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Auditory capabilities of birds in relation to the structural diversity of the basilar papilla
Hearing Research 273 (2011) 80e88
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Auditory capabilities of birds in relation to the structural diversity of the basilar papilla O. Gleich a, *, U. Langemann b a b
ENT-Department, University of Regensburg, Franz-Joseph-Strauss-Allee 11, Postfach, D-93042 Regensburg, Germany University of Oldenburg, Carl von Ossietzky Str. 9-11, 26129 Oldenburg, Germany
a r t i c l e i n f o
a b s t r a c t
Article history: Received 28 October 2009 Received in revised form 18 January 2010 Accepted 22 January 2010 Available online 29 January 2010
The basilar papilla length increases systematically with body mass for 41 species from more than 10 avian orders and this relation does not differ between phylogenetic groups. Audiograms of 25 nonstrigiform and 12 owl species, normalized relative to best frequency and best threshold, were used to compare audiogram shapes. The analysis revealed that the high frequency flank of the audiogram was remarkably similar across non-strigiform species. The high-frequency limit was on average 1.1 octaves above the best frequency, the low-frequency flank was less steep and showed much more species dependent variability. Audiogram shape in owls was much more variable. Morphological gradients along the basilar papilla revealed a small species dependent variability for the basal region of the basilar papilla and an increasing degree of variability towards the apex. In non-strigiform species, frequency selectivity for 2 and 4 kHz varied systematically with the space on the basilar papilla devoted to processing the corresponding frequency range. Space on the papilla did not vary systematically with frequency selectivity at 1 kHz. This difference between test frequencies might be related to the transition from electrical hair-cell tuning, that dominates below 1e2 kHz, to micromechanical tuning at higher frequencies. Ó 2010 Elsevier B.V. All rights reserved.
1. Introduction Today, about 10,000 bird species are found in a wide range of different habitats. This speciation has led to very divergent anatomical and behavioural adaptations including vocal communication and the physiology of the auditory system. Among birds, some extreme examples of auditory specialization have been documented. For example, barn owls are highly specialized nocturnal hunters that successfully capture mice in total darkness using only auditory cues. The basilar papilla (BP), i.e., the sensory epithelium of the barn owl’s inner ear is unusually elongated (Köppl et al., 1993) and exhibits an over-representation of the 5e10 kHz frequency range. Similar over-representation is found in central auditory nuclei (Konishi, 1993). In the pigeon (Kreithen and Quine, 1979; Schermuly and Klinke, 1990a) and the chicken (Warchol and Dallos, 1989) a capability for infra-sound perception has been reported. Infra-sound responses originate from specialized apical regions of the BP in these species (Schermuly and Klinke,
Abbreviations: BP, basilar papilla; CR, critical ratio; CAP, compound action potential. * Corresponding author. Tel.: þ49 941 944 9426; fax: þ49 941 944 9424. E-mail addresses: [email protected] (O. Gleich), ulrike. [email protected] (U. Langemann). 0378-5955/$ e see front matter Ó 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.heares.2010.01.009
1990b; Warchol and Dallos, 1989; Lavigne-Rebillard et al., 1985). Finally, some bird species use clicks for echolocation, however, specializations of their auditory system in that context have not yet been identified (Konishi and Knudsen, 1979; Thomassen et al., 2007). The purpose of the following analysis is to demonstrate the range of inter-species structural and functional variability and to search for systematic relationships between structure and function. One problem in compiling an overview on structure and function relationships of the inner ear in birds is the fact that many studies addressed diverse questions using different methodologies. From the literature, we assembled all relevant data for a direct comparison between bird species with respect to anatomical parameters and perceptual abilities. 1.1. Structural aspects Birds are amniotes and their auditory sensory epithelium evolved from the BP of primitive reptiles (stem reptiles). The “modern” BP of birds shows a number of derived features. Compared to the primitive condition in stem reptiles, the modern BP is elongated and the total number of hair cells is increased. Hair cells are differentiated across the width of the BP and classified as “tall” and “short” based on their shape (Takasaka and Smith, 1971), but a functionally more relevant distinction is based on the
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innervation pattern (Fischer, 1994). In addition, a range of anatomical gradients (e.g., hair cell dimensions, hair bundle orientation, stereovilli dimensions, etc.) vary along and across the BP in birds (reviewed in Gleich et al. (2004)). Besides this common basic pattern, the avian BP shows considerable species specific differentiation. This is, for example, obvious for the length of the papilla, which varies from near 2 mm in small songbirds (Gleich et al., 1994) to around 4 mm in pigeon and chicken (Gleich and Manley, 1988; Manley et al., 1996), 5.5 mm in the emu (Köppl and Manley, 1997) and reaching almost 12 mm in the barn owl (Köppl et al., 1993). Also, the number of hair cells varies considerably from around 3000 in small songbirds to more than 16,000 in the emu and barn owl. Generally, the width and the number of hair cells across the BP increases from the basal highfrequency end to the apical low-frequency end. In addition, there are complex species specific differences regarding the distribution of tall and short hair cells (Fischer et al., 1988, 1992; Fischer, 1992, 1994, 1998). Further anatomical gradients (e.g., number of stereovilli per hair cell, orientation of stereovilli bundles, etc.) along and across the papilla have only been characterized in a few species (review in Gleich et al. (2004)). Besides the variations at the level of the BP there are also species differences in the central auditory pathway. For example, the number of auditory nerve fibers and the ratio between hair cells and auditory nerve fibers varies between species (Köppl et al., 2000). Thus, besides structural variation in the BP that will affect the input to the auditory nerve, variation in central processing will also contribute to auditory performance.
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Table 1 Sources for body mass of bird species, as of 1st of October 2009. Bird species
Website with information on body mass
African jackass penguin Mute swan White stork Black stork Grey parrot Raven Goldcrest Great spotted kiwi Orange fronted conure Grasshopper sparrow Racket-tailed drongo
http://de.wikipedia.org/wiki/Brillenpinguin http://de.wikipedia.org/wiki/H%C3%B6ckerschwan http://de.wikipedia.org/wiki/Wei%C3%9Fstorch http://de.wikipedia.org/wiki/Schwarzstorch http://de.wikipedia.org/wiki/Graupapagei http://de.wikipedia.org/wiki/Kolkrabe http://de.wikipedia.org/wiki/Wintergoldh%C3%A4hnchen http://en.wikipedia.org/wiki/Kiwi http://www.parrots.org/index.php/encyclopedia/profile/ orange_fronted_conure/ http://www.ct.gov/dep/cwp/view.asp?A¼2723&Q¼326016 http://www.answers.com/topic/greater-racket-taileddrongo
2. Methods
[Casuarius casuarius], ostrich [Struthio camelus], blackbird [Turdus merula], jay [Garrulus glandarius], buzzard [Buteo buteo], duck [Anas plathyrynchos], herring gull [Larus argentatus], quail [Coturnix coturnix], pine siskin [Carduelis pinus], sparrow [Passer domesticus], grasshopper sparrow [Ammodramus savannarum] (Lohr et al., 2006). To obtain BP length values representative for the living state, measurements determined by scanning electron microscopy were corrected by multiplication with a factor of 1.29 to compensate for shrinkage (Gleich and Manley, 1988). Cochlear duct length for 17 bird species was determined from images of the dissected inner ears published by Gray (1908, for details see Gleich et al. (2005)). The raw endosseous cochlear duct length measurements for 19 avian species are provided in the Supplementary material of Walsh et al. (2009) and we calculated the mean of the left and right ear for each species. Thus in 10 species direct measurements of BP length and cochlear duct length were available (ostrich, emu, cassowary, tufted duck, mallard duck, chicken, budgerigar, zebra finch, buzzard, barn owl). The best fit linear regression line for the plot of cochlear duct length as a function of BP length for nine species (excluding the data point from the barn owl that was far outside the distribution of the other birds’ data) revealed a significant correlation between the two variables (regression line: y ¼ 1.4875x þ 0.0905; R2 ¼ 0.767; p ¼ 0.002). The slope of the regression line indicates that a scaling factor of 2/3 is adequate to obtain an estimate of BP length from cochlear duct measurements (see also Gleich et al. (2005)). In the following, we will adopt this scaling factor when including the cochlear duct measurements in the comparison of BP length. A measure representing body size that can be readily found for most species in the literature is body mass. References to most anatomical data shown in this paper are listed in the Supplementary material of Gleich et al. (2005). The body mass of the nightingale [Luscinia megarhynchos] was found in Kipper et al. (2006). The body mass from additional species was derived from the websites listed in Table 1.
2.1. Anatomical data
2.2. Audiograms
For starling [Sturnus vulgaris], zebra finch [Taeniopygia guttata], canary [Serinus canarius], barn owl [Tyto alba], budgerigar [Melopsittacus undulatus], chicken [Gallus gallus domesticus], pigeon [Columba livia], tufted duck [Aythya fuligula], and emu [Dromaius novaehollandiae] anatomical gradients along and across the BP have been analyzed in detail (see review in Gleich et al. (2004)). For the following additional species, the length of the BP has been measured by light or scanning electron microscopy: cassowary
The sources of behavioural audiograms from most bird species have been listed in Gleich et al. (2005). In the present study, we have added audiogram data from the hooded crow [Corvus corone cornix] (Jensen and Klokker, 2006), the orange fronted conure [Aratinga canicularis] (Wright et al., 2003) and the grasshopper sparrow (Lohr et al., 2006). Using the original raw audiogram data that were available for each species, 3rd-order polynomial fits were calculated. Comparing
1.2. Functional aspects One of the most basic descriptions of auditory capability is the audiogram, that characterizes the frequency dependent variation of absolute sensitivity. Partly due to the columella type single ossicle middle ear of birds, sound transduction deteriorates above 4 kHz and the high frequency hearing range in birds is limited to frequencies at or slightly above 10 kHz (Saunders et al., 2000; Manley, 2010). Based on data from 23 species, Dooling (1992) described differences in audiogram characteristics between different avian orders and between different families of songbirds with respect to absolute sensitivity and best audiogram frequency (i.e., the frequency with the lowest absolute threshold). As will be shown below, factors beyond phylogenetic relationships affect audiogram parameters. In birds, the most sensitive thresholds were reported to vary between 15 and 25 dB SPL (e.g., Fay, 1992). Best audiogram frequencies in a sample of 37 bird species varied considerably between 1.1 and 5.6 kHz (e.g., Gleich et al., 2005). The frequency distribution along the BP, i.e., the place-frequency map, is known for several avian species. The length of the BP and the space available for coding of a given frequency range shows speciesspecific variability (e.g., reviewed in Gleich et al. (2004)). One important question addressed here is whether the available space on the BP affects frequency selectivity.
