We measured the auditory sensitivity of the barn owl ( Tyto alba ), using a behavioural Go/NoGo paradigm in two different age groups, one younger than 2 years ( n = 4) and another more than 13 years of age ( n = 3). In addition, we obtained thresholds from one individual aged 23 years, three times during its lifetime. For computing audiograms, we presented test frequencies of between 0.5 and 12 kHz, covering the hearing range of the barn owl. Average thresholds in quiet were below 0 dB sound pressure level (SPL) for frequencies between 1 and 10 kHz. The lowest mean threshold was –12.6 dB SPL at 8 kHz. Thresholds were the highest at 12 kHz, with a mean of 31.7 dB SPL. Test frequency had a significant effect on auditory threshold but age group had no significant effect. There was no significant interaction between age group and test frequency. Repeated threshold estimates over 21 years from a single individual showed only a slight increase in thresholds. We discuss the auditory sensitivity of barn owls with respect to other species and suggest that birds, which generally show a remarkable capacity for regeneration of hair cells in the basilar papilla, are naturally protected from presbycusis.

1. Background

Growing old as a human is commonly accompanied by a progressive deterioration of hearing abilities. Typically, this deficit is already evident at the most peripheral stages of the auditory system—middle and inner ear (cochlea)—and is summarized under the term presbycusis or age-related hearing loss. Of course, not only humans suffer from presbycusis, the sensory deficit generally applies to all ageing mammals and is most prominent at high frequencies [1]. Presbycusis has been shown, for example, in Mongolian gerbils (Meriones unguiculatus) [2,3], in mice (Mus musculus) [4] and in chinchillas (Chinchilla laniger) [5]. Presbycusis in mammals is commonly associated with a loss of hair cells at the sensory epithelium, i.e. the organ of Corti of the cochlea. While mammals are able to at least partly regenerate sensory hair cells in the vestibular system, they cannot replace hair cells in the cochlea [6]. By contrast, some vertebrate groups other than mammals have conserved the ability to regrow hair cells in the inner ear and are thus much less susceptible to permanent damage [6]. Birds, in particular, have been studied extensively for mechanisms of hair-cell regeneration after various insults to their basilar papilla, the avian homologue of the mammalian organ of corti [6–9]. Importantly, several studies [10–12] reported a very low level of ongoing hair-cell proliferation even in undamaged basilar papillae of different bird species, suggesting that the regenerative mechanisms remain active throughout life. Studies involving acoustic trauma or treatment with ototoxic drugs have revealed a remarkable capacity for regeneration and concomitant recovery of auditory function in birds [8,13–16]. There are also limits, however, and hair-cell regeneration remains incomplete if the damage extends to supporting cells, which are the source of new hair cells [13,14]. Some structural abnormalities may persist in regenerated regions of the basilar papilla, such as an incomplete tectorial membrane or an abnormal innervation pattern [13]. Depending on the original extent of damage, functional recovery of auditory sensitivity tended to be less complete at higher frequencies [14,15]. It is therefore an interesting question whether the regenerative capacity is sufficient to prevent presbycusis during the entire lifespan of a bird. Langemann et al. [17] conducted the first long-term study to investigate the change in auditory performance in a bird, the European starling (Sturnus vulgaris), with behavioural methods. They measured auditory sensitivity at different times over the lifespan of European starlings and found no substantial age-related hearing loss. So far, to our knowledge, this is still the only study with behavioural data on age-related hearing loss in birds. Here, we characterize the auditory sensitivity of the barn owl (Tyto alba) at different times during its life. The barn owl is a predatory bird with remarkably sensitive hearing that also outperforms other vertebrates in spatial hearing (reviewed in [18]).

