Parasites as ecosystem modulators: foliar pathogens suppress top-down effects of large herbivores.

Parasites can catalyze or inhibit interactions between their hosts and other species, but the ecosystem-level effects of such interaction modifications are poorly understood. We conducted a large-scale field experiment in temperate grasslands of China to understand how foliar fungal pathogens influenced top-down effects of cattle on plant diversity and productivity. When foliar pathogens were suppressed, cattle grazing strongly reduced biomass of the dominant grass, Leymus chinensis, generating competitive release that significantly increased community-level species richness and evenness. In the absence of grazing, pathogen attack on L. chinensis had no measurable effect on host biomass. However, pathogens disrupted top-down effects of herbivory by inhibiting grazing effects on plant biomass and species richness. Mechanistically, fungal pathogens were linked to increased alkaloid and reduced nitrogen levels in leaf tissue, which appeared to deter cattle grazing on L. chinensis. In conclusion, foliar pathogens can suppress top-down effects of large herbivores on grassland community composition and ecosystem function by modifying the strength of their host's interactions with dominant consumers. Parasites may act as modulators of ecosystem function when their direct effects on host abundance are overshadowed by powerful influences on host traits that modify their interactions with competitors, herbivores, or predators.

Seed predator effects on plants: Moving beyond time-corrected proxies.

We previously demonstrated that small mammals impact plant recruitment globally via size-dependent seed predation, generating a unimodal pattern across ecosystems. Chen et al. (2021) critiqued our seed removal analysis, advocating corrections for exposure time. We show such manipulations are unwarranted and argue for increased emphasis on plant recruitment metrics.

Seed size predicts global effects of small mammal seed predation on plant recruitment.

Recent studies demonstrate that by focusing on traits linked to fundamental plant life-history trade-offs, ecologists can begin to predict plant community structure at global scales. Yet, consumers can strongly affect plant communities, and means for linking consumer effects to key plant traits and community assembly processes are lacking. We conducted a global literature review and meta-analysis to evaluate whether seed size, a trait representing fundamental life-history trade-offs in plant offspring investment, could predict post-dispersal seed predator effects on seed removal and plant recruitment. Seed size predicted small mammal seed removal rates and their impacts on plant recruitment consistent with optimal foraging theory, with intermediate seed sizes most strongly impacted globally - for both native and exotic plants. However, differences in seed size distributions among ecosystems conditioned seed predation patterns, with relatively large-seeded species most strongly affected in grasslands (smallest seeds), and relatively small-seeded species most strongly affected in tropical forests (largest seeds). Such size-dependent seed predation has profound implications for coexistence among plants because it may enhance or weaken opposing life-history trade-offs in an ecosystem-specific manner. Our results suggest that seed size may serve as a key life-history trait that can integrate consumer effects to improve understandings of plant coexistence.

The fluctuating resource hypothesis explains invasibility, but not exotic advantage following disturbance.

Invasibility is a key indicator of community susceptibility to changes in structure and function. The fluctuating resource hypothesis (FRH) postulates that invasibility is an emergent community property, a manifestation of multiple processes that cannot be reliably predicted by individual community attributes like diversity or productivity. Yet, research has emphasized the role of these individual attributes, with the expectation that diversity should deter invasibility and productivity enhance it. In an effort to explore how these and other factors may influence invasibility, we evaluated the relationship between invasibility and species richness, productivity, resource availability, and resilience in experiments crossing disturbance with exotic seed addition in 1-m2 plots replicated over large expanses of grasslands in Montana, USA and La Pampa, Argentina. Disturbance increased invasibility as predicted by FRH, but grasslands were more invasible in Montana than La Pampa whether disturbed or not, despite Montana's higher species richness and lower productivity. Moreover, invasibility correlated positively with nitrogen availability and negatively with native plant cover. These patterns suggested that resource availability and the ability of the community to recover from disturbance (resilience) better predicted invasibility than either species richness or productivity, consistent with predictions from FRH. However, in ambient, unseeded plots in Montana, disturbance reduced native cover by >50% while increasing exotic cover >200%. This provenance bias could not be explained by FRH, which predicts that colonization processes act on species' traits independent of origins. The high invasibility of Montana grasslands following disturbance was associated with a strong shift from perennial to annual species, as predicted by succession theory. However, this shift was driven primarily by exotic annuals, which were more strongly represented than perennials in local exotic vs. native species pools. We attribute this provenance bias to extrinsic biogeographic factors such as disparate evolutionary histories and/or introduction filters selecting for traits that favor exotics following disturbance. Our results suggest that (1) invasibility is an emergent property best explained by a community's efficiency in utilizing resources, as predicted by FRH but (2) understanding provenance biases in biological invasions requires moving beyond FRH to incorporate extrinsic biogeographic factors that may favor exotics in community assembly.

