Tree host-pathogen interactions as influenced by drought timing: linking physiological performance, biochemical defence and disease severity.

There is increasing concern about tree mortality around the world due to climatic extremes and associated shifts in pest and pathogen dynamics. Yet, empirical studies addressing the interactive effect of biotic and abiotic stress on plants are very rare. Therefore, in this study, we examined the interaction between drought stress and a canker pathogen, Quambalaria coyrecup, on the eucalypt - Corymbia calophylla (marri), which is experiencing increasing drought stress. We hypothesized that drought stress would increase marri's susceptibility to canker disease, and cankers would have the largest negative effect on plants that are already drought stressed before pathogen inoculation. To test the hypotheses, in a glasshouse, marri saplings were exposed to drought either before or after pathogen inoculation, or were well-watered or droughted throughout the experiment either with or without inoculation. Canker development was greater in well-watered saplings than in droughted saplings, with the fastest development occurring in well-watered saplings that had experienced drought stress before inoculation. Irrespective of water treatments, marri saplings employed phenol-based localized biochemical defence against the pathogen. Drought reduced photosynthesis and growth, however, a negative effect of canker disease on saplings' physiological performance was only observed in well-watered saplings. In well-watered saplings, canker-induced loss of sapwood function contributed to reduced whole-plant hydraulic conductance, photosynthesis and growth. The results provide evidence that timing of drought stress influences host physiology, and host condition influences canker disease susceptibility through differences in induced biochemical defence mechanisms. The observations highlight the importance of explicitly incorporating abiotic and biotic stress, as well as their interactions, in future studies of tree mortality in drought-prone regions worldwide.

A climate change context for the decline of a foundation tree species in south-western Australia: insights from phylogeography and species distribution modelling.

BACKGROUND AND AIMS: A worldwide increase in tree decline and mortality has been linked to climate change and, where these represent foundation species, this can have important implications for ecosystem functions. This study tests a combined approach of phylogeographic analysis and species distribution modelling to provide a climate change context for an observed decline in crown health and an increase in mortality in Eucalyptus wandoo, an endemic tree of south-western Australia. METHODS: Phylogeographic analyses were undertaken using restriction fragment length polymorphism analysis of chloroplast DNA in 26 populations across the species distribution. Parsimony analysis of haplotype relationships was conducted, a haplotype network was prepared, and haplotype and nucleotide diversity were calculated. Species distribution modelling was undertaken using Maxent models based on extant species occurrences and projected to climate models of the last glacial maximum (LGM). KEY RESULTS: A structured pattern of diversity was identified, with the presence of two groups that followed a climatic gradient from mesic to semi-arid regions. Most populations were represented by a single haplotype, but many haplotypes were shared among populations, with some having widespread distributions. A putative refugial area with high haplotype diversity was identified at the centre of the species distribution. Species distribution modelling showed high climatic suitability at the LGM and high climatic stability in the central region where higher genetic diversity was found, and low suitability elsewhere, consistent with a pattern of range contraction. CONCLUSIONS: Combination of phylogeography and paleo-distribution modelling can provide an evolutionary context for climate-driven tree decline, as both can be used to cross-validate evidence for refugia and contraction under harsh climatic conditions. This approach identified a central refugial area in the test species E. wandoo, with more recent expansion into peripheral areas from where it had contracted at the LGM. This signature of contraction from lower rainfall areas is consistent with current observations of decline on the semi-arid margin of the range, and indicates low capacity to tolerate forecast climatic change. Identification of a paleo-historical context for current tree decline enables conservation interventions to focus on maintaining genetic diversity, which provides the evolutionary potential for adaptation to climate change.

Isometric partitioning of hydraulic conductance between leaves and stems: balancing safety and efficiency in different growth forms and habitats.

Recent advances in modelling the architecture and function of the plant hydraulic network have led to improvements in predicting and interpreting the consequences of functional trait variation on CO2 uptake and water loss. We build upon one such model to make novel predictions for scaling of the total specific hydraulic conductance of leaves and shoots (kL and kSH , respectively) and variation in the partitioning of hydraulic conductance. Consistent with theory, we observed isometric (slope = 1) scaling between kL and kSH across several independently collected datasets and a lower ratio of kL and kSH , termed the leaf-to-shoot conductance ratio (CLSCR ), in arid environments and in woody species. Isometric scaling of kL and kSH supports the concept that hydraulic design is coordinated across the plant. We propose that CLSCR is an important adaptive trait that represents the trade-off between efficiency and safety at the scale of the whole plant.

