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(Cynopterus Brachyotis) Non-Echolocating Fruit Bats

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(Cynopterus Brachyotis) Non-Echolocating Fruit Bats Hearing Research Hearing Research 221 (2006) 17–25 www.elsevier.com/locate/heares Research paper Hearing in large (Eidolon helvum) and small (Cynopterus brachyotis) non-echolocating fruit bats R.S. Heffner *, G. Koay, H.E. Heffner Department of Psychology, University of Toledo, Toledo, OH 43606, United States Received 17 March 2006; received in revised form 16 May 2006; accepted 16 June 2006 Available online 18 September 2006 Abstract Comparing the hearing abilities of echolocating and non-echolocating bats can provide insight into the effect of echolocation on more basic hearing abilities. Toward this end, we determined the audiograms of two species of non-echolocating bats, the straw-col- ored fruit bat (Eidolon helvum), a large (230–350 g) African fruit bat, and the dog-faced fruit bat (Cynopterus brachyotis), a small (30– 45 g) bat native to India and Southeast Asia. A conditioned suppression/avoidance procedure with a fruit juice reward was used for testing. At 60 dB SPL, the hearing range of E. helvum extends from 1.38 to 41 kHz with best sensitivity at 8 kHz; the hearing range of C. brachyotis extends from 2.63 to 70 kHz with best sensitivity at 10 kHz. As with all other bats tested so far, neither species was able to hear below 500 Hz, suggesting that they may not use a time code for perceiving pitch. Comparison of the high-frequency hearing abilities of echolocating and non-echolocating bats suggests that the use of laryngeal echolocation has resulted in additional selective pressure to hear high frequencies. However, the typical high-frequency sensitivity of small non-echolocating mammals would have been sufficient to support initial echolocation in the early evolution of bats, a finding that supports the possibility of multiple origins of echolocation. Ó 2006 Elsevier B.V. All rights reserved. Keywords: Audiogram; Megachiroptera; Yinpterochiroptera; Pteropodiformes; Straw-colored fruit bat; Dog-faced fruit bat; Echolocation; Evolution 1. Introduction Accordingly, the extent to which basic auditory abilities might differ between echolocating and non-echolocating In bats, we are presented with an opportunity to directly bats remains largely unexamined. Although the audio- compare the hearing abilities of echolocating and non- grams of several echolocating bats have been determined, echolocating species within a taxonomic order to provide including Rousettus aegyptiacus, an exceptional pteropid insight to auditory adaptations that might be unique to bat that does echolocate (e.g., Heffner et al., 2003; Koay echolocation. Although most of the approximately 1000 et al., 1998a), the only estimates of hearing in non-echolo- species of bats rely largely on echolocation to detect and cating bats have been physiological (Calford and McA- identify objects, there are approximately 150 species of nally, 1987; Grinnell and Hagiwara, 1972; Neuweiler non-echolocating bats in the family Pteropodidae that rely et al., 1984), thus making comparison between echolocat- on vision and olfaction for orientation and foraging. ing and non-echolocating bats difficult. Recently, we have Because echolocation is such a specialized use of hearing, had the opportunity to study the hearing of two non-echo- it has been the main target of studies of audition in bats, locating Pteropodidae: the straw-colored fruit bat (Eidolon leaving other aspects of their hearing relatively unexplored. helvum), a large (230–350 g) African fruit bat, and the dog- faced fruit bat (Cynopterus brachyotis), a small (30–45 g) * Corresponding author. Tel.: +1 419 530 2684; fax: +1 419 530 2136. species native to India and Southeast Asia. This has E-mail address: Rickye.Heff[email protected] (R.S. Heffner). allowed us to address two issues regarding bat hearing. 0378-5955/$ - see front matter Ó 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.heares.2006.06.008 18 R.S. Heffner et al. / Hearing Research 221 (2006) 17–25 The first issue involves the high-frequency hearing of study. Two male C. brachyotis (bat A, 2 years, 35 g; bat B, bats. Mammals are unique among vertebrates in that virtu- 3 years, 32 g) were also tested. All bats were captive born ally all mammals hear higher than 10 kHz (Heffner and and on loan from the Lubee Bat Conservancy where they Heffner, 2003), whereas non-mammalian vertebrates that had been housed in outdoor enclosures in a quiet rural set- hear higher than 10 kHz are considered remarkable (e.g., ting. While on test, they were housed individually in wood Popper et al., 2004). The main source of selective pressure and plastic mesh cages (48 · 39 · 95 cm). for this high-frequency hearing in mammals has been to The use of animals in this study was approved by the enable them to use the two high-frequency sound-localiza- University of Toledo Animal