The native distribution of a common legume shrub is limited by the range of its nitrogen-fixing mutualist.

Plant-microbe mutualisms, such as the legume-rhizobium symbiosis, are influenced by the geographical distributions of both partners. However, limitations on the native range of legumes, resulting from the absence of a compatible mutualist, have rarely been explored. We used a combination of a large-scale field survey and controlled experiments to determine the realized niche of Calicotome villosa, an abundant and widespread legume shrub. Soil type was a major factor affecting the distribution and abundance of C. villosa. In addition, we found a large region within its range in which neither C. villosa nor Bradyrhizobium, the bacterial genus that associates with it, were present. Seedlings grown in soil from this region failed to nodulate and were deficient in nitrogen. Inoculation of this soil with Bradyrhizobium isolated from root nodules of C. villosa resulted in the formation of nodules and higher growth rate, leaf N and shoot biomass compared with un-inoculated plants. We present evidence for the exclusion of a legume from parts of its native range by the absence of a compatible mutualist. This result highlights the importance of the co-distribution of both the host plant and its mutualist when attempting to understand present and future geographical distributions of legumes.

Competition-induced downregulation of symbiotic nitrogen fixation.

Controlled experiments at the level of individual plants show that legume species use different strategies for the regulation of symbiotic dinitrogen fixation in response to nitrogen availability. These strategies were suggested to improve legume fitness in the context of the plant community, although rarely studied at this level. We evaluated how nitrogen availability and conspecific vs heterospecific interactions influenced the strategy of regulation of nitrogen fixation. We grew two species of herbaceous legumes representing two different strategies of regulation without interaction, under treatments of deficient and sufficient nitrogen availability, with conspecific or heterospecific interaction. We found that Hymenocarpus circinnatus maintained a facultative strategy of downregulating nitrogen fixation when nitrogen was available under both con- and heterospecific interactions, as was also found for this species when grown alone. Vicia palaestina also downregulated nitrogen fixation under both con- and heterospecific interactions but did not regulate fixation when grown alone. Our results showed that under nitrogen limitation, interaction with a neighboring plant reduced fitness, reflecting a competitive effect. Our findings suggest that when interacting with other plants, downregulation of nitrogen fixation is more likely, therefore reducing the energetic cost of fixation, and improving plant performance in competitive ecological communities, especially when nitrogen is available.

Responses of two Acacia species to drought suggest different water-use strategies, reflecting their topographic distribution.

Introduction: Soil water availability is a key factor in the growth of trees. In arid deserts, tree growth is limited by very dry soil and atmosphere conditions. Acacia tree species are distributed in the most arid deserts of the globe, therefore they are well adapted to heat and long droughts. Understanding why some plants do better than others in some environments is a key question in plant science. Methods: Here we conducted a greenhouse experiment to continuously and simultaneously track the whole-plant water-balance of two desert Acacia species, in order to unravel their physiological responses to low water availability. Results: We found that even under volumetric water content (VWC) of 5-9% in the soil, both species maintained 25% of the control plants, with a peak of canopy activity at noon. Moreover, plants exposed to the low water availability treatment continued growing in this period. A. tortilis applied a more opportunistic strategy than A. raddiana, and showed stomatal responses at a lower VWC (9.8% vs. 13.1%, t4= -4.23, p = 0.006), 2.2-fold higher growth, and faster recovery from drought stress. Discussion: Although the experiment was done in milder VPD (~3 kPa) compared to the natural conditions in the field (~5 kPa), the different physiological responses to drought between the two species might explain their different topographic distributions. A. tortilis is more abundant in elevated locations with larger fluctuations in water availability while A. raddiana is more abundant in the main channels with higher and less fluctuating water availability. This work shows a unique and non-trivial water-spending strategy in two Acacia species adapted to hyper-arid conditions.

Differential climatic conditions drive growth of Acacia tortilis tree in its range edges in Africa and Asia.

