Leaf habit and plant architecture integrate whole-plant economics and contextualize trait-climate associations within ecologically diverse genus Rhododendron.

Plant resource strategies negotiate a trade-off between fast growth and stress resistance, characterized by specific leaf area (SLA). How SLA relates to leaf structure and function or plant climate associations remains open for debate, and leaf habit and plant architecture may alter the costs versus benefits of individual traits. We used phylogenetic canonical correspondence analysis and phylogenetic least squares to understand the relationship of anatomy and gas exchange to published data on root, wood, architectural and leaf economics traits and climate. Leaf anatomy was structured by leaf habit and carbon to nitrogen ratio was a better predictor of gas exchange than SLA. We found significant correspondence of leaf anatomy with branch architecture and wood traits, gas exchange corresponded with climate, while leaf economics corresponded with climate, architecture, wood and root traits. Species from the most seasonal climates had the highest trait-climate correspondence, and different aspects of economics and anatomy reflected leaf carbon uptake versus water use. Our study using phylogenetic comparative methods including plant architecture and leaf habit provides insight into the mechanism of whole-plant functional coordination and contextualizes individual traits in relation to climate, demonstrating the evolutionary and ecological relevance of trait-trait correlations within a genus with high biodiversity.

Juniperus virginiana sourced from colder climates maintain higher ratios of soluble sugars to starch during cold acclimation.

Non-structural carbohydrates (NSCs) are carbon compounds that serve a large variety of purposes, which makes it hard to disentangle how their concentrations change in response to environmental stress. Soluble sugars can accumulate in plants as metabolic demand decreases, e.g. in response to drought or as seasonal temperatures decrease. Alternatively, actively allocating to NSCs could be beneficial in cold acclimation or periods of increased aridity because soluble sugars serve non-metabolic functions as cryoprotectants and in osmoregulation. We used Juniperus virginiana, a woody plant currently expanding its range, to investigate whether plants sourced from colder and more arid locations maintained higher concentrations of NSCs. We sourced three populations of J. virginiana from across an environmental gradient, and we compared these with the closely related Juniperus scopulorum. We grew the plants in a common garden in northeast Ohio, part of J. virginiana's historic range. We exposed the plants to a drought treatment during the summer and then measured NSC concentrations and cold hardiness as the plants acclimated to colder temperatures and shorter days. We found that individuals originating from the warmer, more southern, range edge were initially not as cold hardy as plants from the other source populations and only reached similar hardiness after prolonged low temperatures. We did not find an effect of drought on NSCs, although this may be due to other traits conferring a high level of drought tolerance in J. virginiana. Across all plants, the NSCs concentration increased over the cold acclimation period, specifically as sugars. Although the highest concentrations of sugars were found in plants from southern populations, the plants from colder environments maintained higher ratios of sugars to starch. These results highlight the importance of NSCs in cold acclimation, and that plants sourced from different climates showed different physiological responses to shortening days and low temperatures.

Effects of post oak (Quercus stellata) and smooth brome (Bromus inermis) competition on water uptake and root partitioning of eastern redcedar (Juniperus virginiana).

Eastern redcedar Juniperus virginiana is encroaching into new habitats, which will affect native ecosystems as this species competes with other plants for available resources, including water. We designed a greenhouse experiment to investigate changes in soil moisture content and rooting depths of two-year-old J. virginiana saplings growing with or without competition. We had four competition treatments: 1) none, 2) with a native tree (Quercus stellata), 3) with an invasive grass (Bromus inermis), and 4) with both Q. stellata and B. inermis. We measured soil moisture content over two years as well as root length, total biomass, relative water content, midday water potential, and mortality at the end of the experiment. When J. virginiana and B. inermis grew together, water depletion occurred at both 30-40 cm and 10-20 cm. Combined with root length results, we can infer that J. virginiana most likely took up water from the deeper layers whereas B. inermis used water from the top layers. We found a similar pattern of water depletion and uptake when J. virginiana grew with Q. stellata, indicating that J. virginiana took up water from the deeper layers and Q. stellata used water mostly from the top soil layers. When the three species grew together, we found root overlap between J. virginiana and Q. stellata. Despite the root overlap, our relative water content and water potential indicate that J. virginiana was not water stressed in any of the plant combinations. Regardless, J. virginiana saplings had less total biomass in treatments with B. inermis and we recorded a significantly higher mortality when J. virginiana grew with both competitors. Root overlap and partitioning can affect how J. virginiana perform and adapt to new competitors and can allow their co-existence with grasses and other woody species, which can facilitate J. virginiana encroachment into grasslands and woodlands. Our data also show that competition with both Q. stellata and B. inermis could limit establishment, regardless of water availability.

