A snail prefers native over exotic freshwater plants: implications for the enemy release hypotheses

1. One of the most popular single‐factor hypotheses that have been proposed to explain the naturalization and spread of introduced species is the enemy release hypothesis (ERH). Most studies have considered how specialist consumers might affect the success of exotics, but the importance of generalist herbivores has received little attention 2. In this study, we compared the palatability of native and exotic freshwater plants in both phylogenetic pairings and in region‐wide assays, using a generalist consumer (the pond snail Radix swinhoei). 3. Our study indicated that, when plants were paired by taxonomic relatedness, the snail preferred native over exotic freshwater plants by a 2 : 1 ratio. The snail also preferred native over exotic plants when tested across 20 native and seven exotic species found growing in Liangzi Lake. 4. Snails consumed more biomass of native than exotic plants, providing support for the ERH and suggesting that exotic species have a potential advantage in most lakes of the middle and lower reaches of the Yangtze River in China, thus helping their invasion.     

Phylogenetic isolation increases plant success despite increasing susceptibility to generalist herbivores

Aim Theory suggests that introduced species that are phylogenetically distant from their recipient communities should be more successful than closely related introduced species because they can exploit open niches and escape enemies in their new range, i.e. Darwin’s Naturalization Hypothesis. Alternatively, it has also been hypothesized that closely related invaders might be more successful than novel invaders because they are pre‐adapted to conditions in their new range; a paradox coined Darwin’s Naturalization Conundrum. To date, these hypotheses have been tested primarily at the regional scale, not within local plant communities where introduced species colonize, compete and encounter herbivores. Location Global. Methods and Results We used community phylogenetics to analyse data from 49 published experiments to examine the importance of phylogenetic relatedness and generalist herbivory on native and exotic plant success at the community level. Plants that were categorized as ‘invasive’ were indeed less related to the recipient community than ‘non‐pest’ exotic plants. Distantly related exotic plants were also more abundant than closely related species. Phylogenetic relatedness predicted herbivore impact, but in a way that was opposite to predictions, as herbivores had stronger, not lesser, impacts on distantly related plants. Importantly, these same patterns generally held for native plants, as distantly related native plants were more abundant and more susceptible to herbivores than closely related species, ultimately resulting in herbivores suppressing community‐level phylogenetic diversity. Main conclusions Distantly related plants were more locally successful despite experiencing stronger control by generalist herbivores, a finding that was robust across native and exotic species. To our knowledge, this is the first evidence that phylogenetic matching influences the local success of both native and exotic species and that herbivores can influence community phylodiversity. Phylogenetic relatedness explained a relatively small portion of the variance in the data even after taking herbivory into account, however, suggesting that phylogenetic matching works in combination with other factors to influence community assembly.     

Does Plant Origin Influence the Fitness Impact of Flower Damage? A Meta-Analysis

Herbivory has been long considered an important component of plant-animal interactions that influences the success of invasive species in novel habitats. One of the most important hypotheses linking herbivory and invasion processes is the enemy-release hypothesis, in which exotic plants are hypothesized to suffer less herbivory and fitness-costs in their novel ranges as they leave behind their enemies in the original range. Most evidence, however, comes from studies on leaf herbivory, and the importance of flower herbivory for the invasion process remains largely unknown. Here we present the results of a meta-analysis of the impact of flower herbivory on plant reproductive success, using as moderators the type of damage caused by floral herbivores and the residence status of the plant species. We found 51 papers that fulfilled our criteria. We also included 60 records from unpublished data of the laboratory, gathering a total of 143 case studies. The effects of florivory and nectar robbing were both negative on plant fitness. The methodology employed in studies of flower herbivory influenced substantially the outcome of flower damage. Experiments using natural herbivory imposed a higher fitness cost than simulated herbivory, such as clipping and petal removal, indicating that studies using artificial herbivory as surrogates of natural herbivory underestimate the real fitness impact of flower herbivory. Although the fitness cost of floral herbivory was high both in native and exotic plant species, floral herbivores had a three-fold stronger fitness impact on exotic than native plants, contravening a critical element of the enemy-release hypothesis. Our results suggest a critical but largely unrecognized role of floral herbivores in preventing the spread of introduced species into newly colonized areas.     

