Since the discovery of echolocation in bats, the final phase of an attack on a flying insect, the ‘terminal buzz’, has proved enigmatic. During the buzz, bats increase information update rates by producing vocalizations up to 220 times s−1. The buzz's ubiquity in hawking and trawling bats implies its importance for hunting success. Superfast muscles, previously unknown in mammals, are responsible for the extreme vocalization rate. Some bats produce a second phase—buzz II—defined by a large drop in the fundamental frequency (F0) of their calls. By doing so, bats broaden their acoustic field of view and should thereby reduce the likelihood of insect escape. We make the case that the buzz was a critical adaptation for capturing night-flying insects, and suggest that the drop in F0 during buzz II requires novel, unidentified laryngeal mechanisms in order to counteract increasing muscle tension. Furthermore, we propose that buzz II represents a countermeasure against the evasive flight of eared prey in the evolutionary arms-race that saw the independent evolution of bat-detecting ears in various groups of night-flying insects.
More than 1000 of the approximately 1200 bat species from Yangochiroptera and Yinpterochiroptera are laryngeal echolocators (; figure 1). They produce high-frequency calls and use the returning echoes to orient themselves and estimate the position, size and shape of objects in their vicinity. The majority of these bats forage on airborne insects at night, which they capture in flight in open air (aerial hawking) and, in a few species, close to water surfaces (trawling). Indeed, powered flight and echolocation are considered to be key innovations that allowed bats to exploit this hitherto unrealized foraging niche [3,4]. Despite huge variation in echolocation call design (e.g. peak frequency varies from 9 to 212 kHz) between and within families of echolocating bats [1,4], the way call rate increases over the course of the aerial pursuit of prey appears highly conserved [4–6]. Laryngeal specializations that allow for production of calls of high fundamental frequencies (F0) and fast, smooth frequency modulation also appear similar across species [6,7].
Over the course of an attack, aerially hawking and water trawling bats increase call production rate while reducing call duration [3,4,8]. Attacks, successful or not, almost always end in a ‘terminal buzz’, where bats produce calls at rates above 100 calls s−1 and, in some species, up to and beyond 200 calls s−1 (figures 1 and 2) [3,6–9]. While the apparent function of the buzz is to quickly update the relative position of moving targets [4–6], how bats produce calls at such rates was until recently unknown. We now know that rare superfast muscles power the buzz . For laryngeal echolocating bats, each call emitted is under active neuromuscular control [6,7]; we therefore assume that all bats that buzz possess superfast laryngeal muscles.
During the buzz, some bats (figures 1 and 2) produce a distinct second phase, buzz II, characterized by up to a one-octave drop in the F0 of their calls [3,5,10]. This drop in frequency has been argued to result from a physiological constraint on producing very short calls quickly (see Schmieder et al.  for review). However, the fastest buzzing bat, Craseonycteris thonglongyai (approx. 220 calls s−1), does not lower F0, suggesting otherwise (figure 1; ). An alternative, adaptive hypothesis proposes that bats reduce F0 to broaden their sonar beam. For a given emitter size (e.g. gape in mouth-emitting bats), the lower the frequency, the broader the sound beam [5,9]. Beam broadening has been demonstrated in the vespertilionids, Myotis daubentonii and Eptesicus serotinus (figure 2; ). In close quarters, even a small positional change on the part of the insect could put it outside the bat's acoustic field of view; hence, sonar beam broadening should improve bats' ability to track evasive prey as target distance decreases . A drop in F0 and, presumably, a broad acoustic field of view during the buzz describe most species in Vespertilionidae and Molossidae [3,5,8], and the emballonurid, Rynchonycteris naso (figure 1). Buzz II is sometimes also observed during complicated landing manoeuvres, indicating its importance in motor control [11,12].
In this opinion piece, our goal is to provide a plausible functional explanation for the buzz and the drop in frequency that characterizes buzz II. We suggest an evolutionary scenario, where production of high repetition rate buzzes and thus superfast muscles were an adaptation for exploiting the niche of night-flying insects. Nocturnal insects from a variety of taxa then evolved ultrasound-sensitive ears and auditory-evoked evasive flight manoeuvres [4,13]. We hypothesize that buzz II beam broadening represents an evolutionary countermeasure selected for as a result of the unpredictable evasive flight manoeuvres of eared, night-flying insects. Beam broadening during the buzz would have improved a bat's ability to secure ever more evasive prey during the final phase of pursuit . As we argue below, lowering F0 requires recruitment of an unknown laryngeal mechanism.
Laryngeally echolocating bats produce sound by airflow-induced oscillation of the specialized vocal membranes in the larynx (figures 1 and 2; [6,7]). These oscillations cause pressure changes in the vocal tract, radiated as sound. While observations of vocal fold oscillations have not yet been attempted in bats, in other mammals, the oscillation frequency and thus F0 of the sound wave is determined by fold tension . Fold tension is under neural control and affected by rotation of the thyroid relative to the cricoid cartilages (figure 2). This rotation is primarily controlled by a contraction of hypertrophied cricothyroid muscles. Cricothyroid muscle contraction increases tension, increasing sound frequency [6,7]. Consequently, the frequency-modulated downwards sweep of bats' calls is produced as the cricothyroid muscles lengthen and relax.
