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.

Intensive cycling of nickel in a New Caledonian forest dominated by hyperaccumulator trees.

The hyperaccumulator Pycnandra acuminata is a New Caledonian rainforest tree known to have the highest concentration of nickel in any living organism, with 25 wt% nickel in its latex. All trees (with a diameter of >10 cm) and soil profiles in a 0.25-hectare permanent plot were sampled to assess the biogeochemical compartmentalisation of nickel in a dense stand of P. acuminata trees. Nickel stable isotope analysis permitted insights into the cycling of nickel in this ecosystem. The total tree biomass of the plot was calculated to be 281 tonnes ha-1 , which contained 0.44 kg of cobalt, 49.1 kg of manganese, 257 kg of nickel and 6.76 kg of zinc. Nickel stable isotope analysis identified the biotic origin of the nickel in the soil upper layers, with P. acuminata shoots enriched in lighter nickel isotopes. The δ60 Ni latex signature suggests that long-distance transport, radial xylem and phloem loading are at play in P. acuminata.

Novel Insights Into the Hyperaccumulation Syndrome in Pycnandra (Sapotaceae).

The discovery of nickel hyperaccumulation, in Pycnandra acuminata, was the start of a global quest in this fascinating phenomenon. Despite recent advances in the physiology and molecular genetics of hyperaccumulation, the mechanisms and tolerance of Ni accumulation in the most extreme example reported to date, P. acuminata, remains enigmatic. We conducted a hydroponic experiment to establish Ni tolerance levels and translocation patterns in roots and shoots of P. acuminata, and analyzed elemental partitioning to gain insights into Ni regulation. We combined a phylogeny and foliar Ni concentrations to assess the incidence of hyperaccumulation within the genus Pycnandra. Hydroponic dosing experiments revealed that P. acuminata can resist extreme Ni concentrations in solution (up to 3,000 µM), and dosing at 100 µM Ni was beneficial to growth. All plant parts were highly enriched in Ni, but the latex had extreme Ni concentrations (124,000 µg g-1). Hyperaccumulation evolved independently in only two subgenera and five species of the genus Pycnandra. The extremely high level of Ni tolerance is posited to derive from the unique properties of laticifers. The evolutionary and ecological significance of Ni hyperaccumulation in Pycnandra is discussed in light of these findings. We suggest that Ni-rich laticifers might be more widespread in the plant kingdom and that more investigation is warranted.

Nickel hyperaccumulation in New Caledonian Hybanthus (Violaceae) and occurrence of nickel-rich phloem in Hybanthus austrocaledonicus.

BACKGROUND AND AIMS: Hybanthus austrocaledonicus (Violaceae) is a nickel (Ni) hyperaccumulator endemic to New Caledonia. One of the specimens stored at the local herbarium had a strip of bark with a remarkably green phloem tissue attached to the sheet containing over 4 wt% Ni. This study aimed to collect field samples from the original H. austrocaledonicus locality to confirm the nature of the green 'nickel-rich phloem' in this taxon and to systematically assess the occurrence of Ni hyperaccumulation in H. austrocaledonicus and Hybanthus caledonicus populations. METHODS: X-ray fluorescence spectroscopy scanning of all collections of the genus Hybanthus (236 specimens) was undertaken at the Herbarium of New Caledonia to reveal incidences of Ni accumulation in populations of H. austrocaledonicus and H. caledonicus. In parallel, micro-analytical investigations were performed via synchrotron X-ray fluorescence microscopy (XFM) and scanning electron microscopy with X-ray microanalysis (SEM-EDS). KEY RESULTS: The extensive scanning demonstrated that Ni hyperaccumulation is not a characteristic common to all populations in the endemic Hybanthus species. Synchrotron XFM revealed that Ni was exclusively concentrated in the epidermal cells of the leaf blade and petiole, conforming with the majority of (tropical) Ni hyperaccumulator plants studied to date. SEM-EDS of freeze-dried and frozen-hydrated samples revealed the presence of dense solid deposits in the phloem bundles that contained >8 wt% nickel. CONCLUSIONS: The occurrence of extremely Ni-rich green phloem tissues appears to be a characteristic feature of tropical Ni hyperaccumulator plants.

Retracing the contours of the early angiosperm environmental niche.

