Sharon Y. Strauss

The ecology and evolution of plant tolerance to herbivory

The tolerance of plants to herbivory reflects the degree to which a plant can regrow and reproduce after damage from herbivores. Autoecological factors, as well as the influence of competitors and mutualists, affect the level of plant tolerance. Recent work indicates that there is a heritable basis for tolerance and that it can evolve in natural plant populations. Although tolerance is probably not a strict alternative to plant resistance, there could be inter- and intraspecific tradeoffs between these defensive strategies.

Direct and ecological costs of resistance to herbivory

Herbivores can consume significant amounts of plant biomass in many environments. Yet plants are not defenseless against such attack. Although defenses might benefit plants in the presence of herbivores, herbivore attack varies both spatially and temporally, and the expression of plant resistance to herbivores can be costly in the absence of plant enemies. Costs can be described as allocation costs, resource-based tradeoffs between resistance and fitness, or as ecological costs, decreases in fitness resulting from interactions with other species. Here, we update the seminal 1996 Bergelson and Purrington review of resistance costs and find that many more studies have documented costs of resistance (sensu lato) than found during the 1996 survey. Eighty-two percent of studies in which genetic background is controlled, demonstrate significant fitness reductions associated with herbivore resistance. We categorize studies by type of resistance, induced or constitutive, by type of cost, and also by the degree to which investigators controlled for genetic background. Recent work has commonly detected both direct resistance costs, such as resource-based tradeoffs, and ecological costs, which depend on interactions with other species.

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.

COSTS OF INDUCED RESPONSES AND TOLERANCE TO HERBIVORY IN MALE AND FEMALE FITNESS COMPONENTS OF WILD RADISH

Theory predicts that plant defensive traits are costly due to trade‐offs between allocation to defense and growth and reproduction. Most previous studies of costs of plant defense focused on female fitness costs of constitutively expressed defenses. Consideration of alternative plant strategies, such as induced defenses and tolerance to herbivory, and multiple types of costs, including allocation to male reproductive function, may increase our ability to detect costs of plant defense against herbivores. In this study we measured male and female reproductive costs associated with induced responses and tolerance to herbivory in annual wild radish plants (Raphanus raphanistrum). We induced resistance in the plants by subjecting them to herbivory by Pieris rapae caterpillars. We also induced resistance in plants without leaf tissue removal using a natural chemical elicitor, jasmonic acid; in addition, we removed leaf tissue without inducing plant responses using manual clipping. Induced responses included increased concentrations of indole glucosinolates, which are putative defense compounds. Induced responses, in the absence of leaf tissue removal, reduced plant fitness when five fitness components were considered together; costs of induction were individually detected for time to first flower and number of pollen grains produced per flower. In this system, induced responses appear to impose a cost, although this cost may not have been detected had we only quantified the traditionally measured fitness components, growth and seed production. In the absence of induced responses, 50% leaf tissue removal, reduced plant fitness in three out of the five fitness components measured. Induced responses to herbivory and leaf tissue removal had additive effects on plant fitness. Although plant sibships varied greatly (49–136%) in their level of tolerance to herbivory, costs of tolerance were not detected, as we did not find a negative association between the ability to compensate for damage and plant fitness in the absence of damage. We suggest that consideration of alternative plant defense strategies and multiple costs will result in a broader understanding of the evolutionary ecology of plant defense.

Mutual Feedbacks Maintain Both Genetic and Species Diversity in a Plant Community

The forces that maintain genetic diversity among individuals and diversity among species are usually studied separately. Nevertheless, diversity at one of these levels may depend on the diversity at the other. We have combined observations of natural populations, quantitative genetics, and field experiments to show that genetic variation in the concentration of an allelopathic secondary compound in Brassica nigra is necessary for the coexistence of B. nigra and its competitor species. In addition, the diversity of competing species was required for the maintenance of genetic variation in the trait within B. nigra. Thus, conservation of species diversity may also necessitate maintenance of the processes that sustain the genetic diversity of each individual species.

Foliar Herbivory Affects Floral Characters and Plant Attractiveness to Pollinators: Implications for Male and Female Plant Fitness

