Why are graminoid species more dominant? Trait-mediated plant-soil feedbacks shape community composition.

Species traits may determine plant interactions along with soil microbiome, further shaping plant-soil feedbacks (PSFs). However, how plant traits modulate PSFs and, consequently, the dominance of plant functional groups remains unclear. We used a combination of field surveys and a two-phase PSF experiment to investigate whether forbs and graminoids differed in PSFs and in their trait-PSF associations. When grown in forb-conditioned soils, forbs experienced stronger negative feedbacks, while graminoids experienced positive feedbacks. Graminoid-conditioned soil resulted in neutral PSFs for both functional types. Forbs with thin roots and small seeds showed more-negative PSFs than those with thick roots and large seeds. Conversely, graminoids with acquisitive root and leaf traits (i.e., thin roots and thin leaves) demonstrated greater positive PSFs than graminoids with thick roots and tough leaves. By distinguishing overall and soil biota-mediated PSFs, we found that the associations between plant traits and PSFs within both functional groups were mainly mediated by soil biota. A simulation model demonstrated that such differences in PSFs could lead to a dominance of graminoids over forbs in natural plant communities, which might explain why graminoids dominate in grasslands. Our study provides new insights into the differentiation and adaptation of plant life-history strategies under selection pressures imposed by soil biota.

Biodiversity increases resistance of grasslands against plant invasions under multiple environmental changes.

Biodiversity often helps communities resist invasion. However, it is unclear whether this diversity-invasion relationship holds true under environmental changes. Here, we conduct a meta-analysis of 1010 observations from 25 grassland studies in which plant species richness is manipulated together with one or more environmental change factors to test invasibility (measured by biomass or cover of invaders). We find that biodiversity increases resistance to invaders across various environmental conditions. However, the positive biodiversity effect on invasion resistance is strengthened under experimental warming, whereas it is weakened under experimentally imposed drought. When multiple factors are imposed simultaneously, the positive biodiversity effect is strengthened. Overall, we show that biodiversity helps grassland communities resist plant invasions under multiple environmental changes. Therefore, investment in the protection and restoration of native biodiversity is not only important for prevention of invasions under current conditions but also under continued global environmental change.

Genotype diversity enhances invasion resistance of native plants via soil biotic feedbacks.

Although native species diversity is frequently reported to enhance invasion resistance, within-species diversity of native plants can also moderate invasions. While the positive diversity-invasion resistance relationship is often attributed to competition, indirect effects mediated through plant-soil feedbacks can also influence the relationship. We manipulated the genotypic diversity of an endemic species, Scirpus mariqueter, and evaluated the effects of abiotic versus biotic feedbacks on the performance of a global invader, Spartina alterniflora. We found that invader performance on live soils decreased non-additively with genotypic diversity of the native plant that trained the soils, but this reversed when soils were sterilized to eliminate feedbacks through soil biota. The influence of soil biota on the feedback was primarily associated with increased levels of microbial biomass and fungal diversity in soils trained by multiple-genotype populations. Our findings highlight the importance of plant-soil feedbacks mediating the positive relationship between genotypic diversity and invasion resistance.

Plant invasion and naturalization are influenced by genome size, ecology and economic use globally.

Human factors and plant characteristics are important drivers of plant invasions, which threaten ecosystem integrity, biodiversity and human well-being. However, while previous studies often examined a limited number of factors or focused on a specific invasion stage (e.g., naturalization) for specific regions, a multi-factor and multi-stage analysis at the global scale is lacking. Here, we employ a multi-level framework to investigate the interplay between plant characteristics (genome size, Grime's adaptive CSR-strategies and native range size) and economic use and how these factors collectively affect plant naturalization and invasion success worldwide. While our findings derived from structural equation models highlight the substantial contribution of human assistance in both the naturalization and spread of invasive plants, we also uncovered the pivotal role of species' adaptive strategies among the factors studied, and the significantly varying influence of these factors across invasion stages. We further revealed that the effects of genome size on plant invasions were partially mediated by species adaptive strategies and native range size. Our study provides insights into the complex and dynamic process of plant invasions and identifies its key drivers worldwide.

