Economic and hydraulic divergences underpin ecological differentiation in the Bromeliaceae

Leaf economic and hydraulic theories have rarely been applied to the ecological differentiation of speciose herbaceous plant radiations. The role of character trait divergences and network reorganization in the differentiation of the functional types in the megadiverse Neotropical Bromeliaceae was explored by quantifying a range of leaf economic and hydraulic traits in 50 diverse species. Functional types, which are defined by combinations of C₃ or Crassulacean acid metabolism (CAM) photosynthesis, terrestrial or epiphytic habits, and non‐specialized, tank‐forming or atmospheric morphologies, segregated clearly in trait space. Most classical leaf economic relationships were supported, but they were weakened by the presence of succulence. Functional types differed in trait‐network architecture, suggesting that rewiring of trait‐networks caused by innovations in habit and photosynthetic pathway is an important aspect of ecological differentiation. The hydraulic data supported the coupling of leaf hydraulics and gas exchange, but not the hydraulic safety versus efficiency hypothesis, and hinted at an important role for the extra‐xylary compartment in the control of bromeliad leaf hydraulics. Overall, our findings highlight the fundamental importance of structure–function relationships in the generation and maintenance of ecological diversity.     

Leaf economics and hydraulic traits are decoupled in five species‐rich tropical‐subtropical forests

Leaf economics and hydraulic traits are critical to leaf photosynthesis, yet it is debated whether these two sets of traits vary in a fully coordinated manner or there is room for independent variation. Here, we tested the relationship between leaf economics traits, including leaf nitrogen concentration and leaf dry mass per area, and leaf hydraulic traits including stomatal density and vein density in five tropical‐subtropical forests. Surprisingly, these two suites of traits were statistically decoupled. This decoupling suggests that independent trait dimensions exist within a leaf, with leaf economics dimension corresponding to light capture and tissue longevity, and the hydraulic dimension to water‐use and leaf temperature maintenance. Clearly, leaf economics and hydraulic traits can vary independently, thus allowing for more possible plant trait combinations. Compared with a single trait dimension, multiple trait dimensions may better enable species adaptations to multifarious niche dimensions, promote diverse plant strategies and facilitate species coexistence.     

散孔材与环孔材树种枝干、叶水力学特性的比较研究

为揭示散孔材与环孔材树种树木水分生理特性的差异,选取了常见的3种散孔材落叶树种(毛白杨、法国梧桐和樱花)和3种环孔材落叶树种(刺槐、合欢和白蜡),研究了其枝干与叶水力学性质的差异及其协调性。结果表明:3种环孔材树种枝干横截面积基础上的最大比导水率(Ks-max)大于3种散孔材树种,但其木质部对空穴化的脆弱性(P50branch)高于散孔材树种,6种树木枝干的水分传输能力和抵抗空穴化能力之间存在一种相互制约的权衡关系。3种散孔材与3种环孔材树种的叶最大水力导度(Kl-max)和水力脆弱性(P50leaf)并无显著差异;对于3种散孔材树种,叶的水力脆弱性要高于枝干,但对3种环孔材树种而言,枝干的水力脆弱性要高于叶。6种树木枝干和叶的水力学性质(Kmax、P50)之间并无相关关系。这些结果表明:散孔材与环孔材树种的枝干水力学特性有明显差异,但叶水力学特性无差异;枝干与叶水力学性质之间是相互独立的。     

Climate change and the invasion of California by grasses

Over the next century, changes in the global climate are expected to have major consequences for plant communities, possibly including the exacerbation of species invasions. We evaluated this possibility in the grass flora of California, which is economically and ecologically important and heavily invaded. We used a novel, trait‐based approach involving two components: identifying differences in trait composition between native and exotic components of the grass flora and evaluating contemporary trait–climate relationships across the state. The combination of trait–climate relationships and trait differences between groups allows us to predict changes in the exotic‐native balance under climate change scenarios. Exotic species are more likely to be annual, taller, with larger leaves, larger seeds, higher specific leaf area, and higher leaf N percentage than native species. Across the state, all these traits are associated with regions with higher temperature. Therefore, we predict that increasing temperatures will favor trait states that tend to be possessed by exotic species, increasing the dominance of exotic species. This prediction is corroborated by the current distribution of exotic species richness relative to native richness in California; warmer areas contain higher proportions of exotic species. This pattern was very well captured by a simple model that predicts invasion severity given only the trait–climate relationship for native species and trait differences between native and exotic species. This study provides some of the first evidence for an important interaction between climate change and species invasions across very broad geographic and taxonomic scales.     