Care and Use Committee. tion cues, namely, the pinna cues that result from the direc- tionality of the pinnae, and the binaural spectral-difference 2.2. Behavioral apparatus cue, the difference in the frequency-intensity spectrum of a sound reaching the two ears. Because these cues require The behavioral testing was carried out in separate cus- that an animal hear sounds of wavelengths short enough tom-built wire mesh cages (Fig. 1). Each cage was sized to be affected by its head and pinnae, mammals with small appropriately for the species and large enough that the bats heads and pinnae typically hear higher frequencies than could maneuver easily. The test apparatus had the follow- larger mammals (for a review, see Heffner and Heffner, ing pertinent features: the reward spouts were 3-mm brass 2003). As a result, it is not surprising that bats, with their tubing with small oval lickplates at the top (25 · 18 mm for relatively small size, hear higher frequencies than most E. helvum;12· 8 mm for C. brachyotis) and projected ver- mammals. Recently, however, we noted that echolocating tically through the floor at the front of the cage at a height bats hear slightly higher than their small head size would convenient for the bats to reach while they perched on the predict—on average, half an octave higher (Heffner et al., small platform in the middle of the test cage. This configu- 2003). This raises the question whether the extended ration minimized acoustic obstructions between the bats high-frequency hearing of these echolocating bats is also and the loudspeakers. The platform was covered with found in non-echolocating bats, or if it is restricted to bats damp carpet to provide traction and electrical contact for that echolocate. The second issue involves the low-frequency hearing ability of bats. We have previously noted that the distribu- tion of mammalian low-frequency hearing is bimodal, with animals falling into two groups: those that hear below about 250 Hz, and those that do not (Heffner and Heffner, 2003; Heffner et al., 2001a). One implication of this finding is that animals whose limits do not fall below 250 Hz do not use temporal coding for the perception of pitch, but rely solely on place coding. So far, all bats whose audio- grams have been determined fall into the group that does not hear below 250 Hz. Indeed, as Calford and colleagues (1985) noted in their physiological studies, even very large Pteropodidae may not hear as low as similar sized prima- tes. Thus, we wished to verify behaviorally if non-echolo- cating bats have low-frequency hearing as restricted as that of echolocating bats. 2. Methods The equipment and procedures described below are sim- ilar to those used in earlier reports from this laboratory on the hearing of a wide range of different mammals, including bats. Any modifications made were to accommodate the body size and motor abilities of particular species. (For additional detail on behavioral and acoustical apparatus and procedures suitable for testing small mammals, see Heffner et al., 2006). 2.1. Subjects Fig. 1. Drawing of Cynopterus brachyotis in the test cage. The test cage Two E. helvum, one adult male (bat A, 9.5 years, 350 g) was designed to minimize obstructions and reflective surfaces in the sound and one female (bat B, 3.5 years, 260 g) were tested in this field. R.S. Heffner et al. / Hearing Research 221 (2006) 17–25 19 the bat. (For specifics of cage construction see Heffner (SPL re 20 lN/m2) was measured daily with a 1/4-in. et al., 2003; Koay et al., 1998a.) Fruit juice was used as (0.64-cm) microphone (Bru¨el & Kjaer 4939, corrected for the reward and consisted of a mix of cantaloupe, pear juice, free-field with the protection grid on), preamplifier (Bru¨el and vitamin supplement, finely blended and sieved. It was & Kjaer, 2669), and measuring amplifier (Bru¨el & Kjaer, dispensed using a syringe pump housed in a foam-lined 2608, set to 22.4 Hz high pass). The output of the measur- box made of high-density polyethylene and located at the ing amplifier was then routed to a spectrum analyzer back of the test chamber to eliminate dispenser noise. A (Zonic A & D 3525) to monitor the acoustic signal for har- bat was required to maintain mouth contact with the spout monics or distortion. Subsequent testing demonstrated that in order to receive a steady trickle of juice, thus keeping its any measurable harmonics were at least 50 dB below the head in a fixed position within the sound field. A shock level of the fundamental frequency and at least 25 dB generator was connected between the reward spout and below the animals’ thresholds and thus did not contribute platform, and the shock was adjusted for each bat to the unwanted cues. Care was also taken to produce a homoge- lowest level that produced a consistent avoidance response neous sound field (within ±1 dB) in the area occupied by (backing away slightly or lifting the head from the spout).
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