Acoustic Communication in Insects REVIEW

Home , Oecanthus pellucens, Stridulation, Subgenual organ

REVIEW Acoustic communication in insects

Edith Julieta Sarmiento Ponce1

1Deparment of Zoology, University of Cambridge. Downing St. Cambridge. CB2 3EJ, United Kingdom. Correo-e: [email protected]; [email protected]

Recibido el 13 de junio de 2014/ Aceptado el 25 de agosto de 2014

RESUMEN ABSTRACT La investigación de comunicación acústica y audición en insectos Research on acoustic communication and hearing in insects has ha sido extensamente estudiada desde hace 70 años. Estudios been extensively studied in the past 70 years. Behavioural stu- de comportamiento de insectos han demostrado la importancia dies have pointed out the relevance of insect hearing for intraspe- de la audición para la atracción de pareja, cortejo, rivalidad y cific acoustic communication (mate attraction, courtship, rivalry comportamiento territorial, así como para detección de presas, and territorial behaviour), prey detection, predator avoidance, evasión de depredadores y localización de huésped parasitario. and parasitic host localization. This review describes the asso- Esta revisión exhaustiva describe la asociación entre el soni- ciation between insect sound and behavioural responses, as well do de insectos y su correspondiente comportamiento, así como, as compile and exemplify the five categories of sound-producing comprende y ejemplifica cinco categorías de mecanismos de mechanisms in insects: vibration (tremulation), percussion, stri- producción de sonido en insectos: vibración (tremulación), per- dulation, click mechanisms and air expulsion. Additionally, the cusión, estridulación, mecanismos de clicks y expulsión aérea. insects hearing organs are described (hair sensillae, chordotonal Adicionalmente, se describen los órganos auditivos en insectos sensillae, Johnston’s organ, tympanal organs, and sub-genual (sensilas, sensila cordotonal, órgano de Johnston, órgano tim- organ), indicating its position in the insect body, the Order that pánico y órgano sub-genual) indicando su posición en el cuerpo present it, and the preferred stimulus. Finally, I mention the case del insecto, el Orden que lo presenta, y su principal fuente de study of the Mediterranean Field Cricket (Gryllus bimaculatus) estimulación. Finalmente, se menciona el caso de estudio del explaining the phonotactic process, where the female is attracted Grillo de Campo Mediterraneo (Gryllus bimaculatus) explican- towards the male by its species-specific calling song. do la fonotaxis, el cual es el proceso donde la hembra es atraida hacia el macho por su llamado. Keywords: Communication; hearing; insect; percussion; sound; stridulation; tremulation; vibration Palabras clave: Audición, comunicación; estridulación; insec- to; percusión; sonido; tremulación; vibración the insect hearing organs, indicating its body 1. Insect acoustic communication position, the Order that present it, and the tri- Insects, representing approximately 70 per- ggering stimulus. Finally, a case study of the cent of the world’s species, are by far the most Mediterranean Field Cricket (G. bimaculatus) successful, and variable group of living speci- phonotactic behaviour is mentioned. mens which have evolved on our planet. The- During the early 1900’s, detailed anatomi- se arthropods are among the oldest terrestrial cal descriptions of hearing organs of distinct animals, and have existed for more than 400 groups of insects were carried out (Eggers, million years (Straub & Lakes-Harlan, 2014). 1911; Schwabe, 1906). But only after 1940, Insects present various lifestyles (aquatic, two comprehensive reviews on “Hearing in In- terrestrial, epizoic, among others), but per- sects” (Pumphrey 1940) and “Insect sounds” haps one of their most interesting features is (Haskell 1961) were performed, where insect its acoustic communication. This manuscript sound was defined as “any mechanical distur- compiles a comprehensive review on the acous- bance whatever which is potentially referable tic communication behaviour in insects, inclu- by the insect to an external and localized sour- ding the behaviours associated with the insect ce. Since those early studies in the field, the sound of communication within the same development of new techniques and suitable species, prey detection, predator avoidance, equipment for the recording and analysis of and parasitic host localization. A compilation sounds have allowed the field to progress ra- and exemplification of the five categories of pidly (Claridge, 2005; Hedwig, 2014; Huber, sound production mechanisms in insects is 1960; Roeder & Treat, 1957; Roeder, 1969; shown. Additionally, there is a description of Suga & Katsuki, 1961).

