Do male white-lipped frogs use seismic signals for intraspecific communication?

Do Male White-Lipped Frogs Use Seismic Signals for Intraspecific Communication?1

SYNOPSIS. Modern frogs and toads possess a structurally unique saccule, endowing them with seismic sensitivity greater than that observed so far in any other group of terrestrial vertebrates. In synchrony with their advertisement calls, approximately half of the calling males of one frog species, the Puerto-Rican white-- lipped frog (Leptodactylus albilabris), produce impulsive seismic signals (thumps). The spectral distribution of power in these seismic signals matches precisely the spectral sensitivity of the frog's saccule. The signals have sufficient amplitude to be sensed easily by the frog's saccule up to several meters from the source-well beyond the typical spacing when these frogs are calling in a group. This circumstantial evidence suggests that white-lipped frogs may use the seismic channel in intraspecific communication, possibly as an alternative to the airborne channel, which often is cluttered with noise and interference. Using the frog's vocalizations as our assay, we set out to test that proposition. In response to playback calls, the male white-lipped frog adjusts several of its own calling parameters. The most conspicuous of these involves call timing-specifically the tendency for a gap in the distribution of call onsets, precisely timed with respect to the onsets of the playback calls. When the airborne component is unavailable (e.g., masked by noise), approximately one in five animals produces the calling gap in response to the seismic signals alone.

INTRODUCTION

The inner ears of frogs and toads (anurans) are known to be sensitive to both airborne sound and substrate borne vibration. Based on the connections of anatomical elements, Figure 1 shows putative pathways, into and through the inner ear of a typical modern frog or toad, for the microscopic structural (acoustic) displacements induced by these two modes of stimuli at the animal's periphery (see Lewis and Narins, 1998). The pectoral girdle is connected not only to the ground (e.g., via the forelimbs) but also to the air (e.g., via the body wall). The opercular system (comprising a skeletal element inserted into the oval window and a muscle connecting that element to the pectoral girdle) thus may conduct acoustic displacements from airborne sound as well as ground-borne vibrations (see Lombard and Straughan, 1974; Narins et al., 1988). Whatever their peripheral sources might be, all pathways converge at the oval window. The length and diameter of the bypass channel (periotic duct) dictate that only a tiny fraction of the total acoustic displacement at the oval window is diverted through that channel. Almost all of it passes through the inner ear sensors.

Being the common element in all three paths through the inner ear, the saccule is especially intriguing. Making the anuran saccule even more intriguing is the fact that the volume occupied by it is approximately equal to that occupied by all of the anuran inner ear's seven other sensory organs taken together. What the saccule evidently gives frogs and toads is exquisite sensitivity to substrate vibration, together with an extension of the range of general acoustic sensitivity to frequencies well below those covered by the two auditory papillae (amphibian and basilar).

Most of the anuran saccular volume is filled with a viscous suspension of calcium carbonate crystals (otoconia). The suspension is bounded on its lateral side by a very thin epithelial wall. On its medial side it is bounded in part by the thick connective-tissue core of the membranous labyrinth. Outside the thin epithelial wall is a volume filled with a sodium-rich aqueous solution (periotic fluid) and coupled directly to the oval window. In terrestrial vertebrates, otoconia are found in three inner-ear sensors, the saccule, the utricle, and the lagena. Each of these sensors is equipped with a pad of epithelial tissue (the macula) in which the mechanoreceptor cells (hair cells) are embedded and to which afferent and efferent axons project. In almost every case, the macula is embedded in thick connective tissue and appears to be coupled rigidly to the core of the membranous labyrinth. The one exception among terrestrial vertebrates is the saccular macula of the more recently derived frogs and toads, including Rana catesbeiana and Leptodactylus albilabris, the subjects of this paper. In those animals, the thin epithelial wall is extended and bounds the viscous suspension of otoconia ventrally and medially (in part) as well as laterally. The macular pad forms an island on the ventromedial part of the thin wall. On one side of the pad is the otoconial suspension; on the other side is periotic fluid (rather than thick connective tissue). In adult North American bullfrogs (R. catesbeiana), the saccular macula has approximately 2,500 hair cells (the number increases as the frog grows) and is innervated by approximately 1,100 axons (Lewis and Li, 1973; Dunn, 1978). It is interesting that this sensor, with its large investment in volume and its unique macular structure, is innervated by fewer axons than all but one of the seven other sensors in the bullfrog inner ear. The utricle, for example, has nearly four times as many axons; and the lagena has nearly twice as many. Only the basilar papilla has fewer.