Box 43 Reception of communication molecules

i i-lymph cavity

-cuticle -epidermal cell

- ciliary sinus

- thecogen cell

- trichogen cell -tormogen cell axons

Pheromones, and indeed all signaling chemicals (semio-chemicals), must be detectable in the smallest quantities. For example, the moth approaching a pheromone source portrayed in Fig. 4.7, must detect an initially weak signal, and then respond appropriately by orientating towards it, distinguishing abrupt changes in concentration ranging from zero to short-lived concentrated puffs. This involves a physiological ability to monitor continuously and respond to aerial pheromone levels in a process involving extra- and intracellular events.

Ultrastructural studies of Drosophila melanogaster and several species of moth allow identification of several types of chemoreceptive (olfactory) sensilla: namely sensilla basiconica, sensilla trichodea, and sensilla coeloconica. These sensillar types are widely distributed across insect taxa and structures but most often are concentrated on the antenna. Each sensilla has from two to multiple subtypes which differ in their sensitivity and tuning to different communication chemicals. The structure of a generalized multiporous olfactory sensillum in the accompanying illustration follows Birch and Haynes (1982) and Zacharuk (1985).

To be detected, first the chemical must arrive at a pore of an olfactory sensillum. In a multiporous sensillum, it enters a pore kettle and contacts and crosses the cuticular lining of a pore tubule. Because pheromones (and other semiochemicals) largely are hydrophobic (lipophilic) compounds they must be made soluble to reach the receptors. This role falls to odorant-binding proteins (OBP) produced in the tormogen and trichogen cells (Fig. 4.1), from which they are secreted into the sensillum-lymph cavity that surrounds the dendrite of the receptor. Specific OBPs bind the semiochemical into a soluble ligand (OBP-pheromone complex) which is protected as it diffuses through the lymph to the dendrite surface. Here, interaction with negatively charged sites transforms the complex, releasing the pheromone to the binding site of the appropriate olfactory receptors located on the dendrite of the neuron, triggering a cascade of neural activity leading to appropriate behavior.

Much research has involved detection of pheromones because of their use in pest management (see section 16.9), but the principles revealed apparently apply to semiochemical reception across a range of organs and taxa. Thus, experiments with the electroantennogram (Box 4.2) using a single sensillum show highly specific responses to particular semiochemicals, and failure to respond even to "trivially" modified compounds. Studied OBPs appear to be one-to-one matched with each semiochemical, but insects apparently respond to more chemical cues than there are OBPs yet revealed. Additionally, olfactory receptors on the dendrite surface seemingly may be less specific, being triggered by a range of unrelated ligands. Furthermore, the model above does not address the frequently observed synergistic effects, in which a cocktail of chemicals provokes a stronger response than any component alone. It remains an open question as to exactly how insects are so spectacularly sensitive to so many specific chemicals, alone or in combination. This is an active research area, with microphysiology and molecular tools providing many new insights.

axons

Fig. 4.6 The antennae of a male moth of Trictena atripalpis (Lepidoptera: Hepialidae): (a) anterior view of head showing tripectinate antennae of this species; (b) cross-section through the antenna showing the three branches; (c) enlargement of tip of outer branch of one pectination showing olfactory sensilla.

Fig. 4.6 The antennae of a male moth of Trictena atripalpis (Lepidoptera: Hepialidae): (a) anterior view of head showing tripectinate antennae of this species; (b) cross-section through the antenna showing the three branches; (c) enlargement of tip of outer branch of one pectination showing olfactory sensilla.

definite behavior or developmental process. This definition remains valid today, despite the discovery of a hidden complexity of pheromone cocktails.

Pheromones are predominantly volatile but sometimes are liquid contact chemicals. All are produced by exocrine glands (those that secrete to the outside of the body) derived from epidermal cells. The scent organs may be located almost anywhere on the body. Thus, sexual scent glands on female Lepidoptera lie in eversible sacs or pouches between the eighth and ninth abdominal segments; the organs are mandibular in the female honey bee, but are located on the swollen hind tibiae of female aphids, and within the midgut and genitalia in cockroaches.

