Role In Biological Invasions Research Articles

Variable viral loads and immune response in an invasive ant's native and introduced ranges

AbstractAimPathogens can play an important role in biological invasions. Introduced populations may be particularly vulnerable to pathogens due to factors such as low genetic diversity and high population density. However, introduced populations that escape their natural pathogens may reallocate resources away from immunity and towards growth and reproduction. Interestingly, introduced ants have been suggested to have increased tolerance to new pathogens, contributing to their success as introduced species. In this study, we aimed to investigate whether introduced Argentine ant populations harbour different viral loads compared to native populations and if these differences were related to immunity‐related gene expression.LocationThe study was conducted across the native range of Argentine ants in Argentina and four introduced regions in California, France, Australia and New Zealand.MethodsWe used RT‐qPCR to quantify viral loads and gene expression in the ants. We analysed 15 different potentially pathogenic viruses across the Argentine ant's native and introduced ranges.ResultsWe found that five viruses, LhuPcV1, LhuPiLV1, LhuCV1, Kashmir Bee virus and LHUV‐1, presented high loads in Argentine ants compared to the other viruses we screened. We found a significant effect of range on viral infections: high viral loads were commonly found in ants from introduced populations, which also exhibited increased immune gene expression. We found highly significant correlations between viral loads and expression of immune and metabolic genes. However, these associations were not fully consistent across the studied regions, indicating the complexity of eco‐immunological phenomena.Main ConclusionsOur results suggest that introduced Argentine ant populations host different viral communities compared to native populations and that these differences are correlated with changes in immunity‐related gene expression. The study highlights the complex role of pathogens in biological invasions and the importance of considering eco‐immunological factors when assessing the impact of introduced species.

Let’s talk aliens - Stakeholder perceptions of an alien species differ in time and space

Humans play an integral role in biological invasions, from aiding introductions of alien species to experiencing their impacts and holding the ability to manage them. The importance of understanding the dynamics of stakeholders’ perceptions on alien species is therefore increasingly recognized. In this study, we used anonymous online surveys to contrast recreational anglers’ perceptions towards European flounder (Platichthys flesus, Linnaeus, 1758) in Iceland, where it is classified as a potentially invasive species, to the perceptions prevailing amongst recreational anglers in the species’ native range. We furthermore explored potential temporal changes in the perception of Icelandic recreational anglers. Our results indicate that Icelandic recreational anglers have a highly negative perception towards the European flounder, while in its native range, recreational anglers have positive perceptions towards this species. In Iceland, we have furthermore detected a significant change towards less negative perceptions between the surveys administered in October 2019 and March 2023. Finally, we compared the results of the online surveys and novel, conservation culturomics tools to further explore stakeholder perceptions and public interest in Iceland. The comparison highlighted some limitations that should be considered when using culturomics in very small societies or for small languages. For example, the text mining approaches on newspaper articles and social media conservations detected neutral perceptions in the communication to the public and within the targeted stakeholder group via social media in contrary to the perceptions detected in the online surveys. Moreover, we detected short-term peaks in the public’s interest in European flounder and potential drivers of those peaks using Wikipedia pageviews but Google Trends provided mixed and unreproducible results. Overall, our study highlights that stakeholders’ perceptions towards an alien species as well as the public’s interest in it vary over time and space, though the drivers of these changes are often difficult to identify.

Host-related traits influence the microbial diversity of the invasive signal crayfish Pacifastacus leniusculus

The microbiome influences a variety of host-environment interactions, and there is mounting evidence of its significant role in biological invasions. During invasion, shifts in microbial diversity and function can occur due to both changing characteristics of the novel environment and physiological condition of the host. The signal crayfish (Pacifastacus leniusculus) is one of the most successful crayfish invaders in Europe. During range expansion, its populations often exhibit differences in many traits along the invasion range, including sex-composition, size-structure and aggressiveness, but to date it was not studied whether crayfish traits can also drive changes in the host microbiome. Thus, we used 16S rRNA gene amplicon sequencing to examine the effects of host-related traits, namely total length (TL), body condition index (FCF), hepatosomatic index (HSI) and sex on the microbial diversity of the signal crayfish. We examined both external (exoskeletal) and internal (intestinal, hepatopancreatic, hemolymph) microbiomes of 110 signal crayfish individuals from four sites along its invasion range in the Korana River, Croatia. While sex did not exhibit a significant effect on the microbial diversity in any of the examined tissues, exoskeletal, intestinal and hemolymph microbial diversity significantly decreased with increasing crayfish size. Additionally, significant effects of signal crayfish condition (FCF, HSI) on microbial diversity were recorded in the hepatopancreas, a main energy storage organ in crayfish that supports reproduction and growth and also regulates immune response. Our findings provide a baseline for evaluating the contribution of microbiome to an invader's overall health, fitness and subsequent invasion success.

