Introduction

Except for investigations of fruit flies (genus Drosophila) and a few economically important species, rather little research has been done on behavior in Diptera, and investigation specifically on aspects of communication is limited to a few examples only. There are no social Diptera, and signals are used almost entirely in a sexual context. Thus a review of communication in Diptera entails a discussion of the stimuli involved in courtship and mating. Much of the information comes from qualitative descriptions of courtship behavior, and communication involving several sensory modalities is implicit in many of these. However, in the absence of experimentation, it is often difficult to identify the relevant signals and to assess their relative importance. Thus, for example, while the courtship behavior of various Drosophila species and in particular D. melanogaster has been described in detail starting with Sturtevant in 1915 and followed by Weidmann (1951), Spieth (1952), and Bastock and Manning (1955), only in 1962 did Shorey show that courting males produced songs, and it was in 1967 that the significance of these was demonstrated (Bennet-Clark and Ewing, 1967). The involvement of a pheromone in courtship was first described by Shorey and Bartell in 1970. In spite of intensive research carried out on the sexual behavior of D. melanogaster, a complete description of the signals involved in courtship is still not forthcoming.

As communication in D. melanogaster is probably better understood than that of any other dipteran species, except for those with very simple courtships, this example illustrates the fragmentary state of our knowledge. Even in those species with apparently simple behavior, the lack of complication may merely reflect our ignorance.

In this review I have used a certain amount of selectivity and have ignored some of the more anecdotal accounts that abound in the early literature. While some of these are of considerable potential interest, they are often difficult to interpret. Richards (1924) has compiled a bibliography of much of this work.

Mycetophilidae

There is one well-known example of light production in Diptera, which is in the mycetophilid midge Arachnocampa luminosa from New Zealand (Hudson, 1926), although complex bioluminescent behavior, as found in many Coleoptera where species-specific patterns of light production are used by both sexes, has not been described. These midges live in caves and other damp places, and their great numbers in, for example, the Glow-worm Grotto of Waitomo Cave constitute a tourist attraction. Larvae, pupae, and adults possess a light organ in the last abdominal segment. It is derived from the swollen distal ends of four malpighian tubules and, like analogous structures in other animals, has a reflector. Control of light production appears to be neural and is mediated by disinhibition from the brain (Gatenby, 1959). The carnivorous larvae construct mucous snares into which small phototactic insects are attracted. The larvae pupate suspended on a mucous thread, and female pupae luminesce particularly strongly when touched and also just prior to ecdysis. Males are attracted by the light to female pupae and have been observed waiting to mate as soon as the females emerge. Male pupae and adults also produce light, although not so readily as females, but the significance of this is unknown (Richards, 1960). Other luminescent Mycetophilids have been described from Australia and Tasmania, but their behavior has not been studied (Gatenby, 1960).

Culicidae, Chironomidae

One of the best-known examples of acoustic communication in insects is the flight tone in the mating of mosquitoes. Most mosquitoes, and indeed probably the majority of Diptera, form mating swarms. Roth (1948) demonstrated that the stimulus produced by the females of Aedes aegypti that acted as a sexual attractant for the male in these swarms was the flight sound. He further demonstrated that odor was not involved as an attractant. The mating swarms of mosquitoes and other Diptera do not appear primarily to be the result of any communication between individuals, but rather are due to species-specific preferences for particular swarm markers, which are often conspicuous objects in the environment such as the edge of a lake or an isolated tree (Downes, 1969).

Roth showed that the flight tone of males and females differed such that the frequency of the former was above the response threshold of males, and, under normal conditions, males were only attracted to the flight tone of the opposite sex. The flight tones of both sexes became higher with age, and those of newly emerged males were sufficiently low to attract other males. However, this occurred only in the abnormal laboratory situation, and immature males do not usually fly voluntarily. Further, in immature females the flight tone is below the threshold of male hearing, and the time at which it becomes audible coincides with the onset of female sexual receptivity. This synchronization of behavior and physiological state is found on the receptor side also. The flight sounds are perceived by Johnson's Organ, situated at the base of the antenna, and activated by vibration of the arista, which in males bears many fibrillae. Thus amputation or loading of the antennae renders males unresponsive to the female flight tone. In Anopheles quadrimaculatus, the fibrillae are retracted on eclosion and are only extended when males are 15-24 hours old. Males will not attempt to mate until this has occurred, and it coincides with rotation of the male genitalia, which is a prerequisite for successful copulation.