Winning and losing with microbes: how microbially mediated fitness differences influence plant diversity

Interactions between plants and soil microbes can strongly influence plant diversity and community dynamics. Soil microbes may promote plant diversity by driving negative frequency‐dependent plant population dynamics, or may favor species exclusion by providing one species an average fitness advantage over others. However, past empirical research has focused overwhelmingly on the consequences of frequency‐dependent feedbacks for plant species coexistence and has generally neglected the consequences of microbially mediated average fitness differences. Here we use theory to develop metrics that quantify microbially mediated plant fitness differences, and show that accounting for these effects can profoundly change our understanding of how microbes influence plant diversity. We show that soil microbes can generate fitness differences that favour plant species exclusion when they disproportionately harm (or favour) one plant species over another, but these fitness differences may also favor coexistence if they trade off with competition for other resources or generate intransitive dominance hierarchies among plants. We also show how the metrics we present can quantify microbially mediated fitness differences in empirical studies, and explore how microbial control over coexistence varies along productivity gradients. In all, our analysis provides a more complete theoretical foundation for understanding how plant–microbe interactions influence plant diversity.     

The rhizosphere microbiome: Plant–microbial interactions for resource acquisition

While horticulture tools and methods have been extensively developed to improve the management of crops, systems to harness the rhizosphere microbiome to benefit plant crops are still in development. Plants and microbes have been coevolving for several millennia, conferring fitness advantages that expand the plant’s own genetic potential. These beneficial associations allow the plants to cope with abiotic stresses such as nutrient deficiency across a wide range of soils and growing conditions. Plants achieve these benefits by selectively recruiting microbes using root exudates, positively impacting their nutrition, health and overall productivity. Advanced knowledge of the interplay between root exudates and microbiome alteration in response to plant nutrient status, and the underlying mechanisms there of, will allow the development of technologies to increase crop yield. This review summarizes current knowledge and perspectives on plant–microbial interactions for resource acquisition and discusses promising advances for manipulating rhizosphere microbiomes and root exudation.     

Friend or foe? The role of leaf-inhabiting fungal pathogens and endophytes in tree-insect interactions

Trees are large organisms that structure forest ecosystems by providing an environment for an enormous diversity of animal, microbial and plant species. As these species use trees as their common hosts, many are likely to interact with each other directly or indirectly. From studies on herbaceous plant species we know that microbes can affect the interaction of plants with herbivorous insects, for example via changes in plant metabolite profiles. The consequences of fungal colonization for tree-insect interactions are, however, barely known, despite the importance of these ecological communities. In this review we explore the interaction of leaf-inhabiting pathogenic and endophytic fungi with trees and the consequences for tree-living insect herbivores. We discuss molecular, physiological, chemical, biochemical and ecological aspects of tree-fungus interactions and summarize the current knowledge on the direct and indirect effects of tree-inhabiting fungi on insect herbivores.Our mechanistic understanding of the tripartite interaction of trees with leaf-inhabiting fungi and insect herbivores is still in its infancy. We are currently facing substantial drawbacks in experimental methodology that prevent us from revealing the effect of one single fungal species on a particular insect herbivore species and vice versa. Future studies applying a versatile toolbox of modern molecular, chemical analytical and ecological techniques in combined laboratory and field experiments will unequivocally lead to a better understanding of fungus-tree-insect interactions.     

Proportion of exotics and relatedness of host species mediate the positive effect of plant richness on the species richness of fruit flies

1. All else being equal, the greater the local species richness of plants, the greater the number of associated herbivore species. Because most herbivore insects feed on a subset of closely related plant species, plant phylogenetic diversity is expected to play a key role in determining the number of herbivore species. What is not well known, however, is how an increase in the species richness of exotic plants affects the species richness of herbivores. 2. In this study, we used plant–fruit fly interactions to investigate the influence of the proportion and species richness of exotic host plants on the species richness of herbivorous insects. We also tested whether the phylogenetic diversity of host plants increases when the number of exotic plant species increases. 3. We found that the species richness of fruit flies is more accurately predicted by the richness of native host plants than by total plant species richness (including both native and exotic species). The proportion of exotic host species and the phylogenetic diversity of host plants had negative and positive effects, respectively, on the species richness of fruit flies. 4. Our findings suggest that a positive effect of plant richness on herbivore richness occurs only when an increase in plant diversity involves plant species with which native herbivores share some evolutionary history.     

