Combining botanical collections and ecological data to better describe plant community diversity.

In this age of rapid biodiversity loss, we must continue to refine our approaches to describing variation in life on Earth. Combining knowledge and research tools from multiple disciplines is one way to better describe complex natural systems. Understanding plant community diversity requires documenting both pattern and process. We must first know which species exist, and where (i.e., taxonomic and biogeographic patterns), before we can determine why they exist there (i.e., ecological and evolutionary processes). Floristic botanists often use collections-based approaches to elucidate biodiversity patterns, while plant ecologists use hypothesis-driven statistical approaches to describe underlying processes. Because of these different disciplinary histories and research goals, floristic botanists and plant ecologists often remain siloed in their work. Here, using a case study from an urban greenway in Colorado, USA, we illustrate that the collections-based, opportunistic sampling of floristic botanists is highly complementary to the transect- or plot-based sampling of plant ecologists. We found that floristic sampling captured a community species pool four times larger than that captured using ecological transects, with rarefaction and non-parametric species estimation indicating that it would be prohibitive to capture the "true" community species pool if constrained to sampling within transects. We further illustrate that the discrepancy in species pool size between approaches led to a different interpretation of the greenway's ecological condition in some cases (e.g., transects missed uncommon cultivated species escaping from nearby gardens) but not others (e.g., plant species distributions among functional groups were similar between species pools). Finally, we show that while using transects to estimate plant relative abundances necessarily trades off with a fuller assessment of the species pool, it is an indispensable indicator of ecosystem health, as evidenced by three non-native grasses contributing to 50% of plant cover along the highly modified urban greenway. We suggest that actively fostering collaborations between floristic botanists and ecologists can create new insights into the maintenance of species diversity at the community scale.

Global change stressors alter resources and shift plant interactions from facilitation to competition over time.

Global change stressors such as drought and plant invasion can affect ecosystem structure and function via mediation of resource availability and plant competition outcomes. Yet, it remains uncertain how native plants respond to drought stress that co-occurs with potentially novel resource conditions created by a nonnative invader. Further, there is likely to be temporal variation in competition outcomes between native and nonnative plant species depending on which resources are most limiting at a given time. Interacting stressors coupled with temporal variation make it difficult to predict how global change will impact native plant communities. To address this knowledge gap, we conducted a 5-yr factorial field experiment to quantify how simulated drought, plant invasion (by cogongrass, Imperata cylindrica), and these stressors combined, affected resource availability (soil moisture and light) and competition dynamics between the invader and native longleaf pine (Pinus palustris), a foundation species in southeast U.S. forests. Drought and invasion mediated the survival and performance of pine seedlings in temporally dynamic and unexpected ways. Drought and invasion alone each significantly reduced pine seedling survival. However, when the stressors occurred together, the invader offset drought stress for pine seedlings by maintaining high levels of soil moisture, humidity, and shade compared to uninvaded vegetation. This facilitative effect was pronounced for 2 yr, yet shifted to strong competitive exclusion as the invasion progressed and the limiting resource switched from soil moisture to light. After 3 yr, pine tree survival was low except for pines growing with uninvaded vegetation under ambient precipitation conditions. After 5 yr, pines experiencing a single stressor were taller and had greater height to diameter ratios than pines under no stress or both stressors. This outcome revealed a filtering effect where poorly performing trees were culled under stressful conditions, especially when pines were growing with the invader. Together, these results demonstrate that although drought and invasion suppressed a foundation tree species, the invader temporarily moderated stressful drought conditions, and at least some trees were able to survive despite increasingly strong competition. Such unpredictable effects of interacting global change stressors on native plant species highlight the need for additional long-term studies.

Methods to test the interactive effects of drought and plant invasion on ecosystem structure and function using complementary common garden and field experiments.

