Correlational selection and genetic architecture shape the evolution of the leaf economics spectrum in a perennial grass

SummaryThe leaf economics spectrum (LES) has been an organizing framework of plant functional ecology for the past decade. TheLESdescribes a set of trade‐offs among traits related to plant carbon balance. Species with a long leaf life span (LLS) invest additional material for leaf protection and structural support and consequently tend to have a lower leaf photosynthetic rate per unit mass than species with a shorterLLS.While theLESis most apparent in comparing species with extreme differences in their traits, it has nonetheless been adopted as a general explanation of leaf trait variation at all scales and in all plants. It highlights the ‘trait‐based’ approach to plant ecology, which has generally used a small set of traits to predict whole organism and even whole ecosystem attributes. Few studies have investigated the relationships betweenLEStraits and organismal attributes not directly related to carbon economy.We explored theLESin 32 deciduous woody species ofViburnum(Adoxaceae). We found no evidence for any mass‐basedLEStrade‐offs. Rather, on an area basis, photosynthetic rates were positively correlated with leaf mass per area (LMA); higherLMAwas associated with greater investment in photosynthetic tissue, with most of the variation due to changes in the thickness of photosynthetic mesophyll.Species’ meanLLSvaried between 19 and 26 weeks and was not correlated with otherLEStraits. Instead,LLSwas strongly associated with the diverse set of whole‐plant branching patterns inViburnum. In the most common growth pattern,LLSwas significantly correlated with flowering time, because branches end in terminal inflorescences, and all leaves and inflorescences are pre‐formed in overwintering buds.Synthesis. Plants may recover the cost of their leaves early in the growing season, allowingLLSto vary independently of the plant carbon budget. In deciduous species,LLSmay be strongly influenced by whole plant architecture, which, inViburnum, is evolutionarily conserved. In general, positive area‐basedLEStrait relationships will limit the relevance ofLLSto this spectrum and allowLLSto vary for reasons that are not directly related to carbon economy.

The leaf economics spectrum ranges from cheap, short-lived leaves to expensive, long-lived leaves. Species with low leaf mass per area (LMA) and short leaf life span tend to be fast growing and shade intolerant (early successional), whereas species with high LMA and long leaf life span tend to be slow growing and shade tolerant (late successional). However, we have limited understanding of how different leaf mass components (e.g., metabolically active photosynthetic components vs. structural toughness components) contribute to variation in LMA and other leaf economics spectrum traits. Here, we develop a model of plant community dynamics in which species differ in just two traits, photosynthetic and structural LMA components, and we identify optimal values of these traits for early- and late-successional species. Most of the predicted increase in LMA from early- to late-successional species was due to structural LMA. Photosynthetic LMA did not differ consistently between early- and late-successional species, but the photosynthetic LMA to structural LMA ratio declined from early- to late-successional species. Early-successional species had high rates of instantaneous return on leaf mass investment, whereas late-successional species had high lifetime return. Our results provide theoretical support for the primary role of structural (rather than photosynthetic) LMA variation in driving relationships among leaf economics spectrum traits.

Photosynthetic acclimation of two co-occurring deciduous oaks (Quercus petraea and Quercus pyrenaica) to a natural light gradient was studied during one growing season. In the spring of 2003, 90 seedlings per species were planted along a transect resulting from a dense Pinus sylvestris stand, an adjacent thinned area and a 10-m-wide firebreak (16.5–60.9% Global Site Factor (GSF)). In two dates of the following summer, we measured leaf gas exchange, carboxylation efficiency (CE), chlorophyll and nitrogen content, light–response curves of chlorophyll a fluorescence parameters, and leaf mass per area (LMA). Summer was mild, as evidenced by leaf predawn water potential (Ψpd), which reduced the interactive effect of water stress on the response of seedlings to light. Q. pyrenaica had higher LMA, CE, stomatal conductance (g s max) and photosynthesis per unit area $$(A_{\max }^a )$$ than Q. petraea at all growth irradiances. $$A_{\max }^a$$ , LMA, g s max and electron transport rate (ETR) all increased with light availability (GSF) in a similar fashion in both species. Light had also a clear effect on the organization of Photosystem II (PS II), as deduced by chlorophyll a fluorescence curves. Chlorophyll concentration (Chlm) decreased with increasing light availability in Q. pyrenaica but it did not in Q. petraea. Seedlings of Q. petraea acclimated to higher irradiances showed a greater non-photochemical quenching (NPQ) than those of Q. pyrenaica. This suggests a higher susceptibility to high light in Q. petraea, which would be consistent with a better adaptation to shade, inferred from the lower LMA or the lower rate of photosynthesis.

