The triangular space of abiotic stress tolerance in woody species: a unified trade-off model.

Tolerance of abiotic stress in woody plants is known to be constrained by biological trade-offs between different forms of stress, especially shade and drought. However, there is still considerable uncertainty on the relationship between tolerances and the limits on tolerance combinations. Using the most extensive database available on shade, drought, waterlogging and cold tolerance for 799 northern hemisphere woody species, we determined the number of dimensions needed to summarise their tolerance combinations, and the best trade-off model among those currently available, for description of the interdependence between tolerances. Two principal component analysis (PCA) dimensions summarised stress tolerance combinations. They defined a triangular stress tolerance space (STS). The first STS dimension reflected segregation between drought-tolerant and waterlogging-tolerant species. The second reflected shade tolerance, which is independent of the other tolerances. Cold tolerance scaled weakly with both dimensions. Tolerance combinations across the species in the database were limited by boundary-line trade-offs. The STS reconciles all major theories about trade-offs between abiotic stress tolerances, providing a unified trade-off model and a set of coordinates that can be used to examine how other aspects of plant biology, such as plant functional traits, change within the limits of abiotic stress tolerance.

Publisher Correction: Contrasting latitudinal patterns in phylogenetic diversity between woody and herbaceous communities.

A correction to this article has been published and is linked from the HTML and PDF versions of this paper. The error has been fixed in the paper.

Contrasting latitudinal patterns in phylogenetic diversity between woody and herbaceous communities.

Although many studies have shown that species richness decreases from low to high latitudes (the Latitudinal Diversity Gradient), little is known about the relationship between latitude and phylogenetic diversity. Here we examine global latitudinal patterns of phylogenetic diversity using a dataset of 459 woody and 589 herbaceous plant communities. We analysed the relationships between community phylogenetic diversity, latitude, biogeographic realm and vegetation type. Using the most recent global megaphylogeny for seed plants and the standardised effect sizes of the phylogenetic diversity metrics 'mean pairwise distance' (SESmpd) and 'mean nearest taxon distance' (SESmntd), we found that species were more closely-related at low latitudes in woody communities. In herbaceous communities, species were more closely-related at high latitudes than at intermediate latitudes, and the strength of this effect depended on biogeographic realm and vegetation type. Possible causes of this difference are contrasting patterns of speciation and dispersal. Most woody lineages evolved in the tropics, with many gymnosperms but few angiosperms adapting to high latitudes. In contrast, the recent evolution of herbaceous lineages such as grasses in young habitat types may drive coexistence of closely-related species at high latitudes. Our results show that high species richness commonly observed at low latitudes is not associated with high phylogenetic diversity.

Drivers of vegetative dormancy across herbaceous perennial plant species.

Vegetative dormancy, that is the temporary absence of aboveground growth for ≥ 1 year, is paradoxical, because plants cannot photosynthesise or flower during dormant periods. We test ecological and evolutionary hypotheses for its widespread persistence. We show that dormancy has evolved numerous times. Most species displaying dormancy exhibit life-history costs of sprouting, and of dormancy. Short-lived and mycoheterotrophic species have higher proportions of dormant plants than long-lived species and species with other nutritional modes. Foliage loss is associated with higher future dormancy levels, suggesting that carbon limitation promotes dormancy. Maximum dormancy duration is shorter under higher precipitation and at higher latitudes, the latter suggesting an important role for competition or herbivory. Study length affects estimates of some demographic parameters. Our results identify life historical and environmental drivers of dormancy. We also highlight the evolutionary importance of the little understood costs of sprouting and growth, latitudinal stress gradients and mixed nutritional modes.

Predicting evolution in response to climate change: the example of sprouting probability in three dormancy-prone orchid species.

Although many ecological properties of species respond to climate change, their evolutionary responses are poorly understood. Here, we use data from long-term demographic studies to predict evolutionary responses of three herbaceous perennial orchid species, Cypripedium parviflorum, C. candidum and Ophrys sphegodes, to predicted climate changes in the habitats they occupy. We focus on the evolution of sprouting probability, because all three species exhibit long-term vegetative dormancy, i.e. individual plants may not emerge above-ground, potentially for several consecutive years. The drivers of all major vital rates for populations of the species were analysed with general linear mixed models (GLMMs). High-dimensionality function-based matrix projection models were then developed to serve as core elements of deterministic and stochastic adaptive dynamics models used to analyse the adaptive context of sprouting in all populations. We then used regional climate forecasts, derived from high-resolution general atmospheric circulation models, of increased mean annual temperatures and spring precipitation at the occupied sites, to predict evolutionary trends in sprouting. The models predicted that C. parviflorum and O. sphegodes will evolve higher and lower probabilities of sprouting, respectively, by the end of the twenty-first century, whereas, after considerable variation, the probability of sprouting in C. candidum will return to its current level. These trends appear to be driven by relationships between mortality and size: in C. parviflorum and C. candidum, mortality is negatively related to size in the current year but positively related to growth since the previous year, whereas in O. sphegodes, mortality is positively related to size.