PREMISE: Tree growth is a fundamental biological process that is essential to ecosystem functioning and water and element cycling. Climate exerts a major impact on tree growth, with tree species often requiring a unique set of conditions to initiate and maintain growth throughout the growing season. Still, little is known about the specific climatic factors that enable tree growth in savannah and desert tree species. Among the global tree species, Acacia tortilis occupies one of the largest distribution ranges (crossing 6500 km and 54 latitudes), spanning large parts of Africa and into the Middle East and Asia. METHODS: Here we collected climate data and monitored Acacia tortilis tree growth (continuous measurements of stem circumference) in its southern and northern range edges in South Africa (SA) and Israel (IL), respectively, to elucidate whether the growth-climate interactions were similar in both edges. RESULTS: Growth occurred during the summer (between December and March) in SA and in IL during early summer and autumn (April-June and October-November, respectively). Surprisingly, annual growth was 40% higher in IL than in SA. Within the wide distribution range of Acacia tortilis, our statistical model showed that climatic drivers of tree growth differed between the two sites. CONCLUSIONS: High temperatures facilitated growth at the hot and arid IL site, while high humidity permitted growth at the more humid SA site. Our results confer an additional understanding of tree growth adaptation to extreme conditions in Acacia's world range edges, a major point of interest with ongoing climate change.

Dryland mechanisms could widely control ecosystem functioning in a drier and warmer world.

Responses of terrestrial ecosystems to climate change have been explored in many regions worldwide. While continued drying and warming may alter process rates and deteriorate the state and performance of ecosystems, it could also lead to more fundamental changes in the mechanisms governing ecosystem functioning. Here we argue that climate change will induce unprecedented shifts in these mechanisms in historically wetter climatic zones, towards mechanisms currently prevalent in dry regions, which we refer to as 'dryland mechanisms'. We discuss 12 dryland mechanisms affecting multiple processes of ecosystem functioning, including vegetation development, water flow, energy budget, carbon and nutrient cycling, plant production and organic matter decomposition. We then examine mostly rare examples of the operation of these mechanisms in non-dryland regions where they have been considered irrelevant at present. Current and future climate trends could force microclimatic conditions across thresholds and lead to the emergence of dryland mechanisms and their increasing control over ecosystem functioning in many biomes on Earth.

Biome boundary maintained by intense belowground resource competition in world's thinnest-rooted plant community.

Recent findings point to plant root traits as potentially important for shaping the boundaries of biomes and for maintaining the plant communities within. We examined two hypotheses: 1) Thin-rooted plant strategies might be favored in biomes with low soil resources; and 2) these strategies may act, along with fire, to maintain the sharp boundary between the Fynbos and Afrotemperate Forest biomes in South Africa. These biomes differ in biodiversity, plant traits, and physiognomy, yet exist as alternative stable states on the same geological substrate and in the same climate conditions. We conducted a 4-y field experiment to examine the ability of Forest species to invade the Fynbos as a function of growth-limiting nutrients and belowground plant-plant competition. Our results support both hypotheses: First, we found marked biome differences in root traits, with Fynbos species exhibiting the thinnest roots reported from any biome worldwide. Second, our field manipulation demonstrated that intense belowground competition inhibits the ability of Forest species to invade Fynbos. Nitrogen was unexpectedly the resource that determined competitive outcome, despite the long-standing expectation that Fynbos is severely phosphorus constrained. These findings identify a trait-by-resource feedback mechanism, in which most species possess adaptive traits that modify soil resources in favor of their own survival while deterring invading species. Our findings challenge the long-held notion that biome boundaries depend primarily on external abiotic constraints and, instead, identify an internal biotic mechanism-a selective feedback among traits, plant-plant competition, and ecosystem conditions-that, along with contrasting fire regime, can act to maintain biome boundaries.

The nitrogen economic spectrum of legume stoichiometry and fixation strategy.

Leaf nitrogen concentration often is higher in leguminous plants, which associate with dinitrogen-fixing bacteria, compared with nonlegume plants. However, the range of nitrogen concentrations in legumes is wide, likely related to the range of nitrogen fixation strategies. We evaluated how carbon and nitrogen allocation to roots, stems and leaves is influenced by the type of strategy of nitrogen fixation regulation. We grew herbaceous annual legumes (Medicago truncatula, Hymenocarpos circinnatus and Vicia palaestina) under two nitrogen availability treatments (none/sufficient), with and without bacterial inoculation. We found facultative downregulation of the rate of nitrogen fixation when nitrogen was available in H. circinnatus, and an obligate similar fixation rate in both nitrogen treatments in M. truncatula and V. palaestina. Uninoculated plants invested more biomass in roots and contained lower nitrogen concentrations. However, nitrogen concentration in the entire plant and in the leaves was lower and more plastic in the species with a facultative fixation strategy, whereas species with an obligate fixation strategy also maintained high nitrogen concentrations. Our results suggest a suite of functional traits associated with the strategies of allocation and symbiotic nitrogen fixation. This suite of traits probably shapes successional and functional niches of different leguminous species in specious plant communities.

