Hotspots of biogeochemical activity linked to aridity and plant traits across global drylands.

Perennial plants create productive and biodiverse hotspots, known as fertile islands, beneath their canopies. These hotspots largely determine the structure and functioning of drylands worldwide. Despite their ubiquity, the factors controlling fertile islands under conditions of contrasting grazing by livestock, the most prevalent land use in drylands, remain virtually unknown. Here we evaluated the relative importance of grazing pressure and herbivore type, climate and plant functional traits on 24 soil physical and chemical attributes that represent proxies of key ecosystem services related to decomposition, soil fertility, and soil and water conservation. To do this, we conducted a standardized global survey of 288 plots at 88 sites in 25 countries worldwide. We show that aridity and plant traits are the major factors associated with the magnitude of plant effects on fertile islands in grazed drylands worldwide. Grazing pressure had little influence on the capacity of plants to support fertile islands. Taller and wider shrubs and grasses supported stronger island effects. Stable and functional soils tended to be linked to species-rich sites with taller plants. Together, our findings dispel the notion that grazing pressure or herbivore type are linked to the formation or intensification of fertile islands in drylands. Rather, our study suggests that changes in aridity, and processes that alter island identity and therefore plant traits, will have marked effects on how perennial plants support and maintain the functioning of drylands in a more arid and grazed world.

Intransitivity in plant-soil feedbacks is rare but is associated with multispecies coexistence.

Although plant-soil feedback (PSF) is being recognized as an important driver of plant recruitment, our understanding of its role in species coexistence in natural communities remains limited by the scarcity of experimental studies on multispecies assemblages. Here, we experimentally estimated PSFs affecting seedling recruitment in 10 co-occurring Mediterranean woody species. We estimated weak but significant species-specific feedback. Pairwise PSFs impose similarly strong fitness differences and stabilizing-destabilizing forces, most often impeding species coexistence. Moreover, a model of community dynamics driven exclusively by PSFs suggests that few species would coexist stably, the largest assemblage with no more than six species. Thus, PSFs alone do not suffice to explain coexistence in the studied community. A topological analysis of all subcommunities in the interaction network shows that full intransitivity (with all species involved in an intransitive loop) would be rare but it would lead to species coexistence through either stable or cyclic dynamics.

Plant canopies promote climatic disequilibrium in Mediterranean recruit communities.

Current rates of climate change are exceeding the capacity of many plant species to track climate, thus leading communities to be in disequilibrium with climatic conditions. Plant canopies can contribute to this disequilibrium by buffering macro-climatic conditions and sheltering poorly adapted species to the oncoming climate, particularly in their recruitment stages. Here we analyse differences in climatic disequilibrium between understorey and open ground woody plant recruits in 28 localities, covering more than 100,000 m2 , across an elevation range embedding temperature and aridity gradients in the southern Iberian Peninsula. This study demonstrates higher climatic disequilibrium under canopies compared with open ground, supporting that plant canopies would affect future community climatic lags by allowing the recruitment of less arid-adapted species in warm and dry conditions, but also it endorse that canopies could favour warm-adapted species in extremely cold environments as mountain tops, thus pre-adapting communities living in these habitats to climate change.

Transitivity and intransitivity in soil bacterial networks.

Competition can lead to the exclusion of bacterial taxa when there is a transitive relationship among competitors with a hierarchy of competitive success. However, competition may not prevent bacterial coexistence if competitors form intransitive loops, in which none is able to outcompete all the rest. Both transitive and intransitive competition have been demonstrated in bacterial model systems. However, in natural soil microbial assemblages competition is typically understood as a dominance relationship leading to the exclusion of weak competitors. Here, we argue that transitive and intransitive interactions concurrently determine the structure of soil microbial communities. We explain why pairwise interactions cannot depict competition correctly in complex communities, and propose an alternative through the detection of strongly connected components (SCCs) in microbial networks. We finally analyse the existence of SCCs in soil bacterial communities in two Mediterranean ecosystems, for illustrative purposes only (rather than with the aim of providing a methodological tool) due to current limitations, and discuss future avenues to experimentally test the existence of SCCs in nature.

