Blocking then stinging as a case of two-step evolution of defensive cage architectures in herbivore-driven ecosystems.

Dense branching and spines are common features of plant species in ecosystems with high mammalian herbivory pressure. While dense branching and spines can inhibit herbivory independently, when combined, they form a powerful defensive cage architecture. However, how cage architecture evolved under mammalian pressure has remained unexplored. Here we show how dense branching and spines emerged during the age of mammalian radiation in the Combretaceae family and diversified in herbivore-driven ecosystems in the tropics. Phylogenetic comparative methods revealed that modern plant architectural strategies defending against large mammals evolved via a stepwise process. First, dense branching emerged under intermediate herbivory pressure, followed by the acquisition of spines that supported higher speciation rates under high herbivory pressure. Our study highlights the adaptive value of dense branching as part of a herbivore defence strategy and identifies large mammal herbivory as a major selective force shaping the whole plant architecture of woody plants.

Why incorporate plant architecture into trait-based ecology?

Trait-based ecology has improved our understanding of the functioning of organisms, communities, ecosystems, and beyond. However, its predictive ability remains limited as long as phenotypic integration and temporal dynamics are not considered. We highlight how the morphogenetic processes that shape the 3D development of a plant during its lifetime affect its performance. We show that the diversity of architectural traits allows us to go beyond organ-level traits in capturing the temporal and spatial dimensions of ecological niches and informing community assembly processes. Overall, we argue that consideration of multilevel topological, geometrical, and ontogenetic features provides a dynamic view of the whole-plant phenotype and a relevant framework for investigating phenotypic integration, plant adaptation and performance, and community structure and dynamics.

Petal-shaped femoral lobes facilitate gliding in orchid mantises.

To glide in forest canopies, arboreal vertebrates evolved various skin-derived aerodynamic structures, such as patagial membranes or webbing, but no comparable structure has been reported from wingless arboreal arthropods.1,2,3 Orchid mantises (Hymenopus coronatus) have been traditionally considered a textbook example of flower mimicry for ∼200 years due to their highly expanded, petal-shaped femoral lobes. However, the empirical evidence substantiating the petal-mimicry function of the femoral lobes has not been entirely conclusive.4,5,6 Observational and experimental evidence suggests that these lobes do not contribute to flower mimicry for luring pollinators6,7 and likely serve other functions.7,8 After observing their aerial escape initiated with active jumping, we hypothesized that orchid mantises can glide and that their femoral lobes are used for gliding. Through behavioral investigations and morphological analyses, we show that orchid mantis nymphs are excellent gliders, exhibiting the shallowest gliding trajectories observed in terrestrial invertebrates.9,10,11,12,13 The lobe extensions on their femoral segments are cambered airfoils, which increase the mantis projected area by ∼36% and play a vital role in the aerodynamic underpinning of the observed gliding. Despite a 165-fold increase in body mass throughout ontogeny, older female mantis nymphs maintained a persistent gliding capability. We further showed a notable 40%-56% reduction in wing loading attributed to the positive size allometry of these lobes, indicating a clear promotion of gliding throughout ontogeny. This is the first documentation of gliding-adapted "leg wings" in a wingless arthropod. The evolution of such structures is potentially common among arboreal arthropods and demands a systematic re-examination.

Why woody plant modularity through time and space must be integrated in fire research?

Different ecosystems evolved and are maintained by fire, with their vegetation hosting species with a wide diversity of persistence strategies allowing them to insulate their body and resprout new branches after fire disturbance. Changes in fire regime are predicted due to climate change, either by promoting more frequent and/or severe fires or by reducing the number of fire events due to the limitation of fuel load. Predicting the future of fire-driven ecosystems is a complex task as species' survival depends on many factors that vary in space and time. Since plants are constantly experiencing new environments as they grow through meristem development, woody plant modularity, modules morpho-physiological aspects and their integration should be considered when investigating species strategies in fire-prone ecosystems: according to their position and their tissue composition, plants' modules experience fire differently and will contribute differently to other modules and the whole plant survival, with consequences cascading over the overall vegetation structure. Growth modules may hold the key to understanding how fast plants can get protected from fire, ultimately helping us to predict which species will persist across changing fire regimes. We present an empirical example showing how different fire-return intervals translate into distinct pressures on the timing, protection and location of modules, and discuss how these can translate into modifications in the vegetation structure due to climate change.

Bark production of generalist and specialist species across savannas and forests in the Cerrado.

