Plant-Insect Interactions (Insects)

At the ecological level, the interactions of plants and their herbivores center upon the primary (nutritional) and secondary (allelochemical) composition of plants or plant parts, and the adaptations of the insect to feeding and/or living on that plant. At the evolutionary level, insect feeding patterns involve population genetics, host race formation, evolutionary divergence, speciation, and historical (phylogenetic) patterns.

ECOLOGICAL ISSUES

The fundamental limitations for insect use of plants as food involve nutrients (nitrogen/protein, water, lipids, and various minerals) as well as various classes of secondary chemical defenses (including alkaloids, cyanogenic glycosides, glucosinolates, terpenoids, pheno-lics, phytoecdysteroids, and polyacetates). The location (“findability”) and utilization (suitability) of plant parts as insect food may depend on phenotypic variation induced by previous herbivores and microbes, as well as a wide array of interactions involving environmental factors such as nutrient availability, light regime, water, temperature, carbon dioxide, and various pollutants. Seasonal (ontogenetic) changes in plant growth, reproduction, and chemical/physical defenses also are important. Natural declines during plant maturation in the concentration of many low-molecular-weight allelochemicals (often called qualitative defenses) are contrasted with other higher molecular weight chemicals (such as tannins, lignins, and fiber; sometimes called quantitative defenses). In leaves of plants, a general pattern of decline in the concentrations of total nitrogen, water, and many qualitative chemical defenses usually accompanies leaf maturation. The phyto-chemical suitability of leaves for insect herbivores (the leaf-chewing guild in particular) also has genetically based biochemical variation. Together these factors affect the physiological and ecological suitability of the plant for supporting herbivore feeding, growth, survival, and reproduction. Specialization by insects is the common theme in most insect-plant interactions, but behavioral or physiological efficiency is not often associated (but see Fig. 1).


HOST-PLANT RESISTANCE AND INSECT COUNTERADAPTATIONS

In natural terrestrial communities, approximately 10% of the annual plant production on average is consumed by herbivores, a percentage that is generally greater than the plant biomass allocated to reproduction. In addition to the well-known defensive structures of thorns, barbs, spines, trichomes, hairiness or fuzziness, and physical toughness, plants possess a large array of chemicals that defend against the herbivore and pathogen enemies. Artificial selection also has produced insect-resistant genotypes and cultivars of crop plants, which has helped reduce the reliance on broad-spectrum synthetic pesticides. Plant breeders have recently been able to use techniques of molecular biology to incorporate new arrays of biochemical or microbial “pesticides” for plant defenses that have not been previously evolved by the plants (but that may occur naturally in the plant environment or even on the leaf surface).
Insects may respond to these secondary plant products physiologically (e.g., by sequestration or enhanced excretion rates), biochemically with resistance (e.g., via target site insensitivity or enzymatic detoxification), or behaviorally (e.g., by reducing exposure or consumption by changes in feeding behavior). Many of these phytochemicals may be used by adapted herbivores that sequester the bioactive compounds in their wings or other body parts where they may serve a protective function from herbivore enemies (such as in distasteful models with aposematic or warning coloration) and often in various insect mimicry complexes.

PLANT DEFENSE AND HERBIVORE OUTBREAK THEORY

An understanding of the full array of potential insect-plant interactions is probably beyond comprehension. The geographic, altitudinal, and seasonal variation in plant chemistry in even a single plant species and the associated responses of insect herbivores (each species with its own geographical and genetic variation) make the task truly daunting. However, out of this complexity, ecologists have attempted to identify general patterns and organizing principles. The development of a series of general explanatory hypotheses or proposed models of insect herbivory, population dynamics, and plant defenses (generated since the 1970s) are not mutually exclusive and have often built upon the theories of their predecessors with details of the historical development of plant defense theory nicely summarized in 1997 by Price, with a phylogenetic/coevolutionary/coadaptation perspective recently provided by Scriber in 2002 and Agrawal in 2006.

Climatic Release

This hypothesis suggests that bad weather, lack of food, or lack of their natural enemies (predators, parasites, or diseases) were the primary insect population regulators. The indirect effects of the climate and abiotic environment as mediated through changes in host-plant nutritional quality will likely be of increased significance in the near future, given increasing concentrations of certain atmospheric gases (e.g., carbon dioxide), acid rain, global warming, and increased pollution.