RecruitNet: A global database of plant recruitment networks.

Plant recruitment interactions (i.e., what recruits under what) shape the composition, diversity, and structure of plant communities. Despite the huge body of knowledge on the mechanisms underlying recruitment interactions among species, we still know little about the structure of the recruitment networks emerging in ecological communities. Modeling and analyzing the community-level structure of plant recruitment interactions as a complex network can provide relevant information on ecological and evolutionary processes acting both at the species and ecosystem levels. We report a data set containing 143 plant recruitment networks in 23 countries across five continents, including temperate and tropical ecosystems. Each network identifies the species under which another species recruits. All networks report the number of recruits (i.e., individuals) per species. The data set includes >850,000 recruiting individuals involved in 118,411 paired interactions among 3318 vascular plant species across the globe. The cover of canopy species and open ground is also provided. Three sampling protocols were used: (1) The Recruitment Network (RN) protocol (106 networks) focuses on interactions among established plants ("canopy species") and plants in their early stages of recruitment ("recruit species"). A series of plots was delimited within a locality, and all the individuals recruiting and their canopy species were identified; (2) The paired Canopy-Open (pCO) protocol (26 networks) consists in locating a potential canopy plant and identifying recruiting individuals under the canopy and in a nearby open space of the same area; (3) The Georeferenced plot (GP) protocol (11 networks) consists in using information from georeferenced individual plants in large plots to infer canopy-recruit interactions. Some networks incorporate data for both herbs and woody species, whereas others focus exclusively on woody species. The location of each study site, geographical coordinates, country, locality, responsible author, sampling dates, sampling method, and life habits of both canopy and recruit species are provided. This database will allow researchers to test ecological, biogeographical, and evolutionary hypotheses related to plant recruitment interactions. There are no copyright restrictions on the data set; please cite this data paper when using these data in publications.

TRY plant trait database - enhanced coverage and open access.

Plant traits-the morphological, anatomical, physiological, biochemical and phenological characteristics of plants-determine how plants respond to environmental factors, affect other trophic levels, and influence ecosystem properties and their benefits and detriments to people. Plant trait data thus represent the basis for a vast area of research spanning from evolutionary biology, community and functional ecology, to biodiversity conservation, ecosystem and landscape management, restoration, biogeography and earth system modelling. Since its foundation in 2007, the TRY database of plant traits has grown continuously. It now provides unprecedented data coverage under an open access data policy and is the main plant trait database used by the research community worldwide. Increasingly, the TRY database also supports new frontiers of trait-based plant research, including the identification of data gaps and the subsequent mobilization or measurement of new data. To support this development, in this article we evaluate the extent of the trait data compiled in TRY and analyse emerging patterns of data coverage and representativeness. Best species coverage is achieved for categorical traits-almost complete coverage for 'plant growth form'. However, most traits relevant for ecology and vegetation modelling are characterized by continuous intraspecific variation and trait-environmental relationships. These traits have to be measured on individual plants in their respective environment. Despite unprecedented data coverage, we observe a humbling lack of completeness and representativeness of these continuous traits in many aspects. We, therefore, conclude that reducing data gaps and biases in the TRY database remains a key challenge and requires a coordinated approach to data mobilization and trait measurements. This can only be achieved in collaboration with other initiatives.

Plant species abundance and phylogeny explain the structure of recruitment networks.

Established plants can affect the recruitment of young plants, filtering out some and allowing the recruitment of others, with profound effects on plant community dynamics. Recruitment networks (RNs) depict which species recruit under which others. We investigated whether species abundance and phylogenetic distance explain the structure of RNs across communities. We estimated the frequency of canopy-recruit interactions among woody plants in 10 forest assemblages to describe their RNs. For each RN, we determined the functional form (linear, power or exponential) best describing the relationship of interaction frequency with three predictors: canopy species abundance, recruit species abundance and phylogenetic distance. We fitted models with all combinations of predictor variables, from which we simulated RNs. The best functional form of each predictor was the same in most communities (linear for canopy species abundance, power for recruit species abundance and exponential for phylogenetic distance). The model including all predictor variables was consistently the best in explaining interaction frequency and showed the best performance in predicting RN structure. Our results suggest that mechanisms related to species abundance are necessary but insufficient to explain the assembly of RNs. Evolutionary processes affecting phylogenetic divergence are critical determinants of RN structure.