BACKGROUND AND AIMS: Bark allows species to survive fire, protecting their inner tissues and allowing new branches to resprout from aerial buds. Thus, bark production is likely to be selected with aerial bud protection in fire-prone ecosystems. By considering the coexistence of fire-prone and fire-free ecosystems, in addition to the different impacts of flames on different growth forms, in this study we tested whether: (1) species from areas with higher fire frequencies have a faster bark production; (2) bark growth rate differs between trees and shrubs; (3) generalists adjust their bark production according to their environment (fire-prone or fire-free ecosystems); and (4) fast bark production results in better aerial bud protection. METHODS: We sampled two different types of forests and savannas in the Cerrado and registered every woody individual with height between 1.5 and 3 m tall (directly exposed to the flames). For the 123 species registered, we sampled three different individuals in each vegetation type where the species occurred to assess their bark production and aerial bud protection. We then checked, for each species, their preferred habitat (savanna and forest specialists or generalists) and their predominant growth form. KEY RESULTS: A minimal threshold of 0.13 mm per growth unit of bark production differentiated woody communities from savannas and forests. Shrubs and trees did not differ in terms of bark growth rate, despite being exposed to the flames in a different manner. Generalist species in savannas were able to produce bark above the threshold. However, when these species were in forests they produced bark below the threshold. Finally, a higher bark growth rate accounted for a better aerial bud protection. CONCLUSIONS: Generalist species are likely to be capable of displaying plasticity in their bark production, which could be important for their success in contrasting ecosystems. The relationship between aerial bud protection and bark growth rate suggests that bark production plays an important role in protecting the dormant buds, in addition to being selected in fire-prone ecosystems.

If self-shading is so bad, why is there so much? Short shoots reconcile costs and benefits.

If trees minimize self-shading, new foliage in shaded parts of the crown should remain minimal. However, many species have abundant foliage on short shoots inside their crown. In this paper, we test the hypothesis that short shoots allow trees to densify their foliage in self-shaded parts of the crown thanks to reduced costs. Using 30 woody species in Mediterranean and tropical biomes, we estimated the contribution of short shoots to total plant foliage, calculated their costs relative to long shoots including wood cost and used 3D plant simulations calibrated with field measurements to quantify their light interception, self-shading and yield. In species with short shoots, leaves on short shoots account for the majority of leaf area. The reduced cost of short stems enables the production of leaf area with 36% less biomass. Simulations show that although short shoots are more self-shaded, they benefit the plant because they cost less. Lastly, the morphological properties of short shoots have major implications for whole plant architecture. Taken together, our results question the validity of only assessing leaf costs to understand leaf economics and call for more integrated observations at the crown scale to understand light capture strategies in woody plants.

Trunk spines of trees: a physical defence against bark removal and climbing by mammals?

BACKGROUND AND AIMS: The defensive role of spines has previously been related to leaves, young shoots and reproductive organs. However, some woody species harbour spines on their trunks where none of those organs are present. Several explanations are plausible: they could be (1) climbing aids, (2) remnants from defence of leaves or reproductive organs during an earlier development phase, or (3) an as-yet undescribed defence. Here we investigate whether they could play a role against either bark feeding or preventing climbing animals accessing food resources in the tree canopy. METHODS: We described 31 woody species with spines on their trunk, growing in a botanical garden, to test whether morphological strategies could be identified and suggest what could be their most likely function. As testing their function is difficult experimentally for large pools of species, we performed virtual experiments to evaluate the potential roles of trunk spines against bark removal and climbing animals of different sizes. We then compared for each species and their confamilial non-spiny species the nutritional profiles of leaf, bark and reproductive organs to test whether trunk spines were associated with a nutritious organ (more likely targeted by herbivores). KEY RESULTS: We identified four morphological syndromes of trunk spines. Two corresponded to already known functions (anchorage for lianas and crown defence against large ground mammals), and two strategies are newly described trait syndromes with traits suggesting a defence against bark feeding and climbing mammals. By simulation, we show how each strategy could translate into defence against debarking and prevent herbivores from climbing. CONCLUSIONS: We identified trunk spine strategies and the criteria to classify them, their most likely function and the likely feeding mode and size of animal against which different trunk spine strategies may be effective. We discuss further perspectives for testing their function and their ecological significance.

Incorporating clonality into the plant ecology research agenda.

A longstanding research divide exists in plant ecology: either focusing on plant clonality, with no ambition to address nonclonal plants, or focusing on all plants, ignoring that many ecological processes can be affected by the fact that some plants are clonal while others are not. This gap cascades into a lack of distinction and knowledge about the similarities and differences between clonal and nonclonal plants. Here we aim to bridge this gap by identifying areas that would benefit from the incorporation of clonal growth into one integrated research platform: namely, response to productivity and disturbance, biotic interactions, and population dynamics. We are convinced that this will provide a roadmap to gain valuable insights into the ecoevolutionary dynamics relevant to all plants.

A nuclear phylogenomic study of the angiosperm order Myrtales, exploring the potential and limitations of the universal Angiosperms353 probe set.

