Two Congeneric Shrubs from the Atacama Desert Show Different Physiological Strategies That Improve Water Use Efficiency under a Simulated Heat Wave.

Desert shrubs are keystone species for plant diversity and ecosystem function. Atriplex clivicola and Atriplex deserticola (Amaranthaceae) are native shrubs from the Atacama Desert that show contrasting altitudinal distribution (A. clivicola: 0-700 m.a.s.l.; A. deserticola: 1500-3000 m.a.s.l.). Both species possess a C4 photosynthetic pathway and Kranz anatomy, traits adaptive to high temperatures. Historical records and projections for the near future show trends in increasing air temperature and frequency of heat wave events in these species' habitats. Besides sharing a C4 pathway, it is not clear how their leaf-level physiological traits associated with photosynthesis and water relations respond to heat stress. We studied their physiological traits (gas exchange, chlorophyll fluorescence, water status) before and after a simulated heat wave (HW). Both species enhanced their intrinsic water use efficiency after HW but via different mechanisms. A. clivicola, which has a higher LMA than A. deserticola, enhances water saving by closing stomata and maintaining RWC (%) and leaf Ψmd potential at similar values to those measured before HW. After HW, A. deserticola showed an increase of Amax without concurrent changes in gs and a significant reduction of RWC and Ψmd. A. deserticola showed higher values of Chla fluorescence after HW. Thus, under heat stress, A. clivicola maximizes water saving, whilst A. deserticola enhances its photosynthetic performance. These contrasting (eco)physiological strategies are consistent with the adaptation of each species to their local environmental conditions at different altitudes.

Trade-off between plant resistance and tolerance to herbivory: Mechanical defenses outweigh chemical defenses.

Plant resistance includes mechanical and chemical defenses that reduce herbivory, whereas plant tolerance reduces the fitness impact of herbivory. Because defenses are costly and investing in both resistance and tolerance may be superfluous, trade-offs among them are expected. In forest ecosystems, the mechanical strengthening of leaves is linked both to shade adaptation and antiherbivore defenses, but it also compromises resource uptake, therefore limiting regrowth following damage, suggesting a trade-off between mechanical defenses and tolerance. We tested for the resistance-tolerance trade-off across 11 common tree species in a temperate rainforest and explored mechanistic explanations by measuring chemical and mechanical defenses. Herbivory damage was negatively associated with leaf toughness and fiber content, whereas there was no significant relationship between herbivory and secondary metabolites (flavonols, gallic acid, tannins, and terpenoids). We detected a resistance-tolerance trade-off, as expected. We found a negative relationship between mechanical defenses and tolerance, estimated as the survival ratio between experimentally damaged and undamaged seedlings. Tolerance and secondary metabolites showed no significant association. Results suggest that selective forces other than herbivory acting on defensive traits can favor a resistance-tolerance trade-off. Therefore, plant adaptation to contrasting light environments may contribute to the evolution of resistance-tolerance trade-offs.

Sunspot activity influences tree growth: Molecular evidence and ecological implications.

Solar activity has a significant influence on Earth's climate and may drive many biological processes. Here, we measured growth in 11 tree species distributed along an ≈600-km latitudinal gradient in South-Central Chile, recording the width of their growth-rings among periods of maximum (highest number of sunspots) and minimum (lowest number of sunspots) solar activity. In one of these species, Quillaja saponaria, we experimentally assessed three ecophysiological traits (CO2 fixation through photosynthesis [Amax ], growth and leaf production) as well as the expression of five genes related to cell wall elongation and expansion following exposure to high and low levels of UV-B radiation, simulating scenarios of maximum and minimum solar activity, respectively. We found lower tree growth during the periods of maximum solar activity, with this trend being more evident at lower latitudes, where UV-B radiation is higher. Exposure of Q. saponaria to higher levels of UV-B affected the ecophysiological parameters, revealing a decrease in Amax , growth and leaf production. In addition, higher levels of UV-B led to repression in four of the five genes studied. Our results may help foresee environmental scenarios for different plant species associated with solar activity.

