Frequency and temporal pattern-dependent phonotaxis of crickets (Teleogryllus oceanicus) during tethered flight and compensated walking
Phonotactic responses ofTeleogryllus oceanicus were studied with two methods. Tethered crickets were stimulated with sound while they performed stationary flight, and steering responses were indicated by abdominal movements. Walking crickets tracked a sound source while their translational movements were compensated by a spherical treadmill, and their walking direction and velocity were recorded.
During both flight and walking, crickets attempted to locomote towards the sound source when a song model with 5 kHz carrier frequency was broadcast (positive phonotactic response) and away from the source when a song model with 33 kHz carrier frequency was used (negative phonotactic response) (Figs. 2, 4).
One-eared crickets attempted, while flying, to steer towards the side of the remaining ear when stimulated with the 5 kHz model, and away from that side in response to the 33 kHz model (Fig. 3). While walking, one-eared crickets circled towards and away from the intact side in response to the 5 kHz and 33 kHz models, respectively (Fig. 6).
Positive and negative responses differed in their temporal pattern requirements. Phonotactic responses were not elicited when a non-calling song pattern (2 pulses/s) was played with a carrier frequency appropriate for positive phonotactic responses (5 kHz), but this pattern did elicit negative responses with 33 kHz carrier frequency (Figs. 7–10). When an intermediate carrier frequency, 15 kHz, was used, the response type (positive or negative) depended on the stimulus temporal pattern; the calling song pattern elicited primarily positive responses, while the non-calling song pattern elicited negative responses (Figs. 11, 12, 14, 15). A curious phenomenon was often observed in the flight steering responses; while most responses to 15 kHz song pattern were primarily positive, they often had an initial negative component which was supplanted by the positive component of the response after approximately 2–5 s (Figs. 11, 12).
In recent experiments onGryllus campestris, Thorson et al. (1982) described frequency-dependent errors in phonotactic direction (anomalous phonotaxis) and showed how such errors might arise from the frequency-dependent directional properties of the cricket's auditory apparatus. Our findings, particularly the dependence of response type on temporal pattern when 15 kHz carrier frequency was used, argue that frequency-dependent directional properties alone cannot account for positive and negative phonotaxis inT. oceanicus. Rather, these represent qualitatively different attempts to locomote towards and away from the sound source, respectively.
We discuss the possibility that central integration of these opposing tendencies might contribute to anomalous phonotaxis.
Unable to display preview. Download preview PDF.
- Bell GP (1982) Behavioral and ecological aspects of gleaning by a desert insectivorous bat,Antrozous pallidus (Chiroptera: Vespertilionidae). Behav Ecol Sociobiol 10:217–223Google Scholar
- Boyan GS (1981) Two-tone suppression of an identified auditory neurone in the brain of the cricketGryllus bimaculatus (DeGeer). J Comp Physiol 144:117–125Google Scholar
- Camhi JM (1970) Yaw-correcting postural changes in locusts. J Exp Biol 52:519–531Google Scholar
- Casaday GB, Hoy RR (1977) Auditory interneurons in the cricketTeleogryllus oceanicus: physiological and anatomical properties. J Comp Physiol 121:1–13Google Scholar
- Dugard JJ (1967) Directional changes in flying locusts. J Insect Physiol 13:1055–1063Google Scholar
- Elsner N, Popov AV (1978) Neuroethology of acoustic communication. Adv Insect Physiol 13:229–355Google Scholar
- Fenton MB, Bell GP (1979) Echolocation and feeding behaviour in four species ofMyotis (Chiroptera). Can J Zool 57:1271–1277Google Scholar
