Leaf carbon isotope tracks the facilitation pattern of legume shrubs shaped by water availability and species replacement along a large elevation gradient in Trans-Himalayas.

BACKGROUND AND AIMS: Understanding patterns and mechanisms of nurse plant facilitation is important to predict the resilience of arid/semi-arid ecosystems to climate change. We investigate whether water availability and nurse species turnover interact to shape the facilitation pattern of widespread legume shrubs along a large elevation gradient. We also investigate whether leaf δ13C of nurse plants can track the facilitation pattern. METHODS: We measured the relative interaction index (RII) of the number of species within and outside the canopy of two widespread legume shrub species (Caragana gerardiana and Caragana versicolor) alternatively distributed along a large elevation gradient in the Trans-Himalayas. We also assessed the proportional increase of species richness (ISR) at the community level using the paired plot data. To determine site-specific water availability, we measured the leaf δ13C of nurse shrubs and calculated the Thornthwaite moisture index (MI) for each elevation site. KEY RESULTS: Elevational variations in RII, ISR and δ13C were mainly explained by the MI when the effects of soil nitrogen and plant traits (leaf nitrogen and shrub size) were controlled. Variations in RII and ISR across the two nurse species were explained better by δ13C than by smoothly changing climatic factors along elevation. At the transition zone between the upper limit of C. gerardiana (4100 m) and the lower limit of C. versicolor (4200 m), RII and ISR were much higher in C. versicolor than in C. gerardiana under a similar MI. Such an abrupt increase in facilitation induced by nurse species replacement was well tracked by the variation of δ13C. CONCLUSIONS: Water availability and nurse species replacement are crucial to shaping facilitation patterns by legume shrubs along a large elevation gradient in dry mountainous regions, such as the Trans-Himalayas. Turnover in nurse species under global change might significantly alter the pattern of nurse plant facilitation associated with water availability, which can be well tracked by leaf δ13C.

Shrub-mediated effects on soil nitrogen determines shrub-herbaceous interactions in drylands of the Tibetan Plateau.

Introduction: Shrub promotes the survival, growth and reproduction of understory species by buffering the environmental extremes and improving limited resources (i.e., facilitation effect) in arid and semiarid regions. However, the importance of soil water and nutrient availability on shrub facilitation, and its trend along a drought gradient have been relatively less addressed in water-limited systems. Methods: We investigated species richness, plant size, soil total nitrogen and dominant grass leaf δ13C within and outside the dominant leguminous cushion-like shrub Caragana versicolor along a water deficit gradient in drylands of Tibetan Plateau. Results: We found that C. versicolor increased grass species richness but had a negative effect on annual and perennial forbs. Along the water deficit gradient, plant interaction assessed by species richness (RIIspecies) showed a unimodal pattern with shift from increase to decrease, while plant interaction assessed by plant size (RIIsize) did not vary significantly. The effect of C. versicolor on soil nitrogen, rather than water availability, determined its overall effect on understory species richness. Neither the effect of C. versicolor on soil nitrogen nor water availability affected plant size. Discussion: Our study suggests that the drying tendency in association with the recent warming trends observed in drylands of Tibetan Plateau, will likely hinder the facilitation effect of nurse leguminous shrub on understories if moisture availability crosses a critical minimum threshold.

Higher leaf nitrogen content is linked to tighter stomatal regulation of transpiration and more efficient water use across dryland trees.

The least-cost economic theory of photosynthesis shows that water and nitrogen are mutually substitutable resources to achieve a given carbon gain. However, vegetation in the Sahel has to cope with the dual challenge imposed by drought and nutrient-poor soils. We addressed how variation in leaf nitrogen per area (Narea ) modulates leaf oxygen and carbon isotopic composition (δ18 O, δ13 C), as proxies of stomatal conductance and water-use efficiency, across 34 Sahelian woody species. Dryland species exhibited diverging leaf δ18 O and δ13 C values, indicating large interspecific variation in time-integrated stomatal conductance and water-use efficiency. Structural equation modeling revealed that leaf Narea is a pivotal trait linked to multiple water-use traits. Leaf Narea was positively linked to both δ18 O and δ13 C, suggesting higher carboxylation capacity and tighter stomatal regulation of transpiration in N-rich species, which allows them to achieve higher water-use efficiency and more conservative water use. These adaptations represent a key physiological advantage of N-rich species, such as legumes, that could contribute to their dominance across many dryland regions. This is the first report of a robust mechanistic link between leaf Narea and δ18 O in dryland vegetation that is consistent with core principles of plant physiology.