Plant Stress

This hypothesis suggests that water stress in plants may affect the availability of soluble nitrogen (especially for those in the plant-sucking or sap-feeding guilds). Nitrogen generally limits insect herbivores and population growth rates.

Plant Apparency

This hypothesis was developed following study of insect herbivores on oak trees in England and those on the cabbage family (Cruciferae) in North America. P. P. Feeny noted the divergent patterns of chemical defense used by these two plant types. The tree leaves were composed of relatively high concentrations (2.5-5% dry weight) of compounds believed to be digestibility reducers (tannins, lignins, resins, cellulose, silica). In contrast, herbaceous crucifers (forbs) had low concentrations (usually lower than 1%) of biosyn-thetically “less expensive” toxins (such as mustard oil glycosides or other low-molecular-weight chemicals such as alkaloids, cyanogenic glycosides, and coumaric acids).
Herbivore food was prevalent and predictable (i.e., apparent) in trees and mature plant leaves containing these convergent digestibility reducers, or quantitative defenses or hurdles to herbivores, whereas the food resources for forb-feeding herbivores seemed less predictable, with divergent, qualitative (toxic) barriers in annual plants/herbs and very early immature (i.e., unapparent) plant parts. The “bound-to-be-found” trees were late successional, frequently in pure stands, large, and long-lived, with large amounts of general chemical defenses (effective against specialists as well as generalists) that acted in a dose-dependent (i.e., quantitative) manner. In contrast, the annual plants were short-lived, hidden from enemies in space and in time (unapparent), and defended by small quantities of qualitative allelochemicals such as mustard oils that repel nonspe-cialized insects (but are not effective against adapted herbivores) and that are effective at very low levels (basically not dose dependent). The explanatory value and rigor of the apparency concept has been questioned because of the difficulty in its quantification. Most plants and plant parts have a dynamic continuum of both quantitative and qualitative chemical defenses, as well as phenological changes in the nutritional quality of leaves (as indexed, e.g., by leaf water and total leaf nitrogen concentrations). Tannins were also shown not to be the general dose-dependent, digestibility-reducing chemicals they were originally believed to be. Instead, tannins evoke a wide variety of physiological effects such as increased mortality, decreased consumption rates, histopathological effects in the gut, and elevated metabolic costs for insect herbivores. In 2005, Boege and Marquis reviewed and reemphasized these ontogenetic patterns originally described in 1981 by Scriber and Slansky.

Induced Defenses

This hypothesis arose with the occurrence of phytochemical induction with leaf damage as observed since the late 1970s. Plant-to-plant chemical communications and plant-to-insect parasite/ predators have subsequently been included as multitrophic-level chemical synomones (plant volatiles that benefit both the sender and its receiver). Herbivore-damaged plants have been shown to provide carnivorous enemies of insect herbivores with important volatile chemical cues, detectable from a distance and aid natural enemies in locating suitable herbivore prey.

Resource Availability and plant Vigor for defense against harbivores

A relationship between resource availability and plant defense was noted, as reduced nitrogen availability for plants usually resulted in reduced nitrogen-based defenses (usually toxins), but not necessarily in reduced carbon-based defenses (digestibility reducers). Thus, on nutrient-poor and late-successional sites, inherently slow growth rates of plants may select for more carbon-based herbivore defenses (e.g., resins or phenolics) that could be reduced with fertilization with nitrogen (with corresponding increases in the nutritional value for herbivores). Low carbon conditions (e.g., shade and reduced photosynthesis) may result in slow growth despite high nitrogen, which could then be used for N-based defenses (e.g., alkaloids, cyanogenic glycosides). These hypotheses about the carbon-nutrient balance and resource availability for slow-growing and fast-growing plants received support from many researchers in the 1980s. In many instances, predictions of the apparency, resource availability, and growth-differentiation balance hypotheses are in agreement. For example, trends in the types of chemical defense of early successional plants and late successional plant communities are congruent. However, equally apparent plants in resource-rich and resource-poor environments suggest that the resource availability hypothesis may have greater explanatory power than the apparency concept, because the fast growers in resource-rich environments (nutrients and light) seem to support high herbivory (and may be predisposed to rapidly recyclable defenses such as alkaloids or other toxins) that can contrast with slow growers in the tropics, temperate zone, and arctic communities. A preference of herbivores for fast-growing plants has led to the suggestion that interactions may relate most simply to “plant vigor” (as a general hypothesis) to explain not only persistent differences in plant defenses between species, but also quality differences within a single plant species, genotype, or even individual. These indices of resistance can be induced by her-bivory itself, as well as being constitutive.
In summary, despite the different roles of an overwhelming diversity of secondary plant chemicals, the fundamental limitations on herbivore growth rates seem to relate to the nutritional suitability of the insect food. Different leaf water and leaf nitrogen contents for different plant tissues correlate well with maximum achievable insect growth rates and efficiencies for most guilds and hundreds of different herbivore species. Many biotic and abiotic factors (and their interactions) affect the realized growth performance and fitness for insect herbivores (see below).