The mycobiome of a successful crayfish invader and its changes along the environmental gradient

BackgroundThe microbiome plays an important role in biological invasions, since it affects various interactions between host and environment. However, most studies focus on the bacteriome, insufficiently addressing other components of the microbiome such as the mycobiome. Microbial fungi are among the most damaging pathogens in freshwater crayfish populations, colonizing and infecting both native and invasive crayfish species. Invading crayfish may transmit novel fungal species to native populations, but also, dispersal process and characteristics of the novel environment may affect the invaders’ mycobiome composition, directly and indirectly affecting their fitness and invasion success. This study analyzes the mycobiome of a successful invader in Europe, the signal crayfish, using the ITS rRNA amplicon sequencing approach. We explored the mycobiomes of crayfish samples (exoskeletal biofilm, hemolymph, hepatopancreas, intestine), compared them to environmental samples (water, sediment), and examined the differences in fungal diversity and abundance between upstream and downstream segments of the signal crayfish invasion range in the Korana River, Croatia.ResultsA low number of ASVs (indicating low abundance and/or diversity of fungal taxa) was obtained in hemolymph and hepatopancreas samples. Thus, only exoskeleton, intestine, sediment and water samples were analyzed further. Significant differences were recorded between their mycobiomes, confirming their uniqueness. Generally, environmental mycobiomes showed higher diversity than crayfish-associated mycobiomes. The intestinal mycobiome showed significantly lower richness compared to other mycobiomes. Significant differences in the diversity of sediment and exoskeletal mycobiomes were recorded between different river segments (but not for water and intestinal mycobiomes). Together with the high observed portion of shared ASVs between sediment and exoskeleton, this indicates that the environment (i.e. sediment mycobiome) at least partly shapes the exoskeletal mycobiome of crayfish.ConclusionThis study presents the first data on crayfish-associated fungal communities across different tissues, which is valuable given the lack of studies on the crayfish mycobiome. We demonstrate significant differences in the crayfish exoskeletal mycobiome along the invasion range, suggesting that different local environmental conditions may shape the exoskeletal mycobiome during range expansion, while the mycobiome of the internal organ (intestine) remained more stable. Our results provide a basis for assessing how the mycobiome contributes to the overall health of the signal crayfish and its further invasion success.

Alien, Naturalized and Invasive Plants in China.

Invasive species are a subset of naturalized species, and naturalized species are a subset of alien species. Determining the relationship among these three assemblages would be helpful in predicting and preventing biological invasion. Here, we reviewed the families, lifeforms, origins, introduction pathways and phylogenetic diversity of alien, naturalized and invasive vascular plants in China. The results show that species in the Asteraceae, Fabaceae and Poaceae families had a high dominance among alien, naturalized and invasive species. Moreover, almost all alien species in the Amaranthaceae, Solanaceae, Convolvulaceae and Euphorbiaceae families became naturalized species, and about 26.7% of the naturalized species became invasive species. Perennial herbs comprised a higher proportion of alien species than did annual herbs, though annual herbs were more suited to becoming invasive than perennial herbs. A considerable proportion (57.8%) of invasive species were introduced from America. More than half (56.5%) of alien species were introduced for their ornamental value, and half of these have become naturalized in China. Moreover, about half (55.2%) of all invasive species were introduced for their economic value (including ornamental, foraging and medicinal purposes). Invasive species were phylogenetically clustered and phylogenetically distant from alien and naturalized species, which indicates that phylogenetic differences could be helpful in becoming invasive. There is no doubt that human activity plays a significant role in biological invasion. This study suggests that when introducing alien species to a region, decision-makers should certainly consider the species’ phylogeny, beyond just its fundamental characteristics.