Invading plants remain undetected in a lag phase while they explore suitable climates.

Successful alien species may experience a period of quiescence, known as the lag phase, before becoming invasive and widespread. The existence of lags introduces severe uncertainty in risk analyses of aliens as the present state of species is a poor predictor of future distributions, invasion success and impact. Predicting a species' ability to invade and pose negative impacts requires a quantitative understanding of the commonality and magnitude of lags, environmental factors and mechanisms likely to terminate lag. Using herbarium and climate data, we analysed over 5,700 time series (species × regions) in 3,505 naturalized plant species from nine regions in temperate and tropical climates to quantify lags and test whether there have been shifts in the species' climatic space during the transition from the lag phase to the expansion phase. Lags were identified in 35% of the assessed invasion events. We detected phylogenetic signals for lag phases in temperate climate regions and that annual self-fertilizing species were less likely to experience lags. Where lags existed, they had an average length of 40 years and a maximum of 320 years. Lengthy lags (>100 years) were more likely to occur in perennial plants and less frequent in self-pollinating species. For 98% of the species with a lag phase, the climate spaces sampled during the lag period differed from those in the expansion phase based on the assessment of centroid shifts or degree of climate space overlap. Our results highlight the importance of functional traits for the onset of the expansion phase and suggest that climate discovery may play a role in terminating the lag phase. However, other possibilities, such as sampling issues and climate niche shifts, cannot be ruled out.

Cultivated alien plants with high invasion potential are more likely to be traded online in China.

Biological invasions have become a worldwide problem, and measures to efficiently prevent and control invasions are still in development. Like many other parts of the world, China is undergoing a dramatic increase in plant invasions. Most of the currently 933 established (i.e., naturalized) plant species, of which 214 are categorized as invasive, have been introduced into China for cultivation. It is likely that many of those species are still being traded, particularly online, by plant nurseries. However, studies assessing whether naturalized and invasive species are currently being traded more or less than nonnaturalized aliens are rare. We extracted online-trade information for 13,718 cultivated alien plant taxa on 1688.com, the largest website for domestic B2B in China. We analyzed how the presence in online-nursery catalogs, the number of online nurseries that offerred the species for sale, and the product type (i.e., seeds, live plants and vegetative organs) differed among nonnaturalized, naturalized noninvasive, and invasive species. Compared to nonnaturalized taxa, naturalized noninvasive and invasive taxa were 3.7-5.2 times more likely to be available for purchase. Naturalized noninvasive and invasive taxa were more frequently offered as seeds by online nurseries, whereas nonnaturalized taxa were more frequently offered as live plants. Based on these findings, we propose that, to reduce the further spread of invasive and potentially invasive plants, implementation of plant-trade regulations and a monitoring system of the online horticultural supply chain will be essential.

Plants forage for soil patches free of plastic pollution but cannot bag the profits.

Microplastics can affect their surroundings physically and chemically, resulting in diverse effects on plant-soil systems. Similar to other substances (e.g. nutrients and water), microplastics in the environment occur in patches. Such heterogeneous distributions could affect plant responses to plastic pollution. Yet, this has remained untested. We conducted a multispecies experiment including 29 herbaceous plant species and three different microplastic treatments (a control without microplastics, a homogeneous and a heterogeneous microplastic distribution). Based on biomass and root-morphological traits, we assessed how different plastic distributions affect the performance and root-foraging behavior of plants, and whether stronger root foraging is beneficial when microplastics are distributed patchily. Next to general effects on plant productivity and root morphology, we found very strong evidence for root-foraging responses to patchy plastic distributions, with a clear preference for plastic-free patches, resulting in 25% longer roots and 20% more root biomass in the plastic-free patches. Interestingly, however, these foraging responses were correlated with a reduced plant performance, indicating that the benefits of plastic avoidance did not compensate for the associated investments. Our results provide new insights in plant-microplastic interactions and suggest that plants might not just be passively affected by but could also actively respond to environmental plastic pollution.