Network motifs involving both competition and facilitation predict biodiversity in alpine plant communities.

Biological diversity depends on multiple, cooccurring ecological interactions. However, most studies focus on one interaction type at a time, leaving community ecologists unsure of how positive and negative associations among species combine to influence biodiversity patterns. Using surveys of plant populations in alpine communities worldwide, we explore patterns of positive and negative associations among triads of species (modules) and their relationship to local biodiversity. Three modules, each incorporating both positive and negative associations, were overrepresented, thus acting as "network motifs." Furthermore, the overrepresentation of these network motifs is positively linked to species diversity globally. A theoretical model illustrates that these network motifs, based on competition between facilitated species or facilitation between inferior competitors, increase local persistence. Our findings suggest that the interplay of competition and facilitation is crucial for maintaining biodiversity.

Co-ordination between xylem anatomy, plant architecture and leaf functional traits in response to abiotic and biotic drivers in a nurse cushion plant.

BACKGROUND AND AIMS: Plants in dry Mediterranean mountains experience a double climatic stress: at low elevations, high temperatures coincide with water shortage during summer, while at high elevations temperature decreases and water availability increases. Cushion plants often act as nurses by improving the microclimate underneath their canopies, hosting beneficiary species that may reciprocally modify their benefactors' microenvironment. We assess how the nurse cushion plant Arenaria tetraquetra subsp. amabilis adjusts its hydraulic system to face these complex abiotic and biotic constraints. METHODS: We evaluated intra-specific variation and co-ordination of stem xylem anatomy, leaf functional traits and plant architecture in response to elevation, aspect and the presence of beneficiary species in four A. tetraquetra subsp. amabilis populations in the Sierra Nevada mountains, southern Spain. KEY RESULTS: Xylem anatomical and plant architectural traits were the most responsive to environmental conditions, showing the highest mutual co-ordination. Cushions were more compact and had smaller, more isolated conductive vessels in the southern than in the northern aspect, which allow minimization of the negative impacts of more intense drought. Only vessel size, leaf mass per area and terminal branch length varied with elevation. Nurse cushions co-ordinated plant architecture and xylem traits, having higher canopy compactness, fewer leaves per branch and fewer, more isolated vessels than non-nurse cushions, which reflects the negative effects of beneficiary plants on nurse water status. In non-nurse cushions, plant architecture co-ordinated with leaf traits instead. The interacting effects of aspect and elevation on xylem traits showed that stress due to frost at high elevation constrained xylem anatomy in the north, whereas stress due to drought had a parallel effect in the south. CONCLUSIONS: Trait co-ordination was weaker under more demanding environmental conditions, which agrees with the hypothesis that trait independence allows plants to better optimize different functions, probably entailing higher adjustment potential against future environmental changes.

Climate change effects on plant-soil feedbacks and consequences for biodiversity and functioning of terrestrial ecosystems.

Plant-soil feedbacks (PSFs) are interactions among plants, soil organisms, and abiotic soil conditions that influence plant performance, plant species diversity, and community structure, ultimately driving ecosystem processes. We review how climate change will alter PSFs and their potential consequences for ecosystem functioning. Climate change influences PSFs through the performance of interacting species and altered community composition resulting from changes in species distributions. Climate change thus affects plant inputs into the soil subsystem via litter and rhizodeposits and alters the composition of the living plant roots with which mutualistic symbionts, decomposers, and their natural enemies interact. Many of these plant-soil interactions are species-specific and are greatly affected by temperature, moisture, and other climate-related factors. We make a number of predictions concerning climate change effects on PSFs and consequences for vegetation-soil-climate feedbacks while acknowledging that they may be context-dependent, spatially heterogeneous, and temporally variable.

