Belowground morphology as a clue for plant response to disturbance and productivity in a temperate flora.

Plants possess a large variety of nonacquisitive belowground organs, such as rhizomes, tubers, bulbs, and coarse roots. These organs determine a whole set of functions that are decisive in coping with climate, productivity, disturbance, and biotic interactions, and have been hypothesized to affect plant distribution along environmental gradients. We assembled data on belowground organ morphology for 1712 species from Central Europe and tested these hypotheses by quantifying relationships between belowground morphologies and species optima along ecological gradients related to productivity and disturbance. Furthermore, we linked these data with species co-occurrence in 30 115 vegetation plots from the Czech Republic to determine relationships between belowground organ diversity and these gradients. The strongest gradients determining belowground organ distribution were disturbance severity and frequency, light, and moisture. Nonclonal perennials and annuals occupy much smaller parts of the total environmental space than major types of clonal plants. Forest habitats had the highest diversity of co-occurring belowground morphologies; in other habitats, the diversity of belowground morphologies was generally lower than the random expectation. Our work shows that nonacquisitive belowground organs may be partly responsible for plant environmental niches. This adds a new dimension to the plant trait spectrum, currently based on acquisitive traits (leaves and fine roots) only.

Determinants of interspecific variation in season length of perennial herbs.

BACKGROUND AND AIMS: Perennial plants in seasonal climates need to optimize their carbon balance by adjusting their active season length to avoid risks of tissue loss under adverse conditions. As season length is determined by two processes, namely spring growth and senescence, it is likely to vary in response to several potentially contrasting selective forces. Here we aim to disentangle the cascade of ecological determinants of interspecific differences in season length. METHODS: We measured size trajectories in 231 species in a botanical garden. We examined correlations between their spring and autumn size changes and determined how they make up season length. We used structural equation models (SEMs) to determine how niche parameters and species traits combine in their effect on species-specific season length. KEY RESULTS: Interspecific differences in season length were mainly controlled by senescence, while spring growth was highly synchronized across species. SEMs showed that niche parameters (light and moisture) had stronger, and often trait-independent, effects compared to species traits. Several niche (light) and trait variables (plant height, clonal spreading) had opposing effects on spring growth and senescence. CONCLUSIONS: The findings indicate different drivers and potential risks in growth and senescence. The strong role of niche-based predictors implies that shifts in season length due to global change are likely to differ among habitats and will not be uniform across the whole flora.

Functional trait trade-offs define plant population stability across different biomes.

Ecological theory posits that temporal stability patterns in plant populations are associated with differences in species' ecological strategies. However, empirical evidence is lacking about which traits, or trade-offs, underlie species stability, especially across different biomes. We compiled a worldwide collection of long-term permanent vegetation records (greater than 7000 plots from 78 datasets) from a large range of habitats which we combined with existing trait databases. We tested whether the observed inter-annual variability in species abundance (coefficient of variation) was related to multiple individual traits. We found that populations with greater leaf dry matter content and seed mass were more stable over time. Despite the variability explained by these traits being low, their effect was consistent across different datasets. Other traits played a significant, albeit weaker, role in species stability, and the inclusion of multi-variate axes or phylogeny did not substantially modify nor improve predictions. These results provide empirical evidence and highlight the relevance of specific ecological trade-offs, i.e. in different resource-use and dispersal strategies, for plant populations stability across multiple biomes. Further research is, however, necessary to integrate and evaluate the role of other specific traits, often not available in databases, and intraspecific trait variability in modulating species stability.

The shape of root systems in a mountain meadow: plastic responses or species-specific architectural blueprints?

The efficient uptake of nutrients depends on the ability of roots to respond to gradients of these resources. Although pot experiments have shown that species differ in their ability to proliferate their roots in nutrient-rich patches, the role of such differences in determining root shapes in the field is unclear. We used fine-scale quantitative (q)PCR-based species-specific mapping of roots in a grassland community to reconstruct species-specific root system shapes. We linked them with data from pot experiments on the ability of these species to proliferate in nutrient-rich patches and their rooting depth. We found remarkable diversity in root system shapes, from cylindrical to conical. Interspecific differences in rooting depths in pots were the main determinant of rooting depths in the field, whereas differences in foraging ability played only a minor role. Although some species with strong foraging ability did place their roots into nutrient-rich soil layers, it was not a universal pattern. The results imply that although the vertical differentiation of grassland species is pronounced, it is primarily not driven by the differential plastic response of species to soil nutrient gradients. This may constrain the coexistence of species with similar rooting depths and may instead favour coexistence of species differing in their architectural blueprints.