Flight tone rises markedly with temperature. Römer and Rosin (1969) have shown in Chironomos plumosus that the males' response curve follows the change in flight tone over the temperature range of 12° to 24°. The range of frequencies over which males will respond is quite large, presumably because of the changes in flight tone and in the males' response curve with age and because of the temperature effect which, in a very precise system, would reduce the probability of mating. Also, because of the breadth of frequency discrimination, the flight tone is probably not useful as a species-specific signal, and it seems probable that ecological factors are important in maintaining sexual isolation.

Not all mosquitoes and midges form mating swarms; there are a number of species in which males do not have plumose antennae, and in these, female flight tone does not appear to be an attractant. An example is Culiseta inornata, in which females produce a sex pheromone and which mate satisfactorily even if the wings of females or the antennae of males are removed (Kliewer et al., 1966). Similarly, in sabethine mosquitoes sex recognition is not auditory, and, as they are often brightly colored, visual components are probably involved (Haddow and Corbet, 1961). In the aberrant Opifex fuscus and Deinocerties cancer, males locate pupae on the water surface and attempt to copulate during emergence. Sex is discriminated only on attempted copulation. However, even in such an apparently simple mating system the published account suggests that during the brief "courtship," tactile, chemical, visual, and auditory stimuli may be involved (Provost and Haeger, 1967).

Empididae

One of the most widely known examples of visual signals employed in dipteran courtship is in the Empids. The males of many species present females with an insect or "balloon," which is constructed from foam or silk and which may contain an insect or inanimate object. Most Empids form mating swarms of one or both sexes, and those consisting of males carrying balloons are very conspicuous. Females approach males carrying the appropriate object and fly a few centimeters above; both then rise for a short distance, the female drops toward the male, and, as they both dive toward the ground, the male turns over and presents the female with the "gift" and immediately copulates with her. This description, which is fairly typical for many species, refers primarily to Empis barbatoides and E. poplitea (Alcock, 1973).

It is possible to construct a graded series from those that mate without the males' producing a courtship gift (e.g., Tachydromia spp.), through species in which the males provide an unadorned prey (e.g., E. barbatoides, Ramphomya nigrita), to those that wrap the prey in silk (Hilara quadrivittata) or wrap inanimate objects in silk (e.g., H. maura) or offer the females a silk or froth balloon alone (e.g., H. sartor: Hamm, 1928; Kessel, 1955; Alcock, 1973). Kessel (1955) recognizes eight discrete stages in this evolutionary process of ritualization of the behavior, concluding with the final emancipation of the signal from its original function. He suggests that the initial function of the behavior was to divert the predaceous intentions of the female, but there appears to be no evidence for this view. It seems probable, at least in some species, that only the males hunt, but do not themselves feed on the prey; while the females' only protein meal, which is necessary for maturation of the ovaries, comes from the prey presented during courtship (Downes, 1970). This ritual is similar in principle to the courtship feeding in some birds, which not only acts as an important stimulus in establishing and maintaining the pair bond but also provides necessary food for the female (Nisbet, 1973).

Recent descriptions of Empid courtship suggest that only a male carrying prey or prey surrogate is an adequate stimulus to the female although, as all aerial meetings do not result in copulation, some further degree of sexual selection must occur (Alcock, 1973). Also unclear is the basis of species recognition. Alcock reports that the two species E. poplitea and E. barbatoides fly in the same area but do not interact sexually; perhaps small differences in flight pattern are sufficient to discriminate between them. In some species males may recognize conspecific females because the females possess adornments such as fringed legs or eversible abdominal sacs (H. flavinceris), the latter suggesting production of a pheromone (Richards, 1924).

Some species of Empid, such as R. ursinella, mate on the ground without food transfer, and Downes (1970) suggests that this is an adaptation for life in arctic conditions. However, courtship of the aberrant Xanthempis trigramma is quite different. In this species females take up a station on the substrate and vibrate their wings. This signal is answered by males via a similar vibration when they approach to within 12-18 inches. The sexes then alternate wing vibration as the male approaches the female. The signals are presumably acoustic, as this behavior can occur with flies in visual isolation. This is followed by mutual tarsal contacting, and copulation occurs when the female signals her acceptance by turning (Hamm, 1933).