Disentangling the mechanisms underpinning disturbance-mediated invasion.

Disturbances can play a major role in biological invasions: by destroying biomass, they alter habitat and resource abundances. Previous field studies suggest that disturbance-mediated invader success is a consequence of resource influxes, but the importance of other potential covarying causes, notably the opening up of habitats, have yet to be directly tested. Using experimental populations of the bacterium Pseudomonas fluorescens, we determined the relative importance of disturbance-mediated habitat opening and resource influxes, plus any interaction between them, for invader success of two ecologically distinct morphotypes. Resource addition increased invasibility, while habitat opening had little impact and did not interact with resource addition. Both invaders behaved similarly, despite occupying different ecological niches in the microcosms. Treatment also affected the composition of the resident population, which further affected invader success. Our results provide experimental support for the observation that resource input is a key mechanism through which disturbance increases invasibility.

Effects of maternal source and progeny microhabitat on natural selection and population dynamics in Alliaria petiolata

The success or failure of propagules in contrasting microhabitats may play a role in biological invasion. We tested for variation in demographic performance and phenotypic trait expression during invasion by Alliaria petiolata in different microhabitats. We performed a reciprocal transplant experiment with Alliaria petiolata from edge, intermediate, and forest understory microhabitats to determine the roles of the environment and maternal source on traits, fecundity, population growth rates (λ), and selection. Observations of in situ populations show that edge populations had the highest density and reproductive output, and forest populations had the lowest. In experimental populations, population growth rates and reproductive output were highest in the edge, and the intermediate habitat had the lowest germination and juvenile survival. Traits exhibited phenotypic plasticity in response to microhabitat, but that plasticity was not adaptive. There were few effects of maternal source location on fitness components or traits. Alliaria petiolata appears to be viable, or nearly so, in all three microhabitat types, with edge populations likely providing seed to the other microhabitats. The intermediate microhabitat may filter propagules at the seed stage, but discrepancies between in situ observations and experimental transplants preclude clear conclusions about the role of each microhabitat in niche expansion. However, edge microhabitats show the highest seed output in both analyses, suggesting that managing edge habitats might reduce spread to the forest understory.

Cytological and morphological variation of Fallopia sect. Reynoutria taxa (Polygonaceae) in the Krivánska Malá Fatra Mountains (Slovakia)

Representatives of Fallopia sect. Reynoutria (knotweeds) belong to the most aggressive invasive plants in Europe. Despite their significant role in biological invasions and the major interest devoted to them by botanists and environmentalists, the identification of the members of this group is still very difficult and often mistaken. We studied the distribution of this group in the northwestern part of the Krivanska Mala Fatra Mountains (northwestern Slovakia). Forty-three Fallopia sect. Reynoutria stands (53 stems, 106 leaves) were used in flow cytometry and multivariate morphometrics to evaluate their genome size and morphological variation. Our research revealed that the group in the study area includes three knotweed taxa and that each of them is represented by only one cytotype: hexaploid (2n = 6x ~ 66) in F. ×bohemica (23 stands), octoploid (2n = 8x ~ 88) in F. japonica var. japonica (18 stands) and tetraploid (2n = 4x ~ 44) in F. sachalinensis (2 stands). Morphometrics of 23 leaf characters revealed that the most reliable distinguishing character of Fallopia sect. Reynoutria taxa is leaf indumentum. Analyses showed that F. ×bohemica is much more similar in leaf morphology to F. japonica var. japonica than to F. sachalinensis, thus explaining the fact that F. ×bohemica is, in both Slovakia and Europe, very often confused with F. japonica var. japonica, whose presence outside cultivation is overestimated. Compared to the other two knotweed taxa, occurrences of F. japonica var. japonica in the study area were situated mainly along watercourses, due to its exclusively vegetative propagation.