Classification of pheromones by chemical structure reveals that many naturally occurring compounds (such as host odors) and pre-existing metabolites (such as cuticular waxes) have been co-opted by insects to serve in the biochemical synthesis of a wide variety of compounds that function in communication. Chemical classification, although of interest, is of less value for many entomologists than the behaviors that the chemicals elicit. Very many behaviors of insects are governed by chemicals; nevertheless, we can distinguish pheromones that release specific behaviors from those that prime long-term, irreversible physiological changes. Thus, the stereotyped sexual behavior of a male moth is released by the female-emitted sex phero-mone, whereas the crowding pheromone of locusts will prime maturation of gregarious phase individuals (section 6.10.5). Here, further classification of pheromones is based on five categories of behavior associated with sex, aggregation, spacing, trail forming, and alarm.

Sex pheromones

Male and female conspecific insects often communicate with chemical sex pheromones. Mate location and courtship may involve chemicals in two stages, with sex attraction pheromones acting at a distance, followed by close-up courtship pheromones employed prior to mating. The sex pheromones involved in attraction often differ from those used in courtship. Production and release of sex attractant pheromones tends to be restricted to the female, although there are lepidopterans and scorpionflies in which males are the releasers of distance attractants that lure females. The producer releases volatile pheromones that stimulate characteristic behavior in those members of the opposite sex within range of the odorous plume. An aroused recipient raises the antennae, orientates towards the source and walks or flies upwind to the source, often in a zig-zag track (Fig. 4.7) based on ability to respond rapidly to minor changes in pheromone concentration

Sex Pheromone
Fig. 4.7 Location of pheromone-emitting female by male moth tacking upwind. The pheromone trail forms a somewhat discontinuous plume because of turbulence, intermittent release, and other factors. (After Haynes & Birch 1985.)

by direction change (Box 4.3). Each successive action appears to depend upon an increase in concentration of this airborne pheromone. As the insect approaches the source, cues such as sound and vision may be involved in close-up courtship behavior.

Courtship (section 5.2), which involves co-ordination of the two sexes, may require close-up chemical stimulation of the partner with a courtship pheromone. This pheromone may be simply a high concentration of the attractant pheromone, but "aphrodisiac" chemicals do exist, as seen in the queen butterfly (Nymphalidae: Danaus gilippus). The males of this species, as with several other lepidopterans, have extrusible abdominal hairpencils (brushes), which produce a pheromone that is dusted directly onto the antennae of the female, whilst both are in flight (Fig. 4.8). The effect of this pheromone is to placate a natural escape reaction of the female, who alights, folds her wings and allows copulation. In D. gilippus, this male courtship pheromone, a pyrrolixidine alkaloid called danaidone, is essential to successful courtship. However, the butterfly cannot synthesize it without acquiring the chemical precursor by feeding on selected plants as an adult. In the arctiid moth, Creatonotus gangis, the precursor of the male courtship pheromone likewise cannot be synthesized by the moth, but is sequestered by the larva in the form of a toxic alkaloid from the host plant. The larva uses the chemical in its defense and at metamorphosis the toxins are transferred to the adult. Both sexes use them as defensive compounds, with the male additionally

Aphrodisiacs Danaus
Fig. 4.8 A pair of queen butterflies, Danaus gilippus (Lepidoptera: Nymphalidae: Danainae), showing aerial "hairpencilling" by the male. The male (above) has splayed hairpencils (at his abdominal apex) and is applying pheromone to the female (below). (After Brower et al. 1965.)

converting them to his pheromone. This he emits from inflatable abdominal tubes, called coremata, whose development is regulated by the alkaloid pheromone precursor.