Global variability in leaf respiration in relation to climate, plant functional types and leaf traits.

Leaf dark respiration (Rdark ) is an important yet poorly quantified component of the global carbon cycle. Given this, we analyzed a new global database of Rdark and associated leaf traits. Data for 899 species were compiled from 100 sites (from the Arctic to the tropics). Several woody and nonwoody plant functional types (PFTs) were represented. Mixed-effects models were used to disentangle sources of variation in Rdark . Area-based Rdark at the prevailing average daily growth temperature (T) of each site increased only twofold from the Arctic to the tropics, despite a 20°C increase in growing T (8-28°C). By contrast, Rdark at a standard T (25°C, Rdark (25) ) was threefold higher in the Arctic than in the tropics, and twofold higher at arid than at mesic sites. Species and PFTs at cold sites exhibited higher Rdark (25) at a given photosynthetic capacity (Vcmax (25) ) or leaf nitrogen concentration ([N]) than species at warmer sites. Rdark (25) values at any given Vcmax (25) or [N] were higher in herbs than in woody plants. The results highlight variation in Rdark among species and across global gradients in T and aridity. In addition to their ecological significance, the results provide a framework for improving representation of Rdark in terrestrial biosphere models (TBMs) and associated land-surface components of Earth system models (ESMs).

Simulation of the evolution of root water foraging strategies in dry and shallow soils.

BACKGROUND AND AIMS: The dynamic structural development of plants can be seen as a strategy for exploiting the limited resources available within their environment, and we would expect that evolution would lead to efficient strategies that reduce costs while maximizing resource acquisition. In particular, perennial species endemic to habitats with shallow soils in seasonally dry environments have been shown to have a specialized root system morphology that may enhance access to water resources in the underlying rock. This study aimed to explore these hypotheses by applying evolutionary algorithms to a functional-structural root growth model. METHODS: A simulation model of a plant's root system was developed, which represents the dynamics of water uptake and structural growth. The model is simple enough for evolutionary optimization to be computationally feasible, yet flexible enough to allow a range of structural development strategies to be explored. The model was combined with an evolutionary algorithm in order to investigate a case study habitat with a highly heterogeneous distribution of resources, both spatially and temporally--the situation of perennial plants occurring on shallow soils in seasonally dry environments. Evolution was simulated under two contrasting fitness criteria: (1) the ability to find wet cracks in underlying rock, and (2) maximizing above-ground biomass. KEY RESULTS: The novel approach successfully resulted in the evolution of more efficient structural development strategies for both fitness criteria. Different rooting strategies evolved when different criteria were applied, and each evolved strategy made ecological sense in terms of the corresponding fitness criterion. Evolution selected for root system morphologies which matched those of real species from corresponding habitats. CONCLUSIONS: Specialized root morphology with deeper rather than shallower lateral branching enhances access to water resources in underlying rock. More generally, the approach provides insights into both evolutionary processes and ecological costs and benefits of different plant growth strategies.

Spatio-temporal water dynamics in mature Banksia menziesii trees during drought.

Southwest Australian Banksia woodlands are highly diverse plant communities that are threatened by drought- or temperature-induced mortality due to the region's changing climate. We examined water relations in dominant Banksia menziesii R. Br. trees using magnetic leaf patch clamp pressure (ZIM-) probes that allow continuous, real-time monitoring of leaf water status. Multiple ZIM-probes across the crown were complemented by traditional ecophysiological measurements. During summer, early stomatal downregulation of transpiration prevented midday balancing pressures from exceeding 2.5 MPa. Diurnal patterns of ZIM-probe and pressure chamber readings agreed reasonably well, however, ZIM-probes recorded short-term dynamics, which are impossible to capture using a pressure chamber. Simultaneous recordings of three ZIM-probes evenly spaced along leaf laminas revealed intrafoliar turgor gradients, which, however, did not develop in a strictly basi- or acropetal fashion and varied with cardinal direction. Drought stress manifested as increasing daily signal amplitude (low leaf water status) and occasionally as rising baseline at night (delayed rehydration). These symptoms occurred more often locally than across the entire crown. Microclimate effects on leaf water status were strongest in crown regions experiencing peak morning radiation (East and North). Extreme spring temperatures preceded the sudden death of B. menziesii trees, suggesting a temperature- or humidity-related tipping point causing rapid hydraulic failure as evidenced by collapsing ZIM-probe readings from an affected tree. In a warmer and drier future, increased frequency of B. menziesii mortality will result in significantly altered community structure and ecosystem function.