Voltinism-Suitability Hypothesis

This hypothesis was developed in 1992 by Scriber and Lederhouse, with the observations that at certain latitudes or in geographically localized cold pockets, seasonal thermal unit constraints (degree days as a resource) can determine whether an additional insect herbivore generation is feasible in any given year, depending on its selection of the most nutritional host-plant species, which varies with the timing of leaf bud break and phenological (seasonal) patterns, which differ at various locations. Thus, abiotic factors have been shown to affect host-plant choice (acceptability) and host-plant suitability for herbivores. High nitrogen and high water content generally reflect the most rapid leaf and cell growth and presumably plant vigor as well. Insect growth performance usually correlates well with these plant quality indices. The range of host plants utilized at a given latitude (or local climatic zone) may be the result of natural selection in relation to these abiotic factors. Thermal constraints for the summer growing season (as in Alaska or in similar localized cold pockets in the continental United States) contrast ecologically with thermally relaxed zones (i.e., where choice of either excellent or poor host-plant species or leaves does not influence the possibility of an extra generation per season). The difficulty in the voltinism-suitability model is that a good host typically is more than just a particular plant species and its allelochemical acceptability, nutritional suitability, and the abiotic thermal regime in which the herbivores are trying to optimize their growth and survival. The biotic community of natural enemies (e.g., enemy-free space as a resource) must also be considered as a critical determinant of the real ecological/ evolutionary suitability of any plant. The relative roles in plant defense played by natural enemies, weather-induced stress, herbivore-induced stress, and various abiotic factors remain complex, generating many unique and dynamic variations on the suitability hypothesis.

SPECIALIZED VS. GENERALIZED HERBIVORES

Among the world’s herbivorous insects, the number of feeding specialist (stenophagous) species dominates generalist species (poly-phagous) for most taxa and feeding guilds (see Slansky and Rodriguez, 1987). Ecological advantages to herbivores of such stenophagy may involve efficient location and use of host plants, timing of critical life stages with budbreak and plant phenology, or enemy avoidance via cryptic matching of the herbivore eggs, larvae, pupae, or adults to plant parts. Mate finding may also be more efficient (e.g., with host races and habitat specificity). As host race populations genetically diverge, and perhaps even develop reproductive isolation, speciation may result.
The evolutionary benefits of host specialization have been presumed to be at a “cost” (e.g., tradeoffs in other performance measures; Fig. 1), but determining the existence or the amount of such evolutionary costs is as difficult as it was for the “feeding specialization/ physiological efficiency” hypothesis at the ecological level (reviewed in 2005 by Scriber). Key innovations (e.g., furanocoumarin-metabolizing enzymes of the cytochrome P-450 gene families) allow circumvention of powerful antibiotic plant defenses for plants over millions of years from basal (ancient) angiosperms to current insect species (Scriber et al., 2007). It is also remarkable that one or two base pair substitutions may enable new detoxification capabilities and therefore open up new host-plant families for use by related herbivores (Mao et al., 2007).
However, not all interactions of insects and plants (herbivores or pollinators) become increasingly specialized: (1) evolutionary “reversals” have shown that specialization is not necessarily an evolutionary “dead end”; (2) homoploid recombinant hybrid speciation has recently been described in several insects, some with new host race affiliations, but some in polyphagous species (temporally isolated from parent species); (3) some taxa oscillate from specialists to generalists in their phylogenetic development; and (4) ecological specialization (strong selection with gene flow) has been recognized as an important process leading to new insect species. All of these points have recently been addressed by topics in Tilmon.

