Host Seeking, for Plants (Insects)

Plant-feeding insects may find their hosts by seeking appropriate habitats, by increases in activity that maximize the chances of encountering a plant, by completely random activity in combination with strong arrestant properties of the host, or by attraction to a plant from a distance by smell or vision or both. Often generalized plant odors are attractive, but commonly host-specific odors can be distinguished by specialist insects, and recently it has become known that most such insects are highly sensitive to one or a few host odors that are particularly attractive. Host color and shape can be important in plants with characteristic visual features and in insects that are day flying, although visually mediated responses are usually relatively unspecific.

FINDING HOSTS INDIRECTLY

Habitat location appears to be the first step for a number of species, although it is difficult to prove in practice. For example, grass-feeding grasshoppers are attracted to open habitats where grasses are generally abundant, but there are likely to be other reasons for this behavior. The pierid butterfly Euchloe belemia, however, is attracted to patches of thorn plants where, typically, its small host plants grow most densely.
Some small insects that find their hosts within fairly short distances may simply rely on increases in activity and turning behavior when they detect the appropriate odor, so that they are more likely to encounter their hosts. Among chrysomelid beetles, some engage in random movements that show little change with level of host odor; crucifer flea beetles in the genus Phyllotreta, for example, move randomly within and between host patches. It has been shown mathematically that random activity is important in overall efficiency of search strategies because, under many circumstances and especially when host signals are weak and plant suitability variable, exploratory search enhances the likelihood that an individual will contact the better plants.

USING ODORS TO FIND HOSTS

There are many examples of insects being attracted to the odors of their host plants, both by flying and by walking or crawling. Generalists such as the moths Trichoplusia ni and Heliothis vires-cens and the desert locust Schistocerca gregaria fly or walk upwind in wind tunnels toward general green plant odors, and there are examples among all orders of specialist herbivores being attracted to chemicals arising specifically from their host plants (Table I).

Because of air turbulence, concentration gradients that an insect might follow do not generally exist, except within centimeters of the plant. Instead, there are pockets of odor-carrying air that are carried downwind in a rough plume, and an insect encounters and perceives an irregular series of these pockets. An insect usually responds in two stages. First, there is “arousal,” preparing the insect to respond to some further stimulus. Then orientation occurs, either on the substrate or in the air. Usually the orientation response is a response to the wind, with the insect turning upwind, and this is termed an odor-induced upwind (positive) anemotaxis. Among flying moths, this has been demonstrated clearly in wind tunnels, and the same kind of response may be seen when males fly upwind toward the source of female pheromone.
Once airborne, the insect needs to monitor its ground speed, so that it can increase its airspeed if the wind is strong. To do this it uses visual information (i.e., image movement across the eyes from front to back). If the wind is too strong and the insect is unable to keep the images flowing, it turns and flies downwind or lands. The use of visual images by a flying or swimming insect to maintain orientation to a current flow is called an optomotor reaction. It enables the insect to maintain an orientation at any angle to the wind, not just directly up- or downwind. If the insect is unable to see the pattern of objects on the ground, it cannot orient. As well as generally flying upwind in response to a particular odor, many moths and beetles follow zigzag flight paths. This behavior, which evidently is programmed in the insect central nervous system, has the possible function of increasing the chances of encountering a pocket of odor.
Walking insects also show odor-induced anemotaxis. This has been demonstrated in locust nymphs, certain beetles, and aphids, for example, where individuals walk upwind in response to host odors.
In a number of smaller insects such as phytophagous flies, the odor-induced anemotaxis is slightly different; this is well studied are the onion maggot, Delia antiqua, and the cabbage maggot, D. radicum. In these species, after perception of the host odor, an individual fly turns into the wind and makes short flights. After landing, and again detecting the odor, it reorients into the wind and takes off. This tactic is particularly effective for host finding in vegetation, where the path to the food plant may be rather devious and the odor plume very broken.
A different response to host odor after the initial arousal is to move toward or land on a relevant visual target. This odor-induced visual orientation is believed to occur, for example, in the cabbage seed weevil, which uses odor-conditioned anemotaxis from a distance and then odor-conditioned landing responses on yellow targets close to the source. A number of insect species may be readily trapped by means of a yellow water trap combined with a host odor source, and it is probably generally true that landing responses induced by the host odor are responsible.
Insects living in soil use odors alone to find hosts. Since, the air moves little in soil, steep gradients of volatile chemicals can be achieved and maintained. Carbon dioxide is commonly used by such larvae, but for specialists, host-specific compounds are also used. Root-feeding larvae, such as that of the carrot fly, Psila rosae, and the corn rootworm, respond by moving directly up a concentration gradient. Larvae of the carrot fly respond to a mixture of five compounds found in carrot odor.
For insects that fly or walk, the distances from which olfactory cues elicit responses vary from less than a meter as in the Colorado potato beetle, Leptinotarsa decemlineata, to about 30 m in some bark beetles and 100 m in some flies such as the onion maggot. Those that crawl in soil respond from just a few centimeters.

