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Vibratory Signals of Four Neotropical Stink Bug Species

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Vibratory Signals of Four Neotropical Stink Bug Species Physiological Entomology (2005) 30, 175–188 Vibratory signals of four Neotropical stink bug species MARIA CAROLINA BLASSIOLI MORAES1 , RAUL ALBERTO LAUMANN1 , ANDREJ COKL2 andMIGUEL BORGES1 1Embrapa Recursos Gene´ticos e Biotecnologia, Brası´lia-DF, Brazil and 2National Institute of Biology, Ljubljana, Slovenia Abstract. The stink bugs Acrosternum impicticorne, Euschistus heros, Piezodorus guildinii and Thyanta perditor (Heteroptera: Pentatomidae) feed and mate on the same host plants and constitute major components of the soybean pest complex in Brazil. During mating, they communicate with species and sex-specific vibratory signals whose spectral properties are characteristic of the subfamily Pentatominae. Songs differ between species in the time structure and amplitude modulation of their units. The repertoire of A. impicticorne, E. heros and T. perditor fits into the scheme described for most investigated stink bugs: females call with a sequence of pulses that differ between species in their duration and repetition rate, and males respond with courtship songs of species-specific temporal structure and amplitude modulation of complex pulse trains. Female calling and male courtship songs are the main constituents of vibratory communication between sexes in the mating period. The other vibratory emissions appear to represent either transitional songs, support recognition during close-range courtship, or are involved in male rivalry. The first recorded vibratory emissions of P. guildinii confirm that the genus Piezodorus represents an exception within the Pentatominae. Irregularly repeated female vibratory signals of P. guildinii do not trigger typical male court- ship responses as they would in the small stink bugs Holcostethus strictus and Murgantia histrionica. On the other hand, complex rivalry with extensive frequency modulation of pulses, as also described in Piezodorus lituratus, opens a new insight into the role of vibratory communication in stink bugs. Key words. Brazil, mating behaviour, soybean pest complex, stink bugs, substrate-borne vibrational signals. Introduction Acrosternum hilare (Cˇokl et al., 2001), Thyanta custator accerra and Thyanta pallidovirens (McBrien et al., 2002), Pentatomidae, with its 4123 described species, is one of the Holcostethus strictus (Pavlovcˇicˇ&Cˇokl, 2001), Euschistus largest families within the Heteroptera, and plant-feeding conspersus (McBrien & Millar, 2003) and Murgantia stink bugs (Pentatominae) comprise its largest subfamily histrionica (Cˇokl et al., 2004). Although the exchange of with several economically important pest species (Panizzi species- and sex-specific vibratory signals plays a key role et al., 2000). Vibratory signals have been recorded, analysed before copulation, data indicate that species recognition and correlated with mating behaviour in Nezara viridula based on different temporal patterns of vibratory songs (Cˇokl et al., 2000a, b), Nezara antennata (Kon et al., 1988), does not completely prevent intra- and interspecific Palomena prasina and Palomena viridissima (Cˇokl et al., hybridization. For example, interspecific copulations 1978), Piezodorus lituratus (Gogala & Razpotnik, 1974), have been observed in the field between N. antennata and N. viridula (Kiritani et al., 1963) and species-specific temporal characteristics do not prevent cross mating between different southern green stink bug populations Correspondence: Dr Maria Carolina Blassioli Moraes, Embrapa ˇ Recursos Gene´ticos e Biotecnologia, Caixa Postal 02372, 70849- (Cokl et al., 2000b). In this respect, male-emitted phero- 970 Brazilia-DF, Brazil. Tel.: þ55 61 4484683; fax: þ55 61 mones may provide an additional barrier to hybridiza- 4484673; e-mail: [email protected] tion, and recent data confirm that species-specific # 2005 The Royal Entomological Society 175 176 M. C. B. Moraes et al. chemical (McBrien & Millar, 1999) and vibratory signals Recording and analysing vibratory songs (Cˇokl & Virant-Doberlet, 2003) interact during commu- nication in the premating period (Miklas et al., 2003). Vibratory signals were recorded from virgin and sexually Although basic steps in the mating behaviour of stink mature bugs (15–25 days after the final moult) (Brennan bugs have been described (Borges et al., 1987) and later et al., 1977; Costa et al., 1998) between 08.00 and 21.00 h confirmed in several species (Cˇokl & Virant-Doberlet, in a sound insulated cage (80 Â 80 Â 80 cm) under daylight 2003), there are still several open questions. There is no conditions, room temperature (26.0 Æ 1.0 C) and humidity information about the modality of signals that trigger (65 Æ 10%). To begin the experiment, a male and