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the raw data plots and the best fit functions indicated that the 3rdorder polynomial fits were a good representation of the audiograms. This was confirmed by a quantitative analysis of the coefficient of determination (i.e., the squared correlation coefficient) for the linear regression comparing the raw and the best fit thresholds for the behavioural audiogram of each species. This analysis was performed for 40 species. In all species the regression revealed a significant correlation between the raw and the best fit thresholds (p # 0.02) and for 36 of these species the significance level was p # 0.001. The mean coefficient of determination for all 40 audiograms analyzed was 0.912. Nine species showed coefficients of determination between 0.8 and 0.9, four species were below 0.8. This high degree of correlation supports the qualitative impression that the best fit functions are an adequate representation for comparing audiogram characteristics across species. To derive audiogram characteristics, the best fit function for each species was calculated in 100 Hz steps for the frequency range covered by the raw data. For each species, the frequency with the lowest threshold was defined as the best audiogram frequency. Additional parameters were determined; for example, low- and high-frequency limits describe the frequencies below and above the best audiogram frequency with thresholds 30 dB above the best frequency. The range between the low- and high-frequency limits was used as an indicator of the hearing range and was expressed in octaves. We did not extrapolate audiograms beyond the actual threshold data. Thus the low- and high-frequency limits of the audiogram were only derived when they were within the frequency range where thresholds had actually been collected during behavioural testing and are thus not available for all species. 3. Results and discussion 3.1. Basilar papilla length and body mass Gleich et al. (2005) demonstrated a significant positive correlation between the length of the BP and body mass. Although the barn owl is the only strigiform species where the BP length is available, it was excluded from this analysis since its papilla length was clearly outside the range of other birds (see also additional arguments for a separate analysis as discussed below). By adding the data from Walsh et al. (2009) to those presented by Gleich et al. (2005), the relation was compiled for a total of 41 non-strigiform species. Fig. 1 demonstrates the systematic relationship between the length of the BP and body mass. Different groups of birds are coded by separate symbols. The definition of groups is based on suggestions by Feduccia (1980, 1995) and Olsen (1985). The
Fig. 1. The length of the basilar papilla as a function of body mass in four phylogenetic groups of birds (see text for explanations).
palaeognathous birds in the present sample are represented by emu, cassowary, ostrich, two kiwi species and the great tinamou (black triangles). The neognathous birds can be separated into a waterbird assembly (shown as blue diamonds and represented by Anseriformes [ducks and swan], Gaviformes [red throated diver], Charadriformes [herring gull], Pelicaniformes [cape gannet, cormorant], Sphenisciformes [African jackass penguin] and Ciconiiformes [storks and herons]) and a landbird assembly. Landbirds are further subdivided in primitive landbirds (shown by green circles and represented by Columbiformes [pigeons], Galliformes [chicken, quails, turkey, grouse], Gruiformes [crane] and Psittaciformes [parrots]) and advanced landbirds (shown by red circles and represented by Passeriformes [songbirds] and Falconiformes [falcon, sparrowhawk and buzzard]). In non-strigiform bird species, BP length varied between 1.9 mm in the goldcrest and 5.5 mm in the emu while body mass varied from a few grams in small songbirds to near 100 kg in the ostrich. The data from the different avian groups represented by different colours in Fig. 1 seem to represent a continuum and they are well described by a common best fit regression line. This regression suggests that the relation between body mass and BP length does not systematically differ between different phylogenetic avian groups.
3.2. Absolute thresholds The best sensitivity (i.e., lowest absolute threshold) as a function of best audiogram frequency (i.e., the frequency with the lowest absolute threshold) for 40 species is shown in Fig. 2. The best audiogram frequency varied between 2.0 and 4.5 kHz in non-strigiform birds. From 12 owl species, 2 had lower best frequencies (brown fish owl 1.1 kHz; great horned owl 1.4 kHz) and 3 had higher best frequencies (African wood owl and long eared owl 5.5 kHz; barn owl 5.6 kHz) than the other bird species. The only owl species studied in detail is the barn owl: Its best audiogram frequency was only slightly higher than those of song birds with the highest best audiogram frequencies (4.5 kHz for great tit and grasshopper sparrow). This is somewhat surprising given that the barn owl exhibits features that are distinctly different from other bird species. For example, the high frequency specialization in barn owls is reflected in an over-representation of the 5e10 kHz region on the BP (Köppl et al., 1993). This one octave frequency range occupies around 5 mm on the BP and thus represents a much
Fig. 2. The best (i.e., lowest) audiogram threshold as a function of best audiogram frequency illustrates the species-specific variability. Different symbols indicate waterbirds (blue diamond, here represented by the duck) being the least advanced followed by primitive (green circles, N ¼ 9) and advanced (red circles, N ¼ 18) landbirds. The strigiformes (orange asterisks, N ¼ 12) are shown separately as a highly specialized group of advanced landbirds.
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higher space constant than seen in any other bird species, where space constants are typically between 0.5 and 1 mm/oct (Gleich et al., 2004). While best audiogram thresholds in all strigiformes were below 0 dB SPL (mean 15.04 dB SPL), only three of the non-strigiform species had a best thresholds below 0 dB SPL. The mean best threshold in all non-strigiform species was 6.78 dB SPL. The best threshold in owls was thus on average approximately 20 dB lower compared to other birds. At least for the barn owl, it has been shown that the facial ruff feathers form an external ear analogous to the mammalian pinna, providing an acoustic gain of about 20 dB between 3 and 9 kHz (Coles and Guppy, 1988). The extreme sensitivity of owls is thus likely related to the specialized external ear structures that are typically absent in other avian species. Consequently threshold comparisons between Strigiformes and other avian groups are not really valid. 3.3. Audiograms Examples of best 3rd-order fits used to derive audiogram characteristics are illustrated for those species where both the audiogram and the length of the BP are known. Fig. 3A gives an idea of frequency and threshold variations. For a better comparison of the audiogram shapes, Fig. 3B shows audiograms normalized relative to best frequency and to best threshold for the 25 nonstrigiform species in which the high-frequency limit of 30 dB was reached. The high frequency flanks of these normalized audiograms were quite similar across species and showed little variation. The low frequency flank of the audiograms was much more variable between species and less steep than the high frequency flank. Fig. 3C illustrates normalized audiograms from 12 owl species. The slopes of the high frequency audiogram flanks varied over a wider range compared to non-strigiform species. The high-frequency slope was steeper than in non-strigiform species in 7 of the 12 owl species. In addition, the low-frequency flanks appeared very shallow in some owl species. This comparison showed that the shapes of owl audiograms were much more variable and consequently we analyzed owls and non-strigiform species separately.
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across species in the basal high-frequency region and large variability in the apical-low frequency region. 3.5. Frequency representation and frequency selectivity The frequency representation along the avian BP is tonotopically arranged with high frequencies represented at the basal and low frequencies represented at the apical end of the papilla. One obvious question is whether auditory frequency selectivity is related to the spatial representation of frequency on the BP: Does the amount of space along the BP devoted to a certain frequency range affect frequency resolution? The hearing range perceived by a given species is transduced by the BP which varies in length between 2 and 6 mm in non-strigiform species. Frequency maps describing the distribution of frequency along the BP are known for 9 species (see review in Gleich et al. (2004)). The mapping of frequency along the BP and the space devoted to a given frequency range differs between bird species. When frequency is plotted on a logarithmic scale, the slope of the place-frequency map is a quantitative measure of the “space constant” that indicates the
3.4. Anatomy and gradients along the papilla Several gradients change systematically along the BP in parallel with the tonotopic organization of frequency. However, the relation between a given morphological parameter and frequency position on the BP differs considerably between species (e.g., Gleich et al., 2004). This is exemplified for the variation of the number of hair cells across the BP in Fig. 4A. For example, at 1 kHz the number of hair cells across the papilla varied between about 21 in the canary and 33 hair cells in the barn owl. Plotting the number of hair cells across the BP as a function of frequency did not lead to a match of this morphological gradient across species (see Fig. 4A). A match of the gradients along the papilla as a function of frequency was also not achieved for additional morphological parameters like the width of the papilla, the number of stereovilli per hair cell and the maximum height of the stereovilli (Gleich et al., 2004). This demonstrates that none of these single parameters alone can determine the frequency response at a given BP location. The frequency response rather results from an interaction of different parameters. Replotting the number of hair cells across the BP as a function of distance from the base illustrates that the number is small at the base in all species. As hair cell number grows toward the apex the variability across species increases (Fig. 4B and C). Taken together, the comparison of the normalized audiograms in Fig. 3 and the morphological gradients illustrated in Fig. 4 reveal small variability
Fig. 3. (A) Audiogram shapes of nine bird species where the length of the basilar papilla is known. (B) Audiograms of 25 non-strigiform species with a high-frequency limit of more than 30 dB. (blue for duck, green for primitive landbirds, red for advanced landbirds). (C) Audiograms of 12 owl species (orange for barn owl, black lines for all other owl species). Audiograms in (B) and (C) have been normalized with respect to the best audiogram frequency (expressed in octaves) and to the best auditory threshold. The horizontal dotted line indicates 30 dB above best audiogram threshold.