Facilitation influences patterns of perennial species abundance and richness in a subtropical dune system.

Positive interactions in plant communities are under-reported in subtropical systems most likely because they are not identified as stressful environments. However, environmental factors or disturbance can limit plant growth in any system and lead to stressful conditions. For instance, salinity and low nutrient and water availability generate a gradient of stressful conditions in coastal systems depending on distance to shore. In a tropical coastal system in SE Brazil, we aimed to assess whether Guapira opposita, a shrub common in restinga environments, acted as nurse involved in ecological succession and which factors influenced its facilitation process. We sampled perennial species above 10 cm in height under the canopy of 35 G. opposita individuals and in neighbouring open areas. Shrub height, canopy area and distance to freshwater bodies were measured in the field, and distance to the ocean was obtained from aerial images. In addition, we measured the distance to the closest forest patch as a potential source of seeds. Plant abundance and species richness were higher under the canopy of G. opposita than in open areas. Facilitation by G. opposita was mainly determined by shrub height, which had a positive relationship with woody and bromeliads abundance and species richness while there was no relationship with the other factors. Overall, our data evidence that tropical environments may be highly stressful for plants and that nurse species play a key role in the regeneration of restinga environments, where their presence is critical to maintain ecosystem diversity and function.

Symbiotic soil fungi enhance ecosystem resilience to climate change.

Substantial amounts of nutrients are lost from soils through leaching. These losses can be environmentally damaging, causing groundwater eutrophication and also comprise an economic burden in terms of lost agricultural production. More intense precipitation events caused by climate change will likely aggravate this problem. So far it is unresolved to which extent soil biota can make ecosystems more resilient to climate change and reduce nutrient leaching losses when rainfall intensity increases. In this study, we focused on arbuscular mycorrhizal (AM) fungi, common soil fungi that form symbiotic associations with most land plants and which increase plant nutrient uptake. We hypothesized that AM fungi mitigate nutrient losses following intensive precipitation events (higher amount of precipitation and rain events frequency). To test this, we manipulated the presence of AM fungi in model grassland communities subjected to two rainfall scenarios: moderate and high rainfall intensity. The total amount of nutrients lost through leaching increased substantially with higher rainfall intensity. The presence of AM fungi reduced phosphorus losses by 50% under both rainfall scenarios and nitrogen losses by 40% under high rainfall intensity. Thus, the presence of AM fungi enhanced the nutrient interception ability of soils, and AM fungi reduced the nutrient leaching risk when rainfall intensity increases. These findings are especially relevant in areas with high rainfall intensity (e.g., such as the tropics) and for ecosystems that will experience increased rainfall due to climate change. Overall, this work demonstrates that soil biota such as AM fungi can enhance ecosystem resilience and reduce the negative impact of increased precipitation on nutrient losses.

The shift from plant-plant facilitation to competition under severe water deficit is spatially explicit.

The stress-gradient hypothesis predicts a higher frequency of facilitative interactions as resource limitation increases. Under severe resource limitation, it has been suggested that facilitation may revert to competition, and identifying the presence as well as determining the magnitude of this shift is important for predicting the effect of climate change on biodiversity and plant community dynamics. In this study, we perform a meta-analysis to compare temporal differences of species diversity and productivity under a nurse plant (Retama sphaerocarpa) with varying annual rainfall quantity to test the effect of water limitation on facilitation. Furthermore, we assess spatial differences in the herbaceous community under nurse plants in situ during a year with below-average rainfall. We found evidence that severe rainfall deficit reduced species diversity and plant productivity under nurse plants relative to open areas. Our results indicate that the switch from facilitation to competition in response to rainfall quantity is nonlinear. The magnitude of this switch depended on the aspect around the nurse plant. Hotter south aspects under nurse plants resulted in negative effects on beneficiary species, while the north aspect still showed facilitation. Combined, these results emphasize the importance of spatial heterogeneity under nurse plants for mediating species loss under reduced precipitation, as predicted by future climate change scenarios. However, the decreased water availability expected under climate change will likely reduce overall facilitation and limit the role of nurse plants as refugia, amplifying biodiversity loss.

