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.

Genome size is strongly linked to carbohydrate storage and weakly linked to root sprouting ability in herbs.

BACKGROUND AND AIMS: Several lines of evidence indicate that carbohydrate storage in plant below-ground organs might be positively related to genome size because both these plant properties represent resource sinks and can affect cell size, cell cycle time, water-use efficiency and plant growth. However, plants adapted to disturbance, such as root sprouters, could be an exception because their strategy would require higher carbohydrate reserves to fuel biomass production but small genomes to complete their cell cycles faster. METHODS: We used data from a field survey to test the relationship between genome size and the probability of root sprouting ability in 172 Central European herbaceous species. Additionally, we conducted a pot experiment with 19 herbaceous species with different sprouting ability (nine congeneric pairs plus one species), and measured root non-structural carbohydrate concentrations and pools at the end of a growing season. KEY RESULTS: In the Central European flora, the probability of root sprouting ability was lower in large-genome species but this pattern was weak. In the pot experiment, both total non-structural and water-soluble carbohydrates (mainly fructans) were positively and non-linearly related to genome size, regardless of sprouting strategy. The concentrations of mono- and disaccharides and all carbohydrate pools showed no link to genome size, and starch was absent in large-genome species. The link between genome size and carbohydrate storage was less apparent at a small phylogenetic scale because we only observed a higher carbohydrate concentration in species with larger genomes for four of the species pairs. CONCLUSIONS: Root sprouters may have smaller genomes because of their frequent occurrence in dry and open habitats. Large-genome species with presumably large cells and vacuoles could accumulate more water-soluble carbohydrates at the end of the growing season to fuel their growth and perhaps protect vulnerable organs from freezing early in the next season.

Herbs are not just small plants: What biomass allocation to rhizomes tells us about differences between trees and herbs.

PREMISE: Biomass accumulation over years in vertical stems of trees leads to hypoallometric scaling between stem and leaf biomass within this growth form, while for herbaceous species, biomass allocation between these organ types typically exhibits isometry. However, biomass accumulation in herbs can occur in belowground perennating organs (e.g., rhizomes) that are, contrary to aboveground parts of herbs, long-lived. Although ecologically important, biomass allocation and accumulation in rhizomes (and similar organs) have mostly not been studied. METHODS: We assembled data on biomass investments into plant organs for 111 rhizomatous herbs based on a literature survey and greenhouse experiment. We estimated the proportion of whole-plant biomass invested into rhizomes and, using allometric relationships, analyzed scaling between rhizome and leaf biomass and whether it is more variable than for other organs. RESULTS: On average, rhizomes comprise 30.2% of the total plant biomass. The proportion allocated to rhizomes does not change with plant size. Scaling between rhizome and leaf biomass is isometric, and allocation to rhizomes is not more variable than allocation to other organs. CONCLUSIONS: Rhizomatous herbs accumulate substantial biomass in rhizomes, and rhizome biomass scales isometrically with leaves, contrary to the hypoallometric relationship between stem and leaves in trees. This difference suggests that the rhizome biomass is in balance with aboveground biomass-a resource of carbon for rhizome formation that, at the same time, is dependent on carbon stored in rhizomes for its seasonal regrowth.

What determines root-sprouting ability: Injury or phytohormones?

PREMISE: Root-sprouting (RS) is an evolutionarily independent alternative to axillary stem branching for a plant to attain its architecture. Root-sprouting plants are better adapted to disturbance than non-RS plants, and their vigor is frequently boosted by biomass removal. Nevertheless, RS plants are rarer than plants that are not root-sprouters, possibly because they must overcome developmental barriers such as intrinsic phytohormonal balance or because RS ability is conditioned by injury to the plant body. The objective of this study was to identify whether phytohormones or injury enable RS. METHODS: In a greenhouse experiment, growth variables, root respiration, and phytohormones were analyzed in two closely related clonal herbs that differ in RS ability (spontaneously RS Inula britannica and rhizomatous non-RS I. salicina) with and without severe biomass removal. RESULTS: As previously reported, I. britannica is a root-sprouter, but injury did not boost its RS ability. Root respiration did not differ between the two species and decreased continuously with time irrespectively of injury, but their phytohormone profiles differed significantly. In RS species, the auxins-to-cytokinins ratio was low, and injury further decreased it. CONCLUSIONS: This first attempt to test drivers behind different plant growth forms suggests that intrinsic phytohormone regulation, especially the auxins-to-cytokinins ratio, might be behind RS ability. Injury, causing a phytohormonal imbalance, seems to be less important in spontaneously RS species than expected for RS species in general.