Abiotic global change drivers affect ecosystem structure and function, but how they interact with biotic factors such as invasive plants is understudied. Such interactions may be additive, synergistic, or offsetting, and difficult to predict. We present methods to test the individual and interactive effects of drought and plant invasion on native ecosystems. We coupled a factorial common garden experiment containing resident communities exposed to drought (imposed with rainout shelters) and invasion with a field experiment where the invader was removed from sites spanning a natural soil moisture gradient. We detail treatments and their effects on abiotic conditions, including soil moisture, light, temperature, and humidity, which shape community and ecosystem responses. Ambient precipitation during the garden experiment exceeded historic norms despite severe drought in prior years. Soil moisture was 48% lower in drought than ambient plots, but the invader largely offset drought effects. Additionally, temperature and light were lower and humidity higher in invaded plots. Field sites spanned up to a 10-fold range in soil moisture and up to a 2.5-fold range in light availability. Invaded and resident vegetation did not differentially mediate soil moisture, unlike in the garden experiment. Herbicide effectively removed invaded and resident vegetation, with removal having site-specific effects on soil moisture and light availability. However, light was generally higher in invader-removal than control plots, whereas resident removal had less effect on light, similar to the garden experiment. Invasion mitigated a constellation of abiotic conditions associated with drought stress in the garden experiment. In the field, where other factors co-varied, these patterns did not emerge. Still, neither experiment suggested that drought and invasion will have synergistic negative effects on ecosystems, although invasion can limit light availability. Coupling factorial garden experiments with field experiments across environmental gradients will be effective for predicting how multiple stressors interact in natural systems.

Geographic structuring and transgenerational maternal effects shape germination in native, but not introduced, populations of a widespread plant invader.

PREMISE OF THE STUDY: Germination is critical in determining species distributions and invasion dynamics. However, is it unclear how often invasive populations evolve germination characteristics different from native populations, because few studies have isolated genetic variation by using seed from garden-grown plants. Additionally, while herbivore-induced transgenerational effects are common, it is unknown whether maternal herbivory differentially shapes germination in native and introduced offspring. METHODS: We explored germination in native and introduced populations of the North American invader Verbascum thapsus using seed from garden-grown maternal plants, half of which were protected from herbivores. To elucidate (1) germination niche breadth and (2) whether germination conditions affected expression of genetic structuring among populations, we germinated seed under four ecologically relevant temperature regimes. KEY RESULTS: Native populations had a wide germination niche breadth, germinating as well as or better than introduced populations. At cooler temperatures, native populations exhibited a genetically based environmental cline indicative of local adaptation, with populations from warmer locales germinating better than populations from cooler locales. However, this cline was obscured when maternal plants were attacked by herbivores, revealing that local stressors can override the expression of geographic structuring. Introduced populations did not exhibit clinal variation, suggesting its disruption during the introduction process. CONCLUSIONS: Native and introduced populations have evolved genetic differences in germination. The result of this difference manifests in a wider germination niche breadth in natives, suggesting that the invasive behavior of V. thapsus in North America is attributable to other factors.

Naturalization of central European plants in North America: species traits, habitats, propagule pressure, residence time.

The factors that promote invasive behavior in introduced plant species occur across many scales of biological and ecological organization. Factors that act at relatively small scales, for example, the evolution of biological traits associated with invasiveness, scale up to shape species distributions among different climates and habitats, as well as other characteristics linked to invasion, such as attractiveness for cultivation (and by extension propagule pressure). To identify drivers of invasion it is therefore necessary to disentangle the contribution of multiple factors that are interdependent. To this end, we formulated a conceptual model describing the process of invasion of central European species into North America based on a sequence of "drivers." We then used confirmatory path analysis to test whether the conceptual model is supported by a statistical model inferred from a comprehensive database containing 466 species. The path analysis revealed that naturalization of central European plants in North America, in terms of the number of North American regions invaded, most strongly depends on residence time in the invaded range and the number of habitats occupied by species in their native range. In addition to the confirmatory path analysis, we identified the effects of various biological traits on several important drivers of the conceptualized invasion process. The data supported a model that included indirect effects of biological traits on invasion via their effect on the number of native range habitats occupied and cultivation in the native range. For example, persistent seed banks and longer flowering periods are positively correlated with number of native habitats, while a stress-tolerant life strategy is negatively correlated with native range cultivation. However, the importance of the biological traits is nearly an order of magnitude less than that of the larger scale drivers and highly dependent on the invasion stage (traits were associated only with native range drivers). This suggests that future research should explicitly link biological traits to the different stages of invasion, and that a failure to consider residence time or characteristics of the native range may seriously overestimate the role of biological traits, which, in turn, may result in spurious predictions of plant invasiveness.