Endophytic bacterial communities are associated with leaf mimicry in the vine Boquila trifoliolata.

The mechanisms behind the unique capacity of the vine Boquila trifoliolata to mimic the leaves of several tree species remain unknown. A hypothesis in the original leaf mimicry report considered that microbial vectors from trees could carry genes or epigenetic factors that would alter the expression of leaf traits in Boquila. Here we evaluated whether leaf endophytic bacterial communities are associated with the mimicry pattern. Using 16S rRNA gene sequencing, we compared the endophytic bacterial communities in three groups of leaves collected in a temperate rainforest: (1) leaves from the model tree Rhaphithamnus spinosus (RS), (2) Boquila leaves mimicking the tree leaves (BR), and (3) Boquila leaves from the same individual vine but not mimicking the tree leaves (BT). We hypothesized that bacterial communities would be more similar in the BR-RS comparison than in the BT-RS comparison. We found significant differences in the endophytic bacterial communities among the three groups, verifying the hypothesis. Whereas non-mimetic Boquila leaves and tree leaves (BT-RS) showed clearly different bacterial communities, mimetic Boquila leaves and tree leaves (BR-RS) showed an overlap concerning their bacterial communities. The role of bacteria in this unique case of leaf mimicry should be studied further.

Global trends in phenotypic plasticity of plants.

Predicting plastic responses is crucial to assess plant species potential to adapt to climate change, but little is known about which factors drive the biogeographical patterns of phenotypic plasticity in plants. Theory predicts that climatic variability would select for increased phenotypic plasticity, whereas evidence indicates that stressful conditions can limit phenotypic plasticity. Using a meta-analytic, phylogeny-corrected approach to global data on plant phenotypic plasticity, we tested whether latitude, climate, climatic variability and/or stressful conditions are predictors of plastic responses at a biogeographical scale. We found support for a positive association between phenotypic plasticity and climatic variability only for plasticity in allocation. Plasticity in leaf morphology, size and physiology were positively associated with mean annual temperature. We also found evidence that phenotypic plasticity in physiology is limited by cold stress. Overall, plant plastic responses to non-climatic factors were stronger than responses to climatic factors. However, while climatic conditions were associated with plant plastic responses to climatic factors, they generally did not relate to plastic responses to other abiotic or biotic factors. Our study highlights the need to consider those factors that favour and limit phenotypic plasticity in order to improve predictive frameworks addressing plant species' potential to adapt to climate change.

Evolution of physiological performance in invasive plants under climate change.

Climate change is expected to promote biological invasions. Invasive species often undergo adaptive evolution, but whether invasive species show greater evolutionary potential than their native counterparts under climate change has rarely been evaluated. We conducted experimental evolution trials comparing the evolution of physiological performance (light-saturated photosynthetic rate, Amax ) of coexisting and closely related (1) invasive-native species pairs from Arid, Alpine, and Antarctic ecosystems, and (2) an invasive-naturalized species pair from a Mediterranean ecosystem differing in invasiveness. Experiments were conducted over three generations and under four environments of temperature and water availability resembling typical and climate change conditions in each ecosystem. Amax increased across generations for most species. Invasive species from Arid, Alpine, and Antarctic ecosystems showed similar, greater, and lesser evolution of Amax than their native counterparts, respectively. The Mediterranean invasive species showed greater evolution of Amax than its naturalized congener. Similar patterns were observed in all four experimental environments for each ecosystem, suggesting that comparable responses may be expected under climate change scenarios. All study species showed a positive association between Amax and reproductive output. Results suggest that invasive plants and their native (or naturalized) counterparts would show similar evolutionary responses of physiological performance to global warming and drought.

Fungal endophytes can eliminate the plant growth-defence trade-off.

A trade-off between growth and defence functions is commonly observed in plants. We propose that the association of plants with Epichloë fungal endophytes may eliminate this trade-off. This would be a consequence of the double role of these endophytes in host plants: the stimulation of plant growth hormones (e.g. gibberellins) and the fungal production of antiherbivore alkaloids. We put forward a model that integrates this dual effect of endophytes on plant growth and defence and test its predictions by means of meta-analysis of published literature. Our results support the notion that the enhanced plant resistance promoted by endophytes does not compromise plant growth. The limits and ecological benefits of this endophyte-mediated lack of plant growth-defence trade-off are discussed.

