Functional traits and performance of woody species on oil-affected soils of the Ecuadorian Amazon / Rasgos funcionales y comportamiento de especies leñosas en suelos afectados por petróleo de la Amazonía ecuatoriana

Abstract Introduction: Plant functional traits are widely used to predict community productivity. However, they are rarely used to predict the performance (in terms of growth diameter, growth height, survival, and integral response index) of woody species planted in degraded soils. Objective: To evaluate the relationship between the functional traits and the performance of 25 woody species planted in disturbed soils affected by oil extraction activities in Ecuadorian Amazon. Methods: Eighteen permanent sampling plots were established and five 6-month-old seedlings of each 25 species were randomly planted in each plot (125 individuals per plot), at a distance of 4×4 m. Eight quantitative functional traits (leaf size, specific leaf area, leaf nitrogen concentration, leaf phosphorus concentration, leaf minimum unit, leaf dry matter content, stem specific density and leaf tensile strength) were determined for each species. Results: The woody species with high performance shows greater leaf size, specific leaf area and Stem Specific Density than those showing low performance. Leaf nitrogen concentration and stem specific density had a direct relationship with the integral response index. The leaf size, leaf phosphorus concentration, leaf dry matter content and leaf tensile strength showed a negative relationship with the integral response index. Conclusions: Our study demonstrated that the performance of woody species o disturbed soils can be predicted satisfyingly by leaf and stem functional traits, presumably because these traits capture most of environmental and neighborhood conditions.

Resumen Introducción: Los rasgos funcionales de las plantas han sido ampliamente utilizados para predecir la productividad (en términos de crecimiento en diámetro, crecimiento en altura, sobrevivencia e índice de respuesta integral) de las comunidades vegetales. Sin embargo, rara vez han sido utilizados para predecir el desempeño de las especies leñosas plantadas en suelos degradados. Objetivo: Evaluar la relación entre el desempeño y los rasgos funcionales de 25 especies leñosas plantadas en suelos afectados por actividades de extracción de petróleo en la Amazonía ecuatoriana. Métodos: Se establecieron 18 parcelas permanentes de muestreo y en cada parcela se sembraron aleatoriamente cinco plántulas de 6 meses de las 25 especies (125 individuos por parcela), a una distancia de 4×4 m. Se determinaron ocho rasgos funcionales (área foliar, área foliar específica, concentración de nitrógeno foliar, concentración de fósforo foliar, unidad mínima foliar, contenido foliar de materia seca, densidad específica del fuste y fuerza tensil foliar) de cada especie. Resultados: Las especies leñosas con alto desempeño presentaron mayor área foliar, área foliar específica y densidad específica del fuste que las especies de bajo desempeño. La concentración de nitrógeno foliar y la densidad específica del fuste mostraron una relación directa. El área foliar, la concentración de fósforo foliar, el contenido de materia seca foliar y la fuerza tensil foliar presentaron una relación inversa con el Índice de Respuesta Integral. Conclusión: Se demostró que el desempeño de las especies leñosas plantadas en suelos alterados puede predecirse satisfactoriamente por rasgos funcionales de hoja y de tallo, debido posiblemente a que los rasgos influyen en el crecimiento y supervivencia de las especies, y reflejan la mayoría de las condiciones ambientales.

The role of phenotypic plasticity in shaping ecological networks.

Plasticity-mediated changes in interaction dynamics and structure may scale up and affect the ecological network in which the plastic species are embedded. Despite their potential relevance for understanding the effects of plasticity on ecological communities, these effects have seldom been analysed. We argue here that, by boosting the magnitude of intra-individual phenotypic variation, plasticity may have three possible direct effects on the interactions that the plastic species maintains with other species in the community: may expand the interaction niche, may cause a shift from one interaction niche to another or may even cause the colonization of a new niche. The combined action of these three factors can scale to the community level and eventually expresses itself as a modification in the topology and functionality of the entire ecological network. We propose that this causal pathway can be more widespread than previously thought and may explain how interaction niches evolve quickly in response to rapid changes in environmental conditions. The implication of this idea is not solely eco-evolutionary but may also help to understand how ecological interactions rewire and evolve in response to global change.

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.

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.

Phenotypic plasticity guides Moricandia arvensis divergence and convergence across the Brassicaceae floral morphospace.