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space available per octave (mm/oct; e.g., Manley, 2000). A logarithmic function with an invariant space constant along the BP has been found in several species. Deviations from this logarithmic function occurred in the barn owl, starling, chicken and budgerigar, that show decreasing space constants towards the apical lowfrequency end of the BP, thus extending the hearing range towards low frequencies. A comparison across avian species revealed a systematic correlation between the space devoted to the 1e2 kHz range and the length of the BP, varying from 0.5 mm in the canary with a BP length of 2.1 mm to 0.9 mm in the emu with a 5.5 mm long BP (Gleich et al., 2004). A common measure of auditory frequency selectivity is the critical ratio (CR). The CR is determined in a behavioural masking
experiment and yields the detection threshold of a tone relative to the noise spectrum level of a wide-band noise masker (i.e., the signal-to-noise ratio in dB). The CR bandwidth of the corresponding rectangular auditory filter (in Hz) can then be estimated from this ratio (e.g., Langemann et al., 1995). Low CR values indicate high frequency selectivity, and high CR values indicate low frequency selectivity. In Fig. 5 we plot the CR as a function of the octaves mapped to 1 mm on the BP (the inverse of the space constant) for three different test frequencies. We included data from bird species where both the CR (starling e Langemann et al., 1995, budgerigar e Saunders et al., 1978, pigeon e Hienz and Sachs, 1987, canary and zebra finch e Okanoya and Dooling, 1987a, barn owl e Dyson et al., 1998) and the space constants (derived from the maps published in Gleich et al. (2004)) were available. The two data points with values below 1 oct/mm were from the barn owl (where the CR has not been determined for 1 kHz). All other data with values above 1 oct/ mm are from non-strigiform species. The linear regression lines for the data at 2 kHz (triangles, dotted line, p ¼ 0.03) and at 4 kHz (asterisks, thin continuous line, p ¼ 0.04) show a significant correlation between the CR and the number of octaves mapped to 1 mm on the basilar papilla: the less space was available on the papilla (i.e., more octaves mapped to 1 mm), the lower was the frequency selectivity (indicated by higher CR values) at 2 and 4 kHz. The function at 4 kHz appeared shifted to the left compared to the function at 2 kHz. Consequently, in the 4 kHz compared to the 2 kHz region more space was associated with a given CR. The data for the 1 kHz test frequency (circles) did not indicate a similar correlation between space and frequency selectivity (see coefficients of determination in the upper left of Fig. 5; p ¼ 0.57). Although on average more octaves are mapped onto the BP in the 1 kHz region compared to the higher frequencies, frequency selectivity was relatively high as indicated by the low CR values. At 1 kHz the average CR was 23.4 dB and was associated with 1.996 octaves mapped to 1 mm of the BP. Estimates based on the regression lines shown in Fig. 5 reveal that more space was associated with a CR of 23.4 dB at higher frequencies. At 2 kHz 1.588 octaves and at 4 kHz 1.331 octaves were mapped to 1 mm of the BP at a CR of 23.4 dB.
Fig. 4. The number of hair cells across the basilar papilla shows a systematic gradient from the base towards the apex. Black is used for the emu, blue for the duck, green for primitive landbirds, red for advanced landbirds and orange for the barn owl. (A) The position along the basilar papilla was converted to frequency based on the placefrequency maps presented in Gleich et al. (2004). (B) The number of hair cells is plotted as a function of the distance (in mm) from the basal end of the papilla (the length was limited to 6 mm excluding the apical half of the barn owl basilar papilla). The x-axis was reversed for a better comparison with the frequency scales shown in (A) and in Fig. 3. (C) The number of hair cells was normalized and is plotted as a function of the distance (in %) from the basal end of the papilla.
Fig. 5. The critical ratio (a behavioural measure of frequency selectivity) is shown as a function of the frequency range (expressed in octaves) mapped to 1 mm on the basilar papilla. Green symbols: primitive land birds, red symbols: advanced landbirds, orange symbols: barn owl. The figure includes data from six bird species (starling, budgerigar, pigeon, canary, zebra finch, barn owl; see text). The test frequency is indicated by different symbols (circle: 1 kHz, triangle: 2 kHz, asterisk: 4 kHz). The coefficient of determination for a linear regression through the data at the different test frequencies (excluding the owl data points) is given in the top left. The best fit linear regression lines are shown for significant correlations at 4 kHz (thin continuous line) and 2 kHz (dotted line).
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Fig. 6. Audiograms from 4 galliform species (primitive landbirds). (A) Absolute threshold is shown as a function of frequency. (B) The comparison of normalized audiograms emphasizes the broadly tuned audiogram of the adult chicken.
The finding that the space on the BP and frequency selectivity correlate at a test frequency of 2 and 4 kHz, but not at 1 kHz, may be related to the transition of the tuning mechanisms between low and high frequencies that contribute to frequency selectivity in the avian BP (Gleich and Manley, 2000). Electrical tuning dominates at low frequencies and is determined by the electrical properties of an individual hair cell’s membrane. It is independent of the properties of neighbouring hair cells. Consequently space is not a major factor determining frequency selectivity at low frequencies. Mechanical tuning due to the interaction of the micromechanical properties of the BP, basilar membrane, tectorial membrane and the hair cell complex becomes dominant for higher frequencies above 1e2 kHz. Tuning due to micromechanical properties is influenced by mechanical coupling to neighbouring structures, and thus space will affect frequency selectivity (Manley, 2000). The two left most data points refer to the CR data of the barn owl at 2 and 4 kHz. Both values were off the distribution for non-strigiform data. With the ample space available on the barn owl basilar papilla, much higher frequency selectivity could have been expected (see also Dyson et al. (1998)). Estimates of frequency selectivity derived from measures of otoacoustic emissions also showed that frequency tuning in the barn owl was not better than average (Köppl et al., 1998). In addition, the frequency selectivity of single auditory nerve fibers in the barn owl was not increased in the region of expanded frequency mapping as might be expected based on the equal distance hypothesis (Köppl, 1997). The extended space on the BP of the barn owl is obviously not associated with increased frequency selectivity.
3.6. Hearing in chickens For a better comparison of audiogram shapes, Fig. 3B shows audiograms normalized relative to best frequency and best threshold for all 25 non-strigiform species, where a high-frequency limit of more than 30 dB was available. Fig. 6 compares the data from 4 galliform species (turkey, chicken, quail, bobwhite quail). The chicken audiogram appears quite different from other audiograms (see also Fig. 3), with the low and high frequency audiogram flanks being shallower than in any other non-strigiform species. It is not clear why the chicken audiogram is so broadly tuned. Although the best audiogram threshold in the chicken is relatively high (16 dB SPL) it is still within the higher range observed in other non-strigiform species and does not indicate a severe hearing loss like in the Belgian Waterslager canary strain (Okanoya and Dooling, 1985, 1987b). The chicken audiogram data reported by Saunders and Salvi (1993) were collected in white leghorn chickens that were older than 26 weeks. However, it appears unlikely that BP pathology as described for broiler and egg layer chickens (Durham et al., 2002; Smittkamp et al., 2002) could explain the shallow flanks of the chicken audiogram (Fig. 6), especially for the high frequency side. Basilar papilla pathology affecting the base, and leading to a loss of high frequency distortion product otoacoustic emissions as described by Durham et al. (2002) should be associated with a pronounced high frequency hearing loss. The much shallower high frequency flank of the chicken behavioural audiogram compared to other species is also in contrast to audiograms derived from the compound action
Fig. 7. (A) Behavioural audiograms of 4 species where also CAP audiograms have been published. (B) CAP audiograms of the same species where behavioural audiograms are shown on the left. The lines show 3rd-order polynomial fits to the data from chicken (thinner, darker green line), pigeon (thicker, brighter green line), canary (red line) and the barn owl (orange line).
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Fig. 8. (A) The high-frequency limit of the audiogram is plotted as a function of best audiogram frequency for 25 non-strigiform species and 12 owl species. (B) The high-frequency limit in octaves relative to the best audiogram frequency is plotted as a function of best audiogram frequency. The linear regression is shown for the data from non-strigiform species. Blue diamond: duck, green circles: primitive landbirds, red circles: advanced landbirds, orange asterisks: strigiformes.
potential (CAP). Fig. 7 compares on the left side four behavioural audiograms and shows the corresponding CAP audiograms on the right side (chicken e Rebillard and Rubel, 1981; Patuzzi and Bull, 1991; Salvi et al., 1992, pigeon e Gummer et al., 1987, canary e Gleich et al., 1995, barn owl e Köppl and Gleich, 2007). CAP audiograms typically show higher thresholds as compared to behavioural audiograms, but in general both types of audiograms share basic characteristics, as illustrated in Fig. 7. The shape of behavioural and CAP audiograms is not identical for a given species. These discrepancies may relate to methodology. Physiological measures use synchronized neural responses to the onset of short tones. Behavioural testing typically uses tones with a duration of several hundred milliseconds, where temporal integration may contribute to lower thresholds. Differences between studies may also arise from sampling problems since sample size is often small. Nevertheless, the high frequency flank of the CAP audiogram in immature chickens was not obviously different from that of other birds (Fig. 7B), while it appeared considerably shallower in the behavioural audiogram from the adult chickens (see Figs. 6 and 7A). The morphological analysis of the chicken inner ear (e.g., Fig. 4; Manley et al., 1996) typically used very young chickens and the structural changes observed in chickens beyond 30 weeks of age (Durham et al., 2002) suggest a pronounced high frequency hearing loss and do not explain the shallow high frequency slope of the audiogram determined in adult chickens (Saunders and Salvi, 1993). The relatively shallow low frequency flank of the chicken audiogram (see normalized audiograms in Fig. 6B) might be related to a specialization for
low frequency perception (Lavigne-Rebillard et al., 1985; Warchol and Dallos, 1989). 3.7. High-frequency limit of hearing in birds While the upper limit of hearing in mammals typically extends to the ultra-sound range, birds are limited to frequencies around 10 kHz. In mammals the evolution of high frequency hearing was interpreted in the context of sound localization (e.g., Heffner and Heffner, 1992). Extending the hearing range towards higher frequencies would require either shifting the frequency range of the whole audiogram toward higher frequencies or decreasing the high frequency slope of the audiogram. For a quantitative comparison beyond the qualitative comparison illustrated in Fig. 3 we analyzed the high-frequency limit of the audiogram as a function of best audiogram frequency for all species including owls. The high-frequency limit of the audiogram increased roughly linearly with best frequency in non-strigiform species (Fig. 8A). Although some owl data points (orange asterisks) fitted very well into the distribution, some clearly deviated from the pattern seen in non-strigiform species. Plotting the high-frequency limit in octaves (relative to the best audiogram frequency) as a function of best audiogram frequency revealed a small but significant decrease of the upper audiogram frequency limit with increasing best frequency in non-strigiform bird species (see best fit regression line in Fig. 8B). However, the slope of the regression function was small (0.0607 oct/kHz), resulting in an estimated difference of only 0.15 octaves between the non-strigiform species with the lowest (2 kHz,
Fig. 9. (A) The best audiogram frequency (diamonds) as well as the low (triangles) and high (circles) frequency limits of the audiogram are shown as a function of basilar papilla length. The best fit exponential lines illustrate a systematic decrease with increasing papilla length. (B) The high- (circles) and low- (triangles) frequency limits in octaves relative to the best audiogram frequency are plotted as a function of basilar papilla length. The dotted line at zero represents the best audiogram frequency. Blue: duck, green: primitive landbirds, red: advanced landbirds.