Different effects of two exotic herbivores on the pollinator-mediated effect of an exotic plant on a native plant

Exotic plants can affect native plants indirectly through various biotic interactions. However, combinations of the multiple indirect effects of exotic plants on native plants have been rarely evaluated. Herbivory can either positively or negatively influence plant–pollinator interactions. Here, we addressed whether the pollinator-mediated plant interaction between exotic and native plants is altered through the introduction of exotic herbivores by conducting a 2-year common garden experiment. We compared the effects of pollinator-mediated indirect effects of an exotic plant, Solidago altissima, on the co-flowering native plant Aster microcephalus in geographically different populations reflecting differences in insect herbivore communities. We found a positive effect of co-flowering S. altissima on pollinator visitation of A. microcephalus, which varied between gardens and years. The co-flowering S. altissima did not significantly affect the seed set of A. microcephalus in the first year but had a negative effect in the second year. The facilitative effect of S. altissima on A. microcephalus pollination was suggested to be negatively affected by an exotic aphid, while it was not significantly affected by an exotic lace bug. Our study suggests that the phenology and feeding guilds of the herbivores may be critical for predicting the effect of exotic plants on native plants through herbivore–pollinator interactions. Integrated effects between plant interactions via multiple species interactions under different abiotic and biotic environments are necessary to understand the impact of exotic plants under complex interactions in nature.     

Predicting novel herbivore–plant interactions

As human‐aided range expansions and climate change alter the distributions of plants and their herbivores, predicting and addressing novel species interactions will become increasingly pressing for community ecologists. In this context, a key, surprisingly understudied question is: when an exotic plant is introduced, which herbivores will adopt this new potential host? Whether the plant is a weed, an ornamental, or a crop, the development versus non‐development of a novel plant–insect interaction can have profound effects for both economic and conservation applications. In this paper, we sketch mechanistic and statistical frameworks for predicting these interactions, based on how plant and herbivore traits as well as shared evolutionary history can influence detection, recognition, and digestion of novel plants. By emphasizing mechanisms at each of these steps, we hope to clarify different aspects of novel interactions and why they may or may not occur. We also emphasize prediction and forecasting, as a major goal is to know in advance which interactions will develop from the many plant or insect introductions that occur in natural and man‐made systems.     

Competition and facilitation in multispecies plant-herbivore systems of productive environments

We develop a multispecies plant-herbivore model to explore how plant competition for light and the selectivity of herbivores affect abundance patterns of plants and herbivores along productivity gradients. The model considers a small and a tall plant species, a generalist herbivore, and a selective herbivore. The selective herbivore feeds only on the small plant species. In the absence of the generalist herbivore, the tall plant species becomes increasingly dominant with increasing productivity, and the small plant and its selective herbivore disappear. The model shows that generalist herbivores can facilitate selective herbivores by suppressing competition for light. This favours the small plant species, and thereby the selective herbivores. The model predictions are qualitatively consistent with field studies of multispecies plant-herbivore systems.     

Exotic vertebrate and invertebrate herbivores differ in their impacts on native and exotic plants: a meta-analysis

Herbivores modify various ecological processes including interactions between native and exotic plants that may affect invasion success by the exotic plants. It is unknown whether different types of exotic herbivores have similar effects on native and exotic plants. Using two distinct data sets, we ran meta-analyses to compare exotic vertebrate and invertebrate herbivore preferences for, and effects on performance and population sizes of native and exotic plants. We found that exotic vertebrate herbivores have positive effects on exotic plant performance and population sizes, and no significant effects on native plants. Exotic invertebrates have significant negative effects on performance and population sizes of both exotic and native plants. Vertebrates prefer to feed on native plants relative to exotic plants, while invertebrates prefer the exotic plants to native plants. Thus the exotic vertebrate herbivores may aid invasiveness of exotic plants, in accordance with the invasional meltdown hypothesis, while exotic invertebrate herbivores probably have no net effect on invasion process of the exotic plants. Invertebrate herbivore preferences for exotic plants support the biotic resistance hypothesis, as the native plants probably resist the invertebrate herbivory. We also tested an evolutionary logic that posits that herbivores with similar evolutionary history as plants will affect the plants less negatively than plants with which they have not co-evolved. Our results indicate that there is no consistent pattern in effects of exotic vertebrate and invertebrate herbivores on exotic plants with or without which they have co-evolved.     