The barn owl is a famous model in auditory research. It relies on its sense of hearing for hunting prey, similar to some other birds like the marsh hawk (Circus cyaneus) or the tawny owl (Strix aluco) [19–21]. The typical lifespan of a barn owl is rather short for a bird of its size, and most barn owls in the wild live between about 1 and 4 years [22–26]. Owing to a nocturnal lifestyle that heavily relies on auditory cues for hunting, the barn owl has been extensively studied with respect to sound localization [20,27]. A host of anatomical and physiological specializations has been found to contribute to the barn owl's superb localization performance, starting with the facial ruff and asymmetrical ear openings that generate enhanced physical cues [28,29]. The sensitive hearing range of the barn owl extends from about 200 Hz up to 12 kHz, which is extended on the high-frequency side relative to that of most other bird species [28]. This has its basis in a specialized cochlea with a basilar papilla that is by far the longest among birds [30,31]. Its low-frequency apical part appears morphologically similar to the basilar papilla of other birds, but the high-frequency basal region shows several unusual features, suggesting a specialization for high-frequency processing [30,32]. The tonotopic frequency representation along a typical bird basilar papilla is described by an exponential function [33,34]. By contrast, barn owls show a tonotopic distribution with an extreme over-representation between 4 and 10 kHz: more than half of the length of the basilar papilla represents this narrow frequency range [31]. Such an extreme specialization is found in no other bird species. However, it resembles the ‘auditory fovea’ that is known from constant frequency bats like the horseshoe bat (Rhinolophus rouxi) and the moustached bat (Pteronotus parnelii) [35,36]. Thus, the question arises whether, compared to the relatively unspecialized starling, the barn owl's ability to regenerate hair cells is not lost as a result of these specializations.

The aim of this study was to determine the auditory sensitivity of the barn owl into old age. For computing audiograms, we measured auditory thresholds at different test frequencies covering the hearing range of the barn owl. We had two different groups of barn owls, one group younger than 2 years and another group of owls more than 13 years old. In addition, we obtained auditory thresholds from one individual barn owl three times during its 23 years of life. We discuss differences between the two different age groups and raise the question whether birds that generally show a remarkable capacity for repairing damage to the basilar papilla might be naturally protected from presbycusis. Since age-related hearing loss in mammals is most obvious at high frequencies, the high-frequency over-representation of the barn owl might be the ideal case to test for presbycusis in birds.

2. Material and methods

(a) Subjects

Our subjects were seven barn owls (Tyto alba), three of which hatched in 1993 (Weiss, Grün, Rot) and two in 1997 (Lisa, Bart) at the Technical University of Munich. Two further individuals hatched in 2015 at University of Oldenburg (Ugle, Sova). The birds from each group were siblings and they were hand reared from the age of about 12 days. The barn owls were divided into two groups: Four individuals were assigned to the group of ‘young barn owls’ (Ugle, Sova, Grün, Rot) and the remaining three were assigned to the group of ‘old barn owls’ (Bart, Lisa, Weiss). If we had thresholds from the same individual at ‘young’ and ‘old’ age, we had assigned them to only one age group to obtain independent data. The ‘young’ owls were less than 2 years old at the start of the measurement, whereas the ‘old’ owls were 13 years and 17 years of age (two individuals and one individual, respectively). The barn owls wore jesses and were trained to come onto the experimenter's fist on demand, e.g. at the start or the end of an experimental session. The barn owls were housed individually in indoor aviaries. Food rewards during the experiment and supplementary food consisted of small pieces of one-day chicks (Gallus gallus). The owls' weight was monitored daily and the motivation of the animals was controlled by maintaining a body weight 10–15% below their free-feeding weight. The care and treatment of the birds were approved by the Regierung von Oberbayern, Bavaria, Germany, and by the Landesamt für Verbraucherschutz und Lebensmittelsicherheit, Lower Saxony, Germany.

(b) Test signals

To measure the auditory threshold curve, we tested frequencies of 0.5, 1, 2, 4, 6.3, 8, 10 and 12 kHz. All of these signals were pure tones with a total duration of 300 ms (10 ms Hanning ramps). The first thresholds obtained in 1994 [37] were determined with a longer duration of 800 ms (50 ms linear rise and fall time). Assessing temporal summation in another bird species, Klump & Maier [38] found that temporal summation in the European starling was most effective for signals shorter than 200 ms [38]. We therefore concluded that comparing barn owl auditory thresholds using different, longer durations was valid.