A latitudinal gradient in Darwin's naturalization conundrum at the global scale for flowering plants.

Darwin's naturalization conundrum describes two seemingly contradictory hypotheses regarding whether alien species closely or distantly related to native species should be more likely to naturalize in regional floras. Both expectations have accumulated empirical support, and whether such apparent inconsistency can be reconciled at the global scale is unclear. Here, using 219,520 native and 9,531 naturalized alien plant species across 487 globally distributed regions, we found a latitudinal gradient in Darwin's naturalization conundrum. Naturalized alien plant species are more closely related to native species at higher latitudes than they are at lower latitudes, indicating a greater influence of preadaptation in harsher climates. Human landscape modification resulted in even steeper latitudinal clines by selecting aliens distantly related to natives in warmer and drier regions. Our results demonstrate that joint consideration of climatic and anthropogenic conditions is critical to reconciling Darwin's naturalization conundrum.

The poleward naturalization of intracontinental alien plants.

Plant introductions outside their native ranges by humans have led to substantial ecological consequences. While we have gained considerable knowledge about intercontinental introductions, the distribution and determinants of intracontinental aliens remain poorly understood. Here, we studied naturalized (i.e., self-sustaining) intracontinental aliens using native and alien floras of 243 mainland regions in North America, South America, Europe, and Australia. We revealed that 4510 plant species had intracontinental origins, accounting for 3.9% of all plant species and 56.7% of all naturalized species in these continents. In North America and Europe, the numbers of intracontinental aliens peaked at mid-latitudes, while the proportion peaked at high latitudes in Europe. Notably, we found predominant poleward naturalization, primarily due to larger native species pools in low-latitudes. Geographic and climatic distances constrained the naturalization of intracontinental aliens in Australia, Europe, and North America, but not in South America. These findings suggest that poleward naturalizations will accelerate, as high latitudes become suitable for more plant species due to climate change.

Evolutionary imbalance, climate and human history jointly shape the global biogeography of alien plants.

Human activities are causing global biotic redistribution, translocating species and providing them with opportunities to establish populations beyond their native ranges. Species originating from certain global regions, however, are disproportionately represented among naturalized aliens. The evolutionary imbalance hypothesis posits that differences in absolute fitness among biogeographic divisions determine outcomes when biotas mix. Here, we compile data from native and alien distributions for nearly the entire global seed plant flora and find that biogeographic conditions predicted to drive evolutionary imbalance act alongside climate and anthropogenic factors to shape flows of successful aliens among regional biotas. Successful aliens tend to originate from large, biodiverse regions that support abundant populations and where species evolve against a diverse backdrop of competitors and enemies. We also reveal that these same native distribution characteristics are shared among the plants that humans select for cultivation and economic use. In addition to influencing species' innate potentials as invaders, we therefore suggest that evolutionary imbalance shapes plants' relationships with humans, impacting which species are translocated beyond their native distributions.

Soil microbes mediate the effects of resource variability on plant invasion.

A fundamental question in ecology is which species will prevail over others amid changes in both environmental mean conditions and their variability. Although the widely accepted fluctuating resource hypothesis predicts that increases in mean resource availability and variability therein will promote nonnative plant invasion, it remains unclear to what extent these effects might be mediated by soil microbes. We grew eight invasive nonnative plant species as target plants in pot-mesocosms planted with five different synthetic native communities as competitors, and assigned them to eight combinations of two nutrient-fluctuation (constant vs. pulsed), two nutrient-availability (low vs. high) and two soil-microbe (living vs. sterilized) treatments. We found that when plants grew in sterilized soil, nutrient fluctuation promoted the dominance of nonnative plants under overall low nutrient availability, whereas the nutrient fluctuation had minimal effect under high nutrient availability. In contrast, when plants grew in living soil, nutrient fluctuation promoted the dominance of nonnative plants under high nutrient availability rather than under low nutrient availability. Analysis of the soil microbial community suggests that this might reflect that nutrient fluctuation strongly increased the relative abundance of the most dominant pathogenic fungal family or genus under high nutrient availability, while decreasing it under low nutrient availability. Our findings are the first to indicate that besides its direct effect, environmental variability could also indirectly affect plant invasion via changes in soil microbial communities.