When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypotheses

Two venerable hypotheses, widely cited as explanations for either the success or failure of introduced species in recipient communities, are the natural enemies hypothesis and the biotic resistance hypothesis. The natural enemies hypothesis posits that introduced organisms spread rapidly because they are liberated from their co‐evolved predators, pathogens and herbivores. The biotic resistance hypothesis asserts that introduced species often fail to invade communities because strong biotic interactions with native species hinder their establishment and spread. We reviewed the evidence for both of these hypotheses as they relate to the importance of non‐domesticated herbivores in affecting the success or failure of plant invasion.
To evaluate the natural enemies hypothesis, one must determine how commonly native herbivores have population‐level impacts on native plants. If native herbivores seldom limit native plant abundance, then there is little reason to think that introduced plants benefit from escape from these enemies. Studies of native herbivore‐native plant interactions reveal that plant life‐history greatly mediates the strength with which specialist herbivores suppress plant abundance. Relatively short‐lived plants that rely on current seed production for regeneration are most vulnerable to herbivory that reduces seed production. As such, these plants may gain the greatest advantage from escaping their specialist enemies in recipient communities. In contrast, native plants that are long lived or that possess long‐lived seedbanks may not be kept “in check” by native herbivores. For these species, escape from native enemies may have little to do with their success as exotics; they are abundant both where they are native and introduced.
Evidence for native herbivores providing biotic resistance to invasion by exotics is conflicting. Our review reveals that: 1) introduced plants can attract a diverse assemblage of native herbivores and that 2) native herbivores can reduce introduced plant growth, seed set and survival. However, the generality of these impacts is unclear, and evidence that herbivory actually limits or reduces introduced plant spread is scarce. The degree to which native herbivores provide biotic resistance to either exotic plant establishment or spread may be greatly determined by their functional and numerical responses to exotic plants, which we know little about. Generalist herbivores, through their direct effects on seed dispersal and their indirect effects in altering the outcome of native–non‐native plant competitive interactions, may have more of a facilitative than negative effect on exotic plant abundance.     

Elevated carbon dioxide concentrations indirectly affect plant fitness by altering plant tolerance to herbivory

Global environmental changes, such as rising atmospheric CO₂ concentrations, have a wide range of direct effects on plant physiology, growth, and fecundity. These environmental changes also can affect plants indirectly by altering interactions with other species. Therefore, the effects of global changes on a particular species may depend on the presence and abundance of other community members. We experimentally manipulated atmospheric CO₂ concentration and amounts of herbivore damage (natural insect folivory and clipping to simulate browsing) to examine: (1) how herbivores mediate the effects of elevated CO₂ (eCO₂) on the growth and fitness of Arabidopsis thaliana; and (2) how predicted changes in CO₂ concentration affect plant resistance to herbivores, which influences the amount of damage plants receive, and plant tolerance of herbivory, or the fitness consequences of damage. We found no evidence that CO₂ altered resistance, but plants grown in eCO₂ were less tolerant of herbivory—clipping reduced aboveground biomass and fruit production by 13 and 22%, respectively, when plants were reared under eCO₂, but plants fully compensated for clipping in ambient CO₂ (aCO₂) environments. Costs of tolerance in the form of reduced fitness of undamaged plants were detected in eCO₂ but not aCO₂ environments. Increased costs could reduce selection on tolerance in eCO₂ environments, potentially resulting in even larger fitness effects of clipping in predicted future eCO₂ conditions. Thus, environmental perturbations can indirectly affect both the ecology and evolution of plant populations by altering both the intensity of species interactions as well as the fitness consequences of those interactions.     