Negative plant-soil feedbacks increase with plant abundance, and are unchanged by competition.

Plant-soil feedbacks and interspecific competition are ubiquitous interactions that strongly influence the performance of plants. Yet few studies have examined whether the strength of these interactions corresponds with the abundance of plant species in the field, or whether feedbacks and competition interact in ways that either ameliorate or exacerbate their effects in isolation. We sampled soil from two intermountain grassland communities where we also measured the relative abundance of plant species. In greenhouse experiments, we quantified the direction and magnitude of plant-soil feedbacks for 10 target species that spanned a range of abundances in the field. In soil from both sites, plant-soil feedbacks were mostly negative, with more abundant species suffering greater negative feedbacks than rare species. In contrast, the average response to competition for each species was unrelated with its abundance in the field. We also determined how competitive response varied among our target species when plants competed in live vs. sterile soil. Interspecific competition reduced plant size, but the strength of this negative effect was unchanged by plant-soil feedbacks. Finally, when plants competed interspecifically, we asked how conspecific-trained, heterospecific-trained, and sterile soil influenced the competitive responses of our target species and how this varied depending on whether target species were abundant or rare in the field. Here, we found that both abundant and rare species were not as harmed by competition when they grew in heterospecific-trained soil compared to when they grew in conspecific-cultured soil. Abundant species were also not as harmed by competition when growing in sterile vs. conspecific-trained soil, but this was not the case for rare species. Our results suggest that abundant plants accrue species-specific soil pathogens to a greater extent than rare species. Thus, negative feedbacks may be critical for preventing abundant species from becoming even more abundant than rare species.

Quantifying "apparent" impact and distinguishing impact from invasiveness in multispecies plant invasions.

The quantification of invader impacts remains a major hurdle to understanding and managing invasions. Here, we demonstrate a method for quantifying the community-level impact of multiple plant invaders by applying Parker et al.'s (1999) equation (impact = range x local abundance x per capita effect or per unit effect) using data from 620 survey plots from 31 grasslands across west-central Montana, USA. In testing for interactive effects of multiple invaders on native plant abundance (percent cover), we found no evidence for invasional meltdown or synergistic interactions for the 25 exotics tested. While much concern exists regarding impact thresholds, we also found little evidence for nonlinear relationships between invader abundance and impacts. These results suggest that management actions that reduce invader abundance should reduce invader impacts monotonically in this system. Eleven of 25 invaders had significant per unit impacts (negative local-scale relationships between invader and native cover). In decomposing the components of impact, we found that local invader abundance had a significant influence on the likelihood of impact, but range (number of plots occupied) did not. This analysis helped to differentiate measures of invasiveness (local abundance and range) from impact to distinguish high-impact invaders from invaders that exhibit negligible impacts, even when widespread. Distinguishing between high- and low-impact invaders should help refine trait-based prediction of problem species. Despite the unique information derived from evaluation of per unit effects of invaders, invasiveness 'scores based on range and local abundance produced similar rankings to impact scores that incorporated estimates of per unit effects. Hence, information on range and local abundance alone was sufficient to identify problematic plant invaders at the regional scale. In comparing empirical data on invader impacts to the state noxious weed list, we found that the noxious weed list captured 45% of the high impact invaders but missed 55% and assigned the lowest risk category to the highest-impact invader. While such subjective weed lists help to guide invasive species management, empirical data are needed to develop more comprehensive rankings of ecological impacts. Using weed lists to classify invaders for testing invasion theory is not well supported.

Invasive plant erodes local song diversity in a migratory passerine.