Trait-based analysis of decline in plant species ranges during the 20th century: a regional comparison between the UK and Estonia.

Although the distribution ranges and abundance of many plant species have declined dramatically in recent decades, detailed analysis of these changes and their cause have only become possible following the publication of second- and third-generation national distribution atlases. Decline can now be compared both between species and in different parts of species' ranges. We extracted data from distribution atlases to compare range persistence of 736 plant species common to both the UK and Estonia between survey periods encompassing almost the same years (1969 and 1999 in the UK and 1970 and 2004 in Estonia). We determined which traits were most closely associated with variation in species persistence, whether these were the same in each country, and the extent to which they explained differences in persistence between the countries. Mean range size declined less in Estonia than in the UK (24.3% vs. 30.3%). One-third of species in Estonia (239) maintained >90% of their distribution range compared with one-fifth (141) in the UK. In Estonia, 99 species lost >50% of their range compared with 127 species in the UK. Persistence was very positively related to original range in both countries. Major differences in species persistence between the studied countries were primarily determined by biogeographic (affiliation to floristic element) and ecoevolutionary (plant strategy) factors. In contrast, within-country persistence was most strongly determined by tolerance of anthropogenic activities. Decline of species in the families Orchidaceae and Potamogetonaceae was significantly greater in the UK than in Estonia. Almost all of the 736 common and native European plant species in our study are currently declining in their range due to pressure from anthropogenic activities. Those species with low tolerance of human activity, with biotic pollination vectors and in the families referred to above are the most vulnerable, especially where human population density is high.

Comment on "Worldwide evidence of a unimodal relationship between productivity and plant species richness".

Fraser et al. (Reports, 17 July 2015, p. 302) report that a hump-backed model describes the worldwide relationship between productivity and plant species richness in grassland communities. We reanalyze their data from a larger-scale perspective, using local species pool. This influences richness far more strongly than productivity, and, when this is taken into account, the hump-backed richness-productivity relationship disappears.

Potential disruption of pollination in a sexually deceptive orchid by climatic change.

Warmer springs advance many phenological events, including flowering time in plants and the flight time of insects. Pollination by insects, an ecosystem service of immense economic and conservation importance, depends on synchrony between insect activity and flowering time. If plants and their pollinators show different phenological responses to climate warming, pollination could fail. Information about the effects of warming on specific plant-insect mutualisms is difficult to obtain from complex pollination networks. In contrast, the extraordinarily specific deceptions evolved by orchids that attract a very narrow range of pollinators allow direct examination of the potential for climatic warming to disrupt synchrony. Here we show that a sexually deceptive orchid and the solitary bee on which it depends for pollination will diverge in phenology with increasing spring temperature. Male bees inadvertently pollinate the orchid flowers during pseudocopulation. Analysis of museum specimens (1893-2007) and recent field-based records (1975-2009) showed that flight date of the solitary bee Andrena nigroaenea is advanced more by higher temperatures than is flowering date in the deceptive orchid Ophrys sphegodes. Male bees emerged slightly earlier than females, which attract male copulatory attentions away from the deceptive flowers. Warming by as little as 2°C increased both the probability of male flight and the proportion of females flying in the bee population before orchid flowering; this would reduce the frequency of pseudocopulation and thus lower pollination success rate in the orchid. Our results demonstrate a significant potential for coevolved plant-pollinator relationships to be disrupted by climatic warming.

Plants do not count or do they? New perspectives on the universality of senescence.