(c) Experimental set-up

Experiments were carried out in two different sound-attenuating, echo-reduced chambers: in 1994 in a custom-built chamber of 1.8 × 1.7 × 2.0 m3 [37], later in an IAC (Industrial Acoustics) chamber type 1203-A of 2.2 × 2.1 × 2.0 m3 (inside dimensions). The chambers were lined with sound-absorbing foam (Illbruck GmbH; cut-off frequency 500 Hz, α > 0.99; total attenuation: 48 dB at 500 Hz, greater than 57 dB for frequencies greater than or equal to 1 kHz) and illuminated by a 20 W halogen light. The owls worked either within an experimental cage (1.2 × 1.0 × 1.0 m3) or were allowed to freely roam the chamber without being confined by a cage. In either case, there were two perches, a waiting perch and a target perch, mounted between the mesh walls of the cage or on a pedestal. A single loudspeaker (in 1994: KEF C35; 2010 and 2016: Vifa XT25TG30-04) was located at 0° in azimuth, opposite the owl's waiting perch. Close to the target perch (but outside the main sound transmission path) was a custom-built automatic feeder delivering food rewards. To monitor the owl's position and behaviour, the perches were equipped with infrared light barriers and the entire experiment was video-monitored.

In 1994, all behavioural protocols including the delivery of food rewards were computer controlled. Pure tone signals were produced by an 8-bit digital-to-analogue converter and amplified using a Harmon-Kardon HK6500 amplifier [37]. In the later experiments, a Linux-operated computer controlled the experiments via an enhanced real-time processor (RP2, Tucker Davis Technologies). The signals were generated by an external soundcard (Hammerfall DSP Multiface II, RME) and passed through a Rotel RMB-1048 amplifier to drive the loudspeaker. The sound field of the acoustic chamber was calibrated before the start of the experiments with the microphone (Brüel & Kjær 4188 microphone and 2238 Mediator sound level meter) placed at a range of positions where the barn owl's head would be during experimental test sessions.

(d) Procedure of operant testing

Auditory thresholds in quiet were estimated using a Go/NoGo paradigm. The owls were trained to sit and stay on the waiting perch with their head oriented towards the loudspeaker. During one experimental session, an owl had to complete a series of test trials. As soon as the light barrier of the waiting perch was interrupted by the perching owl, a trial was started and a random time interval between 1 and 30 s initiated after which a test signal was presented. If the owl responded by flying to the target perch within 5 s after the onset of the test signal, this response was scored as a ‘hit’ and the animal was rewarded. The response period in 1994 was set to 10 s; however, Dyson et al. [37] observed that 99% of all the responses occurred within 5 s. If the owl did not respond, then that test trial was scored as a ‘miss’. To assess the rate of spontaneous responses, we introduced ‘catch trials’ where no test signal was presented (20–30% of all trials). A response of the owl to a catch trial was scored as a ‘false alarm’, and no response was scored as a ‘correct rejection’.

(e) Estimating auditory thresholds

For each individual owl, the test frequency was kept constant for successive experimental sessions until a threshold for this frequency was obtained; thereafter the test frequency was changed. To minimize training effects, the sequence of test frequencies was randomized for each individual. Depending on the training level of the owl (young, inexperienced; old, very experienced) each test frequency required between about one and two weeks until the final threshold was reached. Thresholds for each test frequency were obtained by the method of constant stimuli [39]. A block of eight trials, consisting of two catch trials and a set of six test trials differing in sound-pressure level by a step-size of 3 dB was repeated several times during a session, with a randomized sequence of trials in each block (in 1994 blocks consisted of three catch trials and seven test trials [37]). In all measurements, experimental sessions were excluded from the analysis if the false alarm rate exceeded 20% or if the two signals with the highest sound-pressure levels (SPLs) were reported with a probability below 80%. For a final threshold estimate, we collected at least four valid experimental sessions to ensure that each SPL was presented 20 times (in 1994 at least 15 times). The final threshold was then computed by linear interpolation of the psychometric function as the SPL for which the value of the signal-detection measure d' was 1.8.

