10 Acoustic Communication in Neuropterid Insects

Home , Ascalaphidae, Eremochrysa, Megaloptera

Charles S. Henry

CONTENTS

Introduction ...... 153 Neuropterida ...... 154 Types of Acoustic Communication in Neuropterida ...... 155 Acoustic Communication in Megaloptera and Raphidioptera...... 156 Megaloptera: Sialidae and Corydalidae ...... 156 Sialidae ...... 156 Corydalidae ...... 157 Raphidioptera: Raphidiidae and Inocelliidae ...... 157 Perspective ...... 157 Acoustic Communication in Neuroptera ...... 157 Sisyridae and Coniopterygidae ...... 158 Sisyridae ...... 158 Coniopterygidae ...... 158 Perspective ...... 158 Berothidae ...... 159 Hemerobiidae ...... 159 Chrysopidae ...... 159 Stridulation ...... 159 Wing Fluttering ...... 160 Percussion ...... 161 Tremulation ...... 161 Cryptic Species ...... 162 Speciation ...... 164 Overview ...... 165 Acknowledgements ...... 166

INTRODUCTION Insects are noisemakers. Their hardened exoskeletons click and tap or grind and crunch with nearly every movement, much like mechanical toys madeofplastic. Insects and other arthropods are predisposed by their ground plan for acoustic communication, especially through stridulation (the rubbing of body parts together), and they have independently evolved an extraordinary array of sound-producing devices (Ewing, 1989, p. 16). Their noises, songs and music often appealtoour own auditory sensitivities,and havebeen the subject of muchdescription, analysis and experimentation (reviewed in the current volume and in manyotherworks, e.g.Pierce, 1948; Alexander, 1960; Busnel, 1963; Otte, 1977; Lewis, 1983; Ewing, 1989,Bailey, 1991; Bailey and Ridsdill-Smith, 1991; Gerhardt and Huber, 2002; Greenﬁeld, 2002). Yet clearly audible songs are

153 154 Insect Sounds and Communication: Physiology,Behaviour,Ecology and Evolution not evenly distributed across the 28 orders of insects. Orders such as Orthoptera and Hemiptera are repletewith singing species, but others are nearly mute. The superorderNeuropterida, comprising the ordersRaphidioptera(snakeflies), Megaloptera (dobson- and alderflies), and Neuroptera (lacewings), is arelatively silent taxon. Although insectsare preadapted for airbornesound production, several constraints affect the audibility of their acoustic signals and strongly influence the evolution and phylogenetic distribution of such signals.The best-known factor is body size. Insects need to be small due to surface-area-to- volume considerations which reduce the effectivenessofthe exoskeleton and the tracheal system at larger body sizes. Smaller sizes in turn reduce the efficiency of energy transfer from the body to the air during sound production (Bennet-Clark, 1998). Therefore, communication using airbornesound should be limited to relatively large insects, as exemplified by crickets, katydids, grasshoppers (Orthoptera, Greenfield, 1997) and cicadas (Hemiptera, Bennet-Clark and Daws, 1999). Aless recognised constraint on sound production is the sclerotisation of an insect’s body. Hard-bodied or heavily armoured insects can produceloud airborne sounds quite easily,whereas soft-bodied insects, even the large ones, will be lessable to sing, especially via stridulation (Greenfield, 2002, p. 127). Moreover,body planstend to characterise entire insect orders, so certain orders will include more loud singers than others. Leathery front wings are afocus of sound production in ensiferan Orthoptera, but soft-bodied stoneflies(Plecoptera) or caddisflies (Trichoptera) lack stronglysclerotised structureswhich might be coopted for sound production. For thoseinsects, abetter alternative to airbornesound for intraspecific communication is substrate-bornevibration. This “silent” acoustic mode has several advantages for small insects as well, notably long-distance propagation of signals through plant stems and leaves (Ossiannilsson, 1949; Michelsen et al., 1982; Markl, 1983; Gogala, 1985a; Stewart, 1997; C ˇ okl and Doberlet, 2003). As predicted, vibratory signals are particularly common in weakly sclerotised and small- bodiedrepresentatives of the clades Plecoptera, Psocoptera, Hemiptera, Neuropterida, Diptera and Trichoptera (Stewart, 1997). Predominantly, neuropterid insectsare not only small in size, but alsosoft-bodied.Perhaps because of these dual constraints, and like other insect groups of similar size and body plan, neuropterids communicate largelythrough their substrates (Devetak, 1998). In this chapter, Idescribe what is known of air-and substrate-borne acoustic signals in Neuropterida, taking a phylogenetic perspective when possible.