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.

Comparative analysis of root sprouting and its vigour in temperate herbs: anatomical correlates and environmental predictors.

BACKGROUND AND AIMS: Root sprouting (RS), i.e. the ability to form adventitious buds on roots, is an important form of clonal growth in a number of species, and serves as both a survival strategy and a means of spatial expansion, particularly in plants growing in severely and recurrently disturbed habitats. Occurrence and/or success of plants in severely and recurrently disturbed habitats are determined by two components, namely the ability to produce adventitious buds on roots and the vigour of their production. As mechanisms behind different magnitudes of RS remain unclear, our study investigates: (1) whether the presence or absence of specific tissues in roots can promote or limit RS; and (2) whether there is some relationship between RS ability, RS vigour and species niche. METHODS: We studied RS ability together with RS vigour in 182 Central European herbaceous species under controlled experimental conditions. We used phylogenetic logistic regressions to model the presence of RS, RS vigour, the relationship between RS and anatomical traits and the relationship between RS and parameters of species niches. KEY RESULTS: A quarter of herbs examined were able to produce adventitious buds on roots. They were characterized by their preference for open dry habitats, the presence of secondary root thickening and the occurrence of sclerified cortical cells in roots. Root sprouting vigour was not associated with any specific anatomical pattern, but was correlated with the environmental niches of different species, indicating that preferred disturbed and dry habitats might represent a selection pressure for more vigorous root sprouters than undisturbed and wet habitats. CONCLUSIONS: Our study shows that sprouting from roots is quite common in temperate dicotyledonous herbs. Two components of RS - ability and vigour - should be considered separately in future studies. We would also like to focus more attention on RS in herbs from other regions as well as on external forces and internal mechanisms regulating evolution and the functions of RS in both disturbed and undisturbed habitats.

Inflorescence preformation prior to winter: a surprisingly widespread strategy that drives phenology of temperate perennial herbs.

Organ preformation in overwintering buds of perennial plants has been known for almost two centuries. It is hypothesized to underlie fast growth and early flowering, but its frequency, phylogenetic distribution, and ecological relevance have never been systematically examined. We microscopically observed inflorescence preformation in overwintering buds (IPB) in the autumn. We studied a phylogenetically and ecologically representative set of 330 species of temperate perennial angiosperms and linked these observations with quantitative data on species' flowering phenology, genome size, and ecology. IPB was observed in 34% of species examined (in 14% species the stamens and/or pistils were already developed). IPB is fairly phylogenetically conserved and frequent in many genera (Alchemilla, Carex, Euphorbia, Geranium, Primula, Pulmonaria) or families (Ranunculaceae, Euphorbiaceae, Violaceae, Boraginaceae). It was found in species of any genome size, although it was almost universal in those with large genomes. Compared with non-IPB species, IPB species flowered 38 d earlier on average and were more common in shaded and undisturbed habitats. IPB is a surprisingly widespread adaptation for early growth in predictable (undisturbed) conditions. It contributes to temporal niche differentiation and has important consequences for understanding plant phenology, genome size evolution, and phylogenetic structure of plant communities.

Synchrony matters more than species richness in plant community stability at a global scale.

The stability of ecological communities is critical for the stable provisioning of ecosystem services, such as food and forage production, carbon sequestration, and soil fertility. Greater biodiversity is expected to enhance stability across years by decreasing synchrony among species, but the drivers of stability in nature remain poorly resolved. Our analysis of time series from 79 datasets across the world showed that stability was associated more strongly with the degree of synchrony among dominant species than with species richness. The relatively weak influence of species richness is consistent with theory predicting that the effect of richness on stability weakens when synchrony is higher than expected under random fluctuations, which was the case in most communities. Land management, nutrient addition, and climate change treatments had relatively weak and varying effects on stability, modifying how species richness, synchrony, and stability interact. Our results demonstrate the prevalence of biotic drivers on ecosystem stability, with the potential for environmental drivers to alter the intricate relationship among richness, synchrony, and stability.