Friend or foe? A parasitic wasp shifts the cost/benefit ratio in a nursery pollination system impacting plant fitness

Nursery pollination systems are species interactions where pollinators also act as fruit/seed herbivores of the plant partner. While the plants depend on associated insects for pollination, the insects depend on the plants’ reproductive structures for larval development. The outcome of these interactions is thus placed on a gradient between mutualism and antagonism. Less specialized interactions may fluctuate along this gradient with the ecological context, where natural enemies can play an important role. We studied whether a natural enemy may impact the level of seed consumption of a nursery pollinator and how this in turn may influence individual plant fitness. We used the plant Silene latifolia, its herbivore Hadena bicruris, and its ectoparasitoid Bracon variator as a model plant–herbivore–natural enemy system. We investigated seed output, germination, survival, and flower production as proxies for individual plant fitness. We show that B. variator decreases the level of seed consumption by H. bicruris larvae which in turn increased seed output in S. latifolia plants, suggesting that parasitism by B. variator may act as a regulator in the system. However, our results also show that plant survival and flower production decrease with higher seed densities, and therefore, an increase in seed output may be less beneficial for plant fitness than estimated from seed output alone. Our study should add another layer to the complex discussion of whether parasitoids contribute to plant fitness, as we show that taking simple proxies such as seed output is insufficient to determine the net effect of multitrophic interactions.     

Wired to the roots: Impact of root-beneficial microbe interactions on aboveground plant physiology and protection

Often, plant-pathogenic microbe interactions are discussed in a host-microbe two-component system, however very little is known about how the diversity of rhizospheric microbes that associate with plants affect host performance against pathogens. There are various studies, which specially direct the importance of induced systemic defense (ISR) response in plants interacting with beneficial rhizobacteria, yet we don’t know how rhizobacterial associations modulate plant physiology. In here, we highlight the many dimensions within which plant roots associate with beneficial microbes by regulating aboveground physiology. We review approaches to study the causes and consequences of plant root association with beneficial microbes on aboveground plant-pathogen interactions. The review provides the foundations for future investigations into the impact of the root beneficial microbial associations on plant performance and innate defense responses.     

The role of plant resistance and tolerance to herbivory in mediating the effects of introduced herbivores

While the generally negative consequences of introduced species are well known, little is appreciated on the role of the evolutionary history of plants with herbivores in mediating the indirect impacts of herbivory. We examined how variation in plant resistance and tolerance traits can mediate the effects of herbivory and can have differential indirect impacts on other species and processes. We used two examples of a native and an introduced herbivore, Castor canadensis (American beaver) and Cervus elaphus (Rocky Mountain elk) with Populus spp. to test a conceptual model regarding possible outcomes of species interactions with native and exotic mammalian herbivores. Using these two herbivore test cases, we make two predictions to create testable hypotheses across systems and taxa: First, adaptive traits of tolerance or resistance to herbivory will be fewer when exotic species feed on plant species with which they have no evolutionary history. Second, historical constraints of species interactions will allow for negative feedbacks to stabilize the effects of herbivory by a native species. Overall, these two case studies illustrate that plant resistance and tolerance traits can mediate the indirect consequences of herbivory on associated interacting species. Specifically, when there is no evolutionary history between the plants and herbivores, which is often the case with species introductions, the effects of herbivory are more likely to reduce genetic variation and habitat mosaics, thus indirectly affecting associated species.     

Comparisons of arthropod assemblages on an invasive and native trees: abundance,diversity and damage

The success of exotic plants may be due to lower herbivore loads than those on native plants (Enemies Release Hypothesis). Predictions of this hypothesis include lower herbivore abundances, diversity, and damage on introduced plant species compared to native ones. Greater density or diversity of predators and parasitoids on exotic versus native plants may also reduce regulation of exotic plants by herbivores. To test these predictions, we measured arthropod abundance, arthropod diversity, and foliar damage on invasive Chinese tallow tree (Triadica sebifera) and three native tree species: silver maple (Acer saccharinum), sycamore (Platanus occidentalis), and sweetgum (Liquidambar styraciflua). Arthropod samples were collected with canopy sweep nets from six 20 year old monoculture plots of each species at a southeast Texas site. A total of 2,700 individuals and 285 species of arthropods were caught. Overall, the species richness and abundance of arthropods on tallow tree were similar to the natives. But, ordination (NMS) showed community composition differed on tallow tree compared to all three native trees. It supported an arthropod community that had relatively lower herbivore abundance but relatively more predator species compared to the native species examined. Leaves were collected to determine damage. Tallow tree experienced less mining damage than native trees. The results of this study supported the Enemies Release Hypothesis predictions that tallow tree would have low herbivore loads which may contribute to its invasive success. Moreover, a shift in the arthropod community to fewer herbivores without a reduction in predators may further limit regulation of this exotic species by herbivores in its introduced range.     