NEUROPTERIDA Neuropterida is arelatively small taxonofthree archaic insect orders united by afew weak morphological synapomorphies (Kristensen, 1999). Recent DNA sequence data nonetheless supportthe clade (Whiting, 2002; Haringand Aspo¨ ck, 2004). It is thought to be the sister clade of the Coleoptera, and together the two taxa constitute the monophyletic “neuropteroid complex” or “Neuropterodea”ofEndopterygota (Holometabola). The globally distributed neuropterid order Megaloptera includessome 300 species in two families. Raphidiopteraisasmall Holarctic order of two families and about 200 species. Cosmopolitan Neuroptera is much larger, at 6000 described species.Neuropteraisalso the most neatly delimited of the three orders: although its 17 families are extraordinarily disparate in morphology and habits, all shareasuite of specialised suctorial mouthpart structures in their larvae. In contrast, neither Megalopteranor Raphidioptera possess compelling morphological synapomorphies, and their phylogenetic positions within Neuropterida are uncertain (reviewedinAspo¨ ck et al., 2001). Nevertheless,monophyly of Megalopteraand Raphidiopterahas been afﬁrmed by DNA sequence data (Haring and Aspo¨ ck, 2004). The most recent morphological and molecular studies (Figure 10.1)supportaclade of Megaloptera þ Neuroptera, with Raphidiopteraasits outgroup (Aspo¨ ck et al., 2001; Aspo¨ ck, 2002; Haringand Aspo¨ ck, 2004). Acoustic Communication in Neuropterid Insects 155

idae ygidae thidae idae meleontidae ylidae ysopidae idae ydalidaevror lystoechotidae Coniopter COLEOPTERARaphidiidaeInocelliidaeSialidaeCor Ne PsychopsidaeNemopterNymphidaeMyr AscalaphidaeIthonidaePo Osm Chr Hemerobiidae Sisyr Dilar MantispidaeRhachiberothidaeBerothidae

vena triplica (many synapomorphies)

phytosuccivorous larva with unique head capsule morphology

larva with robust, loss of gula in larva curvedjaws a a Myrmeleontiformia Hemerobiiformia larva with unique head capsule morphology terrestrial larva with reduced gula Nevrorthiformia Megalopter and cryptonephry airborne sound Raphidiopter unique abdominal tremulation male genitalia Neuroptera tremulation &airborne sound elongate suctorial larval elytra prothorax Unresolved relationships aquatic larva mouthparts Neuropterida (after Aspöck et al., 2001, with elongated stipes Haring &Aspöck, 2004, et al.)

FIGURE 10.1 Phylogenetic hypothesis for the relationships of the 21 families of the superorder Neuropterida, indicating taxa within which acoustic communication has been described.

TYPES OF ACOUSTIC COMMUNICATION IN NEUROPTERIDA As mentioned, the neuropteridsare notnoted singers.Acoustic or vibratory signals, in the context of sexual behaviour,have been confirmed in just nine of 21 families (Figure 10.1). In most of these, communication is by substrate-borne vibratory signals, although putative stridulatorydevices have been described in several genera of green lacewings (Chrysopidae: Adams, 1962; Riek, 1967; Brooks, 1987). Becausevibratory signals are not easily detected, acoustic communication will likely be found in additional neuropterid taxa whenappropriate instrumentation is used. Vibratory signals in neuropteridsmay be produced percussively or by tremulation. Percussive (drumming) signals result from somepart of the insect’s body, usually the abdomen or wings in neuropterids, which actually strike the substrate such that compressionwaves are propagated through the material. In contrast, tremulation produces bending waves in the substrate (Michelsen et al., 1982). As the insect vibrates its abdomen vigorously in the vertical plane, the lightweight stem or leaf upon which it is standingisshaken up and down at low frequencies ranging typically between10and 150 Hz. Tremulation produces amoreconstrained, consistent signal than percussion. Whereas the frequency structure (tone or pitch) of apercussive signal dependsupon the resonant properties of the substrate, that of atremulation signal is largely independent of substrate characteristics and insteadaccurately reflects the frequencyofvibration of the abdomen itself. As we shall see, tremulation is much more common than percussion for signal production in neuropterids. Several species of green lacewings have evolved modified regions of the wings which are hammered against the substrate during courtship and mating (see later discussion), while other chrysopids and some sialids (Megaloptera) will strike the substrate with the vibrating abdomen rather than (or in addition to) tremulating. Even whenaudible (airborne) sound results from 156 Insect Sounds and Communication: Physiology,Behaviour,Ecology and Evolution percussive behaviour,asinsome lacewings,itisnever very loud. Thesubstrate-bornecomponent of such signals probably carriesmostofthe information. Structures and behaviour specifically dedicated to the production of airbornesound are very rare in neuropterids, again beinglimited to Chrysopidae. These will be reviewed in asection devoted to greenlacewing acoustic communication.

ACOUSTIC COMMUNICATION IN MEGALOPTERAAND RAPHIDIOPTERA Tremulation is found in all four families of Megalopteraand Raphidioptera (Figure 10.1). In every case, it includes“bouts” or volleys of abdominal vibrations which initiate and accompany courtship, sometimes in both sexes. These bouts may be accompanied by ﬂuttering of the wings, which can produce faint but audible airbornesounds.Inthosespecies in which both sexes “sing”, duetting betweenmales and females is usually present.

M EGALOPTERA: S IALIDAEAND C ORYDALIDAE Courtship and mating within Megaloptera have been described for just one genus of Sialidae (alderflies) and five of Corydalidae (dobsonfliesand fishflies). Adetailed overview of megalopteran matingsystems can be found in Henry (1997).

