The EICA is dead? Long live the EICA!

An important hypothesis for how plants respond to introduction to new ranges is the evolution of increased competitive ability (EICA). EICA predicts that biogeographical release from natural enemies initiates a trade-off in which exotic species in non-native ranges become larger and more competitive, but invest less in consumer defences, relative to populations in native ranges. This trade-off is exceptionally complex because detecting concomitant biogeographical shifts in competitive ability and consumer defence depends upon which traits are targeted, how competition is measured, the defence chemicals quantified, whether defence chemicals do more than defend, whether 'herbivory' is artificial or natural, and where consumers fall on the generalist-specialist spectrum. Previous meta-analyses have successfully identified patterns but have yet to fully disentangle this complexity. We used meta-analysis to reevaluate traditional metrics used to test EICA theory and then expanded on these metrics by partitioning competitive effect and competitive tolerance measures and testing Leaf-Specific Mass in detail as a response trait. Unlike previous syntheses, our meta-analyses detected evidence consistent with the classic trade-off inherent to EICA. Plants from non-native ranges imposed greater competitive effects than plants from native ranges and were less quantitatively defended than plants from native ranges. Our results for defence were not based on complex leaf chemistry, but instead were estimated from tannins, toughness traits and primarily Leaf-Specific Mass. Species specificity occurred but did not influence the general patterns. As for all evidence for EICA-like trade-offs, we do not know if the biogeographical differences we found were caused by trade-offs per se, but they are consistent with predictions derived from the overarching hypothesis. Underestimating physical leaf structure may have contributed to two decades of tepid perspectives on the trade-offs fundamental to EICA.

Trait variation, trade-offs, and attributes may contribute to colonization and range expansion of a globally distributed weed.

PREMISE: Trait variation, trade-offs, and attributes can facilitate colonization and range expansion. We explored how those trait features compare between ancestral and nonnative populations of the globally distributed weed Centaurea solstitialis. METHODS: We measured traits related to survival, size, reproduction, and dispersal in field sampling following major environmental gradients; that of elevation in Anatolia (ancestral range) and that of precipitation in Argentina (nonnative range). We also estimated abundance. RESULTS: We found that overall variation in traits in ancestral populations was similar to that in nonnative populations. Only one trait-seed mass-displayed greater variation in ancestral than nonnative populations; coincidentally, seed mass has been shown to track global range expansion of C. solstitialis. Traits displayed several associations, among which seed mass and number were positively related in both ranges. Many traits varied with elevation in the ancestral range, whereas none varied with precipitation in the nonnative one. Interestingly, most traits varying with elevation within the ancestral range also displayed differences in attributes between ancestral and nonnative ranges. Unexpectedly, ancestral plants were more fecund than nonnative plants, but density was greater in the nonnative than ancestral range, indicating that C. solstitialis survives at larger proportions in the nonnative than ancestral range. CONCLUSIONS: Our results suggest that maintaining levels of trait variation in nonnative populations comparable to those in ancestral populations, avoiding trait trade-offs, and developing differences in trait attributes between ranges can play a major role in the success of many weeds in novel environments.

Plant interactions balance under biotic and abiotic stressors: the importance of herbivory in semi-arid ecosystems.

Biotic and abiotic stressors commonly co-occur in plant communities and influence interactions between plants. However, their combined effects on plant interactions have not been widely studied and are still unclear. Here, we assessed the balance of interactions between neighboring plants along a grazing gradient and under two water regimes. We conducted a three-year-field experiment in semi-arid central Argentina with transplants of the dominant palatable grass Piptochaetium napostaense growing in Baccharis ulicina and open microsites across a gradient of grazing pressure. Additionally, we established a water addition treatment along that gradient. We recorded herbivory, size, and fecundity of P. napostaense. During the first two years, P. napostaense was consumed less and was larger below Baccharis than in the open. These differences were greatest under high grazing pressure. Differences in fecundity between microsites were only detected under high and medium grazing pressure in the first two years. In the third year, Baccharis lost their leaves for unclear reasons and provided poor herbivory protection; hence, P. napostaense plants in Baccharis were larger than those in the open only under medium and low grazing pressure, and there were no differences in fecundity between microsites under any grazing condition. Water additions exerted no effect on plant interactions. The balance of interactions changed from positive under heavy grazing to neutral at low and no grazing and water availability did not alter that balance. We conclude that herbivore pressure is an important driver of the balance of plant interactions in semi-arid environments.

The Neolithic Plant Invasion Hypothesis: the role of preadaptation and disturbance in grassland invasion.

