Species-specific herbivore–herbivore interactions and plant responses to sequential attack by multiple herbivores on a perennial woody plant

When plants are sequentially attacked by multiple herbivores, herbivore identity and host specialization can greatly influence the patterns of herbivore–herbivore and plant–herbivore interactions. However, how prior herbivory and the resulting induced plant responses potentially affect subsequent herbivores deserves further investigation. In this study, we conducted a common-garden experiment that manipulated sequential herbivory by the specialist caterpillar Gadirtha fusca Pogue (Lepidoptera: Nolidae) and the generalist caterpillar Spodoptera litura (Fabricius) (Lepidoptera: Noctuidae) on Chinese tallow, Triadica sebifera (L.) Small (Euphorbiaceae). We tested how prior exposure to herbivores with different levels of host specialization affected the performance of subsequently arriving con- and heterospecifics, as well as plant growth and defense responses under subsequent herbivory. We found that prior exposure to the specialist G. fusca facilitated the performance of subsequent conspecifics, resulting in a significant decrease in the growth (height and stem diameter at ground level) of tallow plants. However, prior exposure to the generalist S. litura did not affect the feeding of subsequent con- or heterospecifics or the growth of tallow plants. Sequential herbivory by specialist and generalist conspecifics resulted in lower levels of tannins and flavonoids, respectively, in leaves of tallow plants, whereas sequential herbivory by the two species did not affect the levels of tannins or flavonoids, compared to a single damage event. We conclude that herbivore species-specific plant responses appear to be more important than herbivore identity or specialization in determining herbivore–herbivore interactions and plant responses to sequential herbivore attack.     

Thresholds in plant–herbivore interactions: predicting plant mortality due to herbivore browse damage

Patterns of herbivore browse at small scales, such as the rate of leaf consumption or plant preferences, drive the impact of herbivores on whole-plant processes, such as growth or survival, and subsequent changes in plant population structure. However, herbivore impacts are often non-linear, highly variable and context-dependent. Understanding the effect of herbivores on plant populations therefore requires a detailed understanding of the relationships that drive small-scale processes, and how these interact to generate dynamics at larger scales. We derive a mathematical model to predict annual rates of browse-induced tree mortality. We model individual plant mortality as a result of rates of foliage production, turnover and herbivore intake, and extend the model to the population scale by allowing for between-tree variation in levels of herbivore browse. The model is configurable for any broadleaved tree species subject to vertebrate or invertebrate browse, and is designed to be parameterized from field data typically collected as part of browse damage assessments. We parameterized and tested the model using data on foliage cover and browse damage recorded on kamahi trees (Weinmannia racemosa) browsed by possums (Trichosurus vulpecula) in New Zealand forests. The model replicated observed patterns of tree mortality at 12 independent validation sites with a wide range of herbivore densities and browse damage. The model reveals two key thresholds; in plant foliar cover, indicating when individual trees may be at high risk from browse-induced mortality, and in herbivore intake, leading to high rates of mortality across the whole population.     

Comparing the conservatism of ecological interactions in plant–pollinator and plant–herbivore networks

Conservatism in species interaction, meaning that related species tend to interact with similar partners, is an important feature of ecological interactions. Studies at community scale highlight variations in conservatism strength depending on the characteristics of the ecological interaction studied. However, the heterogeneity of datasets and methods used prevent to compare results between mutualistic and antagonistic networks. Here we perform such a comparison by taking plant–insect communities as a study case, with data on plant–herbivore and plant–pollinator networks. Our analysis reveals that plants acting as resources for herbivores exhibit the strongest conservatism in species interaction among the four interacting groups. Conservatism levels are similar for insect pollinators, insect herbivores and plants as interacting partners of pollinators, although insect pollinators tend to have a slightly higher conservatism than the two others. Our results thus clearly support the current view that within antagonistic networks, conservatism is stronger for species as resources than for species as consumer. Although the pattern tends to be opposite for plant–pollinator networks, our results suggest that asymmetry in conservatism is much less pronounced between the pollinators and the plant they interact with. We discuss these differences in conservatism strength in relation with the processes structuring plant–insect communities.     