Many flowers exhibit phenotypic plasticity. By inducing the production of several phenotypes, plasticity may favour the rapid exploration of different regions of the floral morphospace. We investigated how plasticity drives Moricandia arvensis, a species displaying within-individual floral polyphenism, across the floral morphospace of the entire Brassicaceae family. We compiled the multidimensional floral phenotype, the phylogenetic relationships, and the pollination niche of over 3000 species to construct a family-wide floral morphospace. We assessed the disparity between the two M. arvensis floral morphs (as the distance between the phenotypic spaces occupied by each morph) and compared it with the family-wide disparity. We measured floral divergence by comparing disparity with the most common ancestor, and estimated the convergence of each floral morph with other species belonging to the same pollination niches. Moricandia arvensis exhibits a plasticity-mediated floral disparity greater than that found between species, genera and tribes. The novel phenotype of M. arvensis moves outside the region occupied by its ancestors and relatives, crosses into a new region where it encounters a different pollination niche, and converges with distant Brassicaceae lineages. Our study suggests that phenotypic plasticity favours floral divergence and rapid appearance of convergent flowers, a process which facilitates the evolution of generalist pollination systems.

Prediction model for sap flow in cacao trees under different radiation intensities in the western Colombian Amazon.

In this study, we measured diurnal patterns of sap flow (Vs) in cacao trees growing in three types of agroforestry systems (AFs) that differ in the incident solar radiation they receive. We modeled the relationship of Vs with several microclimatic characteristics of the AFs using mixed linear models. We characterized microclimatic variables that may have an effect on diurnal patterns of sap flow: air relative humidity, air temperature, photosynthetically active radiation and vapor pressure deficit. Overall, our model predicted the differences between cacao Vs in the three different AFs, with cacao plants with dense Musaceae plantation and high mean diurnal incident radiation (HPAR) displaying the highest differences compared to the other agroforestry arrangements. The model was also able to predict situations such as nocturnal transpiration in HPAR and inverse nocturnal sap flows indicative of hydraulic redistribution in the other AFs receiving less incident radiation. Overall, the model we present here can be a useful and cost-effective tool for predicting transpiration and water use in cacao trees, as well as for managing cacao agroforestry systems in the Amazon rainforest.

Within-individual phenotypic plasticity in flowers fosters pollination niche shift.

Phenotypic plasticity, the ability of a genotype of producing different phenotypes when exposed to different environments, may impact ecological interactions. We study here how within-individual plasticity in Moricandia arvensis flowers modifies its pollination niche. During spring, this plant produces large, cross-shaped, UV-reflecting lilac flowers attracting mostly long-tongued large bees. However, unlike most co-occurring species, M. arvensis keeps flowering during the hot, dry summer due to its plasticity in key vegetative traits. Changes in temperature and photoperiod in summer trigger changes in gene expression and the production of small, rounded, UV-absorbing white flowers that attract a different assemblage of generalist pollinators. This shift in pollination niche potentially allows successful reproduction in harsh conditions, facilitating M. arvensis to face anthropogenic perturbations and climate change.

Photosynthesis limitations in cacao leaves under different agroforestry systems in the Colombian Amazon.

Cacao (Theobroma cacao L.) has traditionally been considered a crop that requires shade, and consequently it is implemented under agroforestry systems (AFs) in order to regulate the level of incident solar radiation. However, optimal shade levels for this tree crop may vary depending on the climate conditions of where it is grown. Here we analyzed the physiological performance of cacao under three different AFs in the Colombian Amazon that differed in solar radiation patterns: high (HPAR), medium (MPAR), or low (LPAR) mean daily incident radiation. The physiological performance was characterized using photosynthetic variables in leaves such as light- and CO2-response curves, chlorophyll a fluorescence parameters, and total chlorophyll and carotenoid contents, in conjunction with other leaf functional traits. Cacao trees exposed to HPAR showed an improved physiological performance as compared to those from the other two AFs. Compared to MPAR and LPAR, cacao trees in HPAR doubled the rate of net carbon assimilation and reached higher maximum rates of RuBisCO carboxylation and RuBP regeneration. Moreover, cacao trees in HPAR presented photoprotection mechanisms that avoided photoinhibition, which was accompanied by a greater non-photochemical quenching coefficient and biochemical and morphological adjustments (low chlorophyll but higher carotenoid contents and low specific leaf area) compared to cacao trees from the other AFs. Overall, our results show that, due to the high cloud cover in the Colombian Amazon, cacao plantations under conditions of sparse shade maximized their carbon use, showing an improved physiological performance as a result of higher photosynthetic rates and energy dissipation mechanisms. If the crop were managed with sparse shade, the paradigm that favors the cultivation of cacao under shade would be called into question in the Colombian Amazon and other regions with similar climatic conditions.

