John L. Maron

Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems

Biological invasions cause ecological and economic impacts across the globe. However, it is unclear whether there are strong patterns in terms of their major effects, how the vulnerability of different ecosystems varies and which ecosystem services are at greatest risk. We present a global meta-analysis of 199 articles reporting 1041 field studies that in total describe the impacts of 135 alien plant taxa on resident species, communities and ecosystems. Across studies, alien plants had a significant effect in 11 of 24 different types of impact assessed. The magnitude and direction of the impact varied both within and between different types of impact. On average, abundance and diversity of the resident species decreased in invaded sites, whereas primary production and several ecosystem processes were enhanced. While alien N-fixing species had greater impacts on N-cycling variables, they did not consistently affect other impact types. The magnitude of the impacts was not significantly different between island and mainland ecosystems. Overall, alien species impacts are heterogeneous and not unidirectional even within particular impact types. Our analysis also reveals that by the time changes in nutrient cycling are detected, major impacts on plant species and communities are likely to have already occurred.

RAPID EVOLUTION OF AN INVASIVE PLANT

Exotic plants often face different conditions from those experienced where they are native. The general issue of how exotics respond to unfamiliar environments within their new range is not well understood. Phenotypic plasticity has historically been seen as the primary mechanism enabling exotics to colonize large, environmentally diverse areas. However, new work indicates that exotics can evolve quickly, suggesting that contemporary evolution may be more important in invasion ecology than previously appreciated. To determine the influence of contemporary evolution, phenotypic plasticity, and founder ef- fects in affecting phenotypic variation among introduced plants, we compared the size, fecundity, and leaf area of St. Johns wort ( Hypericum perforatum) collected from native European and introduced western and central North American populations in common gardens in Washington, California, Spain, and Sweden. We also determined genetic rela- tionships among these plants by examining variation in amplified fragment length poly- morphism (AFLP) markers. There was substantial genetic variation among introduced populations and evidence for multiple introductions of H. perforatum into North America. Across common gardens in- troduced plants were neither universally larger nor more fecund than natives. However, within common gardens, both introduced and native populations exhibited significant lat- itudinally based clines in size and fecundity. Clines among introduced populations broadly converged with those among native populations. Introduced and native plants originating from northern latitudes generally outperformed those originating from southern latitudes when grown in northern latitude gardens of Washington and Sweden. Conversely, plants from southern latitudes performed best in southern gardens in Spain and California. Clinal patterns in leaf area, however, did not change between gardens; European and central North American plants from northern latitudes had larger leaves than plants from southern latitudes within these regions in both Washington and California, the two gardens where this trait was measured. Introduced plants did not always occur at similar latitudes as their most closely related native progenitor, indicating that pre-adaptation (i.e., climate matching) is unlikely to be the sole explanation for clinal patterns among introduced populations. Instead, results suggest that introduced plants are evolving adaptations to broad-scale environmental conditions in their introduced range.

When is a trophic cascade a trophic cascade

Trophic cascades are the time-honored focal point of food-web dynamics. They are the best loved example of indirect effects in undergraduate ecology textbooks and they represent a potentially useful application of theory. Researchers have found them from the Arctic to the tropics. But, can we agree on what they are? Here, we seek to clarify the terminology of trophic cascades and call for a consensus on how to quantify cascading effects in the future.

Filling key gaps in population and community ecology

We propose research to fill key gaps in the areas of population and community ecology, based on a National Science Foundation workshop identifying funding priorities for the next 5-10 years. Our vision for the near future of ecology focuses on three core areas: predicting the strength and context-dependence of species interactions across multiple scales; identifying the importance of feedbacks from individual interactions to ecosystem dynam- ics; and linking pattern with process to understand species coexistence. We outline a combination of theory devel- opment and explicit, realistic tests of hypotheses needed to advance population and community ecology.

