Stephen P. Bonser

Plant phenotypic plasticity in a changing climate

Climate change is altering the availability of resources and the conditions that are crucial to plant performance. One way plants will respond to these changes is through environmentally induced shifts in phenotype (phenotypic plasticity). Understanding plastic responses is crucial for predicting and managing the effects of climate change on native species as well as crop plants. Here, we provide a toolbox with definitions of key theoretical elements and a synthesis of the current understanding of the molecular and genetic mechanisms underlying plasticity relevant to climate change. By bringing ecological, evolutionary, physiological and molecular perspectives together, we hope to provide clear directives for future research and stimulate cross-disciplinary dialogue on the relevance of phenotypic plasticity under climate change.

Land-use intensification reduces functional redundancy and response diversity in plant communities.

Ecosystem resilience depends on functional redundancy (the number of species contributing similarly to an ecosystem function) and response diversity (how functionally similar species respond differently to disturbance). Here, we explore how land-use change impacts these attributes in plant communities, using data from 18 land-use intensity gradients that represent five biomes and > 2800 species. We identify functional groups using multivariate analysis of plant traits which influence ecosystem processes. Functional redundancy is calculated as the species richness within each group, and response diversity as the multivariate within-group dispersion in response trait space, using traits that influence responses to disturbances. Meta-analysis across all datasets showed that land-use intensification significantly reduced both functional redundancy and response diversity, although specific relationships varied considerably among the different land-use gradients. These results indicate that intensified management of ecosystems for resource extraction can increase their vulnerability to future disturbances.

Plasticity in reproduction and growth among 52 range-wide populations of a Mediterranean conifer: adaptive responses to environmental stress

A plastic response towards enhanced reproduction is expected in stressful environments, but it is assumed to trade off against vegetative growth and efficiency in the use of available resources deployed in reproduction [reproductive efficiency (RE)]. Evidence supporting this expectation is scarce for plants, particularly for long‐lived species. Forest trees such as Mediterranean pines provide ideal models to study the adaptive value of allocation to reproduction vs. vegetative growth given their among‐population differentiation for adaptive traits and their remarkable capacity to cope with dry and low‐fertility environments. We studied 52 range‐wide Pinus halepensis populations planted into two environmentally contrasting sites during their initial reproductive stage. We investigated the effect of site, population and their interaction on vegetative growth, threshold size for female reproduction, reproductive–vegetative size relationships and RE. We quantified correlations among traits and environmental variables to identify allocation trade‐offs and ecotypic trends. Genetic variation for plasticity was high for vegetative growth, whereas it was nonsignificant for reproduction. Size‐corrected reproduction was enhanced in the more stressful site supporting the expectation for adverse conditions to elicit plastic responses in reproductive allometry. However, RE was unrelated with early reproductive investment. Our results followed theoretical predictions and support that phenotypic plasticity for reproduction is adaptive under stressful environments. Considering expectations of increased drought in the Mediterranean, we hypothesize that phenotypic plasticity together with natural selection on reproductive traits will play a relevant role in the future adaptation of forest tree species.

Patterns of variation in meristem allocation across genotypes and species in monocarpic Brassicaceae

The three principal functions of axillary meristems in plants are branching or vegetative growth (G), reproduction (R), and inactivity (I). The purpose of this study was to test for pattern in the trade-off between these three meristem functions across monocarpic species and genotypes (of one species) in the family Brassicaceae and to examine the relationship between meristem allocation and other fitness components: plant height, plant size (vegetative biomass), and reproductive biomass allocation. Results from three independent tests showed a strong positive relationship between % G and % R meristem functions (and a correspondingly strong negative relationship between % 1 and % R meristem functions and between % 1 and % G meristem functions) at three different taxonomic levels: across ten genotypes (inbred lines) of Arabidopsis thaliana, across five species of Brassica, and across 13 species of Brassicaceae growing in natural populations. We interpret these results in terms of adaptive strategies along light gradients. Since there is only one reproductive opportunity in monocarpic (annual/biennial) species, lifetime seed production should be maximized by the total number of meristems that can be developed into flowers (R meristems) within one or two years. This should be maximized by high branching intensity (high allocation to G meristem function) under relatively weak competition for light, thus explaining the strong positive relationship between % G and % R meristem functions. Under more intense competition for light, however, lifetime seed production should be maximized by a taller, less branched growth form through higher allocation to I meristem function (imposed by stronger apical dominance). The detected trade-offs therefore may be interpreted as the cost of reproduction (high % R meristem function) and/or branching (high % G meristem function) measured as reduced apical dominance (low % I meristem function). Alternatively, the data may be interpreted as the cost of apical dominance (high % I meristem function) measured as reduced branching intensity (low % G meristem function) and reduced reproductive effort (low % R meristem function). Significant relationships between meristem allocation and other fitness components were detected only in A. thaliana genotypes: reproductive biomass allocation was best predicted by % R and % G meristem functions whereas both height and vegetative biomass were best predicted by % I meristem function.