Sialidae

Best studied of all Megalopteraare two European alderflies, Sialis lutaria (Linnaeus) and Sialis fuliginosa F. Pictet. In S. fuliginosa ,Killington first described tremulation as amutual “twitching of abdomens upward at intervals” in both sexes (Killington, 1932, p. 67). Much later, Rupprecht (1975) distinguished two types of tremulation signals in both species,which he described as “rhythmic” vs. “prolonged, unstructured”. “Rhythmic” vibrations are relatively short volleys of low frequency abdominal tremulation repeatedatregular intervals by both sexes.These signals “allow mutual approach and recognition of species and sex” (Rupprecht, 1975, p. 305). Volley characteristics are similar in both species. The duration of each volley is several hundredmilliseconds, and carrierfrequency gradually decreases(i.e.ismodulated) within each volley from ameanof200 Hz at volley onset to about 120 Hz at the finish. Volley period ranges from 250 msecto2sec, depending on the behavioural context.Both species use only rhythmic tremulation signals during heterosexual duets. However, duetting in Sialis is not precise: the stimulus produced by one courting insect does not triggera predictably timed response from its partner. Rupprecht’s “prolonged, unstructured” vibrations were found only in males of the two Sialis species he studied. These signals do not show consistent temporal or frequencycharacteristics. They appeartoreflectageneral state of sexualreceptivity in males,and often segue into periods of organised volley production, courtship and copulation (Rupprecht, 1975, Figure 4). Rupprecht also noted percussive signals in Sialis,produced by “tappingofabdomen and wings on the ground”(Rupprecht,1975, p. 305). These he interpreted as providing encouraging feedback from one partner to the other during the early stages of courtship. Drumming occurs only in males of S. lutaria,but in both sexes of S. fuliginosa .Femalesofthe latter species can drum very rapidly, at arate of nearly 20 strikes/sec (Rupprecht, 1975, Figure7). If acoustic signals have evolved in the context of premating reproductive isolation, one expects them to be significantly different in closely related, sympatric species,whether because of stabilising selection on different mate recognition systems (Paterson, 1985; Butlin, 1995) or because of reinforcement and reproductive character displacement (Butlin, 1989; Howard, 1993; Liou and Price, 1994). Yet few consistent differences are found between the vibratory “songs”of S. lutaria and S. fuliginosa ,suggesting that alternative evolutionary dynamicshave been at work. Acoustic Communication in Neuropterid Insects 157

Corydalidae The mostcomplete description of acoustic communication in corydalids is Parfin’s(1952) on the North and Central Americanspecies Corydalus cornutus (Linnaeus). Additional relevantanecdotes are mentioned in New and Theischinger (1993). Anumber of other excellent studies focus on nonacoustic aspects of reproductive behaviour,including intrasexual selection,mate guarding, nuptial gifts, courtship feeding, spermatophore investment and sperm cooperation (Hayashi, 1993, 1996; Contreras-Ramos, 1999). Parfin (1952, pp.429–432) described how the male of C. cornutus approachedthe female, laid his long mandibles across her wings for several minutes, withdrew to aposition next to the female, and then “wriggled his soft abdomen for about half aminutewith three to four series of several rapid quivers each” prior to final approach and copulation. From this, it is clear that corydalids can tremulate in the samemanner as sialids, producing discrete volleys of abdominal vibration during courtship. However, tremulation in corydalids seems to be limited to males,and possibly to Corydalus alone; for example, in his careful study of prematingbehaviour in Platyneuromus sp., Contreras-Ramos (1999) reportednosuch vibratory signalling, only wing fluttering.Norecordings or analyses of corydalid male “songs”have been published.

R APHIDIOPTERA: R APHIDIIDAE AND I NOCELLIIDAE Courtship and mating in this order have been described for three generaofRaphidiidae and one genus of Inocelliidae (reviewed in Henry, 1997). Unfortunately, observations of inocelliids have generally been merged with thoseofraphidiids, so it is notpossible here to treat acoustic communication in the two families separately. It has been recognised for yearsthat abdominal vibration accompanies courtship in snakeflies (Eglin, 1939; Zabel, 1941: Raphidia ophiopsis Linnaeus and Inocellia crassicornis (Schummel); Woglum and McGregor, 1958: Agulla bractea Carpenter; Acker, 1966: three species of Agulla). The mostdetailed descriptions are found in Kovarik et al.(1991) in their studyofNorth American Agulla bicolor (Albarda) (as Raphidia bicolor Albarda). Courtshipinsnakeflies is similar to that of alderflies (Sialidae). Males and females approach each other and vigorously vibrate their abdomens for sustained periods. As in sialids, the courting individualsestablish duets, such that “prolonged vibrations by apersistent male often elicit asimilar response from the courted female” (Kovarik et al., 1991, p. 362). Acker (1966) had earlier made note of the samekind of sustained abdominal vibration in Agulla astuta (Banks), A. adnixa (Hagen) and A. bicolor (Albarda), additionally observingthat signals in females are less intense than in males. Audiblewing fluttering usually accompanies courtshipactivity. No formal descriptions of snakefly tremulation exist, but Kovarik’s statementthat “the female often responds with short vigorous vibrations”implies that abdominal vibration in A. bicolor is temporally organised into discrete volleys,asin Sialis (Rupprecht, 1975).