Evolution of clonal growth forms in angiosperms.

Clonal growth of plants is attained by a number of morphologically different organs (e.g. stolons, rhizomes, and roots), which are not functionally equivalent. Consequently, these clonal growth organ (CGO) types can determine functional traits that are associated with clonality, although little is known about their evolutionary flexibility or the constraining role they play on clonal traits. We investigated the rates of evolutionary change by which individual CGOs are acquired and lost using a set of 2652 species of Central European flora. Furthermore, we asked how these individual CGOs constrain functionally relevant clonal traits, such as lateral spread, number of offspring, and persistence of connections. We show that plants can easily switch in evolution among individual types of CGO and between clonal and nonclonal habits. However, not all these transitions are equally probable. Namely, stem-based clonal growth and root-based clonal growth constitute evolutionarily separate forms of clonal growth. Clonal traits are strongly constrained by individual CGO types. Specifically, fast lateral spread is attained by stolons or hypogeogenous rhizomes, and persistent connections are attained by all rhizome types. However, the ease with which clonal organs appear and disappear in evolution implies that plants can overcome these constraints by adjusting their morphologies.

Disentangling phylogenetic and functional components of shape variation among shoot apical meristems of a wide range of herbaceous angiosperms.

PREMISE: The shoot apical meristem (SAM) is the basic determinant of plant body organization, but interspecific variation in SAM shape and its relationship to stem and leaf morphological traits is not well known. Here we tested the hypothesis that different SAM shapes are associated with specific shoot traits of the plant body and examined the phylogenetic conservatism of these relationships. METHODS: We used geometric morphometrics of SAM outlines for a phylogenetically representative set of 110 herbaceous angiosperms and examined their relationship to a number of shoot traits. RESULTS: We found large variations in SAM shapes across angiosperm lineages, but covering only a subset of geometrically possible shapes. Part of this variation was allometric (due to SAM size), but the dominant shape variation (dome-shaped vs. flat surface) was size-independent and strongly phylogenetically conserved. SAM shapes were largely independent of their cell size and therefore of the number of cells involved. Different patterns in shape variation of outer and inner SAM boundaries were associated with stem thickness, leaf area, and leafiness of the stem. CONCLUSIONS: The findings show that geometric interdependence of meristem zones gives rise to correlations among organ numbers, sizes, and their proportions. Phylogenetic conservatism in these correlations indicates conservatism in regulatory processes that underlie the correlations, or the individual traits, that give rise to plant architecture.

Root:shoot ratio in developing seedlings: How seedlings change their allocation in response to seed mass and ambient nutrient supply.

Root:shoot (R:S) biomass partitioning is one of the keys to the plants' ability to compensate for limiting resources in the environment and thus to survive and succeed in competition. In adult plants, it can vary in response to many factors, such as nutrient availability in the soil or reserves in the roots from the previous season. The question remains whether, at the interspecific level, reserves in seeds can affect seedlings' R:S ratio in a similar way. Proper allocation to resource-acquiring organs is enormously important for seedlings and is likely to determine their survival and further success. Therefore, we investigated the effect of seed mass on seedling R:S biomass partitioning and its interaction with nutrient supply in the substrate. We measured seedling biomass partitioning under two different nutrient treatments after 2, 4, 6, and 12 weeks for seventeen species differing in seed mass and covering. We used phylogenetically informed analysis to determine the independent influence of seed mass on seedling biomass partitioning. We found consistently lower R:S ratios in seedlings with higher seed mass. Expectedly, R:S was also lower with higher substrate nutrient supply, but substrate nutrient supply had a bigger effect on R:S ratio for species with higher seed mass. These findings point to the importance of seed reserves for the usage of soil resources. Generally, R:S ratio decreased over time and, similarly to the effect of substrate nutrients, R:S ratio decreased faster for large-seeded species. We show that the seed mass determines the allocation patterns into new resource-acquiring organs during seedling development. Large-seeded species are more flexible in soil nutrient use. It is likely that faster development of shoots provides large-seeded species with the key advantage in asymmetric above-ground competition, and that this could constitute one of the selective factors for optimum seed mass.