The indirect role of species‐level factors in biological invasions

AbstractAimBiological invasions are driven by factors related to species, locations and events. Species‐level factors (namely functional traits) often distinguish successful invaders from other groups of species in trait‐only analyses. However, traits are routinely found to be much less important than event‐level (e.g. propagule pressure) or location‐level (e.g. abiotic or congeneric effects) factors when included in the same model. We hypothesized that this rift exists largely because traits have (often overlooked) indirect effects that affect invasion success by influencing other mechanisms.LocationGlobal.MethodsWe developed a conceptual path diagram hypothesizing indirect effects on invasion success of species traits directly affecting (1) native range size, (2) propagule pressure, and (3) climate matching between native and non‐native ranges. We used structural equation modelling to evaluate our hypothesis using open‐access datasets on: (1) the naturalization success of non‐native Pinus in New Zealand (McGregor et al., 2012, Diversity and Distributions, 18, 1013–1023), and (2) the global establishment success of non‐native reptiles (Mahoney et al., 2015, Diversity and Distributions, 21, 64–74). Both these studies found little to no direct importance of traits on invasion success.ResultsOur analyses revealed indirect effects of species traits and native range size on invasion success. Traits indirectly affected Pinus naturalization success and reptile establishment success by affecting introduction effort and native range size. Consistent with the original analyses, traits had little measurable direct effect on invasion success.Main conclusionsSpecies‐level factors have both direct and indirect roles in biological invasions. Consideration of the indirect effects of functional traits may help to reconcile disparities in findings on the relative role of traits versus other contributors to the invasion process.

Photosynthetic electron-transfer reactions in the gametophyte of Pteris multifida reveal the presence of allelopathic interference from the invasive plant species Bidens pilosa

To date, the response of the fern gametophyte to its environment has received considerable attention. However, studies on the influence of plant invasion on the fern gametophyte are fewer. Allelopathy has been hypothesized to play an important role in biological invasion. Hence, it is necessary to study the allelopathy of invasive plant species to the fern gametophyte and elucidate the mechanisms by which invasive plants cause phytotoxicity. As one of the main invasive plants in China, Bidens pilosa exhibits allelopathic effects on the gametophytic growth of Pteris multifida. The root exudate plays an important role among various allelochemical delivery mechanisms in B. pilosa. The effect invasive plant species has on photosynthesis in native species is poorly understood. To elucidate this effect, the changes in photosynthesis in the gametophytes of P. multifida are analyzed to examine the mechanisms of the root exudates of B. pilosa. Meanwhile, a non-invasive plant, Coreopsis basalis, was also applied to investigate the effects on fluorescence and pigments in P. multifida gametophytes. We found that gametophytes exposed to both B. pilosa and C. basalis had decreased fluorescence parameters in comparison with the control, except for non-photochemical quenching. Furthermore, it was found that these parameters were markedly affected from day 2 to day 10 in the presence of both exudates at a concentration of 25% or above. B. pilosa exudate had a negative dose-dependent effect on chlorophyll a, chlorophyll b, carotenoid, and the total chlorophyll in the gametophyte. The inhibitory effects increased with increasing exudate concentrations of both species, exhibiting the greatest inhibition at day 10. In conclusion, B. pilosa irreversibly affected the photosynthesis of P. multifida on both PS I and PS II. Root exudates caused the primary damage with respect to the decrease of the acceptors and donors of photon and electron in photosynthetic units and the production and the relative yield of photochemical quantum in PS II. With the effects of exudates, part of the energy is released as heat in chloroplasts. The comparison of invasive and non-invasive plants in allelopathic experiments demonstrated that invasive plants were responsible for the critical damage to the photosynthetic process in local species.

An alien fish threatens an endangered parasitic bivalve: the relationship between brook trout (Salvelinus fontinalis) and freshwater pearl mussel (Margaritifera margaritifera) in northern Europe