The leaf economic spectrum (LES) describes a set of universal trade-offs between leaf mass per area (LMA), leaf nitrogen (N), leaf phosphorus (P) and leaf photosynthesis that influence patterns of primary productivity and nutrient cycling. Many questions regarding vegetation-climate feedbacks can be addressed with a better understanding of LES traits and their controls. Remote sensing offers enormous potential for generating large-scale LES trait data. Yet so far, canopy studies have been limited to imaging spectrometers onboard aircraft, which are rare, expensive to deploy and lack fine-scale resolution. In this study, we measured VNIR (visible-near infrared (400–1050 nm)) reflectance of individual sun and shade leaves in 7 one-ha tropical forest plots located along a 1200–2000 mm precipitation gradient in West Africa. We collected hyperspectral imaging data from 3 of the 7 plots, using an octocopter-based unmanned aerial vehicle (UAV), mounted with a hyperspectral mapping system (450–950 nm, 9 nm FWHM). Using partial least squares regression (PLSR), we found that the spectra of individual sun leaves demonstrated significant (p < 0.01) correlations with LMA and leaf chemical traits: r2 = 0.42 (LMA), r2 = 0.43 (N), r2 = 0.21 (P), r2 = 0.20 (leaf potassium (K)), r2 = 0.23 (leaf calcium (Ca)) and r2 = 0.14 (leaf magnesium (Mg)). Shade leaf spectra displayed stronger relationships with all leaf traits. At the airborne level, four of the six leaf traits demonstrated weak (p < 0.10) correlations with the UAV-collected spectra of 58 tree crowns: r2 = 0.25 (LMA), r2 = 0.22 (N), r2 = 0.22 (P), and r2 = 0.25 (Ca). From the airborne imaging data, we used LMA, N and P values to map the LES across the three plots, revealing precipitation and substrate as co-dominant drivers of trait distributions and relationships. Positive N-P correlations and LMA-P anticorrelations followed typical LES theory, but we found no classic trade-offs between LMA and N. Overall, this study demonstrates the application of UAVs to generating LES information and advancing the study and monitoring tropical forest functional diversity.

Variability in traits forming the Leaf Economics Spectrum (LES) among and within crop species plays a key role in governing agroecosystem processes. However, studies evaluating the extent, causes, and consequences of within-species variation in LES traits for some of the world’s most common crops remain limited. This study quantified variations in nine leaf traits measured across 90 vines of five common wine grape (Vitis vinifera L.) varieties at two growth stages (post-flowering and veraison). Grape traits in these varieties covary along an intraspecific LES, in patterns similar to those documented in wild plants. Across the five varieties evaluated here, high rates of photosynthesis (A) and leaf nitrogen (N) concentrations were coupled with low leaf mass per area (LMA), whereas the opposite suite of traits defined the “resource-conserving end” of this intraspecific LES in grape. Variety identity was the strongest predictor of leaf physiological (A) and morphological traits (i.e., leaf area and leaf mass), whereas leaf chemical traits and LMA were best explained by growth stage. All five varieties expressed greater resource-conserving trait syndromes (i.e., higher LMA, lower N, and lower Amass) later in the growing season. Traits related to leaf hydraulics, including instantaneous water-use efficiency (WUE), were unrelated to LES and other resource capture traits, and were better explained by spatial location. These results highlight the relative contributions of genetic, developmental, and phenotypic factors in structuring trait variation in the five wine grape varieties evaluated here, and point to a key role of domestication in governing trait relationships in the world’s crops.

There is tremendous interspecific variability in O3 sensitivity among C3 species, but variation among C4 species has been less clearly documented. It is also unclear whether stomatal conductance and leaf structure such as leaf mass per area (LMA) determine the variation in sensitivity to O3 across species. In this study, we investigated leaf morphological, chemical, and photosynthetic responses of 22 genotypes of four C4 bioenergy species (switchgrass, sorghum, maize, and miscanthus) to elevated O3 in side‐by‐side field experiments using free‐air O3 concentration enrichment (FACE). The C4 species varied largely in leaf morphology, physiology, and nutrient composition. Elevated O3 did not alter leaf morphology, nutrient content, stomatal conductance, chlorophyll fluorescence, and respiration in most genotypes but reduced net CO2 assimilation in maize and photosynthetic capacity in sorghum and maize. Species with lower LMA and higher stomatal conductance tended to show greater losses in photosynthetic rate and capacity in elevated O3 compared with species with higher LMA and lower stomatal conductance. Stomatal conductance was the strongest determinant of leaf photosynthetic rate and capacity. The response of both area‐ and mass‐based leaf photosynthetic rate and capacity to elevated O3 were not affected by LMA directly but negatively influenced by LMA indirectly through stomatal conductance. These results demonstrate that there is significant variation in O3 sensitivity among C4 species with maize and sorghum showing greater sensitivity of photosynthesis to O3 than switchgrass and miscanthus. Interspecific variation in O3 sensitivity was determined by direct effects of stomatal conductance and indirect effects of LMA. This is the first study to provide a test of unifying theories explaining variation in O3 sensitivity in C4 bioenergy grasses. These findings advance understanding of O3 tolerance in C4 grasses and could aid in optimal placement of diverse C4 bioenergy feedstock across a polluted landscape.

