Published Work

Front. Ecol. Evol., 30 October 2018 | https://doi.org/10.3389/fevo.2018.00172

Response Mode Choice in a Multimodally Duetting Paleotropical Pseudophylline Bushcricket

• Centre for Ecological Sciences, Indian Institute of Science, Bangalore, India

• Department of Biology and Psychology, Ashoka University, Sonipat, India

Females of the pseudophylline bushcricket species Onomarchus uninotatus respond to a conspecific acoustic call with bouts of tremulation, followed by phonotaxis in some cases. This tremulation sends out a vibratory signal that propagates along the branch of the jackfruit trees where these animals are almost always found, and the male is able to localize the signal and perform vibrotaxis toward the female. Males are unable to localize the signal if it emanates from a branch unconnected to their perch, and therefore, female tremulation might not be a productive response when the nearest male is on an adjacent, disconnected tree. We hypothesized that female behavioral response choice between tremulation and phonotaxis might vary with distance from the caller. A semi-naturalistic experiment indicates that if the male and female are 4 m apart on a connected perch, females tremulate, and never perform phonotaxis while males perform vibrotaxis. However, at a distance of 9 m, 4 out of 10 females begin phonotaxis after a period of tremulation. We then hypothesized that features of the male call that indicate caller distance, such as call sound pressure level (SPL), might be responsible for this distance-dependent variation in the choice between phonotaxis and tremulation However, we found that at all SPLs, the female tremulates in response to male calls before attempting phonotaxis and that the probability of phonotaxis and tremulation both increased with calling song SPL. We conclude that our first hypothesis is upheld and that females do behave differently with respect to distance from the male, but that the cue affecting the distance-dependent increase in the probability of initiation of phonotaxis in female response choice is not the SPL of the male's advertisement call.

© 2015. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2015) 00, 1-9 doi:10.1242/jeb.122911

A novel acoustic-vibratory multimodal duet

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 example of bushcricket female tremulation in response to a long-range male acoustic signal and of a multimodal duet among animals.

The Journal of Experimental Biology 216, 777-787 © 2013. Published by The Company of Biologists Ltd doi:10.1242/jeb.078352

Low-pass filters and differential tympanal tuning in a paleotropical bushcricket with an unusually low frequency call

Low-frequency sounds are advantageous for long-range acoustic signal transmission, but for small animals they constitute a challenge for signal detection and localization. The efficient detection of sound in insects is enhanced by mechanical resonance either in the tracheal or tympanal system before subsequent neuronal amplification. Making small structures resonant at low sound frequencies poses challenges for insects and has not been adequately studied. Similarly, detecting the direction of longwavelength sound using interaural signal amplitude and/or phase differences is difficult for small animals. Pseudophylline bushcrickets predominantly call at high, often ultrasonic frequencies, but a few paleotropical species use lower frequencies. We investigated the mechanical frequency tuning of the tympana of one such species, Onomarchus uninotatus, a large bushcricket that produces a narrow bandwidth call at an unusually low carrier frequency of 3.2kHz. Onomarchus uninotatus, like most bushcrickets, has two large tympanal membranes on each fore-tibia. We found that both these membranes vibrate like hinged flaps anchored at the dorsal wall and do not show higher modes of vibration in the frequency range investigated (1.5–20kHz). The anterior tympanal membrane acts as a low-pass filter, attenuating sounds at frequencies above 3.5kHz, in contrast to the highpass filter characteristic of other bushcricket tympana. Responses to higher frequencies are partitioned to the posterior tympanal membrane, which shows maximal sensitivity at several broad frequency ranges, peaking at 3.1, 7.4 and 14.4kHz. This partitioning between the two tympanal membranes constitutes an unusual feature of peripheral auditory processing in insects. The complex tracheal shape of O. uninotatus also deviates from the known tube or horn shapes associated with simple band-pass or high-pass amplification of tracheal input to the tympana. Interestingly, while the anterior tympanal membrane shows directional sensitivity at conspecific call frequencies, the posterior tympanal membrane is not directional at conspecific frequencies and instead shows directionality at higher frequencies.

Department of Molecular and Cellular Biology, Harvard University, Cambridge, Massachusetts 02138

ON Ganglion Cells Are Intrinsically Photosensitive in the Tiger Salamander Retina

Intrinsically photosensitive retinal ganglion cells (ipRGCs) have been well characterized in mammalian systems, both morphologically and electrophysiologically. They show slow, sustained responses to bright light in the absence of photoreceptor-based input, mediated by the photopigment melanopsin. Only one mammalian melanopsin gene is expressed in a small fraction of the retinal ganglion cell population, but there are two genes for melanopsin among nonmammalian vertebrates that are widely expressed in a variety of retinal and extraretinal cell types, along with other photosensitive pigments. The current study provides an electrophysiological study of ipRGCs in the larval tiger salamander (Ambystoma tigrinum), a nonmammalian vertebrate with a well-characterized retina. The results show that the ipRGC population is equivalent to the ON ganglion cell population in the tiger salamander retina. This sheds light on the evolutionary trajectory and functional significance of intrinsic photosensitivity through the vertebrate lineage and also affects our understanding of ON cell activity and development. We have characterized the nature of the intrinsic responses of the ON cell population, compared intrinsic and synaptically based receptive fields, and quantified the spectrum of the intrinsic activity. A wider action spectrum of intrinsic photosensitivity was obtained than would be expected for a single opsin photopigment, suggesting the expression of multiple photopigments in the salamander ipRGC. J. Comp. Neurol. 520:200–210, 2012.