USING VISION TO FIND HOSTS

Visual attraction can result from responding to the color or form of the host plant. Because these vary so greatly within a species, and because there is relatively little specificity of shape among plant species, visual responses often occur only in the presence of an appropriate olfactory signal.
In a few examples, visual responses to host features have been demonstrated without the presence of odors. Walking insects of several species are attracted to narrow vertical targets in a plain arena, but the precise significance of this attraction is unknown. Perhaps it is a response to potential vegetation or shelter. Several species of
butterflies, however, have been shown to land preferentially on leaves of particular shapes, with further discrimination occurring only after landing. Shape may interact with color as in the apple maggot, Rhagoletis pomonella. Host odors play a role here, but when colored rectangles are offered, the only color to attract flies is yellow, perhaps representing vegetation. If colored spheres are presented, the red and black shapes attract flies, perhaps representing the host fruit.
With respect to color, both wavelength and intensity are important. D. radicum lands preferentially on leaves with a leaf reflectance pattern characteristic of its host, whereas the western flower thrips, Frankliniella occidentalis, land most on yellows and whites, and more at highest intensities of reflected light. Patterns can also matter. For example, females of Heliconius butterflies lay their eggs on Passiflora leaves but tend not to oviposit on leaves that already have eggs on them. This is known to be a visual response to the yellow eggs, because if the eggs are painted green to match the leaf, butterflies do not discriminate against them.
A response to color is often coupled with a chemical cue. Pieris rapae require the presence of glucosinolates to oviposit but still responds to these chemicals only if they are on blue, yellow, green, or white substrates. Females reject red or black substrates.
Visual cues are usually important only at close range, though occasionally they attract specific herbivores from 10 m or so. This is true for the apple maggot, which has a very clear signal in the bright red fruits of its host substrate.

LEARNING IN HOST SEEKING

Although the studies are few, it is clear that many insects take advantage of experience in their foraging activities and thus improve efficiency of host finding. For example, butterflies learn to land on leaf shapes that resemble their hosts’ leaf shapes, making many fewer mistakes with experience, and they learn many visual cues, especially color, when these are coupled with nectar rewards. Grasshoppers have been shown to learn that certain colored backgrounds are associated with the presence of high-quality food, and the time taken to find the food inside colored boxes in laboratory training experiments with Melanoplus sanguinipes was reduced from about 40min for naive individuals to less than 10 min after a single experience.
Less is known about olfactory learning, but the work so far suggests that it may be more important than visual learning. Grasshoppers in experiments have been trained with different food odors associated with high-protein, low-carbohydrate diets and low-protein, high-carbohydrate diets. They were then fed untreated diets of one or the other type of imbalance until they were relatively deprived of one or the other major nutrient. Then, given a choice, grasshoppers tended to select against the odor that had originally been paired with the unbalanced food. Thus, if they were overfed protein and underfed carbohydrate, they were more likely to avoid the odor that had originally been paired with high-protein food and instead be attracted to the odor that had originally been paired with high-carbohydrate food.
Food aversion learning has been demonstrated in grasshoppers and caterpillars, whereby individuals having a deleterious postinges-tive experience after eating a certain food thereafter reject it or eat little of it. However, the role of odor and the importance of the associated cues in behaviors prior to contact have not yet been investigated.