48 Quehacer Científico en Chiapas 9 (2) 2014 2. Behaviours associated with insect sound and olfaction in the nocturnal predators. Noc- Acoustic signals (sounds) can be associated turnal acoustic hunters include felids, canids, with several insect behaviours, mainly mate owls, rodents, which are all passive listeners. attraction, courtship and territorial behaviour. Bats are also passive listeners, but also active For instance, the mature unmated female cric- echolocators. According to Conner (2014), all ket Gryllus campestris and long-horn gras- traits including visual, chemical tactile, electric, shopper Thamnotrizon apterus, are attracted and acoustic cues, that minimize the probability by the singing (chirping) of the males (Regen, of a prey being detected when potentially detec- 1913). Even flight noises in mosquitos are used table to an observer, can be called Crypsis. For for mate attraction (Kahn & Offenhauser, example, certain moths interrupt their sexual 1949). However, insect sounds can also be used acoustic calls in the presence of acoustic preda- in other behaviours, as mentioned below. tors, to avoid detection by the predator (Green- field, 2014; Spangler, 1984). Similar adaptive A. Intraspecific communication: rivalry and silence behaviour have been reported in cric- territorial behaviour kets and katydids (Bailey & Haythornthwaite, Some grasshoppers have developed one of the 1998; Belwood & Morris, 1987; Conner, 2014; most highly intricate song behaviour amongst Faure & Hoy, 2000; Spangler, 1984). insects, called the “rival duet” behaviour. If a The cricket Teleogryllus oceanicus depicts male grasshopper, singing his courtship song to one of the most remarkable examples of adap- a female, is interrupted by the appearance of a tive silence (Hedwig & Robert, 2014; Zuk, Ro- second male who also tries to court the female; tenberry, & Tinghitella, 2006). The male field the first male leaves the female, faces the intru- cricket stridulates by scissoring the wings; der, and sings the “rivalry song”. This behaviour females are attracted to the males’ songs. In- produces an abrupt and similar response from terestingly, an Australian and Pacific Island the interloper, and the two males sing against species of T. oceanicus, have been forced to one another. The contest may be brief, when one alter that strategy because of an acoustically or other leaves the field and the remaining male orienting parasitoid fly Ormia ochracea. Like returns to his courtship, or so long that the fema- the female cricket, this fly is attracted to the le abandons the scene herself (Haskell, 1961). male cricket’s calling song. After locating the Busnel (1953) described the territorial be- male cricket, the fly deposits her offspring haviour of the cricket Oecanthus pellucens; the on or near the male. The larvae burrow into male lives in bushes, about 50 cm above the the male, killing him as they develop. Within ground and stays for the great majority of its approximately 20 generations of intense selec- life restrained to a small area approximately tion has resulted in a morphological change in 50 sq cm. The male moves around this terri- the wings of the male crickets on Kauai. Mute tory, patrolling, singing its normal song, if it males, called flatwing males, have wings- si encounters another interfering male, it sings milar in appearance to those of females. Mute a type of song called the “warning song”. This males have lost their file and scraper and are interesting behaviour appears analogous to the thereby silenced. Flatwing males produce no territory marking of certain song-birds, which calling song and do not attract the parasitoid. is established by the male by singing at the However, it is not clear how the silent flatwing territorial boundaries prior to the commence- males now attract mates, although Cade (1980) ment of the mating season (Haskell, 1961). suggested that they function as satellite males, waiting close to calling males, and intercepting B. Detection and avoidance of predators females as they move toward them. Numerous predators utilize a combination of “Whispering” moths exemplify another sensors to hunt insects: vision, olfaction, and antidetection strategy (Nakano et al., 2008). hearing are the main ones; with a bias toward Ostrinia furnicalis, male Asian corn borer mo- vision in diurnal animals and toward hearing ths, use specialized very low intensity courts-

