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.

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.

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.

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.

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.

Woody climbers show greater population genetic differentiation than trees: Insights into the link between ecological traits and diversification.

The climbing habit is a key innovation in plants: climbing taxa have higher species richness than nonclimbing sister groups. We evaluated the hypothesis that climbing plant species show greater among-population genetic differentiation than nonclimber species. We compared the among-population genetic distance in woody climbers (eight species, 30 populations) and trees (seven species, 29 populations) coexisting in nine communities in a temperate rainforest. We also compared within-population genetic diversity in co-occurring woody climbers and trees in two communities. Mean genetic distance between populations of climbers was twice that of trees. Isolation by distance (increase in genetic distance with geographic distance) was greater for climbers. Climbers and trees showed similar within-population genetic diversity. Our longevity estimate suggested that climbers had shorter generation times, while other biological features often associated with diversification (dispersal and pollination syndromes, mating system, size, and metabolic rate) did not show significant differences between groups. We hypothesize that the greater population differentiation in climbers could result from greater evolutionary responses to local selection acting on initially higher within-population genetic diversity, which could be driven by neutral processes associated with shorter generation times. Increased population genetic differentiation could be incorporated as another line of evidence when testing for key innovations.

Species divergence and phylogenetic variation of ecophysiological traits in lianas and trees.

The climbing habit is an evolutionary key innovation in plants because it is associated with enhanced clade diversification. We tested whether patterns of species divergence and variation of three ecophysiological traits that are fundamental for plant adaptation to light environments (maximum photosynthetic rate [A(max)], dark respiration rate [R(d)], and specific leaf area [SLA]) are consistent with this key innovation. Using data reported from four tropical forests and three temperate forests, we compared phylogenetic distance among species as well as the evolutionary rate, phylogenetic distance and phylogenetic signal of those traits in lianas and trees. Estimates of evolutionary rates showed that R(d) evolved faster in lianas, while SLA evolved faster in trees. The mean phylogenetic distance was 1.2 times greater among liana species than among tree species. Likewise, estimates of phylogenetic distance indicated that lianas were less related than by chance alone (phylogenetic evenness across 63 species), and trees were more related than expected by chance (phylogenetic clustering across 71 species). Lianas showed evenness for R(d), while trees showed phylogenetic clustering for this trait. In contrast, for SLA, lianas exhibited phylogenetic clustering and trees showed phylogenetic evenness. Lianas and trees showed patterns of ecophysiological trait variation among species that were independent of phylogenetic relatedness. We found support for the expected pattern of greater species divergence in lianas, but did not find consistent patterns regarding ecophysiological trait evolution and divergence. R(d) followed the species-level pattern, i.e., greater divergence/evolution in lianas compared to trees, while the opposite occurred for SLA and no pattern was detected for A(max). R(d) may have driven lianas' divergence across forest environments, and might contribute to diversification in climber clades.

Is physiological performance a good predictor for fitness? Insights from an invasive plant species.

Is physiological performance a suitable proxy of fitness in plants? Although, several studies have been conducted to measure some fitness-related traits and physiological performance, direct assessments are seldom found in the literature. Here, we assessed the physiology-fitness relationship using second-generation individuals of the invasive plant species Taraxacum officinale from 17 localities distributed in five continents. Specifically, we tested if i) the maximum quantum yield is a good predictor for seed-output ii) whether this physiology-fitness relationship can be modified by environmental heterogeneity, and iii) if this relationship has an adaptive consequence for T. officinale individuals from different localities. Overall, we found a significant positive relationship between the maximum quantum yield and fitness for all localities evaluated, but this relationship decreased in T. officinale individuals from localities with greater environmental heterogeneity. Finally, we found that those individuals from localities where environmental conditions are highly seasonal performed better under heterogeneous environmental conditions. Contrarily, under homogeneous controlled conditions, those individuals from localities with low environmental seasonality performed much better. In conclusion, our results suggest that the maximum quantum yield seem to be good predictors for plant fitness. We suggest that rapid measurements, such as those obtained from the maximum quantum yield, could provide a straightforward proxy of individual's fitness in changing environments.

Herbivores modify selection on plant functional traits in a temperate rainforest understory.

There is limited evidence regarding the adaptive value of plant functional traits in contrasting light environments. It has been suggested that changes in these traits in response to light availability can increase herbivore susceptibility. We tested the adaptive value of plant functional traits linked with carbon gain in contrasting light environments and also evaluated whether herbivores can modify selection on these traits in each light environment. In a temperate rainforest, we examined phenotypic selection on functional traits in seedlings of the pioneer tree Aristotelia chilensis growing in sun (canopy gap) and shade (forest understory) and subjected to either natural herbivory or herbivore exclusion. We found differential selection on functional traits depending on light environment. In sun, there was positive directional selection on photosynthetic rate and relative growth rate (RGR), indicating that selection favors competitive ability in a high-resource environment. Seedlings with high specific leaf area (SLA) and intermediate RGR were selected in shade, suggesting that light capture and conservative resource use are favored in the understory. Herbivores reduced the strength of positive directional selection acting on SLA in shade. We provide the first demonstration that natural herbivory rates can change the strength of selection on plant ecophysiological traits, that is, attributes whose main function is resource uptake. Research addressing the evolution of shade tolerance should incorporate the selective role of herbivores.

Herbivory on temperate rainforest seedlings in sun and shade: resistance, tolerance and habitat distribution.

Differential herbivory and/or differential plant resistance or tolerance in sun and shade environments may influence plant distribution along the light gradient. Embothrium coccineum is one of the few light-demanding tree species in the temperate rainforest of southern South America, and seedlings are frequently attacked by insects and snails. Herbivory may contribute to the exclusion of E. coccineum from the shade if 1) herbivory pressure is greater in the shade, which in turn can result from shade plants being less resistant or from habitat preferences of herbivores, and/or 2) consequences of damage are more detrimental in the shade, i.e., shade plants are less tolerant. We tested this in a field study with naturally established seedlings in treefall gaps (sun) and forest understory (shade) in a temperate rainforest of southern Chile. Seedlings growing in the sun sustained nearly 40% more herbivore damage and displayed half of the specific leaf area than those growing in the shade. A palatability test showed that a generalist snail consumed ten times more leaf area when fed on shade leaves compared to sun leaves, i.e., plant resistance was greater in sun-grown seedlings. Herbivore abundance (total biomass) was two-fold greater in treefall gaps compared to the forest understory. Undamaged seedlings survived better and showed a slightly higher growth rate in the sun. Whereas simulated herbivory in the shade decreased seedling survival and growth by 34% and 19%, respectively, damaged and undamaged seedlings showed similar survival and growth in the sun. Leaf tissue lost to herbivores in the shade appears to be too expensive to replace under the limiting light conditions of forest understory. Following evaluations of herbivore abundance and plant resistance and tolerance in contrasting light environments, we have shown how herbivory on a light-demanding tree species may contribute to its exclusion from shade sites. Thus, in the shaded forest understory, where the seedlings of some tree species are close to their physiological tolerance limit, herbivory could play an important role in plant establishment.