(f) Data analysis

We performed a two-way repeated measures analysis of variance (ANOVA) to test for the within-subject effects of frequency (0.5, 1.0, 2.0, 4.0, 6.3, 8.0, 10.0, 12.0 kHz) and the between-subject effect of age (young/old) on the owls' auditory thresholds (in dB SPL). Tukey tests were used for post hoc comparisons. For main effects and interactions, we computed partial Eta squared (η2) as a measure of effect size. Partial η2 measures the degree of association between an effect and the dependent variable and can be interpreted as the proportion of variance in the dependent variable that is attributable to each effect (partial η2 varies between 0 and 1, and is non-additive). The influence of a variable is thus not judged by the magnitude of the associated p-value. In addition, partial η2 is a reliable indicator of relevant effects also in cases when sample size is too small to detect a significant difference at the conventional significance level of 0.05. Statistical analyses were performed using SPSS v. 23.0 (IBM SPSS Statistics) or SigmaStat v. 4.0 (Systat Software, Inc.).

3. Results

(a) Comparing young and old barn owls

In a behavioural paradigm, we estimated the auditory sensitivity of barn owls from two different age groups. Test frequencies for obtaining individual audiograms were between 0.5 and 12 kHz. Barn owls are far more sensitive than most other bird species, their thresholds in quiet being below 0 dB SPL for a wide range of frequencies. The mean thresholds in quiet are shown in figure 1, and individual thresholds are listed in tables 1 and 2. The lowest thresholds were found between 2 and 8 kHz in both age groups (figure 1). At test frequencies of 0.5, 1.0 and 6.3 kHz, the thresholds of the old owls were slightly lower (better) than those of the young owls (mean differences between 0.1 and 3.1 dB). At the remaining test frequencies, the thresholds of the young owls were lower than those of the old owls (mean differences between 0.9 and 9.6 dB). These differences were not significant, however (see statistics below). Young owls had average thresholds of −6.9, −10.4, −6.5 and −15.5 dB SPL at 2, 4, 6.3 and 8 kHz, respectively. The mean thresholds of old owls were very similar: −5.9, −7.8, −6.6 and −8.6 dB SPL at 2, 4, 6.3 and 8 kHz, respectively. In both age groups, 8 kHz was the test frequency with the lowest mean threshold (figure 1; tables 1 and 2). The highest thresholds were those at the extremes of the audiogram, about 5 dB at 0.5 kHz and about 32 dB at 12 kHz, reflecting the decrease in sensitivity at both ends of the basilar papilla [40]. Individual thresholds were most variable at 6.3 kHz (tables 1 and 2), however, without any relation to age. Two young individuals as well as one of the old individuals showed relatively high thresholds, whereas the remaining two young and two old individuals showed rather low thresholds. The most sensitive frequency of the individual audiogram was at either 6.3 or 8 kHz (tables 1 and 2). We probed for significant differences between the two age groups by means of a repeated measure ANOVA. Test frequency had a significant effect on auditory thresholds (F = 76.700, p < 0.001, η2 = 0.939). This main effect explained most of the variation in thresholds, as indicated by the effect size. By contrast, age group was not a significant predictor of auditory thresholds (F = 1.407, p = 0.289, η2 = 0.220). There was no significant interaction between frequency and age group (F = 1.729, p = 0.134, η2 = 0.257). We used multiple-comparisons to identify test frequencies that were significantly different from each other. The test frequency of 12 kHz was significantly different to any of the other test frequencies (Tukey tests, q-values between 27.0 and 16.9, all p < 0.001). Similarly, 0.5 kHz was significantly different to all other test frequencies (q-values between 10.1 and 4.6, p ≤ 0.001 with one exception: p = 0.047 for 0.5 versus 1 kHz). We also found a significant difference between 1 and 8 kHz (q = 5.5, p = 0.01). None of the remaining pairwise-comparisons were significant. Figure 1. Thresholds in quiet as a function of frequency in barn owls. Open symbols represent the mean values and s.d. of our young barn owls (n = 4) and closed black symbols represent mean values and s.d. of the old barn owls (n = 3). The green triangles represent data from Konishi 1973 (n = 1). To improve visibility of the error bars, the symbols for young and old owls were slightly shifted off the actual test frequencies (tables 1 and 2). (Online version in colour.)