Evidence of indirect biotic resistance: native ants decrease invasive plant fitness by enhancing aphid infestation.

The biotic resistance hypothesis asserts that native species may hinder the invasion of exotic species, which can occur either directly or indirectly by influencing interactions between exotic and local species. Aphid-tending ants may play a key role in the indirect biotic resistance to plant invasion. Ants may protect aphids, thus increasing their negative effect on exotic plants, but may also deter chewing herbivores, thus benefiting exotic plants. We studied native aphid-tending ants (Dorymyrmex tener, Camponotus distinguendus, and Dorymyrmex richteri) on exotic nodding thistles (Carduus thoermeri), which are attacked by thistle aphids (Brachycaudus cardui) and thistle-head weevils (Rhinocyllus conicus). We evaluated the impact of ants, aphids, and weevils on thistle seed set. We compared ant species aggressiveness towards aphid predators and weevils and performed ant-exclusion experiments to determine the effects of ants on aphid predators and weevils. We analysed whether ant species affected thistle seed set through their effects on aphids and/or weevils. The ant D. tener showed the most aggressive behaviour towards aphid predators and weevils. Further, D. tener successfully removed aphid predators from thistles but did not affect weevils. Excluding D. tener from thistles increased seed set. Analyses supported a negative indirect pathway between the aggressive D. tener and thistle seed set through aphid populations, while the other ant species showed no indirect effects on thistle reproduction. Therefore, aggressive aphid-tending ants may enhance biotic resistance by increasing aphid infestation on exotic invasive plants. This study highlights the importance of indirect biotic resistance in modulating the success of invasive species.

Habitat-islands in the coastal Atacama Desert: loss of functional redundancy, but not of functional diversity, with decreased precipitation.

BACKGROUND AND AIMS: Aridity is increasing in many regions of the world, but microclimatic conditions may buffer plant communities from the direct effects of decreased precipitation, creating habitat islands. However, reduced precipitation can also impact these communities indirectly by decreasing the suitability of the surrounding habitat, thus limiting incoming propagules and increasing the chances of population decline and species loss. We test whether decreased precipitation results in loss of species and functional diversity within habitat islands, evaluating in particular whether declines in species diversity and abundance are less likely to result in loss of functional diversity if species/individual loss is stochastic (i.e. independent of species/individual traits) and communities/populations are functionally redundant. METHODS: Lomas communities are discrete plant communities embedded in the Atacama Desert, maintained by the microclimatic conditions created by fog. We recorded species and functional diversity in six Lomas communities along a 500 km long precipitation gradient in northern Chile. Functional traits were measured in 20 individuals per species, in those species that accounted for approx. 75 % of the abundance at each site. We calculated functional diversity and functional redundancy of the community, and intraspecific functional variation. KEY RESULTS: Decreased precipitation was associated with lower species diversity and lower species abundances. However, no traits or functional strategies increased or decreased consistently with precipitation, suggesting stochastic species/individual loss. Species with stress-tolerant strategies were predominant in all sites. Although species diversity decreased with decreasing precipitation, functional diversity remained unchanged. Lower functional redundancy in the drier sites suggests that mainly functionally redundant species were lost. Likewise, intraspecific functional variation was similar among communities, despite the lower species abundance in drier sites. CONCLUSIONS: Decreased precipitation can impact habitat island communities indirectly by decreasing the suitability of the surrounding habitat. Our results support the idea that a stochastic loss of species/individuals from functionally redundant communities and populations does not result in loss of functional diversity.

Disturbance reinforces community assembly processes differentially across spatial scales.

