172 and Consolider Ingenio Montes (CSD2008-00040), by the European project NEU NITROEUROPE (GOCE017841), and by the Catalan Government project SGR 2009-458.