ECOLOGICAL INTERACTIONS

The abiotic environment and the presence of other organisms influence host-seeking behavior in nature. Among abiotic factors, temperature constraints and needs are probably the most important.
For example, thermoregulating grasshoppers choose sites off the ground for cooling, and warm sunny substrates for basking. This can dictate the plants that are immediately available for feeding upon, so selection of thermoregulatory sites influences food selection. For example, the black lubber grasshopper, Taeniopoda eques, is highly polyphagous; when temperatures become very high in its desert environment in the middle of the day, it roosts as high off the ground as possible on mesquite or acacia bushes, and thus, any feeding is on these plants. During the cooler mornings and evenings it feeds only on plants at ground level. Many temperate butterflies seek out sunny or warm patches, and thus plants in those patches. For example, the meadow brown butterfly, Pararge aegeria, oviposits on various grasses but the actual choice depends on the temperature of the leaves, which in turn is influenced by whether the leaves are in sun or shade.
Wind is important for most insects. Wind speed and constancy influence odor plumes used by orienting insects. The wind speed also limits flight, with larger, stronger flying species remaining airborne at higher speeds. Very small insects are often carried by wind, and depending on the terrain, are deposited preferentially in certain places, such as the lee side of trees and hedges.
The presence of certain nonhost plants and the relative abundance or clumpiness of the host plant can alter the detailed behaviors involved in host seeking. For example, butterflies ovipositing in a habitat where two or more host plant species occur commonly tend to choose the species they laid eggs on previously, so that they land more often on the common host. In other insects, the host being selected for oviposition is dependent on factors such as the need for additional resources. In one example, the celery fly, Phylophylla heraclei, requires trees near to the celery host because this is where mating occurs and the adult food of aphid honeydew is available.
Insects that show odor-induced anemotaxis to their host plants presented alone in a wind tunnel in the laboratory do not always show the same behavior in field situations. For example, the Colorado potato beetle is attracted, at least from short distances, to its preferred host, potato. However, if nonhosts are also present, the response may be reduced or absent, and the host odor is said to be masked. Such interactions reduce the distance over which some host odors can be detected by phytophagous insects, and the phenomenon may be one of the mechanisms involved in reduction of pest numbers in certain crop mixtures.
In addition, some insects are influenced by olfactory or visual evidence of prior occupation of a plant, competitors of the same or different species, and of the presence of natural enemies.

PHYSIOLOGY OF THE HERBIVORE

Host-seeking behavior is restricted to times when the ovipositing or feeding insect is in a suitable physiological state. For example, insects about to molt do not feed and are generally not responsive to host odors; in adult females, a load of eggs ready for laying alters motivation so that searching for a host takes priority over other behaviors. Similarly, an insect that has been deprived of food seeks hosts more readily than one that is replete. In nymphs of the desert locust, for example, positive anemotactic responses to the odor of grass in a wind tunnel were not seen in well-fed individuals but were dramatic in nymphs that had been deprived of food for 4 h.
In the bean aphid, Aphis fabae, winged individuals that fly distances from one host to another are attracted, when they take off, to the short wavelengths of the blue sky. After flying certain distances, they are preferentially attracted to the longer wavelengths of yellow, so that they then tend to land on plants in the vicinity. A number of aphid species bias their landings toward the yellower greens that often are associated with plants in an appropriate physiological state rather than toward plants of a particular species.