PREMISE: To further advance the understanding of the species-rich, economically and ecologically important angiosperm order Myrtales in the rosid clade, comprising nine families, approximately 400 genera and almost 14,000 species occurring on all continents (except Antarctica), we tested the Angiosperms353 probe kit. METHODS: We combined high-throughput sequencing and target enrichment with the Angiosperms353 probe kit to evaluate a sample of 485 species across 305 genera (76% of all genera in the order). RESULTS: Results provide the most comprehensive phylogenetic hypothesis for the order to date. Relationships at all ranks, such as the relationship of the early-diverging families, often reflect previous studies, but gene conflict is evident, and relationships previously found to be uncertain often remain so. Technical considerations for processing HTS data are also discussed. CONCLUSIONS: High-throughput sequencing and the Angiosperms353 probe kit are powerful tools for phylogenomic analysis, but better understanding of the genetic data available is required to identify genes and gene trees that account for likely incomplete lineage sorting and/or hybridization events.

Evolving the structure: climatic and developmental constraints on the evolution of plant architecture. A case study in Euphorbia.

Plant architecture strongly influences ecological performance, yet its role in plant evolution has not been explored in depth. By testing both phylogenetic and environmental signals, it is possible to separate architectural traits into four categories: development constraints (phylogenetic signal only); convergences (environmental dependency only); key confluences to the environmental driver (both); unknown (neither). We analysed the evolutionary history of the genus Euphorbia, a model clade with both high architectural diversity and a wide environmental range. We conducted comparative analyses of 193 Euphorbia species world-wide using 73 architectural traits, a dated phylogeny, and climate data. We identified 14 architectural types in Euphorbia based on trait combinations. We found 22 traits and three types representing convergences under climate groups, 21 traits and four types showing phylogenetic signal but no relation to climate, and 16 traits and five types with both climate and phylogenetic signals. Major drivers of architectural trait evolution likely include water stress in deserts (selected for succulence, continuous branching), frost disturbance in temperate systems (selected for simple, prostrate, short-lived shoots) and light competition (selected for arborescence). Simple architectures allowed resilience to disturbance, and frequent transitions into new forms. Complex architectures with functional specialisation developed under stable climates but have low evolvability.

The Neglected Belowground Dimension of Plant Dominance.

Dominants are key species that shape ecosystem functioning. Plant dominance is typically assessed on aboveground features. However, belowground, individual species may not scale proportionally in relation to their aboveground dimension. This is especially important in ecosystems where most biomass is allocated belowground, including grassy and shrubby biomes.

Savanna tree evolutionary ages inform the reconstruction of the paleoenvironment of our hominin ancestors.

Ideas on hominin evolution have long invoked the emergence from forests into open habitats as generating selection for traits such as bipedalism and dietary shifts. Though controversial, the savanna hypothesis continues to motivate research into the palaeo-environments of Africa. Reconstruction of these ancient environments has depended heavily on carbon isotopic analysis of fossil bones and palaeosols. The sparsity of the fossil record, however, imposes a limit to the strength of inference that can be drawn from such data. Time-calibrated phylogenies offer an additional tool for dating the spread of savanna habitat. Here, using the evolutionary ages of African savanna trees, we suggest an initial tropical or subtropical expansion of savanna between 10 and 15 Ma, which then extended to higher latitudes, reaching southern Africa ca. 3 Ma. Our phylogenetic estimates of the origin and latitudinal spread of savannas broadly correspond with isotopic age estimates and encompass the entire hominin fossil record. Our results are consistent with the savanna hypothesis of early hominin evolution and reignite the debate on the drivers of savanna expansion. Our analysis demonstrates the utility of phylogenetic proxies for dating major ecological transitions in geological time, especially in regions where fossils are rare or absent or occur in discontinuous sediments.

Developmental constraints and resource environment shape early emergence and investment in spines in saplings.

BACKGROUND AND AIMS: Herbivory by large mammals imposes a critical recruitment bottleneck on plants in many systems. Spines defend plants against large herbivores, and how early they emerge in saplings may be one of the strongest predictors of sapling survival in herbivore-rich environments. Yet little effort has been directed at understanding the variability in spine emergence across saplings. METHODS: We present a multispecies study examining whether and how sapling size, spine type and species' environmental niche (light and precipitation environment) influence early emergence and biomass investment in spines. A phylogenetically diverse pool of 45 species possessing different spine types (spines, prickles and thorns; that are derived from distinct plant organs: leaf, epidermis or cortex, and branch, respectively), were grown under common-garden conditions, and patterns of spine emergence and biomass allocation to spines at 5 and 15 weeks after transplanting were characterized. KEY RESULTS: Spine type and species' resource niche were the main factors driving early emergence and investment patterns. Spines emerged earliest in leaf spine-bearing species, and latest in thorn-bearing species. The probability of early spine emergence increased with decreasing precipitation, and was greater in species from open than from closed habitats. Sapling investment in spines changed with plant mass but was contingent on spine type and habitat type. CONCLUSIONS: Different spine types have strikingly different timing of expression, suggesting that developmental origins of spines play a critical role in sapling defences. Furthermore, species from different precipitation and light environments (open vs. closed habitats) showed contrasting patterns of early spine expression, suggesting that resource limitation in their native range may have driven divergent evolution of early defence expression.