BACKGROUND AND AIMS: There is a paucity of empirical research and a lack of predictive models concerning the interplay between spatial scale and disturbance as they affect the structure and assembly of plant communities. We proposed and tested a trait dispersion-based conceptual model hypothesizing that disturbance reinforces assembly processes differentially across spatial scales. Disturbance would reinforce functional divergence at the small scale (neighbourhood), would not affect functional dispersion at the intermediate scale (patch) and would reinforce functional convergence at the large scale (site). We also evaluated functional and species richness of native and exotic plants to infer underlying processes. Native and exotic species richness were expected to increase and decrease with disturbance, respectively, at the neighbourhood scale, and to show similar associations with disturbance at the patch (concave) and site (negative) scales. METHODS: In an arid shrubland, we estimated species richness and functional dispersion and richness within 1 m2 quadrats (neighbourhood) nested within 100 m2 plots (patch) along a small-scale natural disturbance gradient caused by an endemic fossorial rodent. Data for the site scale (2500 m2 plots) were taken from a previous study. We also tested the conceptual model through a quantitative literature review and a meta-analysis. KEY RESULTS: As spatial scale increased, disturbance sequentially promoted functional divergence, random trait dispersion and functional convergence. Functional richness was unaffected by disturbance across spatial scales. Disturbance favoured natives over exotics at the neighbourhood scale, while both decreased under high disturbance at the patch and site scales. CONCLUSIONS: The results supported the hypothesis that disturbance reinforces assembly processes differentially across scales and hampers plant invasion. The quantitative literature review and the meta-analysis supported most of the model predictions.

Sand-swimming behaviour reduces ectoparasitism in an iguanian lizard.

Sand swimming behaviour occurs in several lizard clades. Known ecological advantages of sand swimming include reduced predation risk and enhanced thermoregulation. We addressed whether, by way of sand abrasion, sand-swimming reduces ectoparasitism in the lizard Microlophus occipitalis, whose natural habitat includes sandy substrates (beach) and firm soil (dry forest). We hypothesised that, aside from habitat differences in infestation probability, ectoparasite prevalence and load would be lower in the beach than in the forest because of ectoparasite removal caused by sand-swimming. In an experiment with lizards confined in boxes with substrate from both habitats, lizards in beach boxes showed a greater decrease in ectoparasite load compared with lizards in forest boxes. Ectoparasite prevalence and load were much higher in the forest than in the beach across seasons. Larger lizards showed higher ectoparasite loads, and there were no sex differences in ectoparasite infestation. We provide evidence that sand swimming may confer another ecological advantage to lizards: reduced ectoparasitism.

Parallel functional differentiation of an invasive annual plant on two continents.

Rapid local adaptation frequently occurs during the spread of invading species. It remains unclear, however, how consistent, and therefore potentially predictable, such patterns of local adaptation are. One approach to this question is to measure patterns of local differentiation in functional traits and plasticity levels in invasive species in multiple regions. Finding consistent patterns of local differentiation in replicate regions suggests that these patterns are adaptive. Further, this outcome indicates that the invading species likely responds predictably to selection along environmental gradients, even though standing genetic variation is likely to have been reduced during introduction. We studied local differentiation in the invasive annual plant Erodium cicutarium in two invaded regions, California and Chile. We collected seeds from across strong gradients in precipitation and temperature in Mediterranean-climate parts of the two regions (10 populations per region). We grew seeds from maternal families from these populations through two generations and exposed the second generation to contrasting levels of water and nutrient availability. We measured growth, flowering time and leaf functional traits across these treatments to obtain trait means and plasticity measures. We found strong differentiation among populations in all traits. Plants from drier environments flowered earlier, were less plastic in flowering time and reached greater size in all treatments. Correlations among traits within regions suggested a coordinated evolutionary response along environmental gradients associated with growing season length. There was little divergence in traits and trait intercorrelations between regions, but strongly parallel divergence in traits within regions. Similar, statistically consistent patterns of local trait differentiation across two regions suggest that local adaptation to environmental gradients has aided the spread of this invasive species, and that the formation of ecotypes in newly invaded environments has been relatively consistent and predictable.

Biotic homogenization within and across eight widely distributed grasslands following invasion by Bromus inermis.