Symbiotic dinitrogen fixation is seasonal and strongly regulated in water-limited environments.

Plants, especially perennials, growing in drylands and seasonally dry ecosystems are uniquely adapted to dry conditions. Legume shrubs and trees, capable of symbiotic dinitrogen (N2 ) fixation, often dominate in drylands. However, the strategies that allow symbiotic fixation in these ecosystems, and their influence on the nitrogen cycle, are largely unresolved. We evaluated the climatic, biogeochemical and ontogenetic factors influencing nitrogen fixation in an abundant Mediterranean legume shrub, Calicotome villosa. We measured nodulation, fixation rate, nitrogen allocation and soil biogeochemistry in three field sites over a full year. A controlled experiment evaluated differences in plant regulation of fixation as a function of soil nutrient availability and seedling and adult developmental stages. We found a strong seasonal pattern, shifting between high fixation rates during the rainy season at flowering and seed-set times to almost none in the rainless season. Under controlled conditions, plants downregulated fixation in response to soil nitrogen availability, but this response was stronger in seedlings than in adult shrubs. Finally, we did not find elevated soil nitrogen under N2 -fixing shrubs. We conclude that seasonal nitrogen fixation, regulation of fixation, and nitrogen conservation are key adaptations influencing the dominance of dryland legumes in the community, with broader consequences on the ecosystem nitrogen cycle.

A theoretical foundation for multi-scale regular vegetation patterns.

Self-organized regular vegetation patterns are widespread and thought to mediate ecosystem functions such as productivity and robustness, but the mechanisms underlying their origin and maintenance remain disputed. Particularly controversial are landscapes of overdispersed (evenly spaced) elements, such as North American Mima mounds, Brazilian murundus, South African heuweltjies, and, famously, Namibian fairy circles. Two competing hypotheses are currently debated. On the one hand, models of scale-dependent feedbacks, whereby plants facilitate neighbours while competing with distant individuals, can reproduce various regular patterns identified in satellite imagery. Owing to deep theoretical roots and apparent generality, scale-dependent feedbacks are widely viewed as a unifying and near-universal principle of regular-pattern formation despite scant empirical evidence. On the other hand, many overdispersed vegetation patterns worldwide have been attributed to subterranean ecosystem engineers such as termites, ants, and rodents. Although potentially consistent with territorial competition, this interpretation has been challenged theoretically and empirically and (unlike scale-dependent feedbacks) lacks a unifying dynamical theory, fuelling scepticism about its plausibility and generality. Here we provide a general theoretical foundation for self-organization of social-insect colonies, validated using data from four continents, which demonstrates that intraspecific competition between territorial animals can generate the large-scale hexagonal regularity of these patterns. However, this mechanism is not mutually exclusive with scale-dependent feedbacks. Using Namib Desert fairy circles as a case study, we present field data showing that these landscapes exhibit multi-scale patterning-previously undocumented in this system-that cannot be explained by either mechanism in isolation. These multi-scale patterns and other emergent properties, such as enhanced resistance to and recovery from drought, instead arise from dynamic interactions in our theoretical framework, which couples both mechanisms. The potentially global extent of animal-induced regularity in vegetation-which can modulate other patterning processes in functionally important ways-emphasizes the need to integrate multiple mechanisms of ecological self-organization.

Ecological feedbacks. Termite mounds can increase the robustness of dryland ecosystems to climatic change.

