Physiological Entomology (2003) 28, 157–174

REVIEW ARTICLE duets: underlying mechanisms and their evolution

WINSTON J. BAILEY Department of Biology, University of Western Australia, Nedlands, Western Australia

Abstract. Duetting between the sexes in involves the use of airborne acoustic signals, substrate vibration and bioluminescence. Unlike avian duets, in which females may initiate the interaction, among insects the duet starts with the male, and the female usually provides a brief reply. Insect duets are characterized by low variance in the reply latency of the female (the time between a key element in the male call and the onset of the female’s response). Duetting is reviewed principally in but also in Plecoptera, Hemiptera, Neuroptera and bioluminescence in the Coleoptera. The mechanisms of the duet are examined first, followed by evolution and the associated change in searching strategies of each sex. As defined, the duet has distinct temporal characteristics and these are compared with acoustic interactions among males in those species that exhibit male–male synchrony and alternation. For insects, the key element of a duet for species’ recognition is low variance in the reply latency of females. In cases in which the male’s initiating signal is extremely short, reply latencies become indi- cators of species’ recognition. However, in those species in which the initiating male call is under selection through female choice, the male call is predictably longer and occasionally more complex. Under these circumstances, reply latencies often increase, creating an opportunity for alternative male tactics. When alternative tactics exist in nature, males may decrease the intensity of their call, insert a trigger pulse that signals to the female the end of its complex call, or males may even add a masking signal that obscures the competing signal. Key words. acoustic communication, bioluminescence, Coleoptera, duet, female call preference, Hemiptera, mate-guarding, Neuroptera, Orthoptera, Plecoptera.

Introduction stereotyped temporal association between initiating call and the reply. Other authors have used the more conservative A duet is usually considered as an acoustic interaction term dialogue for male–female signal interactions (e.g. between two partners. For biologists who study duetting Greenfield, 1994a, 2002; Buck & Case, 2002). However, behaviour in birds, primates, ungulates, frogs or , such a term suggests a loosely structured interaction rather the interaction is between the sexes. The most compelling than one with low temporal variance between initiating and aspect of the term used in animal communication, and hence reply signals. its use in this review, is that there are only two participants A stereotypic interaction is possible between calling whose signal interaction is marked by the predictable and males, and although interactions may involve just two males, and therefore qualify as a duet, more often calling males are part of a chorus of aggregated individuals. For Correspondence: Winston J. Bailey, Department of Animal this reason, although many of the ideas developed around Biology, University of Western Australia, Nedlands, Western chorusing behaviour also apply to duetting, the voluminous Australia 6009. Tel.: þ61 (0)8 93802241; fax: þ61 (0)8 93801029; literature on male call interactions has been excluded from e-mail: [email protected] this review (see Schwartz, 1991; Greenfield, 1994a, b, 2002).

# 2003 The Royal Entomological Society 157 158 W. J. Bailey

To draw common threads from studies on male–female This review examines both the proximate mechanisms of signalling in insects, the remarkable bioluminescent inter- the insect duet and the evolutionary significance of different actions of fireflies (Buck & Case, 2002) and interactions duetting and searching tactics. The first section defines the based on substrate vibration have been included. duet by illustrating various insect duetting systems that use Many insects incorporate sound as part of the courtship bioluminescence and both airborne and substrate acoustic display but not all of these constitute duets. For example, signals. Aspects of the duetting signal that function in drosophilid fruit flies produce long and complex courtship species’ recognition are identified and attention is drawn patterns in which females may signal their presence and to features of the signal that may be subject to natural willingness to mate (Bennet-Clark et al., 1980; Crossley selection in the form of energy requirement and predation et al., 1995). In these cases the temporal organization events, and also sexual selection through female choice. between call and responding courtship signal is seldom Predictably, acoustic elements subject to female choice will fixed and few would consider such acts of acoustic court- contain information that reflects female-preferred male ship as a duet. Similarly, many leaf and plant hoppers traits and as a consequence will be long, loud or elaborate. produce calls in response to males, and these calls either The second part of this review focuses on what may be increase male searching patterns (Claridge, 1985) or may considered evolutionary consequences of developing a assist males in locating receptive females (Shaw et al., 1974; duet. The questions are addressed of why duet at all, and Ichikawa, 1976; Booij, 1982). Although duetting may occur what are the costs to both the initiating calling males and of in some species of plant hopper (e.g. Nuhardiyati, 1998), for searching by females. As relative parental investment shifts most species the female reply is seldom fixed in its latency between the sexes, calling and searching roles are predicted and so workers have not considered variation in reply latency to change. As in birds (Levin, 1996), females rather than as an important aspect of signalling in these groups. One case males may take on a calling role, and males may take a of call interaction in cicadas provides a classic example of more significant role in searching. It is argued that where costs of male searching as part of a duet in homopteran costs are to males, perhaps through directional selection signalling (Gwynne, 1987). Thus sporadic evidence of fixed through female choice, the expectation is that males unable temporal strategies exists within the Homoptera, in which the to compete will adopt alternative mate tactics. In addition, putative duet induces males rather than females to adopt a where such conditional tactics are maintained within a searching role. The treatment of homopteran signalling as a population through density-dependent mechanisms, males duet may encourage a careful re-examination of calling and exposed to cheat tactics will inevitably evolve devices that searching strategies in this large and diverse group of insects. reduce the chance of take-over by alternative low-cost The largest literature on duetting or antiphonal singing strategies. This feature of insect duetting, which may be exists for birds and primates (see review by Farabaugh, described as precopulatory mate-guarding, has received 1982). In these groups the duet allows the sexes to establish very little attention. a pair bond that may eventually lead to copulation and, more importantly, duetting behaviour develops over a considerable time, often reinforcing an existing relationship. Mechanisms Duets of this nature have variously been thought of as: devices that maintain contact between pairs (Sonnenschein The insect duet & Reyer, 1983); a means of establishing and maintaining territory (Thorpe, 1963; Wickler, 1980; Haimoff, 1986; Conventional signalling by male insects involves the pro- Levin, 1996), with a commitment to the pair bond by either duction of a call of varying length, often in the presence of party (Zahavi, 1977); or, importantly for the discussion competing males. The call has a distinctive temporal pat- included in this review, as a form of mate-guarding tern, which marks the species and may vary in length both (Sonnenschein & Reyer, 1983; Hall & Magrath, 2000). within and between individuals within a population. The In this context, to provide a comparison with the avian signal’s duty cycle is a ratio between signal duration and literature the term ‘pair bond’ is used cautiously here to signal period – effectively how long the call is ‘on air’ for indicate a fixed association between the caller and the any period of calling – and is often consistent across species. duetting partner in insects. In many cases this will lead to Although duty cycle is a relevant concept that may be used copulation, which is the primary function of the duet. The to compare different calling strategies, it has less relevance ‘temporary’ pair bond so established is quite different from for duets where the relationship between the initiating signal a competing male, calling from within an aggregation and and the reply is the major concern. Thus a duet may be attracting a female orientating towards his signal from some initiated by a distinctive calling song of the male, with a distance outside the aggregation. This does not imply a female replying within a time window that is often unique to continuing association between pairs after copulation as a given species (Zimmerman et al., 1989). In this case it is with birds, although this may occur in certain stenopelmatid the temporal aspect of calling that allows recognition. Orthoptera such as New Zealand wetas, in which males Athough the term ‘time window’ has been used frequently form harems (Field, 1993), but at least the use of the term with regard to duetting by phaneropterine tettigoniids to allows a better comparison between insect duets and those define the period in which the female reply is capable of of both birds and primates. initiating male searching behaviour or phonotaxis, the more