<p>Leaf construction can be costly to plants with a short leaf lifespan (LLS), with a necessity to pay back the investment in leaf deployment. Costs of leaf construction are often measured as leaf mass per area (LMA) and the deciduousness strategies (deciduous, semideciduous or evergreen) used as proxy to LLS (evergreen species having longest leaf duration compared to semideciduous and deciduous species). According to the leaf economic spectrum theory, a positive correlation between LMA and LLS is expected, with evergreen species having higher LMA than deciduous species. Nonetheless, aridity constraints increase leaf maintenance costs in plants, and the deciduous strategy turns to be the most common leaf exchange behavior in Seasonally Dry Tropical Forests (SDTF). In this study we are testing if the relation of LMA and LLS is influenced by aridity in SDTF, using the length of growing season (LOS) as a proxy of overall response for drought. We expect that LMA: LLS relationship will become stronger towards driest sites. The caatinga vegetation is the largest SDTF in the New World, covering an area of ca. 850,000 km<sup>2</sup> located in North-eastern Brazil. Although the region is characterized by having low amount of rainfall (<1100 mm per year), there is a gradient of aridity that affects plants living across these areas. We applied the near-surface remote method trough the usage of phenocams to simultaneously monitor leaf phenology of 27 tree species from four areas of Caatinga, in a gradient of aridity ranging from 387 mm to 800 mm total annual rainfall. For these species, we used the green chromatic coordinate (Gcc) time series to calculate the phenological transition dates of Start (SOS) and End (EOS) and the Length (LOS) of Growing Season, during two to four growing seasons, from 2017 to 2021. LOS presented high variability among species, ranging from 143 days for <em>Manihot pseudoglaziovii</em> and 314 days for <em>Aspidosperma pyrifolium</em>. In general, LOS tend to be shorter for species towards driest sites and analyes of the relation between LMA and LLS are suggesting trade-offs important to understand the acquisitive strategies of plants from semi-arid vegetation with implications for carbon fluxes.</p><p>Supported by FAPESP (#2019/11835-2); FAPESP-NERC (FAPESP #2015/50488-5; #2017/17380-1), by CNPq and FACEPE (Caatinga-FLUX, #483223/2011-5 and Caatinga-FLUX Fase 2, #0062-1.07/15); UNESP CAPES-PrInt Program (grant #88887.310463/2018-00; schoolarship ##88887.512218/2020-00) and CNPq productitivity fellowship (#428055/2018-4).</p>

Canopy structure influences forest productivity through its effects on the distribution of radiation and the light-induced changes in leaf physiological traits. Due to the difficulty of accessing and measuring forest canopies, few field-based studies have quantitatively linked these divergent scales of canopy functioning. The objective of our study was to investigate how canopy structure affects light profiles within a forest canopy and whether leaves of mature trees adjust morphologically and biochemically to the light environments characteristic of canopies with different structural complexity. We used a combination of light detection and ranging (LiDAR) data and hemispherical photographs to quantify canopy structure and light environments, respectively, and a telescoping pole to sample leaves. Leaf mass per area (LMA), nitrogen on an area basis (Narea) and chlorophyll on a mass basis (Chlmass) were measured in red maple (Acer rubrum), american beech (Fagus grandifolia), white pine (Pinus strobus), and northern red oak (Quercus rubra) at different heights in plots with similar leaf area index but contrasting canopy complexity (rugosity). We found that more complex canopies had greater porosity and reduced light variability in the midcanopy while total light interception was unchanged relative to less complex canopies. Leaf phenotypes of F. grandifolia, Q. rubra and P. strobus were more sun-acclimated in the midstory of structurally complex canopies while leaf phenotypes of A. rubrum were more shade-acclimated (lower LMA) in the upper canopy of more complex stands, despite no differences in total light interception. Broadleaf species showed further differences in acclimation with increased Narea and reduced Chlmass in leaves with higher LMA, while P. strobus showed no change in Narea and Chlmass with higher LMA. Our results provide new insight on how light distribution and leaf acclimation in mature trees might be altered when natural and anthropogenic disturbances cause structural changes in the canopy.