Potential interactive effects between invasive Lumbricus terrestris earthworms and the invasive plant Alliaria petiolata on a native plant Podophyllum peltatum in northeastern Ohio, USA.

We test whether the invasive earthworm Lumbricus terrestris and leaf litter of the invasive herbaceous plant Alliaria petiolata interact to influence the native plant, Podophyllum peltatum, using both observational field data and a multi-year experiment. We hypothesized invader interactive effects on the native plant might result from either changes in allelochemical distribution in the soil or nutrient availability mediated by the invasive earthworm pulling leaf litter down into the soil. Within the field data we found that Alliaria petiolata presence and higher soil nitrogen correlated with reduced Podophyllum peltatum cover, and no evidence for an invader-invader interaction. Within the factorial experiment, we found a super-additive effect of the two invaders on plant biomass only when activated carbon was present. In the absence of activated carbon, there were no differences in Podophyllum peltatum biomass across treatments. In the presence of activated carbon, Podophyllum peltatum biomass was significantly reduced by the presence of both Lumbricus terrestris and Alliaria petiolata leaf litter. The absence of an effect of Alliaria petiolata leaves without activated carbon, combined with a failure to detect arbuscular mycorrhizal colonization, suggests that indirect effects of allelochemicals on arbuscular mycorrhizal fungi were not the primary driver of treatment responses. Rather direct nutrient availability might influence a potential interaction between these invaders. Leaf nitrogen content was higher and leaf CO2 concentration was lower in the presence of Lumbricus terrestris, but treatment did not influence maximum photosynthetic rate. While the field data do not suggest a negative interaction between these invaders, the experiment suggests that such an interaction is possible with greater environmental stress, such as increasing nitrogen deposition. Further, even plants with rapid physiological responses to increased nitrogen availability may have other physiological limits on growth that prevent them from compensating from the harm caused by multiple invaders.

The soil biotic community protects Rhododendron spp. across multiple clades from the oomycete Phytophthora cinnamomi at a cost to plant growth.

The effects of whole soil biotic communities on plants is a result of positive and negative interactions from a complex suite of mutualists and pathogens. However, few experiments have evaluated the composite effects of whole soil biotic communities on plant growth and disease resistance. We conducted a factorial greenhouse experiment with 14 Rhododendron species grown with and without live conspecific soil biota and with and without the disease, Phytophthora cinnamomi. We tested the prediction that the presence of whole soil biotic communities influences survival in the presence of disease. We also explored functional trait correlations with disease susceptibility across the phylogeny. The presence of live soil biota led to higher survival in the presence of disease compared with sterilized soils, and the direction of this effect was consistent for seven species across four clades. The presence of live soil biota also significantly reduced plant growth rate and decreased shoot biomass, relative to plants grown in sterilized soil, indicating that live soil biota might influence plant allocation strategies. We found that Rhododendron species with higher Root Shoot Ratios were less susceptible to Phytophthora, suggesting that water relations influence disease susceptibility. Our findings that disease resistance and susceptibility occur independently across multiple clades and that whole soil biotic communities consistently enhance disease resistance across clades, suggest that soil biota may play an important role in disease resistance and can moderate disease-induced mortality.

Vestured pits and scalariform perforation plate morphology modify the relationships between angiosperm vessel diameter, climate and maximum plant height.

Shared ancestry among species and correlation between vessel diameter and plant height can obscure the mechanisms linking vessel diameter to current climate distributions of angiosperms. Because wood is complex, various traits may interact to influence vessel function. Specifically, pit vesturing (lignified cell wall protuberances associated with bordered pits) and perforation plate morphology could alter the relationships between vessel diameter, climate and plant height. Using phylogenetically informed analyses, we tested for associations between vessel diameter, climate and maximum plant height across angiosperm species with different pit vesturing (presence/absence) and perforation plate morphology (simple/scalariform and quantitative variation). We show significantly larger changes in vessel diameter and maximum plant height across climates for species with vestures and simple perforation plates, compared to nonvestured species and those with scalariform plates. We also found a significantly greater increase in height for a given increase in vessel diameter with lower percentage of scalariform plates. Our study provides novel insights into the evolution of angiosperm xylem by showing that vessel pit vesturing and perforation plate morphologies can modify relationships among xylem vessels, climate and height. Our findings highlight the complexity of xylem adaptations to climate, substantiating an integrative view of xylem function in the study of wood evolution.

Decoupled leaf and root carbon economics is a key component in the ecological diversity and evolutionary divergence of deciduous and evergreen lineages of genus Rhododendron.