Exotic plant invasions threaten ecosystems globally, but we still know little about the specific consequences for animals. Invasive plants can alter the quality of breeding habitat for songbirds, thereby impacting important demographic traits such as dispersal, philopatry, and age structure. These demographic effects may in turn alter song-learning conditions to affect song structure and diversity. We studied Chipping Sparrows (Spizella passerina) breeding in six savannas that were either dominated by native vegetation or invaded by spotted knapweed (Centaurea stoebe), an exotic forb known to diminish food resources and reproductive success. Here, we report that the prevalence of older birds was relatively low in knapweed-invaded habitat, where recruitment of yearlings compensated for diminished site fidelity to sustain territory abundance. In both habitat types, yearling males tended to adopt songs similar to their neighbors and match the songs of older birds rather than introducing new song types, a pattern seen in many songbird species. As a consequence, in invaded habitat where age structure was skewed away from older birds serving as potential song models, yearlings converged on fewer song types. Similarity of songs among individuals was significantly higher and the overall number of song types averaged nearly 20% lower in invaded relative to native habitat. Degradation of habitat quality generally impacts site fidelity and age ratios in migratory songbirds and hence may commonly alter song-learning conditions. Associated shifts in song attributes known to influence reproductive success could in turn enforce demographic declines driven by habitat degradation. Local song structure may serve as an important indicator of habitat quality and population status for songbirds.

Seed Size, Seed Dispersal Traits, and Plant Dispersion Patterns for Native and Introduced Grassland Plants.

Most terrestrial plants disperse by seeds, yet the relationship between seed mass, seed dispersal traits, and plant dispersion is poorly understood. We quantified seed traits for 48 species of native and introduced plants from the grasslands of western Montana, USA, to investigate the relationships between seed traits and plant dispersion patterns. Additionally, because the linkage between dispersal traits and dispersion patterns might be stronger for actively dispersing species, we compared these patterns between native and introduced plants. Finally, we evaluated the efficacy of trait databases versus locally collected data for examining these questions. We found that seed mass correlated positively with the presence of dispersal adaptations such as pappi and awns, but only for introduced plants, for which larger-seeded species were four times as likely to exhibit dispersal adaptations as smaller-seeded species. This finding suggests that introduced plants with larger seeds may require dispersal adaptations to overcome seed mass limitations and invasion barriers. Notably, larger-seeded exotics also tended to be more widely distributed than their smaller-seeded counterparts, again a pattern that was not apparent for native taxa. These results suggest that the effects of seed traits on plant distribution patterns for expanding populations may be obscured for long-established species by other ecological filters (e.g., competition). Finally, seed masses from databases differed from locally collected data for 77% of the study species. Yet, database seed masses correlated with local estimates and generated similar results. Nonetheless, average seed masses differed up to 500-fold between data sources, suggesting that local data provides more valid results for community-level questions.

Population-level compensation impedes biological control of an invasive forb and indirect release of a native grass.

The intentional introduction of specialist insect herbivores for biological control of exotic weeds provides ideal but understudied systems for evaluating important ecological concepts related to top-down control, plant compensatory responses, indirect effects, and the influence of environmental context on these processes. Centaurea stoebe (spotted knapweed) is a notorious rangeland weed that exhibited regional declines in the early 2000s, attributed to drought by some and to successful biocontrol by others. We initiated an experiment to quantify the effects of the biocontrol agent, Cyphocleonus achates, on Ce. stoebe and its interaction with a dominant native grass competitor, Pseudoroegneria spicata, under contrasting precipitation conditions. Plots containing monocultures of each plant species or equal mixtures of the two received factorial combinations of Cy. achates herbivory (exclusion or addition) and precipitation (May-June drought or "normal," defined by the 50-year average) for three years. Cy. achates herbivory reduced survival of adult Ce. stoebe plants by 9% overall, but this effect was stronger under normal precipitation compared to drought conditions, and stronger in mixed-species plots compared to monocultures. Herbivory had no effect on Ce. stoebe per capita seed production or on recruitment of seedlings or juveniles. In normal-precipitation plots of mixed composition, greater adult mortality due to Cy. achates herbivory resulted in increased recruitment of new adult Ce. stoebe. Due to this compensatory response to adult mortality, final Ce. stoebe densities did not differ between herbivory treatments regardless of context. Experimental drought reduced adult Ce. stoebe survival in mixed-species plots but did not impede recruitment of new adults or reduce final Ce. stoebe densities, perhaps due to the limited duration of the treatment. Ce. stoebe strongly depressed P. spicata reproduction and recruitment, but these impacts were not substantively alleviated by herbivory on Ce. stoebe. Population-level compensation by dominant plants may be an important factor inhibiting top-down effects in herbivore-driven and predator-driven cascades.