Abstract:The relationship between leaf longevity and other leaf traits was compared among different life-form categories (trees, herbs, climbers and epiphytes) of 101 plant species in a tropical montane forest on Mt. Halimun, West Java, Indonesia. We applied the Cox proportional hazards regression to estimate the leaf longevity of each species from 30 mo of census data. We examined whether estimated longevity was explained by either species life-form categories, taxonomic groupings (eudicots, monocots, magnoliids and chloranthales, and ferns) or such leaf traits as leaf area, leaf mass per area (LMA), mass-based leaf nitrogen, penetrometer reading, condensed-tannin-free total phenolics and condensed tannin. There was a wide-ranged interspecific variation in leaf longevity, mostly 10–50 mo, similarly across life-form categories. LMA showed a strong positive influence on leaf longevity. We found that relationships between leaf longevity and some leaf traits were different among various life forms. Trees tended to have high LMA, while climbers tended to have low LMA at the same leaf longevity. We hypothesize that such difference among life forms reflects shoot architecture characteristics. Multi-shoot trees with branching architecture need to have self-supporting leaves, whereas semi-epiphytic climbers can maintain relatively low biomass investment to leaves hanging or relying upon the mechanical support from host plants.

Large variations are found in leaf morphology and physiology across species in nature, reflecting diversity in carbon fixation and growth strategies. These variations in leaf traits are not random; rather, they are tightly coordinated with each other. Leaf traits can be expressed per leaf dry mass or per leaf area. A leaf-mass basis reflects leaf economics, i.e., revenues and expenditures per unit investment of biomass, while a leaf-area basis reflects fluxes in relation to surfaces. Leaf N and P concentrations, and photosynthetic and respiration rates – all considered on a mass basis, are negatively correlated with leaf mass per area (LMA) whilst leaf lifespan is positively correlated with LMA. These correlations are summarized into a single major axis called the “leaf economics spectrum” that runs from “quick-return” to “slow-return” species. On the other hand, correlations among area-based traits are less consistent and less understood in relation to leaf economy. LMA was positively correlated with leaf N content but mostly independent from photosynthetic rates per unit leaf area. Given that N is an essential element in photosynthetic proteins and thus photosynthesis, clarifying the mechanisms why the efficiency of photosynthesis (photosynthesis per unit N) decreases with LMA is a major concern in understanding the correlations among area-based traits in relation to leaf economy. Currently available data suggest that greater amounts of cell wall are required for long-lived leaves, which reduces the efficiency of photosynthesis by lowering (1) the fraction of leaf N invested in photosynthetic proteins and (2) CO2 diffusion rates through thicker and denser mesophyll cell walls. These physiological and structural constraints are a fundamental mechanism underpinning the general correlations among leaf economic traits.

Plants use physical barriers and chemical compounds to defend themselves against natural enemies. For instance, tough leaves are considered to be better defended than soft leaves, part of a spectrum of defences defined by functional traits such as leaf chemistry, lifespan, toughness and leaf mass per area (LMA). Plants with longer lifespans, which invest more in leaf tissue and higher LMA, typically feature robust constitutive defences (e.g. toughness, thickness and dense cell walls). In contrast, plants with lower LMA and more leaf nutrients often invest more in induced defences. Leaf traits represent an environmental filter for foliar endophytic fungi (FEF), which may play an additional role in plant defence. Our overarching assumption is that FEF alter leaf fate by interacting directly or indirectly with leaf traits, thus shaping successive FEF colonization, development of leaf traits and response to plant enemies. To evaluate this hypothesis, we inoculated seedlings of seven tropical tree species, which varied in leaf traits, with natural and diverse endophyte communities. We characterized leaves by low FEF load (E‐low) and high FEF load (E‐high) based on culturing and culture‐free amplicon sequencing. We measured leaf removal by leaf‐cutter ants and leaf necrosis due to a generalist fungal pathogen. Across the experiment, we observed greater leaf removal from the E‐low treatment compared to the E‐high treatment, but no difference in pathogen damage. Dimensionality reduction of leaf functional traits (i.e. LMA, toughness, thickness and anthocyanin levels) revealed relationships among traits and distinct host species characteristics. All leaf functional traits had significant correlations with FEF community composition. In turn, indicator species analyses revealed functional traits and taxonomic identities of FEF associated with high and low leaf damage by natural enemies. Our findings highlight the complex dynamics of plant‐herbivore‐pathogen relationships and underscore the importance of endophytes as a potentially low‐cost, preemptive defence strategy for plants, especially during early growth stages. These insights shed light on the nuanced role of endophytes in plant ecology. Further, they open avenues for future research, particularly in exploring strategic resource allocation in plants and the specific contributions of endophytes to plant resilience. Read the free Plain Language Summary for this article on the Journal blog.