Heterospecific plant-soil feedback and its relationship to plant traits, species relatedness, and co-occurrence in natural communities.

Plant-soil feedback is one of the mechanisms affecting co-existence of species, ecological succession, and species invasiveness. However, in contrast to conspecific plant-soil feedback, general patterns in heterospecific feedback are mostly unknown. We used a meta-analysis to search for correlations between heterospecific feedback and species relatedness, functional traits, and field co-occurrence patterns. We searched published literature and compiled a data set of 618 PSF interactions. We gathered data on species traits reflecting plant size and growth rate (height, specific leaf area, and life span), co-occurrence in habitats and phylogenetic distance between species pairs. We found that species grew better in soil conditioned by (i) close relatives than in conspecific soil, whereas there was no relationship with phylogeny for distantly related species, (ii) species of greater plant height (but there was no relationship with species SLA or life span), and (iii) species more frequently co-occurring in the field. The results show that heterospecific plant-soil feedback can be explained by plant traits (height) and is reflected in co-occurrence patterns. Phylogeny was a significant predictor of feedbacks over short phylogenetic distance, suggesting fast evolution of traits related to feedback. The low variability explained by the models, however, indicates that other factors such as environmental conditions possibly alter plant-soil feedback responses.

Shoot apical meristem and plant body organization: a cross-species comparative study.

Background and Aims: The shoot apical meristem (SAM) is the key organizing element in the plant body and is responsible for the core of plant body organization and shape. Surprisingly, there are almost no comparative data that would show links between parameters of the SAM and whole-plant traits as drivers of the plant's response to the environment. Methods: Interspecific differences in SAM anatomy were examined in 104 perennial herbaceous angiosperms. Key Results: There were differences in SAM parameters among individual species, their phylogenetic patterns, and how their variation is linked to variation in plant above-ground organs and hence species' environmental niches. SAM parameters were correlated with the size-related traits of leaf area, seed mass and stem diameter. Of the two key SAM parameters (cell size and number), variation in all organ traits was linked more strongly to cell number, with cell size being important only for seed mass. Some of these correlations were due to shared phylogenetic history (e.g. SAM diameter versus stem diameter), whereas others were due to parallel evolution (e.g. SAM cell size and seed mass). Conclusion: These findings show that SAM parameters provide a functional link among sizes and numbers of plant organs, constituting species' environmental responses.

On Plant Modularity Traits: Functions and Challenges.

On-spot persistence, space occupancy, and recovery after damage are key plant functions largely understudied. Traits relevant to these functions are difficult to assess because of their relationships to plant modularity. We suggest that developing collection protocols for these traits is feasible and could facilitate their inclusion in global syntheses.

Polyploid species rely on vegetative reproduction more than diploids: a re-examination of the old hypothesis.

Background and Aims: Polyploidy is arguably the single most important genetic mechanism in plant speciation and diversification. It has been repeatedly suggested that polyploids show higher vegetative reproduction than diploids (to by-pass low fertility after the polyploidization), but there are no rigorous tests of it. Methods: Data were analysed by phylogenetic regressions of clonal growth parameters, and vegetative reproduction in culture on the ploidy status of a large set of species (approx. 900) from the Central European Angiosperm flora. Further, correlated evolution of ploidy and clonal traits was examined to determine whether or not polyploidy precedes vegetative reproduction. Key Results: The analyses showed that polyploidy is strongly associated with vegetative reproduction, whereas diploids rely more on seed reproduction. The rate of polyploid speciation is strongly enhanced by the existence of vegetative reproduction (namely extensive lateral spread), whereas the converse is not true. Conclusions: These findings confirm the old hypothesis that polyploids can rely on vegetative reproduction which thus may save many incipient polyploids from extinction. A closer analysis also shows that the sequence of events begins with development of vegetative reproduction, which is then followed by polyploidy. Vegetative reproduction is thus likely to play an important role in polyploid speciation.

Cytotype coexistence in the field cannot be explained by inter-cytotype hybridization alone: linking experiments and computer simulations in the sexual species Pilosella echioides (Asteraceae).