AbstractHost–parasite interactions may play a significant role in biological invasions: for example, an invader may benefit from lower infectivity by native parasites in competition against the native hosts (‘enemy release hypothesis’).The invasive North American brook trout (Salvelinus fontinalis) is replacing the native salmonid hosts of the freshwater pearl mussel (FPM,Margaritifera margaritifera) in northern Europe, but the suitability of brook trout as a host for FPM is poorly known. In this study its suitability was investigated using an array of laboratory and field experiments, and several FPM populations from a catchment in northern Finland. The occurrence of brook trout in FPM rivers in the area was also studied.There were differences with respect to numbers and size of FPM larvae among the fish exposed to FPM, but generally brook trout was an unsuitable host or was clearly a poorer host for FPM than the native European salmonids, brown trout (Salmo trutta) or Atlantic salmon (Salmo salar). However, in one river a few FPM glochidia remained encysted in wild brook trout for at least 9 months, suggesting successful development – the first observation of its kind in Europe.A tendency was found for higher occurrence of brook trout in brown trout rivers with FPM than in brown trout rivers without FPM, being consistent with the enemy release hypothesis: as FPM infection is costly to the host, a higher glochidial load in brown trout may offer a competitive advantage to brook trout in FPM rivers.Generally, these results indicate that northern European FPM populations cannot typically use brook trout as their host fish. Therefore, the invasion and dispersal of brook trout, potentially leading to the disappearance of native salmonids, should also be considered as a potential threat to the endangered FPM populations.Copyright © 2016 John Wiley & Sons, Ltd.

Changes in gametophyte physiology of Pteris multifida induced by the leaf leachate treatment of the invasive Bidens pilosa.

In recent years, the response of fern gametophytes to environment has raised much attention. However, studies on the influence of plant invasion to fern gametophytes are scarce. Allelopathy plays an important role in biological invasion. Hence, it is necessary to study the allelopathic effects of invasive plants on fern gametophytes and elucidate the mechanisms by which invasive plants cause phytotoxicity. As one of the main invasive plants in China, Bidens pilosa exhibits allelopathic effects on spermatophyte growth. Field investigation shows that many ferns are threatened by the invasion of B. pilosa. The distribution of Pteris multifida overlaps with that of B. pilosa in China. To examine the potential involvement of allelopathic mechanisms of B. pilosa leaves, changes in the physiology in P. multifida gametophytes are analyzed. We found that cell membrane and antioxidant enzyme activities as well as photosynthesis pigment contents of the gametophytes were affected by B. pilosa leachates. Gametophytes of P. multifida exposed to B. pilosa had increased damages to cell membranes, expressed in thiobarbituric acid reacting substance (TBARS) concentrations, malondialdehyde (MDA), electrolyte leakage (membrane permeability), and degree of injury. Enzyme activities, assessed by superoxide dismutase (SOD) and catalase (CAT) as well as guaiacol peroxidase (GPX) enhanced with the increase in leachate concentration after 2-day exposure. Meanwhile, lower chlorophyll a (Chl a), chlorophyll b (Chl b), carotenoid (Car), and the total chlorophyll were measured as leachate concentrations increased. At day 10, leaf leachates of B. pilosa exhibited the greatest inhibition. These results suggest that the observed inhibitory or stimulatory effects on the physiology studied can have an adverse effect on P. multifida and that allelopathic interference seems to have involved in this process.

Harmonia + and Pandora +: risk screening tools for potentially invasive plants, animals and their pathogens

Given the large number of alien species that may potentially develop into invasives, there is a clear need for robust schemes that allow to screen species for such risks. The Harmonia+ framework presented here brings together 30 questions that refer to distinct components of invasion. Together, they cover the stages of introduction, establishment, spread, and multiple kinds of impacts, viz. referring to the health of the environment (including wild species), cultivated plants, domesticated animals and man. In a complete assessment, input is provided by choosing among predefined ordinal answers and by supplementing these with textual clarification. Uncertainty is covered by indicating levels of confidence. By converting answers into scores, which are then condensed into summary statistics, Harmonia+ allows for quantitative output on stage-specific and general risks. Test assessments on five species emerging in Belgium showed the perceived environmental risks of Procambarus clarkii to be highest (0.72), and that of Threskiornis aethiopicus to be lowest (0.13). Given the considerable parallels that exist between invasive alien species and emerging infectious diseases, we additionally created Pandora, which is a risk analysis scheme for pathogens and parasites. It consists of 13 key questions and has the same structure as Harmonia+. Since diseases play a paramount role in biological invasions, results of Pandora assessments may feed into Harmonia+ through a slightly adapted, host-specific version named Pandora+. Harmonia+, Pandora and Pandora+ may be used both for prioritization purposes and for underpinning detailed risk analyses, and can be consulted online through http://ias.biodiversity.be.