P ERSPECTIVE Tremulation using abdominal vibration is afundamental component of mating behaviour in Megaloptera and Raphidioptera.The archaic (plesiomorphic) nature of both orders implies that abdominal tremulation is part of the ground plan of Neuropterida, and that male–female duetting using these vibratory signals is included within that ground plan. Thechallenge is therefore to assess retention, loss and perhaps secondary gain of tremulation in the principal neuropterid order, Neuroptera.

ACOUSTIC COMMUNICATION IN NEUROPTERA Communication usingsometype of sound or substrate vibration hasbeen conﬁrmed in just ﬁve of the 17 families of the order Neuroptera, all within the suborder Hemerobiiformia (Figure 10.1). 158 Insect Sounds and Communication: Physiology,Behaviour,Ecology and Evolution

Abdominal tremulation is found in Sisyridae (spongilla ﬂies), Hemerobiidae (brown lacewings) and Chrysopidae (green lacewings), while Coniopterygidae (dusty-wings) and Berothidae (beaded lacewings) simplyvibrate or ﬂutter their wings during courtship. Only in Chrysopidae has acoustic signalling becomesophisticated and diverse. Additionalaspects of courtship and mating systems throughout the order are compiled in Henry (1997).

S ISYRIDAE AND C ONIOPTERYGIDAE Arecent cladistic analysis based on 36 morphological features argues for asister-group relationship betweenthese two families of small to minute Neuropterans (Aspo¨ ck et al., 2001; Aspo¨ ck, 2002). However, earlier work came to very different conclusions(summarised in New, 1991), and molecular data have so far failed to support the hypothesised relationship (Haring and Aspo¨ ck, 2004). These twofamilies will be considered together because both include species which communicate acoustically.

Sisyridae

Spongilla-flies are small, peculiarNeuropterans whoselarvae are subaquatic predators of freshwater sponges. Although constituting only 50 described species,Sisyridae is nonetheless cosmopolitan in distribution (Pupedis, 1980, 1985). Reproductive behaviour has been observed in a handful of species.InNorth American Climacia areolaris (Hagen), courtship includeshorizontal extension and rapid vibration of the wings on one side of the male’sbody, whereby he “fans” the head of the femaleand perhaps produces afaint sound (Brown, 1952). In contrast, Holarctic Sisyra nigra (Retzius) ( S. fuscata [Fabricius]) foregoes wing fanning in favourofabdominal tremulation (Killington, 1936; Rupprecht, 1995). Here, males and females oscillate their abdomens erratically during courtship at frequencies between100 and 450 Hz. Additionally, publishedsonograms show some evidence of percussive drumming during tremulation (Rupprecht, 1995, see figure). Tremulation in spongilla flies does not seem to be organisedinto discretevolleys of vibration.

Coniopterygidae

The reproductive behaviour of the “dusty-wings” or “waxflies” (Plant, 1991) has been little studied, probably because they are so small. More than 300 species have been described, but courtship and mating have been seen in only seven (Withycombe, 1922; Collyer, 1951; Henry, 1976; Johnson and Morrison, 1979). In hisrecent review of the subject, Devetak(1998) mentions“vibratory signals”in Coniopterygidae, but only precopulatorywing fluttering was actually documented in the cited study (Johnson and Morrison, 1979). Johnsonand Morrison reported wing fluttering in males and females of the three California species they examined. Furthermore, fluttering appeared to be temporally structured into 1to2sec “calls”, delivered intermittently. It is therefore not out of the questionthat abdominal vibration accompanies or even causeswing fluttering, but was simply overlookedinsuch tiny insects.

P ERSPECTIVE The phylogenetic positionsofSisyridae and Coniopterygidae have not been determined. Both families have been perceived at various times either as highly specialised and of relatively recent origin (Aspo¨ ck et al., 2001; Aspo¨ ck, 2002), or as ancient,plesiomorphic lineages (Withycombe, 1925; Klingstedt, 1937; Hughes-Schrader, 1975; Gaumont, 1976; Henry, 1982b; New, 1991). Of interest in this regard is the “staggered parallel, femaleabove” copulation position seen in coniopterygine Coniopterygidae (Johnson and Morrison, 1979), which is shared only with the archaic Megaloptera (Sialidae)and Raphidioptera (both families). If Sisyridae and Acoustic Communication in Neuropterid Insects 159

Coniopterygidae are one another’sclosest relatives (Aspo¨ ck et al., 2001) and also of ancient origin, then the presence in the clade of abdominal vibration and wing ﬂuttering during courtshipand mating couldbeinterpreted as retention of thosetraits, alongwith copulation position,from the ground plan of Neuropterida.