Table 1.Thresholds in quiet in dB SPL, and mean values of four young barn owls (Sova, Ugle, Grün and Rot) as a function of signal frequency (kHz). (The age of each animal during measurement is shown below the name.) Collapse frequency (kHz) Ugle 14–18 months Sova 16–19 months Grün 19–23 months Rot 19–25 months mean s.d. 0.5 3.8 5.7 3.8 10.5 5.9 3.2 1.0 −2.8 1.7 −3.5 −7.0 −2.9 3.6 2.0 −6.9 −4.7 −9.8 −6.0 −6.9 2.2 4.0 −10.2 −5.3 −13.4 −12.6 −10.4 3.6 6.3 −20.2 3.8 −15.7 6.2 −6.5 13.4 8.0 −17.2 −16.3 −13.1 −15.5 −15.5 1.8 10.0 −18.0 −13.8 −8.0 −14.1 −13.5 4.1 12.0 25.5 32.8 30.3 28.0 29.1 3.1

Table 2.Thresholds in quiet in dB SPL, and mean values and s.d. of three old barn owls aged more than 13 years (Lisa, Bart and Weiss) as a function of signal frequency (kHz). (The age of each animal during measurement is shown together with the name.) Collapse frequency (kHz) Bart 13 years Lisa 13 years Weiss 17 years mean s.d. 0.5 2.8 −0.3 6.0 2.8 3.2 1.0 −5.0 −2.8 −2.2 −3.3 1.5 2.0 −6.3 −7.6 −3.9 −5.9 1.9 4.0 −8.9 −10.1 −4.4 −7.8 3.0 6.3 −8.0 −12.1 0.3 −6.6 6.3 8.0 −9.3 −11.0 −5.6 −8.6 2.8 10.0 −3.6 −9.0 0.8 −3.9 4.9 12.0 31.5 31.6 42.1 35.1 6.1

(b) Tracking Lifetime thresholds

From one of the individuals (Weiss) we obtained audiograms several times during its lifetime. Thresholds were measured for the first time at the age of 22 months (started at 18 months, completed at 22 months of age), i.e. when the auditory sensitivity of the barn owl is fully developed [41]. Additional audiograms were obtained much later, at the age of 17 and 23 years, as shown in figure 2. Threshold changes were larger between the first and the second threshold estimate than between the second and the third estimate. Between about 2 and 17 years of age, threshold at test frequencies of 2, 4, 6.3, 10 and 12 kHz increased between 10.5 and 14.5 dB, while thresholds at 0.5, 1 and 8 kHz changed much less (−1.0, +7.2, +6.9 dB, respectively). Between 17 and 23 years of age, thresholds were within a few decibels (between about −4 and +4 dB), with the exception at 10 kHz, where thresholds increased by about 11 dB. These repeated threshold estimates from a single individual show that thresholds changed, but did not necessarily deteriorate, with age. Figure 2. Variation of thresholds in quiet of one barn owl (Weiss), measured between 1994 and 2016. Frequency is the parameter. (Online version in colour.)

4. Discussion

(a) Auditory sensitivity in young and old barn owls

Overall, the young owls were more sensitive than the old owls (on average 2.8 dB), the threshold difference and the direction of the difference were frequency dependent (figure 1). Statistical testing, however, found no significant differences between the two age groups. The variability in thresholds between individuals was largest at 6.3 kHz, although the mean thresholds for young and old owls were essentially identical (−6.5 and −6.6 dB, respectively, tables 1 and 2). In addition, threshold variability was not related to the acoustic chamber in which they were measured. Overall, our data from the two age groups and from the single individual measured several times indicate that barn owl ears do not deteriorate with age.