Herbivory: effects on plant abundance, distribution and population growth

Plants are attacked by many different consumers. A critical question is how often, and under what conditions, common reductions in growth, fecundity or even survival that occur due to herbivory translate to meaningful impacts on abundance, distribution or dynamics of plant populations. Here, we review population-level studies of the effects of consumers on plant dynamics and evaluate: (i) whether particular consumers have predictably more or less influence on plant abundance, (ii) whether particular plant life-history types are predictably more vulnerable to herbivory at the population level, (iii) whether the strength of plant–consumer interactions shifts predictably across environmental gradients and (iv) the role of consumers in influencing plant distributional limits. Existing studies demonstrate numerous examples of consumers limiting local plant abundance and distribution. We found larger effects of consumers on grassland than woodland forbs, stronger effects of herbivory in areas with high versus low disturbance, but no systematic or unambiguous differences in the impact of consumers based on plant life-history or herbivore feeding mode. However, our ability to evaluate these and other patterns is limited by the small (but growing) number of studies in this area. As an impetus for further study, we review strengths and challenges of population-level studies, such as interpreting net impacts of consumers in the presence of density dependence and seed bank dynamics.

THE IMPACTS OF A NONINDIGENOUS MARINE PREDATOR IN A CALIFORNIA BAY

Coastal marine ecosystems worldwide are being altered rapidly by the invasion of nonindigenous species. Unlike terrestrial and freshwater systems, the impacts of an invading species have never been quantified on multiple trophic levels for a marine food web. We measured the impact of the nonindigenous green crab, Carcinus maenas, on a coastal marine food web in central California and found that this predator exerted strong “top-down” control, significantly reducing the abundances of several of the 20 invertebrate species monitored over a 9-yr period. Densities of native clams, Nutricola tantilla and Nutricola confusa, and native shore crabs, Hemigrapsus oregonensis, showed 5-fold to 10-fold declines within 3 yr of the arrival of green crabs. Field and laboratory experiments indicated that green crab predation caused these declines. We also tested for indirect responses of invertebrates and vertebrates to green crab predation. There were significant increases in the abundances of two polychaete taxa, Lumbr...

A native nitrogen-fixing shrub facilitates weed invasion

Invasions by exotic weedy plants frequently occur in highly disturbed or otherwise anthropogenically altered habitats. Here we present evidence that, within California coastal prairie, invasion also can be facilitated by a native nitrogen-fixing shrub, bush lupine (Lupinus arboreus). Bush lupines fix nitrogen and grow rapidly, fertilizing the sandy soil with nitrogen-rich litter. The dense lupine canopy blocks light, restricting vegetative growth under bushes. Heavy insect herbivory kills lupines, opening exposed nitrogen-rich sites within the plant community. Eventual re-establishment of lupine occurs because of an abundant and long-lived seed bank. Lupine germination, rapid growth, shading and fertilization of sites, and then death after only a few years, results in a mosaic of nutrient-rich sites that are available to invading species. To determine the role of bush lupine death and nitrogen enrichment in community composition, we examined nutrient dynamics and plant community characteristics within a site only recently colonized by lupine, comparing patches where lupines had recently died or were experimentally killed with adjacent areas lacking lupine. In experimentally killed patches, instantaneous pool sizes of exchangeable ammonium and nitrate nitrogen were higher than in adjacent sites free of lupine. Seedlings of the introduced grass Bromus diandrus accumulated 48% greater root biomass and 93% more shoot biomass when grown in a greenhouse in soil collected under experimentally killed lupines compared to B. diandrus seedlings grown in soil collected at least 1 m away from lupines. At the end of the spring growing season, total above-ground live plant biomass was more than twice as great in dead lupine patches as in the adjacent lupine-free grassland, but dead lupine patches contained 47% fewer plant species and 57% fewer native species. Sites where lupines have repeatedly died and reestablished during recent decades support an interstitial grassland community high in productivity but low in diversity, composed of mostly weedy introduced annual plants. In contrast, at a site only recently colonized by bush lupines, the interstitial grassland consists of a less productive but more diverse set of native and introduced species. We suggest that repeated bouts of lupine germination, establishment, and death can convert a rich native plant community into a less diverse collection of introduced weeds.

