The fly Ormia ochracea (Diptera, Tachinidae, Ormiini) is a larviparous parasitoid that relies on acoustic cues to detect and localise its host, singing male field crickets (Orthoptera, Gryllidae) (Cade, 1975; Walker, 1986). Since the presence of tympanal hearing was established in flies (Lakes-Harlan and Heller, 1992; Robert et al., 1992), the auditory capacity of O. ochracea has attracted some attention at the level of its anatomy (Robert et al., 1994; Edgecomb et al., 1995), neurophysiology (Robert et al., 1992), biomechanics (Miles et al., 1995; Robert et al., 1996; Robert et al., 1998) and behaviour (Walker, 1993; Wagner, 1995; Ramsauer and Robert, 2000). Constituting an evolutionary innovation within the order Diptera, these hearing organs are also endowed with an original method of sensing the direction of a sound source. Directional hearing is mediated by intertympanal mechanical coupling, a process that amplifies small acoustic cues into significant interaural time and amplitude differences (Miles et al., 1995; Robert et al., 1996; Robert and Hoy, 1998). Previous research has shown that the gravid female fly – as a gregarious parasitoid – will deposit a clutch of larvae on a host, even when the host has already been parasitised. Larvae hatching from the first clutch develop into adults with a larger mass and body size (Adamo et al., 1995). Such adults also benefit from a higher survival rate (Adamo et al., 1995). Therefore, a female fly’s reproductive success is expected to depend directly on her search efficiency which, in turn, is related to the fly’s auditory capacity and to the cricket’s acoustic conspicuousness. Several studies show that female flies prefer cricket calling songs with a longer chirp duration and a higher chirp amplitude (Wagner, 1995; Lehmann and Heller, 1998; Zuk et al., 1997). Hence, crickets would be expected to modify their song structure to reduce their conspicuousness, at least to parasitoid flies. Alternatively, crickets may also shift their diel activity pattern (Zuk et al., 1993) or interrupt their song completely in the presence of an acoustic parasitoid. Little is known about the phonotactic behaviour of these gracile and elusive flies, mainly because they are crepuscular and nocturnal. Information about phonotactic flight paths may provide deeper insights into auditory perception in O. ochracea and may ultimately also help to explain the evolutionary constraints that resulted in the development of such small hearing organs. Flight trajectories were recorded to address questions about stimulus detectability and localisation and about the strategy of phonotactic orientation. The possible strategy of song interruption employed by the cricket host to reduce his attractiveness to acoustic parasitoids was also analysed. 1039 The Journal of Experimental Biology 204, 1039–1052 (2001) Printed in Great Britain © The Company of Biologists Limited 2001 JEB3140 To reproduce, females of the parasitoid fly Ormia ochracea detect and localise a calling male cricket upon which they deposit their endoparasitic larvae. Calling male crickets are therefore subject to both sexual and natural selection by simultaneously attracting mates and phonotactic parasitoids. The possible strategy of song interruption employed by the cricket host to reduce his attractiveness to acoustic parasitoids was tested in the laboratory by examining the fly’s phonotactic quest in response to synthetic cricket songs. Phonotactic flight trajectories were recorded in three dimensions with a stereo infrared video tracking system while the sound stimulus was controlled on-line as a function of the fly’s position in space. Within a single flight, three distinct phases could be observed: a take-off phase, a cruising phase, during which course and altitude were rather constant, and a landing phase characterised by a spiralling descent towards the sound source. The flies showed remarkable phonotactic accuracy in darkness; they landed at a mean distance of 8.2 cm from the centre of the loudspeaker after a flight distance of approximately 4 m. The present data illustrate the fly’s surprising ability to gauge the direction and distance of a sound source in three dimensions and, subsequently, to find it in darkness and silence. Key words: acoustics, directional hearing, orientation, Diptera, parasite, Ormia ochracea, three-dimensional trajectory. Summary Introduction A SHOT IN THE DARK: THE SILENT QUEST OF A FREE-FLYING PHONOTACTIC FLY PIE MÜLLER* AND DANIEL ROBERT Laboratory for Bioacoustics, Institute of Zoology, University of Zürich, Winterthurerstrasse 190, CH-8057 Zürich, Switzerland *e-mail: piemue@zool.unizh.ch Accepted 11 December 2000; published on WWW 26 February 2001