Hearing in African Pygmy Hedgehogs (Atelerix albiventris): Audiogram, Sound Localization, and Ear Anatomy

Methods

Subjects

Behavioral hearing tests were carried out on four African pygmy hedgehogs (Atelerix albiventris), approximately 5 months old at the beginning of the study. Hedgehogs A (340 g) and B (410 g) were male, and hedgehogs C (340 g) and D (290 g) were female. The animals were housed separately with free access to dry cat food (Purina). They received their water during their daily test sessions. The animals were weighed daily to monitor their condition.

Hearing thresholds were determined for animals A, B, and C from 1-50 kHz; D was tested from 1-32 kHz; A and C were tested at additional frequencies to further define the audiogram. Minimum audible angles for brief noise were determined for hedgehogs A, B, and C. Finally, tone localization performance at 60° separation was determined using pure tones from 3-32 kHz for hedgehog C.Two of the individuals that had been tested behaviorally (A and B) were perfused with formalin for anatomical analysis. These two specimens were dissected in the University of California, Los Angeles, in 2001. The condylobasal length of A was 41.2 mm and of B was 43.1 mm. The frozen body of one further A. albiventris specimen, an albino female (hedgehog E), was provided by a commercial pet supplier in the UK in 2008, and was dissected in the University of Cambridge, UK, in 2021. Its condylobasal length was 41.9 mm.

Behavioral Apparatus

The hedgehogs were tested using a conditioned-avoidance procedure in which a thirsty animal was trained to continuously lick a spout to receive a steady trickle of water. In the audiogram task, warning sounds were then presented intermittently, followed at their offset by a mild electric shock delivered via the spout. The animals learned to avoid the shock by breaking contact with the spout when they heard a warning sound (Heffner and Heffner, 1995). Absolute thresholds were determined by successively reducing the magnitude of the warning tones in blocks of 6-10 trials until the animal could no longer detect it above chance. Noise localization thresholds were determined by training the animals to break contact with the spout when a sound was presented from a speaker to its left, while maintaining contact when a sound was presented from a speaker to its right. The angle of separation between two speakers (centered on the midline) was then reduced in blocks of 8 trials until the animals failed to discriminate between left vs. right sounds. Finally, the ability to use the binaural time and intensity cues was assessed by examining an animals’ asymptotic performance in localizing pure tone pulses at a fixed angle of 60° loudspeaker separation (±30° from midline).

Testing was conducted in a carpeted, double-walled acoustic chamber (IAC model 1204; 2.55x2.75x2.05 m), the walls and ceiling of which were lined with egg-crate foam to reduce sound reflection. The equipment for stimulus generation and behavioral measurement was located outside the chamber and the animals were observed via closed-circuit television.

The hedgehogs were tested in a cage (38 x 21 x 23 cm) constructed of 0.5-in. (1.27 cm) hardware cloth (see Fig. 1). The cage was mounted on a camera tripod 100 cm above the chamber floor. A water spout was mounted vertically in the front of the cage, coming up through the floor to a level of 5 cm above the cage floor. The spout consisted of a brass tube (3 mm outer diameter) with an oval brass disk (2 x 2.5 cm), mounted on the top of the spout at a 50-degree angle and sloping down toward the animal. In this arrangement, the animals faced the front of the cage and maintained normal posture while drinking from the spout. The water spout was connected by plastic tubing to a syringe pump located outside of the chamber. A contact circuit, connected between the spout and cage floor, served to detect when an animal made electrical contact with the spout and activated the syringe pump. Finally, a constant current shock generator was also connected between the spout and cage floor, and a 25-W light mounted 0.5 m below the cage was used to signal the onset and duration of the shock.

Acoustic Apparatus

Audiogram

Pure tones from 1 to 50 kHz were produced using a signal generator (Krohn-Hite 2400 AM/FM) and continuously verified by a frequency counter (Fluke 1900A). The intensity of the tones was adjusted in 5-dB steps using an attenuator (Hewlett Packard 350D), the linearity of which was calibrated throughout the voltage range used for the different intensities being tested. The signal was then was pulsed 400 ms on and 100 ms off for 5 pulses (Coulbourn S53-21), shaped by a rise/fall gate (Coulbourn S84-04) allowing 10 ms rise/fall times for all frequencies, bandpass filtered (Krohn-Hite 3550; ± 1/3 octave) to reduce possible electrical noise, and finally routed to an amplifier (Crown D75). Output from the amplifier was monitored for distortion and noise with an oscilloscope (Tektronix TDS 210) and routed to a loudspeaker inside the sound chamber. The loudspeaker was placed at ear level, approximately 1 m in front of the animal when it was drinking from the spout. Loudspeaker distance was occasionally varied to achieve an easily detectable starting intensity for the animal. Loudspeakers used included a woofer (Infinity RS 2000) for the lower frequencies (1-2 kHz), while piezo (Motorola KSN1005A) and ribbon tweeters (Foster 110T02) were used for frequencies higher than 2 kHz. Frequencies tested were 1, 2, 3, 4, 5.6, 8, 12.5, 16, 32, 40, 45, and 50 kHz.

The sound-pressure level (SPL re 20 µN/m²) was measured daily with a .25-in (.64 cm) microphone (Bruel & Kjaer 4135), microphone pre-amp (Bruel & Kjaer 2619), and measuring amplifier (Bruel & Kjaer 2608). The output from the measuring amplifier was sent to a spectrum analyzer (Zonic A & D 3525), where the signal was inspected for possible harmonics and overtones. The measuring system was calibrated with a sound level calibrator (Bruel & Kjaer 4230). Sound measurements were taken by placing the microphone in the position occupied by the hedgehog’s head when it was drinking at the spout, and pointing it directly toward the loudspeaker (0° incidence). Care was taken to produce a homogeneous sound field (± 1 dB) in the area occupied by the animal’s head and ears.

