Physiological and ecological constraints play key roles in the evolution of plant growth patterns, especially in relation to defenses against herbivores. Phenotypic and life history theories are unified within the growth-differentiation balance (GDB) framework, forming an integrated system of theories explaining and predicting patterns of plant defense and competitive interactions in ecological and evolutionary time. Plant activity at the cellular level can be classified as growth (cell division and enlargement) of differentiation (chemical and morphological changes leading to cell maturation and specialization). The GDB hypothesis of plant defense is premised upon a physiological trade-off between growth and differentiation processes. The trade-off between growth and defense exists because secondary metabolism and structural reinforcement are physiologically constrained in dividing and enlarging cells, and because they divert resources from the production of new leaf area. Hence the dilemma of plants: Th...

https://www.jstor.org/stable/pdfplus/2830650.pdf

The dilemma of plants: To grow or defend.

To curb the future economic and environmental impacts of invasive exotic species, we need to understand the mechanisms behind exotic invasions. One commonly accepted mechanism for exotic plant invasions is the enemy release hypothesis (ERH), which states that plant species, on introduction to an exotic region, experience a decrease in regulation by herbivores and other natural enemies, resulting in a rapid increase in distribution and abundance. The success of classical biological control has been used as support for ERH, but this observational evidence does not directly test ERH, and the more experimental evidence is equivocal. Competitive release through greater generalist enemy impact on natives seems to be an important but understudied mechanism of enemy release, but there is a serious need for experiments involving exclusion of natural enemies in invaded plant communities. With a clearer understanding of the role of enemy release in exotic plant invasions, we can begin to build a comprehensive predictive model of exotic plant invasions.

https://www.cell.com/trends/ecology-evolution/pdf/S0169-5347(02)02499-0.pdf

Exotic plant invasions and the enemy release hypothesis

Host plant quality is a key determinant of the fecundity of herbivorous insects. Components of host plant quality (such as carbon, nitrogen, and defensive metabolites) directly affect potential and achieved herbivore fecundity. The responses of insect herbivores to changes in host plant quality vary within and between feeding guilds. Host plant quality also affects insect reproductive strategies: Egg size and quality, the allocation of resources to eggs, and the choice of oviposition sites may all be influenced by plant quality, as may egg or embryo resorption on poor-quality hosts. Many insect herbivores change the quality of their host plants, affecting both inter- and intraspecific interactions. Higher-trophic level interactions, such as the performance of predators and parasitoids, may also be affected by host plant quality. We conclude that host plant quality affects the fecundity of herbivorous insects at both the individual and the population scale.

Host plant quality and fecundity in herbivorous insects

Half of all insect species are dependent on living plant tissues, consuming about 10% of plant annual production in natural habitats and an even greater percentage in agricultural systems, despite sophisticated control measures. Plants are generally remarkably well-protected against insect attack, with the result that most insects are highly specialized feeders. The mechanisms underlying plant resistance to invading herbivores on the one side, and insect food specialization on the other, are the main subjects of this book. For insects these include food-plant selection and the complex sensory processes involved, with their implications for learning and nutritional physiology, as well as the endocrinological spects of life cycle synchronization with host plant phenology. In the case of plants exposed to insect herbivores, they include the activation of defence systems in order to minimize damage, as well as the emission of chemical signals that may attract natural enemies of the invading herbivores and maybe exploited by neighbouring plants that mount defences as well.

Insect-plant biology

While ecologists involved in management or policy often are advised to learn to deal with uncertainty, there are a number of components of global environmental change of which we are certain–certain that they are going on, and certain that they are human—caused. Some of these are largely ecological changes, and all have important ecological consequences. Three of the well—documented global changes are: increasing concentrations of carbon dioxide in the atmosphere; alterations in the biogeochemistry of the global nitrogen cycle; and ongoing land use/land cover change. Human activity–now primarily fossil fuel combustion– has increased carbon dioxide concentrations from °280 to 355 mL/L since 1800; the increase is unique, at least in the past 160 000 yr, and several lines of evidence demonstrate unequivocally that it is human—caused. This increase is likely to have climatic consequences–and certainly it has direct effects on biota in all Earth's terrestrial ecosystems. The global nitrogen cycle has been altered by human activity to such an extent that more nitrogen is fixed annually by humanity (primarily for nitrogen fertilizer, also by legume crops and as a by product of fossil fuel combustion) than by all natural pathways combined. This added nitrogen alters the chemistry of the atmosphere and of aquatic ecosystems, contributes to eutrophiction of the biosphere, and has substantial regional effects on biological diversity in the most affected areas. Finally, human land use/land cover change has transformed one—their to one—half of Earth's ice—free surface. This in and of itself probably represents the most important component of global change now and will for some decades to come; it has profound effects on biological diversity on land and on ecosystems downwind and downstream of affected areas. Overall, any clear dichotomy between pristine ecosystems and human—altered areas that may have existed in the past has vanished, and ecological research should account for this reality. These three and other equally certain components of global environmental change are the primary causes of anticipated changes in climate, and of ongoing losses of biological diversity. They are caused in turn by the extraordinary growth in size and resource use of the human population. On a broad scale, there is little uncertainty about any of these components of change or their causes. However, much of the public believes the causes–even the existence–of global change to be uncertain and contentious topics. By speaking out effectively, we can help to shift the focus of public discussion towards what can and should be done about global environmental change.