# 2003 The Royal Entomological Society, Physiological Entomology, 28, 157–174 Insect duets 159 general term ‘reply latency’ is used in this review (Bailey & with females alternating their calls between the pulsed Hammond, 2003a). phrases of the male call. For example, the North American Insects that have long complex calls initiating a duet katydid, Ambylocorypha parvipennis produces repeated often insert a trigger pulse (Fig. 1) at the conclusion of the phrases that may synchronize or alternate with neighbouring call (Heller, 1990; Bailey & Field, 2000; Stumpner & Meyer, male calls; females insert their replies (Fig. 1) between the 2001). This brief sound may indicate to the female the phrases of a selected male (Spooner, 1968a; Galliart & conclusion of an often variable-length signal, and so may Shaw, 1996). Although insects are able to listen to the act as a cue on which she may reply – the male places a calls of conspecifics while calling (Poulet & Hedwig, 2002), full-stop at the end of its message. in this species females insert their calls periodically between Figure 1 provides a few examples of insect duets, and the calls (phrases or chirps) of the male. The aperiodic Table 1 a list of those duetting insects included in this nature of this interaction is distinct therefore from the classic review. Whereas some insect duets are formed of brief male–male alternation common in this species (Greenfield, interactions between the sexes, others are far more complex 1994b).

Ancistrura nigrovittata () Chrysopa minora (Neuroptera)

Steropleurus stali (Ephippigerinae)

100 ms 500 ms

Poecilimon affinis (Phaneropterinae) 1 s Cicadetta quadricincta (Cicadidae)

Bullacris membracioides (Acrididae)

50 ms 200 ms

Amblycorypha parvipennis (Phaneropterinae) Eucoptura xanthenes (Plecoptera)

1 s

500 ms

200 ms

Fig. 1. A sampler of insect duets. The left-hand column shows three bushcricket (Phaneropterinae) duets, of which the upper two show the influence of a trigger pulse on the female reply following the main call (Ancistrura nigrovittata) and a second with a loud conclusion of the single wing movement (Poecilimon affinis). The almost continuous call of Amblycorypha parvipennis is interspersed with female replies between the pulsed sections of the male call. The centre column shows an example of an ephippigerine bushcricket (Steropleurus stali) duet, in which the female replies with a similar call to the male (upper) and the duet of the bladder grasshopper (Bullacris membracioides). The right-hand column shows three non-orthopteran duets: the lacewing, Chrysopa minora (upper), tick-tock cicada, Cicadetta quadricincta, with the female replying with wing-flicks (centre), and the stonefly, Eucoptura xanthenes (bottom). In each example, male calls are shown in the upper trace, and those of females in the lower trace. All examples are re-drawn from Gwynne (1987), Maketon & Stewart (1988), Henry & Johnson (1989), Shaw et al. (1990), Hartley (1993), Dobler et al. (1994) or Van Staaden & Ro¨mer (1997).

# 2003 The Royal Entomological Society, Physiological Entomology, 28, 157–174 160 .J Bailey J. W.

Table 1. The systematic organization of duetting insects referred to in this review.

Order/Suborder Family Subfamily Genus/Species Author reference within the text Plecoptera Perlodidae Hydroperla crosbyi Need. & Claas. Zeigler & Stewart (1985) Pteronarcys princes (Banks) Zeigler & Stewart (1985) Orthoptera Ephippigerinae Platystolis obvius (Nav) Hartley et al. (1974); Hartley (1993) Ephippigerinae Steropleurus stali (Bol.) Bateman (2001) Ephippigerinae Ephippiger ephippiger (Fieb.) Ritchie (1991) Phaneropterinae Ambylocorypha parvipennis Stal Shaw et al. (1990), Tuckerman et al. (1993) Phaneropterinae Ancistrura nigrovittata (Brunner) Dobler et al. (1994), Heller et al. (1997) Phaneropterinae Leptophyes punctatissima (Bosc.) Hartley & Robinson (1976), Robinson et al. (1986 ), Zimmermann et al. (1989) # Phaneropterinae Poecilimon ornatus (Schmidt) von Helversen et al. (2001) 03TeRylEtmlgclSociety, Entomological Royal The 2003 Phaneropterinae Poecilimon veluchianus (Ramme) Heller & Helversen (1990), Heller (1992) Phaneropterinae Poecilimon affinis (Frivaldski) Heller (1992) Phaneropterinae Scudderia curvicauda (De Geer) Spooner (1968a), Tuckerman et al. (1993) Phaneropterinae Phaneroptera nana (Fieber) Tauber et al. (2001) Phaneropterinae Elephantodeta nobilis (Walker) Bailey & Field (2000) Phaneropterinae Caedicia sp. 12 Hammond & Bailey (2003), Bailey & Hammond (2003b) Acrididae Gomphocerinae Syrbula admirabilis Uhler Otte (1972) Gomphocerinae Chorthippus biguttulus L. von Helversen & von Helversen (1997), Stumpner & Ronacher (1991), Ronacher & Krahe (1998), Balakrishnan et al. (2001) Pneumoridae Bullacris membracioides (Walker) Van Staaden & Ro¨mer (1997) Homoptera Cicadidae Cicadidae Cicadetta quadricincta (Walker) Gwynne (1987) Cicadellidae Balclutha incisa (Matsumura) Nuhardiyati (1998) Gerridae Gerris remigis Say Wilcox & Stephano (1991) hsooia Entomology Physiological Neuroptera Chrysopidae Chrysoperla agilis Henry & Brooks Henry (1979), Henry et al. (2003) Coleoptera Lampyridae Photinus greeni Lloyd Buck & Buck (1972), Buck & Case (1986) Photinus macdermotti Lloyd Lloyd (1966), Carlson et al. (1976) Photinus pyralis L Lloyd (1966), Case (1984), Carlson & Copeland (1985), Buck & Case (2002) Photinus concimilis Green Braham & Greenfield (1996) , 28 157–174 , Insect duets 161