Climate change decreases suitable areas for rapeseed cultivation in Europe but provides new opportunities for white mustard as an alternative oilseed for biofuel production.

Oilseed crops, including several mustards, are cultivated as biofuel sources worldwide. However, common mustard crops (e.g., the rapeseed Brassica napus) grow naturally in mesic temperate regions, which are expected to be impaired by global warming and increased aridity. In particular, increased aridity is predicted to reduce the oil concentration and seed yield of rapeseed crops. There is therefore an urgent need to identify alternative bioenergy crops that are preadapted to future climatic conditions. An alternative to conventional Brassica species for biodiesel production is the white mustard Sinapis alba, which is native to the circum-Mediterranean region and has a high seed lipid content. S. alba grows spontaneously in olive groves and other widespread Mediterranean crops; accordingly, it could be easily cultivated by companion planting to improve ecosystem function by decreasing soil loss, controlling microbial disease, and assisting in the maintenance of biodiversity. In this study, using species distribution modeling, we predicted climatically suitable areas for the cultivation of S. alba in Western Europe across the Mediterranean Basin under present climatic conditions and several climate change scenarios. We show that current climatically suitable areas for S. alba cultivation do not overlap with those for B. napus. Unlike B. napus, S. alba could be cultivated throughout most of the circum-Mediterranean region. According to our models, increases in aridity and annual mean temperatures will expand the climatically suitable areas for S. alba in the Mediterranean Basin. However, suitable areas for the cultivation of B. napus will decrease significantly in Western Europe. Our results indicate that S. alba is a strong, environmentally safe candidate for biofuel production throughout the Mediterranean Basin and other Western European countries, especially under climate change scenarios that are expected to impair current oilseed crops.

The interplay between aridity and competition determines colonization ability, exclusion and ecological segregation in the heteroploid Brachypodium distachyon species complex.

A higher competitive advantage of polyploid plants compared with their parental diploids is frequently invoked to explain their establishment success, colonization of novel environments and cytotypic ecological segregation, yet there is scarce experimental evidence supporting such hypotheses. Here, we investigated whether differential competitive ability of species of the Brachypodium distachyon (Poaceae) species complex, a model system for genomic, ecological and evolutionary studies of temperate grasses, contributes to explaining their ecological segregation as well as their coexistence in diploid/allotetraploid contact zones. We conducted two field experiments in dry and humid localities to evaluate the tolerance to competition of diploids and allotetraploids in densely occupied environments, and to parameterize models of intra- and intercytotype competition as a mechanism for species exclusion/coexistence. We provide experimental evidence supporting the hypothesis that, under natural field conditions, allotetraploids have superior ecological success compared with one of their parental diploids in terms of both colonizing competitive habitats and intercytotypic competition, with the balance of intra/intercytotype competition favoring polyploid population establishment. These findings, together with previous data on ecogeographic segregation and adaptive response to water stress, suggest that the interplay between aridity and competitive outcome determines the ability to colonize competitive environments, the exclusion of diploids, especially in arid localities, and species geographic segregation.

Facilitation contributes to Mediterranean woody plant diversity but does not shape the diversity-productivity relationship along aridity gradients.