Quehacer Científico en Chiapas 9 (2) 2014 49 hip songs (46 dB sound pressure level at 1 (1989) described a most recognised classifica- cm) produced by sex-specific scales on the fo- tion compiling five categories of sound produ- rewings and mesothorax. In order to protect cing mechanisms (Claridge, 2005) (Table 1). the pair from conspecific competitors and predators, this male moth produces the sounds A. Vibration (including Tremulation) – in the immediate vicinity of the female’s ear, Sound emissions that result from vibrations of which provide a private communication chan- relatively unspecialized body parts of the insect, nel between the male singer and the female generally oscillations of the abdomen, either listener (Conner, 2014). dorso-ventrally or laterally. The oscillatory movement of the wings of an insect sets up regions C. Host localization by parasitoid insects of compression and rarefaction and a vibratio- Animal acoustic signalling uncommonly cons- nal sound is produced. Tremulation sound is titutes a confidential communication channel. transmitted through the legs to the substrate Sound tends to propagate in all directions, on which the insect is walking or standing. broadcasting towards hardly predictable des- The flight sound, made by the wings, in swar- tinations and, sometimes, is unintentionally ming mosquitoes is considered to be used for received by predators and parasitoids. The species-specific recognition (e.g. Gibson, Warren, Dipteran parasitic family Tachinidae and & Russell, 2010; Pennetier, Warren, Dabiré, the flesh flies family Sarcophagidae take ad- Russell, & Gibson, 2010; Roth, 1948). Wing vi- vantage of acoustic signalling in Orthoptera bration is also used in the courtship dances of (crickets) and Hemiptera (cicadas), enabling Drosophila species (Von Schilcher, 1976). the parasitic exploitation. Guided by acoustic communication signals, these flies identify B. Percussion – Striking one part of the body and localize their singing target, depositing against another as a communication system their larvae on or close the host. Larvae then for pair formation, as known for example, the develop as endoparasites, eventually killing Australian moth (Lepidoptera); males produ- the host (W. Cade, 1975; Fowler, 1987; Hed- ce ultrasonic acoustical long distance signals wig & Robert, 2014; Leonide, 1969; Soper, to attract sexually receptive females and to Shewell, & Tyrrell, 1976). establish territorial residency in competition with other males (Alcock & Bailey, 1995). 3. Sound-producing mechanisms in insects Striking the substrate with the tip of the Insects, as small living species in a large ecosys- abdomen is also considerate as a “percussion” tem, require specific methods of communica- signal. An example of an insect that uses per- tion to overcome the relatively large distances cussion as a sound-producing mechanism is a separating individuals from potential mates. species of the suborder Arctoperlaria (Plecop- Their small size poses the intrinsic problem of tera), which produce drumming signals on the separation of the sexes by relatively enormous substrate as a mating system. The male emits distances. To overcome this problem, insects a species-specific call searching for the fema- have evolved behavioural strategies and com- le, once the female answer a duet is establis- munication systems, largely visual, chemical, hed with vibrational signals then she became or acoustical, to insure effective mate finding stationary; the male starts localizing the sta- (Capinera, 2008). tionary female until location and mating are Insects have evolved special features that accomplished (Stewart & Sandberg, 2005). allow them to be acoustical animals. Many groups have specialized mechanisms of sound C. Stridulation – In general the term stri- production and hearing organs, which are dulation is inaccurately used to name any used in intraspecific acoustic communication mechanism of sound production in insects (Claridge, 2005). Researchers have classified (Haskell, 1961), however that denies the utili- sound producing mechanisms in insects. Ewing ty of the term. Stridulation consists of sounds