BACKGROUND AND AIMS: Our aim was to understand the environmental conditions of the emergence and radiation of early angiosperms. Such a question has long remained controversial because various approaches applied in the past have drawn conflicting images of early angiosperm ecology. METHODS: We provided a new perspective on the question by using support vector machines to model the environmental niche of 51 species belonging to ten genera of extant lineages that diverged early during angiosperm evolution (basal angiosperms). Then, we analysed the resulting pattern of niche overlap and determined whether this pattern deviates from what would be expected on the basis of a null model or whether it might mirror a legacy of a common primitive niche based on a phylogenetic reconstruction. KEY RESULTS: The niche of three-quarters of the species and all genera converged towards tropical montane cloud forests (TMCFs). The latitudinal pattern of basal angiosperm richness indeed culminated in the tropics, and the elevational pattern revealed a humpback curve peaking between 2000 m and 3500 m when accounting for the effect of area. At first glance, this diversity pattern does not significantly differ from null predictions. However, we revealed a tendency for the basal-most taxa to occur in TMCFs so that phylogenetic reconstructions indicated that the niche of the common ancestor of the sampled basal angiosperms had a probability of 0.85-0.93 to overlap with TMCFs. CONCLUSIONS: Our new approach indicates that the environmental convergence of extant basal angiosperms towards TMCFs would reflect a legacy of an ancestral niche from which the least basal taxa would have diverged following a random pattern under geometric constraints.

Similar hydraulic efficiency and safety across vesselless angiosperms and vessel-bearing species with scalariform perforation plates.

The evolution of xylem vessels from tracheids is put forward as a key innovation that boosted hydraulic conductivity and photosynthetic capacities in angiosperms. Yet, the role of xylem anatomy and interconduit pits in hydraulic performance across vesselless and vessel-bearing angiosperms is incompletely known, and there is a lack of functional comparisons of ultrastructural pits between species with different conduit types. We assessed xylem hydraulic conductivity and vulnerability to drought-induced embolism in 12 rain forest species from New Caledonia, including five vesselless species, and seven vessel-bearing species with scalariform perforation plates. We measured xylem conduit traits, along with ultrastructural features of the interconduit pits, to assess the relationships between conduit traits and hydraulic efficiency and safety. In spite of major differences in conduit diameter, conduit density, and the presence/absence of perforation plates, the species studied showed similar hydraulic conductivity and vulnerability to drought-induced embolism, indicating functional similarity between both types of conduits. Interconduit pit membrane thickness (Tm) was the only measured anatomical feature that showed a relationship to significant vulnerability to embolism. Our results suggest that the incidence of drought in rain forest ecosystems can have similar effects on species bearing water-conducting cells with different morphologies.

Evolution of Plant Architecture, Functional Diversification and Divergent Evolution in the Genus Atractocarpus (Rubiaceae) for New Caledonia.

The diversification of ecological roles and related adaptations in closely related species within a lineage is one of the most important processes linking plant evolution and ecology. Plant architecture offers a robust framework to study these processes as it can highlight how plant structure influences plant diversification and ecological strategies. We investigated a case of gradual evolution of branching architecture in Atractocarpus spp. (Rubiaceae), forming a monophyletic group in New Caledonia that has diversified rapidly, predominantly in rainforest understory habitats. We used a transdisciplinary approach to depict architectural variations and revealed multiple evolutionary transitions from a branched (Stone's architectural model) to a monocaulous habit (Corner's architectural model), which involved the functional reduction of branches into inflorescences. We propose an integrative functional index that assesses branching incidence on functional traits influencing both assimilation and exploration functions. We showed that architectural transitions correlate with ecologically important functional traits. Variation in ecologically important traits among closely relatives, as supported by the architectural analysis, is suggestive of intense competition that favored divergence among locally coexisting species. We propose that Pleistocene climatic fluctuations causing expansion and contraction of rainforest could also have offered ecological opportunities for colonizers in addition to the process of divergent evolution.

Plant height and hydraulic vulnerability to drought and cold.

Understanding how plants survive drought and cold is increasingly important as plants worldwide experience dieback with drought in moist places and grow taller with warming in cold ones. Crucial in plant climate adaptation are the diameters of water-transporting conduits. Sampling 537 species across climate zones dominated by angiosperms, we find that plant size is unambiguously the main driver of conduit diameter variation. And because taller plants have wider conduits, and wider conduits within species are more vulnerable to conduction-blocking embolisms, taller conspecifics should be more vulnerable than shorter ones, a prediction we confirm with a plantation experiment. As a result, maximum plant size should be short under drought and cold, which cause embolism, or increase if these pressures relax. That conduit diameter and embolism vulnerability are inseparably related to plant size helps explain why factors that interact with conduit diameter, such as drought or warming, are altering plant heights worldwide.