a female female calling in the first steps of substrate-borne vibra- were placed on the membrane of a loudspeaker (10 cm in tional communication on a plant. In small pentatomid spe- diameter low-midrange loudspeaker, 40–6000 Hz frequency cies, such as H. strictus and M. histrionica, the calling phase response, impedance 8 O, Radioshack, Taiwan). A 2-cm is lacking or less expressed by females and they are not high, vaseline-coated translucent plastic cylinder was placed always first to start vibrational communication (Pavlovcˇicˇ& over the speaker without contacting the loudspeaker mem- Cˇokl, 2001; Cˇokl et al., 2004). Furthermore, no female brane to prevent the insect moving away from the songs have been recorded in P. lituratus (Gogala & membrane surface. The loudspeaker was positioned on a Razpotnik, 1974) and the first emitted male song has, vibration-free base within a sound insulated cage to avoid in many species, a less stable temporal structure, indicat- environmental noise. Vibrations recorded by the loudspeaker ing that it may represent a transitional form either to were amplified by a microphone amplifier (Sonifex male courtship or rivalry song. Redbox, Type RB-MA1; http://www.sonifex.co.uk/redbox/ For a better understanding of the pentatomid language index.shtml) and home-made operational amplifier expressed by vibratory signals transmitted through plants, TL081CN; http://www.mouser.com), digitized (Aardvark- songs have to be recorded and analysed from many differ- Direct Pro 24/96; Aardvark Computer Systems, Washington, ent species from different continents. Compared with North District of Columbia) and stored on a computer by the use America or Europe, there are few data on vibrational songs of Cool EditPro software (Syntrillium Software 2001; Fort of species living in South America (Cˇokl et al., 2000b). Wayne, Indiana). Thus, the vibratory song repertoire of the four stink bug Vibrations emitted by the insect pair were followed in real species living in Brazil that constitute the major components time with headphones and recorded until they stopped sing- of the soybean pest complex is investigated in the present ing for more than 5 min. To determine the male or female study. The vibratory songs of Acrosternum impicticorne origin of emitted signals, one bug of a dueting couple was (Sta˚l), Euschistus heros (F.), Piezedorus guildinii (Westwood) removed and, to evoke rivalry singing, two males were and Thyanta perditor (F.) are recorded, analysed to deter- combined with one female. Behaviour during singing on a mine the level of species specificity of their spectral and loudspeaker was visually monitored by an observer and temporal properties, and compared with songs of other each individual bug was tested only once per day. previously investigated stink bugs. The aim of the study is Vibratory signals were analysed using Sound Forge 4.5 to determine general characteristics of Pentatominae lan- software (Sonic Foundry; http://www.sonicfoundry.com). guage as expressed by vibratory signals and, in particular, A pulse was defined as a unitary homogeneous parcel of to illuminate differences between these four sympatric spe- vibration of finite duration (Broughton, 1963), pulse trains cies, which feed and mate on the same host plants in Brazil. as repeatable and temporally distinct groups of pulses and a song as a sequence of pulses and/or pulse trains with a distinct beginning and end. Spectra were characterized by Materials and methods the dominant, first harmonic and other subdominant fre- quency peaks, by the spectral width 20 dB below the domin- Insects ant frequency value and by frequency modulation described as downward- or upward-orientated frequency sweep- All experiments were conducted on adult stink bugs of quantified by the frequency difference per signal duration the species A. impicticorne, E. heros, P. guildinii and (Hz sÀ1). Temporal characteristics of pulses and/or pulse T. perditor from laboratory colonies started from adults trains were presented as pulse/or pulse train duration and and nymphs collected on soybean fields near Brazilia, DF, repetition time (the time difference between onsets of two Brazil (15470S and 47550W). Males and females, separated consecutive pulses or pulse trains). Songs were classified, 2 days after the final moult, were reared in plastic cages according to their order of appearance in a dueting couple (height 26 cm, diameter 22 cm) at Embrapa Research (Cˇokl et al., 2001), as female songs 1 and 2 (FS-1 and FS-2), Institute in Brazilia in an environmental room at 26.0 Æ 1.0 C male songs 1, 2 and 3 (MS-1, MS-2 and MS-3) or male and 60 Æ 10% RH, under an LD 14 : 10 h photoperiod with rivalry song (MRS). lighting provided by 16 fluorescent lights of 40 W. Insects Data are presented as means Æ SD, together with the were reared on sunflower
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