50 Quehacer Científico en Chiapas 9 (2) 2014 produced by frictional mechanisms, involving ce that sound plays in their biology. Different the movements of two specialized body parts mechanisms have evolved in the same orders against each other in a systematic patterned of insects; this suggests that sound-producing manner (Claridge, 2005). mechanisms may have evolved many times Stridulation has been associated to three pha- over the phylogeny of a group (Haskell, 1961). ses of mating behaviour in certain Orthoptera. The first phase comprises of the response stri- 4. Insect hearing dulation from the receptive female orientation Insects are adapted to produce and receive towards and locomotion to the male. The female acoustic signals (sounds), which they use in di- arrived near the male, stridulating in response fferent behavioural contexts, primarily intras- to mate song; the male, once noticing the female, pecific communication (e.g. mate attraction, sings the courtship song, engages the genitalia courtship and rivalry behaviour), detection and and copulation occurs (Haskell, 1958). avoidance of predators and host localization by parasitoid insects (Straub & Lakes-Harlan, D. Click mechanisms – These sounds de- 2014). All sounds derive from vibrations trans- pend on the deformation of a modified area of mitted through solid substrates or fluid media, cuticle, generally by contraction and relaxa- such as air and water. Insects have specialised tion specialized musculature within the insect receptors that detect external vibrations as body. This movement results in a succession airborne and substrate transmitted emissions of clicks which may be repeated quickly in (Claridge, 2005). distinctive patterns. Tymbal is the name of There are five main types of hearing organs the specialized area of cuticle, as exempli- in insects (Table 2). These are: fied in the loud singing cicadas (Hemiptera). For example, the males of Tibicina (Hemip- A. Hair sensillae of various types – Insects tera) cicada species produce a sustained and have numerous sensory organs scattered over monotonous calling song by tymbal activity. and within their body. Many of the sensory This acoustic signal constitutes the first step structures are mechanical sensors that bend, in pair formation, attracting females at long indicating contact with a surface or wind and distances, and is involved in male-male inte- air movement over the structure. The simplest ractions (Sueur & Aubin, 2003). of mechanoreceptors may consist of a single hair or seta that projects from the cuticle surface. E. Air expulsion – This is an unusual sound- Sensillum is called at the simple receptor, gene- producing mechanism within insects. This rally with only one sensory neuron connecting it sound is described as an exhalatory sound, to the central nervous system (Capinera, 2008). frequently expelled via the tracheal spiracles, however little is known about its function B. Scattered chordotonal sensillae – More (Ewing, 1989). The Madagascar hissing coc- complex sensory organs are composed of many kroach Gromphadorhina portentosa, is able sensillae, that is, they have many sensory to produce audible hisses from a pair of modi- neurons connecting to the central nervous fied spiracles. Adult males hiss in three social system. Whether one or many, each sensory contexts: during courtship, during copulation, neuron is enclosed in one to several sheath and during aggressive encounter. Adults and cells, and connected by a relatively long axon nymphs of both sexes also hiss when distur- to the central nervous system. The scolopale, bed (Nelson & Fraser, 1980). sclerotized cap cell, is in contact with the site The above-mentioned categories are not where stimulation will occur, usually some in- completely exclusive and some insects may use ternal structure or the cuticular surface. Any combinations of them. There are a great va- stretching or movement of the structure to riety of sound-producing mechanisms evolved which the scolopale is attached will stimulate by insects; this should suggest the importan- the dendrites of the sensory neuron and may

Quehacer Científico en Chiapas 9 (2) 2014 51 Table 1. Insect vibrational communication categories Sound-producing mechanisms in insects Five categories Description Representative Orders Major function(s) (Ewing, 1989) (Claridge, 2005) (Capinera, 2008; Klots, 1977) (Capinera, 2008) A. Vibration Sound emissions which result from vibrations, most usua- -Diptera -Neuroptera -Mate finding (Tremulation) lly oscillations of the abdomen, either dorso-ventrally or -Hemiptera -Plecoptera -Species-specific recognition laterally, and/or by the wings. Tremulation - sound pro- -Heteroptera -Trichoptera -Mating inducement duction transmitted through the legs to the substrate on (Neuroptera) which the insect is walking or standing. B. Percussion Striking of one body part against another or striking of -Blattodea -Lepidoptera -Mate finding the substrate with the tip of the abdomen. -Coleoptera -Orthoptera -Species-specific recognition -Hemiptera -Plecoptera -Mating inducement (Blattodea) -Heteroptera -Psocoptera -Queen stimulation -Hymenoptera -Trichoptera (Hymenoptera) -Isoptera -Colony alarm (Hymenoptera, Isoptera) C. Stridulation Sounds produced by frictional mechanisms, involving the -Blattodea -Orthoptera -Mate finding movements of two specialized insect body parts against -Hemiptera -Plecoptera -Mating inducement (Blattodea) each other in a regular patterned manner. -Heteroptera -Species-specific recognition -Defensive and territorial behaviour D. Click These sounds rely on the deformation of a modified -Hemiptera -Mate finding Mechanisms area of cuticle, generally by contraction and relaxation -Heteroptera of special musculature within the insect body. This movement results in a succession of clicks which may be repeated quickly in distinctive patterns. Tymbal is the name of the specialized area of cuticle. E. Air Expulsion Unusual exhalatory sounds, often expelled via the tra- -Blattodea -Mate finding cheal spiracles. -Lepidoptera -Defensive and territorial behaviour