A long-standing hypothesis is that many European plants invade temperate grasslands globally because they are introduced simultaneously with pastoralism and cultivation, to which they are 'preadapted' after millennia of exposure dating to the Neolithic era ('Neolithic Plant Invasion Hypothesis' (NPIH)). These 'preadaptations' are predicted to maximize their performance relative to native species lacking this adaptive history. Here, we discuss the explanatory relevance of the NPIH, clarifying the importance of evolutionary context vs other mechanisms driving invasion. The NPIH makes intuitive sense given established connections between invasion and agricultural-based perturbation. However, tests are often incomplete given the need for performance contrasts between home and away ranges, while controlling for other mechanisms. We emphasize six NPIH-based predictions, centring on trait similarity of invaders between home vs away populations, and differing perturbation responses by invading and native plants. Although no research has integrated all six predictions, we highlight studies suggesting preadaptation influences on invasion. Given that many European grasslands are creations of human activity from the past, current invasions by these flora may represent the continuation of processes dating to the Neolithic. Ironically, European Neolithic-derived grasslands are becoming rarer, reflecting changes in management and illustrating the importance of human influences on these species.

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.

Competition does not come at the expense of colonization in seed morphs with increased size and dispersal.

PREMISE OF THE STUDY: Seed-level trade-offs of heterocarpic species remain poorly understood. We propose that seedlings emerging from seeds with a permanent pappus (dispersing seeds) are stronger competitors than those emerging from seeds without a pappus (nondispersing seeds) because dispersing seeds are larger and germinate faster than nondispersing seeds in Centaurea solstitialis. METHODS: We conducted a competition experiment with both seed morphs, in which we recorded emergence rate and proportion, estimated seed dispersal by wind (anemochory) and by mammals (exozoochory), and measured size and abundance of seed morphs. KEY RESULTS: We found that seedlings from pappus seeds had greater competitive abilities than those from non-pappus seeds. Similarly, pappus seedlings emerged at much faster rates and larger proportions than non-pappus seedlings. Pappus seeds were larger, were more numerous, and displayed improved exozoochory compared to non-pappus seeds. Anemochory was poor for both seed morphs. CONCLUSIONS: We found support for our hypothesis, raising in turn the possibility that competition and colonization are positively associated in seed morphs of heterocarpic species with enhanced exozoochory of larger seeds. These findings are not consistent with those from heterocarpic species with enhanced anemochory of smaller seeds or slower-germinating seeds. Our results additionally suggest that pappus and non-pappus seeds of C. solstitialis display a task-division strategy in which pappus morphs colonize and preempt unoccupied sites through improved dispersal and fast and large emergence of seedlings with increased competitive abilities, whereas non-pappus morphs promote site persistence through delayed germination and dormancy. This strategy may contribute to the success of C. solstitialis in highly variable environments.

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.

Native and non-native ruderals experience similar plant-soil feedbacks and neighbor effects in a system where they coexist.

Recent applications of coexistence theory to plant invasions posit that non-natives establish in resident communities through either niche differences or traits conferring them with fitness advantages, the former being associated with coexistence and the latter with dominance and competitive exclusion. Plant-soil feedback is a mechanism that is known to explain both coexistence and dominance. In a system where natives and non-natives appear to coexist, we explored how plant-soil feedbacks affect the performance of nine native and nine non-native ruderal species-the prevalent life-history strategy among non-natives-when grown alone and with a phytometer. We also conducted field samplings to estimate the abundance of the 18 species, and related feedbacks to abundances. We found that groups of native and non-native ruderals displayed similar frequencies of negative, positive, and neutral feedbacks, resulting in no detectable differences between natives and non-natives. Likewise, the phytometer exerted comparable negative impacts on native and non-native plants, which were unchanged by plant-soil feedbacks. Finally, feedbacks explained plant abundances only after removing one influential species which exhibited strong positive feedbacks but low abundance. Importantly, however, four out of five species with negative feedbacks were rare in the field. These findings suggest that soil feedbacks and plant-plant interactions do not confer an advantage to non-native over native species, but do contribute to the observed coexistence of these groups in the system. By comparing natives and non-natives with overlapping abundances and strategies, our work broadens understanding of the consequences of plant-soil feedbacks in plant invasion and, more generally, coexistence within plant communities.

Trait evolution during a rapid global weed invasion despite little genetic differentiation.

Invasive species often possess a great capacity to adapt to novel environments in the form of spatial trait variation, as a result of varying selection regimes, genetic drift, or plasticity. We explored the geographic differentiation in several phenotypic traits related to plant growth, reproduction, and defense in the highly invasive Centaurea solstitialis by measuring neutral genetic differentiation (F ST), and comparing it with phenotypic differentiation (P ST), in a common garden experiment in individuals originating from regions representing the species distribution across five continents. Native plants were more fecund than non-native plants, but the latter displayed considerably larger seed mass. We found indication of divergent selection for these two reproductive traits but little overall genetic differentiation between native and non-native ranges. The native versus invasive P ST-F ST comparisons demonstrated that, in several invasive regions, seed mass had increased proportionally more than the genetic differentiation. Traits displayed different associations with climate variables in different regions. Both capitula numbers and seed mass were associated with winter temperature and precipitation and summer aridity in some regions. Overall, our study suggests that rapid evolution has accompanied invasive success of C. solstitialis and provides new insights into traits and their genetic bases that can contribute to fitness advantages in non-native populations.