Invasive species can alter the structure and function of the communities they invade, as well as lead to biotic homogenization across their invasive range, thus affecting large-scale diversity patterns. The mechanisms by which invasive species can lead to biotic homogenization are poorly understood. We argue that invasive species acting as strong, deterministic, and consistent filters within and across invaded communities are likely to cause biotic homogenization at multiple spatial scales. We studied Bromus inermis Leyss. invasion into eight grasslands covering most of the grassland and parkland natural regions of Alberta (western Canada). Specifically, we tested whether B. inermis (1) has a strong impact on species richness and composition, (2) consistently alters resources (nutrients, light, and soil moisture), imposing the same ecological filter to species establishment and persistence across sites, and hence (3) whether it leads to biotic homogenization within and across sites. We recorded plant cover and resources across native-to-invaded transition areas combining space-for-time substitutions with time-series data analyses. Bromus inermis invasion was associated with rapid biotic homogenization of communities, within and among the eight grasslands. The sharp changes in species relative abundances following invasion was the initial driver of biotic homogenization, and species loss was delayed. Supporting the idea that biotic homogenization can occur when an invasive species presents a broad and consistent filter, resources modified by B. inermis invasion (particularly light and certain nutrients) were altered rather consistently within and across sites. The 50% reduction in light was likely the initial driver of biotic homogenization, and the increase in nutrient availability probably facilitates the displacement of species from the invaded areas and could lead to the establishment of self-reinforcing dynamics. Overall, our results support the idea that invaders acting as strong, deterministic, and consistent ecological filters are likely to cause biotic homogenization of the communities they invade.

Maternal experience and soil origin influence interactions between resident species and a dominant invasive species.

Invasive species dominance in invaded communities may not be long-lasting due to regulatory processes, such as plant-soil feedbacks and neighboring species adaptation. Further, the change in species competitive ability may be contingent upon neighbor identity (i.e., specialized response) or consistent across neighbors (i.e., generalized response). Specialized responses can facilitate overall coexistence, while generalized responses may result in competitive exclusion. We set up a greenhouse experiment to test, in three species, the effect of soil conditions (non-invaded vs. invaded soil) and maternal experience (offspring of maternal plants from invaded vs. non-invaded areas) on species competitive ability against the invader Bromus inermis and conspecifics. If changes in species competitive ability against B. inermis were also evident when interacting with conspecifics, it would suggest a generalized increased/decreased competitive ability. Maternal experience resulted in reduced suppression of B. inermis in the three species and no change in tolerance. On the other hand, tolerance to B. inermis was enhanced when plants grew in soil from invaded areas, compared to non-brome soil. Importantly, both the decreased suppression due to maternal experience with B. inermis and the increased tolerance in invaded soil appear to be invader specific, as no such effects were observed when interacting with conspecifics. Specialized responses should facilitate coexistence, as no individual/species is a weaker or stronger competitor against all other neighbors or under all local soil conditions. Further, the negative plant-soil feedback for B. inermis should facilitate native species recovery in invaded areas and result in lower B. inermis performance and dominance over time.

Tolerance to herbivory and the resource availability hypothesis.

The resource availability hypothesis (RAH), the most successful theory explaining plant defence patterns, predicts that defence investment is related to the relative growth rate (RGR) of plant species, which is associated with habitat quality. Thus, fast-growing species should show lower resistance than slow-growing species, which would lead fast growers to sustain higher herbivory rates, but the fitness consequences of herbivory would be greater for slow growers. The latter is often assumed but rarely tested. In a temperate rainforest, we tested the expected pattern of tolerance to herbivory derived from the RAH: that fast-growing species should be more tolerant than slow-growing species. We also evaluated whether other plant features covary with RGR (leaf lifespan, shade tolerance and leaf toughness) and thus could also contribute to the patterns of tolerance to herbivory. As expected, seedlings from tree species with higher RGR showed greater tolerance to herbivory. Among the three plant features included, only leaf lifespan showed a significant association with RGR, but RGR was the best predictor of tolerance. We argue that plant tolerance to herbivory must be evaluated to properly verify the assumptions of the RAH.

Disturbance by an endemic rodent in an arid shrubland is a habitat filter: effects on plant invasion and taxonomical, functional and phylogenetic community structure.