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turkey) and highest best frequencies (4.5 kHz, great tit and grasshopper sparrow). From a practical point of view the effect of best frequency on the high-frequency limit is very small and the high frequency audiogram slope is quite similar across non-strigiform species (see also Fig. 3B), being on average slightly more than one octave above the best audiogram frequency. These observations indicate that the high frequency slope of the audiogram does not vary between phylogenetic groups in non-strigiform species. Some of the owl data points deviated considerably from the distribution of the other birds, with lower values indicating a steeper high frequency flank of the audiogram. Only in the great horned owl was the upper frequency limit of 4.6 kHz 1.7 octaves above the best audiogram frequency of 1.4 kHz, indicating a shallower high frequency audiogram flank. 3.8. Basilar papilla length and frequency range Best audiogram frequency and BP length are inversely related (Gleich et al., 2005). Fig. 9 shows that in addition to the best audiogram frequency, the low and high-frequency limits of the audiogram decrease with increasing BP length. Consistent with the typically shallower low frequency slope of the audiogram, the distance between the best frequency and the low-frequency limit was larger (on a logarithmic scale) than the distance between the best frequency and the high-frequency limit (Fig. 9A). On a logarithmic scale, the effect of BP length on the low-frequency limit was more pronounced than for the high-frequency limit (Fig. 9A). Best frequency and the high-frequency limit decreased approximately by 0.4 oct/mm increase of BP length while the decrease for the lowfrequency limit was 1.4 oct/mm. Fig. 9B plots the high and lowfrequency limits in octaves with respect to the best frequency as a function of BP length. Independent of BP length, and consistent with the data presented in Fig. 8, the high-frequency limit was on average 1.1 octaves higher than the best frequency (Fig. 9B). In contrast, the low-frequency limit increased from an average of 2.5 octaves below best frequency in small songbirds (BP length slightly above 2 mm) to 4.5 octaves below best frequency in the pigeon (4 mm BP length). The corresponding hearing range in octaves increased from around 3.5 octaves to 5.5 octaves, respectively (see Fig. 9B). Acknowledgements Roots of the basic concept for a comparative analysis of structureefunction relationships of the avian inner ear reach back to research within the SFB 204 “Gehör” that was funded by the DFG from 1983 to 1997. The collaboration between O.G. and U.L. was funded by the DFG within the SFB/TRR 31 “The active auditory system”. We thank G.A. Manley and two anonymous reviewers for helpful suggestions for improving the initial version of the manuscript. References Coles, R.B., Guppy, A., 1988. Directional hearing in the barn owl (Tyto alba). J. Comp. Physiol. A 163, 117e133. Dooling, R.J., 1992. Hearing in birds. In: Webster, D.B., Fay, R.R., Popper, A.N. (Eds.), The Evolutionary Biology of Hearing. Springer-Verlag, Heidelberg, New York, pp. 545e559. Durham, D., Park, D.L., Girod, D.A., 2002. Breed differences in cochlear integrity in adult, commercially raised chickens. Hear. Res. 166, 82e95. Dyson, M.L., Klump, G.M., Gauger, B., 1998. Absolute hearing thresholds and critical masking ratios in the European barn owl: a comparison with other owls. J. Comp. Physiol. A 182, 695e702. Fay, R.R., 1992. Structure and function in sound discrimination among vertebrates. In: Webster, D.B., Fay, R.R., Popper, A.N. (Eds.), The Evolutionary Biology of Hearing. Springer-Verlag, New York, pp. 229e263. Feduccia, A., 1980. The Age of Birds. Harvard University Press, Cambridge.
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Feduccia, A., 1995. Explosive evolution in tertiary birds and mammals. Science 267, 637e638. Fischer, F.P., 1992. Quantitative analysis of the innervation of the chicken basilar papilla. Hear. Res. 61, 167e178. Fischer, F.P., 1994. General pattern and morphological specializations of the avian cochlea. Scanning Microsc. 8, 351e364. Fischer, F.P., 1998. Hair cell morphology and innervation in the basilar papilla of the emu (Dromaius novaehollandiae). Hear. Res. 121, 112e124. Fischer, F.P., Köppl, C., Manley, G.A., 1988. The basilar papilla of the barn owl Tyto alba: a quantitative morphological SEM analysis. Hear. Res. 34, 87e101. Fischer, F.P., Miltz, C., Singer, I., Manley, G.A., 1992. Morphological gradients in the starling basilar papilla. J. Morphol. 213, 225e240. Gleich, O., Manley, G.A., 1988. Quantitative morphological analysis of the sensory epithelium of the starling and pigeon basilar papilla. Hear. Res. 34, 69e86. Gleich, O., Manley, G.A., 2000. The hearing organ of birds and crocodilia. In: Dooling, R.J., Fay, R.R., Popper, A.N. (Eds.), Comparative Hearing: Birds and Reptiles. Springer, New York, pp. 70e138. Gleich, O., Manley, G.A., Mandl, A., Dooling, R.J., 1994. The basilar papilla of the canary and the zebra finch: a quantitative scanning electron microscopic description. J. Morphol. 221, 1e24. Gleich, O., Klump, G.M., Dooling, R.J., 1995. Peripheral basis for the auditory deficit in Belgian Waterslager canaries (Serinus canarius). Hear. Res. 82, 100e108. Gleich, O., Fischer, F.P., Köppl, C., Manley, G.A., 2004. Hearing organ evolution and specialization: archosaurs. In: Manley, G.A., Popper, A.N., Fay, R.R. (Eds.), Evolution of the Vertebrate Auditory System. Springer, New York, pp. 225e260. Gleich, O., Dooling, R.J., Manley, G.A., 2005. Audiogram, body mass, and basilar papilla length: correlations in birds and predictions for extinct archosaurs. Naturwissenschaften 92, 595e598. Gray, A.A., 1908. The Labyrinth of Animals Including Mammals, Birds, Reptiles and Amphibians, vol. II. J. & A. Churchill, London. Gummer, A.W., Smolders, J.W., Klinke, R., 1987. Basilar membrane motion in the pigeon measured with the Mössbauer technique. Hear. Res. 29, 63e92. Heffner, R.S., Heffner, H.E., 1992. Evolution of sound localization in mammals. In: Webster, D.B., Fay, R.R., Popper, A.N. (Eds.), The Evolutionary Biology of Hearing. Springer-Verlag, Heidelberg, New York, pp. 691e715. Hienz, R.D., Sachs, M.B., 1987. Effects of noise on pure-tone thresholds in blackbirds (Agelaius phoeniceus and Molothrus ater) and pigeons (Columba livia). J. Comp. Psychol. 101, 16e24. Jensen, K.K., Klokker, S., 2006. Hearing sensitivity and critical ratios of hooded crows (Corvus corone cornix). J. Acoust. Soc. Am. 119, 1269e1276. Kipper, S., Mundry, R.M., Sommer, C., Hultsch, H., Todt, D., 2006. Song repertoire size is correlated with body measures and arrival date in common nightingales, Luscinia megarhynchos. Anim. Behav. 71, 211e217. Konishi, M., 1993. Listening with two ears. Sci. Am. 268, 66e73. Konishi, M., Knudsen, E.I., 1979. The oilbird: hearing and echolocation. Science 204, 425e427. Köppl, C., 1997. Frequency tuning and spontaneous activity in the auditory nerve and cochlear nucleus magnocellularis of the barn owl Tyto alba. J. Neurophysiol. 77, 364e377. Köppl, C., Gleich, O., 2007. Evoked cochlear potentials in the barn owl. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 193, 601e612. Köppl, C., Manley, G.A., 1997. Frequency representation in the emu basilar papilla. J. Acoust. Soc. Am. 101, 1574e1584. Köppl, C., Gleich, O., Manley, G.A., 1993. An auditory fovea in the barn owl cochlea. J. Comp. Physiol. A 171, 695e704. Köppl, C., Klump, G.M., Taschenberger, G., Dyson, M.L., Manley, G.A., 1998. The auditory fovea of the barn owl e no correlation with enhanced frequency resolution. In: Palmer, A.R., Rees, A., Summerfield, A.Q., Meddis, R. (Eds.), Psychophysical and Physiological Advances in Hearing. Whurr Publishers, London, pp. 153e159. Köppl, C., Wegscheider, A., Gleich, O., Manley, G.A., 2000. A quantitative study of cochlear afferent axons in birds. Hear. Res. 139, 123e143. Kreithen, M.L., Quine, D.B., 1979. Infrasound detection by the homing pigeon: a behavioural audiogram. J. Comp. Physiol. A 129, 1e4. Langemann, U., Klump, G.M., Dooling, R.J., 1995. Critical bands and critical-ratio bandwidth in the European starling. Hear. Res. 84, 167e176. Lavigne-Rebillard, M., Cousillas, H., Pujol, R., 1985. The very distal part of the basilar papilla in the chicken: a morphological approach. J. Comp. Neurol. 238, 340e347. Lohr, B., Gleich, O., Ryals, B.M., Dooling, R.J., 2006. Auditory sensitivity and its morphological correlates in the grasshopper sparrow (Ammodramus savannarum). Abstr. Assoc. Res. Otolaryngol. 29, 323e324. Manley, G.A., 2000. Cochlear mechanisms from a phylogenetic viewpoint. Proc. Natl. Acad. Sci. USA 97, 11736e11743. Manley, G.A., 2010. An evolutionary perspective on middle ears. Hear. Res. 263, 3e8. Manley, G.A., Meyer, B., Fischer, F.P., Schwabedissen, G., Gleich, O., 1996. Surface morphology of the basilar papilla of the tufted duck Aythya fuligula and the domestic chicken Gallus gallus domesticus. J. Morphol. 227, 197e212. Okanoya, K., Dooling, R.J., 1985. Colony differences in auditory thresholds in the canary (Serinus canarius). J. Acoust. Soc. Am. 78, 1170e1176. Okanoya, K., Dooling, R.J., 1987. Hearing in passerine and psittacine birds: a comparative study of absolute and masked auditory thresholds. J. Comp. Psychol. 101, 7e15. Okanoya, K., Dooling, R.J., 1987. Strain differences in auditory thresholds in the canary (Serinus canarius). J. Comp. Psychol. 101, 213e215.
