Effects of snow on reproduction of perennial Thalictrum dioicum: Plants survive but seedlings fail to recruit with reduced snow cover.

PREMISE: Future reductions in snow cover are expected in temperate climates, likely leading to more soil-freezing events and damage to plant tissues. However, whether and how plants can compensate for this damage may depend on the timing of damage and on plant allocations to seed size and number. We need more information about how seed production, germination, and seedling recruitment might respond to changes in snow cover. METHODS: We manipulated snow cover over three seasons in a common garden experiment with four treatments: (1) "control," where snowpack was left unmanipulated throughout the winter season; (2) "late addition," where snowpack was experimentally increased at the end of the winter season in order to delay the onset of spring; (3) "late removal," where snowpack was experimentally reduced at the end of the winter season in order to advance the onset of spring; and (4) "freeze," a consistent removal treatment, where snowpack was experimentally reduced following every substantial snowfall in order to induce freeze-thaw events in the soil. In all treatments, we measured survival, growth, reproduction, and recruitment of a native perennial herb, Thalictrum dioicum. RESULTS: Reduced snow cover minimally influenced adult survival. Instead, individuals that experienced reduced snow cover throughout the winter produced more massive seeds, whereas individuals that experienced a single snow removal at the end of the season produced less massive seeds. Seedling recruitment was lower in the removal treatments than in the control, as a result of failure to germinate in the freeze treatment and seedling mortality in the late removal treatment. CONCLUSIONS: Both reduced snow cover throughout the winter and a single late snow removal in the spring reduced seedling recruitment, but for different reasons, suggesting that a holistic approach to the life cycle is needed to understand responses to shifting climates.

The myriad of complex demographic responses of terrestrial mammals to climate change and gaps of knowledge: A global analysis.

Approximately 25% of mammals are currently threatened with extinction, a risk that is amplified under climate change. Species persistence under climate change is determined by the combined effects of climatic factors on multiple demographic rates (survival, development and reproduction), and hence, population dynamics. Thus, to quantify which species and regions on Earth are most vulnerable to climate-driven extinction, a global understanding of how different demographic rates respond to climate is urgently needed. Here, we perform a systematic review of literature on demographic responses to climate, focusing on terrestrial mammals, for which extensive demographic data are available. To assess the full spectrum of responses, we synthesize information from studies that quantitatively link climate to multiple demographic rates. We find only 106 such studies, corresponding to 87 mammal species. These 87 species constitute <1% of all terrestrial mammals. Our synthesis reveals a strong mismatch between the locations of demographic studies and the regions and taxa currently recognized as most vulnerable to climate change. Surprisingly, for most mammals and regions sensitive to climate change, holistic demographic responses to climate remain unknown. At the same time, we reveal that filling this knowledge gap is critical as the effects of climate change will operate via complex demographic mechanisms: a vast majority of mammal populations display projected increases in some demographic rates but declines in others, often depending on the specific environmental context, complicating simple projections of population fates. Assessments of population viability under climate change are in critical need to gather data that account for multiple demographic responses, and coordinated actions to assess demography holistically should be prioritized for mammals and other taxa.

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.

Tests of alternative evolutionary models are needed to enhance our understanding of biological invasions.

Contents Summary 701 I. Introduction 701 II. Why we need an explicitly evolutionary perspective 702 III. A case study invasion experiment 702 IV. The way forward 703 V. Conclusions 705 Acknowledgements 706 References 706 SUMMARY: Comparing models of trait evolution might generate new insights into the role of evolutionary history in biological invasions. Assumptions underlying Darwin's naturalization conundrum suggest that close relatives are functionally similar. However, newer work is suggesting more complex relationships between phylogenetic and functional distance. We present an example in which communities of close relatives are functionally divergent in leaf traits and have greater invader biomass. Such an approach leads to new questions, such as: When might selection lead to divergence between close relatives? For example, a history of sympatry might correspond with divergence. We suggest that moving beyond a simplistic version of Darwin's naturalization conundrum as alternative hypotheses will lead to a more nuanced view on how evolution has shaped biological invasions.