A spectacular example of deceitful sexual signaling occurs in bolas spiders, which do not build a web, but whirl a single thread terminating in a sticky globule towards their moth prey (like gauchos using a bolas to hobble cattle). The spiders lure male moths to within reach of the bolas using synthetic lures of sex-attractant pheromone cocktails. The proportions of the components vary according to the abundance of particular moth species available as prey. Similar principles are applied by humans to control pest insects using lures containing synthetic sex pheromones or other attract-ants (section 16.9). Certain chemical compounds (e.g. methyl eugenol), that either occur naturally in plants or can be synthesized in the laboratory, are used to lure male fruit flies (Tephritidae) for pest management purposes. These male lures are sometimes called para-pheromones, probably because the compounds may be used by the flies as a component in the synthesis of their sex pheromones and have been shown to improve mating success, perhaps by enhancing the male's sexual signals.

Sex pheromones once were thought to be unique, species-specific chemicals, but in reality often they are chemical blends. The same chemical (e.g. a particular 14-carbon chain alcohol) may be present in a range of related and unrelated species, but it occurs in a blend of different proportions with several other chemicals. An individual component may elicit only one part of the sex attraction behavior, or a partial or complete mixture may be required. Often the blend produces a greater response than any individual component, a synergism that is widespread in insects that produce pheromone mixtures. Chemical structural similarity of pheromones may indicate systematic relationship amongst the producers. However, obvious anomalies arise when identical or very similar pheromones are synthesized from chemicals derived from identical diets by unrelated insects.

Even if individual components are shared by many species, the mixture of pheromones is very often species-specific. It is evident that pheromones, and the stereotyped behaviors that they evoke, are highly significant in maintenance of reproductive isolation between species. The species-specificity of sex phero-mones avoids cross-species mating before males and females come into contact.

Aggregation pheromones

The release of an aggregation pheromone causes conspecific insects of both sexes to crowd around the source of the pheromone. Aggregation may lead to increased likelihood of mating but, in contrast to many sex pheromones, both sexes may produce and respond to aggregation pheromones. The potential benefits provided by the response include security from predation, maximum utilization of a scarce food resource, overcoming of host resistance, or cohesion of social insects, as well as the chance to mate.

Aggregation pheromones are known in six insect orders, including cockroaches, but their presence and mode of action has been studied in most detail in Coleoptera, particularly in economically damaging species such as stored-grain beetles (from several families) and timber and bark beetles (Curculionidae: Scolytinae). A well-researched example of a complex suite of aggregation pheromones is provided by the Californian western pine beetle, Dendroctonus brevi-comis (Scolytinae), which attacks ponderosa pine (Pinus ponderosa). On arrival at a new tree, colonizing females release the pheromone exo-brevicomin augmented by myrcene, a terpene originating from the damaged pine tree. Both sexes of western pine beetle are attracted by this mixture, and newly arrived males then add to the chemical mix by releasing another pheromone, frontalin. The cumulative lure of frontalin, exo-brevi-comin, and myrcene is synergistic, i.e. greater than any one of these chemicals alone. The aggregation of many pine beetles overwhelms the tree's defensive secretion of resins.

Spacing pheromones

There is a limit to the number of western pine beetles (D. brevicomis; see above) that attack a single tree. Cessation is assisted by reduction in the attractant aggregation pheromones, but deterrent chemicals also are produced. After the beetles mate on the tree, both sexes produce "anti-aggregation" pheromones called verbenone and trans-verbenone, and males also emit ipsdienol. These deter further beetles from landing close by, encouraging spacing out of new colonists. When the resource is saturated, further arrivals are repelled.

Such semiochemicals, called spacing, epideictic, or dispersion pheromones, may effect appropriate spacing on food resources, as with some phytophagous insects. Several species of tephritid flies lay eggs singly in fruit where the solitary larva is to develop. Spacing occurs because the ovipositing female deposits an oviposition-deterrent pheromone on the fruit on which she has laid an egg, thereby deterring subsequent oviposition. Social insects, which by definition are aggregated, utilize pheromones to regulate many aspects of their behavior, including the spacing between colonies. Spacer pheromones of colony-specific odors may be used to ensure an even dispersal of colonies of conspecifics, as in African weaver ants (Formicidae: Oecophylla longinoda).