EVOLUTIONARY LEVEL

Coevolutionary or reciprocal changes between plants and insects are the foundation of numerous phytochemical defense theories. However, there is surprisingly little direct evidence that insects select for plant phytochemical defenses. Most insect-plant interactions are diffuse without mutual counteradaptations. They will be, at best, a geographic mosaic with isolated and dynamic hot spots. Additional studies of different geographical populations (with and without herbivore selection pressure), plant and herbivore genetic analyses, phytochemical dynamics in relation to abiotic factors, and historical biogeography all seem to be warranted and critically needed to understand the historical patterns that produced current ones. For example, furanocoumarin cytochrome P-450 detoxification gene family may represent the “key innovation” for multimillion year phylogenetic mechanisms for processing ancient angiosperms (see Scriber et al., 2008) as well as current ecologically significant physiological induction abilities (Li et al., 2007). The ecologically enigmatic problem seems to be that our understanding of both plant resistance and insect counteradapta-tions ultimately depends on the identification of specific molecular pathways and an elucidation of the relative roles of genetic and environmentally induced variation between interactive populations.

INSECT HERBIVORES CAN BENEFIT PLANTS

It has been generally accepted that insect herbivory results in plant tissue damage that is detrimental for plant growth, survival, or reproduction; however, insect herbivory and subsequent frass fall can be beneficial for plant and ecosystem productivity. Although many crops and other plants can sustain 30-40% defoliation with little obvious impact on production, such feeding, if repeated annually or if on flowers and/or seeds, can be much more damaging. Insects provide direct nutritional benefit to some plants. Carnivorous plants that “digest” insects and use chemicals from their bodies for nutrients (especially nitrogen) are represented by many species, including pitcher plants, bladderworts, Venus flytraps, and sundews. Carnivorous plants are often found in soils that are low in available nitrogen, which may have been an important selection pressure for the evolution of these botanical life history traits.

SUMMARY

Insect-plant interactions involve a wide array of biotic and abiotic environmental influences as well as geographical and temporal variations built upon the diverse genetic foundations and inducible phenotypic plasticity of species, populations, and individuals. It, therefore, seems very appealing when theories arise that seem to have predictive power for these complex interactions. Such complexity is amplified when the variety of insect feeding guilds and variations in response of different plant parts and tissues are considered.
Larva of Papilio troilus, a swallowtail butterfly that specializes on only 1-2 species of the Lauraceae plant family, has the highest feeding efficiency and fastest growth rates of any Lepidopteran tree feeder known (including several other specialized species; Scriber, 2005). This species grows at two to three times the efficiency and two to five times the rate of the generalist sister species, P. glaucus on the same spicebush (Lindera benzoin) leaves. This species, therefore, provides strong support for the " feeding specialization/physiological efficiency hypothesis," and may exemplify the expected ecological/evolutionary "trade-offs" for specialists; it lacks the cytochrome P-450 furanocoumarin genes for metabolizing Rutaceae and other families used by the P. glaucus species group (Lauraceae lack furanocoumarins). Whether or not this inability represents an evolutionary loss for the specialized P. troilus, this species is chemically constrained (oviposition preference and larval performance); currently unable to feed on plants in any other family tested in North America and Australia, and unwilling to oviposit on anything but a few Lauraceae hosts (Scriber, 2005).
FIGURE 1 Larva of Papilio troilus, a swallowtail butterfly that specializes on only 1-2 species of the Lauraceae plant family, has the highest feeding efficiency and fastest growth rates of any Lepidopteran tree feeder known (including several other specialized species; Scriber, 2005). This species grows at two to three times the efficiency and two to five times the rate of the generalist sister species, P. glaucus on the same spicebush (Lindera benzoin) leaves. This species, therefore, provides strong support for the ” feeding specialization/physiological efficiency hypothesis,” and may exemplify the expected ecological/evolutionary “trade-offs” for specialists; it lacks the cytochrome P-450 furanocoumarin genes for metabolizing Rutaceae and other families used by the P. glaucus species group (Lauraceae lack furanocoumarins). Whether or not this inability represents an evolutionary loss for the specialized P. troilus, this species is chemically constrained (oviposition preference and larval performance); currently unable to feed on plants in any other family tested in North America and Australia, and unwilling to oviposit on anything but a few Lauraceae hosts (Scriber, 2005).
The relationships between normal phenological changes in plant leaf (or part) composition throughout the growing season, carbon-nutrient stress, mineral nutrition, plant vigor, phytochemical induction of resistance in damaged/diseased leaves, increases in certain atmospheric gases, global warming, metabolism of different forms of carbon, and annual vs. perennial growth forms need coordinated biocomplexity studies. With such knowledge, the suitability of such plant tissues for insect and other herbivores (or the resistance of plants to their enemies) may become much more predictable, both in ecological and evolutionary time.

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