set up a series of nerve impulses transmit- cuticular tympanum stretched across a frame ted to the central nervous system. If only one backed by an air sac or other tracheal struc- sensory neuron and scolopale is present, the ture behind the tympanum, and sensory neu- single unit is called a scolopodium, or chordo- rons organized in scolopidia attached to the tonal sensillum (Capinera, 2008). tympanal membrane. Air-borne sound waves cause the tympanum to oscillate, and activa- C. Johnston’s organ – Johnston’s organ is te sensory neurons enclosed by sending nerve a large complex chordotonal organ (collection signals to the central nervous system. The air of sensory cells) that usually consists of many cavity or tracheal sac plays an important role scolopidia. This organ is located between the as a resonating chamber and for directional second (the pedicel) and third joints of each an- processing (Capinera, 2008). tenna of most adult insects; some hexapods (Co- llembola and Diplura) do not have a Johnston’s E. Sub-genual organ – This hearing organ organ. This organ responds to several kinds of is a complex chordotonal organ composed of stimuli in different insects, including acting as numerous scolopidia. The name “subgenual” a proprioceptor to indicate movement of the means below the knee (from Latin for knee, antennae; serving as a gravity indicator; moni- genu).This complex chordotonal organ usually toring wing-beat frequency in relation to flight is located near the joint between the femur speed in some Diptera; indicating ripples at the and tibia. It acts as a proprioceptor (a recep- water surface in gyrinid beetles; and functio- tor of internal stimuli) and detects vibrations ning as a sound reception in mosquitoes and of the substrate on which the insect rests. The perhaps other insects (Capinera, 2008). subgenual organ is especially well developed D. Tympanal organs – Paired structures in crickets (Gryllidae) and katydids (Tettigo- are characterized by the presence of a thin nidae) and is closely associated with a tym-

52 Quehacer Científico en Chiapas 9 (2) 2014 panal organ, with both organs located on the appear, (2) from which sensory precursor or- tibia (Capinera, 2008). gan did an ear evolve, (3) under which selec- Straub & Lakes-Harlan (2014) mentioned tion pressure(s) did the ear originate, (4) how that tympanal organs have evolved at least 18 did the hearing organ diversify further, and times independently in diverse taxa of seven (5) which physiological and behavioural adap- insect orders as: Lepidoptera (butterflies and tations occurred with a hearing sense? moths), Orthoptera (locusts, crickets, bush crickets, and katyids), Diptera (flies), Hemip- 5. Case of study-Cricket acoustic communication tera (cicadas and water striders), Coleoptera Crickets use acoustic signals for communica- (beetles), Mantodea (mantids) and Neuropte- tion; their melodic songs can be appreciated on ra (lacewings). However, according to Straub a warm summer evening. Male crickets produce & Lakes-Harlan (2014) further studies on a calling, courtship and rivalry song by rhyth- the evolution of hearing are required to solve mically rubbing their wings against each other some central evolutionary questions, mainly (Hedwig, 2014). The calling song of the Medi- (1) where in a given lineage did tympanal ears terranean Field Cricket (Gryllus bimaculatus)

Table 2. Insect hearing organs

Insect hearing organs Receptor Order Position Preferred Stimulus (Haskell, 1961) A. Hair sensillae of various -All orders Almost anywhere. Found predomi- Usually tactile sensillae, but types nantly on thorax and abdomen of respond to fairly high intensi- Orthoptera and Lepidoptera and ty air-borne sound on anal cerci of Orthoptera B. Scattered chordotonal sen- -All orders Almost anywhere in the body Air-borne sound sillae Water-borne sound Vibration of the substrate

C. Johnston’s organ -All orders 2nd segment of antenna Air-borne sound Water-borne sound Vibration of the substrate D. Tympanal organs -Orthoptera: Acridoidea 1st segment abdomen Air-borne sound Tettigonioidea Tibia of fore leg Detection of high frequency Grylloidea Tibia of fore leg sound waves in the air