Trail-marking pheromones

Many social insects use pheromones to mark their trails, particularly to food and the nest. Trail-marking pheromones are volatile and short-lived chemicals that evaporate within days unless reinforced (perhaps as a response to a food resource that is longer lasting than usual). Trail pheromones in ants are commonly metabolic waste products excreted by the poison gland. These need not be species-specific for several species share some common chemicals. Dufour's gland secretions of some ant species may be more species-specific chemical mixtures associated with marking of territory and pioneering trails. Ant trails appear to be non-polar, i.e. the direction to nest or food resource cannot be determined by the trail odor.

In contrast to trails laid on the ground, an airborne trail - an odor plume - has directionality because of increasing concentration of the odor towards the source. An insect may rely upon angling the flight path relative to the direction of the wind that brings the odor, resulting in a zig-zag upwind flight towards the source. Each directional shift is produced where the odor diminishes at the edge of the plume (Fig. 4.7).

Alarm pheromones

Nearly two centuries ago it was recognized that workers of honey bees (Apis mellifera) were alarmed by a freshly extracted sting. In the intervening years many aggregating insects have been found to produce chemical releasers of alarm behavior - alarm pheromones - that characterize most social insects (termites and eusocial hymenopterans). In addition, alarm pheromones are known in several hemipterans, including subsocial treehoppers (Membracidae), aphids (Aphididae), and some other true bugs. Alarm phero-mones are volatile, non-persistent compounds that are readily dispersed throughout the aggregation. Alarm is provoked by the presence of a predator, or in many social insects, a threat to the nest. The behavior elicited may be rapid dispersal, such as in hemipterans that drop from the host plant; or escape from an unwinnable conflict with a large predator, as in poorly defended ants living in small colonies. The alarm behavior of many eusocial insects is most familiar to us when disturbance of a nest induces many ants, bees, or wasps to an aggressive defense. Alarm pheromones attract aggressive workers and these recruits attack the cause of the disturbance by biting, stinging, or firing repellent chemicals. Emission of more alarm pheromone mobilizes further defenders. Alarm pheromone may be daubed over an intruder to aid in directing the attack.

Alarm pheromones may have been derived over evolutionary time from chemicals used as general anti-predator devices (allomones; see below), utilizing glands co-opted from many different parts of the body to produce the substances. For example, hymenop-terans commonly produce alarm pheromones from mandibular glands and also from poison glands, meta-pleural glands, the sting shaft, and even the anal area. All these glands also may be production sites for defensive chemicals.

4.3.3 Semiochemicals: kairomones, allomones, and synomones

Communication chemicals (semiochemicals) may function between individuals of the same species (pheromones) or between different species (allelo-chemicals). Interspecific semiochemicals may be grouped according to the benefits they provide to the producer and receiver. Those that benefit the receiver but disadvantage the producer are kairomones. Allomones benefit the producer by modifying the behavior of the receiver although having a neutral effect on the receiver. Synomones benefit both the producer and the receiver. This terminology has to be applied in the context of the specific behavior induced in the recipient, as seen in the examples discussed below. A particular chemical can act as an intraspecific pheromone and may also fulfill all three categories of interspecific communication, depending on circumstances. The use of the same chemical for two or more functions in different contexts is referred to as semio-chemical parsimony.