Mechanisms for producing a duet by the female have Homoepisodic events of this nature (Walker, 1969) evolved independently a number of times in insects, and require the individual to detect the signal and then respond. the structures used may be quite different from that used Such behaviour is in contrast to events involving close syn- by males. For example, males of many homopteran cicadellids chrony, in which mechanisms allow the responding insect to and cicadas produce sound or substrate vibration by a tymbal, produce and then modulate a series of repeated signals that whereas females reply with vibrations or even sound created are more or less in synchrony with its neighbour. Response by movement of the wings (Claridge, 1985; Gwynne, 1987). times for this kind of event, resulting in near synchrony, can Among the Tettigoniidae, females may use wing/tegmen be extremely short – close to 5 ms (Galliart & Shaw, 1992) – stridulatory devices that differ from the usual tegmen/tegmen whereas, for duetting systems, the fastest response time by stridulation of males (Robinson, 1990). In this taxon, the female is 15 ms in Ancistrura nigrovittata (Hartley & however, female stridulatory organs appear to have evolved Robinson, 1976; Heller & Helversen, 1986; Heller et al., independently using a variety of devices even within a single 1997) and 20–30 ms in Leptophyes punctatissima (Robinson family (Nickle & Carlysle, 1975; Pfau & Schroeter, 1988; et al., 1986). These rapid response times are comparable Heller, 1990). By comparison, in bushcrickets, such as with the ‘startle’ reactions of flying insects to the sonar of Platystolis obvius (Ephippigerinae) (Hartley et al., 1974; bats, and may be mediated by a reflex that bypasses Hartley, 1993) and Steropleurus stali (Ephippigerinae) information from the brain: noctuid moths, 20–30 ms (Fig. 1) (Bateman, 2001) females have homologous stridula- (Roeder, 1966); arctiid moths, 29 ms (Fullard, 1982); and tory structures on the tegmen to those of males. It can be green lacewings, 40 ms (Miller, 1975). presumed that, just as intense selection through bat predation In bushcrickets, acoustic information is transmitted to has resulted in a plethora of ear morphologies in moths the brain via the fast conducting T-fibre as well as through (Fullard & Yack, 1993), similar levels of selection for alter- descending interneurones to the mesothoracic wing- native calling patterns have resulted in large variations in controlling ganglia. Delay from signal to T-fibre response female stridulatory organs. approaches 10 ms (Rheinlaender et al., 1986), which leaves some 10 ms for processing and the generation of flight muscle contraction. By comparison, in fireflies such as Photinus greeni, in which the male produces a pair of adver- Oscillators and pattern recognition tising flashes, with each flash some 100 ms in duration and 1300 ms apart and with phrases (Buck & Buck, 1972; Buck Signalling by bioluminescent lampyrid beetles was & Case, 1986) with an interval of about 5 s, the female considered in the review of co-operative signalling by answers with a flash of about 200 ms duration and a latency Greenfield (1994a). Greenfield points out how biolumines- of 850 ms. The bioluminescent system is far slower than the cent signals, unlike olfactory signals, are transmitted almost acoustic signal, and females tolerate significant variation in instantaneously and have similar properties of signal to the male signal (Buck & Case, 1986). Indeed, using manu- noise as acoustic signals. The signal does not fade and is ally controlled stimulation of the male’s stimulus phrase, used primarily as a mate-location device (see review by Buck & Buck (1972) found that females accepted a wide Buck & Case, 2002). variance in interphrase interval. Furthermore, females Interestingly, neural oscillators controlling the rhythmic tolerated electronically controlled intervals wider than that nature of both light flashing and sound production may produced in nature. The authors speculate on the reasons have a similar basis. Both are a series of discrete elements for this tolerance, and one explanation may be female grouped into species-specific patterns. The pacemaker motivation (Buck & Case, 1986). A second and simpler neural model producing the rhythmic signal has been explanation is the relatively easy task of flying while flash- described as a key element within the insect’s central nervous ing within uneven vegetation, which may produce its own system (Elsner & Popov, 1978; Carlson & Copeland, degree of variance as perceived by the receiving insect; 1985; Ronacher, 1989). But in the context of a duet it flashes may be randomly obscured by vegetation as the is the female response and the latency of reply that is crucial insect passes behind leaves and branches. for maintaining a duet, or any stimulus–response system During a duet, one sex recognizes the other and alters its such as synchronous and alternating signalling by males behaviour in response; the responding party can change its within an aggregation. The difference between alternating call pattern or its flight or walking path. For example, males and the female reply is that the female reply is far Photinus macdermotti males give a 2–22 rhythm flash from rhythmic; rather, it is the reply latency that appears when patrolling and a 2–42–4– flash sequence when duet- set, and it is this species’ interval that is analogous to the ting with a female or an artificial light source (Lloyd, 1966; male call oscillator. Greenfield’s model suggests that the Carlson et al., 1976). This observation suggests that the timing of responses of interacting males depends on the female is responding to the change in male flash and that responding oscillator, which is triggered by an effector a duet is established between caller and responder leading to delay. This delay in turn is controlled by the velocity of recognition and a temporary pair bond. neural transmission and the duration of the effector ‘activa- Buck & Case (2002) describe the simple duet of Photinus tion’. In other words, there is a minimum delay between the pyralis, in which the flying male emits single flashes in a 6-s receipt or perception of the signal and its reply. rhythm, and the perched female answers each flash with a

# 2003 The Royal Entomological Society, Physiological Entomology, 28, 157–174 162 W. J. Bailey single flash delayed by some 2 s. In general, males do not the neural process setting this latency – the reply time flash in reply but within 0.5 s turn towards the female in window. However, as with the tettigoniid system (Zimmerman response to her signal. The female flash is sufficient to et al., 1989), there will be some time delay in the transfer change the flight path of the male (Lloyd, 1966; Case, of information from the afferent to efferent system. The 1984; Carlson & Copeland, 1985) and the female responds coding of this delay may also be species-specific and be in a characteristic manner, often twisting her abdomen to subject to the same oscillator system as that used in interval direct the light to the male more effectively (Lloyd, 1966). recognition. The focus for duetting among the Orthoptera has been towards bushcrickets and particularly members of the Pha- neropterinae, but duetting is also common among acridid Sex-specific tuning grasshoppers and particularly among the gomphocerines (Acridinae) in which the behaviour has again evolved a Where the mechanism of female stridulation has evolved number of times (Riede, 1987). Early studies of grasshop- independently from that of the male (Hartley et al., 1974; pers indicated that males and females commonly commu- Robinson, 1990), females may often use very different body nicate acoustically during courtship (Otte, 1972). Males set parts to effect sound production, and each body part may up a series of stridulatory signals by repeated movements of have different acoustic properties. Are the carrier or central the hind legs and females recognize and respond to their frequencies of these calls different, and if so is there sex- conspecifics with similar stridulation and complex visual specific tuning of the ears? For species whose males and not displays. Whereas for grasshoppers there is evidence that females call, the ear of each sex is tuned to the carrier the duet provides cues for mate location, it is the paradigm frequency of the call; males must hear the calls of conspe- of species’ recognition that has dominated the literature cifics under selection through male competition, and (e.g. von Helversen & von Helversen, 1983). Remarkably, females must also hear the calls of males in order to locate however, there have been few studies on grasshoppers that a mate. But in duetting species, such as the phaneropterine, examine the role of the duet per se in pair formation. Otte Ancistrura nigrovittata, in which males call with a long series (1972) described the complex courtship behaviour of of syllables and the female provides a brief click in reply, the Syrbula admirabilis, in which female acoustic replies are ears appear to be sex-specific in their tuning. Males of this linked with elaborate visual displays. Otte (1972) supplied species produce a call that has most energy close to 15 kHz no data on reply latencies or, indeed, on the unique role of whereas the call of the female has maximum energy around the female acoustic response as part of a duet. More 27 kHz (Heller & Helversen, 1986). The ears of both sexes recently, observations on song pattern recognition in are broadly tuned and cover both call frequency ranges Chorthippus biguttulus (Balakrishnan et al., 2001) identified (Stumpner, 1997), but behavioural thresholds differ the importance of the unique syllable onset of this species, between sexes; females were most sensitive to calls at which consists of syllables alternating with noisy pauses. 15 kHz and males to replies at 27 kHz (Dobler et al., These authors tested the responsiveness of females to the 1994). Thus the frequency of the male calls best evokes a sound level (dB) of the onset and off-set of the distinctive response in the female and the frequency of the female reply element of the call. Interestingly, there was large variation best induces phonotaxis by the male. As in non-duetting between individuals with respect to both aspects of the call, species, however, males must also be attentive to the calls of but although recognition of the signal’s onset was always conspecific competing males. necessary, there was significant higher variation in responsiveness to the signals off-set. From these data, and an extensive understanding of the Tracking the duetting partner neural processes of signal recognition (Stumpner & Ronacher, 1991; von Helversen & von Helversen, 1997; Figure 2 summarizes the calling and searching strategies Ronacher & Krahe, 1998), a simple model for the mechan- used by duetting insects based on a scheme devised by ism of syllable-pause detection emerged (Balakrishnan Spooner (1995). As already indicated, by far the commonest et al., 2001). At least two processes were involved: first, the behaviour is for males to track responding females, as detection of signal onset and, second, the detection and/or illustrated by many duetting Plecoptera, Orthoptera, rejection of pauses longer than 30 ms at 30 C. One mechan- Homoptera, Neuroptera and fireflies. However, in some ism set up the response/recognition process and the other species, females may begin searching once males are close, recognized an appropriate signal. Onset detection may and thus as the perceived intensity of the male call increases, involve neurones that respond phasically to changing so too does the likelihood of females increasing their search intensity levels at the start of the signal, although the detec- behaviour. But as indicated above, many male insects tion of long pauses may involve more than one neurone. reduce the intensity of their signals once a female has been Such neurones may be activated by continuous noise, or attracted. For example, the bladder grasshopper, Bullacris sounds with high duty cycle and the response of the unit membracioides, with its extremely loud call and wide- would be added to that of the syllable onset-detector at the ranging search strategy, reduces call intensity once it has next level of processing. Whereas female response latency heard a female reply (Van Staaden & Ro¨mer, 1997). appears relatively fixed, these authors do not comment on The behaviour is also common among the duetting