Plant-aphid interactions: molecular and ecological perspectives

Many aphids are major agricultural pests because of their unparalleled reproductive capacity and their ability to manipulate host plant physiology. Aphid population growth and its impact on plant fitness are strongly influenced by interactions with other organisms, including plant pathogens, endophytes, aphid endosymbionts, predators, parasitoids, ants, and other herbivores. Numerous molecular and genomic resources have recently been developed to identify sources of aphid resistance in plants, as well as potentially novel targets for control in aphids. Moreover, the same model systems that are used to explore direct molecular interactions between plants and aphids can be utilized to study the ecological context in which they occur.     

Transgenerational consequences of plant responses to herbivory: an adaptive maternal effect?

Herbivory has many effects on plants, ranging from shifts in primary processes such as photosynthesis, growth, and phenology to effects on defense against subsequent herbivores and other species interactions. In this study, I investigated the effects of herbivory on seed and seedling characteristics of several families of wild radish (Raphanus raphanistrum) to test the hypothesis that herbivory may affect the quality of offspring and the resistance of offspring to plant parasites. Transgenerational effects of herbivory may represent adaptive maternal effects or factors that constrain or amplify natural selection on progeny. Caterpillar (Pieris rapae) herbivory to greenhouse-grown plants caused plants in some families to produce smaller seeds and those in other families to produce larger seeds compared with undamaged controls. Seed mass was positively associated with probability of emergence in the field. The number of setose trichomes, a putative plant defense, was higher in the progeny of damaged plants in some families and lower in the progeny of damaged plants in other families. In a field experiment, plant families varied in their resistance to several herbivores and pathogens as well as in growth rate and time to flowering. Seeds from damaged parent plants were more likely to become infested with a plant virus. Although herbivory on maternal plants did not directly affect interactions of offspring with other plant parasites, seed mass influenced plant resistance to several attackers. Thus, herbivory affected seed characters, which mediated interactions between plants and their parasites. Finally, irrespective of seed mass, herbivory on maternal plants influenced components of progeny fitness, which was dependent on plant family. Natural selection may act on plant responses to herbivory that affect seedling-parasite interactions and, ultimately, fitness.     

Experimental assemblage of novel plant–herbivore interactions: ecological host shifts after 40 million years of isolation

Geographic isolation is the first step in insect herbivore diet specialization. Such specialization is postulated to increase insect fitness, but may simultaneously reduce insect ability to colonize novel hosts. During the Paleocene‐Eocene, plants from the order Zingiberales became isolated either in the Paleotropics or in the Neotropics. During the Cretaceous, rolled‐leaf beetles diversified in the Neotropics concurrently with Neotropical Zingiberales. Using a community of Costa Rican rolled‐leaf beetles and their Zingiberales host plants as study system, we explored if previous geographic isolation precludes insects to expand their diets to exotic hosts. We recorded interactions between rolled‐leaf beetles and native Zingiberales by combining DNA barcodes and field records for 7450 beetles feeding on 3202 host plants. To determine phylogenetic patterns of diet expansions, we established 20 experimental plots in the field, in which we planted plots five exotic Zingiberales, recording beetles feeding on these exotic hosts. In the laboratory, using both native and exotic host plants, we reared a subset of insect species that had expanded their diets to the exotic plants. The original plant–herbivore community comprised 24 beetle species feeding on 35 native hosts, representing 103 plant–herbivore interactions. After exotic host plant introduction, 20 percent of the beetle species expanded their diets to exotic Zingiberales. Insects only established on exotic hosts that belong to the same plant family as their native hosts. Laboratory experiments show that beetles are able to complete development on these novel hosts. In conclusion, rolled‐leaf beetles are preadapted to expand their diets to novel host plants even after millions of years of geographic isolation.