Noise Localization

To determine minimum audible angle, a single 100-ms broadband noise burst was emitted from one of ten piezo tweeters (Motorola KSN1005A, five pairs with closely matched spectra) mounted on a 2.3-m diameter semi-circular perimeter bar and placed symmetrically left and right of midline. Noise was generated (Zonic A & D 3525), bandpass filtered from 2-50 kHz (Krohn-Hite 3202), pulsed (Coulbourn S53-21), and randomly attenuated through a 3.5-dB range (in .5 dB increments; Coulbourn S85-08) to prevent any slight intensity imbalance from serving as a cue. The signal was then split into two channels and routed to rise/fall gates (Coulbourn S84-04) set to 0 ms rise-decay, amplified (Crown D75), and continuously monitored (Tektronix TDS 210) before being sent to one of the five pairs of speakers inside the sound chamber. Matching the speaker pairs, together with randomizing the intensity on each trial, served to prevent the animals from cueing on acoustic features other than locus cues (later corroborated by the animals falling to chance at the smallest angles tested).

The intensity of the noise bursts was set to 68 dB SPL, an easily detectable level for these animals. Noise bursts were measured and their level equated daily for each speaker pair. Procedures for sound measurement are the same as described above.

Tone Localization

Pure tones used in localization tests were generated and calibrated using the same equipment used to present tones in the audiogram, with the exceptions that the electrical signal was randomly attenuated up to 3.5 dB (in 0.5-dB increments), split into two channels after the filter, and routed to separate channels of the stereo amplifier. Testing was carried out at all frequencies within the hedgehog’s hearing range that could be produced at a 40 dB HL (hearing level) without distortion. For consistency of comparison with different species tested previously, the loudspeakers were placed at a fixed angle of 30° to the left and right of midline (60° total separation) on the perimeter bar.

Each trial consisted of a single tone pulse (100 ms on, 2.3 s off), with intertrial intervals of 1.5 s. Rise-decay times of 10 ms were used for all frequencies to prevent onset and offset transients. The acoustic signals were checked for overtones using a spectrum analyzer (Zonic A & D 3525) and the loudspeakers were matched for intensity before each session. As in the noise localization task, the intensity of the tones was randomly attenuated on each trial over a 3.5-dB range (in .5 dB increments; Coulbourn S85-08). Piezo speakers (Motorola KSN 1005A) were used to present the different frequencies. Frequencies tested were 3, 4, 5.6, 8, 16, 25, and 32 kHz. Additional tests were carried out with a 3-kHz tone that was sinusoidally amplitude modulated (Krohn-Hite 2400 AM/FM, 100% modulation depth) at a rate of 250 or 500 Hz, which produced an ongoing time difference cue in the envelope of the higher-frequency carrier tone (3 kHz).

Behavioral Procedure

Thirsty hedgehogs were trained to make continuous contact with the spout to obtain a steady trickle of water. Drinking from the spout oriented the animals to 0° azimuth. For audiogram determination, a train of 5 tone pulses (400 ms on, 100 ms off; 10 ms rise-fall) was presented at random intervals, followed by a mild electric shock (300 ms maximum duration) delivered through the spout. The hedgehogs learned to avoid the shock by breaking contact with the spout whenever they heard the tone pulses. (The majority of shocks were successfully avoided, in which cases the presence of the shock was signaled by the light that was switched on during the shock.) The shock was adjusted for each animal to the lowest level that would reliably produce an avoidance response to a loud signal. Note that the animals did not develop a fear of the spout, as they readily returned to it after the shock.

Test sessions were divided into 2.4-s trials separated by 1.5-s intertrial intervals. Approximately 22% of the trials contained a warning signal (pulsing tone for the audiogram or a sound from the left of midline for localization), whereas the remaining trials contained safe signals (silence, or sounds from the right of midline for localization). A response was recorded if a hedgehog broke contact for more than half of the last 150 ms of a trial. In the audiogram task, the response was classified as a hit if the trial contained a tone and as a false alarm if no tone was presented. Similarly, a response following a left (warning) sound is a hit while breaking contact following a right (safe) sound would be a false alarm in the localization tasks.

Both the hit and false-alarm rates were determined for each block of 6 to 10 warning trials (approximately 30 associated safe trials) for each stimulus intensity. The hit rate was then corrected for false alarms to produce a performance measure using the following formula: Performance = hit rate – (false alarm rate x hit rate). This measurement proportionally reduces the hit rate by the false alarm rate observed under each stimulus intensity condition and varies from 0 (no hits) to 1 (100% hit rate and 0% false-alarm rate).

Absolute thresholds were determined by reducing the intensity of a tone in successive blocks of 6 to 10 warning trials until the hedgehog no longer responded to the signal above chance (p > .05, binomial distribution). Once a preliminary threshold had been obtained, final threshold determination was conducted by presenting tones varying in intensity in 5 dB increments extending from 10 dB above to 10 dB below the estimated threshold. Threshold was defined as the intensity corresponding to a performance level of 0.50, which was usually obtained by linear interpolation. For a particular frequency, testing was considered complete when the thresholds obtained in at least 3 different sessions were within 3 dB of each other and not improving. Once an audiogram was completed each threshold was rechecked to ensure reliability. In view of the finding that all three hedgehogs were relatively insensitive to sounds, even at their best frequencies (from 5.6-16 kHz), additional testing was conducted to determine if hearing thresholds improved over time. Specifically, additional thresholds were determined at 5.6 kHz for hedgehog A, at 8 kHz for hedgehog B, and at 16 kHz for hedgehog C.