Trypetidae (= Tephritidae)

The mating behavior of members of several genera within this economically important family of fruit flies has been described. Olfactory and acoustic signals are probably important in the courtship of most species and, as many of these have patterned wings that may be displayed, visual stimuli are possibly also involved, although direct evidence for this is lacking.

The best-studied species is Dacus tryoni, the Queensland fruit fly, in which the sexually mature males produce a pheromone from sacs extruded from the posterior region of the rectum (Fletcher, 1969). This species also produces acoustic signals, which have been recorded by Monro (1953). They consist of 3 kHz tone bursts, each of approximately 8 cycles and with a repetition rate of 290 per sec. Monro suggests that the sound is produced by the edge of the wing, which is modified in males, being scraped across an abdominal comb. However, the wave form of the sound and the structure of the comb are not easily reconciled to this interpretation, and, as Reiser et al. (1973) state that the sounds produced by related species can still be heard after wing amputation, this hypothesis clearly requires further investigation.

As the acoustic signal is sufficiently loud to be heard by the unaided human ear and as the pheromone can also be detected by humans, it is probable that both stimuli could act as long-distance attractants for females. Males produce both stimuli at dusk, at which time the females are sexually receptive (Fletcher, 1969). Munro (1953) suggests that sound production is also involved in causing the males to aggregate.

Other species of Dacus produce pheromones via rectal glands, but it is not known to what extent these are species-specific. The possibility that acoustic signals are involved in sexual isolation has been investigated by Myers (1952), who states that the sounds produced by D. cacuminatus are higher in frequency than those of D. tryoni and that, in a choice situation, females of the former species selectively approach conspecific calling males. D. tryoni females, however, approached the nearest male and only rejected D. cacuminatus males after contact, presumably on the basis of contact chemoreception. Males attempt to copulate indiscriminately, and thus, as in most dipteran groups, it is the female that exercises choice of mate.

Pheromone production has been described in other Dacus species by Schultz and Boush (1971) and Economopoulos et al. (1971). The latter authors, working with D. oleae observed, as in D. tryoni, that the males produce the pheromone in a sexual context. They further note that a weak odor is produced by the females of this species. However, Haniotakis (1974), using bioassay techniques, has shown that it is the females of D. oleae that produce the chemical sex attractant and not the males (in contrast to the situation in other Trypetids so far investigated) and that the function of the pheromone produced by males is obscure. Female pheromone production commences on the third day after eclosion, when the ovaries are mature, and is switched off for seven days following mating.

The males of D. oleae also produce acoustic signals, which have been recorded by Féron and Andrieu (1962). These consist of an irregular song with tone bursts of up to four seconds' duration with a fundamental frequency of 320 Hz.

Another species shown to produce both a pheromone and an acoustic signal is the Mediterranean fruit fly, Ceratitis capitata, whose males have a rectal gland everted by haemolymph pressure (Lhoste and Roche, 1960; Féron, 1962). In this case the pheromone acts as a primary attractant for the female, and it is only after her approach that the male vibrates his wings. The sex pheromone of C. capitata has been identified and synthesized by Jacobson et al. (1973) and consists of two fractions, methyl (E)-6-nonenoate and (E)-6-nonen-l-ol. Bioassays showed that maximum attractiveness was found only if an acidic fraction were added.

In all the preceding species the wing vibrations of the males during courtship are probably primarily concerned with producing acoustic stimuli, although this requires formal proof in some of the species. However, Fletcher (1969) suggests that this may have been derived from wing movements whose initial function was to disperse a pheromone; this may occur in the Caribbean fruit fly (Anastrepha suspensa). This species releases a pheromone from the distended pleural region of the third, fourth, and fifth abdominal segments, and "cleaning" movements of the legs are interspersed with wing fanning. The leg movements possibly serve to spread the pheromone on the wings, which is then dispersed by fanning (Nation, 1972).