1. Senescence, the physiological decline that results in decreasing survival and/or reproduction with age, remains one of the most perplexing topics in biology. Most theories explaining the evolution of senescence (i.e. antagonistic pleiotropy, accumulation of mutations, disposable soma) were developed decades ago. Even though these theories have implicitly focused on unitary animals, they have also been used as the foundation from which the universality of senescence across the tree of life is assumed. 2. Surprisingly, little is known about the general patterns, causes and consequences of whole-individual senescence in the plant kingdom. There are important differences between plants and most animals, including modular architecture, the absence of early determination of cell lines between the soma and gametes, and cellular division that does not always shorten telomere length. These characteristics violate the basic assumptions of the classical theories of senescence and therefore call the generality of senescence theories into question. 3. This Special Feature contributes to the field of whole-individual plant senescence with five research articles addressing topics ranging from physiology to demographic modelling and comparative analyses. These articles critically examine the basic assumptions of senescence theories such as age-specific gene action, the evolution of senescence regardless of the organism's architecture and environmental filtering, and the role of abiotic agents on mortality trajectories. 4.Synthesis. Understanding the conditions under which senescence has evolved is of general importance across biology, ecology, evolution, conservation biology, medicine, gerontology, law and social sciences. The question 'why is senescence universal or why is it not?' naturally calls for an evolutionary perspective. Senescence is a puzzling phenomenon, and new insights will be gained by uniting methods, theories and observations from formal demography, animal demography and plant population ecology. Plants are more amenable than animals to experiments investigating senescence, and there is a wealth of published plant demographic data that enable interpretation of experimental results in the context of their full life cycles. It is time to make plants count in the field of senescence.

A modular concept of plant foraging behaviour: the interplay between local responses and systemic control.

In this paper we examined the notion that plant foraging for resources in heterogeneous environments must involve: (1) plasticity at the level of individual modules in reaction to localized environmental signals; and (2) the potential for modification of these responses either by the signals received from connected modules that may be exposed to different conditions, or by the signals reflecting the overall resource status of the plant. A conceptual model is presented to illustrate how plant foraging behaviour is achieved through these processes acting in concert, from the signal reception through signal transduction to morphological or physiological response. Evidence to support the concept is reviewed, using selective root placement under nutritionally heterogeneous conditions and elongation responses of stems and petioles to shade as examples. We discussed how the adoption of this model can promote understanding of the ecological significance of foraging behaviour. We also identified a need to widen the experimental repertoires of both molecular physiology and ecology in order to increase our insight into both the regulation and functioning of foraging responses, and their relationship with the patterns of environmental heterogeneity under which plants have evolved.

Foraging for space and avoidance of physical obstructions by plant roots: a comparative study of grasses from contrasting habitats.

Physical obstructions that reduce space for root growth can profoundly affect plant performance. The aim of this study was to investigate the ability of roots to avoid obstructions and forage for usable space, and to reveal the mechanism involved. Eight grass species from four genera were examined. Each genus included species characteristic of habitats with high and low nutrient availability. The ability to limit root mass and to adjust morphology within substrate containing obstructions in the form of gravel was investigated. A treatment with activated carbon, which adsorbs organic compounds, was used to examine the possible involvement of root exudates in responses to obstructions. Only species characteristic of nutrient-poor habitats restricted placement of root mass in substrate containing obstructions, and this response disappeared in the presence of activated carbon. Root morphological responses to obstructions differed from those shown in response to nutrient-poor conditions or compacted soil. These results suggest that the ability to avoid obstructions is dependent on the sensitivity of roots to their own exudates accumulating in the vicinity of obstructions. This is similar to other behavioural responses in which cues or signals are used to adjust growth before stressful conditions are encountered.

Effects of physical connection and genetic identity of neighbouring ramets on root-placement patterns in two clonal species.

Root-placement patterns were examined in the clonal species Glechoma hederacea and Fragaria vesca when grown with different types of neighbours. Three different patterns were predicted as consequences of different types of interactions between roots: the avoidance pattern if root growth decreases in the presence of neighbouring roots; the intrusive pattern if root growth increases towards neighbouring roots; and the unresponsive pattern if root growth is unaffected by neighbouring roots. Experiments were conducted in which physical connection between ramets, and the genetic identity of neighbouring ramets, were manipulated. The patterns of distribution of entire root systems and elongation rates of individual roots were measured. Root systems and individual roots of G. hederacea avoided contact with roots of neighbouring ramets, irrespective of connection to the neighbour and its genetic or specific identity. In contrast, F. vesca roots grew equally towards and away from intraspecific ramet neighbours and their elongation was stimulated by contact with roots of G. hederacea ramets. These results demonstrate that root-placement patterns of plants grown with different types of neighbours vary between species, and suggest that factors additional to resource depletion could be involved in their development.

The effects of environmental heterogeneity on root growth and root/shoot partitioning.