For determining minimum audible angle (MAA), matched and paired speakers were placed at five different angles of separation on the perimeter bar, with one pair used for each block of 8 warning trials and associated safe trials. Safe trials consisted of single 100-ms noise bursts emitted every 3.8 s from the right speaker of the pair; approximately 22% of trials were warning trials in which the noise burst was emitted from the left speaker and followed by avoidable shock. The speakers were arranged before each session, such that some angles were well above discrimination threshold and at least one angle was below threshold. Angles of separation between speakers were fixed at 180, 90, 60, 45, 30, 20, 15, 10, and 5 deg. Testing was considered complete when scores at every angle stabilized and were no longer improving with practice. Asymptotic performance was calculated by averaging the three blocks of trials with the highest scores at each angle; these scores were taken from three different sessions. The means were then plotted as the performance curve for each hedgehog. Threshold was defined as the angle at which mean performance equaled 50%, which was determined by interpolation.

Finally, one hedgehog (C) was also tested for its ability to localize pure tone bursts, separated by a fixed angle of 60 deg. Each 2.4 s trial consisted of a single 100-ms tone burst (10 ms rise/decay), presented from either the right or left speaker, in blocks of 8 left (warning) trials. The distribution of safe and warning trials was the same as described above in the noise localization task. All tones were presented at 40 dB above absolute threshold and randomly attenuated by as much as 3.5 dB. Testing was carried out on a single frequency per session for frequencies that sustained good performance. However, if the animal had difficulty or was unable to localize a particular frequency, broadband noise was presented for several trials to verify that it remained sufficiently motivated. Each frequency was tested for at least three sessions for an average of 80 warning trials. The performance measure of interest was asymptotic performance, defined as the mean of the best 50% of the trial blocks at each frequency.

Anatomical Methods

For specimens A and B, following dissection, tympanic membrane and stapes footplate areas were measured by positioning the structures in a plane perpendicular to the axis of the microscope, and then constructing scale diagrams on graph paper using a calibrated grid eyepiece lens. The areas were calculated as for flat surfaces; inflections were ignored. The volume of the right middle ear cavity of each specimen was estimated by injecting water into it through the Eustachian tube, a small hole having been made in the pars flaccida for air release. A 1.0 ml hypodermic syringe marked with .01 ml gradations was used. Although the possibility of air bubbles remaining in the middle ear cavity could not be excluded, repeated measurements obtained in this way in each specimen were reliable.Ossicular masses were obtained to the nearest 10 μg using a Sartorius Research R200D balance. To free each malleus for weighing, its anterior process was broken where it joins to the ectotympanic, so the malleus mass did not include the section of this process fused to the ectotympanic.

The head of hedgehog E, with skin removed, was wrapped in cellophane and scanned using a Nikon XT H 225 micro-CT scanner. The settings used were 130 kV, 130 μA, 1080 projections, 1 sec exposure and 2 frames averaged per projection, and the cubic voxel side-length was 26 μm. CT Agent XT 3.1.9 and CT Pro 3D XT 3.1.9 (Nikon Metrology, 2004–2013) were used in the reconstructions. The left temporal bone was then dissected out and scanned using the same settings, but with cubic voxel side-lengths of 8.9 μm. Tomograms were converted to 8-bit JPEG files using Adobe Photoshop CS 8.0 and imported into Stradview 6.13 (written by Graham Treece & Andrew Gee of the Department of Engineering, University of Cambridge). For the purposes of reconstruction in Stradview, outlines of the structures of the middle ear were determined using automated threshold identification or, where boundaries were less clear, manual identification. Middle ear cavity volume, which included only the air-space, was calculated by Stradview based on the scaled reconstruction.

The middle ears of hedgehog E were then dissected. Tympanic membrane and stapes footplate areas were measured from scaled photomicrographs taken using a GX-CAM digital camera, and the ossicles were weighed using a Cahn C-31 microbalance, to the nearest microgram.

Average values for these anatomical measurements were calculated from one ear each from hedgehogs A, B, and E. Where data were available from both ears, measurements from the right ear were used in calculating the average.

Results

Audiogram

The audiograms of the four hedgehogs (A-D) were determined in octave steps from 1 kHz to 32 kHz, with additional thresholds at 3, 5.6, 12.5, 40, 45, and 50 kHz. As shown in Fig. 2, at the lowest testable frequency of 1 kHz, the average threshold was 83.5 dB SPL. Sensitivity improved as frequency increased, with thresholds of 30 dB or lower between 4 and 16 kHz. At 60 dB SPL, their hearing range extended from 2 kHz to 46 kHz, a range of 4.6 octaves. Their best sensitivity of 21.5 dB SPL was achieved at 8 kHz. The thresholds of the four individuals show good agreement throughout the hearing range, with some variation above 40 kHz as their high-frequency limit was reached.

Sound Localization

Fig. 3 shows azimuthal noise-localization performance around the midline for three hedgehogs. All three were able to perform at 90% or better (corrected detection) at large angles of separation, with performance falling rapidly at angles of separation smaller than 30°. Their 50% performance threshold (minimum audible angle) was interpolated to be 14°. The close agreement among well-trained individuals suggests that this threshold represents a good estimate for this species. Performance fell to chance at smaller angles of 5° and 10°, indicating that no unintended cues were present to distinguish the speakers.