The resource regulation hypothesis and positive feedback loops in plant–herbivore interactions

Resource regulation occurs when herbivory maintains or increases plant susceptibility to further herbivory by the same species. A review of the literature indicates it is a widespread plant–animal interaction involving a diverse array of herbivores. At least three mechanisms can produce this positive feedback cycle. First, phytophagous insect and mammalian herbivore damage can stimulate dormant buds to produce vigorous juvenile growth, which is preferred for further attack. Juvenilization cycles may have repeatedly evolved because herbivores are able to take advantage of a generalized plant compensatory response to any type of damage. Second, herbivores can manipulate plant source–sink relationships to attain more resources, and this alteration of plant growth may benefit subsequent herbivore generations. Third, herbivory can alter plant nutrition or defensive chemistry in a way that makes a plant susceptible to more herbivory. Resource regulation probably occurs because damage to resources preferred by the herbivores induces a generalized plant response that produces more preferred resources. Alternatively, manipulation of plant resources to induce resource regulation may have evolved in herbivores with a high degree of philopatry due to selection to alter plant resources to benefit their offspring. Resource regulation can stabilize insect population dynamics by maintaining a supply of high-quality plant resources. It can also increase the heterogeneity of host-plant resources for herbivores by altering the physiological age structure and the distribution of resources within plants. Resource regulation may have strong plant-mediated effects on other organisms that use that host plant, but these effects have not yet been explored.     

The consequences of synthetic auxin herbicide on plant–herbivore interactions

Although herbicide drift is a common side effect of herbicide application in agroecosystems, its effects on the ecology and evolution of natural communities are rarely studied. A recent shift to dicamba, a synthetic auxin herbicide known for ‘drifting’ to nontarget areas, necessitates the examination of drift effects on the plant–insect interactions that drive eco-evo dynamics in weed communities. We review current knowledge of direct effects of synthetic auxin herbicides on plant–insect interactions, focusing on plant herbivory, and discuss potential indirect effects, which are cascading effects on organisms that interact with herbicide-exposed plants. We end by developing a framework for the study of plant–insect interactions given drift, highlighting potential changes to plant developmental timing, resource quantity, quality, and cues.     

Individual flowering phenology shapes plant–pollinator interactions across ecological scales affecting plant reproduction

The balance of pollination competition and facilitation among co-flowering plants and abiotic resource availability can modify plant species and individual reproduction. Floral resource succession and spatial heterogeneity modulate plant–pollinator interactions across ecological scales (individual plant, local assemblage, and interaction network of agroecological infrastructure across the farm). Intraspecific variation in flowering phenology can modulate the precise level of spatio-temporal heterogeneity in floral resources, pollen donor density, and pollinator interactions that a plant individual is exposed to, thereby affecting reproduction. We tested how abiotic resources and multi-scale plant–pollinator interactions affected individual plant seed set modulated by intraspecific variation in flowering phenology and spatio-temporal floral heterogeneity arising from agroecological infrastructure. We transplanted two focal insect-pollinated plant species (Cyanus segetum and Centaurea jacea, n = 288) into agroecological infrastructure (10 sown wildflower and six legume–grass strips) across a farm-scale experiment (125 ha). We applied an individual-based phenologically explicit approach to match precisely the flowering period of plant individuals to the concomitant level of spatio-temporal heterogeneity in plant–pollinator interactions, potential pollen donors, floral resources, and abiotic conditions (temperature, water, and nitrogen). Individual plant attractiveness, assemblage floral density, and conspecific pollen donor density (C. jacea) improved seed set. Network linkage density increased focal species seed set and modified the effect of local assemblage richness and abundance on C. segetum. Mutual dependence on pollinators in networks increased C. segetum seed set, while C. jacea seed set was greatest where both specialization on pollinators and mutual dependence was high. Abiotic conditions were of little or no importance to seed set. Intra- and interspecific plant–pollinator interactions respond to spatio-temporal heterogeneity arising from agroecological management affecting wild plant species reproduction. The interplay of pollinator interactions within and between ecological scales affecting seed set implies a co-occurrence of pollinator-mediated facilitative and competitive interactions among plant species and individuals.     