Structure of biological soil crust communities in Callitris glaucophylla woodlands of New South Wales, Australia

Abstract Question: What is the nature of the relationships between cover, diversity and abundance of biological soil crusts, cover and diversity of vascular plants, and annual rainfall, soil texture and forestry practices in Callitris glaucophylla woodlands? Location: Arid and semi-arid Callitris glaucophylla-dominated woodlands of eastern Australia. Methods: We documented soil crust-forming mosses, lichens and liverworts at 83 woodland sites along a gradient of declining rainfall. Linear and non-linear regression were used to examine relationships between soil crust species and attributes of vascular plant communities, and a similarity matrix (species abundance × sites) was subjected to Non-metric Multi-Dimensional Scaling (MDS), and Analysis of Similarities (ANOSIM) to show the degree of association between groups of taxa, and soil texture, rainfall classes and forestry practices. Results: We collected 86 taxa. Mosses were dominated by the family Pottiaceae, and lichens were dominated by squamulose forms. Average annual rainfall was highly correlated with soil crust community composition, and loamy soils supported a greater cover and diversity of taxa compared with sandy soils. Increases in tree cover were associated with significant, though weak, increases in abundance, but not diversity, of crusts. Crusts tended to be more diverse in areas that (1) had a sparse cover of ground-storey plants; (2) were relatively stable – as indicated by the proportion of perennial and/or native plants; (3) had more stable soil surfaces; and (4) were unlogged. Litter cover, overstorey thinning, and livestock grazing had no appreciable effect on crust diversity or cover. Conclusions: Callitris glaucophylla woodlands provide substantial habitat for soil crust organisms, and the dense tree cover and closed canopies of Callitris do not appear to have a major influence on the structure of biological crust communities. Unlike other woodland systems, relatively few patches would be required to reserve a high diversity of crust species. Nomenclature: McCarthy (1991) for lichens; Streimann & Klazenga (2002) for mosses; Scott (1985) for liverworts.

Plants Can Benefit from Herbivory: Stimulatory Effects of Sheep Saliva on Growth of Leymus chinensis

Background Plants and herbivores can evolve beneficial interactions. Growth factors found in animal saliva are probably key factors underlying plant compensatory responses to herbivory. However, there is still a lack of knowledge about how animal saliva interacts with herbivory intensities and how saliva can mobilize photosynthate reserves in damaged plants. Methodology/Principal Findings The study examined compensatory responses to herbivory and sheep saliva addition for the grass species Leymus chinensis in three experiments over three years. The first two experiments were conducted in a factorial design with clipping (four levels in 2006 and five in 2007) and two saliva treatment levels. The third experiment examined the mobilization and allocation of stored carbohydrates following clipping and saliva addition treatments. Animal saliva significantly increased tiller number, number of buds, and biomass, however, there was no effect on height. Furthermore, saliva effects were dependent on herbivory intensities, associated with meristem distribution within perennial grass. Animal saliva was found to accelerate hydrolyzation of fructans and accumulation of glucose and fructose. Conclusions/Significance The results demonstrated a link between saliva and the mobilization of carbohydrates following herbivory, which is an important advance in our understanding of the evolution of plant responses to herbivory. Herbivory intensity dependence of the effects of saliva stresses the significance of optimal grazing management.

High reproductive efficiency as an adaptive strategy in competitive environments

Summary Reproductive efficiency (the efficiency of conversion of resources from vegetative tissue to reproductive output) is a central to our understanding of reproductive allocation and the evolution of reproductive strategies in plants. Plant strategy theory predicts that reproductive efficiency should decrease under competition. Short-lived semelparous species are not predicted to evolve under competition and therefore should not express adaptive responses to the presence of competitors. Long-lived iteroparous species are predicted to delay reproduction in favour of growth and resource acquisition in the presence of competitors. I use life-history theory to advance a prediction that reproductive efficiency increases under competition in both short-lived semelparous and potentially longer-lived iteroparous species. Contrary to the predictions of plant strategy theory, short-lived semelparous species are frequently observed to live in highly competitive environments. Further, iteroparous species under intense competition may die long before they reach competitive dominance or an optimal size for reproduction. I surveyed the literature for studies on plant species including measurements of vegetative and reproductive allocation in high and low (or no) competition treatments. Across species, relative reproductive efficiency (reproductive efficiency under high competition/reproductive efficiency under low competition) significantly increased with increasing competition intensity. Patterns of allocation to reproduction under competition support the existence of a competitive annual strategy and a reproductive perennial strategy. Under these strategies, short-lived semelparous species and long-lived iteroparous species express high reproductive efficiency under competition as an adaptation to high neighbour density. In addition, some species also expressed patterns of allocation to reproduction consistent with plant strategy theories. Under this interpretation, I predict that competitive strategies, where plants delay reproduction in competitive environments to gain competitive superiority, are favoured not under intense competition but under modest competition. Including a life-history interpretation in reproductive efficiency under competition provides a much needed predictive framework for strategies of reproduction observed across species.