-Homoptera: Metathorax and base of abdomen Air-borne sound Cicadidae Diptera

-Lepidoptera: Noctuoidea Metathorax Air-borne sound Pyralidina Abdomen Geometroidea 1st or 2nd segment abdomen except Axiidae 7th segment abdomen

-Heteroptera: Corixidae Water-borne sound, perhaps Notonectidae Metathorax air-borne as well Pleidae Metathorax Nepidae Metathorax Naucoridae Metathorax Metathorax E. Sub-genual organ -Orthoptera Commonly the proximal region Vibration of the substrate -Plecoptera of the tibia of all legs -Lepidoptera -Hymenoptera -Hemiptera

Quehacer Científico en Chiapas 9 (2) 2014 53 consists of chirps of four to five sound pulses Insects, as small living species in large ecosys- (Figure 1A) that are repeated at 2-3 times per tems, require specific methods of communication second. Female crickets are attracted by this to overcome the relatively large distances separa- calling song and walk or fly towards singing ting individuals from potential mates. To overco- males (Figure 1B). This acoustic orientation me this problem, insects have evolved behavioural is called phonotaxis (Doherty, 1985; Hedwig, strategies and communication systems, largely 2006; Popov & Shuvalov, 1977). visual, chemical or acoustical, to insure effective Phonotactic behaviour can be studied by mate finding. Many groups of insects have spe- playing computer generated artificial calling cialised mechanisms of sound production and songs to a female cricket walking on a trac- hearing organs, which are used in acoustic com- kball. This method allows a highly precise munication within the same species. measure of the female walking speed and direc- The acoustic signals that the insects produ- tion towards a sound pattern (Doherty, 1991; ce can be associated with insect behaviours, Hedwig & Poulet, 2004, 2005). Song pattern, such as mate attraction, courtship, and terri- frequency, and intensity are parameters that torial behaviour. Interestingly, sound can be can be tested in order to identify the species- used not only for communication within the specific female preferences for a calling song. same species, but also between different species. This interspecific behaviour is present CONCLUSIONS in flesh flies who take advantage of acoustic signalling in crickets and cicadas. Guided by Insects are highly acoustic animals that have fas- acoustic communication signals, these flies cinated nature scientists since many centuries. identify and localise their singing target, de-

Figure 1. A. Natural calling song of the Mediterranean Field Cricket (Gryllus bimaculatus) consisting of chirps of four sound pulses. B. Male Medite- rranean Field Cricket singing rubbing his wings against each other. In addition, the ear of the cricket can be visualized as a white spot in his front leg.