Native herbivore exerts contrasting effects on fire regime and vegetation structure.

Although native herbivores can alter fire regimes by consuming herbaceous vegetation that serves as fine fuel and, less commonly, accumulating fuel as nest material and other structures, simultaneous considerations of contrasting effects of herbivores on fire have scarcely been addressed. We proposed that a colonial rodent, vizcacha (Lagostomus maximus), reduces and increases fire intensity at different stages in its population cycle in the semiarid scrub of Argentina. Specifically, we hypothesized that, when colonies are active, vizcachas create natural fire-breaks through intense grazing, generating over time patches of large unburned shrubs in grazed zones. In contrast, when colonies are abandoned, recovery of fine fuels and previous accumulation of coarse wood on colonies during territorial displays increases fire intensity, creating patches of high shrub mortality. To test these hypotheses, we estimated stem age of the dominant shrub (Larrea divaricata) and measured aboveground biomass in zones actively grazed by vizcachas and in ungrazed zones, and compared densities of live and dead shrubs on abandoned colonies and adjacent zones following fire. In active colonies, age and biomass of shrubs were much greater in grazed than ungrazed zones. In abandoned colonies that had been burnt, density of dead, burned shrubs was higher and density of live shrubs was lower than in adjacent zones. These results support our hypotheses and reveal a new interaction between native herbivores and fire, in which herbivores augment fire intensity by gathering fuel. Our findings indicate that, through opposing effects on fire, native herbivores enhance the heterogeneity of vegetation in woody-dominated ecosystems.

Globally, plant-soil feedbacks are weak predictors of plant abundance.

Plant-soil feedbacks (PSFs) have been shown to strongly affect plant performance under controlled conditions, and PSFs are thought to have far reaching consequences for plant population dynamics and the structuring of plant communities. However, thus far the relationship between PSF and plant species abundance in the field is not consistent. Here, we synthesize PSF experiments from tropical forests to semiarid grasslands, and test for a positive relationship between plant abundance in the field and PSFs estimated from controlled bioassays. We meta-analyzed results from 22 PSF experiments and found an overall positive correlation (0.12 ≤  r ¯  ≤ 0.32) between plant abundance in the field and PSFs across plant functional types (herbaceous and woody plants) but also variation by plant functional type. Thus, our analysis provides quantitative support that plant abundance has a general albeit weak positive relationship with PSFs across ecosystems. Overall, our results suggest that harmful soil biota tend to accumulate around and disproportionately impact species that are rare. However, data for the herbaceous species, which are most common in the literature, had no significant abundance-PSFs relationship. Therefore, we conclude that further work is needed within and across biomes, succession stages and plant types, both under controlled and field conditions, while separating PSF effects from other drivers (e.g., herbivory, competition, disturbance) of plant abundance to tease apart the role of soil biota in causing patterns of plant rarity versus commonness.

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.

Extensive analysis of native and non-native Centaurea solstitialis L. populations across the world shows no traces of polyploidization.

Centaurea solstitialis L. (yellow starthistle, Asteraceae) is a Eurasian native plant introduced as an exotic into North and South America, and Australia, where it is regarded as a noxious invasive. Changes in ploidy level have been found to be responsible for numerous plant biological invasions, as they are involved in trait shifts critical to invasive success, like increased growth rate and biomass, longer life-span, or polycarpy. C. solstitialis had been reported to be diploid (2n = 2x = 16 chromosomes), however, actual data are scarce and sometimes contradictory. We determined for the first time the absolute nuclear DNA content by flow cytometry and estimated ploidy level in 52 natural populations of C. solstitialis across its native and non-native ranges, around the world. All the C. solstitialis populations screened were found to be homogeneously diploid (average 2C value of 1.72 pg, SD = ±0.06 pg), with no significant variation in DNA content between invasive and non-invasive genotypes. We did not find any meaningful difference among the extensive number of native and non-native C. solstitialis populations sampled around the globe, indicating that the species invasive success is not due to changes in genome size or ploidy level.

Are local filters blind to provenance? Ant seed predation suppresses exotic plants more than natives.

