Phytophagous Insects

Phytophagous insects are generally considered to be those that feed on green plants. They include species that attack roots, JL. stems, leaves, flowers, and fruits, either as larvae or as adults or in both stages. Leaf feeders may be external (exophytic) or they may mine the tissues, sometimes even specializing on a particular cell type. Typically nectar and pollen feeders are not included. “Phytophagous” is often synonymous with “herbivorous,” although the latter term is sometimes restricted to those species feeding on herbs (i.e., herbaceous plants). Commonly, species that use only one plant genus or species are called monophagous and species that use plants within a tribe or family are called oligophagous. The term stenophagous is less commonly used and includes both of these. Polyphagous species are those that use plants in several to many plant families.

DIVERSITY

Phytophagous insects are highly diverse and the total species number is at least 500,000. This represents about 25% of known multicellular animals. There are phytophagous insect species in the majority of insect orders, including Orthoptera, Lepidoptera, Coleoptera, Heteroptera, Hymenoptera, and Diptera but there are very large differences in numbers of species in the different groups (Table I ). All green plants are eaten by one or more species of phytophagous insects.
Major differences occur among orders in the ways in which hosts are selected and the life forms that use plants. Thus, grasshoppers usually lay eggs in the soil so that the nymphal stages must select the plant resource. In the Orthoptera and Hemiptera, which are hemime-tabolous, the nymphal and adult stages generally have similar feeding habits. By contrast, among Lepidoptera and Hymenoptera adults commonly feed on pollen or nectar while only the larvae are phytophagous, and among Coleoptera the larvae and adults of leaf beetles have similar habits, while larvae of wood borers often have adults with different feeding habits. Thus, there is a dichotomy (with some notable exceptions) between species in which the mother chooses for her offspring and species in which all stages are independent.
The great diversity of insects feeding on plants is matched by a remarkable diversity of lifestyles, mouthparts and gut morphological adaptations to the food eaten, cuticular morphology and coloration adapted for crypsis or aposematism, and behavioral adaptations for use of particular plants and escape from natural enemies. Many of the remarkable pictures of insects in popular journals involve surprisingly effective visual and behavioral crypsis.
Insects feeding on plants had their origin early in the history of life on land, with all the major orders that feed on plants today being present 300 million years ago (with the possible exception of Lepidoptera). This means that partitioning of food resources had occurred then, because there were spore feeders, sap suckers, and gall makers as well as miners and external feeders. This can be determined from information provided by fossils of insects and damaged plants and fossilized remains of insect feces. The diversity of insect mouthparts required for the different feeding guilds was established well before the appearance of angiosperms 200 mya, but diversification of families, genera, and species has continued unabated ever since. The diversification is now known to be clearly related to angiosperm diversity and believed to be related largely to the diversity of plant secondary metabolites. These chemicals provide the signals for acceptance or rejection of potential host plants.

Mouthparts and Feeding

Although each of the major phytophagous orders of insects has distinctive biting and chewing or sucking mouthparts, the structures are highly diversified to handle every type of physical problem. For example, caterpillar species feeding on different plants can often be recognized by their mandibular morphology, and species feeding on physically similar plant parts tend to have similar morphology, whether they have a common ancestry or not. Among grasshoppers (Acrididae),

those that feed only on grasses have highly specialized mandibles with incisor regions for snipping through the tough parallel veins and molar regions for grinding the tissue. These highly characteristic mandibles have evolved independently at least eight times during the evolution of grasshoppers. It is probable that the details of mouthpart structure evolve quite quickly to suit changing diet, because it has been found in certain seed-sucking bugs (e.g., Jadera) that beak length has evolved to suit different fruit sizes within the past 100 years. Such rapid evolution may reflect the need to process food efficiently to maximize growth as well as the need to ingest food very rapidly to minimize predation risk.
Unless they utilize such structures as seeds and pollen, most phytophagous insects deal with the low protein levels characteristic of much plant tissue by eating relatively large amounts, and the gut throughput rates are high, with food in some cases taking only a couple of hours to pass through the digestive system. Some supplement their diets with carnivory or use symbionts to upgrade the levels of essential amino acids. Aphids, for example, which feed on phloem, tend to be particularly short of certain essential amino acids such as tryptophan, and their symbiotic bacteria commonly have multiple copies of genes involved in making tryptophan, so that the aphid obtains its requirements with the help of the symbionts.
Unlike many vertebrate herbivores, insects that feed on plant tissues often do not make nutritional use of the cellulose, which makes up a large proportion of plant bulk. This may partly reflect the fact that for phytophagous insects, protein is more likely to be limiting than carbohydrate. As heterotherms (animals whose body temperature varies with that of the environment) they are not concerned with the use of diets that are high in calories for maintenance of body temperature. Those species that do use cellulose, such as beetles feeding on wood or termites feeding on dead and decaying plants, often have symbionts that break down the cellulose, releasing non-protein amino acids as well as sugars. It is possible that the digestion of cellulose in these cases is a mechanism for releasing nonprotein amino acids that are bound to cellulose but that can be converted to useful amino acids for the insects by the resident symbionts.
Apart from the need to obtain sufficient quantities of major nutrients such as protein, insects (like other animals) often require nutrients in suitable ratios. For example, the proportions of protein and carbohydrate required for maximal growth vary among taxa; if a particular resource is limited in one respect the balance can be improved behav-iorally. Thus, individual insects with a choice of high-protein/low-carbohydrate food and low-protein/high-carbohydrate food can eat a mixture of both. Studies indicate that species in different taxonomic groups are able to select among the foods available to optimize the balance ingested. This ability depends on a variety of mechanisms, including nutrient feedbacks that influence taste receptor sensitivity to sugars and amino acids, a tendency to move away from a food that has recently proved unsuitable, and a tendency to select foods with new and different flavors following experience on an unsuitable food. In addition, it has been demonstrated that insects can learn to avoid unsuitable food and to associate particular odors with high-quality foods.

