Introduction

One of the most important fields of recent ecological inquiry has been that of plant-herbivore interactions. There are several reasons for the rapid developments in this field. (i) Herbivores are ecologically important. Globally it is estimated that herbivores consume from 7% (Pimentel 1988) to 18% (Cyr and Pace 1993) of leaf area in terrestrial ecosystems and from 30% to 79% of plant net production in aquatic ecosystems (Cyr and Pace 1993). (ii) Caught between "plants and predators" (Olff et al. 1999), herbivores must deal with the chemical and morphological defenses of plants while simultaneously defending themselves from their own predators. The study of plants and their herbivores leads to new understandings of interactions involving more than two trophic levels. (iii) Herbivores have been, and still are, important to the evolution of plants and other animals. Through their activities, herbivores have evolutionarily shaped the plant community, partially determining the diversity, abundance, and life form of plants. This, in turn, affects what other types of animals are present and influences ecosystem processes such as energy flow and nutrient cycling. (iv) Herbivores are economically important. In agricultural systems, herbivores may often consume 50% of net productivity and therefore depress yield. Under the worst of circumstances agricultural crops may be wiped out. Furthermore, the animals we raise for food and other products are almost all herbivores themselves. Thus a better understanding of plant-herbivore relationships is crucial to the success of our agricultural endeavors. (v) Plant-herbivore interactions provide unique opportunities to investigate basic ecological and evolutionary processes such as coevolution, food webs, plant chemistry, animal foraging, competition, and ecosystem processes such as nutrient cycling.

The relationship between plant "secondary compounds" and herbivore-plant relationships was first outlined by Fraenkel (1959). Since the compounds under discussion are not part of the primary metabolism of plants, they were and still are known as "secondary compounds." Fraenkel suggested that plant secondary compounds have evolved as defenses against herbivores and herbivores have strongly affected plant evolution. Since the publication of his paper research has exploded in the fields of plant-herbivore relationships and chemical ecology. Ecologists such as Harborne (1993, 1997) and Hartley and Jones (1997) accept that the major functions of plant secondary compounds are as defenses against herbivores. Skeptics, such as Smith and Smith (2001) have asserted that there is little evidence that plants evolved secondary compounds for a defensive purpose. However, as Hartley and Jones (1997) put it, although "we are still not sure why plants have such a huge array of secondary compounds or how this came to be, we do know that these chemicals are important in keeping the world green."

The basic theory, which has guided ecological thinking concerning plant-herbivore interactions, was set forth by Ehrlich and Raven (1964). At that time the great diversity of chemical compounds produced by plants was already widely recognized. Many chemists and botanists referred to these compounds as waste products of plant metabolism, lacking any adaptive value. Ehrlich and Raven, by contrast, asserted that secondary compounds were the product of coevolution with herbivores. Plants that produced secondary chemicals made their tissues unpalatable or toxic, lowered herbivore damage, and had a selective advantage since they could devote more energy to competition and reproduction. If less energy were lost to herbivores, then plants would grow more rapidly and enjoy competitive success. Any genes that allowed the plant to produce these chemicals would spread throughout the population. By the same argument, herbivores could be expected to adapt to plant defenses. Again, an herbivore that evolved a detoxification enzyme, or other adaptation to allow it to feed on protected plants, would enjoy competitive success compared to individuals unable to feed on these plants. As discussed previously, some herbivores have turned defensive chemicals to their own advantage. That is, by modifying and storing plant toxins, the herbivore itself became unpalatable to predators. Thus an herbivore, which evolved an adaptation for feeding on a chemically defended plant, could potentially enjoy both competitive success and protection from its own predators.

Faced with an increasing number of herbivores adapted to a particular chemical defense, plants have, according to Ehrlich and Raven's theory, counter-adapted by producing additional defensive chemicals. This process of evolution and counter-evolution of chemical defenses is often referred to as the "evolutionary arms race" and is thought to have helped produce the great diversity of both angiosperms and the insects that feed upon them. Taken together, land plants (particularly angiosperms) and insects make up more than half of all known terrestrial species on earth (excluding microorganisms).

The Ehrlich-Raven theory is based on the following assumptions:

1 Herbivore activity is harmful to plants. This would seem to be obvious, but this assumption cannot be accepted unequivocally.

2 Plants are able to evolve defenses that are effective in deterring feeding by herbivores. Note that, although the Ehrlich-Raven theory stresses herbivores, these plant chemical defenses could just as easily have been evolved to defend plants against attacks by fungi, bacteria, and other microorganisms. Those chemicals that evolved as antifungal defenses, for example, might also be effective against other microorganisms or herbivores.

3 Herbivore feeding activities, growth, reproduction, and evolution have been guided by the ability of plants to defend themselves, both physically and chemically.

4 Although there exist herbivores that feed on plants of many species, genera, or families with seemingly little regard for the identity of the plants, these "generalists" are actually much more selective than they appear. Generalists engage in a broad "sampling program" in which they eat small amounts of material from many plant species. The majority of what they consume, however, comes from a much smaller species list (Rockwood 1976, 1977, Rockwood and Glander 1979). The careful manner in which generalists eat is thought to be consistent with the central importance of secondary compounds in plant-herbivore interactions.

5 The majority of herbivore species are not generalists, but are specialists, feeding on just one plant species, one plant genus, or perhaps one plant family (for example the Cruciferae or mustard family). Such specialization is consistent with the idea that an herbivore that evolves a way of feeding on a particular plant type eventually loses the ability to feed on other plants.

For example, one simple hypothesis, based on these assumptions, is that plants with few specialized chemical defenses will be fed upon primarily by generalist herbivores, while plants with specialized, complex chemical defenses will by fed upon mostly by specialist herbivores. When Berenbaum (1981) examined the chemical defenses in the Apiaceae (the carrot family) she found some species defended by a relatively simple phenolic (coumarin), some by linear furanocoumarins, and some by sophisticated angular furano-coumarins. As the defenses became more complex the herbivores feeding on the plants changed from mostly generalists (defined as feeding on more than three plant families), to mostly specialists (those feeding on only 1-3 genera).

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