AIMS: The purpose of this Botanical Briefing is to stimulate reappraisal of root growth, root/shoot partitioning, and analysis of other aspects of plant growth under heterogeneous conditions. SCOPE: Until recently, most knowledge of plant growth was based upon experimental studies carried out under homogeneous conditions. Natural environments are heterogeneous at scales relevant to plants and in forms to which they can respond. Responses to environmental heterogeneity are often localized rather than plant-wide, and not always predictable from traditional optimization arguments or from knowledge of the ontogenetic trends of plants growing under homogeneous conditions. These responses can have substantial impacts, both locally and plant-wide, on patterns of resource allocation, and significant effects on whole-plant growth. Results from recent studies are presented to illustrate responses of plants, plant populations and plant communities to nutritionally heterogeneous conditions. CONCLUSIONS: Environmental heterogeneity is a constant presence in the natural world that significantly influences plant behaviour at a variety of levels of complexity. Failure to understand its effects on plants prevents us from fully exploiting aspects of plant behaviour that are only revealed under patchy conditions. More effort should be invested into analysis of the behaviour of plants under heterogeneous conditions.

Effect of cadmium, zinc and substrate heterogeneity on yield, shoot metal concentration and metal uptake by Brassica juncea: implications for human health risk assessment and phytoremediation.

• Heavy metal contaminants are usually heterogeneously distributed in soils. However, their effects on plants are usually studied under homogeneous conditions. Here we examined the effects of Cd, Zn, and their spatial distribution on shoot yield, shoot metal concentrations, and total metal uptake by Brassica juncea. • One Cd concentration and three Zn concentrations were used. Metals were applied to the substrate either singly or in combination. • Heterogeneous metal distribution enabled growth reduction to be avoided, even at concentrations that were highly phytotoxic when distribution was homogeneous. Moderate Zn contamination reduced Cd uptake by 40%. With high Zn contamination, metal concentrations were two to four times lower when metals were heterogeneously, rather than homogeneously, distributed; shoot yields were up to 24-times greater and total shoot Cd and Zn uptakes were on average six-times higher. • It is suggested that human health risk from consuming plant parts grown on Cd-contaminated substrates is lower when Zn is also present and metal distribution is heterogeneous, and that phytoremediation potential is greater when contaminant distribution is heterogeneous.

Differential response to shading in orthotropic and plagiotropic shoots of the clonal herb Glechoma hirsuta.

Previous studies have shown that internodes and petioles of closely related erect and stoloniferous species show marked differences in their response to shading. Vertical structures show strong elongation responses while horizontal structures show significantly smaller elongation responses. This paper reports an experiment designed to test whether internodes and petioles on orthotropic (vertically oriented) and plagiotropic (horizontally oriented) shoots produced by the same plant, also show such differential responses. The study species, Glechoma hirsuta, produces plagiotropic shoots in its vegetative stage and orthotropic shoots during its generative stage. Shoots of G. hirsuta were grown either in full daylight or under simulated canopy shade. Internode and petiole elongation, biomass investment patterns and other growth-related parameters were measured on plants in each light treatment. In orthotropic shoots the length of internodes responded more strongly to shading than the length of petioles, while the opposite was true for plagiotropic shoots, confirming the hypothesis that vertical spacers have higher degrees of shade-induced plasticity than horizontally oriented spacers. Growth and development of horizontally oriented shoots was reduced by shading, whereas that of vertically oriented shoots was unaffected by light treatment. The results are discussed in terms of the differences in function of vertically and horizontally oriented spacers, and the probable benefits of plasticity in enhancing essential activities including photosynthesis, habitat exploration and seed dispersal.

AN ANALYSIS OF THE INFLUENCE OF CLONE SIZE AND STOLON CONNECTIONS BETWEEN RAMETS ON THE GROWTH OF GLECHOMA HEDERACEA L.

Two experiments were conducted in which the influence of size of clones and the persistence of stolon connections on subsequent development were examined in Glechoma hederacea. In the first experiment, clones were grown from either one unrooted ramet or from either one, two or three connected, rooted ramets, for 8 weeks, in either nutrient-rich or nutrient-poor sand. The survival, number of ramets and dry weight of the clones produced were dependent on the number of established ramets at the start of the experiment. Clones in nutrient-rich sand developed a greater number of ramets, stolon branches, total length of stolon, mean leaf area per ramet and total leaf area per clone than clones of corresponding initial size in nutrient-poor sand. In the second experiment, the stolon connections between ramets of G. hederacea clones growing in boxes were either left intact or severed soon after each ramet had rooted. After 10 weeks of growth, the total dry weight of the intact clones and the mean dry weight of their ramets were significantly greater than the corresponding values for severed clones. The spatial distribution of ramets showed marked differences between the treatments. Severed clones produced a greater number of rooted ramets within the boxes and a smaller number of unrooted ramets beyond the box edges than intact clones. Density of ramets more than doubled when stolons were severed. Maintenance of stolon connections in G. hederacea is advantageous because it improves the probability of daughter ramet survival, promotes rapid lateral expansion of the clone and reduces inter-ramet competition through the production of fewer, larger ramets.