Scale‐dependent trait correlations in a temperate tree community

Recent investigations of relationships among plant traits have generated important insights into plant form and function. However, relationships involving leaf area, leaf shape and plant height remain poorly resolved. Previous work has also focused on correlations between average trait values for individual species. It is unclear whether similar relationships occur within species. We searched for novel plant trait correlations by comparing leaf area, leaf circularity, specific leaf area (SLA) and plant height among 16 common woody plant species from a temperate forest in New Zealand. Analyses were conducted both within species (intra‐specifically) and among species (inter‐specifically) to determine whether trait correlations were scale dependent. Leaf area was unrelated to other leaf traits inter‐specifically. However, leaf area declined with plant height and increased with SLA intra‐specifically. Leaf circularity decreased with plant height inter‐specifically, but increased with plant height intra‐specifically. SLA increased with plant height both inter‐ and intra‐specifically. Leaf circularity increased with SLA inter‐specifically, but decreased with SLA intra‐specifically. Overall results showed that leaf shape, SLA and plant height are interrelated. However, intra‐specific relationships often differed substantially from inter‐specific relationships, suggesting that the processes shaping relationships between this suite of plant traits are scale‐dependent.     

Increase in light interception cost and metabolic mass component of leaves are coupled for efficient resource use in the high altitude vegetation

Global syntheses of leaf trait scaling relationships report an increase in light interception costs or ‘diminishing returns’ with increase in leaf area. However, variation in light interception costs across ecological gradients and plant strategies to cope up with these costs are not adequately understood. We analyzed leaf area (A) – leaf dry mass (M), leaf water mass (W) – M and W – A scaling relationships in plants occurring in a high altitude region of western Himalaya across environmental gradients to understand changes in light interception cost and metabolic mass component. M represents light interception cost, whereas, W is considered as a proxy of metabolic mass component for liquid phase being the ultimate source of metabolic activity. Trait values were measured from 9278 leaves belonging to 136 dominant species occurring at different sites, slope aspects, elevations and habitat types. Overall, light interception cost increased with increasing A (scaling exponent (α) < 1 in A–M relationship) and metabolic mass component increased disproportionately high with increasing M and A. We found significant differences in scaling exponents of leaf trait relationship between sites, elevations, slope aspects and habitat types, indicating that increase in light interception cost was more evident at higher elevations, southern slopes and open habitats. Further, with increase in light interception cost, metabolic mass component also increased (α > 1 in W–M and W–A relationships). The changes in scaling exponents of various leaf trait relationships across ecological gradients indicated that vegetation of different regions have differences in light interception cost and metabolic mass component. Moreover, increasing light interception cost (increase in mechanical and hydraulic tissues) with increasing A and increasing metabolic mass (leaf thickness) with increasing A and M are favored in high altitude vegetation. This could be a key strategy of high altitude plants for efficient resource capture and use in harsh environments.     

Functional and historical drivers of leaf shape evolution in palms (Arecaceae)

Aim

Leaves display a remarkable variety of shapes, each with potential ecological advantages in specific climates. While the relations between leaf shape and either climate or height have been relatively well studied in eudicots, the macroecological drivers of shape remain poorly known in monocots. Here, we investigated the associations between climate and plant height with the evolution of leaf shape in a clade with high species and morphological diversity.

Location

Global.

Time period

Cretaceous to contemporary.

Major taxa studied

Palms (Arecaceae).