Genetics of a Lessepsian sprinter: the bluespotted cornetfish, Fistularia commersonii

Our current understanding of the mechanisms that lead to successful biological invasions is limited. Although local adaptation plays a central role in biological invasions, genetic studies have failed to produce a unified theory so far. The bluespotted cornetfish, a recent invader of the Mediterranean Sea from the Red Sea via the Suez Canal, provides an ideal case study to research the mechanisms of invasive genetics. Previous genetic work based on mitochondrial markers has shown the genetic diversity of the Mediterranean population was greatly reduced in comparison to the natural population in the Red Sea. In the current study, we expand upon these studies by adding mitochondrial and nuclear markers. Mitochondrial results confirm previous findings. The nuclear marker, however, does not show evidence of reduction in diversity. We interpret these results as either a differential dispersal capability in males and females, or the presence of selection on the invading Mediterranean population.

Two-Way but Asymmetrical Reproductive Interference between an Invasive <i>Veronica</i> Species and a Native Congener

Recent studies have suggested that reproductive interference, a deleterious interspecific interaction in the mating process, plays an important role in biological invasions. In the system of plant species, however, the border with the pollen limitation has often been vague in past studies. This study, using field and laboratory experiments and field observations, examined the reproductive success of an endangered native herbaceous plant, Veronica polita lilacina, in the context of the reproductive interference by the alien congener, V. persica. The auto-pollination experiment confirmed that both species can usually produce seeds even without external conspecific pollens. Results of the artificial pollination experiment demonstrated that pollination with the heterospecific pollens significantly decreases the number of seeds in the native species, but not in the alien species. A transplant experiment revealed that the coexistence with the alien species reduced the fruiting success of the native species. Field observations have shown the interaction between two species in the native patch with only one intruding alien species. They demonstrated that native individuals placed closer to the alien individual suffered a greater decrease in fruiting success and the seed production and that the alien intruder produced no seed. These results demonstrate that species that could reproduce via the auto-pollination suffered the reproductive interference and that the native species also exert the resistive reproductive interference slightly. These interactions can explain the displacement pattern of the native species by the alien congener in Japan.

Seed production is reduced by small population size in natural populations of the invasive grass Lolium multiflorum

As founders of new invasions or survivors of control efforts, small populations can play important roles in biological invasions. Theory and models have explored how population size can affect invasion probability and dynamics. In contrast, there have been few studies of small population size and invasions in the wild, especially for plants. Here, we identified 21 naturally-occurring small populations of the invasive annual grass Lolium multiflorum to elucidate the effects of population size on plant reproduction and potential invasiveness. We compared seed production of focal plants to three attributes of the population: population size, a focal plant’s floret neighborhood (a measure of the size and pollen production of nearby potential pollen donors), and focal plant size. Population size and floret neighborhood were weighted by inter-plant distance to account for variation in density and spatial arrangement. Variation among populations in the proportion of florets producing a seed was explained by population size and floret neighborhood. In contrast, the focal plant’s size did not significantly affect the seed production proportion. A decrease in reproduction due to the size and density of the population (while accounting for maternal size) is an Allee effect, which may limit the ability to predict invasion risks and rates early in the invasion process, particularly if the effect is not recognized.

Testing the directed dispersal hypothesis: are native ant mounds (Formica sp.) favorable microhabitats for an invasive plant?

Ant-mediated seed dispersal may be a form of directed dispersal if collected seeds are placed in a favorable microhabitat (e.g., in or near an ant nest) that increases plant establishment, growth, and/or reproduction relative to random locations. We investigated whether the native ant community interacts with invasive leafy spurge (Euphorbia esula) in a manner consistent with predictions of the directed dispersal hypothesis. Resident ants quickly located and dispersed 60% of experimentally offered E. esula seeds. Additionally, 40% of seeds whose final deposition site was observed were either brought inside or placed on top of an ant nest. Seed removal was 100% when seeds were placed experimentally on foraging trails of mound-building Formica obscuripes, although the deposition site of these seeds is unknown. Natural density and above-ground biomass of E. esula were greater on Formica mound edges compared to random locations. However, seedling recruitment and establishment from experimentally planted E. esula seeds was not greater on mound edges than random locations 3 m from the mound. Soil from Formica mound edges was greater in available nitrogen and available phosphorus relative to random soil locations 3 m from the mound. These results suggest Formica ant mounds are favorable microhabitats for E. esula growth following seedling establishment, a likely consequence of nutrient limitation during plant growth. The results also indicate positive species interactions may play an important role in biological invasions.