There is strong circumstantial evidence that wing movements in some species serve to provide visual stimuli. Thus in A. suspensa, following the approach of the female, the male may make wing-waving movements that are not the same as fanning. Similarly, in Tephritis stigmatica and Euleia fratria, during courtship one or both sexes make characteristic movements of the wings with the wings tilted so as to be visually oriented toward the partner. In the former species the wings are initially moved synchronously like windshield wipers, and this is followed by alternate wing extensions along the longitudinal plane of the body. At 45° of extension the wings are vibrated, suggesting an auditory component. In E. fratria the wings are alternately waved forwards and backwards, and, when the male is close to the female, he extends his wings 90° to the substrate and remains stationary for a period. Following that he runs toward the female, wings extended and vibrating (Tauber and Toschi, 1965a, 1965b).

In the island fruit fly (Rioxa pornia) also, following attraction of the female to the male by means of a pheromone, both sexes carry out movements of the patterned wings. The final stage in the courtship of this species is the production by the male of a mound of foam on which the female feeds while the male attempts to copulate (Pritchard, 1967). The production of similar gustatory stimuli has been recorded also in Eutreta species (Stolzfus and Foot, 1965) and in Afrocneros mundus (Oldroyd, 1964). It is unlikely that this can be considered a communicatory device; it probably functions to keep the female stationary while the male mounts.

Finally, visual stimuli may be important in both courtship and aggression within the genus Rhagoletis (Prokopy and Bush, 1973; Bush, 1966; Biggs, 1972). All the species examined have patterned wings, which may be waved during courtship by both sexes or by males during territorial fights. However, copulation often occurs in R. pomonella in the absence of the wing display and it is not therefore an essential component in courtship. It is of interest that members of the pomonella and cingulata specics groups, which consist mainly of sibling species that are often sympatric, are very similar morphologically and sexual isolation is maintained by strict host-plant specificity. By contrast, members of the suavis species group infest only walnuts and the patterning of the wings is distinct in the different species, suggesting that visual stimuli may be involved in the maintainance of sexual isolation (Bush, 1969).

A representative pattern of normal courtship behavior within the Trypetidae might be as follows. Males take up station on the host plant, in particular, on the fruit; the host-plant specificity in itself is in many cases sufficient to ensure some degree of sexual isolation. The males produce a pheromone from abdominal glands, and pheromone dispersal may be facilitated by fanning movements of the wings. Alternatively or concurrently, a sound signal is produced, and these stimuli attract sexually receptive females. The signals are probably also species-specific and are thus factors in maintaining isolation. In almost all species the males will attempt to copulate without any further courtship and are apparently often successful. It is clear that contact chemoreception may play a part at this stage; the males, which are initially undiscriminating, will mate only with conspecifics, and the females will reject foreign males. In addition, further components of courtship containing visual or acoustic components may be interposed between the initial attraction and attempted copulation. Unfortunately, in the almost total absence of quantitative analyses of courtship behavior, it is impossible to evaluate the relative importance of the different stimuli or to speculate on what basis sexual selection may occur. Reiser et al. (1973) have shown that the mating success of D. Cucurbitae, D. dorsalis and C. capitata is reduced in the dark and a further reduction occurs if the flies are also wingless. Removal of the wings alone depresses the success level of the last species only. These observations merely suggest that the relative importance of visual and acoustic stimuli may be different in the members of the two genera studied.

Drosophilidae

The courtship behavior of over three hundred species of Drosophilid have been described. While these qualitative descriptions, which are mainly by Spieth (1952, 1966, 1968, 1969), indicate an extraordinarily diverse and interesting repertoire of behavior, detailed studies are confined to a very few species. Indeed it is in only one species, D. melanogaster, that a comprehensive understanding of the various stimuli involved in courtship is emerging, and I will therefore concentrate on that species.

Most Drosophila, except for the Hawaiian species (Spieth, 1966), probably court and mate on the food source, where male courtship behavior is triggered by visual stimuli (Sturtevant, 1915; Milani, 1950; Spieth, 1974). Males orient to other flies or objects of approximately the right size. Before starting to court, males of most species tap the other fly with their fore-tarsi, presumably to receive chemotactile information concerning sex and conspecificity. This chemical specificity can take some time to develop after eclosion, and Manning (1959) has shown that D. melanogaster males will court newly emerged females of the sibling species D. simulans, but by the time females are four days old most males do not court following tapping. Males with their fore-tarsi removed, however, court a significantly greater number of mature D. simulans females. Tapping may also provide the male with information on the physiological state of the female in some species. Spieth (1969) states that D. sulfurigaster males turn away after tapping inseminated females who have not exhausted their sperm supply. It is probable that more than one surface pheromone is involved in these male responses.