Methods

We apply a Bayesian phylogenetic mixed model to test for associations between climate and leaf shape (all – entire-leaved, pinnate-dissected, palmate-dissected and costapalmate). We further reconstruct the ancestral leaf shape using multistate speciation and extinction models and compare the frequency of shapes with global temperatures through time.

Results

We find that plant height associates with dissected leaves and that annual precipitation associates with pinnate shapes. The ancestral leaf shape is unclear, but early diversification was dominated by pinnate-dissected palms, which has remained the most species-rich form of leaves throughout palm history.

Main Conclusions

Palms that are tall and live in humid regions are more likely to have pinnate leaves. Through geological time scales, temperature did not play an obvious role in determining leaf shapes. This study contributes to our understanding of how the diversity of leaf shapes is linked to biological and climatic factors.     

Functional design space of single-veined leaves: role of tissue hydraulic properties in constraining leaf size and shape

BACKGROUND AND AIMS: Morphological diversity of leaves is usually quantified with geometrical characters, while in many cases a simple set of biophysical parameters are involved in constraining size and shape. One of the main physiological functions of the leaf is transpiration and thus one can expect that leaf hydraulic parameters can be used to predict potential morphologies, although with the caveat that morphology in turn influences physiological parameters including light interception and boundary layer thickness and thereby heat transfer and net photosynthesis. METHODS: An iterative model was used to determine the relative sizes and shapes that are functionally possible for single-veined leaves as defined by their ability to supply the entire leaf lamina with sufficient water to prevent stomatal closure. The model variables include the hydraulic resistances associated with vein axial and radial transport, as well as with water movement through the mesophyll and the leaf surface. KEY RESULTS: The four parameters included in the model are sufficient to define a hydraulic functional design space that includes all single-veined leaf shapes found in nature, including scale-, awl- and needle-like morphologies. This exercise demonstrates that hydraulic parameters have dissimilar effects: surface resistance primarily affects leaf size, while radial and mesophyll resistances primarily affect leaf shape. CONCLUSIONS: These distinctions between hydraulic parameters, as well as the differential accessibility of different morphologies, might relate to the convergent evolutionary patterns seen in a variety of fossil lineages concerning overall morphology and anatomical detail that frequently have evolved in linear and simple multi-veined leaves.     

Vertical gradients in leaf trait diversity in a New Zealand forest

Leaves come in a remarkable diversity of sizes and shapes. However, spatial patterns in leaf trait diversity are rarely investigated and poorly resolved. We used a hierarchical approach to evaluate vertical variability in leaf morphology (i.e., leaf trait diversity) in 16 common tree and shrub species inhabiting a New Zealand forest. Height-related heterogeneity in leaf area, specific leaf area, circularity and length to width ratio was analyzed at three scales: (1) among leaves within plants, (2) among plants within species and (3) among species within functional groups (i.e., trees vs. shrubs). Results were scale dependent. Among-leaf morphological diversity was unrelated to plant height. Among-individual morphological diversity increased with the average height of each species, indicating that taller plant species express a greater range of leaf traits than shorter species. Among-species morphological diversity was higher in shrubs than in trees. We hypothesize that scale-dependent patterns in leaf trait diversity result from scale-dependent adaptations to forest environmental conditions. As trees grow from the forest floor into the canopy, they are exposed to a range of environmental conditions, which may select for a range of leaf traits through ontogeny. Conversely, shrubs never reach the forest canopy and may instead be differentially adapted to suites of environmental conditions associated with different stages of forest recovery from tree-fall disturbances. Overall results indicate that vertical patterns in leaf trait diversity exist. However, their strength and directionality are strongly scale-dependent, suggesting that different processes govern leaf shape diversity at different levels of ecological organization.     