Summary 1 Leaf life span (LL) and leaf mass per area (LMA) are fundamental traits in the carbon economy of plants, representing the investment required per unit leaf area (LMA) and the duration of the resulting benefit (LL). Species on dry and infertile soils converge towards higher LMA. It has been generally assumed that this allows species from low-resource habitats to achieve longer average leaf life spans, as LMA and LL are often correlated. 2 Leaf life span and LMA were measured for 75 perennial species from eastern Australia. Species were sampled from nutrient-rich and nutrient-poor sites within high and low rainfall regions. LL and LMA were positively correlated across species within each site. In addition, evolutionary divergences in LL and LMA were correlated within each site, indicating that cross-species relationships were not simply driven by differences between higher taxonomic groups. 3 Within a rainfall zone, LL–LMA combinations shifted as expected along common axes of variation such that species on poorer soils had higher LMA and longer LL, but significantly so only at high rainfall. 4 Low rainfall species were expected to have shorter LL at a given LMA or, equally, require higher LMA to achieve a given LL, i.e. shift to a parallel axis of variation, and this was observed on both nutrient-rich and nutrient-poor soils. On average, 30% higher LMA was seemingly required at dry sites to achieve a given LL. Thus, convergence towards higher LMA has different consequences for leaf life span in dry and nutrient-poor habitats. 5 The broad shifts in LL–LMA combinations between site types were also seen when comparing closely related species-pairs (phylogenetically independent contrasts) occurring on nutrient-rich and nutrient-poor soils (within each rainfall zone), and at high- and low-rainfall sites (at each soil nutrient level).

SummaryTheory suggests that the dominance of resprouting and seeding, two key mechanisms through which plants persist with recurrent fire, both depend on other traits and vary with fire regime. However, these patterns remain largely untested over broad scales.We analysed the relationships between mean fire frequency, derived from MODIS satellite data, and resprouting and seeding strategies, respectively, for c. 10 000 woody and herbaceous species in Australia. We tested whether leaf economics traits differed among these strategies.Probability of resprouting exhibits a monotonic increase with fire frequency for woody plants; for herbaceous plants, a hump‐shaped relationship is observed. Probability of seeding exhibits a hump shape with fire frequency in woody plants. In herbaceous plants, probability of resprouting was associated with higher leaf mass per area (LMA), and probability of seeding with lower LMA. A broader range of leaf investment strategies occurred in woody plants.Our findings provide the largest empirical support to date for theory connecting fire response strategy to fire frequency. Woody seeders appear constrained by immaturity and senescence risk. Herbaceous and woody seeders showed different placements along the leaf economics spectrum, suggesting an important interaction between growth form and growth rate for seeders.

Microbial inoculations or 'biofertilizers' represent novel contributions to sustainable agriculture. While belowground mechanisms surrounding how biofertilizers enhance crop production are well described, their role in aboveground trait expression remains less well explored. We quantified infraspecific variation in leaf economics spectrum (LES) traits in response to 10 biofertilizer treatments in basil (Ocimum basiclicum) cultivated under hydroponic conditions. Multiple physiological (i.e. maximum photosynthesis rates (A), dark respiration (R), and leaf-level light compensation points) and morphological (i.e. leaf mass per area (LMA) and leaf thickness) traits varied significantly across microbial treatments. Following treatments, basil plants differentiated from one another along an infraspecific LES, with certain plants expressing more resource-acquiring LES trait values (i.e. high A, R, leaf N, and low LMA), versus others that expressed the opposite suite of resource-conserving LES trait values. Infraspecific trait covariation largely matched LES patterns observed among plants globally. Bivariate and multivariate trait analyses further revealed that certain treatments-namely those including closely related Bacillus and Brevibacillus species strains-increased leaf resource capture traits such as A and leaf N. Biofertilizers influence plant performance through a role in moderating infraspecific leaf trait variation, thereby suggesting aboveground leaf traits may be used to diagnose optimal biofertilizer formulations in basil and other crops.

Assessing the relationship between trait-based and horticultural classifications of plant responses to drought