Tapping, while seen in a majority of Drosophila species, is not the inevitable precursor of courtship even in D. melanogaster, and courting males will switch females without tapping again. This element must therefore be of minor importance in effecting sexual isolation, particularly as several species may be seen at the same time on a food source. Tapping may provide stimuli for females as well as males, since unreceptive females will repel males on being tapped. It is possible, however, that the discrimination by the female is made on some other basis and tapping merely triggers the repelling action. Airborne as well as contact pheromones are involved in the courtship of D. melanogaster and of other species. One of these is concerned in the "minority effect," first described by Petit (1958). She showed that when males of two genotypes were mixed, females preferentially mated with the rare genotype, and Ehrman (1969) has shown that male scents are responsible for the phenomenon.

Another pheromonal effect, similar to that found in Musca domestica, where male sexual activity is increased by a female odor, has been reported in D. melanogaster by Shorey and Bartell (1970). As it has also been found in D. pseudoobscura (Sloane and Spiess, 1971), it is likely to be a common phenomenon in the genus.

Subsequent to tapping, the male orients toward the female and attempts to follow her when she moves off. Orientation ensures contact without itself having any specific signal value. Visual stimuli are not important in the courtship of D. melanogaster and are probably unimportant in most Drosophila species. There are major visual components in the displays of some species, such as D. subobscura (Brown, 1965), D. suzukii (Manning, 1965), the Hawaiian species (Spieth, 1966), and in some members of the nasuta subgroup, which have silvery markings on the head that are probably conspicuous to the female. One of these species, D. pulaua, does not appear to produce auditory signals, although the related D. albomicans and D. kepulauana do. This suggests that D. pulaua, which will not mate in the dark, is highly dependent on visual stimuli (Wright, 1974). Mating in a large number of Drosophila species is light-dependent (see, e.g., Grossfield, 1966). However, the majority of experiments merely demonstrate that mating does not occur in the dark, a condition that may be due to a number of different causes. For example, I have observed that one light-dependent species, D. auraria (Spieth and Hsu, 1950), is totally inactive throughout the dark period.

Some form of wing display providing acoustic stimuli is seen in most Drosophila species. In D. melanogaster one wing is extended to 90° and vibrated horizontally through approximately 30° (Bennet-Clark and Ewing, 1968). The acoustic signal produced during vibration is the major one involved in sexually stimulating females. The sounds consist of a series of sinusoidal pulses of 3 ms duration and a pulse repetition rate of 30 per sec at 25°C (Shorey, 1962; BennetClark and Ewing, 1967). The mating success of wingless males is increased by substituting artifically produced courtship songs, thus demonstrating that the pulse train is the effective stimulus. Further, we showed that songs with half and double the normal repetition rate were ineffective, suggesting that the songs may also be important as isolating mechanisms (BennetClark and Ewing, 1969). The species-specific nature of the songs lends weight to this supposition (Ewing and Bennet-Clark, 1968; Ewing, 1970). Further, the songs of sibling or closely related species tend to be distinct (Waldron, 1964; Ewing and Bennet-Clark, 1968; Ewing, 1970; Patty et al., 1973). Thus, for example, the sibling pair D. persimilis and D. pseudoobscura have songs that differ with respect to intrapulse frequency as well as interval (Ewing, 1969), while within the melanogaster species group, the five sibling species D. melanogaster, D. simulans, D. erecta, D.yakuba, and D. tiessieri produce pulsed songs with intrapulse intervals (at 25°C) of 34, 48, 42, 96, and 52 ms, respectively. Also, all the species, except possibly D. yakuba produce "sine song" (see Fig. 1), and D. erecta has an additional pulsed song that is polycyclic and at a higher frequency (Ewing, unpublished).

The patterning of the bursts of song is also important, and intermittent song production is significantly more effective than continuous song. A pattern of two seconds of artifically produced song followed by three seconds of silence, which most closely mimics the normal situation, almost restores the courtship success of wingless males to that of normal flies (Bennet-Clark, Ewing, and Manning, unpublished).