Plant traits moderate pollen limitation of introduced and native plants: a phylogenetic meta-analysis of global scale.

The role of pollination in the success of invasive plants needs to be understood because invasives have substantial effects on species interactions and ecosystem functions. Previous research has shown both that reproduction of invasive plants is often pollen limited and that invasive plants can have high seed production, motivating the questions: How do invasive populations maintain reproductive success in spite of pollen limitation? What species traits moderate pollen limitation for invaders? We conducted a phylogenetic meta-analysis with 68 invasive, 50 introduced noninvasive and 1931 native plant populations, across 1249 species. We found that invasive populations with generalist pollination or pollinator dependence were less pollen limited than natives, but invasives and introduced noninvasives did not differ. Invasive species produced 3× fewer ovules/flower and >250× more flowers per plant, compared with their native relatives. While these traits were negatively correlated, consistent with a tradeoff, this did not differ with invasion status. Invasive plants that produce many flowers and have floral generalisation are able to compensate for or avoid pollen limitation, potentially helping to explain the invaders' reproductive successes.

Species composition, functional and phylogenetic distances correlate with success of invasive Chromolaena odorata in an experimental test.

Biotic resistance may influence invasion success; however, the relative roles of species richness, functional or phylogenetic distance in predicting invasion success are not fully understood. We used biomass fraction of Chromolaena odorata, an invasive species in tropical and subtropical areas, as a measure of 'invasion success' in a series of artificial communities varying in species richness. Communities were constructed using species from Mexico (native range) or China (non-native range). We found strong evidence of biotic resistance: species richness and community biomass were negatively related with invasion success; invader biomass was greater in plant communities from China than from Mexico. Harvesting time had a greater effect on invasion success in plant communities from China than on those from Mexico. Functional and phylogenetic distances both correlated with invasion success and more functionally distant communities were more easily invaded. The effects of plant-soil fungi and plant allelochemical interactions on invasion success were species-specific.

Symbioses with nitrogen-fixing bacteria: nodulation and phylogenetic data across legume genera.

How species interactions shape global biodiversity and influence diversification is a central - but also data-hungry - question in evolutionary ecology. Microbially based mutualisms are widespread and could cause diversification by ameliorating stress and thus allowing organisms to colonize and adapt to otherwise unsuitable habitats. Yet the role of these interactions in generating species diversity has received limited attention, especially across large taxonomic groups. In the massive angiosperm family Leguminosae, plants often associate with root-nodulating bacteria that ameliorate nutrient stress by fixing atmospheric nitrogen. These symbioses are ecologically-important interactions, influencing community assembly, diversity, and succession, contributing ~100-290 million tons of N annually to natural ecosystems, and enhancing growth of agronomically-important forage and crop plants worldwide. In recent work attempting to determine whether mutualism with N-fixing bacteria led to increased diversification across legumes, we were unable to definitively resolve the relationship between diversification and nodulation. We did, however, succeed in compiling a very large searchable, analysis-ready database of nodulation data for 749 legume genera (98% of Leguminosae genera; LPWG 2017), which, along with associated phylogenetic information, will provide a valuable resource for future work addressing this question and others. For each legume genus, we provide information about the species richness, frequency of nodulation, subfamily association, and topological correspondence with an additional data set of 100 phylogenetic trees curated for database compatibility. We found 386 legume genera were confirmed nodulators (i.e., all species examined for nodulation nodulated), 116 were non-nodulating, four were variable (i.e., containing both confirmed nodulators and confirmed non-nodulators), and 243 had not been examined for nodulation in published studies. Interestingly, data exploration revealed that nodulating legume genera are ~3 × more species-rich than non-nodulating genera, but we did not find evidence that this difference in diversity was due to differences in net diversification rate. Our metadata file describes in more detail the structure of these data that provide a foundational resource for future work as more nodulation data become available, and as greater phylogenetic resolution of this ca. 19,500-species family comes into focus. We release this data set under the Creative Commons 4.0 Attribution-ShareAlike License (https://creativecommons.org/licenses/by-sa/4.0/). The data may be used, distributed, and reproduced with proper citation of this article.