Self-organized spatial vegetation patterning is widespread and has been described using models of scale-dependent feedback between plants and water on homogeneous substrates. As rainfall decreases, these models yield a characteristic sequence of patterns with increasingly sparse vegetation, followed by sudden collapse to desert. Thus, the final, spot-like pattern may provide early warning for such catastrophic shifts. In many arid ecosystems, however, termite nests impart substrate heterogeneity by altering soil properties, thereby enhancing plant growth. We show that termite-induced heterogeneity interacts with scale-dependent feedbacks to produce vegetation patterns at different spatial grains. Although the coarse-grained patterning resembles that created by scale-dependent feedback alone, it does not indicate imminent desertification. Rather, mound-field landscapes are more robust to aridity, suggesting that termites may help stabilize ecosystems under global change.

Countervailing effects on pine and oak leaf litter decomposition in human-altered Mediterranean ecosystems.

Species affect the dynamics of litter decay through the intrinsic properties of their litter, but also by influencing the environmental conditions imposed by their canopy, roots, and litter layers. We examined how human-induced changes in the relative abundances of two dominant Mediterranean trees-Pinus halepensis and Quercus calliprinos-impact leaf litter decomposition. A reciprocal transplant experiment tested decomposition of pine, oak, and mixed leaf litter in oak woodland and pine forest ecosystems with different relative abundances of pine and oak. Using likelihood methods, we tested the importance and magnitude of the environmental effects of local species abundance, litter layer composition, and soil properties on litter mass loss. Oak litter decomposition was slower than pine, and had an antagonistic effect on mixed litter decay. These results differ from other reported pine-oak associations, and are probably associated with a higher content of tannins and phenols in oak compared to pine litter in our study sites. The environmental effects of the two species were opposite to their litter decomposition dynamics. An increased proportion of pine in the oak woodlands and a higher content of pine needles in the litter layer of pine forests reduced decay rates. The presence of more oak and broadleaf litter in the litter layer accelerated decomposition in pine forests. Our results highlight the importance of considering multidimensional species effects mediated by both chemical and physical properties, and imply that man-made changes in the composition and configuration of plant communities may result in complex unpredicted consequences to ecosystem biogeochemistry.

Biome-scale nitrogen fixation strategies selected by climatic constraints on nitrogen cycle.

Dinitrogen fixation by plants (in symbiosis with root bacteria) is a major source of new nitrogen for land ecosystems(1). A long-standing puzzle(2) is that trees capable of nitrogen fixation are abundant in nitrogen-rich tropical forests, but absent or restricted to early successional stages in nitrogen-poor extra-tropical forests. This biome-scale pattern presents an evolutionary paradox(3), given that the physiological cost(4) of nitrogen fixation predicts the opposite pattern: fixers should be out-competed by non-fixers in nitrogen-rich conditions, but competitively superior in nitrogen-poor soils. Here we evaluate whether this paradox can be explained by the existence of different fixation strategies in tropical versus extra-tropical trees: facultative fixers (capable of downregulating fixation(5,6) by sanctioning mutualistic bacteria(7)) are common in the tropics, whereas obligate fixers (less able to downregulate fixation) dominate at higher latitudes. Using a game-theoretic approach, we assess the ecological and evolutionary conditions under which these fixation strategies emerge, and examine their dependence on climate-driven differences in the nitrogen cycle. We show that in the tropics, transient soil nitrogen deficits following disturbance and rapid tree growth favour a facultative strategy and the coexistence of fixers and non-fixers. In contrast, sustained nitrogen deficits following disturbance in extra-tropical forests favour an obligate fixation strategy, and cause fixers to be excluded in late successional stages. We conclude that biome-scale differences in the abundance of nitrogen fixers can be explained by the interaction between individual plant strategies and climatic constraints on the nitrogen cycle over evolutionary time.

An integrative analysis of the dynamics of landscape- and local-scale colonization of Mediterranean woodlands by Pinus halepensis.