The diversity-productivity relationship (humped-back model (HBM)) and the stress-gradient (SGH) hypotheses may be connected when productivity is limited primarily by aridity. We analytically connect both hypotheses and assess the contribution of facilitation to woody plant richness along the aridity gradient of the Western Mediterranean floristic region. We monitored regeneration niches of woody plants, obtaining rarefied species richness and plant relative interaction indices in 54 forests and scrublands in a 1750-km geographical range across Spain, Morocco and the Canary Islands. We verified the monotonic increase in facilitation with aridity postulated by SGH and the humped-shape pattern of species richness expected from HBM, which became manifest after expanding the aridity gradient or crossing vegetation types. Along the gradient, interaction balance turned into facilitation earlier in forest than in scrublands. The effects of aridity and interaction balance on species diversity were additive rather than interdependent. Facilitation is an important driver of woody species richness at macroecological scales because it added up to diversity in most sites, with enhanced contribution with increased stress. The HBM was not shaped by species interactions. Results suggest that facilitation may act in Mediterranean vegetation buffering against critical transitions between states allowing woody plant communities to cope with the rise in aridity expected with global warming.

Development and characterization of microsatellite primers in the endangered Mediterranean shrub Ziziphus lotus (Rhamnaceae).

PREMISE OF THE STUDY: Microsatellite primers were developed to characterize and evaluate patterns of genetic diversity and structure in the endangered Mediterranean shrub Ziziphus lotus (Rhamnaceae). METHODS AND RESULTS: Twenty microsatellite primers were developed for Z. lotus, of which 14 were polymorphic. We evaluated microsatellite polymorphism in 97 specimens from 18 Spanish and seven Moroccan populations. Between two and eight alleles were found per locus, and the average number of alleles was 5.54. Observed heterozygosity and expected heterozygosity ranged from 0.08 to 0.90 and from 0.08 to 0.82, respectively. Nine of these primers also amplified microsatellite loci in Z. jujuba. CONCLUSIONS: The microsatellite markers described here will be useful in studies on genetic variation, population genetic structure, and gene flow in the fragmented habitat of this species. These markers are a valuable resource for designing appropriate conservation measures for the species in the Mediterranean range.

Geographic mosaic of plant evolution: extrafloral nectary variation mediated by ant and herbivore assemblages.

Herbivory is an ecological process that is known to generate different patterns of selection on defensive plant traits across populations. Studies on this topic could greatly benefit from the general framework of the Geographic Mosaic Theory of Coevolution (GMT). Here, we hypothesize that herbivory represents a strong pressure for extrafloral nectary (EFN) bearing plants, with differences in herbivore and ant visitor assemblages leading to different evolutionary pressures among localities and ultimately to differences in EFN abundance and function. In this study, we investigate this hypothesis by analyzing 10 populations of Anemopaegma album (30 individuals per population) distributed through ca. 600 km of Neotropical savanna and covering most of the geographic range of this plant species. A common garden experiment revealed a phenotypic differentiation in EFN abundance, in which field and experimental plants showed a similar pattern of EFN variation among populations. We also did not find significant correlations between EFN traits and ant abundance, herbivory and plant performance across localities. Instead, a more complex pattern of ant-EFN variation, a geographic mosaic, emerged throughout the geographical range of A. album. We modeled the functional relationship between EFNs and ant traits across ant species and extended this phenotypic interface to characterize local situations of phenotypic matching and mismatching at the population level. Two distinct types of phenotypic matching emerged throughout populations: (1) a population with smaller ants (Crematogaster crinosa) matched with low abundance of EFNs; and (2) seven populations with bigger ants (Camponotus species) matched with higher EFN abundances. Three matched populations showed the highest plant performance and narrower variance of EFN abundance, representing potential plant evolutionary hotspots. Cases of mismatched and matched populations with the lowest performance were associated with abundant and highly detrimental herbivores. Our findings provide insights on the ecology and evolution of plant-ant guarding systems, and suggest new directions to research on facultative mutualistic interactions at wide geographic scales.

Glandular trichomes as an inflorescence defence mechanism against insect herbivores in Iberian columbines.