Vulnerability to xylem embolism as a major correlate of the environmental distribution of rain forest species on a tropical island.

Increases in drought-induced tree mortality are being observed in tropical rain forests worldwide and are also likely to affect the geographical distribution of tropical vegetation. However, the mechanisms underlying the drought vulnerability and environmental distribution of tropical species have been little studied. We measured vulnerability to xylem embolism (P50 ) of 13 woody species endemic to New Caledonia and with different xylem conduit morphologies. We examined the relation between P50 , along with other leaf and xylem functional traits, and a range of habitat variables. Selected species had P50 values ranging between -4.03 and -2.00 MPa with most species falling in a narrow range of resistance to embolism above -2.7 MPa. Embolism vulnerability was significantly correlated with elevation, mean annual temperature and percentage of species occurrences located in rain forest habitats. Xylem conduit type did not explain variation in P50 . Commonly used functional traits such as wood density and leaf traits were not related to embolism vulnerability. Xylem embolism vulnerability stands out among other commonly used functional traits as a major driver of species environmental distribution. Drought-induced xylem embolism vulnerability behaves as a physiological trait closely associated with the habitat occupation of rain forest woody species.

Trait coordination, mechanical behaviour and growth form plasticity of Amborella trichopoda under variation in canopy openness.

Understanding the distribution of traits across the angiosperm phylogeny helps map the nested hierarchy of features that characterize key nodes. Finding that Amborella is sister to the rest of the angiosperms has raised the question of whether it shares certain key functional trait characteristics, and plastic responses apparently widespread within the angiosperms at large. With this in mind, we test the hypothesis that local canopy openness induces plastic responses. We used this variation in morphological and functional traits to estimate the pervasiveness of trait scaling and leaf and stem economics. We studied the architecture of Amborella and how it varies under different degrees of canopy openness. We analyzed the coordination of 12 leaf and stem structural and functional traits, and the association of this covariation with differing morphologies. The Amborella habit is made up of a series of sympodial modules that vary in size and branching pattern under different canopy openness. Amborella stems vary from self-supporting to semi-scandent. Changes in stem elongation and leaf size in Amborella produce distinct morphologies under different light environments. Correlations were found between most leaf and stem functional traits. Stem tissue rigidity decreased with increasing canopy openness. Despite substantial modulation of leaf size and leaf mass per area by light availability, branches in different light environments had similar leaf area-stem size scaling. The sympodial growth observed in Amborella could point to an angiosperm synapomorphy. Our study provides evidence of intraspecific coordination between leaf and stem economic spectra. Trait variation along these spectra is likely adaptive under different light environments and is consistent with these plastic responses having been present in the angiosperm common ancestor.

Bouldering: an alternative strategy to long-vertical climbing in root-climbing hortensias.

In the Neotropics, the genus Hydrangea of the popular ornamental hortensia family is represented by climbing species that strongly cling to their support surface by means of adhesive roots closely positioned along specialized anchoring stems. These root-climbing hortensia species belong to the nearly exclusive American Hydrangea section Cornidia and generally are long lianescent climbers that mostly flower and fructify high in the host tree canopy. The Mexican species Hydrangea seemannii, however, encompasses not only long lianescent climbers of large vertical rock walls and coniferous trees, but also short 'shrub-like' climbers on small rounded boulders. To investigate growth form plasticity in root-climbing hortensia species, we tested the hypothesis that support variability (e.g. differences in size and shape) promotes plastic responses observable at the mechanical, structural and anatomical level. Stem bending properties, architectural axis categorization, tissue organization and wood density were compared between boulder and long-vertical tree-climbers of H. seemannii. For comparison, the mechanical patterns of a closely related, strictly long-vertical tree-climbing species were investigated. Hydrangea seemannii has fine-tuned morphological, mechanical and anatomical responses to support variability suggesting the presence of two alternative root-climbing strategies that are optimized for their particular environmental conditions. Our results suggest that variation of some stem anatomical traits provides a buffering effect that regulates the mechanical and hydraulic demands of two distinct plant architectures. The adaptive value of observed plastic responses and the importance of considering growth form plasticity in evolutionary and conservation studies are discussed.

Universal hydraulics of the flowering plants: vessel diameter scales with stem length across angiosperm lineages, habits and climates.