Negative effects of EPDM microplastic and cork granules on plant growth are mitigated by earthworms and likely caused by their structural properties.

Soil microplastic pollution can have negative effects on organisms, including plants, but the underlying mechanisms are not fully understood. We tested whether structural or chemical properties of a microplastic cause its effects on plant above- and belowground growth and whether these effects can be influenced by earthworms. We conducted a factorial experiment in a greenhouse with seven common Central European grassland species. Microplastic granules of the synthetic rubber ethylene propylene diene monomer (EPDM),1 a frequently used infill material of artificial turfs, and cork granules with a comparable size and shape to the EPDM granules were used to test for structural effects of granules in general. To test for chemical effects, EPDM-infused fertilizer was used, which should have contained any leached water-soluble chemical components of EPDM. Two Lumbricus terrestris individuals were added to half of the pots, to test whether these earthworms modify effects of EPDM on plant growth. EPDM granules had a clear negative effect on plant growth, but since cork granules had a negative effect of similar magnitude, with an average decrease in biomass of 37 % in presence of granules, this is likely due to the structural properties of granules (i.e., size and shape). For some belowground plant traits, EPDM had a stronger effect than cork, which shows that there must be other factors playing into the effects of EPDM on plant growth. The EPDM-infused fertilizer did not have any significant effect on plant growth by itself, but it had in interaction with other treatments. Earthworms had an overall positive effect on plant growth and mitigated most of the negative effects of EPDM. Our study shows that EPDM microplastic can have negative effects on plant growth, and that these might be more related to its structural than to its chemical properties.

Small genome size and variation in ploidy levels support the naturalization of vascular plants but constrain their invasive spread.

Karyological characteristics are among the traits underpinning the invasion success of vascular plants. Using 11 049 species, we tested the effects of genome size and ploidy levels on plant naturalization (species forming self-sustaining populations where they are not native) and invasion (naturalized species spreading rapidly and having environmental impact). The probability that a species naturalized anywhere in the world decreased with increasing monoploid genome size (DNA content of a single chromosome set). Naturalized or invasive species with intermediate monoploid genomes were reported from many regions, but those with either small or large genomes occurred in fewer regions. By contrast, large holoploid genome sizes (DNA content of the unreplicated gametic nucleus) constrained naturalization but favoured invasion. We suggest that a small genome is an advantage during naturalization, being linked to traits favouring adaptation to local conditions, but for invasive spread, traits associated with a large holoploid genome, where the impact of polyploidy may act, facilitate long-distance dispersal and competition with other species.

Climatic stability and geological history shape global centers of neo- and paleoendemism in seed plants.

Assessing the distribution of geographically restricted and evolutionarily unique species and their underlying drivers is key to understanding biogeographical processes and critical for global conservation prioritization. Here, we quantified the geographic distribution and drivers of phylogenetic endemism for ~320,000 seed plants worldwide and identified centers and drivers of evolutionarily young (neoendemism) and evolutionarily old endemism (paleoendemism). Tropical and subtropical islands as well as tropical mountain regions displayed the world's highest phylogenetic endemism. Most tropical rainforest regions emerged as centers of paleoendemism, while most Mediterranean-climate regions showed high neoendemism. Centers where high neo- and paleoendemism coincide emerged on some oceanic and continental fragment islands, in Mediterranean-climate regions and parts of the Irano-Turanian floristic region. Global variation in phylogenetic endemism was well explained by a combination of past and present environmental factors (79.8 to 87.7% of variance explained) and most strongly related to environmental heterogeneity. Also, warm and wet climates, geographic isolation, and long-term climatic stability emerged as key drivers of phylogenetic endemism. Neo- and paleoendemism were jointly explained by climatic and geological history. Long-term climatic stability promoted the persistence of paleoendemics, while the isolation of oceanic islands and their unique geological histories promoted neoendemism. Mountainous regions promoted both neo- and paleoendemism, reflecting both diversification and persistence over time. Our study provides insights into the evolutionary underpinnings of biogeographical patterns in seed plants and identifies the areas on Earth with the highest evolutionary and biogeographical uniqueness-key information for setting global conservation priorities.