Fig. 4 illustrates the performance of one hedgehog localizing pure tones (at a sound level of 40 dB above its detection threshold) at a relatively large fixed angle of 60° separation—30° to the left and right of the midline. A simple physical model of the hedgehog’s head based on a smooth, 46-mm diameter sphere, suggests that the intensity-difference cue should be available above about 11.6 kHz and the interaural phase-difference cue should be theoretically unambiguous below about 7.7 kHz (e.g., Kuhn, 1977; Christensen-Dalsgaard, 2005). The hedgehog successfully localized pure tones of 16 kHz and higher, thereby demonstrating use of the interaural intensity-difference cue. The hedgehog’s performance at low frequencies (3 and 4 kHz) was at chance, indicating that it could not localize those pure tones using the phase-difference cue (a subset of the binaural time-difference cue).

To further explore localization using a time cue, we tested the animal’s ability to localize a 3-kHz carrier tone, itself unlocalizable, while it was sinusoidally amplitude modulated at rates of 500 Hz and 1 kHz. The modulation provided an envelope on which to base an interaural phase difference analysis if the hedgehogs were capable of such an analysis (cf. Heffner et al., 2015). However, performance remained at chance, demonstrating that this hedgehog is not able to use the interaural phase-difference cue for sound localization—either on a tonal signal or on the envelope of a tone modulated at a rate of .5-1 kHz.

Anatomy of the Ear

The external auditory meatus of Atelerix is relatively short and contains many fine hairs. In both animals A and B, tested behaviorally, and one further individual (E), the external ear canals on both sides were filled with a soft, cream-colored exudate thought to be cerumen (ear-wax). We considered the possibility that this might have compromised their hearing sensitivity. However, we noted that inspection of the ears of animals A, B, C, and D during behavioral testing failed to reveal any abnormalities. Further, previous experience with ear mites in cats (unpublished observations) and cattle (Heffner and Heffner, 1983) showed both species of mites to be associated with inflammation and ulceration of the lining of the ear canals, neither of which were observed in these hedgehogs. We also found that ear mites caused great variation in absolute thresholds both within and between individuals, but that did not occur with the hedgehogs. Finally, these specimens had been immersed in water-based fluid (10% formalin for A and B, water for E to soften dried tissue): cerumen absorbs water, which leads to its expansion. Thus, we believe that it is unlikely that the thresholds of the hedgehogs were affected by abnormal amounts of cerumen.

Proximally, the external auditory meatus expands into a shallow recessus meatus, the dorso-caudal wall of which is formed from the pars flaccida of the tympanic membrane. The robust ectotympanic, which supports the oval pars tensa, is roughly crescent-shaped (Fig. 5). A bony shelf covers the anterior half of the pars tensa from external view, while a rostrolateral projection seems to represent the tip of the anterior process of the malleus, to which the ectotympanic is synostosed. The pars tensa area (10.9 mm², n=3) is around 2.5 times the area of the pars flaccida. The two are continuous; the junction between them spans the gap between the two crura of the ectotympanic. The manubrium of the malleus (Fig. 6) extends roughly two-thirds of the way along the long axis of the pars tensa.

The ectotympanic is overlapped by the tympanic wing of the basisphenoid medially, but it has only a ligamentous attachment to the surrounding basicranial bones, and hence there is no complete bulla. The middle ear cavity (Fig. 5b) is largely contained between the ectotympanic, the tympanic wing of the basisphenoid and the petrosal bone caudally, but there are regions rostrally, ventromedially and dorsally where it lacks bony walls and is instead framed by soft tissue. Simple in structure, the main volume of the cavity is located rostral to the promontory, which forms a very low projection into its caudo-medial wall. The oval window is located just caudal to the promontory, with the round window niche ventromedial to this. The epitympanic recess, which houses the heads of the malleus and incus, is very shallow. From the CT scans of hedgehog E, the heads of the ossicles were separated from the bony roof of the recess only by a very thin layer of soft tissue. The volume of the entire middle ear cavity was measured using water-filling as 40 μl and 30 μl in hedgehogs A and B respectively; in hedgehog E, the volume measured more accurately from the CT reconstruction was 43 μl.

The soft tissue features of the middle ear cavity include the large m. tensor tympani, the body of which lies on the dorsolateral promontory. The long, thin tendon of this muscle takes an oblique course towards its insertion on the malleus. The body of the m. stapedius is largely contained within a bony canal projecting into the middle ear cavity from the caudal direction; it seems to insert directly onto the stapes without any significant intervening tendon. No Paaw’s cartilage was found. The large internal carotid artery (Fig. 5b) enters the middle ear cavity just posterior to the tympanic wing of the basisphenoid: it divides into a promontorial branch, which runs rostrally over the promontory, and a larger stapedial branch, which passes through the intercrural foramen of the stapes before turning rostrally, to run beside the m. tensor tympani. Just before leaving the middle ear cavity, the shallow canal containing the ramus inferior of the stapedial artery becomes covered in bone, but the arteries of the middle ear are not otherwise contained within bony tubes. The facial nerve runs in a deep canal (the facial sulcus) dorsal to the oval window.

Auditory Ossicles

The malleus of Atelerix (Figs. 5, 6) has a small head, caudal to which is the saddle-shaped articulation facet for the incus. Rostrally, the malleus head extends into the large anterior process. This process is relatively narrow proximally, but it expands into a wide, flattened structure which becomes indistinguishably synostosed with the ectotympanic. This articulation is very firm; the distal half of the anterior process could not be separated from the ectotympanic. The mass of the free part of the malleus averaged 2.11 mg (n=2). Below the head and the base of the anterior process is a thin, roughly rectangular transversal lamina. The caudal edge of the lamina is thickened, a projection from its medial side forming the prominent muscular process for the insertion of the m. tensor tympani tendon. The lamina expands into a more substantial mass of bone at the base of the manubrium. The mass of bone extends ventromedially as a projection representing an orbicular apophysis, although this is not very prominent. The triangular, tapering manubrium extends rostromedially, approximately parallel to the anterior process. It curves slightly at the tip where it supports the umbo of the pars tensa. The manubrium is directly attached to the membrane along its entire length, by means of its flattened inserting margin. There is no discrete lateral process at the base of the manubrium. The internal margin of the manubrium is only slightly thickened.

