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Acoustic Communication in Insects REVIEW

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Acoustic Communication in Insects REVIEW 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 pre- dators, this male moth produces the sounds A. Vibration (including Tremulation) – in the immediate vicinity of the female’s
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