BACKGROUND: Processes driving ploidal diversity at the population level are virtually unknown. Their identification should use a combination of large-scale screening of ploidy levels in the field, pairwise crossing experiments and mathematical modelling linking these two types of data. We applied this approach to determine the drivers of frequencies of coexisting cytotypes in mixed-ploidy field populations of the fully sexual plant species Pilosella echioides. We examined fecundity and ploidal diversity in seeds from all possible pairwise crosses among 2x, 3x and 4x plants. Using these data, we simulated the dynamics of theoretical panmictic populations of individuals whose progeny structure is identical to that determined by the hybridization experiment. RESULTS: The seed set differed significantly between the crossing treatments, being highest in crosses between diploids and tetraploids and lowest in triploid-triploid crosses. The number of progeny classes (with respect to embryo and endosperm ploidy) ranged from three in the 2x-2x cross to eleven in the 3x-3x cross. Our simulations demonstrate that, provided there is no difference in clonal growth and/or survival between cytotypes, it is a clear case of minority cytotype exclusion depending on the initial conditions with two stable states, neither of which corresponds to the ploidal structure in the field: (i) with prevalent diploids and lower proportions of other ploidies, and (ii) with prevalent tetraploids and 9% of hexaploids. By contrast, if clonal growth differs between cytotypes, minority cytotype exclusion occurs only if the role of sexual reproduction is high; otherwise differences in clonal growth are sufficient to maintain triploid prevalence (as observed in the field) independently of initial conditions. CONCLUSIONS: The projections of our model suggest that the ploidal structure observed in the field can only be reached via a relatively high capacity for clonal growth (and proportionally lower sexual reproduction) in all cytotypes combined with higher clonal growth in the prevailing cytotype (3x).

CLO-PLA: a database of clonal and bud-bank traits of the Central European flora.

This dataset presents comprehensive and easy-to-use information on 29 functional traits of clonal growth, bud banks, and lifespan of members of the Central European flora. The source data were compiled from a number of published sources (see the reference file) and the authors' own observations or studies. In total, 2,909 species are included (2,745 herbs and 164 woody species), out of which 1,532 (i.e., 52.7% of total) are classified as possessing clonal growth organs (1,480, i.e., 53.9%, if woody plants are excluded). This provides a unique, and largely unexplored, set of traits of clonal growth that can be used in studies on comparative plant ecology, plant evolution, community assembly, and ecosystem functioning across the large flora of Central Europe. It can be directly imported into a number of programs and packages that perform trait-based and phylogenetic analyses aimed to answer a variety of open and pressing ecological questions.

Root Foraging Performance and Life-History Traits.

Plants use their roots to forage for nutrients in heterogeneous soil environments, but different plant species vastly differ in the intensity of foraging they perform. This diversity suggests the existence of constraints on foraging at the species level. We therefore examined the relationships between the intensity of root foraging and plant body traits across species in order to estimate the degree of coordination between plant body traits and root foraging as a form of plant behavior. We cultivated 37 perennial herbaceous Central European species from open terrestrial habitats in pots with three different spatial gradients of nutrient availability (steep, shallow, and no gradient). We assessed the intensity of foraging as differences in root placement inside pots with and without a spatial gradient of resource supply. For the same set of species, we retrieved data about body traits from available databases: maximum height at maturity, mean area of leaf, specific leaf area, shoot lifespan, ability to self-propagate clonally, maximal lateral spread (in clonal plants only), realized vegetative growth in cultivation, and realized seed regeneration in cultivation. Clonal plants and plants with extensive vegetative growth showed considerably weaker foraging than their non-clonal or slow-growing counterparts. There was no phylogenetic signal in the amount of expressed root foraging intensity. Since clonal plants foraged less than non-clonals and foraging intensity did not seem to be correlated with species phylogeny, we hypothesize that clonal growth itself (i.e., the ability to develop at least partly self-sustaining ramets) may be an answer to soil heterogeneity. Whereas unitary plants use roots as organs specialized for both resource acquisition and transport to overcome spatial heterogeneity in resource supply, clonal plants separate these two functions. Becoming a clonal plant allows higher specialization at the organ level, since a typical clonal plant can be viewed as a network of self-sustainable harvesting units connected together with specialized high-throughput connection organs. This may be an effective alternative for coping with spatial heterogeneity in resource availability.