The incus of Atelerix (Fig. 6) is much smaller than the malleus, averaging .68 mg (n=3) in mass. Its body and head are wide and deeply excavated rostrally to form the saddle-shaped articulation that is the counterpart to that of the malleus. The incudal short process is stumpy, and quite firmly anchored by means of ligamentous material to a fossa in the posterior wall of the tympanic cavity. The long process gently curves inwards as it narrows into the pedicle that supports the relatively large, oval lenticular apophysis. The internal side of the long process is slightly excavated by a shallow sulcus, at its deepest near the pedicle.

The stapes (Figs. 6, 7) is very lightly-built, weighing an average of .15 mg (n=3). The slender crura bow outwards between the small, flattened stapes head and the footplate; there is no well-defined neck region to the ossicle. The elliptical footplate has an ill-developed labrum which is bound to the rim of the oval window by ligamentous tissue. Footplate area is .30 mm² (n=3). The posterior crus supports a very small muscular process for the insertion of the m. stapedius, where it joins the head.

The articulation between malleus and incus, and the articulation between the lenticular apophysis of the incus and the stapes, were both relatively weak, separating readily during the dissection process.

Inner ear

A brief description of the inner ear is described here for completeness but is not discussed further. Based on a CT reconstruction of the bony labyrinth of hedgehog E, Atelerix has 1.9 cochlear turns. The endolymphatic duct runs adjacent to the crus commune. The posterior end of the lateral semicircular canal enters the vestibule separately from the posterior semicircular canal with no secondary crus commune. While the mammalian perilymphatic duct typically runs from near the round window into the cranial cavity via a narrow channel through the petrosal bone called the canaliculus cochleae (Ekdale, 2013), in Atelerix there was a short and very wide opening in this region. The volume of the entire bony labyrinth was 9.3 μl, but there was some uncertainty in the boundaries of the canaliculus opening, and a small part of the anterior semicircular canal had been damaged in the dissection process so was not included in this volume measurement.

Discussion

This discussion presents a convergence of two complementary approaches to explaining mammalian hearing. The proximate approach is that species hear the way they do because of the mechanical structure of their ears. The ultimate approach refers to selective pressures that favor particular hearing abilities, and the structures that enable those abilities, that confer an advantage for survival and reproduction.

The middle ear and hearing range

The middle ear of the African pygmy hedgehog shows characteristics generally regarded as ancestral features of therian mammals. These features include a ‘loose’ U-shaped ectotympanic which does not form a complete auditory bulla, a relatively large pars flaccida of the tympanic membrane, and the retention of both middle ear muscles (Henson, 1961; Segall, 1969; Novacek, 1977; Fleischer, 1978). The malleus in such ears has what Fleischer (1978) referred to as ‘ancestral-type’ morphology, including a long anterior process which is tightly connected to the ectotympanic, and a manubrium approximately parallel to that process. Fleischer’s ‘microtype’ malleus, found in small mammals such as mice, bats and shrews, is very similar but for the development of the orbicular apophysis, a projection from near the base of the manubrium. The malleus of African pygmy hedgehogs conforms to this microtype morphology, although its orbicular apophysis (Fig. 6) is not as prominent as in some of the smaller ‘microtype’ species. Other eulipotyphlans, including other hedgehogs, shrews, solenodons and some talpid moles, share similar microtype middle ear features to Atelerix (Wassif, 1948; McDowell, 1958; Henson, 1961; Segall, 1970; Mason, 2006; Wible, 2008; Zaytseva et al., 2015), with variable levels of development of the orbicular apophysis. Although African pygmy hedgehogs are somewhat larger than other species possessing microtype ears, their middle ear measurements fit closely with the regression relationships for microtype species reported by Mason (2013). Hedgehogs like Atelerix can be regarded as relatively large microtype species, with otherwise primitive therian middle ear characteristics.

At low frequencies, sound transmission through the middle ear is affected by acoustic compliance (see Mason, 2016b for a review). The main determinants of compliance likely include the volume of the middle ear cavity and the stiffness of the conducting apparatus, i.e. tympanic membrane and ossicular chain. Low-frequency sound transmission could then be improved by a larger cavity volume and a less-stiff tympanic-ossicular chain, but their relative contributions can differ. Compared to non-microtype mammals of similar body mass, microtype species have smaller middle ear cavities, a difference especially evident in smaller microtype species (Mason, 2016a). Microtype species also have a particularly stiff articulation between an expanded anterior process of the malleus and the tympanic bone: in Atelerix we found the two bones to be fused, i.e., synostosed. It is unclear whether the low tympanic cavity volume or the high tympanic-ossicular stiffness is more limiting to low-frequency hearing in microtype species.

Low-frequency hearing

The hearing of the African pygmy hedgehog differs in both absolute sensitivity and frequency range from that of Hemiechinus auratus, the only other hedgehog the hearing of which has been behaviorally determined. (Ravizza et al., 1969). Fig. 8 compares these two species and shows that the long-eared hedgehog hears 1.87 octaves further into the low frequencies and is also more sensitive throughout its hearing range. Nevertheless, both species of hedgehogs fall into the group of mammals that do not hear frequencies below about 400 Hz (at a level of 60 dB or less), as illustrated in Fig. 9 (cf. Heffner et al., 2020). This bimodal distribution of low-frequency hearing (unlike the approximately normal distribution of high-frequency hearing, Heffner et al., 2001b) suggests that it would be instructive to consider environmental factors that might exert selective pressure on low-frequency hearing, as well as anatomical mechanisms.

