Elsevier

Hearing Research

Volume 296, February 2013, Pages 42-50
Hearing Research

Research paper
Hearing in American leaf-nosed bats. IV: The Common vampire bat, Desmodus rotundus

https://doi.org/10.1016/j.heares.2012.09.011Get rights and content

Abstract

We behaviorally determined the audiograms of three Common vampire bats (Phyllostomidae, Desmodus rotundus), a species specialized to exist exclusively on blood. The bats were trained to respond to pure tones in a conditioned suppression/avoidance procedure for a blood reward and a mild punisher for failures to detect the tones. Common vampire bats have a hearing range from 716 Hz to 113 kHz at a level of 60 dB. Their best hearing is at 20 kHz where they are slightly more sensitive than other bats, and they have a second peak of good sensitivity at 71 kHz. They have unusually good sensitivity to low frequencies compared to other bats, but are less sensitive to low frequencies than most mammals. Selective pressures affecting high-frequency hearing in bats and mammals in general are discussed.

Highlights

► We trained Common vampire bats, Desmodus rotundus, to respond whenever they heard a tone. ► Thresholds were obtained at 30 frequencies from 250 Hz to 116 kHz ► At a sound pressure level of 60 dB, D. rotundus can hear from 716 Hz to 113 kHz ► D. rotundus is more sensitive to low frequencies than any other bat tested behaviorally but does not hear low frequencies as well as most mammals.

Introduction

Despite a common inner ear design and organization of the central auditory system, mammals vary widely in their hearing abilities. Even within a single specialized order, such as bats, there are differences in hearing range and absolute sensitivity, passive sound localization acuity, and echolocation (e.g., Heffner et al., 2001b; Jones and Teeling, 2006; Neuweiler, 2003). The presence of variation among evolutionarily closely related species allows us to explore differences in hearing that may be affected by lifestyle and enabled by differences in anatomy and physiology. The family, Phyllostomidae, offers such an opportunity. It is a large family of New-World leaf-nosed bats with more than 150 species that range from the southwestern United States through Central and South America to Argentina (Greenhall et al., 1983). We have previously reported on the hearing abilities of three species in this family (Short-tailed fruit bat, Jamaican fruit bat, and Greater spear-nosed bat), ranging in size from 18 to 110 g, and having different specializations for foraging—nectar, fruit, or insects and other mammals (Heffner et al., 2003; Koay et al., 2002, 2003). These different diets entail different demands on echolocation, from hovering and echolocating in leaf clutter for fruit or nectar, to finding prey in open flight, to gleaning prey from a substrate (Kalko and Condon, 1998); these in turn may exert different pressures on hearing that should become apparent in a more extensive sample of bats.

Perhaps the most unusual lifestyle in Phyllostomidae is that of vampire bats, of which the Common vampire, Desmodus rotundus, is the most studied. There is little that is not remarkable about vampire bats (e.g., Greenhall and Schmidt, 1988). Their prey are more than four orders of magnitude larger than themselves. Their digestive system is highly derived enabling them to feed off the blood of large mammals such as capybara, peccaries, tapir, and cattle; hence they are an important pest of livestock and, occasionally, of humans. Unlike other bats, vampire bats spend considerable time on the ground and often approach prey from below, climbing up a leg to bite near the foot, or onto the back to bite other highly vascular areas. They are extraordinarily agile on the ground and can take flight from a standing leap to escape the defensive reactions of their large prey—they are the chiropteran equivalent of harrier jets (Greenhall and Schmidt, 1988). Vampire bats are also unusual in that they have infrared heat detectors in three pits surrounding their noseleaf that help them detect blood vessels near the surface (Kurten and Schmidt, 1982). Finally, it has been reported that they use passive hearing to locate prey and have the capacity to identify specific individuals by their breathing sounds (Gröger and Wiegrebe, 2006; Schmidt, 1988; Schmidt et al., 1991).

Common vampire bats may also have atypical hearing in comparison to other bats. Physiological responses from the cochlea and midbrain of vampire bats and the appearance of their brainstem auditory nuclei suggest that they may have significantly better low-frequency hearing than other bats (Kuwabara and Bhatnagar, 1999; Schmidt et al., 1991; Vernon and Peterson, 1966). However, the only behavioral test of hearing in this species used narrowband noises and, while demonstrating that vampire bats have good sensitivity in the midrange of their audiogram, did not determine the entire frequency range of their hearing (Gröger and Wiegrebe, 2006). Thus far no echolocating bat has been found to hear significantly below 1.7 kHz, even though the ability to hear frequencies lower than that is nearly universal among non-chiropteran mammals, among which low-frequency hearing limits range from 17 Hz to 3.6 kHz (e.g., Heffner et al., 2006, 2001a). Therefore it seemed especially worthwhile to determine whether a small echolocating bat could indeed hear below 1 kHz. Accordingly, we here report the audiogram of the Common vampire bat D. rotundus, and compare its hearing to that of other mammals.

Section snippets

Methods

The bats were tested with a conditioned suppression/avoidance procedure in which a bat continuously licked a spout to receive a steady trickle of blood. It was then trained to break contact with the spout whenever it detected a tone to avoid impending shock (Heffner and Heffner, 1995). Thresholds were determined by successively reducing the intensity of the tone until the bats could no longer detect it above chance.

Results

The initial adaptation of the bats to the apparatus, learning to drink from the spout, learning to respond to sound, and becoming reliable observers, altogether required approximately 60–70 sessions. In a typical session lasting approximately 30 min, a bat would consume up to 15 ml of blood (approximately half their body weight). However, we observed that the bats quickly become lethargic after about 12 ml and were less vigilant to warning sounds than they were earlier in the session. Thus data

Previous behavioral studies

A previous behavioral study of auditory thresholds for D. rotundus was conducted by Gröger and Wiegrebe (2006) using narrow bands of noise centered from 3 to 80 kHz (bandpass filtered with a −3 dB attenuation at ±10% of the center frequency). The behavioral task consisted of walking to the source of a sound in a 3-choice apparatus, and a statistical definition of threshold was applied. (A statistical definition of threshold applied to the psychophysical functions in this report would have

Acknowledgements

Supported by NIH R15-DC009321.

We thank the Milwaukee County Zoo for the use of these bats for behavioral research. We also thank Steve Wing for his very helpful manual for the maintenance and husbandry of Common vampire bats.

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