Variation in multiple traits of vegetative and reproductive seagrass tissues influences plant–herbivore interactions

Plant–herbivore interactions have strong ecological and evolutionary consequences, but have been traditionally overlooked in marine higher plants. Despite recent advances in seagrass ecology that highlight the importance of herbivory, the mechanisms that regulate the feeding behaviour of seagrass consumers remain largely unknown. Herbivores have been shown to reduce the sexual reproductive success of seagrasses through direct consumption of inflorescences and seeds, but we know little about intraspecific variation in susceptibility to grazing of different seagrass tissues. We contrasted the relative palatability of reproductive and vegetative tissues of the temperate seagrass Posidonia oceanica in the field, and we assessed the feeding preferences among these tissues of the main consumers of the plant, the fish Sarpa salpa and the urchin Paracentrotus lividus. Moreover, we identified the plant traits that explained the observed feeding behaviour. We provide strong evidence for herbivore selectivity among seagrass tissues. In the field, 70–90% of inflorescences were damaged by herbivores compared to 3–60% of leaves of similar age. In feeding assays, the urchin P. lividus showed over a twofold preference for reproductive tissue at various stages of development. By contrast, we detected no feeding activity on either leaves or inflorescences from the fish S. salpa, which is known to migrate to deeper waters soon after flowering starts and during the period of fruit maturation. Despite being the preferred food of urchins, inflorescences were chemically defended, had higher levels of phenolics and lower nutrient and calorific content than leaves. We experimentally demonstrated that leaf structural defences are the primary factor in determining urchin feeding preferences. Removal of plant structure results in a drastic shift in urchin selectivity towards the most nutritious and less chemically defended leaf tissue, indicating that multiple mechanisms of defence to herbivory may coexist in seagrasses.     

Seedling–herbivore interactions: insights into plant defence and regeneration patterns

Background

Herbivores have the power to shape plant evolutionary trajectories, influence the structure and function of vegetation, devastate entire crops, or halt the spread of invasive weeds, and as a consequence, research into plant–herbivore interactions is pivotal to our understanding of plant ecology and evolution. However, the causes and consequences of seedling herbivory have received remarkably little attention, despite the fact that plants tend to be most susceptible to herbivory during establishment, and this damage can alter community composition and structure.

Scope

In this Viewpoint article we review why herbivory during early plant ontogeny is important and in so doing introduce an Annals of Botany Special Issue that draws together the latest work on the topic. In a synthesis of the existing literature and a collection of new studies, we examine several linked issues. These include the development and expression of seedling defences and patterns of selection by herbivores, and how seedling selection affects plant establishment and community structure. We then examine how disruption of the seedling–herbivore interaction might affect normal patterns of plant community establishment and discuss how an understanding of patterns of seedling herbivory can aid our attempts to restore semi-natural vegetation. We finish by outlining a number of areas where more research is required. These include a need for a deeper consideration of how endogenous and exogenous factors determine investment in seedling defence, particularly for the very youngest plants, and a better understanding of the phylogenetic and biogeographical patterns of seedling defence. There is also much still be to be done on the mechanisms of seedling selection by herbivores, particularly with respect to the possible involvement of volatile cues. These inter-related issues together inform our understanding of how seedling herbivory affects plant regeneration at a time when anthropogenic change is likely to disrupt this long-established, but all-too-often ignored interaction.     

Modeling the dynamics of woody plant–herbivore interactions with age-dependent toxicity