# 2003 The Royal Entomological Society, Physiological Entomology, 28, 157–174 Insect duets 163

Male Female

Male calls and moves to answering female (a)

Male moves to low Female moves to intensity female reply high intensity call (b)

Sexes far apart

Male moves to high Female moves to intensity female reply low intensity call (c)

Sexes close together

Male and female move together (d)

Fig. 2. Calling and searching strategies of duetting insects: (a) male calls and females replies – males search for a stationary female; (b) male calls and female replies – males search for females but as the male approaches and the intensity of the call increases, the female moves towards the male; (c) female moves towards the calling male and as the female approaches the male begins to search; (d) both males and females have equal calling, answering and searching roles. The broken lines indicate phonotaxis close to the target sex (redrawn after Spooner, 1995). phaneropterines such as Poecilimon ornatus, in which males tional difference is that, whereas in non-duetting species the reduce call intensity as they approach the female (von insect merely turns to the most stimulated side (serial Helversen et al., 2001). More rarely, males change their processing – Pollack, 1986; Schul et al., 1998), in duetting calling rate once they have entered a duet with the female. species the key recognition element is the female reply For example, male Steropleurus stali double the call rate within a specific time window. Hence, when two clicks once duetting commences (Bateman, 2001), a situation arrive from different directions and at different intervals, paralleled by the change in flash frequency of many fireflies the outputs of the left and right neuronal recognition (Buck & Case, 2002). network should be equal (von Helversen et al., 2001). von Among phaneropterine tettigoniids, females as well as Helversen et al. (2001) suggest that duetting evolved at the male Amblycorypha parvipennis (Spooner, 1968a; Shaw expense of poor acoustic orientation owing to the reliance et al., 1990) and Elephantodeta nobilis (Bailey & Field, on the limited information contained in short clicks. But the 2000) track the duetting partner, and either sex may also ambivalent actions of male P. ornatus might arise if males track a stationary broadcasting loudspeaker (Galliart & decided, at the last possible moment, that one or another of Shaw, 1996). Male A. parvipennis form choruses with the females might have already had a duetting partner too males alternating or calling in near synchrony with other distant for the moving male to detect. At a different level, neighbouring males. But one male may lead the other within Bateman (2001) found that male Steropleurus stali were the chorus (Greenfield & Shaw, 1983; Shaw et al., 1990), significantly more accurate in their phonotaxis and faster and in this situation the female click is inserted between than females. Females varied in their speed of approach; phrases (Shaw et al., 1990). Males may move towards the virgin females tended to be much faster and more accurate female click, but if the female does not perceive the male as than non-virgin females. Although non-duetting females moving she may commence searching (Spooner, 1995; orientated and approached the male call, they were far less Galliart & Shaw, 1996). accurate in their approach than females engaging males in a Although nocturnal insects are expected to use acoustic duet. The duet clearly enhanced the speed with which the cues alone for orientation, there is an increasing literature sexes were brought together. that suggests that, even at low light levels, orientating males The acoustic duet in many cases allows the participants to or females augment the acoustic cue with vision; they take a estimate distance between initiator and respondent and, fix on parts of the habitat close to the sound source (von potentially, any estimation of distance may be under Helversen & Wendler, 2000; Bailey et al., 2003). Remark- significant selection through predation. Zimmermann et al. ably, when male Poecilimon ornatus are presented with two (1989) showed how male Leptophyes punctatissima would female calls at different intensities, and with different only respond to their female duet within a very narrow time latencies relative to the male call, the track bisects the two window, which was 25–55 ms after its own call. As a result, calling positions. Interestingly, and unlike A. parvipennis, the male failed to track clicks indiscriminately or sounds the time difference between two male calls can be up to unrelated to its own call; they would only track females that 80 ms with no effect on female call preference. The sug- were close. The time for sound to travel between duetting gested reason for the males’ inability to resolve this direc- partners is about 3 ms for every 1 m. The experimentally