Angiosperm hydraulic performance is crucially affected by the diameters of vessels, the water conducting conduits in the wood. Hydraulic optimality models suggest that vessels should widen predictably from stem tip to base, buffering hydrodynamic resistance accruing as stems, and therefore conductive path, increase in length. Data from 257 species (609 samples) show that vessels widen as predicted with distance from the stem apex across angiosperm orders, habits and habitats. Standardising for stem length, vessels are only slightly wider in warm/moist climates and in lianas, showing that, rather than climate or habit, plant size is by far the main driver of global variation in mean vessel diameter. Terminal twig vessels become wider as plant height increases, while vessel density decreases slightly less than expected tip to base. These patterns lead to testable predictions regarding evolutionary strategies allowing plants to minimise carbon costs per unit leaf area even as height increases.

Major trends in stem anatomy and growth forms in the perianth-bearing Piperales, with special focus on Aristolochia.

BACKGROUND AND AIMS: The order Piperales has the highest diversity of growth forms among the earliest angiosperm lineages, including trees, shrubs, climbers and herbs. However, within the perianth-bearing Piperales (Asarum, Saruma, Lactoris, Hydnora, Prosopanche, Thottea and Aristolochia), climbing species only occur in the most species-rich genus Aristolochia. This study traces anatomical and morphological traits among these lineages, to detect trends in growth form evolution and developmental processes. METHODS: Transverse stem sections of different developmental stages of representatives of Asarum, Saruma, Lactoris, Hydnora, Thottea and Aristolochia were compared and anatomical traits were linked to growth form evolution. Biomechanical properties of representative climbers were determined in three-point bending tests and are discussed based on the anatomical observations. Growth form evolution of the perianth-bearing Piperales was reconstructed by ancestral character state reconstruction using Mesquite. KEY RESULTS: While species of Asarum and Saruma are exclusively herbaceous, species of the remaining genera show a higher diversity of growth habit and anatomy. This growth form diversity is accompanied by a more complex stem anatomy and appropriate biomechanical properties. The ancestral growth form of the perianth-bearing Piperales is reconstructed with either a shrub-like or herbaceous character state, while the following three backbone nodes in the reconstruction show a shrub-like character state. Accordingly, the climbing habit most probably evolved in the ancestor of Aristolochia. CONCLUSIONS: Since the ancestor of the perianth-bearing Piperales has been reconstructed with a herb- or shrub-like habit, it is proposed that the climbing habit is a derived growth form, which evolved with the diversification of Aristolochia, and might have been a key feature for its diversification. Observed anatomical synapomorphies, such as the perivascular fibres in Lactoris, Thottea and Aristolochia, support the phylogenetic relationship of several lineages within the perianth-bearing Piperales. In addition, the hypothesis that the vegetative organs of the holoparasitic Hydnoraceae are most probably rhizomes is confirmed.

Escaping the lianoid habit: evolution of shrub-like growth forms in Aristolochia subgenus Isotrema (Aristolochiaceae).

PREMISE OF THE STUDY: A large range of growth forms is a notable aspect of angiosperm diversity and arguably a key element of their success. However, few studies within a phylogenetic context have explored how anatomical, developmental, and biomechanical traits are linked with growth form evolution. Aristolochia (∼500 species) consists predominantly of climbers, but a handful of shrub-like species are known from Aristolochia subgenus Isotrema (hereafter, shortened to Isotrema). We test hypotheses proposing that the establishment of functional traits linked to lianescence might limit the ability to evolve structurally diverse growth forms, particularly self-supporting forms. • METHODS: We focus on the origin of the shrub habit in Isotrema, from which we sampled representatives from climbing to self-supporting forms. Morphological, anatomical, and biomechanical characters are optimized on a chloroplast- and nuclear-derived phylogeny. • KEY RESULTS: Character-state reconstructions revealed that the climbing habit is plesiomorphic in Isotrema and shrub-like forms are derived from climbers. However, shrubs do not constitute a monophyletic group. Both shrubs and climbers show large multiseriate rays, but differ in terms of vessel size and proportion of fibers and soft tissues. • CONCLUSION: We suggest that while shrub-like species might have partly escaped from the constraints of life as lianas; their height size and stability are not typical of self-supporting shrubs and trees. Shrubs retained lianoid stem characters that are known to promote flexibility such as ray parenchyma. The transitions to a shrub-like form likely involved relatively simple, developmental changes that may be attributed to heterochronic processes.

Biomechanics of climbing palms and how they climb.