B EROTHIDAE Only wingfluttering has been reportedfrom the “beaded lacewings”. This is asmall but widespread family of about 60 species,belonging to aclade, Mantispoidea, which includesRhachiberothidae, Mantispidae (mantis flies) and Dilaridae (pleasing lacewings)(Willmann, 1990; Aspo¨ ck, 2002). MacLeod and Adams (1967) describecourting individuals of North American Lomamyia spp. lifting their wings to ahorizontal positionand alternately “vibrating” these at one another in abrief duet before copulating, which is reminiscent of “wing fanning” behaviour in the sisyrid Climacia areolaris (Brown, 1952). Withinthe Mantispoidea, it is not known whethersuch behaviour is uniquetoBerothidae or also present in one or more of the otherthree families. The phylogenetic position of Mantispoidea within the Neuroptera is not well understood, making interpretation of character origin and evolution difficult. However, wing fluttering in Berothidae appears to be simple and therefore perhaps evolutionarily labile; as such, the trait might not have larger phylogenetic significance. Thus, the occurrence of wing fluttering in disparate taxa such as Berothidae, Corydalidae, Raphidiidae, Sisyridae and Coniopterygidae (see above) couldbe incidental, that is, aconsequence of convergent evolution.

H EMEROBIIDAE No publishedrecords of acoustic communication in the brown lacewings exist, even thoughthe family includessome 550 species (Oswald, 1993). However, Ihave personally observed receptive males of Hemerobius sp. vibrating their abdomens in atemporally structuredmanner, much like Chrysopidae. Until very recently, hemerobiids and chrysopids have been treated as sister taxa, so the simplest hypothesis explaining the presence of tremulation in brownlacewings is the inheritance of that trait from amostrecent common ancestor with green lacewings. However, Aspo¨ ck et al. (2001) challenged that view on morphological grounds, arguing insteadfor acloser relationship of Chrysopidae with Osmylidae (but see Haring and Aspo¨ ck, 2004, for amolecular alternative). In any case,relationships among the families of Hemerobiiformia are sufﬁciently uncertain to preclude accuratetracing of signal evolution within the suborder.

C HRYSOPIDAE The green lacewings number about 1200 species,making it one of the largest families of Neuroptera. Here, acoustic communication has blossomed, such that awide variety of low-intensity sounds and vibrations are used by different taxa.

S TRIDULATION Airborne sound production via stridulation has been inferred in Chrysopidae from morphology but never demonstrated in living individuals. Adams (1962) was the first to notice rows of striaeonthe lateral margins of the secondand third abdominal sternites in both sexes of Meleoma schwartzi (Banks), togetherwith arow of wart-like tubercles on the inner surface of each hind femur. He concluded that vertical movements of the abdomen would cause the striae to scrape against the femoraltubercles, producing asound. Tauber (1969) confirmed these observations and reported similar structuresintwo related species, Meleoma pinalena (Banks)and M. adamsi Tauber. Subsequently, Brooks (1987) conducted acomprehensive search for putative stridulatory structures in the family, finding and describing them in Meleoma Fitch (three of the 22 known species, both 160 Insect Sounds and Communication: Physiology,Behaviour,Ecology and Evolution

a Glenochrysa) ochrys

MalladaAnomalochrysaChrysocerca EremochrysaChrysopiellaChrysoperla Chrysopa Meleoma NOTHOCHRYSINAEAPOCHRYSINAELEUCOCHRYSINIBELANOPTERYGINIANKYLOPTERYGINI(Suarius, Brinckochrysa (others) CeraePlesiochrysa Yumachrysa(others)Ungla (others)

(?) duets ---duets--- duets (?)

Mallada Chrysopa Ungla Others group group group

CHRYSOPINI

airborne sound abdominal tremulation CHRYSOPINAE tremulation &airborne sound putative stridulatory structures Chrysopidae (after Brooks 1997, Winterton &Brooks 2002, et al.)

FIGURE 10.2 Phylogenetic hypothesis for the relationships of the subfamilies and tribes of Chrysopidae, including the major genera of tribe Chrysopini.Taxa with some type of acoustic communication are indicated. Relationships within Chrysopini are those hypothesised by Dr. Stephen Brooks (personal communication, July 2004; see Acknowledgments). sexes in each), Brinckochrysa Tjeder (all 13 species,both sexes), and Chrysocerca Weele (one of ﬁve species, males only). He suggested independent evolutionary origins for thesestructures in each of the three genera, based upon fundamental differencesintheir anatomy and placement. That conclusion is also supported by phylogeny (Figure10.2)—the three genera are not particularly close relativesand they do not trace their origin back to amore distant common ancestor possessing a“stridulatory” apparatus. Circumstantial evidence for stridulation in green lacewings is compelling, even though sounds have not yet been recorded.Based on morphology, such signals are likelytobefaint, of relatively high frequency and probably sexually dimorphic because the femoralpegs are usually larger in males than females and the form of the abdominal striae differs betweenthe sexes (Brooks, 1987). The presence of tremulation in several close relatives of “stridulating” genera is also signiﬁcant because abdominal vibration couldhave provided the initial behavioural basis for stridulation (Adams, 1962). Astridulatoryfunction has also been ascribed to interacting patches of microtrichia, locatedat the point where the folded forewings contact the metanotum (Riek, 1967; Eichele and Villiger, 1974). However, these“organs” are widely distributed in otherNeuropteran families, Trichoptera and micro-Lepidoptera, and are more likely to function in wing positioning than sound production (Henry,1979; Brooks, 1987).