# 2003 The Royal Entomological Society, Physiological Entomology, 28, 157–174 164 W. J. Bailey determined largest delay for L. punctatissima is about 45 ms, (Maketon & Stewart, 1988). Virgin female stoneflies duet so that the travelling time of the call and the reply to and with males where communication distances may be up to from a calling male, at similar temperatures, cannot exceed 8 m on a suitable substrate (Abbott & Stewart, 1993) and, 20 ms, which is equivalent to about 3.3 m separation. For once the male perceives the answering female, he walks these tiny insects in their complex leafy vegetation this may rapidly to the sound source. Female Hydroperla crosbyi represent a substantial distance. reply to the male’s initial call with numerous drumming Similar calculations were made for Poecilimon ornatus replies, but as contact is established reply rate declines (von Helversen et al., 2001) in which, by using a walking (Zeigler & Stewart, 1985). In species such as Pteronarcys compensator (Weber et al., 1981), it was established that princeps, the female reply can overlap the end of the male males responded optimally, both in their preparedness to call, but more often is separated from the call by a latency engage in phonotaxis and in the speed (velocity) of their of some 400 ms. The sequence of the duet in many species walking movements, to female responses close to the mean can be extremely variable with male calls simply followed reply latency in nature. For searching males a female reply by the female (m/f) or a sequence of replies (m/f/m/f/m) or latency of some 60–70 ms would still arrive within the male’s (m/f/m/f) (Zeigler & Stewart, 1985). phonotaxis time window when females were as far away as 8–10 m. Orthoptera. Substrate vibration or tremulation is Duetting may be seen as one strategy that increases the common among bushcrickets and katydids (Belwood, effectiveness of sound transmission, but whereas the 1990). Although a number of species have been described initiating signal may be efficient in terms of information as performing tremulation (Sismondo, 1980; Morris & transfer, its effectiveness is limited by the male’s ability to Beier, 1982; Morris et al., 1988) this mode of calling varies detect the female reply. Often female reply signals are far from distance signalling, with no part played by the female, lower in intensity than the male call. The case of duetting in to a distinct duet, with females responding to male tremulation the South African bladder grasshopper, Bullacris membra- in a similar manner to that described for other tettigoniids. cioides (Orthoptera; Pneumoridae), is perhaps an extreme Signalling in stenopelmatidid (wetas) and gryllacridid example of signal difference between the sexes in which the (raspy crickets) Orthoptera is often in association with very low-frequency male call can be transmitted over several both defence and mating and may involve femur/abdominal hundreds of metres and orders of magnitude greater than stridulation (Rentz & John, 1990; Field, 1993) or drumming the effective calling range of the female (Van Staaden & with the hind leg (Field & Bailey, 1997). The former is more Ro¨mer, 1997). often associated with defensive signals, whereas the later is Finally, are duetting species more accurate in their ability often used in courtship. In an undescribed nocturnal species to find the calling target than those that do not duet? Unlike of the Australian genus Ametrus (Gryllacrididae), the male the extensive work on cricket (Grylloidea) phonotaxis signals by drumming its hind leg on the substrate and the (Gerhardt & Huber, 2002), there has been little work on female sets up a duet with a similar drumming with a reply the accuracy of searching by duetting bushcrickets. How- latency of some 700 ms; the male moves towards the female. ever, where phonotaxis paths have been calculated, males Males will respond to each other, or even to an artificial appear remarkably accurate in an open arena (Bailey & stimulus, and females that are able to recognize a close male Field, 2000) or on a motion-compensating wheel (von call will follow this signal. It is unclear as to whether the Helversen et al., 2001). pair bond so formed allows the female to assess the male or is simply a device to bring the sexes of a given species together (Field & Bailey, 1997). Duetting and the use of substrate vibration Hemiptera. Substrate signalling is common among plant Information may be transmitted through a substrate by hoppers (Delphacidae), leaf hoppers (Cicadellidae) and frog longitudinal waves generated in the substrate, which may hoppers (Cercopidae), and the production of alternating be water, the surface of the ground, plant stems, leaves and calls by courting cicadellid and delphacids has been noted silk webs (Rovener & Barth, 1981; Michelsen et al., 1982; on numerous occasions as part of the courtship sequence Bailey, 1991; Greenfield, 2002; Cokl & Virant-Doberlet, (Shaw et al., 1974; Ichikawa, 1976; Shaw, 1976; Claridge, 2003). As with airborne signals, substrate duets differ 1985; for a review see Cokl & Virant-Doberlet, 2003). Leaf slightly from standard courtship signalling – there is low and plant hoppers, like their cicada relatives, have small variance in reply latency. For example, there are many tymbals whose action is transmitted to the substrate by the reports of plant bugs, including pentatomid stink bugs of legs or in some cases via the mouthparts (Nuhardiyati, the genus Nezara, using substrate vibration as a cue for 1998). Importantly, as in many true duetting species, the mate location (Cokl et al., 2000), but there is no indication reply of the female attracts the male. For example, in the that courting pairs use a duet format. cicadellid leafhopper, Balclutha incisa (Nuhardiyati, 1998), females spontaneously call in short irregular bouts with a Plecoptera. More obvious duetting systems using sub- call length of about 200 ms, but when duetting with a male strate-transmitted signals are found among stoneflies these bouts become distinctly periodic and last 150–200 ms.

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Once males hear a replying female they walk or fly to plant tion – female call preference and male–male competition – stems close to the reply, and then perform complex court- to produce long or more complex signals. In such cases it is ship sequences that may eventually lead to mate-guarding only males that call, and mute females search for and behaviour. choose between potential mates on the basis of longer Arnqvist (1997) describes two mating tactics in water bouts of calling, call length, signals repeated at a higher striders (Gerridae). One tactic is for males to search for rate or loudness (for a useful review see Greenfield, 2002). and then overpower females (Sih et al., 2002), and a second As predation risks increase so call length should decrease, involves males signalling from a suitable plant-oviposition or at least those elements of the call that most attract either site by creating ripples on the water. These are detected and parasitic flies or gleaning bats (Fig. 3b); male calls may answered by females and other males (Wilcox, 1972). The become short and extremely infrequent. There are convin- use of surface vibratory signals would appear an ideal mode cing arguments from studies on crickets (Zuk et al., 2001) as for two-way communication but it is the gerrids that well as bushcrickets (katydids) (Morris, 1980; Belwood, illustrate an intersexual communication system that most 1990) including comparative studies of phaneropterine closely resembles a duet (Nummelin, 1987). Although species (Heller, 1992) that suggest call length is under strong females may call spontaneously, it is the male that signals selection through such predation events. his readiness to mate over a distance many times his body If call length decreases through natural selection then length. In this case, as the female approaches, the surface searching strategies of females may also change – there waves increase in frequency but reduce in amplitude. will be less information on which to base call preference Females answer the male call with a distinct courtship signal and females will have less directional information for pho- before accepting the male. notaxis (Fig. 3b). So, where calls are extremely short, one Mating risks for signalling and copulating water striders tactic would be for females to develop alternative answering appears to be high, mainly from backswimmers (Notonec- systems that provide an auditory cue for competing males tidae) (Arnqvist, 1989; Rowe et al., 1994) and frogs (Fig. 3c). The duet so formed now places both calling and (Fairbairn, 1993). Both predators detect their prey by searching functions on the male; females may choose surface ripples. Interestingly, the production of vibratory between males on the basis of call. But short signals from signals by the water strider, Gerris remigis, during copula- males have little information and there is experimental tion appears to reduce attempts by intruding males to evidence to suggest that females can be extremely nondis- interrupt copulation (Wilcox & Stefano, 1991) and, criminatory in their replies (Heller et al., 1997; see Fig. 3, although this is not a device incorporated within the duet, central abcissa). For example, duetting female Leptophyes the behaviour is an example of copulatory mate-guarding punctatissima respond to any ultrasonic click (Hartley & (see discussion below). Final evidence for the mate-guarding Robinson, 1976), and female Ancistrura nigroviatta even hypothesis comes from the reduction in male call intensity respond to clicks and initial calls of other species (Dobler once a duet has been established, and examples of this et al., 1994). Spooner (1968b) describes how some species of behaviour are described in the next section. bushcrickets respond to and track simple finger clicks. One hypothesis that explains this phenomenon is that such Neuroptera. Lacewings duet by tremulation (Henry, 1979, indiscriminate behaviour has evolved in response to males 1980) and duetting appears to be a necessary precursor to rather than females taking on the searching role; species’ copulation (Henry & Wells, 1990). As with the substrate sig- recognition is now based on reply latency (Robinson et al., nalling of leaf and plant hoppers, each species’ song is unique. 1986; Zimmerman et al., 1989). But, as with the often- In a typical song species such as Chrysoperla agilis,malesor quoted story of firefly ‘femmes fatales’ (Lloyd, 1975), the females may initiate displays by a vertical movement or vibra- system would appear to be open to exploitation by preda- tion of the abdomen producing signal volleys of about 3–6 s tors, and, in the context of this review, to eavesdropping duration and repeated every 7–13 s (Henry, 1979; Henry et al., males. 2003). If an individual of the opposite sex is sexually receptive Once the female answering system has evolved as part of and within about 15 cm, it answers the call with a volley of its a duet and selection is reduced from predation events, then own. As with duetting phaneropterine tettigoniids the interval it can be predicted that selection should lead to female between each burst appears sex- and species-specific. preferences for calling traits that best reflect male quality (Fig. 3d). As females no longer have the exclusive searching role, as in non-duetting species, the only indication of female preference will be her reply – either its timing or its The evolution of duetting behaviour length. An increase in reply length may provide the male with more information with which to conclude an effective Calling strategies – why duet? search. As predicted, females of many duetting species show significant variation in reply length. For example, within the Figure 3 illustrates a scenario that describes the conflict- Ephippigerinae (Bradyporinae, Tettigoniidae) the female ing evolutionary pressures on the signalling process and call is almost the same length as that of the male (Bateman, particularly the length of the male signal. At one extreme 2001); moreover, in many phaneropterine bushcrickets (Fig. 3a) males may be under selection through sexual selec- female reply length varies within and among species and,