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Olsen, S.L., 1985. The fossil record of birds. In: Farner, D., King, J., Parkes, K. (Eds.), 1985. Avian Biology, vol. 8. Academic Press, New York, pp. 79e238. Patuzzi, R.B., Bull, C.L., 1991. Electrical responses from the chicken basilar papilla. Hear. Res. 53, 57e77. Rebillard, G., Rubel, E.W., 1981. Electrophysiological study of the maturation of auditory responses from the inner ear of the chick. Brain Res. 229, 15e23. Salvi, R.J., Saunders, S.S., Powers, N.L., Boettcher, F.A., 1992. Discharge patterns of cochlear ganglion neurons in the chicken. J. Comp. Physiol. A 170, 227e241. Saunders, S.S., Salvi, R.J., 1993. Psychoacoustics of normal adult chickens: thresholds and temporal integration. J. Acoust. Soc. Am. 94, 83e90. Saunders, J.C., Denny, R.M., Bock, G.R., 1978. Critical bands in the parakeet (Melopsittacus undulatus). J. Comp. Physiol. A 125, 359e365. Saunders, J.C., Duncan, R.K., Doan, D.E., Werner, Y.L., 2000. The middle ear of reptiles and birds. In: Dooling, R.J., Fay, R.R., Popper, A.N. (Eds.), Comparative Hearing: Birds and Reptiles. Springer, New York, pp. 13e69. Schermuly, L., Klinke, R., 1990. Infrasound sensitive neurones in the pigeon’s cochlear ganglion. J. Comp. Physiol. A 166, 355e363.
Schermuly, L., Klinke, R., 1990. Origin of infrasound sensitive neurones in the papilla basilaris of the pigeon: a HRP study. Hear. Res. 48, 69e78. Smittkamp, S.E., Colgan, A.L., Park, D.L., Girod, D.A., Durham, D., 2002. Time course and quantification of changes in cochlear integrity observed in commercially raised broiler chickens. Hear. Res. 170, 139e154. Takasaka, T., Smith, C.A., 1971. The structure and innervation of the pigeon’s basilar papilla. J. Ultrastruct. Res. 35, 20e65. Thomassen, H.A., Gea, S., Maas, S., Bout, R.G., Dirckx, J.J., Decraemer, W.F., Povel, G.D., 2007. Do Swiftlets have an ear for echolocation? The functional morphology of Swiftlets’ middle ears. Hear. Res. 225, 25e37. Walsh, S.A., Barrett, P.M., Milner, A.C., Manley, G., Witmer, L.M., 2009. Inner ear anatomy is a proxy for deducing auditory capability and behaviour in reptiles and birds. Proc. Biol. Sci. 276 (1660), 1355e1360. Warchol, M.E., Dallos, P., 1989. Neural response to very low-frequency sound in the avian cochlear nucleus. J. Comp. Physiol. A 166, 83e95. Wright, T.F., Cortopassi, K.A., Bradbury, J.W., Dooling, R.J., 2003. Hearing and vocalizations in the orange-fronted conure (Aratinga canicularis). J. Comp. Psychol. 117, 87e95.
Contents lists available at ScienceDirect
Hearing Research journal homepage: www.elsevier.com/locate/heares
Auditory capabilities of birds in relation to the structural diversity of the basilar papilla O. Gleich a, *, U. Langemann b a b
ENT-Department, University of Regensburg, Franz-Joseph-Strauss-Allee 11, Postfach, D-93042 Regensburg, Germany University of Oldenburg, Carl von Ossietzky Str. 9-11, 26129 Oldenburg, Germany
a r t i c l e i n f o
a b s t r a c t
Article history: Received 28 October 2009 Received in revised form 18 January 2010 Accepted 22 January 2010 Available online 29 January 2010
The basilar papilla length increases systematically with body mass for 41 species from more than 10 avian orders and this relation does not differ between phylogenetic groups. Audiograms of 25 nonstrigiform and 12 owl species, normalized relative to best frequency and best threshold, were used to compare audiogram shapes. The analysis revealed that the high frequency flank of the audiogram was remarkably similar across non-strigiform species. The high-frequency limit was on average 1.1 octaves above the best frequency, the low-frequency flank was less steep and showed much more species dependent variability. Audiogram shape in owls was much more variable. Morphological gradients along the basilar papilla revealed a small species dependent variability for the basal region of the basilar papilla and an increasing degree of variability towards the apex. In non-strigiform species, frequency selectivity for 2 and 4 kHz varied systematically with the space on the basilar papilla devoted to processing the corresponding frequency range. Space on the papilla did not vary systematically with frequency selectivity at 1 kHz. This difference between test frequencies might be related to the transition from electrical hair-cell tuning, that dominates below 1e2 kHz, to micromechanical tuning at higher frequencies. Ó 2010 Elsevier B.V. All rights reserved.
1. Introduction Today, about 10,000 bird species are found in a wide range of different habitats. This speciation has led to very divergent anatomical and behavioural adaptations including vocal communication and the physiology of the auditory system. Among birds, some extreme examples of auditory specialization have been documented. For example, barn owls are highly specialized nocturnal hunters that successfully capture mice in total darkness using only auditory cues. The basilar papilla (BP), i.e., the sensory epithelium of the barn owl’s inner ear is unusually elongated (Köppl et al., 1993) and exhibits an over-representation of the 5e10 kHz frequency range. Similar over-representation is found in central auditory nuclei (Konishi, 1993). In the pigeon (Kreithen and Quine, 1979; Schermuly and Klinke, 1990a) and the chicken (Warchol and Dallos, 1989) a capability for infra-sound perception has been reported. Infra-sound responses originate from specialized apical regions of the BP in these species (Schermuly and Klinke,
Abbreviations: BP, basilar papilla; CR, critical ratio; CAP, compound action potential. * Corresponding author. Tel.: þ49 941 944 9426; fax: þ49 941 944 9424. E-mail addresses: [email protected] (O. Gleich), ulrike. [email protected] (U. Langemann). 0378-5955/$ e see front matter Ó 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.heares.2010.01.009
1990b; Warchol and Dallos, 1989; Lavigne-Rebillard et al., 1985). Finally, some bird species use clicks for echolocation, however, specializations of their auditory system in that context have not yet been identified (Konishi and Knudsen, 1979; Thomassen et al., 2007). The purpose of the following analysis is to demonstrate the range of inter-species structural and functional variability and to search for systematic relationships between structure and function. One problem in compiling an overview on structure and function relationships of the inner ear in birds is the fact that many studies addressed diverse questions using different methodologies. From the literature, we assembled all relevant data for a direct comparison between bird species with respect to anatomical parameters and perceptual abilities. 1.1. Structural aspects Birds are amniotes and their auditory sensory epithelium evolved from the BP of primitive reptiles (stem reptiles). The “modern” BP of birds shows a number of derived features. Compared to the primitive condition in stem reptiles, the modern BP is elongated and the total number of hair cells is increased. Hair cells are differentiated across the width of the BP and classified as “tall” and “short” based on their shape (Takasaka and Smith, 1971), but a functionally more relevant distinction is based on the
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innervation pattern (Fischer, 1994). In addition, a range of anatomical gradients (e.g., hair cell dimensions, hair bundle orientation, stereovilli dimensions, etc.) vary along and across the BP in birds (reviewed in Gleich et al. (2004)). Besides this common basic pattern, the avian BP shows considerable species specific differentiation. This is, for example, obvious for the length of the papilla, which varies from near 2 mm in small songbirds (Gleich et al., 1994) to around 4 mm in pigeon and chicken (Gleich and Manley, 1988; Manley et al., 1996), 5.5 mm in the emu (Köppl and Manley, 1997) and reaching almost 12 mm in the barn owl (Köppl et al., 1993). Also, the number of hair cells varies considerably from around 3000 in small songbirds to more than 16,000 in the emu and barn owl. Generally, the width and the number of hair cells across the BP increases from the basal highfrequency end to the apical low-frequency end. In addition, there are complex species specific differences regarding the distribution of tall and short hair cells (Fischer et al., 1988, 1992; Fischer, 1992, 1994, 1998). Further anatomical gradients (e.g., number of stereovilli per hair cell, orientation of stereovilli bundles, etc.) along and across the papilla have only been characterized in a few species (review in Gleich et al. (2004)). Besides the variations at the level of the BP there are also species differences in the central auditory pathway. For example, the number of auditory nerve fibers and the ratio between hair cells and auditory nerve fibers varies between species (Köppl et al., 2000). Thus, besides structural variation in the BP that will affect the input to the auditory nerve, variation in central processing will also contribute to auditory performance.