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.

Enhanced facilitation at the extreme end of the aridity gradient in the Atacama Desert: a community-level approach.

Plant facilitation is now recognized as an important process in severe environments. However, there is still no agreement on how facilitation changes as conditions become increasingly severe. The classic stress gradient hypothesis (SGH) predicts a monotonic increase in facilitation, which rises in frequency as conditions approach the extreme end of the environmental gradient. However, few studies have evaluated the validity of the SGH at the community level, the level at which it was formulated. Moreover, few studies have tested the SGH at either extreme of the gradient, and very few have excluded the effect of livestock on community response to stress. In line with the SGH, we hypothesized that several spatial pattern summary statistics would change monotonically from the least to the most arid sites, indicating increasingly aggregated patterns. In this study, we performed an evaluation of the SGH both within communities of shrub species and across a large portion of the Atacama Desert, and we isolated the abiotic component of the SGH. Our environmental gradient covered an extreme aridity gradient (< 20-130 mm annual precipitation). To perform point pattern analysis, we established 13 sites with environmental conditions representing four distinct levels of this gradient. Further, we conducted species co-occurrence analyses at 19 sites along the gradient. Both sets of analyses showed stronger positive spatial associations among plants at the most extreme end of the gradient. This was true regardless of whether we included all individuals, only small individuals located around large ones, or individuals in species pairs. Moreover, species tended to show greater co-occurrence as environmental severity increased. This increase in aggregation in the plant community seems to correlate with an increase in the strength of positive interspecific interactions, rather than greater clustering within each species. These monotonic increases in species co-occurrence and spatial association in more severe environments are consistent with some of the predictions of SGH, and collectively these results suggest that as the climate becomes more arid, positive species pairs interactions tend to be prevalent in the community.

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.

The effect of hydraulic lift on organic matter decomposition, soil nitrogen cycling, and nitrogen acquisition by a grass species.

Hydraulic lift (HL) is the passive movement of water through plant roots, driven by gradients in water potential. The greater soil-water availability resulting from HL may in principle lead to higher plant nutrient uptake, but the evidence for this hypothesis is not universally supported by current experiments. We grew a grass species common in North America in two-layer pots with three treatments: (1) the lower layer watered, the upper one unwatered (HL), (2) both layers watered (W), and (3) the lower layer watered, the upper one unwatered, but with continuous light 24 h a day to limit HL (no-HL). We inserted ingrowth cores filled with enriched-nitrogen organic matter ((15)N-OM) in the upper layer and tested whether decomposition, mineralization and uptake of (15)N were higher in plants performing HL than in plants without HL. Soils in the upper layer were significantly wetter in the HL treatment than in the no-HL treatment. Decomposition rates were similar in the W and HL treatments and lower in no-HL. On average, the concentration of NH(4)(+)-N in ingrowth cores was highest in the W treatment, and NO(3)(-)-N concentrations were highest in the no-HL treatment, with HL having intermediate values for both, suggesting differential mineralization of organic N among treatments. Aboveground biomass, leaf (15)N contents and the (15)N uptake in aboveground tissues were higher in W and HL than in no-HL, indicating higher nutrient uptake and improved N status of plants performing HL. However, there were no differences in total root nitrogen content or (15)N uptake by roots, indicating that HL affected plant allocation of acquired N to photosynthetic tissues. Our evidence for the role of HL in organic matter decomposition and nutrient cycling suggests that HL could have positive effects on plant nutrient dynamics and nutrient turnover.

Hydraulic lift promotes selective root foraging in nutrient-rich soil patches.

Hydraulic lift (HL) - the passive movement of water through plant roots from deep wet to shallow drier soil layers - can improve root survival in dry soils by providing a source of moisture to shallow roots. It may also enhance plant nutrient capture, though empirical evidence for this is scarce and whether HL promotes the selective placement of roots in nutrient-rich soil enhancing nutrient capture in dry soils remains unknown. We tested this with a split-pot design in which we separated the root system of Retama sphaerocarpa (L.) Boiss shrubs into two pot compartments: a lower, well-watered one; and an upper, drier one. Half the shrubs grew under natural light conditions hence allowed to perform HL, whereas the other half had impaired HL by maintaining continuous illumination at night. Resource-rich (organic matter enriched in 15N and P) and resource-poor soil patches were inserted in the upper compartment after a drought treatment was imposed. Artificial illumination did impair HL at night. Soil moisture in both the whole upper compartment and in soil patches was lower in plants illuminated at night and reduced the allocation of roots to nutrient-rich soil patches at the expense of root growth in nutrient-poor patches (i.e. root foraging precision). Plant nitrogen capture was also lower in shrubs with impaired HL. Overall, these results demonstrate that HL favoured the selective placement of roots in nutrient-rich patches as well as nutrient capture under drought, a process that may secure nutrient capture and maintain plant performance during drought periods.