THE IMPORTANCE OF PLANT SECONDARY METABOLITES

The great diversity of secondary metabolites in plants profoundly affects the behavior of phytophagous insects and, thus, the evolution of that behavior. These compounds may be repellent, or deterrent after contact. In addition, the deleterious postingestive effects of them enable insects to learn to reject a plant. Such food aversion learning has been demonstrated particularly in grasshoppers.
Many plant secondary metabolites serve as relatively nonspecific attractants or feeding stimulants for insects that feed on plants, although more commonly one or several particular compounds in a plant species serve as highly specific attractants or stimulants for feeding/oviposi-tion by insects adapted to that plant. Thus, specialist phytophagous insects generally have a genetic predisposition to accept plants with a particular chemical or suite of chemicals present, the so-called sign stimuli; indeed, the sign stimuli may act as valuable signals in the sense of improving the speed of decision-making and discrimination by these insects. Some examples of sign stimuli are shown in Table II .
Apart from Orthoptera (specifically grasshoppers), the majority of phytophagous insect species tend to be specialists. That is, they feed on just a few species, genera, or tribes of plants. It is common among Lepidoptera (moths and butterflies), for example, to find species that feed on plants in one family, one tribe, one genus, or one species of plant. It appears that the degree of specialization is related to the occurrence of one or a few chemicals that characterize that plant group. In addition, the narrower the host range, the more likely it is that nonhost chemicals will repel or deter the insects at relatively low concentrations. Many of these chemicals that reduce feeding or oviposition behavior are not noxious if ingested, suggesting that their role in these cases is more as signals of nonhosts than as signals of toxicity in specifically evolved plant defenses. Nonetheless, there are situations in which plants probably evolved high concentrations of particular chemicals in response to the attack of insects. Insects, over time, would be likely to evolve countermeasures. Thus one can envisage, as many have done, that a chemical arms race between plants and phytophagous insects has occurred (and is occurring).
Diet breadth variation occurs in all phytophagous insect orders, and there is evidence from molecular and other studies that evolution of diet breadth can occur in either direction. What drives these changes has been a subject of much controversy. Included in the hypotheses are the following: arms race coevolution in which specialists are in some way more successful, sequential evolution of insects in which species benefit from the use of specific plant signals to improve behavioral efficiency, adoption of specific plant hosts from which specialists may sequester high levels of particular protective chemicals, and the selection pressure of parasites and predators that involve adoption of limited host-plant species as a means of better avoiding attack (e.g., by enhanced visual or chemical crypsis).

The study of host-plant selection by phytophagous insects has been important in theories of resource use and whether it should be flexible in ecological or evolutionary time. For example, a change in host use may involve a change in specificity (how many different resources are acceptable) or a change in preference (which of a limited number of available resources is ranked highest). A change in specificity could result from a simple change in gustatory or olfactory sensitivity to many plant secondary metabolites or a change in the central nervous system affecting the relative importance of negative inputs from chemoreceptors. A change in preference, however, probably involves a change in receptor conformation or proportions of receptors with different conformations, at the level of the sensillum.

VARIATION IN HOST USE

Advances in how evolutionary changes occur or have occurred are being studied by examining genetic variation currently seen within populations of particular species, geographic variation that occurs in host specificity or preference, and historical changes in host use together with the physiological mechanisms underlying them. Experiential change can influence host preference, in turn altering the nature of selection pressure on those individuals and their offspring.
Host shifts or increases in host range have provided models of evolutionary change including the study of sympatric speciation, whereby populations of an insect species become associated with different hosts. Because many species mate on or near their hosts, gene flow between populations using different hosts drops and speciation becomes possible. An example of this kind of divergence is with the apple maggot Rhagoletis pomonella in North America. Some populations moved from the ancestral Crataegus to apple and, currently, populations are diverging and evolving additional differences.
The interaction of phytophagous insects and plants is greatly influenced by predators and parasites. This is because they are major mortality factors for the phytophagous insects and yet use the plants themselves for sources of nectar and places to shelter, as well as places where they find their prey and hosts. In many cases, they are attracted to the odors of plants that are being attacked by plant-feeding species. The phytophagous insects that can remain visually or chemically cryptic by being specialists, or sequester plant toxins and become warn-ingly colored, will be selected for by these natural enemies.

AGRICULTURE

The study of phytophagous insects has been very important in agriculture. Probably from ancient times, humans have selected varieties of crop plants that are minimally attacked by insects, and in the last 100 years breeding programs have been important in specifically increasing plant resistance. For example, resistance in rice to the rice brown planthopper (Nilaparvata lugens) and resistance in wheat to the greenbug (Schizaphis graminum) have resulted from dedicated research effort. Today, genes that express resistance factors against particular insect pests are inserted into some crops. For example, a toxic protein from the insect disease bacterium Bacillus thuringiensis can be produced in plants genetically modified by introduction of the bacterial gene.
Research in all areas of the biology of phytophagous insects has found application in agriculture. For example, behavioral studies of attractants has led to the use of traps for specific pests, and the study of antifeedants has had use in development of such materials in crop protection. Plant resistance is sometimes indirect, with plants expressing characteristics that favor natural enemies of the phytophagous species. For example, some crop plant varieties have hairs distributed at such densities that the parasitoids of pest whiteflies are slowed down in their running on a plant to a speed that improves host recognition. In other crops, surfaces lacking a wax bloom enable small predators to run more easily and thus efficiently find small caterpillars.