The middle ear morphologies of most terrestrial mammals fall on a spectrum between two extreme types, the small and stiffly-articulated microtype referred to earlier, and a more compliant ear referred to as ‘freely mobile’ (Fleischer, 1978; Mason, 2013). Being small and stiff, microtype ears (and the ancestral ears, which are similar) should be good transmitters of high frequencies from tympanic membrane to inner ear, while transitional ears and freely-mobile ears should be better than microtype ears at transmitting low frequencies (Mason, 2016b). Thus, it is of interest to consider whether grouping the ears in this way is congruent with the bimodal distribution of mammalian low-frequency hearing shown in Fig. 9 and Table 1 (Heffner et al., 2001b).

Fig. 9 illustrates the bimodal distribution of low-frequency hearing limits of terrestrial mammals, excluding the aquatic/amphibious species with their highly specialized ears. The upper mode consists of mammals, including both species of hedgehogs, that do not hear low frequencies (below approximately 400 Hz at 60 dB SPL). It includes 24 terrestrial species, 22 of which have been classified as having a microtype ear, plus two marsupials with ancestral middle ears, which are very similar to the microtype except for the lack of the orbicular apophysis. None of these 24 terrestrial species have freely mobile ears. Thus, the microtype/ancestral morphology seems to be found in species that do not hear low frequencies.

On the other hand, there are 43 terrestrial species known to hear below 400 Hz (the lower mode in Fig. 9). Of these 43, all have been classified as having more flexible middle ears (often labeled either freely mobile or transitional)—and despite the good high-frequency hearing of most of them, none has a microtype ear. We do not suggest that non-microtype ears preclude good high-frequency hearing, only that, because of their higher compliance, they are likely to be better transmitters of low-frequency sound. This is illustrated by relatively large, non-microtype species with good high-frequency hearing, such as pigs (42 Hz to 40.7 kHz, Heffner and Heffner, 1990) and cats (55 Hz to 79 kHz, Heffner and Heffner, 1985). Perhaps more surprisingly, this group also includes many small species that not only hear below 50 Hz, but also frequencies as high as 60 kHz (gerbil and least weasel, both weighing about 80 g). It would appear, then, that the broad categorization of an ear as freely mobile/transitional as opposed to microtype/ancestral allows us to predict whether the animal in question can or cannot hear sound below 400 Hz. However, high-frequency hearing limits are normally distributed and no clear division is found in the upper frequency limits of hearing that can be linked to ear type.

Both the hedgehogs, A. albiventris and H. auritus, fall within the group of mammals with limited low-frequency hearing, and both possess microtype middle ears. One key difference between the two species relates to the volume of the middle ear cavity. In A. albiventris, cavity volume was measured here at around 40 μl, while the volume for two specimens of H. auritus was 120 and 140 μl (Packer, 1987). Because acoustic compliance is directly proportional to cavity volume, acoustic compliance will be three times greater in H. auritus. This is consistent with the superior low-frequency hearing of H. auritus compared to A. albiventris(Fig. 8), although other differences in their ears, including tympanic-ossicular stiffness, are also potential contributors. In speculating on an evolutionary explanation for their difference in hearing and anatomical configuration, we would look to differences in their habitat or lifestyle. It has long been known that many small mammals living in arid habitats have enlarged auditory bullae, which are associated with improved low-frequency hearing in an environment in where that may be ecologically advantageous (see Mason, 2016a for a review). Whether the differences between the anatomy and audiograms of Hemiechinus and Atelerix relate in a similar way to differences in their natural habitats remains unexplored.

High-frequency hearing

The high-frequency hearing limit of A. albiventrisisconsistent with selective pressure on small species to hear high frequencies in order to localize sound using interaural intensity differences (e.g., Heffner and Heffner, 2016). High-frequency hearing is strongly correlated with functional interaural distance, measured as the time required for a sound to travel from one auditory meatus to the other, whether in air or in water (r = – .76, p < .0001, n = 74). The correlation is based on the apparent selective pressure on species with smaller functional interaural distances to hear frequencies high enough to be shadowed by their head and pinnae and produces a binaural intensity/spectral-difference cue that can be used to localize sound sources. With a functional interaural distance of 135 μs, the 46-kHz high-frequency hearing limit of A. albiventrisdoes not deviate significantly from the mammalian regression line (p > .05). Hedgehogs, despite their unusual anti-predator behavior of rolling into a ball which seemingly relies more on detecting predators than requiring a directional escape response, have high-frequency hearing consistent with this overall mammalian pattern.

Sound-Localization

Fig. 10 shows that the localization thresholds of both hedgehogs fall near the midrange of the distribution of 41 mammals (mean 13.1°, median 14.0°). At 14°, the African pygmy hedgehog is slightly better than the only other hedgehog with known localization acuity, Paraechinus hypomelas (Brandt’s hedgehog, previously known asHemiechinus hypomelas)with its threshold of 19° (Chambers, 1971). As such their localization acuity is not unusual among mammals as a whole.