Plants are subject o selection exerted by both herbivores and pollinators simultaneously. Despite this fact, no previous tudy has directly linked foliar herbivory and pollination. A few studies have addressed how floral displays that attract pollinators may subsequently attract seed predators, when flowers mature to fruits (Campbell 1991; Brody 1992), but no one has examined how folivore-caused changes in floral characters, particularly corolla characters, affect pollinators. In the past, it has been assumed that floral characters, and particularly corolla characters, are relatively invariant because of the fitness consequences that reduced attractiveness to pollinators may have for self-incompatible plants (e.g., Harper 1977, p. 195). However, it is well known that natural variation in flower size, flower number, nectar production, and pollen production affects the attractiveness of plants to pollinators (e.g., Schemske 1980; Roubick and Buchmann 1984; Willmer 1986; Stanton and Preston 1988; Galen 1989). Effects of foliar herbivory on floral traits other than flower number are not well known (but see McKone 1989; Frazee and Marquis 1994; Quesada et al. 1995). Herbivore damage directly to corollas reduced the attractiveness of flowers to pollinators (Karban and Strauss 1993). The effects of foliar damage by herbivores on floral traits and, in turn, on the attractiveness of plants to pollinators have been generally ignored (Crawley 1989; Marquis 1992). The significance of floral responses to foliar herbivory is twofold. First, estimates of the effects of herbivory on plant fitness based on female fitness (seed production) may be misleading if plants suffer a reduction in male fitness (number of seeds sired on other plants through pollen). Herbivory affecting attractiveness to pollinators has the potential to strongly influence plant fitness through male function, since visitation rates can often affect male fitness (number of seeds sired by pollen) more strongly than female plant fitness (numbers of seeds set) (Bell 1985). Only a handful of studies have documented male and female plant fitness imultaneously, and at least three have shown that male and female plant fitness are either negatively or only weakly correlated (Bertin 1982; Ennos and Dodson 1987; Schlichting and Devlin 1989; Broyles and Wyatt 1990; Devlin and Ellstrand 1990). Thus, the impact of herbivory on the fitness of hermaphroditic plants requires knowledge of both male and female reproductive success. Second, how plants have evolved to respond to damage from herbivores in allocation patterns to floral resources may be influenced or constrained by floral adaptations

FLORAL CHARACTERS LINK HERBIVORES, POLLINATORS, AND PLANT FITNESS

Our past focus on seed production as a surrogate for total plant fitness may have created a bias in our assessments of the effects of herbivory on plants. This bias may be especially pronounced if male and female plant fitness are differentially affected by damage. I describe the effects of leaf herbivory on several floral characters, including traits associated with male plant fitness. Changes in floral traits caused by foliar herbivory can also affect plant relationships with pollinators. Here, I highlight some understudied, indirect ways in which total plant fitness is affected by leaf herbivory. I then describe how considering these other routes to total plant fitness might contribute to current investigations on the evolution of plant defense and floral traits. Because data are lacking on several important aspects of these relationships, this contribution focuses primarily on new ideas and approaches to determining how herbivores and pollinators together shape plant characters.

More closely related species are more ecologically similar in an experimental test

The relationship between phylogenetic distance and ecological similarity is key to understanding mechanisms of community assembly, a central goal of ecology. The field of community phylogenetics uses phylogenetic information to infer mechanisms of community assembly; we explore, the underlying relationship between phylogenetic similarity and the niche. We combined a field experiment using 32 native plant species with a molecular phylogeny and found that closely related plant species shared similar germination and early survival niches. Species also competed more with close relatives than with distant relatives in field soils; however, in potting soil this pattern reversed, and close relatives might even have more mutalistic relationships than distant relatives in these soils. Our results suggest that niche conservatism (habitat filtering) and species interactions (competition or facilitation) structure community composition, that phylogenetic relationships influence the strength of species’ interactions, and that conserved aspects of plant niches include soil attributes.

Empirical and theoretical challenges in aboveground–belowground ecology

A growing body of evidence shows that aboveground and belowground communities and processes are intrinsically linked, and that feedbacks between these subsystems have important implications for community structure and ecosystem functioning. Almost all studies on this topic have been carried out from an empirical perspective and in specific ecological settings or contexts. Belowground interactions operate at different spatial and temporal scales. Due to the relatively low mobility and high survival of organisms in the soil, plants have longer lasting legacy effects belowground than aboveground. Our current challenge is to understand how aboveground–belowground biotic interactions operate across spatial and temporal scales, and how they depend on, as well as influence, the abiotic environment. Because empirical capacities are too limited to explore all possible combinations of interactions and environmental settings, we explore where and how they can be supported by theoretical approaches to develop testable predictions and to generalise empirical results. We review four key areas where a combined aboveground–belowground approach offers perspectives for enhancing ecological understanding, namely succession, agro-ecosystems, biological invasions and global change impacts on ecosystems. In plant succession, differences in scales between aboveground and belowground biota, as well as between species interactions and ecosystem processes, have important implications for the rate and direction of community change. Aboveground as well as belowground interactions either enhance or reduce rates of plant species replacement. Moreover, the outcomes of the interactions depend on abiotic conditions and plant life history characteristics, which may vary with successional position. We exemplify where translation of the current conceptual succession models into more predictive models can help targeting empirical studies and generalising their results. Then, we discuss how understanding succession may help to enhance managing arable crops, grasslands and invasive plants, as well as provide insights into the effects of global change on community re-organisation and ecosystem processes.

The evolutionary ecology of metacommunities.

Research on the interactions between evolutionary and ecological dynamics has largely focused on local spatial scales and on relatively simple ecological communities. However, recent work demonstrates that dispersal can drastically alter the interplay between ecological and evolutionary dynamics, often in unexpected ways. We argue that a dispersal-centered synthesis of metacommunity ecology and evolution is necessary to make further progress in this important area of research. We demonstrate that such an approach generates several novel outcomes and substantially enhances understanding of both ecological and evolutionary phenomena in three core research areas at the interface of ecology and evolution.