Prolonged milk provisioning in a jumping spider.

Lactation is a mammalian attribute, and the few known nonmammal examples have distinctly different modalities. We document here milk provisioning in a jumping spider, which compares functionally and behaviorally to lactation in mammals. The spiderlings ingest nutritious milk droplets secreted from the mother's epigastric furrow until the subadult stage. Milk is indispensable for offspring survival in the early stages and complements their foraging in later stages. Maternal care, as for some long-lived vertebrates, continues after the offspring reach maturity. Furthermore, a female-biased adult sex ratio is acquired only when the mother is present. These findings demonstrate that mammal-like milk provisioning and parental care for sexually mature offspring have also evolved in invertebrates, encouraging a reevaluation of their occurrence across the animal kingdom, especially in invertebrates.

Human impacts in African savannas are mediated by plant functional traits.

Tropical savannas have a ground cover dominated by C4 grasses, with fire and herbivory constraining woody cover below a rainfall-based potential. The savanna biome covers 50% of the African continent, encompassing diverse ecosystems that include densely wooded Miombo woodlands and Serengeti grasslands with scattered trees. African savannas provide water, grazing and browsing, food and fuel for tens of millions of people, and have a unique biodiversity that supports wildlife tourism. However, human impacts are causing widespread and accelerating degradation of savannas. The primary threats are land cover-change and transformation, landscape fragmentation that disrupts herbivore communities and fire regimes, climate change and rising atmospheric CO2 . The interactions among these threats are poorly understood, with unknown consequences for ecosystem health and human livelihoods. We argue that the unique combinations of plant functional traits characterizing the major floristic assemblages of African savannas make them differentially susceptible and resilient to anthropogenic drivers of ecosystem change. Research must address how this functional diversity among African savannas differentially influences their vulnerability to global change and elucidate the mechanisms responsible. This knowledge will permit appropriate management strategies to be developed to maintain ecosystem integrity, biodiversity and livelihoods.

Steal the light: shade vs fire adapted vegetation in forest-savanna mosaics.

Shade cast by trees, which suppresses grass growth, and fire fuelled by grass biomass, which prevents tree sapling establishment, are mutually exclusive and self-reinforcing drivers of biome distribution in savanna-forest mosaics. We investigated how shade depth, represented by canopy leaf area index (LAI), is generated by adult trees across savanna-forest boundaries and how a shade gradient filters tree functioning, and grass composition and biomass. Forest trees exerted greater shading through increased stem density and greater light interception per unit biomass. A critical transition at LAI c. 1.5 was linked to tree shifts from savanna to forest species, functional shifts from fire-tolerant to light-competitive species, and grass composition shifts from C4 to C3 pathways. A second transition to grass fuel loads too low to support fires, occurred at a lower canopy density (LAI > 0.5), accompanied by shifts in C4 subtype dominance. This pattern suggests that shade suppression of grass biomass is an essential first step for the maintenance of alternative stable states.

Geometagenomics illuminates the impact of agriculture on the distribution and prevalence of plant viruses at the ecosystem scale.

Disease emergence events regularly result from human activities such as agriculture, which frequently brings large populations of genetically uniform hosts into contact with potential pathogens. Although viruses cause nearly 50% of emerging plant diseases, there is little systematic information about virus distribution across agro-ecological interfaces and large gaps in understanding of virus diversity in nature. Here we applied a novel landscape-scale geometagenomics approach to examine relationships between agricultural land use and distributions of plant-associated viruses in two Mediterranean-climate biodiversity hotspots (Western Cape region of South Africa and Rhône river delta region of France). In total, we analysed 1725 geo-referenced plant samples collected over two years from 4.5 × 4.5 km2 grids spanning farmlands and adjacent uncultivated vegetation. We found substantial virus prevalence (25.8-35.7%) in all ecosystems, but prevalence and identified family-level virus diversity were greatest in cultivated areas, with some virus families displaying strong agricultural associations. Our survey revealed 94 previously unknown virus species, primarily from uncultivated plants. This is the first effort to systematically evaluate plant-associated viromes across broad agro-ecological interfaces. Our findings indicate that agriculture substantially influences plant virus distributions and highlight the extent of current ignorance about the diversity and roles of viruses in nature.