Variability in mycorrhizal status of plant species is much larger within than between plots in grassland and coastal habitats.

Community-level studies linking plant mycorrhizal status to environment usually do not account for within-plot mycorrhizal status variability; thus, patterns of plant mycorrhizal status diversity are largely unknown. Here, we assessed the relative importance of within- and between-plot variability components in mycorrhizal status and examined how plant mycorrhizal status diversity is related to soil nutrient availability. We hypothesised larger between-plot variability in mycorrhizal status and higher plant mycorrhizal status diversity in P-poor soils. To test these hypotheses, we used plant phylogenies, vegetation, soil and plant mycorrhizal status data from Czech semi-natural grasslands and Scottish coastal habitats. We divided plant mycorrhizal status diversity into divergence and evenness and tested their relations to soil P, K, Ca and Mg. Within-plot variability component of mycorrhizal status was always, on average, at least 2.2 times larger than between-plot variability in our datasets. Plant mycorrhizal status divergence was positively related to Ca (in both datasets) and Mg (only in grasslands and when accounting for phylogeny). In grasslands, the relationship between Mg and plant mycorrhizal status evenness was negative when accounting for phylogeny, while it was positive when not accounting for phylogeny. Plant mycorrhizal status diversity was not linked to P and its relation to K was inconsistent. Our results suggest that high Ca in the soil can promote coexistence of mycorrhizal, facultatively mycorrhizal and non-mycorrhizal plant species. We encourage future studies to also focus on within-plot variability in mycorrhizal status, because it appears to be highly relevant in herbaceous systems.

Stoichiometry versus ecology: the relationships between genome size and guanine-cytosine content, and tissue nitrogen and phosphorus in grassland herbs.

BACKGROUND AND AIMS: Plant tissue nitrogen (N) and phosphorus (P) and genome traits, such as genome size and guanine-cytosine (GC) content, scale with growth or metabolic rates and are linked to plant ecological strategy spectra. Tissue NP stoichiometry and genome traits are reported to affect plant growth, metabolic rates or ecological strategies in contrasting ways, although the elemental costs for building and maintaining DNA are typically overlooked. METHODS: We formulated stoichiometry- and ecology-based predictions on the relationship between genome size and GC content to tissue N, P and N : P and tested them on a set of 130 herbaceous species from a temperate grassland using ordinary, phylogenetic and quantile regression. KEY RESULTS: Genome size was only negatively linked to plant N and N : P in species with very small genomes. We found no link between genome size and plant P. GC content was negatively linked to plant N and P but we found these significant links consistently in both GC-rich and GC-poor species. Finally, GC content correlated positively with plant N : P but only in species with GC-rich genomes. CONCLUSIONS: Our results provide stronger support for the ecology-based predictions than the stoichiometry-based predictions, and for the links between GC content and plant N and P stoichiometry than for genome size. We argue that the theories of plant metabolic rates and ecological strategies (resource-acquisitive vs. conservative or ruderal vs. stress-tolerator spectra) better explain interspecific genome-NP stoichiometry relationships at the tissue level (although relatively weakly) than the stoichiometric theory based on the elemental costs for building and maintaining DNA.

A starting guide to root ecology: strengthening ecological concepts and standardising root classification, sampling, processing and trait measurements.