Despite fairly typical acuity for localizing broadband noise sources that provide both time and intensity binaural cues to locus, the African pygmy hedgehog,like Brandt’s hedgehog, does not use both of these cues for localization (cf. Masterton et al., 1975). With a functional interaural delay of approximately 135 μs, the interaural phase-difference cue is expected to become physically ambiguous for African pygmy hedgehogsabove about 7.7 kHz, forcing a reliance on an interaural intensity difference for pure tones above that frequency—frequencies that were localized easily. Similarly, it is estimated that animals with this functional interaural distance would produce little or no intensity difference between the two ears at frequencies below about 11.6 kHz (based on the simple spherical head model), thereby forcing reliance on any available interaural phase differences to localize pure tones at lower frequencies. However, the ability of the nervous system to phase-lock serves to limit the use of the phase cue at frequencies higher than about 5 kHz even when that cue is physically present (cf. Heffner and Heffner, 1987; Heffner et al., 1994, 2001c). Unlike the good performance at high frequencies where the interaural intensity difference was available, localization of lower frequencies deteriorated and fell to chance as pure tones of 4 kHz and below were tested, indicating that this species cannot localize sound sources when forced to rely on the interaural phase-difference cue alone. This result was further supported by the inability to localize a clearly audible 3-kHz tone when it was amplitude-modulated. Such an amplitude-modulated envelope provides a basis for a time comparison between the two ears that enables even small species possessing the ability to use time cues to localize frequencies that are not localizable as pure carrier tones (such as the common vampire bat, Desmodus rotundus, Heffner et al., 2015). However, the envelope did not improve localization performance by African pygmy hedgehogs. Thus, like Brandt’s hedgehog, the African pygmy hedgehog showed no evidence of being able to use interaural phase differences in either the carrier wave, or envelope of a sound.

The inability to use the phase cue at low frequencies suggests that the African pygmy hedgehog also should not be able to localize tones of 5.6 and 8 kHz because the spherical model suggests the only cue would have been a phase difference. There are two reasons for inferring that those frequencies were not localized using the phase cue, but instead relied on an intensity difference. First, even though a phase difference might be physically available at frequencies as high as 7.7 kHz to a small species with a head the size of Atelerix, mammalian auditory systems are not known to phase lock at frequencies above about 5 kHz, hence they are not able to use the cue even though it is physically present. Indeed, the Egyptian fruit bat (Rousettus aegyptiacus) and the Jamaican fruit bat (Artibeus jamaicensis), both echolocators, are the only species known to localize pure tones at such high frequencies—5.6 kHz and 6.3 kHz, respectively, and both of those species use the phase cue at lower frequencies as well (Heffner et al., 1999, 2001c). We know of no species that uses the phase cue at relatively high frequencies, but not at lower frequencies where it is most effective.Instead, the observation that localization was, in fact, possible at5.6 and 8 kHz, islikely owing to an enhancement of interaural intensity differences by the animal’s relatively large pinnae and the non-spherical shape of its head. A simple spherical model cannot take into account the directional properties of the pinnae and head, and provides only an estimate of the lowest frequency at which the head shadow should become effective. More definitive tests would require the placement of headphones on trained hedgehogs.

The inability of both species of hedgehogsto use the binaural phase cue is noteworthy. It demonstrates that even though a sound can be easily audible, it may not be localizable. Perhaps more importantly, it shows that at least average localization acuity for more natural broadband sounds (that produce both time and intensity cues) can be achieved using only one of the binaural cues. Thus, one more species of hedgehog (from a different genus) now joins several species of rodents and bats known not to use the binaural phase cue for sound localization (domestic Norway rats, Rattus norvegicus, Wesolek et al., 2010; domestic house mouse, Mus musculus, Heffner et al., 2001a; spiny mouse, Acomys cahirinus, Mooney, 1992; straw colored fruit bat, Eidolon helvum, and dog-faced fruit bat, Cynopterus brachyotis, Heffner et al., 2010a; greater spear-nosed bat, Phillostomus hastatus, and short-tailed fruit bat, Carollia perspicillata, Heffner et al., 2010b; big brown bat, Eptesicus fuscus, Koay et al., 1998). It might be thought that all of these species that do not use the binaural time cues simply have heads too small to generate useful time delays, but this is contradicted by at least five even-smaller species that do use time cues (Fig. 10: Egyptian fruit bat, Rousettus aegyptiacus (Heffner et al., 1999); kangaroo rat, Dipodomys merriami (Heffner and Masterton, 1980); gerbil, Meriones unguiculatus (Heffner and Heffner, 1988); least weasel, Mustela nivalis (Heffner and Heffner, 1987); common vampire bat, Desmodus rotundus (Heffner et al., 2015); Jamaican fruit bat, Artibeus jamaicensis(Heffner et al., 2001c). It seems the mammalian nervous system is capable of analyzing small interaural time differences for localization, but it does not do so in every species.

Finally, we have noted (Heffner et al., 2010b) that all of the species that do not use the binaural time cue fall into the group of mammals that do not hear low frequencies (Fig. 9, Table 1). As such, we might be tempted to conclude that they simply do not hear low enough to use time cues. Again, this possibility is contradicted by species such as Egyptian fruit bats with a low-frequency hearing limit of 2.25 kHz (Koay et al., 1998), and Jamaican fruit bats with a low-frequency hearing limit of 2.8 kHz (Heffner et al., 2003). These species have similar low-frequency hearing to that of African pygmy hedgehogs, and even poorer low-frequency hearing than Brandt’s hedgehog,yet they retain the ability to use the binaural phase-difference cue even though the frequency range over which it can be used is narrow due to their limited low-frequency hearing.

In summary, the overall localization acuity of both species of hedgehogs is unremarkable compared to other mammals. However, their inability to use the time cue for localization is somewhat unusual. Foregoing the use of time cues for localization, first noted in Brandt’s hedgehog (Paraechinus hypomelas), is not restricted to hedgehogs since it is also found among several rodents and bats. Yet, sound localization that relies on only one of the binaural cues to locus seems surprising when so many species use both cues. This remains unexplained—we still do not have an indication of what selective pressures or neural mechanisms might account for this condition or even how widespread it is among mammals. Indeed, we might ask why so many species devote resources to the maintenance of the dual neural apparatus to process both binaural cues when either one alone seems sufficient for good localization.