Chemical and mechanical defenses vary among maternal lines and leaf ages in Verbascum thapsus L. (Scrophulariaceae) and reduce palatability to a generalist insect.

Intra-specific variation in host-plant quality affects herbivore foraging decisions and, in turn, herbivore foraging decisions mediate plant fitness. In particular, variation in defenses against herbivores, both among and within plants, shapes herbivore behavior. If variation in defenses is genetically based, it can respond to natural selection by herbivores. We quantified intra-specific variation in iridoid glycosides, trichome length, and leaf strength in common mullein (Verbascum thapsus L, Scrophulariaceae) among maternal lines within a population and among leaves within plants, and related this variation to feeding preferences of a generalist herbivore, Trichopulsia ni Hübner. We found significant variation in all three defenses among maternal lines, with T. ni preferring plants with lower investment in chemical, but not mechanical, defense. Within plants, old leaves had lower levels of all defenses than young leaves, and were strongly preferred by T. ni. Caterpillars also preferred leaves with trichomes removed to leaves with trichomes intact. Differences among maternal lines indicate that phenotypic variation in defenses likely has a genetic basis. Furthermore, these results reveal that the feeding behaviors of T. ni map onto variation in plant defense in a predictable way. This work highlights the importance of variation in host-plant quality in driving interactions between plants and their herbivores.

Do invasive species perform better in their new ranges?

A fundamental assumption in invasion biology is that most invasive species exhibit enhanced performance in their introduced range relative to their home ranges. This idea has given rise to numerous hypotheses explaining "invasion success" by virtue of altered ecological and evolutionary pressures. There are surprisingly few data, however, testing the underlying assumption that the performance of introduced populations, including organism size, reproductive output, and abundance, is enhanced in their introduced compared to their native range. Here, we combined data from published studies to test this hypothesis for 26 plant and 27 animal species that are considered to be invasive. On average, individuals of these 53 species were indeed larger, more fecund, and more abundant in their introduced ranges. The overall mean, however, belied significant variability among species, as roughly half of the investigated species (N=27) performed similarly when compared to conspecific populations in their native range. Thus, although some invasive species are performing better in their new ranges, the pattern is not universal, and just as many are performing largely the same across ranges.

Combining optimal defense theory and the evolutionary dilemma model to refine predictions regarding plant invasion.

Optimal defense theory posits that plants with limited resources deploy chemical defenses based on the fitness value of different tissues and their probability of attack. However, what constitutes optimal defense depends on the identity of the herbivores involved in the interaction. Generalists, which are not tightly coevolved with their many host plants, are typically deterred by chemical defenses, while coevolved specialists are often attracted to these same chemicals. This imposes an "evolutionary dilemma" in which generalists and specialists exert opposing selection on plant investment in defense, thereby stabilizing defenses at intermediate levels. We used the natural shift in herbivore community composition that typifies many plant invasions to test a novel, combined prediction of optimal defense theory and the evolutionary dilemma model: that the within-plant distribution of defenses reflects both the value of different tissues (i.e., young vs. old leaves) and the relative importance of specialist and generalist herbivores in the community. Using populations of Verbascum thapsus exposed to ambient herbivory in its native range (where specialist and generalist chewing herbivores are prevalent) and its introduced range (where only generalist chewing herbivores are prevalent), we illustrate significant differences in the way iridoid glycosides are distributed among young and old leaves. Importantly, high-quality young leaves are 6.5x more highly defended than old leaves in the introduced range, but only 2x more highly defended in the native range. Additionally, defense levels are tracked by patterns of chewing damage, with damage restricted mostly to low-quality old leaves in the introduced range, but not the native range. Given that whole-plant investment in defense does not differ between ranges, introduced mullein may achieve increased fitness simply by optimizing its within-plant distribution of defense in the absence of certain specialist herbivores.