Disentangling above- and below-ground facilitation drivers in arid environments: the role of soil microorganisms, soil properties and microhabitat.

Nurse plants promote establishment of other plant species by buffering climate extremes and improving soil properties. Soil biota plays an important role, but an analysis to disentangle the effects of soil microorganisms, soil properties and microclimate on facilitation is lacking. In three microhabitats (gaps, small and large Retama shrubs), we placed six microcosms with sterilized soil, two per soil origin (i.e. from each microhabitat). One in every pair received an alive, and the other a sterile, inoculum from its own soil. Seeds of annual plants were sown into the microcosms. Germination, survival and biomass were monitored. Soil bacterial communities were characterized by pyrosequencing. Germination in living Retama inoculum was nearly double that of germination in sterile inoculum. Germination was greater under Retama canopies than in gaps. Biomass was up to three times higher in nurse than in gap soils. Soil microorganisms, soil properties and microclimate showed a range of positive to negative effects on understory plants depending on species identity and life stage. Nurse soil microorganisms promoted germination, but the effect was smaller than the positive effects of soil properties and microclimate under nurses. Nurse below-ground environment (soil properties and microorganisms) promoted plant growth and survival more than nurse microhabitat.

Functional Plant Types Drive Plant Interactions in a Mediterranean Mountain Range.

Shrubs have positive (facilitation) and negative (competition) effects on understory plants, the net interaction effect being modulated by abiotic conditions. Overall shrubs influence to great extent the structure of plant communities where they have significant presence. Interactions in a plant community are quite diverse but little is known about their variability and effects at community level. Here we checked the effects of co-occurring shrub species from different functional types on a focal understory species, determining mechanisms driving interaction outcome, and tested whether effects measured on the focal species were a proxy for effects measured at the community level. Growth, physiological, and reproductive traits of Euphorbia nicaeensis, our focal species, were recorded on individuals growing in association with four dominant shrub species and in adjacent open areas. We also recorded community composition and environmental conditions in each microhabitat. Shrubs provided environmental conditions for plant growth, which contrasted with open areas, including moister soil, greater N content, higher air temperatures, and lower radiation. Shrub-associated individuals showed lower reproductive effort and greater allocation to growth, while most physiological traits remained unaffected. Euphorbia individuals were bigger and had more leaf N under N-fixing than under non-fixing species. Soil moisture was also higher under N-fixing shrubs; therefore soil conditions in the understory may counter reduced light conditions. There was a significant effect of species identity and functional types in the outcome of plant interactions with consistent effects at individual and community levels. The contrasting allocation strategies to reproduction and growth in Euphorbia plants, either associated or not with shrubs, showed high phenotypic plasticity and evidence its ability to cope with contrasting environmental conditions.

Mutual positive effects between shrubs in an arid ecosystem.

One-way facilitation in plants has been found in many harsh environments and their role as structural forces governing species composition in plant communities is now well established. However, reciprocal positive effects benefiting two interacting species have seldom been reported and, in recent reviews, conceptually considered merely as facilitation when in fact there is room for adaptive strategies and evolutionary responses. We tested the existence of such reciprocal positive effects in an arid environment in SE Spain using spatial pattern analysis, a species removal experiment, and a natural experiment. We found that the spatial association between Maytenus senegalensis and Whitania frutescens, two shrub species of roughly similar size intimately interacting in our community, resulted in mutual benefit for both species. Benefits included improved water relations and nutritional status and protection against browsing, and did occur despite simultaneous competition for resources. Our data suggest two-way facilitation or, rather, a facultative mutualism among higher plant species, a process often overlooked which could be a main driver of plant community dynamics allowing for evolutionary processes.

The effects of foundation species on community assembly: a global study on alpine cushion plant communities.