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.

Spatial heterogeneity of plant-soil feedbacks increases per capita reproductive biomass of species at an establishment disadvantage.

Plant-soil feedbacks have been widely implicated as a driver of plant community diversity, and the coexistence prediction generated by a negative plant-soil feedback can be tested using the mutual invasibility criterion: if two populations are able to invade one another, this result is consistent with stable coexistence. We previously showed that two co-occurring Rumex species exhibit negative pairwise plant-soil feedbacks, predicting that plant-soil feedbacks could lead to their coexistence. However, whether plants are able to reproduce when at an establishment disadvantage ("invasibility"), or what drivers in the soil might correlate with this pattern, are unknown. To address these questions, we created experimental plots with heterogeneous and homogeneous soils using field-collected conditioned soils from each of these Rumex species. We then allowed resident plants of each species to establish and added invader seeds of the congener to evaluate invasibility. Rumex congeners were mutually invasible, in that both species were able to establish and reproduce in the other's resident population. Invaders of both species had twice as much reproduction in heterogeneous compared to homogeneous soils; thus the spatial arrangement of plant-soil feedbacks may influence coexistence. Soil mixing had a non-additive effect on the soil bacterial and fungal communities, soil moisture, and phosphorous availability, suggesting that disturbance could dramatically alter soil legacy effects. Because the spatial arrangement of soil patches has coexistence implications, plant-soil feedback studies should move beyond studies of mean effects of single patch types, to consider how the spatial arrangement of patches in the field influences plant communities.

Functional trait values, not trait plasticity, drive the invasiveness of Rosa sp. in response to light availability.

PREMISE OF THE STUDY: Functional trait plasticity in resource capture traits has been suggested as an underlying mechanism promoting invasive species establishment and spread. Earlier studies on this mechanism treat invasiveness as a discrete characteristic (i.e., invasive vs. noninvasive) and do not consider the potential impacts of evolutionary history. In the present study, we used a continuous measure of invasiveness and a phylogenetic framework to quantify the relationship between functional trait expression, plasticity, and invasiveness in Rosa. METHODS: In a manipulative greenhouse experiment, we evaluated how light availability affects functional traits and their plasticity in Rosa sp. and the out-group species, Potentilla recta, which vary in their invasiveness. KEY RESULTS: Across functional traits, we found no significant relationship between plasticity and invasiveness. However, more invasive roses demonstrated an ability to produce a more branched plant architecture, promoting optimal light capture. Invasiveness also was linked with lower photosynthetic and stomatal conductance rates, leading to increased water-use efficiency (WUE) in more invasive roses. CONCLUSIONS: Our results suggest that functional trait values, rather than plasticity, promote invasive rose success, counter to earlier predictions about the role of plasticity in invasiveness. Furthermore, our study indicates that invasive roses demonstrate key functional traits, such as increased WUE, to promote their success in the high-light, edge habitats they commonly invade.

Plant trait expression responds to establishment timing.

Trait divergence between co-occurring individuals could decrease the strength of competition between these individuals, thus promoting their coexistence. To test this hypothesis, we manipulated establishment timing for four congeneric pairs of perennial plants and assessed trait plasticity. Because soil conditions can affect trait expression and competition, we grew the plants in field-collected soil from each congener. Competition was generally weak across species, but the order of establishment affected divergence in biomass between potmates for three congeneric pairs. The type of plastic response differed among genera, with trait means of early-establishing individuals of Rumex and Solanum spp. differing from late-establishing individuals, and trait divergence between potmates of Plantago and Trifolium spp. depending on which species established first. Consistent with adaptive trait plasticity, higher specific leaf area (SLA) and root-shoot ratio in Rumex spp. established later suggest that these individuals were maximizing their ability to capture light and soil resources. Greater divergence in SLA correlated with increased summed biomass of competitors, which is consistent with trait divergence moderating the strength of competition for some species. Species did not consistently perform better in conspecific or congener soil, but soil type influenced the effect of establishment order. For example, biomass divergence between Rumex potmates was greater in R. obtusifolius soil regardless of which species established first. These results suggest that plant responses to establishment timing act in a species-specific fashion, potentially enhancing coexistence in plant communities.

