Spatial Orientation in the Bushcricket Leptophyes Punctatissima (Phaneropterinae; Orthoptera): I
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J Comp Physiol A DOI 10.1007/s00359-006-0186-6 ORIGINAL PAPER Spatial orientation in the bushcricket Leptophyes punctatissima (Phaneropterinae; Orthoptera): I. Phonotaxis to elevated and depressed sound sources Jürgen Rheinlaender · Manfred Hartbauer · Heiner Römer Received: 8 August 2006 / Revised: 11 October 2006 / Accepted: 15 October 2006 © Springer-Verlag 2006 Abstract Many species of acoustically interacting Abbreviations insects live in a complex, arboreal or semi-arboreal IID Interaural intensity diVerence habitat. Thus mate Wnding by phonotaxis requires SPL Sound pressure level sound localization in the horizontal and vertical plane. Here we investigated the ability of the duetting bush- cricket Leptophyes punctatissima to orient to one of Introduction three speakers, positioned at diVerent levels in an arti- Wcial grid system, where each point in space could be Sound localization in insects has been studied at vari- reached by the male with almost equal probability. The ous levels: behaviour, the physical cues available for system was designed analogous to a spherical calotte the ear, the directionality of the ears, or the peripheral model of bismuth, where, once the male arrived at any and central processing by receptors and interneurones nodal point had to decide between only three direc- (review Lewis 1983; Michelsen 1998; Pollack 2000). So tions: either up or down and/or left and right. This far, almost all studies have been restricted to the per- design does not favour any phonotactic path of the ception of sound in the horizontal plane. One excep- males. All 12 males tested reached the three speaker tion is a study on crickets which demonstrated—by positions (one in the horzontal plane, one elevated by using a habituation–dishabituation test—that Xying 45°, one depressed by 45° relative to the starting posi- crickets were able to discriminate between ultrasound tion) with only little deviation from the shortest possi- sources separated in elevation (Wyttenbach and Hoy ble path. There was no signiWcant diVerence with 1997), conWrming an observation by May et al. (1988) respect to the whole phonotactic time needed, the that Xying crickets respond diVerently to ultrasound number of segments passed, or the number of stimuli from above and below. The second exception is a received for the diVerent speaker positions. This behavioural study on the parasitoid Xy Ormia ochra- remarkable spatial orientation is achieved although the cea, which exhibit a remarkable phonotactic accuracy insects have no specialized external ear structures such in 3D space, so that after a Xight distance of about 4 m as mammals, or some owls. the Xies approach and land on a loudspeaker within close proximity (Müller and Robert 2001). However, Keywords Bushcricket · Spatial orientation · since the one investigation deals with spatial acuity of Sound localization · Phonotaxis ultrasound hearing in the context of nocturnal preda- tion by bats, and the other with the acuity of a parasit- oid to locate its host, nothing is known about spatial orientation of insects in the context of intraspeciWc J. Rheinlaender · M. Hartbauer · H. Römer (&) communication. Department of Zoology, Institut für Zoologie, The perception of source height, i.e., elevation and Karl-Franzens-Universität, Universitätsplatz 2, W Graz, 8010, Austria depression, is certainly signi cant for many crickets e-mail: [email protected] and bushcrickets, and probably some grasshoppers as 123 J Comp Physiol A well. The microhabitat used by many bushcrickets and In the present paper, we used a bushcricket species, crickets are trees and bushes, where the vertical posi- which oVers several advantages to investigate spatial tion of signallers and receivers can diVer by many hearing. Leptophyes punctatissima is a Phaneropterine meters, and thus spatial hearing is essential. Further- bushcricket, which uses an elaborate communication more, many tropical Phaneropterine bushcrickets live system between male and female. Pair formation is in the rainforest at canopy or mid-canopy levels, and achieved by duetting, where the male song elicits an biologically important sounds may arise from positions acoustic reply in the female, to which the male then above and below the receiver, as well as from diVerent responds by phonotaxis with very high probability locations in azimuth. (Hartley and Robinson 1976; Robinson 1980; Robin- Several reasons may contribute to our lack of son et al. 1986; Zimmermann et al. 1989; Bailey 2003). knowledge with respect to spatial hearing in insects: The male call is both a prerequisite for phonotaxis and one may be historical, because the Wrst profound a reliable indicator for the motivation of the male to studies on the proximate mechanisms of hearing and orient to a female. Further, each following localization acoustic communication in insects