Afforestation efforts have resulted in extensive plantations of either native or non-native conifers, which in many regions has led to the spread of those conifers into surrounding natural vegetation. This process of species colonization can trigger profound changes in both community dynamics and ecosystem processes. Our study disentangled the complexity of a process of colonization in a heterogeneous landscape into a simple set of rules. We analyzed the factors that control the colonization of natural woodland ecosystems by Pinus halepensis dispersing from plantations in the Mediterranean region of Israel. We developed maximum-likelihood models to explain the densities of P. halepensis colonizing natural woodlands. Our models unravel how P. halepensis colonization is controlled by factors that determine colonization pressure by dispersing seeds and by factors that control resistance to colonization of the natural ecosystems. Our models show that the combination of different seed arrival processes from local, landscape, and regional scales determine pine establishment potential, but the relative importance of each component varied according to seed source distribution. Habitat resistance, determined by abiotic and biotic conditions, was as important as propagule input in determining the density of pine colonization. Thus, despite the fact that pine propagules disperse throughout the landscape, habitat heterogeneity within the natural ecosystems generates significant variation in the actual densities of colonized pine. Our approach provides quantitative measures of how processes at different spatial scales affect the distribution and densities of colonizing species, and a basis for projection of expected distributions. Variation in colonization rates, due to landscape-scale heterogeneity in both colonization pressure and resistance to colonization, can be expected to produce a diversity of new ecosystems. This work provides a template for understanding species colonization processes, especially in light of anthropogenic impacts, and predicting future transformation of natural ecosystems by species invasion.

Landscape-scale density-dependent recruitment of oaks in planted forests: more is not always better.

Plant colonization studies usually address density-dependent processes in the narrow sense of recruitment constraints due to negative density-dependent seed and seedling mortality. However, complex density-dependent effects may be involved in additional stages of the recruitment process. We hypothesized that seed arrival and seedling establishment are influenced by density dependence acting at small scales at the site of colonization, and at larger scales as a function of the colonizing species' landscape abundance. These hypotheses were tested in a study of colonization of pine forests by oaks in a heterogeneous Mediterranean landscape. Maximum-likelihood models show that density effects switch from positive to negative along the range of landscape-scale oak seed source abundance. Contrary to expectations, high seed source densities limited oak recruitment, suggesting a landscape-scale Janzen-Connell effect. We propose a range of mechanisms that generate positive or negative density dependence during colonization, resulting in nonlinear density-dependent feedbacks that can generate unexpected colonization patterns.

Emerged or imposed: a theory on the role of physical templates and self-organisation for vegetation patchiness.

In this article, we develop a unifying framework for the understanding of spatial vegetation patterns in heterogeneous landscapes. While much recent research has focused on self-organised vegetation the prevailing view is still that biological patchiness is mostly due to top-down control by the physical landscape template, disturbances or predators. We suggest that vegetation patchiness in real landscapes is controlled both by the physical template and by self-organisation simultaneously, and introduce a conceptual model for the relative roles of the two mechanisms. The model considers four factors that control whether vegetation patchiness is emerged or imposed: soil patch size, plant size, resource input and resource availability. The last three factors determine the plant-patch size, and the plant-to-soil patch size ratio determines the impact of self-organisation, which becomes important when this ratio is sufficiently small. A field study and numerical simulations of a mathematical model support the conceptual model and give further insight by providing examples of self-organised and template-controlled vegetation patterns co-occurring in the same landscape. We conclude that real landscapes are generally mixtures of template-induced and self-organised patchiness. Patchiness variability increases due to source-sink resource relations, and decreases for species of larger patch sizes.

Mechanisms of vegetation-ring formation in water-limited systems.

A common patch form in dryland landscapes is the vegetation ring. Vegetation patch formation has recently been attributed to self-organization processes that act to increase the availability of water to vegetation patches under conditions of water scarcity. The view of ring formation as a water-limited process, however, has remained largely unexplored. Using laboratory experiments and model studies we identify two distinct mechanisms of ring formation. The first mechanism pertains to conditions of high infiltration contrast between vegetated and bare soil, under which overland water flow is intercepted at the patch periphery. The decreasing amount of water that the patch core receives as the patch expands, leads to central dieback and ring formation. The second mechanism pertains to plants with large lateral root zones, and involves central dieback and ring formation due to increasing water uptake by the newly recruited individuals at the patch periphery. In general the two mechanisms act in concert, but the relative importance of each mechanism depends on environmental conditions. We found that strong seasonal rainfall variability favors ring formation by the overland-flow mechanism, while a uniform rainfall regime favors ring formation by the water-uptake mechanism. Our results explain the formation of rings by fast-growing species with confined root zones in a dry-Mediterranean climate, such as Poa bulbosa. They also explain the formation of rings by slowly growing species with highly extended root zones, such as Larrea tridentata (Creosotebush).