Exploring rock fissures: does a specialized root morphology explain endemism on granite outcrops?

BACKGROUND AND AIMS: Worldwide, many plant species are confined to open, shallow-soil, rocky habitats. Although several hypotheses have been proposed to explain this habitat specificity, none has been convincing. We suggest that the high level of endemism on shallow soils is related to the edaphic specialization needed to survive in these often extremely drought-prone habitats. Previous research has shown that species endemic to ironstone communities in SW Australia have a specialized root morphology that enhances their chance to access fissures in the underlying rock. Here we test the generality of these findings for species that are confined to a shallow-soil habitat that is of much greater global significance: granite outcrops. METHODS: We compared temporal and spatial root growth and allocation of three endemic woody perennials of SW Australian granite outcrop communities with those of congeners occurring on nearby deeper soils. Seedlings of all species were grown in 1·2 m long custom-made containers with a transparent bottom that allowed monitoring of root growth over time. KEY RESULTS: The granite outcrop endemics mostly differed in a predictable way from their congeners from deeper soils. They generally invested a larger portion of their biomass in roots, distributed their roots faster and more evenly over the container and had a lower specific root length. In different species pairs the outcrop endemics achieved their apparent advantage by a different combination of the aforementioned traits. CONCLUSIONS: Our results are consistent with earlier work, indicating that species restricted to different types of drought-prone shallow-soil communities have undergone similar selection pressures. Although adaptive in their own habitat in terms of obtaining access to fissures in the underlying rock, these root system traits are likely to be maladaptive in deeper soil habitats. Therefore, our results may provide an explanation for the narrow endemism of many shallow-soil endemics.

Climate and landscape drivers of tree decline in a Mediterranean ecoregion.

Climate change and anthropogenic land use are increasingly affecting the resilience of natural ecosystems. In Mediterranean ecoregions, forests and woodlands have shown progressive declines in health. This study focuses on the decline of an endemic woodland tree species, Eucalyptus wandoo (wandoo), occurring in the biodiversity hotspot of southwest Western Australia. We determined the change in health of wandoo stands between 2002 and 2008 across its geographic and climatic range, and associated this change in health with non-biotic variables focusing on: (1) fragment metrics; (2) topography; (3) soil characteristics; and (4) climate. Only fragment metrics and climate variables were found to be significantly related to the observed change in health. Stands that were small with high perimeter/area ratios were found to be most sensitive to health declines. Recent increases in autumn temperatures and decreases in annual rainfall were negatively affecting health of wandoo most prominently in the low rainfall zone of its climatic range. Together, these results suggest the onset of range contraction for this ecologically important species, which is likely to be exacerbated by projected future changes in climate. Our results emphasize the importance of establishing monitoring programs to identify changes in health and decline trends early to inform management strategies, particularly in the sensitive Mediterranean ecoregions.

Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control.

We quantified the biomass allocation patterns to leaves, stems and roots in vegetative plants, and how this is influenced by the growth environment, plant size, evolutionary history and competition. Dose-response curves of allocation were constructed by means of a meta-analysis from a wide array of experimental data. They show that the fraction of whole-plant mass represented by leaves (LMF) increases most strongly with nutrients and decreases most strongly with light. Correction for size-induced allocation patterns diminishes the LMF-response to light, but makes the effect of temperature on LMF more apparent. There is a clear phylogenetic effect on allocation, as eudicots invest relatively more than monocots in leaves, as do gymnosperms compared with woody angiosperms. Plants grown at high densities show a clear increase in the stem fraction. However, in most comparisons across species groups or environmental factors, the variation in LMF is smaller than the variation in one of the other components of the growth analysis equation: the leaf area : leaf mass ratio (SLA). In competitive situations, the stem mass fraction increases to a smaller extent than the specific stem length (stem length : stem mass). Thus, we conclude that plants generally are less able to adjust allocation than to alter organ morphology.