Recently a clearer understanding of the acoustic properties of sound production and reception in small insects has led to more sensitive recordings of Drosophila courtship songs (Bennet-Clark, 1971, 1972). F. von Schilcher (pers. comm.) has recorded a second component in the song of D. melanogaster, which he calls "sine song"; it has also been found in D. albomicans and D. kepulauana (Wright, 1974). The significance of this component is unclear, and it may be a side effect of the mechanics of sound production and without any signal value, although this appears unlikely.

Fig. 1. Acoustic signals produced by Drosophila melanogaster. a. Male courtship song: sine song followed by pulsed song. b. Wing flicks made by unreceptive females that inhibit male courtship. Males courted by other males produce similar sounds, c. Part of male ourtship song interrupted by a repelling buzz made by an immature female.

As in mosquitoes, the acoustic signals are perceived via the antennae. Immobilization of the arista of the antennae in females renders them sexually unreceptive (Manning, 1967).

The function of courtship songs is twofold: to stimulate sexually females that are initially unreceptive and to provide a specific signal that aids in species recognition. These two functions may be served by different components of the signals and, in those species with two distinct songs, by the different songs, but this is difficult to investigate. That a certain amount of song stimulation is necessary before females will copulate and that this stimulation is summated over a period of time have been demonstrated by the use of simulated songs (Bennet-Clark et al., 1973). Bennet-Clark and I suggested that one of the ways in which the courtship songs might act would be to inhibit walking by the female and thus facilitate copulation attempts by the male (Bennet-Clark and Ewing, 1967), and von Schilcher (pers. comm.) has demonstrated that simulated songs do indeed slow down the females. Most interestingly, the simulated songs also affect males but, in contrast to females, their activity is greatly increased. In D. melanogaster and D. simulans the maximum effect occurs at the pulse repetition rate appropriate for that species. It is not clear if this has any natural significance, but is could have a social facilitatory effect that might be adaptive where flies are crowded together on a food source, or it could act as a positive feedback on the singing male and increase his sexual excitation.

Finally, prior to attempted copulation, males of many species including D. melanogaster extend the proboscis and lick the female's genitalia. It is not clear what information is conveyed by this movement. Certainly unreceptive fertilized females that extrude their ovipositors provide inhibiting stimuli for licking males. However it is probable that licking is not merely a test of the female's state of receptivity but provides positive stimuli, presumably chemical and tactile, for both sexes, as licking is repeated frequently throughout a courtship (Bastock and Manning, 1955). In many species licking is prolonged and is a major part of courtship (Spieth, 1952).

In D. melanogaster licking is often followed by attempted copulation. The females of this species do not have any acceptance posture that signals their readiness to mate. Successful attempts probably occur only if the female spreads her genital plates; however, this is unlikely to be perceived by the male. By contrast, females of some Drosophila species, such as members of the D. nasuta subgroup, do show an acceptance posture; they spread their wings to about 45°, depress their abdomens, and turn away from the male displaying in front of them (Spieth, 1969). However, males do not always attempt to copulate in response to this behavior, and it is not clear to what extent it is indeed a signal for the male.

Most of the signals involved in courtship are provided by males. Female signals are limited to a possible acceptance posture in some species, the production of one or more pheromones, and finally to the production of a "buzz" and a wing flick. The former sound is caused by a wing vibration and is made mainly by immature, unreceptive females when courted. Its effect is to inhibit male courtship, and, as it is very similar in several different species, it could function as an interspecific as well as an intraspecific signal (Ewing and Bennet-Clark, 1968). Males, on being courted by other males, also flick their wings, producing an irregular pulse train. The sound produced by female wing flicks is similar, and both have the effect of inhibiting courtship. Fig. 1 illustrates the different sounds produced by D. melanogaster.

The courtships of most Drosophila species show similarities to the patterns described above. One aberrant and very interesting group are the Hawaiian species described by Spieth (1966), which have evolved quite different patterns of courtship behavior. Most species do not court on the food source. Individual males take up small territories on vegetation, which they defend from other males. The flies are cryptic when feeding, and Spieth considers the behavior of the Hawaiian species to have evolved in response to the very intense prédation to which they are subject. Males are often map-winged and may advertise their presence with visual signals. Some trail their abdomens along the substrate, depositing a pheromone (e.g., D. grimshaivi). Others display a behavior similar to that described for Anastrepha suspensa (Nation, 1972), where the abdomen is raised, a drop of fluid is extruded, and the wings are vibrated, presumably for pheromone dispersal (e.g., D. pilimana, Antopocerus tanythrix).