Foundation species can change plant community structure by modulating important ecological processes such as community assembly, yet this topic is poorly understood. In alpine systems, cushion plants commonly act as foundation species by ameliorating local conditions. Here, we analyze diversity patterns of species' assembly within cushions and in adjacent surrounding open substrates (83 sites across five continents) calculating floristic dissimilarity between replicate plots, and using linear models to analyze relationships between microhabitats and species diversity. Floristic dissimilarity did not change across biogeographic regions, but was consistently lower in the cushions than in the open microhabitat. Cushion plants appear to enable recruitment of many relatively stress-intolerant species that otherwise would not establish in these communities, yet the niche space constructed by cushion plants supports a more homogeneous composition of species than the niche space beyond the cushion's influence. As a result, cushion plants support higher α-diversity and a larger species pool, but harbor assemblies with lower ß-diversity than open microhabitats. We conclude that habitats with and without dominant foundation species can strongly differ in the processes that drive species recruitment, and thus the relationship between local and regional species diversity.

The context dependence of beneficiary feedback effects on benefactors in plant facilitation.

Facilitative effects of some species on others are a major driver of biodiversity. These positive effects of a benefactor on its beneficiary can result in negative feedback effects of the beneficiary on the benefactor and reduced fitness of the benefactor. However, in contrast to the wealth of studies on facilitative effects in different environments, we know little about whether the feedback effects show predictable patterns of context dependence. We reanalyzed a global data set on alpine cushion plants, previously used to assess their positive effects on biodiversity and the nature of the beneficiary feedback effects, to specifically assess the context dependence of how small- and large-scale drivers alter the feedback effects of cushion-associated (beneficiary) species on their cushion benefactors using structural equation modelling. The effect of beneficiaries on cushions became negative when beneficiary diversity increased and facilitation was more intense. Local-scale biotic and climatic conditions mediated these community-scale processes, having indirect effects on the feedback effect. High-productivity sites demonstrated weaker negative feedback effects of beneficiaries on the benefactor. Our results indicate a limited impact of the beneficiary feedback effects on benefactor cushions, but strong context dependence. This context dependence may help to explain the ecological and evolutionary persistence of this widespread facilitative system.

Facilitative plant interactions and climate simultaneously drive alpine plant diversity.

Interactions among species determine local-scale diversity, but local interactions are thought to have minor effects at larger scales. However, quantitative comparisons of the importance of biotic interactions relative to other drivers are rarely made at larger scales. Using a data set spanning 78 sites and five continents, we assessed the relative importance of biotic interactions and climate in determining plant diversity in alpine ecosystems dominated by nurse-plant cushion species. Climate variables related with water balance showed the highest correlation with richness at the global scale. Strikingly, although the effect of cushion species on diversity was lower than that of climate, its contribution was still substantial. In particular, cushion species enhanced species richness more in systems with inherently impoverished local diversity. Nurse species appear to act as a 'safety net' sustaining diversity under harsh conditions, demonstrating that climate and species interactions should be integrated when predicting future biodiversity effects of climate change.

A global analysis of bidirectional interactions in alpine plant communities shows facilitators experiencing strong reciprocal fitness costs.

Facilitative interactions are defined as positive effects of one species on another, but bidirectional feedbacks may be positive, neutral, or negative. Understanding the bidirectional nature of these interactions is a fundamental prerequisite for the assessment of the potential evolutionary consequences of facilitation. In a global study combining observational and experimental approaches, we quantified the impact of the cover and richness of species associated with alpine cushion plants on reproductive traits of the benefactor cushions. We found a decline in cushion seed production with increasing cover of cushion-associated species, indicating that being a benefactor came at an overall cost. The effect of cushion-associated species was negative for flower density and seed set of cushions, but not for fruit set and seed quality. Richness of cushion-associated species had positive effects on seed density and modulated the effects of their abundance on flower density and fruit set, indicating that the costs and benefits of harboring associated species depend on the composition of the plant assemblage. Our study demonstrates 'parasitic' interactions among plants over a wide range of species and environments in alpine systems, and we consider their implications for the possible selective effects of interactions between benefactor and beneficiary species.