The adaptive value of functional and life-history traits across fertility treatments in an annual plant

BACKGROUND AND AIMS Plant functional traits are assumed to be adaptive. As selection acts on individuals and not on traits, interpreting the adaptive value of a trait not may be straightforward. For example, productive leaves are associated with fertile environments. However, it is not clear if productive leaves confer an advantage in these habitats, or if they are an advantage as part of a suite of coordinated traits. METHODS Genotypes of Arabidopsis thaliana were grown in high and low nutrient treatments and low, neutral and high pH treatments. Nutrient availability is reduced in acidic or basic soils relative to neutral pH soils. pH treatments were used to alter the availability of resources rather than the amount of resources. KEY RESULTS Leaf function (specific leaf area, SLA) and life history (size at reproduction, age at reproduction) were variable across genotypes and were plastic. High nutrient availability induced higher SLA and larger size at reproduction. Genotypes that reproduced at large size in high nutrient conditions at neutral pH had the greatest fruit production. SLA was only indirectly related to fruit production through a causal relationship with rosette size; in high nutrient conditions, plants with high SLA were large at reproduction and had higher fruit production. In high nutrient and high pH treatments, plants were large at reproduction, but large size at reproduction was associated with low fecundity. This suggests that large size is adaptive under high nutrient availability. CONCLUSIONS Interpreting the adaptive value of functional traits will sometimes only be possible when these traits are considered as a suite of correlated and coordinated traits. Leaf functional traits may be important in defining adaptive strategies in A. thaliana but only through how they affect plant life history. Finally, manipulating soil pH can be a valuable tool in assessing adaptive plasticity on nutrient gradients.

Heteroblastic development and the optimal partitioning of traits among contrasting environments in Acacia implexa

BACKGROUND AND AIMS Optimal partitioning theory (OPT) predicts plants will allocate biomass to organs where resources are limiting. Studies of OPT focus on root, stem and leaf mass ratios where roots and stems are often further sub-divided into organs such as fine roots/tap roots or branches/main stem. Leaves, however, are rarely sub-divided into different organs. Heteroblastic species develop juvenile and adult foliage and provide an opportunity of sub-dividing leaf mass ratio into distinct organs. Acacia implexa (Mimosaceae) is a heteroblastic species that develops compound (juvenile), transitional and phyllode (adult) leaves that differ dramatically in form and function. The aims of the present study were to grow A. implexa to examine patterns of plastic development of whole-plant and leaf traits under the OPT framework. METHODS Plants were grown in a glasshouse under contrasting nutrient, light and water environments in a full factorial design. Allocation to whole-plant and leaf-level traits was measured and analysed with multivariate statistics. KEY RESULTS Whole-plant traits strongly followed patterns predicted by OPT. Leaf-level traits showed a more complex pattern in response to experimental treatments. Compound leaves on low nutrient plants had significantly lower specific leaf area (SLA) and were retained for longer as quantified by a significantly greater compound leaf mass ratio after 120 d. There was no significant difference in SLA of compound leaves in the light treatment, yet transitional SLA was significantly higher under the low light treatment. The timing of heteroblastic shift from compound to transitional leaves was significantly delayed only in the low light treatment. Therefore, plants in the light treatment responded at the whole-plant level by adjusting allocation to productive compound leaves and at the leaf-level by adjusting SLA. There were no significant SLA differences in the water treatment despite strong trends at the whole-plant level. CONCLUSION Explicitly sub-dividing leaves into different types provided greater insights into OPT.

Carbon isotopic signatures of soil organic matter correlate with leaf area index across woody biomes

Leaf area index (LAI), a measure of canopy density, is a key variable for modelling and understanding primary productivity, and also water use and energy exchange in forest ecosystems. However, LAI varies considerably with phenology and disturbance patterns, so alternative approaches to quantifying stand-level processes should be considered. The carbon isotope composition of soil organic matter (C-13(SOM)) provides a time-integrated, productivity-weighted measure of physiological and stand-level processes, reflecting biomass deposition from seasonal to decadal time scales. Our primary aim was to explore how well LAI correlates with C-13(SOM) across biomes. Using a global data set spanning large environmental gradients in tropical, temperate and boreal forest and woodland, we assess the strength of the correlation between LAI and C-13(SOM); we also assess climatic variables derived from the WorldClim database. We found that LAI was strongly correlated with C-13(SOM), but was also correlated with Mean Temperature of the Wettest Quarter, Mean Precipitation of Warmest Quarter and Annual Solar Radiation across and within biomes.Synthesis. Our results demonstrate that C-13(SOM) values can provide spatially explicit estimates of leaf area index (LAI) and could therefore serve as a surrogate for productivity and water use. While C-13(SOM) has traditionally been used to reconstruct the relative abundance of C-3 versus C-4 species, the results of this study demonstrate that within stable C-3- or C-4-dominated biomes, C-13(SOM) can provide additional insights. The fact that LAI is strongly correlated to C-13(SOM) may allow for a more nuanced interpretation of ecosystem properties of palaeoecosystems based on palaeosol C-13 values.