https://www.jstor.org/stable/pdfplus/1941591.pdf

Beyond Global Warming: Ecology and Global Change

Little is known about the effects of enriched CO(2) atmospheres, which may exist in the next century, on natural plant-insect herbivore interactions. Larvae of a specialist insect herbivore, Junonia coenia (Lepidoptera: Nymphalidae), were reared on one of its host plants, Plantago lanceolata (Plantaginaceae), grown in either current low (350 parts per million) or high (700 ppm) CO(2) environments. Those larvae raised on high-CO(2) foliage grew more slowly and experienced greater mortality, especially in early instars, than those raised on low-CO(2) foliage. Poor larval performance on high-CO(2) foliage was probably due to the reduced foliar water and nitrogen concentrations of those plants and not to changes in the concentration of the defensive compounds, iridoid glycosides. Adult pupal weight and female fecundity were not affected by the CO(2) environment of the host plant. These results indicate that interactions between plants and herbivorous insects will be modified under the predicted CO(2) conditions of the 21st century.

http://science.sciencemag.org/content/sci/243/4895/1198.full.pdf

The effects of enriched carbon dioxide atmospheres on plant--insect herbivore interactions.

Plant performance and chemistry may vary due to a variety of factors, such as plant genotype, environmental conditions, presence of herbivores, timing of herbivory, and species of herbivore. The relative importance of these factors, and how the plants respond to them, may affect the dynamics of the plant population, as well as the insect herbivores feeding on those plants. To understand the relative importance of some of these factors on plant performance and chemistry, we used Plantago lanceolata L. (Plantagina- ceae). In an experimental garden at Binghamton, New York, we examined the effects of plant age, plant genotype, and herbivory by generalist or specialist caterpillars on P. lan- ceolata. There were two parts to this experiment. In the first, we examined variation in nutritional quality (nitrogen) and defensive chemistry (the iridoid glycosides aucubin and catalpol) as a consequence of plant age, plant genotype, and leaf age class. We compared these parameters for a set of four pairs of plants of each of five genotypes that were not exposed to herbivores, and were harvested in early July (control-start plants) with another set harvested 6 wk later in mid-August (control-end plants). The older plants harvested in August (control-end plants) had concentrations of aucubin, catalpol, total iridoid glycosides, and nitrogen approximately one-half that of plants harvested 6 wk earlier. Leaf age affected all of these variables, and plant genotype influenced the iridoid glycoside variables but not the nitrogen concentration. Overall, leaf age explained twice as much of the variation in iridoid glycosides as did plant age, which accounted for twice as much variation as did plant genotype. The second part of the experiment compared the effects of herbivory, genotype, and leaf age on plant performance (leaf biomass, scape (flower stalk) biomass, and total biomass) and chemistry (nitrogen, protein, and iridoid glycoside concentration). We compared these measures for a set of four pairs of replicate plants of each of five genotypes, exposed to one of three herbivory treatments: no herbivory, herbivory by specialist caterpillars, and herbivory by generalist caterpillars. The results of this experiment showed that herbivory had little effect on plant performance, and there was no difference due to herbivory by the specialist Junonia coenia Hibner (Nymphalidae), compared to the generalist Spilosoma congrua Wlk. (Arctiidae). However, plant chemistry was significantly affected by herbivory. Herbivory by both caterpillar species induced iridoid glycosides and resulted in an increased concentration of catalpol and an increase in the proportion of catalpol relative to total iridoid glycosides in those plants exposed to herbivores compared to controls. In addition, plants exposed to specialist caterpillars had higher concentrations of catalpol and a higher proportion of total iridoids that was catalpol than those exposed to generalist caterpillars. Overall, in this experiment, leaf age explained three times as much of the variation in iridoid glycosides as did plant genotype and herbivory. The results of the two parts of this experiment show that iridoid glycoside concentration in P. lanceolata leaves decreases over time, and that exposure to herbivores induces increased concentrations of iridoid glycosides.