The courtship behavior itself is extremely varied. Males possess epigamic features involving modifications of mouthparts, antennae, legs, and wings. Complex auditory, tactile, visual, and chemical signals are clearly involved in courtship; however, as the stimuli involved in court ship have not been investigated experimentally I shall not deal further with them.

Chloropidae

One of the clearest examples of a speciesspecific mechanical signal-response system is seen in the gall-forming flies of the genus Lipara (Mook and Bruggemann, 1968; Chvâla et al., 1974). The larvae of these flies form galls on the reed Phragmites communis, and only one individual is found on a stem. Males fly from stem to stem and produce a substrate-transmitted vibration with a pattern of pulses characteristic of the species. If a virgin female is on the reed she will respond by producing a series of pulses that induces the male to search the stem. The flies then countersignal until the male finds the female (see Fig. 2).

Females respond to males up to 2 meters away. As the females are very static, this pattern of behavior is an efficient method of bringing the sexes together. Males of different species produce different patterns of pulses, and Chvâla et al. (1974) have shown that females, whose signals are all similar, respond only to the signals of conspecific males. Mook and Bruggemann could find no stridulatory mechanisms. As the fundamental frequency within the pulses is low (about 300 Hz), the vibrations are probably caused by activation of thoracic flight mechanism, as in Drosophila. They are transmitted to the substrate via the legs and are almost certainly perceived by the sub-genual organs.

It is of interest that while Lipara and Drosophila have similar methods of sound production, they utilize different methods of transmission and reception. The reed stem on which Lipara lives provides an excellent medium for the propagation of the sounds, but this is not so for the food sources on which Drosophila normally court. The latter therefore utilize airborne sounds, which are perceived by the antennae. However, one can still record the sounds produced by courting Drosophila whose wings have been totally removed if they court on the diaphragm of a crystal microphone. The use of substrate transmitted sounds is a possibility in at least some members of this genus also.

Fig. 2. Substrate-transmitted vibrations produced by gall-flies of the genus Lipara. The signals were recorded using a crystal gramophone pickup element in contact with the substrate, a. Signal of male L. lucens followed by part of the answering signal of a female, b-e: Signals of males of different species, b. L. lucens; c. L. similis; d. L. pullitarsis', e. L. rufitarsis. (From Chvâla et al., 1974.)

Calliphoridae, Muscidae

The courtship behavior of flies of these families provides a good example of apparent and misleading simplicity. In many species mounting by males is elicited by extremely generalized visual stimuli, such as any dark object of approximately the appropriate size (see, e.g. Vogel, 1957). Even the visual stimuli are not essential, as mating can occur in the dark. If the attempt is made on a conspecific female, copulation or rejection occurs within one or two seconds, and this does not appear to provide much time for the exchange of complex signals.

The females of Musca domestica and Lucilla cuprina, however, produce pheromones whose action is to stimulate sexual behavior in males (Rogoff et al., 1964; Bartell et al., 1969). Further, in the former species the same or another pheromone acts as a sex attractant. The pheromone can be extracted with benzene and is speciesspecific in its action, as extracts from M autumnalis and Stomoxys calcitrans are ineffective (Rogoff et al., 1964). Recently Tobin and Stoffolano (1973a, 1973b) have filmed the mating behavior of M. domestica and M. autumnalis. They have shown that within the short period between mounting and copulation the male performs a series of complex actions that are probably concerned with tactile, chemical, and auditory stimuli and that the two species differed consistently in details of the behavior.

I have recorded the sounds produced by males of M domestica during the brief courtship. These usually consist of a train of tone bursts of between 160 and 190 Hz and are produced by vibration of the partly folded wings. The first of these is both longer and more variable than the succeeding ones, with a mean duration of about 500 ms. Then follow up to six tone bursts of 240 ms, separated by 40 ms intervals. These sounds, while not as regular as many of those produced by Drosophila species, are patterned in such a way as to suggest that they have signal value. The flies also produce other sounds that may have an aggressive or warning function (Esch and Wilson, 1967).

Summary

This survey, although not exhaustive of the literature, demonstrates very diverse modes of communication within the Diptera, and yet nothing is known about the behavior of perhaps 99.5 percent of described species. This paucity of information is partly due to technical difficulties and to the enormity of the task. It is worthwhile both to consider these difficulties and to see, even with the limited information available, if any generalizations are possible.

