RESEARCH ARTICLE A novel acoustic-vibratory multimodal duet Kaveri Rajaraman 1,2, *, Vamsy Godthi 3 , Rudra Pratap 3 and Rohini Balakrishnan 1 ABSTRACT The communication strategy of most crickets and bushcrickets typically consists of males broadcasting loud acoustic calling songs, while females perform phonotaxis, moving towards the source of the call. Males of the pseudophylline bushcricket species Onomarchus uninotatus produce an unusually low-pitched call, and we found that the immediate and most robust response of females to the male acoustic call was a bodily vibration, or tremulation, following each syllable of the call. We hypothesized that these bodily oscillations might send out a vibrational signal along the substrate on which the female stands, which males could use to localize her position. We quantified these vibrational signals using a laser vibrometer and found a clear phase relationship of alternation between the chirps of the male acoustic call and the female vibrational response. This system therefore constitutes a novel multimodal duet with a reliable temporal structure. We also found that males could localize the source of vibration but only if both the acoustic and vibratory components of the duet were played back. This unique multimodal duetting system may have evolved in response to higher levels of bat predation on searching bushcricket females than calling males, shifting part of the risk associated with partner localization onto the male. This is the first known example of bushcricket female tremulation in response to a long-range male acoustic signal and the first known example of a multimodal duet among animals. KEY WORDS: Tremulation, Phonotaxis, Onomarchus, Vibration, Bushcricket, Katydid INTRODUCTION The acoustic chorus of insects at dusk is mostly produced by male crickets and bushcrickets to advertise their identity and position to potential mates (Alexander, 1967). Females typically do not produce acoustic signals; they perform phonotaxis, moving towards the source of the call (Robinson and Hall, 2002). This paradigm is modified in some bushcricket genera, where females produce acoustic signals, either spontaneously as in the case of some ephippigerine bushcrickets (Platystolus obvius: Korsunovskaya, 2008) or in response to the male call, resulting in acoustic duets. A duet can be defined as a dialogue between two signalers (Bailey and Hammond, 2004), with a stereotyped temporal relationship between the signal from one individual and the reply from the other individual (Bailey, 2003). Duets are common among some ephippigerine bushcrickets such as Steropleurus stali, Steropleurus nobrei, Platystolus obvius (Hartley et al., 1974; Hartley, 1993), Ephippiger ephippiger (Ritchie, 1991) and Deracantha onos (Korsunovskaya, 2008); zaprochiline bushcrickets such as Meconoma thalassina (Robinson, 1990); and phaneropterine bushcrickets such as Leptophyes punctissima (Robinson et al., 1986), Elephantodeta nobilis (Bailey and Field, 2000), Scudderia curvicauda (Spooner, 1968), Phaneroptera nana (Tauber et al., 2001), Metaplastes spp., Euconocercus iris, Amblycorypha uhleri (Korsunovskaya, 2008), Barbitistes spp., (Stumpner and Meyer, 2001), Caedicia spp. (Bailey and Hammond, 2004), Andreiniimon nuptialis, Ancistrura nigrovittata, Isophya lemone and several Poecilimon species (Heller and von Helversen, 1986). Insect duets typically start with a male call, and the female responds with a fixed latency relative to the male call, that latency being important for species recognition (Bailey, 2003). In many bushcricket species that acoustically duet, the timing of the female’s call relative to the male’s call is species specific and crucial in eliciting male phonotactic behavior (Heller and von Helversen, 1986; Robinson et al., 1986; Hartley, 1993; Stumpner and Meyer, 2001; Bailey and Hammond, 2004). Such duetting can result either in phonotaxis by both sexes that engage in the duet, or in stationary female replies and male-only movement. Exclusively male phonotaxis exists among many phaneropterine genera, including Ancistura, Andreiniimon, Leptophyes, Isophya and Poecilimon spp. (Hartley and Robinson, 1976; Heller and von Helversen, 1986). In some ephippigerine species such as S. stali and S. nobrei, where both sexes perform phonotaxis, male phonotaxis has been shown to outperform female phonotaxis in speed and accuracy (Hartley, 1993). Sometimes the female call stimulates an increase in the male’s calling rate, whether phonotaxis is performed exclusively by males (Robinson, 1980) or by both sexes (Hartley et al., 1974). In contrast to the acoustically duetting species described above, males of some neotropical pseudophylline (Belwood and Morris, 1987; Mason et al., 1991; Morris et al., 1994; Römer et al., 2010) and conocephaline (Morris, 1980; Belwood and Morris, 1987; Morris et al., 1994) species switch between the use of acoustic and vibrational signals to advertise their location to females. This is distinct from the phenomenon where a vibrational by-product of acoustic stridulation gets transmitted along the substratum (Keuper and Kuhne, 1983). Such vibratory components of the stridulatory signal may enhance the ability of the female to recognize the conspecific song (Kalmring and Kuhne, 1980), or to localize the male (Latimer and Schatral, 1983; Wiedmann and Keuper, 1987). Males can broadcast vibrational signals independently of acoustic stridulation by tremulating, i.e. by shaking their bodies in the vertical plane while all their legs remain rooted to the substratum (de Luca and Morris, 1998), thereby vibrating the substrate they sit on. Calling tremulations are observed in the absence of females and are thus distinguished from courtship tremulations that manifest themselves after members of a courtship pair find each other through acoustic signaling (Gwynne, 1977; Mason et al., 1991; Korsunovskaya, 2008). Tremulation as a complex, calling signal has mostly been observed among males of neotropical bushcricket Received 29 March 2015; Accepted 24 July 2015 1 Centre for Ecological Sciences, Indian Institute of Science, Bangalore 560012, India. 2 Centre for Neural and Cognitive Sciences, Hyderabad Central University, Gachibowli, Hyderabad 500046, India. 3 Centre for Nano Science and Engineering and Department of Mechanical Engineering, Indian Institute of Science, Bangalore 560012, India. *Author for correspondence (kaveri.indira@gmail.com) 3042 © 2015. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2015) 218, 3042-3050 doi:10.1242/jeb.122911 Journal of Experimental Biology