W ING F LUTTERING Generalised fluttering or rattling of wings during courtship and mating has been reported in several species of Meleoma and Eremochrysa,including Eremochrysa/subgenus Chrysopiella (Duelli and Johnson, 1982). This behaviour seems to be abyproduct of particularly vigorous abdominal Acoustic Communication in Neuropterid Insects 161 vibration characterising Meleoma emuncta (Fitch), M. arizonensis (Banks)and M. furcata (Banks) (Tauber, 1969; P. Duelli, personal communication). The effect is to produceasoft but distinctly audible rustling sound of unknown significance. Aspecialised type of wing fluttering is found in Anomalochrysa maclachlani Blackburn, one of 22 species in this endemicHawaiian genus. Both sexes flick the wings anteriorlysoastoproducea clicking sound which is clearly audible several metersfrom the caller (Tauber et al., 1991). Courting individuals will often producetrains of 50 or more clicks.The clicks are repeated at a steadily increasing rate during each train, from one click every 2sec to three clicks per second. The male and female will alternatelyexchange clicks in aduet which usually continuesuntil copulation. Simultaneous clicking,which could maskthe partner’s signal, is rare. Themechanism of sound production has not been determined, but may involve “a sclerotised structure at the base of the forewings”(Tauber et al., 1991, p. 1024).

P ERCUSSION Malladabasalis (Walker), distributed widely across the Indo-Paciﬁc region, produces audible buzzing noises by striking the modiﬁed costal margins of its vibrating hind wings forcibly against the substrate (Duelli and Johnson, 1982). Only the male has the thickened, hammer-like pterostigma on the wing requiredfor signalling. Males call vigorously in the presence of females, and are capable of producing the loudest airbornesounds of any neuropterid. Percussive sounds can also be found in lacewings which tremulate, e.g.two species in the carnea group of Chrysoperla (Henry et al., 2002, 2003). In such cases, the tremulating abdomen will periodically strike the substrate, usually toward the end of asong consisting of asingle long volley ( Chrysoperla agilis;Henry et al.)ormanyshort volleys ( C. pallida ;Henry et al.). The sound which we hear is alow-intensity ticking or rattling noise, detectableover arange of perhaps 25 cm.

T REMULATION The predominant form of acoustic communication in greenlacewings is tremulation via abdominal vibration. Tremulation signals in chrysopids are remarkably similar to thosein Megaloptera and Raphidioptera,but more diverse and often more complex. Five genera are knowntoinclude tremulating species: Nothochrysa, Eremochrysa (including Chrysopiella), Chrysoperla, Chrysopa and Meleoma. Of the three subfamilies of Chrysopidae,Nothochrysinae is the most plesiomorphic, lacking the ultrasonic “ear”found in all other greenlacewings. Nonetheless, tremulation is present even in this archaic group, based on Toschi’s (1965) observations of Nothochrysa californica Banks. Here, abdominal vibration is apparently confined to males during the “approach”and “contact” phases of courtship. No details of volley structure or frequencyare given. Chrysopa and Meleoma sharemembershipinthe “ Chrysopa group” of Chrysopinae (Figure 10.2;S.Brooks, personal communication), and they share simple tremulation as well. In Meleomaemuncta, M. kennethi Tauber and M. hageni Banks, abdominal vibration has been demonstrated only in courtingmales (Tauber, 1969; Duelli and Johnson, 1982). On the otherhand, Chrysopa definitely exhibits tremulation in both sexes (Smith, 1922; Principi, 1949), and partners will duet using nearly identical, nonoverlapping signals during courtship(Henry, 1982a).The two best-studied species,North American Chrysopa oculata Say and C. chi Fitch, producetrains of simple volleys.Volleys of C. chi are twice as long (160 vs. 82 msec) and three times as far apart (800 vs. 250 msec) as those of C. oculata,and are also lower pitched (77 vs. 109 Hz). Of more significance for premating reproductive isolation, courting partnersof C. chi trade volley-for-volley during duets, while the unit of exchange (the “shortest repeated unit” or SRU) in duets of C. oculata is acluster of multiple volleys (Henry,1982a).Ifcoordinationofsignals during duetsisimportant 162 Insect Sounds and Communication: Physiology,Behaviour,Ecology and Evolution to success in copulation in these two species (as seemslikely), then this basic difference in the mode of duetting will effectivelypreclude heterospecificinteractions. Eremochrysa (including Chrysopiella )and Chrysoperla are two closelyrelated members of the Mallada species group (Figure10.2). “Polite” male–femaleduetting using identical signals is characteristic of both genera. Although Eremochrysa seemstohave retained simpletremulation signals ( e.g. E. minora [Banks]; see Henry and Johnson, 1989), Chrysoperla has become the tremulation champion of the greenlacewings.Tremulation signals have been found whenever lookedfor in this genus, in representatives of each of the four recognised “speciesgroups”(Brooks, 1994). As in Chrysopa and Eremochrysa,their low-frequency signals are sexually monomorphic and organisedinto repeating volleys of abdominal vibration, which in turn are groupedinto identical SRUswhich serve as the currency of exchange during heterosexual duets(Figure10.3). ASRU consists of just one, several or many volleys and may include more than one type of volley, e.g. of different durations or pitches (Figure 10.4,Figure 10.5C). From atheoretical perspective, the temporal and frequency characteristics of the songs are well suited to the general biomechanical properties of plantstems (Michelsen et al., 1982; C ˇ okl and Doberlet, 2003). However, playback experiments comparing signal propagation in grass vs. conifer stems usingtwo lacewing species ecologically associated with thosesubstrates suggestthat songs may not show truly fine-tuned bioacoustic adaptations to specific plant types (Henry and Wells,2004). Courting partners of Chrysoperla lacewings synchronise their songs to one another with remarkable accuracy. Becausesongs of males and females are identical within aspecies,an individual need only recognise its own song in the signal of its partner to establish aduet leading to copulation. Individuals will listentotheir partnerscarefully, quickly and mutually adjusting the tempo of their songs. In fact, if changesinastimulus signal are presented incrementally, it is possibletomorethan doubleorhalve the SRU interval of aresponding male or femaleof C. plorabunda (Figure 10.5, unpublished data). However, song phenotypes with parameters outside the acceptable range for the species elicit little or no response. Sexual interactions of two species singing different songs will terminate quickly, based on the inability of the partners to synchronise their signals and establish the mandatory duet (Wells and Henry, 1992).

