Among the Vocal Vertebrates, Anuran Amphibians (Frogs and Toads) Have Long Been Considered the Champions of Acoustic Simplicity

Acoustic Communication Systems of "Ultrasonic" Frogs

by Victoria Arch, Graduate Student, Ecology and Evolutionary Biology and Center for Tropical Research, Institute of the Environment, UCLA

Among the vocal vertebrates, anuran amphibians (frogs and toads) have long been considered the champions of acoustic simplicity. The majority of anurans produce repetitive, highly stereotyped calls that show little spectral, temporal, or amplitude variation, and contain frequencies between ~100 Hz – 5-6 kHz. However, recent behavioral and neurophysiological research suggests that the tenet of acoustic simplicity may not hold true for all anurans. Among the most striking examples is the Chinese concave-eared torrent frog, Odorrana tormota (previously Amolops tormotus).

Odorrana tormota males not only emit unusually high-pitched calls containing substantial energy in the ultrasonic frequency range (i.e., > 20 kHz), but their h earing extends from ≤ 1 kHz to ~35 kHz, dramatically exceeding previously reported upper limits of anuran frequency sensitivity. Playback experiments demonstrate that the ultrasonic elements are behaviorally relevant, and may be used to avoid masking by broadband but predominately low-frequency stream noise in their habitat. Odorrana tormota is the first non-mammalian vertebrate known to communicate with ultrasound, and its use of this high-frequency channel for intraspecific acoustic communication challenges current understanding of frog sound production and reception mechanisms.

The peripheral auditory system of O. tormota is characterized by a highly unusual morphological feature: the tympanic membranes (i.e., eardrums) are embedded in the skull at the end of canals, similar to those of mammals. These recessed tympana are hypothesized to play a critical role in the reception of ultrasound by facilitating transmission of high-frequency sound waves through the middle-ear. Currently, only one other anuran species, Huia cavitympanum, is known to have recessed tympanic membranes.

Left: Odorrana tormota (photo courtesy of Dr. Albert Feng). Right: Male Huia cavitympanum (photo courtesy of Dr. Ulmar Grafe). Note the morphology of the recessed tympana.

Huia cavitympanum and O. tormota are both Southeast Asian species in the family Ranidae, yet they do not overlap in geographic distribution and are unrelated at the generic level. The habitats in which the frogs are found, however, are remarkably similar; males of both species call in close proximity to rushing streams that produce substantial broadband background noise. Given the similarity of the species’ acoustic environment and peripheral auditory morphology, we predicted that they may have converged on the use of ultrasound for intraspecific communication.

To test this hypothesis, we traveled to Borneo in June and July of 2007 to record the calls of H. cavitympanum using ultrasonic detection and recording equipment. The field team consisted of myself, my advisor Dr. Peter Narins, and Dr. Ulmar Grafe, an Associate Professor of Biology at the University of Brunei Darussalam. We found that the calls of H. cavitympanum are rich, varied and, unexpectedly, include exclusively ultrasonic vocalizations. This is the first time purely ultrasonic vocalizations have been documented in an amphibian. Whether this species uses ultrasound to communicate, however, is yet to be confirmed. If these frogs do communicate ultrasonically, H. cavitympanum and O. tormota present an intriguing comparative system in which to explore the convergence of unusual communication mechanisms in response to similar environmental pressures. The long-term goal of this research is to contribute to a more sophisticated understanding of the mechanistic and evolutionary foundations of high- frequency hearing in vertebrates.

Sound spectrograms (top left panel), waveforms (bottom panel), and instantaneous amplitude spectra (right panel, taken from the approximate center of the recording) of the background noise (a), and five representative calls (b-f) given by a male Huia cavitympanum over a 7-minute period, demonstrating the diversity of its vocal repertoire. Arrows denote the boundary between audible and ultrasonic frequencies. The spectral energy of (d) is entirely in the ultrasound. Temperature during recordings: 26o C.