More closely related species are more ecologically similar in an experimental test.

The relationship between phylogenetic distance and ecological similarity is key to understanding mechanisms of community assembly, a central goal of ecology. The field of community phylogenetics uses phylogenetic information to infer mechanisms of community assembly; we explore, the underlying relationship between phylogenetic similarity and the niche. We combined a field experiment using 32 native plant species with a molecular phylogeny and found that closely related plant species shared similar germination and early survival niches. Species also competed more with close relatives than with distant relatives in field soils; however, in potting soil this pattern reversed, and close relatives might even have more mutalistic relationships than distant relatives in these soils. Our results suggest that niche conservatism (habitat filtering) and species interactions (competition or facilitation) structure community composition, that phylogenetic relationships influence the strength of species' interactions, and that conserved aspects of plant niches include soil attributes.

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.

Greater sexual reproduction contributes to differences in demography of invasive plants and their noninvasive relatives.

An understanding of the demographic processes contributing to invasions would improve our mechanistic understanding of the invasion process and improve the efficiency of prevention and control efforts. However, field comparisons of the demography of invasive and noninvasive species have not previously been conducted. We compared the in situ demography of 17 introduced plant species in St. Louis, Missouri, USA, to contrast the demographic patterns of invasive species with their less invasive relatives across a broad sample of angiosperms. Using herbarium records to estimate spread rates, we found higher maximum spread rates in the landscape for species classified a priori as invasive than for noninvasive introduced species, suggesting that expert classifications are an accurate reflection of invasion rate. Across 17 species, projected population growth was not significantly greater in invasive than in noninvasive introduced species. Among five taxonomic pairs of close relatives, however, four of the invasive species had higher projected population growth rates compared with their noninvasive relative. A Life Table Response Experiment suggested that the greater projected population growth rate of some invasive species relative to their noninvasive relatives was primarily a result of sexual reproduction. The greater sexual reproduction of invasive species is consistent with invaders having a life history strategy more reliant on fecundity than survival and is consistent with a large role of propagule pressure in invasion. Sexual reproduction is a key demographic correlate of invasiveness, suggesting that local processes influencing sexual reproduction, such as enemy escape, might be of general importance. However, the weak correlation of projected population growth with spread rates in the landscape suggests that regional processes, such as dispersal, may be equally important in determining invasion rate.

A phylogenetically controlled analysis of the roles of reproductive traits in plant invasions.

Reproductive traits are tightly linked to plant fitness and may therefore be mechanisms driving biological invasions, including the greater success of more phylogenetically novel introduced species in some systems. We present a phylogenetic comparative analysis of "Baker's law'', that introduced plants with the ability to reproduce autogamous or asexually may be better able to establish on introduction. We gathered data from both published and unpublished sources on pollen limitation of 141 species, including 26 introduced species and 115 native species. Our analysis compared differences in the proportion of autonomous autogamy, asexual reproduction, and pollen limitation among native, introduced noninvasive, and introduced invasive plant species, and included the phylogenetic novelty of the introduced species to the native species in that community. Introduced species were more likely to be autogamous than native species, consistent with Baker's law. On the other hand, introduced species were less likely to have the ability to reproduce asexually. Further, among species with no autonomous autogamy, pollen limitation was greater for introduced compared to native species. Such a result is consistent with the idea that plants entering a new continent receive lower quality or quantity of services from resident pollinators than species native to that continent. Finally, more phylogenetically novel invasive species had lower pollen limitation than less novel invasive species, potentially because they experience less competition for pollinators. This is the first evidence that enhanced pollination may be one mechanism driving the greater invasiveness of phylogenetically novel introduced species observed in some systems.