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Table 1 Sources for body mass of bird species, as of 1st of October 2009. Bird species
Website with information on body mass
African jackass penguin Mute swan White stork Black stork Grey parrot Raven Goldcrest Great spotted kiwi Orange fronted conure Grasshopper sparrow Racket-tailed drongo
http://de.wikipedia.org/wiki/Brillenpinguin http://de.wikipedia.org/wiki/H%C3%B6ckerschwan http://de.wikipedia.org/wiki/Wei%C3%9Fstorch http://de.wikipedia.org/wiki/Schwarzstorch http://de.wikipedia.org/wiki/Graupapagei http://de.wikipedia.org/wiki/Kolkrabe http://de.wikipedia.org/wiki/Wintergoldh%C3%A4hnchen http://en.wikipedia.org/wiki/Kiwi http://www.parrots.org/index.php/encyclopedia/profile/ orange_fronted_conure/ http://www.ct.gov/dep/cwp/view.asp?A¼2723&Q¼326016 http://www.answers.com/topic/greater-racket-taileddrongo
2. Methods
[Casuarius casuarius], ostrich [Struthio camelus], blackbird [Turdus merula], jay [Garrulus glandarius], buzzard [Buteo buteo], duck [Anas plathyrynchos], herring gull [Larus argentatus], quail [Coturnix coturnix], pine siskin [Carduelis pinus], sparrow [Passer domesticus], grasshopper sparrow [Ammodramus savannarum] (Lohr et al., 2006). To obtain BP length values representative for the living state, measurements determined by scanning electron microscopy were corrected by multiplication with a factor of 1.29 to compensate for shrinkage (Gleich and Manley, 1988). Cochlear duct length for 17 bird species was determined from images of the dissected inner ears published by Gray (1908, for details see Gleich et al. (2005)). The raw endosseous cochlear duct length measurements for 19 avian species are provided in the Supplementary material of Walsh et al. (2009) and we calculated the mean of the left and right ear for each species. Thus in 10 species direct measurements of BP length and cochlear duct length were available (ostrich, emu, cassowary, tufted duck, mallard duck, chicken, budgerigar, zebra finch, buzzard, barn owl). The best fit linear regression line for the plot of cochlear duct length as a function of BP length for nine species (excluding the data point from the barn owl that was far outside the distribution of the other birds’ data) revealed a significant correlation between the two variables (regression line: y ¼ 1.4875x þ 0.0905; R2 ¼ 0.767; p ¼ 0.002). The slope of the regression line indicates that a scaling factor of 2/3 is adequate to obtain an estimate of BP length from cochlear duct measurements (see also Gleich et al. (2005)). In the following, we will adopt this scaling factor when including the cochlear duct measurements in the comparison of BP length. A measure representing body size that can be readily found for most species in the literature is body mass. References to most anatomical data shown in this paper are listed in the Supplementary material of Gleich et al. (2005). The body mass of the nightingale [Luscinia megarhynchos] was found in Kipper et al. (2006). The body mass from additional species was derived from the websites listed in Table 1.
2.1. Anatomical data
2.2. Audiograms
For starling [Sturnus vulgaris], zebra finch [Taeniopygia guttata], canary [Serinus canarius], barn owl [Tyto alba], budgerigar [Melopsittacus undulatus], chicken [Gallus gallus domesticus], pigeon [Columba livia], tufted duck [Aythya fuligula], and emu [Dromaius novaehollandiae] anatomical gradients along and across the BP have been analyzed in detail (see review in Gleich et al. (2004)). For the following additional species, the length of the BP has been measured by light or scanning electron microscopy: cassowary
The sources of behavioural audiograms from most bird species have been listed in Gleich et al. (2005). In the present study, we have added audiogram data from the hooded crow [Corvus corone cornix] (Jensen and Klokker, 2006), the orange fronted conure [Aratinga canicularis] (Wright et al., 2003) and the grasshopper sparrow (Lohr et al., 2006). Using the original raw audiogram data that were available for each species, 3rd-order polynomial fits were calculated. Comparing
1.2. Functional aspects One of the most basic descriptions of auditory capability is the audiogram, that characterizes the frequency dependent variation of absolute sensitivity. Partly due to the columella type single ossicle middle ear of birds, sound transduction deteriorates above 4 kHz and the high frequency hearing range in birds is limited to frequencies at or slightly above 10 kHz (Saunders et al., 2000; Manley, 2010). Based on data from 23 species, Dooling (1992) described differences in audiogram characteristics between different avian orders and between different families of songbirds with respect to absolute sensitivity and best audiogram frequency (i.e., the frequency with the lowest absolute threshold). As will be shown below, factors beyond phylogenetic relationships affect audiogram parameters. In birds, the most sensitive thresholds were reported to vary between 15 and 25 dB SPL (e.g., Fay, 1992). Best audiogram frequencies in a sample of 37 bird species varied considerably between 1.1 and 5.6 kHz (e.g., Gleich et al., 2005). The frequency distribution along the BP, i.e., the place-frequency map, is known for several avian species. The length of the BP and the space available for coding of a given frequency range shows speciesspecific variability (e.g., reviewed in Gleich et al. (2004)). One important question addressed here is whether the available space on the BP affects frequency selectivity.
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the raw data plots and the best fit functions indicated that the 3rdorder polynomial fits were a good representation of the audiograms. This was confirmed by a quantitative analysis of the coefficient of determination (i.e., the squared correlation coefficient) for the linear regression comparing the raw and the best fit thresholds for the behavioural audiogram of each species. This analysis was performed for 40 species. In all species the regression revealed a significant correlation between the raw and the best fit thresholds (p # 0.02) and for 36 of these species the significance level was p # 0.001. The mean coefficient of determination for all 40 audiograms analyzed was 0.912. Nine species showed coefficients of determination between 0.8 and 0.9, four species were below 0.8. This high degree of correlation supports the qualitative impression that the best fit functions are an adequate representation for comparing audiogram characteristics across species. To derive audiogram characteristics, the best fit function for each species was calculated in 100 Hz steps for the frequency range covered by the raw data. For each species, the frequency with the lowest threshold was defined as the best audiogram frequency. Additional parameters were determined; for example, low- and high-frequency limits describe the frequencies below and above the best audiogram frequency with thresholds 30 dB above the best frequency. The range between the low- and high-frequency limits was used as an indicator of the hearing range and was expressed in octaves. We did not extrapolate audiograms beyond the actual threshold data. Thus the low- and high-frequency limits of the audiogram were only derived when they were within the frequency range where thresholds had actually been collected during behavioural testing and are thus not available for all species. 3. Results and discussion 3.1. Basilar papilla length and body mass Gleich et al. (2005) demonstrated a significant positive correlation between the length of the BP and body mass. Although the barn owl is the only strigiform species where the BP length is available, it was excluded from this analysis since its papilla length was clearly outside the range of other birds (see also additional arguments for a separate analysis as discussed below). By adding the data from Walsh et al. (2009) to those presented by Gleich et al. (2005), the relation was compiled for a total of 41 non-strigiform species. Fig. 1 demonstrates the systematic relationship between the length of the BP and body mass. Different groups of birds are coded by separate symbols. The definition of groups is based on suggestions by Feduccia (1980, 1995) and Olsen (1985). The
Fig. 1. The length of the basilar papilla as a function of body mass in four phylogenetic groups of birds (see text for explanations).
palaeognathous birds in the present sample are represented by emu, cassowary, ostrich, two kiwi species and the great tinamou (black triangles). The neognathous birds can be separated into a waterbird assembly (shown as blue diamonds and represented by Anseriformes [ducks and swan], Gaviformes [red throated diver], Charadriformes [herring gull], Pelicaniformes [cape gannet, cormorant], Sphenisciformes [African jackass penguin] and Ciconiiformes [storks and herons]) and a landbird assembly. Landbirds are further subdivided in primitive landbirds (shown by green circles and represented by Columbiformes [pigeons], Galliformes [chicken, quails, turkey, grouse], Gruiformes [crane] and Psittaciformes [parrots]) and advanced landbirds (shown by red circles and represented by Passeriformes [songbirds] and Falconiformes [falcon, sparrowhawk and buzzard]). In non-strigiform bird species, BP length varied between 1.9 mm in the goldcrest and 5.5 mm in the emu while body mass varied from a few grams in small songbirds to near 100 kg in the ostrich. The data from the different avian groups represented by different colours in Fig. 1 seem to represent a continuum and they are well described by a common best fit regression line. This regression suggests that the relation between body mass and BP length does not systematically differ between different phylogenetic avian groups.
3.2. Absolute thresholds The best sensitivity (i.e., lowest absolute threshold) as a function of best audiogram frequency (i.e., the frequency with the lowest absolute threshold) for 40 species is shown in Fig. 2. The best audiogram frequency varied between 2.0 and 4.5 kHz in non-strigiform birds. From 12 owl species, 2 had lower best frequencies (brown fish owl 1.1 kHz; great horned owl 1.4 kHz) and 3 had higher best frequencies (African wood owl and long eared owl 5.5 kHz; barn owl 5.6 kHz) than the other bird species. The only owl species studied in detail is the barn owl: Its best audiogram frequency was only slightly higher than those of song birds with the highest best audiogram frequencies (4.5 kHz for great tit and grasshopper sparrow). This is somewhat surprising given that the barn owl exhibits features that are distinctly different from other bird species. For example, the high frequency specialization in barn owls is reflected in an over-representation of the 5e10 kHz region on the BP (Köppl et al., 1993). This one octave frequency range occupies around 5 mm on the BP and thus represents a much
Fig. 2. The best (i.e., lowest) audiogram threshold as a function of best audiogram frequency illustrates the species-specific variability. Different symbols indicate waterbirds (blue diamond, here represented by the duck) being the least advanced followed by primitive (green circles, N ¼ 9) and advanced (red circles, N ¼ 18) landbirds. The strigiformes (orange asterisks, N ¼ 12) are shown separately as a highly specialized group of advanced landbirds.