In the context of a recent massive increase in research on plant root functions and their impact on the environment, root ecologists currently face many important challenges to keep on generating cutting-edge, meaningful and integrated knowledge. Consideration of the below-ground components in plant and ecosystem studies has been consistently called for in recent decades, but methodology is disparate and sometimes inappropriate. This handbook, based on the collective effort of a large team of experts, will improve trait comparisons across studies and integration of information across databases by providing standardised methods and controlled vocabularies. It is meant to be used not only as starting point by students and scientists who desire working on below-ground ecosystems, but also by experts for consolidating and broadening their views on multiple aspects of root ecology. Beyond the classical compilation of measurement protocols, we have synthesised recommendations from the literature to provide key background knowledge useful for: (1) defining below-ground plant entities and giving keys for their meaningful dissection, classification and naming beyond the classical fine-root vs coarse-root approach; (2) considering the specificity of root research to produce sound laboratory and field data; (3) describing typical, but overlooked steps for studying roots (e.g. root handling, cleaning and storage); and (4) gathering metadata necessary for the interpretation of results and their reuse. Most importantly, all root traits have been introduced with some degree of ecological context that will be a foundation for understanding their ecological meaning, their typical use and uncertainties, and some methodological and conceptual perspectives for future research. Considering all of this, we urge readers not to solely extract protocol recommendations for trait measurements from this work, but to take a moment to read and reflect on the extensive information contained in this broader guide to root ecology, including sections I-VII and the many introductions to each section and root trait description. Finally, it is critical to understand that a major aim of this guide is to help break down barriers between the many subdisciplines of root ecology and ecophysiology, broaden researchers' views on the multiple aspects of root study and create favourable conditions for the inception of comprehensive experiments on the role of roots in plant and ecosystem functioning.

Mycorrhizal status is a poor predictor of the distribution of herbaceous species along the gradient of soil nutrient availability in coastal and grassland habitats.

Plant mycorrhizal status (a trait indicating the ability to form mycorrhizas) can be a useful plant trait for predicting changes in vegetation influenced by increased fertility. Mycorrhizal fungi enhance nutrient uptake and are expected to provide a competitive advantage for plants growing in nutrient-poor soils; while in nutrient-rich soils, mycorrhizal symbiosis may be disadvantageous. Some studies in natural systems have shown that mycorrhizal plants can be more frequent in P and N-poor soils (low nutrient availability) or Ca and Mg-high (high pH) soils, but empirical support is still not clear. Using vegetation and soil data from Scottish coastal habitats, and Latvian and Czech grasslands, we examined whether there is a link between plant mycorrhizal status and plant-available P, N, Ca and Mg. We performed the max test analysis (to examine the central tendency) and a combination of quantile regression and meta-analysis (to examine tendencies in different quantiles) on both community and plant species data combined with plant phylogenies. We consistently found no changes in mycorrhizal status at the community and species levels along the gradients of plant-available P, N, Ca and Mg in the central tendency and in almost all quantiles across all datasets. Thus, we found no support for the hypotheses that herbaceous species which are able to form mycorrhizas are more frequent in nutrient-poor and high pH environments. Obligatory, facultatively and non-mycorrhizal herbaceous species appear to assemble randomly along the gradients of nutrient availability in several European herbaceous habitats, suggesting that all these strategies perform similarly under non-extreme soil nutrient conditions.

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.

Strong impact of management regimes on rhizome biomass across Central European temperate grasslands.

Grassland ecosystems account for approximately 40% of terrestrial biomes globally. These communities are characterized by a large allocation to belowground biomass, often exceeding its aboveground counterpart. However, this biomass investment cannot be entirely attributed to the acquisitive function of roots. Grassland plants also allocate to non-acquisitive, stem-derived, belowground organs, such as rhizomes. These organs are responsible for the key plant functions of space occupancy, resprouting after damage, and seasonal rest. However, biomass investment to rhizomes has rarely been studied. Here we gathered community-level aboveground and rhizome biomass data for 52 temperate grasslands in Czech Republic (Central Europe), differing in management intensity. We found that rhizome biomass scaled linearly with aboveground biomass, and more intensive management disproportionally (negatively) affected rhizome biomass. This finding may have important implications for the persistence of temperate grassland plants and their provision of ecosystem services (e.g., soil carbon sequestration, soil stabilization) in relation to changing environments.

Carbohydrate storage in herbs: the forgotten functional dimension of the plant economic spectrum.

BACKGROUND AND AIMS: Although the plant economic spectrum seeks to explain resource allocation strategies, carbohydrate storage is often omitted. Belowground storage organs are the centre of herb perennation, yet little is known about the role of their turnover, anatomy and carbohydrate storage in relation to the aboveground economic spectrum. METHODS: We collected aboveground traits associated with the economic spectrum, storage organ turnover traits, storage organ inner structure traits and storage carbohydrate concentrations for ~80 temperate meadow species. KEY RESULTS: The suites of belowground traits were largely independent of one another, but there was significant correlation of the aboveground traits with both inner structure and storage carbohydrates. Anatomical traits diverged according to leaf nitrogen concentration on the one hand and vessel area and dry matter content on the other; carbohydrates separated along gradients of leaf nitrogen concentration and plant height. CONCLUSIONS: Contrary to our expectations, aboveground traits and not storage organ turnover were correlated with anatomy and storage carbohydrates. Belowground traits associated with the aboveground economic spectrum also did not fall clearly within the fast-slow economic continuum, thus indicating the presence of a more complicated economic space. Our study implies that the generally overlooked role of storage within the plant economic spectrum represents an important dimension of plant strategy.