Climbing plants have fascinated botanists since the pioneering works of Darwin and his contemporaries in the 19(th) century. Diverse plants have evolved different ways of climbing and a wide range of attachment devices and stem biomechanics to cope with the particular physical demands of life as a climber. We investigated the biomechanics of attachment in a range of climbing palms, including true rattans from Southeast Asia and the genus Desmoncus from South America. We found that hook strength and orientation is coordinated with rachis geometry and rigidity. These findings support the notion of a ratchet-type attachment mechanism and partly explain why these spiny plants are so catchy and efficient at attaching to supports.

Tensioning the helix: a mechanism for force generation in twining plants.

Twining plants use their helical stems to clasp supports and to generate a squeezing force, providing stability against gravity. To elucidate the mechanism that allows force generation, we measured the squeezing forces exerted by the twiner Dioscorea bulbifera while following its growth using time-lapse photography. We show that the development of the squeezing force is accompanied by stiffening of the stem and the expansion of stipules at the leaf base. We use a simple thin rod model to show that despite their small size and sparse distribution, stipules impose a stem deformation sufficient to account for the measured squeezing force. We further demonstrate that tensioning of the stem helix, although counter-intuitive, is the most effective mechanism for generating large squeezing forces in twining plants. Our observations and model point to a general mechanism for the generation of the twining force: a modest radial stem expansion during primary growth, or the growth of lateral structures such as leaf bases, causes a delayed stem tensioning that creates the squeezing forces necessary for twining plants to ascend their supports. Our study thus provides the long-sought answer to the question of how twining plants ascend smooth supports without the use of adhesive or hook-like structures.

Moving with climbing plants from Charles Darwin's time into the 21st century.

We provide an overview of research on climbing plants from Charles Darwin to the present day. Following Darwin's interests, this review will focus on functional perspectives including attachment mechanisms and stem structure and function. We draw attention to a number of unsolved problems inviting future research. These include the mechanism for establishment of the twining habit, a quantitative description following the development of a tissue element through space and time, the chemistry of sticky exudates, the microstructure of xylem and the capacity for water storage, the vulnerability to embolism, and the mechanism for embolism repair. In conclusion we cite evidence that, in response to increasing CO(2) concentration, anthropic perturbation and/ or increasing forest fragmentation, lianas are increasing relative to tree species. In the 21st century, we are returning to the multiscale, multidisciplinary approach taken by Darwin to understand natural history.

The climbing habit in palms: Biomechanics of the cirrus and flagellum.

Climbing palms in the Arecoideae (Desmoncus) and Calamoideae (rattan palms) both evolved cirrate leaves armed with hooks and grapnels for climbing. Some species of Calamoideae develop a different climbing organ known as the flagellum, which also bears hooks. The present study indicates that geometry and mechanical properties of the cirrus vary between species. Cirrate leaves are constructed to optimize bending and torsion in relation to the deployment of recurved hooks. Hook development, size, and strength vary along cirri and flagella and are consistent with observations of these attachment organs functioning as a ratchet mechanism: hooks increase in strength toward the base of attachment organs and always fail before the axis in strength tests. Hook size and strength differ between species and are related to body size and ecological preference. Larger species produce larger hooks, but smaller climbing palms of the understory deploy fine sharp hooks that are effective on small diameter supports as well as large branches and trunks. The ephemeral nature of climbing organs in palms provides a challenge to their life-history development, particularly in terms of mechanical constraints and remaining attached to the host vegetation; these differ significantly from many vines and lianas having more perennial modes of attachment.

Biomechanics and development of the climbing habit in two species of the South American palm genus Desmoncus (Arecaceae).

Mechanical properties are investigated in Desmoncus orthacanthos and D. polyacanthos from French Guiana, South America. Differences in size and axis stiffness are related to different trellis requirements and habitats. The leaf sheath surrounds the stem, increasing stiffness of young self-supporting stages and apical parts of older climbing plants. Senescence of the leaf sheath reduces stiffness of older climbing axes of both species. Its eventual loss in D. orthacanthos facilitates deformation into coils and loops when plants slip from their supports following senescence of leaves bearing attachment organs. In smaller climbing axes of D. polyacanthos, the senescent leaf sheath remains attached and axes rarely form loops and coils below attachment. An increase in stiff mechanical properties toward the base of both species is radically different from that of many dicotyledonous lianas. Besides the presence of attachment organs, stem mechanical properties of Desmoncus are similar to those of erect though not fully self-supporting stems of Bactris major, a sympatric species of the sister group genus to Desmoncus. The climbing habit in Desmoncus may have evolved via (1) heterochronic processes including early elongation of internodes relative to increase in stem diameter (reduction of the establishment phase) and (2) increased persistence of leaf sheaths.