Breakdown of self-incompatibility due to genetic interaction between a specific S-allele and an unlinked modifier.

Breakdown of self-incompatibility has frequently been attributed to loss-of-function mutations of alleles at the locus responsible for recognition of self-pollen (i.e. the S-locus). However, other potential causes have rarely been tested. Here, we show that self-compatibility of S1S1-homozygotes in selfing populations of the otherwise self-incompatible Arabidopsis lyrata is not due to S-locus mutation. Between-breeding-system cross-progeny are self-compatible if they combine S1 from the self-compatible cross-partner with recessive S1 from the self-incompatible cross-partner, but self-incompatible with dominant S-alleles. Because S1S1 homozygotes in outcrossing populations are self-incompatible, mutation of S1 cannot explain self-compatibility in S1S1 cross-progeny. This supports the hypothesis that an S1-specific modifier unlinked to the S-locus causes self-compatibility by functionally disrupting S1. Self-compatibility in S19S19 homozygotes may also be caused by an S19-specific modifier, but we cannot rule out a loss-of-function mutation of S19. Taken together, our findings indicate that breakdown of self-incompatibility is possible without disruptive mutations at the S-locus.

Plant-soil feedback effects on conspecific and heterospecific successors of annual and perennial Central European grassland plants are correlated.

Plant-soil feedbacks (PSFs), soil-mediated plant effects on conspecific or heterospecific successors, are a major driver of vegetation development. It has been proposed that specialist plant antagonists drive differences in PSF responses between conspecific and heterospecific plants, whereas contributions of generalist plant antagonists to PSFs remain understudied. Here we examined PSFs among nine annual and nine perennial grassland species to test whether poorly defended annuals accumulate generalist-dominated plant antagonist communities, causing equally negative PSFs on conspecific and heterospecific annuals, whereas well-defended perennial species accumulate specialist-dominated antagonist communities, predominantly causing negative conspecific PSFs. Annuals exhibited more negative PSFs than perennials, corresponding to differences in root-tissue investments, but this was independent of conditioning plant group. Overall, conspecific and heterospecific PSFs did not differ. Instead, conspecific and heterospecific PSF responses in individual species' soils were correlated. Soil fungal communities were generalist dominated but could not robustly explain PSF variation. Our study nevertheless suggests an important role for host generalists as drivers of PSFs.

The impact of land use on non-native species incidence and number in local assemblages worldwide.

While the regional distribution of non-native species is increasingly well documented for some taxa, global analyses of non-native species in local assemblages are still missing. Here, we use a worldwide collection of assemblages from five taxa - ants, birds, mammals, spiders and vascular plants - to assess whether the incidence, frequency and proportions of naturalised non-native species depend on type and intensity of land use. In plants, assemblages of primary vegetation are least invaded. In the other taxa, primary vegetation is among the least invaded land-use types, but one or several other types have equally low levels of occurrence, frequency and proportions of non-native species. High land use intensity is associated with higher non-native incidence and frequency in primary vegetation, while intensity effects are inconsistent for other land-use types. These findings highlight the potential dual role of unused primary vegetation in preserving native biodiversity and in conferring resistance against biological invasions.

Global models and predictions of plant diversity based on advanced machine learning techniques.