PREMISE: We explored trait-trait and trait-climate relationships for 27 Rhododendron species while accounting for phylogenetic relationships and within-species variation to investigate whether leaf and root traits are coordinated across environments and over evolutionary time, as part of a whole-plant economics spectrum. METHODS: We examined specific leaf area (SLA) and four root traits: specific root length (SRL), specific root tip abundance (SRTA), first order diameter, and link average length, for plants growing in a cold, seasonal climate (Kirtland, Ohio) and a warmer, less seasonal climate (Federal Way, Washington) in the United States. We estimated a phylogeny and species' climate of origin, determined phylogenetic signal on mean traits and within-species variation, and used phylogenetically informed analysis to compare trait-trait and trait-climate relationships for deciduous and evergreen lineages. RESULTS: Mean SLA and within-species variation in SRL were more similar between close relatives than expected by chance. SLA and root traits differed according to climate of origin and across growth environments, though SLA differed within- and among-species less than roots. A negative SRL-SRTA correlation indicates investment in foraging scale vs. precision as a fundamental trade-off defining the root economic spectrum. Also, the deciduous clade exhibited a strong negative relationship between SLA and SRL, while evergreen clades showed a weaker positive or no relationship. CONCLUSIONS: Our work suggests that natural selection has shaped relationships between above- and belowground traits in genus Rhododendron and that leaf and root traits may evolve independently. Morphological decoupling may help explain habitat diversity among Rhododendron species, as well as the changes accompanying the divergence of deciduous and evergreen lineages.

Fast-growing Acer rubrum differs from slow-growing Quercus alba in leaf, xylem and hydraulic trait coordination responses to simulated acid rain.

We investigated the effects of historic soil chemistry changes associated with acid rain, i.e., reduced soil pH and a shift from nitrogen (N)- to phosphorus (P)-limitation, on the coordination of leaf water demand and xylem hydraulic supply traits in two co-occurring temperate tree species differing in growth rate. Using a full-factorial design (N × P × pH), we measured leaf nutrient content, water relations, leaf-level and canopy-level gas exchange, total biomass and allocation, as well as stem xylem anatomy and hydraulic function for greenhouse-grown saplings of fast-growing Acer rubrum (L.) and slow-growing Quercus alba (L.). We used principle component analysis to characterize trait coordination. We found that N-limitation, but not P-limitation, had a significant impact on plant water relations and hydraulic coordination of both species. Fast-growing A. rubrum made hydraulic adjustments in response to N-limitation, but trait coordination was variable within treatments and did not fully compensate for changing allocation across N-availability. For slow-growing Q. alba, N-limitation engendered more strict coordination of leaf and xylem traits, resulting in similar leaf water content and hydraulic function across all treatments. Finally, low pH reduced the propensity of both species to adjust leaf water relations and xylem anatomical traits in response to nutrient manipulations. Our data suggest that a shift from N- to P-limitation has had a negative impact on the water relations and hydraulic function of A. rubrum to a greater extent than for Q. alba We suggest that current expansion of A. rubrum populations could be tempered by acidic N-deposition, which may restrict it to more mesic microsites. The disruption of hydraulic acclimation and coordination at low pH is emphasized as an interesting area of future study.

Freezing regime and trade-offs with water transport efficiency generate variation in xylem structure across diploid populations of Larrea sp. (Zygophyllaceae).

PREMISE OF THE STUDY: The impact of changing temperature regime on plant distributions may depend on the nature of physiological variation among populations. The arid-land genus Larrea spans habitats with a range of freezing frequency in North and South America. We hypothesized that variation in xylem anatomy among populations and species within this genus is driven by plasticity and trade-offs between safety from freeze-thaw embolism and water transport efficiency. METHODS: We measured vessel density and diameter distributions to predict freeze-thaw embolism and water transport capacity for high and low latitude populations of three Larrea species grown in the field and a greenhouse common garden. KEY RESULTS: Among field-grown L. divaricata, low latitude plants had larger mean vessel diameter and greater predicted freeze-thaw embolism, but higher water transport capacity compared with high latitude plants. Though high latitude L. tridentata and L. nitida had abundant smaller vessels, these plants also produced very large vessels and had semi ring-porous wood structure. Thus, their predicted embolism and water transport capacity were comparable to those of low latitude plants. Differences among field-grown and common-garden-grown plants demonstrate that plasticity contributes to population differentiation in xylem characters, though high latitude L. divaricata exhibited relatively lower plasticity. CONCLUSIONS: Our results indicate that a trade-off between transport safety and efficiency contributes substantially to variation in xylem structure within the genus Larrea. In addition, we suggest that xylem plasticity may play a role in negotiating these trade-offs, with implications for responses to future climate change.