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SelectionNon-duetting species Selection

Increase in call length (a) Male costs Female advantage

Predation risks Female choice Metabolic energy Male competition Costs of competition Cues for searching

Female searches

Decrease in call length (b) Male advantage Female costs

Reduced predation risk Reduced cues for searching Reduced metabolic energy Reduced cues for choice Increased predation risks Male costs

Complex call interaction Fewer cues for female attraction

Sex role reversal in calling and searching

Duetting species

SelectionIncrease in call length Selection

Male searches Fig. 3. The evolution of duetting behav- iour and selection on male call length (c) Male advantage Female costs among duetting and non-duetting insects: Reduced predation risks Energetic costs - calling as sexual selection (female choice and Reduced metabolic energy (Short male calls) Predation risks male competition) on male call length in Reduced searching costs non-duetting species increases (a), so male signals lengthen. Counter selection through natural selection, such as energy costs and Female advantage (d) Male costs (Long male calls) predation, results in a reduction in male call length with resultant increased costs Female choice Predation risks to the female (b). Searching roles reverse Metabolic energy Male competition and as duetting evolves sexual selection on Costs of competition Cues for searching male call length increases with the result that male calls become longer (d). Finally, both sexes may take on a searching role Males and Females Search (c and d). importantly, within individual females (e.g. Tuckerman linked with a female reply, this system may equally be et al., 1993). However, searching roles may change with derived from long-calling species subject to high levels of the insect’s ecology and, whereas it is more common for predation. This is a suggested route illustrated in Fig. 4. As males to search for responding females, when the male fails call length increases, the main determinant of female choice, to find the female or when sex roles are reversed (females which is species’ recognition, can again be borne by the become competitive for access to males) females may both male. The result is that reply strategies become dynamic call and search (Spooner, 1995; Bailey & Field, 2000; (see Gerhardt, 1991) and open to selection through female Bateman, 2001; see Fig. 3(d) here). choice. To support this scenario, Heller (1990) suggests that Heller (1990) proposed a scenario for changes in call long-calling in duetting species is derived from short-calling length in duetting and non-duetting species of the phaner- ancestors. If females vary the duration of their signal in opterine tribe Barbitistini, which is supported in part from response to variable male call parameters, at least theoretic- phylogeny. The system is redrawn in Fig. 4. Although Heller ally there is the possibility to test for sexual selection on suggests that the most primitive call type is the short call male call structure.

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Duetting species Non-duetting species Trigger

(6) (7)

(5) (8)

(3) (9)

(4)

(10) ?? (2)

(1)

Fig. 4. Heller’s (1990) reconstruction of the possible evolution of duetting and non-duetting songs of the Barbitistini (without the genus Isophya) (Phaneropterinae: Tettigoniidae: Orthoptera). Heller suggests that the ancestral form is at (1), and an alternative is presented in the text that call length could be reduced through selection from predation and therefore the ancestral form might have been at (8) evolving to (10) (broken arrow with question marks). Duetting species increase call length and employ marking devices for the female reply such as loud endings of the call (4) and eventually a trigger (6). Heller discusses the significance of post-trigger pulses in (6) and this is amplified here. (2) Phonochorion satunini; (3) Phonochorion uvarovi; (4) Poecilimon sp. Type A.; (5) Barbitistes sp. Type A; (6) Barbitistes sp. Type B; (7) Poecilimon sp. Type G; (8) Poecilimon sp. Type H; (9) Poecilimon sp. Type G; (10) Poecilimon sp. Type F. Redrawn and simplified after Heller (1990), including Heller’s classification of the Barbitistes and Poecilimon song types.

Sexual selection – female call preference better nutrient reserves can do this faster than smaller males; male size, at least theoretically, should be linked Although many song characters may be under stabilizing with spermatophylax size and therefore should be preferred selection through species’ recognition, others are more by nutrient-seeking females. dynamic, show greater levels of variance within and Perhaps the first to evaluate female call preference out- between males of the same species and, in some cases, are side the species’ choice paradigm were Tuckerman et al. linked with traits that may have direct or indirect benefits to (1993) using the North American bushcricket, Scudderia the female. Thus for non-duetting species, although there is curvicauda. Male S. curvicauda have a call that consists of increasing evidence showing female preference function a series of phrases, with each phrase increasing in syllable among signalling insects, the ability to separate these call number. The female response is a series of ticks in rapid elements from more dynamic and less reliable traits is succession following each phrase of the male by some difficult (Jennions & Petrie, 1997; Ritchie, 2000). One 800 ms (Spooner, 1968a). A female may respond to any problem relates to call intensity, which for most species one or more phrases in the male’s call and, on hearing a appears to have an over-riding influence over female pre- female signal, the male either continues to call with an ference (Bailey et al., 1990). Whereas the trait may reflect increasing number of syllables within each phrase, or starts male size, and therefore be a useful trait linked in some way the call over again. The male then lowers the intensity of the with male quality – perhaps the ability to provide direct call, repeating the duet until the pair is in contact. benefits to the female through a nuptial gift – a loud signal is Tuckerman et al. (1993) established that the mean more likely to indicate male distance (Forrest & Raspet, 1994). number of syllables per phrase, and the number of syllables The direct benefits provided by the energy-rich sperma- in the longest part of the last phrase, were stable and could tophylax of male bushcrickets have allowed workers to be considered the most likely indicators of male quality. manipulate the insect’s ecology to the point at which sexual Although there was no relationship between male mass role reversal results in intense female competition for access and eight measured parameters of the call, there was a to males (e.g. Gwynne & Bailey, 1999). Thus in most positive relationship between male size (pronotum length) bushcricket species the male-donated spermatophylax, and four of the eight characters. These authors found that which forms part of the spermatophore, acts as a nuptial the mean number of syllables per phrase was the best pre- gift and may contribute directly to the fitness of the off- dictor of male size; females responded with most clicks and spring (Bowen et al., 1984). Mated males that re-mate must more often to male calls with more syllables per phrase. This replenish the spermatophore and usually larger males with preference was maintained throughout the experimental