The auditory sensitivity of our barn owls compares favourably to the audiogram of a single barn owl shown in a paper by Konishi [20] (figure 1). At first glance, Konishi's owl seems about 8–10 dB more sensitive than our owls. There are, however, a few differences between the two studies. Firstly, the threshold criteria between our study and the Konishi study were different. While we used the signal-detection measure d' with a threshold criterion of 1.8, Konishi [20] defined 75% correct responses as the threshold criterion, with no indication for the rate of spontaneous responding. Secondly, Konishi [20] presented the audiogram of only one of the three owls tested in his study and stated that these were the data from the barn owl that was the ‘most carefully tested’. We thus have no knowledge about the ‘average performance’ of Konishi's owls. Thirdly, we used barn owls from the Old World species group (Tyto alba), while Konishi employed New World barn owls (Tyto furcata, formerly Tyto alba pratincola) [42,43]. These two groups have different body sizes [41]; the size of their basilar papilla is, however, the same [30,31,44]. Many studies have also employed barn owls from both groups as an animal model in central auditory physiology or anatomy and there appears to be no substantial difference between the species groups [30,31,44]. We thus conclude that the species difference between our study and the Konishi study is negligible.

(b) Long-lived birds with ageless ears

The lack of hearing loss in our old barn owls is remarkable, given that the average life expectancy of barn owls is rather low. Individuals that survive their first year have an average life expectancy of 3–4 years [22–26]. It is assumed that the high mortality rates of first year birds probably arises from a lack of experience in locating and catching prey [25,26] and the low abundance of prey [24,26]. Although barn owls are generally short-lived birds, some may get quite old in the wild. There are observations of free-living barn owls reaching an age of between 11 and 18 years, with exceptions reaching 21 years or even older [22,23,25,45]. Three of our laboratory-reared barn owls (Bart, Lisa, Weiss) thus exceeded the average lifespan by far, but were still within the range as naturally observed. We were able to obtain several threshold estimates for a wide range of test frequencies from one of these individuals (Weiss) during its 23 years of life. Over the whole time period, thresholds both increased and decreased; on average, thresholds increased by about 10 dB over 21 years. Thus we did not find shifts in sensitivity that were comparable to the typical mammalian pattern. Thresholds in aged mammals are typically elevated by at least 20–40 dB (see below). Langemann et al. [17] investigated aspects of presbycusis in another bird species, the European starling, that has an average lifespan of about 22 months. Similar to our barn owls, old starlings did not show any evidence for age-related hearing loss. The starlings' threshold variation over 11 years was on average less than ±4.5 dB [17]. So far, to our knowledge, European starlings and barn owls are the only two bird species where auditory sensitivity in quiet has been investigated in old individuals and both studies clearly indicate that birds are not subject to age-related hearing loss.

(c) Ageing birds and ageing mammals

Compared to birds, auditory sensitivity in mammals deteriorates significantly with age. Moreover, threshold shifts in mammals are most prominent at high frequencies [1]. Although most studies in mammals assessed auditory sensitivity with the use of electrophysiological methods such as auditory brainstem responses (ABR) [2,5], there are a few studies that investigated ageing in the mammalian auditory system with behavioural methods [3,4,46,47]. Mills et al. [2] showed that aged Mongolian gerbils (older than 24 months) experience a shift in ABR thresholds of about 20–35 dB compared to young animals. Behavioural measurements by Hamann et al. [3] in the same species revealed thresholds shift of about 20 dB with ageing. Sinnott et al. [47] found shifts in thresholds for vowel stimuli in Mongolian gerbils by about 10 dB per year when testing animals up to the age of 36 months in a behavioural task. Dum and von Wedel found shifts in ABR threshold of about 30–40 dB in guinea pigs aged 24–36 months, as compared to young animals of six months of age [48]. Studies in rats by Cooper et al. [49] (ABR measurements) and in mice by Ehret [4,46] (behavioural procedures, NMRI mice) and by Li & Borg [50] (ABR measurements, CBA/ca, C57BL/6 J mice) have shown thresholds to be elevated by about 15–50 dB in aged individuals. McFadden and colleagues showed that thresholds in 10–15 year old chinchillas were significantly elevated at several test frequencies, as compared to animals up to 3 years of age [5]. In summary, the loss of auditory sensitivity in these laboratory mammals was always observed at multiple test frequencies within the animals' hearing range and resembled the pattern typically found in humans suffering from presbycusis [51], i.e. a greater loss of sensitivity for high frequencies compared with low frequencies.