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higher space constant than seen in any other bird species, where space constants are typically between 0.5 and 1 mm/oct (Gleich et al., 2004). While best audiogram thresholds in all strigiformes were below 0 dB SPL (mean 15.04 dB SPL), only three of the non-strigiform species had a best thresholds below 0 dB SPL. The mean best threshold in all non-strigiform species was 6.78 dB SPL. The best threshold in owls was thus on average approximately 20 dB lower compared to other birds. At least for the barn owl, it has been shown that the facial ruff feathers form an external ear analogous to the mammalian pinna, providing an acoustic gain of about 20 dB between 3 and 9 kHz (Coles and Guppy, 1988). The extreme sensitivity of owls is thus likely related to the specialized external ear structures that are typically absent in other avian species. Consequently threshold comparisons between Strigiformes and other avian groups are not really valid. 3.3. Audiograms Examples of best 3rd-order fits used to derive audiogram characteristics are illustrated for those species where both the audiogram and the length of the BP are known. Fig. 3A gives an idea of frequency and threshold variations. For a better comparison of the audiogram shapes, Fig. 3B shows audiograms normalized relative to best frequency and to best threshold for the 25 nonstrigiform species in which the high-frequency limit of 30 dB was reached. The high frequency flanks of these normalized audiograms were quite similar across species and showed little variation. The low frequency flank of the audiograms was much more variable between species and less steep than the high frequency flank. Fig. 3C illustrates normalized audiograms from 12 owl species. The slopes of the high frequency audiogram flanks varied over a wider range compared to non-strigiform species. The high-frequency slope was steeper than in non-strigiform species in 7 of the 12 owl species. In addition, the low-frequency flanks appeared very shallow in some owl species. This comparison showed that the shapes of owl audiograms were much more variable and consequently we analyzed owls and non-strigiform species separately.
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across species in the basal high-frequency region and large variability in the apical-low frequency region. 3.5. Frequency representation and frequency selectivity The frequency representation along the avian BP is tonotopically arranged with high frequencies represented at the basal and low frequencies represented at the apical end of the papilla. One obvious question is whether auditory frequency selectivity is related to the spatial representation of frequency on the BP: Does the amount of space along the BP devoted to a certain frequency range affect frequency resolution? The hearing range perceived by a given species is transduced by the BP which varies in length between 2 and 6 mm in non-strigiform species. Frequency maps describing the distribution of frequency along the BP are known for 9 species (see review in Gleich et al. (2004)). The mapping of frequency along the BP and the space devoted to a given frequency range differs between bird species. When frequency is plotted on a logarithmic scale, the slope of the place-frequency map is a quantitative measure of the “space constant” that indicates the
3.4. Anatomy and gradients along the papilla Several gradients change systematically along the BP in parallel with the tonotopic organization of frequency. However, the relation between a given morphological parameter and frequency position on the BP differs considerably between species (e.g., Gleich et al., 2004). This is exemplified for the variation of the number of hair cells across the BP in Fig. 4A. For example, at 1 kHz the number of hair cells across the papilla varied between about 21 in the canary and 33 hair cells in the barn owl. Plotting the number of hair cells across the BP as a function of frequency did not lead to a match of this morphological gradient across species (see Fig. 4A). A match of the gradients along the papilla as a function of frequency was also not achieved for additional morphological parameters like the width of the papilla, the number of stereovilli per hair cell and the maximum height of the stereovilli (Gleich et al., 2004). This demonstrates that none of these single parameters alone can determine the frequency response at a given BP location. The frequency response rather results from an interaction of different parameters. Replotting the number of hair cells across the BP as a function of distance from the base illustrates that the number is small at the base in all species. As hair cell number grows toward the apex the variability across species increases (Fig. 4B and C). Taken together, the comparison of the normalized audiograms in Fig. 3 and the morphological gradients illustrated in Fig. 4 reveal small variability
Fig. 3. (A) Audiogram shapes of nine bird species where the length of the basilar papilla is known. (B) Audiograms of 25 non-strigiform species with a high-frequency limit of more than 30 dB. (blue for duck, green for primitive landbirds, red for advanced landbirds). (C) Audiograms of 12 owl species (orange for barn owl, black lines for all other owl species). Audiograms in (B) and (C) have been normalized with respect to the best audiogram frequency (expressed in octaves) and to the best auditory threshold. The horizontal dotted line indicates 30 dB above best audiogram threshold.
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space available per octave (mm/oct; e.g., Manley, 2000). A logarithmic function with an invariant space constant along the BP has been found in several species. Deviations from this logarithmic function occurred in the barn owl, starling, chicken and budgerigar, that show decreasing space constants towards the apical lowfrequency end of the BP, thus extending the hearing range towards low frequencies. A comparison across avian species revealed a systematic correlation between the space devoted to the 1e2 kHz range and the length of the BP, varying from 0.5 mm in the canary with a BP length of 2.1 mm to 0.9 mm in the emu with a 5.5 mm long BP (Gleich et al., 2004). A common measure of auditory frequency selectivity is the critical ratio (CR). The CR is determined in a behavioural masking
experiment and yields the detection threshold of a tone relative to the noise spectrum level of a wide-band noise masker (i.e., the signal-to-noise ratio in dB). The CR bandwidth of the corresponding rectangular auditory filter (in Hz) can then be estimated from this ratio (e.g., Langemann et al., 1995). Low CR values indicate high frequency selectivity, and high CR values indicate low frequency selectivity. In Fig. 5 we plot the CR as a function of the octaves mapped to 1 mm on the BP (the inverse of the space constant) for three different test frequencies. We included data from bird species where both the CR (starling e Langemann et al., 1995, budgerigar e Saunders et al., 1978, pigeon e Hienz and Sachs, 1987, canary and zebra finch e Okanoya and Dooling, 1987a, barn owl e Dyson et al., 1998) and the space constants (derived from the maps published in Gleich et al. (2004)) were available. The two data points with values below 1 oct/mm were from the barn owl (where the CR has not been determined for 1 kHz). All other data with values above 1 oct/ mm are from non-strigiform species. The linear regression lines for the data at 2 kHz (triangles, dotted line, p ¼ 0.03) and at 4 kHz (asterisks, thin continuous line, p ¼ 0.04) show a significant correlation between the CR and the number of octaves mapped to 1 mm on the basilar papilla: the less space was available on the papilla (i.e., more octaves mapped to 1 mm), the lower was the frequency selectivity (indicated by higher CR values) at 2 and 4 kHz. The function at 4 kHz appeared shifted to the left compared to the function at 2 kHz. Consequently, in the 4 kHz compared to the 2 kHz region more space was associated with a given CR. The data for the 1 kHz test frequency (circles) did not indicate a similar correlation between space and frequency selectivity (see coefficients of determination in the upper left of Fig. 5; p ¼ 0.57). Although on average more octaves are mapped onto the BP in the 1 kHz region compared to the higher frequencies, frequency selectivity was relatively high as indicated by the low CR values. At 1 kHz the average CR was 23.4 dB and was associated with 1.996 octaves mapped to 1 mm of the BP. Estimates based on the regression lines shown in Fig. 5 reveal that more space was associated with a CR of 23.4 dB at higher frequencies. At 2 kHz 1.588 octaves and at 4 kHz 1.331 octaves were mapped to 1 mm of the BP at a CR of 23.4 dB.
Fig. 4. The number of hair cells across the basilar papilla shows a systematic gradient from the base towards the apex. Black is used for the emu, blue for the duck, green for primitive landbirds, red for advanced landbirds and orange for the barn owl. (A) The position along the basilar papilla was converted to frequency based on the placefrequency maps presented in Gleich et al. (2004). (B) The number of hair cells is plotted as a function of the distance (in mm) from the basal end of the papilla (the length was limited to 6 mm excluding the apical half of the barn owl basilar papilla). The x-axis was reversed for a better comparison with the frequency scales shown in (A) and in Fig. 3. (C) The number of hair cells was normalized and is plotted as a function of the distance (in %) from the basal end of the papilla.
Fig. 5. The critical ratio (a behavioural measure of frequency selectivity) is shown as a function of the frequency range (expressed in octaves) mapped to 1 mm on the basilar papilla. Green symbols: primitive land birds, red symbols: advanced landbirds, orange symbols: barn owl. The figure includes data from six bird species (starling, budgerigar, pigeon, canary, zebra finch, barn owl; see text). The test frequency is indicated by different symbols (circle: 1 kHz, triangle: 2 kHz, asterisk: 4 kHz). The coefficient of determination for a linear regression through the data at the different test frequencies (excluding the owl data points) is given in the top left. The best fit linear regression lines are shown for significant correlations at 4 kHz (thin continuous line) and 2 kHz (dotted line).
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Fig. 6. Audiograms from 4 galliform species (primitive landbirds). (A) Absolute threshold is shown as a function of frequency. (B) The comparison of normalized audiograms emphasizes the broadly tuned audiogram of the adult chicken.