# 2003 The Royal Entomological Society, Physiological Entomology, 28, 157–174 168 W. J. Bailey period. However, although the driver for this preference Hence, male mating success and thereby its fitness should be was predicted to be the size of the nuptial gift, there was proportional to flash rate provided that flash number and only a weak correlation between male size and spermato- flash duration approximated the species’ mean. The phore mass. Despite this, the evidence exists for female combination of stabilizing and directional selection on flash preference on male call traits and this research opens an duration and rate, respectively, suggests that flash rate and experimental paradigm that should be exploited. length may be under selection through female preference. In a second North American bushcricket, Amblocorypha parvipennis, Galliart & Shaw (1996) found that, at least in part, male mating success was the result of female choice. Latency, conflict and mate-guarding A. parvipennis is unusual in the way it duets. Males call with repeated phrases that may synchronize or alternate with When male call length is under selection through female neighbouring male calls, and females produce quiet ticks choice, it may also be predicted that males unable to in response to one male at the end of its call (Shaw et al., produce long calls, perhaps due to high energy costs or 1990). In earlier studies, males that were successful in predation risk, may adopt alternative mating tactics (for a mating produced longer and louder calls and longer phrases wider discussion of alternative male behaviour see Gross, and/or were leaders more frequently than followers in male/ 1996). Furthermore, if alternative tactics have evolved in a male interactions (Galliart & Shaw, 1991, 1992). These mating system, then a second prediction is that males able authors showed, in the later study, that females moved to to produce a full signal should defend their opportunities to computer-generated signals showing the same characteris- mate by mate-guarding or its equivalent (Thornhill & tics as natural populations of males. However, female Alcock, 1983). Recent attention has been given to the role tactics in responding with a tick to more than one male of the duet in mate-guarding in some birds, with the may simply be to bring more males into contention and so function of the duet being protection of male paternity increase the opportunity for effective female choice (Shaw (Sonnenschein & Reyer, 1983; Hall & McGrath, 2000). et al., 1990). One hypothesis is that males should increase the use of the Finally, there is equivocal evidence of female call duet when the female has been fertilized by the duetting preference in the phaneropterine bushcricket, Phaneroptera partner. Hall & McGrath (2000) pointed out that this pos- nana, in which preference is compounded by call intensity sibility had not been tested, and addressed the question by (Tauber et al., 2001). P. nana has a very different call type to using the Australian magpie lark, a species in which both A. parvipennis, illustrating the more usual phaneropterine sexes can initiate the duet. Their approach, using genetic system of relatively short and isolated male calls followed markers, could be applicable to the diverse duetting strat- by the female response. However, females may track males egies of the phaneropterine tettigoniids. without duetting – effectively mixing duetting and non- In reviewing reply latencies and calling lengths in a range duetting calling strategies. In this case duetting females of insect species using both sound and light, a positive and responded to loud calls regardless of pulse number within significant relationship between call-length and reply a chirp, but non-duetting searching females preferred their latency was found, which was independent of phylogeny own geographical song race and, moreover, moved towards (Bailey & Hammond, 2003a). This observation suggests songs of another race when played in a two-speaker trial that one cost of providing more information is a delay in 10 dB higher than the female’s own race. This situation the female reply. In a meta-analysis, with phylogenetic con- parallels that of the non-duetting bushcricket Ephippiger trols, Bailey & Hammond (2003a) raised the possibility that ephippiger (Ritchie, 1991). Curiously, duetting female any increase in latency may be associated with increased P. nana responded preferentially to males producing longer risks of vulnerability, particularly from eavesdropping calls when presented with two competing males. With spe- males. In this way, competitive males may either use the cies’ recognition driving female preference, it would appear duet as a cue to move towards the pair (eavesdropping) or that the duetting system is resistant to intraspecific to intercept the female by remaining silent, as do many exploitation; in other words, species’ recognition is of such acoustic insects and frogs (crickets: Cade, 1979; Rowell & high priority that female choice for call traits that may Cade, 1993; grasshoppers: Otte, 1972; Greenfield & Shelly, reflect male quality is either of little consequence or of low 1985; Shelly & Greenfield, 1985; stoneflies: Abbott & priority. Stewart, 1993; frogs: Perrill et al., 1982; Gerhardt & Huber, Evidence for selection from female choice that is indepen- 2002). Eavesdropping is when a receiver extracts information dent of signal power comes from studies of the biolumines- from an interaction in which it takes no part (McGregor, cent displays of the Nearctic firefly species, Photinus 1993; Doutrelant & McGregor, 2000). Alternatively, a male concimilis. By using an optical playback system, Branham may use the silence between initiating call and female reply to & Greenfield (1996) found that females preferred flashes of insert a distracting signal that induces the female to both males that were flying slowly 1–3 m above the ground. The respond and search for the satellite (Bailey & Field, 2000). favoured males exceeded the mean population flash rate, The phaneropterine Elephantodeta nobilis provides an but females also preferred flash lengths that approximated example of the latter tactic (Fig. 5a). Satellite males insert the population mean. Flash rate varied within the popula- a short call just before the trigger pulse of the calling male, tion and was independent of both flash number and length. causing the female to shift the recognition time window of

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1968a; Galliart & Shaw, 1991). Nevertheless, experiments (a) on male countermeasures are rare and, until the recent work on an undescribed Australian bushcricket, Caedicia sp. 12 Male (Hammond & Bailey, 2003), evidence of males providing any countermeasures was non-existent. Experiments with this insect using play-back designed to test hypotheses on eavesdropping required the computer acoustic model to be controlled both by the male initiating signal and the female Satellite reply – the computer-generated signal needs to be ‘intelli- gent’ (see Hammond et al., 2003). Males defend the female reply, once it engages in a duet, by concluding the duet with a masking signal several decibels louder than either the initiating signal or the reply (Fig. 5b here; Hammond & Female Bailey, 2003). The production of a mask, which is an apparent mate-guarding activity, implies that the duet is vulnerable to takeover in nature. In this species males call in loose aggregations on flowering acacias. Such mobile aggregations might allow males to eavesdrop on duets 1000 ms with relative ease, particularly when densities are high. The defensive call has little effect on the female as she has (b) already responded to the male call and has either induced her partner to search or has begun to search herself. Male Using a two-speaker design, Hammond & Bailey (2003) reported how males searched for females within a duet when the male call came from one speaker and the female reply from the other. They then used the male masking call, which was added to the male duet signal. Intruding males that heard the mask failed to search, implying that the mask was an effective mate-guarding device. Female Caedicia produce a reply to the male call with a varying number of Female clicks within a specific time window. The presence of the mask by the duetting male, which is close to the specific time window of the female reply, suggests that once the pair bond is established, the male reduces the effectiveness of a longer reply by the female, which may be a trade-off as he