Water uptake and redistribution during drought in a semiarid shrub species.

In arid systems, most plant mortality occurs during long drought periods when water is not available for plant uptake. In these systems, plants often benefit from scarce rain events occurring during drought but some of the mechanisms underlying this water use remain unknown. In this context, plant water use and redistribution after a large rain event could be a mechanism that allows deep-rooted shrubs to conservatively use water during drought. We tested this hypothesis by comparing soil and plant water dynamics in Artemisia tridentata ssp. vaseyana (Rydb.) Beetle shrubs that either received a rain event (20mm) or received no water. Soil water content (SWC) increased in shallow layers after the event and increased in deep soil layers through hydraulic redistribution (HR). Our results show that Artemisia shrubs effectively redistributed the water pulse downward recharging deep soil water pools that allowed greater plant water use throughout the subsequent drought period, which ameliorated plant water potentials. Shrubs used shallow water pools when available and then gradually shifted to deep-water pools when shallow water was being used up. Both HR recharge and the shift to shallow soil water use helped conserve deep soil water pools. Summer water uptake in Artemisia not only improved plant water relations but also increased deep soil water availability during drought.

Trade-offs between maintenance of ecosystem services and socio-economic development in rural mountainous communities in southern Spain: a dynamic simulation approach.

Mountainous rural communities have traditionally managed their land extensively, resulting in land uses that provide important ecosystem services for both rural and urban areas. Over recent decades, these communities have undergone drastic changes in economic structure, population size and land use. Our understanding of the exact mechanisms that drive these changes is limited, and there is also a lack of integrative approaches to enable decision makers to steer rural development towards a more sustainable path. In this study, we build a dynamic simulation model to calculate the trade-offs between the provisions of two ecosystem services - landscape aesthetic value and water supply for human use - and the economic development associated with different land use changes. The study area for the simulation comprises two rural communities located in southern Spain. Our results show trade-offs between economic development and the provision of the selected ecosystem services in the selected study area. Land use intensification results in economic development but is not enough to prevent population loss and has a negative impact on both the water supply and on aesthetic services. We conclude that more proactive management policies are needed to mitigate a loss in ecosystem services. Simulation models like ours may facilitate the choice of these policies, as they could test the result of land use planning policies contributing therefore, to a more integrative and sustainable management of rural communities.

Foundation species influence trait-based community assembly.

Here, we incorporate facilitation into trait-based community assembly theory by testing two mutually compatible facilitative mechanisms: changes in the environmental filter, causing either an increase in the range of trait values (i.e. a range expansion effect) and/or a shift in trait distributions (i.e. a range shift effect); and changes in trait spacing, suggesting an effect on niche differentiation. We analyzed the distribution of three functional traits - leaf dry matter content, specific leaf area and lateral spread - of plant communities dominated by a cushion-forming foundation species at four sites differing in elevation and aspect. We found support for environmental filtering and niche differentiation mechanisms by cushions, with filtering effects (in particular range shifts) increasing with environmental severity at higher elevation. The effect size of cushions on trait distribution was similar to that of environmental gradients caused by elevation and aspect. The consideration of intraspecific trait variability improved the detection of cushion effects on trait distributions. Our results highlight the importance of facilitation in the modification of taxonomic and functional diversity of ecological communities, and indicate that facilitation can occur through combined effects on environmental filtering and niche differentiation, with strong environmental context dependence of each mechanism.

Water release through plant roots: new insights into its consequences at the plant and ecosystem level.

Hydraulic redistribution (HR) is the passive movement of water between different soil parts via plant root systems, driven by water potential gradients in the soil-plant interface. New data suggest that HR is a heterogeneous and patchy process. In this review we examine the main biophysical and environmental factors controlling HR and its main implications at the plant, community and ecosystem levels. Experimental evidence and the use of novel modelling approaches suggest that HR may have important implications at the community scale, affecting net primary productivity as well as water and vegetation dynamics. Globally, HR may influence hydrological and biogeochemical cycles and, ultimately, climate.