Soil engineering by ants facilitates plant compensation for large herbivore removal of aboveground biomass.

The interplay between top-down and bottom-up processes determines ecosystem productivity. Yet, the factors that mediate the balance between these opposing forces remain poorly understood. Furthering this challenge, complex and often cryptic factors like ecosystem engineering and trait-mediated interactions may play major roles in mediating the outcomes of top-down and bottom-up interactions. In semiarid grasslands of northeastern China, we conducted a large-scale, three-year experiment to evaluate how soil engineering by ants and plasticity in plants independently and jointly influenced the top-down effects of grazing by a ubiquitous herbivore (cattle) on aboveground standing biomass of the dominant perennial grass, Leymus chinensis. Herbivory had strong top-down effects, reducing L. chinensis AB by 25% relative to baseline levels without cattle or ants. In contrast, soil engineering by ants facilitated weak bottom-up effects in the absence of herbivory. However, in the presence of herbivory, soil engineering effects were strong enough to fully offset herbivore removal of aboveground biomass. This outcome was mediated by L. chinensis's plasticity in reallocating growth from below- to aboveground biomass, a result linked to additive effects of engineers and herbivores increasing soil N availability and engineering effects improving soil structure. Soil engineering increased soil N by 12%, promoting aboveground biomass. Herbivores increased soil N by 13% via defecation, but this increase failed to offset their reductions in aboveground biomass in isolation. However, when combined, engineers and herbivores increased soil N by 26% and engineers improved soil bulk density, facilitating L. chinensis to shift resource allocations from below- to aboveground biomass sufficiently to fully offset herbivore suppression of aboveground biomass. Our results demonstrate that soil engineering and trait-mediated effects of plant plasticity can strongly mediate the outcome of top-down and bottom-up interactions. These cryptic but perhaps ubiquitous processes may help to explain the long-debated phenomenon of plant compensatory responses to large grazers.

Fire and mice: seed predation moderates fire's influence on conifer recruitment.

In fire-adapted ecosystems, fire is presumed to be the dominant ecological force, and little is known about how consumer interactions influence forest regeneration. Here, we investigated seed predation by deer mice (Peromyscus maniculatus) and its effects on recruitment of ponderosa pine (Pinus ponderosa) and Douglas-fir (Pseudotsuga menziesii) seedlings in unburned and recently burned fire-adapted montane forests in west-central Montana, USA. Deer mice were almost twice as abundant in burned than unburned stands. Deer mouse removal of seeds from petri dishes was two times higher in burned than in unburned stands, and seed removal levels were 8% higher for ponderosa pine than for the smaller Douglas-fir seeds. In seed-addition experiments, emergence of seedlings in deer mouse-exclusion cages was almost six times higher in burned compared to unburned forest. In both burned and unburned forest, emergence was lower for ponderosa pine than for Douglas-fir. Seedling survival to establishment did not differ between conifer species but was considerably higher in burned than in unburned forest. However, effects of seed predation on recruitment prevailed over fire effects: in cages allowing access by deer mice, emergence and establishment were extremely rare for both conifer species in both burned and unburned forest. This research suggests that consumer interactions can substantially influence recruitment even in fire-adapted forest ecosystems.

Secondary invasion re-redefined: The distinction between invader-facilitated and invader-contingent invasions as subclasses of secondary invasion.

Linked Article: https://doi.org/10.1002/ece3.3964.

Community Assembly Theory as a Framework for Biological Invasions.

Biological invasions present a global problem underlain by an ecological paradox that thwarts explanation: how do some exotic species, evolutionarily naïve to their new environments, outperform locally adapted natives? We propose that community assembly theory provides a framework for addressing this question. Local community assembly rules can be defined by evaluating how native species' traits interact with community filters to affect species abundance. Evaluation of exotic species against this benchmark indicates that exotics that follow assembly rules behave like natives, while those exhibiting novel interactions with community filters can greatly underperform or outperform natives. Additionally, advantages gained by exotics over natives following disturbance can be explained by accounting for extrinsic assembly processes that bias exotic traits toward ruderal strategies.