Biogeographic constraints on the world‐wide leaf economics spectrum

Aim The world‐wide leaf economic spectrum (LES) describes tight coordination of leaf traits across global floras, reported to date as being largely independent of phylogeny and biogeography. Here, we present and test an alternative, historical perspective that predicts that biogeography places significant constraints on global trait evolution. These hypothesized constraints could lead to important deviations in leaf trait relationships between isolated floras that were influenced by different magnitudes of genetic constraint and selection. Location Global, including floristic regions of the Northern and Southern Hemispheres, eastern North America, East Asia (EAS), the Hawaiian Islands and tropical mainland floras. Methods We use a large leaf‐trait database (GLOPNET) and species native distribution data to test for variation in leaf trait relationships modulated by floristic region, controlling for climatic differences. Standardized major axis analyses were used to evaluate biogeographic effects on bivariate relationships between LES traits, including relationships of photosynthetic capacity and dark respiration rate (A_mass–R_d‐mass), leaf lifespan and mass per area ratio (LL–LMA), and photosynthetic capacity and nitrogen content (A_mass–N_mass). Results Independent of climate or biome, floras of different evolutionary histories exhibited different leaf trait allometries. Floras of the Northern Hemisphere exhibited greater rates of return on resource investment (steeper slopes for the trait relationships analysed), and the more diverse temperate EAS flora exhibited greater slopes or intercepts in leaf trait relationships, with the exception of the A_mass–N_mass relationship. In contrast to our hypothesis, plants of the floristically isolated Hawaiian Islands exhibited a similar A_mass–N_mass relationship to those of mainland tropical regions. Main conclusions Differences in leaf trait allometries among global floristic regions support a historical perspective in understanding leaf trait relationships and suggest that independent floras can exhibit different tradeoffs in resource capture strategies.     

Functional traits and trait coordination change over the life of a leaf in a tropical fern species

Premise

Plant ecological strategies are often defined by the integration of underlying traits related to resource acquisition, allocation, and growth. Correlations between key traits across diverse plants suggest that variation in plant ecological strategies is largely driven by a fast–slow continuum of plant economics. However, trait correlations may not be constant through the life of a leaf, and it is still poorly understood how trait function varies over time in long-lived leaves.

Methods

Here, we compared trait correlations related to resource acquisition and allocation across three different mature frond age cohorts in a tropical fern species, Saccoloma inaequale.

Results

Fronds exhibited high initial investments of nitrogen and carbon, but with declining return in photosynthetic capacity after the first year. In the youngest fronds, we found water-use efficiency to be significantly lower than in the oldest mature fronds due to increased transpiration rates. Our data suggest that middle-aged fronds are more efficient relative to younger, less water-use efficient fronds and that older fronds exhibit greater nitrogen investments without higher photosynthetic return. In addition, several trait correlations expected under the leaf economics spectrum (LES) do not hold within this species, and some trait correlations only appear in fronds of a specific developmental age.

Conclusions

These findings contextualize the relationship between traits and leaf developmental age with those predicted to underlie plant ecological strategy and the LES and are among the first pieces of evidence for when relative physiological trait efficiency is maximized in a tropical fern species.

     

Isometric partitioning of hydraulic conductance between leaves and stems: balancing safety and efficiency in different growth forms and habitats

Recent advances in modelling the architecture and function of the plant hydraulic network have led to improvements in predicting and interpreting the consequences of functional trait variation on CO₂ uptake and water loss. We build upon one such model to make novel predictions for scaling of the total specific hydraulic conductance of leaves and shoots (k_L and k_SH, respectively) and variation in the partitioning of hydraulic conductance. Consistent with theory, we observed isometric (slope = 1) scaling between k_L and k_SH across several independently collected datasets and a lower ratio of k_L and k_SH, termed the leaf‐to‐shoot conductance ratio (C_LSCR), in arid environments and in woody species. Isometric scaling of k_L and k_SH supports the concept that hydraulic design is coordinated across the plant. We propose that C_LSCR is an important adaptive trait that represents the trade‐off between efficiency and safety at the scale of the whole plant.     