- Hill KG (1974) Carrier frequency as a factor in phonotactic behaviour of female crickets (Teleogryllus commodus). J Comp Physiol 93:7–18Google Scholar
- Hill KG, Boyan GS (1977) Sensitivity to frequency and direction of sound in the auditory system of crickets (Gryllidae). J Comp Physiol 121:79–97Google Scholar
- Hill KG, Loftus-Hills, JJ, Gartside DF (1972) Premating isolation between the Australian field cricketsTeleogryllus commodus andT. oceanicus (Orthoptera: Gryllidae). Aust J Zool 20:153–163Google Scholar
- Hoy RR (1978) Acoustic communication in crickets: a model system for the study of feature detection. Fed Proc 37:2316–2323Google Scholar
- Hutchings M, Lewis B (1981) Response properties of primary auditory fibers in the cricketTeleogryllus oceanicus (Le Guillou). J Comp Physiol 143:129–134Google Scholar
- Leroy Y (1964) Transmission du paramètre fréquence dans les signaux acoustiques des hybrides F1 et P × F1 de deux grillons:Teleogryllus commodus Walker etT. oceanicus Le Guillou (Orthoptères, Ensifères). C R Acad Sci [D] (Paris) 259:892–895Google Scholar
- Moiseff A, Hoy RR (1983) Sensitivity to ultrasound in an identified auditory interneuron in the cricket: a possible neural link to phonotactic behavior. J Comp Physiol 152:155–167Google Scholar
- Moiseff A, Pollack GS, Hoy RR (1978) Steering responses of flying crickets to sound and ultrasound: Mate attraction and predator avoidance. Proc Natl Acad Sci USA 75:4052–4056Google Scholar
- Murphey RK, Zaretsky MD (1972) Orientation to calling song by female crickets,Scapsipedus marginatus (Gryllidae). J Exp Biol 56:335–352Google Scholar
- Oldfield BP (1980) Accuracy of orientation in female crickets,Teleogryllus oceanicus (Gryllidae): Dependence on song spectrum. J Comp Physiol 141:93–99Google Scholar
- Pollack GS, Hoy RR (1981) Phonotaxis to individual rhythmic components of a complex cricket calling song. J Comp Physiol 144:367–373Google Scholar
- Pollack GS, Plourde N (1982) Directionality of acoustic orientation in flying crickets. J Comp Physiol 146:207–215Google Scholar
- Popov AV, Shuvalov VF (1977) Phonotactic behavior of crickets. J Comp Physiol 119:111–126Google Scholar
- Sandeman DC (1968) A sensitive position measuring device for biological systems. Comp Biochem Physiol 24:635–638Google Scholar
- Schmitz B, Scharstein H, Wendler G (1982) Phonotaxis inGryllus campestris L. (Orthoptera, Gryllidae). I. Mechanism of acoustic orientation in intact female crickets. J Comp Physiol 148:431–444Google Scholar
- Simmons JA, Fenton MB, O'Farrell MJ (1979) Echolocation and pursuit of prey by bats. Science 203:16–21Google Scholar
- Thorson J, Weber T, Huber F (1982) Auditory behavior of the cricket. II. Simplicity of calling-song recognition inGryllus, and anomalous phonotaxis at abnormal carrier frequencies. J Comp Physiol 146:361–378Google Scholar
- Walker TJ (1957) Specificity in the response of female tree crickets (Orthoptera, Gryllidae, Oecanthinae) to calling songs of the males. Ann Entomol Soc Am 50:626–636Google Scholar
- Weber T, Thorson J, Huber F (1981) Auditory behavior of the cricket. I. Dynamics of compensated walking and discrimination paradigms on the Kramer treadmill. J Comp Physiol 141:215–232Google Scholar
- Wendler G, Dambach M, Schmitz B, Scharstein H (1980) Analysis of the acoustic orientation behavior in crickets (Gryllus campestris L.) Naturwissenschaften 67:99–101Google Scholar
- Wohlers DW, Huber F (1978) Intracellular recording and staining of cricket auditory interneurons (Gryllus campestris L.,Gryllus bimaculatus De Geer). J Comp Physiol 127:11–28Google Scholar
- Zaretsky MD (1972) Specificity of the calling song and short term changes in the phonotactic response by female cricketsScapsipedus marginatus (Gryllidae). J Comp Physiol 79:153–172Google Scholar
- Zhantiev RD, Kalinkina IN, Shukanov VS (1975) Characteristics of the directional sensitivity of the tympanal organs in the cricketGryllus bimaculatus DeG. (Orthoptera, Gryllidae). Entomol Obozr 54:249–257Google Scholar