Hemiptera: Membracidae: Umbonia Crassicornis)
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J Comp Physiol A 42000) 186: 695±705 Digital Object Identi®er 4DOI) 10.1007/s003590000123 ORIGINAL PAPER R. B. Cocroft á T. D. Tieu á R. R. Hoy á R. N. Miles Directionality in the mechanical response to substrate vibration in a treehopper Hemiptera: Membracidae: Umbonia crassicornis) Accepted: 16 May 2000 / Published online: 8August 2000 Ó Springer-Verlag 2000 Abstract The use of substrate vibrations in communi- Key words Substrate vibration á Bending waves á cation and predator-prey interactions is widespread in Localization á Treehopper, Umbonia crassicornis arthropods. In many contexts, localization of the vi- bration source plays an important role. For small species on solid substrates, time and amplitude dierences be- Introduction tween receptors in dierent legs may be extremely small, and the mechanisms of vibration localization are un- For many arthropods, vibrations traveling through the clear. Here we ask whether directional information is substrate are important in communication 4reviewed in contained in the mechanical response of an insect's body Markl 1983; Claridge 1985; Gogala 1985; Henry 1994; to substrate vibration. Our study species was a mem- Stewart 1997; Barth 1998) and in the detection of bracid treehopper 4Umbonia crassicornis) that commu- predators and prey 4Brownell 1977; Barth et al. 1988; nicates using bending waves in plant stems. We used a Pfannenstiel et al. 1995; MeyhoÈ fer et al. 1997). In order bending-wave simulator that allows precise control of to ®nd potential mates, capture prey, or avoid predators, the frequency, intensity and direction of the vibrational it often will be necessary to locate the vibration source. stimulus. With laser-Doppler vibrometry, we measured Localization was once thought not to play an important points on the substrate and on the insect's thorax and role in vibration perception, either because vibrational middle leg. Transfer functions showing the response of interactions take place at close range 4Schwartzkop the body relative to the substrate revealed resonance at 1974) or because the high conduction velocity of vibra- lower frequencies and attenuation at higher frequencies. tional waves will minimize directional cues based on There were two modes of vibration along the body's arrival time dierences between receptors 4see Brownell long axis, a translational and a rotational mode. Fur- 1977; Cokl et al. 1985). However, a number of arthro- thermore, the transfer functions measured on the body pods have been shown to accurately localize a vibration diered substantially depending on whether the stimulus source. Four localization tasks have been investigated, originated in front of or behind the insect. Directional including direction on a two-dimensional surface information is thus available in the mechanical response 4Murphey 1971; Wiese 1974; Brownell and Farley 1979; of the body of these insects to substrate vibration. These HergenroÈ der and Barth 1983; Abbot and Stewart 1993; results suggest a vibration localization mechanism that Goulson et al. 1994); direction in the web of orb-weav- could function at very small spatial scales. ing spiders 4KlaÈ rner and Barth 1982; Landolfa and Barth 1996; Barth 1998); direction in one dimension along a plant stem 4Cokl et al. 1985); and choice R. B. Cocroft1 á R. R. Hoy between two stems at a branching point 4Latimer and Neurobiology and Behavior, Cornell University, Ithaca, Schatral 1983; Steidl and Kalmring 1989; Ota and Cokl NY 14853, USA 1991; Roces et al. 1993; Pfannenstiel et al. 1995). Some R. B. Cocroft1 á T. D. Tieu á R. N. Miles 4&) wave types in substrates including sand 4Aicher and Department of Mechanical Engineering, Tautz 1990), water 4Wiese 1974), and plant stems 4Mi- State University of New York, Binghamton, NY 13902, USA chelsen et al. 1982) have relatively low conduction ve- e-mail: [email protected] locities. For arthropods with a spatial array of vibration Fax: +1-607-777-4620 receptors 4primarily in the legs) in contact with the Present address: substrate, the resulting dierences in arrival time at 1 Division of Biological Sciences, University of Missouri, dierent receptors have proved sucient to resolve the Columbia, MO 65211, USA direction of wave propagation 4Murphey 1971; Wiese 696 1974; Brownell and Farley 1979; HergenroÈ der and Barth information that could be used in locating a vibration 1983; see also Aicher and Tautz 1990). In some cases, source. However, we know of no studies that have directional cues may also be gained from amplitude investigated this possibility. dierences along a gradient 4Rupprecht 1968; Brownell In this study we ask whether the mechanical response and Farley 1979; Latimer and Schatral 1983; Her- of an insect's body depends on the direction of wave genroÈ der and Barth 1983; Cokl et al. 1985). propagation in the substrate. The study species is a Mechanisms of localization in small species on solid membracid treehopper 4Umbonia crassicornis) that substrates, for which the time and amplitude