Within‐species patterns challenge our understanding of the leaf economics spectrum

The utility of plant functional traits for predictive ecology relies on our ability to interpret trait variation across multiple taxonomic and ecological scales. Using extensive data sets of trait variation within species, across species and across communities, we analysed whether and at what scales leaf economics spectrum (LES) traits show predicted trait–trait covariation. We found that most variation in LES traits is often, but not universally, at high taxonomic levels (between families or genera in a family). However, we found that trait covariation shows distinct taxonomic scale dependence, with some trait correlations showing opposite signs within vs. across species. LES traits responded independently to environmental gradients within species, with few shared environmental responses across traits or across scales. We conclude that, at small taxonomic scales, plasticity may obscure or reverse the broad evolutionary linkages between leaf traits, meaning that variation in LES traits cannot always be interpreted as differences in resource use strategy.     

Linking leaf veins to growth and mortality rates: an example from a subtropical tree community

A fundamental goal in ecology is to link variation in species function to performance, but functional trait–performance investigations have had mixed success. This indicates that less commonly measured functional traits may more clearly elucidate trait–performance relationships. Despite the potential importance of leaf vein traits, which are expected to be related to resource delivery rates and photosynthetic capacity, there are few studies, which examine associations between these traits and demographic performance in communities. Here, we examined the associations between species traits including leaf venation traits and demographic rates (Relative Growth Rate, RGR and mortality) as well as the spatial distributions of traits along soil environment for 54 co‐occurring species in a subtropical forest. Size‐related changes in demographic rates were estimated using a hierarchical Bayesian approach. Next, Kendall's rank correlations were quantified between traits and estimated demographic rates at a given size and between traits and species‐average soil environment. Species with denser venation, smaller areoles, less succulent, or thinner leaves showed higher RGR for a wide range of size classes. Species with leaves of denser veins, larger area, cheaper construction costs or thinner, or low‐density wood were associated with high mortality rates only in small size classes. Lastly, contrary to our expectations, acquisitive traits were not related to resource‐rich edaphic conditions. This study shows that leaf vein traits are weakly, but significantly related to tree demographic performance together with other species traits. Because leaf traits associated with an acquisitive strategy such as denser venation, less succulence, and thinner leaves showed higher growth rate, but similar leaf traits were not associated with mortality, different pathways may shape species growth and survival. This study suggests that we are still not measuring some of key traits related to resource‐use strategies, which dictate the demography and distributions of species.     

Interspecific plant functional variation prevails over intraspecific variation in driving spider beta diversity

1. Non-trophic interactions between plants and animals can affect community structure and species trait composition. However, it is unclear how changes in intra- and interspecific morphological traits of plant species affect non-trophic interactions at a metacommunity scale. Additionally, whether plant evolutionary history determines taxonomic and functional diversity of plant-dwelling predators is an open question. 2. To address these gaps, this study used a published dataset with spiders dwelling exclusively on bromeliads to investigate if: (i) intra- and interspecific variability in host plant morphological traits affects spider taxonomic and functional diversity; and (ii) bromeliad trait evolution determines present-day patterns of spider trait diversity. 3. Spider and bromeliad traits were measured, and a new statistical framework was used to quantify the response of spider beta diversity to intra- and interspecific variation in bromeliad traits. In addition, bromeliad traits were decomposed across its phylogenetic tree to check whether the current variation in morphological traits of bromeliads is a result of either ancestral or recent diversification. 4. Bromeliad intraspecific variation did not affect spiders, but leaf length variation between bromeliad species had a positive effect on spider functional beta diversity. Interestingly, the most ancestral split between two subfamilies explained most of the variation in bromeliad species, which suggests that spider functional diversity could represent an outcome of bromeliad evolutionary history. 5. Overall, the results of this study suggest that interactions between plants and organisms that do not feed directly on their tissues could be shaped by plant evolutionary history, which in turn suggests that non-trophic interactions can be maintained over time.     