54 Quehacer Científico en Chiapas 9 (2) 2014 positing their larvae on or close the host; lar- Faure, P.A. & Hoy, R.R. (2000). The sounds of silence: cessa- tion of singing and song pausing are ultrasound-induced vae then develop as endoparasites, eventually acoustic startle behaviour in the katydid Neoconocephalus killing the host. ensiger (Orthoptera: Tettigoniidae). Journal of Comparati- The study of animal communication is a very ve Physiology A, 186, 129-142. Fowler, H.G. (1987). Field confirmation of the phonotaxis of interesting discipline that not only enlightens Euphasiopteryx depleta (Diptera: Tachinidae) to calling us with pure biological knowledge, but also can males of Scapteriscus vicinus (Orthoptera: Gryllotalpidae). be useful as a strategy to control insect pests, Florida Entomologist, 70, 409-410. Gibson, G.; Warren, B. & Russell, I.J. (2010). Humming in tune: Sex which affect every year and causes losses of mi- and species recognition by mosquitoes on the wing. Journal of llions of pounds in farming. The communica- the Association for Research in Otolaryngology, 11(4), 527-540. Greenfield, M.D. (2014). Acoustic Communication in the Nocturnal tion of animals still has unrevealed mysteries, Lepidoptera. In: B. Hedwig (Ed.), Insect Hearing and Acoustic which future research will help to discover. Communication (pp. 81-100). London, UK: Springer. Haskell, P.T. (1958). Stridulation and associated behaviour in certain Orthoptera. 2. Stridulation of females and their be- ACKNOWLEDGEMENTS haviour with males. Animal Behaviour, 6(1), 27-42. Haskell, P.T. (1961). Insect sounds (p. 189). Chicago: Quadran- gle Books. I would like to acknowledge the valuable fee- Hedwig, B. (2006). Pulses, patterns and paths: neurobiology of dback on this manuscript from Dr. Hedwig Ber- acoustic behaviour in crickets. Journal of comparative physiology. A, Neuroethology, sensory, neural, and behavioral thold, my PhD supervisor at the Department of physiology, 192, 677-689. Zoology, University of Cambridge, England. Hedwig, B. (2014). Insect Hearing and Acoustic Communica- tion. (B. Hedwig, Ed.) (p. 222). London, UK: Springer. Hedwig, B. & Poulet, J. (2004). Complex auditory behaviour emer- REFERENCES ges from simple reactive steering. Nature, 430, 781-785. Hedwig, B. & Poulet, J. (2005). Mechanisms underlying phono- Alcock, J. & Bailey, W.J. (1995). Acoustical Communication and tactic steering in the cricket Gryllus bimaculatus revealed the Mating System of the Australian Whistling Moth Heca- with a fast trackball system. The Journal of experimental tesia exultans (Noctuidae, Agaristinae). Journal of Zoology, biology, 208, 915-927. 237(3), 337-352. Hedwig, B. & Robert, D. (2014). Auditory Parasitoid Flies Ex- Bailey, W.F. & Haythornthwaite, S. (1998). Risks of calling by ploiting Acoustic Communication of Insects. In: B. Hedwig the field cricketTeleogryllus oceanicus: potential predation by (Ed.), Insect Hearing and Acoustic Communication (pp. 44- Australian long-eared bats. Journal of Zoology, 244, 505-513. 63). London, UK: Springer. Belwood, J.J. & Morris, G.K. (1987). Bat predation and its in- Huber, F. (1960). Untersuchungen über die Funktion des Zen- fluence on calling behaviour in neotropical katydids. Scien- tralnervensystems und insbesondere des Gehirnes bei der ce, 238, 64-67. Fortbewegung und der Lauterzeugung der Grillen. Journal Busnel, M.C. (1953). Contribution à l’étude des émissions of Comparative Physiology A, 44, 60-132. acoustiques des Orthoptères. Recherches sur les spectres Kahn, M.C. & Offenhauser, W. (1949). The identification of de fréquence et sur les intensités. Annales des épiphyties, certain West African mosquitoes by sound. The American 3, 333-421. journal of tropical medicine and hygiene, 1(5), 827-836. Cade, W. (1975). Acoustically orienting parasitoids: Fly phono- Klots, E.B. (1977). 1001 questions answered about insects (p. taxis to cricket song. Science, 190, 1312-1313. 260). Courier Dover Publications. Cade, W.H. (1980). Alternative male reproductive behaviors. Leonide, J.C. (1969). Recherches sur la biologie de divers dip- Florida Entomologist, 63, 30-45. teres endoparasites d’Orthopteres. Memoires du Museum Capinera, J.L. (2008). Encyclopedia of entomology (vol. 2). Springer. National d’histoire Naturelle serie A, Zoologie, 53, 1-246. Claridge, M.F. (2005). Insect Sounds and Communication - An Nakano, R.; Skals, N.; Takanashi, T.; Surlykke, A.; Koike, T.; Introduction. In: S. Drosopoulos & M.F. Claridge (Eds.), In- Yoshida, K.; Maruyama, H. et al. (2008). Moths produ- sect sounds and communication: physiology, behaviour, eco- ce extremely quite ultrasonic courtship songs by rubbing logy, and evolution (pp. 3-10). CRC Taylor & Francis Group. specialize scales. Proceedings of the National Academy of Conner, W.E. (2014). Adaptive Sounds and Silences: Acoustic Sciences, 105, 11812-11817. Nelson, M. & Fraser, J. (1980). Sound production in the cockro- Anti-Predator Strategies in Insects. In: B. Hedwig (Ed.), ach, Gromphadorhina portentosa: evidence for communica- Insect Hearing and Acoustic Communication (pp. 65-79). tion by hissing. Behavioral Ecology and Sociobiology, 6(4), London, UK: Springer. 305-314. Doherty, J. (1985). Phonotaxis in the cricket, Gryllus bimacula- Pennetier, C.; Warren, B.; Dabiré, K.R.; Russell, I.J. & Gibson, tus DeGeer: comparisons of choice and no-choice paradigms. G. (2010). “Singing on the Wing” as a Mechanism for Spe- Journal of Comparative Physiology A, 157, 279-289. cies Recognition in the Malarial Mosquito Anopheles gam- Doherty, J. (1991). Song recognition and localization in the pho- biae. Current Biology, 20(3), 131-136. notaxis behavior of the field cricket, Gryllus bimaculatus (Or- Popov, A.V. & Shuvalov, V.F. (1977). Phonotactic Behavior of Cric- thoptera: Gryllidae). Journal of Comparative Physiology A. kets. Journal of Comparative Physiology A, 119, 111-126. Eggers, F. (1911). Über das thoracale tympanale Organ der Pumphrey, R.J. (1940). Hearing in insects. Biological Reviews, Noctuiden. Sitzungsberichte der Naturforscher-Gesells- 15(1), 107-132. chaft bei der Universität Tartu (Dorpat), 30, 138-145. Regen, D.J. (1913). Über die Anlockung des Weibchens von Gryllus Ewing, A.W. (1989). Arthropod Bioacoustics: Neurobiology and Be- campestris L. durch telephonisch übertragene Stridulationslau- haviour. Ithaca, New York: Comstock Publishing Associates. te des Männchens. Pfltig. Arch. ges. Physiol., 155(1), 193-200.