Evolutionary history underlies plant physiological responses to global change since the last glacial maximum.

Assessing family- and species-level variation in physiological responses to global change across geologic time is critical for understanding factors that underlie changes in species distributions and community composition. Here, we used stable carbon isotopes, leaf nitrogen content and stomatal measurements to assess changes in leaf-level physiology in a mixed conifer community that underwent significant changes in composition since the last glacial maximum (LGM) (21 kyr BP). Our results indicate that most plant taxa decreased stomatal conductance and/or maximum photosynthetic capacity in response to changing conditions since the LGM. However, plant families and species differed in the timing and magnitude of these physiological responses, and responses were more similar within families than within co-occurring species assemblages. This suggests that adaptation at the level of leaf physiology may not be the main determinant of shifts in community composition, and that plant evolutionary history may drive physiological adaptation to global change over recent geologic time.

Increasing atmospheric [CO2] from glacial to future concentrations affects drought tolerance via impacts on leaves, xylem and their integrated function.

Changes in atmospheric carbon dioxide concentration ([CO2]) affect plant carbon/water tradeoffs, with implications for drought tolerance. Leaf-level studies often indicate that drought tolerance may increase with rising [CO2], but integrated leaf and xylem responses are not well understood in this respect. In addition, the influence of the low [CO2] of the last glacial period on drought tolerance and xylem properties is not well understood. We investigated the interactive effects of a broad range of [CO2] and plant water potentials on leaf function, xylem structure and function and the integration of leaf and xylem function in Phaseolus vulgaris. Elevated [CO2] decreased vessel implosion strength, reduced conduit-specific hydraulic conductance, and compromised leaf-specific xylem hydraulic conductance under moderate drought. By contrast, at glacial [CO2], transpiration was maintained under moderate drought via greater conduit-specific and leaf-specific hydraulic conductance in association with increased vessel implosion strength. Our study involving the integration of leaf and xylem responses suggests that increasing [CO2] does not improve drought tolerance. We show that, under glacial conditions, changes in leaf and xylem properties could increase drought tolerance, while under future conditions, greater productivity may only occur when higher water use can be accommodated.

Variation in seedling freezing response is associated with climate in Larrea.

Variation in freezing severity is hypothesized to have influenced the distribution and evolution of the warm desert evergreen genus Larrea. If this hypothesis is correct, performance and survival of species and populations should vary predictably along gradients of freezing severity. If freezing environment changes in the future, the ability of Larrea to adapt will depend on the structure of variation for freezing resistance within populations. To test whether freezing responses vary among and within Larrea populations, we grew maternal families of seedlings from high and low latitude L. divaricata and high latitude L. tridentata populations in a common garden. We measured survival, projected plant area and dark-adapted chlorophyll fluorescence (F (v) /F (m)) before and after cold acclimation and for 2 weeks following a single freeze. We detected significant variation in freezing resistance among species and populations. Maternal family lines differed significantly in their responses to cold acclimation and/or freezing for two out of the three populations: among L. tridentata maternal families and among low latitude L. divaricata maternal families. There were no significant differences across maternal families of high latitude L. divaricata. Our results indicate that increased freezing resistance in high latitude populations likely facilitated historical population expansion of both species into colder climates, but this may have occurred to a greater extent for L. tridentata than for L. divaricata. Differences in the structure of variation for cold acclimation and freezing responses among populations suggest potential differences in their ability to evolve in response to future changes in freezing severity.

Drought increases freezing tolerance of both leaves and xylem of Larrea tridentata.

Drought and freezing are both known to limit desert plant distributions, but the interaction of these stressors is poorly understood. Drought may increase freezing tolerance in leaves while decreasing it in the xylem, potentially creating a mismatch between water supply and demand. To test this hypothesis, we subjected Larrea tridentata juveniles grown in a greenhouse under well-watered or drought conditions to minimum temperatures ranging from -8 to -24 °C. We measured survival, leaf retention, gas exchange, cell death, freezing point depression and leaf-specific xylem hydraulic conductance (k1). Drought-exposed plants exhibited smaller decreases in gas exchange after exposure to -8 °C compared to well-watered plants. Drought also conferred a significant positive effect on leaf, xylem and whole-plant function following exposure to -15 °C; drought-exposed plants exhibited less cell death, greater leaf retention, higher k1 and higher rates of gas exchange than well-watered plants. Both drought-exposed and well-watered plants experienced 100% mortality following exposure to -24 °C. By documenting the combined effects of drought and freezing stress, our data provide insight into the mechanisms determining plant survival and performance following freezing and the potential for shifts in L. tridentata abundance and range in the face of changing temperature and precipitation regimes.