In this paper we study the effects that woody plant chemical defenses may have on interactions between boreal hares that in winter feed almost entirely on twigs. We focus particularly on the fact that toxin concentration often varies with the age of twig segments. The model incorporates the fact that the woody internodes of the youngest segments of the twigs of the deciduous angiosperm species that these hares prefer to eat are more defended by toxins than the woody internodes of the older segments that subtend and support the younger segments. Thus, the per capita daily intake of the biomass of the older segments of twigs by hares is much higher than their intake of the biomass of the younger segments of twigs. This age-dependent toxicity of twig segments is modeled using age-structured model equations which are reduced to a system of delay differential equations involving multiple delays in the woody plant-hare dynamics. A novel aspect of the modeling was that it had to account for mortality of non-consumed younger twig segment biomass when older twig biomass was bitten off and consumed. Basic mathematical properties of the model are established together with upper and lower bounds on the solutions. Necessary and sufficient conditions are found for the linear stability of the equilibrium in which the hare is extinct, and sufficient conditions are found for the global stability of this equilibrium. Numerical simulations confirmed the analytical results and demonstrated the existence of limit cycles over ranges of parameters reasonable for hares browsing on woody vegetation in boreal ecosystems. This showed that age dependence in plant chemical defenses has the capacity to cause hare-plant population cycles, a new result.     

Introduction: Plant–herbivore interactions

This special feature resulted from a symposium entitled "Interactions Between Plants and Their Herbivores," held during the Meeting of the Society of Population Ecology in Ohmi-Shirahama, Shiga, Japan, in October 1999 (Chairperson of Symposium: Professor Emeritus E. Kuno of Kyoto University). This theme emerged from discussions by the organizing committee for this symposium: N. Yamamura, J. Takabayashi, T. Nishida, and N. Ohsaki. Professor Mark D. Rausher of Duke University was invited as a special lecturer. In this series of reports, five of the seven participants illustrate the variation found in plant–herbivore interactions and address some problems inherent in current theory.     

Proteasomal degradation in plant–pathogen interactions

The ubiquitin/26S proteasome pathway is a basic biological mechanism involved in the regulation of a multitude of cellular processes. Increasing evidence indicates that plants utilize the ubiquitin/26S proteasome pathway in their immune response to pathogen invasion, emphasizing the role of this pathway during plant–pathogen interactions. The specific functions of proteasomal degradation in plant–pathogen interactions are diverse, and do not always benefit the host plant. Although in some cases, proteasomal degradation serves as an effective barrier to help plants ward off pathogens, in others, it is used by the pathogen to enhance the infection process. This review discusses the different roles of the ubiquitin/26S proteasome pathway during interactions of plants with pathogenic viruses, bacteria, and fungi.     

Biotrophic transportome in mutualistic plant–fungal interactions

Understanding the mechanisms that underlie nutrient use efficiency and carbon allocation along with mycorrhizal interactions is critical for managing croplands and forests soundly. Indeed, nutrient availability, uptake and exchange in biotrophic interactions drive plant growth and modulate biomass allocation. These parameters are crucial for plant yield, a major issue in the context of high biomass production. Transport processes across the polarized membrane interfaces are of major importance in the functioning of the established mycorrhizal association as the symbiotic relationship is based on a ‘fair trade’ between the fungus and the host plant. Nutrient and/or metabolite uptake and exchanges, at biotrophic interfaces, are controlled by membrane transporters whose regulation patterns are essential for determining the outcome of plant–fungus interactions and adapting to changes in soil nutrient quantity and/or quality. In the present review, we summarize the current state of the art regarding transport systems in the two major forms of mycorrhiza, namely ecto- and arbuscular mycorrhiza.     

Plant–plant interactions in tropical alpine environments

Plant–plant interactions are increasingly recognized as a key driver of community organization and ecosystem processes in alpine environments. However, patterns and mechanisms of plant–plant interactions remain largely uncharacterized in tropical alpine ecosystems (TAE) which represent as much as 10% of the total surface area of alpine ecosystems worldwide. In this paper, we review (1) the ecological and environmental features that are specific to TAE in comparison with other alpine ecosystems, (2) the existing literature on plant–plant interactions in TAE, and (3) whether patterns and mechanisms of plant–plant interactions established in extratropical alpine zones can be extended to TAE. TAE are located predominantly in South America, East Africa, and South-East Asia where they show a unique combination of environmental characteristics, such as absence of persisting snow cover, high frequency of diurnal freeze–thaw cycles and needle-ice activity, and a decrease in precipitation with increasing altitude. These environmental characteristics result in the presence of giant growth forms with a great architectural diversity. These biotic and abiotic characteristics influence the outcome of plant–plant interactions by imposing other types of environmental constraints than those found in extratropical alpine environments, and by potentially generating distinctive patterns of niche differentiation/complementarity between species and populations. To generalize the conceptual framework of plant–plant interactions in alpine environments, we advocate that TAE should be investigated more thoroughly by applying designs, methods and hypotheses that are used currently in temperate areas and by conducting studies along large latitudinal gradients that include tropical regions.     