Insect Herbivores Drive Real-Time Ecological and Evolutionary Change in Plant Populations

Plant Anti-Insect Armaments Because individual plants are unable to relocate, they are subject to extreme selection by the insects feeding upon them. One means by which plants suppress herbivory is to produce toxic compounds to deter feeding (see the Perspective by Hare). Agrawal et al. (p. 113) compared pesticide–treated or untreated evening primroses. Over 5 years of pesticide treatment, the production of defensive chemicals in the fruit reduced and flowering times shifted, and the primroses competitive ability against dandelions improved. Züst et al. (p. 116) examined large-scale geographic patterns in a polymorphic chemical defense locus in the model plant Arabidopsis thaliana and found that it is matched by changes in the relative abundance of two specialist aphids. Thus, herbivory has strong and immediate effects on the local genotypic composition of plants and traits associated with herbivore resistance. Protecting the common evening primrose from being eaten by insects alters its phenotype in only five growing seasons. Insect herbivores are hypothesized to be major factors affecting the ecology and evolution of plants. We tested this prediction by suppressing insects in replicated field populations of a native plant, Oenothera biennis, which reduced seed predation, altered interspecific competitive dynamics, and resulted in rapid evolutionary divergence. Comparative genotyping and phenotyping of nearly 12,000 O. biennis individuals revealed that in plots protected from insects, resistance to herbivores declined through time owing to changes in flowering time and lower defensive ellagitannins in fruits, whereas plant competitive ability increased. This independent real-time evolution of plant resistance and competitive ability in the field resulted from the relaxation of direct selective effects of insects on plant defense and through indirect effects due to reduced herbivory on plant competitors.

Direct and Interactive Effects of Enemies and Mutualists on Plant Performance: a Meta-Analysis

Plants engage in multiple, simultaneous interactions with other species; some (enemies) reduce and others (mutualists) enhance plant performance. Moreover, effects of different species may not be independent of one another; for example, enemies may compete, reducing their negative impact on a plant. The magnitudes of positive and negative effects, as well as the frequency of interactive effects and whether they tend to enhance or depress plant performance, have never been comprehensively assessed across the many published studies on plant-enemy and plant-mutualist interactions. We performed a meta-analysis of experiments in which two enemies, two mutualists, or an enemy and a mutualist were manipulated factorially. Specifically, we performed a factorial meta-analysis using the log response ratio. We found that the magnitude of (negative) enemy effects was greater than that of (positive) mutualist effects in isolation, but in the presence of other species, the two effects were of comparable magnitude. Hence studies evaluating single-species effects of mutualists may underestimate the true effects found in natural settings, where multiple interactions are the norm and indirect effects are possible. Enemies did not on average influence the effects on plant performance of other enemies, nor did mutualists influence the effects of mutualists. However, these averages mask significant and large, but positive or negative, interactions in individual studies. In contrast, mutualists ameliorated the negative effects of enemies in a manner that benefited plants; this overall effect was driven by interactions between pathogens and belowground mutualists (bacteria and mycorrhizal fungi). The high frequency of significant interactive effects suggests a widespread potential for diffuse rather than pairwise coevolutionary interactions between plants and their enemies and mutualists. Pollinators and mycorrhizal fungi enhanced plant performance more than did bacterial mutualists. In the greenhouse (but not the field), pathogens reduced plant performance more than did herbivores, pathogens were more damaging to herbaceous than to woody plants, and herbivores were more damaging to crop than to non-crop plants (suggesting evolutionary change in plants or herbivores following crop domestication). We discuss how observed differences in effect size might be confounded with methodological differences among studies.

Soil fungal pathogens and the relationship between plant diversity and productivity

One robust result from many small-scale experiments has been that plant community productivity often increases with increasing plant diversity. Most frequently, resource-based or competitive interactions are thought to drive this positive diversity-productivity relationship. Here, we ask whether suppression of plant productivity by soil fungal pathogens might also drive a positive diversity-productivity relationship. We created plant assemblages that varied in diversity and crossed this with a ± soil fungicide treatment. In control (non-fungicide treated) assemblages there was a strong positive relationship between plant diversity and above-ground plant biomass. However, in fungicide-treated assemblages this relationship disappeared. This occurred because fungicide increased plant production by an average of 141% at the lower ends of diversity but boosted production by an average of only 33% at the higher ends of diversity, essentially flattening the diversity-productivity curve. These results suggest that soil pathogens might be a heretofore unappreciated driver of diversity-productivity relationships.