Pollen performance of Raphanus sativus (Brassicaceae) declines in response to elevated [CO(2)].

Although increases in atmospheric [CO(2)] are known to affect plant physiology, growth and reproduction, understanding of these effects is limited because most studies of reproductive consequences focus solely on female function. Therefore, we examined the effects of CO(2) enrichment on male function in the annual Raphanus sativus. Pollen donors grown under elevated [CO(2)] initially sired a higher proportion of seeds per fruit than ambient [CO(2)]-grown plants when each was tested against two different standard competitors; however, by the end of the 5-month experiment, these pollen donors sired fewer seeds than ambient [CO(2)]-grown plants and produced a lower proportion of viable pollen grains. The results of this experiment confirm that elevated [CO(2)] can alter reproductive success. Additionally, the change in response to elevated [CO(2)] over time varied among pollen donor families; thus, changes in [CO(2)] could act as a selective force on this species.

The impact of plant and flower age on mating patterns.

BACKGROUND: Over a season, plant condition, amount of ongoing reproduction and biotic and abiotic environmental factors vary. As flowers age, flower condition and amount of pollen donated and received also vary. These internal and external changes are significant for fitness if they result in changes in reproduction and mating. SCOPE: Literature from several fields was reviewed to provide a picture of the changes that occur in plants and flowers that can affect mating over a season. As flowers age, both the entire flower and individual floral whorls show changes in appearance and function. Over a season, changes in mating often appear as alteration in seed production vs. pollen donation. In several species, older, unpollinated flowers are more likely to self. If flowers are receiving pollen, staying open longer may increase the number of mates. In wild radish, for which there is considerable information on seed paternity, older flowers produce fewer seeds and appear to discriminate less among pollen donors. Pollen donor performance can also be linked to maternal plant age. Different pollinators and mates are available across the season. Also in wild radish, maternal plants appear to exert the most control over paternity when they are of intermediate age. CONCLUSIONS: Although much is known about the characters of plants and flowers that can change over a season, there is less information on the effects of age on mating. Several studies document changes in self-pollination over time, but very few, other than those on wild radish, consider more subtle aspects of differential success of pollen donors over time.

Do differences in plant and flower age change mating patterns and alter offspring fitness in Raphanus sativus (Brassicaceae)?

When more pollen is present on stigmas than needed to fertilize all ovules, selection among pollen grains may occur due to effects of both pollen donors and maternal plants. We asked whether increasing plant age and flower age, two changes in maternal condition, altered the pattern of seed paternity after mixed pollination. We also asked whether changes in seed paternity affected offspring success in an experimental garden. While flower age did not affect seed paternity, there was a dramatic shift in pollen donor performance as plants aged. These differences were seen in the offspring as well, where the offspring of one pollen donor, which sired more seeds on young plants, flowered earlier in the season, and the offspring of another pollen donor, which sired more seeds on old plants, flowered later in the season. Thus, change in maternal condition resulted in altered seed paternity, perhaps because the environment for pollen tube growth was different. The pattern of seed paternity and offspring performance suggests that pollen donors may show temporal specialization.

Differences in plastic responses to defoliation due to variation in the timing of treatments for two species of Sesbania (Fabaceae).

BACKGROUND AND AIMS: Plastic responses to stress in components of reproduction can have important effects on plant fitness and can vary both within and between species. Responses may also depend on when in the life cycle stress occurs. Here, it is predicted that the timing of initiation of a stress, defoliation, would affect the pattern of plastic responses. These differences should occur because some components of reproduction, such as flower number, are determined earlier in a plant's life than others, such as individual seed mass. METHODS: To test this prediction, 50 % artificial defoliation treatments were initiated at four different times for Sesbania macrocarpa and S. vesicaria. Responses were measured in plant size, number of flowers, number of flowers/plant size, fruit set, number of seeds per fruit, individual seed mass and total seed mass per plant. KEY RESULTS: For S. vesicaria, changes in the timing of stress changed the severity, but not the pattern of response. For S. macrocarpa, plastic responses to defoliation varied strikingly between early and late treatments. Late treatments resulted in over-compensation in this species. Sesbania macrocarpa was generally more plastic than S. vesicaria and the species showed opposite responses for most components of reproduction. CONCLUSIONS: While there were effects of timing of defoliation and differences between species, the nature of these effects did not precisely fit our predictions. Our results suggest that differences in the length and flexibility of the life cycles of the two species allowed for unexpected variation in responses. For example, because flower production continued after the last treatment in S. vesicaria, responses were not constrained to reductions in individual seed mass.