Background and Aims: Disturbance often drives plant invasion and may modify community assembly. However, little is known about how these modifications of community patterns occur in terms of taxonomic, functional and phylogenetic structure. This study evaluated in an arid shrubland the influence of disturbance by an endemic rodent on community functional divergence and phylogenetic structure as well as on plant invasion. It was expected that disturbance would operate as a habitat filter favouring exotic species with short life cycles. Methods: Sixteen plots were sampled along a disturbance gradient caused by the endemic fossorial rodent Spalacopus cyanus , measuring community parameters and estimating functional divergence for life history traits (functional dispersion index) and the relative contribution to functional divergence of exotic and native species. The phylogenetic signal (Pagel's lambda) and phylogenetic community structure (mean phylogenetic distance and mean nearest taxon phylogenetic distance) were also estimated. The use of a continuous approach to the disturbance gradient allowed the identification of non-linear relationships between disturbance and community parameters. Key Results: The relationship between disturbance and both species richness and abundance was positive for exotic species and negative for native species. Disturbance modified community composition, and exotic species were associated with more disturbed sites. Disturbance increased trait convergence, which resulted in phylogenetic clustering because traits showed a significant phylogenetic signal. The relative contribution of exotic species to functional divergence increased, while that of natives decreased, with disturbance. Exotic and native species were not phylogenetically distinct. Conclusions: Disturbance by rodents in this arid shrubland constitutes a habitat filter over phylogeny-dependent life history traits, leading to phylogenetic clustering, and drives invasion by favouring species with short life cycles. Results can be explained by high phenotypic and phylogenetic resemblance between exotic and native species. The use of continuous gradients when studying the effects of disturbance on community assembly is advocated.

Genetic variation of loci potentially under selection confounds species-genetic diversity correlations in a fragmented habitat.

Positive species-genetic diversity correlations (SGDCs) are often thought to result from the parallel influence of neutral processes on genetic and species diversity. Yet, confounding effects of non-neutral mechanisms have not been explored. Here, we investigate the impact of non-neutral genetic diversity on SGDCs in high Andean wetlands. We compare correlations between plant species diversity and genetic diversity (GD) calculated with and without loci potentially under selection (outlier loci). The study system includes 2188 specimens from five species (three common aquatic macroinvertebrate and two dominant plant species) that were genotyped for 396 amplified fragment length polymorphism loci. We also appraise the importance of neutral processes on SGDCs by investigating the influence of habitat fragmentation features. Significant positive SGDCs were detected for all five species (mean SGDC = 0.52 ± 0.05). While only a few outlier loci were detected in each species, they resulted in significant decreases in GD and in SGDCs. This supports the hypothesis that neutral processes drive species-genetic diversity relationships in high Andean wetlands. Unexpectedly, the effects on genetic diversity GD of the habitat fragmentation characteristics in this study increased with the presence of outlier loci in two species. Overall, our results reveal pitfalls in using habitat features to infer processes driving SGDCs and show that a few loci potentially under selection are enough to cause a significant downward bias in SGDC. Investigating confounding effects of outlier loci thus represents a useful approach to evidence the contribution of neutral processes on species-genetic diversity relationships.

Ecological and evolutionary impacts of changing climatic variability.

While average temperature is likely to increase in most locations on Earth, many places will simultaneously experience higher variability in temperature, precipitation, and other climate variables. Although ecologists and evolutionary biologists widely recognize the potential impacts of changes in average climatic conditions, relatively little attention has been paid to the potential impacts of changes in climatic variability and extremes. We review the evidence on the impacts of increased climatic variability and extremes on physiological, ecological and evolutionary processes at multiple levels of biological organization, from individuals to populations and communities. Our review indicates that climatic variability can have profound influences on biological processes at multiple scales of organization. Responses to increased climatic variability and extremes are likely to be complex and cannot always be generalized, although our conceptual and methodological toolboxes allow us to make informed predictions about the likely consequences of such climatic changes. We conclude that climatic variability represents an important component of climate that deserves further attention.