dierences communicates using plant-borne vibrations 4Cocroft between receptors may be extremely small, have been 1996, 1999). We ®rst determine that U. crassicornis are less well studied. The results from studies of large spe- using bending waves in communication, as has been cies of scorpions, spiders and locusts may not translate concluded for other insects 4Michelsen et al. 1982). We directly to smaller scales. For example, when desert then describe a simulator 4a short segment of dowel scorpions 4with legs spanning 5 cm) were placed on driven with two piezoelectric actuators. Details of this substrates in which conduction velocities were ®ve or simulator will be presented in a forthcoming paper more times higher than in their normal sand substrate, 4R.N. Miles et al., in preparation) that mimics the their responses were no longer directional, apparently properties of bending waves in a stem, allowing precise due to insucient time delays 4Brownell and Farley control of the frequency, intensity, and direction of the 1979). Similarly short delays would be experienced by vibrational stimulus. With a free-standing insect on an animal for which the distances between receptors the simulator, we use laser vibrometry to characterize were ®ve or more times smaller. The size range of spe- the response of the body, especially the thorax, to ran- cies that use vibration in communication or prey loca- dom vibrations originating from in front of and behind tion spans more than two orders of magnitude, from the insect. We ®nd resonance at lower frequencies, two spiders with legs spanning 10 cm 4Barth 1993) to modes of vibration, and a pronounced directionality in white¯ies 4Kanmiya 1996) and parasitoid wasps 4Soko- the mechanical response to substrate vibration. These lowski and Turlings 1987) with legs separated by less results raise the possibility of a directional mechanism in than a millimeter. insect vibration perception that could amplify the eects Here we investigate the possibility of a directional of very small time dierences between inputs. mechanism that does not depend on large amplitude and time dierences among receptors. Our starting point is an analogy with an acoustic sound localization system. Materials and methods In the parasitoid ¯y Ormia ochracea 4Diptera: Tachini- dae), the interaction of two modes of vibration in the Study species mechanically coupled ears generates a directional me- U. crassicornis is a subsocial treehopper 4Hemiptera: Membracidae) chanical response to airborne sound, in spite of ex- that feeds on the sap of trees and shrubs in the mimosoid Legu- tremely small time and amplitude dierences between minosae. Two features of its biology make it a useful species for the two ears 4Miles et al. 1995). Given a system 4i.e., this study. First is its relatively sedentary behavior: individuals some structure with a mechanical response to propa- spend most of their lives on host plant stems, leaving only to dis- gating waves) with two modes, one mode that responds perse to a new stem or plant after reaching reproductive maturity or, in the case of males, to search for mates 4Wood 1983; Wood and to the spatial gradient of the quantity being detected and Dowell 1985; R.B. Cocroft, unpublished data). Correspondingly, one that responds to the spatial average of the signal adults often will remain stationary for an extended period when over the region sampled, the mechanical response of the placed in a new location, allowing for repeated measurements on system can dier signi®cantly depending on the direction an intact, free-standing insect. Second is the central importance of vibrational communication in their biology. Substrate-borne sig- of propagation of the signal. The two modes can com- nals are important in communication within broods of young, in bine to convert a small phase dierence across the region maternal care, and in mate attraction and location 4Cocroft 1996, into a large amplitude dierence at various points on the 1999; R.B. unpublished data). structure 4Gerzon 1994). If there are two or more modes Adult U. crassicornis were collected near Miami, Florida, USA and maintained in the lab on potted host plants 4Leguminosae: of vibration in the oscillation of an insect's body resting Mimosoideae: Albizia julibrissin). We restricted our measurements on its legs, then the mechanical response of the body to to females, both because females tended to remain stationary substrate vibration may dier depending on the direc- longer than males on the stem simulator and because they have tion of wave propagation. Studies of two arthropods been a primary focus of studies of vibrational communication in suggest that the body does constitute a resonant system U. crassicornis 4Cocroft 1996, 1999). For this study we used females that were approximately 14±21 days old, as judged by cuticle when driven by substrate vibration 4Aicher et al. 1983; hardness and color. Females had a length 4from front to back tip of Dierkes and Barth 1995; but see Dambach 1972; Ro- pronotum) of 9.0 0.5 mm 4n 35) and a mass of 48.9 9.2 mg hrseitz and Kilpinen 1997).