Integrating multiple disturbance aspects: management of an invasive thistle, Carduus nutans

Disturbances occur in most ecological systems, and play an important role in biological invasions. We delimit five key disturbance aspects: intensity, frequency, timing, duration and extent. Few studies address more than one of these aspects, yet interactions and interdependence between aspects may lead to complex outcomes. In a two-cohort experimental study, we examined how multiple aspects (intensity, frequency and timing) of a mowing disturbance regime affect the survival, phenology, growth and reproduction of an invasive thistle Carduus nutans (musk thistle). Our results show that high intensity and late timing strongly delay flowering phenology and reduce plant survival, capitulum production and plant height. A significant interaction between intensity and timing further magnifies the main effects. Unexpectedly, high frequency alone did not effectively reduce reproduction. However, a study examining only frequency and intensity, and not timing, would have erroneously attributed the importance of timing to frequency. We used management of an invasive species as an example to demonstrate the importance of a multiple-aspect disturbance framework. Failure to consider possible interactions, and the inherent interdependence of certain aspects, could result in misinterpretation and inappropriate management efforts. This framework can be broadly applied to improve our understanding of disturbance effects on individual responses, population dynamics and community composition.

Mutualism and adaptive divergence: co-invasion of a heterogeneous grassland by an exotic legume-rhizobium symbiosis.

Species interactions play a critical role in biological invasions. For example, exotic plant and microbe mutualists can facilitate each other's spread as they co-invade novel ranges. Environmental context may influence the effect of mutualisms on invasions in heterogeneous environments, however these effects are poorly understood. We examined the mutualism between the legume, Medicago polymorpha, and the rhizobium, Ensifer medicae, which have both invaded California grasslands. Many of these invaded grasslands are composed of a patchwork of harsh serpentine and relatively benign non-serpentine soils. We grew legume genotypes collected from serpentine or non-serpentine soil in both types of soil in combination with rhizobium genotypes from serpentine or non-serpentine soils and in the absence of rhizobia. Legumes invested more strongly in the mutualism in the home soil type and trends in fitness suggested that this ecotypic divergence was adaptive. Serpentine legumes had greater allocation to symbiotic root nodules in serpentine soil than did non-serpentine legumes and non-serpentine legumes had greater allocation to nodules in non-serpentine soil than did serpentine legumes. Therefore, this invasive legume has undergone the rapid evolution of divergence for soil-specific investment in the mutualism. Contrary to theoretical expectations, the mutualism was less beneficial for legumes grown on the stressful serpentine soil than on the non-serpentine soil, possibly due to the inhibitory effects of serpentine on the benefits derived from the interaction. The soil-specific ability to allocate to a robust microbial mutualism may be a critical, and previously overlooked, adaptation for plants adapting to heterogeneous environments during invasion.

Anthropogenically induced adaptation to invade (AIAI): contemporary adaptation to human-altered habitats within the native range can promote invasions.

Adaptive evolution is currently accepted as playing a significant role in biological invasions. Adaptations relevant to invasions are typically thought to occur either recently within the introduced range, as an evolutionary response to novel selection regimes, or within the native range, because of long-term adaptation to the local environment. We propose that recent adaptation within the native range, in particular adaptations to human-altered habitat, could also contribute to the evolution of invasive populations. Populations adapted to human-altered habitats in the native range are likely to increase in abundance within areas frequented by humans and associated with human transport mechanisms, thus enhancing the likelihood of transport to a novel range. Given that habitats are altered by humans in similar ways worldwide, as evidenced by global environmental homogenization, propagules from populations adapted to human-altered habitats in the native range should perform well within similarly human-altered habitats in the novel range. We label this scenario ‘Anthropogenically Induced Adaptation to Invade’. We illustrate how it differs from other evolutionary processes that may occur during invasions, and how it can help explain accelerating rates of invasions.