C RYPTIC S PECIES Lacewing species characterised by sophisticated duetting behaviour,such as thosein Chrysoperla, are often very difficult to delimit morphologically. Accordingly, we now know that the easily recognised and widespread species Chrysoperla carnea ( sensu lato)isreallyacomplex of many cryptic“biological” species, separable chiefly by uniquetremulation signals. Undernatural conditions, courtship duetting prevents mating between individuals with different songs, even thoughmost“song species”ofthe carnea group are potentially interfertile (Wells, 1993; Wells and Henry, 1994). To date, at least 15 crypticspecies of the carnea group have been recognised, fivein North America and ten in Eurasia (Figure 10.3). Each species has abroad geographic range (Wellsand Henry, 1998), yet intraspecificsong variation over that range is remarkably small. Sympatry and even syntopyofspecies is extensive, such that several can be collectedatagivensite on agiven day. Yet hybrids betweensympatric song species, which are easily recognised by their intermediate song phenotypes, have never been found in the field. So far, cryptic, duetting song species have been described only for the carnea group of Chrysoperla.However, it is very likely that hiddentaxonomic diversity will soon be found in other subsections of the genus. For example, complexsignals and duetshave been recorded from four species of the cosmopolitan pudica group: C. comanche (Banks)(Henry, 1989), C. pudica (Nava´ s), C. mutata (McLachlan) and C. congrua (Walker). In addition, both C. comans (Tjeder)and C. volcanicola Ho¨ lzel et al.ofthe Afro-Asian comans group produceremarkably sophisticated tremulation songs and could easily harbour crypticsong species withintheir diagnostic limits (unpublished data). Representatives of the fourth species group, nyerina,remainunstudied. Acoustic Communication in Neuropterid Insects 163

Chrysopa oculata

Chrysoperla rufilabris pudica group C. harrisii

C. downesi

‘ downesi-west’

C. johnsoni

North America C. plorabunda

C. adamsi

C. nipponensis

‘ downesi-Kyrgyzstan’ group

‘ adamsi-Kyrgyzstan’

C. carnea Chrysoperla carnea C. lucasina

Eurasia C. pallida

‘ carnea-Kyrgyzstan’

Cc5 ‘generator’

C. agilis

C. mediterranea

0s2 4 6 8 10 12

FIGURE 10.3 Twelve-second oscillographs of the tremulation songs of 15 song species of the Chrysoperla carnea group, two species from the closely related pudica group and one species from the more distant genus Chrysopa.Arrows indicate where the partner would insert its signal during aheterosexual duet. 164 Insect Sounds and Communication: Physiology,Behaviour,Ecology and Evolution

FIGURE 10.4 Tremulation song of Chrysoperla downesi,aspecies having along, multivolley courtship signal. The oscillograph at the bottom of the ﬁgure shows asingle SRU, which is exchanged in alternating fashion with the SRU of the duetting partner. The box contains a2-sec detail of part of the SRU, showing the temporal and frequency structure of the two distinct volley types.

Oncecrypticspecies have been properly delimited by songs, subtle morphological and ecological differences among them usually become apparent (Henry et al., 2001, 2002a). Eventually, identiﬁcation of such species will be possibleusing more traditional taxonomic tools.

S PECIATION Precise duetting betweenheterosexual partnerssinging the same song has set the stage for rampant speciation within Chrysoperla.Mutual and rapid adjustment of song tempo during the initial phase of the duet assures that acoustically compatible individuals will sing in lockstep. This unusually well-coordinated prematinginteraction betweenconspeciﬁcs has apotent reproductive isolatingeffect betweenspecies singing different songs. Consequently, any randombut measurable change in one type of song —say, due to amutation in asong-controlling gene —could precipitate aspeciation event.Itisthought that occasional changes such as these have probably generated the swarmsofcrypticspecies in Chrysoperla.The driving forceissexualselection, in this case mate choice by both sexes,which quickly segregates the new song typesreproductively from existing ones. Such speciationcould even have been sympatric rather than allopatric. It has alsobeen Acoustic Communication in Neuropterid Insects 165

Response

Stimulus

(a) 015 01520253035404550 55 60

Volley (= SRU) detail Response C.