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.

Herbaceous perennial plants with short generation time have stronger responses to climate anomalies than those with longer generation time.

There is an urgent need to synthesize the state of our knowledge on plant responses to climate. The availability of open-access data provide opportunities to examine quantitative generalizations regarding which biomes and species are most responsive to climate drivers. Here, we synthesize time series of structured population models from 162 populations of 62 plants, mostly herbaceous species from temperate biomes, to link plant population growth rates (λ) to precipitation and temperature drivers. We expect: (1) more pronounced demographic responses to precipitation than temperature, especially in arid biomes; and (2) a higher climate sensitivity in short-lived rather than long-lived species. We find that precipitation anomalies have a nearly three-fold larger effect on λ than temperature. Species with shorter generation time have much stronger absolute responses to climate anomalies. We conclude that key species-level traits can predict plant population responses to climate, and discuss the relevance of this generalization for conservation planning.

Widespread vulnerability of flowering plant seed production to pollinator declines.

Despite evidence of pollinator declines from many regions across the globe, the threat this poses to plant populations is not clear because plants can often produce seeds without animal pollinators. Here, we quantify pollinator contribution to seed production by comparing fertility in the presence versus the absence of pollinators for a global dataset of 1174 plant species. We estimate that, without pollinators, a third of flowering plant species would produce no seeds and half would suffer an 80% or more reduction in fertility. Pollinator contribution to plant reproduction is higher in plants with tree growth form, multiple reproductive episodes, more specialized pollination systems, and tropical distributions, making these groups especially vulnerable to reduced service from pollinators. These results suggest that, without mitigating efforts, pollinator declines have the potential to reduce reproduction for most plant species, increasing the risk of population declines.

Causes and consequences of variation in plant population growth rate: a synthesis of matrix population models in a phylogenetic context.

Explaining variation in population growth rates is fundamental to predicting population dynamics and population responses to environmental change. In this study, we used matrix population models, which link birth, growth and survival to population growth rate, to examine how and why population growth rates vary within and among 50 terrestrial plant species. Population growth rates were more similar within species than among species; with phylogeny having a minimal influence on among-species variation. Most population growth rates decreased over the observation period and were negatively autocorrelated between years; that is, higher than average population growth rates tended to be followed by lower than average population growth rates. Population growth rates varied more through time than space; this temporal variation was due mostly to variation in post-seedling survival and for a subset of species was partly explained by response to environmental factors, such as fire and herbivory. Stochastic population growth rates departed from mean matrix population growth rate for temporally autocorrelated environments. Our findings indicate that demographic data and models of closely related plant species cannot necessarily be used to make recommendations for conservation or control, and that post-seedling survival and the sequence of environmental conditions are critical for determining plant population growth rate.

Land use and pollinator dependency drives global patterns of pollen limitation in the Anthropocene.

Land use change, by disrupting the co-evolved interactions between plants and their pollinators, could be causing plant reproduction to be limited by pollen supply. Using a phylogenetically controlled meta-analysis on over 2200 experimental studies and more than 1200 wild plants, we ask if land use intensification is causing plant reproduction to be pollen limited at global scales. Here we report that plants reliant on pollinators in urban settings are more pollen limited than similarly pollinator-reliant plants in other landscapes. Plants functionally specialized on bee pollinators are more pollen limited in natural than managed vegetation, but the reverse is true for plants pollinated exclusively by a non-bee functional group or those pollinated by multiple functional groups. Plants ecologically specialized on a single pollinator taxon were extremely pollen limited across land use types. These results suggest that while urbanization intensifies pollen limitation, ecologically and functionally specialized plants are at risk of pollen limitation across land use categories.