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Tables

Table 1. Terrestrial mammals for which high and low frequency limits have been behaviorally established. Species are listed in order of lowest frequency audible at 60 dB SPL. Groups of species regarded as having microtype ears are listed by Mason (2013). Opossums have middle ears best classified as ancestral-type (Segall 1970; Sánchez-Villagra et al., 2002; Schmelzle et al., 2005; Wible and Spaulding, 2012; Mason, 2013). These two groups are considered together and referred to here as MA ears (Microtype/Ancestral). All other species in this table are regarded as having freely mobile, Ctenohystrica type or transitional middle ears (see e.g. Fleischer, 1973, 1978; Mason, 2013), here referred to collectively as FT ears.

Species	Functional Interaural Distance in µsec	Highest Frequency Audible at 60dB, in kHz	Lowest Frequency Audible at 60dB, in kHz	Middle Ear Type
Elephant Elephas maximus	3350	10.5	0.017	FT
Cattle Bos taurus	1281	35	0.023	FT
Japanese macaque Macaca fuscata	464	34.5	0.0275	FT
Black-tailed prairie dog Cynomys ludovicianus	134	26	0.028	FT
Human	875	17.6	0.031	FT
Gerbil Meriones unguiculatus	87	58	0.036	FT
Ferret Mustela putorius	180	42	0.036	FT
Chipmunk Tamias striatus	108	52	0.039	FT
Alpaca Lama pacos	544	32.8	0.039	FT
Woodchuck Marmota monax	290	27.5	0.04	FT
Kangaroo rat Dipodomys merriami	90	52	0.042	FT
Pig Sus scrofa	498	40.7	0.042	FT
White-tailed prairie dog Cynomys leucurus	120	26	0.044	FT
Baboon Papio cynocephalus	580	40	0.045	FT
Rhesus macaque Macaca mulatta	424	41	0.045	FT
Blue monkey Cercopithecus mitis	400	48	0.046	FT
Guinea pig Cavia porcellus	160	49	0.047	FT
Chinchilla Chinchilla laniger	225	32.5	0.05	FT
Least weasel Mustela nivalis	76	60	0.05	FT
Red Fox Vulpes vulpes	?	48	0.05	FT
Grey cheeked mangabey Lophocebus albigena			0.051	FT
Blind mole rat Spalax ehrenbergi	87	5.9	0.052	FT
Cat Felis domesticus	258	79	0.055	FT
Horse Equus caballus	684	33.5	0.055	FT
DeBrazza’s monkey Cercopethecus neglectus	420	42	0.063	FT
Naked mole rat Heterocephalus glaber	61	11.5	0.065	FT
Ring tailed lemur Lemur catta	280	58	0.067	FT
Dog Canis familiaris	435	44	0.067	FT
Vervet Chlorocebus pygerythrus (aethiops)	400	45	0.069	FT
Reindeer Rangifer tarandus	548	37.7	0.07	FT
Brown lemur Lemur fulvus	270	43	0.072	FT
Goat Capra hircus	680	37	0.078	FT
Slow loris Nycticebus coucang	218	44	0.083	FT
Bushbaby Galago senegalensis	212	65	0.092	FT
Hamster Mesocricetus auritus	114	46.5	0.096	FT
Rabbit Oryctolagus cuniculus	250	49	0.096	FT
Squirrel monkey Saimiri sciureus	302	43	0.1	FT
Tree shrew Tupaia glis	136	61	0.1	FT
Fox squirrel Sciureus niger	155	49	0.113	FT
Whitetailed Deer Odocoileus virginianus	800	54	0.115	FT
Potto Perodicticus potto	218	42	0.125	FT
Sheep Ovis aries	670		0.125	FT
Gopher Geomys bursarius	111	8.7	0.27	FT
Rabbit Sylvilagus floridanus	122	56	0.3	FT
Hedgehog Hemiechinus auritus	167	59	0.52	MA
Norway rat hooded Rattus norvegicus	150	68	0.54	MA
Common vampire bat Desmodus rotundus	61	112.86	0.71	MA
Wood rat Neotoma floridana	116	56	0.94	MA
Cotton rat Sigmodon hispidus	65	72	1	MA
Opossum Didelphis virginiana	273	68	1.03	MA
Straw-colored fruit bat Eidolon helvum	145	41.3	1.38	MA
Darwin's leaf-eared mouse Phyllotis darwini	64	73.5	1.55	MA
Ground gleaning bat Megaderma lyra			1.7	MA
Greater spear-nosed bat Phyllostomus hastatus	108	105	1.77	MA
Grasshopper mouse Onychomys leucogaster	61	68	1.8	MA
Hedgehog Atelerix albiventris	135	46	1.9	MA
Egyptian fruit bat Rousettus aegyptiacus	134	64	2.25	MA
Wild house mouse Mus musculus	40	92	2.3	MA
Spiny mouse Acomys cahirinus	64	71	2.3	MA
Lesser short-nosed fruit bat Cynopterus brachyotis	86	70	2.63	MA
Jamaican fruit bat Artebeus jamaicensis	89	130	2.8	MA
Short-nosed opossum Monodelphis domestica	114	76	3.15	MA
Mouse opossum Marmosa elegans	60	78	3.6	MA
Big brown bat Eptesicus fuscus	50	105	3.65	MA
Greater horseshoe bat Rhinolophus ferrumequinum	55	103	4.3	MA
Short-tailed bat Carollia perspicillata	47	150	5.2	MA
Greater bulldog bat Noctilio leporinus	87	111	7.5	MA
Little brown bat Myotis lucifugus	41	115	10.3	MA

Hearing in African Pygmy Hedgehogs (Atelerix albiventris): Audiogram, Sound Localization, and Ear Anatomy

Abstract

Introduction

Methods

Results

Discussion

Declarations

References

Tables