The finding that the space on the BP and frequency selectivity correlate at a test frequency of 2 and 4 kHz, but not at 1 kHz, may be related to the transition of the tuning mechanisms between low and high frequencies that contribute to frequency selectivity in the avian BP (Gleich and Manley, 2000). Electrical tuning dominates at low frequencies and is determined by the electrical properties of an individual hair cell’s membrane. It is independent of the properties of neighbouring hair cells. Consequently space is not a major factor determining frequency selectivity at low frequencies. Mechanical tuning due to the interaction of the micromechanical properties of the BP, basilar membrane, tectorial membrane and the hair cell complex becomes dominant for higher frequencies above 1e2 kHz. Tuning due to micromechanical properties is influenced by mechanical coupling to neighbouring structures, and thus space will affect frequency selectivity (Manley, 2000). The two left most data points refer to the CR data of the barn owl at 2 and 4 kHz. Both values were off the distribution for non-strigiform data. With the ample space available on the barn owl basilar papilla, much higher frequency selectivity could have been expected (see also Dyson et al. (1998)). Estimates of frequency selectivity derived from measures of otoacoustic emissions also showed that frequency tuning in the barn owl was not better than average (Köppl et al., 1998). In addition, the frequency selectivity of single auditory nerve fibers in the barn owl was not increased in the region of expanded frequency mapping as might be expected based on the equal distance hypothesis (Köppl, 1997). The extended space on the BP of the barn owl is obviously not associated with increased frequency selectivity.
3.6. Hearing in chickens For a better comparison of audiogram shapes, Fig. 3B shows audiograms normalized relative to best frequency and best threshold for all 25 non-strigiform species, where a high-frequency limit of more than 30 dB was available. Fig. 6 compares the data from 4 galliform species (turkey, chicken, quail, bobwhite quail). The chicken audiogram appears quite different from other audiograms (see also Fig. 3), with the low and high frequency audiogram flanks being shallower than in any other non-strigiform species. It is not clear why the chicken audiogram is so broadly tuned. Although the best audiogram threshold in the chicken is relatively high (16 dB SPL) it is still within the higher range observed in other non-strigiform species and does not indicate a severe hearing loss like in the Belgian Waterslager canary strain (Okanoya and Dooling, 1985, 1987b). The chicken audiogram data reported by Saunders and Salvi (1993) were collected in white leghorn chickens that were older than 26 weeks. However, it appears unlikely that BP pathology as described for broiler and egg layer chickens (Durham et al., 2002; Smittkamp et al., 2002) could explain the shallow flanks of the chicken audiogram (Fig. 6), especially for the high frequency side. Basilar papilla pathology affecting the base, and leading to a loss of high frequency distortion product otoacoustic emissions as described by Durham et al. (2002) should be associated with a pronounced high frequency hearing loss. The much shallower high frequency flank of the chicken behavioural audiogram compared to other species is also in contrast to audiograms derived from the compound action
Fig. 7. (A) Behavioural audiograms of 4 species where also CAP audiograms have been published. (B) CAP audiograms of the same species where behavioural audiograms are shown on the left. The lines show 3rd-order polynomial fits to the data from chicken (thinner, darker green line), pigeon (thicker, brighter green line), canary (red line) and the barn owl (orange line).
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Fig. 8. (A) The high-frequency limit of the audiogram is plotted as a function of best audiogram frequency for 25 non-strigiform species and 12 owl species. (B) The high-frequency limit in octaves relative to the best audiogram frequency is plotted as a function of best audiogram frequency. The linear regression is shown for the data from non-strigiform species. Blue diamond: duck, green circles: primitive landbirds, red circles: advanced landbirds, orange asterisks: strigiformes.
potential (CAP). Fig. 7 compares on the left side four behavioural audiograms and shows the corresponding CAP audiograms on the right side (chicken e Rebillard and Rubel, 1981; Patuzzi and Bull, 1991; Salvi et al., 1992, pigeon e Gummer et al., 1987, canary e Gleich et al., 1995, barn owl e Köppl and Gleich, 2007). CAP audiograms typically show higher thresholds as compared to behavioural audiograms, but in general both types of audiograms share basic characteristics, as illustrated in Fig. 7. The shape of behavioural and CAP audiograms is not identical for a given species. These discrepancies may relate to methodology. Physiological measures use synchronized neural responses to the onset of short tones. Behavioural testing typically uses tones with a duration of several hundred milliseconds, where temporal integration may contribute to lower thresholds. Differences between studies may also arise from sampling problems since sample size is often small. Nevertheless, the high frequency flank of the CAP audiogram in immature chickens was not obviously different from that of other birds (Fig. 7B), while it appeared considerably shallower in the behavioural audiogram from the adult chickens (see Figs. 6 and 7A). The morphological analysis of the chicken inner ear (e.g., Fig. 4; Manley et al., 1996) typically used very young chickens and the structural changes observed in chickens beyond 30 weeks of age (Durham et al., 2002) suggest a pronounced high frequency hearing loss and do not explain the shallow high frequency slope of the audiogram determined in adult chickens (Saunders and Salvi, 1993). The relatively shallow low frequency flank of the chicken audiogram (see normalized audiograms in Fig. 6B) might be related to a specialization for
low frequency perception (Lavigne-Rebillard et al., 1985; Warchol and Dallos, 1989). 3.7. High-frequency limit of hearing in birds While the upper limit of hearing in mammals typically extends to the ultra-sound range, birds are limited to frequencies around 10 kHz. In mammals the evolution of high frequency hearing was interpreted in the context of sound localization (e.g., Heffner and Heffner, 1992). Extending the hearing range towards higher frequencies would require either shifting the frequency range of the whole audiogram toward higher frequencies or decreasing the high frequency slope of the audiogram. For a quantitative comparison beyond the qualitative comparison illustrated in Fig. 3 we analyzed the high-frequency limit of the audiogram as a function of best audiogram frequency for all species including owls. The high-frequency limit of the audiogram increased roughly linearly with best frequency in non-strigiform species (Fig. 8A). Although some owl data points (orange asterisks) fitted very well into the distribution, some clearly deviated from the pattern seen in non-strigiform species. Plotting the high-frequency limit in octaves (relative to the best audiogram frequency) as a function of best audiogram frequency revealed a small but significant decrease of the upper audiogram frequency limit with increasing best frequency in non-strigiform bird species (see best fit regression line in Fig. 8B). However, the slope of the regression function was small (0.0607 oct/kHz), resulting in an estimated difference of only 0.15 octaves between the non-strigiform species with the lowest (2 kHz,
Fig. 9. (A) The best audiogram frequency (diamonds) as well as the low (triangles) and high (circles) frequency limits of the audiogram are shown as a function of basilar papilla length. The best fit exponential lines illustrate a systematic decrease with increasing papilla length. (B) The high- (circles) and low- (triangles) frequency limits in octaves relative to the best audiogram frequency are plotted as a function of basilar papilla length. The dotted line at zero represents the best audiogram frequency. Blue: duck, green: primitive landbirds, red: advanced landbirds.
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turkey) and highest best frequencies (4.5 kHz, great tit and grasshopper sparrow). From a practical point of view the effect of best frequency on the high-frequency limit is very small and the high frequency audiogram slope is quite similar across non-strigiform species (see also Fig. 3B), being on average slightly more than one octave above the best audiogram frequency. These observations indicate that the high frequency slope of the audiogram does not vary between phylogenetic groups in non-strigiform species. Some of the owl data points deviated considerably from the distribution of the other birds, with lower values indicating a steeper high frequency flank of the audiogram. Only in the great horned owl was the upper frequency limit of 4.6 kHz 1.7 octaves above the best audiogram frequency of 1.4 kHz, indicating a shallower high frequency audiogram flank. 3.8. Basilar papilla length and frequency range Best audiogram frequency and BP length are inversely related (Gleich et al., 2005). Fig. 9 shows that in addition to the best audiogram frequency, the low and high-frequency limits of the audiogram decrease with increasing BP length. Consistent with the typically shallower low frequency slope of the audiogram, the distance between the best frequency and the low-frequency limit was larger (on a logarithmic scale) than the distance between the best frequency and the high-frequency limit (Fig. 9A). On a logarithmic scale, the effect of BP length on the low-frequency limit was more pronounced than for the high-frequency limit (Fig. 9A). Best frequency and the high-frequency limit decreased approximately by 0.4 oct/mm increase of BP length while the decrease for the lowfrequency limit was 1.4 oct/mm. Fig. 9B plots the high and lowfrequency limits in octaves with respect to the best frequency as a function of BP length. Independent of BP length, and consistent with the data presented in Fig. 8, the high-frequency limit was on average 1.1 octaves higher than the best frequency (Fig. 9B). In contrast, the low-frequency limit increased from an average of 2.5 octaves below best frequency in small songbirds (BP length slightly above 2 mm) to 4.5 octaves below best frequency in the pigeon (4 mm BP length). The corresponding hearing range in octaves increased from around 3.5 octaves to 5.5 octaves, respectively (see Fig. 9B). Acknowledgements Roots of the basic concept for a comparative analysis of structureefunction relationships of the avian inner ear reach back to research within the SFB 204 “Gehör” that was funded by the DFG from 1983 to 1997. The collaboration between O.G. and U.L. was funded by the DFG within the SFB/TRR 31 “The active auditory system”. We thank G.A. Manley and two anonymous reviewers for helpful suggestions for improving the initial version of the manuscript. References Coles, R.B., Guppy, A., 1988. Directional hearing in the barn owl (Tyto alba). J. Comp. Physiol. A 163, 117e133. Dooling, R.J., 1992. Hearing in birds. In: Webster, D.B., Fay, R.R., Popper, A.N. (Eds.), The Evolutionary Biology of Hearing. Springer-Verlag, Heidelberg, New York, pp. 545e559. Durham, D., Park, D.L., Girod, D.A., 2002. Breed differences in cochlear integrity in adult, commercially raised chickens. Hear. Res. 166, 82e95. Dyson, M.L., Klump, G.M., Gauger, B., 1998. Absolute hearing thresholds and critical masking ratios in the European barn owl: a comparison with other owls. J. Comp. Physiol. A 182, 695e702. Fay, R.R., 1992. Structure and function in sound discrimination among vertebrates. In: Webster, D.B., Fay, R.R., Popper, A.N. (Eds.), The Evolutionary Biology of Hearing. Springer-Verlag, New York, pp. 229e263. Feduccia, A., 1980. The Age of Birds. Harvard University Press, Cambridge.
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