Ligand–receptor interactions in plant hormone signaling

Small-molecule plant hormones principally control plant growth, development, differentiation, and environmental responses. Nine types of plant hormones are ubiquitous in angiosperms, and the molecular mechanisms of their hormone actions have been elucidated during the last two decades by genomic decoding of model plants with genetic mutants. In particular, the discovery of hormone receptors has greatly contributed to the understanding of signal transduction systems. The three-dimensional structure of the ligand–receptor complex has been determined for eight of the nine hormones by X-ray crystal structure analysis, and ligand perception mechanisms have been revealed at the atomic level. Collective research has revealed the molecular function of plant hormones that act as either molecular glue or an allosteric regulator for activation of receptors. In this review, we present an overview of the respective hormone signal transduction and describe the structural bases of ligand–receptor interactions.     

Structural specificity in plant–filamentous pathogen interactions

Plant diseases bear names such as leaf blights, root rots, sheath blights, tuber scabs, and stem cankers, indicating that symptoms occur preferentially on specific parts of host plants. Accordingly, many plant pathogens are specialized to infect and cause disease in specific tissues and organs. Conversely, others are able to infect a range of tissues, albeit often disease symptoms fluctuate in different organs infected by the same pathogen. The structural specificity of a pathogen defines the degree to which it is reliant on a given tissue, organ, or host developmental stage. It is influenced by both the microbe and the host but the processes shaping it are not well established. Here we review the current status on structural specificity of plant–filamentous pathogen interactions and highlight important research questions. Notably, this review addresses how constitutive defence and induced immunity as well as virulence processes vary across plant organs, tissues, and even cells. A better understanding of the mechanisms underlying structural specificity will aid targeted approaches for plant health, for instance by considering the variation in the nature and the amplitude of defence responses across distinct plant organs and tissues when performing selective breeding.     

The roles of ABA in plant–pathogen interactions

Defence against abiotic and biotic stresses is crucial for the fitness and survival of plants under adverse or suboptimal growth conditions. The phytohormone abscisic acid (ABA) is not only important for mediating abiotic stress responses, but also plays a multifaceted and pivotal role in plant immunity. This review presents examples demonstrating the importance of crosstalk between ABA and the key biotic stress phytohormone salicylic acid in determining the outcome of plant–pathogen interactions. We then provide an overview of how ABA influences plant defence responses against various phytopathogens with particular emphasis on the Arabidopsis–Pseudomonas syringae model pathosystem. Lastly, we discuss future directions for studies of ABA in plant immunity with emphasis on, its role in the crosstalk between biotic and abiotic stress responses, the importance of distinguishing direct and indirect effects of ABA, as well as the prospect of utilizing the recently elucidated core ABA signaling network to gain further insights into the roles of ABA in plant immunity.     

Chitooligosaccharide sensing and downstream signaling: contrasted outcomes in pathogenic and beneficial plant–microbe interactions

In plants, short chitin oligosaccharides and chitosan fragments (collectively referred to as chitooligosaccharides) are well-known elicitors that trigger defense gene expression, synthesis of antimicrobial compounds, and cell wall strengthening. Recent findings have shed new light on chitin-sensing mechanisms and downstream activation of intracellular signaling networks that mediate plant defense responses. Interestingly, chitin receptors possess several lysin motif domains that are also found in several legume Nod factor receptors. Nod factors are chitin-related molecules produced by nitrogen-fixing rhizobia to induce root nodulation. The fact that chitin and Nod factor receptors share structural similarity suggests an evolutionary conserved relationship between mechanisms enabling recognition of both deleterious and beneficial microorganisms. Here, we will present an update on molecular events involved in chitooligosaccharide sensing and downstream signaling pathways in plants and will discuss how structurally related signals may lead to such contrasted outcomes during plant–microbe interactions.