have been domi- process can easily be recognized by the experimenter. nated by work on Weld crickets (review Huber et al. Because the male with its short wings is unable to Xy, 1989; Gerhardt and Huber 2002), which were sup- phonotaxis occurs during walking, which facilitates posed to live and orient acoustically near the ground. video-monitoring and quantiWcation. The vertical dis- Thus, sound localisation in the azimuth was supposed tribution of male and female Leptophyes can vary con- to be the only relevant task. Later researchers also siderably during pair formation in the natural habitat, discovered positive and negative phonotaxis of crick- ranging from a position close to the ground to a height ets in Xight, where spatial hearing might become more of up to 5–10 m in a tree (Rheinlaender and Robinson, relevant than for crickets walking on the ground unpublished observations). Thus, a male in nature (Popov and Shuvalov 1977; MoiseV et al. 1978; Huber must distinguish source positions in the azimuth and et al. 1989). Furthermore, experimental paradigms elevation to perform the phonotactic approach towards for studying directional hearing have been applied a female successfully. either to Xat arenas, to Kramer treadmills or to walk- We combined these advantages in a behavioural ing belts, all of which unsuited to study directional paradigm and present for the Wrst time data on spatial hearing in the vertical plane. And Wnally, the only hearing in the context of pair formation of an inverte- valid hypothesis to explain spatial hearing derived brate. from biophysical and behavioural work on mammals and birds like owls, with strong evidence that the detection of the elevation of a sound source depends Methods either on pinnae in mammals or on ear asymmetries in owls (review in Knudsen and Konishi 1979; HeVner Male and female L. punctatissima were collected as and HeVner 1992; Brown 1994). In mammals, the par- larvae during the early summer period of 2004 from ticular shape of the external pinna provides important wild stock locations in the vicinity of Nordkirchen information for the vertical orientation of a sound (Germany). Both sexes were kept physically and source because pinnae act as spatially dependent acoustically isolated from each other in wooden cages Wlters for sound (Butler and Belendiuk 1977; Blauert (90 £ 50 £ 40 cm), supplied with their favoured plant 1983; Fuzessery 1996; Wotton and Simmons 2000). As food (Urtica dioica, Heracleum spondylium, Cirsium a result of this Wltering spectral cues are created that vulgare) and water ad libitum. Pair formation takes humans and other mammals appear to use in localiz- place about 1 week after the Wnal moult of females. ing the elevation of a source. Only males 1–6 weeks after the Wnal moult were used However, Gerhardt and Rheinlaender (1982) were for behavioural experiments. the Wrst to demonstrate that the existence of such struc- Phonotaxis was studied in an artiWcial grid system, in tures may not be essential for spatial hearing. They which each point in space could be reached by the male showed that green tree frogs Hyla cinerea, which lack with equal probability. For this purpose we constructed pinnae or similar anatomical structures; readily localize the most simple model, analogous to a spherical calotte an elevated sound source. Tree frogs and bushcrickets model of bismuth (Fig. 1a). The advantage of such a thus face a similar problem: both live in a complex, 3D-grid is that the male, when arriving at any nodal arboreal or semi-arboreal habitat and need to obtain point has to decide between only three directions: cues about both azimuth and elevation of sound either up or down and/or left and right (Fig. 1b). This is sources without having specialized ear structures. in contrast to a cubic model, where there are Wve possi- 123 J Comp Physiol A the horn, so that they had a diameter of 40 mm and a a depth of 16 mm. They were suspended at the edges of the model, one in a horizontal direction from the start- ing point, and two others at 45° elevated or depressed positions relative to the starting point. Speakers were isolated by about 15 cm from the target sphere (see Fig. 2). They had no direct contact with the grid to pre- vent vibrational transmission of the signal from the active speaker. Furthermore it was guaranteed that also in the Wnal phase phonotaxis took place only in the far Weld of the active speaker (Beranek 1954). The dis- tance between starting point and each speaker was 105 cm. The whole grid was suspended 50 cm above ground level with two ropes attached to a solid bar, so b that any vibration of the soil due to movement of the experimenter did not reach the grid. The model was composed of wooden rods and spheres as nodal points; the distance between two nodal points was 13 cm. This dimension was adapted to the song rate and the walking speed of males, so that a male was expected to produce at least one song ahead of each decision point (but often more than one; see Results).