It is immediately obvious that often more than one channel of communication is used by a single species, sometimes simultaneously. This makes analysis difficult, in comparison with stimulus-response chains. These are not common in Diptera, but one example is the courtship of Tipula oleracea. In this species the males approach and grab the forelegs of the female. The only relevant parameter that triggers the next stage of the male's courtship is the thickness of the female's legs. When the female raises her legs the male mounts; when the female's leg movements cease the male "kisses" the female's head, moves back, and in response to tactile stimuli from the tarsal contact of the female's abdomen, copulates. Stich (1963), in a series of simple but elegant experiments using models, has demonstrated that a specific stimulus is required at each step before the sequence can continue. Unfortunately, most behavior is not amenable to dissection in this manner.

Many species mate in swarms or require specific conditions not easily provided in the laboratory. In either case their behavior is difficult to observe, much less analyze experimentally. Many Diptera utilize sex pheromones to some extent, and of all sensory modalities, the chemosensory ones are probably the most difficult to work on. Without the use of chemical procedures to isolate and identify pheromones it is difficult to know whether the behavior effect under investigation is due to a single pheromone or to a medley: whether the pheromone has a unitary or multiple mode of action.

The use of pheromones is widespread in those species that do not form mating swarms, and even in the swarming species one cannot automatically discard the possibility that contact pheromones are being used. The pheromones can be classified on the basis of function; sex attractants (e.g., Dacus spp., Lucilia cuprina), sex stimulants or aphrodisiacs (e.g., Drosophila spp., Musca domestica), and repellents. The third class has been investigated less and possibly includes two types: those that repel members of other species and those that are produced by sexually unreceptive individuals, usually fertilized females. Repelling pheromones are probably produced by Drosophila species (Spieth, 1969; Cook, 1975) and by the gnat Hippelates collusor, whose females produce a sex attractant when receptive and switch to a repellent when their ovaries contain mature eggs (Adams and Mulla, 1968).

Acoustic signals are also common, but there are technical problems in recording and interpreting signals produced by small sound sources. Recording is difficult partly because acoustic power and distance follow an inverse sixth-power relationship where the wavelength of the sound is less than one-third the diameter of the source (Bennet-Clark, 1971). This is true of many Diptera, whose sound source, the wings, produce sounds of low frequency, in contrast to the majority of the better-known singing insects, such as crickets and cicadas, which produce highfrequency songs. A further complication is that both the type of microphone used and the recording mode of the tape recorder can affect the form of the signal.

The sounds produced by Diptera can be subdivided with regard to function in a manner similar to that used to classify pheromones. Sounds are probably used less as attractants than are pheromones because of the physical limitations mentioned above, but Xanthempis trigramma and some Dacus species produce sounds in this category. Sexual stimulation due to acoustic signals is also common, and both male and female Drosophila produce sounds that repel other flies.

All the communication that I have described occurs in a sexual context. As the females, at least, of many species mate only once or at long intervals, it is clearly adaptive for the sexual signals to be synchronized with the reproductive cycle. Thus the switching on and off of pheromone production at the appropriate time is a general feature of Diptera and of other insects, and the same is probably true of acoustic signals. The synchronization of ovarian development and various aspects of reproductive behavior, including pheromone production, has been shown to be under endocrine control in some insects, but the situation in Diptera awaits investigation (Barth, 1970).

The species-isolating function of communication is clearly seen in Diptera. The selective pressure acting to produce these isolating mechanisms is demonstrated by the extremely diverse song patterns recorded from different species of Drosophila. There are species that produce continuous songs, which may be of a single frequency, of two alternating frequencies, or frequency modulated. The majority of species, however, produce pulsed sounds of different pulse length, pulse frequency, and repetition rate, while some use more than one type of song (Ewing and Bennet-Clark, 1968; Ewing 1970).

An important criterion for signals used as isolating mechanisms is that they should be invariable within species. This is true of the pheromones that have been investigated and of acoustic signals. One possible exception is the scent that mediates the rare genotype advantage in Drosophila. Hay (1973) suggests that this may develop as a colony odor, similar to that found in some social Hymenoptera. However, this odor functions not as an isolating mechanism but as a promoter of genetic heterogeneity within a species.

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