Stimulus

015 015202530 00.50 1.00s (b) Time (s) (c)

FIGURE 10.5 Duetting responses at 258 C(upper oscillographs in (a) and (b)) by an individual of Chrysoperla plorabunda to astimulus signal (lower oscillographs in (a) and (b)) which gradually increases (a) or decreases (b) in SRU period. This species has asingle-volley SRU (c). SRU duration of both stimulus signals was held constant at the species mean, 636 msec (258 C). Initial SRU period for both stimuli was 1230 msec (also the species mean at 258 C). In (a), the period of the stimulus increased to amaximum of 2280 msec; in (b), the period of the stimulus decreased to aminimum of 610 msec. Note that the individual is able to maintain perfect synchrony with the stimulus, regardless of whether the period of the latter markedly increases or decreases. very recent: genetic distances and nucleotide sequence divergences among the song species are vanishingly small (Wells, 1994; Henry et al., 1999). Apredictionofthis modelofspeciationisthat the genetic architecture of song phenotype should be simple, consisting of relatively few genes of large effect. Indeed, the resultsofa hybridisation experiment between C. downesi and C. plorabunda showed that song features segregated in amanner consistent with simplearchitecture (Henry,1985). Furthermore, in a Bayesian Castle-Wright analysisofsong data from C. plorabunda £ C. johnsoni,Henry et al. (2002b)showed that as few as one “genetic element” might be responsible for acrucial duetting difference between thosetwo species.Ifthese conclusions continue to receive supportfrom future studies, Chrysoperla will be seen as arare exemplar of rapid, sympatric speciation causedbysexual selection acting on chancemutational differences in mating signals.

OVERVIEW From the humanperspective, Neuropterida is asilent taxon of insects. That can be blamed on their soft bodies and small size, which togetherconspire to limit their abilities to produce loud sounds. However, manymembers of the superorder have insteadexploited low-frequency acoustic channels which are always available in plant stems and leaves. These are private lines of communication, not so easily accessible to eavesdropping predators, parasites or even conspeciﬁc sexualcompetitors. To sing “silently” in this way, the neuropterids use simplevertical oscillations of their abdomens to producetremulation signals in plant tissues. 166 Insect Sounds and Communication: Physiology,Behaviour,Ecology and Evolution

Substrate-borne tremulation signals have adeep evolutionary historywithinNeuropterida. Abdominal vibration during courtship and mating is found not only in the ancient,relict orders Megalopteraand Raphidioptera,but also in severalplesiomorphic taxaofNeuroptera. Unfortunately, courtship and mating behaviour are poorly known in most families of Neuroptera, so it is currently impossible to trace the evolutionoftremulation with precision or confidence. However, it is very likelythat abdominal tremulation is part of the ground plan of the neuropterids, and in modified form it has contributedtorecent explosive speciation within at least onegenus of Chrysopidae, Chrysoperla. Tremulation may also have been indirectly responsible for the origin of airborne sound production in several otherlacewing generathrough the evolution of putative files and scrapers which apparently use the same vertical jerking motionofthe abdomen. Even if such sounds exist, though, they must be very soft. Afew otherlacewing species producefaintly audible sounds percussively by drumming their abdomens or wing margins against the substrate. Endemic Hawaiian lacewings employ aunique wing-flicking behaviour to produce audible clicks. Acomplete understanding of the taxonomic distributionofacoustic communication in Neuropterida will undoubtedly shed some light on the phylogenetic relationships of the families which are currently controversial.However, as part of the dynamic mating systems of species, sexual signals usuallyundergorapid evolutionary change whichcan quickly overwrite phylogenetic information through convergence, parallelism and reversal. Therefore, mating signals are of greater valuefor the light they can shed on evolutionaryprocesses, particularly speciation. The tremulation songs of Chrysoperla reflect rapid, repeatedand behaviour-based speciation processeswhich challenge the entrenched dogmaofmore gradual allopatric speciation. Future work alongtheselines will certainly yield new surprises.

ACKNOWLEDGEMENTS The researchbythe author described in this chapter was supportedinpart by the Research Foundation of the University of Connecticut. Ithank Drs. Marta M. Wells (University of Connecticut and Yale University, U.S.A.), PeterDuelli (Swiss Federal Research Institute WSL, Switzerland), Stephen J. Brooks (The Natural History Museum, London) and James B. Johnson (University of Idaho,U.S.A.) for fruitful collaboration and friendship over manyyears of work together. For valid species names, Iamindebted to Dr.John Oswald’s web-based searchable index of species names (Oswald,2003). Ialsothank Dr. Cynthia S. Jones,Suegene Noh and David Lubertazzi (UniversityofConnecticut, U.S.A.), who critically read and improved the manuscript.