Despite the paramount role of plant diversity for ecosystem functioning, biogeochemical cycles, and human welfare, knowledge of its global distribution is still incomplete, hampering basic research and biodiversity conservation. Here, we used machine learning (random forests, extreme gradient boosting, and neural networks) and conventional statistical methods (generalized linear models and generalized additive models) to test environment-related hypotheses of broad-scale vascular plant diversity gradients and to model and predict species richness and phylogenetic richness worldwide. To this end, we used 830 regional plant inventories including c. 300 000 species and predictors of past and present environmental conditions. Machine learning showed a superior performance, explaining up to 80.9% of species richness and 83.3% of phylogenetic richness, illustrating the great potential of such techniques for disentangling complex and interacting associations between the environment and plant diversity. Current climate and environmental heterogeneity emerged as the primary drivers, while past environmental conditions left only small but detectable imprints on plant diversity. Finally, we combined predictions from multiple modeling techniques (ensemble predictions) to reveal global patterns and centers of plant diversity at multiple resolutions down to 7774 km2 . Our predictive maps provide accurate estimates of global plant diversity available at grain sizes relevant for conservation and macroecology.

Precipitation predictability affects intra- and trans-generational plasticity and causes differential selection on root traits of Papaver rhoeas.

Climate forecasts show that in many regions the temporal distribution of precipitation events will become less predictable. Root traits may play key roles in dealing with changes in precipitation predictability, but their functional plastic responses, including transgenerational processes, are scarcely known. We investigated root trait plasticity of Papaver rhoeas with respect to higher versus lower intra-seasonal and inter-seasonal precipitation predictability (i.e., the degree of temporal autocorrelation among precipitation events) during a four-year outdoor multi-generation experiment. We first tested how the simulated predictability regimes affected intra-generational plasticity of root traits and allocation strategies of the ancestors, and investigated the selective forces acting on them. Second, we exposed three descendant generations to the same predictability regime experienced by their mothers or to a different one. We then investigated whether high inter-generational predictability causes root trait differentiation, whether transgenerational root plasticity existed and whether it was affected by the different predictability treatments. We found that the number of secondary roots, root biomass and root allocation strategies of ancestors were affected by changes in precipitation predictability, in line with intra-generational plasticity. Lower predictability induced a root response, possibly reflecting a fast-acquisitive strategy that increases water absorbance from shallow soil layers. Ancestors' root traits were generally under selection, and the predictability treatments did neither affect the strength nor the direction of selection. Transgenerational effects were detected in root biomass and root weight ratio (RWR). In presence of lower predictability, descendants significantly reduced RWR compared to ancestors, leading to an increase in performance. This points to a change in root allocation in order to maintain or increase the descendants' fitness. Moreover, transgenerational plasticity existed in maximum rooting depth and root biomass, and the less predictable treatment promoted the lowest coefficient of variation among descendants' treatments in five out of six root traits. This shows that the level of maternal predictability determines the variation in the descendants' responses, and suggests that lower phenotypic plasticity evolves in less predictable environments. Overall, our findings show that roots are functional plastic traits that rapidly respond to differences in precipitation predictability, and that the plasticity and adaptation of root traits may crucially determine how climate change will affect plants.

Number of simultaneously acting global change factors affects composition, diversity and productivity of grassland plant communities.

Plant communities experience impacts of increasing numbers of global change factors (e.g., warming, eutrophication, pollution). Consequently, unpredictable global change effects could arise. However, information about multi-factor effects on plant communities is scarce. To test plant-community responses to multiple global change factors (GCFs), we subjected sown and transplanted-seedling communities to increasing numbers (0, 1, 2, 4, 6) of co-acting GCFs, and assessed effects of individual factors and increasing numbers of GCFs on community composition and productivity. GCF number reduced species diversity and evenness of both community types, whereas none of the individual factors alone affected these measures. In contrast, GCF number positively affected the productivity of the transplanted-seedling community. Our findings show that simultaneously acting GCFs can affect plant communities in ways differing from those expected from single factor effects, which may be due to biological effects, sampling effects, or both. Consequently, exploring the multifactorial nature of global change is crucial to better understand ecological impacts of global change.