Glandular trichomes play a defensive role against herbivores in the leaves of many plant species. However, their functional role in inflorescences has not been studied, even though theory suggests that tissues with a higher fitness value, such as inflorescences, should be better defended. Using manipulative experiments, we analysed the defensive role of glandular trichomes against herbivorous insects in the inflorescence of Iberian columbines (genus Aquilegia), and its inter-population and inter-taxa variation in relation to herbivore abundance and potential selective pressure. The experiments were conducted in eight populations belonging to four subspecies of two columbines (Aquilegia vulgaris and Aquilegia pyrenaica). For each population, we estimated the density of glandular trichomes in the inflorescences, the abundance of insects stuck in the inflorescences, the abundance of small herbivorous insects, the incidence of damage on flowers and fruits, and the fruit set. The density of glandular trichomes on the inflorescence of A. vulgaris and A. pyrenaica was higher in regions of higher herbivore abundance. We also found that when the plants lose the protection of glandular trichomes, small insects have better access to flowers and fruits, causing more damage and reducing plant fitness. This study concludes that glandular trichomes are part of an adaptive response against phytophagous insect herbivory. The observed variation in herbivore pressure between taxa, likely caused by habitat differentiation, might have played a role in trait differentiation through divergent selection. This result adds evidence to the differentiation of the Iberian columbines through habitat specialization.

Linking topological structure and dynamics in ecological networks.

Interaction networks are basic descriptions of ecological communities and are at the core of community dynamics models. Knowledge of their structure should enable us to understand dynamical properties of ecological communities. However, the relationships between dynamical properties of communities and qualitative descriptors of network structure remain unclear. To improve our understanding of such relationships, we develop a framework based on the concept of strongly connected components, which are key structural components of networks necessary to explain stability properties such as persistence and robustness. We illustrate this framework for the analysis of qualitative empirical food webs and plant-plant interaction networks. Both types of networks exhibit high persistence (on average, 99% and 80% of species, respectively, are expected to persist) and robustness (only 0.2% and 2% of species are expected to disappear following the extinction of a species). Each of the networks is structured as a large group of interconnected species accompanied by much smaller groups that most often consist of a single species. This low-modularity configuration can be explained by a negative modularity-stability relationship. Our results suggest that ecological communities are not typically structured in multispecies compartments and that compartmentalization decreases robustness.

Intra-population comparison of vegetative and floral trait heritabilities estimated from molecular markers in wild Aquilegia populations.

Measuring heritable genetic variation is important for understanding patterns of trait evolution in wild populations, and yet studies of quantitative genetic parameters estimated directly in the field are limited by logistic constraints, such as the difficulties of inferring relatedness among individuals in the wild. Marker-based approaches have received attention because they can potentially be applied directly to wild populations. For long-lived, self-compatible plant species where pedigrees are inadequate, the regression-based method proposed by Ritland has the appeal of estimating heritabilities from marker-based estimates of relatedness. The method has been difficult to implement in some plant populations, however, because it requires significant variance in relatedness across the population. Here, we show that the method can be readily applied to compare the ability of different traits to respond to selection, within populations. For several taxa of the perennial herb genus Aquilegia, we estimated heritabilities of floral and vegetative traits and, combined with estimates of natural selection, compared the ability to respond to selection of both types of traits under current conditions. The intra-population comparisons showed that vegetative traits have a higher potential for evolution, because although they are as heritable as floral traits, selection on them is stronger. These patterns of potential evolution are consistent with macroevolutionary trends in the European lineage of the genus.

Linking divergent selection on vegetative traits to environmental variation and phenotypic diversification in the Iberian columbines (Aquilegia).

Divergent selection is a key in the ecological theory of adaptive radiation. Most evidence on its causes and consequences relies on studies of pairs of populations or closely related taxa. However, adaptive radiation involves multiple taxa adapted to different environmental factors. We propose an operational definition of divergent selection to explore the continuum between divergent and convergent selection in multiple populations and taxa, and its links with environmental variation and phenotypic and taxonomic differentiation. We apply this approach to explore phenotypic differentiation of vegetative traits between 15 populations of four taxa of Iberian columbines (Gen. Aquilegia). Differences in soil rockiness impose divergent selection on inflorescence height and the number of flowers per inflorescence, likely affecting the processes of phenotypic and, in the case of inflorescence height, taxonomic diversification between taxa. Elevational variation imposes divergent selection on the number of leaves; however, the current pattern of divergent selection on this trait seems related to ecotypic differentiation within taxa but not to their taxonomic diversification.