500 ms uses this call to locate the female, but reduces the chance of eavesdropping. Fig. 5. Alternative male calling tactics and male defensive behav- An alternative tactic that defends the initiating male’s iour in two phaneropterine bushcrickets. In Elephantodeta nobilis signal by reducing reply latency is the use of a trigger (a), the initiating male concludes its signal with a double trigger pulse (Heller, 1990; Stumpner & Meyer, 2001; Bailey & pulse, which is used by the satellite male to insert a short call. The female replies with her species specific latency set to the satellite call Hammond, 2003b). Species with extremely short reply rather than the initiating male (Bailey & Field, 2000). In (b), a male latencies are effectively defended by the nature of this time of Caedicia concludes its call with an extremely loud chirp, which is window (Zimmerman et al., 1989); no other male can timed immediately after the first female reply. This call masks the respond fast enough to insert a distracting signal. remaining calls of the female to other males and inhibits eavesdropping males (Hammond & Bailey, 2003). Natural selection – costs of calling and searching

Predation on calling insects consists largely of attack from parasitoid flies (Tachinidae), or from foliage-gleaning the reply some milliseconds earlier. The success of this tactic bats on nocturnal prey, and although it is assumed that was shown in a two-speaker trial, in which females were searching by females involves costs of predation (Hedrick presented with a calling male from one speaker and a satel- & Dill, 1993), there have been few studies that show lite male from the other. Females able to search on an open searching is indeed costly (but see studies on scorpionflies arena moved towards the satellite at least some of the time by Thornhill, 1978). Empirical field data supporting (Bailey & Field, 2000). hypotheses concerning searching risks to duetting species Evidence of eavesdropping is often circumstantial, but come from a study of the Australian tick-tock cicada, has been observed for duetting bushcrickets (e.g. Spooner, Cicadetta quadricincta (Gwynne, 1987), whose males call

# 2003 The Royal Entomological Society, Physiological Entomology, 28, 157–174 170 W. J. Bailey and females make an acoustic reply by wing flicking. In this extremely vulnerable, perhaps to eavesdropping by satellite case the female remains stationary while the male calls and males or simply by females moving and mating with flies to the answering female. Gwynne was able to show that competing males. However, it is argued in this review that the risks of searching males being trapped in spiders’ webs where costs of calling and searching are high, perhaps was highly significant; samples of cicadas in webs were through directional selection of female call preference, and significantly male biased (23 : 2). However, more indirect such costly signalling also carries the risk of takeovers by evidence comes from studies in Central America where other males, then defensive tactics should evolve. Although forest katydids were preyed upon by foliage-gleaning bats there have been numerous reports of the natural history of (Belwood & Morris, 1987). Middens of these bats contained this event in both fireflies and orthopteran insects, there insect material of which some 40% included tettigoniids. have been few experiments to test this hypothesis. Although females of the species found in these middens As is so often the case, insect and frog mating systems are mute, about 50% of the material consisted of female have the advantage when it comes to testing more general katydids; there was no evidence as to how these females hypotheses generated from behavioural studies of higher were located but it is highly likely that they were picked up vertebrates (Gerhardt & Huber, 2002). Given the ‘simpler’ by incidental sounds made as they moved through the system in insects, the formation of temporary pair-bonds vegetation. On two occasions, once in the rainforests of often resulting in a single mating as well as the ability to use southern Thailand and more closely during phonotaxis large and manageable sample sizes both in the laboratory trials of the phaneropterine duetting Elephantodeta nobilis, and the field, there should be an opportunity to test hypoth- the leaf-shaped females have been observed (unpublished eses concerning duet behaviour generated from the huge observations WJB) to flatten themselves against the sub- avian literature. strate after each reply to a male. Such behaviour would A recently unpublished review of duetting behaviour in presumably lessen their ‘visibility’ to foliage-gleaning bats. birds (A. Rogers, M. Hall & D. Mennill, unpublished report If there is differential selection on each sex, either through from the duetting workshop of the 9th Congress of the Inter- calling or through searching, then we would predict that national Society of Behavioural Ecology 2002) suggests that there would be different levels of survival. Two species of hypotheses relating to duetting appear diffuse with few for- the phaneropterine genus Poecilimon provide data on malized and testable predictions. It is rare to find good long- differential survival assessed through mark and recapture term avian studies that address specific questions relating to (Heller & Helversen, 1990). P. veluchianus is a non-duetting the role of the duet as it influences individual mating success. species in which males call and females track the male. By Furthermore, there is a need to look at costs and benefits of contrast, P. affinis duets and males search for replying participating in a duet at the level of the individual rather females. There was no difference in survival between the than the pair. Why would one duet rather than sing alone? sexes for P. veluchianus; by comparison, female survival was This review on insects has attempted to apply our knowledge significantly higher for P. affinis, in which males take on of duetting behaviour to some of these hypotheses. Missing, risks of both calling and searching (Heller, 1992). as with the avian studies, are critical experiments comple- Is the evolution of duetting associated with temperature? mented by molecular techniques now used so widely in other For poikilothermic , courting and mating during areas of behavioural ecology. the day may be less energetically costly, particularly in temperate Mediterranean climates, than for nocturnal signallers. Studies of the tettigoniid genus Poecilimon show Acknowledgements that species that have mute females, whose males call and females search, are restricted to night-time calling (Heller & I am grateful to Amy Rogers for the notes discussion Helversen, 1993). By comparison, species that duet call both contained therein from the duetting workshop conducted at during the day and during the night, and two of the species the Montreal Congress of Behavioural Ecology. I am also call almost entirely during daylight hours. Reduced grateful to Charles Henry for comment on lacewings. Much exposure to diurnal predators allows these species to make of the energy and substance for this review comes from most use of warmer daytime temperatures. studies conducted on the duetting behaviour of Australian bushcrickets as part of an ARC-funded studentship to Tom Hammond. The manuscript has been improved by critical Conclusions and future directions comment from Henry Bennet-Clark and John Alcock and by two reviewers. Duetting among insects appears to be an evolved response to limitations imposed on male signalling, principally by predation. The male signal is costly, but so to is female References searching behaviour, and as male signals become shorter, with less signal redundancy, so the costs of female searching Abbott, J.C. & Stewart, K.W. (1993) Male searching behaviour of increase. Unlike in birds, in which a pair bond is established the stonefly, Pteronarcella badia (Hagen) (Plecoptera: Pteronar- and maintained by the process of duetting, in insects the cyidae), in relation to drumming. Journal of Insect Behavior, 6, temporary pair bond formed as males and females duet is 467–481.

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