Plant neighbour identity matters to belowground interactions under controlled conditions.

BACKGROUND: Root competition is an almost ubiquitous feature of plant communities with profound effects on their structure and composition. Far beyond the traditional view that plants interact mainly through resource depletion (exploitation competition), roots are known to be able to interact with their environment using a large variety of mechanisms that may inhibit or enhance access of other roots to the resource or affect plant growth (contest interactions). However, an extensive analysis on how these contest root interactions may affect species interaction abilities is almost lacking. METHODOLOGY/PRINCIPAL FINDINGS: In a common garden experiment with ten perennial plant species we forced pairs of plants of the same or different species to overlap their roots and analyzed how belowground contest interactions affected plant performance, biomass allocation patterns, and competitive abilities under abundant resource supply. Our results showed that net interaction outcome ranged from negative to positive, affecting total plant mass and allocation patterns. A species could be a strong competitor against one species, weaker against another one, and even facilitator to a third species. This leads to sets of species where competitive hierarchies may be clear but also to groups where such rankings are not, suggesting that intransitive root interactions may be crucial for species coexistence. CONCLUSIONS/SIGNIFICANCE: The outcome of belowground contest interactions is strongly dependent on neighbours' identity. In natural plant communities this conditional outcome may hypothetically help species to interact in non-hierarchical and intransitive networks, which in turn might promote coexistence.

Hydraulic lift and tolerance to salinity of semiarid species: consequences for species interactions.

The different abilities of plant species to use ephemeral or permanent water sources strongly affect physiological performance and species coexistence in water-limited ecosystems. In addition to withstanding drought, plants in coastal habitats often have to withstand highly saline soils, an additional ecological stress. Here we tested whether observed competitive abilities and C-water relations of two interacting shrub species from an arid coastal system were more related to differences in root architecture or salinity tolerance. We explored water sources of interacting Juniperus phoenicea Guss. and Pistacia lentiscus L. plants by conducting physiology measurements, including water relations, CO2 exchange, photochemical efficiency, sap osmolality, and water and C isotopes. We also conducted parallel soil analyses that included electrical conductivity, humidity, and water isotopes. During drought, Pistacia shrubs relied primarily on permanent salty groundwater, while isolated Juniperus plants took up the scarce and relatively fresh water stored in upper soil layers. As drought progressed further, the physiological activity of Juniperus plants nearly stopped while Pistacia plants were only slightly affected. Juniperus plants growing with Pistacia had stem-water isotopes that matched Pistacia, unlike values for isolated Juniperus plants. This result suggests that Pistacia shrubs supplied water to nearby Juniperus plants through hydraulic lift. This lifted water, however, did not appear to benefit Juniperus plants, as their physiological performance with co-occurring Pistacia plants was poor, including lower water potentials and rates of photosynthesis than isolated plants. Juniperus was more salt sensitive than Pistacia, which withstood salinity levels similar to that of groundwater. Overall, the different abilities of the two species to use salty water appear to drive the outcome of their interaction, resulting in asymmetric competition where Juniperus is negatively affected by Pistacia. Salt also seems to mediate the interaction between the two species, negating the potential positive effects of an additional water source via hydraulic lift.

Positive interactions among alpine plants increase with stress.

Plants can have positive effects on each other. For example, the accumulation of nutrients, provision of shade, amelioration of disturbance, or protection from herbivores by some species can enhance the performance of neighbouring species. Thus the notion that the distributions and abundances of plant species are independent of other species may be inadequate as a theoretical underpinning for understanding species coexistence and diversity. But there have been no large-scale experiments designed to examine the generality of positive interactions in plant communities and their importance relative to competition. Here we show that the biomass, growth and reproduction of alpine plant species are higher when other plants are nearby. In an experiment conducted in subalpine and alpine plant communities with 115 species in 11 different mountain ranges, we find that competition generally, but not exclusively, dominates interactions at lower elevations where conditions are less physically stressful. In contrast, at high elevations where abiotic stress is high the interactions among plants are predominantly positive. Furthermore, across all high and low sites positive interactions are more important at sites with low temperatures in the early summer, but competition prevails at warmer sites.