Kairomones

Myrcene, the terpene produced by a ponderosa pine when it is damaged by the western pine beetle (see above), acts as a synergist with aggregation phero-mones that act to lure more beetles. Thus, myrcene and other terpenes produced by damaged conifers can be kairomones, disadvantaging the producer by luring damaging timber beetles. A kairomone need not be a product of insect attack: elm bark beetles (Curculionidae: Scolytinae: Scolytus spp.) respond to a-cubebene, a product of the Dutch elm disease fungus Ceratocystis ulmi that indicates a weakened or dead elm tree (Ulmus). Elm beetles themselves inoculate previously healthy elms with the fungus, but pheromone-induced aggregations of beetles form only when the kairomone (fungal a-cubenene) indicates suitability for colonization. Host-plant detection by phytophagous insects also involves reception of plant chemicals, which therefore are acting as kairomones.

Insects produce many communication chemicals, with clear benefits. However, these semiochemicals also may act as kairomones if other insects recognize them. In "hijacking" the chemical messenger for their own use, specialist parasitoids (Chapter 13) use chemicals emitted by the host, or plants attacked by the host, to locate a suitable host for development of its offspring.

Allomones

Allomones are chemicals that benefit the producer but have neutral effects on the recipient. For example, defensive and/or repellent chemicals are allomones that advertise distastefulness and protect the producer from lethal experiment by prospective predators. The effect on a potential predator is considered to be neutral, as it is warned from wasting energy in seeking a distasteful meal.

The worldwide beetle family Lycidae has many distasteful and warning-colored (aposematic) members (see Plate 6.5, facing p. 14), including species of Metrio-rrhynchus that are protected by odorous alkylpyrazine allomones. In Australia, several distantly related beetle families include many mimics that are modeled visually on Metriorrhynchus. Some mimics are remarkably convergent in color and distasteful chemicals, and possess nearly identical alkylpyrazines. Others share the allomones but differ in distasteful chemicals, whereas some have the warning chemical but appear to lack dis-tastefulness. Other insect mimicry complexes involve allomones. Mimicry and insect defenses in general are considered further in Chapter 14.

Some defensive allomones can have a dual function as sex pheromones. Examples include chemicals from the defensive glands of various bugs (Heteroptera), grasshoppers (Acrididae), and beetles (Staphylinidae), as well as plant-derived toxins used by some Lepidoptera (section 4.3.2). Many female ants, bees, and wasps have exploited the secretions of the glands associated with their sting - the poison (or venom) gland and Dufour's gland - as male attractants and releasers of male sexual activity.

A novel use of allomones occurs in certain orchids, whose flowers produce similar odors to female sex pheromone of the wasp or bee species that acts as their specific pollinator. Male wasps or bees are deceived by this chemical mimicry and also by the color and shape of the flower (see Plates 4.4 & 4.5), with which they attempt to copulate (section 11.3.1). Thus the orchid's odor acts as an allomone beneficial to the plant by attracting its specific pollinator, whereas the effect on the male insects is near neutral - at most they waste time and effort.

Synomones

The terpenes produced by damaged pines are kairo-mones for pest beetles, but if identical chemicals are used by beneficial parasitoids to locate and attack the bark beetles, the terpenes are acting as synomones (by benefiting both the producer and the receiver). Thus a-pinene and myrcene produced by damaged pines are kairomones for species of Dendroctonus but synomones for pteromalid hymenopterans that parasitize these timber beetles. In like manner, a-cubebene produced by Dutch elm fungus is a synomone for the braconid hymenopteran parasitoids of elm bark beetles (for which it is a kairomone).

An insect parasitoid may respond to host-plant odor directly, like the phytophage it seeks to parasitize, but this means of searching cannot guarantee the para-sitoid that the phytophage host is actually present. There is a greater chance of success for the parasitoid if it can identify and respond to the specific plant chemical defenses that the phytophage provokes. If an insect-damaged host plant produced a repellent odor, such as a volatile terpenoid, then the chemical could act as:

• an allomone that deters non-specialist phytophages;

• a kairomone that attracts a specialist phytophage;

• a synomone that lures the parasitoid of the phytophage.

Of course, phytophagous, parasitic, and predatory insects rely on more than odors to locate potential hosts or prey, and visual discrimination is implicated in resource location.

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