One major difference between mammals and birds that helps to explain this difference in ageing of ears is that birds are able to restore auditory function after cochlear damage while mammals are not. In contrast to mammals, birds and some other vertebrate groups have the capacity to regenerate lost hair cells in the auditory basilar papilla [6,9,52]. Although mammals have limited capacity to regenerate hair cells in their vestibular sensory epithelia, hair cells in the organ of Corti cannot be replaced [52]. In order to understand the mechanisms of regeneration in the avian basilar papilla, various methods have been used to induce damage. For example, local application of the ototoxic drug gentamicin to the round window of the inner ear in the pigeon led to extensive damage, wiping out hair cells over most of the basilar papilla. About 48 days later, hair cells seemed to have fully recovered [7]. Another method used injected ototoxic substances: chickens treated with ototoxic substances also regenerated new hair cells [53,54]. Similarly, in a more recent study by Woolley et al. [8], Bengalese finches (Lonchura striata domestica) were treated with an ototoxic substance. The treatment resulted in hair-cell loss especially in the basal, high-frequency region of the basilar papilla. Four weeks later, hair cells were almost fully regenerated [8]. The recovery of hair cells after the application of ototoxic substances has also been shown in European starlings, canaries (Serinus canaria) and budgerigars (Melopsittacus undulates) [14,15]. Beside the application of ototoxic substances, physical methods of inducing acoustic trauma were also used to study hair-cell regeneration in birds. Acoustic stimulation with intense SPLs induces overstimulation and death of hair cells. Regeneration of hair cells after acoustic trauma was shown, for example, in quails and in chickens [10,14,55]. In sharp contrast to mammals, all of those studies have conclusively shown the ability of birds to regenerate hair cells after damage and restore auditory function to a remarkable degree [10,14,52].

The ability for continuous regeneration of the sensory epithelium is probably the key feature for retaining ‘ageless ears’. This was previously suggested to prevent age-related hearing loss, as illustrated by behavioural data from the European starling [17]. Also in the barn owl, a bird with superbly sensitive hearing and a highly specialized cochlea, we found no evidence for age-related hearing loss up to an age near the upper limit of its life expectancy. This suggests that the innate capacity for hair-cell regeneration protects birds from age-related hearing loss. As a human being, we can only regard this capability of birds with great respect (if not with envy). Evolution has favoured birds to still benefit from regenerative abilities that were ‘lost’ in the mammalian cochlea. Mammals, including our own species, commonly suffer from a serious loss of auditory sensitivity in old age. Humans being about 65 years old will have lost on average more than 30 dB for frequencies of 4 kHz and above [51], whereas aged birds will probably experience only minimum loss in sensitivity or no deficit at all. The hope and interesting question remains whether, someday, our knowledge on preservation of sensitive hearing in birds will provide new treatment options that could counteract human sensory deficits.

Ethics

All procedures were performed in compliance with the Guidelines for the Use of Animals in Research (Animal Behaviour, 2012, 83, 301–309).

Data accessibility

All data used in statistical analyses and figures are provided as the electronic supplementary material.

Authors' contributions

B.K. and U.L. carried out or supervised data collection for the 2010 and 2016 datasets and performed the statistical analysis and manuscript preparation. The final version of the manuscript resulted from input and discussion between all four authors.

Competing interests

The authors declare no competing interests.

Funding

This work was supported by the Deutsche Forschungsgemeinschaft (SFB TR 31 ‘the Active Auditory System’).

Acknowledgements Threshold data from 1994 to 1995 were previously published in Dyson et al. [37]. We thank Maike Niebuhr and Jella Voelter for their help with behavioural training and data collection and Rainer Beutelmann for continuous technical support. Geoffrey Manley kindly supported us with the final draft reading.

Footnotes

Electronic supplementary material is available online at https://dx.doi.org/10.6084/m9.figshare.c.3866659.