The rate-limiting step for muscle speed in vertebrate synchronous striated muscle contractions—especially in superfast muscles—is relaxation . If there is not enough time to relax, muscle tension will build up, and during relaxation in lengthening–shortening cycles, no net power will be produced . We have found that bat laryngeal muscles can produce power at up to 180 cycles s−1, rates occurring during the buzz . At these high cycling rates, however, we also observed that the superfast vocal muscles could not completely relax to baseline tension (figure 2). As muscle tension positively correlates to oscillation frequency of the vocal membranes and to sound , these results indicate that F0 would increase with call rate. Physiological constraints on muscle performance would therefore increase F0 (figure 2), rather than decrease F0 as previously suggested.
The only means of counteracting an increase in tension in the anterior cricothyroid muscle would be to recruit additional muscles with an antagonistic effect on vocal fold tension . There are few data on the bats' laryngeal morphology and we hesitate to identify candidate muscles. However, in other mammals, an antagonistic effect can be achieved through an intrinsic (e.g. thyroarytenoid) or extrinsic (e.g. cricopharyngeus) laryngeal muscle. Vertical movement of the larynx may rotate the thyroid cartilage and thus also counteract tension .
Two scenarios for the evolution of laryngeal echolocation in bats are most parsimonious (see recent studies [1,4] for review). One suggests that laryngeal echolocation evolved once and was subsequently lost in the fruit- and nectar-feeding Pteropodidae (figure 1). The other scenario suggests that echolocation evolved twice, independently in Yangochiroptera and in Yinpterochiroptera. Regardless, approximately 55 Mya both groups hunted night-flying insects, insects that until then had enjoyed a relatively predator-free existence [2,4]. Today, more than a dozen taxa of insects have bat-detecting ears . Eared or not, many display meandering or erratic flight, but dedicated evasive flight is linked exclusively to bat-sensitive ears in moths, lacewings and orthopterans as well as several other families of night-flying insects . We assume that, before the existence of bats, most night-flying insects flew more directly than their bat-predated descendants do today .
As a result of the higher rate of information update, bats able to buzz should have had greater success in capturing airborne prey than those bats not so able . We propose that in addition to powered flight and laryngeal echolocation, the buzz represents another important innovation that evolved in response to the challenge of capturing flying insects in the dark. Further, we hypothesize that buzz II evolved as a specific countermeasure against evasive prey, and improved the capture success of insects with bat-detecting ears. This hypothesis generates the testable prediction that, among morphologically similar bats, those without buzz II should eat a relatively smaller proportion of eared insects compared with those that do produce a buzz II. Genetics-based diet analysis across a broad range of species and locations would be an appropriate means of testing it.
The Vespertilionoidea is the most species-rich (approx. 500 species) of the four major bat lineages identified today, all of which originated ca 50 Mya (figure 1; ). Vespertilionids (approx. 400 species) and molossids (approx. 100 species)  are often portrayed as ‘advanced echolocators’ (see Jakobsen & Surlykke  for review). Their ability to lower F0, and thus presumably to broaden their beam during the buzz, supports this contention , and we speculate that buzz II may partially account for species-richness in Vespertilionoidea (figure 1). For example, buzz II may have allowed some species to out-compete others, and/or to subdivide foraging niches.
The ‘arms-race’ between bats and nocturnal insects is a textbook example of predator–prey interaction. There is little doubt that the ultrasound-sensitive ears found in many nocturnal insect families are an independently evolved defence against bats [4,13]. However, while a handful of bats use echolocation call frequencies outside the hearing ranges of moths and other eared insects, it is up for debate whether these calls are really a countermeasure against these insects' auditory-evoked defences [1,4,17]. While the use of passive hearing improves some gleaning bats' ability to capture prey, to date, only the very low intensity calls used by the moth-specializing vespertilionid bat, Barbastella barbastellus, have been convincingly demonstrated to be a bat countermeasure during aerial hawking attacks . With respect to buzz II, the lowering of frequency and broadening of the beam can also be interpreted as an unambiguous adaptation to the sudden, unpredictable movements of eared prey. Therefore, we contend that buzz II was and is a countermeasure to insects with bat-detecting ears, a move on the part of bats that strengthens the metaphor of a predator–prey evolutionary arms-race.
We thank Brock Fenton, Hannah ter Hofstede, Jim Quinn and two anonymous reviewers for comments on the manuscript, and Signe Brinkløv, Inga Geipel and Paul Racey for sharing their unpublished data. Grants from the Danish Natural Sciences Research Council (FNU) supported this work.
- Received November 5, 2012.
- Accepted December 3, 2012.
- © 2013 The Author(s) Published by the Royal Society. All rights reserved.