Shallow-soil endemics: adaptive advantages and constraints of a specialized root-system morphology.

Worldwide, many rare plant species occur in shallow-soil, drought-prone environments. For most of these species, the adaptations required to be successful in their own habitats, as well as their possible consequences for establishment and persistence in others, are unknown. Here, two rare Hakea (Proteaceae) species confined to shallow-soil communities in mediterranean-climate south-western Australia were compared with four congeners commonly occurring on deeper soils. Seedlings were grown for 7 months in a glasshouse in individual 1.8 x 0.2-m containers, to allow for unconstrained root development. In addition, a reciprocal transplant experiment was carried out. The rare Hakea species differed consistently from their common congeners in their spatial root placement. They invested more in deep roots and explored the bottom of the containers much more quickly. In the reciprocal transplant experiment they showed increased survival in their own habitat, but not in others. This research suggests that shallow-soil endemics have a specialized root system that allows them to explore a large rock surface area, thereby presumably increasing their chance to locate cracks in the underlying rock. However, this root-system morphology may be maladaptive on deeper soils, providing a possible explanation for the restricted distribution of many shallow-soil endemics.

From individual leaf elongation to whole shoot leaf area expansion: a comparison of three Aegilops and two Triticum species.

BACKGROUND AND AIMS: Rapid leaf area expansion is a desirable trait in the early growth stages of cereal crops grown in low-rainfall areas. In this study, the traits associated with inherent variation in early leaf area expansion rates have been investigated in two wheat species (Triticum aestivum and T. durum) and three of its wild relatives (Aegilops umbellulata, A. caudata and A. tauschii) to find out whether the Aegilops species have a faster leaf area expansion in their early developmental stage than some of the current wheat species. METHODS: Growth of individual leaves, biomass allocation, and gas exchange were measured on hydroponically grown plants for 4 weeks. KEY RESULTS: Leaf elongation rate (LER) was strongly and positively correlated with leaf width but not with leaf elongation duration (LED). The species with more rapidly elongating leaves showed a faster increase with leaf position in LER, leaf width and leaf area, higher relative leaf area expansion rates, and more biomass allocation to leaf sheaths and less to roots. No differences in leaf appearance rate were found amongst the species. CONCLUSIONS: Aegilops tauschii was the only wild species with rapid leaf expansion rates similar to those of wheat, and it achieved the highest photosynthetic rates, making it an interesting species for further study.

The worldwide leaf economics spectrum.

Bringing together leaf trait data spanning 2,548 species and 175 sites we describe, for the first time at global scale, a universal spectrum of leaf economics consisting of key chemical, structural and physiological properties. The spectrum runs from quick to slow return on investments of nutrients and dry mass in leaves, and operates largely independently of growth form, plant functional type or biome. Categories along the spectrum would, in general, describe leaf economic variation at the global scale better than plant functional types, because functional types overlap substantially in their leaf traits. Overall, modulation of leaf traits and trait relationships by climate is surprisingly modest, although some striking and significant patterns can be seen. Reliable quantification of the leaf economics spectrum and its interaction with climate will prove valuable for modelling nutrient fluxes and vegetation boundaries under changing land-use and climate.

Short Communication: Leaf trait relationships in Australian plant species.

Leaf trait data were compiled for 258 Australian plant species from several habitat types dominated by woody perennials. Specific leaf area (SLA), photosynthetic capacity, dark respiration rate and leaf nitrogen (N) and phosphorus (P) concentrations were positively correlated with one another and negatively correlated with average leaf lifespan. These trait relationships were consistent with previous results from global datasets. Together, these traits form a spectrum of variation running from species with cheap but frequently replaced leaves to those with strategies more attuned to a nutrient-conserving lifestyle. Australian species tended to have SLAs at the lower end of the spectrum, as expected in a dataset dominated by sclerophyllous species from low fertility or low rainfall sites. The existence of broad-scale, 'global' relationships does not imply that the same trait relationships will always be observed in small datasets. In particular, the probability of observing concordant patterns depends on the range of trait variation in a dataset, which, itself, may vary with sample size or species-sampling properties such as the range of growth forms, plant functional 'types', or taxa included in a particular study. The considerable scatter seen in these broad-scale trait relationships may be associated with climate, physiology and phylogeny.