Quehacer Científico en Chiapas 9 (2) 2014 55 Roeder, K.D. (1969). Acoustic interneurons in the brain of noc- Stewart, K.W. & Sandberg, J.B. (2005). Vibratory communi- tuid moths. Journal of Insect Physiology, 15(5), 825-838. cation and mate searching behaviour in stoneflies. In: S. Roeder, K.D. & Treat, E.A. (1957). Ultrasonic reception by the Drosopoulos & M. F. Claridge (Eds.), Insect sounds and tympanic organ of noctuid moths. Journal of Experimental communication: physiology, behaviour, ecology, and evolu- Zoology, 134, 127-158. tion (pp. 179-186). CRC Taylor & Francis Group. Roth, L.M. (1948). A study of mosquito behavior. An experimen- Straub, J. & Lakes-Harlan, R. (2014). Evolutionary and Phylo- tal laboratory study of the sexual behavior of Aedes aegypti genetic Origins of Tympanal Hearing Organs in Insects. In (Linnaeus). American Midland Naturalist, 265-352. B. Hedwig (Ed.), Insect Hearing and Acoustic Communica- Von Schilcher, F. (1976). The role of auditory stimuli in the courtship tion (pp. 5-26). London, UK: Springer. of Drosophila melanogaster. Animal Behaviour, 24(1), 18-26. Sueur, J. & Aubin, T. (2003). Specificity of cicada calling songs Schwabe, J. (1906). Beiträge zur Morphologie und Histologie in the genus Tibicina (Hemiptera: Cicadidae). Systematic der tympanalen Sinnesapparate der Orthopteren. Zoologica Entomology, 28(4), 481-492. (Stuttgart) 20, 50, 1-154. Suga, N. & Katsuki, Y. (1961). Central mechanism of hearing in Soper, R.; Shewell, G. & Tyrrell, D. (1976). Colcondamyia auditrix insects. The Journal of Experimental Biology, 38(3), 545-558. nov. sp. (Diptera: Sarcophagidae), a parasite which is attrac- Zuk, M.; Rotenberry, J.T. & Tinghitella, R.M. (2006). Silent night: ted by the mating song of its host, Okanagana rimosa (Ho- adaptive disappearance of a sexual signal in a parasitized moptera: Cicadidae). The Canadian Entomologist, 108, 61-68. population of field crickets. Biology Letters, 2, 521-525. Spangler, H. (1984). Silence as a defense against predatory bats in two species of calling insects. The Southwestern Naturalist, 29, 481-488.

56 Quehacer Científico en Chiapas 9 (2) 2014