The question of whether species' origins influence invasion outcomes has been a point of substantial debate in invasion ecology. Theoretically, colonization outcomes can be predicted based on how species' traits interact with community filters, a process presumably blind to species' origins. Yet, exotic plant introductions commonly result in monospecific plant densities not commonly seen in native assemblages, suggesting that exotic species may respond to community filters differently than natives. Here, we tested whether exotic and native species differed in their responses to a local community filter by examining how ant seed predation affected recruitment of eighteen native and exotic plant species in central Argentina. Ant seed predation proved to be an important local filter that strongly suppressed plant recruitment, but ants suppressed exotic recruitment far more than natives (89% of exotic species vs. 22% of natives). Seed size predicted ant impacts on recruitment independent of origins, with ant preference for smaller seeds resulting in smaller seeded plant species being heavily suppressed. The disproportionate effects of provenance arose because exotics had generally smaller seeds than natives. Exotics also exhibited greater emergence and earlier peak emergence than natives in the absence of ants. However, when ants had access to seeds, these potential advantages of exotics were negated due to the filtering bias against exotics. The differences in traits we observed between exotics and natives suggest that higher-order introduction filters or regional processes preselected for certain exotic traits that then interacted with the local seed predation filter. Our results suggest that the interactions between local filters and species traits can predict invasion outcomes, but understanding the role of provenance will require quantifying filtering processes at multiple hierarchical scales and evaluating interactions between filters.

Dispersal pathways and genetic differentiation among worldwide populations of the invasive weed Centaurea solstitialis L. (Asteraceae).

The natural history of introduced species is often unclear due to a lack of historical records. Even when historical information is readily available, important factors of the invasions such as genetic bottlenecks, hybridization, historical relationships among populations and adaptive changes are left unknown. In this study, we developed a set of nuclear, simple sequence repeat markers and used these to characterize the genetic diversity and population structure among native (Eurasian) and non-native (North and South American) populations of Centaurea solstitialis L., (yellow starthistle). We used these data to test hypotheses about the invasion pathways of the species that were based on historical and geographical records, and we make inferences about historical relationships among populations and demographic processes following invasion. We confirm that the center of diversity and the native range of the species is likely the eastern Mediterranean region in the vicinity of Turkey. From this region, the species likely proceeded to colonize other parts of Europe and Asia via a slow, stepwise range expansion. Spanish populations were the primary source of seed to invade South America via human-mediated events, as was evident from historical records, but populations from the eastern Mediterranean region were also important. North American populations were largely derived from South America, but had secondary contributors. We suggest that the introduction history of non-native populations from disparate parts of the native range have allowed not just one, but multiple opportunities first in South America then again in North America for the creation of novel genotypes via intraspecific hybridization. We propose that multiple intraspecific hybridization events may have created especially potent conditions for the selection of a noxious invader, and may explain differences in genetic patterns among North and South America populations, inferred differences in demographic processes, as well as morphological differences previously reported from common garden experiments.

Range-expanding populations of a globally introduced weed experience negative plant-soil feedbacks.

BACKGROUND: Biological invasions are fundamentally biogeographic processes that occur over large spatial scales. Interactions with soil microbes can have strong impacts on plant invasions, but how these interactions vary among areas where introduced species are highly invasive vs. naturalized is still unknown. In this study, we examined biogeographic variation in plant-soil microbe interactions of a globally invasive weed, Centaurea solstitialis (yellow starthistle). We addressed the following questions (1) Is Centaurea released from natural enemy pressure from soil microbes in introduced regions? and (2) Is variation in plant-soil feedbacks associated with variation in Centaurea's invasive success? METHODOLOGY/PRINCIPAL FINDINGS: We conducted greenhouse experiments using soils and seeds collected from native Eurasian populations and introduced populations spanning North and South America where Centaurea is highly invasive and noninvasive. Soil microbes had pervasive negative effects in all regions, although the magnitude of their effect varied among regions. These patterns were not unequivocally congruent with the enemy release hypothesis. Surprisingly, we also found that Centaurea generated strong negative feedbacks in regions where it is the most invasive, while it generated neutral plant-soil feedbacks where it is noninvasive. CONCLUSIONS/SIGNIFICANCE: Recent studies have found reduced below-ground enemy attack and more positive plant-soil feedbacks in range-expanding plant populations, but we found increased negative effects of soil microbes in range-expanding Centaurea populations. While such negative feedbacks may limit the long-term persistence of invasive plants, such feedbacks may also contribute to the success of invasions, either by having disproportionately negative impacts on competing species, or by yielding relatively better growth in uncolonized areas that would encourage lateral spread. Enemy release from soil-borne pathogens is not sufficient to explain the success of this weed in such different regions. The biogeographic variation in soil-microbe effects indicates that different mechanisms may operate on this species in different regions, thus establishing geographic mosaics of species interactions that contribute to variation in invasion success.