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.

Root traits as drivers of plant and ecosystem functioning: current understanding, pitfalls and future research needs.

The effects of plants on the biosphere, atmosphere and geosphere are key determinants of terrestrial ecosystem functioning. However, despite substantial progress made regarding plant belowground components, we are still only beginning to explore the complex relationships between root traits and functions. Drawing on the literature in plant physiology, ecophysiology, ecology, agronomy and soil science, we reviewed 24 aspects of plant and ecosystem functioning and their relationships with a number of root system traits, including aspects of architecture, physiology, morphology, anatomy, chemistry, biomechanics and biotic interactions. Based on this assessment, we critically evaluated the current strengths and gaps in our knowledge, and identify future research challenges in the field of root ecology. Most importantly, we found that belowground traits with the broadest importance in plant and ecosystem functioning are not those most commonly measured. Also, the estimation of trait relative importance for functioning requires us to consider a more comprehensive range of functionally relevant traits from a diverse range of species, across environments and over time series. We also advocate that establishing causal hierarchical links among root traits will provide a hypothesis-based framework to identify the most parsimonious sets of traits with the strongest links on functions, and to link genotypes to plant and ecosystem functioning.

Young clonal and non-clonal herbs differ in growth strategy but not in aboveground biomass compensation after disturbance.

Clonal plants have more traits enabling individual persistence (larger belowground storage of buds and assimilates), whereas non-clonal plants have more traits enabling population persistence (a higher reliance on regeneration from seeds). This difference presumably makes those groups respond differently to disturbance. We asked whether this difference is already expressed in the first year of the plant's life. In a pot experiment with 17 congeneric pairs of clonal and non-clonal herbs, we investigated response to a disturbance at the individual level. We were interested whether the leaf C/N ratio (a proxy reflecting active growth and photosynthetic efficiency), the R/S ratio (a proxy for belowground storage) and the amount of compensated biomass differ between clonal and non-clonal herbs. Moreover, we asked whether compensation for the loss of aboveground biomass after disturbance can be predicted by the R/S ratio or explained by the leaf C/N ratio. We found that clonal herbs have higher leaf C/N and R/S ratios than non-clonal herbs. Under disturbance, the leaf C/N and R/S ratios decreased in the clonal herbs and increased in the non-clonal herbs. However, the clonal and non-clonal plants did not differ in biomass compensation ability. Neither the R/S ratio nor the leaf C/N ratio explained the compensation abilities of the herbs. These results show that even though the growth strategies of clonal and non-clonal plants and their reactions to disturbance are different, the groups are similarly capable of compensating for the loss of aboveground biomass. Clonal plants do not have an advantage over non-clonal plants under disturbance during their first year of life.

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.

Alpine plant growth and reproduction dynamics in a warmer world.

Climate warming may stimulate growth and reproduction in cold-adapted plants, but also reduce their performance due to warming-induced drought limitation. We tested this theory using a unique experiment with the alpine forb Rumex alpinus. We examined how climate warming over the past four decades affected its annual rhizome growth, leaf production and flowering, and whether responses varied between alpine, subalpine and montane populations. Before the period of accelerated warming in the 1970s and 1980s, the primary limitation on growth had been cold temperatures and short growing seasons. Increased summer temperatures in the 1990s and 2000s enhanced rhizome growth and leaf production, but not flowering. Alpine and subalpine plants profit more than montane plants, currently producing three times longer annual rhizome increments and twice as many leaves as 40 yr ago, and achieving nearly the same values as montane plants. During the warmest 2005-2015 period, growth became contingent on summer precipitation and began to decrease across all populations, likely due to an increasing water shortage in dense monospecific stands. Warming releases plants from cold limitations but induces water shortage. Rumex alpinus exceeds its thermal optimum and becomes water-limited as the climate warms. Our results suggest that warming-induced responses in alpine plants will not be one-sided shifts to higher growth and reproduction, but rather multidimensional and spatiotemporally variable.