Functional relationships between hydraulic traits and the timing of diurnal depression of photosynthesis

The hydraulic coordination along the water transport pathway helps trees provide adequate water supply to the canopy, ensuring that water deficits are minimized and that stomata remain open for CO₂ uptake. We evaluated the stem and leaf hydraulic coordination and the linkages between hydraulic traits and the timing of diurnal depression of photosynthesis across seven evergreen tree species in the southern Andes. There was a positive correlation between stem hydraulic conductivity (k_s) and leaf hydraulic conductance (K_Leaf) across species. All species had similar maximum photosynthetic rates (A_max). The species with higher k_s and K_Leaf attained A_max in the morning, whereas the species with lower k_s and K_Leaf exhibited their A_max in the early afternoon concurrently with turgor loss. These latter species had very negative leaf water potentials, but far from the pressure at which the 88% of leaf hydraulic conductance is lost. Our results suggest that diurnal gas exchange dynamics may be determined by leaf hydraulic vulnerability such that a species more vulnerable to drought restrict water loss and carbon assimilation earlier than species less vulnerable. However, under stronger drought, species with earlier CO₂ uptake depression may increase the risk of hydraulic failure, as their safety margins are relatively narrow.     

Variation in plant functional traits across and within four species of Western Australian Banksia (Proteaceae) along a natural climate gradient

Plant traits are fundamental components of the ecological strategies of plants, relating to how plants acquire and use resources. Their study provides insight into the dynamics of species geographical ranges in changing environments. Here, we assessed the variation in trait values at contrasting points along an environmental gradient to provide insight into the flexibility of species response to environmental heterogeneity. Firstly, we identified how commonly measured functional traits of four congeneric species (Banksia baxteri, B. coccinea, B. media and B. quercifolia) varied along a longitudinal gradient in the South Western Australian Floristic Region. This regional gradient provides significant variation in moisture, temperature and soil nutrients: soil nitrogen content decreases with declining rainfall and increasing temperature. We hypothesized that (i) the regional pattern in trait–environment associations across the species would match those observed on a global scale and (ii) that the direction and slopes of the within‐species relationships would be similar to those across species for each of the measured traits. Along the regional gradient we observed strong shifts in trait values, and cross‐species relationships followed the expected trend: specific leaf area was significantly lower, and leaf N_area and seed dry mass significantly higher, at the drier end of the rainfall gradient. However, traits within species were generally not well correlated with habitat factors: we found weak patterns among populations, either due to the small ecological gradient or perhaps because fine‐scale structuring among populations (at a micro‐evolutionary scale) was low due to high gene flow within species. Understanding how species traits shift as a result of climatic influences, both at the regional (across species) and local (within species) scale, provides insight into plant adaptation to the environment. Such studies have important applications for conservation biology and population management in the face of global change.     

Trait-based community assembly of understory palms along a soil nutrient gradient in a lower montane tropical forest

Two opposing niche processes have been shown to shape the relationship between ecological traits and species distribution patterns: habitat filtering and competitive exclusion. Habitat filtering is expected to select for similar traits among coexisting species that share similar habitat conditions, whereas competitive exclusion is expected to limit the ecological similarity of coexisting species leading to trait differentiation. Here, we explore how functional traits vary among 19 understory palm species that differ in their distribution across a gradient of soil resource availability in lower montane forest in western Panama. We found evidence that habitat filtering influences species distribution patterns and shifts community-wide and intraspecific trait values. Differences in trait values among sites were more strongly related to soil nutrient availability than to variation in light or rainfall. Soil nutrient availability explained a significant amount of variation in site mean trait values for 4 of 15 functional traits. Site mean values of leaf nitrogen and phosphorus increased 37 and 64%, respectively, leaf carbon:nitrogen decreased 38%, and specific leaf area increased 29% with increasing soil nutrient availability. For Geonoma cuneata, the only species occurring at all sites, leaf phosphorus increased 34% and nitrogen:phosphorus decreased 42% with increasing soil nutrients. In addition to among-site variation, most morphological and leaf nutrient traits differed among coexisting species within sites, suggesting these traits may be important for niche differentiation. Hence, a combination of habitat filtering due to turnover in species composition and intraspecific variation along a soil nutrient gradient and site-specific niche differentiation among co-occurring species influences understory palm community structure in this lower montane forest.