Effects of plant age, genotype, and herbivory on plantago performance and chemistry'

The majority of insect species consume plants, many of which produce chemical toxins that defend their tissues from attack. How then are herbivorous insects able to develop on a potentially poisonous diet? While numerous studies have focused on the biochemical counter-adaptations to plant toxins rooted in the insect genome, a separate body of research has recently emphasized the role of microbial symbionts, particularly those inhabiting the gut, in plant-insect interactions. Here we outline the "gut microbial facilitation hypothesis," which proposes that variation among herbivores in their ability to consume chemically defended plants can be due, in part, to variation in their associated microbial communities. More specifically, different microbes may be differentially able to detoxify compounds toxic to the insect, or be differentially resistant to the potential antimicrobial effects of some compounds. Studies directly addressing this hypothesis are relatively few, but microbe-plant allelochemical interactions have been frequently documented from non-insect systems-such as soil and the human gut-and thus illustrate their potential importance for insect herbivory. We discuss the implications of this hypothesis for insect diversification and coevolution with plants; for example, evolutionary transitions to host plant groups with novel allelochemicals could be initiated by heritable changes to the insect microbiome. Furthermore, the ecological implications extend beyond the plant and insect herbivore to higher trophic levels. Although the hidden nature of microbes and plant allelochemicals make their interactions difficult to detect, recent molecular and experimental techniques should enable research on this neglected, but likely important, aspect of insect-plant biology.

Gut microbes may facilitate insect herbivory of chemically defended plants

We examined the effects of a set of four biosynthetically related iridoid glycosides, aucubin, catalpol, loganin, and asperuloside, on larvae of a generalist,Lymantria dispar (Lymantriidae), the gypsy moth, and an adapted specialist, the buckeye,Junonia coenia (Nymphalidae). In general,L. dispar grew and survived significantly less well on artificial diets containing iridoid glycoside, compared to a control diet without iridoid glycosides. In choice tests, previous exposure to a diet containing iridoid glycosides caused larvae subsequently to prefer iridoid glycoside-containing diets even though they were detrimental to growth and survival. In contrast,J coenia larvae grew and survived better on diets with aucubin and catalpol, the two iridoid glycosides found in the host plantPlantago lanceolata (Plantaginaceae), than on diets with no iridoid glycoside or with loganin and asperuloside. The results of choice tests of diets with and without iridoid glycosides and between diets with different iridoid glycosides reflected these differences as well. These results are discussed in terms of (1) differences between generalists and specialists in their response to qualitative variation in plant allelochemical content, (2) the induction of feeding preferences, and (3) the evolution of qualitative allelochemical variation as a plant defense.

Response of generalist and specialist insects to qualitative allelochemical variation.

Selective pressures from host plant chemistry and natural enemies may contribute independently to driving insect herbivores towards narrow diet breadths. We used the specialist caterpillar, Junonia coenia (Nymphalidae), which sequesters defensive compounds, iridoid glycosides, from its host plants to assess the effects of plant chemistry and sequestration on the larval immune response. A series of experiments using implanted glass beads to challenge immune function showed that larvae feeding on diets with high concentrations of iridoid glycosides are more likely to have their immune response compromised than those feeding on diets low in these compounds. These results indicate that larvae feeding on plants with high concentrations of toxins might be more poorly defended against parasitoids, while at the same time being better defended against predators, suggesting that predators and parasitoids can exert different selective pressures on the evolution of herbivore diet breadth.

/pdf/immunological-cost-of-chemical-defence-and-the-evolution-of-i4iouqq86s.pdf

M. Deane Bowers

Papers

The effects of enriched carbon dioxide atmospheres on plant--insect herbivore interactions.

Effects of plant age, genotype, and herbivory on plantago performance and chemistry'

Gut microbes may facilitate insect herbivory of chemically defended plants

Response of generalist and specialist insects to qualitative allelochemical variation.

Immunological cost of chemical defence and the evolution of herbivore diet breadth.